Combating Neurodegenerative Diseases with the Plant Alkaloid Berberine: Molecular Mechanisms and Therapeutic Potential

Author(s): Dahua Fan, Liping Liu, Zhengzhi Wu*, Meiqun Cao*.

Journal Name: Current Neuropharmacology

Volume 17 , Issue 6 , 2019

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Graphical Abstract:


Abstract:

Neurodegenerative diseases are among the most serious health problems affecting millions of people worldwide. Such diseases are characterized by a progressive degeneration and / or death of neurons in the central nervous system. Currently, there are no therapeutic approaches to cure or even halt the progression of neurodegenerative diseases. During the last two decades, much attention has been paid to the neuroprotective and anti-neurodegenerative activities of compounds isolated from natural products with high efficacy and low toxicity. Accumulating evidence indicates that berberine, an isoquinoline alkaloid isolated from traditional Chinese medicinal herbs, may act as a promising anti-neurodegenerative agent by inhibiting the activity of the most important pathogenic enzymes, ameliorating intracellular oxidative stress, attenuating neuroinflammation, triggering autophagy and protecting neurons against apoptotic cell death. This review attempts to summarize the current state of knowledge regarding the therapeutic potential of berberine against neurodegenerative diseases, with a focus on the molecular mechanisms that underlie its effects on Alzheimer’s, Parkinson’s and Huntington’s diseases.

Keywords: Neurodegenerative diseases, berberine, neuroprotection, oxidative stress, neuroinflammation, autophagy.

[1]
Kong, W.; Wei, J.; Abidi, P.; Lin, M.; Inaba, S.; Li, C.; Wang, Y.; Wang, Z.; Si, S.; Pan, H.; Wang, S.; Wu, J.; Wang, Y.; Li, Z.; Liu, J.; Jiang, J.D. Berberine is a novel cholesterol-lowering drug working through a unique mechanism distinct from statins. Nat. Med., 2004, 10(12), 1344-1351.
[http://dx.doi.org/10.1038/nm1135] [PMID: 15531889]
[2]
Imanshahidi, M.; Hosseinzadeh, H. Pharmacological and therapeutic effects of Berberis vulgaris and its active constituent, berberine. Phytother. Res., 2008, 22(8), 999-1012.
[http://dx.doi.org/10.1002/ptr.2399] [PMID: 18618524]
[3]
Liu, B.; Li, W.; Chang, Y.; Dong, W.; Ni, L. Extraction of berberine from rhizome of Coptis chinensis Franch using supercritical fluid extraction. J. Pharm. Biomed. Anal., 2006, 41(3), 1056-1060.
[http://dx.doi.org/10.1016/j.jpba.2006.01.034] [PMID: 16500064]
[4]
Lee, B.; Sur, B.; Shim, I.; Lee, H.; Hahm, D.H. Phellodendron amurense and its major alkaloid compound, berberine ameliorates scopolamine-induced neuronal impairment and memory dysfunction in rats. Korean J. Physiol. Pharmacol., 2012, 16(2), 79-89.
[http://dx.doi.org/10.4196/kjpp.2012.16.2.79] [PMID: 22563252]
[5]
Gentry, E.J.; Jampani, H.B.; Keshavarz-Shokri, A.; Morton, M.D.; Velde, D.V.; Telikepalli, H.; Mitscher, L.A.; Shawar, R.; Humble, D.; Baker, W. Antitubercular natural products: Berberine from the roots of commercial Hydrastis canadensis powder. Isolation of inactive 8-oxotetrahydrothalifendine, canadine, β-hydrastine, and two new quinic acid esters, hycandinic acid esters-1 and -2. J. Nat. Prod., 1998, 61(10), 1187-1193.
[http://dx.doi.org/10.1021/np9701889] [PMID: 9784149]
[6]
Imenshahidi, M.; Hosseinzadeh, H. Berberis vulgaris and berberine: An update review. Phytother. Res., 2016, 30(11), 1745-1764.
[http://dx.doi.org/10.1002/ptr.5693] [PMID: 27528198]
[7]
Amritpal, S.; Sanjiv, D.; Navpreet, K.; Jaswinder, S. Berberine: Alkaloid with wide spectrum of pharmacological activities. J. Nat. Prod., 2010, 3, 64-75.
[8]
Kumar, A. Ekavali; Chopra, K.; Mukherjee, M.; Pottabathini, R.; Dhull, D.K. Current knowledge and pharmacological profile of berberine: An update. Eur. J. Pharmacol., 2015, 761, 288-297.
[http://dx.doi.org/10.1016/j.ejphar.2015.05.068] [PMID: 26092760]
[9]
Kumar, A. Ekavali; Chopra, K.; Mukherjee, M.; Pottabathini, R.; Dhull, D.K. Current knowledge and pharmacological profile of berberine: An update. Eur. J. Pharmacol., 2015, 761, 288-297.
[http://dx.doi.org/10.1016/j.ejphar.2015.05.068] [PMID: 26092760]
[10]
Ye, M.; Fu, S.; Pi, R.; He, F. Neuropharmacological and pharmacokinetic properties of berberine: A review of recent research. J. Pharm. Pharmacol., 2009, 61(7), 831-837.
[11]
Tan, X.S.; Ma, J.Y.; Feng, R.; Ma, C.; Chen, W.J.; Sun, Y.P.; Fu, J.; Huang, M.; He, C.Y.; Shou, J.W.; He, W.Y.; Wang, Y.; Jiang, J.D. Tissue distribution of berberine and its metabolites after oral administration in rats. PLoS One, 2013, 8(10), e77969.
[http://dx.doi.org/10.1371/journal.pone.0077969] [PMID: 24205048]
[12]
Zhang, J.; Yang, J.Q.; He, B.C.; Zhou, Q.X.; Yu, H.R.; Tang, Y.; Liu, B.Z. Berberine and total base from rhizoma coptis chinensis attenuate brain injury in an aluminum-induced rat model of neurodegenerative disease. Saudi Med. J., 2009, 30(6), 760-766.
[PMID: 19526156]
[13]
Habtemariam, S. The therapeutic potential of Berberis darwinii stem-bark: Quantification of berberine and in vitro evidence for Alzheimer’s disease therapy. Nat. Prod. Commun., 2011, 6(8), 1089-1090.
[PMID: 21922905]
[14]
Jiang, H.; Wang, X.; Huang, L.; Luo, Z.; Su, T.; Ding, K.; Li, X. Benzenediol-berberine hybrids: Multifunctional agents for Alzheimer’s disease. Bioorg. Med. Chem., 2011, 19(23), 7228-7235.
[http://dx.doi.org/10.1016/j.bmc.2011.09.040] [PMID: 22041172]
[15]
Kim, M.; Cho, K.H.; Shin, M.S.; Lee, J.M.; Cho, H.S.; Kim, C.J.; Shin, D.H.; Yang, H.J. Berberine prevents nigrostriatal dopaminergic neuronal loss and suppresses hippocampal apoptosis in mice with Parkinson’s disease. Int. J. Mol. Med., 2014, 33(4), 870-878.
[http://dx.doi.org/10.3892/ijmm.2014.1656] [PMID: 24535622]
[16]
Liu, X.; Zhou, J.; Abid, M.D.; Yan, H.; Huang, H.; Wan, L.; Feng, Z.; Chen, J. Berberine attenuates axonal transport impairment and axonopathy induced by Calyculin A in N2a cells. PLoS One, 2014, 9(4), e93974.
[http://dx.doi.org/10.1371/journal.pone.0093974] [PMID: 24713870]
[17]
Lee, T.; Heo, H.; Kim, K.Y.; Kim, K.Y. Effect of berberine on cell survival in the developing rat brain damaged by MK-801. Exp. Neurobiol., 2010, 19(3), 140-145.
[http://dx.doi.org/10.5607/en.2010.19.3.140] [PMID: 22110353]
[18]
Kumar, A. Ekavali; Mishra, J.; Chopra, K.; Dhull, D.K. Possible role of P-glycoprotein in the neuroprotective mechanism of berberine in intracerebroventricular streptozotocin-induced cognitive dysfunction. Psychopharmacology (Berl.), 2016, 233(1), 137-152.
[http://dx.doi.org/10.1007/s00213-015-4095-7] [PMID: 26446867]
[19]
Kalalian-Moghaddam, H.; Baluchnejadmojarad, T.; Roghani, M.; Goshadrou, F.; Ronaghi, A. Hippocampal synaptic plasticity restoration and anti-apoptotic effect underlie berberine improvement of learning and memory in streptozotocin-diabetic rats. Eur. J. Pharmacol., 2013, 698(1-3), 259-266.
[http://dx.doi.org/10.1016/j.ejphar.2012.10.020] [PMID: 23099256]
[20]
Campisi, A.; Acquaviva, R.; Mastrojeni, S.; Raciti, G.; Vanella, A.; De Pasquale, R.; Puglisi, S.; Iauk, L. Effect of berberine and Berberis aetnensis C. Presl. alkaloid extract on glutamate-evoked tissue transglutaminase up-regulation in astroglial cell cultures. Phytother. Res., 2011, 25(6), 816-820.
[http://dx.doi.org/10.1002/ptr.3340] [PMID: 21086546]
[21]
Hsu, Y.Y.; Tseng, Y.T.; Lo, Y.C. Berberine, a natural antidiabetes drug, attenuates glucose neurotoxicity and promotes Nrf2-related neurite outgrowth. Toxicol. Appl. Pharmacol., 2013, 272(3), 787-796.
[http://dx.doi.org/10.1016/j.taap.2013.08.008] [PMID: 23954465]
[22]
Shan, W.J.; Huang, L.; Zhou, Q.; Meng, F.C.; Li, X.S. Synthesis, biological evaluation of 9-N-substituted berberine derivatives as multi-functional agents of antioxidant, inhibitors of acetylcholinesterase, butyrylcholinesterase and amyloid-β aggregation. Eur. J. Med. Chem., 2011, 46(12), 5885-5893.
[http://dx.doi.org/10.1016/j.ejmech.2011.09.051] [PMID: 22019228]
[23]
Ji, H.F.; Shen, L. Molecular basis of inhibitory activities of berberine against pathogenic enzymes in Alzheimer's disease. Sci. World J.,, 2012, 2012
[http://dx.doi.org/10.1100/2012/823201]]
[24]
Abd El-Wahab, A.E.; Ghareeb, D.A.; Sarhan, E.E.; Abu-Serie, M.M.; El Demellawy, M.A. In vitro biological assessment of Berberis vulgaris and its active constituent, berberine: Antioxidants, anti-acetylcholinesterase, anti-diabetic and anticancer effects. BMC Complement. Altern. Med., 2013, 13, 218.
[http://dx.doi.org/10.1186/1472-6882-13-218] [PMID: 24007270]
[25]
Mak, S.; Luk, W.W.; Cui, W.; Hu, S.; Tsim, K.W.; Han, Y. Synergistic inhibition on acetylcholinesterase by the combination of berberine and palmatine originally isolated from Chinese medicinal herbs. J. Mol. Neurosci., 2014, 53(3), 511-516.
[http://dx.doi.org/10.1007/s12031-014-0288-5] [PMID: 24793543]
[26]
Durairajan, S.S.; Liu, L.F.; Lu, J.H.; Chen, L.L.; Yuan, Q.; Chung, S.K.; Huang, L.; Li, X.S.; Huang, J.D.; Li, M. Berberine ameliorates β-amyloid pathology, gliosis, and cognitive impairment in an Alzheimer’s disease transgenic mouse model. Neurobiol. Aging, 2012, 33(12), 2903-2919.
[http://dx.doi.org/10.1016/j.neurobiolaging.2012.02.016] [PMID: 22459600]
[27]
Jia, L.; Liu, J.; Song, Z.; Pan, X.; Chen, L.; Cui, X.; Wang, M. Berberine suppresses amyloid-beta-induced inflammatory response in microglia by inhibiting nuclear factor-kappaB and mitogen-activated protein kinase signalling pathways. J. Pharm. Pharmacol., 2012, 64(10), 1510-1521.
[http://dx.doi.org/10.1111/j.2042-7158.2012.01529.x] [PMID: 22943182]
[28]
Panahi, N.; Mahmoudian, M.; Mortazavi, P.; Hashjin, G.S. Effects of berberine on β-secretase activity in a rabbit model of Alzheimer’s disease. Arch. Med. Sci., 2013, 9(1), 146-150.
[http://dx.doi.org/10.5114/aoms.2013.33354] [PMID: 23516061]
[29]
Zhu, F.; Qian, C. Berberine chloride can ameliorate the spatial memory impairment and increase the expression of interleukin-1beta and inducible nitric oxide synthase in the rat model of Alzheimer’s disease. BMC Neurosci., 2006, 7, 78.
[http://dx.doi.org/10.1186/1471-2202-7-78] [PMID: 17137520]
[30]
Chen, C.C.; Hung, T.H.; Lee, C.Y.; Wang, L.F.; Wu, C.H.; Ke, C.H.; Chen, S.F. Berberine protects against neuronal damage via suppression of glia-mediated inflammation in traumatic brain injury. PLoS One, 2014, 9(12), e115694.
[http://dx.doi.org/10.1371/journal.pone.0115694] [PMID: 25546475]
[31]
Jiang, W.; Wei, W.; Gaertig, M.A.; Li, S.; Li, X.J. Therapeutic effect of berberine on Huntington’s disease transgenic mouse model. PLoS One, 2015, 10(7), e0134142.
[http://dx.doi.org/10.1371/journal.pone.0134142] [PMID: 26225560]
[32]
Huang, M.; Jiang, X.; Liang, Y.; Liu, Q.; Chen, S.; Guo, Y. Berberine improves cognitive impairment by promoting autophagic clearance and inhibiting production of β-amyloid in APP/tau/PS1 mouse model of Alzheimer’s disease. Exp. Gerontol., 2017, 91, 25-33.
[http://dx.doi.org/10.1016/j.exger.2017.02.004] [PMID: 28223223]
[33]
Albert, M.S.; DeKosky, S.T.; Dickson, D.; Dubois, B.; Feldman, H.H.; Fox, N.C.; Gamst, A.; Holtzman, D.M.; Jagust, W.J.; Petersen, R.C.; Snyder, P.J.; Carrillo, M.C.; Thies, B.; Phelps, C.H. The diagnosis of mild cognitive impairment due to Alzheimer’s disease: Recommendations from the National Institute on Aging-Alzheimer’s Association workgroups on diagnostic guidelines for Alzheimer’s disease. Alzheimers Dement., 2011, 7(3), 270-279.
[http://dx.doi.org/10.1016/j.jalz.2011.03.008] [PMID: 21514249]
[34]
Dubois, B.; Feldman, H.H.; Jacova, C.; Hampel, H.; Molinuevo, J.L.; Blennow, K.; DeKosky, S.T.; Gauthier, S.; Selkoe, D.; Bateman, R.; Cappa, S.; Crutch, S.; Engelborghs, S.; Frisoni, G.B.; Fox, N.C.; Galasko, D.; Habert, M.O.; Jicha, G.A.; Nordberg, A.; Pasquier, F.; Rabinovici, G.; Robert, P.; Rowe, C.; Salloway, S.; Sarazin, M.; Epelbaum, S.; de Souza, L.C.; Vellas, B.; Visser, P.J.; Schneider, L.; Stern, Y.; Scheltens, P.; Cummings, J.L. Advancing research diagnostic criteria for Alzheimer’s disease: the IWG-2 criteria. Lancet Neurol., 2014, 13(6), 614-629.
[http://dx.doi.org/10.1016/S1474-4422(14)70090-0] [PMID: 24849862]
[35]
2017 Alzheimer’s disease facts and figures. Alzheimers Dement., 2017, 13(4), 325-373.
[http://dx.doi.org/10.1016/j.jalz.2017.02.001]
[36]
Jiang, T.; Yu, J.T.; Tian, Y.; Tan, L. Epidemiology and etiology of Alzheimer’s disease: from genetic to non-genetic factors. Curr. Alzheimer Res., 2013, 10(8), 852-867.
[http://dx.doi.org/10.2174/15672050113109990155] [PMID: 23919770]
[37]
Talwar, P.; Sinha, J.; Grover, S.; Rawat, C.; Kushwaha, S.; Agarwal, R.; Taneja, V.; Kukreti, R. Dissecting complex and multifactorial nature of alzheimer’s disease pathogenesis: A clinical, genomic, and systems biology perspective. Mol. Neurobiol., 2016, 53(7), 4833-4864.
[http://dx.doi.org/10.1007/s12035-015-9390-0] [PMID: 26351077]
[38]
Coyle, J.T.; Price, D.L.; DeLong, M.R. Alzheimer’s disease: A disorder of cortical cholinergic innervation. Science, 1983, 219(4589), 1184-1190.
[http://dx.doi.org/10.1126/science.6338589] [PMID: 6338589]
[39]
Hardy, J.; Selkoe, D.J. The amyloid hypothesis of Alzheimer’s disease: Progress and problems on the road to therapeutics. Science, 2002, 297(5580), 353-356.
[http://dx.doi.org/10.1126/science.1072994] [PMID: 12130773]
[40]
Grundke-Iqbal, I.; Iqbal, K.; Tung, Y.C.; Quinlan, M.; Wisniewski, H.M.; Binder, L.I. Abnormal phosphorylation of the microtubule-associated protein tau (tau) in Alzheimer cytoskeletal pathology. Proc. Natl. Acad. Sci. USA, 1986, 83(13), 4913-4917.
[http://dx.doi.org/10.1073/pnas.83.13.4913] [PMID: 3088567]
[41]
Ittner, L.M.; Götz, J. Amyloid-β and tau--a toxic pas de deux in Alzheimer’s disease. Nat. Rev. Neurosci., 2011, 12(2), 65-72.
[http://dx.doi.org/10.1038/nrn2967] [PMID: 21193853]
[42]
Akiyama, H.; Barger, S.; Barnum, S.; Bradt, B.; Bauer, J.; Cole, G.M.; Cooper, N.R.; Eikelenboom, P.; Emmerling, M.; Fiebich, B.L.; Finch, C.E.; Frautschy, S.; Griffin, W.S.; Hampel, H.; Hull, M.; Landreth, G.; Lue, L.; Mrak, R.; Mackenzie, I.R.; McGeer, P.L.; O’Banion, M.K.; Pachter, J.; Pasinetti, G.; Plata-Salaman, C.; Rogers, J.; Rydel, R.; Shen, Y.; Streit, W.; Strohmeyer, R.; Tooyoma, I.; Van Muiswinkel, F.L.; Veerhuis, R.; Walker, D.; Webster, S.; Wegrzyniak, B.; Wenk, G.; Wyss-Coray, T. Inflammation and Alzheimer’s disease. Neurobiol. Aging, 2000, 21(3), 383-421.
[http://dx.doi.org/10.1016/S0197-4580(00)00124-X] [PMID: 10858586]
[43]
Heneka, M.T.; Carson, M.J.; El Khoury, J.; Landreth, G.E.; Brosseron, F.; Feinstein, D.L.; Jacobs, A.H.; Wyss-Coray, T.; Vitorica, J.; Ransohoff, R.M.; Herrup, K.; Frautschy, S.A.; Finsen, B.; Brown, G.C.; Verkhratsky, A.; Yamanaka, K.; Koistinaho, J.; Latz, E.; Halle, A.; Petzold, G.C.; Town, T.; Morgan, D.; Shinohara, M.L.; Perry, V.H.; Holmes, C.; Bazan, N.G.; Brooks, D.J.; Hunot, S.; Joseph, B.; Deigendesch, N.; Garaschuk, O.; Boddeke, E.; Dinarello, C.A.; Breitner, J.C.; Cole, G.M.; Golenbock, D.T.; Kummer, M.P. Neuroinflammation in Alzheimer’s disease. Lancet Neurol., 2015, 14(4), 388-405.
[http://dx.doi.org/10.1016/S1474-4422(15)70016-5] [PMID: 25792098]
[44]
Lin, M.T.; Beal, M.F. Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature, 2006, 443(7113), 787-795.
[http://dx.doi.org/10.1038/nature05292] [PMID: 17051205]
[45]
Puglielli, L.; Tanzi, R.E.; Kovacs, D.M. Alzheimer’s disease: The cholesterol connection. Nat. Neurosci., 2003, 6(4), 345-351.
[http://dx.doi.org/10.1038/nn0403-345] [PMID: 12658281]
[46]
Di Paolo, G.; Kim, T.W. Linking lipids to Alzheimer’s disease: Cholesterol and beyond. Nat. Rev. Neurosci., 2011, 12(5), 284-296.
[http://dx.doi.org/10.1038/nrn3012] [PMID: 21448224]
[47]
Anand, R.; Gill, K.D.; Mahdi, A.A. Therapeutics of Alzheimer’s disease: Past, present and future. Neuropharmacology,, 2014, 76(Pt A), 27-50.
[http://dx.doi.org/10.1016/j.neuropharm.2013.07.004]] [PMID: 23891641]
[48]
Guzior, N.; Wieckowska, A.; Panek, D.; Malawska, B. Recent development of multifunctional agents as potential drug candidates for the treatment of Alzheimer’s disease. Curr. Med. Chem., 2015, 22(3), 373-404.
[http://dx.doi.org/10.2174/0929867321666141106122628] [PMID: 25386820]
[49]
León, R.; Garcia, A.G.; Marco-Contelles, J. Recent advances in the multitarget-directed ligands approach for the treatment of Alzheimer’s disease. Med. Res. Rev., 2013, 33(1), 139-189.
[http://dx.doi.org/10.1002/med.20248] [PMID: 21793014]
[50]
Agis-Torres, A.; Sölhuber, M.; Fernandez, M.; Sanchez-Montero, J.M. Multi-target-directed ligands and other therapeutic strategies in the search of a real solution for Alzheimer’s disease. Curr. Neuropharmacol., 2014, 12(1), 2-36.
[http://dx.doi.org/10.2174/1570159X113116660047] [PMID: 24533013]
[51]
Dias, K.S.; Viegas, C., Jr Multi-target directed drugs: a modern approach for design of new drugs for the treatment of Alzheimer’s disease. Curr. Neuropharmacol., 2014, 12(3), 239-255.
[http://dx.doi.org/10.2174/1570159X1203140511153200] [PMID: 24851088]
[52]
Rosini, M.; Simoni, E.; Caporaso, R.; Minarini, A. Multitarget strategies in Alzheimer’s disease: Benefits and challenges on the road to therapeutics. Future Med. Chem., 2016, 8(6), 697-711.
[http://dx.doi.org/10.4155/fmc-2016-0003] [PMID: 27079260]
[53]
Blusztajn, J.K.; Wurtman, R.J. Choline and cholinergic neurons. Science, 1983, 221(4611), 614-620.
[http://dx.doi.org/10.1126/science.6867732] [PMID: 6867732]
[54]
Tuček, S. Regulation of acetylcholine synthesis in the brain. J. Neurochem., 1985, 44(1), 11-24.
[http://dx.doi.org/10.1111/j.1471-4159.1985.tb07106.x] [PMID: 3880580]
[55]
Arendt, T.; Brückner, M.K.; Lange, M.; Bigl, V. Changes in acetylcholinesterase and butyrylcholinesterase in Alzheimer’s disease resemble embryonic development--a study of molecular forms. Neurochem. Int., 1992, 21(3), 381-396.
[http://dx.doi.org/10.1016/0197-0186(92)90189-X] [PMID: 1303164]
[56]
Talesa, V.N. Acetylcholinesterase in Alzheimer’s disease. Mech. Ageing Dev., 2001, 122(16), 1961-1969.
[http://dx.doi.org/10.1016/S0047-6374(01)00309-8] [PMID: 11589914]
[57]
Darvesh, S.; Hopkins, D.A.; Geula, C. Neurobiology of butyrylcholinesterase. Nat. Rev. Neurosci., 2003, 4(2), 131-138.
[http://dx.doi.org/10.1038/nrn1035] [PMID: 12563284]
[58]
Enz, A.; Amstutz, R.; Boddeke, H.; Gmelin, G.; Malanowski, J. Brain selective inhibition of acetylcholinesterase: A novel approach to therapy for Alzheimer’s disease. Prog. Brain Res, 1993, 98, 431-438.
[http://dx.doi.org/10.1016/S0079-6123(08)62429-2] [PMID: 8248533]
[59]
Lane, R.M.; Kivipelto, M.; Greig, N.H. Acetylcholinesterase and its inhibition in Alzheimer disease. Clin. Neuropharmacol., 2004, 27(3), 141-149.
[http://dx.doi.org/10.1097/00002826-200405000-00011] [PMID: 15190239]
[60]
Muñoz-Torrero, D. Acetylcholinesterase inhibitors as disease-modifying therapies for Alzheimer’s disease. Curr. Med. Chem., 2008, 15(24), 2433-2455.
[http://dx.doi.org/10.2174/092986708785909067] [PMID: 18855672]
[61]
Greig, N.H.; Utsuki, T.; Ingram, D.K.; Wang, Y.; Pepeu, G.; Scali, C.; Yu, Q.S.; Mamczarz, J.; Holloway, H.W.; Giordano, T.; Chen, D.; Furukawa, K.; Sambamurti, K.; Brossi, A.; Lahiri, D.K. Selective butyrylcholinesterase inhibition elevates brain acetylcholine, augments learning and lowers Alzheimer β-amyloid peptide in rodent. Proc. Natl. Acad. Sci. USA, 2005, 102(47), 17213-17218.
[http://dx.doi.org/10.1073/pnas.0508575102] [PMID: 16275899]
[62]
Ritchie, C.W.; Ames, D.; Clayton, T.; Lai, R. Metaanalysis of randomized trials of the efficacy and safety of donepezil, galantamine, and rivastigmine for the treatment of Alzheimer disease. Am. J. Geriatr. Psychiatry, 2004, 12(4), 358-369.
[http://dx.doi.org/10.1097/00019442-200407000-00003] [PMID: 15249273]
[63]
Kaduszkiewicz, H.; Zimmermann, T.; Beck-Bornholdt, H.P.; van den Bussche, H. Cholinesterase inhibitors for patients with Alzheimer’s disease: systematic review of randomised clinical trials. BMJ, 2005, 331(7512), 321-327.
[http://dx.doi.org/10.1136/bmj.331.7512.321] [PMID: 16081444]
[64]
Hansen, R.A.; Gartlehner, G.; Webb, A.P.; Morgan, L.C.; Moore, C.G.; Jonas, D.E. Efficacy and safety of donepezil, galantamine, and rivastigmine for the treatment of Alzheimer’s disease: A systematic review and meta-analysis. Clin. Interv. Aging, 2008, 3(2), 211-225.
[PMID: 18686744]
[65]
Huang, L.; Luo, Z.; He, F.; Lu, J.; Li, X. Synthesis and biological evaluation of a new series of berberine derivatives as dual inhibitors of acetylcholinesterase and butyrylcholinesterase. Bioorg. Med. Chem., 2010, 18(12), 4475-4484.
[http://dx.doi.org/10.1016/j.bmc.2010.04.063] [PMID: 20471843]
[66]
Mak, S.; Luk, W.W.; Cui, W.; Hu, S.; Tsim, K.W.; Han, Y. Synergistic inhibition on acetylcholinesterase by the combination of berberine and palmatine originally isolated from Chinese medicinal herbs. J. Mol. Neurosci., 2014, 53(3), 511-516.
[http://dx.doi.org/10.1007/s12031-014-0288-5] [PMID: 24793543]
[67]
Jung, H.A.; Min, B.S.; Yokozawa, T.; Lee, J.H.; Kim, Y.S.; Choi, J.S. Anti-Alzheimer and antioxidant activities of Coptidis Rhizoma alkaloids. Biol. Pharm. Bull., 2009, 32(8), 1433-1438.
[http://dx.doi.org/10.1248/bpb.32.1433] [PMID: 19652386]
[68]
Vassar, R.; Bennett, B.D.; Babu-Khan, S.; Kahn, S.; Mendiaz, E.A.; Denis, P.; Teplow, D.B.; Ross, S.; Amarante, P.; Loeloff, R.; Luo, Y.; Fisher, S.; Fuller, J.; Edenson, S.; Lile, J.; Jarosinski, M.A.; Biere, A.L.; Curran, E.; Burgess, T.; Louis, J.C.; Collins, F.; Treanor, J.; Rogers, G.; Citron, M. β-secretase cleavage of Alzheimer’s amyloid precursor protein by the transmembrane aspartic protease BACE. Science, 1999, 286(5440), 735-741.
[http://dx.doi.org/10.1126/science.286.5440.735] [PMID: 10531052]
[69]
Sinha, S.; Anderson, J.P.; Barbour, R.; Basi, G.S.; Caccavello, R.; Davis, D.; Doan, M.; Dovey, H.F.; Frigon, N.; Hong, J.; Jacobson-Croak, K.; Jewett, N.; Keim, P.; Knops, J.; Lieberburg, I.; Power, M.; Tan, H.; Tatsuno, G.; Tung, J.; Schenk, D.; Seubert, P.; Suomensaari, S.M.; Wang, S.; Walker, D.; Zhao, J.; McConlogue, L.; John, V. Purification and cloning of amyloid precursor protein β-secretase from human brain. Nature, 1999, 402(6761), 537-540.
[http://dx.doi.org/10.1038/990114] [PMID: 10591214]
[70]
Tanzi, R.E.; Bertram, L. Twenty years of the Alzheimer’s disease amyloid hypothesis: A genetic perspective. Cell, 2005, 120(4), 545-555.
[http://dx.doi.org/10.1016/j.cell.2005.02.008] [PMID: 15734686]
[71]
Iwatsubo, T.; Odaka, A.; Suzuki, N.; Mizusawa, H.; Nukina, N.; Ihara, Y. Visualization of A β 42(43) and A β 40 in senile plaques with end-specific A β monoclonals: Evidence that an initially deposited species is A β 42(43). Neuron, 1994, 13(1), 45-53.
[http://dx.doi.org/10.1016/0896-6273(94)90458-8] [PMID: 8043280]
[72]
Scheuner, D.; Eckman, C.; Jensen, M.; Song, X.; Citron, M.; Suzuki, N.; Bird, T.D.; Hardy, J.; Hutton, M.; Kukull, W.; Larson, E.; Levy-Lahad, E.; Viitanen, M.; Peskind, E.; Poorkaj, P.; Schellenberg, G.; Tanzi, R.; Wasco, W.; Lannfelt, L.; Selkoe, D.; Younkin, S. Secreted amyloid β-protein similar to that in the senile plaques of Alzheimer’s disease is increased in vivo by the presenilin 1 and 2 and APP mutations linked to familial Alzheimer’s disease. Nat. Med., 1996, 2(8), 864-870.
[http://dx.doi.org/10.1038/nm0896-864] [PMID: 8705854]
[73]
Haass, C.; Selkoe, D.J. Soluble protein oligomers in neurodegeneration: Lessons from the Alzheimer’s amyloid β-peptide. Nat. Rev. Mol. Cell Biol., 2007, 8(2), 101-112.
[http://dx.doi.org/10.1038/nrm2101] [PMID: 17245412]
[74]
Citron, M. Alzheimer’s disease: strategies for disease modification. Nat. Rev. Drug Discov., 2010, 9(5), 387-398.
[http://dx.doi.org/10.1038/nrd2896] [PMID: 20431570]
[75]
Huang, Y.; Mucke, L. Alzheimer mechanisms and therapeutic strategies. Cell, 2012, 148(6), 1204-1222.
[http://dx.doi.org/10.1016/j.cell.2012.02.040] [PMID: 22424230]
[76]
Asai, M.; Iwata, N.; Yoshikawa, A.; Aizaki, Y.; Ishiura, S.; Saido, T.C.; Maruyama, K. Berberine alters the processing of Alzheimer’s amyloid precursor protein to decrease Abeta secretion. Biochem. Biophys. Res. Commun., 2007, 352(2), 498-502.
[http://dx.doi.org/10.1016/j.bbrc.2006.11.043] [PMID: 17125739]
[77]
Shi, A.; Huang, L.; Lu, C.; He, F.; Li, X. Synthesis, biological evaluation and molecular modeling of novel triazole-containing berberine derivatives as acetylcholinesterase and β-amyloid aggregation inhibitors. Bioorg. Med. Chem., 2011, 19(7), 2298-2305.
[http://dx.doi.org/10.1016/j.bmc.2011.02.025] [PMID: 21397508]
[78]
Zhu, F.; Wu, F.; Ma, Y.; Liu, G.; Li, Z.; Sun, Y.; Pei, Z. Decrease in the production of β-amyloid by berberine inhibition of the expression of β-secretase in HEK293 cells. BMC Neurosci., 2011, 12, 125.
[http://dx.doi.org/10.1186/1471-2202-12-125] [PMID: 22152059]
[79]
Zhang, H.; Zhao, C.; Cao, G.; Guo, L.; Zhang, S.; Liang, Y.; Qin, C.; Su, P.; Li, H.; Zhang, W. Berberine modulates amyloid-β peptide generation by activating AMP-activated protein kinase. Neuropharmacology, 2017, 125, 408-417.
[http://dx.doi.org/10.1016/j.neuropharm.2017.08.013] [PMID: 28822725]
[80]
Haghani, M.; Shabani, M.; Tondar, M. The therapeutic potential of berberine against the altered intrinsic properties of the CA1 neurons induced by Aβ neurotoxicity. Eur. J. Pharmacol., 2015, 758, 82-88.
[http://dx.doi.org/10.1016/j.ejphar.2015.03.016] [PMID: 25861937]
[81]
Hernández, F.; Gómez de Barreda, E.; Fuster-Matanzo, A.; Lucas, J.J.; Avila, J. GSK3: A possible link between beta amyloid peptide and tau protein. Exp. Neurol., 2010, 223(2), 322-325.
[http://dx.doi.org/10.1016/j.expneurol.2009.09.011] [PMID: 19782073]
[82]
Hooper, C.; Killick, R.; Lovestone, S. The GSK3 hypothesis of Alzheimer’s disease. J. Neurochem., 2008, 104(6), 1433-1439.
[http://dx.doi.org/10.1111/j.1471-4159.2007.05194.x] [PMID: 18088381]
[83]
Llorens-Martín, M.; Jurado, J.; Hernández, F.; Avila, J. GSK-3β, a pivotal kinase in Alzheimer disease. Front. Mol. Neurosci., 2014, 7, 46.
[PMID: 24904272]
[84]
Leclerc, S.; Garnier, M.; Hoessel, R.; Marko, D.; Bibb, J.A.; Snyder, G.L.; Greengard, P.; Biernat, J.; Wu, Y.Z.; Mandelkow, E.M.; Eisenbrand, G.; Meijer, L. Indirubins inhibit glycogen synthase kinase-3 beta and CDK5/p25, two protein kinases involved in abnormal tau phosphorylation in Alzheimer’s disease. A property common to most cyclin-dependent kinase inhibitors? J. Biol. Chem., 2001, 276(1), 251-260.
[http://dx.doi.org/10.1074/jbc.M002466200] [PMID: 11013232]
[85]
Sontag, E.; Nunbhakdi-Craig, V.; Lee, G.; Bloom, G.S.; Mumby, M.C. Regulation of the phosphorylation state and microtubule-binding activity of Tau by protein phosphatase 2A. Neuron, 1996, 17(6), 1201-1207.
[http://dx.doi.org/10.1016/S0896-6273(00)80250-0] [PMID: 8982166]
[86]
Sontag, E.; Nunbhakdi-Craig, V.; Lee, G.; Brandt, R.; Kamibayashi, C.; Kuret, J.; White, C.L., III; Mumby, M.C.; Bloom, G.S. Molecular interactions among protein phosphatase 2A, tau, and microtubules. Implications for the regulation of tau phosphorylation and the development of tauopathies. J. Biol. Chem., 1999, 274(36), 25490-25498.
[http://dx.doi.org/10.1074/jbc.274.36.25490] [PMID: 10464280]
[87]
Gong, C.X.; Lidsky, T.; Wegiel, J.; Zuck, L.; Grundke-Iqbal, I.; Iqbal, K. Phosphorylation of microtubule-associated protein tau is regulated by protein phosphatase 2A in mammalian brain. Implications for neurofibrillary degeneration in Alzheimer’s disease. J. Biol. Chem., 2000, 275(8), 5535-5544.
[http://dx.doi.org/10.1074/jbc.275.8.5535] [PMID: 10681533]
[88]
Kins, S.; Crameri, A.; Evans, D.R.; Hemmings, B.A.; Nitsch, R.M.; Gotz, J. Reduced protein phosphatase 2A activity induces hyperphosphorylation and altered compartmentalization of tau in transgenic mice. J. Biol. Chem., 2001, 276(41), 38193-38200.
[PMID: 11473109]
[89]
Yu, G.; Li, Y.; Tian, Q.; Liu, R.; Wang, Q.; Wang, J.Z.; Wang, X. Berberine attenuates calyculin A-induced cytotoxicity and Tau hyperphosphorylation in HEK293 cells. J. Alzheimers Dis., 2011, 24(3), 525-535.
[http://dx.doi.org/10.3233/JAD-2011-101779] [PMID: 21297267]
[90]
Ascherio, A.; Schwarzschild, M.A. The epidemiology of Parkinson’s disease: risk factors and prevention. Lancet Neurol., 2016, 15(12), 1257-1272.
[http://dx.doi.org/10.1016/S1474-4422(16)30230-7] [PMID: 27751556]
[91]
Pringsheim, T.; Jette, N.; Frolkis, A.; Steeves, T.D. The prevalence of Parkinson’s disease: A systematic review and meta-analysis. Mov. Disord., 2014, 29(13), 1583-1590.
[http://dx.doi.org/10.1002/mds.25945] [PMID: 24976103]
[92]
Przedborski, S. The two-century journey of Parkinson disease research. Nat. Rev. Neurosci., 2017, 18(4), 251-259.
[http://dx.doi.org/10.1038/nrn.2017.25] [PMID: 28303016]
[93]
Postuma, R.B.; Berg, D.; Adler, C.H.; Bloem, B.R.; Chan, P.; Deuschl, G.; Gasser, T.; Goetz, C.G.; Halliday, G.; Joseph, L.; Lang, A.E.; Liepelt-Scarfone, I.; Litvan, I.; Marek, K.; Oertel, W.; Olanow, C.W.; Poewe, W.; Stern, M. The new definition and diagnostic criteria of Parkinson’s disease. Lancet Neurol., 2016, 15(6), 546-548.
[http://dx.doi.org/10.1016/S1474-4422(16)00116-2] [PMID: 27302120]
[94]
Postuma, R.B.; Berg, D.; Stern, M.; Poewe, W.; Olanow, C.W.; Oertel, W.; Obeso, J.; Marek, K.; Litvan, I.; Lang, A.E.; Halliday, G.; Goetz, C.G.; Gasser, T.; Dubois, B.; Chan, P.; Bloem, B.R.; Adler, C.H.; Deuschl, G. MDS clinical diagnostic criteria for Parkinson’s disease. Mov. Disord., 2015, 30(12), 1591-1601.
[http://dx.doi.org/10.1002/mds.26424] [PMID: 26474316]
[95]
Schapira, A.H.V.; Chaudhuri, K.R.; Jenner, P. Non-motor features of Parkinson disease. Nat. Rev. Neurosci., 2017, 18(7), 435-450.
[http://dx.doi.org/10.1038/nrn.2017.62] [PMID: 28592904]
[96]
Chaudhuri, K.R.; Healy, D.G.; Schapira, A.H. Non-motor symptoms of Parkinson’s disease: Diagnosis and management. Lancet Neurol., 2006, 5(3), 235-245.
[http://dx.doi.org/10.1016/S1474-4422(06)70373-8] [PMID: 16488379]
[97]
Surmeier, D.J.; Obeso, J.A.; Halliday, G.M. Selective neuronal vulnerability in Parkinson disease. Nat. Rev. Neurosci., 2017, 18(2), 101-113.
[http://dx.doi.org/10.1038/nrn.2016.178] [PMID: 28104909]
[98]
Hirsch, E.C.; Jenner, P.; Przedborski, S. Pathogenesis of Parkinson’s disease. Mov. Disord., 2013, 28(1), 24-30.
[http://dx.doi.org/10.1002/mds.25032] [PMID: 22927094]
[99]
Dexter, D.T.; Jenner, P. Parkinson disease: From pathology to molecular disease mechanisms. Free Radic. Biol. Med., 2013, 62, 132-144.
[http://dx.doi.org/10.1016/j.freeradbiomed.2013.01.018] [PMID: 23380027]
[100]
Dauer, W.; Przedborski, S. Parkinson’s disease: mechanisms and models. Neuron, 2003, 39(6), 889-909.
[http://dx.doi.org/10.1016/S0896-6273(03)00568-3] [PMID: 12971891]
[101]
Braak, H.; Del Tredici, K.; Rüb, U.; de Vos, R.A.; Jansen Steur, E.N.; Braak, E. Staging of brain pathology related to sporadic Parkinson’s disease. Neurobiol. Aging, 2003, 24(2), 197-211.
[http://dx.doi.org/10.1016/S0197-4580(02)00065-9] [PMID: 12498954]
[102]
Damier, P.; Hirsch, E.C.; Agid, Y.; Graybiel, A.M. The substantia nigra of the human brain. II. Patterns of loss of dopamine-containing neurons in Parkinson’s disease. Brain, 1999, 122(Pt 8), 1437-1448.
[http://dx.doi.org/10.1093/brain/122.8.1437] [PMID: 10430830]
[103]
Spillantini, M.G.; Schmidt, M.L.; Lee, V.M.; Trojanowski, J.Q.; Jakes, R.; Goedert, M. α-synuclein in Lewy bodies. Nature, 1997, 388(6645), 839-840.
[http://dx.doi.org/10.1038/42166] [PMID: 9278044]
[104]
Baba, M.; Nakajo, S.; Tu, P.H.; Tomita, T.; Nakaya, K.; Lee, V.M.; Trojanowski, J.Q.; Iwatsubo, T. Aggregation of alpha-synuclein in Lewy bodies of sporadic Parkinson’s disease and dementia with Lewy bodies. Am. J. Pathol., 1998, 152(4), 879-884.
[PMID: 9546347]
[105]
Spillantini, M.G.; Crowther, R.A.; Jakes, R.; Hasegawa, M.; Goedert, M. α-Synuclein in filamentous inclusions of Lewy bodies from Parkinson’s disease and dementia with lewy bodies. Proc. Natl. Acad. Sci. USA, 1998, 95(11), 6469-6473.
[http://dx.doi.org/10.1073/pnas.95.11.6469] [PMID: 9600990]
[106]
Shen, T.; Pu, J.; Si, X.; Ye, R.; Zhang, B. An update on potential therapeutic strategies for Parkinson’s disease based on pathogenic mechanisms. Expert Rev. Neurother., 2016, 16(6), 711-722.
[http://dx.doi.org/10.1080/14737175.2016.1179112] [PMID: 27138872]
[107]
Lindholm, D.; Mäkelä, J.; Di Liberto, V.; Mudò, G.; Belluardo, N.; Eriksson, O.; Saarma, M. Current disease modifying approaches to treat Parkinson’s disease. Cell. Mol. Life Sci., 2016, 73(7), 1365-1379.
[http://dx.doi.org/10.1007/s00018-015-2101-1] [PMID: 26616211]
[108]
Pires, A.O.; Teixeira, F.G.; Mendes-Pinheiro, B.; Serra, S.C.; Sousa, N.; Salgado, A.J. Old and new challenges in Parkinson’s disease therapeutics. Prog. Neurobiol., 2017, 156, 69-89.
[http://dx.doi.org/10.1016/j.pneurobio.2017.04.006] [PMID: 28457671]
[109]
Connolly, B.S.; Lang, A.E. Pharmacological treatment of Parkinson disease: A review. JAMA, 2014, 311(16), 1670-1683.
[http://dx.doi.org/10.1001/jama.2014.3654] [PMID: 24756517]
[110]
Fahn, S.; Poewe, W. Levodopa: 50 years of a revolutionary drug for Parkinson disease. Mov. Disord., 2015, 30(1), 1-3.
[http://dx.doi.org/10.1002/mds.26122] [PMID: 25488146]
[111]
Tomlinson, C.L.; Stowe, R.; Patel, S.; Rick, C.; Gray, R.; Clarke, C.E. Systematic review of levodopa dose equivalency reporting in Parkinson’s disease. Mov. Disord., 2010, 25(15), 2649-2653.
[http://dx.doi.org/10.1002/mds.23429] [PMID: 21069833]
[112]
Fernandez, H.H.; Chen, J.J. Monoamine oxidase-B inhibition in the treatment of Parkin-son's disease. Pharmacotherapy, 2007, 27(12P2), 174S-185S.
[http://dx.doi.org/10.1592/phco.27.12part2.174S]
[113]
Youdim, M.B.; Edmondson, D.; Tipton, K.F. The therapeutic potential of monoamine oxidase inhibitors. Nat. Rev. Neurosci., 2006, 7(4), 295-309.
[http://dx.doi.org/10.1038/nrn1883] [PMID: 16552415]
[114]
LeWitt, P.A. Levodopa therapy for Parkinson’s disease: Pharmacokinetics and pharmacodynamics. Mov. Disord., 2015, 30(1), 64-72.
[http://dx.doi.org/10.1002/mds.26082] [PMID: 25449210]
[115]
Fahn, S.; Oakes, D.; Shoulson, I.; Kieburtz, K.; Rudolph, A.; Lang, A.; Olanow, C.W.; Tanner, C.; Marek, K. Levodopa and the progression of Parkinson’s disease. N. Engl. J. Med., 2004, 351(24), 2498-2508.
[http://dx.doi.org/10.1056/NEJMoa033447] [PMID: 15590952]
[116]
Poletti, M.; Bonuccelli, U. Acute and chronic cognitive effects of levodopa and dopamine agonists on patients with Parkinson’s disease: A review. Ther. Adv. Psychopharmacol., 2013, 3(2), 101-113.
[http://dx.doi.org/10.1177/2045125312470130] [PMID: 24167681]
[117]
Glover, V.; Sandler, M.; Owen, F.; Riley, G.J. Dopamine is a monoamine oxidase B substrate in man. Nature, 1977, 265(5589), 80-81.
[http://dx.doi.org/10.1038/265080a0] [PMID: 834248]
[118]
Westlund, K.N.; Denney, R.M.; Kochersperger, L.M.; Rose, R.M.; Abell, C.W. Distinct monoamine oxidase A and B populations in primate brain. Science, 1985, 230(4722), 181-183.
[http://dx.doi.org/10.1126/science.3875898] [PMID: 3875898]
[119]
Bach, A.W.; Lan, N.C.; Johnson, D.L.; Abell, C.W.; Bembenek, M.E.; Kwan, S.W.; Seeburg, P.H.; Shih, J.C. cDNA cloning of human liver monoamine oxidase A and B: Molecular basis of differences in enzymatic properties. Proc. Natl. Acad. Sci. USA, 1988, 85(13), 4934-4938.
[http://dx.doi.org/10.1073/pnas.85.13.4934] [PMID: 3387449]
[120]
Shih, J.C.; Chen, K.; Ridd, M.J. Monoamine oxidase: From genes to behavior. Annu. Rev. Neurosci., 1999, 22, 197-217.
[http://dx.doi.org/10.1146/annurev.neuro.22.1.197] [PMID: 10202537]
[121]
Hauser, R.A.; Li, R.; Pérez, A.; Ren, X.; Weintraub, D.; Elm, J.; Goudreau, J.L.; Morgan, J.C.; Fang, J.Y.; Aminoff, M.J.; Christine, C.W.; Dhall, R.; Umeh, C.C.; Boyd, J.T.; Stover, N.; Leehey, M.; Zweig, R.M.; Nicholas, A.P.; Bodis-Wollner, I.; Willis, A.; Kieburtz, K.; Tilley, B.C. Longer duration of MAO-B inhibitor exposure is associated with less clinical decline in parkinson’s disease: An analysis of NET-PD LS1. J. Parkinsons Dis., 2017, 7(1), 117-127.
[http://dx.doi.org/10.3233/JPD-160965] [PMID: 27911341]
[122]
Teo, K.C.; Ho, S.L. Monoamine oxidase-B (MAO-B) inhibitors: Implications for disease-modification in Parkinson’s disease. Transl. Neurodegener., 2013, 2(1), 19.
[http://dx.doi.org/10.1186/2047-9158-2-19] [PMID: 24011391]
[123]
Rabey, J.M.; Sagi, I.; Huberman, M.; Melamed, E.; Korczyn, A.; Giladi, N.; Inzelberg, R.; Djaldetti, R.; Klein, C.; Berecz, G. Rasagiline mesylate, a new MAO-B inhibitor for the treatment of Parkinson’s disease: A double-blind study as adjunctive therapy to levodopa. Clin. Neuropharmacol., 2000, 23(6), 324-330.
[http://dx.doi.org/10.1097/00002826-200011000-00005] [PMID: 11575866]
[124]
Tetrud, J.W.; Langston, J.W. The effect of deprenyl (selegiline) on the natural history of Parkinson’s disease. Science, 1989, 245(4917), 519-522.
[http://dx.doi.org/10.1126/science.2502843] [PMID: 2502843]
[125]
Lees, A.J. Comparison of therapeutic effects and mortality data of levodopa and levodopa combined with selegiline in patients with early, mild Parkinson’s disease. BMJ, 1995, 311(7020), 1602-1607.
[http://dx.doi.org/10.1136/bmj.311.7020.1602] [PMID: 8555803]
[126]
Olanow, C.W.; Rascol, O.; Hauser, R.; Feigin, P.D.; Jankovic, J.; Lang, A.; Langston, W.; Melamed, E.; Poewe, W.; Stocchi, F.; Tolosa, E.; Investigators, A.S. A double-blind, delayed-start trial of rasagiline in Parkinson’s disease. N. Engl. J. Med., 2009, 361(13), 1268-1278.
[http://dx.doi.org/10.1056/NEJMoa0809335] [PMID: 19776408]
[127]
A controlled, randomized, delayed-start study of rasagiline in early Parkinson disease. Arch. Neurol., 2004, 61(4), 561-566.
[http://dx.doi.org/10.1001/archneur.61.4.561] [PMID: 15096406]
[128]
Rascol, O.; Brooks, D.J.; Melamed, E.; Oertel, W.; Poewe, W.; Stocchi, F.; Tolosa, E. Rasagiline as an adjunct to levodopa in patients with Parkinson’s disease and motor fluctuations (LARGO, Lasting effect in Adjunct therapy with Rasagiline Given Once daily, study): a randomised, double-blind, parallel-group trial. Lancet, 2005, 365(9463), 947-954.
[http://dx.doi.org/10.1016/S0140-6736(05)71083-7] [PMID: 15766996]
[129]
Robakis, D.; Fahn, S. Defining the role of the monoamine oxidase-B inhibitors for Parkinson’s disease. CNS Drugs, 2015, 29(6), 433-441.
[http://dx.doi.org/10.1007/s40263-015-0249-8] [PMID: 26164425]
[130]
Youdim, M.B.; Edmondson, D.; Tipton, K.F. The therapeutic potential of monoamine oxidase inhibitors. Nat. Rev. Neurosci., 2006, 7(4), 295-309.
[http://dx.doi.org/10.1038/nrn1883] [PMID: 16552415]
[131]
Lee, S.S.; Kai, M.; Lee, M.K. Effects of natural isoquinoline alkaloids on monoamine oxidase activity in mouse brain: Inhibition by berberine and palmatine. Med. Sci. Res., 1999, 27(11), 749-751.
[132]
Castillo, J.; Hung, J.; Rodriguez, M.; Bastidas, E.; Laboren, I.; Jaimes, A. LED fluorescence spectroscopy for direct determination of monoamine oxidase B inactivation. Anal. Biochem., 2005, 343(2), 293-298.
[http://dx.doi.org/10.1016/j.ab.2005.05.027] [PMID: 16004952]
[133]
Zhang, J.; Yang, J.Q.; He, B.C.; Zhou, Q.X.; Yu, H.R.; Tang, Y.; Liu, B.Z. Berberine and total base from rhizoma coptis chinensis attenuate brain injury in an aluminum-induced rat model of neurodegenerative disease. Saudi Med. J., 2009, 30(6), 760-766.
[PMID: 19526156]
[134]
Bae, J.; Lee, D.; Kim, Y.K.; Gil, M.; Lee, J.Y.; Lee, K.J. Berberine protects 6-hydroxydopamine-induced human dopaminergic neuronal cell death through the induction of heme oxygenase-1. Mol. Cells, 2013, 35(2), 151-157.
[http://dx.doi.org/10.1007/s10059-013-2298-5] [PMID: 23329300]
[135]
Shin, K.S.; Choi, H.S.; Zhao, T.T.; Suh, K.H.; Kwon, I.H.; Choi, S.O.; Lee, M.K. Neurotoxic effects of berberine on long-term L-DOPA administration in 6-hydroxydopamine-lesioned rat model of Parkinson’s disease. Arch. Pharm. Res., 2013, 36(6), 759-767.
[http://dx.doi.org/10.1007/s12272-013-0051-4] [PMID: 23539311]
[136]
Kwon, I.H.; Choi, H.S.; Shin, K.S.; Lee, B.K.; Lee, C.K.; Hwang, B.Y.; Lim, S.C.; Lee, M.K. Effects of berberine on 6-hydroxydopamine-induced neurotoxicity in PC12 cells and a rat model of Parkinson’s disease. Neurosci. Lett., 2010, 486(1), 29-33.
[http://dx.doi.org/10.1016/j.neulet.2010.09.038] [PMID: 20851167]
[137]
Bates, G.P.; Dorsey, R.; Gusella, J.F.; Hayden, M.R.; Kay, C.; Leavitt, B.R.; Nance, M.; Ross, C.A.; Scahill, R.I.; Wetzel, R.; Wild, E.J.; Tabrizi, S.J. Huntington disease. Nat. Rev. Dis. Primers, 2015, 1, 15005.
[http://dx.doi.org/10.1038/nrdp.2015.5] [PMID: 27188817]
[138]
Walker, F.O. Huntington’s disease. Lancet, 2007, 369(9557), 218-228.
[http://dx.doi.org/10.1016/S0140-6736(07)60111-1] [PMID: 17240289]
[139]
Rawlins, M.D.; Wexler, N.S.; Wexler, A.R.; Tabrizi, S.J.; Douglas, I.; Evans, S.J.; Smeeth, L. The prevalence of Huntington’s disease. Neuroepidemiology, 2016, 46(2), 144-153.
[http://dx.doi.org/10.1159/000443738] [PMID: 26824438]
[140]
Ross, C.A.; Tabrizi, S.J. Huntington’s disease: From molecular pathogenesis to clinical treatment. Lancet Neurol., 2011, 10(1), 83-98.
[http://dx.doi.org/10.1016/S1474-4422(10)70245-3] [PMID: 21163446]
[141]
Labbadia, J.; Morimoto, R.I. Huntington’s disease: Underlying molecular mechanisms and emerging concepts. Trends Biochem. Sci., 2013, 38(8), 378-385.
[http://dx.doi.org/10.1016/j.tibs.2013.05.003] [PMID: 23768628]
[142]
Identification of genetic factors that modify clinical onset of Huntington’s disease. Cell, 2015, 162(3), 516-526.
[http://dx.doi.org/10.1016/j.cell.2015.07.003] [PMID: 26232222]
[143]
DiFiglia, M.; Sapp, E.; Chase, K.O.; Davies, S.W.; Bates, G.P.; Vonsattel, J.P.; Aronin, N. Aggregation of huntingtin in neuronal intranuclear inclusions and dystrophic neurites in brain. Science, 1997, 277(5334), 1990-1993.
[http://dx.doi.org/10.1126/science.277.5334.1990] [PMID: 9302293]
[144]
Scherzinger, E.; Sittler, A.; Schweiger, K.; Heiser, V.; Lurz, R.; Hasenbank, R.; Bates, G.P.; Lehrach, H.; Wanker, E.E. Self-assembly of polyglutamine-containing huntingtin fragments into amyloid-like fibrils: implications for Huntington’s disease pathology. Proc. Natl. Acad. Sci. USA, 1999, 96(8), 4604-4609.
[http://dx.doi.org/10.1073/pnas.96.8.4604] [PMID: 10200309]
[145]
Bates, G. Huntingtin aggregation and toxicity in Huntington’s disease. Lancet, 2003, 361(9369), 1642-1644.
[http://dx.doi.org/10.1016/S0140-6736(03)13304-1] [PMID: 12747895]
[146]
Cicchetti, F.; Lacroix, S.; Cisbani, G.; Vallières, N.; Saint-Pierre, M.; St-Amour, I.; Tolouei, R.; Skepper, J.N.; Hauser, R.A.; Mantovani, D.; Barker, R.A.; Freeman, T.B. Mutant huntingtin is present in neuronal grafts in Huntington disease patients. Ann. Neurol., 2014, 76(1), 31-42.
[http://dx.doi.org/10.1002/ana.24174] [PMID: 24798518]
[147]
Mangiarini, L.; Sathasivam, K.; Seller, M.; Cozens, B.; Harper, A.; Hetherington, C.; Lawton, M.; Trottier, Y.; Lehrach, H.; Davies, S.W.; Bates, G.P. Exon 1 of the HD gene with an expanded CAG repeat is sufficient to cause a progressive neurological phenotype in transgenic mice. Cell, 1996, 87(3), 493-506.
[http://dx.doi.org/10.1016/S0092-8674(00)81369-0] [PMID: 8898202]
[148]
Andrew, S.E.; Goldberg, Y.P.; Kremer, B.; Telenius, H.; Theilmann, J.; Adam, S.; Starr, E.; Squitieri, F.; Lin, B.; Kalchman, M.A. The relationship between trinucleotide (CAG) repeat length and clinical features of Huntington’s disease. Nat. Genet., 1993, 4(4), 398-403.
[http://dx.doi.org/10.1038/ng0893-398] [PMID: 8401589]
[149]
Morley, J.F.; Brignull, H.R.; Weyers, J.J.; Morimoto, R.I. The threshold for polyglutamine-expansion protein aggregation and cellular toxicity is dynamic and influenced by aging in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA, 2002, 99(16), 10417-10422.
[http://dx.doi.org/10.1073/pnas.152161099] [PMID: 12122205]
[150]
Langbehn, D.R.; Brinkman, R.R.; Falush, D.; Paulsen, J.S.; Hayden, M.R. A new model for prediction of the age of onset and penetrance for Huntington’s disease based on CAG length. Clin. Genet., 2004, 65(4), 267-277.
[http://dx.doi.org/10.1111/j.1399-0004.2004.00241.x] [PMID: 15025718]
[151]
Rué, L.; Bañez-Coronel, M.; Creus-Muncunill, J.; Giralt, A.; Alcalá-Vida, R.; Mentxaka, G.; Kagerbauer, B.; Zomeño-Abellán, M.T.; Aranda, Z.; Venturi, V.; Pérez-Navarro, E.; Estivill, X.; Martí, E. Targeting CAG repeat RNAs reduces Huntington’s disease phenotype independently of huntingtin levels. J. Clin. Invest., 2016, 126(11), 4319-4330.
[http://dx.doi.org/10.1172/JCI83185] [PMID: 27721240]
[152]
Sarkar, S.; Rubinsztein, D.C. Huntington’s disease: Degradation of mutant huntingtin by autophagy. FEBS J., 2008, 275(17), 4263-4270.
[http://dx.doi.org/10.1111/j.1742-4658.2008.06562.x] [PMID: 18637946]
[153]
Martinez-Vicente, M.; Talloczy, Z.; Wong, E.; Tang, G.; Koga, H.; Kaushik, S.; de Vries, R.; Arias, E.; Harris, S.; Sulzer, D.; Cuervo, A.M. Cargo recognition failure is responsible for inefficient autophagy in Huntington’s disease. Nat. Neurosci., 2010, 13(5), 567-576.
[http://dx.doi.org/10.1038/nn.2528] [PMID: 20383138]
[154]
Martin, D.D.; Ladha, S.; Ehrnhoefer, D.E.; Hayden, M.R. Autophagy in Huntington disease and huntingtin in autophagy. Trends Neurosci., 2015, 38(1), 26-35.
[http://dx.doi.org/10.1016/j.tins.2014.09.003] [PMID: 25282404]
[155]
Mizushima, N.; Klionsky, D.J. Protein turnover via autophagy: Implications for metabolism. Annu. Rev. Nutr., 2007, 27, 19-40.
[http://dx.doi.org/10.1146/annurev.nutr.27.061406.093749] [PMID: 17311494]
[156]
Mizushima, N.; Komatsu, M. Autophagy: Renovation of cells and tissues. Cell, 2011, 147(4), 728-741.
[http://dx.doi.org/10.1016/j.cell.2011.10.026] [PMID: 22078875]
[157]
Mizushima, N.; Levine, B.; Cuervo, A.M.; Klionsky, D.J. Autophagy fights disease through cellular self-digestion. Nature, 2008, 451(7182), 1069-1075.
[http://dx.doi.org/10.1038/nature06639] [PMID: 18305538]
[158]
Hara, T.; Nakamura, K.; Matsui, M.; Yamamoto, A.; Nakahara, Y.; Suzuki-Migishima, R.; Yokoyama, M.; Mishima, K.; Saito, I.; Okano, H.; Mizushima, N. Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature, 2006, 441(7095), 885-889.
[http://dx.doi.org/10.1038/nature04724] [PMID: 16625204]
[159]
Nixon, R.A.; Wegiel, J.; Kumar, A.; Yu, W.H.; Peterhoff, C.; Cataldo, A.; Cuervo, A.M. Extensive involvement of autophagy in Alzheimer disease: An immuno-electron microscopy study. J. Neuropathol. Exp. Neurol., 2005, 64(2), 113-122.
[http://dx.doi.org/10.1093/jnen/64.2.113] [PMID: 15751225]
[160]
Boland, B.; Kumar, A.; Lee, S.; Platt, F.M.; Wegiel, J.; Yu, W.H.; Nixon, R.A. Autophagy induction and autophagosome clearance in neurons: Relationship to autophagic pathology in Alzheimer’s disease. J. Neurosci., 2008, 28(27), 6926-6937.
[http://dx.doi.org/10.1523/JNEUROSCI.0800-08.2008] [PMID: 18596167]
[161]
Lee, J.H.; Yu, W.H.; Kumar, A.; Lee, S.; Mohan, P.S.; Peterhoff, C.M.; Wolfe, D.M.; Martinez-Vicente, M.; Massey, A.C.; Sovak, G.; Uchiyama, Y.; Westaway, D.; Cuervo, A.M.; Nixon, R.A. Lysosomal proteolysis and autophagy require presenilin 1 and are disrupted by Alzheimer-related PS1 mutations. Cell, 2010, 141(7), 1146-1158.
[http://dx.doi.org/10.1016/j.cell.2010.05.008] [PMID: 20541250]
[162]
Nixon, R.A.; Yang, D.S. Autophagy failure in Alzheimer’s disease--locating the primary defect. Neurobiol. Dis., 2011, 43(1), 38-45.
[http://dx.doi.org/10.1016/j.nbd.2011.01.021] [PMID: 21296668]
[163]
Cuervo, A.M.; Stefanis, L.; Fredenburg, R.; Lansbury, P.T.; Sulzer, D. Impaired degradation of mutant α-synuclein by chaperone-mediated autophagy. Science, 2004, 305(5688), 1292-1295.
[http://dx.doi.org/10.1126/science.1101738] [PMID: 15333840]
[164]
Martinez-Vicente, M.; Talloczy, Z.; Kaushik, S.; Massey, A.C.; Mazzulli, J.; Mosharov, E.V.; Hodara, R.; Fredenburg, R.; Wu, D.C.; Follenzi, A.; Dauer, W.; Przedborski, S.; Ischiropoulos, H.; Lansbury, P.T.; Sulzer, D.; Cuervo, A.M. Dopamine-modified α-synuclein blocks chaperone-mediated autophagy. J. Clin. Invest., 2008, 118(2), 777-788.
[PMID: 18172548]
[165]
Zhang, H.; Duan, C.; Yang, H. Defective autophagy in Parkinson’s disease: Lessons from genetics. Mol. Neurobiol., 2015, 51(1), 89-104.
[http://dx.doi.org/10.1007/s12035-014-8787-5] [PMID: 24990317]
[166]
Sarkar, S.; Perlstein, E.O.; Imarisio, S.; Pineau, S.; Cordenier, A.; Maglathlin, R.L.; Webster, J.A.; Lewis, T.A.; O’Kane, C.J.; Schreiber, S.L.; Rubinsztein, D.C. Small molecules enhance autophagy and reduce toxicity in Huntington’s disease models. Nat. Chem. Biol., 2007, 3(6), 331-338.
[http://dx.doi.org/10.1038/nchembio883] [PMID: 17486044]
[167]
Floto, R.A.; Sarkar, S.; Perlstein, E.O.; Kampmann, B.; Schreiber, S.L.; Rubinsztein, D.C. Small molecule enhancers of rapamycin-induced TOR inhibition promote autophagy, reduce toxicity in Huntington’s disease models and enhance killing of mycobacteria by macrophages. Autophagy, 2007, 3(6), 620-622.
[http://dx.doi.org/10.4161/auto.4898] [PMID: 17786022]
[168]
Tsvetkov, A.S.; Miller, J.; Arrasate, M.; Wong, J.S.; Pleiss, M.A.; Finkbeiner, S. A small-molecule scaffold induces autophagy in primary neurons and protects against toxicity in a Huntington disease model. Proc. Natl. Acad. Sci. USA, 2010, 107(39), 16982-16987.
[http://dx.doi.org/10.1073/pnas.1004498107] [PMID: 20833817]
[169]
Schapira, A.H.; Olanow, C.W.; Greenamyre, J.T.; Bezard, E. Slowing of neurodegeneration in Parkinson’s disease and Huntington’s disease: Future therapeutic perspectives. Lancet, 2014, 384(9942), 545-555.
[http://dx.doi.org/10.1016/S0140-6736(14)61010-2] [PMID: 24954676]
[170]
Lin, Y.; Sheng, M.; Weng, Y.; Xu, R.; Lu, N.; Du, H.; Yu, W. Berberine protects against ischemia/reperfusion injury after orthotopic liver transplantation via activating Sirt1/FoxO3α induced autophagy. Biochem. Biophys. Res. Commun., 2017, 483(2), 885-891.
[http://dx.doi.org/10.1016/j.bbrc.2017.01.028] [PMID: 28077277]
[171]
He, Q.; Mei, D.; Sha, S.; Fan, S.; Wang, L.; Dong, M. ERK-dependent mTOR pathway is involved in berberine-induced autophagy in hepatic steatosis. J. Mol. Endocrinol., 2016, 57(4), 251-260.
[http://dx.doi.org/10.1530/JME-16-0139] [PMID: 27658958]
[172]
Domitrović, R.; Cvijanović, O.; Pernjak-Pugel, E.; Skoda, M.; Mikelić, L.; Crnčević-Orlić, Z. Berberine exerts nephroprotective effect against cisplatin-induced kidney damage through inhibition of oxidative/nitrosative stress, inflammation, autophagy and apoptosis. Food Chem. Toxicol., 2013, 62, 397-406.
[http://dx.doi.org/10.1016/j.fct.2013.09.003] [PMID: 24025684]
[173]
Jin, Y.; Liu, S.; Ma, Q.; Xiao, D.; Chen, L. Berberine enhances the AMPK activation and autophagy and mitigates high glucose-induced apoptosis of mouse podocytes. Eur. J. Pharmacol., 2017, 794, 106-114.
[http://dx.doi.org/10.1016/j.ejphar.2016.11.037] [PMID: 27887947]
[174]
Zhang, Q.; Bian, H.; Guo, L.; Zhu, H. Pharmacologic preconditioning with berberine attenuating ischemia-induced apoptosis and promoting autophagy in neuron. Am. J. Transl. Res., 2016, 8(2), 1197-1207.
[PMID: 27158406]
[175]
Li, M.H.; Zhang, Y.J.; Yu, Y.H.; Yang, S.H.; Iqbal, J.; Mi, Q.Y.; Li, B.; Wang, Z.M.; Mao, W.X.; Xie, H.G.; Chen, S.L. Berberine improves pressure overload-induced cardiac hypertrophy and dysfunction through enhanced autophagy. Eur. J. Pharmacol., 2014, 728, 67-76.
[http://dx.doi.org/10.1016/j.ejphar.2014.01.061] [PMID: 24508518]
[176]
Zhang, Y.J.; Yang, S.H.; Li, M.H.; Iqbal, J.; Bourantas, C.V.; Mi, Q.Y.; Yu, Y.H.; Li, J.J.; Zhao, S.L.; Tian, N.L.; Chen, S.L. Berberine attenuates adverse left ventricular remodeling and cardiac dysfunction after acute myocardial infarction in rats: Role of autophagy. Clin. Exp. Pharmacol. Physiol., 2014, 41(12), 995-1002.
[http://dx.doi.org/10.1111/1440-1681.12309] [PMID: 25224725]
[177]
Fan, X.; Wang, J.; Hou, J.; Lin, C.; Bensoussan, A.; Chang, D.; Liu, J.; Wang, B. Berberine alleviates ox-LDL induced inflammatory factors by up-regulation of autophagy via AMPK/mTOR signaling pathway. J. Transl. Med., 2015, 13, 92.
[http://dx.doi.org/10.1186/s12967-015-0450-z] [PMID: 25884210]
[178]
Chang, C.F.; Lee, Y.C.; Lee, K.H.; Lin, H.C.; Chen, C.L.; Shen, C.J.; Huang, C.C. Therapeutic effect of berberine on TDP-43-related pathogenesis in FTLD and ALS. J. Biomed. Sci., 2016, 23(1), 72.
[http://dx.doi.org/10.1186/s12929-016-0290-z] [PMID: 27769241]
[179]
Kou, J.Y.; Li, Y.; Zhong, Z.Y.; Jiang, Y.Q.; Li, X.S.; Han, X.B.; Liu, Z.N.; Tian, Y.; Yang, L.M. Berberine-sonodynamic therapy induces autophagy and lipid unloading in macrophage Cell Death Dis., 2017, e8(1), 2558.
[http://dx.doi.org/10.1038/cddis.2016.354]
[180]
Zhou, H.; Feng, L.; Xu, F.; Sun, Y.; Ma, Y.; Zhang, X.; Liu, H.; Xu, G.; Wu, X.; Shen, Y.; Sun, Y.; Wu, X.; Xu, Q. Berberine inhibits palmitate-induced NLRP3 inflammasome activation by triggering autophagy in macrophages: A new mechanism linking berberine to insulin resistance improvement. Biomed. Pharmacother., 2017, 89, 864-874.
[http://dx.doi.org/10.1016/j.biopha.2017.03.003] [PMID: 28282788]
[181]
Chitra, P.; Saiprasad, G.; Manikandan, R.; Sudhandiran, G. Berberine inhibits Smad and non-Smad signaling cascades and enhances autophagy against pulmonary fibrosis. J. Mol. Med. (Berl.), 2015, 93(9), 1015-1031.
[http://dx.doi.org/10.1007/s00109-015-1283-1] [PMID: 25877860]
[182]
Peng, P.L.; Kuo, W.H.; Tseng, H.C.; Chou, F.P. Synergistic tumor-killing effect of radiation and berberine combined treatment in lung cancer: the contribution of autophagic cell death. Int. J. Radiat. Oncol. Biol. Phys., 2008, 70(2), 529-542.
[http://dx.doi.org/10.1016/j.ijrobp.2007.08.034] [PMID: 18207031]
[183]
Wang, N.; Feng, Y.; Zhu, M.; Tsang, C.M.; Man, K.; Tong, Y.; Tsao, S.W. Berberine induces autophagic cell death and mitochondrial apoptosis in liver cancer cells: The cellular mechanism. J. Cell. Biochem., 2010, 111(6), 1426-1436.
[http://dx.doi.org/10.1002/jcb.22869] [PMID: 20830746]
[184]
Hou, Q.; Tang, X.; Liu, H.; Tang, J.; Yang, Y.; Jing, X.; Xiao, Q.; Wang, W.; Gou, X.; Wang, Z. Berberine induces cell death in human hepatoma cells in vitro by downregulating CD147. Cancer Sci., 2011, 102(7), 1287-1292.
[http://dx.doi.org/10.1111/j.1349-7006.2011.01933.x] [PMID: 21443647]
[185]
Yu, R.; Zhang, Z.Q.; Wang, B.; Jiang, H.X.; Cheng, L.; Shen, L.M. Berberine-induced apoptotic and autophagic death of HepG2 cells requires AMPK activation. Cancer Cell Int., 2014, 14, 49.
[http://dx.doi.org/10.1186/1475-2867-14-49] [PMID: 24991192]
[186]
Lee, K.H.; Lo, H.L.; Tang, W.C.; Hsiao, H.H.; Yang, P.M. A gene expression signature-based approach reveals the mechanisms of action of the Chinese herbal medicine berberine. Sci. Rep., 2014, 4, 6394.
[http://dx.doi.org/10.1038/srep06394] [PMID: 25227736]
[187]
Wang, J.; Qi, Q.; Feng, Z.; Zhang, X.; Huang, B.; Chen, A.; Prestegarden, L.; Li, X.; Wang, J. Berberine induces autophagy in glioblastoma by targeting the AMPK/mTOR/ULK1-pathway. Oncotarget, 2016, 7(41), 66944-66958.
[http://dx.doi.org/10.18632/oncotarget.11396] [PMID: 27557493]
[188]
Halicka, H.D.; Garcia, J.; Li, J.; Zhao, H.; Darzynkiewicz, Z. Synergy of 2-deoxy-D-glucose combined with berberine in inducing the lysosome/autophagy and transglutaminase activation-facilitated apoptosis. Apoptosis, 2017, 22(2), 229-238.
[http://dx.doi.org/10.1007/s10495-016-1315-5] [PMID: 27796611]
[189]
La, X.; Zhang, L.; Li, Z.; Yang, P.; Wang, Y. Berberine-induced autophagic cell death by elevating GRP78 levels in cancer cells. Oncotarget, 2017, 8(13), 20909-20924.
[http://dx.doi.org/10.18632/oncotarget.14959] [PMID: 28157699]
[190]
Tansey, M.G.; McCoy, M.K.; Frank-Cannon, T.C. Neuroinflammatory mechanisms in Parkinson’s disease: Potential environmental triggers, pathways, and targets for early therapeutic intervention. Exp. Neurol., 2007, 208(1), 1-25.
[http://dx.doi.org/10.1016/j.expneurol.2007.07.004] [PMID: 17720159]
[191]
Glass, C.K.; Saijo, K.; Winner, B.; Marchetto, M.C.; Gage, F.H. Mechanisms underlying inflammation in neurodegeneration. Cell, 2010, 140(6), 918-934.
[http://dx.doi.org/10.1016/j.cell.2010.02.016] [PMID: 20303880]
[192]
Block, M.L.; Hong, J.S. Microglia and inflammation-mediated neurodegeneration: multiple triggers with a common mechanism. Prog. Neurobiol., 2005, 76(2), 77-98.
[http://dx.doi.org/10.1016/j.pneurobio.2005.06.004] [PMID: 16081203]
[193]
Perry, V.H.; Nicoll, J.A.; Holmes, C. Microglia in neurodegenerative disease. Nat. Rev. Neurol., 2010, 6(4), 193-201.
[http://dx.doi.org/10.1038/nrneurol.2010.17] [PMID: 20234358]
[194]
Perry, V.H.; Holmes, C. Microglial priming in neurodegenerative disease. Nat. Rev. Neurol., 2014, 10(4), 217-224.
[http://dx.doi.org/10.1038/nrneurol.2014.38] [PMID: 24638131]
[195]
Gao, H.M.; Hong, J.S. Why neurodegenerative diseases are progressive: uncontrolled inflammation drives disease progression. Trends Immunol., 2008, 29(8), 357-365.
[http://dx.doi.org/10.1016/j.it.2008.05.002] [PMID: 18599350]
[196]
Heneka, M.T.; Carson, M.J.; El Khoury, J.; Landreth, G.E.; Brosseron, F.; Feinstein, D.L.; Jacobs, A.H.; Wyss-Coray, T.; Vitorica, J.; Ransohoff, R.M.; Herrup, K.; Frautschy, S.A.; Finsen, B.; Brown, G.C.; Verkhratsky, A.; Yamanaka, K.; Koistinaho, J.; Latz, E.; Halle, A.; Petzold, G.C.; Town, T.; Morgan, D.; Shinohara, M.L.; Perry, V.H.; Holmes, C.; Bazan, N.G.; Brooks, D.J.; Hunot, S.; Joseph, B.; Deigendesch, N.; Garaschuk, O.; Boddeke, E.; Dinarello, C.A.; Breitner, J.C.; Cole, G.M.; Golenbock, D.T.; Kummer, M.P. Neuroinflammation in Alzheimer’s disease. Lancet Neurol., 2015, 14(4), 388-405.
[http://dx.doi.org/10.1016/S1474-4422(15)70016-5] [PMID: 25792098]
[197]
Hirsch, E.C.; Hunot, S. Neuroinflammation in Parkinson’s disease: A target for neuroprotection? Lancet Neurol., 2009, 8(4), 382-397.
[http://dx.doi.org/10.1016/S1474-4422(09)70062-6] [PMID: 19296921]
[198]
Klegeris, A.; McGeer, P.L. Non-steroidal anti-inflammatory drugs (NSAIDs) and other anti-inflammatory agents in the treatment of neurodegenerative disease. Curr. Alzheimer Res., 2005, 2(3), 355-365.
[http://dx.doi.org/10.2174/1567205054367883] [PMID: 15974901]
[199]
Szekely, C.A.; Zandi, P.P. Non-steroidal anti-inflammatory drugs and Alzheimer’s disease: The epidemiological evidence. CNS Neurol. Disord. Drug Targets, 2010, 9(2), 132-139.
[http://dx.doi.org/10.2174/187152710791012026] [PMID: 20205647]
[200]
Esposito, E.; Di Matteo, V.; Benigno, A.; Pierucci, M.; Crescimanno, G.; Di Giovanni, G. Non-steroidal anti-inflammatory drugs in Parkinson’s disease. Exp. Neurol., 2007, 205(2), 295-312.
[http://dx.doi.org/10.1016/j.expneurol.2007.02.008] [PMID: 17433296]
[201]
Nam, K.N.; Kim, J.H.; Jung, H.J.; Park, J.M.; Moon, S.K.; Kim, Y.S.; Sun, Y.K.; Lee, E.H. Berberine inhibits inflammatory activation of rat brain microglia. Neural Regen. Res., 2010, 12(1), 1384-1390.
[202]
Lu, D.Y.; Tang, C.H.; Chen, Y.H.; Wei, I.H. Berberine suppresses neuroinflammatory responses through AMP-activated protein kinase activation in BV-2 microglia. J. Cell. Biochem., 2010, 110(3), 697-705.
[http://dx.doi.org/10.1002/jcb.22580] [PMID: 20512929]
[203]
Zhang, Z.; Li, X.; Li, F.; An, L. Berberine alleviates postoperative cognitive dysfunction by suppressing neuroinflammation in aged mice. Int. Immunopharmacol., 2016, 38, 426-433.
[http://dx.doi.org/10.1016/j.intimp.2016.06.031] [PMID: 27376853]
[204]
Jia, L.; Liu, J.; Song, Z.; Pan, X.; Chen, L.; Cui, X.; Wang, M. Berberine suppresses amyloid-beta-induced inflammatory response in microglia by inhibiting nuclear factor-kappaB and mitogen-activated protein kinase signalling pathways. J. Pharm. Pharmacol., 2012, 64(10), 1510-1521.
[http://dx.doi.org/10.1111/j.2042-7158.2012.01529.x] [PMID: 22943182]
[205]
Chen, C.C.; Hung, T.H.; Lee, C.Y.; Wang, L.F.; Wu, C.H.; Ke, C.H.; Chen, S.F. Berberine protects against neuronal damage via suppression of glia-mediated inflammation in traumatic brain injury. PLoS One, 2014, 9(12), e115694.
[http://dx.doi.org/10.1371/journal.pone.0115694] [PMID: 25546475]
[206]
Niedzielska, E.; Smaga, I.; Gawlik, M.; Moniczewski, A.; Stankowicz, P.; Pera, J.; Filip, M. Oxidative stress in neurodegenerative diseases. Mol. Neurobiol., 2016, 53(6), 4094-4125.
[http://dx.doi.org/10.1007/s12035-015-9337-5] [PMID: 26198567]
[207]
Kim, G.H.; Kim, J.E.; Rhie, S.J.; Yoon, S. The role of oxidative stress in neurodegenerative diseases. Exp. Neurobiol., 2015, 24(4), 325-340.
[http://dx.doi.org/10.5607/en.2015.24.4.325] [PMID: 26713080]
[208]
Lin, M.T.; Beal, M.F. Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature, 2006, 443(7113), 787-795.
[http://dx.doi.org/10.1038/nature05292] [PMID: 17051205]
[209]
Barnham, K.J.; Masters, C.L.; Bush, A.I. Neurodegenerative diseases and oxidative stress. Nat. Rev. Drug Discov., 2004, 3(3), 205-214.
[http://dx.doi.org/10.1038/nrd1330] [PMID: 15031734]
[210]
Uttara, B.; Singh, A.V.; Zamboni, P.; Mahajan, R.T. Oxidative stress and neurodegenerative diseases: A review of upstream and downstream antioxidant therapeutic options. Curr. Neuropharmacol., 2009, 7(1), 65-74.
[http://dx.doi.org/10.2174/157015909787602823] [PMID: 19721819]
[211]
Fernandes, C.; Oliveira, C.; Benfeito, S.; Soares, P.; Garrido, J.; Borges, F. Nanotechnology and antioxidant therapy: An emerging approach for neurodegenerative diseases. Curr. Med. Chem., 2014, 21(38), 4311-4327.
[http://dx.doi.org/10.2174/0929867321666140915141836] [PMID: 25245378]
[212]
Danta, C.C.; Piplani, P. The discovery and development of new potential antioxidant agents for the treatment of neurodegenerative diseases. Expert Opin. Drug Discov., 2014, 9(10), 1205-1222.
[http://dx.doi.org/10.1517/17460441.2014.942218] [PMID: 25056182]
[213]
Guerra-Araiza, C.; Álvarez-Mejía, A.L.; Sánchez-Torres, S.; Farfan-García, E.; Mondragón-Lozano, R.; Pinto-Almazán, R.; Salgado-Ceballos, H. Effect of natural exogenous antioxidants on aging and on neurodegenerative diseases. Free Radic. Res., 2013, 47(6-7), 451-462.
[http://dx.doi.org/10.3109/10715762.2013.795649] [PMID: 23594291]
[214]
Sarrafchi, A.; Bahmani, M.; Shirzad, H.; Rafieian-Kopaei, M. Oxidative stress and Parkinson’s disease: New hopes in treatment with herbal antioxidants. Curr. Pharm. Des., 2016, 22(2), 238-246.
[http://dx.doi.org/10.2174/1381612822666151112151653] [PMID: 26561062]
[215]
Shirwaikar, A.; Shirwaikar, A.; Rajendran, K.; Punitha, I.S. In vitro antioxidant studies on the benzyl tetra isoquinoline alkaloid berberine. Biol. Pharm. Bull., 2006, 29(9), 1906-1910.
[http://dx.doi.org/10.1248/bpb.29.1906] [PMID: 16946507]
[216]
Bhutada, P.; Mundhada, Y.; Bansod, K.; Tawari, S.; Patil, S.; Dixit, P.; Umathe, S.; Mundhada, D. Protection of cholinergic and antioxidant system contributes to the effect of berberine ameliorating memory dysfunction in rat model of streptozotocin-induced diabetes. Behav. Brain Res., 2011, 220(1), 30-41.
[http://dx.doi.org/10.1016/j.bbr.2011.01.022] [PMID: 21262264]
[217]
Li, Z.; Geng, Y.N.; Jiang, J.D.; Kong, W.J. Antioxidant and anti-inflammatory activities of berberine in the treatment of diabetes mellitus. Evid. Based Complement. Alternat. Med., 2014, 2014, 289264.
[PMID: 24669227]
[218]
Thirupurasundari, C.J.; Padmini, R.; Devaraj, S.N. Effect of berberine on the antioxidant status, ultrastructural modifications and protein bound carbohydrates in azoxymethane-induced colon cancer in rats. Chem. Biol. Interact., 2009, 177(3), 190-195.
[http://dx.doi.org/10.1016/j.cbi.2008.09.027] [PMID: 18951886]
[219]
Zhou, J.Y.; Zhou, S.W. Protective effect of berberine on antioxidant enzymes and positive transcription elongation factor b expression in diabetic rat liver. Fitoterapia, 2011, 82(2), 184-189.
[http://dx.doi.org/10.1016/j.fitote.2010.08.019] [PMID: 20828602]
[220]
Zhang, S.; Zhang, B.; Dai, W.; Zhang, X. Oxidative damage and antioxidant responses in Microcystis aeruginosa exposed to the allelochemical berberine isolated from golden thread. J. Plant Physiol., 2011, 168(7), 639-643.
[http://dx.doi.org/10.1016/j.jplph.2010.10.005] [PMID: 21131096]
[221]
Tan, Y.; Tang, Q.; Hu, B.R.; Xiang, J.Z. Antioxidant properties of berberine on cultured rabbit corpus cavernosum smooth muscle cells injured by hydrogen peroxide. Acta Pharmacol. Sin., 2007, 28(12), 1914-1918.
[http://dx.doi.org/10.1111/j.1745-7254.2007.00705.x] [PMID: 18031604]
[222]
Siow, Y.L.; Sarna, L. Redox regulation in health and disease – therapeutic potential of Berberine. Food Res. Int., 2011, 44, 2409-2417.
[http://dx.doi.org/10.1016/j.foodres.2010.12.038]
[223]
Germoush, M.O.; Mahmoud, A.M. Berberine mitigates cyclophosphamide-induced hepatotoxicity by modulating antioxidant status and inflammatory cytokines. J. Cancer Res. Clin. Oncol., 2014, 140(7), 1103-1109.
[http://dx.doi.org/10.1007/s00432-014-1665-8] [PMID: 24744190]
[224]
Luo, A.; Fan, Y. Antioxidant activities of berberine hydrochloride. Int. J. Nanomedicine, 2016, 11, 1687-1700.
[PMID: 27217747]
[225]
Liu, W.H.; Hei, Z.Q.; Nie, H.; Tang, F.T.; Huang, H.Q.; Li, X.J.; Deng, Y.H.; Chen, S.R.; Guo, F.F.; Huang, W.G.; Chen, F.Y.; Liu, P.Q. Berberine ameliorates renal injury in streptozotocin-induced diabetic rats by suppression of both oxidative stress and aldose reductase. Chin. Med. J. (Engl.), 2008, 121(8), 706-712.
[http://dx.doi.org/10.1097/00029330-200804020-00009] [PMID: 18701023]
[226]
Hsieh, Y.S.; Kuo, W.H.; Lin, T.W.; Chang, H.R.; Lin, T.H.; Chen, P.N.; Chu, S.C. Protective effects of berberine against low-density lipoprotein (LDL) oxidation and oxidized LDL-induced cytotoxicity on endothelial cells. J. Agric. Food Chem., 2007, 55(25), 10437-10445.
[http://dx.doi.org/10.1021/jf071868c] [PMID: 18001034]
[227]
Sarna, L.K.; Wu, N.; Hwang, S.Y.; Siow, Y.L. O, K. Berberine inhibits NADPH oxidase mediated superoxide anion production in macrophages. Can. J. Physiol. Pharmacol., 2010, 88(3), 369-378.
[http://dx.doi.org/10.1139/Y09-136] [PMID: 20393601]
[228]
Jeong, H.W.; Hsu, K.C.; Lee, J.W.; Ham, M.; Huh, J.Y.; Shin, H.J.; Kim, W.S.; Kim, J.B. Berberine suppresses proinflammatory responses through AMPK activation in macrophages. Am. J. Physiol. Endocrinol. Metab., 2009, 296(4), E955-E964.
[http://dx.doi.org/10.1152/ajpendo.90599.2008] [PMID: 19208854]
[229]
Yokozawa, T.; Ishida, A.; Kashiwada, Y.; Cho, E.J.; Kim, H.Y.; Ikeshiro, Y. Coptidis Rhizoma: protective effects against peroxynitrite-induced oxidative damage and elucidation of its active components. J. Pharm. Pharmacol., 2004, 56(4), 547-556.
[http://dx.doi.org/10.1211/0022357023024] [PMID: 15099450]
[230]
Thirupurasundari, C.J.; Padmini, R.; Devaraj, S.N. Effect of berberine on the antioxidant status, ultrastructural modifications and protein bound carbohydrates in azoxymethane-induced colon cancer in rats. Chem. Biol. Interact., 2009, 177(3), 190-195.
[http://dx.doi.org/10.1016/j.cbi.2008.09.027] [PMID: 18951886]
[231]
Hsu, Y.Y.; Chen, C.S.; Wu, S.N.; Jong, Y.J.; Lo, Y.C. Berberine activates Nrf2 nuclear translocation and protects against oxidative damage via a phosphatidylinositol 3-kinase/Akt-dependent mechanism in NSC34 motor neuron-like cells. Eur. J. Pharm. Sci., 2012, 46(5), 415-425.
[http://dx.doi.org/10.1016/j.ejps.2012.03.004] [PMID: 22469516]
[232]
Hsu, Y.Y.; Tseng, Y.T.; Lo, Y.C. Berberine, a natural antidiabetes drug, attenuates glucose neurotoxicity and promotes Nrf2-related neurite outgrowth. Toxicol. Appl. Pharmacol., 2013, 272(3), 787-796.
[http://dx.doi.org/10.1016/j.taap.2013.08.008] [PMID: 23954465]
[233]
Pandey, M.K.; Sung, B.; Kunnumakkara, A.B.; Sethi, G.; Chaturvedi, M.M.; Aggarwal, B.B. Berberine modifies cysteine 179 of IkappaBalpha kinase, suppresses nuclear factor-kappaB-regulated antiapoptotic gene products, and potentiates apoptosis. Cancer Res., 2008, 68(13), 5370-5379.
[http://dx.doi.org/10.1158/0008-5472.CAN-08-0511] [PMID: 18593939]
[234]
Zhang, X.; Gu, L.; Li, J.; Shah, N.; He, J.; Yang, L.; Hu, Q.; Zhou, M. Degradation of MDM2 by the interaction between berberine and DAXX leads to potent apoptosis in MDM2-overexpressing cancer cells. Cancer Res., 2010, 70(23), 9895-9904.
[http://dx.doi.org/10.1158/0008-5472.CAN-10-1546] [PMID: 20935220]
[235]
Zhou, Y.; Liu, S.Q.; Yu, L.; He, B.; Wu, S.H.; Zhao, Q.; Xia, S.Q.; Mei, H.J. Berberine prevents nitric oxide-induced rat chondrocyte apoptosis and cartilage degeneration in a rat osteoarthritis model via AMPK and p38 MAPK signaling. Apoptosis, 2015, 20(9), 1187-1199.
[http://dx.doi.org/10.1007/s10495-015-1152-y] [PMID: 26184498]
[236]
Wang, Z.; Chen, Z.; Chen, T.; Yi, T.; Zheng, Z.; Fan, H.; Chen, Z. Berberine attenuates inflammation associated with delayed-type hypersensitivity via suppressing Th1 response and inhibiting apoptosis. Inflammation, 2017, 40(1), 221-231.
[http://dx.doi.org/10.1007/s10753-016-0472-6] [PMID: 27832398]
[237]
Lv, X.; Yu, X.; Wang, Y.; Wang, F.; Li, H.; Wang, Y.; Lu, D.; Qi, R.; Wang, H. Berberine inhibits doxorubicin-triggered cardiomyocyte apoptosis via attenuating mitochondrial dysfunction and increasing Bcl-2 expression. PLoS One, 2012, 7(10), e47351.
[http://dx.doi.org/10.1371/journal.pone.0047351] [PMID: 23077597]
[238]
Chen, K.; Li, G.; Geng, F.; Zhang, Z.; Li, J.; Yang, M.; Dong, L.; Gao, F. Berberine reduces ischemia/reperfusion-induced myocardial apoptosis via activating AMPK and PI3K-Akt signaling in diabetic rats. Apoptosis, 2014, 19(6), 946-957.
[http://dx.doi.org/10.1007/s10495-014-0977-0] [PMID: 24664781]
[239]
Wang, Y.; Liu, J.; Ma, A.; Chen, Y. Cardioprotective effect of berberine against myocardial ischemia/reperfusion injury via attenuating mitochondrial dysfunction and apoptosis. Int. J. Clin. Exp. Med., 2015, 8(8), 14513-14519.
[PMID: 26550442]
[240]
Li, W.; Liu, Y.; Wang, B.; Luo, Y.; Hu, N.; Chen, D.; Zhang, X.; Xiong, Y. Protective effect of berberine against oxidative stress-induced apoptosis in rat bone marrow-derived mesenchymal stem cells. Exp. Ther. Med., 2016, 12(6), 4041-4048.
[http://dx.doi.org/10.3892/etm.2016.3866] [PMID: 28101183]
[241]
Guo, J.; Wang, L.; Wang, L.; Qian, S.; Zhang, D.; Fang, J.; Pan, J. Berberine protects human umbilical vein endothelial cells against LPS-induced apoptosis by blocking JNK-mediated signaling. Evid. Based Complement. Alternat. Med., 2016, 2016, 6983956.
[http://dx.doi.org/10.1155/2016/6983956] [PMID: 27478481]
[242]
Adil, M.; Kandhare, A.D.; Dalvi, G.; Ghosh, P.; Venkata, S.; Raygude, K.S.; Bodhankar, S.L. Ameliorative effect of berberine against gentamicin-induced nephrotoxicity in rats via attenuation of oxidative stress, inflammation, apoptosis and mitochondrial dysfunction. Ren. Fail., 2016, 38(6), 996-1006.
[http://dx.doi.org/10.3109/0886022X.2016.1165120] [PMID: 27056079]
[243]
Zhang, X.; Liang, D.; Lian, X.; Jiang, Y.; He, H.; Liang, W.; Zhao, Y.; Chi, Z.H. Berberine activates Nrf2 nuclear translocation and inhibits apoptosis induced by high glucose in renal tubular epithelial cells through a phosphatidylinositol 3-kinase/Akt-dependent mechanism. Apoptosis, 2016, 21(6), 721-736.
[http://dx.doi.org/10.1007/s10495-016-1234-5] [PMID: 26979714]
[244]
Hu, J.; Chai, Y.; Wang, Y.; Kheir, M.M.; Li, H.; Yuan, Z.; Wan, H.; Xing, D.; Lei, F.; Du, L. PI3K p55γ promoter activity enhancement is involved in the anti-apoptotic effect of berberine against cerebral ischemia-reperfusion. Eur. J. Pharmacol., 2012, 674(2-3), 132-142.
[http://dx.doi.org/10.1016/j.ejphar.2011.11.014] [PMID: 22119079]
[245]
Chai, Y.S.; Hu, J.; Lei, F.; Wang, Y.G.; Yuan, Z.Y.; Lu, X.; Wang, X.P.; Du, F.; Zhang, D.; Xing, D.M.; Du, L.J. Effect of berberine on cell cycle arrest and cell survival during cerebral ischemia and reperfusion and correlations with p53/cyclin D1 and PI3K/Akt. Eur. J. Pharmacol., 2013, 708(1-3), 44-55.
[http://dx.doi.org/10.1016/j.ejphar.2013.02.041] [PMID: 23499694]
[246]
Kim, M.; Cho, K.H.; Shin, M.S.; Lee, J.M.; Cho, H.S.; Kim, C.J.; Shin, D.H.; Yang, H.J. Berberine prevents nigrostriatal dopaminergic neuronal loss and suppresses hippocampal apoptosis in mice with Parkinson’s disease. Int. J. Mol. Med., 2014, 33(4), 870-878.
[http://dx.doi.org/10.3892/ijmm.2014.1656] [PMID: 24535622]
[247]
Kalalian-Moghaddam, H.; Baluchnejadmojarad, T.; Roghani, M.; Goshadrou, F.; Ronaghi, A. Hippocampal synaptic plasticity restoration and anti-apoptotic effect underlie berberine improvement of learning and memory in streptozotocin-diabetic rats. Eur. J. Pharmacol., 2013, 698(1-3), 259-266.
[http://dx.doi.org/10.1016/j.ejphar.2012.10.020] [PMID: 23099256]
[248]
Zhou, X.Q.; Zeng, X.N.; Kong, H.; Sun, X.L. Neuroprotective effects of berberine on stroke models in vitro and in vivo. Neurosci. Lett., 2008, 447(1), 31-36.
[http://dx.doi.org/10.1016/j.neulet.2008.09.064] [PMID: 18838103]
[249]
Cui, H.S.; Matsumoto, K.; Murakami, Y.; Hori, H.; Zhao, Q.; Obi, R. Berberine exerts neuroprotective actions against in vitro ischemia-induced neuronal cell damage in organotypic hippocampal slice cultures: involvement of B-cell lymphoma 2 phosphorylation suppression. Biol. Pharm. Bull., 2009, 32(1), 79-85.
[http://dx.doi.org/10.1248/bpb.32.79] [PMID: 19122285]
[250]
Zhang, Q.; Qian, Z.; Pan, L.; Li, H.; Zhu, H. Hypoxia-inducible factor 1 mediates the anti-apoptosis of berberine in neurons during hypoxia/ischemia. Acta Physiol. Hung., 2012, 99(3), 311-323.
[http://dx.doi.org/10.1556/APhysiol.99.2012.3.8] [PMID: 22982719]
[251]
Zhang, X.; Zhang, X.; Wang, C.; Li, Y.; Dong, L.; Cui, L.; Wang, L.; Liu, Z.; Qiao, H.; Zhu, C.; Xing, Y.; Cao, X.; Ji, Y.; Zhao, K. Neuroprotection of early and short-time applying berberine in the acute phase of cerebral ischemia: Up-regulated pAkt, pGSK and pCREB, down-regulated NF-κB expression, ameliorated BBB permeability. Brain Res., 2012, 1459, 61-70.
[http://dx.doi.org/10.1016/j.brainres.2012.03.065] [PMID: 22560097]
[252]
Kim, M.; Shin, M.S.; Lee, J.M.; Cho, H.S.; Kim, C.J.; Kim, Y.J.; Choi, H.R.; Jeon, J.W. Inhibitory effects of isoquinoline alkaloid berberine on ischemia-induced apoptosis via activation of phosphoinositide 3-kinase/protein kinase B signaling pathway. Int. Neurourol. J., 2014, 18(3), 115-125.
[http://dx.doi.org/10.5213/inj.2014.18.3.115] [PMID: 25279238]
[253]
Simões Pires, E.N.; Frozza, R.L.; Hoppe, J.B. Menezes, Bde.M.; Salbego, C.G. Berberine was neuroprotective against an in vitro model of brain ischemia: Survival and apoptosis pathways involved. Brain Res., 2014, 1557, 26-33.
[http://dx.doi.org/10.1016/j.brainres.2014.02.021] [PMID: 24560603]
[254]
Sadeghnia, H.R.; Kolangikhah, M.; Asadpour, E.; Forouzanfar, F.; Hosseinzadeh, H. Berberine protects against glutamate-induced oxidative stress and apoptosis in PC12 and N2a cells. Iran. J. Basic Med. Sci., 2017, 20(5), 594-603.
[PMID: 28656094]
[255]
Liang, Y.; Huang, M.; Jiang, X.; Liu, Q.; Chang, X.; Guo, Y. The neuroprotective effects of berberine against amyloid β-proteininduced apoptosis in primary cultured hippocam-pal neurons via mitochondria-related caspase pathway Neurosci Lett., 2017, S0304-3940, 30540-30542.
[256]
Zhang, Q.; Bian, H.; Guo, L.; Zhu, H. Pharmacologic preconditioning with berberine attenuating ischemia-induced apoptosis and promoting autophagy in neuron. Am. J. Transl. Res., 2016, 8(2), 1197-1207.
[PMID: 27158406]
[257]
Heemels, M.T. Neurodegenerative diseases. Nature, 2016, 539(7628), 179.
[http://dx.doi.org/10.1038/539179a] [PMID: 27830810]
[258]
Yates, D. Neurodegenerative disease: Straining the brain. Nat. Rev. Neurosci., 2016, 17(12), 738.
[http://dx.doi.org/10.1038/nrn.2016.161] [PMID: 27853142]
[259]
Zhang, K.; Rothstein, J.D. Neurodegenerative disease: Two-for-one on potential therapies. Nature, 2017, 544(7650), 302-303.
[http://dx.doi.org/10.1038/nature21911] [PMID: 28405020]
[260]
Newman, D.J.; Cragg, G.M. Natural products as sources of new drugs from 1981 to 2014. J. Nat. Prod., 2016, 79(3), 629-661.
[http://dx.doi.org/10.1021/acs.jnatprod.5b01055] [PMID: 26852623]
[261]
Butler, M.S.; Robertson, A.A.; Cooper, M.A. Natural product and natural product derived drugs in clinical trials. Nat. Prod. Rep., 2014, 31(11), 1612-1661.
[http://dx.doi.org/10.1039/C4NP00064A] [PMID: 25204227]
[262]
Chen, X.; Decker, M. Multi-target compounds acting in the central nervous system designed from natural products. Curr. Med. Chem., 2013, 20(13), 1673-1685.
[http://dx.doi.org/10.2174/0929867311320130007] [PMID: 23410166]
[263]
Ansari, N.; Khodagholi, F. Natural products as promising drug candidates for the treatment of Alzheimer’s disease: Molecular mechanism aspect. Curr. Neuropharmacol., 2013, 11(4), 414-429.
[http://dx.doi.org/10.2174/1570159X11311040005] [PMID: 24381531]
[264]
Khin-Maung-U.. Myo-Khin.; Nyunt-Nyunt-Wai.; Aye-Kyaw.; Tin-U, Clinical trial of berberine in acute watery diarrhoea. Br. Med. J. (Clin. Res. Ed.), 1985, 291(6509), 1601-1605.
[http://dx.doi.org/10.1136/bmj.291.6509.1601] [PMID: 3935203]
[265]
Chen, C.; Tao, C.; Liu, Z.; Lu, M.; Pan, Q.; Zheng, L.; Li, Q.; Song, Z.; Fichna, J. A randomized clinical trial of berberine hydrochloride in patients with diarrhea-predominant irritable bowel syndrome. Phytother. Res., 2015, 29(11), 1822-1827.
[http://dx.doi.org/10.1002/ptr.5475] [PMID: 26400188]
[266]
Caliceti, C.; Franco, P.; Spinozzi, S.; Roda, A.; Cicero, A.F. Berberine: Berberine: New insights from pharmacological aspects to clinical evidences in the management of metabolic disorders. Curr. Med. Chem., 2016, 23(14), 1460-1476.
[http://dx.doi.org/10.2174/0929867323666160411143314] [PMID: 27063256]
[267]
Derosa, G.; Maffioli, P.; Cicero, A.F. Berberine on metabolic and cardiovascular risk factors: An analysis from preclinical evidences to clinical trials. Expert Opin. Biol. Ther., 2012, 12(8), 1113-1124.
[http://dx.doi.org/10.1517/14712598.2012.704014] [PMID: 22780092]
[268]
Cicero, A.F.; Tartagni, E. Antidiabetic properties of berberine: From cellular pharmacology to clinical effects. Hosp Pract, (1995). 2012, 40(2), 56-63.
[http://dx.doi.org/10.3810/hp.2012.04.970] [PMID: 22615079]
[269]
Chang, W.; Chen, L.; Hatch, G.M. Berberine as a therapy for type 2 diabetes and its complications: From mechanism of action to clinical studies. Biochem. Cell Biol., 2015, 93(5), 479-486.
[http://dx.doi.org/10.1139/bcb-2014-0107] [PMID: 25607236]
[270]
Wei, W.; Zhao, H.; Wang, A.; Sui, M.; Liang, K.; Deng, H.; Ma, Y.; Zhang, Y.; Zhang, H.; Guan, Y. A clinical study on the short-term effect of berberine in comparison to metformin on the metabolic characteristics of women with polycystic ovary syndrome. Eur. J. Endocrinol., 2012, 166(1), 99-105.
[http://dx.doi.org/10.1530/EJE-11-0616] [PMID: 22019891]
[271]
An, Y.; Sun, Z.; Zhang, Y.; Liu, B.; Guan, Y.; Lu, M. The use of berberine for women with polycystic ovary syndrome undergoing IVF treatment. Clin. Endocrinol. (Oxf.), 2014, 80(3), 425-431.
[http://dx.doi.org/10.1111/cen.12294] [PMID: 23869585]
[272]
Dong, H.; Zhao, Y.; Zhao, L.; Lu, F. The effects of berberine on blood lipids: A systemic review and meta-analysis of randomized controlled trials. Planta Med., 2013, 79(6), 437-446.
[http://dx.doi.org/10.1055/s-0032-1328321] [PMID: 23512497]
[273]
Pirillo, A.; Catapano, A.L. Berberine, a plant alkaloid with lipid- and glucose-lowering properties: From in vitro evidence to clinical studies. Atherosclerosis, 2015, 243(2), 449-461.
[http://dx.doi.org/10.1016/j.atherosclerosis.2015.09.032] [PMID: 26520899]
[274]
Zeng, X.H.; Zeng, X.J.; Li, Y.Y. Efficacy and safety of berberine for congestive heart failure secondary to ischemic or idiopathic dilated cardiomyopathy. Am. J. Cardiol., 2003, 92(2), 173-176.
[http://dx.doi.org/10.1016/S0002-9149(03)00533-2] [PMID: 12860219]
[275]
Lan, J.; Zhao, Y.; Dong, F.; Yan, Z.; Zheng, W.; Fan, J.; Sun, G. Meta-analysis of the effect and safety of berberine in the treatment of type 2 diabetes mellitus, hyperlipemia and hypertension. J. Ethnopharmacol., 2015, 161, 69-81.
[http://dx.doi.org/10.1016/j.jep.2014.09.049] [PMID: 25498346]
[276]
Wang, X.; Wang, R.; Xing, D.; Su, H.; Ma, C.; Ding, Y.; Du, L. Kinetic difference of berberine between hippocampus and plasma in rat after intravenous administration of Coptidis rhizoma extract. Life Sci., 2005, 77(24), 3058-3067.
[http://dx.doi.org/10.1016/j.lfs.2005.02.033] [PMID: 15996686]
[277]
Wei, W.; Zhao, H.; Wang, A.; Sui, M.; Liang, K.; Deng, H.; Ma, Y.; Zhang, Y.; Zhang, H.; Guan, Y. A clinical study on the short-term effect of berberine in comparison to metformin on the metabolic characteristics of women with polycystic ovary syndrome. Eur. J. Endocrinol., 2012, 166(1), 99-105.
[http://dx.doi.org/10.1530/EJE-11-0616] [PMID: 22019891]
[278]
Zhang, H.; Wei, J.; Xue, R.; Wu, J.D.; Zhao, W.; Wang, Z.Z.; Wang, S.K.; Zhou, Z.X.; Song, D.Q.; Wang, Y.M.; Pan, H.N.; Kong, W.J.; Jiang, J.D. Berberine lowers blood glucose in type 2 diabetes mellitus patients through increasing insulin receptor expression. Metabolism, 2010, 59(2), 285-292.
[http://dx.doi.org/10.1016/j.metabol.2009.07.029] [PMID: 19800084]
[279]
Zeng, X.H.; Zeng, X.J.; Li, Y.Y. Efficacy and safety of berberine for congestive heart failure secondary to ischemic or idiopathic dilated cardiomyopathy. Am. J. Cardiol., 2003, 92(2), 173-176.
[http://dx.doi.org/10.1016/S0002-9149(03)00533-2] [PMID: 12860219]
[280]
Sack, R.B.; Froehlich, J.L. Berberine inhibits intestinal secretory response of Vibrio cholerae and Escherichia coli enterotoxins. Infect. Immun., 1982, 35(2), 471-475.
[PMID: 7035365]
[281]
Li, G.H.; Wang, D.L.; Hu, Y.D.; Pu, P.; Li, D.Z.; Wang, W.D.; Zhu, B.; Hao, P.; Wang, J.; Xu, X.Q.; Wan, J.Q.; Zhou, Y.B.; Chen, Z.T. Berberine inhibits acute radiation intestinal syndrome in human with abdomen radiotherapy. Med. Oncol., 2010, 27(3), 919-925.
[http://dx.doi.org/10.1007/s12032-009-9307-8] [PMID: 19757213]
[282]
Xue, M.; Yang, M.X.; Zhang, W.; Li, X.M.; Gao, D.H.; Ou, Z.M.; Li, Z.P.; Liu, S.H.; Li, X.J.; Yang, S.Y. Characterization, pharmacokinetics, and hypoglycemic effect of berberine loaded solid lipid nanoparticles. Int. J. Nanomedicine, 2013, 8, 4677-4687.
[http://dx.doi.org/10.2147/IJN.S51262] [PMID: 24353417]
[283]
Xue, M.; Zhang, L.; Yang, M.X.; Zhang, W.; Li, X.M.; Ou, Z.M.; Li, Z.P.; Liu, S.H.; Li, X.J.; Yang, S.Y. Berberine-loaded solid lipid nanoparticles are concentrated in the liver and ameliorate hepatosteatosis in db/db mice. Int. J. Nanomedicine, 2015, 10, 5049-5057.
[http://dx.doi.org/10.2147/IJN.S84565] [PMID: 26346310]
[284]
Lin, Y.H.; Lin, J.H.; Chou, S.C.; Chang, S.J.; Chung, C.C.; Chen, Y.S.; Chang, C.H. Berberine-loaded targeted nanoparticles as specific Helicobacter pylori eradication therapy: In vitro and in vivo study. Nanomedicine (Lond.), 2015, 10(1), 57-71.
[http://dx.doi.org/10.2217/nnm.14.76] [PMID: 25177920]
[285]
Chang, C.H.; Huang, W.Y.; Lai, C.H.; Hsu, Y.M.; Yao, Y.H.; Chen, T.Y.; Wu, J.Y.; Peng, S.F.; Lin, Y.H. Development of novel nanoparticles shelled with heparin for berberine delivery to treat Helicobacter pylori. Acta Biomater., 2011, 7(2), 593-603.
[http://dx.doi.org/10.1016/j.actbio.2010.08.028] [PMID: 20813208]
[286]
Yu, F.; Ao, M.; Zheng, X.; Li, N.; Xia, J.; Li, Y.; Li, D.; Hou, Z.; Qi, Z.; Chen, X.D. PEG-lipid-PLGA hybrid nanoparticles loaded with berberine-phospholipid complex to facilitate the oral delivery efficiency. Drug Deliv., 2017, 24(1), 825-833.
[http://dx.doi.org/10.1080/10717544.2017.1321062] [PMID: 28509588]


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