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Endocrine, Metabolic & Immune Disorders - Drug Targets

Editor-in-Chief

ISSN (Print): 1871-5303
ISSN (Online): 2212-3873

Review Article

Molecular Mechanisms of Curcumin in Neuroinflammatory Disorders: A Mini Review of Current Evidences

Author(s): Mahsa Hatami, Mina Abdolahi, Neda Soveyd, Mahmoud Djalali, Mansoureh Togha and Niyaz Mohammadzadeh Honarvar*

Volume 19, Issue 3, 2019

Page: [247 - 258] Pages: 12

DOI: 10.2174/1871530319666181129103056

Price: $65

Abstract

Objective: Neuroinflammatory disease is a general term used to denote the progressive loss of neuronal function or structure. Many neuroinflammatory diseases, including Alzheimer’s, Parkinson’s, and multiple sclerosis (MS), occur due to neuroinflammation. Neuroinflammation increases nuclear factor-κB (NF-κB) levels, cyclooxygenase-2 enzymes and inducible nitric oxide synthase, resulting in the release of inflammatory cytokines, such as interleukin-6 (IL-6), interleukin-1β (IL-1β) and tumor necrosis factor-α (TNF-α). It could also lead to cellular deterioration and symptoms of neuroinflammatory diseases. Recent studies have suggested that curcumin (the active ingredient in turmeric) could alleviate the process of neuroinflammatory disease. Thus, the present mini-review was conducted to summarize studies regarding cellular and molecular targets of curcumin relevant to neuroinflammatory disorders.

Methods: A literature search strategy was conducted for all English-language literature. Studies that assessed the various properties of curcuminoids in respect of neuroinflammatory disorders were included in this review.

Results: The studies have suggested that curcuminoids have significant anti- neuroinflammatory, antioxidant and neuroprotective properties that could attenuate the development and symptom of neuroinflammatory disorders. Curcumin can alleviate neurodegeneration and neuroinflammation through multiple mechanisms, by reducing inflammatory mediators (such as TNF-α, IL-1β, nitric oxide and NF-κB gene expression), and affect mitochondrial dynamics and even epigenetic changes.

Conclusion: It is a promising subject of study in the prevention and management of the neuroinflammatory disease. However, controlled, randomized clinical trials are needed to fully evaluate its clinical potential.

Keywords: Neuroinflammatory disorders, Alzheimer's disease, Parkinson's disease, multiple sclerosis, curcumin, nanocurcumin.

Graphical Abstract
[1]
Ghosh, S.; Banerjee, S.; Sil, P.C. The beneficial role of curcumin on inflammation, diabetes and neurodegenerative disease: A recent update. Food Chem. Toxicol., 2015, 83, 111-124.
[2]
Hurley, L.L.; Tizabi, Y. Neuroinflammation, neurodegeneration, and depression. Neurotox. Res., 2013, 23(2), 131-144.
[3]
Ryan, S.M.; Nolan, Y.M. Neuroinflammation negatively affects adult hippocampal neurogenesis and cognition: can exercise compensate? Neurosci. Biobehav. Rev., 2015, 61, 121-131.
[4]
Lyman, M.; Lloyd, D.G.; Ji, X.; Vizcaychipi, M.P.; Ma, D. Neuroinflammation: The role and consequences. Neurosci. Res., 2014, 79, 1-12.
[5]
Carriba, P.; Comella, J.X. Neurodegeneration and neuroinflammation: two processes, one target. Neural Regen. Res., 2015, 10(10), 1581-1583.
[6]
Deguchi, A. Curcumin targets in inflammation and cancer. Endocr. Metab. Immune Disord. Drug Targets, 2015, 15(2), 88-96.
[7]
Shishodia, S. Molecular mechanisms of curcumin action: Gene expression. Biofactors, 2013, 39(1), 37-55.
[8]
Shehzad, A.; Rehman, G.; Lee, Y.S. Curcumin in inflammatory diseases. Biofactors, 2013, 39(1), 69-77.
[9]
Chen, W.W.; Zhang, X.; Huang, W.J. Role of neuroinflammation in neurodegenerative diseases (Review). Mol. Med. Rep., 2016, 13(4), 3391-3396.
[10]
Gao, H-M.; Hong, J-S. Why neurodegenerative diseases are progressive: uncontrolled inflammation drives disease progression. Trends Immunol., 2008, 29(8), 357-365.
[11]
Brites, D.; Fernandes, A. Neuroinflammation and depression: Microglia activation, extracellular microvesicles and microRNA dysregulation. Front. Cell. Neurosci., 2015, 9, 476.
[12]
Kopitar-Jerala, N. Innate immune response in brain, NF-Kappa B signaling and cystatins. Front. Mol. Neurosci., 2015, 8, 73.
[13]
Klos, A.; Wende, E.; Wareham, K.J.; Monk, P.N. International union of basic and clinical pharmacology. [corrected]. LXXXVII. Complement peptide C5a, C4a, and C3a receptors. Pharmacol. Rev., 2013, 65(1), 500-543.
[14]
Scapagnini, G.; Vasto, S.; Abraham, N.G.; Caruso, C.; Zella, D.; Fabio, G. Modulation of Nrf2/ARE pathway by food polyphenols: A nutritional neuroprotective strategy for cognitive and neurodegenerative disorders. Mol. Neurobiol., 2011, 44(2), 192-201.
[15]
Dumont, M.; Wille, E.; Calingasan, N.Y.; Tampellini, D.; Williams, C.; Gouras, G.K.; Liby, K.; Sporn, M.; Flint Beal, M.; Lin, M.T. Triterpenoid CDDO‐methylamide improves memory and decreases amyloid plaques in a transgenic mouse model of Alzheimer’s disease. J. Neurochem., 2009, 109(2), 502-512.
[16]
Kalyanaraman, B. Teaching the basics of redox biology to medical and graduate students: oxidants, antioxidants and disease mechanisms. Redox Biol., 2013, 1(1), 244-257.
[17]
Szabó, C.; Ischiropoulos, H.; Radi, R. Peroxynitrite: Biochemistry, pathophysiology and development of therapeutics. Nat. Rev. Drug Discov., 2007, 6(8), 662-680.
[18]
Kothur, K.; Wienholt, L.; Brilot, F.; Dale, R.C. CSF cytokines/chemokines as biomarkers in neuroinflammatory CNS disorders: A systematic review. Cytokine, 2016, 77, 227-237.
[19]
Ray, B.; Lahiri, D.K. Neuroinflammation in Alzheimer’s disease: Different molecular targets and potential therapeutic agents including curcumin. Curr. Opin. Pharmacol., 2009, 9(4), 434-444.
[20]
Khairova, R.A.; Machado-Vieira, R.; Du, J.; Manji, H.K. A potential role for pro-inflammatory cytokines in regulating synaptic plasticity in major depressive disorder. Int. J. Neuropsychopharmacol., 2009, 12(4), 561-578.
[21]
Leonard, B.E. Inflammation, depression and dementia: Are they connected? Neurochem. Res., 2007, 32(10), 1749-1756.
[22]
Vojdani, A.; Lambert, J. The role of Th17 in neuroimmune disorders: target for CAM therapy. Part I. Evid. Based Complement. Alternat. Med., 2011, 2011, 927294.
[23]
Morales, I.; Guzman-Martinez, L.; Cerda-Troncoso, C.; Farias, G.A.; Maccioni, R.B. Neuroinflammation in the pathogenesis of Alzheimer’s disease. A rational framework for the search of novel therapeutic approaches. Front. Cell. Neurosci., 2014, 8, 112.
[24]
Aggarwal, B.B.; Sundaram, C.; Malani, N.; Ichikawa, H. Curcumin: The Indian solid gold. In: The molecular targets and therapeutic uses of curcumin in health and disease; Springer, 2007; pp. 1-75.
[25]
Kim, D.S.; Kim, J.Y.; Han, Y. Curcuminoids in neurodegenerative diseases. Recent Patents CNS Drug Discov., 2012, 7(3), 184-204.
[26]
Priyadarsini, K.I. Photophysics, photochemistry and photobiology of curcumin: Studies from organic solutions, bio-mimetics and living cells. J. Photochem. Photobiol. C. Photochem. Rev., 2009, 10(2), 81-95.
[27]
Galano, A.; Álvarez-Diduk, R.; Ramírez-Silva, M.T.; Alarcón-Ángeles, G.; Rojas-Hernández, A. Role of the reacting free radicals on the antioxidant mechanism of curcumin. Chem. Phys., 2009, 363(1-3), 13-23.
[28]
Yanagisawa, D.; Shirai, N.; Amatsubo, T.; Taguchi, H.; Hirao, K.; Urushitani, M.; Morikawa, S.; Inubushi, T.; Kato, M.; Kato, F.; Morino, K.; Kimura, H.; Nakano, I.; Yoshida, C.; Okada, T.; Sano, M.; Wada, Y.; Wada, K-N.; Yamamoto, A.; Tooyama, I. Relationship between the tautomeric structures of curcumin derivatives and their Aβ-binding activities in the context of therapies for Alzheimer’s disease. Biomaterials, 2010, 31(14), 4179-4185.
[29]
(a) Ghalandarlaki, N.; Alizadeh, A.M.; Ashkani-Esfahani, S. Nanotechnology-applied curcumin for different diseases therapy. BioMed Res. Int., 2014, 2014, 394264.
(b) Li, Y.; Wang, P. [Neuroprotective effects of curcumin]. Zhongguo Zhongyao Zazhi, 2009, 34(24), 3173-3175.
[30]
Singh, R.; Sharma, P. Hepatoprotective effect of curcumin on lindane-induced oxidative stress in male Wistar rats. Toxicol. Int., 2011, 18(2), 124-129.
[31]
Aggarwal, B.B.; Harikumar, K.B. Potential therapeutic effects of curcumin, the anti-inflammatory agent, against neurodegenerative, cardiovascular, pulmonary, metabolic, autoimmune and neoplastic diseases. Int. J. Biochem. Cell Biol., 2009, 41(1), 40-59.
[32]
Hurley, L.L.; Akinfiresoye, L.; Nwulia, E.; Kamiya, A.; Kulkarni, A.A.; Tizabi, Y. Antidepressant-like effects of curcumin in WKY rat model of depression is associated with an increase in hippocampal BDNF. Behav. Brain Res., 2013, 239, 27-30.
[33]
Sikora-Polaczek, M.; Bielak-Zmijewska, A.; Sikora, E. [Molecular and cellular mechanisms of curcumin action--beneficial effect on organism]. Postepy Biochem., 2011, 57(1), 74-84.
[34]
Tizabi, Y.; Hurley, L.L.; Qualls, Z.; Akinfiresoye, L. Relevance of the anti-inflammatory properties of curcumin in neurodegenerative diseases and depression. Molecules, 2014, 19(12), 20864-20879.
[35]
Alladi, P.; Mahadevan, A.; Yasha, T.; Raju, T.; Shankar, S.; Muthane, U. Absence of age-related changes in nigral dopaminergic neurons of Asian Indians: relevance to lower incidence of Parkinson’s disease. Neuroscience, 2009, 159(1), 236-245.
[36]
Venigalla, M.; Gyengesi, E.; Munch, G. Curcumin and Apigenin - novel and promising therapeutics against chronic neuroinflammation in Alzheimer’s disease. Neural Regen. Res., 2015, 10(8), 1181-1185.
[37]
Rao, M. Nitric oxide scavenging by curcuminoids. J. Pharm. Pharmacol., 1997, 49(1), 105-107.
[38]
Masuda, T.; Hidaka, K.; Shinohara, A.; Maekawa, T.; Takeda, Y.; Yamaguchi, H. Chemical studies on antioxidant mechanism of curcuminoid: Analysis of radical reaction products from curcumin. J. Agric. Food Chem., 1999, 47(1), 71-77.
[39]
Balogun, E.; Hoque, M.; Gong, P.; Killeen, E.; Green, C.; Foresti, R.; Alam, J.; Motterlini, R. Curcumin activates the haem oxygenase-1 gene via regulation of Nrf2 and the antioxidant-responsive element. Biochem. J., 2003, 371, 887-895.
[40]
Guimarães, M.R.; Leite, F.R.M.; Spolidorio, L.C.; Kirkwood, K.L.; Rossa, C. Curcumin abrogates LPS-induced pro-inflammatory cytokines in RAW 264.7 macrophages. Evidence for novel mechanisms involving SOCS-1,-3 and p38 MAPK. Arch. Oral Biol., 2013, 58(10), 1309-1317.
[41]
Morris, G.; Anderson, G.; Dean, O.; Berk, M.; Galecki, P.; Martin-Subero, M.; Maes, M. The glutathione system: A new drug target in neuroimmune disorders. Mol. Neurobiol., 2014, 50(3), 1059-1084.
[42]
Hu, Y.; Tang, J.S.; Hou, S.X.; Shi, X.X.; Qin, J.; Zhang, T.S.; Wang, X.J. Neuroprotective effects of curcumin alleviate lumbar intervertebral disc degeneration through regulating the expression of iNOS, COX-2, TGF-β1/2, MMP-9 and BDNF in a rat model. Mol. Med. Rep., 2017, 16(5), 6864-6869.
[43]
Kang, G.; Kong, P-J.; Yuh, Y-J.; Lim, S-Y.; Yim, S-V.; Chun, W.; Kim, S-S. Curcumin suppresses lipopolysaccharide-induced cyclooxygenase-2 expression by inhibiting activator protein 1 and nuclear factor. KAPPA. B bindings in bv2 microglial cells. J. Pharmacol. Sci., 2004, 94(3), 325-328.
[44]
Koeberle, A.; Northoff, H.; Werz, O. Curcumin blocks prostaglandin E2 biosynthesis through direct inhibition of the microsomal prostaglandin E2 synthase-1. Mol. Cancer Ther., 2009, 8(8), 2348-2355.
[45]
Huang, M-T.; Lysz, T.; Ferraro, T.; Abidi, T.F.; Laskin, J.D.; Conney, A.H. Inhibitory effects of curcumin on in vitro lipoxygenase and cyclooxygenase activities in mouse epidermis. Cancer Res., 1991, 51(3), 813-819.
[46]
Raposo, C.; Nunes, A.K.; Luna, R.L.; Araújo, S.M.; da Cruz-Höfling, M.A.; Peixoto, C.A. Sildenafil (Viagra) protective effects on neuroinflammation: the role of iNOS/NO system in an inflammatory demyelination model. Mediators Inflamm., 2013, 2013, 321460.
[47]
Jiang, J.; Wang, W.; Sun, Y.J.; Hu, M.; Li, F.; Zhu, D.Y. Neuroprotective effect of curcumin on focal cerebral ischemic rats by preventing blood–brain barrier damage. Eur. J. Pharmacol., 2007, 561(1-3), 54-62.
[48]
Jung, K.K.; Lee, H.S.; Cho, J.Y.; Shin, W.C.; Rhee, M.H.; Kim, T.G.; Kang, J.H.; Kim, S.H.; Hong, S.; Kang, S.Y. Inhibitory effect of curcumin on nitric oxide production from lipopolysaccharide-activated primary microglia. Life Sci., 2006, 79(21), 2022-2031.
[49]
Austin, S.A.; Santhanam, A.V.; Hinton, D.J.; Choi, D.S.; Katusic, Z.S. Endothelial nitric oxide deficiency promotes Alzheimer’s disease pathology. J. Neurochem., 2013, 127(5), 691-700.
[50]
Morales, N.P.; Sirijaroonwong, S.; Yamanont, P.; Phisalaphong, C. Electron paramagnetic resonance study of the free radical scavenging capacity of curcumin and its demethoxy and hydrogenated derivatives. Biol. Pharm. Bull., 2015, 38(10), 1478-1483.
[51]
(a) Menon, V.P.; Sudheer, A.R. Antioxidant and anti-inflammatory properties of curcumin. Adv. Exp. Med. Biol., 2007, 595, 105-125.
(b) Choi, D.K.; Koppula, S.; Suk, K. Inhibitors of microglial neurotoxicity: focus on natural products. Molecules (Basel, Switzerland), 2011, 16(2), 1021-1043.
[52]
He, H-J.; Wang, G-Y.; Gao, Y.; Ling, W-H.; Yu, Z-W.; Jin, T-R. Curcumin attenuates Nrf2 signaling defect, oxidative stress in muscle and glucose intolerance in high fat diet-fed mice. World J. Diabetes, 2012, 3(5), 94.
[53]
Gupta, S.C.; Tyagi, A.K.; Deshmukh-Taskar, P.; Hinojosa, M.; Prasad, S.; Aggarwal, B.B. Downregulation of tumor necrosis factor and other proinflammatory biomarkers by polyphenols. Arch. Biochem. Biophys., 2014, 559, 91-99.
[54]
Balamurugan, A.; Akhov, L.; Selvaraj, G.; Pugazhenthi, S. Induction of antioxidant enzymes by curcumin and its analogues in human islets: implications in transplantation. Pancreas, 2009, 38(4), 454-460.
[55]
He, L.F.; Chen, H.J.; Qian, L.H.; Chen, G.Y.; Buzby, J.S. Curcumin protects pre-oligodendrocytes from activated microglia in vitro and in vivo. Brain Res., 2010, 1339, 60-69.
[56]
Cole, G.M.; Teter, B.; Frautschy, S.A. Neuroprotective effects of curcumin. Adv. Exp. Med. Biol., 2007, 595, 197-212.
[57]
Yu, Y.; Shen, Q.; Lai, Y.; Park, S.Y.; Ou, X.; Lin, D.; Jin, M.; Zhang, W. Anti-inflammatory effects of curcumin in microglial cells. Front. Pharmacol., 2018, 9, 386.
[58]
(a) Sezgin, Z.; Dincer, Y. Alzheimer’s disease and epigenetic diet. Neurochem. Int., 2014, 78, 105-116.
(b) Ullah, F.; Liang, A.; Rangel, A.; Gyengesi, E.; Niedermayer, G.; Münch, G. High bioavailability curcumin: An anti-inflammatory and neurosupportive bioactive nutrient for neurodegenerative diseases characterized by chronic neuroinflammation. Arch. Toxicol., 2017, 91(4), 1623-1634.
[59]
Cole, G.M.; Teter, B.; Frautschy, S.A. Neuroprotective effects of curcumin. In: The molecular targets and therapeutic uses of curcumin in health and disease; Springer, 2007; pp. 197-212.
[60]
Scapagnini, G.; Calabrese, V.; Motterlini, R.; Colombrita, C.; Alkon, D. Use of curcumin derivatives or CAPE in the manufacture of a medicament for the treatment of neuroprotective disorders. WO2004075883A1, September 10, 2004.
[61]
Eckert, G.P.; Renner, K.; Eckert, S.H.; Eckmann, J.; Hagl, S.; Abdel-Kader, R.M.; Kurz, C.; Leuner, K.; Muller, W.E. Mitochondrial dysfunction-A pharmacological target in Alzheimer’s disease. Mol. Neurobiol., 2012, 46(1), 136-150.
[62]
Chen, H.; Detmer, S.A.; Ewald, A.J.; Griffin, E.E.; Fraser, S.E.; Chan, D.C. Mitofusins Mfn1 and Mfn2 coordinately regulate mitochondrial fusion and are essential for embryonic development. J. Cell Biol., 2003, 160(2), 189-200.
[63]
Wang, X.; Su, B.; Fujioka, H.; Zhu, X. Dynamin-like protein 1 reduction underlies mitochondrial morphology and distribution abnormalities in fibroblasts from sporadic Alzheimer’s disease patients. Am. J. Pathol., 2008, 173(2), 470-482.
[64]
Eckert, G.P.; Schiborr, C.; Hagl, S.; Abdel-Kader, R.; Müller, W.E.; Rimbach, G.; Frank, J. Curcumin prevents mitochondrial dysfunction in the brain of the senescence-accelerated mouse-prone 8. Neurochem. Int., 2013, 62(5), 595-602.
[65]
Zhu, Y.G.; Chen, X.C.; Chen, Z.Z.; Zeng, Y.Q.; Shi, G.B.; Su, Y.H.; Peng, X. Curcumin protects mitochondria from oxidative damage and attenuates apoptosis in cortical neurons. Acta Pharmacol. Sin., 2004, 25, 1606-1612.
[66]
Ventura-Clapier, R.; Garnier, A.; Veksler, V. Transcriptional control of mitochondrial biogenesis: the central role of PGC-1α. Cardiovasc. Res., 2008, 79(2), 208-217.
[67]
Boyanapalli, S.S.; Kong, A.N.T. “Curcumin, the King of Spices”: Epigenetic regulatory mechanisms in the prevention of cancer, neurological, and inflammatory diseases. Curr. Pharmacol. Rep., 2015, 1(2), 129-139.
[68]
Chen, K.L.; Wang, S.S.; Yang, Y.Y.; Yuan, R.Y.; Chen, R.M.; Hu, C.J. The epigenetic effects of amyloid-β 1-40 on global DNA and neprilysin genes in murine cerebral endothelial cells. Biochem. Biophys. Res. Commun., 2009, 378(1), 57-61.
[69]
Wada, T.T.; Araki, Y.; Sato, K.; Aizaki, Y.; Yokota, K.; Kim, Y.T.; Oda, H.; Kurokawa, R.; Mimura, T. Aberrant histone acetylation contributes to elevated interleukin-6 production in rheumatoid arthritis synovial fibroblasts. Biochem. Biophys. Res. Commun., 2014, 444(4), 682-686.
[70]
Yun, J.M.; Jialal, I.; Devaraj, S. Epigenetic regulation of high glucose-induced proinflammatory cytokine production in monocytes by curcumin. J. Nutr. Biochem., 2011, 22(5), 450-458.
[71]
Miller, G. A role for epigenetics in cognition. Science, 2010, 329(5987), 27-27.
[72]
Sun, M.; Estrov, Z.; Ji, Y.; Coombes, K.R.; Harris, D.H.; Kurzrock, R. Curcumin (diferuloylmethane) alters the expression profiles of microRNAs in human pancreatic cancer cells. Mol. Cancer Ther., 2008, 7(3), 464-473.
[73]
Mohamed, T.; Shakeri, A.; Rao, P.P. Amyloid cascade in Alzheimer’s disease: Recent advances in medicinal chemistry. Eur. J. Med. Chem., 2016, 113, 258-272.
[74]
Wang, J.; Yu, J.T.; Tan, M.S.; Jiang, T.; Tan, L. Epigenetic mechanisms in Alzheimer’s disease: Implications for pathogenesis and therapy. Ageing Res. Rev., 2013, 12(4), 1024-1041.
[75]
Chouliaras, L.; Mastroeni, D.; Delvaux, E.; Grover, A.; Kenis, G.; Hof, P.R.; Steinbusch, H.W.; Coleman, P.D.; Rutten, B.P.; van den Hove, D.L. Consistent decrease in global DNA methylation and hydroxymethylation in the hippocampus of Alzheimer’s disease patients. Neurobiol. Aging, 2013, 34(9), 2091-2099.
[76]
Cristovao, J.S.; Santos, R. Metals and neuronal metal binding proteins implicated in Alzheimer’s disease. Oxid. Med. Cell. Longev., 2016, 2016, 9812178.
[77]
Venigalla, M.; Sonego, S.; Gyengesi, E.; Sharman, M.J.; Munch, G. Novel promising therapeutics against chronic neuroinflammation and neurodegeneration in Alzheimer’s disease. Neurochem. Int., 2015, 95, 63-74.
[78]
Bassani, T.B.; Turnes, J.M.; Moura, E.L.; Bonato, J.M.; Cóppola-Segovia, V.; Zanata, S.M.; Oliveira, R.M.; Vital, M.A. Effects of curcumin on short-term spatial and recognition memory, adult neurogenesis and neuroinflammation in a streptozotocin-induced rat model of dementia of Alzheimer’s type. Behav. Brain Res., 2017, 335, 41-54.
[79]
Siddique, Y.H.; Naz, F.; Jyoti, S. Effect of curcumin on lifespan, activity pattern, oxidative stress, and apoptosis in the brains of transgenic Drosophila model of Parkinson’s disease. BioMed Res. Int., 2014, 2014, 606928.
[80]
Mogi, M.; Harada, M.; Narabayashi, H.; Inagaki, H.; Minami, M.; Nagatsu, T. Interleukin (IL)-1β, IL-2, IL-4, IL-6 and transforming growth factor-α levels are elevated in ventricular cerebrospinal fluid in juvenile parkinsonism and Parkinson’s disease. Neurosci. Lett., 1996, 211(1), 13-16.
[81]
Urdinguio, R.G.; Sanchez-Mut, J.V.; Esteller, M. Epigenetic mechanisms in neurological diseases: Genes, syndromes, and therapies. Lancet Neurol., 2009, 8(11), 1056-1072.
[82]
Mythri, R.B.; Bharath, M.M. Curcumin: A potential neuroprotective agent in Parkinson’s disease. Curr. Pharm. Des., 2012, 18(1), 91-99.
[83]
(a) Aquilano, K.; Baldelli, S.; Rotilio, G.; Ciriolo, M.R. Role of nitric oxide synthases in Parkinson’s disease: A review on the antioxidant and anti-inflammatory activity of polyphenols. Neurochem. Res., 2008, 33(12), 2416-2426.
(b) Sharma, N.; Sharma, S.; Nehru, B. Curcumin protects dopaminergic neurons against inflammation-mediated damage and improves motor dysfunction induced by single intranigral lipopolysaccharide injection. Inflammopharmacology, 2017, 25(3), 351-368.
[84]
Cui, Q.; Li, X.; Zhu, H. Curcumin ameliorates dopaminergic neuronal oxidative damage via activation of the Akt/Nrf2 pathway. Mol. Med. Rep., 2016, 13(2), 1381-1388.
[85]
Wang, J.; Du, X.X.; Jiang, H.; Xie, J.X. Curcumin attenuates 6-hydroxydopamine-induced cytotoxicity by anti-oxidation and nuclear factor-kappaB modulation in MES23. 5 cells. Biochem. Pharmacol., 2009, 78(2), 178-183.
[86]
Yu, S.; Zheng, W.; Xin, N.; Chi, Z.H.; Wang, N.Q.; Nie, Y.X.; Feng, W.Y.; Wang, Z.Y. Curcumin prevents dopaminergic neuronal death through inhibition of the c-Jun N-terminal kinase pathway. Rejuvenation Res., 2010, 13(1), 55-64.
[87]
Song, J.X.; Sze, S.C.; Ng, T.B.; Lee, C.K.; Leung, G.P.; Shaw, P.C.; Tong, Y.; Zhang, Y.B. Anti-Parkinsonian drug discovery from herbal medicines: what have we got from neurotoxic models? J. Ethnopharmacol., 2012, 139(3), 698-711.
[88]
(a) Abdolahi, M.; Yavari, P.; Honarvar, N.M.; Bitarafan, S.; Mahmoudi, M.; Saboor-Yaraghi, A.A. Molecular mechanisms of the action of vitamin A in Th17/Treg axis in multiple sclerosis. J. Mol. Neurosci., 2015, 57(4), 605-613.
(b) Honarvar, N.M.; Harirchian, M.H.; Abdolahi, M.; Abedi, E.; Bitarafan, S.; Koohdani, F.; Siassi, F.; Sahraian, M.A.; Chahardoli, R.; Zareei, M. Retinyl palmitate supplementation modulates T-bet and interferon gamma gene expression in multiple sclerosis patients. J. Mol. Neurosci., 2016, 59(3), 360-365.
[89]
Honarvar, N.M.; Saedisomeolia, A.; Abdolahi, M.; Shayeganrad, A.; Sangsari, G.T.; Rad, B.H.; Muench, G. Molecular anti-inflammatory mechanisms of retinoids and carotenoids in Alzheimer’s disease: A review of current evidence. J. Mol. Neurosci., 2017, 61(3), 289-304.
[90]
Dorosty-Motlagh, A.R.; Honarvar, N.M.; Sedighiyan, M.; Abdolahi, M. The molecular mechanisms of vitamin A deficiency in multiple sclerosis. J. Mol. Neurosci., 2016, 60(1), 82-90.
[91]
Mastronardi, F.G.; Noor, A.; Wood, D.D.; Paton, T.; Moscarello, M.A. Peptidyl argininedeiminase 2 CpG island in multiple sclerosis white matter is hypomethylated. J. Neurosci. Res., 2007, 85(9), 2006-2016.
[92]
Xie, L.; Li, X.K.; Funeshima-Fuji, N.; Kimura, H.; Matsumoto, Y.; Isaka, Y.; Takahara, S. Amelioration of experimental autoimmune encephalomyelitis by curcumin treatment through inhibition of IL-17 production. Int. Immunopharmacol., 2009, 9(5), 575-581.
[93]
Bondan, E.; Cardoso, C.; Martins, M.D.F. Curcumin decreases astrocytic reaction after gliotoxic injury in the rat brainstem. Arq. Neuropsiquiatr., 2017, 75(8), 546-552.
[94]
Bachmeier, B.E.; Mohrenz, I.V.; Mirisola, V.; Schleicher, E.; Romeo, F.; Höhneke, C.; Jochum, M.; Nerlich, A.G.; Pfeffer, U. Curcumin downregulates the inflammatory cytokines CXCL1 and-2 in breast cancer cells via NFκB. Carcinogenesis, 2008, 29(4), 779-789.
[95]
Kanakasabai, S.; Casalini, E.; Walline, C.C.; Mo, C.; Chearwae, W.; Bright, J.J. Differential regulation of CD4(+) T helper cell responses by curcumin in experimental autoimmune encephalomyelitis. J. Nutr. Biochem., 2012, 23(11), 1498-1507.
[96]
Choi, K.H.; Park, J.W.; Kim, H.Y.; Kim, Y.H.; Kim, S.M.; Son, Y.H.; Park, Y.C.; Eo, S.K.; Kim, K. Cellular factors involved in CXCL8 expression induced by glycated serum albumin in vascular smooth muscle cells. Atherosclerosis, 2010, 209(1), 58-65.
[97]
Xie, L.; Li, X.K.; Takahara, S. Curcumin has bright prospects for the treatment of multiple sclerosis. Int. Immunopharmacol., 2011, 11(3), 323-330.
[98]
Hong, J.; Bose, M.; Ju, J.; Ryu, J.H.; Chen, X.; Sang, S.; Lee, M.J.; Yang, C.S. Modulation of arachidonic acid metabolism by curcumin and related β-diketone derivatives: Effects on cytosolic phospholipase A2, cyclooxygenases and 5-lipoxygenase. Carcinogenesis, 2004, 25(9), 1671-1679.
[99]
Aranami, T.; Yamamura, T. Th17 cells and autoimmune encephalomyelitis (EAE/MS). Allergol. Int., 2008, 57(2), 115-120.
[100]
Abdolahi, M.; Yavari, P.; Honarvar, N.M.; Bitarafan, S.; Mahmoudi, M.; Saboor-Yaraghi, A.A. Molecular mechanisms of the action of vitamin A in Th17/Treg axis in multiple sclerosis. J. Mol. Neurosci., 2015, 57(4), 605-613.
[101]
Zhang, H.J.; Xing, Y.Q.; Jin, W.; Li, D.; Wu, K.; Lu, Y. Effects of curcumin on interleukin-23 and interleukin-17 expression in rat retina after retinal ischemia-reperfusion injury. Int. J. Clin. Exp. Pathol., 2015, 8(8), 9223-9231.
[102]
Qureshi, M.; Al-Suhaimi, E.A.; Wahid, F.; Shehzad, O.; Shehzad, A. Therapeutic potential of curcumin for multiple sclerosis. Neurol. Sci., 2017, 39(2), 207-214.

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