Evaluation of Anti-inflammatory Nutraceuticals in LPS-induced Mouse Neuroinflammation Model: An Update

Author(s): Miryam Nava Catorce, Goar Gevorkian*

Journal Name: Current Neuropharmacology

Volume 18 , Issue 7 , 2020


Become EABM
Become Reviewer
Call for Editor

Graphical Abstract:


Abstract:

It is known that peripheral infections, accompanied by inflammation, represent significant risk factors for the development of neurological disorders by modifying brain development or affecting normal brain aging. The acute effects of systemic inflammation on progressive and persistent brain damage and cognitive impairment are well documented. Anti-inflammatory therapies may have beneficial effects on the brain, and the protective properties of a wide range of synthetic and natural compounds have been extensively explored in recent years. In our previous review, we provided an extensive analysis of one of the most important and widely-used animal models of peripherally induced neuroinflammation and neurodegeneration - lipopolysaccharide (LPS)-treated mice. We addressed the data reproducibility in published research and summarized basic features and data on the therapeutic potential of various natural products, nutraceuticals, with known antiinflammatory effects, for reducing neuroinflammation in this model. Here, recent data on the suitability of the LPS-induced murine neuroinflammation model for preclinical assessment of a large number of nutraceuticals belonging to different groups of natural products such as flavonoids, terpenes, non-flavonoid polyphenols, glycosides, heterocyclic compounds, organic acids, organosulfur compounds and xanthophylls, are summarized. Also, the proposed mechanisms of action of these molecules are discussed.

Keywords: Neuroinflammation, nutraceuticals, LPS, neurodegeneration, peripheral inflammation, mouse model.

[1]
Eikelenboom, P.; van Exel, E.; Hoozemans, J.J.; Veerhuis, R.; Rozemuller, A.J.; van Gool, W.A. Neuroinflammation - an early event in both the history and pathogenesis of Alzheimer’s disease. Neurodegener. Dis., 2010, 7(1-3), 38-41.
[http://dx.doi.org/10.1159/000283480] [PMID: 20160456 ]
[2]
Heneka, M.T.; Kummer, M.P.; Latz, E. Innate immune activation in neurodegenerative disease. Nat. Rev. Immunol., 2014, 14(7), 463-477.
[http://dx.doi.org/10.1038/nri3705] [PMID: 24962261 ]
[3]
Pasqualetti, G.; Brooks, D.J.; Edison, P. The role of neuroinflammation in dementias. Curr. Neurol. Neurosci. Rep., 2015, 15(4), 17.
[http://dx.doi.org/10.1007/s11910-015-0531-7] [PMID: 25716012 ]
[4]
Calsolaro, V.; Edison, P. Neuroinflammation in Alzheimer’s disease: Current evidence and future directions. Alzheimers Dement., 2016, 12(6), 719-732.
[http://dx.doi.org/10.1016/j.jalz.2016.02.010] [PMID: 27179961 ]
[5]
Ransohoff, R.M. How neuroinflammation contributes to neurodegeneration. Science, 2016, 353(6301), 777-783.
[http://dx.doi.org/10.1126/science.aag2590] [PMID: 27540165 ]
[6]
Nichols, M.R.; St-Pierre, M.K.; Wendeln, A.C.; Makoni, N.J.; Gouwens, L.K.; Garrad, E.C.; Sohrabi, M.; Neher, J.J.; Tremblay, M.E.; Combs, C.K. Inflammatory mechanisms in neurodegeneration. J. Neurochem., 2019, 149(5), 562-581.
[http://dx.doi.org/10.1111/jnc.14674] [PMID: 30702751 ]
[7]
Exalto, L.G.; Whitmer, R.A.; Kappele, L.J.; Biessels, G.J. An update on type 2 diabetes, vascular dementia and Alzheimer’s disease. Exp. Gerontol., 2012, 47(11), 858-864.
[http://dx.doi.org/10.1016/j.exger.2012.07.014] [PMID: 22884853 ]
[8]
Ledesma, M.D.; Dotti, C.G. Peripheral cholesterol, metabolic disorders and Alzheimer’s disease. Front. Biosci. (Elite Ed.), 2012, 4, 181-194.
[http://dx.doi.org/10.2741/e368] [PMID: 22201863 ]
[9]
Ferreira, S.T.; Clarke, J.R.; Bomfim, T.R.; De Felice, F.G. Inflammation, defective insulin signaling, and neuronal dysfunction in Alzheimer’s disease. Alzheimers Dement., 2014, 10(1)(Suppl.), S76-S83.
[http://dx.doi.org/10.1016/j.jalz.2013.12.010] [PMID: 24529528 ]
[10]
Holmes, C.; Cotterell, D. Role of infection in the pathogenesis of Alzheimer’s disease: implications for treatment. CNS Drugs, 2009, 23(12), 993-1002.
[http://dx.doi.org/10.2165/11310910-000000000-00000] [PMID: 19958038 ]
[11]
Su, X.; Federoff, H.J. Immune responses in Parkinson’s disease: interplay between central and peripheral immune systems. BioMed Res. Int., 2014, 2014275178
[http://dx.doi.org/10.1155/2014/275178] [PMID: 24822191 ]
[12]
Gale, S.D.; Erickson, L.D.; Berrett, A.; Brown, B.L.; Hedges, D.W. Infectious disease burden and cognitive function in young to middle-aged adults. Brain Behav. Immun., 2016, 52, 161-168.
[http://dx.doi.org/10.1016/j.bbi.2015.10.014] [PMID: 26598104 ]
[13]
Licastro, F.; Porcellini, E. Persistent infections, immune-senescence and Alzheimer’s disease. Oncoscience, 2016, 3(5-6), 135-142.
[PMID: 27489858 ]
[14]
McManus, R.M.; Heneka, M.T. Role of neuroinflammation in neurodegeneration: new insights. Alzheimers Res. Ther., 2017, 9(1), 14.
[http://dx.doi.org/10.1186/s13195-017-0241-2] [PMID: 28259169 ]
[15]
Sankowski, R.; Mader, S.; Valdés-Ferrer, S.I. Systemic inflammation and the brain: novel roles of genetic, molecular, and environmental cues as drivers of neurodegeneration. Front. Cell. Neurosci., 2015, 9, 28.
[http://dx.doi.org/10.3389/fncel.2015.00028] [PMID: 25698933 ]
[16]
Biesmans, S.; Meert, T.F.; Bouwknecht, J.A.; Acton, P.D.; Davoodi, N.; De Haes, P.; Kuijlaars, J.; Langlois, X.; Matthews, L.J.; Ver Donck, L.; Hellings, N.; Nuydens, R. Systemic immune activation leads to neuroinflammation and sickness behavior in mice. Mediators Inflamm., 2013, 2013271359
[http://dx.doi.org/10.1155/2013/271359] [PMID: 23935246 ]
[17]
Hoogland, I.C.M.; Houbolt, C.; van Westerloo, D.J.; van Gool, W.A.; van de Beek, D. Systemic inflammation and microglial activation: systematic review of animal experiments. J. Neuroinflammation, 2015, 12, 114.
[http://dx.doi.org/10.1186/s12974-015-0332-6] [PMID: 26048578 ]
[18]
Schreuder, L.; Eggen, B.J.; Biber, K.; Schoemaker, R.G.; Laman, J.D.; de Rooij, S.E. Pathophysiological and behavioral effects of systemic inflammation in aged and diseased rodents with relevance to delirium: A systematic review. Brain Behav. Immun., 2017, 62, 362-381.
[http://dx.doi.org/10.1016/j.bbi.2017.01.010] [PMID: 28088641 ]
[19]
d’Avila, J.C.; Siqueira, L.D.; Mazeraud, A.; Azevedo, E.P.; Foguel, D.; Castro-Faria-Neto, H.C.; Sharshar, T.; Chrétien, F.; Bozza, F.A. Age-related cognitive impairment is associated with long-term neuroinflammation and oxidative stress in a mouse model of episodic systemic inflammation. J. Neuroinflammation, 2018, 15(1), 28.
[http://dx.doi.org/10.1186/s12974-018-1059-y] [PMID: 29382344 ]
[20]
Zhang, L.; Previn, R.; Lu, L.; Liao, R.F.; Jin, Y.; Wang, R.K. Crocin, a natural product attenuates lipopolysaccharide-induced anxiety and depressive-like behaviors through suppressing NF-kB and NLRP3 signaling pathway. Brain Res. Bull., 2018, 142, 352-359.
[http://dx.doi.org/10.1016/j.brainresbull.2018.08.021] [PMID: 30179677 ]
[21]
Sumbria, R.K.; Grigoryan, M.M.; Vasilevko, V.; Krasieva, T.B.; Scadeng, M.; Dvornikova, A.K.; Paganini-Hill, A.; Kim, R.; Cribbs, D.H.; Fisher, M.J. A murine model of inflammation-induced cerebral microbleeds. J. Neuroinflammation, 2016, 13(1), 218.
[http://dx.doi.org/10.1186/s12974-016-0693-5] [PMID: 27577728 ]
[22]
Catorce, M.N.; Gevorkian, G. LPS-induced murine neuroinflammation model: main features and suitability for pre-clinical assessment of nutraceuticals. Curr. Neuropharmacol., 2016, 14(2), 155-164.
[http://dx.doi.org/10.2174/1570159X14666151204122017] [PMID: 26639457 ]
[23]
Fu, H.Q.; Yang, T.; Xiao, W.; Fan, L.; Wu, Y.; Terrando, N.; Wang, T.L. Prolonged neuroinflammation after lipopolysaccharide exposure in aged rats. PLoS One, 2014, 9(8) e106331
[http://dx.doi.org/10.1371/journal.pone.0106331] [PMID: 25170959 ]
[24]
Anderson, S.T.; Commins, S.; Moynagh, P.N.; Coogan, A.N. Lipopolysaccharide-induced sepsis induces long-lasting affective changes in the mouse. Brain Behav. Immun., 2015, 43, 98-109.
[http://dx.doi.org/10.1016/j.bbi.2014.07.007] [PMID: 25063709 ]
[25]
Skelly, D.T.; Hennessy, E.; Dansereau, M.A.; Cunningham, C. A systematic analysis of the peripheral and CNS effects of systemic LPS, IL-1β, [corrected] TNF-α and IL-6 challenges in C57BL/6 mice. PLoS One, 2013, 8(7)e69123
[http://dx.doi.org/10.1371/journal.pone.0069123] [PMID: 23840908 ]
[26]
Banks, W.A. gray, A.M.; Erickson, M.A.; Salameh, T.S.; Damodarasamy, M.; Sheibani, N.; Meabon, J.S.; Wing, E.E.; Morofuji, Y.; Cook, D.G.; Reed, M.J. Lipopolysaccharide-induced blood-brain barrier disruption: roles of cyclooxugenase, oxidative stress, neuroinflammation, and elements of the neurovascular unit. J. Neuroinflammation, 2015, 12, 223.
[http://dx.doi.org/10.1186/s12974-015-0434-1] [PMID: 26608623 ]
[27]
Lee, E.J.; Ko, H.M.; Jeong, Y.H.; Park, E.M.; Kim, H.S. β-Lapachone suppresses neuroinflammation by modulating the expression of cytokines and matrix metalloproteinases in activated microglia. J. Neuroinflammation, 2015, 12, 133.
[http://dx.doi.org/10.1186/s12974-015-0355-z] [PMID: 26173397 ]
[28]
Nava Catorce, M.; Acero, G.; Pedraza-Chaverri, J.; Fragoso, G.; Govezensky, T.; Gevorkian, G. Alpha-mangostin attenuates brain inflammation induced by peripheral lipopolysaccharide administration in C57BL/6J mice. J. Neuroimmunol., 2016, 297, 20-27.
[http://dx.doi.org/10.1016/j.jneuroim.2016.05.008] [PMID: 27397072 ]
[29]
Szot, P.; Franklin, A.; Figlewicz, D.P.; Beuca, T.P.; Bullock, K.; Hansen, K. banks, W.A.; Raskind, M.A.; Peskind, E.R. Multiple lipopolysaccharide (LPS) injections alter interleukin (IL-6), IL-7,IL-10 and IL-7 and IL-7 receptor mRNA in CNS and spleen. Neuroscience, 2017, 355, 9-21.
[http://dx.doi.org/10.1016/j.neuroscience.2017.04.028] [PMID: 28456715 ]
[30]
He, H.; Geng, T.; Chen, P.; Wang, M.; Hu, J.; Kang, L.; Song, W.; Tang, H. NK cells promote neutrophil recruitment in the brain during sepsis-induced neuroinflammation. Sci. Rep., 2016, 6, 27711.
[http://dx.doi.org/10.1038/srep27711] [PMID: 27270556 ]
[31]
Badshah, H.; Ali, T. Shafiq-ur Rehman; Faiz-ul Amin; Ullah, F.; Kim, T.H.; Kim, M.O. Protective effect of lupeol against lipopolysaccharide-induced neuroinflammation via the p38/c-Jun N-terminal kinase pathway in the adult mouse brain. J. Neuroimmune Pharmacol., 2016, 11(1), 48-60.
[http://dx.doi.org/10.1007/s11481-015-9623-z] [PMID: 26139594 ]
[32]
Li, J.; Xu, B.; Chen, Z.; Zhou, C.; Liao, L.; Qin, Y.; Yang, C.; Zhang, X.; Hu, Z.; Sun, L.; Zhu, D.; Xie, P. PI3K/AKT/JNK/p38 signalling pathway-mediated neural apoptosis in the prefrontal cortex of mice is involved in the antidepressant-like effect of pioglitazone. Clin. Exp. Pharmacol. Physiol., 2018, 45(6), 525-535.
[http://dx.doi.org/10.1111/1440-1681.12918] [PMID: 29359338 ]
[33]
Zhu, W.; Cao, F.S.; Feng, J.; Chen, H.W.; Wan, J.R.; Lu, Q.; Wang, J. NLRP3 inflammasome activation contributes to long-term behavioral alterations in mice injected with lipopolysaccharide. Neuroscience, 2017, 343, 77-84.
[http://dx.doi.org/10.1016/j.neuroscience.2016.11.037] [PMID: 27923741 ]
[34]
Norden, D.M.; Trojanowski, P.J.; Villanueva, E.; Navarro, E.; Godbout, J.P. Sequential activation of microglia and astrocyte cytokine expression precedes increased Iba-1 or GFAP immunoreactivity following systemic immune challenge. Glia, 2016, 64(2), 300-316.
[http://dx.doi.org/10.1002/glia.22930] [PMID: 26470014 ]
[35]
Lopes, P.C. LPS and neuroinflammation: a matter of timing. Inflammopharmacology, 2016, 24(5), 291-293.
[http://dx.doi.org/10.1007/s10787-016-0283-2] [PMID: 27645902 ]
[36]
Panche, A.N.; Diwan, A.D.; Chandra, S.R. Flavonoids: an overview. J. Nutr. Sci., 2016, 5e47
[http://dx.doi.org/10.1017/jns.2016.41] [PMID: 28620474 ]
[37]
Lim, H.; Heo, M.Y.; Kim, H.P. Flavonoids: broad spectrum agents on chronic inflammation. Biomol. Ther. (Seoul), 2019, 27(3), 241-253.
[http://dx.doi.org/10.4062/biomolther.2019.034] [PMID: 31006180 ]
[38]
Spencer, J.P.; Vafeiadou, K.; Williams, R.J.; Vauzour, D. Neuroinflammation: modulation by flavonoids and mechanisms of action. Mol. Aspects Med., 2012, 33(1), 83-97.
[http://dx.doi.org/10.1016/j.mam.2011.10.016] [PMID: 22107709 ]
[39]
Renaud, J.; Martinoli, M.G. Resveratrol as a protective molecule for neuroinflammation: a review of mechanisms. Curr. Pharm. Biotechnol., 2014, 15(4), 318-329.
[http://dx.doi.org/10.2174/1389201015666140617101332] [PMID: 24938890 ]
[40]
Jaeger, B.N.; Parylak, S.L.; Gage, F.H. Mechanisms of dietary flavonoid action in neuronal function and neuroinflammation. Mol. Aspects Med., 2018, 61, 50-62.
[http://dx.doi.org/10.1016/j.mam.2017.11.003] [PMID: 29117513 ]
[41]
Morais, C.A.; de Rosso, V.V.; Estadella, D.; Pisani, L.P. Anthocyanins as inflammatory modulators and the role of the gut microbiota. J. Nutr. Biochem., 2016, 33, 1-7.
[http://dx.doi.org/10.1016/j.jnutbio.2015.11.008] [PMID: 27260462 ]
[42]
Wallace, T.C.; Slavin, M.; Frankenfeld, C.L. Systemic review of anthocyanins and markers of cardiovascular disease. Nutrients, 2016, 8(1)E32
[http://dx.doi.org/10.3390/nu8010032] [PMID: 26761031 ]
[43]
Lee, Y.M.; Yoon, Y.; Yoon, H.; Park, H.M.; Song, S.; Yeum, K.J. Dietary anthocyanins against obesity and inflammation. Nutrients, 2017, 9(10) E1089
[http://dx.doi.org/10.3390/nu9101089] [PMID: 28974032 ]
[44]
Różańska, D.; Regulska-Ilow, B. The significance of anthocyanins in the prevention and treatment of type 2 diabetes. Adv. Clin. Exp. Med., 2018, 27(1), 135-142.
[http://dx.doi.org/10.17219/acem/64983] [PMID: 29521054 ]
[45]
Khan, M.S.; Ali, T.; Kim, M.W.; Jo, M.H.; Jo, M.G.; Badshah, H.; Kim, M.O. Anthocyanins protect against LPS-induced oxidative stress-mediated neuroinflammation and neurodegeneration in the adult mouse cortex. Neurochem. Int., 2016, 100, 1-10.
[http://dx.doi.org/10.1016/j.neuint.2016.08.005] [PMID: 27522965 ]
[46]
Khan, M.S.; Ali, T.; Kim, M.W.; Jo, M.H.; Chung, J.I.; Kim, M.O. Anthocyanins improve hippocampus-dependent memory function and prevent neurodegeneration via JNK/Akt/GSK3β signaling in LPS-treated adult mice. Mol. Neurobiol., 2019, 56(1), 671-687.
[http://dx.doi.org/10.1007/s12035-018-1101-1] [PMID: 29779175 ]
[47]
Carvalho, F.B.; Gutierres, J.M.; Bueno, A.; Agostinho, P.; Zago, A.M.; Vieira, J.; Frühauf, P.; Cechella, J.L.; Nogueira, C.W.; Oliveira, S.M.; Rizzi, C.; Spanevello, R.M.; Duarte, M.M.F.; Duarte, T.; Dellagostin, O.A.; Andrade, C.M. Anthocyanins control neuroinflammation and consequent memory dysfunction in mice exposed to lipopolysaccharide. Mol. Neurobiol., 2017, 54(5), 3350-3367.
[http://dx.doi.org/10.1007/s12035-016-9900-8] [PMID: 27167130 ]
[48]
Hämäläinen, M.; Nieminen, R.; Vuorela, P.; Heinonen, M.; Moilanen, E. Anti-inflammatory effects of flavonoids: genistein, kaempferol, quercetin, and daidzein inhibit STAT-1 and NF-kappaB activations, whereas flavone, isorhamnetin, naringenin, and pelargonidin inhibit only NF-kappaB activation along with their inhibitory effect on iNOS expression and NO production in activated macrophages. Mediators Inflamm., 2007, 2007, 45673.
[http://dx.doi.org/10.1155/2007/45673] [PMID: 18274639 ]
[49]
Vafeiadou, K.; Vauzour, D.; Lee, H.Y.; Rodriguez-Mateos, A.; Williams, R.J.; Spencer, J.P. The citrus flavanone naringenin inhibits inflammatory signalling in glial cells and protects against neuroinflammatory injury. Arch. Biochem. Biophys., 2009, 484(1), 100-109.
[http://dx.doi.org/10.1016/j.abb.2009.01.016] [PMID: 19467635 ]
[50]
Wu, L.H.; Lin, C.; Lin, H.Y.; Liu, Y.S.; Wu, C.Y.; Tsai, C.F.; Chang, P.C.; Yeh, W.L.; Lu, D.Y. Naringenin Suppresses Neuroinflammatory Responses Through Inducing Suppressor of Cytokine Signaling 3 Expression. Mol. Neurobiol., 2016, 53(2), 1080-1091.
[http://dx.doi.org/10.1007/s12035-014-9042-9] [PMID: 25579382 ]
[51]
Liu, X.; Wang, N.; Fan, S.; Zheng, X.; Yang, Y.; Zhu, Y.; Lu, Y.; Chen, Q.; Zhou, H.; Zheng, J. The citrus flavonoid naringenin confers protection in a murine endotoxaemia model through AMPK-ATF3-dependent negative regulation of the TLR4 signalling pathway. Sci. Rep., 2016, 6, 39735.
[http://dx.doi.org/10.1038/srep39735] [PMID: 28004841 ]
[52]
Liu, X.X.; Yu, D.D.; Chen, M.J.; Sun, T.; Li, G.; Huang, W.J.; Nie, H.; Wang, C.; Zhang, Y.X.; Gong, Q.; Ren, B.X. Hesperidin ameliorates lipopolysaccharide-induced acute lung injury in mice by inhibiting HMGB1 release. Int. Immunopharmacol., 2015, 25(2), 370-376.
[http://dx.doi.org/10.1016/j.intimp.2015.02.022] [PMID: 25724384 ]
[53]
Ren, H.; Hao, J.; Liu, T.; Zhang, D.; Lv, H.; Song, E.; Zhu, C. Hesperetin Suppresses Inflammatory Responses in Lipopolysaccharide-Induced RAW 264.7 Cells via the Inhibition of NF-κB and Activation of Nrf2/HO-1 Pathways. Inflammation, 2016, 39(3), 964-973.
[http://dx.doi.org/10.1007/s10753-016-0311-9] [PMID: 26994999 ]
[54]
Tejada, S.; Pinya, S.; Martorell, M.; Capó, X.; Tur, J.A.; Pons, A.; Sureda, A. Potential anti-inflammatory effects of hesperidin from the Genus Citrus. Curr. Med. Chem., 2018, 25(37), 4929-4945.
[http://dx.doi.org/10.2174/0929867324666170718104412] [PMID: 28721824 ]
[55]
Qi, W.; Lin, C.; Fan, K.; Chen, Z.; Liu, L.; Feng, X.; Zhang, H.; Shao, Y.; Fang, H.; Zhao, C.; Zhang, R.; Cai, D. Hesperidin inhibits synovial cell inflammation and macrophage polarization through suppression of the PI3K/AKT pathway in complete Freund’s adjuvant-induced arthritis in mice. Chem. Biol. Interact., 2019, 306, 19-28.
[http://dx.doi.org/10.1016/j.cbi.2019.04.002] [PMID: 30954464 ]
[56]
Ye, J.; Guan, M.; Lu, Y.; Zhang, D.; Li, C.; Li, Y.; Zhou, C. Protective effects of hesperetin on lipopolysaccharide-induced acute lung injury by targeting MD2. Eur. J. Pharmacol., 2019, 852, 151-158.
[http://dx.doi.org/10.1016/j.ejphar.2019.02.042] [PMID: 30807747 ]
[57]
Konsman, J.P.; Veeneman, J.; Combe, C.; Poole, S.; Luheshi, G.N.; Dantzer, R. Central nervous action of interleukin-1 mediates activation of limbic structures and behavioural depression in response to peripheral administration of bacterial lipopolysaccharide. Eur. J. Neurosci., 2008, 28(12), 2499-2510.
[http://dx.doi.org/10.1111/j.1460-9568.2008.06549.x] [PMID: 19087175 ]
[58]
Li, M.; Shao, H.; Zhang, X.; Qin, B. Hesperidin Alleviates Lipopolysaccharide-Induced Neuroinflammation in Mice by Promoting the miRNA-132 Pathway. Inflammation, 2016, 39(5), 1681-1689.
[http://dx.doi.org/10.1007/s10753-016-0402-7] [PMID: 27378528 ]
[59]
He, P.; Yan, S.; Zheng, J.; Gao, Y.; Zhang, S.; Liu, Z.; Liu, X.; Xiao, C. Eriodictyol Attenuates LPS-Induced Neuroinflammation, Amyloidogenesis, and Cognitive Impairments via the Inhibition of NF-κB in Male C57BL/6J Mice and BV2 Microglial Cells. J. Agric. Food Chem., 2018, 66(39), 10205-10214.
[http://dx.doi.org/10.1021/acs.jafc.8b03731] [PMID: 30208700 ]
[60]
He, P.; Yan, S.; Wen, X.; Zhang, S.; Liu, Z.; Liu, X.; Xiao, C. Eriodictyol alleviates lipopolysaccharide-triggered oxidative stress and synaptic dysfunctions in BV-2 microglial cells and mouse brain. J. Cell. Biochem., 2019, 120(9), 14756-14770.
[http://dx.doi.org/10.1002/jcb.28736] [PMID: 31016762 ]
[61]
Zhang, J.; Chen, Y.; Luo, H.; Sun, L.; Xu, M.; Yu, J.; Zhou, Q.; Meng, G.; Yang, S. Recent update on the pharmacological effects and mechanisms of dihydromyricetin. Front. Pharmacol., 2018, 9, 1204.
[http://dx.doi.org/10.3389/fphar.2018.01204] [PMID: 30410442 ]
[62]
Ren, Z.; Yan, P.; Zhu, L.; Yang, H.; Zhao, Y.; Kirby, B.P.; Waddington, J.L.; Zhen, X. Dihydromyricetin exerts a rapid antidepressant-like effect in association with enhancement of BDNF expression and inhibition of neuroinflammation. Psychopharmacology (Berl.), 2018, 235(1), 233-244.
[http://dx.doi.org/10.1007/s00213-017-4761-z] [PMID: 29058041 ]
[63]
Devi, K.P.; Malar, D.S.; Nabavi, S.F.; Sureda, A.; Xiao, J.; Nabavi, S.M.; Daglia, M. Kaempferol and inflammation: From chemistry to medicine. Pharmacol. Res., 2015, 99, 1-10.
[http://dx.doi.org/10.1016/j.phrs.2015.05.002] [PMID: 25982933 ]
[64]
Cheng, X.; Yang, Y.L.; Yang, H.; Wang, Y.H.; Du, G.H. Kaempferol alleviates LPS-induced neuroinflammation and BBB dysfunction in mice via inhibiting HMGB1 release and down-regulating TLR4/MyD88 pathway. Int. Immunopharmacol., 2018, 56, 29-35.
[http://dx.doi.org/10.1016/j.intimp.2018.01.002] [PMID: 29328946 ]
[65]
Yang, Y.L.; Cheng, X.; Li, W.H.; Liu, M.; Wang, Y.H.; Du, G.H. Kaempferol attenuates LPS-induced striatum injury in mice involving anti-neuroinflammation, maintaining BBB integrity, and down-regulating the HMGB1/TLR4 pathway. Int. J. Mol. Sci., 2019, 20(3) E491
[http://dx.doi.org/10.3390/ijms20030491] [PMID: 31016762 ]
[66]
Li, Y.; Yao, J.; Han, C.; Yang, J.; Chaudhry, M.T.; Wang, S.; Liu, H.; Yin, Y. Quercetin, inflammation and immunity. Nutrients, 2016, 8(3), 167.
[http://dx.doi.org/10.3390/nu8030167] [PMID: 26999194 ]
[67]
Khan, A.; Ali, T.; Rehman, S.U.; Khan, M.S.; Alam, S.I.; Ikram, M.; Muhammad, T.; Saeed, K.; Badshah, H.; Kim, M.O. Neuroprotective effect of quercetin against the detrimental effects of LPS in the adult mouse brain. Front. Pharmacol., 2018, 9, 1383.
[http://dx.doi.org/10.3389/fphar.2018.01383] [PMID: 30618732 ]
[68]
Guo, J.; Li, F.; Wu, Q.; Gong, Q.; Lu, Y.; Shi, J. Protective effects of icariin on brain dysfunction induced by lipopolysaccharide in rats. Phytomedicine, 2010, 17(12), 950-955.
[http://dx.doi.org/10.1016/j.phymed.2010.03.007] [PMID: 20382007 ]
[69]
Zeng, K.W.; Fu, H.; Liu, G.X.; Wang, X.M. Icariin attenuates lipopolysaccharide-induced microglial activation and resultant death of neurons by inhibiting TAK1/IKK/NF-kappaB and JNK/p38 MAPK pathways. Int. Immunopharmacol., 2010, 10(6), 668-678.
[http://dx.doi.org/10.1016/j.intimp.2010.03.010] [PMID: 20347053 ]
[70]
Zheng, Y.; Zhu, G.; He, J.; Wang, G.; Li, D.; Zhang, F. Icariin targets Nrf2 signaling to inhibit microglia-mediated neuroinflammation. Int. Immunopharmacol., 2019, 73, 304-311.
[http://dx.doi.org/10.1016/j.intimp.2019.05.033] [PMID: 31128530 ]
[71]
Liu, L.; Zhao, Z.; Lu, L.; Liu, J.; Sun, J.; Wu, X.; Dong, J. Icariin and icaritin ameliorated hippocampus neuroinflammation via inhibiting HMGB1-related pro-inflammatory signals in lipopolysaccharide-induced inflammation model in C57BL/6 J mice. Int. Immunopharmacol., 2019, 68, 95-105.
[http://dx.doi.org/10.1016/j.intimp.2018.12.055] [PMID: 30616172 ]
[72]
Jiang, X.; Liu, J.; Lin, Q.; Mao, K.; Tian, F.; Jing, C.; Wang, C.; Ding, L.; Pang, C. Proanthocyanidin prevents lipopolysaccharide-induced depressive-like behavior in mice via neuroinflammatory pathway. Brain Res. Bull., 2017, 135, 40-46.
[http://dx.doi.org/10.1016/j.brainresbull.2017.09.010] [PMID: 28941603 ]
[73]
Pan, C.H.; Kim, E.S.; Jung, S.H.; Nho, C.W.; Lee, J.K. Tectorigenin inhibits IFN-gamma/LPS-induced inflammatory responses in murine macrophage RAW 264.7 cells. Arch. Pharm. Res., 2008, 31(11), 1447-1456.
[http://dx.doi.org/10.1007/s12272-001-2129-7] [PMID: 19023541 ]
[74]
Kim, Y.P.; Yamada, M.; Lim, S.S.; Lee, S.H.; Ryu, N.; Shin, K.H.; Ohuchi, K. Inhibition by tectorigenin and tectoridin of prostaglandin E2 production and cyclooxygenase-2 induction in rat peritoneal macrophages. Biochim. Biophys. Acta, 1999, 1438(3), 399-407.
[http://dx.doi.org/10.1016/S1388-1981(99)00067-0] [PMID: 10366782 ]
[75]
Ma, C.H.; Liu, J.P.; Qu, R.; Ma, S.P. Tectorigenin inhibits the inflammation of LPS-induced acute lung injury in mice. Chin. J. Nat. Med., 2014, 12(11), 841-846.
[http://dx.doi.org/10.1016/S1875-5364(14)60126-6] [PMID: 25480515 ]
[76]
Lim, H.S.; Kim, Y.J.; Kim, B.Y.; Park, G.; Jeong, S.J. The Anti-neuroinflammatory Activity of Tectorigenin Pretreatment via Downregulated NF-κB and ERK/JNK Pathways in BV-2 Microglial and Microglia Inactivation in Mice With Lipopolysaccharide. Front. Pharmacol., 2018, 9, 462.
[http://dx.doi.org/10.3389/fphar.2018.00462] [PMID: 29867470 ]
[77]
Lai, X.; Ye, Y.; Sun, C.; Huang, X.; Tang, X.; Zeng, X.; Yin, P.; Zeng, Y. Icaritin exhibits anti-inflammatory effects in the mouse peritoneal macrophages and peritonitis model. Int. Immunopharmacol., 2013, 16(1), 41-49.
[http://dx.doi.org/10.1016/j.intimp.2013.03.025] [PMID: 23566810 ]
[78]
Jeong, Y.H.; Park, J.S.; Kim, D.H.; Kim, H.S. Lonchocarpine Increases Nrf2/ARE-Mediated Antioxidant Enzyme Expression by Modulating AMPK and MAPK Signaling in Brain Astrocytes. Biomol. Ther. (Seoul), 2016, 24(6), 581-588.
[http://dx.doi.org/10.4062/biomolther.2016.141] [PMID: 27737527 ]
[79]
Jeong, Y.H.; Park, J.S.; Kim, D.H.; Kang, J.L.; Kim, H.S. Anti-inflammatory mechanism of lonchocarpine in LPS- or poly(I:C)-induced neuroinflammation. Pharmacol. Res., 2017, 119, 431-442.
[http://dx.doi.org/10.1016/j.phrs.2017.02.027] [PMID: 28288940 ]
[80]
Galiniak, S.; Aebisher, D.; Bartusik-Aebisher, D. Health benefits of resveratrol administration. Acta Biochim. Pol., 2019, 66(1), 13-21.
[PMID: 30816367 ]
[81]
Yang, X.; Xu, S.; Qian, Y.; Xiao, Q. Resveratrol regulates microglia M1/M2 polarization via PGC-1α in conditions of neuroinflammatory injury. Brain Behav. Immun., 2017, 64, 162-172.
[http://dx.doi.org/10.1016/j.bbi.2017.03.003] [PMID: 28268115 ]
[82]
Sulakhiya, K.; Kumar, P.; Jangra, A.; Dwivedi, S.; Hazarika, N.K.; Baruah, C.C.; Lahkar, M. Honokiol abrogates lipopolysaccharide-induced depressive like behavior by impeding neuroinflammation and oxido-nitrosative stress in mice. Eur. J. Pharmacol., 2014, 744, 124-131.
[http://dx.doi.org/10.1016/j.ejphar.2014.09.049] [PMID: 25446914 ]
[83]
Li, J.; Geng, D.; Xu, J.; Weng, L.J.; Liu, Q.; Yi, L.T. Antidepressant-like effect of macranthol isolated from Illicium dunnianum tutch in mice. Eur. J. Pharmacol., 2013, 707(1-3), 112-119.
[http://dx.doi.org/10.1016/j.ejphar.2013.03.010] [PMID: 23524090 ]
[84]
Weng, L.; Dong, S.; Wang, S.; Yi, L.; Geng, D. Macranthol attenuates lipopolysaccharide-induced depressive-like behaviors by inhibiting neuroinflammation in prefrontal cortex. Physiol. Behav., 2019, 204, 33-40.
[http://dx.doi.org/10.1016/j.physbeh.2019.02.010] [PMID: 30753846 ]
[85]
Song, F.; Zeng, K.; Liao, L.; Yu, Q.; Tu, P.; Wang, X.; Schizandrin, A.; Schizandrin, A. Inhibits Microglia-Mediated Neuroninflammation through Inhibiting TRAF6-NF-κB and Jak2-Stat3 Signaling Pathways. PLoS One, 2016, 11(2) e0149991
[http://dx.doi.org/10.1371/journal.pone.0149991] [PMID: 26919063 ]
[86]
Basu Mallik, S.; Mudgal, J.; Nampoothiri, M.; Hall, S.; Dukie, S.A.; Grant, G.; Rao, C.M.; Arora, D. Caffeic acid attenuates lipopolysaccharide-induced sickness behaviour and neuroinflammation in mice. Neurosci. Lett., 2016, 632, 218-223.
[http://dx.doi.org/10.1016/j.neulet.2016.08.044] [PMID: 27597761 ]
[87]
Lee, J.; Scagel, C.F. Chicoric acid: chemistry, distribution, and production. Front Chem., 2013, 1, 40.
[http://dx.doi.org/10.3389/fchem.2013.00040] [PMID: 24790967 ]
[88]
Ding, H.; Ci, X.; Cheng, H.; Yu, Q.; Li, D. Chicoric acid alleviates lipopolysaccharide-induced acute lung injury in mice through anti-inflammatory and anti-oxidant activities. Int. Immunopharmacol., 2019, 66, 169-176.
[http://dx.doi.org/10.1016/j.intimp.2018.10.042] [PMID: 30466029 ]
[89]
Liu, Q.; Hu, Y.; Cao, Y.; Song, G.; Liu, Z.; Liu, X. Chicoric Acid Ameliorates Lipopolysaccharide-Induced Oxidative Stress via Promoting the Keap1/Nrf2 Transcriptional Signaling Pathway in BV-2 Microglial Cells and Mouse Brain. J. Agric. Food Chem., 2017, 65(2), 338-347.
[http://dx.doi.org/10.1021/acs.jafc.6b04873] [PMID: 28002939 ]
[90]
Liu, Q.; Chen, Y.; Shen, C.; Xiao, Y.; Wang, Y.; Liu, Z.; Liu, X. Chicoric acid supplementation prevents systemic inflammation-induced memory impairment and amyloidogenesis via inhibition of NF-κB. FASEB J., 2017, 31(4), 1494-1507.
[http://dx.doi.org/10.1096/fj.201601071R] [PMID: 28003341 ]
[91]
Yaidikar, L.; Thakur, S. Punicalagin attenuated cerebral ischemia-reperfusion insult via inhibition of proinflammatory cytokines, up-regulation of Bcl-2, down-regulation of Bax, and caspase-3. Mol. Cell. Biochem., 2015, 402(1-2), 141-148.
[http://dx.doi.org/10.1007/s11010-014-2321-y] [PMID: 25555468 ]
[92]
Kim, Y.E.; Hwang, C.J.; Lee, H.P.; Kim, C.S.; Son, D.J.; Ham, Y.W.; Hellström, M.; Han, S.B.; Kim, H.S.; Park, E.K.; Hong, J.T. Inhibitory effect of punicalagin on lipopolysaccharide-induced neuroinflammation, oxidative stress and memory impairment via inhibition of nuclear factor-kappaB. Neuropharmacology, 2017, 117, 21-32.
[http://dx.doi.org/10.1016/j.neuropharm.2017.01.025] [PMID: 28132781 ]
[93]
Sharkey, T.D.; Yeh, S. Isoprene emission from plants. Annu. Rev. Plant Physiol. Plant Mol. Biol., 2001, 52, 407-436.
[http://dx.doi.org/10.1146/annurev.arplant.52.1.407] [PMID: 11337404 ]
[94]
Fernández, M.A.; de las Heras, B.; García, M.D.; Sáenz, M.T.; Villar, A. New insights into the mechanism of action of the anti-inflammatory triterpene lupeol. J. Pharm. Pharmacol., 2001, 53(11), 1533-1539.
[http://dx.doi.org/10.1211/0022357011777909] [PMID: 11732756 ]
[95]
Saleem, M. Lupeol, a novel anti-inflammatory and anti-cancer dietary triterpene. Cancer Lett., 2009, 285(2), 109-115.
[http://dx.doi.org/10.1016/j.canlet.2009.04.033] [PMID: 19464787 ]
[96]
Ming, L.J.; Yin, A.C. Therapeutic effects of glycyrrhizic acid. Nat. Prod. Commun., 2013, 8(3), 415-418.
[http://dx.doi.org/10.1177/1934578X1300800335] [PMID: 23678825 ]
[97]
Liu, W.; Huang, S.; Li, Y.; Zhang, K.; Zheng, X. Suppressive effect of glycyrrhizic acid against lipopolysaccharide-induced neuroinflammation and cognitive impairment in C57 mice via toll-like receptor 4 signaling pathway. Food Nutr. Res., 2019, 63, 63.
[http://dx.doi.org/10.29219/fnr.v63.1516] [PMID: 31073286 ]
[98]
Park, S.M.; Choi, M.S.; Sohn, N.W.; Shin, J.W. Ginsenoside Rg3 attenuates microglia activation following systemic lipopolysaccharide treatment in mice. Biol. Pharm. Bull., 2012, 35(9), 1546-1552.
[http://dx.doi.org/10.1248/bpb.b12-00393] [PMID: 22975507 ]
[99]
Kang, A.; Xie, T.; Zhu, D.; Shan, J.; Di, L.; Zheng, X. Suppressive Effect of Ginsenoside Rg3 against Lipopolysaccharide-Induced Depression-Like Behavior and Neuroinflammation in Mice. J. Agric. Food Chem., 2017, 65(32), 6861-6869.
[http://dx.doi.org/10.1021/acs.jafc.7b02386] [PMID: 28762741 ]
[100]
Vuddanda, P.R.; Sing, S.; Velaga, S. Boswellic acid – medicinal use of an ancient herbal remedy. J. Herb. Med., 2016, 6, 163-170.
[http://dx.doi.org/10.1016/j.hermed.2016.08.002]
[101]
Goel, A.; Ahmad, F.J.; Singh, R.M.; Singh, G.N. 3-Acetyl-11-keto-beta-boswellic acid loaded-polymeric nanomicelles for topical anti-inflammatory and anti-arthritic activity. J. Pharm. Pharmacol., 2010, 62(2), 273-278.
[http://dx.doi.org/10.1211/jpp.62.02.0016] [PMID: 20487208 ]
[102]
Sayed, A.S.; Gomaa, I.E.O.; Bader, M.; El Sayed, N.S.E.D. Role of 3-Acetyl-11-Keto-Beta-Boswellic Acid in Counteracting LPS-Induced Neuroinflammation via Modulation of miRNA-155. Mol. Neurobiol., 2018, 55(7), 5798-5808.
[http://dx.doi.org/10.1007/s12035-017-0801-2] [PMID: 29079998 ]
[103]
Li, J.; Wang, R.F.; Zhou, Y.; Hu, H.J.; Yang, Y.B.; Yang, L.; Wang, Z.T. Dammarane-type triterpene oligoglycosides from the leaves and stems of Panax notoginseng and their antiinflammatory activities. J. Ginseng Res., 2019, 43(3), 377-384.
[http://dx.doi.org/10.1016/j.jgr.2017.11.008] [PMID: 31308809 ]
[104]
Wang, X.; Yang, L.; Yang, L.; Xing, F.; Yang, H.; Qin, L.; Lan, Y.; Wu, H.; Zhang, B.; Shi, H.; Lu, C.; Huang, F.; Wu, X.; Wang, Z.; Gypenoside, I.X. Suppresses p38 MAPK/Akt/NFκB Signaling Pathway Activation and Inflammatory Responses in Astrocytes Stimulated by Proinflammatory Mediators. Inflammation, 2017, 40(6), 2137-2150.
[http://dx.doi.org/10.1007/s10753-017-0654-x] [PMID: 28822019 ]
[105]
Ríos, J.L.; Máñez, S. New pharmacological opportunities for betulinic acid. Planta Med., 2018, 84(1), 8-19.
[http://dx.doi.org/10.1055/s-0043-123472] [PMID: 29202513 ]
[106]
Chung, P.Y. Novel targets of pentacyclic triterpenoids in Staphylococcus aureus: A systematic review. Phytomedicine, 2019, 152933
[http://dx.doi.org/10.1016/j.phymed.2019.152933] [PMID: 31103429 ]
[107]
Li, C.; Zhang, C.; Zhou, H.; Feng, Y.; Tang, F.; Hoi, M.P.M.; He, C.; Ma, D.; Zhao, C.; Lee, S.M.Y. Inhibitory Effects of Betulinic Acid on LPS-Induced Neuroinflammation Involve M2 Microglial Polarization via CaMKKβ-Dependent AMPK Activation. Front. Mol. Neurosci., 2018, 11, 98.
[http://dx.doi.org/10.3389/fnmol.2018.00098] [PMID: 29666569 ]
[108]
Murakami, A.; Furukawa, I.; Miyamoto, S.; Tanaka, T.; Ohigashi, H. Curcumin combined with turmerones, essential oil components of turmeric, abolishes inflammation-associated mouse colon carcinogenesis. Biofactors, 2013, 39(2), 221-232.
[http://dx.doi.org/10.1002/biof.1054] [PMID: 23233214 ]
[109]
Chen, M.; Chang, Y.Y.; Huang, S.; Xiao, L.H.; Zhou, W.; Zhang, L.Y.; Li, C.; Zhou, R.P.; Tang, J.; Lin, L.; Du, Z.Y.; Zhang, K. Aromatic-Turmerone Attenuates LPS-Induced Neuroinflammation and Consequent Memory Impairment by Targeting TLR4-Dependent Signaling Pathway. Mol. Nutr. Food Res., 2018, 62(2)
[PMID: 28849618 ]
[110]
Pan, C.; Si, Y.; Meng, Q.; Jing, L.; Chen, L.; Zhang, Y.; Bao, H. Suppression of the RAC1/MLK3/p38 Signaling Pathway by β-Elemene Alleviates Sepsis-Associated Encephalopathy in Mice. Front. Neurosci., 2019, 13, 358.
[http://dx.doi.org/10.3389/fnins.2019.00358] [PMID: 31068775 ]
[111]
Palozza, P.; Parrone, N.; Catalano, A.; Simone, R. Tomato Lycopene and Inflammatory Cascade: Basic Interactions and Clinical Implications. Curr. Med. Chem., 2010, 17(23), 2547-2563.
[http://dx.doi.org/10.2174/092986710791556041] [PMID: 20491642 ]
[112]
Zhang, F.; Fu, Y.; Zhou, X.; Pan, W.; Shi, Y.; Wang, M.; Zhang, X.; Qi, D.; Li, L.; Ma, K.; Tang, R.; Zheng, K.; Song, Y. Depression-like behaviors and heme oxygenase-1 are regulated by Lycopene in lipopolysaccharide-induced neuroinflammation. J. Neuroimmunol., 2016, 298, 1-8.
[http://dx.doi.org/10.1016/j.jneuroim.2016.06.001] [PMID: 27609268 ]
[113]
Wang, J.; Li, L.; Wang, Z.; Cui, Y.; Tan, X.; Yuan, T.; Liu, Q.; Liu, Z.; Liu, X. Supplementation of lycopene attenuates lipopolysaccharide-induced amyloidogenesis and cognitive impairments via mediating neuroinflammation and oxidative stress. J. Nutr. Biochem., 2018, 56, 16-25.
[http://dx.doi.org/10.1016/j.jnutbio.2018.01.009] [PMID: 29454265 ]
[114]
Wang, J.; Zou, Q.; Suo, Y.; Tan, X.; Yuan, T.; Liu, Z.; Liu, X. Lycopene ameliorates systemic inflammation-induced synaptic dysfunction via improving insulin resistance and mitochondrial dysfunction in the liver-brain axis. Food Funct., 2019, 10(4), 2125-2137.
[http://dx.doi.org/10.1039/C8FO02460J] [PMID: 30924473 ]
[115]
Pashirzad, M.; Shafiee, M.; Avan, A.; Ryzhikov, M.; Fiuji, H.; Bahreyni, A.; Khazaei, M.; Soleimanpour, S.; Hassanian, S.M. Therapeutic potency of crocin in the treatment of inflammatory diseases: Current status and perspective. J. Cell. Physiol., 2019, 23
[http://dx.doi.org/10.1002/jcp.28177] [PMID: 30673132 ]
[116]
Dai, Y.; Chen, S.R.; Chai, L.; Zhao, J.; Wang, Y.; Wang, Y. Overview of pharmacological activities of Andrographis paniculata and its major compound andrographolide. Crit. Rev. Food Sci. Nutr.,, 2019, 59((sup1)), s17-s19.
[http://dx.doi.org/10.1080/10408398.2018.1501657] [PMID: 30040451 ]
[117]
Tao, L.; Zhang, L.; Gao, R.; Jiang, F.; Cao, J.; Liu, H. Andrographolide Alleviates Acute Brain Injury in a Rat Model of Traumatic Brain Injury: Possible Involvement of Inflammatory Signaling. Front. Neurosci., 2018, 12, 657.
[http://dx.doi.org/10.3389/fnins.2018.00657] [PMID: 30294256 ]
[118]
Chiou, W.F.; Chen, C.F.; Lin, J.J. Mechanisms of suppression of inducible nitric oxide synthase (iNOS) expression in RAW 264.7 cells by andrographolide. Br. J. Pharmacol., 2000, 129(8), 1553-1560.
[http://dx.doi.org/10.1038/sj.bjp.0703191] [PMID: 10780958 ]
[119]
Chang, C.C.; Duann, Y.F.; Yen, T.L.; Chen, Y.Y.; Jayakumar, T.; Ong, E.T.; Sheu, J.R. Andrographolide, a Novel NF-κB Inhibitor, Inhibits Vascular Smooth Muscle Cell Proliferation and Cerebral Endothelial Cell Inflammation. Acta Cardiol Sin, 2014, 30(4), 308-315.
[PMID: 27122804 ]
[120]
Monterrosas-Brisson, N.; Ocampo, M.L.; Jiménez-Ferrer, E.; Jiménez-Aparicio, A.R.; Zamilpa, A.; Gonzalez-Cortazar, M.; Tortoriello, J.; Herrera-Ruiz, M. Anti-inflammatory activity of different agave plants and the compound cantalasaponin-1. Molecules, 2013, 18(7), 8136-8146.
[http://dx.doi.org/10.3390/molecules18078136] [PMID: 23846754 ]
[121]
Herrera-Ruiz, M.; Jiménez-Ferrer, E.; Tortoriello, J.; Zamilpa, A.; Alegría-Herrera, E.; Jiménez-Aparicio, A.R.; Arenas-Ocampo, M.L.; Martínez-Duncker, I.; Monterrosas-Brisson, N. Anti-neuroinflammatory effect of agaves and cantalasaponin-1 in a model of LPS-induced damage. Nat. Prod. Res., 2019, 1-4
[http://dx.doi.org/10.1080/14786419.2019.1608537] [PMID: 31084220 ]
[122]
Zhang, W.J.; Frei, B. Astragaloside IV inhibits NF- κ B activation and inflammatory gene expression in LPS-treated mice. Mediators Inflamm., 2015, 2015 274314
[http://dx.doi.org/10.1155/2015/274314] [PMID: 25960613 ]
[123]
Song, M.T.; Ruan, J.; Zhang, R.Y.; Deng, J.; Ma, Z.Q.; Ma, S.P. Astragaloside IV ameliorates neuroinflammation-induced depressive-like behaviors in mice via the PPARγ/NF-κB/NLRP3 inflammasome axis. Acta Pharmacol. Sin., 2018, 39(10), 1559-1570.
[http://dx.doi.org/10.1038/aps.2017.208] [PMID: 29795356 ]
[124]
Chen, L.; Xiong, Y.Q.; Xu, J.; Wang, J.P.; Meng, Z.L.; Hong, Y.Q. Juglanin inhibits lung cancer by regulation of apoptosis, ROS and autophagy induction. Oncotarget, 2017, 8(55), 93878-93898.
[http://dx.doi.org/10.18632/oncotarget.21317] [PMID: 29212196 ]
[125]
Dong, Z.W.; Yuan, Y.F. Juglanin suppresses fibrosis and inflammation response caused by LPS in acute lung injury. Int. J. Mol. Med., 2018, 41(6), 3353-3365.
[http://dx.doi.org/10.3892/ijmm.2018.3554] [PMID: 29532887]
[126]
Dinda, B.; Dinda, S.; DasSharma, S.; Banik, R.; Chakraborty, A.; Dinda, M. Therapeutic potentials of baicalin and its aglycone, baicalein against inflammatory disorders. Eur. J. Med. Chem., 2017, 131, 68-80.
[http://dx.doi.org/10.1016/j.ejmech.2017.03.004] [PMID: 28288320 ]
[127]
Guo, L.T.; Wang, S.Q.; Su, J.; Xu, L.X.; Ji, Z.Y.; Zhang, R.Y.; Zhao, Q.W.; Ma, Z.Q.; Deng, X.Y.; Ma, S.P. Baicalin ameliorates neuroinflammation-induced depressive-like behavior through inhibition of toll-like receptor 4 expression via the PI3K/AKT/FoxO1 pathway. J. Neuroinflammation, 2019, 16(1), 95.
[http://dx.doi.org/10.1186/s12974-019-1474-8] [PMID: 31068207 ]
[128]
Zhou, J.; Chan, L.; Zhou, S. Trigonelline: a plant alkaloid with therapeutic potential for diabetes and central nervous system disease. Curr. Med. Chem., 2012, 19(21), 3523-3531.
[http://dx.doi.org/10.2174/092986712801323171] [PMID: 22680628 ]
[129]
Chowdhury, A.A.; Gawali, N.B.; Munshi, R.; Juvekar, A.R. Trigonelline insulates against oxidative stress, proinflammatory cytokines and restores BDNF levels in lipopolysaccharide induced cognitive impairment in adult mice. Metab. Brain Dis., 2018, 33(3), 681-691.
[http://dx.doi.org/10.1007/s11011-017-0147-5] [PMID: 29277879 ]
[130]
Guo, W.; Sun, J.; Jiang, L.; Duan, L.; Huo, M.; Chen, N.; Zhong, W.; Wassy, L.; Yang, Z.; Feng, H. Imperatorin attenuates LPS-induced inflammation by suppressing NF-κB and MAPKs activation in RAW 264.7 macrophages. Inflammation, 2012, 35(6), 1764-1772.
[http://dx.doi.org/10.1007/s10753-012-9495-9] [PMID: 22890309 ]
[131]
Wang, K.S.; Lv, Y.; Wang, Z.; Ma, J.; Mi, C.; Li, X.; Xu, G.H.; Piao, L.X.; Zheng, S.Z.; Jin, X. Imperatorin efficiently blocks TNF-α-mediated activation of ROS/PI3K/Akt/NF-κB pathway. Oncol. Rep., 2017, 37(6), 3397-3404.
[http://dx.doi.org/10.3892/or.2017.5581] [PMID: 28440462 ]
[132]
Chowdhury, A.A.; Gawali, N.B.; Shinde, P.; Munshi, R.; Juvekar, A.R. Imperatorin ameliorates lipopolysaccharide induced memory deficit by mitigating proinflammatory cytokines, oxidative stress and modulating brain-derived neurotropic factor. Cytokine, 2018, 110, 78-86.
[http://dx.doi.org/10.1016/j.cyto.2018.04.018] [PMID: 29705395 ]
[133]
Sulakhiya, K.; Keshavlal, G.P.; Bezbaruah, B.B.; Dwivedi, S.; Gurjar, S.S.; Munde, N.; Jangra, A.; Lahkar, M.; Gogoi, R. Lipopolysaccharide induced anxiety- and depressive-like behaviour in mice are prevented by chronic pre-treatment of esculetin. Neurosci. Lett., 2016, 611, 106-111.
[http://dx.doi.org/10.1016/j.neulet.2015.11.031] [PMID: 26620836 ]
[134]
Zhu, L.; Nang, C.; Luo, F.; Pan, H.; Zhang, K.; Liu, J.; Zhou, R.; Gao, J.; Chang, X.; He, H.; Qiu, Y.; Wang, J.; Long, H.; Liu, Y.; Yan, T. Esculetin attenuates lipopolysaccharide (LPS)-induced neuroinflammatory processes and depressive-like behavior in mice. Physiol. Behav., 2016, 163, 184-192.
[http://dx.doi.org/10.1016/j.physbeh.2016.04.051] [PMID: 27133730 ]
[135]
Abdoulaye, I.A.; Guo, Y.J. A Review of Recent Advances in Neuroprotective Potential of 3-N-Butylphthalide and Its Derivatives. BioMed Res. Int., 2016, 2016 5012341
[http://dx.doi.org/10.1155/2016/5012341] [PMID: 28053983 ]
[136]
Zhao, C.Y.; Lei, H.; Zhang, Y.; Li, L.; Xu, S.F.; Cai, J.; Li, P.P.; Wang, L.; Wang, X.L.; Peng, Y. L-3-n-Butylphthalide attenuates neuroinflammatory responses by downregulating JNK activation and upregulating Heme oxygenase-1 in lipopolysaccharide-treated mice. J. Asian Nat. Prod. Res., 2016, 18(3), 289-302.
[http://dx.doi.org/10.1080/10286020.2015.1099524] [PMID: 26675131 ]
[137]
Gao, X.J.; Xie, G.N.; Liu, L.; Fu, Z.J.; Zhang, Z.W.; Teng, L.Z. Sesamol attenuates oxidative stress, apoptosis and inflammation in focal cerebral ischemia/reperfusion injury. Exp. Ther. Med., 2017, 14(1), 841-847.
[http://dx.doi.org/10.3892/etm.2017.4550] [PMID: 28673008 ]
[138]
Liu, Z.; Chen, Y.; Qiao, Q.; Sun, Y.; Liu, Q.; Ren, B.; Liu, X. Sesamol supplementation prevents systemic inflammation-induced memory impairment and amyloidogenesis via inhibition of nuclear factor kappaB. Mol. Nutr. Food Res., 2017, 61(5)
[PMID: 27860258 ]
[139]
Kim, N.; Do, J.; Bae, J.S.; Jin, H.K.; Kim, J.H.; Inn, K.S.; Oh, M.S.; Lee, J.K. Piperlongumine inhibits neuroinflammation via regulating NF-κB signaling pathways in lipopolysaccharide-stimulated BV2 microglia cells. J. Pharmacol. Sci., 2018, 137(2), 195-201.
[http://dx.doi.org/10.1016/j.jphs.2018.06.004] [PMID: 29970291 ]
[140]
Gu, S.M.; Lee, H.P.; Ham, Y.W.; Son, D.J.; Kim, H.Y.; Oh, K.W.; Han, S.B.; Yun, J.; Hong, J.T. Piperlongumine Improves Lipopolysaccharide-Induced Amyloidogenesis by Suppressing NF-KappaB Pathway. Neuromolecular Med., 2018, 20(3), 312-327.
[http://dx.doi.org/10.1007/s12017-018-8495-9] [PMID: 29802525 ]
[141]
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.
[http://dx.doi.org/10.1016/j.abb.2014.06.006] [PMID: 24946050 ]
[142]
Mohan, S.; Syam, S.; Abdelwahab, S.I.; Thangavel, N. An anti-inflammatory molecular mechanism of action of α-mangostin, the major xanthone from the pericarp of Garcinia mangostana: an in silico, in vitro and in vivo approach. Food Funct., 2018, 9(7), 3860-3871.
[http://dx.doi.org/10.1039/C8FO00439K] [PMID: 29953154 ]
[143]
Chen, Y.F.; Wang, Y.W.; Huang, W.S.; Lee, M.M.; Wood, W.G.; Leung, Y.M.; Tsai, H.Y. Trans-Cinnamaldehyde, An Essential Oil in Cinnamon Powder, Ameliorates Cerebral Ischemia-Induced Brain Injury via Inhibition of Neuroinflammation Through Attenuation of iNOS, COX-2 Expression and NFκ-B Signaling Pathway. Neuromolecular Med., 2016, 18(3), 322-333.
[http://dx.doi.org/10.1007/s12017-016-8395-9] [PMID: 27087648 ]
[144]
Zhang, L.; Zhang, Z.; Fu, Y.; Yang, P.; Qin, Z.; Chen, Y.; Xu, Y. Trans-cinnamaldehyde improves memory impairment by blocking microglial activation through the destabilization of iNOS mRNA in mice challenged with lipopolysaccharide., 2016.
[http://dx.doi.org/10.1016/j.neuropharm.2016.08.013]
[145]
Abou El-Ezz, D.; Maher, A.; Sallam, N.; El-Brairy, A.; Kenawy, S. Trans-cinnamaldehyde Modulates Hippocampal Nrf2 Factor and Inhibits Amyloid Beta Aggregation in LPS-Induced Neuroinflammation Mouse Model. Neurochem. Res., 2018, 43(12), 2333-2342.
[http://dx.doi.org/10.1007/s11064-018-2656-y] [PMID: 30302613 ]
[146]
Lee, W.H.; Loo, C.Y.; Bebawy, M.; Luk, F.; Mason, R.S.; Rohanizadeh, R. Curcumin and its derivatives: their application in neuropharmacology and neuroscience in the 21st century. Curr. Neuropharmacol., 2013, 11(4), 338-378.
[http://dx.doi.org/10.2174/1570159X11311040002] [PMID: 24381528 ]
[147]
Sorrenti, V.; Contarini, G.; Sut, S.; Dall’Acqua, S.; Confortin, F.; Pagetta, A.; Giusti, P.; Zusso, M. Curcumin Prevents Acute Neuroinflammation and Long-Term Memory Impairment Induced by Systemic Lipopolysaccharide in Mice. Front. Pharmacol., 2018, 9, 183.
[http://dx.doi.org/10.3389/fphar.2018.00183] [PMID: 29556196 ]
[148]
Pardee, A.B.; Li, Y.Z.; Li, C.J. Cancer therapy with beta-lapachone. Curr. Cancer Drug Targets, 2002, 2(3), 227-242.
[http://dx.doi.org/10.2174/1568009023333854] [PMID: 12188909 ]
[149]
Sitônio, M.M.; Carvalho Júnior, C.H. Campos, Ide.A.; Silva, J.B.; Lima, Mdo.C.; Góes, A.J.; Maia, M.B.; Rolim Neto, P.J.; Silva, T.G. Anti-inflammatory and anti-arthritic activities of 3,4-dihydro-2,2-dimethyl-2H-naphthol[1,2-b]pyran-5,6-dione (β-lapachone). Inflamm. Res., 2013, 62(1), 107-113.
[http://dx.doi.org/10.1007/s00011-012-0557-0] [PMID: 23052183 ]
[150]
Besson, J.C.F.; de Carvalho Picoli, C.; Matioli, G.; Natali, M.R.M. Methyl jasmonate: a phytohormone with potential for the treatment of inflammatory bowel diseases. J. Pharm. Pharmacol., 2018, 70(2), 178-190.
[http://dx.doi.org/10.1111/jphp.12839] [PMID: 29072315 ]
[151]
Eduviere, A.T.; Umukoro, S.; Adeoluwa, O.A.; Omogbiya, I.A.; Aluko, O.M. Possible Mechanisms Involved in Attenuation of Lipopolysaccharide-Induced Memory Deficits by Methyl Jasmonate in Mice. Neurochem. Res., 2016, 41(12), 3239-3249.
[http://dx.doi.org/10.1007/s11064-016-2050-6] [PMID: 27590498 ]
[152]
Solomon, U.; Taghogho, E.A. Methyl jasmonate attenuates memory dysfunction and decreases brain levels of biomarkers of neuroinflammation induced by lipopolysaccharide in mice. Brain Res. Bull., 2017, 131, 133-141.
[http://dx.doi.org/10.1016/j.brainresbull.2017.04.002] [PMID: 28411132 ]
[153]
Adebesin, A.; Adeoluwa, O.A.; Eduviere, A.T.; Umukoro, S. Methyl jasmonate attenuated lipopolysaccharide-induced depressive-like behaviour in mice. J. Psychiatr. Res., 2017, 94, 29-35.
[http://dx.doi.org/10.1016/j.jpsychires.2017.06.007] [PMID: 28647678 ]
[154]
Ghosh, S.; Basak, P.; Dutta, S.; Chowdhury, S.; Sil, P.C. New insights into the ameliorative effects of ferulic acid in pathophysiological conditions. Food Chem. Toxicol., 2017, 103, 41-55.
[http://dx.doi.org/10.1016/j.fct.2017.02.028] [PMID: 28237775 ]
[155]
Rehman, S.U.; Ali, T.; Alam, S.I.; Ullah, R.; Zeb, A.; Lee, K.W.; Rutten, B.P.F.; Kim, M.O. Ferulic Acid Rescues LPS-Induced Neurotoxicity via Modulation of the TLR4 Receptor in the Mouse Hippocampus. Mol. Neurobiol., 2019, 56(4), 2774-2790.
[http://dx.doi.org/10.1007/s12035-018-1280-9] [PMID: 30058023]
[156]
Huang, C.; Wu, J.; Chen, D.; Jin, J.; Wu, Y.; Chen, Z. Effects of sulforaphane in the central nervous system. Eur. J. Pharmacol., 2019, 853, 153-168.
[http://dx.doi.org/10.1016/j.ejphar.2019.03.010] [PMID: 30858063 ]
[157]
Townsend, B.E.; Johnson, R.W. Sulforaphane reduces lipopolysaccharide-induced proinflammatory markers in hippocampus and liver but does not improve sickness behavior. Nutr. Neurosci., 2017, 20(3), 195-202.
[http://dx.doi.org/10.1080/1028415X.2015.1103463] [PMID: 26639573 ]
[158]
Gao, J.; Xiong, B.; Zhang, B.; Li, S.; Huang, N.; Zhan, G.; Jiang, R.; Yang, L.; Wu, Y.; Miao, L.; Zhu, B.; Yang, C.; Luo, A. Sulforaphane Alleviates Lipopolysaccharide-induced Spatial Learning and Memory Dysfunction in Mice: The Role of BDNF-mTOR Signaling Pathway. Neuroscience, 2018, 388, 357-366.
[http://dx.doi.org/10.1016/j.neuroscience.2018.07.052] [PMID: 30086367 ]
[159]
Wu, Y.; Gao, M.; Wu, J.; Hu, P.; Xu, X.; Zhang, Y.; Wang, D.; Chen, Z.; Huang, C. Sulforaphane triggers a functional elongation of microglial process via the Akt signal. J. Nutr. Biochem., 2019, 67, 51-62.
[http://dx.doi.org/10.1016/j.jnutbio.2019.01.019] [PMID: 30856464 ]
[160]
Badshah, H.; Ali, T.; Kim, M.O. Osmotin attenuates LPS-induced neuroinflammation and memory impairments via the TLR4/NFκB signaling pathway. Sci. Rep., 2016, 6, 24493.
[http://dx.doi.org/10.1038/srep24493] [PMID: 27093924 ]
[161]
Lessig, J.; Fuchs, B. Plasmalogens in biological systems: their role in oxidative processes in biological membranes, their contribution to pathological processes and aging and plasmalogen analysis. Curr. Med. Chem., 2009, 16(16), 2021-2041.
[http://dx.doi.org/10.2174/092986709788682164] [PMID: 19519379 ]
[162]
Fujino, T.; Yamada, T.; Asada, T.; Tsuboi, Y.; Wakana, C.; Mawatari, S.; Kono, S. Efficacy and Blood Plasmalogen Changes by Oral Administration of Plasmalogen in Patients with Mild Alzheimer’s Disease and Mild Cognitive Impairment: A Multicenter, Randomized, Double-blind, Placebo-controlled Trial. EBioMedicine, 2017, 17, 199-205.
[http://dx.doi.org/10.1016/j.ebiom.2017.02.012] [PMID: 28259590 ]
[163]
Sejimo, S.; Hossain, M.S.; Akashi, K. Scallop-derived plasmalogens attenuate the activation of PKCδ associated with the brain inflammation. Biochem. Biophys. Res. Commun., 2018, 503(2), 837-842.
[http://dx.doi.org/10.1016/j.bbrc.2018.06.084] [PMID: 29920240 ]
[164]
Jiang, X.; Chen, L.; Shen, L.; Chen, Z.; Xu, L.; Zhang, J.; Yu, X. Trans-astaxanthin attenuates lipopolysaccharide-induced neuroinflammation and depressive-like behavior in mice. Brain Res, 2016, 1649(PtA), 30-37.
[http://dx.doi.org/10.1016/j.brainres.2016.08.029] [PMID: 27559013 ]
[165]
Han, J.H.; Lee, Y.S. Im, J.H.; Ham, Y.W.; Lee, H.P.; Han, S.B.; Hong, J.T. Astaxanthin Ameliorates Lipopolysaccharide-Induced Neuroinflammation, Oxidative Stress and Memory Dysfunction through Inactivation of the Signal Transducer and Activator of Transcription 3 Pathway. Mar. Drugs, 2019, 17(2)E123
[http://dx.doi.org/10.3390/md17020123] [PMID: 30781690 ]
[166]
Chuyen, H.V.; Eun, J.B. Marine carotenoids: Bioactivities and potential benefits to human health. Crit. Rev. Food Sci. Nutr., 2017, 57(12), 2600-2610.
[http://dx.doi.org/10.1080/10408398.2015.1063477] [PMID: 26565683 ]
[167]
Jiang, X.; Wang, G.; Lin, Q.; Tang, Z.; Yan, Q.; Yu, X. Fucoxanthin prevents lipopolysaccharide-induced depressive-like behavior in mice via AMPK- NF-κB pathway. Metab. Brain Dis., 2019, 34(2), 431-442.
[http://dx.doi.org/10.1007/s11011-018-0368-2] [PMID: 30554399 ]
[168]
Shi, Z.; Ren, H.; Huang, Z.; Peng, Y.; He, B.; Yao, X.; Yuan, T.F.; Su, H. Fish Oil Prevents Lipopolysaccharide-Induced Depressive-Like Behavior by Inhibiting Neuroinflammation. Mol. Neurobiol., 2017, 54(9), 7327-7334.
[http://dx.doi.org/10.1007/s12035-016-0212-9] [PMID: 27815837 ]
[169]
Rey, C.; Delpech, J.C.; Madore, C.; Nadjar, A.; Greenhalgh, A.D.; Amadieu, C.; Aubert, A.; Pallet, V.; Vaysse, C.; Layé, S.; Joffre, C. Dietary n-3 long chain PUFA supplementation promotes a pro-resolving oxylipin profile in the brain. Brain Behav. Immun., 2019, 76, 17-27.
[http://dx.doi.org/10.1016/j.bbi.2018.07.025] [PMID: 30086401 ]
[170]
de Gomes, M.G.; Souza, L.C.; Goes, A.R.; Del Fabbro, L.; Filho, C.B.; Donato, F.; Prigol, M.; Luchese, C.; Roman, S.S.; Puntel, R.L.; Boeira, S.P.; Jesse, C.R. Fish oil ameliorates sickness behavior induced by lipopolysaccharide in aged mice through the modulation of kynurenine pathway. J. Nutr. Biochem., 2018, 58, 37-48.
[http://dx.doi.org/10.1016/j.jnutbio.2018.05.002] [PMID: 29870875 ]
[171]
Karlsen, A.; Retterstøl, L.; Laake, P.; Paur, I.; Bøhn, S.K.; Sandvik, L.; Blomhoff, R. Anthocyanins inhibit nuclear factor-kappaB activation in monocytes and reduce plasma concentrations of pro-inflammatory mediators in healthy adults. J. Nutr., 2007, 137(8), 1951-1954.
[http://dx.doi.org/10.1093/jn/137.8.1951] [PMID: 17634269 ]
[172]
Theoharides, T.C.; Asadi, S.; Panagiotidou, S. A case series of a luteolin formulation (NeuroProtek®) in children with autism spectrum disorders. Int. J. Immunopathol. Pharmacol., 2012, 25(2), 317-323.
[http://dx.doi.org/10.1177/039463201202500201] [PMID: 22697063 ]
[173]
Theoharides, T.C.; Stewart, J.M.; Hatziagelaki, E.; Kolaitis, G. Brain “fog,” inflammation and obesity: key aspects of neuropsychiatric disorders improved by luteolin. Front. Neurosci., 2015, 9, 225.
[http://dx.doi.org/10.3389/fnins.2015.00225] [PMID: 26190965 ]
[174]
Xiao, H.; Wignall, N.; Brown, E.S. An open-label pilot study of icariin for co-morbid bipolar and alcohol use disorder. Am. J. Drug Alcohol Abuse, 2016, 42(2), 162-167.
[http://dx.doi.org/10.3109/00952990.2015.1114118] [PMID: 26809351 ]
[175]
Ramírez-Garza, S.L.; Laveriano-Santos, E.P.; Marhuenda-Muñoz, M.; Storniolo, C.E.; Tresserra-Rimbau, A.; Vallverdú-Queralt, A.; Lamuela-Raventós, R.M. marhuenda-Muñoz, M.; Storniolo, C. E.; Tresserra-Rimbau, A.; Vallverdu-Queralt, A.; Lamuela-Raventos, R. M. Health effects of resveratrol: results human intervention trials. Nutrients, 2018, 10(12) E1892
[PMID: 30513922 ]
[176]
Khan, H.; Ullah, H.; Martorell, M.; Valdes, S. E.; Belwal, T.; Tejada, S.; Sureda, A.; Kamal, M. A. Flavonoids nanoparticles in cáncer: treatment, prevention and clinical prospects. Semin. Cancer Biol, 2019, 30S1044-579X(19)30182-8,
[http://dx.doi.org/10.1016/j.semcancer.2019.07.023] [PMID: 31374244 ]
[177]
Li, S.; Wu, B.; Fu, W.; Reddivari, L. The anti-inflammatory effects of dietary anthocyanins against ulcerative colitis. Int. J. Mol. Sci., 2019, 20(10) E2588
[http://dx.doi.org/10.3390/ijms20102588] [PMID: 31137777 ]
[178]
Rebello, C.J.; Beyl, R.A. lertora, J. J. L.; Greenway, F. L.; Ravussin, E.; Ribnicky, D. M.; Pouley, A.; Kennedy, B. J.; Castro, H. F.; Campagna, S. R.; Coulter, A. A.; Redman, L. M. Safety and pharmacokinetics of naringenin: a randomized, controlled, single-ascending-dose clinical trial. Diabetes Obes. Metab., 2019, 22(1), 91-98.
[179]
Vamanu, E. Polyphenolic nutraceuticals to combat oxidative stress through microbiota modulation. Front. Pharmacol., 2019, 10, 492.
[http://dx.doi.org/10.3389/fphar.2019.00492] [PMID: 31130865 ]
[180]
Brown, B.I. Nutritional management of metabolic endotoxemia: a clinical review. Altern. Ther. Health Med., 2017, 23(4), 42-54.
[PMID: 28646814 ]
[181]
McCormick, J.K.; Yarwood, J.M.; Schlievert, P.M. Toxic shock syndrome and bacterial superantigens: an update. Annu. Rev. Microbiol., 2001, 55, 77-104.
[http://dx.doi.org/10.1146/annurev.micro.55.1.77] [PMID: 11544350]


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 18
ISSUE: 7
Year: 2020
Published on: 28 July, 2020
Page: [636 - 654]
Pages: 19
DOI: 10.2174/1570159X18666200114125628
Price: $65

Article Metrics

PDF: 31
HTML: 3
PRC: 1