Therapeutic potential of berberine against neurodegenerative diseases

Takase H, Yamamoto K, Ito K, Yumioka E. Pharmacological studies on antidiarrheal effects of berberine and geranii herba (in Japanese). Nihon Yakurigaku Zasshi, 1993, 102: 101–112 Kheir MM, Wang Y, Hua L, Hu J, Li L, Lei F, Du L. Acute toxicity of berberine and its correlation with the blood concentration in mice. Food Chem Toxicol, 2010, 48: 1105–1110 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 JD. Berberine is a novel cholesterol-lowering drug working through a unique mechanism distinct from statins. Nat Med, 2004, 10: 1344–1351 Zhang H, Wei J, Xue R, Wu JD, Zhao W, Wang ZZ, Wang SK, Zhou ZX, Song DQ, Wang YM, Pan HN, Kong WJ, Jiang, J. D. Berberine lowers blood glucose in type 2 diabetes mellitus patients through increasing insulin receptor expression. Metabolism, 2010, 59: 285–292 Li BX, Yang BF, Zhou J, Xu CQ, Li YR. Inhibitory effects of berberine on IK1, IK, and HERG channels of cardiac myocytes. Acta Pharmacol Sin, 2001, 22: 125–131 Jiang Q, Liu P, Wu X, Liu W, Shen X, Lan T, Xu S, Peng J, Xie X, Huang H. Berberine attenuates lipopolysaccharide-induced extracellular matrix accumulation and inflammation in rat mesangial cells: involvement of NF-κB signaling pathway. Mol Cell Endocrinol, 2011, 331: 34–40 Hayashi K, Minoda K, Nagaoka Y, Hayashi T, Uesato S. Antiviral activity of berberine and related compounds against human cytomegalovirus. Bioorg Med Chem Lett, 2007, 17: 1562–1564 Iizuka N1, Miyamoto K, Okita K, Tangoku A, Hayashi H, Yosino S, Abe T, Morioka T, Hazama S, Oka M. Inhibitory effect of Coptidis Rhizoma and berberine on the proliferation of human esophageal cancer cell lines. Cancer Lett, 2000, 148: 19–25 Sack RB, Froehlich JL. Berberine inhibits intestinal secretory response of Vibrio cholerae and Escherichia coli enterotoxins. Infect Immun, 1982, 35: 471–475 Hong Y, Hui SC, Chan TY, Hou JY. Effect of berberine on regression of pressure-overload induced cardiac hypertrophy in rats. Am J Chin Med, 2002, 30: 589–599 Dong SF, Hong Y, Liu M, Hao YZ, Yu HS, Liu Y, Sun J. N. Berberine attenuates cardiac dysfunction in hyperglycemic and hypercholesterolemic rats. Eur J Pharmacol, 2011, 660: 368–374 Zhang Y, Li X, Zou D, Liu W, Yang J, Zhu N, Huo L, Wang M, Hong J, Wu P, Ren G, Ning G. Treatment of type 2 diabetes and dyslipidemia with the natural plant alkaloid berberine. J Clin Endocrinol Metab, 2008, 93: 2559–2565 Peng PL, Hsieh YS, Wang CJ, Hsu JL, Chou FP. Inhibitory effect of berberine on the invasion of human lung cancer cells via decreased productions of urokinase-plasminogen activator and matrix metalloproteinase-2. Toxicol Appl Pharmacol, 2006, 214: 8–15 Lin TH, Kuo HC, Chou FP, Lu FJ. Berberine enhances inhibition of glioma tumor cell migration and invasiveness mediated by arsenic trioxide. BMC Cancer, 2008, 8: 58 Peng WH, Wu CR, Chen CS, Chen CF, Leu ZC, Hsieh MT. Anxiolytic effect of berberine on exploratory activity of the mouse in two experimental anxiety models: interaction with drugs acting at 5-HT receptors. Life Sci, 2004, 75: 2451–2462 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 Kwon IH, Choi HS, Shin KS, Lee BK, Lee CK, Hwang BY, Lim SC, Lee MK. Effects of berberine on 6-hydroxydopamine-induced neurotoxicity in PC12 cells and a rat model of Parkinson’s disease. Neurosci Lett, 2010, 48: 29–33 Hebert LE, Scherr PA, Beckett LA, Albert MS, Pilgrim DM, Chown MJ, Funkenstein HH, Evans DA. Age-specific incidence of Alzheimer’s disease in a community population. JAMA, 1995, 273: 1354–1359 Hardy J, Allsop D. Amyloid deposition as the central event in the aetiology of Alzheimer’s disease. Trends Pharmacol Sci, 1991, 12: 383–388 Davie CA. A review of Parkinson’s disease. Br Med Bull, 2008, 86: 109–127 Dickson DV. Neuropathology of movement disorders. In: Tolosa E, Jankovic JJ. Parkinson’s disease and movement disorders. Hagerstown, MD: Lippincott Williams & Wilkins, 2007. 271–283 The National Collaborating Centre for Chronic Conditions, ed. “Symptomatic pharmacological therapy in Parkinson’s disease”. Parkinson’s Disease. London: Royal College of Physicians, 2006. 59–100 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: 293–298 Jung HA, Min BS, Yokozawa T, Lee JH, Kim YS, Choi JS. Anti-Alzheimer and antioxidant activities of Coptidis Rhizoma alkaloids. Biol Pharm Bull, 2009, 32: 1433–1438 Panahi N, Mahmoudian M, Mortazavi P, Hashjin GS. Effects of berberine on β-secretase activity in a rabbit model of Alzheimer’s disease. Arch Med Sci, 2013, 9: 146–150 Asai M, Iwata N, Yoshikawa A, Aizaki Y, Ishiura S, Saido TC, Maruyama K. Berberine alters the processing of Alzheimer’s amyloid precursor protein to decrease Abeta secretion. Biochem Biophys Res Commun, 2007, 352: 498–502 Durairajan SSK, Liu LF, Lu JH, Chen LL, Yuan Q, Chung SK, Huang L, Li XS, Huang JD, Li M. Berberine ameliorates β-amyloid pathology, gliosis, and cognitive impairment in an Alzheimer’s disease transgenic mouse model. Neurobiol Aging, 2012, 33: 2903–2919 Kim M, Cho KH, Shin MS, Lee JM, Cho HS, Kim CJ, Shin DH, Yang HJ. Berberine prevents nigrostriatal dopaminergic neuronal loss and suppresses hippocampal apoptosis in mice with Parkinson’s disease. Int J Mol Med, 2014, 33: 870–878 Kwon IH1, Choi HS, Shin KS, Lee BK, Lee CK, Hwang BY, Lim SC, Lee MK. Effects of berberine on 6-hydroxydopamine-induced neurotoxicity in PC12 cells and a rat model of Parkinson’s disease. Neurosci Lett, 2010, 486: 29–33 Shin KS, Choi HS, Zhao TT, Suh KH, Kwon IH, Choi SO, Lee MK. 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: 759–767 Castillo JA, Huang J, Rodriguez M, Bastidas E, Laboren I, Jaimes A. Direct led-fluorescence method for Mao-B inactivation in the treatment of Parkinson’s. In: 5th Iberoamerican Meeting on Optics and 8th Latin American Meeting on Optics, Lasers, and Their Applications. International Society for Optics and Photonics, 2004. 142–148 Kong LD, Cheng CH, Tan RX. Monoamine oxidase inhibitors from rhizoma of Coptis chinensis. Planta Med, 2001, 67: 74–76 Bae J, Lee D, Kim YK, Gil M, Lee JY, Lee KJ. Berberine protects 6-hydroxydopamine-induced human dopaminergic neuronal cell death through the induction of heme oxygenase-1. Mol Cells, 2013, 35: 151–157 Hsu YY, Chen CS, Wu SN, Jong YJ, Lo YC. 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: 415–425 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 Hu J, Chai Y, Wang Y, Kheir MM, 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 ischemiareperfusion. Eur J Pharm, 2012, 674: 132–142 Zhou XQ, Zeng XN, Kong H, Sun XL. Neuroprotective effects of berberine on stroke models in vitro and in vivo. Neurosci Lett, 2008, 447: 31–36 Cui HS, 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: 79–85 Lim JS, Kim HS, Choi YS, Kwon HM, Shin KS, Joung IS, Shin MJ, Kwon YK. Neuroprotective effects of berberine in neurodegeneration model rats induced by ibotenic acid. Anim Cells Syst, 2008, 12: 203–209 Zhang J, Yang JQ, He BC, Zhou QX, Yu HR, Tang Y, Liu BZ. 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: 760–766 Hong JS, Chu YK, Lee H, Ahn BH, Park JH, Kim MJ, Lee S, Ryoo HS, Jang JH, Lee SR, Park JW. Effects of berberine on hippocampal neuronal damage and matrix metalloproteinase-9 activity following transient global cerebral ischemia. J Neurosci Res, 2012, 90: 489–497 Benaissa F, Mohseni-Rad H, Rahimi-Moghaddam P, Mahmoudian M. Berberine reduces the hypoxic-ischemic insult in rat pup brain. Acta Physiol Hung, 2009, 96: 213–220 Lee T, Heo H, Kim Kwon Y. Effect of berberine on cell survival in the developing rat brain damaged by MK-801. Exp Neurobiol, 2010, 19: 140–145 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: 30–41 Mangoni A, Grassi MP, Frattola L, Piolti R, Bassi S, Motta A, Marcone A, Smirne S. Effects of a MAO-B inhibitor in the treatment of Alzheimer disease. Eur Neurol, 1991, 31: 100–107 Rabey JM, Sagi I, Huberman M, Melamed E, Korczyn A, Giladi N, Inzelberg R, Djaldetti R, Klein C, Berecz G; Rasagiline Study Group. 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: 324–330 Kurth JH, Kurth MC, Poduslo SE, Schwankhaus JD. Association of a monoamine oxidase B allele with Parkinson’s disease. Ann Neurol, 1993, 33: 368–372 Cristina RA, Oliveira CR. Mitochondrial dysfunction and reactive oxygen species in excitotoxicity and apoptosis: implications for the pathogenesis of neurodegenerative diseases. Neurochem Res, 2003, 28: 1563–1574 St-Pierre J, Drori S, Uldry M, Silvaggi JM, Rhee J, Jäger S, Handschin C, Zheng K, Lin J, Yang W, Simon DK, Bachoo R, Spiegelman BM. Suppression of reactive oxygen species and neurodegeneration by the PGC-1 transcriptional coactivators. Cell, 2006, 127: 397–408 Lei Y, He HY, Zhang XJ. Increased expression of intranuclear AChE involved in apoptosis of SK-N-SH cells. Neurosci Res, 2002, 42: 261–268 Holzgrabe U, Kapková P, Alptüzün V, Scheiber J, Kugelmann E. Targeting acetylcholinesterase to treat neurodegeneration. Expert Opin Ther Targets, 2007, 11: 161–179 Vargas MR, Johnson DA, Sirkis DW, Messing A, Johnson JA. Nrf2 activation in astrocytes protects against neurodegeneration in mouse models of familial amyotrophic lateral sclerosis. J Neurosci, 2008, 28: 13574–13581 de Vries HE, Witte M, Hondius D, Rozemuller AJ, Drukarch B, Hoozemans J, van Horssen J. Nrf2-induced antioxidant protection: a promising target to counteract ROS-mediated damage in neurodegenerative disease? Free Radic Biol Med, 2008, 45: 1375–1383 Perry T, Holloway HW, Weerasuriya A, Mouton PR, Duffy K, Mattison JA, Greig NH. Evidence of GLP-1-mediated neuroprotection in an animal model of pyridoxine-induced peripheral sensory neuropathy. Exp Neurol, 2007, 203: 293–301 Hölscher C. The role of GLP-1 in neuronal activity and neurodegeneration. Vitam Horm, 2010, 84: 331–354 Li Y, Perry T, Kindy MS, Harvey BK, Tweedie D, Holloway HW, Powers K, Shen H, Egan JM, Sambamurti K, Brossi A, Lahiri DK, Mattson MP, Hoffer BJ, Wang Y, Greig NH. GLP-1 receptor stimulation preserves primary cortical and dopaminergic neurons in cellular and rodent models of stroke and Parkinsonism. Proc Natl Acad Sci USA, 2009, 106: 1285–1290 Kennedy SG, Kandel ES, Cross TK, Hay N. Akt/Protein kinase B inhibits cell death by preventing the release of cytochrome c from mitochondria. Mol Cell Biol, 1999, 19: 5800–5810 Brunet A, Datta SR, Greenberg ME. Transcription-dependent and-independent control of neuronal survival by the PI3K-Akt signaling pathway. Curr Opin Neurobiol, 2001, 11: 297–305 Kazuhiro N, Ito S, Nakashima K. Caffeine activates the PI3K/Akt pathway and prevents apoptotic cell death in a Parkinson’s disease model of SH-SY5Y cells. Neurosci Lett, 2008, 432: 146–150 Mantamadiotis T, Lemberger T, Bleckmann SC, Kern H, Kretz O, Martin Villalba A, Tronche F, Kellendonk C, Gau D, Kapfhammer J, Otto C, Schmid W, Schütz G. Disruption of CREB function in brain leads to neurodegeneration. Nat Genet, 2002, 31: 47–54 Mike D. CREB and neurodegeneration. Front Biosci, 2004, 9: 100–103