Resveratrol Protects from Toxin-Induced Parkinsonism: Plethora of Proofs Hitherto Petty Translational Value

Molecular Neurobiology

Volumn 53, Issue 5, 2016, Pages 2751-2760

  ur Rasheed, Mohd Sami ^a,b   Tripathi, Manish Kumar ^a,b   Mishra, Abhishek Kumar ^a,b   Shukla, Saurabh ^a   Singh, Mahendra Pratap ^a,b  

^a CSIR INDIAN INSTITUTE OF TOXICOLOGY RESEARCH   (India)

^b ACADEMY OF SCIENTIFIC AND INNOVATIVE RESEARCH ACSIR   (India)

Author keywords

Cellular models; Parkinsonism; Resveratrol; Rodent models; Translational value

Indexed keywords

1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; 6 HYDROXYDOPA; ANTIOXIDANT; FREE RADICAL; LIPOPOLYSACCHARIDE; MANEB; PARAQUAT; RESVERATROL; ROTENONE; TOXIN; NEUROPROTECTIVE AGENT; NEUROTOXIN; STILBENE DERIVATIVE;

ANTIOXIDANT ACTIVITY; APOPTOSIS; CELL DEATH; DEGRADATION; DISEASE MODEL; DRUG EFFECT; DRUG EFFICACY; GENETIC MODEL; HUMAN; MACROAUTOPHAGY; NERVE DEGENERATION; NERVOUS SYSTEM INFLAMMATION; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PARKINSON DISEASE; PARKINSONISM; REVIEW; SIGNAL TRANSDUCTION; SUBSTANTIA NIGRA; ANIMAL; INFLAMMATION; PATHOLOGY; TRANSLATIONAL RESEARCH;

ANIMALS; HUMANS; INFLAMMATION; NEUROPROTECTIVE AGENTS; NEUROTOXINS; PARKINSONIAN DISORDERS; STILBENES; TRANSLATIONAL MEDICAL RESEARCH;

EID: 84923052530     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-015-9124-3     Document Type: Review

References (79)

1. Gupta SP, Yadav S, Singhal NK, Tiwari MN, Mishra SK, Singh MP (2014) Does restraining nitric oxide biosynthesis rescue from toxins-induced Parkinsonism and sporadic Parkinson’s disease? Mol Neurobiol 49:262–275
2. Yadav S, Dixit A, Agrawal S, Singh A, Srivastava G, Singh AK, Srivastava PK, Prakash O, Singh MP (2012) Rodent models and contemporary molecular techniques: notable feats yet incomplete explanations of Parkinson’s disease pathogenesis. Mol Neurobiol 46:495–512
3. Singhal NK, Srivastava G, Agrawal S, Jain SK, Singh MP (2012) Melatonin as a neuroprotective agent in the rodent models of Parkinson’s disease: is it all set to irrefutable clinical translation? Mol Neurobiol 45:186–199
4. Srivastava G, Singh K, Tiwari MN, Singh MP (2010) Proteomics in Parkinson’s disease: current trends, translational snags and future possibilities. Expert Rev Proteomics 7:127–139
5. Mishra AK, Ur Rasheed MS, Shukla S, Tripathi MK, Dixit A, Singh MP (2014) Aberrant autophagy and Parkinsonism: does correction rescue from disease progression? Mol Neurobiol. doi:10.1007/s12035-014-8744-3
6. Agrawal S, Singh A, Tripathi P, Mishra M, Singh PK, Singh MP (2014) Cypermethrin-induced nigrostriatal dopaminergic neurodegeneration alters the mitochondrial function: a proteomics study. Mol Neurobiol. doi:10.1007/s12035-014-8696-7
7. Gerhardt E, Gräber S, Szego EM, Moisoi N, Martins LM, Outeiro TF, Kermer P (2011) Idebenone and resveratrol extend lifespan and improve motor function of HtrA2 knockout mice. PLoS One 6:e28855
8. Baur JA, Sinclair DA (2006) Therapeutic potential of resveratrol: the in vivo evidence. Nat Rev Drug Discov 5:493–506
9. Athar M, Back JH, Tang X, Kim KH, Kopelovich L, Bickers DR, Kim AL (2007) Resveratrol: a review of preclinical studies for human cancer prevention. Toxicol Appl Pharmacol 224:274–283
10. Sun AY, Wang Q, Simonyi A, Sun GY (2010) Resveratrol as a therapeutic agent for neurodegenerative diseases. Mol Neurobiol 41:375–383
11. Lofrumento DD, Nicolardi G, Cianciulli A, De Nuccio F, La Pesa V, Carofiglio V, Dragone T, Calvello R, Panaro MA (2014) Neuroprotective effects of resveratrol in an MPTP mouse model of Parkinson’s-like disease: possible role of SOCS-1 in reducing pro-inflammatory responses. Innate Immun 20:249–260
12. Mudò G, Mäkelä J, Di Liberto V, Tselykh TV, Olivieri M, Piepponen P, Eriksson O, Mälkiä A, Bonomo A, Kairisalo M, Aguirre JA, Korhonen L, Belluardo N, Lindholm D (2012) Transgenic expression and activation of PGC-1α protect dopaminergic neurons in the MPTP mouse model of Parkinson’s disease. Cell Mol Life Sci 69:1153–1165
13. Lu KT, Ko MC, Chen BY, Huang JC, Hsieh CW, Lee MC, Chiou RY, Wung BS, Peng CH, Yang YL (2008) Neuroprotective effects of resveratrol on MPTP-induced neuron loss mediated by free radical scavenging. J Agric Food Chem 56:6910–6913
14. Sun AY, Simonyi A, Sun GY (2002) The “French paradox” and beyond: neuroprotective effects of polyphenols. Free Radic Biol Med 32:314–318
15. Singh AK, Tiwari MN, Prakash O, Singh MP (2012) A current review of cypermethrin-induced neurotoxicity and nigrostriatal dopaminergic neurodegeneration. Curr Neuropharmacol 10:64–71
16. Srivastava G, Dixit A, Yadav S, Patel DK, Prakash O, Singh MP (2012) Resveratrol potentiates cytochrome P450 2 d22-mediated neuroprotection in maneb- and paraquat-induced Parkinsonism in the mouse. Free Radic Biol Med 52:1294–1306
17. Albani D, Polito L, Batelli S, De Mauro S, Fracasso C, Martelli G, Colombo L, Manzoni C, Salmona M, Caccia S, Negro A, Forloni G (2009) The SIRT1 activator resveratrol protects SK-N-BE cells from oxidative stress and against toxicity caused by alpha-synuclein or amyloid-beta (1–42) peptide. J Neurochem 110:1445–1456
18. Khan MM, Ahmad A, Ishrat T, Khan MB, Hoda MN, Khuwaja G, Raza SS, Khan A, Javed H, Vaibhav K, Islam F (2010) Resveratrol attenuates 6-hydroxydopamine-induced oxidative damage and dopamine depletion in rat model of Parkinson’s disease. Brain Res 1328:139–151
19. Jin F, Wu Q, Lu YF, Gong QH, Shi JS (2008) Neuroprotective effect of resveratrol on 6-OHDA-induced Parkinson’s disease in rats. Eur J Pharmacol 600:78–82
20. Wu Y, Li X, Zhu JX, Xie W, Le W, Fan Z, Jankovic J, Pan T (2011) Resveratrol-activated AMPK/SIRT1/autophagy in cellular models of Parkinson’s disease. Neurosignals 19:163–174
21. Lin TK, Chen SD, Chuang YC, Lin HY, Huang CR, Chuang JH, Wang PW, Huang ST, Tiao MM, Chen JB, Liou CW (2014) Resveratrol partially prevents rotenone-induced neurotoxicity in dopaminergic SH-SY5Y cells through induction of heme oxygenase-1 dependent autophagy. Int J Mol Sci 15:1625–1646
22. Alvira D, Yeste-Velasco M, Folch J, Verdaguer E, Canudas AM, Pallàs M, Camins A (2007) Comparative analysis of the effects of resveratrol in two apoptotic models: inhibition of complex I and potassium deprivation in cerebellar neurons. Neuroscience 147:746–756
23. Bournival J, Quessy P, Martinoli MG (2009) Protective effects of resveratrol and quercetin against MPP+ -induced oxidative stress act by modulating markers of apoptotic death in dopaminergic neuron. Cell Mol Neurobiol 29:1169–1180
24. Chao J, Li H, Cheng KW, Yu MS, Chang RC, Wang M (2010) Protective effects of pinostilbene, a resveratrol methylated derivative, against 6-hydroxydopamine-induced neurotoxicity in SH-SY5Y cells. J Nutr Biochem 21:482–489
25. Chang CY, Choi DK, Lee DK, Hong YJ, Park EJ (2013) Resveratrol confers protection against rotenone-induced neurotoxicity by modulating myeloperoxidase levels in glial cells. PLoS One 8:e60654
26. Rose KM, Parmar MS, Cavanaugh JE (2014) Dietary supplementation with resveratrol protects against striatal dopaminergic deficits produced by in utero LPS exposure. Brain Res 1573:37–43
27. Dragone T, Cianciulli A, Calvello R, Porro C, Trotta T, Panaro MA (2014) Resveratrol counteracts lipopolysaccharide-mediated microglial inflammation by modulating a SOCS-1 dependent signaling pathway. Toxicol in Vitro 28:1126–1135
28. Zhang F, Shi JS, Zhou H, Wilson B, Hong JS, Gao HM (2010) Resveratrol protects dopamine neurons against lipopolysaccharide-induced neurotoxicity through its anti-inflammatory actions. Mol Pharmacol 78:466–477
29. Bi XL, Yang JY, Dong YX, Wang JM, Cui YH, Ikeshima T, Zhao YQ, Wu CF (2005) Resveratrol inhibits nitric oxide and TNF-alpha production by lipopolysaccharide-activated microglia. Int Immunopharmacol 5:185–193
30. Ferretta A, Gaballo A, Tanzarella P, Piccoli C, Capitanio N, Nico B, Annese T, Di Paola M, Dell’aquila C, De Mari M, Ferranini E, Bonifati V, Pacelli C, Cocco T (2014) Effect of resveratrol on mitochondrial function: implications in Parkin-associated familiar Parkinson’s disease. Biochim Biophys Acta 1842:902–915
31. Ghavami S, Shojaei S, Yeganeh B, Ande SR, Jangamreddy JR, Mehrpour M, Christoffersson J, Chaabane W, Moghadam AR, Kashani HH, Hashemi M, Owji AA, Łos MJ (2014) Autophagy and apoptosis dysfunction in neurodegenerative disorders. Prog Neurobiol 112:24–49
32. Chao J, Yu MS, Ho YS, Wang M, Chang RC (2008) Dietary oxyresveratrol prevents parkinsonian mimetic 6-hydroxydopamine neurotoxicity. Free Radic Biol Med 45:1019–1026
33. Boocock DJ, Faust GE, Patel KR, Schinas AM, Brown VA, Ducharme MP, Booth TD, Crowell JA, Perloff M, Gescher AJ, Steward WP, Brenner DE (2007) Phase I dose escalation pharmacokinetic study in healthy volunteers of resveratrol, a potential cancer chemopreventive agent. Cancer Epidemiol Biomarkers Prev 16:1246–1252
34. Singh S, Singh K, Patel DK, Singh C, Nath C, Singh VK, Singh RK, Singh MP (2009) The expression of CYP2D22, an ortholog of human CYP2D6, in mouse striatum and its modulation in 1-methyl 4-phenyl-1, 2, 3, 6-tetrahydropyridine-induced Parkinson’s disease phenotype and nicotine-mediated neuroprotection. Rejuvenation Res 12:185–197
35. Bagatini PB, Saur L, Rodrigues MF, Bernardino GC, Paim MF, Coelho GP, Silva DV, de Oliveira RM, Schirmer H, Souto AA, Vianna MR, Xavier LL (2011) The role of calcium channel blockers and resveratrol in the prevention of paraquat-induced parkinsonism in Drosophila melanogaster: a locomotor analysis. Invert Neurosci 11:43–51
36. Ye J, Liu Z, Wei J, Lu L, Huang Y, Luo L, Xie H (2013) Protective effect of SIRT1 on toxicity of microglial-derived factors induced by LPS to PC12 cells via the p53-caspase-3-dependent apoptotic pathway. Neurosci Lett 553:72–77
37. Zini R, Morin C, Bertelli A, Bertelli AA, Tillement JP (2002) Resveratrol-induced limitation of dysfunction of mitochondria isolated from rat brain in an anoxia-reoxygenation model. Life Sci 71:3091–3108
38. Okawara M, Katsuki H, Kurimoto E, Shibata H, Kume T, Akaike A (2006) Resveratrol protects dopaminergic neurons in midbrain slice culture from multiple insults. Biochem Pharmacol 73:550–560
39. Singh N, Agrawal M, Dore S (2013) Neuroprotective properties and mechanisms of resveratrol in vitro and in vivo experimental cerebral stroke models. ACS Chem Neurosci 4:1151–1162
40. McCarthy S, Somayajulu M, Sikorska M, Borowy-Borowski H, Pandey S (2004) Paraquat induces oxidative stress and neuronal cell death; neuroprotection by water-soluble coenzyme Q10. Toxicol Appl Pharmacol 201:21–31
41. Liang CL, Sinton CM, Sonsalla PK, German DC (1996) Midbrain dopaminergic neurons in the mouse that contain calbindin-D28k exhibit reduced vulnerability to MPTP-induced neurodegeneration. Neurodegeneration 5:313–318
42. Bharath S, Hsu M, Kaur D, Rajagopalan S, Andersen JK (2002) Glutathione, iron and Parkinson’s disease. Biochem Pharmacol 64:1037–1048
43. Lynch-Day MA, Mao K, Wang KE, Zhao M, Klionsky DJ (2012) The role of autophagy in Parkinson’s disease. Cold Spring Harb Perspect Med 2:a009357
44. Hermida-Ameijeiras A, Méndez-Álvarez E, Sánchez-Iglesias S, Sanmart’ın-Suárez C, Soto-Otero R (2004) Autoxidation and MAO-mediated metabolism of dopamine as a potential cause of oxidative stress: role of ferrous and ferric ions. Neurochem Int 45:103–116
45. Anandhan A, Tamilselvam K, Vijayraja D, Ashokkumar N, Rajasankar S, Manivasagam T (2010) Resveratrol attenuates oxidative stress and improves behaviour in 1 -methyl-4-phenyl-1, 2,3,6-tetrahydropyridine (MPTP) challenged mice. Ann Neurosci 17:113–119
46. Baur JA (2010) Resveratrol, sirtuins, and the promise of a DR mimetic. Mech Ageing Dev 131:261–269
47. Scarpulla RC (2011) Metabolic control of mitochondrial biogenesis through the PGC-1 family regulatory network. Biochim Biophys Acta 1813:1269–1278
48. Dasgupta B, Milbrandt J (2007) Resveratrol stimulates AMP kinase activity in neurons. Proc Natl Acad Sci U S A 104:7217–7222
49. Chen CY, Jang JH, Li MH, Surh YJ (2005) Resveratrol upregulatesheme oxygenase-1 expression via activation of NF-E2-related factor 2 in PC12 cells. Biochem Biophys Res Commun 331:993–1000
50. Niture SK, Khatri R, Jaiswal AK (2014) Regulation of Nrf2-an update. Free Radic Biol Med 66:36–44
51. He X, Wang L, Szklarz G, Bi Y, Ma Q (2012) Resveratrol inhibits paraquat-induced oxidative stress and fibrogenic response by activating the nuclear factor erythroid 2-related factor 2 pathway. J Pharmacol Exp Ther 342:81–90
52. Shin SM, Cho IJ, Kim SG (2009) Resveratrol protects mitochondria against oxidative stress through AMP-activated protein kinase-mediated glycogen synthase kinase-3 inhibition downstream of poly (ADPribose) polymerase-LKB1 pathway. Mol Pharmacol 76:884–895
53. Rigolio R, Miloso M, Nicolini G, Villa D, Scuteri A, Simone M, Tredici G (2005) Reseratrol interference with the cell cycle protects human neuroblastoma SH-SY5Y cell from paclitaxel-induced apoptosis. Neurochem Int 46:205–211
54. 2+ transfer in the control of apoptosis. Oncogene 27:6407–6418
55. Feng X, Liang N, Zhu D, Gao Q, PengL DH, Yue Q, Liu H, Bao L, Zhang J, Hao J, Gao Y, Yu X, Sun J (2013) Resveratrol inhibits β-amyloid-induced neuronal apoptosis through regulation of SIRT1-ROCK1 signaling pathway. PLoS One 8:e59888
56. Lee MK, Kang SJ, Poncz M, Song KJ, Park KS (2007) Resveratrol protects SH-SY5Y neuroblastoma cells from apoptosis induced by dopamine. Exp Mol Med 39:376–384
57. Nicolini G, Rigolio R, Miloso M, Bertelli AAE, Tredici G (2001) Anti-apoptotic effect of trans-resveratrol on paclitaxel-induced apoptosis in the human neuroblastoma SH-SY5Y cell line. Neurosci Lett 302:41–44
58. Renaud J, Bournival J, Zottig X, Martinoli MG (2014) Resveratrol protects DAergic PC12 cells from high glucose-induced oxidative stress and apoptosis: effect on p53 and GRP75 localization. Neurotox Res 25:110–123
59. Kanthasamy K, Gordon R, Jin H, Anantharam V, Ali S, Kanthasamy AG, Kanthasamy A (2011) Neuroprotective effect of resveratrol against methamphetamine-induced dopaminergic apoptotic cell death in a cell culture model of neurotoxicity. Curr Neuropharmacol 9:49–53
60. Bureau G, Longpre F, Martinoli MG (2008) Resveratrol and quercetin, two natural polyphenols, reduce apoptotic neuronal cell death induced by neuroinflammation. J Neurosci Res 86:403–410
61. Jang JH, Surh YJ (2003) Protective effect of resveratrol on beta-amyloid-induced oxidative PC12 cell death. Free Radic Biol Med 34:1100–1110
62. Hirsch EC, Hunot S (2009) Neuroinflammation in Parkinson’s disease: a target for neuroprotection? Lancet Neurol 8:382–397
63. McGeer PL, Itagaki S, Boyes BE, McGeer EG (1988) Reactive microglia are positive for HLA-DR in the substantia nigra of Parkinson’s disease and Alzheimer’s disease brain. Neurology 38:1285–1291
64. Candelario-Jalil E, de Oliveira ACP, Gräf S, Bhatia HS, Hüll M, Muñoz E, Fiebich BL (2007) Resveratrol potently reduces prostaglandin E2 production and free radical formation in lipopolysaccharide-activated primary rat microglia. J Neuroinflammation 4:25
65. Sawada M, Imamura K, Nagatsu T (2006) Role of cytokines in inflammatory process in Parkinson’s disease. J Neural Transm 70:373–381
66. Zong Y, Sun L, Liu B, Deng YS, Zhan D, Chen YL, He Y, Jing L, Zhang ZJ, Sun J, Lu D (2012) Resveratrol inhibits LPS-induced MAPKs activation via activation of the phosphatidylinositol 3-kinase pathway in murine RAW 264.7 macrophage cells. PLoS One 7:e44107
67. Wendeburg L, de Oliveira ACP, Bhatia HS, Candelario-Jalil E, Fiebich BL (2009) Resveratrol inhibits prostaglandin formation in IL-1 β-stimulated SK-N-SH neuronal cells. J Neuroinflammation 6:26
68. Mizushima N, Komatsu M (2011) Autophagy: renovation of cells and tissues. Cell 147:728–741
69. Pallauf K, Rimbach G (2013) Autophagy, polyphenols and healthy ageing. Ageing Res Rev 12:237–252
70. Yao H, Zhao D, Khan SH, Yang L (2013) Role of autophagy in prion protein- induced neurodegenerative diseases. Acta Biochim Biophys Sin 45:494–502
71. Mauthe M, Jacob A, Freiberger S, Hentschel K, Stierhof YD, Codogno P, Cezanne TP (2011) Resveratrol-mediated autophagy requires WIPI-1-regulated LC3 lipidation in the absence of induced phagophore formation. Autophagy 7:1448–1461
72. Pallàs M, Casadesús G, Smith MA, Coto-Montes A, Pelegri C, Vilaplana J, Camins A (2009) Resveratrol and neurodegenerative diseases: activation of SIRT1 as the potential pathway towards neuroprotection. Curr Neurovasc Res 6:70–81
73. Sun AY, Wang Q, Simonyi A (2011) Sun GY (2011) Botanical phenolics and neurodegeneration. In: Benzie IFF, Wachtel-Galor S (eds) Herbal medicine: biomolecular and clinical aspects, 2nd edn. CRC Press, Boca Raton
74. Marchal J, Pifferi F, Aujard F (2013) Resveratrol in mammals: effects on aging biomarkers, age-related diseases, and life span. Ann N Y Acad Sci 1290:67–73
75. Vang O, Ahmad N, Baile CA, Baur JA, Brown K, Csiszar A, Das DK, Delmas D, Gottfried C, Lin HY, Ma QY, Mukhopadhyay P, Nalini N, Pezzuto JM, Richard T, Shukla Y, Surh YJ, Szekeres T, Szkudelski T, Walle T, Wu JM (2011) What is new for an old molecule? Systematic review and recommendations on the use of resveratrol. PLoS One 6:e19881
76. Pandey KB, Rizvi SI (2014) Role of resveratrol in regulation of membrane transporters and integrity of human erythrocytes. Biochem Biophys Res Commun 453:521–526
77. Tiwari MN, Agarwal S, Bhatnagar P, Singhal NK, Tiwari SK, Kumar P, Chauhan LK, Patel DK, Chaturvedi RK, Singh MP, Gupta KC (2013) Nicotine-encapsulated poly(lactic-co-glycolic) acid nanoparticles improve neuroprotective efficacy against MPTP-induced parkinsonism. Free Radic Biol Med 65:704–718
78. Singhal NK, Agarwal S, Bhatnagar S, Tiwari MN, Tiwari SK, Srivastava G, Kumar P, Seth B, Patel DK, Chaturvedi RK, Singh MP, Gupta KC (2015) Mechanism of nanotization-mediated improvement in the efficacy of caffeine against 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-induced Parkinsonism. J Biomed Nanotechnol. doi:10.1166/jbn.2015.2107
79. Wang S, Su R, Nie S, Sun M, Zhang J, Wu D, Moustaid-Moussa N (2014) Application of nanotechnology in improving bioavailability and bioactivity of diet-derived phytochemicals. J Nutr Biochem 25:363–376