Neuroprotective and metabolic effects of resveratrol: Therapeutic implications for Huntington's disease and other neurodegenerative disorders

Experimental Neurology

Volumn 232, Issue 1, 2011, Pages 1-6

  Pasinetti, Giulio Maria ^a   Wang, Jun ^a   Marambaud, Philippe ^a   Ferruzzi, Mario ^a   Gregor, Paul ^a   Knable, Lindsay Alexis ^a   Ho, Lap ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FISETIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; NUCLEAR RESPIRATORY FACTOR 1; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; RESVERATROL; SIRTUIN 1; SRT 501; UNCLASSIFIED DRUG; UNCOUPLING PROTEIN 1;

ALZHEIMER DISEASE; BRAIN ATROPHY; CALORIC RESTRICTION; COGNITION; COLORECTAL CANCER; DEGENERATIVE DISEASE; DEHYDRATION; DIARRHEA; DIET SUPPLEMENTATION; DOWN REGULATION; DRUG BIOAVAILABILITY; DRUG EFFICACY; DRUG METABOLISM; DRUG TARGETING; DRUG TOLERABILITY; DYSLIPIDEMIA; ENZYME ACTIVATION; ENZYME REGULATION; FRIEDREICH ATAXIA; GLYCEMIC CONTROL; GRAPE JUICE; HUMAN; HUNTINGTON CHOREA; INFLAMMATORY DISEASE; MEMORY CONSOLIDATION; METABOLIC SYNDROME X; MOTOR PERFORMANCE; MULTIPLE MYELOMA; NAUSEA AND VOMITING; NERVE DEGENERATION; NEUROPROTECTION; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; NOTE; OBESITY; OUTCOME ASSESSMENT; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SURVIVAL RATE; TRANSGENIC MOUSE; TRAUMATIC BRAIN INJURY; WEIGHT REDUCTION;

ANIMALS; DISEASE MODELS, ANIMAL; HUNTINGTON DISEASE; STILBENES;

EID: 80053937926     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2011.08.014     Document Type: Note

References (65)

1. Abd El-Mohsen M., Bayele H., Kuhnle G., Gibson G., Debnam E., Kaila Srai S., Rice-Evans C., Spencer J.P. Distribution of [3H]trans-resveratrol in rat tissues following oral administration. Br. J. Nutr. 2006, 96:62-70.
2. Baur J.A., Sinclair D.A. Therapeutic potential of resveratrol: the in vivo evidence. Nat. Rev. Drug Discov. 2006, 5:493-506.
3. Baur J.A., Pearson K.J., Price N.L., Jamieson H.A., Lerin C., Kalra A., Prabhu V.V., Allard J.S., Lopez-Lluch G., Lewis K., Pistell P.J., Poosala S., Becker K.G., Boss O., Gwinn D., Wang M., Ramaswamy S., Fishbein K.W., Spencer R.G., Lakatta E.G., Le Couteur D., Shaw R.J., Navas P., Puigserver P., Ingram D.K., de Cabo R., Sinclair D.A. Resveratrol improves health and survival of mice on a high-calorie diet. Nature 2006, 444:337-342.
4. Beher D., Wu J., Cumine S., Kim K.W., Lu S.C., Atangan L., Wang M. Resveratrol is not a direct activator of SIRT1 enzyme activity. Chem. Biol. Drug Des. 2009, 74(6):619-624. Epub 2009 Oct 20.
5. Borra M.T., Smith B.C., Denu J.M. Mechanism of human SIRT1 activation by resveratrol. J. Biol. Chem. 2005, 280:17187-17195.
6. Canto C., Auwerx J. PGC-1alpha, SIRT1 and AMPK, an energy sensing network that controls energy expenditure. Curr. Opin. Lipidol. 2009, 20:98-105.
7. Canto C., Auwerx J. AMP-activated protein kinase and its downstream transcriptional pathways. Cell. Mol. Life Sci. 2010, 67(20):3407-3423.
8. Canto C., Gerhart-Hines Z., Feige J.N., Lagouge M., Noriega L., Milne J.C., Elliott P.J., Puigserver P., Auwerx J. AMPK regulates energy expenditure by modulating NAD+ metabolism and SIRT1 activity. Nature 2009, 458:1056-1060.
9. Carling D., Sanders M.J., Woods A. The regulation of AMP-activated protein kinase by upstream kinases. Int. J. Obes. (Lond.) 2008, 32(Suppl. 4):S55-S59.
10. Chaturvedi R.K., Adhihetty P., Shukla S., Hennessy T., Calingasan N., Yang L., Starkov A., Kiaei M., Cannella M., Sassone J., Ciammola A., Squitieri F., Beal M.F. Impaired PGC-1α function in muscle in Huntington's disease. Hum. Mol. Genet. 2009, 18(16):3048-3065.
11. Chaturvedi R.K., Calingasan N.Y., Yang L., Hennessey T., Johri A., Beal M.F. Impairment of PGC-1alpha expression, neuropathology and hepatic steatosis in a transgenic mouse model of Huntington's disease following chronic energy deprivation. Hum. Mol. Genet. 2010, 19:3190-3205.
12. Citron M. Alzheimer's disease: strategies for disease modification. Nat. Rev. Drug Discov. 2010, 9:387-398.
13. Dasgupta B., Milbrandt J. Resveratrol stimulates AMP kinase activity in neurons. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:7217-7222.
14. Davies S.W., Turmaine M., Cozens B.A., DiFiglia M., Sharp A.H., Ross C.A., Scherzinger E., Wanker E.E., Mangiarini L., Bates G.P. Formation of neuronal intranuclear inclusions underlies the neurological dysfunction in mice transgenic for the HD mutation. Cell 2007, 90(3):537-548.
15. DiFiglia M., Sapp E., Chase K.O., Davies S.W., Bates G.P., Vonsattel J.P., Aronin N. Aggregation of huntingtin in neuronal intranuclear inclusions and dystrophic neuritis in brain. Science 1997, 277(5334):1990-1993.
16. Donmez G., Wang D., Cohen D.E., Guarente L. SIRT1 suppresses beta-amyloid production by activating the alpha-secretase gene ADAM10. Cell 2010, 142:320-332.
17. Duff K., Paulsen J.S., Beglinger L.J., Langbehn D.R., Stout J.C. Psychiatric symptoms in Huntington's disease before diagnosis: the predict-HD study. Biol. Psychiatry 2007, 62(12):1341-1346. Predict-HD Investigators of the Huntington Study Group.
18. Finkel T., Deng C.X., Mostoslavsky R. Recent progress in the biology and physiology of sirtuins. Nature 2009, 460:587-591.
19. Fogarty S., Hawley S.A., Green K.A., Saner N., Mustard K.J., Hardie D.G. Calmodulin-dependent protein kinase kinase-beta activates AMPK without forming a stable complex: synergistic effects of Ca2+ and AMP. Biochem. J. 2010, 426:109-118.
20. Greer E.L., Brunet A. Different dietary restriction regimens extend lifespan by both independent and overlapping genetic pathways in C. elegans. Aging Cell 2009, 8:113-127.
21. Hardie D.G. AMP-activated/SNF1 protein kinases: conserved guardians of cellular energy. Nat. Rev. Mol. Cell Biol. 2007, 8:774-785.
22. Hawley S.A., Ross F.A., Chevtzoff C., Green K.A., Evans A., Fogarty S., Towler M.C., Brown L.J., Ogunbayo O.A., Evans A.M., Hardie D.G. Use of cells expressing gamma subunit variants to identify diverse mechanisms of AMPK activation. Cell Metab. 2010, 11:554-565.
23. Ho L., Pasinetti G.M. Polyphenolic compounds for treating neurodegenerative disorders involving protein misfolding. Expert Rev. Proteomics 2010, 7:579-589.
24. Ho L., Chen L.H., Wang J., Zhao W., Talcott S.T., Ono K., Teplow D., Humala N., Cheng A., Percival S.S., Ferruzzi M., Janle E., Dickstein D.L., Pasinetti G.M. Heterogeneity in red wine polyphenolic contents differentially influences Alzheimer's disease-type neuropathology and cognitive deterioration. J. Alzheimers Dis. 2009, 16(1):59-72.
25. Ho D.J., Calingasan N.Y., Wille E., Dumont M., Beal M.F. Resveratrol protects against peripheral deficits in a mouse model of Huntington's disease. Exp. Neurol. 2010, 225(1):74-84.
26. Howells L.M., Berry D.P., Elliott P.J., Jacobson E.W., Hoffmann E., Hegarty B., Brown K., Steward W., Gescher A.J. Phase I randomized, double-blind pilot study of micronized resveratrol (SRT501) in patients with hepatic metastases -- safety, pharmacokinetics, and pharmacodynamics. Cancer Prev. Res. (Phila) 2011, 4(9):1419-1425.
27. Howitz K.T., Bitterman K.J., Cohen H.Y., Lamming D.W., Lavu S., Wood J.G., Zipkin R.E., Chung P., Kisielewski A., Zhang L.L., Scherer B., Sinclair D.A. Small molecule activators of sirtuins extend Saccharomyces cerevisiae lifespan. Nature 2003, 425:191-196.
28. Johnson S.A., Stout J.C., Solomon A.C., Langbehn D.R., Aylward E.H., Cruce C.B., Ross C.A., Nance M., Kayson E., Julian-Baros E., Hayden M.R., Kieburtz K., Guttman M., Oakes D., Shoulson I., Beglinger L., Duff K., Penziner E., Paulsen J.S. Beyond digust: impaired recognition of negative emotions prior to diagnosis in Huntington's disease. Brain 2007, 130(Pt 7):1732-1744. Predict-HD Investigators of the Huntington Study Group.
29. Karuppagounder S.S., Pinto J.T., Xu H., Chen H.L., Beal M.F., Gibson G.E. Dietary supplementation with resveratrol reduces plaque pathology in a transgenic model of Alzheimer's disease. Neurochem. Int. 2009, 54:111-118.
30. Krikorian R., Nash T.A., Shidler M.D., Shukitt-Hale B., Joseph J.A. Concord grape juice supplementation improves memory function in older adults with mild cognitive impairment. Br. J. Nutr. 2010, 103(5):730-734.
31. Kumar P., Padi S.S., Naidu P.S., Kumar A. Effect of resveratrol on 3-nitropropionic acid-induced biochemical and behavioural changes: possible neuroprotective mechanisms. Behav. Pharmacol. 2006, 17:485-492.
32. Lagouge M., Argmann C., Gerhart-Hines Z., Meziane H., Lerin C., Daussin F., Messadeq N., Milne J., Lambert P., Elliott P., Geny B., Laakso M., Puigserver P., Auwerx J. Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1alpha. Cell 2006, 127:1109-1122.
33. Li Y., Yokota T., Gama V., Yoshida T., Gomez J.A., Ishikawa K., Sasaguri H., Cohen H.Y., Sinclair D.A., Mizusawa H., Matsuyama S. Bax-inhibiting peptide protects cells from polyglutamine toxicity caused by Ku70 acetylation. Cell Death Differ. 2007, 14:2058-2067.
34. MacDonald M.E., Novelletto A., Lin C., Tagle D., Barnes G., Bates G., Taylor S., Allitto B., Altherr M., Myers R., Lehrach H., Collins F.S., Wasmuth J.J., Frontali M., Gusella J.F. The Huntington's disease candidate region exhibits many different haplotypes. Nat. Genet. 1992, 1(2):99-103.
35. Maher P., Dargusch R., Bodai L., Gerard P.E., Purcell J.M., Marsh J.L. ERK activation by the polyphenols fisetin and resveratrol provides neuroprotection in multiple models of Huntington's disease. Hum. Mol. Genet. 2011, 20(2):261-270. Jan 15.
36. Marambaud P., Zhao H., Davies P. Resveratrol promotes clearance of Alzheimer's disease amyloid-beta peptides. J. Biol. Chem. 2005, 280:37377-37382.
37. McGill J.K., Beal M.F. PGC-1alpha, a new therapeutic target in Huntington's disease?. Cell 2006, 127:465-468.
38. Orgogozo J.M., Dartigues J.F., Lafont S., Letenneur L., Commenges D., Salamon R., Renaud S., Breteler M.B. Wine consumption and dementia in the elderly: a prospective community study in the Bordeaux area. Rev. Neurol. (Paris) 1997, 153(3):185-192.
39. Pacholec M., Bleasdale J.E., Chrunyk B., Cunningham D., Flynn D., Garofalo R.S., Griffith D., Griffor M., Loulakis P., Pabst B., Qiu X., Stockman B., Thanabal V., Varghese A., Ward J., Withka J., Ahn K. SRT1720, SRT2183, SRT1460, and resveratrol are not direct activators of SIRT1. J. Biol. Chem. 2010, 285:8340-8351.
40. Parker J.A., Arango M., Abderrahmane S., Lambert E., Tourette C., Catoire H., Neri C. Resveratrol rescues mutant polyglutamine cytotoxicity in nematode and mammalian neurons. Nat. Genet. 2005, 37:349-350.
41. Pearson K.J., Baur J.A., Lewis K.N., Peshkin L., Price N.L., Labinskyy N., Swindell W.R., Kamara D., Minor R.K., Perez E., Jamieson H.A., Zhang Y., Dunn S.R., Sharma K., Pleshko N., Woollett L.A., Csiszar A., Ikeno Y., Le Couteur D., Elliott P.J., Becker K.G., Navas P., Ingram D.K., Wolf N.S., Ungvari Z., Sinclair D.A., de Cabo R. Resveratrol delays age-related deterioration and mimics transcriptional aspects of dietary restriction without extending life span. Cell Metab. 2008, 8:157-168.
42. Penney J.B., Young A.B., Shoulson I., Starosta-Rubenstein S., Snodgrass S.R., Sanchez-Ramos J., Ramos-Arroyo M., Gomez F., Penchaszadeh G., Alvir J., et al. Huntington's disease in Venezuela: 7years of follow-up on symptomatic and asymptomatic individuals. Mov. Disord. 1990, 5(2):93-99.
43. Pfleger C.M., Wang J., Friedman L., Vittorino R., Conley L.M., Ho L., Fivecoat H.C., Pasinetti G.M. Grape-seed polyphenolic extract improves the eye phenotype in a Drosophila model of tauopathy. Int. J. Alzheimers Dis. 2010, 2010. Aug 24, pii: 576357.
44. Qin W., Chachich M., Lane M., Roth G., Bryant M., de Cabo R., Ottinger M.A., Mattison J., Ingram D., Gandy S., Pasinetti G.M. Calorie restriction attenuates Alzheimer's disease type brain amyloidosis in Squirrel monkeys (Saimiri sciureus). J. Alzheimers Dis. 2006, 10:417-422.
45. Qin W., Yang T., Ho L., Zhao Z., Wang J., Chen L., Zhao W., Thiyagarajan M., MacGrogan D., Rodgers J.T., Puigserver P., Sadoshima J., Deng H., Pedrini S., Gandy S., Sauve A.A., Pasinetti G.M. Neuronal SIRT1 activation as a novel mechanism underlying the prevention of Alzheimer disease amyloid neuropathology by calorie restriction. J. Biol. Chem. 2006, 281:21745-21754.
46. Rocha-Gonzalez H.I., Ambriz-Tututi M., Granados-Soto V. Resveratrol: a natural compound with pharmacological potential in neurodegenerative diseases. CNS Neurosci. Ther. 2008, 14:234-247.
47. Ruderman N.B., Xu X.J., Nelson L., Cacicedo J.M., Saha A.K., Lan F., Ido Y. AMPK and SIRT1: a long-standing partnership?. Am. J. Physiol. Endocrinol. Metab. 2010, 298:E751-E760.
48. Selkoe D.J. Alzheimer's disease: genes, proteins, and therapy. Physiol. Rev. 2001, 81:741-766.
49. Solomon A.C., Stout J.C., Johnson S.A., Langbehn D.R., Aylward E.H., Brandt J., Ross C.A., Beglinger L., Hayden M.R., Kieburtz K., Kayson E., Julian-Baros E., Duff K., Guttman M., Nance M., Oakes D., Shoulson I., Penziner E., Paulsen J.S. Verbal episodic memory declines prior to diagnosis in Huntington's disease. Neuropsychologia 2007, 45(8):1767-1776. Predict-HD investigators of the Huntington Study Group.
50. Trottier Y., Lutz Y., Stevanin G., Imbert G., Devys D., Cancel G., Saudou F., Weber C., David G., Tora L., Agid Y., Brice A., Mandel J.L. Polyglutamine expansion as a pathological epitope in Huntington's disease and four dominant cerebellar ataxias. Nature 1995, 378(6555):403-406.
51. Um J.H., Park S.J., Kang H., Yang S., Foretz M., McBurney M.W., Kim M.K., Viollet B., Chung J.H. AMPK-deficient mice are resistant to the metabolic effects of resveratrol. Diabetes 2009, 59(3):554-563.
52. Vingtdeux V., Dreses-Werringloer U., Zhao H., Davies P., Marambaud P. Therapeutic potential of resveratrol in Alzheimer's disease. BMC Neurosci. 2008, 9(Suppl. 2):S6.
53. Vingtdeux V., Giliberto L., Zhao H., Chandakkar P., Wu Q., Simon J.E., Janle E.M., Lobo J., Ferruzzi M.G., Davies P., Marambaud P. AMP-activated protein kinase signaling activation by resveratrol modulates amyloid-beta peptide metabolism. J. Biol. Chem. 2010, 285:9100-9113.
54. Viollet B., Lantier L., Devin-Leclerc J., Hebrard S., Amouyal C., Mounier R., Foretz M., Andreelli F. Targeting the AMPK pathway for the treatment of type 2 diabetes. Front. Biosci. 2009, 14:3380-3400.
55. Vonsattel J.P., Myers R.H., Stevens T.J., Ferrante R.J., Bird E.D., Richardson E.P. Neuropathological classification of Huntington's disease. J. Neuropathol. Exp. Neurol. 1985, 44(6):559-577.
56. Wale T. Bioavailability of resveratrol. Ann. N. Y. Acad. Sci. 2011, 1215:9-15.
57. Walker F.O. Huntington's disease. Semin. Neurol. 2007, 27(2):143-150.
58. Wang J., Ho L., Qin W., Rocher A.B., Seror I., Humala N., Maniar K., Dolios G., Wang R., Hof P.R., Pasinetti G.M. Caloric restriction attenuates beta-amyloid neuropathology in a mouse model of Alzheimer's disease. FASEB J. 2005, 19(6):659-661.
59. Wang J., Ho L., Zhao Z., Seror I., Humala N., Dickstein D.L., Thiyagarajan M., Percival S.S., Talcott S.T., Pasinetti G.M. Moderate consumption of Cabernet Sauvignon attenuates Abeta neuropathology in a mouse model of Alzheimer's disease. FASEB J. 2006, 20(13):2313-2320.
60. Wang J., Ho L., Zhao W., Ono K., Rosensweig C., Chen L., Humala N., Teplow D.B., Pasinetti G.M. Grape-derived polyphenolics prevent Abeta oligomerization and attenuate cognitive deterioration in a mouse model of Alzheimer's disease. J. Neurosci. 2008, 28(25):6388-6392. Jun 18.
61. Wang J., Fivecoat H., Ho L., Pan Y., Ling E., Pasinetti G.M. The role of Sirt1: at the crossroad between promotion of longevity and protection against Alzheimer's disease neuropathology. Biochim. Biophys. Acta 2010, 1804:1690-1694.
62. Wang J., Pfleger C., Friedman L., Vittorino R., Zhao W., Qian X.J., Conley L., Ho L., Pasinetti G.M. Potential application of grape derived polyphenols in Huntington's disease. Transl. Neurosci. 2010, 1(2):95-100.
63. Wenzel E., Soldo T., Erbersdobler H., Somoza V. Bioactivity and metabolism of trans-resveratrol orally administered to Wistar rats. Mol. Nutr. Food Res. 2005, 49(5):482-494. May.
64. Weydt P., Pineda V.V., Torrence A.E., Libby R.T., Satterfield T.F., Lazarowski E.R., Gilbert M.L., Morton G.J., Bammler T.K., Strand A.D., Cui L., Beyer R.P., Easley C.N., Smith A.C., Krainc D., Luquet S., Sweet I.R., Schwartz M.W., La Spada A.R. Thermoregulatory and metabolic defects in Huntington's disease transgenic mice implicate PGC-1? in Huntington's disease neurodegeneration. Cell Metab. 2006, 5:349-362.
65. Yamamoto A., Lucas J.J., Hen R. Reversal of neuropathology and motor dysfunction in a conditional model of Huntington's disease. Cell 2000, 101(1):57-66.