Neuroprotective role of trans-resveratrol in a murine model of familial alzheimer's disease

Journal of Alzheimer's Disease

Volumn 42, Issue 4, 2014, Pages 1209-1220

  Porquet, David ^a,e   Griñán Ferré, Christian ^a   Ferrer, Isidre ^d,e   Camins, Antoni ^a,e   Sanfeliu, Coral ^b   Del Valle, Jaume ^a,c,e   Pallàs, Mercè ^a,e  

^a UNIVERSITY OF BARCELONA   (Spain)

^b INSTITUT D INVESTIGACIONS BIOMÈDIQUES AUGUST PI I SUNYER IDIBAPS   (Spain)

^c UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^d HOSPITAL UNIVERSITARI DE BELLVITGE   (Spain)

^e CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED SOBRE ENFERMEDADES NEURODEGENERATIVAS CIBERNED   (Spain)

Author keywords

AMPK; inflammation; mitochondria; resveratrol; sirtuin 1

Indexed keywords

ADAM10 ENDOPEPTIDASE; AMYLOID; BETA SECRETASE; CATALASE; CYTOCHROME C OXIDASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; INTERLEUKIN 1BETA; RESVERATROL; RNA; SIRTUIN 1; SUPEROXIDE DISMUTASE; TUMOR NECROSIS FACTOR; AMYLOID PRECURSOR PROTEIN; APP PROTEIN, HUMAN; NEUROPROTECTIVE AGENT; PRESENILIN 1; PSEN1 PROTEIN, HUMAN; STILBENE DERIVATIVE;

ALZHEIMER DISEASE; AMNESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG EFFECT; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; GENE EXPRESSION; HIPPOCAMPUS; MALE; MOUSE; NEUROPROTECTION; NONHUMAN; NOVEL OBJECT RECOGNITION TEST; OXIDATIVE STRESS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; RNA ISOLATION; SHORT TERM MEMORY; UPREGULATION; WESTERN BLOTTING; ANIMAL; BRAIN; DISEASE MODEL; DRUG EFFECTS; GENETICS; MEMORY DISORDERS; METABOLISM; ORAL DRUG ADMINISTRATION; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; PLAQUE, AMYLOID; PSYCHOLOGY; RECOGNITION; TRANSGENIC MOUSE;

ADMINISTRATION, ORAL; ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; BRAIN; DISEASE MODELS, ANIMAL; MALE; MEMORY DISORDERS; MEMORY, SHORT-TERM; MICE, TRANSGENIC; NEUROPROTECTIVE AGENTS; PLAQUE, AMYLOID; PRESENILIN-1; RECOGNITION (PSYCHOLOGY); STILBENES;

EID: 84908000931     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-140444     Document Type: Article

References (50)

1. Donmez G, Wang D, Cohen DE, Guarente L (2010) SIRT1 suppresses beta-amyloid production by activating the alpha-secretase gene ADAM10. Cell 142, 320-332.
2. Lin MT, Beal MF (2006) Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 443, 787-795.
3. Maurer I, Zierz S, Möller HJ (2000) A selective defect of cytochrome c oxidase is present in brain of Alzheimer disease patients. Neurobiol Aging 21, 455-462.
4. Nunomura A, Castellani RJ, Zhu X, Moreira PI, Perry G, Smith MA (2006) Involvement of oxidative stress in Alzheimer disease. J Neuropathol Exp Neurol 65, 631-641.
5. Sultana R, Mecocci P, Mangialasche F, Cecchetti R, Baglioni M, Butterfield DA (2011) Increased protein and lipid oxida-tive damage in mitochondria isolated from lymphocytes from patients with Alzheimer's disease: Insights into the role of oxidative stress in Alzheimer's disease and initial investigations into a potential biomarker for this. J Alzheimers Dis 24, 77-84.
6. Reddy PH, Beal MF (2008) Amyloid beta, mitochondrial dysfunction and synaptic damage: Implications for cognitive decline in aging and Alzheimer's disease. Trends Mol Med 14, 45-53.
7. Beaudoin M-S, Snook LA, Arkell AM, Simpson JA, Hol-loway GP, Wright DC (2013) Resveratrol supplementation improves white adipose tissue function in a depot-specific mannerinZucker diabetic fatty rats. Am J Physiol Regul Integr Comp Physiol 305, 542-551.
8. Estrela JM, Ortega A, Mena S, Rodriguez ML, Asensi M (2013) Pterostilbene: Biomedical applications. Crit Rev Clin Lab Sci 50, 65-78.
9. Jayasena T, Poljak A, Smythe G, Braidy N, Münch G, Sachdev P (2013) The role of polyphenols in the modulation of sirtuins and other pathways involved in Alzheimer's disease. Ageing Res Rev 12, 867-883.
10. Um J-H, Park S-J, Kang H, Yang S, Foretz M, McBurney MW, Kim MK, Viollet B, Chung JH (2010) AMP-activated protein kinase-deficient mice are resistant to the metabolic effects of resveratrol. Diabetes 59, 554-563.
11. De Lange P, Farina P, Moreno M, Ragni M, Lombardi A, Silvestri E, Burrone L, Lanni A, Goglia F (2006) Sequential changes in the signal transduction responses of skeletal muscle following food deprivation. FASEB J 20, 2579-2581.
12. Garcia-Alloza M, Robbins EM, Zhang-Nunes SX, Purcell SM, Betensky RA, Raju S, Prada C, Greenberg SM, Bacskai BJ, Frosch MP (2006) Characterization ofamyloid deposition in the APPswe/PS1dE9 mouse model of Alzheimer disease. Neurobiol Dis 24, 516-524.
13. Huang HJ, Liang KC, Ke HC, Chang YY, Hsieh-Li HM (2011) Long-term social isolation exacerbates the impairment of spatial working memory in APP/PS1 transgenic mice. Brain Res 1371, 150-160.
14. Minkeviciene R, Ihalainen J, Malm T, Matilainen O, Keksa-Goldsteine V, Goldsteins G, Iivonen H, Leguit N, Glennon J, Koistinaho J, Banerjee P, Tanila HJ (2008) Age-related decrease in stimulated glutamate release and vesicular gluta-mate transporters in APP/PS1 transgenic and wild-type mice. Neurochem 105, 584-594.
15. Savonenko A, Xu GM, Melnikova T, Morton JL, Gonzales V, Wong MP, Price DL, Tang F, Markowska AL, Borchelt DR (2005) Episodic-like memory deficits in the APPswe/PS1dE9 mouse model of Alzheimer's disease: Relationships to beta-amyloid deposition and neurotransmitter abnormalities. Neurobiol Dis 18, 602-617.
16. Webster SJ, Bachstetter AD, Van Eldik LJ (2013) Comprehensive behavioral characterization of an APP/PS-1 double knock-in mouse model of Alzheimer's disease. Alzheimers Res Ther 5, 28.
17. Torres M, Jimenez S, Sanchez-Varo R, Navarro V, Trujillo-Estrada L, Sanchez-Mejias E, Carmona I, Davila JC, Vizuete M, Gutierrez A, Vitorica J (2012) Defective lysosomal proteolysis and axonal transport are early pathogenic events that worsen with age leading to increased APP metabolism and synaptic Abetain transgenic APP/PS1 hippocampus. Mol Neurodegener 7, 59.
18. Reinhardt S, Schuck F, Grosgen S, Riemenschneider M, Hartmann T, Postina R, Grimm M, Endres K (2014) Unfolded protein response signaling by transcription factor XBP-1 regulates ADAM10 and is affected in Alzheimer's disease. FASEB J 28, 978-997.
19. Perez-Gonzalez R, Alvira-Botero MX, Robayo O, Antequera D, Garzon M, Martín-Moreno AM, Brera B, de Ceballos ML, Carro E (2014) Leptin gene therapy attenuates neuronal damages evoked by amyloidfj and rescues memory deficits in APP/PS1mice. Gene Ther 21, 298-308.
20. Yan JJ, Jung JS, Kim TK, Hasan A, Hong CW, Nam JS, Song DK (2013) Protective effects of ferulic acid in amyloid precursor protein plus presenilin-1 transgenic mouse model of Alzheimer disease. Biol Pharm Bull 36, 140-143.
21. Wang TH, Jiang Y, Xiao LP (2013) Expression of amyloid beta-protein in bone tissue of APP/PS1 transgenic mouse. Zhonghua Yi Xue Za Zhi 93, 65-68.
22. Porquet D, Casadesus G, Bayod S, Vicente A, Canudas AM, Vilaplana J, Pelegŕi C, Sanfeliu C, Camins A, Pallas M, del Valle J (2013) Dietary resveratrol prevents Alzheimer's markers and increases life span in SAMP8. Age (Dordr) 35, 1851-1865.
23. Puighermanal E, Marsicano G, Busquets-Garcia A, Lutz B, Maldonado R, Ozaita A (2009) Cannabinoid modulation of hippocampal long-term memory is mediated by mTOR signaling. Nat Neurosci 12, 1152-1158.
24. Aso E, Lomoio S, Lopez-Gonzalez I, Joda L, Carmona M, Fernandez-Yagüe N, Moreno J, Juves S, Pujol A, Pamplona R, Portero-Otin M, Martín V, Diaz M, Ferrer I (2012) Amyloid generation and dysfunctional immuno-proteasome activation with disease progression in animal model of familial Alzheimer's disease. Brain Pathol 22, 636-653.
25. Pallas M, Porquet D, Vicente A, Sanfeliu C (2013) Resveratrol: New avenues for a natural compound in neuroprotection. Curr Pharm Des 19, 6726-6731.
26. Karuppagounder SS, Pinto JT, Xu H, Chen H-L, Beal MF, Gibson GE (2009) Dietary supplementation with resveratrol reduces plaque pathology in a transgenic model of Alzheimer's disease. Neurochem Int 54, 111-118.
27. Keller JN, Hanni KB, Markesbery WR (2000) Impaired pro-teasome function in Alzheimer's disease. J Neurochem 75, 436-439.
28. Lopez Salon M, Morelli L, Castano EM, Soto EF, Pasquini JM (2000) Defective ubiquitination of cerebral proteins in Alzheimer's disease. J Neurosci Res 15, 302-310.
29. Van Tijn P, Dennissen FJA, Gentier RJG, Hobo B, Hermes D, Steinbusch HWM, Van Leeuwen FW, Fischer DF (2012) Mutant ubiquitin decreases amyloid fj plaque formation in a transgenic mouse model of Alzheimer's disease. Neurochem Int 61, 739-748.
30. Marambaud P, Zhao H, Davies P (2005) Resveratrol promotes clearance of Alzheimer's disease amyloid-beta peptides. J Biol Chem 280, 37377-37382.
31. Antunes M, Biala G (2012) The novel object recognition memory: Neurobiology, test procedure, and its modifications. Cogn Process 13, 93-110.
32. Webster SJ, Bachstetter AD, Van Eldik LJ (2013) Comprehensive behavioral characterization of an APP/PS-1 double knock-in mouse model of Alzheimer's disease. Alzheimers Res Ther 5, 28.
33. Lok K, Zhao H, Zhang C, He N, Shen H, Wang Z, Zhao W, Yin M (2013) Effects of accelerated senescence on learning and memory, locomotion and anxiety-like behavior in APP/PS1 mouse model of Alzheimer's disease. J Neurol Sci 335, 145-154.
34. Dasgupta B, Milbrandt J (2007) Resveratrol stimulates AMP kinase activity in neurons. Proc Natl Acad Sci USA 104, 7217-7222.
35. Quincozes-Santos A, Bobermin LD, Tramontina AC, Wartchow KM, Tagliari B, Souza DO, Wyse AT, Goncalves CA (2014) Oxidative stress mediated by NMDA, AMPA/KA channels in acute hippocampal slices: Neuroprotective effect of resveratrol. Toxicol In Vitro 28, 544-551.
36. Son Y, Byun SJ, Pae HO (2013) Involvement of heme oxygenase-1 expression in neuroprotection by piceatannol, a natural analog and a metabolite of resveratrol, against glutamate-mediated oxidative injury in HT22 neuronal cells. Amino Acids 45, 393-401.
37. Serpente M, Bonsi R, Scarpini E, Galimberti D (2014) Innate immune system and inflammation in Alzheimer's disease: From pathogenesis to treatment. Neuroimmunomodulation 21, 79-87.
38. Kim D, Nguyen MD, Dobbin MM, Fischer A, Sananbenesi F, Rodgers JT, Delalle I, Baur JA, Sui G, Armour SM, Puigserver P, Sinclair DA, Tsai LH (2007) SIRT1 deacetylase protects against neurodegeneration in models for Alzheimer's disease and amyotrophic lateral sclerosis. EMBO J 26, 3169-3179.
39. 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 (2006) Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1alpha. Cell 127, 1109-1122.
40. Della-Morte D, Dave KR, DeFazio RA, Bao YC, Raval AP, Perez-Pinzon MA (2009) Resveratrol pretreatment protects rat brain from cerebral ischemic damage via a sirtuin 1-uncoupling protein 2 pathway. Neuroscience 159, 993-1002.
41. Du L-L, Xie J-Z, Cheng X-S, Li X-H, Kong F-L, Jiang X, Ma ZW, Wang JZ, Chen C, Zhou XW (2014) Activation of sirtuin 1 attenuates cerebral ventricular streptozotocin-induced tau hyperphosphorylation and cognitive injuries in rat hippocampi. Age (Dordr) 36, 613-623.
42. Kaeberlein M, McDonagh T, Heltweg B, Hixon J, Westman EA, Caldwell SD, Napper A, Curtis R, DiStefano PS, Fields S, Bedalov A, Kennedy BK (2005) Substrate-specific activation of sirtuins by resveratrol. J Biol Chem 280, 17038-17045.
43. Hwang J-T, Kwak DW, Lin SK, Kim HM, Kim YM, Park OJ (2007) Resveratrol induces apoptosis in chemoresistant cancer cells via modulation of AMPK signaling pathway. Ann N Y Acad Sci 1095, 441-448.
44. Zang M, Xu S, Maitland-Toolan KA, Zuccollo A, Hou X, Jiang B, Wierzbicki M, Verbeuren TJ, Cohen RA (2006) Polyphenols stimulate AMP-activated protein kinase, lower lipids, and inhibit accelerated atherosclerosis in diabetic LDL receptor-deficient mice. Diabetes 55, 2180-2191.
45. Cantó C, Auwerx J (2009) PGC-1alpha, SIRT1 and AMPK, an energy sensing network that controls energy expenditure. Curr Opin Lipidol 20, 98-105.
46. Lan F, Cacicedo JM, Ruderman N, Ido Y (2008) SIRT1 modulation of the acetylation status, cytosolic localization, and activity of LKB1. Possible role in AMP-activated protein kinase activation. J Biol Chem 283, 27628-27635.
47. Duan W (2013) Sirtuins: From metabolic regulation to brain aging. Front Aging Neurosci 5, 36.
48. Hardie DG, Ross FA, Hawley SA (2012) AMPK: A nutrient and energy sensor that maintains energy homeostasis. Nat Rev Mol Cell Biol 13, 251-262.
49. Mancuso R, Del Valle J, Modol L, Martinez A, Granado-Serrano AB, Ramirez-Núñez O, Pallás M, Portero-Otin M, Osta R, Navarro X (2014) Resveratrol improves motoneuron function and extends survival in SOD1 (G93A) ALS mice. Neurotherapeutics 11, 419-432.
50. Wang J, Ho L, Zhao Z, Seror I, Humala N, Dickstein DL, Thiyagarajan M, Percival SS, Talcott ST, Pasinetti GM (2006) Moderate consumption of Cabernet Sauvignon attenuates Abeta neuropathology in a mouse model of Alzheimer's disease. FASEB J 20, 2313-2320.