Resveratrol extends lifespan and preserves glia but not neurons of the Nothobranchius guentheri optic tectum

Experimental Gerontology

Volumn 48, Issue 2, 2013, Pages 202-212

  Genade, T ^a   Lang, D M ^a  

^a UNIVERSITY OF CAPE TOWN   (South Africa)

Author keywords

Ageing; Glia; Neurodegeneration; Neuroprotection; Nothobranchius; Perineuronal nets; Resveratrol

Indexed keywords

GLIAL FIBRILLARY ACIDIC PROTEIN; NERVE CELL ADHESION MOLECULE; RESVERATROL; TENASCIN;

AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN FUNCTION; BRAIN REGION; CELL DENSITY; CELLULAR DISTRIBUTION; COGNITION; CONTROLLED STUDY; DOWN REGULATION; DRUG MECHANISM; DRUG TARGETING; FRESHWATER FISH; GLIA; IMMUNOHISTOCHEMISTRY; LIFE EXTENSION; NERVE DEGENERATION; NEUROFILAMENT; NEUROPROTECTION; NONHUMAN; NOTHOBRANCHIUS FURZERI; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SUPERIOR COLLICULUS;

ANIMALS; BIOLOGICAL MARKERS; CELL SURVIVAL; FISHES; GLIAL FIBRILLARY ACIDIC PROTEIN; IMMUNOHISTOCHEMISTRY; LONGEVITY; NEURAL CELL ADHESION MOLECULES; NEUROGLIA; NEURONS; NEUROPROTECTIVE AGENTS; STILBENES; SUPERIOR COLLICULI; TENASCIN;

NOTHOBRANCHIUS; NOTHOBRANCHIUS FURZERI; NOTHOBRANCHIUS GUENTHERI; VERTEBRATA;

EID: 84872535970     PISSN: 05315565     EISSN: 18736815     Source Type: Journal    
DOI: 10.1016/j.exger.2012.11.013     Document Type: Article

References (74)

1. Aldridge G.M., Podrebarac D.M., Greenough W.T., Weiler I.J. The use of total protein stains as loading controls: an alternative to high-abundance single protein controls in semi-quantitative immunoblotting. J. Neurosci. Methods 2008, 172:250-254. (URL http://www.ncbi.nlm.nih.gov/pubmed/18571732).
2. Anderton B.H. Changes in the aging brain in health and disease. Philos. Trans. R. Soc. Lond. (Biol.) 1997, 352:1781-1792. (URL http://www.ncbi.nlm.nih.gov/pubmed/9460061).
3. Ankerhold R., Leppert C.A., Bastmeyer M., Stuermer C.A.O. E587 antigen is upregulated by goldfish oligodendrocytes after optic nerve lesion and supports retinal axon regeneration. Glia 1998, 23:257-270. (URL http://www.ncbi.nlm.nih.gov/pubmed/9633810).
4. Barger J.L., Kayo T., Vann J.M., Arias E.B., Wang J., Hacker T.A., Wang Y., Raederstorff D., Morrow J.D., Leeuwenburgh C., Allison D.B., Saupe K.W., Cartee G.D., Weindruch R., Prolla T.A. A low dose of dietry resveratrol partially mimics caloric restriction and retards aging parameters in mice. PLoS One 2008, 3:e2264. (URL http://www.ncbi.nlm.nih.gov/pubmed/18523577).
5. 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., Fishnein 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. (URL http://www.ncbi.nlm.nih.gov/pubmed/17086191).
6. Blechingberg J., Holm I.E., Nielsen K.B., Jensen T.H., Jørgensen A.L., Nielsen A.L. Identification and characterization of GFAPkappa, a novel glial fibrillary acidic protein isoform. Glia 2007, 55:497-507. (Apr, URL http://www.ncbi.nlm.nih.gov/pubmed/17203480).
7. Calabrese E.J., Mattson M.P., Calabrese V. Resveratrol commonly displays hormesis: occurence and biomedical significance. Hum. Exp. Toxicol. 2010, 29:980-1015. (URL http://www.ncbi.nlm.nih.gov/pubmed/21115559).
8. Candal E., Anadon R., DeGrip W.J., Rodriguez-Moldes I. Patterns of cell proliferation and cell death in the developing retina and optic tectum of the brown trout. Brain Res. Dev. Brain Res. 2005, 154(1):101-119. (Jan, URL http://www.ncbi.nlm.nih.gov/pubmed/15617760).
9. Carulli D., Rhodes K.E., Brown D.J., Bonnet T.P., Pollack S.J., Oliver K., Strata P., Fawcett J.W. Composition of perineuronal nets in the adult rat cerebellum and the cellular origin of the their components. J. Comp. Neurol. 2006, 494:559-577. (URL http://www.ncbi.nlm.nih.gov/pubmed/16374793).
10. Chen S., Mantei N., Dong L., Schachner M. Prevention of neuronal cell death by neural adhesion molecules L1 and CHL1. J. Neurobiol. 1999, 38:428-439. (Feb, URL http://www.ncbi.nlm.nih.gov/pubmed/10022583).
11. Clarke G., Collins R.A., Leavitt B.R., Andrews D.F., Hayden M.R., Lumsden C.J., McInnes R.R. A one-hit model of cell death in inherited neuronal degenerations. Nature 2000, 406:195-199. (URL http://www.ncbi.nlm.nih.gov/pubmed/10910361).
12. Cumming G., Fidler F., Vaux D.L. Error bars in experimental biology. J. Cell Biol. 2007, 177:7-11. (URL http://www.ncbi.nlm.nih.gov/pubmed/17420288).
13. Damjanac M., Rioux B.A., Barrier L., Pontcharraud R., Anne C., Hugon J., Page G. Fluoro-Jade B staining as useful tool to identify activated microglia and astrocytes in a mouse transgenic model of Alzheimer's disease. Brain Res. 2007, 1128:40-49. (URL http://www.ncbi.nlm.nih.gov/pubmed/17125750).
14. D'Angelo L., de Girolamo P., Cellerino A., Tozzini E.T., Castaldo L., Lucini C. Neurotrophin Trk receptors in the brain of a teleost fish, Nothobranchius furzeri. Microsc. Res. Tech. 2011, 75:81-88. (Jun, URL http://www.ncbi.nlm.nih.gov/pubmed/21678525).
15. di Cicco E., Tozzini E.T., Rossi G., Cellerino A. The short-lived annual fish Nothobranchius furzeri shows a typical teleost aging process reinforced by high incidence of age-dependent neoplasias. Mech. Aging Dev. 2010, 46:249-256. (URL http://www.ncbi.nlm.nih.gov/pubmed/21056099).
16. Easter S.S., Stuermer C.A.O. An evaluation of the hypothesis of shifting terminals in goldfish optic tectum. J. Neurosci. 1984, 4:1052-1063. (URL http://www.ncbi.nlm.nih.gov/pubmed/6325603).
17. Ethell I., Ethell D.W. Matrix metalloproteinases in brain development and remodeling: synaptic functions and targets. J. Neurosci. Res. 2007, 85:2813-2823. (URL http://www.ncbi.nlm.nih.gov/pubmed/17387691).
18. Faissner A., Pyka M., Geissler M., Sobik T., Frischknecht R., Gundelfinger E.D., Seidenbercher C. Contributions of astrocytes to synapse formation and maturation-potential functions of the perisynaptic extracellular matrix. Brain Res. Rev. 2010, 63:26-38. (URL http://www.ncbi.nlm.nih.gov/pubmed/20096729).
19. Galtrey C.M., Kwok J.C., Carulli D., Rhodes K.E., Fawcett J.W. Distribution and synthesis of extracellular matrix proteoglycans, hyaluronan, link proteins and tenascin-R in the rat spinal cord. Eur. J. Neurosci. 2008, 27:1373-1390. (URL http://www.ncbi.nlm.nih.gov/pubmed/18364019).
20. Genade T. Laboratory Manual for Culturing N. furzeri 2005, Nothobranchius information center, (URL http://www.nothobranchius.info).
21. Genade T., Benedetti M., Terzibasi E., Roncaglia P., Valenzano D.R., Cattaneo A., Cellerino A. Annual fishes of the genus Nothobranchius as a model system for aging research. Aging Cell 2005, 4:223-233. (URL http://www.ncbi.nlm.nih.gov/pubmed/16164422).
22. Genade T., Lang D.M. Antibody markers for studying neurodegeneration in the Nothobranchius central nervous system. J. Cytol. Histol. 2011, 2:1000120. (URL http://dx.doi.org/10.4172/2157-7099.1000120).
23. Giordano D.L., Murray M., Cunningham T.J. Naturally occuring neuron death in the optic layers of superior colliculus of the postnatal rat. J. Neurocytol. 1980, 9:603-614. (URL http://www.ncbi.nlm.nih.gov/pubmed/7441305).
24. Hartmann N., Reichwald K., Wittig I., Drose S., Schmeisser S., Luck C., Hahn C., Graf M., Gausmann U., Terzibasi E., Cellerino A., Ristow M., Brandt U., Platzer M., Englert C. Mitochondrial DNA copy number and function decrease with age in the short-lived fish Nothobranchius furzeri. Aging Cell 2011, 10:824-831. (Oct, URL http://www.ncbi.nlm.nih.gov/pubmed/21624037).
25. Hilbig H., Bidmon H.J., Steingrüber S., Reinke H., Dinse H.R. Enriched environmental conditions reverse age-dependent gliosis and losses of neurofilaments and extracellular matrix components but do not alter lipofuscin accumulation in the hindlimb area of the aging rat brain. J. Chem. Neuroanat. 2002, 23. (URL http://www.ncbi.nlm.nih.gov/pubmed/11861126).
26. Huber K., Superti-Furga G. After the grape rush: sirtuins as epigenetic drug targets in neurodegenerative disorders. Bioorg. Med. Chem. 2011, 19:3616-3624. (URL http://www.ncbi.nlm.nih.gov/pubmed/21306906).
27. Jucker M., Ingram D.K. Age-related fibrillar material in mouse brain. Assessing its potential as a biomarker of aging and as a model of human neurodegenerative disease. Ann. N. Y. Acad. Sci. 1994, 719. (URL http://www.ncbi.nlm.nih.gov/pubmed/8010596).
28. Jung M., Pesheva P., Schachner M., Trotter J. Astrocytes and neurons regulate the expression of the neural recognition molecule Janusin by cultured oligodendrocytes. Glia 1993, 9:163-175. (URL http://www.ncbi.nlm.nih.gov/pubmed/8294147).
29. Kamphuis W., Mamber C., Moeton M., Kooijman L., Sluijs J.A., Jansen A.H., Verveer M., de Groot L.R., Smith V.D., Rangarajan S., Rodriguez J.J., Orre M., Hol E.M. GFAP isoforms in adult mouse brain with a focus on neurogenic astrocytes and reactive astrogliosis in mouse models of Alzheimer disease. PLoS One 2012, 7(8):e42823. (URL http://www.ncbi.nlm.nih.gov/pubmed/22912745).
30. Karetko-Sysa M., Skangiel-Kramska J., Nowicka D. Disturbance of perineuronal nets in the perilesional area after thrombosis is not associated with neuronal death. Exp. Neurol. 2011, 231. (URL http://www.ncbi.nlm.nih.gov/pubmed/21683696).
31. Kaur M., Sharma S., Kaur G. Age-related impairments in neuronal plasticity markers and astrocytic GFAP and their reversal by late-onset short term dietary restriction. Biogerontology 2008, 9:441-454. (URL http://www.ncbi.nlm.nih.gov/pubmed/18763049).
32. Kennedy D.O., Wightman E.L., Reay J.L., Lietz G., Okello E.J., Wilde A., Haskell C.F. Effects of resveratrol on cerebral blood flow variables and cognitive performance in humans: a double-blind, placebo-controlled, crossover investigation. Am. J. Clin. Nutr. 2010, 91(6):1590-1597. (Jun, URL http://www.ncbi.nlm.nih.gov/pubmed/20357044).
33. Kim K.-Y., Ju W.-K., Neufeld A.H. Neuronal susceptibility to damage: comparison of the retinas of young, old and old/caloric restricted rats before and after transient ischemia. Neurobiol. Aging 2004, 25:491-500. (URL http://www.ncbi.nlm.nih.gov/pubmed/15013570).
34. Korolainen M.A., Auriola S., Nyman T.A., Alanfuzoff I., Pirttilä T. Proteomic analysis of glial fibrillary acidic protein in Alzheimer's disease and aging brain. Neurobiol. Dis. 2005, 20:858-870. (URL http://www.ncbi.nlm.nih.gov/pubmed/15979880).
35. Lang D.M., Monson-Mayor M., del Mar Romero-Aleman M., Yanes C., Santos E., Pesheva P. Tenascin-R and axon growth promoting molecules are up regulated in the regenerating visual pathway of the lizard (Gallotia galloti). Dev. Neurobiol. 2008, 68:899-916. (URL http://www.ncbi.nlm.nih.gov/pubmed/18361401).
36. Lee V.M., Carden M.J., Schaepfer W.W., Trojanowski J.Q. Monoclonal antibodies distinguish several differentially phosphorylated states of the two largest rat neurofilament subunits (NF-H and NF-M) and demonstrate their existence in the normal nervous system of adult rats. J. Neurosci. 1987, 7:3474-3488. (URL http://www.ncbi.nlm.nih.gov/pubmed/3119789).
37. Li H.L., Wang H.H., Liu S.J., Deng Y.Q., Zhang Y.J., Tian Q., Wang X.C., Chen X.Q., Yang Y., Zhang J.Y., Wang Q., Xu H., Liao F.F., Wang J.-Z. Phosphorylation of tau antagonizes apoptosis by stabilizing β-catenin, a mechanism involved in Alzheimer's neurodegeneration. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:3591-3596. (URL http://www.ncbi.nlm.nih.gov/pubmed/17360687).
38. Liu C., Wang X., Feng W., Li G., Su F., Zhang S. Differential expression of aging biomarkers at different life stages of the annual fish Nothobranchius guentheri. Biogerontology 2012, 13:501-510. (Aug, URL http://www.ncbi.nlm.nih.gov/pubmed/22923174).
39. + consumption by SIRT1 may endanger energetically compromised neurons. Neruomol. Med. 2009, 11:28-42. (URL http://www.ncbi.nlm.nih.gov/pubmed/19288225).
40. Maretzky T., Schulte M., Ludwig A., Rose-John S., Blobel C., Hartmann D., Altevogt P., Saftig P., Reiss K. L1 is sequentially processed by two differently activated metalloproteases and presenilin/γ-secretase and regulates neural cell adhesion, cell migration, and neurite outgrowth. Mol. Cell. Biol. 2005, 25:9040-9053. (URL http://www.ncbi.nlm.nih.gov/pubmed/16199880).
41. Mattison J.A., Roth G.S., Beasley T.M., Tilmont E.M., Handy A.M., Herbert R.L., Longo D.L., Allison D.B., Young J.E., Bryant M., Barnard D., Ward W.F., Qi W., Ingram D.K., de Cabo R. Impact of caloric restriction on health and survival in rhesus monkeys from the NIA study. Nature 2012, 489:318-321. (Epub, URL http://www.ncbi.nlm.nih.gov/pubmed/22932268).
42. Middeldorp J., Hol E.M. GFAP in health and disease. Prog. Neurobiol. 2011, 93:421-443. (URL http://www.ncbi.nlm.nih.gov/pubmed/21219963).
43. Morrison J.H., Hof P.R. Life and death of neurons in the aging brain. Science 1997, 278:412-419. (URL http://www.ncbi.nlm.nih.gov/pubmed/9334292).
44. Müller M., Best J. Ocular dominance plasticity in adult cat visual cortex after transplantation of cultured astrocytes. Nature 1989, 342:427-430. (URL http://www.ncbi.nlm.nih.gov/pubmed/2586611).
45. Murase T., Haramizu S., Ota N., Hase T. Suppression of the aging-associated decline in physical performance by a combination of resveratrol intake and habitual exercise in senescence-accelerated mice. Biogerontology 2009, 10(4):423-434. (Aug, URL http://www.ncbi.nlm.nih.gov/pubmed/18830683).
46. Olabarria M., Noristani H.N., Verkhratsky A., Rodrǵuez J.J. Concomitant astroglial atrophy and astrogliosis in a tripple transgenic animal model of Alzheimer's Disease. Glia 2010, 58:831-838. (URL http://www.ncbi.nlm.nih.gov/pubmed/20140958).
47. Oomen C.A., Farkas E., Roman V., van der Beek E.M., Luiten P.G., Meerlo P. Resveratrol preserves cerebrovascular density and cognitive function in aging mice. Front. Aging Neurosci. 2009, 1:4. (URL http://www.ncbi.nlm.nih.gov/pubmed/20552055).
48. Overall C.M. Molecular determinants of metalloproteinase substrate specificity: matrix metalloproteinase substrate binding domains, modules, and exosites. Mol. Biotechnol. 2002, 22(1):51-86. (Sep, URL http://www.ncbi.nlm.nih.gov/pubmed/12353914).
49. 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., Woolett 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 lifespan. Cell Metab. 2008, 8:157-168. (URL http://www.ncbi.nlm.nih.gov/pubmed/18599363).
50. Pekny M., Nilsson M. Astrocyte activation and reactive gliosis. Glia 2005, 50:427-434. (URL http://www.ncbi.nlm.nih.gov/pubmed/15846805).
51. Qiu G., Liu S., So K.F. Dietary restriction and brain health. Neurosci. Bull. 2010, 26(1):55-65. (Feb, URL http://www.ncbi.nlm.nih.gov/pubmed/20101273).
52. Quincozes-Santos A., Gottfried C. Resveratrol modulates astroglial functions: neuroprotective hypothesis. Ann. N. Y. Acad. Sci. 2011, 1215:72-78. (Jan, URL http://www.ncbi.nlm.nih.gov/pubmed/21261643).
53. Ramassamy C. Emerging role of polyphenolic compounds in the treatment of neurodegenerative disease: a review of their intracellular targets. Eur. J. Pharmacol. 2006, 545:51-64. (URL http://www.ncbi.nlm.nih.gov/pubmed/16904103).
54. Reichwald K., Lauber C., Nanda I., Kirschner J., Hartmann N., Schories S., Gausmann U., Taudien S., Schilhabel M.B., Szafranski K., Glockner G., Schmid M., Cellerino A., Schartl M., Englert C., Platzer M. High tandem repeat content in the genome of the short-lived annual fish Nothobranchius furzeri: a new vertebrate model for aging research. Genome Biol. 2009, 10:R16. (URL http://www.ncbi.nlm.nih.gov/pubmed/19210790).
55. Roelofs R.F., Fischer D.F., Houtman S.H., Sluijs J.A., Van Haren W., Van Leeuwen F.W., Hol E.M. Adult human subventricular, subgranular, and subpial zones contain astrocytes with a specialized intermediate filament cytoskeleton. Glia 2005, 52:289-300. (Dec, URL http://www.ncbi.nlm.nih.gov/pubmed/16001427).
56. Rudrabhatla P., Jaffe H., Pant H.C. Direct evidence of phosphorylated neuronal intermediate filament proteins in neurofibrillary tangles (NFTs): phosphoproteomics of Alzheimer's NFTs. FASEB J. 2011, 25:3896-3905. (URL http://www.ncbi.nlm.nih.gov/pubmed/21828286).
57. Schmid R.S., Maness P.F. L1 and NCAM adhesion molecules as signaling coreceptors in neuronal migration and process outgrowth. Curr. Opin. Neurobiol. 2008, 18:245-250. (URL http://www.ncbi.nlm.nih.gov/pubmed/18760361).
58. Sloane J.A., Hollander W., Rosene D.L., Moss M.B., Kemper T., Abraham C.R. Astrocytic hypertrophy and altered GFAP degradation with age in subcortical white matter of the rhesus monkey. Brain Res. 2000, 862:1-10. (URL http://www.ncbi.nlm.nih.gov/pubmed/10799662).
59. Stanley P. Using ImageJ for Densitometry 2004, Pamela Stanley Lab., (URL http://stanxterm.aecom.yu.edu/Pamela Stanley lab wiki - Using ImageJ.pdf).
60. Streit W.J., Braak H., Xue Q.S., Bechmann I. Dystrophic (senescent) rather than activated microglial cells are associated with tau pathology and likely precede neurodegeneration in Alzheimer's Disease. Acta Neuropathol. 2009, 118:475-485. (URL http://www.ncbi.nlm.nih.gov/pubmed/19513731).
61. Strekova H., Bihmann C., Kleene R., Eggers C., Saffell J., Hemperly J., Weiler C., Müller-Thomsen T., Schachner M. Elevated levels of neuronal recognition molecule L1 in the cerebrospinal fluid of patients with Alzheimer disease and other dementia syndromes. Neurobiol. Aging 2006, 27:1-9. (URL http://www.ncbi.nlm.nih.gov/pubmed/16298234).
62. Syková E. Glial diffusion barriers during aging and pathological states. Prog. Brain Res. 2001, 132:339-363. (URL http://www.ncbi.nlm.nih.gov/pubmed/11545002).
63. Terzibasi E., Lefrancois C., Domenici P., Hartmann N., Graf M., Cellerino A. Effects of dietary restriction on mortality and age-related phenotypes in the short-lived fish Nothobranchius furzeri. Aging Cell 2009, 8:88-99. (URL http://www.ncbi.nlm.nih.gov/pubmed/19302373).
64. Terzibasi E., Valenzano D.R., Benedetti M., Roncaglia P., Cattaneo A., Domenici L., Cellerino A. Large differences in aging phenotype between strains of the short-lived annual fish Nothobranchius furzeri. PLoS One 2008, 3:e3866. (URL http://www.ncbi.nlm.nih.gov/pubmed/19052641).
65. Terzibasi E., Valenzano D.R., Cellerino A. The short-lived fish Nothobranchius furzeri as a new model system for aging studies. Exp. Gerontol. 2007, 42:81-89. (URL http://www.ncbi.nlm.nih.gov/pubmed/17049789).
66. Tozzini E., Baumgart M., Battistoni G., Cellerino A. Adult neurogenesis in the short-lived teleost Nothobranchius furzeri: localization of neurogenic niches, molecular characterization and effects of aging. Aging Cell 2011, 11:241-251. (Dec, URL http://www.ncbi.nlm.nih.gov/pubmed/22171971).
67. Valenzano D.R., Terzibasi E., Genade T., Cattaneo A., Domenici L., Cellerino A. Resveratrol prolongs lifespan and retards the onset of age-related markers in a short-lived vertebrate. Curr. Biol. 2006, 16:296-300. (URL http://www.ncbi.nlm.nih.gov/pubmed/16461283).
68. Wang C., Wheeler C.T., Alberico T., Sun X., Seeberger J., Laslo M., Spangler E., Kern B., de Cabo R., Zou S. The effect of resveratrol on lifespan depends on both gender and dietary nutrient composition in Drosophila melanogaster. Age (Dordr.) 2011, (2011 Nov 16, Electronic publication ahead of print, URL http://www.ncbi.nlm.nih.gov/pubmed/22083438).
69. Wang J., Tung Y.C., Wang Y., Li X.T., Iqbal K., Grundke-Iqbal I. Hyperphosphorylation and accumulation of neurofilament proteins in Alzheimer Disease brain and in okadaic acid-treated SY5Y cells. FEBS Lett. 2001, 507:81-87. (URL http://www.ncbi.nlm.nih.gov/pubmed/11682063).
70. Wright J.W., Harding J.W. Contributions of matrix metalloproteinases to neural plasticity, habituation, associative learning and drug addiction. Neural Plast. 2009, 2009. (Electronic publication ahead of print 2010 Feb 10, Article ID 579382, URL http://www.ncbi.nlm.nih.gov/pubmed/20169175. 10.1155/2009/579382.
71. Wu Y., Li X., Zhu J.X., Xie W., Le W., Fan Z., Jankovic J., Pan T. Resveratrol-activated AMPK/SIRT1/autophagy in cellular models of Parkinson's Disease. Neurosignals 2011, 19:163-174. (URL http://www.ncbi.nlm.nih.gov/pubmed/21778691).
72. Yang X., Yang Y., Luo Y., Li G., Yang E.S. Hyperphosphorylation and accumulation of neurofilament proteins in transgenic mice with Alzheimer presenilin 1 mutation. Cell. Mol. Neurobiol. 2009, 29:497-501. (URL http://www.ncbi.nlm.nih.gov/pubmed/19137424).
73. Yu X., Li G. Effects of resveratrol on longevity, cognitive ability and aging-related histological markers in the annual fish Nothobranchius guentheri. Exp. Gerontol. 2012, 47:940-949. (Aug, URL http://www.ncbi.nlm.nih.gov/pubmed/22960591).
74. Zupanc G.K. Adult neurogenesis and neuronal regeneration in the brain of teleost fish. J. Physiol. Paris 2008, 102(4-6):357-373. (URL http://www.ncbi.nlm.nih.gov/pubmed/18984045).