Protective effects of resveratrol on aging-induced cognitive impairment in rats

Neurobiology of Learning and Memory

Volumn 131, Issue , 2016, Pages 131-136

  Gocmez, Semil Selcen ^a   Gacar, Nejat ^a   Utkan, Tijen ^a   Gacar, Gulcin ^a   Scarpace, Philip J ^b   Tumer, Nihal ^b,c  

^a KOCAELI UNIVERSITY   (Turkey)

^b UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Aging; Inflammatory cytokines; Learning and memory; Resveratrol

Indexed keywords

INTERLEUKIN 1BETA; RESVERATROL; TUMOR NECROSIS FACTOR ALPHA; CYTOKINE; NONSTEROID ANTIINFLAMMATORY AGENT; STILBENE DERIVATIVE;

AGING; ANIMAL EXPERIMENT; ARTICLE; COGNITIVE DEFECT; CONTROLLED STUDY; CYTOKINE PRODUCTION; LOCOMOTION; MALE; MORRIS WATER MAZE TEST; NEUROPROTECTION; NONHUMAN; PASSIVE AVOIDANCE TEST; PROTEIN BLOOD LEVEL; RAT; SPATIAL LEARNING; SPATIAL MEMORY; TREATMENT DURATION; ANIMAL; ANIMAL BEHAVIOR; AVOIDANCE BEHAVIOR; DISEASE MODEL; DRUG EFFECTS; INFLAMMATION; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; WISTAR RAT;

AGING; ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; AVOIDANCE LEARNING; BEHAVIOR, ANIMAL; COGNITIVE DYSFUNCTION; CYTOKINES; DISEASE MODELS, ANIMAL; INFLAMMATION; MALE; RATS, WISTAR; SPATIAL LEARNING; STILBENES;

EID: 84962132730     PISSN: 10747427     EISSN: 10959564     Source Type: Journal    
DOI: 10.1016/j.nlm.2016.03.022     Document Type: Article

References (60)

1. Abraham J., Johnson R.W. Consuming a diet supplemented with resveratrol reduced infection-related neuroinflammation and deficits in working memory in aged mice. Rejuvenation Research 2009, 12:445-453.
2. Alvarez A., Cacabelos R., Sanpedro C., Garcia-Fantini M., Aleixandre M. Serum TNF-α levels are increased and correlate negatively with free IGF-I in Alzheimer disease. Neurobiology of Aging 2007, 28:533-536.
3. Anekonda T.S. Resveratrol-A boon for treating Alzheimer's disease?. Brain Research Reviews 2006, 52:316-326.
4. Bagci B., Sarioglu Y., Yazir Y., Utkan T., Aricioglu F. Agmatine attenuates vascular dementia in ageing. European Neuropsychopharm 2014, 24(2):S340-S341.
5. Baur J.A., Sinclair D.A. Therapeutic potential of resveratrol: The in vivo evidence. Nature Reviews Drug Discovery 2006, 5:493-506.
6. Belarbi K., Jopson T., Tweedie D., Arellano C., Luo W., Greig N.H., Rosi S. TNF-α protein ynthesis inhibitor restores neuronal function and reverses cognitive deficits induced by chronic neuroinflammation. Journal of Neuroinflammation 2012, 9:23-36.
7. Bermejo P., Martin-Aragon S., Benedi J., Susin C., Felici E., Gil P., Villar A.M. Differences of peripheral inflammatory markers between mild cognitive impairment and Alzheimer's disease. Immunology Letters 2008, 117:198-202.
8. Blalock E.M., Chen K.C., Sharrow K., Herman J.P., Porter N.M., Foster T.C., Landfield P.W. Gene microarrays in hippocampal aging: Statistical profiling identifies novel processes correlated with cognitive impairment. Journal of Neuroscience 2003, 23:3807-3819.
9. Bradamante S., Barenghi L., Villa A. Cardiovascular protective effects of resveratrol. Cardiovascular Drug Reviews 2004, 22:169-188.
10. Bruunsgaard H., Andersen-Ranberg K., Jeune B., Pedersen A.N., Skinhoj P., Pedersen B.K. A high plasma concentration of TNF-α is associated with dementia in centenarians. The Journals of Gerontology Series A: Biological Sciences and Medical Sciences 1999, 7:357-364.
11. Butcher S.K., Lord J.M. Stress responses and innate immunity: Aging as a contributory factor. Aging Cell 2004, 151-160.
12. Cantuti-Castelvetri B., Shukitt-Hale J.A. Joseph, Neurobehavioral aspects of 327 antioxidants in aging. International Journal of Developmental Neuroscience 2000, 18:367-381. 328.
13. Chen J., Buchanan J.B., Sparkman N.L., Godbout J.P., Freund G.G., Johnson R.W. Neuroinflammation and disruption in working memory in aged mice after acute stimulation of the peripheral innate immune system. Brain, Behavior, and Immunity 2008, 22:301-311.
14. Dimopoulos N., Piperi C., Salonicioti A., Mitropoulos P., Kallai E., Liappas I., Kalofoutis A. Indices of low-grade chronic inflammation correlate with early cognitive deterioration in an elderly Greek population. Neuroscience Letters 2006, 398:118-123.
15. Engelhart M.J., Geerlings M.I., Meijer J., Kiliaan A., Ruitenberg A., van Swieten J.C., Breteler M.M. Inflammatory proteins in plasma and the risk of dementia: The rotterdam study. Archives of Neurology 2004, 61:668-672.
16. Figurov A., Pozzo-Miller L.D., Olafsson P., Wang T., Lu B. Regulation of synaptic responses to high-frequency stimulation and LTP by neurotrophins in the hippocampus. Nature 1996, 381:706-709.
17. Fillit H., Ding W.H., Buee L., Kalman J., Altstiel L., Lawlor B., Wolf-Klein G. Elevated circulating tumor necrosis factor levels in Alzheimer's disease. Neuroscience Letters 1991, 129:318-320.
18. Gacar N., Gocmez S., Utkan T., Gacar G., Komsuoglu I., Tugay M., Utkan N.Z. Effects of resveratrol on ileal smooth muscle reactivity in polymicrobial sepsis model. Journal of Surgical Research 2012, 174:339-343.
19. Gacar N., Mutlu O., Utkan T., Komsuoglu Celikyurt I., Gocmez S.S., Ulak G. Beneficial effects of resveratrol on scopolamine but not mecamylamine induced memory impairment in the passive avoidance and Morris water maze tests in rats. Pharmacology, Biochemistry and Behavior 2011, 99:316-323.
20. Gemma C., Vila J., Bachstetter A., Bickford P.C. Oxidative stres and the aging brain: From theory to prevention. Brain aging: Models, methods, and mechanisms 2007, CRC Press, FL.
21. Gezen-Ak D., Dursun E., Hanagasi H., Bilgic B., Lohman E., Araz O.S., Yilmazer S. BDNF, TNFalpha, HSP90, CFH, and IL-10 serum levels in patients with early or late onset Alzheimer's disease or mild cognitive impairment. Journal of Alzheimer's Disease 2013, 37:185-195.
22. Gocmez S.S., Whidden M.A., Erdos B., Kirichenko N., Sakarya Y., Tumer N. Resveratrol treatment reverses age-related vascular dysfunction in mesenteric arteries. The FASEB Journal 2011, 25:1075.1. (Abstracts of Experimental Biology 2011, April 9-13, 2011, Washington, DC, USA).
23. Godbout J.P., Chen J., Abraham J., Richwine A.F., Berg B.M., Kelley K.W., Johnson R.W. Exaggerated neuroinflammation and sickness behavior in aged mice following activation of inhibition of LPS-induced sickness in aged mice the peripheral innate immune system. The FASEB Journal 2005, 19:1329-1331.
24. Griffin R., Nally R., Nolan Y., McCartney Y., Linden J., Lynch M.A. The age-related attenuation in long-term potentiation is associated with microglial activation. Journal of Neurochemistry 2006, 99:1263-1272.
25. Han Y.S., Zheng W.H., Bastianetto S., Chabot J.G., Quiron R. Neuroprotective effects of resveratrol against beta-amyloid-induced neurotoxicity in rat hippocampal neurons: Involvement of protein kinase C. British Journal of Pharmacology 2004, 141:997-1005.
26. Harman D. Free-radical theory of aging. Increasing the functional life span. Annals of the New York Academy of Sciences 1994, 717:1-15.
27. Jang M., Cai L., Udeani G.O., Slowing K.V., Thomas C.F., Beecher C.W., Fong H.H., Pezzuto J.M. Cancer chemopreventative activity of resveratrol, a natural product derived from grapes. Science 1997, 275:218-220.
28. Kang H., Schuman E.M. Long-lasting neurotrophin-induced enhancement of synaptic transmission in the adult hippocampus. Science 1995, 267:1658-1662.
29. Karege F., Perret G., Bondolfi G., Schwald M., Bertschy G., Aubry J.M. Decreased serum brain-derived neurotrophic factor levels in major depressed patients. Psychiatry Research 2002, 109:143-148.
30. Karson A., Demirtaş T., Bayramgürler D., Balci F., Utkan T. Chronic administration of infliximab (TNF-α inhibitor) decreases depression and anxiety-like behaviour in rat model of chronic mild stress. Basic & Clinical Pharmacology & Toxicology 2013, 112:335-340.
31. Karson A., Utkan T., Balci F., Aricioglu F., Ates N. Age-dependent decline in learning and memory performances of WAG/Rij rat model of absence epilepsy. Behavioral and Brain Functions 2012, 8:51.
32. Kodali M., Parihar V.K., Hattiangady B., Mishra V., Shuai B., Shetty A.K. Resveratrol prevents age-related memory and mood dysfunction with increased hippocampal neurogenesis and microvasculature, and reduced glial activation. Scientific Reports 2014, 5:1-16.
33. Licastro F., Pedrini S., Caputo L., Annoni G., Davis L.J., Ferri C., Grimaldi L.M. Increased plasma levels of interleukin-1, interleukin-6 and α-antichymotrypsin in patients with Alzheimer's disease: Peripheral inflammation or signals from the brain?. Journal of Neuroimmunology 2000, 103:97-102.
34. Monleon S., Urquiza A., Carmen Arenas M., Vinader-Caerols C., Parra A. Chronic administration of fluoxetine impairs inhibitory avoidance in male but not female mice. Behavioural Brain Research 2002, 136:483-488.
35. Mucke L. Neuroscience: Alzheimer's disease. Nature 2009, 461(7266):895-897.
36. Navarro A., Sanchez D.P.M., Gomez C., Peralta J.L., Boveris A. Behavioral dysfunction, brain oxidative stres, and impaired mitochondrial electron transfer in aging mice. American Journal of Physiology: Regulatory, Integrative and Comparative Physiology 2002, 282:R985-R992.
37. Ono K., Ondron M.M., Ho L., Wang L., Zhao W., Pasinetti G.M., Teplow D.B. Effects of grape seed-derived polphenols on amyloid beta-protein self assembly and cytotoxicity. The Journal of Biological Chemistry 2008, 283:32176-33287.
38. Peng S., Wuu J., Mufson E.J., Fahnestock M. Precursor form of brainderived neurotrophic factor and mature brain-derived neurotrophic factor are decreased in the pre-clinical stages of Alzheimer's disease. Journal of Neurochemistry 2005, 93:1412-1421.
39. Phelps E.A. Human emotion and memory: interactions of the amygdala and hippocampal complex. Current Opinion in Neurobiology 2004, 14:198-202.
40. Pieramico V., Esposito R., Cesinaro S., Frazzini V., Sensi S.L. Effects of non-pharmacological or pharmacological interventions on cognition and brain plasticity of agingindividuals. Frontiers in Systems Neuroscience 2014, 8:153.
41. Porquet D., Casadesus G., Bayod S., Vicente A., Canudas A.M., Vilaplana, del Vale J. Dietary resveratrol prevents Alzheimer's markers and increases life span in SAMP8. Age 2012, 35:1851-1865.
42. Pothion S., Bizot J.C., Trovero F., Belzung C. Strain differences in sucrose preference and in the consequences of unpredictable chronic mild stress. Behavioural Brain Research 2004, 155:135-146.
43. Poulose S.M., Thangthaeng N., Miller M.G., Shukitt-Hale B. Effects of pterostilben and resveratrol on brain and behavior. Neurochemistry International 2015, 89:227-233.
44. Roozendaal B., McReynolds J.R., McGaugh J.L. The basolateral amygdala interacts with themedial prefrontal cortex in regulating glucocorticoid effects onworkingmemory impairment. Journal of Neuroscience 2004, 24:1385-1392.
45. Saiko P., Szakmary A., Jaeger W., Szekeres T. Resveratrol and its analogs: Defense against cancer, coronary disease and neurodegenerative maladies or just a fad?. Mutation Research/Revews in Mutation Research 2008, 658:68-69.
46. Sharma M., Gupta Y.K. Chronic treatment with transresveratrol prevents intracerebroventricular streptozotocin induced cognitive impairment and oxidative stress in rats. Life Sciences 2002, 71:2489-2498.
47. Svajger U., Jeras M. Anti-inflammatory effects of resveratrol and its potential use in therapy of immune-mediated diseases. International Reviews of Immunology 2012, 31:202-222.
48. Swanson K.S., Vester B.M., Apanavicius C.J., Kirby N.A., Schook L.B. Implications of age and diet on canine cerebral cortex transcription. Neurobiology of Aging 2009, 30:1314-1326.
49. Tarkowski E., Blennow K., Wallin A., Tarkowski A. Intracerebral production of tumor necrosis factor-alpha, a local neuroprotective agent, in Alzheimer disease and vascular dementia. Journal of Clinical Immunology 1999, 19:223-230.
50. Trollor J.N., Smith E., Agars E., Kuan S.A., Baune B.T., Campbell L., Sachdev P. The association between systemic inflammation and cognitive performance in the elderly: The Sydney memory and ageing study. Age (Dordr) 2011, 34:1295-1308.
51. Tromp D., Dufour A., Lithfous S., Pebayle T., Despres O. Episodic memory in normal aging and Alzheimer Disease: Insights from imaging and behavioral studies. Ageing Research Reviews 2015, 10.1016/j.arr.2015.08.006.
52. Turner R.S., Thomas R.G., Craft S., van Dyck C.H., Mintzer J., Reynolds B.A., Aisen P.S. A randomized, double-blind, placebo-controlledtrial of resveratrol for Alzheimer disease. Neurology 2015, 85:1383-1391.
53. Vetrivel K.S., Thinakaran G. Membrane rafts in Alzheimer's disease beta-amyloid production. Biochimica et Biophysica Acta 2010, 1801(8):860-867.
54. Vinson J.A. Falvanoids in foods as in vitro and in vivo antioxidants. Advances in Experimental Medicine and Biology 1998, 439:151-164.
55. Wang Q., Xu J., Rottinhaus G.E. Resveratrol protects against global cerebral ischemic injury in gerbils. Brain Research 2002, 958:439-447.
56. Wang Q., Yu S., Simonyi A., Rottinhaus G.E. Resveratrol protects against neurotoxicity induced by kainic acid. Neurochemical Research 2005, 29:2105-2112.
57. Yazir Y., Utkan T., Gacar N., Aricioglu F. Resveratrol exerts anti-inflammatory and neuroprotective effects to prevent memory deficits in rats exposed to chronic unpredictable mild stress. Physiology & Behavior 2015, 138:297-304.
58. Zhao Y., Li W., Li F., Zhang Z., Dai Y., Xu A., Gao J. Resveratrol improves learning and memory in normally aged mice through microRNA-CREB pathway. Biochemical and Biophysical Research Communications 2013, 435:597-602.
59. Zuliani G., Cavalieri M., Galvani M., Passaro A., Munari M.R., Bosi C., Fellin R. Markers of endothelial dysfunction in older subjects with late onset Alzheimer's disease or vascular dementia. Journal of the Neurological Sciences 2008, 272:164-170.
60. Zuliani G., Ranzini M., Guerra G., Rossi L., Munari M.R., Zurlo A., Fellin R. Plasma cytokines profile in older subjects with late onset Alzheimer's disease or vascular dementia. Journal of Psychiatric Research 2007, 41:686-693.