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Journal of Diabetes Research
Volume 2017, Article ID 7121827, 11 pages
https://doi.org/10.1155/2017/7121827
Review Article

SIRT1 Regulates Cognitive Performance and Ability of Learning and Memory in Diabetic and Nondiabetic Models

Department of Endocrinology and Metabolism, The First Hospital of Jilin University, Changchun, Jilin, China

Correspondence should be addressed to Guixia Wang; nc.ude.ulj@861gnawg

Received 20 June 2017; Accepted 8 August 2017; Published 15 October 2017

Academic Editor: Judy de Haan

Copyright © 2017 Yue Cao et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. C. Fritschi, U. G. Bronas, C. G. Park, E. G. Collins, and L. Quinn, “Early declines in physical function among aging adults with type 2 diabetes,” Journal of Diabetes and its Complications, vol. 31, pp. 347–352, 2017. View at Publisher · View at Google Scholar · View at Scopus
  2. S. Yoon, H. Cho, J. Kim et al., “Brain changes in overweight/obese and normal-weight adults with type 2 diabetes mellitus,” Diabetologia, vol. 60, pp. 1207–1217, 2017. View at Publisher · View at Google Scholar
  3. W. Li, T. Wang, and S. Xiao, “Type 2 diabetes mellitus might be a risk factor for mild cognitive impairment progressing to Alzheimer’s disease,” Neuropsychiatric Disease and Treatment, vol. 12, pp. 2489–2495, 2016. View at Publisher · View at Google Scholar · View at Scopus
  4. H. Ascher-Svanum, Y. F. Chen, A. Hake et al., “Cognitive and functional decline in patients with mild Alzheimer dementia with or without comorbid diabetes,” Clinical Therapeutics, vol. 37, pp. 1195–1205, 2015. View at Publisher · View at Google Scholar · View at Scopus
  5. P. J. Fried, L. Schilberg, A. K. Brem et al., “Humans with type-2 diabetes show abnormal long-term potentiation-like cortical plasticity associated with verbal learning deficits,” Journal of Alzheimer's Disease, vol. 55, pp. 89–100, 2017. View at Publisher · View at Google Scholar · View at Scopus
  6. K. Talbot, H. Y. Wang, H. Kazi et al., “Demonstrated brain insulin resistance in Alzheimer’s disease patients is associated with IGF-1 resistance, IRS-1 dysregulation, and cognitive decline,” The Journal of Clinical Investigation, vol. 122, pp. 1316–1338, 2012. View at Publisher · View at Google Scholar · View at Scopus
  7. M. W. Strachan, “R D Lawrence Lecture 2010. The brain as a target organ in type 2 diabetes: exploring the links with cognitive impairment and dementia,” Diabetic Medicine, vol. 28, pp. 141–147, 2011. View at Publisher · View at Google Scholar · View at Scopus
  8. T. B. Chen, S. Y. Yiao, Y. Sun et al., “Comorbidity and dementia: a nationwide survey in Taiwan,” PLoS One, vol. 12, article e0175475, 2017. View at Publisher · View at Google Scholar
  9. B. J. North and E. Verdin, “Sirtuins: Sir2-related NAD-dependent protein deacetylases,” Genome Biology, vol. 5, p. 224, 2004. View at Publisher · View at Google Scholar · View at Scopus
  10. M. Kitada, S. Kume, A. Takeda-Watanabe, K. Kanasaki, and D. Koya, “Sirtuins and renal diseases: relationship with aging and diabetic nephropathy,” Clinical Science (London, England), vol. 124, pp. 153–164, 2013. View at Publisher · View at Google Scholar · View at Scopus
  11. M. Kaeberlein, M. McVey, and L. Guarente, “The SIR2/3/4 complex and SIR2 alone promote longevity in Saccharomyces cerevisiae by two different mechanisms,” Genes & Development, vol. 13, pp. 2570–2580, 1999. View at Publisher · View at Google Scholar · View at Scopus
  12. E. Michishita, J. Y. Park, J. M. Burneskis, J. C. Barrett, and I. Horikawa, “Evolutionarily conserved and nonconserved cellular localizations and functions of human SIRT proteins,” Molecular Biology of the Cell, vol. 16, pp. 4623–4635, 2005. View at Publisher · View at Google Scholar · View at Scopus
  13. Y. Cao, X. Jiang, H. Ma, Y. Wang, P. Xue, and Y. Liu, “SIRT1 and insulin resistance,” Journal of Diabetes and its Complications, vol. 30, pp. 178–183, 2016. View at Publisher · View at Google Scholar · View at Scopus
  14. T. Ogawa, C. Wakai, T. Saito et al., “Distribution of the longevity gene product, SIRT1, in developing mouse organs,” Congenital Anomalies (Kyoto), vol. 51, pp. 70–79, 2011. View at Publisher · View at Google Scholar · View at Scopus
  15. S. M. Zakhary, D. Ayubcha, J. N. Dileo et al., “Distribution analysis of deacetylase SIRT1 in rodent and human nervous systems,” Anatomical Record (Hoboken, N.J. : 2007), vol. 293, pp. 1024–1032, 2010. View at Publisher · View at Google Scholar · View at Scopus
  16. T. Shan, Y. Wang, T. Wu et al., “Porcine sirtuin 1 gene clone, expression pattern, and regulation by resveratrol,” Journal of Animal Science, vol. 87, pp. 895–904, 2009. View at Publisher · View at Google Scholar · View at Scopus
  17. S. Michan, Y. Li, M. M. Chou et al., “SIRT1 is essential for normal cognitive function and synaptic plasticity,” The Journal of Neuroscience, vol. 30, pp. 9695–9707, 2010. View at Publisher · View at Google Scholar · View at Scopus
  18. Q. Wang, C. Yan, M. Xin, L. Han, Y. Zhang, and M. Sun, “Sirtuin 1 (Sirt1) overexpression in BaF3 cells contributes to cell proliferation promotion, apoptosis resistance and pro-inflammatory cytokine production,” Medical Science Monitor, vol. 23, pp. 1477–1482, 2017. View at Publisher · View at Google Scholar
  19. A. Sathyanarayan, M. T. Mashek, and D. G. Mashek, “ATGL promotes autophagy/lipophagy via SIRT1 to control hepatic lipid droplet catabolism,” Cell Reports, vol. 19, pp. 1–9, 2017. View at Publisher · View at Google Scholar
  20. H. L. Cheng, R. Mostoslavsky, S. Saito et al., “Developmental defects and p53 hyperacetylation in Sir2 homolog (SIRT1)-deficient mice,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, pp. 10794–10799, 2003. View at Publisher · View at Google Scholar · View at Scopus
  21. K. Nagao, T. Jinnouchi, S. Kai, and T. Yanagita, “Pterostilbene, a dimethylated analog of resveratrol, promotes energy metabolism in obese rats,” The Journal of Nutritional Biochemistry, vol. 43, pp. 151–155, 2017. View at Publisher · View at Google Scholar
  22. H. J. Lee and S. J. Yang, “Aging-related correlation between serum sirtuin 1 activities and basal metabolic rate in women, but not in men,” Clinical Nutrition Research, vol. 6, pp. 18–26, 2017. View at Publisher · View at Google Scholar
  23. M. M. Bellet, S. Masri, G. Astarita, P. Sassone-Corsi, M. A. Della Fazia, and G. Servillo, “Histone deacetylase SIRT1 controls proliferation, circadian rhythm, and lipid metabolism during liver regeneration in mice,” The Journal of Biological Chemistry, vol. 291, pp. 23318–23329, 2016. View at Publisher · View at Google Scholar · View at Scopus
  24. R. H. Wang, T. Zhao, K. Cui et al., “Negative reciprocal regulation between Sirt1 and Per2 modulates the circadian clock and aging,” Scientific Reports, vol. 6, article 28633, 2016. View at Publisher · View at Google Scholar · View at Scopus
  25. M. C. Haigis and D. A. Sinclair, “Mammalian sirtuins: biological insights and disease relevance,” Annual Review of Pathology, vol. 5, pp. 253–295, 2010. View at Publisher · View at Google Scholar · View at Scopus
  26. S. Fusco, G. Maulucci, and G. Pani, “Sirt1: def-eating senescence?” Cell Cycle, vol. 11, pp. 4135–4146, 2012. View at Publisher · View at Google Scholar · View at Scopus
  27. W. Grabowska, E. Sikora, and A. Bielak-Zmijewska, “Sirtuins, a promising target in slowing down the ageing process,” Biogerontology, vol. 18, no. 4, pp. 447–476, 2017. View at Publisher · View at Google Scholar
  28. D. F. Silva, J. E. Selfridge, J. Lu et al., “Bioenergetic flux, mitochondrial mass and mitochondrial morphology dynamics in AD and MCI cybrid cell lines,” Human Molecular Genetics, vol. 22, pp. 3931–3946, 2013. View at Publisher · View at Google Scholar · View at Scopus
  29. S. H. Cho, J. A. Chen, F. Sayed et al., “SIRT1 deficiency in microglia contributes to cognitive decline in aging and neurodegeneration via epigenetic regulation of IL-1beta,” The Journal of Neuroscience, vol. 35, pp. 807–818, 2015. View at Publisher · View at Google Scholar · View at Scopus
  30. Y. Y. Chen, L. Zhang, D. L. Shi et al., “Resveratrol attenuates subacute systemic inflammation-induced spatial memory impairment via inhibition of astrocyte activation and enhancement of synaptophysin expression in the hippocampus,” Annals of Clinical and Laboratory Science, vol. 47, pp. 17–24, 2017. View at Google Scholar
  31. R. Wang, Y. Zhang, J. Li, and C. Zhang, “Resveratrol ameliorates spatial learning memory impairment induced by Abeta1-42 in rats,” Neuroscience, vol. 344, pp. 39–47, 2017. View at Publisher · View at Google Scholar
  32. Y. Nomura and Y. Okuma, “Age-related defects in lifespan and learning ability in SAMP8 mice,” Neurobiology of Aging, vol. 20, pp. 111–115, 1999. View at Publisher · View at Google Scholar · View at Scopus
  33. T. Takeda, “Senescence-accelerated mouse (SAM) with special references to neurodegeneration models, SAMP8 and SAMP10 mice,” Neurochemical Research, vol. 34, pp. 639–659, 2009. View at Publisher · View at Google Scholar · View at Scopus
  34. J. C. Lopez-Ramos, M. T. Jurado-Parras, C. Sanfeliu, D. Acuña-Castroviejo, and J. M. Delgado-García, “Learning capabilities and CA1-prefrontal synaptic plasticity in a mice model of accelerated senescence,” Neurobiology of Aging, vol. 33, article 627.e613-626, 2012. View at Publisher · View at Google Scholar · View at Scopus
  35. X. R. Cheng, X. L. Cui, Y. Zheng et al., “Nodes and biological processes identified on the basis of network analysis in the brain of the senescence accelerated mice as an Alzheimer’s disease animal model,” Frontiers in Aging Neuroscience, vol. 5, p. 65, 2013. View at Publisher · View at Google Scholar · View at Scopus
  36. X. R. Cheng, W. X. Zhou, and Y. X. Zhang, “The behavioral, pathological and therapeutic features of the senescence-accelerated mouse prone 8 strain as an Alzheimer’s disease animal model,” Ageing Research Reviews, vol. 13, pp. 13–37, 2014. View at Publisher · View at Google Scholar · View at Scopus
  37. J. E. Morley, H. J. Armbrecht, S. A. Farr, and V. B. Kumar, “The senescence accelerated mouse (SAMP8) as a model for oxidative stress and Alzheimer’s disease,” Biochimica et Biophysica Acta, vol. 1822, pp. 650–656, 2012. View at Publisher · View at Google Scholar · View at Scopus
  38. J. E. Morley, S. A. Farr, V. B. Kumar, and H. J. Armbrecht, “The SAMP8 mouse: a model to develop therapeutic interventions for Alzheimer’s disease,” Current Pharmaceutical Design, vol. 18, pp. 1123–1130, 2012. View at Publisher · View at Google Scholar · View at Scopus
  39. H. Wang, K. Lian, B. Han et al., “Age-related alterations in the metabolic profile in the hippocampus of the senescence-accelerated mouse prone 8: a spontaneous Alzheimer’s disease mouse model,” Journal of Alzheimer's Disease, vol. 39, pp. 841–848, 2014. View at Publisher · View at Google Scholar · View at Scopus
  40. H. Gong, J. Pang, Y. Han et al., “Age-dependent tissue expression patterns of Sirt1 in senescence-accelerated mice,” Molecular Medicine Reports, vol. 10, pp. 3296–3302, 2014. View at Publisher · View at Google Scholar · View at Scopus
  41. T. Takeda, M. Hosokawa, and K. Higuchi, “Senescence-accelerated mouse (SAM): a novel murine model of accelerated senescence,” Journal of the American Geriatrics Society, vol. 39, pp. 911–919, 1991. View at Publisher · View at Google Scholar · View at Scopus
  42. M. Cosin-Tomas, M. J. Alvarez-Lopez, S. Sanchez-Roige et al., “Epigenetic alterations in hippocampus of SAMP8 senescent mice and modulation by voluntary physical exercise,” Frontiers in Aging Neuroscience, vol. 6, p. 51, 2014. View at Publisher · View at Google Scholar · View at Scopus
  43. H. S. Kim, S. Moon, J. H. Paik et al., “Activation of the 5-AMP-activated protein kinase in the cerebral cortex of young senescence-accelerated P8 mice and association with GSK3β- and PP2A-dependent inhibition of p-tau396 expression,” Journal of Alzheimer's Disease, vol. 46, pp. 249–259, 2015. View at Publisher · View at Google Scholar · View at Scopus
  44. M. Pallas, J. G. Pizarro, J. Gutierrez-Cuesta et al., “Modulation of SIRT1 expression in different neurodegenerative models and human pathologies,” Neuroscience, vol. 154, pp. 1388–1397, 2008. View at Publisher · View at Google Scholar · View at Scopus
  45. B. L. Xu, R. Wang, L. N. Ma et al., “Effects of caloric intake on learning and memory function in juvenile C57BL/6J mice,” BioMed Research International, vol. 2015, Article ID 759803, 7 pages, 2015. View at Publisher · View at Google Scholar · View at Scopus
  46. Y. A. Lee, E. J. Cho, and T. Yokozawa, “Protective effect of persimmon (Diospyros kaki) peel proanthocyanidin against oxidative damage under H2O2-induced cellular senescence,” Biological & Pharmaceutical Bulletin, vol. 31, pp. 1265–1269, 2008. View at Publisher · View at Google Scholar · View at Scopus
  47. T. Yokozawa, Y. A. Lee, E. J. Cho, K. Matsumoto, C. H. Park, and N. Shibahara, “Anti-aging effects of oligomeric proanthocyanidins isolated from persimmon fruits,” Drug Discoveries & Therapeutics, vol. 5, pp. 109–118, 2011. View at Publisher · View at Google Scholar
  48. K. Kakefuda, Y. Fujita, A. Oyagi et al., “Sirtuin 1 overexpression mice show a reference memory deficit, but not neuroprotection,” Biochemical and Biophysical Research Communications, vol. 387, pp. 784–788, 2009. View at Publisher · View at Google Scholar · View at Scopus
  49. K. N. Green, J. S. Steffan, H. Martinez-Coria et al., “Nicotinamide restores cognition in Alzheimer’s disease transgenic mice via a mechanism involving sirtuin inhibition and selective reduction of Thr231-phosphotau,” The Journal of Neuroscience, vol. 28, pp. 11500–11510, 2008. View at Publisher · View at Google Scholar · View at Scopus
  50. L. Sansone, V. Reali, L. Pellegrini et al., “SIRT1 silencing confers neuroprotection through IGF-1 pathway activation,” Journal of Cellular Physiology, vol. 228, pp. 1754–1761, 2013. View at Publisher · View at Google Scholar · View at Scopus
  51. A. Vaquero, M. Scher, D. Lee, H. Erdjument-Bromage, P. Tempst, and D. Reinberg, “Human SirT1 interacts with histone H1 and promotes formation of facultative heterochromatin,” Molecular Cell, vol. 16, pp. 93–105, 2004. View at Publisher · View at Google Scholar · View at Scopus
  52. H. Vaziri, S. K. Dessain, E. Ng Eaton et al., “hSIR2SIRT1 functions as an NAD-dependent p53 deacetylase,” Cell, vol. 107, pp. 149–159, 2001. View at Google Scholar
  53. J. Luo, A. Y. Nikolaev, S. Imai et al., “Negative control of p53 by Sir2alpha promotes cell survival under stress,” Cell, vol. 107, pp. 137–148, 2001. View at Publisher · View at Google Scholar · View at Scopus
  54. S. Bayod, C. Guzman-Brambila, S. Sanchez-Roige et al., “Voluntary exercise promotes beneficial anti-aging mechanisms in SAMP8 female brain,” Journal of Molecular Neuroscience, vol. 55, pp. 525–532, 2015. View at Publisher · View at Google Scholar · View at Scopus
  55. D. Porquet, G. Casadesus, S. Bayod et al., “Dietary resveratrol prevents Alzheimer’s markers and increases life span in SAMP8,” Age (Dordrecht, Netherlands), vol. 35, pp. 1851–1865, 2013. View at Publisher · View at Google Scholar · View at Scopus
  56. R. Cristofol, D. Porquet, R. Corpas et al., “Neurons from senescence-accelerated SAMP8 mice are protected against frailty by the sirtuin 1 promoting agents melatonin and resveratrol,” Journal of Pineal Research, vol. 52, pp. 271–281, 2012. View at Publisher · View at Google Scholar · View at Scopus
  57. B. L. Xu, R. Wang, L. N. Ma et al., “Comparison of the effects of resveratrol and caloric restriction on learning and memory in juvenile C57BL/6J mice,” Iranian Journal of Basic Medical Sciences, vol. 18, pp. 1118–1123, 2015. View at Google Scholar
  58. Z. Zheng, H. Chen, J. Li et al., “Sirtuin 1-mediated cellular metabolic memory of high glucose via the LKB1/AMPK/ROS pathway and therapeutic effects of metformin,” Diabetes, vol. 61, pp. 217–228, 2012. View at Publisher · View at Google Scholar · View at Scopus
  59. C. Canto, Z. Gerhart-Hines, J. N. Feige et al., “AMPK regulates energy expenditure by modulating NAD+ metabolism and SIRT1 activity,” Nature, vol. 458, pp. 1056–1060, 2009. View at Publisher · View at Google Scholar · View at Scopus
  60. L. L. Du, D. M. Chai, L. N. Zhao et al., “AMPK activation ameliorates Alzheimer’s disease-like pathology and spatial memory impairment in a streptozotocin-induced Alzheimer’s disease model in rats,” Journal of Alzheimer's Disease, vol. 43, pp. 775–784, 2015. View at Publisher · View at Google Scholar · View at Scopus
  61. K. J. Pearson, J. A. Baur, K. N. Lewis et al., “Resveratrol delays age-related deterioration and mimics transcriptional aspects of dietary restriction without extending life span,” Cell Metabolism, vol. 8, pp. 157–168, 2008. View at Publisher · View at Google Scholar · View at Scopus
  62. M. Khan, S. A. Shah, and M. O. Kim, “17β-estradiol via SIRT1/acetyl-p53/NF-kB signaling pathway rescued postnatal rat brain against acute ethanol intoxication,” Molecular Neurobiology, pp. 1–12, 2017. View at Publisher · View at Google Scholar
  63. F. Lan, J. M. Cacicedo, N. Ruderman, and Y. Ido, “SIRT1 modulation of the acetylation status, cytosolic localization, and activity of LKB1. Possible role in AMP-activated protein kinase activation,” The Journal of Biological Chemistry, vol. 283, pp. 27628–27635, 2008. View at Publisher · View at Google Scholar · View at Scopus
  64. A. Salminen, J. Huuskonen, J. Ojala, A. Kauppinen, K. Kaarniranta, and T. Suuronen, “Activation of innate immunity system during aging: NF-kB signaling is the molecular culprit of inflamm-aging,” Ageing Research Reviews, vol. 7, pp. 83–105, 2008. View at Publisher · View at Google Scholar · View at Scopus
  65. L. L. Du, J. Z. Xie, X. S. Cheng et al., “Activation of sirtuin 1 attenuates cerebral ventricular streptozotocin-induced tau hyperphosphorylation and cognitive injuries in rat hippocampi,” Age (Dordrecht, Netherlands), vol. 36, pp. 613–623, 2014. View at Publisher · View at Google Scholar · View at Scopus
  66. Y. I. Kitamura, T. Kitamura, J. P. Kruse et al., “FoxO1 protects against pancreatic beta cell failure through NeuroD and MafA induction,” Cell Metabolism, vol. 2, pp. 153–163, 2005. View at Publisher · View at Google Scholar · View at Scopus
  67. H. Y. Cohen, C. Miller, K. J. Bitterman et al., “Calorie restriction promotes mammalian cell survival by inducing the SIRT1 deacetylase,” Science, vol. 305, pp. 390–392, 2004. View at Publisher · View at Google Scholar · View at Scopus
  68. J. T. Rodgers, C. Lerin, W. Haas, S. P. Gygi, B. M. Spiegelman, and P. Puigserver, “Nutrient control of glucose homeostasis through a complex of PGC-1alpha and SIRT1,” Nature, vol. 434, pp. 113–118, 2005. View at Publisher · View at Google Scholar · View at Scopus
  69. L. R. Saunders, A. D. Sharma, J. Tawney et al., “miRNAs regulate SIRT1 expression during mouse embryonic stem cell differentiation and in adult mouse tissues,” Aging (Albany NY), vol. 2, pp. 415–431, 2010. View at Publisher · View at Google Scholar
  70. M. Tajes, J. Gutierrez-Cuesta, J. Folch et al., “Neuroprotective role of intermittent fasting in senescence-accelerated mice P8 (SAMP8),” Experimental Gerontology, vol. 45, pp. 702–710, 2010. View at Publisher · View at Google Scholar · View at Scopus
  71. J. Gutierrez-Cuesta, M. Tajes, A. Jimenez, A. Coto-Montes, A. Camins, and M. Pallàs, “Evaluation of potential pro-survival pathways regulated by melatonin in a murine senescence model,” Journal of Pineal Research, vol. 45, pp. 497–505, 2008. View at Publisher · View at Google Scholar · View at Scopus
  72. R. Corpas, S. Revilla, S. Ursulet et al., “SIRT1 overexpression in mouse hippocampus induces cognitive enhancement through proteostatic and neurotrophic mechanisms,” Molecular Neurobiology, vol. 54, no. 7, pp. 5604–5619, 2017. View at Publisher · View at Google Scholar · View at Scopus
  73. H. R. Lee, H. K. Shin, S. Y. Park et al., “Cilostazol suppresses β-amyloid production by activating a disintegrin and metalloproteinase 10 via the upregulation of SIRT1-coupled retinoic acid receptor-β,” Journal of Neuroscience Research, vol. 92, pp. 1581–1590, 2014. View at Publisher · View at Google Scholar · View at Scopus
  74. V. L. Villemagne, V. Dore, P. Bourgeat et al., “Abeta-amyloid and tau imaging in dementia,” Seminars in Nuclear Medicine, vol. 47, pp. 75–88, 2017. View at Publisher · View at Google Scholar
  75. W. Guo, L. Qian, J. Zhang et al., “Sirt1 overexpression in neurons promotes neurite outgrowth and cell survival through inhibition of the mTOR signaling,” Journal of Neuroscience Research, vol. 89, pp. 1723–1736, 2011. View at Publisher · View at Google Scholar · View at Scopus
  76. J. F. Codocedo, C. Allard, J. A. Godoy, L. Varela-Nallar, and N. C. Inestrosa, “SIRT1 regulates dendritic development in hippocampal neurons,” PLoS One, vol. 7, article e47073, 2012. View at Publisher · View at Google Scholar · View at Scopus
  77. M. F. Xu, Y. Y. Xiong, J. K. Liu, J. J. Qian, L. Zhu, and J. Gao, “Asiatic acid, a pentacyclic triterpene in Centella asiatica, attenuates glutamate-induced cognitive deficits in mice and apoptosis in SH-SY5Y cells,” Acta Pharmacologica Sinica, vol. 33, pp. 578–587, 2012. View at Publisher · View at Google Scholar · View at Scopus
  78. I. B. Zovkic, B. S. Paulukaitis, J. J. Day, D. M. Etikala, and J. D. Sweatt, “Histone H2A.Z subunit exchange controls consolidation of recent and remote memory,” Nature, vol. 515, pp. 582–586, 2014. View at Publisher · View at Google Scholar · View at Scopus
  79. T. Baptista, I. Graca, E. J. Sousa et al., “Regulation of histone H2A.Z expression is mediated by sirtuin 1 in prostate cancer,” Oncotarget, vol. 4, pp. 1673–1685, 2013. View at Publisher · View at Google Scholar
  80. K. S. Petersen and C. Smith, “Ageing-associated oxidative stress and inflammation are alleviated by products from grapes,” Oxidative Medicine and Cellular Longevity, vol. 2016, Article ID 6236309, 12 pages, 2016. View at Publisher · View at Google Scholar · View at Scopus
  81. S. Garcia-Matas, N. Vera, A. O. Aznar et al., “In vitro and in vivo activation of astrocytes by amyloid-β is potentiated by pro-oxidant agents,” Journal of Alzheimer's Disease, vol. 20, pp. 229–245, 2010. View at Publisher · View at Google Scholar · View at Scopus
  82. R. Quiroz-Baez, D. Flores-Dominguez, and C. Arias, “Synaptic aging is associated with mitochondrial dysfunction, reduced antioxidant contents and increased vulnerability to amyloid-beta toxicity,” Current Alzheimer Research, vol. 10, pp. 324–331, 2013. View at Publisher · View at Google Scholar · View at Scopus
  83. A. Navarro and A. Boveris, “The mitochondrial energy transduction system and the aging process,” American Journal of Physiology. Cell Physiology, vol. 292, pp. C670–C686, 2007. View at Publisher · View at Google Scholar · View at Scopus
  84. J. Valle, J. Duran-Vilaregut, G. Manich et al., “Cerebral amyloid angiopathy, blood-brain barrier disruption and amyloid accumulation in SAMP8 mice,” Neurodegenerative Diseases, vol. 8, pp. 421–429, 2011. View at Publisher · View at Google Scholar · View at Scopus
  85. H. Ota, M. Akishita, T. Akiyoshi et al., “Testosterone deficiency accelerates neuronal and vascular aging of SAMP8 mice: protective role of eNOS and SIRT1,” PLoS One, vol. 7, article e29598, 2012. View at Publisher · View at Google Scholar · View at Scopus
  86. T. Wang, G. Di, L. Yang et al., “Saponins from Panax japonicus attenuate D-galactose-induced cognitive impairment through its anti-oxidative and anti-apoptotic effects in rats,” The Journal of Pharmacy and Pharmacology, vol. 67, pp. 1284–1296, 2015. View at Publisher · View at Google Scholar · View at Scopus
  87. J. Liu, G. Hu, R. Xu et al., “Rhein lysinate decreases the generation of β-amyloid in the brain tissues of Alzheimer’s disease model mice by inhibiting inflammatory response and oxidative stress,” Journal of Asian Natural Products Research, vol. 15, pp. 756–763, 2013. View at Publisher · View at Google Scholar · View at Scopus
  88. H. M. Wang, L. W. Wang, X. M. Liu, C. L. Li, S. P. Xu, and A. D. Farooq, “Neuroprotective effects of forsythiaside on learning and memory deficits in senescence-accelerated mouse prone (SAMP8) mice,” Pharmacology, Biochemistry, and Behavior, vol. 105, pp. 134–141, 2013. View at Publisher · View at Google Scholar · View at Scopus
  89. Y. Yoshiyama, M. Higuchi, B. Zhang et al., “Synapse loss and microglial activation precede tangles in a P301S tauopathy mouse model,” Neuron, vol. 53, pp. 337–351, 2007. View at Publisher · View at Google Scholar · View at Scopus
  90. A. Z. Herskovits and L. Guarente, “SIRT1 in neurodevelopment and brain senescence,” Neuron, vol. 81, pp. 471–483, 2014. View at Publisher · View at Google Scholar · View at Scopus
  91. J. Gao, W. Y. Wang, Y. W. Mao et al., “A novel pathway regulates memory and plasticity via SIRT1 and miR-134,” Nature, vol. 466, pp. 1105–1109, 2010. View at Publisher · View at Google Scholar · View at Scopus
  92. Y. N. Zhao, W. F. Li, F. Li et al., “Resveratrol improves learning and memory in normally aged mice through microRNA-CREB pathway,” Biochemical and Biophysical Research Communications, vol. 435, pp. 597–602, 2013. View at Publisher · View at Google Scholar · View at Scopus
  93. C. Feng, J. Gu, F. Zhou et al., “The effect of lead exposure on expression of SIRT1 in the rat hippocampus,” Environmental Toxicology and Pharmacology, vol. 44, pp. 84–92, 2016. View at Publisher · View at Google Scholar · View at Scopus
  94. A. Cardoso, F. Marrana, and J. P. Andrade, “Caloric restriction in young rats disturbs hippocampal neurogenesis and spatial learning,” Neurobiology of Learning and Memory, vol. 133, pp. 214–224, 2016. View at Publisher · View at Google Scholar · View at Scopus
  95. P. S. Koekkoek, L. J. Kappelle, E. van den Berg, G. E. Rutten, and G. J. Biessels, “Cognitive function in patients with diabetes mellitus: guidance for daily care,” Lancet Neurology, vol. 14, pp. 329–340, 2015. View at Publisher · View at Google Scholar · View at Scopus
  96. D. Qi, A. Wang, Y. Chen et al., “Default mode network connectivity and related white matter disruption in type 2 diabetes mellitus patients concurrent with amnestic mild cognitive impairment,” Current Alzheimer Research, 2017. View at Publisher · View at Google Scholar
  97. J. F. Jansen, F. C. Bussel, H. J. Haar et al., “Cerebral blood flow, blood supply, and cognition in type 2 diabetes mellitus,” Scientific Reports, vol. 6, p. 10, 2016. View at Publisher · View at Google Scholar
  98. R. O. Roberts, D. S. Knopman, Y. E. Geda et al., “Association of diabetes with amnestic and nonamnestic mild cognitive impairment,” Alzheimers Dement, vol. 10, pp. 18–26, 2014. View at Publisher · View at Google Scholar · View at Scopus
  99. C. C. Chung, D. Pimentel, A. J. Jor'dan, Y. Hao, W. Milberg, and V. Novak, “Inflammation-associated declines in cerebral vasoreactivity and cognition in type 2 diabetes,” Neurology, vol. 85, pp. 450–458, 2015. View at Publisher · View at Google Scholar · View at Scopus
  100. J. Mehla, B. C. Chauhan, and N. B. Chauhan, “Experimental induction of type 2 diabetes in aging-accelerated mice triggered Alzheimer-like pathology and memory deficits,” Journal of Alzheimer's Disease, vol. 39, pp. 145–162, 2014. View at Publisher · View at Google Scholar · View at Scopus
  101. D. Sweetnam, A. Holmes, K. A. Tennant et al., “Diabetes impairs cortical plasticity and functional recovery following ischemic stroke,” The Journal of Neuroscience, vol. 32, pp. 5132–5143, 2012. View at Publisher · View at Google Scholar · View at Scopus
  102. V. Palomera-Avalos, C. Grinan-Ferre, V. Izquierdo, A. Camins, C. Sanfeliu, and M. Pallàs, “Metabolic stress induces cognitive disturbances and inflammation in aged mice: protective role of resveratrol,” Rejuvenation Research, vol. 20, no. 3, pp. 202–217, 2017. View at Publisher · View at Google Scholar
  103. V. Palomera-Avalos, C. Grinan-Ferre, D. Puigoriol-Ilamola et al., “Resveratrol protects SAMP8 brain under metabolic stress: focus on mitochondrial function and Wnt pathway,” Molecular Neurobiology, vol. 54, no. 3, pp. 1661–1676, 2017. View at Publisher · View at Google Scholar · View at Scopus
  104. R. H. Wang, H. S. Kim, C. Xiao, X. Xu, O. Gavrilova, and C. X. Deng, “Hepatic Sirt1 deficiency in mice impairs mTorc2/Akt signaling and results in hyperglycemia, oxidative damage, and insulin resistance,” The Journal of Clinical Investigation, vol. 121, pp. 4477–4490, 2011. View at Publisher · View at Google Scholar · View at Scopus
  105. B. Zhou, C. Li, W. Qi et al., “Downregulation of miR-181a upregulates sirtuin-1 (SIRT1) and improves hepatic insulin sensitivity,” Diabetologia, vol. 55, pp. 2032–2043, 2012. View at Publisher · View at Google Scholar · View at Scopus
  106. S. Frojdo, C. Durand, L. Molin et al., “Phosphoinositide 3-kinase as a novel functional target for the regulation of the insulin signaling pathway by SIRT1,” Molecular and Cellular Endocrinology, vol. 335, pp. 166–176, 2011. View at Publisher · View at Google Scholar · View at Scopus
  107. A. Chalkiadaki and L. Guarente, “High-fat diet triggers inflammation-induced cleavage of SIRT1 in adipose tissue to promote metabolic dysfunction,” Cell Metabolism, vol. 16, pp. 180–188, 2012. View at Publisher · View at Google Scholar · View at Scopus
  108. B. Draznin, “Molecular mechanisms of insulin resistance: serine phosphorylation of insulin receptor substrate-1 and increased expression of p85α: the two sides of a coin,” Diabetes, vol. 55, pp. 2392–2397, 2006. View at Publisher · View at Google Scholar · View at Scopus
  109. Y. Liu, Z. Yao, L. Zhang, H. Zhu, W. Deng, and C. Qin, “Insulin induces neurite outgrowth via SIRT1 in SH-SY5Y cells,” Neuroscience, vol. 238, pp. 371–380, 2013. View at Publisher · View at Google Scholar · View at Scopus
  110. M. Uittenbogaard, K. K. Baxter, and A. Chiaramello, “The neurogenic basic helix-loop-helix transcription factor NeuroD6 confers tolerance to oxidative stress by triggering an antioxidant response and sustaining the mitochondrial biomass,” ASN Neuro, vol. 2, article e00034, 2010. View at Publisher · View at Google Scholar · View at Scopus
  111. R. Lennox, D. W. Porter, P. R. Flatt, C. Holscher, N. Irwin, and V. A. Gault, “Comparison of the independent and combined effects of sub-chronic therapy with metformin and a stable GLP-1 receptor agonist on cognitive function, hippocampal synaptic plasticity and metabolic control in high-fat fed mice,” Neuropharmacology, vol. 86, pp. 22–30, 2014. View at Publisher · View at Google Scholar · View at Scopus
  112. N. M. Pathak, V. Pathak, A. M. Lynch, N. Irwin, V. A. Gault, and P. R. Flatt, “Stable oxyntomodulin analogues exert positive effects on hippocampal neurogenesis and gene expression as well as improving glucose homeostasis in high fat fed mice,” Molecular and Cellular Endocrinology, vol. 412, pp. 95–103, 2015. View at Publisher · View at Google Scholar · View at Scopus
  113. M. Mendez-del Villar, M. Gonzalez-Ortiz, E. Martinez-Abundis, K. G. Pérez-Rubio, and R. Lizárraga-Valdez, “Effect of resveratrol administration on metabolic syndrome, insulin sensitivity, and insulin secretion,” Metabolic Syndrome and Related Disorders, vol. 12, pp. 497–501, 2014. View at Publisher · View at Google Scholar · View at Scopus
  114. J. Wang, C. Tang, M. G. Ferruzzi et al., “Role of standardized grape polyphenol preparation as a novel treatment to improve synaptic plasticity through attenuation of features of metabolic syndrome in a mouse model,” Molecular Nutrition & Food Research, vol. 57, pp. 2091–2102, 2013. View at Publisher · View at Google Scholar · View at Scopus
  115. S. Bastianetto, C. Menard, and R. Quirion, “Neuroprotective action of resveratrol,” Biochimica et Biophysica Acta, vol. 1852, pp. 1195–1201, 2015. View at Publisher · View at Google Scholar · View at Scopus
  116. M. Kodali, V. K. Parihar, B. Hattiangady, V. Mishra, B. Shuai, and A. K. Shetty, “Resveratrol prevents age-related memory and mood dysfunction with increased hippocampal neurogenesis and microvasculature, and reduced glial activation,” Scientific Reports, vol. 5, p. 8075, 2015. View at Publisher · View at Google Scholar · View at Scopus
  117. D. Bonnefont-Rousselot, “Resveratrol and cardiovascular diseases,” Nutrients, vol. 8, 2016. View at Publisher · View at Google Scholar · View at Scopus
  118. P. C. Tang, Y. F. Ng, S. Ho, M. Gyda, and S. W. Chan, “Resveratrol and cardiovascular health – promising therapeutic or hopeless illusion?” Pharmacological Research, vol. 90, pp. 88–115, 2014. View at Publisher · View at Google Scholar · View at Scopus
  119. G. Wang, S. Amato, J. Gilbert, and H. Y. Man, “Resveratrol up-regulates AMPA receptor expression via AMP-activated protein kinase-mediated protein translation,” Neuropharmacology, vol. 95, pp. 144–153, 2015. View at Publisher · View at Google Scholar · View at Scopus
  120. X. M. Li, M. T. Zhou, X. M. Wang, M. H. Ji, Z. Q. Zhou, and J. J. Yang, “Resveratrol pretreatment attenuates the isoflurane-induced cognitive impairment through its anti-inflammation and -apoptosis actions in aged mice,” Journal of Molecular Neuroscience, vol. 52, pp. 286–293, 2014. View at Publisher · View at Google Scholar · View at Scopus
  121. J. Chang, A. Rimando, M. Pallas et al., “Low-dose pterostilbene, but not resveratrol, is a potent neuromodulator in aging and Alzheimer’s disease,” Neurobiology of Aging, vol. 33, pp. 2062–2071, 2012. View at Publisher · View at Google Scholar · View at Scopus
  122. R. A. Miller, D. E. Harrison, C. M. Astle et al., “Rapamycin, but not resveratrol or simvastatin, extends life span of genetically heterogeneous mice,” The Journals of Gerontology. Series A, Biological Sciences and Medical Sciences, vol. 66, pp. 191–201, 2011. View at Publisher · View at Google Scholar · View at Scopus
  123. R. H. Wong, D. Raederstorff, and P. R. Howe, “Acute resveratrol consumption improves neurovascular coupling capacity in adults with type 2 diabetes mellitus,” Nutrients, vol. 8, 2016. View at Publisher · View at Google Scholar · View at Scopus
  124. R. H. Wong, R. S. Nealon, A. Scholey, and P. R. Howe, “Low dose resveratrol improves cerebrovascular function in type 2 diabetes mellitus,” Nutrition, Metabolism, and Cardiovascular Diseases, vol. 26, pp. 393–399, 2016. View at Publisher · View at Google Scholar · View at Scopus
  125. H. M. Evans, P. R. Howe, and R. H. Wong, “Effects of resveratrol on cognitive performance, mood and cerebrovascular function in post-menopausal women; a 14-week randomised placebo-controlled intervention trial,” Nutrients, vol. 9, 2017. View at Publisher · View at Google Scholar
  126. K. Zortea, V. C. Franco, P. Guimaraes, and P. S. Belmonte-de-Abreu, “Resveratrol supplementation did not improve cognition in patients with schizophrenia: results from a randomized clinical trial,” Frontiers in Psychiatry, vol. 7, p. 159, 2016. View at Publisher · View at Google Scholar · View at Scopus