The lifespan extension effects of resveratrol are conserved in the honey bee and may be driven by a mechanism related to caloric restriction

Aging

Volumn 4, Issue 7, 2012, Pages 499-508

  Rascón, Brenda ^a   Hubbard, Basil P ^b   Sinclair, David A ^b   Amdam, Gro V ^a,c  

^a NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

^b HARVARD MEDICAL SCHOOL   (United States)

^c ARIZONA STATE UNIVERSITY   (United States)

Author keywords

Aging; Apis mellifera; Hyperoxia; Learning performance; Lifespan; Resveratrol

Indexed keywords

EID: 84868101259     PISSN: 19454589     EISSN: None     Source Type: Journal    
DOI: 10.18632/aging.100474     Document Type: Article

References (78)

1. Arking R. Altering Aging: Interventions That Modify Longevity and Aging. In: Arking R, ed. The Biology of Aging: Observations and Principles. (New York: Oxford University Press), 2006; pp. 202-236.
2. Howitz KT, Bitterman KJ, Cohen HY, Lamming DW, Lavu S, Wood JG, Zipkin RE, Chung P, Kisielewski A, Zhang LL, Scherer B and Sinclair DA. Small molecule activators of sirtuins extend Saccharomyces cerevisiae lifespan. Nature. 2003; 425:191-196.
3. Valenzano DR, Terzibasi E, Genade T, Cattaneo A, Domenici L and Cellerino A. Resveratrol prolongs lifespan and retards the onset of age-related markers in a short-lived vertebrate. Curr Biol. 2006; 16:296-300.
4. Wood JG, Rogina B, Lavu S, Howitz K, Helfand SL, Tatar M and Sinclair D. Sirtuin activators mimic caloric restriction and delay ageing in metazoans. Nature. 2004; 430:686-689.
5. Bass TM, Weinkove D, Houthoofd K, Gems D and Partridge L. Effects of resveratrol on lifespan in Drosophila melanogaster and Caenorhabditis elegans. Mechanisms of ageing and development. 2007; 128:546-552.
6. Kaeberlein M, McDonagh T, Heltweg B, Hixon J, Westman EA, Caldwell SD, Napper A, Curtis R, DiStefano PS, Fields S, Bedalov A and Kennedy BK. Substrate-specific activation of sirtuins by resveratrol. The Journal of biological chemistry. 2005; 280:17038-17045.
7. Feige JN, Lagouge M, Canto C, Strehle A, Houten SM, Milne JC, Lambert PD, Mataki C, Elliott PJ and Auwerx J. Specific SIRT1 activation mimics low energy levels and protects against dietinduced metabolic disorders by enhancing fat oxidation. Cell metabolism. 2008; 8:347-358.
8. Smith JJ, Kenney RD, Gagne DJ, Frushour BP, Ladd W, Galonek HL, Israelian K, Song J, Razvadauskaite G, Lynch AV, Carney DP, Johnson RJ, Lavu S, et al. Small molecule activators of SIRT1 replicate signaling pathways triggered by calorie restriction in vivo. BMC systems biology. 2009; 3:31.
9. Bastianetto S, Zheng WH and Quirion R. Neuroprotective abilities of resveratrol and other red wine constituents against nitric oxide-related toxicity in cultured hippocampal neurons. British journal of pharmacology. 2000; 131:711-720.
10. Han YS, Zheng WH, Bastianetto S, Chabot JG and Quirion R. Neuroprotective effects of resveratrol against beta-amyloidinduced neurotoxicity in rat hippocampal neurons: involvement of protein kinase C. British journal of pharmacology. 2004; 141:997-1005.
11. Jang JH and Surh YJ. Protective effect of resveratrol on betaamyloid-induced oxidative PC12 cell death. Free radical biology & medicine. 2003; 34:1100-1110.
12. Marambaud P, Zhao H and Davies P. Resveratrol promotes clearance of Alzheimer's disease amyloid-beta peptides. The Journal of biological chemistry. 2005; 280:37377-37382.
13. Mokni M, Elkahoui S, Limam F, Amri M and Aouani E. Effect of Resveratrol on Antioxidant Enzyme Activities in the Brain of Healthy Rat. Neurochemical Research. 2007; 32:981-987.
14. Joseph JA, Fisher DR, Cheng V, Rimando AM and Shukitt-Hale B. Cellular and behavioral effects of stilbene resveratrol analogues: implications for reducing the deleterious effects of aging. Journal of agricultural and food chemistry. 2008; 56:10544-10551.
15. Sonmez U, Sonmez A, Erbil G, Tekmen I and Baykara B. Neuroprotective effects of resveratrol against traumatic brain injury in immature rats. Neuroscience letters. 2007; 420:133-137.
16. Jin F, Wu Q, Lu YF, Gong QH and Shi JS. Neuroprotective effect of resveratrol on 6-OHDA-induced Parkinson's disease in rats. European journal of pharmacology. 2008; 600:78-82.
17. Baur JA, Pearson KJ, Price NL, Jamieson HA, Lerin C, Kalra A, Prabhu VV, Allard JS, Lopez-Lluch G, Lewis K, Pistell PJ, Poosala S, Becker KG, et al. Resveratrol improves health and survival of mice on a high-calorie diet. Nature. 2006; 444:337-342.
18. Amdam GV and Page RE, Jr. Intergenerational transfers may have decoupled physiological and chronological age in a eusocial insect. Ageing research reviews. 2005; 4:398-408.
19. Kirkwood TB. Evolution of ageing. Nature. 1977; 270:301-304.
20. Bauer JH, Goupil S, Garber GB and Helfand SL. An accelerated assay for the identification of lifespan-extending interventions in Drosophila melanogaster. Proceedings of the National Academy of Sciences of the United States of America. 2004; 101:12980-12985.
21. Gruber J, Tang SY and Halliwell B. Evidence for a trade-off between survival and fitness caused by resveratrol treatment of Caenorhabditis elegans. Annals of the New York Academy of Sciences. 2007; 1100:530-542.
22. Jarolim S, Millen J, Heeren G, Laun P, Goldfarb DS and Breitenbach M. A novel assay for replicative lifespan in Saccharomyces cerevisiae. FEMS yeast research. 2004; 5:169-177.
23. Viswanathan M, Kim SK, Berdichevsky A and Guarente L. A role for SIR-2.1 regulation of ER stress response genes in determining C. elegans life span. Developmental cell. 2005; 9:605-615.
24. Howitz KT and Sinclair DA. Xenohormesis: sensing the chemical cues of other species. Cell. 2008; 133:387-391.
25. de la Lastra CA and Villegas I. Resveratrol as an antioxidant and pro-oxidant agent: mechanisms and clinical implications. Biochemical Society transactions. 2007; 35:1156-1160.
26. Mahal H and Mukherjee T. Scavenging of reactive oxygen radicals by resveratrol: antioxidant effect. Research on Chemical Intermediates. 2006; 32:59-71.
27. Ahmad A, Syed FA, Singh S and Hadi SM. Prooxidant activity of resveratrol in the presence of copper ions: Mutagenicity in plasmid DNA. Toxicology Letters. 2005; 159:1-12.
28. Zheng L-F, Wei Q-Y, Cai Y-J, Fang J-G, Zhou B, Yang L and Liu Z-L. DNA damage induced by resveratrol and its synthetic analogues in the presence of Cu (II) ions: Mechanism and structure-activity relationship. Free Radical Biology and Medicine. 2006; 41:1807-1816.
29. Rascon B and Harrison JF. Lifespan and oxidative stress show a non-linear response to atmospheric oxygen in Drosophila. The Journal of experimental biology. 2011; 213:3441-3448.
30. Kloek GP. Survivorship of drosophila in nitrogen reduced hypobaric atmospheres. Aviation, space, and environmental medicine. 1978; 49:720-721.
31. Miquel J, Lundgren PR and Bensch KG. Effects of exygennitrogen (1:1) at 760 Torr on the life span and fine structure of Drosophila melanogaster. Mechanisms of ageing and development. 1975; 4:41-57.
32. Gruenewald C, Botella JA, Bayersdorfer F, Navarro JA and Schneuwly S. Hyperoxia-induced neurodegeneration as a tool to identify neuroprotective genes in Drosophila melanogaster. Free radical biology & medicine. 2009; 46:1668-1676.
33. Yang NC, Lee CH and Song TY. Evaluation of resveratrol oxidation in vitro and the crucial role of bicarbonate ions. Bioscience, biotechnology, and biochemistry. 2010; 74:63-68.
34. Lin SJ, Defossez PA and Guarente L. Requirement of NAD and SIR2 for life-span extension by calorie restriction in Saccharomyces cerevisiae. Science New York, NY. 2000; 2892126-2128.
35. Rogina B and Helfand SL. Sir2 mediates longevity in the fly through a pathway related to calorie restriction. Proceedings of the National Academy of Sciences of the United States of America. 2004; 101:15998-16003.
36. Wang C, Chen L, Hou X, Li Z, Kabra N, Ma Y, Nemoto S, Finkel T, Gu W, Cress WD and Chen J. Interactions between E2F1 and SirT1 regulate apoptotic response to DNA damage. Nature cell biology. 2006; 8:1025-1031.
37. Frye RA. Phylogenetic classification of prokaryotic and eukaryotic Sir2-like proteins. Biochemical and biophysical research communications. 2000; 273:793-798.
38. Boily G, Seifert EL, Bevilacqua L, He XH, Sabourin G, Estey C, Moffat C, Crawford S, Saliba S, Jardine K, Xuan J, Evans M, Harper ME, et al. SirT1 regulates energy metabolism and response to caloric restriction in mice. PloS one. 2008; 3:e1759.
39. Imai S, Armstrong CM, Kaeberlein M and Guarente L. Transcriptional silencing and longevity protein Sir2 is an NADdependent histone deacetylase. Nature. 2000; 403:795-800.
40. Vaziri H, Dessain SK, Ng Eaton E, Imai SI, Frye RA, Pandita TK, Guarente L and Weinberg RA. hSIR2(SIRT1) functions as an NADdependent p53 deacetylase. Cell. 2001; 107:149-159.
41. Rizki G, Iwata TN, Li J, Riedel CG, Picard CL, Jan M, Murphy CT and Lee SS. The evolutionarily conserved longevity determinants HCF-1 and SIR-2.1/SIRT1 collaborate to regulate DAF-16/FOXO. PLoS genetics. 2011; 7:e1002235.
42. Tissenbaum HA and Guarente L. Increased dosage of a sir-2 gene extends lifespan in Caenorhabditis elegans. Nature. 2001; 410:227-230.
43. Burnett C, Valentini S, Cabreiro F, Goss M, Somogyvari M, Piper MD, Hoddinott M, Sutphin GL, Leko V, McElwee JJ, Vazquez-Manrique RP, Orfila AM, Ackerman D, et al. Absence of effects of Sir2 overexpression on lifespan in C. elegans and Drosophila. Nature. 2011; 477:482-485.
44. Bordone L, Cohen D, Robinson A, Motta MC, van Veen E, Czopik A, Steele AD, Crowe H, Marmor S, Luo J, Gu W and Guarente L. SIRT1 transgenic mice show phenotypes resembling calorie restriction. Aging cell. 2007; 6:759-767.
45. Antosh M, Fox D, Helfand SL, Cooper LN and Neretti N. New comparative genomics approach reveals a conserved health span signature across species. Aging. 2011; 3:576-583.
46. Dal-Pan A, Blanc S and Aujard F. Resveratrol suppresses body mass gain in a seasonal non-human primate model of obesity. BMC physiology. 2010; 10:11.
47. Banks AS, Kon N, Knight C, Matsumoto M, Gutierrez-Juarez R, Rossetti L, Gu W and Accili D. SirT1 gain of function increases energy efficiency and prevents diabetes in mice. Cell metabolism. 2008; 8:333-341.
48. Cakir I, Perello M, Lansari O, Messier NJ, Vaslet CA and Nillni EA. Hypothalamic Sirt1 regulates food intake in a rodent model system. PloS one. 2009; 4:e8322.
49. Price NL, Gomes AP, Ling AJ, Duarte FV, Martin-Montalvo A, North BJ, Agarwal B, Ye L, Ramadori G, Teodoro JS, Hubbard BP, Varela AT, Davis JG, et al. SIRT1 is required for AMPK activation and the beneficial effects of resveratrol on mitochondrial function. Cell metabolism. 2012; 15:675-690.
50. Dolinoy DC, Huang D and Jirtle RL. Maternal nutrient supplementation counteracts bisphenol A-induced DNA hypomethylation in early development. Proceedings of the National Academy of Sciences of the United States of America. 2007; 104:13056-13061.
51. Dolinoy DC, Weidman JR, Waterland RA and Jirtle RL. Maternal genistein alters coat color and protects Avy mouse offspring from obesity by modifying the fetal epigenome. Environmental health perspectives. 2006; 114:567-572.
52. Kaati G, Bygren LO, Pembrey M and Sjostrom M. Transgenerational response to nutrition, early life circumstances and longevity. Eur J Hum Genet. 2007; 15:784-790.
53. Kucharski R, Maleszka J, Foret S and Maleszka R. Nutritional control of reproductive status in honeybees via DNA methylation. Science New York, NY. 2008; 319:1827-1830.
54. O'Hagan HM, Mohammad HP and Baylin SB. Double strand breaks can initiate gene silencing and SIRT1-dependent onset of DNA methylation in an exogenous promoter CpG island. PLoS genetics. 2008; 4:e1000155.
55. Lopatina N, Haskell JF, Andrews LG, Poole JC, Saldanha S and Tollefsbol T. Differential maintenance and de novo methylating activity by three DNA methyltransferases in aging and immortalized fibroblasts. Journal of cellular biochemistry. 2002; 84:324-334.
56. Casillas MA, Jr., Lopatina N, Andrews LG and Tollefsbol TO. Transcriptional control of the DNA methyltransferases is altered in aging and neoplastically-transformed human fibroblasts. Molecular and cellular biochemistry. 2003; 252:33-43.
57. Eden A, Gaudet F, Waghmare A and Jaenisch R. Chromosomal instability and tumors promoted by DNA hypomethylation. Science New York, NY. 2003; 300:455.
58. Gonzalo S, Jaco I, Fraga MF, Chen T, Li E, Esteller M and Blasco MA. DNA methyltransferases control telomere length and telomere recombination in mammalian cells. Nature cell biology. 2006; 8:416-424.
59. Oberdoerffer P, Michan S, McVay M, Mostoslavsky R, Vann J, Park SK, Hartlerode A, Stegmuller J, Hafner A, Loerch P, Wright SM, Mills KD, Bonni A, et al. SIRT1 redistribution on chromatin promotes genomic stability but alters gene expression during aging. Cell. 2008; 135:907-918.
60. Cao Z, Fang J, Xia C, Shi X and Jiang BH. trans-3,4,5'-Trihydroxystibene inhibits hypoxia-inducible factor 1alpha and vascular endothelial growth factor expression in human ovarian cancer cells. Clin Cancer Res. 2004; 10:5253-5263.
61. Dasgupta B and Milbrandt J. Resveratrol stimulates AMP kinase activity in neurons. Proceedings of the National Academy of Sciences of the United States of America. 2007; 104:7217-7222.
62. Frojdo S, Cozzone D, Vidal H and Pirola L. Resveratrol is a class IA phosphoinositide 3-kinase inhibitor. The Biochemical journal. 2007; 406:511-518.
63. Jia K, Chen D and Riddle DL. The TOR pathway interacts with the insulin signaling pathway to regulate C. elegans larval development, metabolism and life span. Development (Cambridge, England). 2004; 131:3897-3906.
64. Kapahi P, Zid BM, Harper T, Koslover D, Sapin V and Benzer S. Regulation of lifespan in Drosophila by modulation of genes in the TOR signaling pathway. Curr Biol. 2004; 14:885-890.
65. Powers RW, 3rd, Kaeberlein M, Caldwell SD, Kennedy BK and Fields S. Extension of chronological life span in yeast by decreased TOR pathway signaling. Genes & development. 2006; 20:174-184.
66. Bjedov I, Toivonen JM, Kerr F, Slack C, Jacobson J, Foley A and Partridge L. Mechanisms of life span extension by rapamycin in the fruit fly Drosophila melanogaster. Cell metabolism. 2010; 11:35-46.
67. Harrison DE, Strong R, Sharp ZD, Nelson JF, Astle CM, Flurkey K, Nadon NL, Wilkinson JE, Frenkel K, Carter CS, Pahor M, Javors MA, Fernandez E, et al. Rapamycin fed late in life extends lifespan in genetically heterogeneous mice. Nature. 2009; 460:392-395.
68. Demidenko ZN and Blagosklonny MV. At concentrations that inhibit mTOR, resveratrol suppresses cellular senescence. Cell cycle (Georgetown, Tex. 2009; 8:1901-1904.
69. Demidenko ZN and Blagosklonny MV. Quantifying pharmacologic suppression of cellular senescence: prevention of cellular hypertrophy versus preservation of proliferative potential. Aging. 2009; 1:1008-1016.
70. Armour SM, Baur JA, Hsieh SN, Land-Bracha A, Thomas SM and Sinclair DA. Inhibition of mammalian S6 kinase by resveratrol suppresses autophagy. Aging. 2009; 1:515-528.
71. Longo VD. The Ras and Sch9 pathways regulate stress resistance and longevity. Experimental gerontology. 2003; 38:807-811.
72. Madia F, Gattazzo C, Wei M, Fabrizio P, Burhans WC, Weinberger M, Galbani A, Smith JR, Nguyen C, Huey S, Comai L and Longo VD. Longevity mutation in SCH9 prevents recombination errors and premature genomic instability in a Werner/Bloom model system. The Journal of cell biology. 2008; 180:67-81.
73. Wei M, Fabrizio P, Hu J, Ge H, Cheng C, Li L and Longo VD. Life span extension by calorie restriction depends on Rim15 and transcription factors downstream of Ras/PKA, Tor, and Sch9. PLoS genetics. 2008; 4:e13.
74. Patel PH and Tamanoi F. Increased Rheb-TOR signaling enhances sensitivity of the whole organism to oxidative stress. Journal of cell science. 2006; 119:4285-4292.
75. Medvedik O, Lamming DW, Kim KD and Sinclair DA. MSN2 and MSN4 link calorie restriction and TOR to sirtuin-mediated lifespan extension in Saccharomyces cerevisiae. PLoS biology. 2007; 5:e261.
76. Crailsheim K. The protein balance of the honey bee worker. Apidologie. 1990; 21:417-429.
77. Naiem E-S, Hrassnigg N and Crailsheim K. Nurse bees support the physiological development of young bees (Apis mellifera L.). J Comp Physiol B 1999; 169:271-279.
78. Amdam GV, Fennern E, Baker N and Rascón B. Honeybee associative learning performance and metabolic stress resilience are positively associated. PloS one. 2010; 5:e9740.