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Oxidative Medicine and Cellular Longevity
Volume 2013 (2013), Article ID 528935, 11 pages
http://dx.doi.org/10.1155/2013/528935
Review Article

Effects of Caloric Restriction on Cardiac Oxidative Stress and Mitochondrial Bioenergetics: Potential Role of Cardiac Sirtuins

Division of Geriatric Medicine, Department of Internal Medicine, Keio University School of Medicine, 35 Shinanomachi, Shinjuku-ku, Tokyo 160-8582, Japan

Received 10 February 2013; Accepted 18 February 2013

Academic Editor: Nilanjana Maulik

Copyright © 2013 Ken Shinmura. 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. K. Jin, “Modern biological theories of aging,” Aging and Disease, vol. 1, no. 2, pp. 72–74, 2010.
  2. B. R. Troen, “The biology of aging,” Mount Sinai Journal of Medicine, vol. 70, no. 1, pp. 3–22, 2003. View at Scopus
  3. K. B. Beckman and B. N. Ames, “The free radical theory of aging matures,” Physiological Reviews, vol. 78, no. 2, pp. 547–581, 1998. View at Scopus
  4. D. Harman, “Aging: a theory based on free radical and radiation chemistry,” Journal of Gerontology, vol. 11, no. 3, pp. 298–300, 1956. View at Scopus
  5. R. S. Sohal, “Role of oxidative stress and protein oxidation in the aging process,” Free Radical Biology and Medicine, vol. 33, no. 1, pp. 37–44, 2002. View at Publisher · View at Google Scholar · View at Scopus
  6. A. W. Linnane, S. Marzuki, T. Ozawa, and M. Tanaka, “Mitochondrial DNA mutations as an important contributor to ageing and degenerative diseases,” Lancet, vol. 1, no. 8639, pp. 642–645, 1989. View at Scopus
  7. J. Miquel, A. C. Economos, J. Fleming, and J. E. Johnson, “Mitochondrial role in cell aging,” Experimental Gerontology, vol. 15, no. 6, pp. 575–591, 1980. View at Publisher · View at Google Scholar · View at Scopus
  8. S. Judge and C. Leeuwenburgh, “Cardiac mitochondrial bioenergetics, oxidative stress, and aging,” American Journal of Physiology, vol. 292, no. 6, pp. C1983–C1992, 2007. View at Publisher · View at Google Scholar · View at Scopus
  9. G. Lenaz, C. Bovina, M. D'Aurelio et al., “Role of mitochondria in oxidative stress and aging,” Annals of the New York Academy of Sciences, vol. 959, pp. 199–213, 2002. View at Scopus
  10. G. López-Lluch, P. M. Irusta, P. Navas, and R. de Cabo, “Mitochondrial biogenesis and healthy aging,” Experimental Gerontology, vol. 43, no. 9, pp. 813–819, 2008. View at Publisher · View at Google Scholar · View at Scopus
  11. B. J. Merry, “Oxidative stress and mitochondrial function with aging—the effects of calorie restriction,” Aging Cell, vol. 3, no. 1, pp. 7–12, 2004. View at Publisher · View at Google Scholar · View at Scopus
  12. M. H. Vendelbo and K. S. Nair, “Mitochondrial longevity pathways,” Biochimica et Biophysica Acta, vol. 1813, no. 4, pp. 634–644, 2011. View at Publisher · View at Google Scholar · View at Scopus
  13. E. J. Masoro, “Overview of caloric restriction and ageing,” Mechanisms of Ageing and Development, vol. 126, no. 9, pp. 913–922, 2005. View at Publisher · View at Google Scholar · View at Scopus
  14. R. S. Sohal and R. Weindruch, “Oxidative stress, caloric restriction, and aging,” Science, vol. 273, no. 5271, pp. 59–63, 1996. View at Scopus
  15. Z. Ungvari, C. Parrado-Fernandez, A. Csiszar, and R. De Cabo, “Mechanisms underlying caloric restriction and lifespan regulation: implications for vascular aging,” Circulation Research, vol. 102, no. 5, pp. 519–528, 2008. View at Publisher · View at Google Scholar · View at Scopus
  16. T. M. Hagen, R. Moreau, J. H. Suh, and F. Visioli, “Mitochondrial decay in the aging rat heart: evidence for improvement by dietary supplementation with acetyl-L-carnitine and/or lipoic acid,” Annals of the New York Academy of Sciences, vol. 959, pp. 491–507, 2002. View at Scopus
  17. W. C. Orr and R. S. Sohal, “Extension of life-span by overexpression of superoxide dismutase and catalase in Drosophila melanogaster,” Science, vol. 263, no. 5150, pp. 1128–1130, 1994. View at Scopus
  18. S. E. Schriner, N. J. Linford, G. M. Martin et al., “Medecine: extension of murine life span by overexpression of catalase targeted to mitochondria,” Science, vol. 308, no. 5730, pp. 1909–1911, 2005. View at Publisher · View at Google Scholar · View at Scopus
  19. T. J. Schulz, K. Zarse, A. Voigt, N. Urban, M. Birringer, and M. Ristow, “Glucose restriction extends Caenorhabditis elegans life span by inducing mitochondrial respiration and increasing oxidative stress,” Cell Metabolism, vol. 6, no. 4, pp. 280–293, 2007. View at Publisher · View at Google Scholar · View at Scopus
  20. G. Bjelakovic, D. Nikolova, L. L. Gluud, R. G. Simonetti, and C. Gluud, “Antioxidant supplements for prevention of mortality in healthy participants and patients with various diseases,” Cochrane Database of Systematic Reviews, no. 2, article CD007176, 2008. View at Scopus
  21. D. P. Vivekananthan, M. S. Penn, S. K. Sapp, A. Hsu, and E. J. Topol, “Use of antioxidant vitamins for the prevention of cardiovascular disease: meta-analysis of randomised trials,” Lancet, vol. 361, no. 9374, pp. 2017–2023, 2003. View at Publisher · View at Google Scholar · View at Scopus
  22. M. Ristow and K. Zarse, “How increased oxidative stress promotes longevity and metabolic health: the concept of mitochondrial hormesis (mitohormesis),” Experimental Gerontology, vol. 45, no. 6, pp. 410–418, 2010. View at Publisher · View at Google Scholar · View at Scopus
  23. D. C. Wallace, “A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: a dawn for evolutionary medicine,” Annual Review of Genetics, vol. 39, pp. 359–407, 2005. View at Publisher · View at Google Scholar · View at Scopus
  24. A. Boveris and B. Chance, “The mitochondrial generation of hydrogen peroxide. General properties and effect of hyperbaric oxygen,” Biochemical Journal, vol. 134, no. 3, pp. 707–716, 1973. View at Scopus
  25. S. K. Dhar and D. K. St Clair, “Manganese superoxide dismutase regulation and cancer,” Free Radical Biology and Medicine, vol. 52, no. 11-12, pp. 2209–2222, 2012. View at Publisher · View at Google Scholar
  26. M. K. Shigenaga, T. M. Hagen, and B. N. Ames, “Oxidative damage and mitochondrial decay in aging,” Proceedings of the National Academy of Sciences of the United States of America, vol. 91, no. 23, pp. 10771–10778, 1994. View at Publisher · View at Google Scholar · View at Scopus
  27. M. L. Hamilton, H. Van Remmen, J. A. Drake et al., “Does oxidative damage to DNA increase with age?” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 18, pp. 10469–10474, 2001. View at Publisher · View at Google Scholar · View at Scopus
  28. S. Anderson, A. T. Bankier, and B. G. Barrell, “Sequence and organization of the human mitochondrial genome,” Nature, vol. 290, no. 5806, pp. 457–465, 1981. View at Scopus
  29. M. J. Bibb, R. A. Van Etten, C. T. Wright, M. W. Walberg, and D. A. Clayton, “Sequence and gene organization of mouse mitochondrial DNA,” Cell, vol. 26, no. 2, part 2, pp. 167–180, 1981. View at Publisher · View at Google Scholar
  30. J. W. Palmer, B. Tandler, and C. L. Hoppel, “Biochemical properties of subsarcolemmal and interfibrillar mitochondria isolated from rat cardiac muscle,” Journal of Biological Chemistry, vol. 252, no. 23, pp. 8731–8739, 1977. View at Scopus
  31. J. W. Palmer, B. Tandler, and C. L. Hoppel, “Biochemical differences between subsarcolemmal and interfibrillar mitochondria from rat cardiac muscle: effects of procedural manipulations,” Archives of Biochemistry and Biophysics, vol. 236, no. 2, pp. 691–702, 1985. View at Scopus
  32. S. W. Fannin, E. J. Lesnefsky, T. J. Slabe, M. O. Hassan, and C. L. Hoppel, “Aging selectively decreases oxidative capacity in rat heart interfibrillar mitochondria,” Archives of Biochemistry and Biophysics, vol. 372, no. 2, pp. 399–407, 1999. View at Publisher · View at Google Scholar · View at Scopus
  33. S. Judge, M. J. Young, A. Smith, T. Hagen, and C. Leeuwenburgh, “Age-associated increases in oxidative stress and antioxidant enzyme activities in cardiac interfibrillar mitochondria: implications for the mitochondrial theory of aging,” The FASEB Journal, vol. 19, no. 3, pp. 419–421, 2005. View at Publisher · View at Google Scholar · View at Scopus
  34. E. J. Lesnefsky, T. I. Gudz, S. Moghaddas et al., “Aging decreases electron transport complex III activity in heart interfibrillar mitochondria by alteration of the cytochrome c binding site,” Journal of Molecular and Cellular Cardiology, vol. 33, no. 1, pp. 37–47, 2001. View at Publisher · View at Google Scholar · View at Scopus
  35. T. Cocco, P. Sgobbo, M. Clemente et al., “Tissue-specific changes of mitochondrial functions in aged rats: effect of a long-term dietary treatment with N-acetylcysteine,” Free Radical Biology and Medicine, vol. 38, no. 6, pp. 796–805, 2005. View at Publisher · View at Google Scholar · View at Scopus
  36. E. Delaval, M. Perichon, and B. Friguet, “Age-related impairment of mitochondrial matrix aconitase and ATP-stimulated protease in rat liver and heart,” European Journal of Biochemistry, vol. 271, no. 22, pp. 4559–4564, 2004. View at Publisher · View at Google Scholar · View at Scopus
  37. M. S. Manzelmann and H. J. Harmon, “Lack of age-dependent changes in rat heart mitochondria,” Mechanisms of Ageing and Development, vol. 39, no. 3, pp. 281–288, 1987. View at Scopus
  38. L. Yan, H. Ge, H. Li et al., “Gender-specific proteomic alterations in glycolytic and mitochondrial pathways in aging monkey hearts,” Journal of Molecular and Cellular Cardiology, vol. 37, no. 5, pp. 921–929, 2004. View at Publisher · View at Google Scholar · View at Scopus
  39. A. L. Andreu, M. A. Arbos, A. Perez-Martos et al., “Reduced mitochondrial DNA transcription in senescent rat heart,” Biochemical and Biophysical Research Communications, vol. 252, no. 3, pp. 577–581, 1998. View at Publisher · View at Google Scholar · View at Scopus
  40. C. Castelluccio, A. Baracca, R. Fato et al., “Mitochondrial activities of rat heart during ageing,” Mechanisms of Ageing and Development, vol. 76, no. 2-3, pp. 73–88, 1994. View at Publisher · View at Google Scholar · View at Scopus
  41. L. K. Kwong and R. S. Sohal, “Age-related changes in activities of mitochondrial electron transport complexes in various tissues of the mouse,” Archives of Biochemistry and Biophysics, vol. 373, no. 1, pp. 16–22, 2000. View at Publisher · View at Google Scholar · View at Scopus
  42. G. Lenaz, C. Bovina, C. Castelluccio et al., “Mitochondrial complex I defects in aging,” Molecular and Cellular Biochemistry, vol. 174, no. 1-2, pp. 329–333, 1997. View at Publisher · View at Google Scholar · View at Scopus
  43. Ò. Miró, J. Casademont, E. Casals et al., “Aging is associated with increased lipid peroxidation in human hearts, but not with mitochondrial respiratory chain enzyme defects,” Cardiovascular Research, vol. 47, no. 3, pp. 624–631, 2000. View at Publisher · View at Google Scholar · View at Scopus
  44. G. Petrosillo, M. Matera, N. Moro, F. M. Ruggiero, and G. Paradies, “Mitochondrial complex I dysfunction in rat heart with aging: critical role of reactive oxygen species and cardiolipin,” Free Radical Biology and Medicine, vol. 46, no. 1, pp. 88–94, 2009. View at Publisher · View at Google Scholar · View at Scopus
  45. S. Sugiyama, M. Takasawa, M. Hayakawa, and T. Ozawa, “Changes in skeletal muscle, heart and liver mitochondrial electron transport activities in rats and dogs of various ages,” Biochemistry and Molecular Biology International, vol. 30, no. 5, pp. 937–944, 1993. View at Scopus
  46. M. Takasawa, M. Hayakawa, S. Sugiyama, K. Hattori, T. Ito, and T. Ozawa, “Age-associated damage in mitochondrial function in rat hearts,” Experimental Gerontology, vol. 28, no. 3, pp. 269–280, 1993. View at Publisher · View at Google Scholar · View at Scopus
  47. R. Gredilla, A. Sanz, M. Lopez-Torres, and G. Barja, “Caloric restriction decreases mitochondrial free radical generation at complex I and lowers oxidative damage to mitochondrial DNA in the rat heart,” The FASEB Journal, vol. 15, no. 9, pp. 1589–1591, 2001. View at Scopus
  48. T. Ozawa, “Genetic and functional changes in mitochondria associated with aging,” Physiological Reviews, vol. 77, no. 2, pp. 425–464, 1997. View at Scopus
  49. L. A. Gómez, J. S. Monette, J. D. Chavez, C. S. Maier, and T. M. Hagen, “Supercomplexes of the mitochondrial electron transport chain decline in the aging rat heart,” Archives of Biochemistry and Biophysics, vol. 490, no. 1, pp. 30–35, 2009. View at Publisher · View at Google Scholar · View at Scopus
  50. E. J. Lesnefsky, P. Minkler, and C. L. Hoppel, “Enhanced modification of cardiolipin during ischemia in the aged heart,” Journal of Molecular and Cellular Cardiology, vol. 46, no. 6, pp. 1008–1015, 2009. View at Publisher · View at Google Scholar · View at Scopus
  51. G. Paradies, F. M. Ruggiero, G. Petrosillo, and E. Quagliariello, “Peroxidative damage to cardiac mitochondria: cytochrome oxidase and cardiolipin alterations,” FEBS Letters, vol. 424, no. 3, pp. 155–158, 1998. View at Publisher · View at Google Scholar · View at Scopus
  52. S. M. K. Davies, A. Poljak, M. W. Duncan, G. A. Smythe, and M. P. Murphy, “Measurements of protein carbonyls, ortho- and meta-tyrosine and oxidative phosphorylation complex activity in mitochondria from young and old rats,” Free Radical Biology and Medicine, vol. 31, no. 2, pp. 181–190, 2001. View at Publisher · View at Google Scholar · View at Scopus
  53. E. Guerrieri, G. Capozza, A. Fratello, F. Zanotti, and S. Papa, “Functional and molecular changes in F0F1 ATP-synthase of cardiac muscle during aging,” Cardioscience, vol. 4, no. 2, pp. 93–98, 1993. View at Scopus
  54. C. S. Yarian, D. Toroser, and R. S. Sohal, “Aconitase is the main functional target of aging in the citric acid cycle of kidney mitochondria from mice,” Mechanisms of Ageing and Development, vol. 127, no. 1, pp. 79–84, 2006. View at Publisher · View at Google Scholar · View at Scopus
  55. J. Kanski, A. Behring, J. Pelling, and C. Schöneich, “Proteomic identification of 3-nitrotyrosine-containing rat cardiac proteins: effects of biological aging,” American Journal of Physiology, vol. 288, no. 1, pp. H371–H381, 2005. View at Publisher · View at Google Scholar · View at Scopus
  56. K. B. Choksi, J. E. Nuss, J. H. DeFord, and J. Papaconstantinou, “Age-related alterations in oxidatively damaged proteins of mouse skeletal muscle mitochondrial electron transport chain complexes,” Free Radical Biology and Medicine, vol. 45, no. 6, pp. 826–838, 2008. View at Publisher · View at Google Scholar · View at Scopus
  57. J. Chang, J. E. Cornell, H. Van Remmen, K. Hakala, W. F. Ward, and A. Richardson, “Effect of aging and caloric restriction on the mitochondrial proteome,” Journals of Gerontology A, vol. 62, no. 3, pp. 223–234, 2007. View at Scopus
  58. K. Shinmura, “Post-translational modification of mitochondrial proteins by caloric restriction: possible involvement in caloric restriction-induced cardioprotection,” Trends in Cardiovascular Medicine, vol. 23, no. 1, pp. 18–25, 2013. View at Publisher · View at Google Scholar
  59. G. Barja and A. Herrero, “Oxidative damage to mitochondrial DNA is inversely related to maximum life span in the heart and brain of mammals,” The FASEB Journal, vol. 14, no. 2, pp. 312–318, 2000. View at Scopus
  60. E. R. Stadtman, “Protein oxidation in aging and age-related diseases,” Annals of the New York Academy of Sciences, vol. 928, pp. 22–38, 2001. View at Scopus
  61. J. J. Chen and B. P. Yu, “Alterations in mitochondrial membrane fluidity by lipid peroxidation products,” Free Radical Biology and Medicine, vol. 17, no. 5, pp. 411–418, 1994. View at Publisher · View at Google Scholar · View at Scopus
  62. R. M. Anson, D. L. Croteau, R. H. Stierum, C. Filburn, R. Parsell, and V. A. Bohr, “Homogenous repair of singlet oxygen-induced DNA damage in differentially transcribed regions and strands of human mitochondrial DNA,” Nucleic Acids Research, vol. 26, no. 2, pp. 662–668, 1998. View at Publisher · View at Google Scholar · View at Scopus
  63. N. C. Souza-Pinto, D. L. Croteau, E. K. Hudson, R. G. Hansford, and V. A. Bohr, “Age-associated increase in 8-oxo-deoxyguanosine glycosylase/AP lyase activity in rat mitochondria,” Nucleic Acids Research, vol. 27, no. 8, pp. 1935–1942, 1999. View at Publisher · View at Google Scholar · View at Scopus
  64. L. L. Ji, D. Dillon, and E. Wu, “Myocardial aging: antioxidant enzyme systems and related biochemical properties,” American Journal of Physiology, vol. 261, no. 2, pp. R386–R392, 1991. View at Scopus
  65. S. Phaneuf and C. Leeuwenburgh, “Cytochrome c release from mitochondria in the aging heart: a possible mechanism for apoptosis with age,” American Journal of Physiology, vol. 282, no. 2, pp. R423–R430, 2002. View at Scopus
  66. G. R. Budas, M. H. Disatnik, and D. Mochly-Rosen, “Aldehyde dehydrogenase 2 in cardiac protection: a new therapeutic target?” Trends in Cardiovascular Medicine, vol. 19, no. 5, pp. 158–164, 2009. View at Publisher · View at Google Scholar · View at Scopus
  67. B. Friguet, E. R. Stadtman, and L. I. Szweda, “Modification of glucose-6-phosphate dehydrogenase by 4-hydroxy-2-nonenal. Formation of cross-linked protein that inhibits the multicatalytic protease,” Journal of Biological Chemistry, vol. 269, no. 34, pp. 21639–21643, 1994. View at Scopus
  68. K. Okada, C. Wangpoengtrakul, T. Osawa, S. Toyokuni, K. Tanaka, and K. Uchida, “4-Hydroxy-2-nonenal-mediated impairment of intracellular proteolysis during oxidative stress. Identification of proteasomes as target molecules,” Journal of Biological Chemistry, vol. 274, no. 34, pp. 23787–23793, 1999. View at Publisher · View at Google Scholar · View at Scopus
  69. J. Endo, M. Sano, T. Katayama et al., “Metabolic remodeling induced by mitochondrial aldehyde stress stimulates tolerance to oxidative stress in the heart,” Circulation Research, vol. 105, no. 11, pp. 1118–1127, 2009. View at Publisher · View at Google Scholar · View at Scopus
  70. S. Adams, P. Green, R. Claxton et al., “Reactive carbonyl formation by oxidative and non-oxidative pathways,” Front Biosci, vol. 6, pp. A17–A24, 2001. View at Scopus
  71. K. Shinmura, K. Tamaki, M. Sano et al., “Impact of long-term caloric restriction on cardiac senescence: caloric restriction ameliorates cardiac diastolic dysfunction associated with aging,” Journal of Molecular and Cellular Cardiology, vol. 50, no. 1, pp. 117–127, 2011. View at Publisher · View at Google Scholar · View at Scopus
  72. R. Pamplona, M. Portero-Otín, J. Requena, R. Gredilla, and G. Barja, “Oxidative, glycoxidative and lipoxidative damage to rat heart mitochondrial proteins is lower after 4 months of caloric restriction than in age-matched controls,” Mechanisms of Ageing and Development, vol. 123, no. 11, pp. 1437–1446, 2002. View at Publisher · View at Google Scholar · View at Scopus
  73. K. Shinmura, “Cardiovascular protection afforded by caloric restriction: essential role of nitric oxide synthase,” Geriatrics and Gerontology International, vol. 11, no. 2, pp. 143–156, 2011. View at Publisher · View at Google Scholar · View at Scopus
  74. A. J. Lambert, B. Wang, J. Yardley, J. Edwards, and B. J. Merry, “The effect of aging and caloric restriction on mitochondrial protein density and oxygen consumption,” Experimental Gerontology, vol. 39, no. 3, pp. 289–295, 2004. View at Publisher · View at Google Scholar · View at Scopus
  75. B. Niemann, Y. Chen, H. Issa, R. E. Silber, and S. Rohrbach, “Caloric restriction delays cardiac ageing in rats: role of mitochondria,” Cardiovascular Research, vol. 88, no. 2, pp. 267–276, 2010. View at Publisher · View at Google Scholar · View at Scopus
  76. A. Sanz, R. Gredilla, R. Pamplona et al., “Effect of insulin and growth hormone on rat heart and liver oxidative stress in control and caloric restricted animals,” Biogerontology, vol. 6, no. 1, pp. 15–26, 2005. View at Publisher · View at Google Scholar · View at Scopus
  77. X. Qiu, K. Brown, M. D. Hirschey, E. Verdin, and D. Chen, “Calorie restriction reduces oxidative stress by SIRT3-mediated SOD2 activation,” Cell Metabolism, vol. 12, no. 6, pp. 662–667, 2010. View at Publisher · View at Google Scholar · View at Scopus
  78. S. Someya, W. Yu, W. C. Hallows et al., “Sirt3 mediates reduction of oxidative damage and prevention of age-related hearing loss under caloric restriction,” Cell, vol. 143, no. 5, pp. 802–812, 2010. View at Publisher · View at Google Scholar · View at Scopus
  79. M. Abdellatif, “Sirtuins and pyridine nucleotides,” Circulation Research, vol. 111, no. 5, pp. 642–656, 2012. View at Publisher · View at Google Scholar
  80. R. H. Houtkooper, E. Pirinen, and J. Auwerx, “Sirtuins as regulators of metabolism and healthspan,” Nature Reviews Molecular Cell Biology, vol. 13, no. 4, pp. 225–238, 2012.
  81. T. Nakagawa and L. Guarente, “Sirtuins at a glance,” Journal of Cell Science, vol. 124, no. 6, pp. 833–838, 2011. View at Publisher · View at Google Scholar · View at Scopus
  82. B. Colom, J. Oliver, P. Roca, and F. J. Garcia-Palmer, “Caloric restriction and gender modulate cardiac muscle mitochondrial H2O2 production and oxidative damage,” Cardiovascular Research, vol. 74, no. 3, pp. 456–465, 2007. View at Publisher · View at Google Scholar · View at Scopus
  83. S. Judge, A. Judge, T. Grune, and C. Leeuwenburgh, “Short-term CR decreases cardiac mitochondrial oxidant production but increases carbonyl content,” American Journal of Physiology, vol. 286, no. 2, pp. R254–R259, 2004. View at Scopus
  84. K. Shinmura, K. Tamaki, M. Sano et al., “Caloric restriction primes mitochondria for ischemic stress by deacetylating specific mitochondrial proteins of the electron transport chain,” Circulation Research, vol. 109, no. 4, pp. 396–406, 2011. View at Publisher · View at Google Scholar
  85. E. Nisoli, C. Tonello, A. Cardile et al., “Cell biology: calorie restriction promotes mitochondrial biogenesis by inducing the expression of eNOS,” Science, vol. 310, no. 5746, pp. 314–317, 2005. View at Publisher · View at Google Scholar · View at Scopus
  86. M. Tanno, A. Kuno, T. Yano et al., “Induction of manganese superoxide dismutase by nuclear translocation and activation of SIRT1 promotes cell survival in chronic heart failure,” Journal of Biological Chemistry, vol. 285, no. 11, pp. 8375–8382, 2010. View at Publisher · View at Google Scholar · View at Scopus
  87. B. Drew, P. A. Dirks, C. Selman et al., “Effects of aging and caloric restriction on mitochondrial energy production in gastrocnemius muscle and heart,” American Journal of Physiology, vol. 284, no. 2, pp. R474–R480, 2003. View at Scopus
  88. K. Shinmura, K. Tamaki, and R. Bolli, “Impact of 6-mo caloric restriction on myocardial ischemic tolerance: possible involvement of nitric oxide-dependent increase in nuclear Sirt1,” American Journal of Physiology, vol. 295, no. 6, pp. H2348–H2355, 2008. View at Publisher · View at Google Scholar · View at Scopus
  89. M. M. Sung, C. L. Soltys, G. Masson, J. J. Boisvenue, and J. R. Dyck, “Improved cardiac metabolism and activation of the RISK pathway contributes to improved post-ischemic recovery in calorie restricted mice,” Journal of Molecular Medicine, vol. 89, no. 3, pp. 291–302, 2011. View at Publisher · View at Google Scholar · View at Scopus
  90. L. M. Hunt, E. W. Hogeland, M. K. Henry, and S. J. Swoap, “Hypotension and bradycardia during caloric restriction in mice are independent of salt balance and do not require ANP receptor,” American Journal of Physiology, vol. 287, no. 4, pp. H1446–H1451, 2004. View at Publisher · View at Google Scholar · View at Scopus
  91. J. B. Young, D. Mullen, and L. Landsberg, “Caloric restriction lowers blood pressure in the spontaneously hypertensive rat,” Metabolism, vol. 27, no. 12, pp. 1711–1714, 1978. View at Scopus
  92. L. Fontana, T. E. Meyer, S. Klein, and J. O. Holloszy, “Long-term calorie restriction is highly effective in reducing the risk for atherosclerosis in humans,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 17, pp. 6659–6663, 2004. View at Publisher · View at Google Scholar · View at Scopus
  93. I. Mattagajasingh, C. S. Kim, A. Naqvi et al., “SIRT1 promotes endothelium-dependent vascular relaxation by activating endothelial nitric oxide synthase,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 37, pp. 14855–14860, 2007. View at Publisher · View at Google Scholar · View at Scopus
  94. H. Ota, M. Akishita, M. Eto, K. Iijima, M. Kaneki, and Y. Ouchi, “Sirt1 modulates premature senescence-like phenotype in human endothelial cells,” Journal of Molecular and Cellular Cardiology, vol. 43, no. 5, pp. 571–579, 2007. View at Publisher · View at Google Scholar · View at Scopus
  95. A. E. Civitarese, S. Carling, L. K. Heilbronn et al., “Calorie restriction increases muscle mitochondrial biogenesis in healthy humans,” PLoS Medicine, vol. 4, no. 3, article e76, pp. 485–494, 2007. View at Publisher · View at Google Scholar · View at Scopus
  96. N. Basso, R. Cini, A. Pietrelli, L. Ferder, N. A. Terragno, and F. Inserra, “Protective effect of long-term angiotensin II inhibition,” American Journal of Physiology, vol. 293, no. 3, pp. H1351–H1358, 2007. View at Publisher · View at Google Scholar · View at Scopus
  97. A. Benigni, D. Corna, C. Zoja et al., “Disruption of the Ang II type 1 receptor promotes longevity in mice,” Journal of Clinical Investigation, vol. 119, no. 3, pp. 524–530, 2009. View at Publisher · View at Google Scholar · View at Scopus
  98. H. Massudi, R. Grant, N. Braidy, J. Guest, B. Farnsworth, and G. J. Guillemin, “Age-associated changes in oxidative stress and NAD+ metabolism in human tissue,” PLoS One, vol. 7, no. 7, Article ID e42357, 2012. View at Publisher · View at Google Scholar
  99. A. R. Collins, C. M. Gedik, B. Olmedilla, S. Southon, and M. Bellizzi, “Oxidative DNA damage measured in human lymphocytes: large differences between sexes and between countries, and correlations with heart disease mortality rates,” The FASEB Journal, vol. 12, no. 13, pp. 1397–1400, 1998. View at Scopus
  100. P. Voss and W. Siems, “Clinical oxidation parameters of aging,” Free Radical Research, vol. 40, no. 12, pp. 1339–1349, 2006. View at Publisher · View at Google Scholar · View at Scopus
  101. L. K. Heilbronn, L. De Jonge, M. I. Frisard et al., “Effect of 6-month calorie restriction on biomarkers of longevity, metabolic adaptation, and oxidative stress in overweight individuals: a randomized controlled trial,” Journal of the American Medical Association, vol. 295, no. 13, pp. 1539–1548, 2006. View at Publisher · View at Google Scholar · View at Scopus
  102. R. J. Colman, R. M. Anderson, S. C. Johnson et al., “Caloric restriction delays disease onset and mortality in rhesus monkeys,” Science, vol. 325, no. 5937, pp. 201–204, 2009. View at Publisher · View at Google Scholar · View at Scopus
  103. J. A. Mattison, G. S. Roth, T. Mark Beasley et al., “Impact of caloric restriction on health and survival in rhesus monkeys from the NIA study,” Nature, vol. 489, no. 7415, pp. 318–321, 2012. View at Publisher · View at Google Scholar
  104. T. A. Zainal, T. D. Oberley, D. B. Allison, L. I. Szweda, and R. Weindruch, “Caloric restriction of rhesus monkeys lowers oxidative damage in skeletal muscle,” The FASEB Journal, vol. 14, no. 12, pp. 1825–1836, 2000. View at Scopus
  105. T. Yamamoto and J. Sadoshima, “Protection of the heart against ischemia/reperfusion by silent information regulator 1,” Trends in Cardiovascular Medicine, vol. 21, no. 1, pp. 27–32, 2011. View at Publisher · View at Google Scholar
  106. H. Ota, M. Eto, S. Ogawa, K. Iijima, M. Akishita, and Y. Ouchi, “Sirt1/eNOS axis as a potential target against vascular senescence, dysfunction and atherosclerosis,” Journal of Atherosclerosis and Thrombosis, vol. 17, no. 5, pp. 431–435, 2010. View at Scopus
  107. V. W. Dolinsky and J. R. Dyck, “Calorie restriction and resveratrol in cardiovascular health and disease,” Biochim Biophys Acta, vol. 1812, no. 11, pp. 1477–1489, 2011. View at Publisher · View at Google Scholar
  108. N. L. Price, A. P. Gomes, A. J. Y. Ling et al., “SIRT1 is required for AMPK activation and the beneficial effects of resveratrol on mitochondrial function,” Cell Metabolism, vol. 15, no. 5, pp. 675–690, 2012. View at Publisher · View at Google Scholar