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Oxidative Medicine and Cellular Longevity
Volume 2018, Article ID 1941285, 23 pages
https://doi.org/10.1155/2018/1941285
Review Article

The Good, the Bad, and the Ugly of ROS: New Insights on Aging and Aging-Related Diseases from Eukaryotic and Prokaryotic Model Organisms

1Institut National de la Santé et de la Recherche Médicale, U1001 & Université Paris Descartes, Sorbonne Paris Cité, Paris, France
2Defence Institute of Physiology and Allied Sciences, DRDO, New Delhi, India

Correspondence should be addressed to Ana L. Santos; rf.mresni@sotnas.ana

Received 4 August 2017; Revised 18 December 2017; Accepted 2 January 2018; Published 18 March 2018

Academic Editor: Sergio Di Meo

Copyright © 2018 Ana L. Santos 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. L. Partridge and D. Gems, “Mechanisms of ageing: public or private?” Nature Reviews Genetic, vol. 3, no. 3, pp. 165–175, 2002. View at Publisher · View at Google Scholar · View at Scopus
  2. P. Davalli, T. Mitic, A. Caporali, A. Lauriola, and D. D’Arca, “ROS, cell senescence, and novel molecular mechanisms in aging and age-related diseases,” Oxidative Medicine and Cellular Longevity, vol. 2016, Article ID 3565127, 18 pages, 2016. View at Publisher · View at Google Scholar · View at Scopus
  3. World Health Organization, “World report on aging and health,” Tech. Rep., 2015. View at Google Scholar
  4. E. A. Kikis, T. Gidalevitz, and R. I. Morimoto, “Protein homeostasis in models of aging and age-related conformational disease,” Experimental Medicine and Biology, vol. 694, pp. 138–159, 2010. View at Publisher · View at Google Scholar · View at Scopus
  5. K. Jin, J. W. Simpkins, X. Ji, M. Leis, and I. Stambler, “The critical need to promote research of aging and aging-related diseases to improve health and longevity of the elderly population,” Aging and Disease, vol. 6, no. 1, pp. 1–5, 2015. View at Publisher · View at Google Scholar · View at Scopus
  6. R. J. Mailloux, “Teaching the fundamentals of electron transfer reactions in mitochondria and the production and detection of reactive oxygen species,” Redox Biology, vol. 4, pp. 381–398, 2015. View at Publisher · View at Google Scholar · View at Scopus
  7. 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 Publisher · View at Google Scholar
  8. K. Krumova and G. Cosa, “Chapter 1. Overview of reactive oxygen species,” in Singlet Oxygen: Applications in Biosciences and Nanosciences, Volume 1, pp. 1–21, The Royal Society of Chemistry, 2016. View at Publisher · View at Google Scholar
  9. V. K. Koltover, “Free radical timer of aging: from chemistry of free radicals to systems theory of reliability,” Current Aging Science, vol. 10, no. 1, pp. 12–17, 2017. View at Publisher · View at Google Scholar · View at Scopus
  10. G. Barja, “Chapter one - The mitochondrial free radical theory of aging,” in The Mitochondrion in Aging and Disease, pp. 1–27, Academic Press, 2014. View at Publisher · View at Google Scholar · View at Scopus
  11. M. Ristow and S. Schmeisser, “Extending life span by increasing oxidative stress,” Free Radical Biology and Medicine, vol. 51, no. 2, pp. 327–336, 2011. View at Publisher · View at Google Scholar · View at Scopus
  12. J. M. Van Raamsdonk and S. Hekimi, “Superoxide dismutase is dispensable for normal animal lifespan,” Proceedings of the National Academy of Sciences, vol. 109, no. 15, pp. 5785–5790, 2012. View at Publisher · View at Google Scholar · View at Scopus
  13. J. Lapointe and S. Hekimi, “When a theory of aging ages badly,” Cellular and Molecular Life Sciences, vol. 67, no. 1, pp. 1–8, 2010. View at Publisher · View at Google Scholar · View at Scopus
  14. D. Gems and R. Doonan, “Antioxidant defense and aging in C. elegans: is the oxidative damage theory of aging wrong?” Cell Cycle, vol. 8, no. 11, pp. 1681–1687, 2009. View at Publisher · View at Google Scholar · View at Scopus
  15. 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
  16. M. Ristow and K. Schmeisser, “Mitohormesis: promoting health and lifespan by increased levels of reactive oxygen species (ROS),” Dose-Response, vol. 12, no. 2, pp. 288–341, 2014. View at Publisher · View at Google Scholar · View at Scopus
  17. T. Ogawa, Y. Kodera, D. Hirata, T. K. Blackwell, and M. Mizunuma, “Natural thioallyl compounds increase oxidative stress resistance and lifespan in Caenorhabditis elegans by modulating SKN-1/Nrf,” Scientific Reports, vol. 6, no. 1, pp. 1–13, 2016. View at Publisher · View at Google Scholar · View at Scopus
  18. N. Fischer, C. Büchter, K. Koch, S. Albert, R. Csuk, and W. Wätjen, “The resveratrol derivatives trans-3,5-dimethoxy-4-fluoro-4-hydroxystilbene and trans-2,4,5-trihydroxystilbene decrease oxidative stress and prolong lifespan in Caenorhabditis elegans,” Journal of Pharmacy and Pharmacology, vol. 69, no. 1, pp. 73–81, 2017. View at Publisher · View at Google Scholar · View at Scopus
  19. J. M. Van Raamsdonk and S. Hekimi, “Deletion of the mitochondrial superoxide dismutase sod-2 extends lifespan in Caenorhabditis elegans,” PLoS Genetics, vol. 5, no. 2, article e1000361, 2009. View at Publisher · View at Google Scholar · View at Scopus
  20. W. Yang and S. Hekimi, “A mitochondrial superoxide signal triggers increased longevity in Caenorhabditis elegans,” PLoS Biology, vol. 8, no. 12, article e1000556, 2010. View at Publisher · View at Google Scholar · View at Scopus
  21. M. Holzenberger, J. Dupont, B. Ducos et al., “IGF-1 receptor regulates lifespan and resistance to oxidative stress in mice,” Nature, vol. 421, no. 6919, pp. 182–187, 2002. View at Publisher · View at Google Scholar · View at Scopus
  22. E. Migliaccio, M. Giorgio, S. Mele et al., “The p66shc adaptor protein controls oxidative stress response and life span in mammals,” Nature, vol. 402, no. 6759, pp. 309–313, 1999. View at Publisher · View at Google Scholar · View at Scopus
  23. Y. Zhang, A. Unnikrishnan, S. S. Deepa et al., “A new role for oxidative stress in aging: the accelerated aging phenotype in Sod1-/- mice is correlated to increased cellular senescence,” Redox Biology, vol. 11, pp. 30–37, 2017. View at Publisher · View at Google Scholar · View at Scopus
  24. S. E. Schriner, N. J. Linford, G. M. Martin et al., “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
  25. P. M. Treuting, N. J. Linford, S. E. Knoblaugh et al., “Reduction of age-associated pathology in old mice by overexpression of catalase in mitochondria,” The Journals of Gerontology Series A: Biological Sciences and Medical Sciences, vol. 63, no. 8, pp. 813–822, 2008. View at Publisher · View at Google Scholar
  26. T. T. Huang, E. J. Carlson, A. M. Gillespie, Y. Shi, and C. J. Epstein, “Ubiquitous overexpression of CuZn superoxide dismutase does not extend life span in mice,” The Journals of Gerontology Series A: Biological Sciences and Medical Sciences, vol. 55, pp. B5–B9, 2000. View at Publisher · View at Google Scholar
  27. V. I. Perez, H. Van Remmen, A. Bokov, C. J. Epstein, J. Vijg, and A. Richardson, “The overexpression of major antioxidant enzymes does not extend the lifespan of mice,” Aging Cell, vol. 8, no. 1, pp. 73–75, 2009. View at Publisher · View at Google Scholar · View at Scopus
  28. Y. S. Ho, J. L. Magnenat, R. T. Bronson et al., “Mice deficient in cellular glutathione peroxidase develop normally and show no increased sensitivity to hyperoxia,” Journal of Biological Chemistry, vol. 272, no. 26, pp. 16644–16651, 1997. View at Publisher · View at Google Scholar · View at Scopus
  29. Y. Zhang, Y. Ikeno, W. Qi et al., “Mice deficient in both Mn superoxide dismutase and glutathione peroxidase-1 have increased oxidative damage and a greater incidence of pathology but no reduction in longevity,” The Journals of Gerontology Series A: Biological Sciences and Medical Sciences, vol. 64A, no. 12, pp. 1212–1220, 2009. View at Publisher · View at Google Scholar · View at Scopus
  30. M. Soerensen, K. Christensen, T. Stevnsner, and L. Christiansen, “The Mn-superoxide dismutase single nucleotide polymorphism rs4880 and the glutathione peroxidase 1 single nucleotide polymorphism rs1050450 are associated with aging and longevity in the oldest old,” Mechanisms of Ageing and Development, vol. 130, no. 5, pp. 308–314, 2009. View at Publisher · View at Google Scholar · View at Scopus
  31. S.-E. Yoo, L. Chen, R. Na et al., “Gpx4 ablation in adult mice results in a lethal phenotype accompanied by neuronal loss in brain,” Free Radical Biology and Medicine, vol. 52, no. 9, pp. 1820–1827, 2012. View at Publisher · View at Google Scholar · View at Scopus
  32. Q. Ran, H. Liang, M. Gu et al., “Transgenic mice overexpressing glutathione peroxidase 4 are protected against oxidative stress-induced apoptosis,” Journal of Biological Chemistry, vol. 279, no. 53, pp. 55137–55146, 2004. View at Publisher · View at Google Scholar · View at Scopus
  33. V. I. Pérez, A. Bokov, H. Van Remmen et al., “Is the oxidative stress theory of aging dead?” Biochimica et Biophysica Acta (BBA) - General Subjects, vol. 1790, no. 10, pp. 1005–1014, 2009. View at Publisher · View at Google Scholar · View at Scopus
  34. L. Nonn, R. R. Williams, R. P. Erickson, and G. Powis, “The absence of mitochondrial thioredoxin 2 causes massive apoptosis, exencephaly, and early embryonic lethality in homozygous mice,” Molecular and Cellular Biology, vol. 23, no. 3, pp. 916–922, 2003. View at Publisher · View at Google Scholar · View at Scopus
  35. V. I. Pérez, C. M. Lew, L. A. Cortez et al., “Thioredoxin 2 haploinsufficiency in mice results in impaired mitochondrial function and increased oxidative stress,” Free Radical Biology and Medicine, vol. 44, no. 5, pp. 882–892, 2008. View at Publisher · View at Google Scholar · View at Scopus
  36. V. I. Pérez, L. A. Cortez, C. M. Lew et al., “Thioredoxin 1 overexpression extends mainly the earlier part of life span in mice,” The Journals of Gerontology Series A: Biological Sciences and Medical Sciences, vol. 66A, no. 12, pp. 1286–1299, 2011. View at Publisher · View at Google Scholar · View at Scopus
  37. C. E. Schaar, D. J. Dues, K. K. Spielbauer et al., “Mitochondrial and cytoplasmic ROS have opposing effects on lifespan,” PLOS Genetics, vol. 11, no. 2, article e1004972, 2015. View at Publisher · View at Google Scholar · View at Scopus
  38. F. Scialò, A. Sriram, D. Fernández-Ayala et al., “Mitochondrial ROS produced via reverse electron transport extend animal lifespan,” Cell Metabolism, vol. 23, no. 4, pp. 725–734, 2016. View at Publisher · View at Google Scholar · View at Scopus
  39. X. Liu, N. Jiang, B. Hughes, E. Bigras, E. Shoubridge, and S. Hekimi, “Evolutionary conservation of the clk-1-dependent mechanism of longevity: loss of mclk1 increases cellular fitness and lifespan in mice,” Genes & Development, vol. 19, no. 20, pp. 2424–2434, 2005. View at Publisher · View at Google Scholar · View at Scopus
  40. C. Dell'Agnello, S. Leo, A. Agostino et al., “Increased longevity and refractoriness to Ca(2+)-dependent neurodegeneration in Surf1 knockout mice,” Human Molecular Genetics, vol. 16, no. 4, pp. 431–444, 2007. View at Publisher · View at Google Scholar · View at Scopus
  41. J. M. Van Raamsdonk, Y. Meng, D. Camp et al., “Decreased energy metabolism extends life span in Caenorhabditis elegans without reducing oxidative damage,” Genetics, vol. 185, no. 2, pp. 559–571, 2010. View at Publisher · View at Google Scholar · View at Scopus
  42. T. Lindahl and D. E. Barnes, “Repair of Endogenous DNA Damage,” Cold Spring Harbor Symposia on Quantitative Biology, vol. 65, no. 0, pp. 127–134, 2000. View at Publisher · View at Google Scholar
  43. H. L. Gensler and H. Bernstein, “DNA damage as the primary cause of aging,” The Quarterly Review of Biology, vol. 56, no. 3, pp. 279–303, 1981. View at Publisher · View at Google Scholar · View at Scopus
  44. L. Szilard, “On the nature of the aging process,” Proceedings of the National Academy of Sciences, vol. 45, no. 1, pp. 30–45, 1959. View at Publisher · View at Google Scholar
  45. M. M. Vilenchik and A. G. Knudson, “Inverse radiation dose-rate effects on somatic and germ-line mutations and DNA damage rates,” Proceedings of the National Academy of Sciences, vol. 97, no. 10, pp. 5381–5386, 2000. View at Publisher · View at Google Scholar · View at Scopus
  46. T. Lindahl and B. Nyberg, “Heat-induced deamination of cytosine residues in deoxyribonucleic acid,” Biochemistry, vol. 13, no. 16, pp. 3405–3410, 1974. View at Publisher · View at Google Scholar · View at Scopus
  47. T. Lindahl and B. Nyberg, “Rate of depurination of native deoxyribonucleic acid,” Biochemistry, vol. 11, no. 19, pp. 3610–3618, 1974. View at Publisher · View at Google Scholar · View at Scopus
  48. F. R. de Gruijl and H. Rebel, “Early events in UV carcinogenesis--DNA damage, target cells and mutant p53 foci,” Photochemistry and Photobiology, vol. 84, no. 2, pp. 382–387, 2008. View at Publisher · View at Google Scholar · View at Scopus
  49. M. C. Poirier, R. M. Santella, and A. Weston, “Carcinogen macromolecular adducts and their measurement,” Carcinogenesis, vol. 21, no. 3, pp. 353–359, 2000. View at Publisher · View at Google Scholar
  50. K. A. Cimprich and D. Cortez, “ATR: an essential regulator of genome integrity,” Nature Reviews Molecular Cell Biology, vol. 9, no. 8, pp. 616–627, 2008. View at Publisher · View at Google Scholar · View at Scopus
  51. F. Lazzaro, M. Giannattasio, F. Puddu et al., “Checkpoint mechanisms at the intersection between DNA damage and repair,” DNA Repair, vol. 8, no. 9, pp. 1055–1067, 2009. View at Publisher · View at Google Scholar · View at Scopus
  52. S. Dukan, A. Farewell, M. Ballesteros, F. Taddei, M. Radman, and T. Nyström, “Protein oxidation in response to increased transcriptional or translational errors,” Proceedings of the National Academy of Sciences, vol. 97, no. 11, pp. 5746–5749, 2000. View at Publisher · View at Google Scholar · View at Scopus
  53. K. Tanaka, “The proteasome: overview of structure and functions,” Proceedings of the Japan Academy, Series B, vol. 85, no. 1, pp. 12–36, 2009. View at Publisher · View at Google Scholar · View at Scopus
  54. T. Jung, N. Bader, and T. Grune, “Oxidized proteins: intracellular distribution and recognition by the proteasome,” Archives of Biochemistry and Biophysics, vol. 462, no. 2, pp. 231–237, 2007. View at Publisher · View at Google Scholar · View at Scopus
  55. P. Fortini, B. Pascucci, E. Parlanti, M. D'Errico, V. Simonelli, and E. Dogliotti, “8-Oxoguanine DNA damage: at the crossroad of alternative repair pathways,” Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis, vol. 531, no. 1-2, pp. 127–139, 2003. View at Publisher · View at Google Scholar · View at Scopus
  56. H. E. Krokan and M. Bjoras, “Base excision repair,” Cold Spring Harbor Perspectives in Biology, vol. 5, no. 4, article a012583, 2013. View at Publisher · View at Google Scholar · View at Scopus
  57. O. D. Scharer, “Nucleotide excision repair in eukaryotes,” Cold Spring Harbor Perspectives in Biology, vol. 5, no. 10, article a012609, 2013. View at Publisher · View at Google Scholar · View at Scopus
  58. M. R. Lieber, “The mechanism of double-strand DNA break repair by the nonhomologous DNA end-joining pathway,” Annual Review of Biochemistry, vol. 79, no. 1, pp. 181–211, 2010. View at Publisher · View at Google Scholar · View at Scopus
  59. J. K. Moore and J. E. Haber, “Cell cycle and genetic requirements of two pathways of nonhomologous end-joining repair of double-strand breaks in Saccharomyces cerevisiae,” Molecular and Cellular Biology, vol. 16, no. 5, pp. 2164–2173, 1996. View at Publisher · View at Google Scholar · View at Scopus
  60. G. Xu, M. Herzig, V. Rotrekl, and C. A. Walter, “Base excision repair, aging and health span,” Mechanisms of Ageing and Development, vol. 129, no. 7-8, pp. 366–382, 2008. View at Publisher · View at Google Scholar · View at Scopus
  61. R. Mostoslavsky, K. F. Chua, D. B. Lombard et al., “Genomic instability and aging-like phenotype in the absence of mammalian SIRT6,” Cell, vol. 124, no. 2, pp. 315–329, 2006. View at Publisher · View at Google Scholar · View at Scopus
  62. J. Kanungo, “DNA-dependent protein kinase and DNA repair: relevance to Alzheimer’s disease,” Alzheimer's Research & Therapy, vol. 5, no. 2, p. 13, 2013. View at Publisher · View at Google Scholar · View at Scopus
  63. V. N. Vyjayanti and K. S. Rao, “DNA double strand break repair in brain: reduced NHEJ activity in aging rat neurons,” Neuroscience Letters, vol. 393, no. 1, pp. 18–22, 2006. View at Publisher · View at Google Scholar · View at Scopus
  64. J. German, “Bloom syndrome: a mendelian prototype of somatic mutational disease,” Medicine, vol. 72, no. 6, pp. 393–406, 1993. View at Publisher · View at Google Scholar · View at Scopus
  65. C. J. Epstein, G. M. Martin, A. L. Schultz, and A. G. Motulsky, “A review of its symptomatology, natural history, pathologic features, genetics and relationship to the natural aging process,” Medicine, vol. 45, no. 3, pp. 177–221, 1966. View at Publisher · View at Google Scholar
  66. A. S. Balajee, A. Machwe, A. May et al., “The Werner syndrome protein is involved in RNA polymerase II transcription,” Molecular Biology of the Cell, vol. 10, no. 8, pp. 2655–2668, 1999. View at Publisher · View at Google Scholar · View at Scopus
  67. B. Li and L. Comai, “Functional interaction between Ku and the werner syndrome protein in DNA end processing,” Journal of Biological Chemistry, vol. 275, no. 37, pp. 28349–28352, 2000. View at Publisher · View at Google Scholar · View at Scopus
  68. P. Hasty, “The impact of DNA damage, genetic mutation and cellular responses on cancer prevention, longevity and aging: observations in humans and mice,” Mechanisms of Ageing and Development, vol. 126, no. 1, pp. 71–77, 2005. View at Publisher · View at Google Scholar · View at Scopus
  69. J. H. J. Hoeijmakers, “DNA damage, aging, and cancer,” New England Journal of Medicine, vol. 361, no. 15, pp. 1475–1485, 2009. View at Publisher · View at Google Scholar · View at Scopus
  70. K. Kashiyama, Y. Nakazawa, D. T. Pilz et al., “Malfunction of nuclease ERCC1-XPF results in diverse clinical manifestations and causes Cockayne syndrome, xeroderma pigmentosum, and Fanconi anemia,” The American Journal of Human Genetics, vol. 92, no. 5, pp. 807–819, 2013. View at Publisher · View at Google Scholar · View at Scopus
  71. L. J. Niedernhofer, G. A. Garinis, A. Raams et al., “A new progeroid syndrome reveals that genotoxic stress suppresses the somatotroph axis,” Nature, vol. 444, no. 7122, pp. 1038–1043, 2006. View at Publisher · View at Google Scholar · View at Scopus
  72. M. A. Blasco, “Telomere length, stem cells and aging,” Nature Chemical Biology, vol. 3, no. 10, pp. 640–649, 2007. View at Publisher · View at Google Scholar · View at Scopus
  73. H. Vallabhaneni, F. Zhou, R. W. Maul et al., “Defective repair of uracil causes telomere defects in mouse hematopoietic cells,” Journal of Biological Chemistry, vol. 290, no. 9, pp. 5502–5511, 2015. View at Publisher · View at Google Scholar · View at Scopus
  74. H. Vallabhaneni, N. O'Callaghan, J. Sidorova, and Y. Liu, “Defective repair of oxidative base lesions by the DNA glycosylase Nth1 associates with multiple telomere defects,” PLoS Genetics, vol. 9, no. 7, article e1003639, 2013. View at Publisher · View at Google Scholar · View at Scopus
  75. C. Richter, J. W. Park, and B. N. Ames, “Normal oxidative damage to mitochondrial and nuclear DNA is extensive,” Proceedings of the National Academy of Sciences, vol. 85, no. 17, pp. 6465–6467, 1988. View at Publisher · View at Google Scholar · View at Scopus
  76. S. P. Ledoux and G. L. Wilson, “Base excision repair of mitochondrial DNA damage in mammalian cells,” Progress in Nucleic Acid Research and Molecular Biology, vol. 68, pp. 273–284, 2001. View at Publisher · View at Google Scholar
  77. W. J. Driggers, S. P. LeDoux, and G. L. Wilson, “Repair of oxidative damage within the mitochondrial DNA of RINr 38 cells,” Journal of Biological Chemistry, vol. 268, no. 29, pp. 22042–22045, 1993. View at Google Scholar
  78. G. L. Dianov, N. Souza-Pinto, S. G. Nyaga, T. Thybo, T. Stevnsner, and V. A. Bohr, “Base excision repair in nuclear and mitochondrial DNA,” Progress in Nucleic Acid Research and Molecular Biology, vol. 68, pp. 285–297, 2001. View at Publisher · View at Google Scholar · View at Scopus
  79. J. A. Stuart, K. Hashiguchi, D. M. Wilson 3rd, W. C. Copeland, N. C. Souza-Pinto, and V. A. Bohr, “DNA base excision repair activities and pathway function in mitochondrial and cellular lysates from cells lacking mitochondrial DNA,” Nucleic Acids Research, vol. 32, no. 7, pp. 2181–2192, 2004. View at Publisher · View at Google Scholar · View at Scopus
  80. R. Chattopadhyay, L. Wiederhold, B. Szczesny et al., “Identification and characterization of mitochondrial abasic (AP)-endonuclease in mammalian cells,” Nucleic Acids Research, vol. 34, no. 7, pp. 2067–2076, 2006. View at Publisher · View at Google Scholar · View at Scopus
  81. A. Bender, K. J. Krishnan, C. M. Morris et al., “High levels of mitochondrial DNA deletions in substantia nigra neurons in aging and Parkinson disease,” Nature Genetics, vol. 38, no. 5, pp. 515–517, 2006. View at Publisher · View at Google Scholar · View at Scopus
  82. A. Trifunovic, A. Hansson, A. Wredenberg et al., “Somatic mtDNA mutations cause aging phenotypes without affecting reactive oxygen species production,” Proceedings of the National Academy of Sciences, vol. 102, no. 50, pp. 17993–17998, 2005. View at Publisher · View at Google Scholar · View at Scopus
  83. J. N. Octave, “Alzheimer disease: cellular and molecular aspects,” Bulletin et memoires de l’Academie royale de medecine de Belgique, vol. 160, pp. 441–445, 2005. View at Google Scholar
  84. A. Chomyn and G. Attardi, “MtDNA mutations in aging and apoptosis,” Biochemical and Biophysical Research Communications, vol. 304, no. 3, pp. 519–529, 2003. View at Publisher · View at Google Scholar · View at Scopus
  85. P. E. Coskun, M. F. Beal, and D. C. Wallace, “Alzheimer’s brains harbor somatic mtDNA control-region mutations that suppress mitochondrial transcription and replication,” Proceedings of the National Academy of Sciences, vol. 101, no. 29, pp. 10726–10731, 2004. View at Publisher · View at Google Scholar · View at Scopus
  86. M. T. Lin, D. K. Simon, C. H. Ahn, L. M. Kim, and M. F. Beal, “High aggregate burden of somatic mtDNA point mutations in aging and Alzheimer’s disease brain,” Human Molecular Genetics, vol. 11, no. 2, pp. 133–145, 2002. View at Publisher · View at Google Scholar
  87. T. Nystrom, “Role of oxidative carbonylation in protein quality control and senescence,” The EMBO Journal, vol. 24, no. 7, pp. 1311–1317, 2005. View at Publisher · View at Google Scholar · View at Scopus
  88. Y. J. Suzuki, M. Carini, and D. A. Butterfield, “Protein carbonylation,” Antioxidants & Redox Signaling, vol. 12, no. 3, pp. 323–325, 2010. View at Publisher · View at Google Scholar · View at Scopus
  89. Q. Chen, J. Thorpe, J. R. Dohmen, F. Li, and J. N. Keller, “Ump1 extends yeast lifespan and enhances viability during oxidative stress: central role for the proteasome?” Free Radical Biology and Medicine, vol. 40, no. 1, pp. 120–126, 2006. View at Publisher · View at Google Scholar · View at Scopus
  90. L. Knuppertz and H. D. Osiewacz, “Orchestrating the network of molecular pathways affecting aging: role of nonselective autophagy and mitophagy,” Mechanisms of Ageing and Development, vol. 153, pp. 30–40, 2016. View at Publisher · View at Google Scholar · View at Scopus
  91. Q. Zhao, J. Wang, I. V. Levichkin, S. Stasinopoulos, M. T. Ryan, and N. J. Hoogenraad, “A mitochondrial specific stress response in mammalian cells,” The EMBO Journal, vol. 21, no. 17, pp. 4411–4419, 2002. View at Publisher · View at Google Scholar · View at Scopus
  92. T. Yoneda, C. Benedetti, F. Urano, S. G. Clark, H. P. Harding, and D. Ron, “Compartment-specific perturbation of protein handling activates genes encoding mitochondrial chaperones,” Journal of Cell Science, vol. 117, no. 18, pp. 4055–4066, 2004. View at Publisher · View at Google Scholar · View at Scopus
  93. C. O'Neill, A. P. Kiely, M. F. Coakley, S. Manning, and C. M. Long-Smith, “Insulin and IGF-1 signalling: longevity, protein homoeostasis and Alzheimer’s disease,” Biochemical Society Transactions, vol. 40, no. 4, pp. 721–727, 2012. View at Publisher · View at Google Scholar · View at Scopus
  94. J. F. Morley and R. I. Morimoto, “Regulation of longevity in Caenorhabditis elegans by heat shock factor and molecular chaperones,” Molecular Biology of the Cell, vol. 15, no. 2, pp. 657–664, 2003. View at Publisher · View at Google Scholar · View at Scopus
  95. E. Cohen, J. Bieschke, R. M. Perciavalle, J. W. Kelly, and A. Dillin, “Opposing activities protect against age-onset proteotoxicity,” Science, vol. 313, no. 5793, pp. 1604–1610, 2006. View at Publisher · View at Google Scholar · View at Scopus
  96. S. Alavez, M. C. Vantipalli, D. J. S. Zucker, I. M. Klang, and G. J. Lithgow, “Amyloid-binding compounds maintain protein homeostasis during ageing and extend lifespan,” Nature, vol. 472, no. 7342, pp. 226–229, 2011. View at Publisher · View at Google Scholar · View at Scopus
  97. M. J. Vos, S. Carra, B. Kanon et al., “Specific protein homeostatic functions of small heat-shock proteins increase lifespan,” Aging Cell, vol. 15, no. 2, pp. 217–226, 2016. View at Publisher · View at Google Scholar · View at Scopus
  98. S. Kaushik and A. M. Cuervo, “Proteostasis and aging,” Nature Medicine, vol. 21, no. 12, pp. 1406–1415, 2015. View at Publisher · View at Google Scholar · View at Scopus
  99. T. Grune, “Oxidative stress, aging and the proteasomal system,” Biogerontology, vol. 1, no. 1, pp. 31–40, 2000. View at Publisher · View at Google Scholar
  100. P. A. Szweda, M. Camouse, K. C. Lundberg, T. D. Oberley, and L. I. Szweda, “Aging, lipofuscin formation, and free radical-mediated inhibition of cellular proteolytic systems,” Ageing Research Reviews, vol. 2, no. 4, pp. 383–405, 2003. View at Publisher · View at Google Scholar · View at Scopus
  101. Q. Ding, E. Dimayuga, W. R. Markesbery, and J. N. Keller, “Proteasome inhibition induces reversible impairments in protein synthesis,” The FASEB Journal, vol. 20, no. 8, pp. 1055–1063, 2006. View at Publisher · View at Google Scholar · View at Scopus
  102. Q. Ding, E. Dimayuga, and J. N. Keller, “Proteasome regulation of oxidative stress in aging and age-related diseases of the CNS,” Antioxidants & Redox Signaling, vol. 8, no. 1-2, pp. 163–172, 2006. View at Publisher · View at Google Scholar · View at Scopus
  103. A. L. Santos and A. B. Lindner, “Protein posttranslational modifications: roles in aging and age-related disease,” Oxidative Medicine and Cellular Longevity, vol. 2017, Article ID 5716409, 19 pages, 2017. View at Publisher · View at Google Scholar · View at Scopus
  104. J. N. Keller, F. F. Huang, and W. R. Markesbery, “Decreased levels of proteasome activity and proteasome expression in aging spinal cord,” Neuroscience, vol. 98, no. 1, pp. 149–156, 2000. View at Publisher · View at Google Scholar · View at Scopus
  105. J. N. Keller, K. B. Hanni, and W. R. Markesbery, “Possible involvement of proteasome inhibition in aging: implications for oxidative stress,” Mechanisms of Ageing and Development, vol. 113, no. 1, pp. 61–70, 2000. View at Publisher · View at Google Scholar · View at Scopus
  106. E. Kevei and T. Hoppe, “Ubiquitin sets the timer: impacts on aging and longevity,” Nature Structural & Molecular Biology, vol. 21, no. 4, pp. 290–292, 2014. View at Publisher · View at Google Scholar · View at Scopus
  107. N. Hoe, C. M. Huang, G. Landis et al., “Ubiquitin over-expression phenotypes and ubiquitin gene molecular misreading during aging in Drosophila melanogaster,” Aging, vol. 3, no. 3, pp. 237–261, 2011. View at Publisher · View at Google Scholar
  108. H.-Y. Liu and C. M. Pfleger, “Mutation in E1, the ubiquitin activating enzyme, reduces Drosophila lifespan and results in motor impairment,” PLoS One, vol. 8, no. 1, article e32835, 2013. View at Publisher · View at Google Scholar · View at Scopus
  109. A. C. Carrano, A. Dillin, and T. Hunter, “A Krüppel-like factor downstream of the E3 ligase WWP-1 mediates dietary-restriction-induced longevity in Caenorhabditis elegans,” Nature Communications, vol. 5, 2014. View at Publisher · View at Google Scholar · View at Scopus
  110. R. A. Gottlieb and R. S. Carreira, “Autophagy in health and disease. 5. Mitophagy as a way of life,” American Journal of Physiology-Cell Physiology, vol. 299, no. 2, pp. C203–C210, 2010. View at Publisher · View at Google Scholar · View at Scopus
  111. S. Mai, B. Muster, J. Bereiter-Hahn, and M. Jendrach, “Autophagy proteins LC3B, ATG5 and ATG12 participate in quality control after mitochondrial damage and influence lifespan,” Autophagy, vol. 8, no. 1, pp. 47–62, 2014. View at Publisher · View at Google Scholar · View at Scopus
  112. J. N. Keller, E. Dimayuga, Q. Chen, J. Thorpe, J. Gee, and Q. Ding, “Autophagy, proteasomes, lipofuscin, and oxidative stress in the aging brain,” The International Journal of Biochemistry & Cell Biology, vol. 36, no. 12, pp. 2376–2391, 2004. View at Publisher · View at Google Scholar · View at Scopus
  113. T. Hara, K. Nakamura, M. Matsui et al., “Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice,” Nature, vol. 441, no. 7095, pp. 885–889, 2006. View at Publisher · View at Google Scholar · View at Scopus
  114. M. Dodson, V. Darley-Usmar, and J. Zhang, “Cellular metabolic and autophagic pathways: traffic control by redox signaling,” Free Radical Biology and Medicine, vol. 63, pp. 207–221, 2013. View at Publisher · View at Google Scholar · View at Scopus
  115. K. Palikaras, E. Lionaki, and N. Tavernarakis, “Coordination of mitophagy and mitochondrial biogenesis during ageing in C. elegans,” Nature, vol. 521, no. 7553, pp. 525–528, 2015. View at Publisher · View at Google Scholar · View at Scopus
  116. A. Rana, M. Rera, and D. W. Walker, “Parkin overexpression during aging reduces proteotoxicity, alters mitochondrial dynamics, and extends lifespan,” Proceedings of the National Academy of Sciences, vol. 110, no. 21, pp. 8638–8643, 2013. View at Publisher · View at Google Scholar · View at Scopus
  117. J. Lee, S. Giordano, and J. Zhang, “Autophagy, mitochondria and oxidative stress: cross-talk and redox signalling,” Biochemical Journal, vol. 441, no. 2, pp. 523–540, 2012. View at Publisher · View at Google Scholar · View at Scopus
  118. E. F. Fang, M. Scheibye-Knudsen, K. F. Chua, M. P. Mattson, D. L. Croteau, and V. A. Bohr, “Nuclear DNA damage signalling to mitochondria in ageing,” Nature Reviews Molecular Cell Biology, vol. 17, no. 5, pp. 308–321, 2016. View at Publisher · View at Google Scholar · View at Scopus
  119. P. Bai, C. Cantó, H. Oudart et al., “PARP-1 inhibition increases mitochondrial metabolism through SIRT1 activation,” Cell Metabolism, vol. 13, no. 4, pp. 461–468, 2011. View at Publisher · View at Google Scholar · View at Scopus
  120. S. Imai and L. Guarente, “NAD(+) and sirtuins in aging and disease,” Trends in Cell Biology, vol. 24, no. 8, pp. 464–471, 2014. View at Publisher · View at Google Scholar · View at Scopus
  121. S. Park, R. Mori, and I. Shimokawa, “Do sirtuins promote mammalian longevity?: a critical review on its relevance to the longevity effect induced by calorie restriction,” Molecules and Cells, vol. 35, no. 6, pp. 474–480, 2013. View at Publisher · View at Google Scholar · View at Scopus
  122. K. T. Howitz, K. J. Bitterman, H. Y. Cohen et al., “Small molecule activators of sirtuins extend Saccharomyces cerevisiae lifespan,” Nature, vol. 425, no. 6954, pp. 191–196, 2003. View at Publisher · View at Google Scholar · View at Scopus
  123. E. Morselli, M. C. Maiuri, M. Markaki et al., “Caloric restriction and resveratrol promote longevity through the sirtuin-1-dependent induction of autophagy,” Cell Death & Disease, vol. 1, no. 1, article e10, 2010. View at Publisher · View at Google Scholar · View at Scopus
  124. E. Verdin, M. D. Hirschey, L. W. S. Finley, and M. C. Haigis, “Sirtuin regulation of mitochondria: energy production, apoptosis, and signaling,” Trends in Biochemical Sciences, vol. 35, no. 12, pp. 669–675, 2010. View at Publisher · View at Google Scholar · View at Scopus
  125. E. F. Fang, M. Scheibye-Knudsen, L. E. Brace et al., “Defective mitophagy in XPA via PARP1 hyperactivation and NAD+/SIRT1 reduction,” Cell, vol. 157, no. 4, pp. 882–896, 2014. View at Publisher · View at Google Scholar · View at Scopus
  126. T. Radovits, L. Seres, D. Gerő et al., “Single dose treatment with PARP-inhibitor INO-1001 improves aging-associated cardiac and vascular dysfunction,” Experimental Gerontology, vol. 42, no. 7, pp. 676–685, 2007. View at Publisher · View at Google Scholar · View at Scopus
  127. P. Pacher, J. G. Mabley, F. G. Soriano, L. Liaudet, K. Komjáti, and C. Szabó, “Endothelial dysfunction in aging animals: the role of poly(ADP-ribose) polymerase activation,” British Journal of Pharmacology, vol. 135, no. 6, pp. 1347–1350, 2002. View at Publisher · View at Google Scholar · View at Scopus
  128. G. Zhang, M. Chao, L. Hui et al., “Poly(ADP-ribose)polymerase 1 inhibition protects against age-dependent endothelial dysfunction,” Clinical and Experimental Pharmacology and Physiology, vol. 42, no. 12, pp. 1266–1274, 2015. View at Publisher · View at Google Scholar · View at Scopus
  129. S. Shall and G. de Murcia, “Poly(ADP-ribose) polymerase-1: what have we learned from the deficient mouse model?” Mutation Research/DNA Repair, vol. 460, no. 1, pp. 1–15, 2000. View at Publisher · View at Google Scholar · View at Scopus
  130. T. S. Piskunova, M. N. Yurova, A. I. Ovsyannikov et al., “Deficiency in poly(ADP-ribose) polymerase-1 (PARP-1) accelerates aging and spontaneous carcinogenesis in mice,” Current Gerontology and Geriatrics Research, vol. 2008, Article ID 754190, 11 pages, 2008. View at Publisher · View at Google Scholar
  131. A. Mangerich and A. Bürkle, “Pleiotropic cellular functions of PARP1 in longevity and aging: genome maintenance meets inflammation,” Oxidative Medicine and Cellular Longevity, vol. 2012, Article ID 321653, 19 pages, 2012. View at Publisher · View at Google Scholar · View at Scopus
  132. A. A. Freitas and J. P. de Magalhaes, “A review and appraisal of the DNA damage theory of ageing,” Mutation Research/Reviews in Mutation Research, vol. 728, no. 1-2, pp. 12–22, 2011. View at Publisher · View at Google Scholar · View at Scopus
  133. N. J. Curtin, “DNA repair dysregulation from cancer driver to therapeutic target,” Nature Reviews Cancer, vol. 12, no. 12, pp. 801–817, 2012. View at Publisher · View at Google Scholar · View at Scopus
  134. T. A. Prolla and J. M. Denu, “NAD+ deficiency in age-related mitochondrial dysfunction,” Cell Metabolism, vol. 19, no. 2, pp. 178–180, 2014. View at Publisher · View at Google Scholar · View at Scopus
  135. F. Li, Z. Z. Chong, and K. Maiese, “Cell life versus cell longevity: the mysteries surrounding the NAD(+) precursor nicotinamide,” Current Medicinal Chemistry, vol. 13, no. 8, pp. 883–895, 2006. View at Publisher · View at Google Scholar · View at Scopus
  136. M. S. Bonkowski and D. A. Sinclair, “Slowing ageing by design: the rise of NAD+ and sirtuin-activating compounds,” Nature Reviews Molecular Cell Biology, vol. 17, no. 11, pp. 679–690, 2016. View at Publisher · View at Google Scholar · View at Scopus
  137. S. Imai and L. Guarente, “It takes two to tango: NAD+ and sirtuins in aging/longevity control,” npj Aging and Mechanisms of Disease, vol. 2, no. 1, article 16017, 2016. View at Publisher · View at Google Scholar
  138. K. Maiese, Z. Z. Chong, J. Hou, and Y. C. Shang, “The vitamin nicotinamide: translating nutrition into clinical care,” Molecules, vol. 14, no. 12, pp. 3446–3485, 2009. View at Publisher · View at Google Scholar · View at Scopus
  139. J. Y. Kwak, H. J. Ham, C. M. Kim, and E. S. Hwang, “Nicotinamide exerts antioxidative effects on senescent cells,” Molecules and Cells, vol. 38, no. 3, pp. 229–235, 2015. View at Publisher · View at Google Scholar · View at Scopus
  140. K. Tsubota, “The first human clinical study for NMN has started in Japan,” npj Aging and Mechanisms of Disease, vol. 2, no. 1, p. 16021, 2016. View at Publisher · View at Google Scholar
  141. T. Hashimoto, M. Horikawa, T. Nomura, and K. Sakamoto, “Nicotinamide adenine dinucleotide extends the lifespan of Caenorhabditis elegans mediated by sir-2.1 and daf-16,” Biogerontology, vol. 11, no. 1, pp. 31–43, 2010. View at Publisher · View at Google Scholar · View at Scopus
  142. H. Zhang, D. Ryu, Y. Wu et al., “NAD+ repletion improves mitochondrial and stem cell function and enhances life span in mice,” Science, vol. 352, no. 6292, pp. 1436–1443, 2016. View at Publisher · View at Google Scholar · View at Scopus
  143. L. Mouchiroud, R. H. Houtkooper, N. Moullan et al., “The NAD(+)/sirtuin pathway modulates longevity through activation of mitochondrial UPR and FOXO signaling,” Cell, vol. 154, no. 2, pp. 430–441, 2013. View at Publisher · View at Google Scholar · View at Scopus
  144. M. B. Jensen and H. Jasper, “Mitochondrial proteostasis in the control of aging and longevity,” Cell Metabolism, vol. 20, no. 2, pp. 214–225, 2014. View at Publisher · View at Google Scholar · View at Scopus
  145. T. Arnould, S. Michel, and P. Renard, “Mitochondria retrograde signaling and the UPR mt: where are we in mammals?” International Journal of Molecular Sciences, vol. 16, no. 8, pp. 18224–18251, 2015. View at Publisher · View at Google Scholar · View at Scopus
  146. M. Borch Jensen, Y. Qi, R. Riley, L. Rabkina, and H. Jasper, “PGAM5 promotes lasting FoxO activation after developmental mitochondrial stress and extends lifespan in Drosophila,” Elife, vol. 6, 2017. View at Publisher · View at Google Scholar · View at Scopus
  147. C. J. Fiorese and C. M. Haynes, “Integrating the UPRmtinto the mitochondrial maintenance network,” Critical Reviews in Biochemistry and Molecular Biology, vol. 52, no. 3, pp. 304–313, 2017. View at Publisher · View at Google Scholar · View at Scopus
  148. K. Gariani, K. J. Menzies, D. Ryu et al., “Eliciting the mitochondrial unfolded protein response by nicotinamide adenine dinucleotide repletion reverses fatty liver disease in mice,” Hepatology, vol. 63, no. 4, pp. 1190–1204, 2016. View at Publisher · View at Google Scholar · View at Scopus
  149. C. Lerner, A. Bitto, D. Pulliam et al., “Reduced mammalian target of rapamycin activity facilitates mitochondrial retrograde signaling and increases life span in normal human fibroblasts,” Aging Cell, vol. 12, no. 6, pp. 966–977, 2013. View at Publisher · View at Google Scholar · View at Scopus
  150. M. Kaeberlein, D. Hu, E. O. Kerr et al., “Increased life span due to calorie restriction in respiratory-deficient yeast,” PLoS Genetics, vol. 1, no. 5, article e69, 2005. View at Publisher · View at Google Scholar · View at Scopus
  151. S.-J. Lin, E. Ford, M. Haigis, G. Liszt, and L. Guarente, “Calorie restriction extends yeast life span by lowering the level of NADH,” Genes & Development, vol. 18, no. 1, pp. 12–16, 2004. View at Publisher · View at Google Scholar · View at Scopus
  152. P. Kyryakov, A. Beach, V. R. Richard et al., “Caloric restriction extends yeast chronological lifespan by altering a pattern of age-related changes in trehalose concentration,” Frontiers in Physiology, vol. 3, 2012. View at Publisher · View at Google Scholar · View at Scopus
  153. A. Leonov, R. Feldman, A. Piano et al., “Caloric restriction extends yeast chronological lifespan via a mechanism linking cellular aging to cell cycle regulation, maintenance of a quiescent state, entry into a non-quiescent state and survival in the non-quiescent state,” Oncotarget, vol. 8, no. 41, pp. 69328–69350, 2017. View at Publisher · View at Google Scholar · View at Scopus
  154. T. L. Kaeberlein, E. D. Smith, M. Tsuchiya et al., “Lifespan extension in Caenorhabditis elegans by complete removal of food,” Aging Cell, vol. 5, no. 6, pp. 487–494, 2006. View at Publisher · View at Google Scholar · View at Scopus
  155. B. N. Heestand, Y. Shen, W. Liu et al., “Dietary restriction induced longevity is mediated by nuclear receptor NHR-62 in Caenorhabditis elegans,” PLoS Genetics, vol. 9, no. 7, article e1003651, 2013. View at Publisher · View at Google Scholar · View at Scopus
  156. I. Bjedov, J. M. Toivonen, F. Kerr et al., “Mechanisms of life span extension by rapamycin in the fruit fly Drosophila melanogaster,” Cell Metabolism, vol. 11, no. 1, pp. 35–46, 2010. View at Publisher · View at Google Scholar · View at Scopus
  157. 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, vol. 66A, no. 2, pp. 191–201, 2011. View at Publisher · View at Google Scholar · View at Scopus
  158. V. N. Anisimov, M. A. Zabezhinski, I. G. Popovich et al., “Rapamycin increases lifespan and inhibits spontaneous tumorigenesis in inbred female mice,” Cell Cycle, vol. 10, no. 24, pp. 4230–4236, 2011. View at Publisher · View at Google Scholar · View at Scopus
  159. D. E. Harrison, R. Strong, Z. D. Sharp et al., “Rapamycin fed late in life extends lifespan in genetically heterogeneous mice,” Nature, vol. 460, no. 7253, pp. 392–395, 2009. View at Publisher · View at Google Scholar · View at Scopus
  160. R. J. Colman, T. M. Beasley, J. W. Kemnitz, S. C. Johnson, R. Weindruch, and R. M. Anderson, “Caloric restriction reduces age-related and all-cause mortality in rhesus monkeys,” Nature Communications, vol. 5, 2014. View at Publisher · View at Google Scholar · View at Scopus
  161. C. K. Martin, L. K. Heilbronn, L. de Jonge et al., “Effect of calorie restriction on resting metabolic rate and spontaneous physical activity,” Obesity, vol. 15, no. 12, pp. 2964–2973, 2007. View at Publisher · View at Google Scholar · View at Scopus
  162. K. Hagopian, J. J. Ramsey, and R. Weindruch, “Enzymes of glycerol and glyceraldehyde metabolism in mouse liver: effects of caloric restriction and age on activities,” Bioscience Reports, vol. 28, no. 2, pp. 107–115, 2008. View at Publisher · View at Google Scholar · View at Scopus
  163. S. Summermatter, D. Mainieri, A. P. Russell et al., “Thrifty metabolism that favors fat storage after caloric restriction: a role for skeletal muscle phosphatidylinositol-3-kinase activity and AMP-activated protein kinase,” The FASEB Journal, vol. 22, no. 3, pp. 774–785, 2008. View at Publisher · View at Google Scholar · View at Scopus
  164. P. B. M. De Andrade, L. A. Neff, M. K. Strosova et al., “Caloric restriction induces energy-sparing alterations in skeletal muscle contraction, fiber composition and local thyroid hormone metabolism that persist during catch-up fat upon refeeding,” Frontiers in Physiology, vol. 6, 2015. View at Publisher · View at Google Scholar · View at Scopus
  165. D. W. Lamming and R. M. Anderson, “Metabolic effects of caloric restriction,” in eLS. Chichester, John Wiley & Sons Ltd, 2014. View at Publisher · View at Google Scholar
  166. A. J. Donato, A. E. Walker, K. A. Magerko et al., “Life-long caloric restriction reduces oxidative stress and preserves nitric oxide bioavailability and function in arteries of old mice,” Aging Cell, vol. 12, no. 5, pp. 772–783, 2013. View at Publisher · View at Google Scholar · View at Scopus
  167. 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
  168. A. R. Heydari, A. Unnikrishnan, L. V. Lucente, and A. Richardson, “Caloric restriction and genomic stability,” Nucleic Acids Research, vol. 35, no. 22, pp. 7485–7496, 2007. View at Publisher · View at Google Scholar · View at Scopus
  169. W. E. Sonntag, C. D. Lynch, W. T. Cefalu et al., “Pleiotropic effects of growth hormone and insulin-like growth factor (IGF)-1 on biological aging: inferences from moderate caloric-restricted animals,” The Journals of Gerontology Series A: Biological Sciences and Medical Sciences, vol. 54, no. 12, pp. B521–B538, 1999. View at Publisher · View at Google Scholar
  170. I. Shimokawa, Y. Higami, T. Tsuchiya et al., “Life span extension by reduction of the growth hormone-insulin-like growth factor-1 axis: relation to caloric restriction,” The FASEB Journal, vol. 17, no. 9, pp. 1108-1109, 2003. View at Publisher · View at Google Scholar
  171. S. D. Hursting, S. M. Smith, L. M. Lashinger, A. E. Harvey, and S. N. Perkins, “Calories and carcinogenesis: lessons learned from 30 years of calorie restriction research,” Carcinogenesis, vol. 31, no. 1, pp. 83–89, 2010. View at Publisher · View at Google Scholar · View at Scopus
  172. J. H. Um, S. J. Kim, D. W. Kim et al., “Tissue-specific changes of DNA repair protein Ku and mtHSP70 in aging rats and their retardation by caloric restriction,” Mechanisms of Ageing and Development, vol. 124, no. 8-9, pp. 967–975, 2003. View at Publisher · View at Google Scholar · View at Scopus
  173. D. C. Cabelof, S. Yanamadala, J. J. Raffoul, Z. Guo, A. Soofi, and A. R. Heydari, “Caloric restriction promotes genomic stability by induction of base excision repair and reversal of its age-related decline,” DNA Repair, vol. 2, no. 3, pp. 295–307, 2003. View at Publisher · View at Google Scholar · View at Scopus
  174. V. Calabrese, C. Cornelius, S. Cuzzocrea, I. Iavicoli, E. Rizzarelli, and E. J. Calabrese, “Hormesis, cellular stress response and vitagenes as critical determinants in aging and longevity,” Molecular Aspects of Medicine, vol. 32, no. 4-6, pp. 279–304, 2011. View at Publisher · View at Google Scholar · View at Scopus
  175. M. V. Blagosklonny, “Calorie restriction: decelerating mTOR-driven aging from cells to organisms (including humans),” Cell Cycle, vol. 9, no. 4, pp. 683–688, 2014. View at Publisher · View at Google Scholar · View at Scopus
  176. S. Robida-Stubbs, K. Glover-Cutter, D. W. Lamming et al., “TOR signaling and rapamycin influence longevity by regulating SKN-1/Nrf and DAF-16/FoxO,” Cell Metabolism, vol. 15, no. 5, pp. 713–724, 2012. View at Publisher · View at Google Scholar · View at Scopus
  177. S. L. Hands, C. G. Proud, and A. Wyttenbach, “mTOR’s role in ageing: protein synthesis or autophagy?” Aging, vol. 1, no. 7, pp. 586–597, 2009. View at Publisher · View at Google Scholar
  178. C. H. Jung, S.-H. Ro, J. Cao, N. M. Otto, and D.-H. Kim, “mTOR regulation of autophagy,” FEBS Letters, vol. 584, no. 7, pp. 1287–1295, 2010. View at Publisher · View at Google Scholar · View at Scopus
  179. M. Kaeberlein, R. W. Powers 3rd, K. K. Steffen et al., “Regulation of yeast replicative life span by TOR and Sch9 in response to nutrients,” Science, vol. 310, no. 5751, pp. 1193–1196, 2005. View at Publisher · View at Google Scholar · View at Scopus
  180. P. Kapahi, B. M. Zid, T. Harper, D. Koslover, V. Sapin, and S. Benzer, “Regulation of lifespan in Drosophila by modulation of genes in the TOR signaling pathway,” Current Biology, vol. 14, no. 10, pp. 885–890, 2004. View at Publisher · View at Google Scholar · View at Scopus
  181. T. Vellai, K. Takacs-Vellai, Y. Zhang, A. L. Kovacs, L. Orosz, and F. Muller, “Genetics: influence of TOR kinase on lifespan in C. elegans,” Nature., vol. 426, no. 6967, p. 620, 2003. View at Publisher · View at Google Scholar
  182. L. Fontana, L. Partridge, and V. D. Longo, “Extending healthy life span—from yeast to humans,” Science, vol. 328, no. 5976, pp. 321–326, 2010. View at Publisher · View at Google Scholar · View at Scopus
  183. C. Slack, M. E. Giannakou, A. Foley, M. Goss, and L. Partridge, “dFOXO-independent effects of reduced insulin-like signaling in Drosophila,” Aging Cell, vol. 10, no. 5, pp. 735–748, 2011. View at Publisher · View at Google Scholar · View at Scopus
  184. A. Ortega-Molina, A. Efeyan, E. Lopez-Guadamillas et al., “Pten positively regulates brown adipose function, energy expenditure, and longevity,” Cell Metabolism, vol. 15, no. 3, pp. 382–394, 2012. View at Publisher · View at Google Scholar · View at Scopus
  185. M. M. Mihaylova and R. J. Shaw, “The AMPK signalling pathway coordinates cell growth, autophagy and metabolism,” Nature Cell Biology, vol. 13, no. 9, pp. 1016–1023, 2011. View at Publisher · View at Google Scholar · View at Scopus
  186. D. G. Hardie, “AMP-activated protein kinase: an energy sensor that regulates all aspects of cell function,” Genes & Development, vol. 25, no. 18, pp. 1895–1908, 2011. View at Publisher · View at Google Scholar · View at Scopus
  187. G. R. Steinberg and B. E. Kemp, “AMPK in health and disease,” Physiological Reviews, vol. 89, no. 3, pp. 1025–1078, 2009. View at Publisher · View at Google Scholar · View at Scopus
  188. B. Onken and M. Driscoll, “Metformin induces a dietary restriction–like state and the oxidative stress response to extend C. elegans healthspan via AMPK, LKB1, and SKN-1,” PLoS One, vol. 5, no. 1, article e8758, 2010. View at Publisher · View at Google Scholar · View at Scopus
  189. J. Apfeld, G. O'Connor, T. McDonagh, P. S. DiStefano, and R. Curtis, “The AMP-activated protein kinase AAK-2 links energy levels and insulin-like signals to lifespan in C. elegans,” Genes & Development, vol. 18, no. 24, pp. 3004–3009, 2004. View at Publisher · View at Google Scholar · View at Scopus
  190. V. N. Anisimov, “Metformin for cancer and aging prevention: is it a time to make the long story short?” Oncotarget, vol. 6, no. 37, pp. 39398–39407, 2015. View at Publisher · View at Google Scholar · View at Scopus
  191. M. Sorensen, A. Sanz, J. Gomez et al., “Effects of fasting on oxidative stress in rat liver mitochondria,” Free Radical Research, vol. 40, no. 4, pp. 339–347, 2009. View at Publisher · View at Google Scholar · View at Scopus
  192. A. B. Crujeiras, D. Parra, E. Goyenechea, and J. A. Martinez, “Sirtuin gene expression in human mononuclear cells is modulated by caloric restriction,” Eur J Clin Invest., vol. 38, no. 9, pp. 672–678, 2008. View at Publisher · View at Google Scholar · View at Scopus
  193. 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
  194. S. Michan and D. Sinclair, “Sirtuins in mammals: insights into their biological function,” Biochemical Journal, vol. 404, no. 1, pp. 1–13, 2007. View at Publisher · View at Google Scholar · View at Scopus
  195. M. T. Borra, B. C. Smith, and J. M. Denu, “Mechanism of human SIRT1 activation by resveratrol,” Journal of Biological Chemistry, vol. 280, no. 17, pp. 17187–17195, 2005. View at Publisher · View at Google Scholar · View at Scopus
  196. M. Gertz, G. T. T. Nguyen, F. Fischer et al., “A molecular mechanism for direct sirtuin activation by resveratrol,” PLoS One, vol. 7, no. 11, article e49761, 2012. View at Publisher · View at Google Scholar · View at Scopus
  197. B. Dasgupta and J. Milbrandt, “Resveratrol stimulates AMP kinase activity in neurons,” Proceedings of the National Academy of Sciences, vol. 104, no. 17, pp. 7217–7222, 2007. View at Publisher · View at Google Scholar · View at Scopus
  198. L. M. V. de Almeida, M. C. Leite, A. P. Thomazi et al., “Resveratrol protects against oxidative injury induced by H2O2 in acute hippocampal slice preparations from Wistar rats,” Archives of Biochemistry and Biophysics, vol. 480, no. 1, pp. 27–32, 2008. View at Publisher · View at Google Scholar · View at Scopus
  199. L. M. V. de Almeida, C. C. Piñeiro, M. C. Leite et al., “Protective effects of resveratrol on hydrogen peroxide induced toxicity in primary cortical astrocyte cultures,” Neurochemical Research, vol. 33, no. 1, pp. 8–15, 2008. View at Publisher · View at Google Scholar · View at Scopus
  200. L. Liu, L. Gu, Q. Ma, D. Zhu, and X. Huang, “Resveratrol attenuates hydrogen peroxide-induced apoptosis in human umbilical vein endothelial cells,” European Review for Medical and Pharmacological Sciences, vol. 17, no. 1, pp. 88–94, 2013. View at Google Scholar
  201. L. M. V. de Almeida, C. C. Piñeiro, M. C. Leite et al., “Resveratrol increases glutamate uptake, glutathione content, and S100B secretion in cortical astrocyte cultures,” Cellular and Molecular Neurobiology, vol. 27, no. 5, pp. 661–668, 2007. View at Publisher · View at Google Scholar · View at Scopus
  202. 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,” The Journals of Gerontology Series A: Biological Sciences and Medical Sciences, vol. 62, no. 3, pp. 223–234, 2007. View at Publisher · View at Google Scholar · View at Scopus
  203. G. López-Lluch, N. Hunt, B. Jones et al., “Calorie restriction induces mitochondrial biogenesis and bioenergetic efficiency,” Proceedings of the National Academy of Sciences, vol. 103, no. 6, pp. 1768–1773, 2006. View at Publisher · View at Google Scholar · View at Scopus
  204. 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
  205. L. Guarente, “NO link between calorie restriction and mitochondria,” Nature Chemical Biology, vol. 1, no. 7, pp. 355-356, 2005. View at Publisher · View at Google Scholar · View at Scopus
  206. A. Richardson, S. N. Austad, Y. Ikeno, A. Unnikrishnan, and R. J. McCarter, “Significant life extension by ten percent dietary restriction,” Annals of the New York Academy of Sciences, vol. 1363, no. 1, pp. 11–17, 2016. View at Publisher · View at Google Scholar · View at Scopus
  207. Y. Zhang, Y. Ikeno, A. Bokov et al., “Dietary restriction attenuates the accelerated aging phenotype of Sod1-/- mice,” Free Radical Biology and Medicine, vol. 60, pp. 300–306, 2013. View at Publisher · View at Google Scholar · View at Scopus
  208. Y. C. Jang, Y. Liu, C. R. Hayworth et al., “Dietary restriction attenuates age-associated muscle atrophy by lowering oxidative stress in mice even in complete absence of CuZnSOD,” Aging Cell, vol. 11, no. 5, pp. 770–782, 2012. View at Publisher · View at Google Scholar · View at Scopus
  209. M. Meydani and W. J. Evans, “Free radicals, exercise, and aging,” in Free Radicals in Aging, B. P. Yu, Ed., pp. 183–204, CRC Press, Boca Raton, 1993. View at Google Scholar
  210. L. L. Ji, “Antioxidants and oxidative stress in exercise,” Proceedings of the Society for Experimental Biology and Medicine, vol. 222, no. 3, pp. 283–292, 1999. View at Publisher · View at Google Scholar
  211. J. Bejma, P. R. Ramires, C. Donahue, and L. L. Ji, “Aging and acute exercise enhances free radical generation and oxidative damage in skeletal muscle,” Medicine & Science in Sports & Exercise, vol. 30, Supplement, p. 322, 1998. View at Publisher · View at Google Scholar
  212. M.-C. Gomez-Cabrera, C. Borrás, F. V. Pallardó, J. Sastre, L. L. Ji, and J. Viña, “Decreasing xanthine oxidase-mediated oxidative stress prevents useful cellular adaptations to exercise in rats,” The Journal of Physiology, vol. 567, no. 1, pp. 113–120, 2005. View at Publisher · View at Google Scholar · View at Scopus
  213. M. A. Naseeb and S. L. Volpe, “Protein and exercise in the prevention of sarcopenia and aging,” Nutrition Research, vol. 40, pp. 1–20, 2017. View at Publisher · View at Google Scholar · View at Scopus
  214. A. T. Ludlow and S. M. Roth, “Physical activity and telomere biology: exploring the link with aging-related disease prevention,” Journal of Aging Research, vol. 2011, Article ID 790378, 12 pages, 2011. View at Publisher · View at Google Scholar · View at Scopus
  215. B. Hurley and I. Reuter, “Aging, physical activity, and disease prevention,” Journal of Aging Research, vol. 2011, Article ID 782546, 2 pages, 2011. View at Publisher · View at Google Scholar · View at Scopus
  216. N. Garatachea, H. Pareja-Galeano, F. Sanchis-Gomar et al., “Exercise attenuates the major hallmarks of aging,” Rejuvenation Research, vol. 18, no. 1, pp. 57–89, 2015. View at Publisher · View at Google Scholar · View at Scopus
  217. J. Hollander, J. Bejma, T. Ookawara, H. Ohno, and L. L. Ji, “Superoxide dismutase gene expression in skeletal muscle: fiber-specific effect of age,” Mechanisms of Ageing and Development, vol. 116, no. 1, pp. 33–45, 2000. View at Publisher · View at Google Scholar · View at Scopus
  218. A. McArdle and M. J. Jackson, “Exercise, oxidative stress and ageing,” Journal of Anatomy, vol. 197, no. 4, pp. 539–541, 2000. View at Publisher · View at Google Scholar
  219. Y.-J. Kim and D. M. Wilson III, “Overview of base excision repair biochemistry,” Current Molecular Pharmacology, vol. 5, no. 1, pp. 3–13, 2012. View at Publisher · View at Google Scholar · View at Scopus
  220. M. Bar-Shai, E. Carmeli, and A. Z. Reznick, “The role of NF-κB in protein breakdown in immobilization, aging, and exercise: from basic processes to promotion of health,” Annals of the New York Academy of Sciences, vol. 1057, no. 1, pp. 431–447, 2005. View at Publisher · View at Google Scholar · View at Scopus
  221. Z. Radak, H. Y. Chung, E. Koltai, A. W. Taylor, and S. Goto, “Exercise, oxidative stress and hormesis,” Ageing Research Reviews, vol. 7, no. 1, pp. 34–42, 2008. View at Publisher · View at Google Scholar · View at Scopus
  222. Z. Radak, H. Y. Chung, and S. Goto, “Exercise and hormesis: oxidative stress-related adaptation for successful aging,” Biogerontology, vol. 6, no. 1, pp. 71–75, 2005. View at Publisher · View at Google Scholar · View at Scopus
  223. L. L. Ji, “Antioxidant signaling in skeletal muscle: a brief review,” Experimental Gerontology, vol. 42, no. 7, pp. 582–593, 2007. View at Publisher · View at Google Scholar · View at Scopus
  224. B. Chance, H. Sies, and A. Boveris, “Hydroperoxide metabolism in mammalian organs,” Physiological Reviews, vol. 59, no. 3, pp. 527–605, 1979. View at Publisher · View at Google Scholar
  225. T. Akimoto, S. C. Pohnert, P. Li et al., “Exercise stimulates Pgc-1α transcription in skeletal muscle through activation of the p38 MAPK pathway,” Journal of Biological Chemistry, vol. 280, no. 20, pp. 19587–19593, 2005. View at Publisher · View at Google Scholar · View at Scopus
  226. J. St-Pierre, S. Drori, M. Uldry et al., “Suppression of reactive oxygen species and neurodegeneration by the PGC-1 transcriptional coactivators,” Cell, vol. 127, no. 2, pp. 397–408, 2006. View at Publisher · View at Google Scholar · View at Scopus
  227. L. L. Ji, “Exercise at old age: does it increase or alleviate oxidative stress?” Annals of the New York Academy of Sciences, vol. 928, pp. 236–247, 2001. View at Google Scholar
  228. Z. Radák, H. Y. Chung, H. Naito et al., “Age-associated increase in oxidative stress and nuclear factor κB activation are attenuated in rat liver by regular exercise,” The FASEB Journal, vol. 18, no. 6, pp. 749-750, 2004. View at Publisher · View at Google Scholar
  229. C. S. Broome, A. C. Kayani, J. Palomero et al., “Effect of lifelong overexpression of HSP70 in skeletal muscle on age-related oxidative stress and adaptation after nondamaging contractile activity,” The FASEB Journal, vol. 20, no. 9, pp. 1549–1551, 2006. View at Publisher · View at Google Scholar · View at Scopus
  230. T. A. Hornberger, R. D. Mateja, E. R. Chin, J. L. Andrews, and K. A. Esser, “Aging does not alter the mechanosensitivity of the p38, p70S6k, and JNK2 signaling pathways in skeletal muscle,” Journal of Applied Physiology, vol. 98, no. 4, pp. 1562–1566, 2005. View at Publisher · View at Google Scholar · View at Scopus
  231. D. Williamson, P. Gallagher, M. Harber, C. Hollon, and S. Trappe, “Mitogen-activated protein kinase (MAPK) pathway activation: effects of age and acute exercise on human skeletal muscle,” The Journal of Physiology, vol. 547, no. 3, pp. 977–987, 2003. View at Publisher · View at Google Scholar · View at Scopus
  232. M. Gleeson, N. C. Bishop, D. J. Stensel, M. R. Lindley, S. S. Mastana, and M. A. Nimmo, “The anti-inflammatory effects of exercise: mechanisms and implications for the prevention and treatment of disease,” Nature Reviews Immunology, vol. 11, no. 9, pp. 607–615, 2011. View at Publisher · View at Google Scholar · View at Scopus
  233. I. Gath, E. I. Closs, U. Gödtel-Armbrust et al., “Inducible NO synthase II and neuronal NO synthase I are constitutively expressed in different structures of guinea pig skeletal muscle: implications for contractile function,” The FASEB Journal, vol. 10, no. 14, pp. 1614–1620, 1996. View at Publisher · View at Google Scholar
  234. M. R. Rose, Evolutionary biology of aging, Oxford University Press, Oxford, UK, 1994.
  235. M. Ackermann, S. C. Stearns, and U. Jenal, “Senescence in a bacterium with asymmetric division,” Science, vol. 300, no. 5627, p. 1920, 2003. View at Publisher · View at Google Scholar · View at Scopus
  236. M. Ackermann, L. Chao, C. T. Bergstrom, and M. Doebeli, “On the evolutionary origin of aging,” Aging Cell, vol. 6, no. 2, pp. 235–244, 2007. View at Publisher · View at Google Scholar · View at Scopus
  237. E. J. Stewart, R. Madden, G. Paul, and F. Taddei, “Aging and death in an organism that reproduces by morphologically symmetric division,” PLoS Biology, vol. 3, no. 2, article e45, 2005. View at Publisher · View at Google Scholar · View at Scopus
  238. J.-W. J. Veening, E. J. Stewart, T. W. Berngruber, F. Taddei, O. P. Kuipers, and L. W. Hamoen, “Bet-hedging and epigenetic inheritance in bacterial cell development,” Proceedings of the National Academy of Sciences, vol. 105, no. 11, pp. 4393–4398, 2008. View at Publisher · View at Google Scholar · View at Scopus
  239. B. B. Aldridge, M. Fernandez-Suarez, D. Heller et al., “Asymmetry and aging of mycobacterial cells lead to variable growth and antibiotic susceptibility,” Science, vol. 335, no. 6064, pp. 100–104, 2012. View at Publisher · View at Google Scholar · View at Scopus
  240. T. Nyström, “Conditional senescence in bacteria: death of the immortals,” Molecular Microbiology, vol. 48, no. 1, pp. 17–23, 2003. View at Publisher · View at Google Scholar · View at Scopus
  241. K. A. Steinkraus, M. Kaeberlein, and B. K. Kennedy, “Replicative aging in yeast: the means to the end,” Annual Review of Cell and Developmental Biology, vol. 24, no. 1, pp. 29–54, 2008. View at Publisher · View at Google Scholar · View at Scopus
  242. J. Winkler, A. Seybert, L. König et al., “Quantitative and spatio-temporal features of protein aggregation in Escherichia coli and consequences on protein quality control and cellular ageing,” The EMBO Journal, vol. 29, no. 5, pp. 910–923, 2010. View at Publisher · View at Google Scholar · View at Scopus
  243. A. B. Lindner, R. Madden, A. Demarez, E. J. Stewart, and F. Taddei, “Asymmetric segregation of protein aggregates is associated with cellular aging and rejuvenation,” Proceedings of the National Academy of Sciences, vol. 105, no. 8, pp. 3076–3081, 2008. View at Publisher · View at Google Scholar · View at Scopus
  244. M. Coelho and I. M. Tolic, “Asymmetric damage segregation at cell division via protein aggregate fusion and attachment to organelles,” Bioessays, vol. 37, no. 7, pp. 740–747, 2015. View at Publisher · View at Google Scholar · View at Scopus
  245. R. Higuchi-Sanabria, W. M. A. Pernice, J. D. Vevea, D. M. Alessi Wolken, I. R. Boldogh, and L. A. Pon, “Role of asymmetric cell division in lifespan control in Saccharomyces cerevisiae,” FEMS Yeast Research, vol. 14, no. 8, pp. 1133–1146, 2014. View at Publisher · View at Google Scholar · View at Scopus
  246. H. Aguilaniu, L. Gustafsson, M. Rigoulet, and T. Nyström, “Asymmetric inheritance of oxidatively damaged proteins during cytokinesis,” Science, vol. 299, no. 5613, pp. 1751–1753, 2003. View at Publisher · View at Google Scholar · View at Scopus
  247. A.-S. Coquel, J.-P. Jacob, M. Primet et al., “Localization of protein aggregation in Escherichia coli is governed by diffusion and nucleoid macromolecular crowding effect,” PLoS Computational Biology, vol. 9, no. 4, article e1003038, 2013. View at Publisher · View at Google Scholar · View at Scopus
  248. B. Desnues, C. Cuny, G. Grégori, S. Dukan, H. Aguilaniu, and T. Nyström, “Differential oxidative damage and expression of stress defence regulons in culturable and non-culturable Escherichia coli cells,” EMBO Reports, vol. 4, no. 4, pp. 400–404, 2003. View at Publisher · View at Google Scholar · View at Scopus
  249. I. Dalle-Donne, G. Aldini, M. Carini, R. Colombo, R. Rossi, and A. Milzani, “Protein carbonylation, cellular dysfunction, and disease progression,” Journal of Cellular and Molecular Medicine, vol. 10, no. 2, pp. 389–406, 2006. View at Publisher · View at Google Scholar · View at Scopus
  250. I. Dalle-Donne, D. Giustarini, R. Colombo, R. Rossi, and A. Milzani, “Protein carbonylation in human diseases,” Trends in Molecular Medicine, vol. 9, no. 4, pp. 169–176, 2003. View at Publisher · View at Google Scholar · View at Scopus
  251. T. Nyström, “The free-radical hypothesis of aging goes prokaryotic,” Cellular and Molecular Life Sciences (CMLS), vol. 60, no. 7, pp. 1333–1341, 2003. View at Publisher · View at Google Scholar · View at Scopus
  252. A. L. Santos, V. Oliveira, I. Baptista et al., “Wavelength dependence of biological damage induced by UV radiation on bacteria,” Archives of Microbiology, vol. 195, no. 1, pp. 63–74, 2013. View at Publisher · View at Google Scholar · View at Scopus
  253. F. Bosshard, K. Riedel, T. Schneider, C. Geiser, M. Bucheli, and T. Egli, “Protein oxidation and aggregation in UVA-irradiated Escherichia coli cells as signs of accelerated cellular senescence,” Environmental Microbiology, vol. 12, no. 11, pp. 2931–2945, 2010. View at Publisher · View at Google Scholar · View at Scopus
  254. S. Dukan, T. Nyström, and T. Nystro, “Oxidative stress defense and deterioration of growth-arrested Escherichia coli cells,” Journal of Biological Chemistry, vol. 274, no. 37, pp. 26027–26032, 1999. View at Publisher · View at Google Scholar · View at Scopus
  255. F. B. Johnson, D. A. Sinclair, and L. Guarente, “Molecular biology of aging,” Cell, vol. 96, no. 2, pp. 291–302, 1999. View at Publisher · View at Google Scholar · View at Scopus
  256. S. Dukan and T. Nyström, “Bacterial senescence: stasis results in increased and differential oxidation of cytoplasmic proteins leading to developmental induction of the heat shock regulon,” Genes & Development, vol. 12, no. 21, pp. 3431–3441, 1998. View at Publisher · View at Google Scholar · View at Scopus
  257. J. Tamarit, E. Cabiscol, and J. Ros, “Identification of the major oxidatively damaged proteins in Escherichia coli cells exposed to oxidative stress,” Journal of Biological Chemistry, vol. 273, no. 5, pp. 3027–3032, 1998. View at Publisher · View at Google Scholar · View at Scopus
  258. E. Cabiscol, E. Piulats, P. Echave, E. Herrero, and J. Ros, “Oxidative stress promotes specific protein damage in Saccharomyces cerevisiae,” Journal of Biological Chemistry, vol. 275, no. 35, pp. 27393–27398, 2000. View at Publisher · View at Google Scholar · View at Scopus
  259. 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
  260. L.-J. Yan, R. L. Levine, and R. S. Sohal, “Oxidative damage during aging targets mitochondrial aconitase,” Proceedings of the National Academy of Sciences, vol. 94, no. 21, pp. 11168–11172, 1997. View at Publisher · View at Google Scholar · View at Scopus
  261. A. Castegna, M. Aksenov, M. Aksenova et al., “Proteomic identification of oxidatively modified proteins in Alzheimer’s disease brain. Part I: Creatine kinase BB, glutamine synthase, and ubiquitin carboxy-terminal hydrolase L-1,” Free Radical Biology and Medicine, vol. 33, no. 4, pp. 562–571, 2002. View at Publisher · View at Google Scholar · View at Scopus
  262. A. Matin, “The molecular basis of carbon-starvation-induced general resistance in Escherichia coli,” Molecular Microbiology, vol. 5, no. 1, pp. 3–10, 1991. View at Publisher · View at Google Scholar · View at Scopus
  263. D. E. Jenkins, J. E. Schultz, and A. Matin, “Starvation-induced cross protection against heat or H2O2 challenge in Escherichia coli,” Journal of Bacteriology, vol. 170, no. 9, pp. 3910–3914, 1988. View at Publisher · View at Google Scholar · View at Scopus
  264. R. A. Miller, “Cell stress and aging: new emphasis on multiplex resistance mechanisms,” The Journals of Gerontology Series A: Biological Sciences and Medical Sciences, vol. 64A, no. 2, pp. 179–182, 2009. View at Publisher · View at Google Scholar · View at Scopus
  265. L. E. Enell, N. Kapan, J. A. E. Soderberg, L. Kahsai, and D. R. Nassel, “Insulin signaling, lifespan and stress resistance are modulated by metabotropic GABA receptors on insulin producing cells in the brain of Drosophila,” PLoS One, vol. 5, no. 12, article e15780, 2010. View at Publisher · View at Google Scholar · View at Scopus
  266. S. Ayyadevara, M. R. Engle, S. P. Singh et al., “Lifespan and stress resistance of Caenorhabditis elegans are increased by expression of glutathione transferases capable of metabolizing the lipid peroxidation product 4-hydroxynonenal,” Aging Cell, vol. 4, no. 5, pp. 257–271, 2005. View at Publisher · View at Google Scholar · View at Scopus
  267. M. Shaposhnikov, E. Proshkina, L. Shilova, A. Zhavoronkov, and A. Moskalev, “Lifespan and stress resistance in Drosophila with overexpressed DNA repair genes,” Scientific Reports, vol. 5, no. 1, article 15299, 2015. View at Publisher · View at Google Scholar · View at Scopus
  268. V. D. Longo, J. Mitteldorf, and V. P. Skulachev, “Programmed and altruistic ageing,” Nature Reviews Genetics, vol. 6, no. 11, pp. 866–872, 2005. View at Publisher · View at Google Scholar · View at Scopus
  269. M. Ballesteros, A. Fredriksson, J. Henriksson, and T. Nyström, “Bacterial senescence: protein oxidation in non-proliferating cells is dictated by the accuracy of the ribosomes,” The EMBO Journal, vol. 20, no. 18, pp. 5280–5289, 2001. View at Publisher · View at Google Scholar · View at Scopus
  270. H. Aguilaniu, L. Gustafsson, M. Rigoulet, and T. Nyström, “Protein oxidation in G0 cells of Saccharomyces cerevisiae depends on the state rather than rate of respiration and is enhanced in pos9 but not yap1 mutants,” Journal of Biological Chemistry, vol. 276, no. 38, pp. 35396–35404, 2001. View at Publisher · View at Google Scholar · View at Scopus
  271. T. Nyström, “Not quite dead enough: on bacterial life, culturability, senescence, and death,” Archives of Microbiology, vol. 176, no. 3, pp. 159–164, 2001. View at Google Scholar
  272. A. Battesti, N. Majdalani, and S. Gottesman, “The RpoS-mediated general stress response in Escherichia coli,” Annual Review of Microbiology, vol. 65, no. 1, pp. 189–213, 2011. View at Publisher · View at Google Scholar · View at Scopus
  273. T. L. Testerman, A. Vazquez-Torres, Y. Xu, J. Jones-Carson, S. J. Libby, and F. C. Fang, “The alternative sigma factor σE controls antioxidant defences required for Salmonella virulence and stationary-phase survival,” Molecular Microbiology, vol. 43, no. 3, pp. 771–782, 2002. View at Publisher · View at Google Scholar · View at Scopus
  274. F. Fontaine, E. J. Stewart, A. B. Lindner, and F. Taddei, “Mutations in two global regulators lower individual mortality in Escherichia coli,” Molecular Microbiology, vol. 0, no. 0, pp. 2–14, 2007. View at Publisher · View at Google Scholar · View at Scopus
  275. S. Gonidakis, S. E. Finkel, and V. D. Longo, “Genome-wide screen identifies Escherichia coli TCA-cycle-related mutants with extended chronological lifespan dependent on acetate metabolism and the hypoxia-inducible transcription factor ArcA,” Aging Cell, vol. 9, no. 5, pp. 868–881, 2010. View at Publisher · View at Google Scholar · View at Scopus
  276. L. Yu and C. Yu, “Interaction between succinate dehydrogenase and ubiquinone-binding protein from succinate-ubiquinone reductase,” Biochimica et Biophysica Acta (BBA) - Bioenergetics, vol. 593, no. 1, pp. 24–38, 1980. View at Publisher · View at Google Scholar · View at Scopus
  277. K. R. Messner and J. A. Imlay, “Mechanism of superoxide and hydrogen peroxide formation by fumarate reductase, succinate dehydrogenase, and aspartate oxidase,” Journal of Biological Chemistry, vol. 277, no. 45, pp. 42563–42571, 2002. View at Publisher · View at Google Scholar · View at Scopus
  278. S. Gonidakis, S. E. Finkel, and V. D. Longo, “E. coli hypoxia-inducible factor ArcA mediates lifespan extension in a lipoic acid synthase mutant by suppressing acetyl-CoA synthetase,” Biological Chemistry, vol. 391, no. 10, pp. 1139–1147, 2010. View at Publisher · View at Google Scholar · View at Scopus
  279. A. S. Lynch and E. C. Lin, “Transcriptional control mediated by the ArcA two-component response regulator protein of Escherichia coli: characterization of DNA binding at target promoters,” Journal of Bacteriology, vol. 178, no. 21, pp. 6238–6249, 1996. View at Publisher · View at Google Scholar · View at Scopus