Role of reactive oxygen species-mediated signaling in aging

Antioxidants and Redox Signaling

Volumn 19, Issue 12, 2013, Pages 1362-1372

  Labunskyy, Vyacheslav M ^a   Gladyshev, Vadim N ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE; KELCH LIKE ECH ASSOCIATED PROTEIN 1; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR NRF2;

AGING; DIABETES MELLITUS; HOMEOSTASIS; LIFESPAN; LONGEVITY; MACROMOLECULAR CROWDING; MAMMAL; NEOPLASM; NERVE DEGENERATION; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PATHOGENESIS; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION;

AGING; ANIMALS; CYSTEINE; HUMANS; LONGEVITY; OXIDATION-REDUCTION; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION;

EID: 84885211241     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2012.4891     Document Type: Review

References (87)

1. Bienert GP, Moller AL, Kristiansen KA, Schulz A, Moller IM, Schjoerring JK, and Jahn TP. Specific aquaporins facilitate the diffusion of hydrogen peroxide across membranes. J Biol Chem 282: 1183-1192, 2007. (Pubitemid 47076557)
2. Biteau B, Labarre J, and Toledano MB. ATP-dependent reduction of cysteine-sulphinic acid by S. cerevisiae sulphiredoxin. Nature 425: 980-984, 2003. (Pubitemid 37376931)
3. Bozonet SM, Findlay VJ, Day AM, Cameron J, Veal EA, and Morgan BA. Oxidation of a eukaryotic 2-Cys peroxiredoxin is a molecular switch controlling the transcriptional response to increasing levels of hydrogen peroxide. J Biol Chem 280: 23319-23327, 2005. (Pubitemid 40853245)
4. Brunelle JK, Bell EL, Quesada NM, Vercauteren K, Tiranti V, Zeviani M, Scarpulla RC, and Chandel NS. Oxygen sensing requires mitochondrial ROS but not oxidative phosphorylation. Cell Metab 1: 409-414, 2005. (Pubitemid 43960624)
5. Bulua AC, Simon A, Maddipati R, Pelletier M, Park H, Kim KY, Sack MN, Kastner DL, and Siegel RM. Mitochondrial reactive oxygen species promote production of proinflammatory cytokines and are elevated in TNFR1-associated periodic syndrome (TRAPS). J Exp Med 208: 519-533, 2011.
6. Cabreiro F, Ackerman D, Doonan R, Araiz C, Back P, Papp D, Braeckman BP, and Gems D. Increased life span from overexpression of superoxide dismutase in Caenorhabditis elegans is not caused by decreased oxidative damage. Free Radic Biol Med 51: 1575-1582, 2011.
7. Calabrese V, Sultana R, Scapagnini G, Guagliano E, Sapienza M, Bella R, Kanski J, Pennisi G, Mancuso C, Stella AM, and Butterfield DA. Nitrosative stress, cellular stress response, and thiol homeostasis in patients with Alzheimer's disease. Antioxid Redox Signal 8: 1975-1986, 2006. (Pubitemid 46489625)
8. Cao J, Schulte J, Knight A, Leslie NR, Zagozdzon A, Bronson R, Manevich Y, Beeson C, and Neumann CA. Prdx1 inhibits tumorigenesis via regulating PTEN/AKT activity. Embo J 28: 1505-1517, 2009.
9. Chen Q, Vazquez EJ, Moghaddas S, Hoppel CL, and Lesnefsky EJ. Production of reactive oxygen species by mitochondria: Central role of complex III. J Biol Chem 278: 36027-36031, 2003. (Pubitemid 37139922)
10. Chiappetta G, Ndiaye S, Igbaria A, Kumar C, Vinh J, and Toledano MB. Proteome screens for Cys residues oxidation: The redoxome. Methods Enzymol 473: 199-216, 2010.
11. Conway JP and Kinter M. Dual role of peroxiredoxin I in macrophage-derived foam cells. J Biol Chem 281: 27991-28001, 2006. (Pubitemid 44414512)
12. D'Autreaux B and Toledano MB. ROS as signalling molecules: Mechanisms that generate specificity in ROS homeostasis. Nat Rev Mol Cell Biol 8: 813-824, 2007. (Pubitemid 47462134)
13. David DC, Ollikainen N, Trinidad JC, Cary MP, Burlingame AL, and Kenyon C. Widespread protein aggregation as an inherent part of aging in C. elegans. PLoS Biol 8: e1000450, 2010.
14. Day AM, Brown JD, Taylor SR, Rand JD, Morgan BA, and Veal EA. Inactivation of a peroxiredoxin by hydrogen peroxide is critical for thioredoxin-mediated repair of oxidized proteins and cell survival. Mol Cell 45: 398-408, 2012.
15. Delaunay A, Pflieger D, Barrault MB, Vinh J, and Toledano MB. A thiol peroxidase is an H2O2 receptor and redoxtransducer in gene activation. Cell 111: 471-481, 2002. (Pubitemid 35356554)
16. Doonan R, McElwee JJ, Matthijssens F, Walker GA, Houthoofd K, Back P, Matscheski A, Vanfleteren JR, and Gems D. Against the oxidative damage theory of aging: superoxide dismutases protect against oxidative stress but have little or no effect on life span in Caenorhabditis elegans. Genes Dev 22: 3236-3241, 2008.
17. Durieux J, Wolff S, and Dillin A. The cell-non-autonomous nature of electron transport chain-mediated longevity. Cell 144: 79-91, 2011.
18. Edgar RS, Green EW, Zhao Y, van Ooijen G, Olmedo M, Qin X, Xu Y, Pan M, Valekunja UK, Feeney KA, Maywood ES, Hastings MH, Baliga NS, Merrow M, Millar AJ, Johnson CH, Kyriacou CP, O'Neill JS, and Reddy AB. Peroxiredoxins are conserved markers of circadian rhythms. Nature 485: 459-464, 2012.
19. Finkel T. Signal transduction by reactive oxygen species. J Cell Biol 194: 7-15, 2011.
20. Fomenko DE and Gladyshev VN. Comparative genomics of thiol oxidoreductases reveals widespread and essential functions of thiol-based redox control of cellular processes. Antioxid Redox Signal 16: 193-201, 2012.
21. Fomenko DE, Koc A, Agisheva N, Jacobsen M, Kaya A, Malinouski M, Rutherford JC, Siu KL, Jin DY, Winge DR, and Gladyshev VN. Thiol peroxidases mediate specific genome-wide regulation of gene expression in response to hydrogen peroxide. Proc Natl Acad Sci USA 108: 2729-2734, 2011.
22. Fomenko DE, Marino SM, and Gladyshev VN. Functional diversity of cysteine residues in proteins and unique features of catalytic redox-active cysteines in thiol oxidoreductases. Mol Cells 26: 228-235, 2008.
23. Fomenko DE, Xing W, Adair BM, Thomas DJ, and Gladyshev VN. High-throughput identification of catalytic redoxactive cysteine residues. Science 315: 387-389, 2007. (Pubitemid 46175521)
24. Fridovich I. Superoxide radical and superoxide dismutases. Annu Rev Biochem 64: 97-112, 1995.
25. Gadjev I, Stone JM, and Gechev TS. Programmed cell death in plants: New insights into redox regulation and the role of hydrogen peroxide. In International Review of Cell and Molecular Biology, edited by Jeon KW. San Diego, CA: Academic Press, 2008, pp. 87-144.
26. Gems D and Doonan R. Antioxidant defense and aging in C. elegans: Is the oxidative damage theory of aging wrong? Cell Cycle 8: 1681-1687, 2009.
27. Gil-del Valle L, de la CML, Toledo A, Vilaro N, Tapanes R, and Otero MA. Altered redox status in patients with diabetes mellitus type I. Pharmacol Res 51: 375-380, 2005. (Pubitemid 40439182)
28. Giorgio M, Migliaccio E, Orsini F, Paolucci D, Moroni M, Contursi C, Pelliccia G, Luzi L, Minucci S, Marcaccio M, Pinton P, Rizzuto R, Bernardi P, Paolucci F, and Pelicci PG. Electron transfer between cytochrome c and p66Shc generates reactive oxygen species that trigger mitochondrial apoptosis. Cell 122: 221-233, 2005. (Pubitemid 41032986)
29. Guo Z, Kozlov S, Lavin MF, Person MD, and Paull TT. ATM activation by oxidative stress. Science 330: 517-521, 2011.
30. Guzy RD, Hoyos B, Robin E, Chen H, Liu L, Mansfield KD, Simon MC, Hammerling U, and Schumacker PT. Mitochondrial complex III is required for hypoxia-induced ROS production and cellular oxygen sensing. Cell Metab 1: 401-408, 2005. (Pubitemid 43960623)
31. Hall A, Karplus PA, and Poole LB. Typical 2-Cys peroxiredoxins- Structures, mechanisms and functions. FEBS J 276: 2469-2477, 2009.
32. Harman D. Aging: A theory based on free radical and radiation chemistry. J Gerontol 11: 298-300, 1956.
33. Hidalgo E and Demple B. An iron-sulfur center essential for transcriptional activation by the redox-sensing SoxR protein. EMBO J 13: 138-146, 1994.
34. Imlay JA. Pathways of oxidative damage. Annu Rev Microbiol 57: 395-418, 2003. (Pubitemid 37392949)
35. Ishii N, Fujii M, Hartman PS, Tsuda M, Yasuda K, Senoo-Matsuda N, Yanase S, Ayusawa D, and Suzuki K. A mutation in succinate dehydrogenase cytochrome b causes oxidative stress and ageing in nematodes. Nature 394: 694-697, 1998. (Pubitemid 28389798)
36. Karplus PA and Poole LB. Peroxiredoxins as molecular triage agents, sacrificing themselves to enhance cell survival during a peroxide attack. Mol Cell 45: 275-278, 2012.
37. Kayser EB, Morgan PG, Hoppel CL, and Sedensky MM. Mitochondrial expression and function of GAS-1 in Caenorhabditis elegans. J Biol Chem 276: 20551-20558, 2001.
38. Kim EB, Fang X, Fushan AA, Huang Z, Lobanov AV, Han L, Marino SM, Sun X, Turanov AA, Yang P, Yim SH, Zhao X, Kasaikina MV, Stoletzki N, Peng C, Polak P, Xiong Z, Kiezun A, Zhu Y, Chen Y, Kryukov GV, Zhang Q, Peshkin L, Yang L, Bronson RT, Buffenstein R, Wang B, Han C, Li Q, Chen L, Zhao W, Sunyaev SR, Park TJ, Zhang G, Wang J, and Gladyshev VN. Genome sequencing reveals insights into physiology and longevity of the naked mole rat. Nature 479: 223-227, 2011.
39. Kobayashi M and Yamamoto M. Nrf2-Keap1 regulation of cellular defense mechanisms against electrophiles and reactive oxygen species. Adv Enzyme Regul 46: 113-140, 2006. (Pubitemid 44301353)
40. Kwon J, Lee SR, Yang KS, Ahn Y, Kim YJ, Stadtman ER, and Rhee SG. Reversible oxidation and inactivation of the tumor suppressor PTEN in cells stimulated with peptide growth factors. Proc Natl Acad Sci USA 101: 16419-16424, 2004. (Pubitemid 39557728)
41. Lee KS, Iijima-Ando K, Iijima K, Lee WJ, Lee JH, Yu K, and Lee DS. JNK/FOXO-mediated neuronal expression of fly homologue of peroxiredoxin II reduces oxidative stress and extends life span. J Biol Chem 284: 29454-29461, 2009.
42. Leichert LI, Gehrke F, Gudiseva HV, Blackwell T, Ilbert M, Walker AK, Strahler JR, Andrews PC, and Jakob U. Quantifying changes in the thiol redox proteome upon oxidative stress in vivo. Proc Natl Acad Sci USA 105: 8197-8202, 2008. (Pubitemid 351904734)
43. Levine RL, Moskovitz J, and Stadtman ER. Oxidation of methionine in proteins: Roles in antioxidant defense and cellular regulation. IUBMB Life 50: 301-307, 2000. (Pubitemid 32289088)
44. Lithgow GJ and Miller RA. The determination of aging rate by coordinated resistance to multiple forms of stress. In The Molecular Biology of Aging, edited by Wallace DC. Cold Spring Harbor, NY: Cold Spring Harbor Press, 2008, pp. 427-481.
45. Mansfield KD, Guzy RD, Pan Y, Young RM, Cash TP, Schumacker PT, and Simon MC. Mitochondrial dysfunction resulting from loss of cytochrome c impairs cellular oxygen sensing and hypoxic HIF-alpha activation. Cell Metab 1: 393-399, 2005. (Pubitemid 43960625)
46. Martindale JL and Holbrook NJ. Cellular response to oxidative stress: Signaling for suicide and survival. J Cell Physiol 192: 1-15, 2002. (Pubitemid 34587382)
47. Mates JM, Segura JA, Alonso FJ, and Marquez J. Intracellular redox status and oxidative stress: Implications for cell proliferation, apoptosis, and carcinogenesis. Arch Toxicol 82: 273-299, 2008.
48. Miller EW, Dickinson BC, and Chang CJ. Aquaporin-3 mediates hydrogen peroxide uptake to regulate downstream intracellular signaling. Proc Natl Acad Sci USA 107: 15681-15686, 2010.
49. Molin M, Yang J, Hanzen S, Toledano MB, Labarre J, and Nystrom T. Life span extension and H(2)O(2) resistance elicited by caloric restriction require the peroxiredoxin Tsa1 in Saccharomyces cerevisiae. Mol Cell 43: 823-833, 2011.
50. Muller FL, Lustgarten MS, Jang Y, Richardson A, and Van Remmen H. Trends in oxidative aging theories. Free Radic Biol Med 43: 477-503, 2007. (Pubitemid 47058228)
51. Murphy MP, Holmgren A, Larsson NG, Halliwell B, Chang CJ, Kalyanaraman B, Rhee SG, Thornalley PJ, Partridge L, Gems D, Nystrom T, Belousov V, Schumacker PT, and Winterbourn CC. Unraveling the biological roles of reactive oxygen species. Cell Metab 13: 361-366, 2011.
52. Nakahira K, Haspel JA, Rathinam VA, Lee SJ, Dolinay T, Lam HC, Englert JA, Rabinovitch M, Cernadas M, Kim HP, Fitzgerald KA, Ryter SW, and Choi AM. Autophagy proteins regulate innate immune responses by inhibiting the release of mitochondrial DNA mediated by the NALP3 inflammasome. Nat Immunol 12: 222-230, 2011.
53. Nathan C. Specificity of a third kind: Reactive oxygen and nitrogen intermediates in cell signaling. J Clin Invest 111: 769-778, 2003. (Pubitemid 37074948)
54. Okazaki S, Naganuma A, and Kuge S. Peroxiredoxinmediated redox regulation of the nuclear localization of Yap1, a transcription factor in budding yeast. Antioxid Redox Signal 7: 327-334, 2005. (Pubitemid 40279802)
55. Okazaki S, Tachibana T, Naganuma A, Mano N, and Kuge S. Multistep disulfide bond formation in Yap1 is required for sensing and transduction of H2O2 stress signal. Mol Cell 27: 675-688, 2007. (Pubitemid 47238631)
56. Olahova M, Taylor SR, Khazaipoul S, Wang J, Morgan BA, Matsumoto K, Blackwell TK, and Veal EA. A redox-sensitive peroxiredoxin that is important for longevity has tissue-and stress-specific roles in stress resistance. Proc Natl Acad Sci USA 105: 19839-19844, 2008.
57. Pan Y, Schroeder EA, Ocampo A, Barrientos A, and Shadel GS. Regulation of yeast chronological life span by TORC1 via adaptive mitochondrial ROS signaling. Cell Metab 13: 668-678, 2011.
58. Perez VI, Buffenstein R, Masamsetti V, Leonard S, Salmon AB, Mele J, Andziak B, Yang T, Edrey Y, Friguet B, Ward W, Richardson A, and Chaudhuri A. Protein stability and resistance to oxidative stress are determinants of longevity in the longest-living rodent, the naked mole-rat. Proc Natl Acad Sci USA 106: 3059-3064, 2009.
59. Poon HF, Vaishnav RA, Getchell TV, Getchell ML, and Butterfield DA. Quantitative proteomics analysis of differential protein expression and oxidative modification of specific proteins in the brains of old mice. Neurobiol Aging 27: 1010-1019, 2006.
60. Rhee SG, Kang SW, Jeong W, Chang TS, Yang KS, and Woo HA. Intracellular messenger function of hydrogen peroxide and its regulation by peroxiredoxins. Curr Opin Cell Biol 17: 183-189, 2005. (Pubitemid 40380942)
61. Ristow M and Zarse K. How increased oxidative stress promotes longevity and metabolic health: The concept of mitochondrial hormesis (mitohormesis). Exp Gerontol 45: 410-418, 2010.
62. Ross SJ, Findlay VJ, Malakasi P, and Morgan BA. Thioredoxin peroxidase is required for the transcriptional response to oxidative stress in budding yeast. Mol Biol Cell 11: 2631-2642, 2000. (Pubitemid 30645032)
63. Salmeen A, Andersen JN, Myers MP, Meng TC, Hinks JA, Tonks NK, and Barford D. Redox regulation of protein tyrosine phosphatase 1B involves a sulphenyl-amide intermediate. Nature 423: 769-773, 2003. (Pubitemid 36735701)
64. Scherz-Shouval R, Shvets E, Fass E, Shorer H, Gil L, and Elazar Z. Reactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4. EMBO J 26: 1749-1760, 2007. (Pubitemid 46624042)
65. Schulz TJ, Zarse K, Voigt A, Urban N, Birringer M, and Ristow M. Glucose restriction extends Caenorhabditis elegans life span by inducing mitochondrial respiration and increasing oxidative stress. Cell Metab 6: 280-293, 2007. (Pubitemid 47468090)
66. Squier TC. Oxidative stress and protein aggregation during biological aging. Exp Gerontol 36: 1539-1550, 2001. (Pubitemid 32768730)
67. Stadtman ER. Protein oxidation and aging. Science 257: 1220-1224, 1992.
68. St-Pierre J, Buckingham JA, Roebuck SJ, and Brand MD. Topology of superoxide production from different sites in the mitochondrial electron transport chain. J Biol Chem 277: 44784-44790, 2002. (Pubitemid 36159072)
69. Tachibana T, Okazaki S, Murayama A, Naganuma A, Nomoto A, and Kuge S. A major peroxiredoxin-induced activation of Yap1 transcription factor is mediated by reduction-sensitive disulfide bonds and reveals a low level of transcriptional activation. J Biol Chem 284: 4464-4472, 2009.
70. Thamsen M, Kumsta C, Li F, and Jakob U. Is overoxidation of peroxiredoxin physiologically significant? Antioxid Redox Signal 14: 725-730, 2011.
71. Tu BP and Weissman JS. The FAD-and O(2)-dependent reaction cycle of Ero1-mediated oxidative protein folding in the endoplasmic reticulum. Mol Cell 10: 983-994, 2002. (Pubitemid 35453820)
72. Tullet JM, Hertweck M, An JH, Baker J, Hwang JY, Liu S, Oliveira RP, Baumeister R, and Blackwell TK. Direct inhibition of the longevity-promoting factor SKN-1 by insulinlike signaling in C. elegans. Cell 132: 1025-1038, 2008. (Pubitemid 351391953)
73. Van Raamsdonk JM and Hekimi S. Deletion of the mitochondrial superoxide dismutase sod-2 extends lifespan in Caenorhabditis elegans. PLoS Genet 5: e1000361, 2009.
74. Van Raamsdonk JM and Hekimi S. Reactive oxygen species and aging in Caenorhabditis elegans: Causal or casual relationship? Antioxid Redox Signal 13: 1911-1953, 2010.
75. Van Raamsdonk JM and Hekimi S. Superoxide dismutase is dispensable for normal animal lifespan. Proc Natl Acad Sci USA 109: 5785-5790, 2012.
76. Veal EA, Findlay VJ, Day AM, Bozonet SM, Evans JM, Quinn J, and Morgan BA. A 2-Cys peroxiredoxin regulates peroxide-induced oxidation and activation of a stress-activated MAP kinase. Mol Cell 15: 129-139, 2004. (Pubitemid 38850225)
77. Vivancos AP, Castillo EA, Biteau B, Nicot C, Ayte J, Toledano MB, and Hidalgo E. A cysteine-sulfinic acid in peroxiredoxin regulates H2O2-sensing by the antioxidant Pap1 pathway. Proc Natl Acad Sci USA 102: 8875-8880, 2005. (Pubitemid 40881046)
78. Weerapana E, Wang C, Simon GM, Richter F, Khare S, Dillon MB, Bachovchin DA, Mowen K, Baker D, and Cravatt BF. Quantitative reactivity profiling predicts functional cysteines in proteomes. Nature 468: 790-795, 2010.
79. Winterbourn CC and Metodiewa D. Reactivity of biologically important thiol compounds with superoxide and hydrogen peroxide. Free Radic Biol Med 27: 322-328, 1999. (Pubitemid 29395424)
80. Woo HA, Chae HZ, Hwang SC, Yang KS, Kang SW, Kim K, and Rhee SG. Reversing the inactivation of peroxiredoxins caused by cysteine sulfinic acid formation. Science 300: 653-656, 2003. (Pubitemid 36520592)
81. Woo HA, Yim SH, Shin DH, Kang D, Yu DY, and Rhee SG. Inactivation of peroxiredoxin I by phosphorylation allows localized H(2)O(2) accumulation for cell signaling. Cell 140: 517-528, 2010.
82. Wood ZA, Poole LB, and Karplus PA. Peroxiredoxin evolution and the regulation of hydrogen peroxide signaling. Science 300: 650-653, 2003. (Pubitemid 36520591)
83. Wu RF, Ma Z, Liu Z, and Terada LS. Nox4-derived H2O2 mediates endoplasmic reticulum signaling through local Ras activation. Mol Cell Biol 30: 3553-3568, 2010.
84. Yang W and Hekimi S. A mitochondrial superoxide signal triggers increased longevity in Caenorhabditis elegans. PLoS Biol 8: e1000556, 2010.
85. Yang W and Hekimi S. Two modes of mitochondrial dysfunction lead independently to lifespan extension in Caenorhabditis elegans. Aging Cell 9: 433-447, 2010.
86. Zhang DD and Hannink M. Distinct cysteine residues in Keap1 are required for Keap1-dependent ubiquitination of Nrf2 and for stabilization of Nrf2 by chemopreventive agents and oxidative stress. Mol Cell Biol 23: 8137-8151, 2003. (Pubitemid 37377505)
87. Zuin A, Carmona M, Morales-Ivorra I, Gabrielli N, Vivancos AP, Ayte J, and Hidalgo E. Lifespan extension by calorie restriction relies on the Sty1 MAP kinase stress pathway. EMBO J 29: 981-991, 2010.