A measurable increase in oxidative damage due to reduction in superoxide detoxification fails to shorten the life span of long-lived mitochondrial mutants of Caenorhabditis elegans

Genetics

Volumn 177, Issue 4, 2007, Pages 2063-2074

  Yang, Wen ^a   Li, Jingjing ^a   Hekimi, Siegfried ^a,b  

^a MCGILL UNIVERSITY   (Canada)

^b Department of Biology ^*  (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE; MANGANESE SUPEROXIDE DISMUTASE;

AGING; ARTICLE; CAENORHABDITIS ELEGANS; CELL MUTANT; CONTROLLED STUDY; DETOXIFICATION; ELECTRON TRANSPORT; ENZYME DEGRADATION; LIFESPAN; LONGEVITY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL;

ANIMALS; CAENORHABDITIS ELEGANS; GENES, MITOCHONDRIAL; LONGEVITY; MUTATION; OXIDATIVE STRESS; SUPEROXIDE DISMUTASE; SUPEROXIDES;

CAENORHABDITIS ELEGANS;

EID: 37249016870     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.107.080788     Document Type: Article

References (66)

1. BALABAN, R. S., S. NEMOTO and T. FINKEL, 2005 Mitochondria, oxidants, and aging. Cell 120: 483-495.
2. BECKMAN, K. B., and B. N. AMES, 1998 The free radical theory of aging matures. Physiol. Rev. 78: 547-581.
3. BOEHM, M., and F. SLACK, 2005 A developmental timing microRNA and its target regulate life span in C. elegans. Science 310: 1954-1957.
4. BRAECKMAN, B. P., K. HOUTHOOFD, K. BRYS, I. LENAERTS, A. DE VREESE et al., 2002a No reduction of energy metabolism in Clk mutants. Mech. Ageing Dev. 123: 1447-1456.
5. BRAECKMAN, B. P., K. HOUTHOOFD and J. R. VANFLETEREN, 2002b Assessing metabolic activity in aging Caenorhabditis elegans: concepts and controversies. Aging Cell 1: 82-88; discussion 102-103.
6. DALLE-DONNE, I., R. ROSSI, D. GIUSTARINI, A. MILZANI and R. COLOMBO, 2003 Protein carbonyl groups as biomarkers of oxidative stress. Clin. Chim. Acta 329: 23-38.
7. DE CASTRO, E., S. HEGI DE CASTRO and T. E. JOHNSON, 2004 Isolation of long-lived mutants in Caenorhabditis elegans using selection for resistance to juglone. Free Radic. Biol. Med. 37: 139-145.
8. DILLIN, A., A. L. HSU, N. ARANTES- OLIVEIRA, J. LEHRER-GRAIWER, H. HSIN et al., 2002 Rates of behavior and aging specified by mitochondrial function during development. Science 298: 2398-2401.
9. DROGE, W., 2003 Oxidative stress and aging. Adv. Exp. Med. Biol. 543: 191-200.
10. DUTTAROY, A., A. PAUL, M. KUNDU and A. BELTON, 2003 A Sod2 null mutation confers severely reduced adult life span in Drosophila. Genetics 165: 2295-2299.
11. EWBANK, J. J., T. M. BARNES, B. LAKOWSKI, M. LUSSIER, H. BUSSEY et al., 1997 Structural and functional conservation of the Caenorhabditis elegans timing gene clk-1. Science 275: 980-983.
12. FABRIZIO, P., L. L. LIOU, V. N. MOY, A. DIASPRO, J. S. VALENTINE et al., 2003 SOD2 functions downstream of Sch9 to extend longevity in yeast. Genetics 163: 35-46.
13. FELKAI, S., J. J. EWBANK, J. LEMIEUX, J. C. LABBE, G. G. BROWN et al., 1999 CLK-1 controls respiration, behavior and aging in the nematode Caenorhabditis elegans. EMBO J. 18: 1783-1792.
14. FENG, J., F. BUSSIERE and S. HEKIMI, 2001 Mitochondrial electron transport is a key determinant of life span in Caenorhabditis elegans. Dev. Cell 1: 633-644.
15. FUJII, M., N. ISHII, A. JOGUCHI, K. YASUDA and D. AYUSAWA, 1998 A novel superoxide dismutase gene encoding membrane-bound and extracellular isoforms by alternative splicing in Caenorhabditis elegans. DNA Res. 5: 25-30.
16. GIGLIO, A. M., T. HUNTER, J. V. BANNISTER, W. H. BANNISTER and G. J. HUNTER, 1994 The copper/zinc superoxide dismutase gene of Caenorhabditis elegans. Biochem. Mol. Biol. Int. 33: 41-44.
17. GOLDEN, T. R., D. A. HINERFELD and S. MELOV, 2002 Oxidative stress and aging: beyond correlation. Aging Cell 1: 117-123.
18. GUARENTE, L., and C. KENYON, 2000 Genetic pathways that regulate ageing in model organisms. Nature 408: 255-262.
19. HAMILTON, M. L., H. VAN REMMEN, J. A. DRAKE, H. YANG, Z. M. GUO et al., 2001 Does oxidative damage to DNA increase with age? Proc. Natl. Acad. Sci. USA 98: 10469-10474.
20. HARRIS, N., V. COSTA, M. MACLEAN, M. MOLLAPOUR, P. MORADAS-FERREIRA et al., 2003 Mnsod overexpression extends the yeast chronological (G(0)) life span but acts independently of Sir2p histone deacetylase to shorten the replicative life span of dividing cells. Free Radic. Biol. Med. 34: 1599-1606.
21. HEKIMI, S., and L. GUARENTE, 2003 Genetics and the specificity of the aging process. Science 299: 1351-1354.
22. HEKIMI, S., C. BENARD, R. BRANICKY, J. BURGESS, A. K. HIHI et al., 2001a Why only time will tell. Mech. Ageing Dev. 122: 571-594.
23. HEKIMI, S., J. BURGESS, F. BUSSIERE, Y. MENG and C. BENARD, 2001b Genetics of life span in C. elegans: molecular diversity, physiological complexity, mechanistic simplicity. Trends Genet. 17: 712-718.
24. HONDA, Y., and S. HONDA, 2002 Oxidative stress and life span determination in the nematode Caenorhabditis elegans. Ann. NY Acad. Sci. 959: 466-474.
25. HUANG, T. T., E. J. CARLSON, A. M. GILLESPIE, Y. SHI and C. J. EPSTEIN, 2000 Ubiquitous overexpression of CuZn superoxide dismutase does not extend life span in mice. J. Gerontol. A Biol. Sci. Med. Sci. 55: B5-B9.
26. HUNTER, T., W. H. BANNISTER and G. J. HUNTER, 1997 Cloning, expression, and characterization of two manganese superoxide dismutases from Caenorhabditis elegans. J. Biol. Chem. 272: 28652-28659.
27. ISHII, N., M. FUJII, P. S. HARTMAN, M. TSUDA, K. YASUDA et al., 1998 A mutation in succinate dehydrogenase cytochrome b causes oxidative stress and ageing in nematodes. Nature 394: 694-697.
28. JENSEN, L. T., and V. C. CULOTTA, 2005 Activation of CuZn superoxide dismutases from Caenorhabditis elegans does not require the copper chaperone CCS. J. Biol. Chem. 280: 41373-41379.
29. KAMATH, R. S., M. MARTINEZ-CAMPOS, P. ZIPPERLEN, A. G. FRASER and J. AHRINGER, 2001 Effectiveness of specific RNA-mediated interference through ingested double-stranded RNA in Caenorhabditis elegans. Genome Biol. 2: RESEARCH0002.
30. KAYSER, E. B., M. M. SEDENSKY and P. G. MORGAN, 2004 The effects of complex I function and oxidative damage on life span and anesthetic sensitivity in Caenorhabditis elegans. Mech. Ageing Dev. 125: 455-464.
31. KEANEY, M., F. MATTHIJSSENS, M. SHARPE, J. VANFLETEREN and D. GEMS, 2004 Superoxide dismutase mimetics elevate superoxide dismutase activity in vivo but do not retard aging in the nematode Caenorhabditis elegans. Free Radic. Biol. Med. 37: 239-250.
32. KENYON, C., 2005 The plasticity of aging: insights from long-lived mutants. Cell 120: 449-460.
33. KENYON, C., J. CHANG, E. GENSCH, A. RUDNER and R. TABTIANG, 1993 A C. elegans mutant that lives twice as long as wild type. Nature 366: 461-464.
34. KIMURA, K. D., H. A. TISSENBAUM, Y. LIU and G. RUVKUN, 1997 daf-2, an insulin receptor-like gene that regulates longevity and diapause in Caenorhabditis elegans. Science 277: 942-946.
35. KOC, A., A. P. GASCH, J. C. RUTHERFORD, H. Y. KIM and V. N. GLADYSHEV, 2004 Methionine sulfoxide reductase regulation of yeast life span reveals reactive oxygen species-dependent and -independent components of aging. Proc. Natl. Acad. Sci. USA 101: 7999-8004.
36. KUJOTH, G. C., A. HIONA, T. D. PUGH, S. SOMEYA, K. PANZER et al., 2005 Mitochondrial DNA mutations, oxidative stress, and apoptosis in mammalian aging. Science 309: 481-484.
37. LAKOWSKI, B., and S. HEKIMI, 1996 Determination of life-span in Caenorhabditis elegans by four clock genes. Science 272: 1010-1013.
38. LAKOWSKI, B., and S. HEKIMI, 1998 The genetics of caloric restriction in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 95: 13091-13096.
39. LEE, S. S., R. Y. LEE, A. G. FRASER, R. S. KAMATH, J. AHRINGER et al., 2003 A systematic RNAi screen identifies a critical role for mitochondria in C. elegans longevity. Nat. Genet. 33: 40-48.
40. LEVINE, R. L., and E. R. STADTMAN, 2001 Oxidative modification of proteins during aging. Exp. Gerontol. 36: 1495-1502.
41. MANSOURI, A., F. L. MULLER, Y. LIU, R. NG, J. FAULKNER et al., 2006 Alterations in mitochondrial function, hydrogen peroxide release and oxidative damage in mouse hind-limb skeletal muscle during aging. Mech. Ageing Dev. 127: 298-306.
42. MELOV, S., S. R. DOCTROW, J. A. SCHNEIDER, J. HABERSON, M. PATEL et al., 2001 Life span extension and rescue of spongiform encephalopathy in superoxide dismutase 2 nullizygous mice treated with superoxide dismutase-catalase mimetics. J. Neurosci. 21: 8348-8353.
43. MIYADERA, H., H. AMINO, A. HIRAISHI, H. TAKA, K. MURAYAMA et al., 2001 Altered quinone biosynthesis in the long-lived clk-1 mutants of Caenorhabditis elegans. J. Biol. Chem. 276: 7713-7716.
44. O'BRIEN, K. M., R. DIRMEIER, M. ENGLE and R. O. POYTON, 2004 Mitochondrial protein oxidation in yeast mutants lacking manganese-(MnSOD) or copper- and zinc-containing superoxide dismutase (CuZnSOD): evidence that MnSOD and CuZnSOD have both unique and overlapping functions in protecting mitochondrial proteins from oxidative damage. J. Biol. Chem. 279: 51817-51827.
45. OKADO-MATSUMOTO, A., and I. FRIDOVICH, 2001 Subcellular distribution of superoxide dismutases (SOD) in rat liver: Cu,Zn-SOD in mitochondria. J. Biol. Chem. 276: 38388-38393.
46. ORR, W. C., and R. S. SOHAL, 2003 Does overexpression of Cu,Zn-SOD extend life span in Drosophila melanogaster? Exp. Gerontol. 38: 227-230.
47. PARKES, T. L., A. J. HILLIKER and J. P. PHILLIPS, 1999 Motorneurons, reactive oxygen, and life span in Drosophila. Neurobiol. Aging 20: 531-535.
48. PHILLIPS, J. P., S. D. CAMPBELL, D. MICHAUD, M. CHARBONNEAU and A. J. HILLIKER, 1989 Null mutation of copper/zinc superoxide dismutase in Drosophila confers hypersensitivity to paraquat and reduced longevity. Proc. Natl. Acad. Sci. USA 86: 2761-2765.
49. RAHA, S., and B. H. ROBINSON, 2000 Mitochondria, oxygen free radicals, disease and ageing. Trends Biochem. Sci. 25: 502-508.
50. SCHRINER, S. E., N. J. LINFORD, G. M. MARTIN, P. TREUTING, C. E. OGBURN et al., 2005 Extension of murine life span by overexpression of catalase targeted to mitochondria. Science 308: 1909-1911.
51. SEDENSKY, M. M., and P. G. MORGAN, 2006 Mitochondrial respiration and reactive oxygen species in C. elegans. Exp. Gerontol. 41: 957-967.
52. SENOO-MATSUDA, N., K. YASUDA, M. TSUDA, T. OHKUBO, S. YOSHIMURA et al., 2001 A defect in the cytochrome b large subunit in complex II causes both superoxide anion overproduction and abnormal energy metabolism in Caenorhabditis elegans. J. Biol. Chem. 276: 41553-41558.
53. SENOO-MATSUDA, N., P. S. HARTMAN, A. AKATSUKA, S. YOSHIMURA and N. ISHII, 2003 A complex II defect affects mitochondrial structure, leading to ced-3- and ced-4-dependent apoptosis and aging. J. Biol. Chem. 278: 22031-22036.
54. SHACTER, E., 2000 Quantification and significance of protein oxidation in biological samples. Drug Metab. Rev. 32: 307-326.
55. SHIBATA, Y., R. BRANICKY, I. O. LANDAVERDE and S. HEKIMI, 2003 Redox regulation of germline and vulval development in Caenorhabditis elegans. Science 302: 1779-1782.
56. SOHAL, R. S., 2002 Oxidative stress hypothesis of aging. Free Radic. Biol. Med. 33: 573-574.
57. STENMARK, P., J. GRUNLER, J. MATTSSON, P. J. SINDELAR, P. NORDLUND et al., 2001 A new member of the family of di-iron carboxylate proteins. Coq7 (clk-1), a membrane-bound hydroxylase involved in ubiquinone biosynthesis. J. Biol. Chem. 276: 33297-33300.
58. STURTZ, L. A., K. DIEKERT, L. T. JENSEN, R. LILL and V. C. CULOTTA, 2001 A fraction of yeast Cu,Zn-superoxide dismutase and its metallochaperone, CCS, localize to the intermembrane space of mitochondria. A physiological role for SOD1 in guarding against mitochondrial oxidative damage. J. Biol. Chem. 276: 38084-38089.
59. SUN, J., D. FOLK, T. J. BRADLEY and J. TOWER, 2002 Induced overexpression of mitochondrial Mn-superoxide dismutase extends the life span of adult Drosophila melanogaster. Genetics 161: 661-672.
60. TISSENBAUM, H. A., and L. GUARENTE, 2002 Model organisms as a guide to mammalian aging. Dev. Cell 2: 9-19.
61. VANFLETEREN, J. R., and B. P. BRAECKMAN, 1999 Mechanisms of life span determination in Caenorhabditis elegans. Neurobiol. Aging 20: 487-502.
62. VAN REMMEN, H., and A. RICHARDSON, 2001 Oxidative damage to mitochondria and aging. Exp. Gerontol. 36: 957-968.
63. VAN REMMEN, H., Y. IKENO, M. HAMILTON, M. PAHLAVANI, N. WOLF et al., 2003 Life-long reduction in MnSOD activity results in increased DNA damage and higher incidence of cancer but does not accelerate aging. Physiol. Genomics 16: 29-37.
64. WONG, A., P. BOUTIS and S. HEKIMI, 1995 Mutations in the clk-1 gene of Caenorhabditis elegans affect developmental and behavioral timing. Genetics 139: 1247-1259.
65. YASUDA, K., H. ADACHI, Y. FUJIWARA and N. ISHII, 1999 Protein carbonyl accumulation in aging dauer formation-defective (daf) mutants of Caenorhabditis elegans. J. Gerontol. A Biol. Sci. Med. Sci. 54: B47-B51; discussion B52-B43.
66. YASUDA, K., T. ISHII, H. SUDA, A. AKATSUKA, P. S. HARTMAN et al., 2006 Age-related changes of mitochondrial structure and function in Caenorhabditis elegans. Mech. Ageing Dev. 127: 763-770.