Repression of the mitochondrial peroxiredoxin antioxidant system does not shorten life span but causes reduced fitness in Caenorhabditis elegans

Free Radical Biology and Medicine

Volumn 63, Issue , 2013, Pages 381-389

  Ranjan, Manickaratnam ^a   Grubern, Jan ^a   Ng, Li Fang ^a   Halliwell, Barry ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

C. elegans; Mitochondria; Peroxiredoxin 3; Reactive oxygen species

Indexed keywords

ADENOSINE TRIPHOSPHATE; ANTIOXIDANT; HYDROGEN PEROXIDE; PEROXIREDOXIN 2; PEROXIREDOXIN 3; PEROXIREDOXIN 6; SUPEROXIDE DISMUTASE;

ANIMAL EXPERIMENT; ARTICLE; BACTERIAL CELL; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; GENE REPRESSION; LIFE EXTENSION; LIFESPAN; MITOCHONDRIAL MEMBRANE POTENTIAL; MOLECULAR CLONING; NONHUMAN; OXIDATIVE PHOSPHORYLATION UNCOUPLING; OXYGEN CONSUMPTION; PHENOTYPE; PRIORITY JOURNAL; RNA ISOLATION; STEADY STATE;

CAENORHABDITIS ELEGANS; NEMATODA;

EID: 84879468493     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2013.05.025     Document Type: Article

References (42)

1. Collins, J.; Huang, C.; Hughes, S.; Kornfeld, K. The measurement and analysis of age-related changes in Caenorhabditis elegans. WormBook 24: 1-21; 2008.
2. Holliday, R. Aging is no longer an unsolved problem in biology. Ann. N. Y. Acad. Sci 1067: 1-9; 2006. (Pubitemid 43806303)
3. Harman, D. Aging: a theory based on free radical and radiation chemistry. J. Gerontol. 11 : 298-300; 1956.
4. Harman, D. The biologic clock: the mitochondria? J. Am. Geriatr. Soc. 20: 14 5-147 ; 197 2 .
5. Kumsta, C.; Jakob, U. Redox-regulated chaperones. Biochemistry. 48: 4666-4676; 2009.
6. Cox, A.; Winterbourn, C.; Hampton, M. Mitochondrial peroxiredoxin involvement in antioxidant defence and redox signalling. Biochem. J. 425: 313-325; 2009.
7. Huang, T. T.; Carlson, E. J.; Kozy, H. M.; Mantha, S.; Goodman, S. I.; Ursell, P. C., et al. Genetic modification of prenatal lethality and dilated cardiomyopathy in Mn superoxide dismutase mutant mice. Free Radic. Biol. Med. 31: 110 1 -1110 ; 2001. (Pubitemid 33000132)
8. Phillips, J. P.; Campbell, S. D.; Michaud, D.; Charbonneau, M.; Hilliker, A. J. Null mutation of copper/zinc superoxide dismutase in Drosophila confers hyper-sensitivity to paraquat and reduced longevity. Proc. Natl. Acad. Sci. USA 86: 2761-2765; 1989. (Pubitemid 19112621)
9. Duttaroy, A.; Paul, A.; Kundu, M.; Belton, A. A Sod2 null mutation confers severely reduced adult life span in Drosophila. Genetics 165: 2295-2299; 2003. (Pubitemid 38040309)
10. Sun, J.; Folk, D.; Bradley, T. J.; Tower, J. Induced overexpression of mitochon-drial Mn-superoxide dismutase extends the life span of adult Drosophila melanogaster. Genetics 161: 661-672; 2002. (Pubitemid 34705407)
11. Schriner, S. E.; Linford, N. J. Extension of mouse lifespan by overexpression of catalase. Age (Dordrecht, Netherlands) 28: 209-218; 2006. (Pubitemid 44197731)
12. Oláhová, M.; Taylor, S. R.; Khazaipoul, S.; Wang, J.; Morgan, B. A.; Matsumoto, K., et al. A redox-sensitive peroxiredoxin that is important for longevity has tissue- and stress-specific roles in stress resistance. Proc. Natl. Acad. Sci. USA 10 5 : 19839-19844; 2008.
13. Hartman, P.; Belmont, P.; Zuber, S.; Ishii, N.; Anderson, J. Relationship between catalase and life span in recombinant inbred strains of Caenorhabditis elegans. J. Nematol. 35: 314-319; 2003. (Pubitemid 37518971)
14. Larsen, P. L. Aging and resistance to oxidative damage in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 90: 8905-8909; 1993. (Pubitemid 23306419)
15. Petriv, O. I.; Rachubinski, R. A. Lack of peroxisomal catalase causes a progeric phenotype in Caenorhabditis elegans. J. Biol. Chem. 279: 19996-20001; 2004. (Pubitemid 38623442)
16. Miwa, S.; Riyahi, K.; Partridge, L.; Brand, M. Lack of correlation between mitochondrial reactive oxygen species production and life span in Drosophila. Ann. N. Y. Acad. Sci 1019: 388-391; 2004. (Pubitemid 38951342)
17. Van Raamsdonk, J. M.; Hekimi, S. Reactive oxygen species and aging in Caenorhabditis elegans: causal or casual relationship? Antioxid Redox Signaling 13: 1911-1953; 2010.
18. Doonan, R.; McElwee, J. J.; Matthijssens, F.; Walker, G. A.; Houthoofd, K.; Back, P.; Matscheski, A.; Vanfleteren, J. R.; Gems, D. Against the oxidative damage theory of aging superoxide dismutases protect against oxidative stress but have little or no effect on lifespan in Caenorhabditis elegans. Genes Dev. 22: 3236-3241; 2008.
19. Pérez, V. I.; Bokov, A.; Van Remmen, H.; Mele, J.; Ran, Q.; Ikeno, Y.; Richardson, A. Is the oxidative stress theory of aging dead? Biochim Biophys. Acta 1790: 1005-1014; 2009.
20. Isermann, K.; Liebau, E.; Roeder, T.; Bruchhaus, I. A peroxiredoxin specifically expressed in two types of pharyngeal neurons is required for normal growth and egg production in Caenorhabditis elegans. J. Mol. Biol. 338: 745-755; 2004. (Pubitemid 38507419)
21. Yang, W.; Li, J.; Hekimi, S. A measurable increase in oxidative damage due to reduction in superoxide detoxification fails to shorten the lifespan of long-lived mitochondrial mutants of Caenorhabditis elegans. Genetics 177: 2063-2074; 2007. (Pubitemid 350276988)
22. Raamsdonk, J. M. V.; Hekimi, S. Deletion of the mitochondrial superoxide dismutase sod-2 extends lifespan in Caenorhabditis elegans. PLoS Genet. 5: e1000361; 2009.
23. Gruber, J.; Ng, L. F.; Fong, S.; Wong, Y T.; Koh, S. A.; Chen, C. B.; Shui, G.; Cheong, W. F.; Schaffer, S.; Wenk, M. R.; Halliwell, B. Mitochondrial changes in ageing Caenorhabditis elegans - what do we learn from superoxide dismutase knockouts? PLoS One e19444; 2011.
24. Kamath, R.S.; Martinez-Campos, M.; Zipperlen, P.; Fraser, A.G.; Ahringer, J. Effectiveness of specific RNA-mediated interference through ingested double-stranded RNA in Caenorhabditis elegans. Genome Biol. 2(1): 2001.
25. Stiernagle, T. Maintenance of C. elegans. WormBook 11: 1-11; 2006.
26. Lewis, J. A.; Fleming, J. T. Basic culture methods. Methods Cell Biol. 48: 3-29; 1995.
27. Invitrogen. Transformation protocol. Available from (http://tools. invitrogen. com/content/sfs/manuals/subcloningefficiencydh5alpha-man.pdf) [updated 2012; accessed 12 December 2012].
28. Timmons, L.; Fire, A. Specific interference by ingested dsRNA. Nature 395: 854; 1998.
29. Herndon, L A.; Schmeissner, P. J.; Dudaronek, J. M.; Brown, P. A.; Listner, K. M.; Sakano, Y; Paupard, M. C; Hall, D. H.; Driscoll, M. Stochastic and genetic factors influence tissue-specific decline in ageing C. elegans. Nature 419: 808-814; 2002. (Pubitemid 35238561)
30. Halliwell, B.; Gutteridge, J. M. C. Free Radicals in Biology and Medicine. Oxford: Oxford Univ. Press; 2007.
31. Chen, X.; Zhong, Z.; Xu, Z.; Chen, L; Wang, Y 2',7'- Dichlorodihydrofluorescein as a fluorescent probe for reactive oxygen species measurement: forty years of application and controversy. Free Radic. Res. 44: 587-604; 2010.
32. Schaffer, S.; Gruber, J.; Ng, L.; Fong, S.; Wong, Y; Tang, S.; Halliwell, B. The effect of dichloroacetate on health- and lifespan in C. elegans. Biogerontology 12: 195-209; 2011.
33. Dinis-Oliveira, R. J.; Duarte, J. A.; Sánchez-Navarro, A.; Remião, F.; Bastos, M. L; Carvalho, F. Paraquat poisonings: mechanisms of lung toxicity, clinical features, and treatment. Crit. Rev. Toxicol. 38: 13-71; 2008.
34. Iser, W B.; Kim, D.; Bachman, E.; Wolkow, C. Examination of the requirement for ucp-4, a putative homolog of mammalian uncoupling proteins, for stress tolerance and longevity in C. elegans. Mech. AgeingDev. 126: 1090-1096; 2005. (Pubitemid 41253860)
35. Holliday, R.; Rattan, S. I. S. Longevity mutants do not establish any "new science" of ageing. Biogerontology 11: 507-511; 2010.
36. Radyuk, S. N.; Rebrin, I.; Klichko, V. I.; Sohal, B. H.; Michalak, K.; Benes, J.; Sohal, R. S.; Orr, W C. Mitochondrial peroxiredoxins are critical for the maintenance of redox state and the survival of adult Drosophila. Free Radic. Biol. Med. 49: 1892-1902; 2010.
37. Li, L; Shoji, W; Oshima, H.; Obinata, M.; Fukumoto, M.; Kanno, N. Crucial role of peroxiredoxin III in placental antioxidant defense of mice. FEBS Lett. 582: 2431-2434; 2008.
38. Li, L.; Kaifu, T.; Obinata, M.; Takai, T. Peroxiredoxin III-deficiency sensitizes macrophages to oxidative stress. J. Biochem. 145: 425-427; 2009.
39. Forman, H. J.; Maiorino, M.; Ursini, F. Signaling functions of reactive oxygen species. Biochemistry 49: 835-842; 2010.
40. D'Autréaux, B.; Toledano, M. B. ROS as signalling molecules: mechanisms that generate specificity in ROS homeostasis. Nat. Rev. Mol. Cell Biol. 8: 813-824; 2007. (Pubitemid 47462134)
41. Jain, C; Yun, M.; Politz, S.; Rao, R. A pathogenesis assay using Saccharomyces cerevisiae and Caenorhabditis elegans reveals novel roles for yeast AP-1, Yap1, and host dual oxidase BLI-3 in fungal pathogenesis. Eukaryotic Cell 8: 1218-1227; 2009.
42. Chávez, V.; Mohri-Shiomi, A.; Maadani, A.; Vega, L.; Garsin, D. Oxidative stress enzymes are required for DAF-16-mediated immunity due to generation of reactive oxygen species by Caenorhabditis elegans. Genetics 176: 1567-1577; 2007. (Pubitemid 47105218)