Effects of sod gene overexpression and deletion mutation on the expression profiles of reporter genes of major detoxification pathways in Caenorhabditis elegans

Experimental Gerontology

Volumn 45, Issue 7-8, 2010, Pages 603-610

  Back, Patricia ^a   Matthijssens, Filip ^a   Vlaeminck, Caroline ^a   Braeckman, Bart P ^a   Vanfleteren, Jacques R ^a  

^a GHENT UNIVERSITY   (Belgium)

Author keywords

Aging; Caenorhabditis elegans; Compensatory gene regulation; Insulin like signaling; Reporter gene expression; SOD; Sod Deletion mutants; Sod 1 Overexpressor

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE; MANGANESE SUPEROXIDE DISMUTASE; MESSENGER RNA; SUPEROXIDE DISMUTASE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR DAF 16; TRANSCRIPTION FACTOR DAF 2; TRANSCRIPTION FACTOR SKN 1; TRANSCRIPTION FACTOR SOD; UNCLASSIFIED DRUG;

ARTICLE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; CYTOSOL; DELETION MUTANT; DETOXIFICATION; DOWN REGULATION; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE OVEREXPRESSION; GENE TARGETING; LARVA; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; REPORTER GENE; SIGNAL TRANSDUCTION; TEMPERATURE; TRANSCRIPTION REGULATION; UPREGULATION;

AGING; ANIMALS; ANIMALS, GENETICALLY MODIFIED; BINDING SITES; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; DNA-BINDING PROTEINS; GATA TRANSCRIPTION FACTORS; GENE DELETION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, HELMINTH; GENES, REPORTER; LONGEVITY; METABOLIC DETOXICATION, DRUG; MUTATION; OXIDATIVE STRESS; PROMOTER REGIONS, GENETIC; RNA, HELMINTH; RNA, MESSENGER; SIGNAL TRANSDUCTION; SUPEROXIDE DISMUTASE; TRANSCRIPTION FACTORS;

ANIMALIA; CAENORHABDITIS ELEGANS;

EID: 77953358884     PISSN: 05315565     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.exger.2010.01.014     Document Type: Article

References (64)

1. An J.H., Blackwell T.K. SKN-1 links C. elegans mesendodermal specification to a conserved oxidative stress response. Genes Dev. 2003, 17:1882-1893.
2. An J.H., Vranas K., Lucke M., Inoue H., Hisamoto N., Matsumoto K., Blackwell T.K. Regulation of the Caenorhabditis elegans oxidative stress defense protein SKN-1 by glycogen synthase kinase-3. Proc. Natl. Acad. Sci. USA 2005, 102:16275-16280.
3. Apfeld J., O'connor G., Mcdonagh T., Distefano P.S., Curtis R. The AMP-activated protein kinase AAK-2 links energy levels and insulin-like signals to lifespan in C. elegans. Genes Dev. 2004, 18:3004-3009.
4. Berdichevsky A., Guarente L. A stress response pathway involving sirtuins, forkheads and 14-3-3 proteins. Cell Cycle 2006, 5:2588-2591.
5. Berdichevsky A., Viswanathan M., Horvitz H.R., Guarente L. C. elegans SIR-2.1 interacts with 14-3-3 proteins to activate DAF-16 and extend life span. Cell 2006, 125:1165-1177.
6. Bokov A., Chaudhuri A., Richardson A. The role of oxidative damage and stress in aging. Mech. Ageing Dev. 2004, 125:811-826.
7. Budovskaya Y.V., Wu K., Southworth L.K., Jiang M., Tedesco P., Johnson T.E., Kim S.K. An elt-3/elt-5/elt-6 GATA transcription circuit guides aging in C. elegans. Cell 2008, 134:291-303.
8. Curtis R., O'connor G., Distefano P.S. Aging networks in Caenorhabditis elegans: AMP-activated protein kinase (AAK-2) links multiple aging and metabolism pathways. Aging Cell 2006, 5:119-126.
9. Daitoku H., Fukamizu A. FOXO transcription factors in the regulatory networks of longevity. J. Biochem. 2007, 141:769-774.
10. Donko A., Peterfi Z., Sum A., Leto T., Geiszt M. Dual oxidases. Phil. Trans. R. Soc. B 2005, 360:2301-2308.
11. 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 life span in Caenorhabditis elegans. Genes Dev. 2008, 22:3236-3241.
12. Duret L., Guex N., Peitsch M.C., Bairoch A. New insulin-like proteins with atypical disulfide bond pattern characterized in Caenorhabditis elegans by comparative sequence analysis and homology modeling. Genome Res. 1998, 8:348-353.
13. Essers M.A., de Vries-Smits L.M., Barker N., Polderman P.E., Burgering B.M., Korswagen H.C. Functional interaction between β-catenin and FOXO in oxidative stress signaling. Science 2005, 308:1181-1184.
14. Fujii M., Ishii N., Joguchi A., Yasuda K., Ayusawa D. A novel superoxide dismutase gene encoding membrane-bound and extracellular isoforms by alternative splicing in Caenorhabditis elegans. DNA Res. 1998, 5:25-30.
15. Giglio M.P., Hunter T., Bannister J.V., Bannister W.H., Hunter G.J. The manganese superoxide dismutase gene of Caenorhabditis elegans. Biochem. Mol. Biol. Int. 1994, 33:37-40.
16. Goldstein B.J., Mahadev K., Wu X. Redox paradox: insulin action is facilitated by insulin-stimulated reactive oxygen species with multiple potential signaling targets. Diabetes 2005, 54:311-321.
17. Hamilton B., Dong Y., Shindo M., Liu W., Odell I., Ruvkun G., Lee S.S. A systematic RNAi screen for longevity genes in C. elegans. Genes Dev. 2005, 19:1544-1555.
18. Hardie D.G. The AMP-activated protein kinase pathway - new players upstream and downstream. J. Cell Sci. 2004, 117:5479-5487.
19. Harman D. Aging: a theory based on free radical and radiation chemistry. J. Gerontol. 1956, 11:298-300.
20. Hartwig K., Heidler T., Moch J., Daniel H., Wenzel U. Feeding a ROS-generator to Caenorhabditis elegans leads to increased expression of small heat shock protein HSP-16.2 and hormesis. Genes Nutr. 2009, 4:59-67.
21. Hellemans J., Mortier G., De Paepe A., Speleman F., Vandesompele J. QBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol. 2007, 8:R19.
22. Henderson S.T., Johnson T.E. Daf-16 integrates developmental and environmental inputs to mediate aging in the nematode Caenorhabditis elegans. Curr. Biol. 2001, 11:1975-1980.
23. Hertweck M., Gobel C., Baumeister R. C. elegans SGK-1 is the critical component in the Akt/PKB kinase complex to control stress response and life span. Dev. Cell 2004, 6:577-588.
24. Hofmann B., Hecht H.J., Flohe L. Peroxiredoxins. Biol. Chem. 2002, 383:347-364.
25. Honda Y., Honda S. The daf-2 gene network for longevity regulates oxidative stress resistance and Mn-superoxide dismutase gene expression in Caenorhabditis elegans. FASEB J. 1999, 13:1385-1393.
26. Honda Y., Tanaka M., Honda S. Modulation of longevity and diapause by redox regulation mechanisms under the insulin-like signaling control in Caenorhabditis elegans. Exp. Gerontol. 2008, 43:520-529.
27. Hoogewijs D., Houthoofd K., Matthijssens F., Vandesompele J., Vanfleteren J.R. Selection and validation of a set of reliable reference genes for quantitative sod gene expression analysis in C. elegans. BMC Mol. Biol. 2008, 9:9.
28. Horng J.T., Lin F.M., Lin J.H., Huang H.D., Liu B.J. Database of repetitive elements in complete genomes and data mining using transcription factor binding sites. IEEE Trans. Inf. Technol. Biomed. 2003, 7:93-100.
29. Houthoofd K., Fidalgo M.A., Hoogewijs D., Braeckman B.P., Lenaerts I., Brys K., Matthijssens F., De Vreese A., Van Eygen S., Munoz M.J., Vanfleteren J.R. Metabolism, physiology and stress defense in three aging Ins/IGF-1 mutants of the nematode Caenorhabditis elegans. Aging Cell 2005, 4:87-95.
30. Hsu A.L., Murphy C.T., Kenyon C. Regulation of aging and age-related disease by DAF-16 and heat-shock factor. Science 2003, 300:1142-1145.
31. Inoue H., Hisamoto N., An J.H., Oliveira R.P., Nishida E., Blackwell T.K., Matsumoto K. The C. elegans p38 MAPK pathway regulates nuclear localization of the transcription factor SKN-1 in oxidative stress response. Genes Dev. 2005, 19:2278-2283.
32. Kimura K., Tanaka N., Nakamura N., Takano S., Ohkuma S. Knockdown of mitochondrial heat shock protein 70 promotes progeria-like phenotypes in Caenorhabditis elegans. J. Biol. Chem. 2007, 282:5910-5918.
33. Kimura K.D., Tissenbaum H.A., Liu Y., Ruvkun G. Daf-2, an insulin receptor-like gene that regulates longevity and diapause in Caenorhabditis elegans. Science 1997, 277:942-946.
34. Kondo M., Yanase S., Ishii T., Hartman P.S., Matsumoto K., Ishii N. The p38 signal transduction pathway participates in the oxidative stress-mediated translocation of DAF-16 to Caenorhabditis elegans nuclei. Mech. Ageing Dev. 2005, 126:642-647.
35. Larsen P.L. Aging and resistance to oxidative damage in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 1993, 90:8905-8909.
36. Lee H., Cho J.S., Lambacher N., Lee J., Lee S.J., Lee T.H., Gartner A., Koo H.S. The Caenorhabditis elegans AMP-activated protein kinase AAK-2 is phosphorylated by LKB1 and is required for resistance to oxidative stress and for normal motility and foraging behavior. J. Biol. Chem. 2008, 283:14988-14993.
37. 2. J. Biol. Chem. 2002, 277:20336-20342.
38. Lehtinen M.K., Yuan Z.Q., Boag P.R., Yang Y., Villen J., Becker E.B.E., Dibacco S., De La Iglesia N., Gygi S., Blackwell T.K., Bonni A. A conserved MST-FOXO signaling pathway mediates oxidative-stress responses and extends life span. Cell 2006, 125:987-1001.
39. Leslie N.R., Bennett D., Lindsay Y.E., Stewart H., Gray A., Downes C.P. Redox regulation of PI 3-kinase signalling via inactivation of PTEN. EMBO J. 2003, 22:5501-5510.
40. Lin K., Dorman J.B., Rodan A., Kenyon C. Daf-16: an HNF-3/forkhead family member that can function to double the life-span of Caenorhabditis elegans. Science 1997, 278:1319-1322.
41. Link C.D., Cypser J.R., Johnson C.J., Johnson T.E. Direct observation of stress response in using a reporter transgene. Cell Stress Chaperones 1999, 4:235-242.
42. Loots G.G., Ovcharenko I., Pachter L., Dubchak I., Rubin E.M. RVista for comparative sequence-based discovery of functional transcription factor binding sites. Genome Res. 2002, 12:832-839.
43. McElwee J.J., Schuster E., Blanc E., Thomas J.H., Gems D. Shared transcriptional signature in Caenorhabditis elegans dauer larvae and long-lived daf-2 mutants implicates detoxification system in longevity assurance. J. Biol. Chem. 2004, 279:44533-44543.
44. Morris J.Z., Tissenbaum H.A., Ruvkun G. A phosphatidylinositol-3-OH kinase family member regulating longevity and diapause in Caenorhabditis elegans. Nature 1996, 382:536-539.
45. Murphy C.T., Mccarroll S.A., Bargmann C.I., Fraser A., Kamath R.S., Ahringer J., Li H., Kenyon C. Genes that act downstream of DAF-16 to influence the lifespan of Caenorhabditis elegans. Nature 2003, 424:277-284.
46. Ogg S., Paradis S., Gottlieb S., Patterson G.I., Lee L., Tissenbaum H.A., Ruvkun G. The Fork head transcription factor DAF-16 transduces insulin-like metabolic and longevity signals in C. elegans. Nature 1997, 389:994-999.
47. Ogg S., Ruvkun G. The C. elegans PTEN homolog, DAF-18, acts in the insulin receptor-like metabolic signaling pathway. Mol. Cell 1998, 2:887-893.
48. Oh S.W., Mukhopadhyay A., Svrzikapa N., Jiang F., Davis R.J., Tissenbaum H.A. JNK regulates lifespan in Caenorhabditis elegans by modulating nuclear translocation of forkhead transcription factor/DAF-16. Proc. Natl. Acad. Sci. USA 2005, 102:4494-4499.
49. Paradis S., Ailion M., Toker A., Thomas J.H., Ruvkun G. A PDK1 homolog is necessary and sufficient to transduce AGE-1 PI3 kinase signals that regulate diapause in Caenorhabditis elegans. Genes Dev. 1999, 13:1438-1452.
50. Paradis S., Ruvkun G. Caenorhabditis elegans Akt/PKB transduces insulin receptor-like signals from AGE-1 PI3 kinase to the DAF-16 transcription factor. Genes Dev. 1998, 12:2488-2498.
51. Park S.K., Tedesco P.M., Johnson T.E. Oxidative stress and longevity in Caenorhabditis elegans as mediated by SKN-1. Aging Cell 2009, 8:258-269.
52. Patel D.S., Garza-Garcia A., Nanji M., McElwee J.J., Ackerman D., Driscoll P.C., Gems D. Clustering of genetically defined allele classes in the Caenorhabditis elegans DAF-2 insulin/IGF-1 receptor. Genetics 2008, 178:931-946.
53. Pierce S.B., Costa M., Wisotzkey R., Devadhar S., Homburger S.A., Buchman A.R., Ferguson K.C., Heller J., Platt D.M., Pasquinelli A.A., Liu L.X., Doberstein S.K., Ruvkun G. Regulation of DAF-2 receptor signaling by human insulin and ins-1, a member of the unusually large and diverse C. elegans insulin gene family. Genes Dev. 2001, 15:672-686.
54. Sulston J.E., Hodgkin J. Methods, in: The Nematode Caenorhabditis elegans 1988, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
55. Tullet J.M., Hertweck M., An J.H., Baker J., Hwang J.Y., Liu S., Oliveira R.P., Baumeister R., Blackwell T.K. Direct inhibition of the longevity-promoting factor SKN-1 by insulin-like signaling in C. elegans. Cell 2008, 132:1025-1038.
56. Van Raamsdonk J.M., Hekimi S. Deletion of the mitochondrial superoxide dismutase sod-2 extends lifespan in Caenorhabditis elegans. PLoS Genet. 2009, 5:e1000361.
57. Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A., Speleman, F., 2002. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 3, RESEARCH0034.
58. Vanfleteren J.R. Oxidative stress and ageing in Caenorhabditis elegans. Biochem. J. 1993, 292(Pt 2):605-608.
59. Wang Y., Oh S.W., Deplancke B., Luo J., Walhout A.J., Tissenbaum H.A. C. elegans 14-3-3 proteins regulate life span and interact with SIR-2.1 and DAF-16/FOXO. Mech. Ageing Dev. 2006, 127:741-747.
60. Weinkove D., Halstead J.R., Gems D., Divecha N. Long-term starvation and ageing induce AGE-1/PI 3-kinase-dependent translocation of DAF-16/FOXO to the cytoplasm. BMC Biol. 2006, 4:1.
61. Wolff S., Ma H., Burch D., Maciel G.A., Hunter T., Dillin A. SMK-1, an essential regulator of DAF-16-mediated longevity. Cell 2006, 124:1039-1053.
62. Yanase S., Onodera A., Tedesco P., Johnson T.E., Ishii N. SOD-1 deletions in Caenorhabditis elegans alter the localization of intracellular reactive oxygen species and show molecular compensation. J. Gerontol. A. Biol. Sci. Med. Sci. 2009, 64:530-539.
63. Yang W., Li J.J., Hekimi S. 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 2007, 177:2063-2074.
64. Yokoyama K., Fukumoto K., Murakami T., Harada S., Hosono R., Wadhwa R., Mitsui Y., Ohkuma S. Extended longevity of Caenorhabditis elegans by knocking in extra copies of hsp70F, a homolog of mot-2 (mortalin)/mthsp70/Grp75. FEBS Lett. 2002, 516:53-57.