Caenorhabditis elegans ATR checkpoint kinase ATL-1 influences life span through mitochondrial maintenance

Mitochondrion

Volumn 13, Issue 6, 2013, Pages 729-735

  Suetomi, Kazuhiro ^a   Mereiter, Stefan ^a,b   Mori, Chihiro ^a   Takanami, Takako ^a   Higashitani, Atsushi ^a  

^a TOHOKU UNIVERSITY   (Japan)

^b UNIVERSITY OF VIENNA   (Austria)

Author keywords

Ataxia telangiectasia; DAF 16; Ethidium bromide; Longevity; Rotenone; SOD

Indexed keywords

ATR PROTEIN; CHECKPOINT KINASE ATL 1; ETHIDIUM BROMIDE; EXTRACELLULAR SUPEROXIDE DISMUTASE; LIPID; MALONALDEHYDE; MITOCHONDRIAL DNA; ROTENONE; TRANSCRIPTION FACTOR DAF 16; TRANSCRIPTION FACTOR FOXO; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; ATL 1 GENE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENZYME ACTIVITY; GENE; GENE DOSAGE; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; LIFESPAN; LIPID PEROXIDATION; LONGEVITY; MITOCHONDRION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; SOD 3 GENE; SOD 5 GENE;

ATAXIA TELANGIECTASIA; CAENORHABDITIS ELEGANS; EUKARYOTA; MAMMALIA;

4′,6-DIAMINO-2-PHENYLINDOLE; AT; ATAXIA TELANGIECTASIA; ATAXIA TELANGIECTASIA AND RAD3 RELATED PROTEIN; ATAXIA TELANGIECTASIA MUTATED; ATM; ATR; DAF-16; DAPI; DIMETHYL SULFOXIDE; DMSO; ELECTRON TRANSPORT CHAIN; ETBR; ETC.; ETHIDIUM BROMIDE; LONGEVITY; MALONDIALDEHYDE; MDA; MITOCHONDRIAL DNA; MTDNA; NEMATODE GROWTH MEDIUM; NGM; REACTIVE OXYGEN SPECIES; ROS; ROTENONE; SOD; SUPER OXIDE DISMUTASE;

ANIMALS; ATAXIA TELANGIECTASIA MUTATED PROTEINS; BASE SEQUENCE; CAENORHABDITIS ELEGANS; DNA PRIMERS; ENZYME ACTIVATION; LIPID PEROXIDATION; LONGEVITY; MALONDIALDEHYDE; MITOCHONDRIA; MUTATION; POLYMERASE CHAIN REACTION; SUPEROXIDE DISMUTASE; TRANSCRIPTION, GENETIC;

EID: 84887016160     PISSN: 15677249     EISSN: 18728278     Source Type: Journal    
DOI: 10.1016/j.mito.2013.02.004     Document Type: Article

References (54)

1. Abraham R.T. Cell cycle checkpoint signaling though the ATM and ATR kinases. Genes Dev. 2001, 15:2177-2196.
2. Aoki H., Sato S., Takanami T., Ishihara T., Katsura I., Takahashi H., Higashitani A. Characterization of Ce-atl-1, an ATM-like gene from Caenorhabditis elegans. Mol. Gen. Genet. 2000, 264:119-126.
3. Boder E. Ataxia-telangiectasia: some historic, clinical and pathologic observations. Birth Defects Orig. Artic. Ser. 1975, 11:255-270.
4. Boulton S.J., Gartner A., Reboul J., Vaglio P., Dyson N., Hill D.E., Vidal M. Combined functional genomic maps of the C. elegans DNA damage response. Science 2002, 295:127-131.
5. Brown E.J., Baltimore D. ATR disruption leads to chromosomal fragmentation and early embryonic lethality. Genes Dev. 2000, 14:397-402.
6. Cliby W.A., Roberts C.J., Cimprich K.A., Stringer C.M., Lamb J.R., Schreiber S.L., Friend S.H. Overexpression of a kinase-inactive ATR protein causes sensitivity to DNA-damaging agents and defects in cell cycle checkpoints. EMBO J. 1998, 17:159-169.
7. Cortez D., Guntuku S., Qin J., Elledge S.J. ATR and ATRIP: partners in checkpoint signaling. Science 2001, 294:1713-1716.
8. deKlein, A., Muijtjens, M., van Os, R., Verhoeven, Y., Smit, B., Carr, A.M., Lehmann, A.R., Hoeijmakers, J.H., 2000. Targeted disruption of the cell-cycle checkpoint gene ATR leads to early embryonic lethality in mice. 10:479-482. http://dx.doi.org/10.1111/gtc.12034.
9. Durocher D., Jackson S.P. DNA-PK, ATM and ATR as sensors of DNA damage: variations on a theme?. Curr. Opin. Cell Biol. 2001, 13:225-231.
10. Eaton J.S., Lin Z.P., Sartorelli A.C., Bonawitz N.D., Shadel G.S. Ataxia-telangiectasia mutated kinase regulates ribonucleotide reductase and mitochondrial homeostasis. J. Clin. Invest. 2007, 117:2723-2734.
11. Fridovich I. Superoxide radical and superoxide dismutases. Annu. Rev. Biochem. 1995, 64:97-112.
12. Garcia-Muse T., Boulton S.J. Distinct modes of ATR activation after replication stress and DNA double-strand breaks in Caenorhabditis elegans. EMBO J. 2005, 24:4345-4355.
13. Garsin D.A., Villanueva J.M., Begun J., Kim D.H., Sifri C.D., Calderwood S.B., Ruvkun G., Ausubel F.M. Long-lived C. elegans daf-2 mutants are resistant to bacterial pathogens. Science 2003, 300:1921.
14. Hartman P.S., Ishii N., Kayser E.B., Morgan P.G., Sedensky M.M. Mitochondrial mutations differentially affect aging, mutability and anesthetic sensitivity in Caenorhabditis elegans. Mech. Ageing Dev. 2001, 122:1187-1201.
15. 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.
16. 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.
17. Horgan D.J., Singer T.P., Casida J.E. Studies on the respiratory chain-linked reduced nicotinamide adenine dinucleotide dehydrogenase. XIII. Binding sites of rotenone, piericidin A, and amytal in the respiratory chain. J. Biol. Chem. 1967, 243:834-843.
18. 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.
19. Hunter T., Bannister W.H., Hunter G.J. Cloning, expression, and characterization of two manganese superoxide dismutases from Caenorhabditis elegans. J. Biol. Chem. 1997, 272:28652-28659.
20. Hurov K.E., Cotta-Ramusino C., Elledge S.J. A genetic screen identifies the Triple T complex required for DNA damage signaling and ATM and ATR stability. Genes Dev. 2010, 24:1939-1950.
21. Kimura T., Takanami T., Sakashita T., Wada S., Kobayashi Y., Higashitani A. Innate immune genes including a mucin-like gene, mul-1, induced by ionizing radiation in Caenorhabditis elegans. Radiat. Res. 2012, 178:313-320.
22. Kondo M., Senoo-Matsuda N., Yanase S., Ishii T., Hartman P.S., Ishii N. Effect of oxidative stress on translocation of DAF-16 in oxygen-sensitive mutants, mev-1 and gas-1 of Caenorhabditis elegans. Mech. Ageing Dev. 2005, 126:637-641.
23. Kwon E.S., Narasimhan S.D., Yen K., Tissenbaum H.A. A new DAF-16 isoform regulates longevity. Nature 2010, 466:498-502.
24. Lee R.Y., Hench J., Ruvkun G. Regulation of C. elegans DAF-16 and its human ortholog FKHRL1 by the daf-2 insulin-like signaling pathway. Curr. Biol. 2001, 11:1950-1957.
25. Lee S.S., Lee R.Y., Fraser A.G., Kamath R.S., Ahringer J., Ruvkun G. A systematic RNAi screen identifies a critical role for mitochondria in C. elegans longevity. Nat. Genet. 2003, 33:40-48.
26. Lewis J.A., Fleming J.T. Basic culture methods. Methods Cell Biol. 1995, 48:3-29.
27. Li J., Han Y.R., Plummer M.R., Herrup K. Cytoplasmic ATM in neurons modulates synaptic function. Curr. Biol. 2009, 19:2091-2096.
28. 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.
29. Lin K., Hsin H., Libina N., Kenyon C. Regulation of the Caenorhabditis elegans longevity protein DAF-16 by insulin/IGF-1 and germline signaling. Nat. Genet. 2001, 28:139-145.
30. Mori C., Takanami T., Higashitani A. Maintenance of mitochondrial DNA by the Caenorhabditis elegans ATR checkpoint protein ATL-1. Genetics 2008, 180:681-686.
31. Mori, C., Yamaguchi, Y., Teranishi, M., Takanami, T., Nagase, T., Kanno, S., Yasui, A., Higashitani, A., in press. Overexpression of ATR causes autophagic cell death. Genes Cells. http://dx.doi.org/10.1111/gtc.12034.
32. Morrow D.M., Tagle D.A., Shiloh Y., Collins F.S., Hieter P. TEL1, an S. cerevisiae homolog of the human gene mutated in ataxia telangiectasia, is functionally related to the yeast checkpoint gene MEC1. Cell 1995, 82:831-840.
33. Murakami S., Johnson T.E. A genetic pathway conferring life extension and resistance to UV stress in Caenorhabditis elegans. Genetics 1996, 143:1207-1218.
34. Murga M., Bunting S., Montana M.F., Soria R., Mulero F., Canamero M., Lee Y., McKinnon P.J., Nussenzweig A., Fernandez-Capetillo O. A mouse model of ATR-Seckel shows embryonic replicative stress and accelerated aging. Nat. Genet. 2009, 41:891-898.
35. Nass M.M. Differential effects of ethidium bromide on mitochondrial and nuclear DNA synthesis in vivo in cultured mammalian cells. Exp. Cell Res. 1972, 72:211-222.
36. O'Driscoll M. Mouse models for ATR deficiency. DNA Repair 2009, 8:1333-1337.
37. O'Driscoll M., Ruiz-Perez V.L., Woods C.G., Jeggo P.A., Goodship J.A. A splicing mutation affecting expression of ataxia-telangiectasia and Rad3-related protein (ATR) results in Seckel syndrome. Nat. Genet. 2003, 33:497-501.
38. Patel A.Y., McDonald T.M., Spears L.D., Ching J.K., Fisher J.S. Ataxia telangiectasia mutated influences cytochrome c oxidase activity. Biochem. Biophys. Res. Commun. 2011, 405:599-603.
39. Ritchie K.B., Mallory J.C., Petes T.D. Interactions of TLC1 (which encodes the RNA subunit of telomerase), TEL1, and MEC1 in regulating telomere length in the yeast Saccharomyces cerevisiae. Mol. Cell. Biol. 1999, 19:6065-6075.
40. Sampayo J.N., Gill M.S., Lithgow G.L. Oxidative stress and aging - the use of superoxide dismutase/catalase mimetics to extend lifespan. Biochem. Soc. Trans. 2003, 31:1305-1307.
41. Shanske A., Caride D.G., Menasse-Palmer L., Bogdanow A., Marion R.W. Central nervous system anomalies in Seckel syndrome: report of a new family and review of the literature. Am. J. Med. Genet. 1997, 70:155-158.
42. Shiloh Y. ATM (ataxia telangiectasia mutated): expanding roles in the DNA damage response and cellular homeostasis. Biochem. Soc. Trans. 2001, 29:661-666.
43. Shiloh Y. ATM and related protein kinases: safeguarding genome integrity. Nat. Rev. Cancer 2003, 3:155-168.
44. Sugimoto T., Dazai K., Sakashita T., Funayama M., Wada S., Hamada N., Kakizaki T., Kobayashi Y., Higashitani A. Cell cycle arrest and apoptosis in Caenorhabditis elegans germline cells following heavy-ion microbeam irradiation. Int. J. Radiat. Biol. 2006, 82:31-38.
45. Sugimoto T., Mori C., Takanami T., Sasagawa Y., Saito R., Ichiishi E., Higashitani A. Caenorhabditis elegans par2.1/mtssb-1 is essential for mitochondrial DNA replication and its defect causes comprehensive transcriptional alterations including a hypoxia response. Exp. Cell Res. 2008, 314:103-114.
46. Takai H., Wang R.C., Takai K.K., Yang H., de Lange T. Tel2 regulates the stability of PI3K-related protein kinases. Cell 2007, 131:1248-1259.
47. Takai H., Xie Y., de Lange T., Pavletich N.P. Tel2 structure and function in the Hsp90-dependent maturation of mTOR and ATR complexes. Genes Dev. 2010, 24:2019-2030.
48. Thomas A.W., Majid A., Sherratt E.J., Gagg J.W., Alcolado J.C. Differential expression of mRNA in human thyroid cells depleted of mitochondrial DNA by ethidium bromide treatment. Clin. Sci. (Lond.) 1999, 97:207-213.
49. Tsang W.Y., Lemire B.D. Mitochondrial genome content is regulated during nematode development. Biochem. Biophys. Res. Commun. 2002, 291:8-16.
50. Valentin-Vega Y.A., Maclean K.H., Tait-Mulder J., Milasta S., Steeves M., Dorsey F.C., Cleveland J.L., Green D.R., Kastan M.B. Mitochondrial dysfunction in ataxia-telangiectasia. Blood 2012, 119:1490-1500.
51. Ventura N., Rea S.L., Testi R. Long-lived C. elegans mitochondrial mutants as a model for human mitochondrial-associated diseases. Exp. Gerontol. 2006, 41:974-991.
52. Ventura N., Rea S.L., Schiavi A., Torgovnick A., Testi R., Johnson T.E. p53/CEP-1 increases or decreases lifespan, depending on level of mitochondrial bioenergetic stress. Aging Cell 2009, 8:380-393.
53. Wright J.A., Keegan K.S., Herendeen D.R., Bentley N.J., Carr A.M., Hoekstra M.F., Concannon P. Protein kinase mutants of human ATR increase sensitivity to UV and ionizing radiation and abrogate cell cycle checkpoint control. Proc. Natl. Acad. Sci. 1998, 95:7445-7450.
54. Yanase S., Ishii N. Hyperoxia exposure induced hormesis decreases mitochondrial superoxide radical levels via Ins/IGF-1 signaling pathway in a long-lived age-1 mutant of Caenorhabditis elegans. J. Radiat. Res. 2008, 49:211-218.