Human Rad51 promotes mitochondrial DNA synthesis under conditions of increased replication stress

Mitochondrion

Volumn 13, Issue 4, 2013, Pages 350-356

  Sage, Jay M ^a   Knight, Kendall L ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

MtDNA copy number; MtDNA replication; Oxidative stress; Rad51; Replication restart

Indexed keywords

MITOCHONDRIAL DNA; RAD51 PROTEIN;

ARTICLE; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; DNA SYNTHESIS; DNA SYNTHESIS INHIBITION; GENE DOSAGE; HUMAN; HUMAN CELL; MITOCHONDRIAL DNA DEPLETION; MITOCHONDRIAL DNA REPLICATION; OSTEOSARCOMA CELL; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN FUNCTION; UPREGULATION;

CELL LINE; DNA REPLICATION; DNA, MITOCHONDRIAL; HUMANS; MITOCHONDRIA; RAD51 RECOMBINASE; STRESS, PHYSIOLOGICAL;

EID: 84877918786     PISSN: 15677249     EISSN: 18728278     Source Type: Journal    
DOI: 10.1016/j.mito.2013.04.004     Document Type: Article

References (47)

1. Arnaudeau C., Lundin C., Helleday T. DNA double-strand breaks associated with replication forks are predominantly repaired by homologous recombination involving an exchange mechanism in mammalian cells. J. Mol. Biol. 2001, 307:1235-1245.
2. Bacman S.R., Williams S.L., Moraes C.T. Intra- and inter-molecular recombination of mitochondrial DNA after in vivo induction of multiple double-strand breaks. Nucleic Acids Res. 2009, 37:4218-4226.
3. Bennett B.T., Knight K.L. Cellular localization of human Rad51C and regulation of ubiquitin-mediated proteolysis of Rad51. J. Cell. Biochem. 2005, 96:1095-1109.
4. Brown T.A., Clayton D.A. Release of replication termination controls mitochondrial DNA copy number after depletion with 2',3'-dideoxycytidine. Nucleic Acids Res. 2002, 30:2004-2010.
5. Chen F., Nastasi A., Shen Z., Brenneman M., Crissman H., Chen D.J. Cell cycle-dependent protein expression of mammalian homologs of yeast DNA double-strand break repair genes Rad51 and Rad52. Mutat. Res. 1997, 384:205-211.
6. Cox M.M., Goodman M.F., Kreuzer K.N., Sherratt D.J., Sandler S.J., Marians K.J. The importance of repairing stalled replication forks. Nature 2000, 404:37-41.
7. Davis A.F., Clayton D.A. In situ localization of mitochondrial DNA replication in intact mammalian cells. J. Cell Biol. 1996, 135:883-893.
8. Davis A.P., Symington L.S. RAD51-dependent break-induced replication in yeast. Mol. Cell. Biol. 2004, 24:2344-2351.
9. Feng J.Y., Johnson A.A., Johnson K.A., Anderson K.S. Insights into the molecular mechanism of mitochondrial toxicity by AIDS drugs. J. Biol. Chem. 2001, 276:23832-23837.
10. Ferecatu I., Bergeaud M., Rodriguez-Enfedaque A., Le Floch N., Oliver L., Rincheval V., Renaud F., Vallette F.M., Mignotte B., Vayssiere J.-L. Mitochondrial localization of the low level p53 protein in proliferative cells. Biochem. Biophys. Res. Commun. 2009, 387:772-777.
11. Flores-Rozas H., Kolodner R.D. Links between replication, recombination and genome instability in eukaryotes. Trends Biochem. Sci. 2000, 25:196-200.
12. Graziewicz M.A., Longley M.J., Copeland W.C. DNA polymerase gamma in mitochondrial DNA replication and repair. Chem. Rev. 2006, 106:383-405.
13. Groth P., Orta M.L., Elvers I., Majumder M.M., Lagerqvist A., Helleday T. Homologous recombination repairs secondary replication induced DNA double-strand breaks after ionizing radiation. Nucleic Acids Res. 2012, 40:6585-6594.
14. Hartlerode A., Odate S., Shim I., Brown J., Scully R. Cell cycle-dependent induction of homologous recombination by a tightly regulated I-SceI fusion protein. PLoS One 2011, 6:e16501.
15. Helleday T. Pathways for mitotic homologous recombination in mammalian cells. Mutat. Res. 2003, 532:103-115.
16. Heller R.C., Marians K.J. Replisome assembly and the direct restart of stalled replication forks. Nat. Rev. Mol. Cell Biol. 2006, 7:932-943.
17. Henson S.E., Tsai S.C., Malone C.S., Soghomonian S.V., Ouyang Y., Wall R., Marahrens Y., Teitell M.A. Pir51, a Rad51-interacting protein with high expression in aggressive lymphoma, controls mitomycin C sensitivity and prevents chromosomal breaks. Mutat. Res. 2006, 601:113-124.
18. Jeng J.Y., Yeh T.S., Lee J.W., Lin S.H., Fong T.H., Hsieh R.H. Maintenance of mitochondrial DNA copy number and expression are essential for preservation of mitochondrial function and cell growth. J. Cell. Biochem. 2008, 103:347-357.
19. Kajander O.A., Karhunen P.J., Holt I.J., Jacobs H.T. Prominent mitochondrial DNA recombination intermediates in human heart muscle. EMBO Rep. 2001, 2:1007-1012.
20. Kim T.M., Ko J.H., Hu L., Kim S.A., Bishop A.J., Vijg J., Montagna C., Hasty P. RAD51 mutants cause replication defects and chromosomal instability. Mol. Cell. Biol. 2012, 32:3663-3680.
21. Ko J.-C., Chen H.-J., Huang Y.-C., Tseng S.-C., Weng S.-H., Wo T.-Y., Huang Y.-J., Chiu H.-C., Tsai M.-S., Chiou R.Y.Y., Lin Y.-W. HSP90 inhibition induces cytotoxicity via down-regulation of Rad51 expression and DNA repair capacity in non-small cell lung cancer cells. Regul. Toxicol. Pharmacol. 2012, 64:415-424.
22. Kreuzer K.N. Interplay between DNA replication and recombination in prokaryotes. Annu. Rev. Microbiol. 2005, 59:43-67.
23. Lee H.C., Wei Y.H. Mitochondrial biogenesis and mitochondrial DNA maintenance of mammalian cells under oxidative stress. Int. J. Biochem. Cell Biol. 2005, 37:822-834.
24. Lee H.C., Yin P.H., Lu C.Y., Chi C.W., Wei Y.H. Increase of mitochondria and mitochondrial DNA in response to oxidative stress in human cells. Biochem. J. 2000, 348(Pt 2):425-432.
25. Lee H.C., Yin P.H., Chi C.W., Wei Y.H. Increase in mitochondrial mass in human fibroblasts under oxidative stress and during replicative cell senescence. J. Biomed. Sci. 2002, 9:517-526.
26. Liu P., Demple B. DNA repair in mammalian mitochondria: much more than we thought?. Environ. Mol. Mutagen. 2010, 51:417-426.
27. Lundin C., Erixon K., Arnaudeau C., Schultz N., Jenssen D., Meuth M., Helleday T. Different roles for nonhomologous end joining and homologous recombination following replication arrest in mammalian cells. Mol. Cell. Biol. 2002, 22:5869-5878.
28. Lundin C., Schultz N., Arnaudeau C., Mohindra A., Hansen L.T., Helleday T. RAD51 is involved in repair of damage associated with DNA replication in mammalian cells. J. Mol. Biol. 2003, 328:521-535.
29. Marchenko N.D., Zaika A., Moll U.M. Death signal-induced localization of p53 to mitochondria. A potential role in apoptotic signaling. J. Biol. Chem. 2000, 275:16202-16212.
30. McGlynn P., Lloyd R.G. Recombinational repair and restart of damaged replication forks. Nat. Rev. Mol. Cell Biol. 2002, 3:859-870.
31. Mineri R., Pavelka N., Fernandez-Vizarra E., Ricciardi-Castagnoli P., Zeviani M., Tiranti V. How do human cells react to the absence of mitochondrial DNA?. PLoS One 2009, 4:e5713.
32. Petermann E., Helleday T. Pathways of mammalian replication fork restart. Nat. Rev. Mol. Cell Biol. 2010, 11:683-687.
33. Pohjoismaki J.L., Goffart S. Of circles, forks and humanity: topological organisation and replication of mammalian mitochondrial DNA. BioEssays 2011, 33:290-299.
34. Pohjoismaki J.L., Goffart S., Tyynismaa H., Willcox S., Ide T., Kang D., Suomalainen A., Karhunen P.J., Griffith J.D., Holt I.J., Jacobs H.T. Human heart mitochondrial DNA is organized in complex catenated networks containing abundant four-way junctions and replication forks. J. Biol. Chem. 2009, 284:21446-21457.
35. Pohjoismaki J.L., Goffart S., Taylor R.W., Turnbull D.M., Suomalainen A., Jacobs H.T., Karhunen P.J. Developmental and pathological changes in the human cardiac muscle mitochondrial DNA organization, replication and copy number. PLoS One 2010, 5:e10426.
36. Raderschall E., Stout K., Freier S., Suckow V., Schweiger S., Haaf T. Elevated levels of Rad51 recombination protein in tumor cells. Cancer Res. 2002, 62:219-225.
37. Roseaulin L., Yamada Y., Tsutsui Y., Russell P., Iwasaki H., Arcangioli B. Mus81 is essential for sister chromatid recombination at broken replication forks. EMBO J. 2008, 27:1378-1387.
38. Rothkamm K., Kruger I., Thompson L.H., Lobrich M. Pathways of DNA double-strand break repair during the mammalian cell cycle. Mol. Cell. Biol. 2003, 23:5706-5715.
39. Sage J.M., Gildemeister O.S., Knight K.L. Discovery of a novel function for human Rad51: maintenance of the mitochondrial genome. J. Biol. Chem. 2010, 285:18984-18990.
40. Saintigny Y., Delacote F., Vares G., Petitot F., Lambert S., Averbeck D., Lopez B.S. Characterization of homologous recombination induced by replication inhibition in mammalian cells. EMBO J. 2001, 20:3861-3870.
41. Salazar J.J., Van Houten B. Preferential mitochondrial DNA injury caused by glucose oxidase as a steady generator of hydrogen peroxide in human fibroblasts. Mutat. Res. 1997, 385:139-149.
42. Saleh-Gohari N., Bryant H.E., Schultz N., Parker K.M., Cassel T.N., Helleday T. Spontaneous homologous recombination is induced by collapsed replication forks that are caused by endogenous DNA single-strand breaks. Mol. Cell. Biol. 2005, 25:7158-7169.
43. Shokolenko I., Venediktova N., Bochkareva A., Wilson G.L., Alexeyev M.F. Oxidative stress induces degradation of mitochondrial DNA. Nucleic Acids Res. 2009, 37:2539-2548.
44. Stewart J.D., Schoeler S., Sitarz K.S., Horvath R., Hallmann K., Pyle A., Yu-Wai-Man P., Taylor R.W., Samuels D.C., Kunz W.S., Chinnery P.F. POLG mutations cause decreased mitochondrial DNA repopulation rates following induced depletion in human fibroblasts. Biochim. Biophys. Acta 2011, 1812:321-325.
45. Vispe S., Cazaux C., Lesca C., Defais M. Overexpression of Rad51 protein stimulates homologous recombination and increases resistance of mammalian cells to ionizing radiation. Nucleic Acids Res. 1998, 26:2859-2864.
46. Wei Y.H., Lee C.F., Lee H.C., Ma Y.S., Wang C.W., Lu C.Y., Pang C.Y. Increases of mitochondrial mass and mitochondrial genome in association with enhanced oxidative stress in human cells harboring 4,977 BP-deleted mitochondrial DNA. Ann. N. Y. Acad. Sci. 2001, 928:97-112.
47. Zimmermann W., Chen S.M., Bolden A., Weissbach A. Mitochondrial DNA replication does not involve DNA polymerase alpha. J. Biol. Chem. 1980, 255:11847-11852.