Evidence for a role of FEN1 in maintaining mitochondrial DNA integrity

DNA Repair

Volumn 8, Issue 10, 2009, Pages 1242-1249

  Kalifa, Lidza ^a   Beutner, Gisela ^b   Phadnis, Naina ^a   Sheu, Shey Shing ^b   Sia, Elaine A ^a  

^a UNIVERSITY OF ROCHESTER   (United States)

^b UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

FEN1; Mitochondria; Mitochondrial base excision repair; Mitochondrial DNA

Indexed keywords

DEOXYRIBONUCLEASE I; EXONUCLEASE; FLAP STRUCTURE SPECIFIC ENDONUCLEASE 1; MITOCHONDRIAL DNA; PROTEIN RAD27; UNCLASSIFIED DRUG;

ARTICLE; CELL AGING; CELL COMPARTMENTALIZATION; CELLULAR DISTRIBUTION; DNA DAMAGE; DNA INTEGRATION; DNA REPAIR; DNA SYNTHESIS; MITOCHONDRION; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SACCHAROMYCES CEREVISIAE;

ANIMALS; DNA REPAIR; DNA, MITOCHONDRIAL; FLAP ENDONUCLEASES; GENE DELETION; MALE; MICE; MICROSCOPY, FLUORESCENCE; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

MAMMALIA; MUS; SACCHAROMYCES CEREVISIAE;

EID: 70149110390     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2009.07.008     Document Type: Article

References (68)

1. Wallace D.C. Mitochondrial diseases in man and mouse. Science 283 (1999) 1482-1488
2. Bohr V.A. Repair of oxidative DNA damage in nuclear and mitochondrial DNA, and some changes with aging in mammalian cells. Free Radic Biol Med 32 (2002) 804-812
3. Hu J.P., Vanderstraeten S., and Foury F. Isolation and characterization of ten mutator alleles of the mitochondrial DNA polymerase-encoding MIP1 gene from Saccharomyces cerevisiae. Gene 160 (1995) 105-110
4. Trifunovic A., Wredenberg A., Falkenberg M., Spelbrink J.N., Rovio A.T., Bruder C.E., Bohlooly-Y M., Gidlof S., Oldfors A., Wibom R., Tornell J., Jacobs H.T., and Larsson N.-G. Premature ageing in mice expressing defective mitochondrial DNA polymerase. Nature 429 (2004) 417-423
5. Zhang H., Chatterjee A., and Singh K.K. Saccharomyces cerevisiae polymerase zeta functions in mitochondria. Genetics 172 (2006) 2683-2688
6. Kalifa L., and Sia E.A. Analysis of Rev1p and Pol zeta in mitochondrial mutagenesis suggests an alternative pathway of damage tolerance. DNA Repair (Amst) 6 (2007) 1732-1739
7. Phadnis N., Sia R.A., and Sia E.A. Analysis of repeat-mediated deletions in the mitochondrial genome of Saccharomyces cerevisiae. Genetics 71 (2005) 1549-1559
8. Morel F., Renoux M., Lachaume P., and Alziari S. Bleomycin-induced double-strand breaks in mitochondrial DNA of Drosophila cells are repaired. Mutat Res 637 (2008) 111-117
9. Pinz K.G., Shibutani S., and Bogenhagen D.F. Action of mitochondrial DNA polymerase gamma at sites of base loss or oxidative damage. J Biol Chem 270 (1995) 9202-9206
10. Stuart J.A., and Brown M.F. Mitochondrial DNA maintenance and bioenergetics. Biochim Biophys Acta 1757 (2006) 79-89
11. Croteau D.L., Stierum R.H., and Bohr V.A. Mitochondrial DNA repair pathways. Mutat Res 434 (1999) 137-148
12. Bohr V.A., Stevnsner T., and de Souza-Pinto N.C. Mitochondrial DNA repair of oxidative damage in mammalian cells. Gene 286 (2002) 127-134
13. Akbari M., Visnes T., Krokan H.E., and Otterlei M. Mitochondrial base excision repair of uracil and AP sites takes place by single-nucleotide insertion and long-patch DNA synthesis. DNA Repair (Amst) 7 (2008) 605-616
14. Liu P., Qian L., Sung J.S., de Souza-Pinto N.C., Zheng L., Bogenhagen D.F., Bohr V.A., Wilson III D.M., Shen B., and Demple B. Removal of oxidative DNA damage via FEN1-dependent long-patch base excision repair in human cell mitochondria. Mol Cell Biol 28 (2008) 4975-4987
15. Szczesny B., Tann A.W., Longley M.J., Copeland W.C., and Mitra S. Long patch base excision repair in mammalian mitochondrial genomes. J Biol Chem 283 (2008) 26349-26356
16. Wu X., and Wang Z. Relationships between yeast Rad27 and Apn1 in response to apurinic/apyrimidinic (AP) sites in DNA. Nucleic Acids Res 27 (1999) 956-962
17. Liu Y., Kao H.I., and Bambara R.A. Flap endonuclease 1: a central component of DNA metabolism. Annu Rev Biochem 73 (2004) 589-615
18. Sommers C.H., Miller E.J., Dujon B., Prakash S., and Prakash L. Conditional lethality of null mutations in RTH1 that encodes the yeast counterpart of a mammalian 5′- to 3′-exonuclease required for lagging strand DNA synthesis in reconstituted systems. J Biol Chem 270 (1995) 4193-4196
19. Reagan M.S., Pittenger C., Siede W., and Friedberg E.C. Characterization of a mutant strain of Saccharomyces cerevisiae with a deletion of the RAD27 gene, a structural homolog of the RAD2 nucleotide excision repair gene. J Bacteriol 177 (1995) 364-371
20. Zhu F.X., Biswas E.E., and Biswas S.B. Purification and characterization of the DNA polymerase alpha associated exonuclease: the RTH1 gene product. Biochemistry 36 (1997) 5947-5954
21. Turchi J.J., Huang L., Murante R.S., Kim Y., and Bambara R.A. Enzymatic completion of mammalian lagging-strand DNA replication. Proc Natl Acad Sci U S A 91 (1994) 9803-9807
22. Waga S., Bauer G., and Stillman B. Reconstitution of complete SV40 DNA replication with purified replication factors. J Biol Chem 269 (1994) 10923-10934
23. Ishimi Y., Claude A., Bullock P., and Hurwitz J. Complete enzymatic synthesis of DNA containing the SV40 origin of replication. J Biol Chem 263 (1988) 19723-19733
24. Ayyagari R., Gomes X.V., Gordenin D.A., and Burgers P.M. Okazaki fragment maturation in yeast. I. Distribution of functions between FEN1 AND DNA2. J Biol Chem 278 (2003) 1618-1625
25. Rossi M.L., and Bambara R.A. Reconstituted Okazaki fragment processing indicates two pathways of primer removal. J Biol Chem 281 (2006) 26051-26061
26. Johnson R.E., Kovvali G.K., Prakash L., and Prakash S. Requirement of the yeast RTH1 5′ to 3′ exonuclease for the stability of simple repetitive DNA. Science 269 (1995) 238-240
27. Tishkoff D.X., Filosi N., Gaida G.M., and Kolodner R.D. A novel mutation avoidance mechanism dependent on S. cerevisiae RAD27 is distinct from DNA mismatch repair. Cell 88 (1997) 253-263
28. Kokoska R.J., Stefanovic L., Tran H.T., Resnick M.A., Gordenin D.A., and Petes T.D. Destabilization of yeast micro- and minisatellite DNA sequences by mutations affecting a nuclease involved in Okazaki fragment processing (rad27) and DNA polymerase delta (pol3-t). Mol Cell Biol 18 (1998) 2779-2788
29. Callahan J.L., Andrews K.J., Zakian V.A., and Freudenreich C.H. Mutations in yeast replication proteins that increase CAG/CTG expansions also increase repeat fragility. Mol Cell Biol 23 (2003) 7849-7860
30. Yang J., and Freudenreich C.H. Haploinsufficiency of yeast FEN1 causes instability of expanded CAG/CTG tracts in a length-dependent manner. Gene 393 (2007) 110-115
31. Wu X., Wilson T.E., and Lieber M.R. A role for FEN-1 in nonhomologous DNA end joining: the order of strand annealing and nucleolytic processing events. Proc Natl Acad Sci U S A 96 (1999) 1303-1308
32. Ejchart A., and Putrament A. Mitochondrial mutagenesis in Saccharomyces cerevisiae. I. Ultraviolet radiation. Mutat Res 60 (1979) 173-180
33. Greene A.L., Snipe J.R., Gordenin D.A., and Resnick M.A. Functional analysis of human FEN1 in Saccharomyces cerevisiae and its role in genome stability. Hum Mol Genet 8 (1999) 2263-2273
34. Xie Y., Liu Y., Argueso J.L., Henricksen L.A., Kao H.I., Bambara R.A., and Alani E. Identification of rad27 mutations that confer differential defects in mutation avoidance, repeat tract instability, and flap cleavage. Mol Cell Biol 21 (2001) 4889-4899
35. Sor F., and Fukuhara H. Identification of two erythromycin resistance mutations in the mitochondrial gene coding for the large ribosomal RNA in yeast. Nucleic Acids Res 10 (1982) 6571-6577
36. Sor F., and Fukuhara H. Erythromycin and spiramycin resistance mutations of yeast mitochondria: nature of the rib2 locus in the large ribosomal RNA gene. Nucleic Acids Res 12 (1984) 8313-8318
37. Cui Z., and Mason T.L. A single nucleotide substitution at the rib2 locus of the yeast mitochondrial gene for 21S rRNA confers resistance to erythromycin and cold-sensitive ribosome assembly. Curr Genet 16 (1989) 273-279
38. Vanderstraeten S., Van den Brule S., Hu J., and Foury F. The role of 3′-5′ exonucleolytic proofreading and mismatch repair in yeast mitochondrial DNA error avoidance. J Biol Chem 273 (1998) 23690-23697
39. Mookerjee S.A., Lyon H.D., and Sia E.A. Analysis of the functional domains of the mismatch repair homologue Msh1p and its role in mitochondrial genome maintenance. Curr Genet 47 (2005) 84-99
40. Huh W.K., Falvo J.V., Gerke L.C., Carroll A.S., Howson R.W., Weissman J.S., and O'Shea E.K. Global analysis of protein localization in budding yeast. Nature 425 (2003) 686-691
41. Lahaye A., Stahl H., Thines-Sempoux D., and Foury F. PIF1: a DNA helicase in yeast mitochondria. EMBO J 10 (1991) 997-1007
42. Zhou J., Monson E.K., Teng S.C., Schulz V.P., and Zakian V.A. Pif1p helicase, a catalytic inhibitor of telomerase in yeast. Science 289 (2000) 771-774
43. Shulga N., Roberts P., Gu Z., Spitz L., Tabb M.M., Nomura M., and Goldfarb D.S. In vivo nuclear transport kinetics in Saccharomyces cerevisiae: a role for heat shock protein 70 during targeting and translocation. J Cell Biol 135 (1996) 329-339
44. Newlon C.S., and Fangman W.L. Mitochondrial DNA synthesis in cell cycle mutants of Saccharomyces cerevisiae. Cell 5 (1975) 423-428
45. Kai Y., Takamatsu C., Tokuda K., Okamoto M., Irita K., and Takahashi S. Rapid and random turnover of mitochondrial DNA in rat hepatocytes of primary culture. Mitochondrion 6 (2006) 299-304
46. Schweitzer J.K., and Livingston D.M. Expansions of CAG repeat tracts are frequent in a yeast mutant defective in Okazaki fragment maturation. Hum Mol Genet 7 (1998) 69-74
47. Nakabeppu Y. Regulation of intracellular localization of human MTH1, OGG1, and MYH proteins for repair of oxidative DNA damage. Prog Nucleic Acid Res Mol Biol 68 (2001) 75-94
48. Nilsen H., Otterlei M., Haug T., Solum K., Nagelhus T.A., Skorpen F., and Krokan H.E. Nuclear and mitochondrial uracil-DNA glycosylases are generated by alternative splicing and transcription from different positions in the UNG gene. Nucleic Acids Res 25 (1997) 750-755
49. Otterlei M., Haug T., Nagelhus T.A., Slupphaug G., Lindmo T., and Krokan H.E. Nuclear and mitochondrial splice forms of human uracil-DNA glycosylase contain a complex nuclear localisation signal and a strong classical mitochondrial localisation signal, respectively. Nucleic Acids Res 26 (1998) 4611-4617
50. Slupphaug G., Markussen F.H., Olsen L.C., Aasland R., Aarsaether N., Bakke O., Krokan H.E., and Helland D.E. Nuclear and mitochondrial forms of human uracil-DNA glycosylase are encoded by the same gene. Nucleic Acids Res 21 (1993) 2579-2584
51. Chatterjee A., and Singh K.K. Uracil-DNA glycosylase-deficient yeast exhibit a mitochondrial mutator phenotype. Nucleic Acids Res 29 (2001) 4935-4940
52. Singh K.K., Sigala B., Sikder H.A., and Schwimmer C. Inactivation of Saccharomyces cerevisiae OGG1 DNA repair gene leads to an increased frequency of mitochondrial mutants. Nucleic Acids Res 29 (2001) 1381-1388
53. You H.J., Swanson R.L., Harrington C., Corbett A.H., Jinks-Robertson S., Senturker S., Wallace S.S., Boiteux S., Dizdaroglu M., and Doetsch P.W. Saccharomyces cerevisiae Ntg1p and Ntg2p: broad specificity N-glycosylases for the repair of oxidative DNA damage in the nucleus and mitochondria. Biochemistry 38 (1999) 11298-11306
54. Steele D.F., Butler C.A., and Fox T.D. Expression of a recoded nuclear gene inserted into yeast mitochondrial DNA is limited by mRNA-specific translational activation. Proc Natl Acad Sci U S A 93 (1996) 5253-5257
55. Methods in Yeast Genetics (1998), Cold Spring harbor Laboratory Press, Cold Spring Harbor
56. Sheff M.A., and Thorn K.S. Optimized cassettes for fluorescent protein tagging in Saccharomyces cerevisiae. Yeast 21 (2004) 661-670
57. Fox T.D., Folley L.S., Mulero J.J., McMullin T.W., Thorsness P.E., Hedin L.O., and Costanzo M.C. Analysis and manipulation of yeast mitochondrial genes. In: Guthrie C., and Fink G.R. (Eds). Methods in Enzymology (1991), Academic Press, Inc., San Diego 149-165
58. Phadnis N., and Sia E.A. Role of the putative structural protein sed1p in mitochondrial genome maintenance. J Mol Biol 342 (2004) 1115-1129
59. Sia E.A., Butler C.A., Dominska M., Greenwell P., Fox T.D., and Petes T.D. Analysis of microsatellite mutations in the mitochondrial DNA of Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 97 (2000) 250-255
60. Lea D.E., and Coulson C.A. The distribution of the number of mutants in bacterial populations. J Genet 49 (1949) 264-284
61. Phadnis N., Mehta R., Meednu N., and Sia E.A. Ntg1p, the base excision repair protein, generates mutagenic intermediates in yeast mitochondrial DNA. DNA Repair 5 (2006) 829-839
62. Ausubel F.M., Brent R., Kingston R.E., Moore D.D., Seidman J.G., Smith J.A., and Struhl K. Current Protocols in Molecular Biology (1994), Wiley, New York
63. Meisinger C., Sommer T., and Pfanner N. Purification of Saccharomyces cerevisiae mitochondria devoid of microsomal and cytosolic contaminations. Anal Biochem 287 (2000) 339-342
64. He S., and Fox T.D. Membrane translocation of mitochondrially coded Cox2p: distinct requirements for export of N and C termini and dependence on the conserved protein Oxa1p. Mol Biol Cell 8 (1997) 1449-1460
65. Rehncrona S., Mela L., and Siesjo B.K. Recovery of brain mitochondrial function in the rat after complete and incomplete cerebral ischemia. Stroke 10 (1979) 437-446
66. Pallotti F., and Lenaz G. Isolation and subfractionation of mitochondria from animal cells and tissue culture lines. In: Pon L.A., and Schon E.A. (Eds). Methods in Cell Biology (2001), Academic Press, San Diego
67. m reveals lack of downstream reinitiation. Mol Gen Genet 262 (2000) 1036-1046
68. Mookerjee S.A., and Sia E.A. Overlapping contributions of Msh1p and putative recombination proteins Cce1p, Din7p, and Mhr1p in large-scale recombination and genome sorting events in the mitochondrial genome of Saccharomyces cerevisiae. Mutat Res 595 (2006) 91-106