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

Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis

Volumn 595, Issue 1-2, 2006, Pages 91-106

  Mookerjee, Shona A ^a   Sia, Elaine A ^a  

^a UNIVERSITY OF ROCHESTER   (United States)

Author keywords

CCE1; DIN7; Heteroplasmy; MHR1; Mitochondria; MSH1

Indexed keywords

MITOCHONDRIAL DNA;

ARTICLE; CONTROLLED STUDY; DNA TRANSFER; GENE FUNCTION; GENE MUTATION; GENOMICS; MISMATCH REPAIR; MITOCHONDRION; NONHUMAN; PHENOTYPE; PREDICTION; PRIORITY JOURNAL; REPORTER GENE; SACCHAROMYCES CEREVISIAE; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; CELL RESPIRATION; DIMERIZATION; DIPLOIDY; DNA, FUNGAL; DNA, MITOCHONDRIAL; EXODEOXYRIBONUCLEASES; FUNGAL PROTEINS; GENES, FUNGAL; GENOME, FUNGAL; GENOMIC INSTABILITY; HOLLIDAY JUNCTION RESOLVASES; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; POINT MUTATION; PROTEIN TRANSPORT; RECOMBINATION, GENETIC; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE DELETION; TRANSCRIPTION FACTORS;

SACCHAROMYCES CEREVISIAE;

EID: 33244497588     PISSN: 00275107     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mrfmmm.2005.10.006     Document Type: Article

References (70)

1. B. Dujon Mitochondrial genetics and functions J.N. Strathern E.W. Jones J.R. Broach Molecular Biology of the Yeast Saccharomyces: Life Cycle and Inheritance 1981 Cold Spring Harbor Laboratory Press Cold Spring Harbor, NY 505 635
2. D.B. Stern, and J.D. Palmer Recombination sequences in plant mitochondrial genomes: diversity and homologies to known mitochondrial genes Nucl. Acids Res. 12 1984 6141 6157
3. C. Fauron, M. Casper, Y. Gao, and B. Moore The maize mitochondrial genome: dynamic, yet functional Trends Genet. 11 1995 228 235
4. C.J. Birky Transmission genetics of mitochondria and chloroplasts Annu. Rev. Genet. 12 1978 471 512
5. B. Thyagarajan, R.A. Padua, and C. Campbell Mammalian mitochondria possess homologous DNA recombination activity J. Biol. Chem. 271 1996 27536 27543
6. M. D'Aurelio, C. Gajewski, M. Lin, W. Mauck, L. Shao, G. Lenaz, C.T. Moraes, and G. Manfredi Heterologous mitochondrial DNA recombination in human cells Human Mol. Genet. 13 2004 3171 3179
7. O. Kajander, P.J. Karhunen, I.J. Holt, and H.T. Jacobs Prominent mitochondrial DNA recombination intermediates in human heart muscle EMBO Rep. 2 2001 1007 1012
8. Y. Kraytsberg, M. Schwartz, T.A. Brown, K. Ebralidse, W.S. Kunz, D.A. Clayton, J. Vissing, and K. Khrapko Recombination of human mitochondrial DNA Science 304 2004 981
9. G. Zsurka, Y. Kraytsberg, T. Kudina, C. Kornblum, C. Elger, K. Khrapko, and W.S. Kunz Recombination of mitochondrial DNA in skeletal muscle of individuals with multiple mitochondrial DNA heteroplasmy Nat. Genet. 37 2005 873 877
10. P. Awadalla, A. Eyre-Walker, and J.M. Smith Linkage disequilibrium and recombination in hominid mitochondrial DNA Science 286 1999 2524 2525
11. A.D. Tsaousis, D.P. Martin, E.D. Ladoukakis, D. Posada, and E. Zouros Widespread recombination in published animal mtDNA sequences Mol. Biol. Evol. 22 2005 925 933
12. N.O. Bianchi, M.S. Bianchi, and S.M. Richard Mitochondrial genome instability in human cancers Mutat. Res. 488 2001 9 23
13. A. Trifunovic, A. Wredenberg, M. Falkenberg, J.N. Spelbrink, A.T. Rovio, C.E. Bruder, M. Bohlooly-Y, S. Gedlof, A. Oldfors, R. Wibom, J. Tornell, H.T. Jacobs, and N.-G. Larsson Premature ageing in mice expressing defective mitochondrial DNA polymerase Nature 429 2004 417 421
14. M. Zeviani, A. Spinazzola, and V. Carelli Nuclear genes in mitochondrial disorders Curr. Opin. Genet. Dev. 13 2003 262 270
15. F. Odoardi, M. Rana, A. Broccolini, M. Mirabella, A. Modoni, A. D'Amico, M. Papacci, P. Tonali, S. Servidei, and G. Silvestri Pathogenic role of mtDNA duplications in mitochondrial diseases associated with mtDNA deletions Am. J. Med. Genet. 118A 2003 247 254
16. O. Kajander, P.J. Karhunen, and H.T. Jacobs The relationship between somatic mtDNA rearrangements, human heart disease and aging Human Mol. Genet. 11 2002 317 324
17. B.S. Mandavilli, J.H. Santos, and B. Van Houten Mitochondrial DNA repair and aging Mutat. Res. 509 2002 127 151
18. E.A. Shoubridge Nuclear genetic defects of oxidative phosphorylation Human Mol. Genet. 10 2001 2277 2284
19. S.G. Zweifel, and W.L. Fangman A nuclear mutation reversing a biased transmission of yeast mitochondrial DNA Genetics 128 1991 241 249
20. S. Kleff, B. Kemper, and R. Sternglanz Identification and characterization of yeast mutants and the gene for a cruciform cutting endonuclease EMBO J. 11 1992 699 704
21. U.R. Ezekiel, and H.P. Zassenhaus Localization of a cruciform cutting endonuclease to yeast mitochondria Mol. Gen. Genet. 240 1993 414 418
22. D. Lockshon, S.G. Zweifel, L.L. Freeman-Cook, H.E. Lorimer, B.J. Brewer, and W.L. Fangman A role for recombination junctions in the segregation of mitochondrial DNA in yeast Cell 81 1995 947 955
23. P. Mieczkowski, W. Dajweski, A. Podlaska, A. Skonecza, Z. Ciesla, and E. Sledziewska-Gojska Characterization of a novel DNA damage-inducible gene of Saccharomyces cerevisiae, DIN7, which is a structural homolog of the RAD2 and RAD27 DNA repair genes Mol. Genet. Genom. 253 1997 655 665
24. M.U. Fikus, P.A. Mieczkowski, P. Koprowski, J. Rytka, E. Sledziewska-Gonjska, and Z. Ciesla The product of the DNA damage-inducible gene of Saccharomyces cerevisiae, DIN7, specifically functions in mitochondria Genetics 154 2000 73 81
25. P. Koprowski, M.U. Fikus, P. Dzierzbicki, P. Mieczkowski, J. Lazowska, and Z. Ciesla Enhanced expression of the DNA damage-inducible gene DIN7 results in increased mutagenesis of mitochondrial DNA in Saccharomyces cerevisiae Mol. Gen. Genom. 269 2003 632 639
26. F. Ling, F. Makishima, N. Morishima, and T. Shibata A nuclear mutation defective in mitochondrial recombination in yeast EMBO J. 14 1995 4090 4101
27. F. Ling, and T. Shibata Recombination-dependent mtDNA partitioning: in vivo role of Mhr1p to promote pairing of homologous DNA EMBO J. 21 2002 4730 4740
28. F. Ling, H. Morioka, E. Ohtsuka, and T. Shibata A role for MHR1, a gene required for mitochondrial genetic recombination, in the repair of damage spontaneously introduced in yeast mtDNA Nucl. Acids Res. 15 2000 4956 4963
29. R.M. Spell, and S. Jinks-Robertson Role of mismatch repair in the fidelity of RAD51- and RAD59-dependent recombination in Saccharomyces cerevisiae Genetics 165 2003 3 12
30. E. Evans, and E. Alani Roles for mismatch repair factors in regulating genetic recombination Mol. Cell. Biol. 20 2000 7839 7844
31. N. Sugawara, T. Goldfarb, B. Studamire, E.A. Alani, and J.E. Haber Heteroduplex rejection during single-strand annealing requires Sgs1 helicase and mismatch repair proteins Msh2 and Msh6 but not Pms1 Proc. Natl. Acad. Sci. 101 2004 9315 9320
32. A. Nicholson, M. Hendrix, S. Jinks-Robertson, and G.F. Crouse Regulation of mitotic homeologous recombination in yeast: functions of mismatch repair and nucleotide excision repair genes Genetics 154 2000 133 146
33. M.C. Earley, and G.F. Crouse The role of mismatch repair in the prevention of base pair mutations in Saccharomyces cerevisiae Proc. Natl. Acad. Sci. 95 1998 15487 15941
34. M. Vulic, R.E. Lenski, and M. Radman Mutation, recombination, and incipient speciation of bacteria in the laboratory Proc. Natl. Acad. Sci. 96 1999 7348 7351
35. E.L. Ivanov, N. Sugawara, J. Fishman-Lobell, and J.E. Haber Genetic requirements for the single-strand annealing pathway of double-strand break repair in Saccharomyces cerevisiae Genetics 142 1996 693 704
36. N. Sugawara, G. Ira, and J.E. Haber DNA length dependence of the single-strand annealing pathway and the role of Saccharomyces cerevisiae RAD59 in double-strand break repair Mol. Cell. Biol. 20 2000 5300 5309
37. N. Sugawara, F. Paques, M. Colaiacovo, and J.M. Haber Role of Saccharomyces cerevisiae Msh2 and Msh3 repair proteins in double-strand break-induced recombination Proc. Natl. Acad. Sci. 94 1997 9214 9219
38. R.A. Reenan, and R.D. Kolodner Isolation and characterization of two Saccharomyces cerevisiae genes encoding homologs of the bacterial HexA and MutS mismatch repair proteins Genetics 132 1992 963 973
39. S.A. Mookerjee, H.D. Lyon, and E.A. Sia 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. R.A.G. Reenan, and R.D. Kolodner Characterization of insertion mutations in the Saccharomyces cerevisiae MSH1 and MSH2 genes: evidence for separate mitochondrial and nuclear functions Genetics 132 1992 975 985
41. E.A. Sia, C.A. Butler, M. Dominska, P. Greenwell, T.D. Fox, and T.D. Petes Analysis of microsatellite mutations in the mitochondrial DNA of Saccharomyces cerevisiae Proc. Natl. Acad. Sci. 97 2000 250 255
42. D.F. Steele, C.A. Butler, and T.D. Fox Expression of a recoded nuclear gene inserted into yeast mitochondrial DNA is limited by mRNA-specific translational activation Genetics 93 1996 5253 5257
43. D.Y. Wu, L. Ugozzoli, B.K. Pak, J. Qian, and R.B. Wallace The effect of temperature and oligonucleotide primer length on the specificity and efficiency of amplification by the polymerase chain reaction DNA Cell Biol. 176 1991 233 238
44. N. Phadnis, and E.A. Sia Role of the putative structural protein Sed1p in mitochondrial genome maintenance J. Mol. Biol. 342 2004 1115 1129
45. P.E. Thorsness, and T.D. Fox Nuclear mutations in Saccharomyces cerevisiae that affect the escape of DNA from mitochondria to the nucleus Genetics 134 1993 21 28
46. T.D. Fox, L.S. Folley, J.J. Mulero, T.W. McMullin, P.E. Thorsness, L.O. Hedin, and M.C. Costanzo Analysis and manipulation of yeast mitochondrial genes C. Guthrie G.R. Fink Guide to Yeast Genetics and Molecular Biology 1991 Academic Press San Diego, CA 149 165
47. D.E. Lea, and C.A. Coulson The distribution of the number of mutants in bacterial populations J. Genet. 49 1949 264 285
48. N. Phadnis, R.A. Sia, E.A. Sia, Analysis of repeat-mediated deletions in the mitochondrial genome of Saccharomyces cerevisiae Genetics (2005), in press.
49. J. Bowers, T. Sokolsky, T. Quach, and E. Alani A mutation in the MSH6 subunit of the Saccharomyces cerevisiae MSH2-MSH6 complex disrupts mismatch recognition J. Biol. Chem. 274 1999 16115 16125
50. P. Dufner, G. Marra, M. Raschle, and J. Jiricny Mismatch recognition and DNA-dependent stimulation of the ATPase activity of hMutSalpha is abolished by a single mutation in the hMSH6 subunit J. Biol. Chem. 275 2000 36550 36555
51. M.J. Schofield, F.J. Brownewell, S. Nayak, C. Du, E.T. Kool, and P. Hsieh The Phe-X-Glu DNA binding motif of MutS J. Biol. Chem. 276 2001 45505 45508
52. A. Yamamoto, M.J. Schofield, I. Biswas, and P. Hsieh Requirement for Phe36 for DNA binding and mismatch repair by Escherichia coli MutS protein Nucl. Acids Res. 28 2000 3564 3569
53. K. Drotschmann, W. Yang, F.E. Brownewell, E.T. Kool, and T.A. Kunkel Asymmetric recognition of DNA local distortion: structure-based functional studies of eukaryotic Msh2-Msh6 J. Biol. Chem. 276 2001 46225 46229
54. E. Alani, T. Sokolsky, B. Studamire, J.J. Miret, and R.S. Lahue Genetic and biochemical analysis of Msh2p-Msh6p: role of ATP hydrolysis and Msh2p-Msh6p subunit interactions in mismatch base pair recognition Mol. Cell. Biol. 17 1997 2436 2447
55. B. Studamire, T. Quach, and E. Alani Saccharomyces cerevisiae Msh2p and Msh6p ATPase activities are both required during mismatch repair Mol. Cell. Biol. 18 1998 7590 7601
56. B. Studamire, G. Price, N. Sugawara, J.E. Haber, and E.A. Alani Separation-of-function mutations in Saccharomyces cerevisiae that confer mismatch repair defects but do not affect nonhomologous-tail removal during recombination Mol. Cell. Biol. 19 1999 7558 7567
57. A.W. Kijas, B. Studamire, and E.A. Alani Msh2 separation of function mutations confer defects in the initiation steps of mismatch repair J. Mol. Biol. 331 2003 128 138
58. Z. Cui, and T.L. Mason 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
59. M. Strand, T.A. Prolla, R.M. Liskay, and T.D. Petes Destabilization of tracts of simple repetitive DNA in yeast by mutations affecting DNA mismatch repair Nature 365 1993 274 276
60. E.A. Sia, R.J. Kokoska, M. Dominska, P. Greenwell, and T.D. Petes Microsatellite instability in yeast: dependence on repeat unit size and DNA mismatch repair genes Mol. Cell. Biol. 17 1997 2851 2858
61. G.T. Marsischky, N. Filosi, M.F. Kane, and R. Kolodner Redundancy of Saccharomyces cerevisiae MSH3 and MSH6 in MSH2-dependent mismatch repair Genes Dev. 10 1996 407 420
62. M.H. Lamers, H.H. Winterwerp, and T.K. Sixma The alternating ATPase domains of MutS control DNA mismatch repair EMBO J. 22 2003 746 756
63. D.M. MacAlpine, K. Okamoto, R.A. Butow, and P.S. Perlman Replication and preferential inheritance of hypersuppressive petite mitochondrial DNA EMBO J. 20 2001 1807 1817
64. S. Meeusen, and J. Nunnari Evidence for a two membrane-spanning autonomous mitochondrial DNA replisome J. Cell Biol. 163 2003 503 510
65. F. Ling, and T. Shibata Mhr1p-dependent concatemeric mitochondrial DNA formation for generating yeast mitochondrial homoplasmic cells Mol. Cell. Biol. 15 2004 310 322
66. J. Nunnari, W.F. Marshall, A. Straight, A.W. Murray, J.W. Sedat, and P. Walter Mitochondrial transmission during mating in Saccharomyces cerevisiae is determined by mitochondrial fusion and fission and the intramitochondrial segregation of mitochondrial DNA Mol. Biol. Cell 8 1997 1233 1242
67. L.T. Haber, and G.C. Walker Altering the conserved nucleotide binding motif in the Salmonella typhimurium MutS mismatch repair protein affects both its ATPase and mismatch binding activities EMBO J. 10 1991 2707 2715
68. N. Chi, and R.D. Kolodner The effect of DNA mismatches on the ATPase activity of MSH1, a protein in yeast mitochondria that recognizes DNA mismatches J. Biol. Chem. 269 1994 29993 29997
69. N. Chi, and R.D. Kolodner Purification and characterization of MSH1, a yeast mitochondrial protein that binds to DNA mismatches J. Biol. Chem. 269 1994 29984 29992
70. R.V. Abdelnoor, R. Yule, A. Elo, A.C. Christensen, G. Meyer-Gauen, and S.A. Mackenzie Substoichiometric shifting in the plant mitochondrial genome is influenced by a gene homologous to MutS Proc. Natl. Acad. Sci. 100 2003 5968 5973