MLH1 mutations differentially affect meiotic functions in Saccharomyces cerevisiae

Genetics

Volumn 163, Issue 2, 2003, Pages 515-526

  Hoffmann, Eva R ^a,b   Shcherbakova, Polina V ^c   Kunkel, Thomas A ^c   Borts, Rhona H ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF LEICESTER   (United Kingdom)

^c NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; DNA; HETERODUPLEX; PROTEIN MLH1;

ARTICLE; BINDING AFFINITY; CHROMOSOME SEGREGATION; COLORECTAL CANCER; CONTROLLED STUDY; CROSSING OVER; DNA BINDING; FUNGAL GENE; GAMETE; GAMETOGENESIS; GENE MUTATION; HYDROLYSIS; MEASUREMENT; MEIOSIS; MISMATCH REPAIR; MISSENSE MUTATION; MITOSIS; MUTATION RATE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; PROTEIN INTERACTION; SACCHAROMYCES CEREVISIAE; YEAST;

AMINO ACID SEQUENCE; ANEUPLOIDY; CROSSING OVER, GENETIC; DNA REPAIR; FUNGAL PROTEINS; MEIOSIS; MOLECULAR SEQUENCE DATA; NONDISJUNCTION, GENETIC; SACCHAROMYCES CEREVISIAE; SEQUENCE ALIGNMENT;

SACCHAROMYCES; SACCHAROMYCES CEREVISIAE;

EID: 0037295481     PISSN: 00166731     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (60)

1. ABDULLAH, M. F. F., 2002 Transcription factors and mismatch repair proteins in meiotic recombination. Ph.D. Thesis, University of Oxford, Oxford.
2. ABDULLAH, M. F. F., and R. H. BORTS, 2001 Meiotic recombination frequencies are affected by nutritional states in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 98: 14524-14529.
3. ALANI, A., R. A. REENAN and R. D. KOLODNER, 1994 Interaction between mismatch repair and genetic recombination in Saccharomyces cerevisiae. Genetics 137: 19-39.
4. AMIN, N. S., M. N. NGUYEN, S. OH and R. D. KOLODNER, 2001 exol-Dependent mutator mutations: model system for studying functional interactions in mismatch repair. Mol. Cell. Biol. 21: 5142- 5155.
5. ANDERSON, L. K., A. REEVES, L. M. WEBB and T. ASHLEY, 1999 Distribution of crossing over on mouse synaptonemal complexes using immunofluorescent localization of MLH1 protein. Genetics 151: 1569-1579.
6. ARGUESO, J. L., S. SARIN, A. KIJAS and E. ALANI, 2002 Analysis of conditional mutations in the Saccharomyces cerevisiae MLH1 gene in mismatch repair and crossing over. Genetics 160: 909-921.
7. ARGUESO, J. L., A. W. KIJAS, S. SARIN, J. HECK, M. WAASE et al., 2003 Systematic mutagenesis of the Saccharomyces cerevisiae MLH1 gene reveals distinct roles for Mlh1p in meiotic crossing over and in vegetative and meiotic mismatch repair. Mol. Cell. Biol. 23: 873-886.
8. BAKER, S. M., A. W. PLUG, T. A. PROLLA, C. E. BRONNER, A. C. HARRIS et al., 1996 Involvement of mouse Mlh1 in DNA mismatch repair and meiotic crossing over. Nat. Genet. 13: 336-342.
9. BAN, C., and W. YANG, 1998a Crystal structure and ATPase activity of MutL: implications for DNA repair and mutagenesis. Cell 95: 541-552.
10. BAN, C., and W. YANG, 1998b Structural basis for MutH activation in E. coli mismatch repair and relationship of MutH to restriction endonucleases. EMBO J. 17: 1526-1534.
11. BAN, C., M. JUNOP and W. YANG, 1999 Transformation of MutL by ATP binding and hydrolysis: a switch in DNA mismatch repair. Cell 97: 85-97.
12. BARLOW, A. L., and M. A. HULTEN, 1998 Crossing over analysis at pachytene in man. Eur. J. Hum. Genet. 6: 350-358.
13. BORTS, R. H., and J. E. HABER, 1989 Length and distribution of meiotic gene conversion tracts and crossovers in Saccharomyces cerevisiae. Genetics 123: 69-80.
14. BORTS, R. H., S. R. CHAMBERS and M. F. F. ABDULLAH, 2000 The many faces of mismatch repair in meiosis. Mutat. Res. 451: 129-150.
15. CARPENTER, A. T. C., 1994 Chiasma function. Cell 77: 959-962.
16. COHEN, P. E., and J. W. POLLARD, 2001 Regulation of meiotic recombination and prophase I progression in mammals. Bioessays 23: 996-1009.
17. EDELMANN, W., P. E. COHEN, M. KANE, K. LAU, B. MORROW et al., 1996 Meiotic pachytene arrest in MLH1-deficient mice. Cell 85: 1125-1134.
18. EDELMANN, W., P. E. COHEN, B. KNEITZ, N. WINAND, M. LIA et al., 1999 Mammalian MutS homologue 5 is required for chromosome pairing in meiosis. Nat. Genet. 21: 123-127.
19. ERDENIZ, N., U. H. MORTENSEN and R. ROTHSTEIN, 1997 Cloning-free PCR-based allele replacement methods. Genome Res. 7: 1174-1185.
20. GILBERTSON, L. A., and F. W. STAHL, 1996 A test of the double-strand break model for meiotic recombination in Saccharomyces cerevisiae. Genetics 144: 27-41.
21. GUARNE, A., M. S. JUNOP and W. YANG, 2001 Structure and function of the N-terminal 40 kDa fragment of human PMS2: a monomeric GHL ATPase. EMBO J. 20: 5521-5531.
22. HALL, M. C., J. R. JORDAN and S. W. MATSON, 1998 Evidence for a physical interaction between the Escherichia coli methyl-directed mismatch repair proteins MutL and UvrD. EMBO J. 17: 1535-1541.
23. HALL, M. C., P. V. SHCHERBAKOVA and T. A. KUNKEL, 2002 Differential ATP binding and intrinsic ATP hydrolysis by amino terminal domains of the yeast Mlh1 and Pms1 proteins. J. Biol. Chem. 277: 3673-3679.
24. HARFE, B. D., and S. JINKS-ROBERTSON, 2000 DNA mismatch repair and genetic instability. Annu. Rev. Genet. 34: 359-399.
25. HOLLINGSWORTH, N. M., L. PONTE, and C. HALSEY, 1995 MSH5, a novel MutS homolog, facilitates meiotic reciprocal recombination between homologs in Saccharomyces cerevisiae but not mismatch repair. Genes Dev. 9: 1728-1739.
26. HUNTER, N., and R. H. BORTS, 1997 Mlh1p is unique among mismatch repair proteins in its ability to promote crossing-over during meiosis. Genes Dev. 11: 1573-1582.
27. JAGER, A. C., M. RASMUSSEN, H. C. BISGAARD, K. K. SINGH, F. C. NIELSEN et al., 2001 HNPCC mutations in the human DNA mismatch repair gene hMLH1 influence assembly of hMutLa1pha and hMLH1-hEXO1 complexes. Oncogene 20: 3590-3595.
28. KHAZANEHDARI, K., and R. H. BORTS, 2000 EXO1 and MSH4 differentially affect crossing-over and segregation. Chromosoma 109:94-102.
29. KIRKPATRICK, D. T., R. J. FERGUSON, T. D. PETES and L. S. SYMINGTON, 2000 Decreased meiotic intergenic recombination and increased meiosis I nondisjunction in exo1 mutants of Saccharomyces cerevisiae. Genetics 156: 1549-1557.
30. KNEITZ, B., P. E. COHEN, E. AVDIEVICH, L. ZHU, M. F. KANE et al., 2000 MutS homolog 4 localization to meiotic chromosomes is required for chromosome pairing during meiosis in male and female mice. Genes Dev. 14: 1085-1097.
31. KONDO, E., A. HORH and S. FUKUSHIGE, 2001 The interacting domains of three MutL heterodimers in man: hMLH1 interacts with 36 homologous amino acid residues within hMLH3, hPMS1 and hPMS2. Nucleic Acids Res. 29: 1695-1702.
32. LANGLAND, G., J. KORDICH, J. CREANEY, K. H. GOSS, K. LILLARD-WETHERELL et al., 2001 The Bloom's syndrome protein (BLM) interacts with MLH1 but is not required for DNA mismatch repair. J. Biol. Chem. 276: 30031-30035.
33. LIPKIN, S. M., P. B. MOENS, V. WANG, M. LENZI, D. SHANMUGARAJAH et al., 2002 Meiotic arrest and aneuploidy in MLH3-deficient mice. Nat. Genet. 31: 385-390.
34. NOVAK, J. E., P. B. ROSS-MACDONALD and G. S. ROEDER, 2001 The budding yeast Msh4 protein functions in chromosome synapsis and the regulation of crossover distribution. Genetics 158: 1013-1025.
35. PANG, Q. S., T. A. PROLLA and R. M. LISKAY, 1997 Functional domains of the Saccharomyces cerevisiae Mlh1p and Pms1p DNA mismatch repair proteins and their relevance to human hereditary nonpolyposis colorectal cancer-associated mutations. Mol. Cell. Biol. 17: 4465-4473.
36. PAPAZIAN, H. P., 1952 The analysis of tetrad data. Genetics 37: 175-188.
37. PEDRAZZI, G., C. PERRERA, H. BLASER, P. KUSTER, G. MARRA et al., 2001 Direct association of Bloom's syndrome gene product with the human mismatch repair protein MLH1. Nucleic Acids Res. 29: 4378-4386.
38. PELTOMAKI, P., 2001 DNA mismatch repair and cancer. Mutat. Res. 488: 77-85.
39. PERKINS, D. D., 1949 Biochemical mutants in the smut fungus Ustilago maydis. Genetics 34: 607-626.
40. PROLLA, T. A., D.-M. CHRISTIE and R. M. LISKAY, 1994 Dual requirement in yeast DNA mismatch repair for MLH1 and PMS1, two homologs of the bacterial mutLgene. Mol. Cell. Biol. 14:407-415.
41. REENAN, R. A., and R. D. KOLODNER, 1992 Characterization of insertion mutations in the Saccharomyces cerevisiae MSH1 and MSH2 genes: evidence for separate mitochondrial and nuclear functions. Genetics 132: 975-985.
42. ROSS-MACDONALD, P., and G. S. ROEDER, 1994 Mutation of a meiosis-specific MutS homolog decreases crossing-over but not mismatch correction. Cell 79: 1069-1080.
43. SANTUCCI-DARMANIN, S., D. WALPITA, F. LESPINASSE, C. DESNUELLE, T. ASHLEY et al., 2000 MSH4 acts in conjunction with MLH1 during mammalian meiosis. FASEB J. 14: 1539-1547.
44. SANTUCCI-DARMANIN, S., S. NEYTON, F. LESPINASSE, A. SAUNIERES, P. GAUDRAY et al., 2002 The DNA mismatch-repair MLH3 protein interacts with MSH4 in meiotic cells, supporting a role for this MutL homolog in mammalian meiotic recombination. Hum. Mol. Genet. 11: 1697-1706.
45. SHCHERBAKOVA, P. V., and T. A. KUNKEL, 1999 Mutator phenotypes conferred by MLH1 overexpression and by heterozygosity for mlh1 mutations. Mol. Cell. Biol. 19: 3177-3183.
46. SOKAL, R. R., and F.J. ROHLF, 1969 Biometry. W. H. Freeman, San Francisco.
47. SOKOLSKY, T., and E. ALANI, 2000 EXO1 and MSH6 are high-copy suppressors of conditional mutations in the MSH2 mismatch repair gene of Saccharomyces cerevisiae. Genetics 155: 589-599.
48. SPAMPINATO, C., and P. MODRICH, 2000 The MutL ATPase is required for mismatch repair. J. Biol. Chem. 275: 9863-9869.
49. STAHL, F. W., and R. LANDE, 1995 Estimating interference and linkage map distance from two-factor tetrad data. Genetics 139: 1449-1454.
50. TISHKOFF, D. X., A. L. BOERGER, P. BERTRAND, N. FILOSI, G. M. GAIDA et al., 1997 Identification and characterization of Saccharomyces cerevisiae EXO1 a gene encoding an exonuclease that interacts with MSH2. Proc. Natl. Acad. Sci. USA 94: 7487-7492.
51. TRAN, H. T., J. D. KEEN, M. KRICKER, M. A. RESNICK and D. A. GORDENIN, 1997 Hypermutability of homonucleotide runs in mismatch repair and DNA polymerase proofreading yeast mutants. Mol. Cell. Biol. 17: 2859-2865.
52. TRAN, P. T., and R. M. LISKAY, 2000 Functional studies on the candidate ATPase domains of Saccharomyces cerevisiae MutLα. Mol. Cell. Biol. 20: 6390-6398.
53. TRAN, P. T., J. A. SIMON and R. M. LISKAY, 2001 Interactions of Exo1p with components of MutLα in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 98: 9760-9765.
54. WACH, A., A. BRACHAT, R. POHLMANN and P. PHILIPPSEN, 1994 New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae. Yeast 10: 1793-1808.
55. WANG, T., and W. KUNG, 2002 Supercomplex formation between Mlh1-Mlh3 and Sgs1-Top3 heterocomplexes in meiotic yeast cells. Biochem. Biophys. Res. Commun. 296: 949.
56. WANG, T.-F., N. KLECKNER and N. HUNTER, 1999 Functional specificity of MutL homologs in yeast: evidence for three Mllt1-based heterocomplexes with distinct roles during meiosis in recombination and mismatch correction. Proc. Natl. Acad. Sci. USA 96: 13914-13919.
57. WILLIAMSON, M. S., J. C. GAME and S. FOGEL., 1985 Meiotic gene conversion mutants in Saccharomyces cerevisiae. I. Isolation and characterization of pms1-1 and pms1-2. Genetics 110: 609-646.
58. WU, Y., M. J. BERENDS, J. G. POST, R. G. MENSINK, E. VERLIND et al., 2001 Germline mutations of EXO1 gene in patients with hereditary nonpolyposis colorectal cancer (HNPCC) and atypical HNPCC forms. Gastroenterology 120: 1580-1587.
59. YUAN, Z. Q., B. GOTTLIEB, L. K. BEITEL, N. WONG, P. H. GORDON et al., 2002 Polymorphisms and HNPCC: PMS2-MLHI protein interactions diminished by single nucleotide polymorphisms. Hum. Mutat. 19: 108-113.
60. ZALEVSKY, J., A. J. MACQUEEN, J. B. DUFFY, K. J. KEMPHUES and A. M. VILLENEUVE, 1999 Crossing over during Caenorhabditis elegans meiosis requires a conserved MutS-based pathway that is partially dispensable in budding yeast. Genetics 153: 1271-1283.