The many faces of mismatch repair in meiosis

Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis

Volumn 451, Issue 1-2, 2000, Pages 129-150

  Borts, Rhona H ^a   Chambers, S R ^a   Abdullah, M F F ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Meiosis; Mismatch repair; Mismatch repair proteins

Indexed keywords

HETERODUPLEX;

CROSSING OVER; DNA RECOMBINATION; DNA REPAIR; DNA REPLICATION; DNA STRUCTURE; GENE CONVERSION; GENETIC SELECTION; GENETIC VARIABILITY; MEIOSIS; MISSENSE MUTATION; MUTATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW;

BASE PAIR MISMATCH; DNA REPAIR; GENE CONVERSION; GERM CELLS; HUMANS; MEIOSIS; NUCLEIC ACID HETERODUPLEXES; RECOMBINATION, GENETIC;

SACCHAROMYCES CEREVISIAE;

EID: 0034733691     PISSN: 00275107     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0027-5107(00)00044-0     Document Type: Review

References (151)

1. Fishel R., Kolodner R.D. Identification of mismatch repair genes and their role in the development of cancer. Curr. Opin. Genet. Dev. 5:1995;382-395.
2. Kolodner R.D. Mismatch repair: mechanisms and relationship to cancer susceptibility. TIBS. 20:1995;397-401.
3. Kolodner R. Biochemistry and genetics of eukaryotic mismatch repair. Genes Dev. 10:1996;1433-1442.
4. Kolodner R.D., Marsischky G.T. Eukaryotic mismatch repair. Curr. Opin. Genet. Dev. 9:1999;89-96.
5. Modrich P., Lahue R. Mismatch repair in replication fidelity, genetic recombination, and cancer biology. Annu. Rev. Biochem. 65:1996;101-133.
6. Crouse G.F. Mismatch repair systems in Saccharomyces cerevisiae. Heokstra M.F., Nickloff J.A. DNA Damage and Repair - Biochemistry, Genetics and Cell Biology. 1998;411-448 Humana Press, Totowa, NJ.
7. Smith K.N., Nicolas A. Recombination at work for meiosis. Curr. Opin. Genet. Dev. 8:1998;200-211.
8. Orr-Weaver T.L., Szostak J.W. Fungal recombination. Microbiol. Rev. 49:1985;33-58.
9. Pâques F., Haber J.E. Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 63:1999;349-404.
10. Jinks-Robertson S. Mutat. Res. 2000;. this issue.
11. Modrich P. DNA mismatch correction. Annu. Rev. Biochem. 56:1987;435-466.
12. Radman M., Wagner R. Mismatch repair in Escherichia coli. Annu. Rev. Genet. 20:1986;523-538.
13. Williamson M.S., Game J.C., Fogel S. Meiotic gene conversion mutants in Saccharomyces cerevisiae: I. Isolation and characterization of pms1-1 and pms1-2. Genetics. 110:1985;609-646.
14. Kramer W., Kramer B., Williamson M.S., Fogel S. Cloning and nucleotide sequence of DNA mismatch repair gene PMS1 from Saccharomyces cerevisiae: homology to prokaryotic MutL and HexB. J. Bacteriol. 171:1989;5339-5346.
15. Kramer B., Kramer W., Williamson M.S., Fogel S. Heteroduplex DNA correction in Saccharomyces cerevisiae is mismatch specific and requires functional PMS genes. Mol. Cell. Biol. 9:1989;4432-4440.
16. Prolla T.A., Pang Q., Alani E., Kolodner R.D., Liskay R.M. MLH1, PMS1 and MSH2 interactions during the initiation of DNA mismatch repair in yeast. Science. 265:1994;1091-1093.
17. Alani A., Reenan R.A., Kolodner R.D. Interaction between mismatch repair and genetic recombination in Saccharomyces cerevisiae. Genetics. 137:1994;19-39.
18. Reenan R.A., Kolodner R.D. Isolation and characterisation of two Saccharomyces cerevisiae genes encoding homologs of the bacterial HexA and MutS mismatch repair proteins. Genetics. 132:1992;963-973.
19. Reenan R.A., Kolodner R.D. Characterisation of insertion mutations in the Saccharomyces cerevisiae MSH1 and MSH2 genes: evidence for separate mitochondrial and nuclear functions. Genetics. 132:1992;975-985.
20. New L., Liu K., Crouse G.F. The yeast gene MSH3 defines a new class of eukaryotic MutS homologues. Mol. Gen. Genet. 239:1993;97-108.
21. Prolla T.A., Christie D.-M., Liskay R.M. Dual requirement in yeast DNA mismatch repair for MLH1 and PMS1, two homologs of the bacterial mutL gene. Mol. Cell. Biol. 14:1994;407-415.
22. Hollingsworth N.M., Ponte L., Halsey C. MSH5, a novel MutS homolog, facilitates meiotic reciprocal recombination between homologs in Saccharomyces cerevisiae but not mismatch repair. Genes Dev. 9:1995;1728-1739.
23. Marsischky G.T., Filosi N., Kane M.F., Kolodner R. Redundancy of Saccharomyces cerevisiae MSH3 and MSH6 in MSH2-dependent mismatch repair. Genes Dev. 10:1996;407-420.
24. Ross-Macdonald P., Roeder G.S. Mutation of a meiosis-specific MutS homolog decreases crossing-over but not mismatch correction. Cell. 79:1994;1069-1080.
25. Fedorova I.V., Gracheva L.M., Kovaltzova S.V., Evstuhina T.A., Alekseev S.Y., Korolev V.G. The yeast HSM3 gene acts in one of the mismatch repair pathways. Genetics. 148:1998;963-973.
26. Chi N.-W., Kolodner R.D. Purification and characterisation of MSH1, a yeast mitochondrial protein that binds to DNA mismatches. J. Biol. Chem. 269:1994;29984-29992.
27. Pochart P., Woltering D., Hollingsworth N.M. Conserved properties between functionally distinct MutS homologs in yeast. J. Biol. Chem. 272:1997;30345-30349.
28. Hunter N., Borts R.H. Mlh1p is unique among mismatch repair proteins in its ability to promote crossing-over during meiosis. Genes Dev. 11:1997;1573-1582.
29. Wang T.-F., Kleckner N., Hunter N. Functional specificity of MutL homologs in yeast: evidence for three Mlh1-based heterocomplexes with distinct roles during meiosis in recombination and mismatch correction. Proc. Natl. Acad. Sci. U.S.A. 96:1999;13914-13919.
30. M.F.F. Abdullah, R.H. Borts, unpublished observations.
31. Flores-Rozas H., Kolodner R.D. The Saccharomyces cerevisiae MLH3 gene functions in MSH3-dependent suppression of frameshift mutations. Proc. Natl. Acad. Sci. U. S. A. 95:1998;12404-12409.
32. Jeyaprakash A., Das Gupta R., Kolodner R. Saccharomyces cerevisiae pms2 mutations are alleles of MLH1, and pms2-2 corresponds to a hereditary nonpolyposis colorectal carcinoma-causing missense mutation. Mol. Cell. Biol. 16:1996;3008-3011.
33. Bishop D.K., Kolodner R.D. Repair of Heteroduplex plasmid DNA after transformation into Saccharomyces cerevisiae. Mol. Cell. Biol. 6:1986;3401-3409.
34. Bishop D.K., Andersen J., Kolodner R.D. Specificity of mismatch repair following transformation of Saccharomyces cerevisiae with heteroduplex plasmid DNA. Proc. Natl. Acad. Sci. U. S. A. 86:1989;3713-3717.
35. Alani E. The Saccharomyces cerevisiae Msh2 and Msh6 proteins form a complex that specifically binds to duplex oligonucleotides containing mismatched DNA base pairs. Mol. Cell. Biol. 16:1996;5604-5615.
36. Habraken Y., Sung P., Prakash L., Prakash S. Binding of insertion/deletion DNA mismatches by the heterodimer of yeast mismatch repair proteins MSH2 and MSH3. Curr. Biol. 6:1996;1185-1187.
37. Pang Q.S., Prolla T.A., Liskay R.M. 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. 17:1997;4465-4473.
38. Johnson R.E., Kovvali G.K., Prakash L., Prakash S. Requirement of the yeast MSH3 and MSH6 genes for MSH2-dependent genomic stability. J. Biol. Chem. 271:1996;7285-7288.
39. Durant S.T., Morris M.M., Illand M., McKay H.J., McCormick C., Hirst G.L., Borts R.H., Brown R. Dependence on Rad52 and Rad1 for anticancer drug resistance mediated by inactivation of mismatch repair genes. Curr. Biol. 9:1999;51-54.
40. Bawa S., Xiao W. A mutation in the MSH5 gene results in methylation tolerance. Cancer Res. 57:1997;2715-2720.
41. Early M.C., Crouse G.F. The role of mismatch repair in the prevention of base pair mutations in Saccharomyces cerevisiae. Proc. Nat. Acad. Sci. U. S. A. 95:1998;15487-15491.
42. Leadon S.A., Avrutskaya A.V. Requirement for DNA mismatch repair proteins in the transcription-coupled repair of thymine glycols in Saccharomyces cerevisiae. Mutat. Res. 407:1998;177-187.
43. Huang K.N., Symington L.S. A 5′-3′ exonuclease from Saccharomyces cerevisiae is required for in vitro recombination between linear DNA molecules with overlapping homology. Mol. Cell. Biol. 13:1993;3125-3134.
44. Fiorentini P., Huang K.N., Tishkoff D.X., Kolodner R.D., Symington L.S. Exonuclease I of Saccharomyces cerevisiae functions in mitotic recombination in vivo and in vitro. Mol. Cell. Biol. 17:1997;2764-2773.
45. Tishkoff D.X., Boerger A.L., Bertrand P., Filosi N., Gaida G.M., Kane M.F., Kolodner R.D. Identification and characterization of Saccharomyces cerevisiae EXO1 a gene encoding an exonuclease that interacts with MSH2. Proc. Natl. Acad. Sci. U. S. A. 94:1997;7487-7492.
46. Holliday R. A mechanism for gene conversion in fungi. Genet. Res. 5:1964;282-304.
47. White J.H., Lusnak K., Fogel S. Mismatch-specific post-meiotic segregation frequency in yeast suggests a heteroduplex recombination intermediate. Nature. 315:1985;350-352.
48. Detloff P., Sieber J., Petes T. Repair of specific base pair mismatches during meiotic recombination in the yeast Saccharomyces cerevisiae. Mol. Cell. Biol. 11:1991;737-745.
49. N. Hunter, PhD Thesis, The role of mismatch repair in meiosis, Oxford University, 1997.
50. Khazanehdari K., Khazanehdari B.R.H. EXO1, MSH4 differentially affect crossing-over and segregation. Chromosoma. 109:2000;94-102.
51. Kirkpatrick D.T., Petes T.D. Repair of DNA loops involves DNA mismatch and nucleotide excision repair proteins. Nature. 387:1997;929-931.
52. Kirkpatrick D.T. Roles of the DNA mismatch repair and nucleotide excision repair proteins during meiosis. Cell. Mol. Life Sci. 55:1999.
53. Fleck O., Lehmann E., Schaer P., Kohli J. Involvement of nucleotide-excision repair in msh2 pms1-independent mismatch repair. Nat. Genet. 21:1999;314-317.
54. Szostak J.W., Orr-Weaver T.L., Rothstein R.J., Stahl F.W. The double-strand-break repair model for recombination. Cell. 33:1983;25-35.
55. Resnick M.A. The repair of double-strand breaks in DNA: a model involving recombination. J. Theor. Biol. 59:1976;97-106.
56. Gilbertson L.A., Stahl F.W. A test of the double-strand break model for meiotic recombination in Saccharomyces cerevisiae. Genetics. 144:1996;27-41.
57. Hillers K.J., Stahl F.W. The conversion gradient at HIS4 of Saccharomyces cerevisiae: I. Rejection and restoration of Mendelian segregation. Genetics. 153:1999;555-572.
58. Foss G.M., Hillers K.J., Stahl F.W. The conversion gradient at HIS4 of Saccharomyces cerevisiae: II. A role for mismatch repair directed by biased resolution of the recombinational intermediate. Genetics. 153:1999;573-583.
59. Hastings P.J. Recombination in the eukaryotic nucleus. BioEssays. 9:1988;61-64.
60. Hastings P.J. Measurement of restoration and conversion: its meaning for the mismatch repair hypothesis of conversion. Cold Spring Harbor Symp. Quant. Biol. 49:1984;49-54.
61. Petes T.D., Malone R.E., Syminton L.S. Recombination in yeast. Broach J.R., Pringle J.R., Jones E.W. The Molecular and Cellular Biology of the Yeast Saccharomyces. 1991;407-521 Cold Spring Harbor Laboratory Press.
62. Nag D.K., Petes T.D. Physical detection of heteroduplexes during meiotic recombination in the yeast Saccharomyces cerevisiae. Mol. Cell. Biol. 13:1993;2324-2331.
63. Schwacha A., Kleckner N. Identification of double Holliday junctions as intermediates in meiotic recombination. Cell. 83:1995;738-791.
64. Goyon C., Lichten M. Timing of molecular events in meiosis in Saccharomyces cerevisiae: stable heteroduplex is formed late in meiotic prophase. Mol. Cell. Biol. 13:1993;373-382.
65. Panyutin I.G., Hsieh P. Formation of a single base mismatch impedes spontaneous DNA branch migration. J. Mol. Biol. 230:1993;413-424.
66. Panyutin I.G., Biswas I., Hsieh P. A pivotal role for the structure of the Holliday Junction in DNA branch migration. EMBO J. 14:1995;1819-1826.
67. Nicolas A., Petes T.D. Polarity of meiotic gene conversion in fungi: contrasting views. Experientia. 50:1994;242-252.
68. Porter S.E., White M.A., Petes T.D. Genetic evidence that the meiotic recombination hotspot at the HIS4 locus of Saccharomyces cerevisiae does not represent a site for a symmetrically processed double-strand break. Genetics. 134:1993;5-19.
69. Worth L.J., Clark S., Radman M., Modrich P. Mismatch repair proteins MutS and MutL inhibit RecA-catalysed strand transfer between diverged DNAs. Proc. Natl. Acad. Sci. U. S. A. 91:1994;3238-3241.
70. Borts R.H., Haber J.E. Length and distribution of meiotic gene conversion tracts and crossovers in Saccharomyces cerevisiae. Genetics. 123:1989;69-80.
71. Borts R.H., Haber J.E. Meiotic recombination in yeast: alteration by multiple heterozygosities. Science. 237:1987;1459-1463.
72. Rossignol J.L., Paquette N., Nicolas A. Aberrant 4:4 asci, disparity in the direction of conversion, and frequencies of conversion in Ascobolous immersus. Cold Spring Harbour Symp. Quant. Biol. 43:1978;1343-1356.
73. Kitani Y. Absence of interference in association with gene conversion in Sordaria fimicola, and presence of interference in association with ordinary recombination. Genetics. 89:1978;467-497.
74. Fogel S., Mortimer R.K., Lusnak K. Mechanisms of meiotic gene conversion, or "wanderings on a foreign strand" Strathern J.N., Jones E.W., Broach J.R. The Molecular Biology of the Yeast Saccharomyces: Life Cycle and Inheritance. 1981;289-339 Cold Spring Harbor Laboratory, New York.
75. Fogel S., Mortimer R.K., Lusnak K., Tavares F. Meiotic gene conversion: a signal of the basic recombination event in yeast. Cold Spring Harbor Symp. Quant. Biol. 43:1979;1325-1341.
76. Detloff P., White M.A., Petes T.D. Analysis of a gene conversion gradient at the HIS4 locus in Saccharomyces cerevisiae. Genetics. 132:1992;113-123.
77. Kirkpatrick D.T., Dominska M., Petes T.D. Conversion-type and restoration-type repair of DNA mismatches formed during meiotic recombination in Saccharomyces cerevisiae. Genetics. 149:1998;1693-1705.
78. Nag K.K., White M.A., Petes T.D. Palindromic sequences in heteroduplex DNA inhibit mismatch repair in yeast. Nature. 340:1989;318-320.
79. Stahl F.W., Hillers K.J. Heteroduplex rejection? Genetics. 154:2000;1913-1916.
80. Zalevsky J., MacQueen A.J., Duffy J.B., Kemphues K.J., Villeneuve A.M. Crossing over during Caenorhabditis elegans meiosis requires a conserved MutS-based pathway that is partially dispensable in budding yeast. Genetics. 153:1999;1271-1283.
81. Alani E., Lee S., Kane M., Griffith J., Kolodner R. Saccharomyces cerevisiae MSH2, a mispaired base recognition protein, also recognizes Holliday junctions in DNA. J. Mol. Biol. 265:1997;289-301.
82. Marsischky G.T., Lee S., Griffith J., Kolodner R.D. Saccharomyces cerevisiae MSH2/6 complex interacts with Holliday junctions and facilitates their cleavage by phage resolution enzymes. J. Biol. Chem. 274:1999;7200-7206.
83. Edelman W., Cohen P.E., Kneitz B., Winand N., Lia M., Heyer J., Kolodner R., Pollard J.W., Kucherlapati R. Mammalian MutS homologue 5 is required for chromosome pairing in meiosis. Nat. Genet. 21:1999;123-127.
84. de Vries S.S., Baart E.B., Dekker M., Siezen A., de Rooij D.G., de Boer P., te Riele H. Mouse MutS-like protein Msh5 is required for proper chromosome synapsis in male and female meiosis. Genes Dev. 13:1999;523-531.
85. Baker S.M., Plug A.W., Prolla T.A., Bronner C.E., Harris A.C., Yao X., Christie D.-M., Monell C., Arnheim N., Bradley A., Ashley T., Liskay M. Involvement of mouse Mlh1 in DNA mismatch repair and meiotic crossing over. Nat. Genet. 13:1996;336-342.
86. Anderson L.K., Reeves A., Webb L.M., Ashley T. Distribution of crossing over on mouse synaptonemal complexes using immunofluorescent localization of MLH1 protein. Genetics. 151:1999;1569-1579.
87. Barlow A.L., Hulten M.A. Crossing over analysis at pachytene in man. Eur. J. Hum. Genet. 6:1998;350-358.
88. Carpenter A.T.C. Gene conversion, recombination nodules, and the initiation of meiotic synapsis. BioEssays. 6:1987;232-236.
89. + gene of Schizosaccharomyces pombe encodes a homologue of mismatch repair enzymes. Nucleic Acids Res. 9:1992;2271-2278.
90. Rudolph C., Kunz C., Parisi S., Lehmann E., Hartsuiker E., Fartmann B., Kramer W., Kohli J., Fleck O. The msh2 gene of Schizosaccharomyces pombe is involved in mismatch repair, mating-type switching, and meiotic chromosome organisation. Mol. Cell. Biol. 19:1999;241-250.
91. Umar A., Buermeyer A.B., Simon J.A., Thomas D.C., Clark A.B., Liskay R.M., Kunkel T.A. Requirement for PCNA in DNA mismatch repair at a step preceding DNA resynthesis. Cell. 87:1996;65-73.
92. Manivasakam P., Rosenberg S.M., Hastings P.J. Poorly repaired mismatches in heteroduplex DNA are hyper-recombinagenic in Saccharomyces cerevisiae. Genetics. 142:1996;407-416.
93. Southern E.M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J. Mol. Biol. 98:1975;503-517.
94. Symington L.S., Petes T.D. Expansions and contractions of the genetic map relative to the physical map of yeast chromosome III. Mol. Cell. Biol. 8:1988;595-604.
95. Judd R.S., Petes T.D. Physical lengths of meiotic and mitotic gene conversion tracts in Saccharomyces cerivisiae. Genetics. 118:1988;401-410.
96. E.A. Shoubochkina, T.L. Nielsen, T. Nilsson-Tillgren, personal communication.
97. Meselson M.S., Radding C.M. A general model for recombination. Proc. Natl. Acad. Sci. U. S. A. 72:1975;358-361.
98. Borts R.H., Lichten M., Haber J.E. Analysis of meiosis-defective mutations in yeast by physical monitoring of recombination. Genetics. 113:1986;551-567.
99. Borts R.H., Leung W.-Y., Kramer K., Kramer B., Williamson M.S., Fogel S., Haber J.E. Mismatch repair-induced meiotic recombination requires the PMS1 gene product. Genetics. 124:1990;573-584.
100. Detloff P., Petes T.D. Measurements of excision repair tracts formed during meiotic recombination in Saccharomyces cerevisiae. Mol. Cell. Biol. 12:1992;1805-1814.
101. Fogel S., Hurst D.D. Meiotic gene conversion in yeast tetrads and the theory of recombination. Genetics. 57:1967;455-481.
102. Sun H., Treco D., Szostak J. Extensive 3′-overhanging, single-stranded DNA associated with the meiosis-specific double-strand breaks at the ARG4 recombination initiation site. Cell. 64:1991;1155-1161.
103. Sun H., Treco D., Schultes N.P., Szostak J.W. Double-strand breaks at an initiation site for meiotic gene conversion. Nature. 338:1989;87-90.
104. Bishop D.K., Park L., Xu L., Kleckner N. DMC1: a meiosis-specific yeast homolog of E. coli recA required for recombination, synaptonemal complex formation, and cell cycle progression. Cell. 69:1992;439-456.
105. Vedel M., Nicolas A. CYS3, a hotspot of meiotic recombination in Saccharomyes cerevisiae: effects of heterozygosity and mismatch repair functions on gene conversion and recombination intermediates. Genetics. 151:1999;1245-1259.
106. R.H. Borts, unpublished observations.
107. Savage E., Hastings P.J. Marker effects and the nature of the recombination event. Curr. Genet. 3:1981;37-47.
108. Nilsson-Tillgren T., Gjermansen C., Kielland-Brandt M.C., Peterson J.G.L., Holmberg S. Genetic differences between Saccharomyces carlsbergensis and Saccharomyces cerevisiae; analysis of chromosome III by single chromosome transfer. Carlsberg Res. Commun. 46:1981;65-71.
109. Holmberg S. Genetic differences between Saccharomyces carlsbergensis and S. cerevisiae: II. Restriction endonuclease analysis of genes in chromosome III. Carlsberg Res. Commun. 47:1982;232-244.
110. Kielland-Brandt M.C., Nilsson-Tillgren T., Gjermansen C., Holmberg S., Pederson M.B. Genetics of Brewing Yeasts. 1995;Academic Press, London.
111. Radman M. Mismatch repair and fidelity of genetic recombination. Genome. 31:1989;68-73.
112. Radman M. Mismatch repair and genetic recombination. Kucherlapati R., Smith G.R. Genetic Recombination. 1988;169-192 American Society for Microbiology, Washington, DC.
113. Rayssiguier C., Thaler D.S., Radman M. The barrier to recombination between Escherichia coli and Salmonella typhimurium is disrupted in mismatch-repair mutants. Nature. 342:1989;396-400.
114. Radman M., Wagner R. Mismatch recognition in chromosomal interactions and speciation. Chromosoma. 102:1993;369-373.
115. Matic I., Rayssiguier C., Radman M. Interspecies gene exchange in bacteria: the role of SOS and mismatch repair systems in evolution of species. Cell. 80:1995;507-515.
116. Vulic M., Dionisio F., Taddei F., Radman M. Molecular keys to speciation: DNA polymorphism and the control of genetic exchange in enterobacteria. Proc. Natl. Acad. Sci. U. S. A. 94:1997;9763-9767.
117. Stambuk S., Radman M. Mechanism and control of interspecies recombination in Escherichia coli: I. Mismatch repair, methylation, recombination and replication functions. Genetics. 150:1998;533-542.
118. Zahrt T.C., Malloy S. Barriers to recombination between closely related bacteria: MutL and RecBCD inhibit recombination between Salmonella typhimurium and Salmonella typhi. Proc. Natl. Acad. Sci. U. S. A. 94:1997;9786-9791.
119. Glickman B.W., Radman M. Escherichia coli mutator mutants defective in methylation-instructed DNA mismatch correction. Proc. Natl. Acad. Sci. U. S. A. 77:1980;1063-1067.
120. Marinus M.G., Morris N.R. Isolation of deoxyribonucleic acid methylase mutants of Escherichia coli K12. J. Bacteriol. 114:1973;1143-1150.
121. + revertants and suppressor mutations that modify secondary phenotypes of dam-3 strains of Escherichia coli K12. Mol. Gen. Genet. 178:1980;309-315.
122. Peterson K.R., Wertman K.F., Mount D.W., Marinus M.G. Viability of Escherichia coli K12 DNA adenine methylase (dam) mutants requires increased expression of specific genes of the SOA regulons. Mol. Gen. Genet. 210:1985;14-19.
123. Wang T.V., Smith K.C. Inviability of dam recA and dam recB cells of Escherichia coli is correlated with their inability to repair DNA double-strand breaks produced by mismatch repair. J. Bacteriol. 165:1986;1023-1025.
124. Doutriaux M.-P., Wagner R., Radman M. Mismatch-stimulated killing. Proc. Natl. Acad. Sci. U. S. A. 83:1986;2576-2578.
125. Chambers S.R., Hunter N., Louis E.J., Borts R.H. The mismatch repair system reduces meiotic homeologous recombination and stimulates recombination-dependent chromosome loss. Mol. Cell. Biol. 16:1996;6110-6120.
126. Hunter N., Chambers S.R., Louis E.J., Borts R.H. The mismatch repair system contributes to meiotic sterility in an interspecific yeast hybrid. EMBO J. 15:1996;1726-1733.
127. Roeder G.S. Meiotic chromosomes: it takes two to tango. Genes Dev. 11:1997;2600-2621.
128. Roeder G.S. Sex and the single cell: meiosis in yeast. Proc. Natl. Acad. Sci. U. S. A. 92:1995;10450-10456.
129. Kleckner N. Meiosis: how could it work? Proc. Natl. Acad. Sci. U. S. A. 93:1996;8167-8174.
130. Selva E.M., New L., Crouse G.F., Lahue R.S. Mismatch correction acts as a barrier to homeologous recombination in Saccharomyces cerevisiae. Genetics. 139:1995;1175-1188.
131. Datta A., Adjiri A., New L., Crouse G.F., Jinks-Robertson S. Mitotic crossovers between diverged sequences are regulated by mismatch repair proteins in Saccharomyces cerevisiae. Mol. Cell. Biol. 16:1996;1085-1093.
132. Chen W., Jinks-Robertson S. The role of the mismatch repair machinery in regulating mitotic and meiotic recombination between diverged sequences in yeast. Genetics. 151:1999;1299-1313.
133. Majewski J., Cohan F.M. The effect of mismatch repair on heteroduplex formation on sexual isolation in Bacillus. Genetics. 148:1998;13-18.
134. Chen W., Jinks-Robertson S. Mismatch repair protein regulate heteroduplex formation during mitotic recombination in yeast. Mol. Cell. Biol. 18:1998;6525-6537.
135. Datta A., Hendrix M., Lipsitch M., Jinks-Robertson S. Dual roles for DNA sequence identity and the mismatch repair system in the regulation of mitotic crossing-over in yeast. Proc. Natl. Acad. Sci. U. S. A. 94:1997;9757-9762.
136. Haber J.E., Hearn M. RAD52-independent mitotic gene conversion in Saccharomyces cerevisiae frequently results in chromosomal loss. Genetics. 111:1985;7-22.
137. S.R. Chambers, PhD Thesis, DNA mismatch repair and meiotic homeologous recombination, Oxford Brookes University, 1999.
138. Wicksteed B.L., Collins I., Dershowitz A., Stateva L.I., Green R.P., Oliver S.G., Brown A.J.P., Newlon C.S. A physical comparison of chromosome III in six strains of Saccharomyces cerevisiae. Yeast. 10:1994;39-57.
139. de Wind N., Dekker M., Berns A., Radman M., te Riele H. Inactivation of the mouse Msh2 gene results in mismatch repair deficiency, methylation tolerance, hyperrecombination, and predisposition to cancer. Cell. 82:1995;321-330.
140. M.F.F. Abdullah, A. Underwood, E.J. Louis, R.H. Borts, unpublished observations.
141. Cargill M., Altshuler D., Ireland J., Sklar P., Ardlie K., Patil N., Lane C.R., Lim E.P., Kalyanaraman N., Nemesh J., Ziaugra L., Friedland L., Rolfe A., Warrington J., Lipshutz R., Daley G.Q., Lander E.S. Characterization of single-nucleotide polymorphisms in coding regions of human genes. Nat. Genet. 22:1999;231-238.
142. Shen P., Huang H.V. Homologous recombination in Escherichia coli: dependent on substrate length and homology. Genetics. 112:1986;441-457.
143. Shen P., Huang H.V. Effect of base pair mismatches on recombination via the RecBCD pathway. Mol. Gen. Genet. 218:1989;358-360.
144. R.H. Borts, E.J. Louis, unpublished observations.
145. Nicolaidis O., Petersen M.B. Origin and mechanisms of non-disjunction in human autosomal trisomies. Hum. Reprod. 13:1998;313-319.
146. Hassold T., Merrill M., Adkins K., Freeman S., Sherman S. Recombination and maternal age-dependent nondisjunction: molecular studies of trisomy 16. Am. J. Hum. Genet. 57:1995;867-874.
147. Lamb N.E., Freeman S.B., Savage-Austin A., Pettay D., Taft L., Hersey J., Gu Y., Shen J., Saker D., Avramopoulos D., Petersen M.B., Hallberg A., Mikkelsen M., Hassold T.J., Sherman S.L. Susceptible chiasmate configurations of chromosome 21 predispose to non-disjunction in both maternal meiosis I and meiosis II. Nat. Genet. 14:1996;400-405.
148. Schultes N.P., Szostak J.W. Decreasing gradients of gene conversion on both sides of the initiation site for meiotic recombination at the ARG4 locus in yeast. Genetics. 126:1990;813-822.
149. Malone R.E., Kim S., Bullard S.A., Lundquist S., Hutchings-Crow L., Cramton S., Lutfiyya L., Lee J. Analysis of a recombination hotspot for gene conversion occurring at the HIS2 gene of Saccharomyces cerevisiae. Genetics. 137:1994;5-18.
150. Malone R.E., Bullard S.A., Lundquist S., Kim S., Tarkowski T. A meiotic gene conversion gradient opposite to the direction of transcription. Nature. 359:1992;154-155.
151. Baudat F., Nicolas A. Clustering of meiotic double-strand breaks on yeast chromosome III. Proc. Natl. Acad. Sci. U. S. A. 94:1997;5213-5218.