Requirement of Mismatch Repair Genes MSH2 and MSH3 in the RAD1-RAD10 Pathway of Mitotic Recombination in Saccharomyces cerevisiae

INVESTIGATIONS

Requirement of Mismatch Repair Genes MSH2 and MSH3 in the RAD1-RAD10 Pathway of Mitotic Recombination in Saccharomyces cerevisiae

M. Saparbaev, L. Prakash and S. Prakash
Sealy Center for Molecular Science, University of Texas Medical Branch, Galveston, Texas 77555-1061

The RAD1 and RAD10 genes of Saccharomyces cerevisiae are required for nucleotide excision repair and they also act in mitotic recombination. The Rad1-Rad10 complex has a single-stranded DNA endonuclease activity. Here, we show that the mismatch repair genes MSH2 and MSH3 function in mitotic recombination. For both his3 and his4 duplications, and for homologous integration of a linear DNA fragment into the genome, the msh3{Delta} mutation has an effect on recombination similar to that of the rad1{Delta} and rad10{Delta} mutations. The msh2{Delta} mutation also reduces the rate of recombination of the his3 duplication and lowers the incidence of homologous integration of a linear DNA fragment. Epistasis analyses indicate that MSH2 and MSH3 function in the RAD1-RAD10 recombination pathway, and studies presented here suggest an involvement of the RAD1-RAD10 pathway in reciprocal recombination. The possible roles of Msh2, Msh3, Rad1, and Rad10 proteins in genetic recombination are discussed. Coupling of mismatch binding proteins with the recombinational machinery could be important for ensuring genetic fidelity in the recombination process.

This article has been cited by other articles:

A. M. Lyndaker, T. Goldfarb, and E. Alani
Mutants Defective in Rad1-Rad10-Slx4 Exhibit a Unique Pattern of Viability During Mating-Type Switching in Saccharomyces cerevisiae
Genetics, August 1, 2008; 179(4): 1807 - 1821.
[Abstract] [Full Text] [PDF]

C. Welz-Voegele and S. Jinks-Robertson
Sequence Divergence Impedes Crossover More Than Noncrossover Events During Mitotic Gap Repair in Yeast
Genetics, July 1, 2008; 179(3): 1251 - 1262.
[Abstract] [Full Text] [PDF]

J. A. Smith, L. A. Bannister, V. Bhattacharjee, Y. Wang, B. C. Waldman, and A. S. Waldman
Accurate Homologous Recombination Is a Prominent Double-Strand Break Repair Pathway in Mammalian Chromosomes and Is Modulated by Mismatch Repair Protein Msh2
Mol. Cell. Biol., November 15, 2007; 27(22): 7816 - 7827.
[Abstract] [Full Text] [PDF]

R. L. Barnes and R. McCulloch
Trypanosoma brucei homologous recombination is dependent on substrate length and homology, though displays a differential dependence on mismatch repair as substrate length decreases
Nucleic Acids Res., May 11, 2007; 35(10): 3478 - 3493.
[Abstract] [Full Text] [PDF]

A. Nicholson, R. M. Fabbri, J. W. Reeves, and G. F. Crouse
The Effects of Mismatch Repair and RAD1 Genes on Interchromosomal Crossover Recombination in Saccharomyces cerevisiae
Genetics, June 1, 2006; 173(2): 647 - 659.
[Abstract] [Full Text] [PDF]

J. A. Smith, B. C. Waldman, and A. S. Waldman
A Role for DNA Mismatch Repair Protein Msh2 in Error-Prone Double-Strand-Break Repair in Mammalian Chromosomes
Genetics, May 1, 2005; 170(1): 355 - 363.
[Abstract] [Full Text] [PDF]

L. J. Barber, T. A. Ward, J. A. Hartley, and P. J. McHugh
DNA Interstrand Cross-Link Repair in the Saccharomyces cerevisiae Cell Cycle: Overlapping Roles for PSO2 (SNM1) with MutS Factors and EXO1 during S Phase
Mol. Cell. Biol., March 15, 2005; 25(6): 2297 - 2309.
[Abstract] [Full Text] [PDF]

K.-C. Li, C.-T. Liu, W. Sun, S. Yuan, and T. Yu
A system for enhancing genome-wide coexpression dynamics study
PNAS, November 2, 2004; 101(44): 15561 - 15566.
[Abstract] [Full Text] [PDF]

L. D. Langston and L. S. Symington
Gene targeting in yeast is initiated by two independent strand invasions
PNAS, October 26, 2004; 101(43): 15392 - 15397.
[Abstract] [Full Text] [PDF]

M. U. Keller-Seitz, U. Certa, C. Sengstag, F. E. Wurgler, M. Sun, and M. Fasullo
Transcriptional Response of Yeast to Aflatoxin B1: Recombinational Repair Involving RAD51 and RAD1
Mol. Biol. Cell, September 1, 2004; 15(9): 4321 - 4336.
[Abstract] [Full Text] [PDF]

C. E. Schrader, J. Vardo, E. Linehan, M. Z. Twarog, L. J. Niedernhofer, J. H.J. Hoeijmakers, and J. Stavnezer
Deletion of the Nucleotide Excision Repair Gene Ercc1 Reduces Immunoglobulin Class Switching and Alters Mutations Near Switch Recombination Junctions
J. Exp. Med., August 2, 2004; 200(3): 321 - 330.
[Abstract] [Full Text] [PDF]

J. S. Bell and R. McCulloch
Mismatch Repair Regulates Homologous Recombination, but Has Little Influence on Antigenic Variation, in Trypanosoma brucei
J. Biol. Chem., November 14, 2003; 278(46): 45182 - 45188.
[Abstract] [Full Text] [PDF]

J.-F. Villemure, C. Abaji, I. Cousineau, and A. Belmaaza
MSH2-deficient Human Cells Exhibit a Defect in the Accurate Termination of Homology-directed Repair of DNA Double-Strand Breaks
Cancer Res., June 15, 2003; 63(12): 3334 - 3339.
[Abstract] [Full Text] [PDF]

N. J. Morey, P. W. Doetsch, and S. Jinks-Robertson
Delineating the Requirements for Spontaneous DNA Damage Resistance Pathways in Genome Maintenance and Viability in Saccharomyces cerevisiae
Genetics, June 1, 2003; 164(2): 443 - 455.
[Abstract] [Full Text] [PDF]

A. Galli, T. Cervelli, and R. H. Schiestl
Characterization of the Hyperrecombination Phenotype of the pol3-t Mutation of Saccharomyces cerevisiae
Genetics, May 1, 2003; 164(1): 65 - 79.
[Abstract] [Full Text] [PDF]

S. Palmer, E. Schildkraut, R. Lazarin, J. Nguyen, and J. A. Nickoloff
Gene conversion tracts in Saccharomyces cerevisiae can be extremely short and highly directional
Nucleic Acids Res., February 15, 2003; 31(4): 1164 - 1173.
[Abstract] [Full Text] [PDF]

L. S. Symington
Role of RAD52 Epistasis Group Genes in Homologous Recombination and Double-Strand Break Repair
Microbiol. Mol. Biol. Rev., December 1, 2002; 66(4): 630 - 670.
[Abstract] [Full Text] [PDF]

G. M. Manthey and A. M. Bailis
Multiple Pathways Promote Short-Sequence Recombination in Saccharomyces cerevisiae
Mol. Cell. Biol., August 1, 2002; 22(15): 5347 - 5356.
[Abstract] [Full Text] [PDF]

H. M. Kearney, D. T. Kirkpatrick, J. L. Gerton, and T. D. Petes
Meiotic Recombination Involving Heterozygous Large Insertions in Saccharomyces cerevisiae: Formation and Repair of Large, Unpaired DNA Loops
Genetics, August 1, 2001; 158(4): 1457 - 1476.
[Abstract] [Full Text] [PDF]

C. Tornier, S. Bessone, I. Varlet, C. Rudolph, M. Darmon, and O. Fleck
Requirement for Msh6, but Not for Swi4 (Msh3), in Msh2-Dependent Repair of Base-Base Mismatches and Mononucleotide Loops in Schizosaccharomyces pombe
Genetics, May 1, 2001; 158(1): 65 - 75.
[Abstract] [Full Text]

B. Elliott and M. Jasin
Repair of Double-Strand Breaks by Homologous Recombination in Mismatch Repair-Defective Mammalian Cells
Mol. Cell. Biol., April 15, 2001; 21(8): 2671 - 2682.
[Abstract] [Full Text]

E. Evans and E. Alani
Roles for Mismatch Repair Factors in Regulating Genetic Recombination
Mol. Cell. Biol., November 1, 2000; 20(21): 7839 - 7844.
[Full Text]

A. J. R. Bishop, E. J. Louis, and R. H. Borts
Minisatellite Variants Generated in Yeast Meiosis Involve DNA Removal During Gene Conversion
Genetics, September 1, 2000; 156(1): 7 - 20.
[Abstract] [Full Text]

A. J. Rattray, B. K. Shafer, and D. J. Garfinkel
The Saccharomyces cerevisiae DNA Recombination and Repair Functions of the RAD52 Epistasis Group Inhibit Ty1 Transposition
Genetics, February 1, 2000; 154(2): 543 - 556.
[Abstract] [Full Text]

N. J. Morey, C. N. Greene, and S. Jinks-Robertson
Genetic Analysis of Transcription-Associated Mutation in Saccharomyces cerevisiae
Genetics, January 1, 2000; 154(1): 109 - 120.
[Abstract] [Full Text]

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, January 1, 2000; 154(1): 133 - 146.
[Abstract] [Full Text]

T. Nakagawa, A. Datta, and R. D. Kolodner
Multiple functions of MutS- and MutL-related heterocomplexes
PNAS, December 7, 1999; 96(25): 14186 - 14188.
[Full Text] [PDF]

B. Studamire, G. Price, N. Sugawara, J. E. Haber, and E. Alani
Separation-of-Function Mutations in Saccharomyces cerevisiae MSH2 That Confer Mismatch Repair Defects but Do Not Affect Nonhomologous-Tail Removal during Recombination
Mol. Cell. Biol., November 1, 1999; 19(11): 7558 - 7567.
[Abstract] [Full Text] [PDF]

O. Inbar and M. Kupiec
Homology Search and Choice of Homologous Partner during Mitotic Recombination
Mol. Cell. Biol., June 1, 1999; 19(6): 4134 - 4142.
[Abstract] [Full Text] [PDF]

R. L. Swanson, N. J. Morey, P. W. Doetsch, and S. Jinks-Robertson
Overlapping Specificities of Base Excision Repair, Nucleotide Excision Repair, Recombination, and Translesion Synthesis Pathways for DNA Base Damage in Saccharomyces cerevisiae
Mol. Cell. Biol., April 1, 1999; 19(4): 2929 - 2935.
[Abstract] [Full Text] [PDF]

M. P. Colaiácovo, F. Pâques, and J. E. Haber
Removal of One Nonhomologous DNA End During Gene Conversion by a RAD1- and MSH2-Independent Pathway
Genetics, April 1, 1999; 151(4): 1409 - 1423.
[Abstract] [Full Text]

C. Flores and W. Engels
Microsatellite instability in Drosophila spellchecker1 (MutS homolog) mutants
PNAS, March 16, 1999; 96(6): 2964 - 2969.
[Abstract] [Full Text] [PDF]

G. T. Marsischky, S. Lee, J. Griffith, and R. D. Kolodner
`Saccharomyces cerevisiae MSH2/6 Complex Interacts with Holliday Junctions and Facilitates Their Cleavage by Phage Resolution Enzymes
J. Biol. Chem., March 12, 1999; 274(11): 7200 - 7206.
[Abstract] [Full Text] [PDF]

H. T. Tran, D. A. Gordenin, and M. A. Resnick
The 3'right-arrow5' Exonucleases of DNA Polymerases delta and varepsilon and the 5'right-arrow3' Exonuclease Exo1 Have Major Roles in Postreplication Mutation Avoidance in Saccharomyces cerevisiae
Mol. Cell. Biol., March 1, 1999; 19(3): 2000 - 2007.
[Abstract] [Full Text] [PDF]

C. Rudolph, C. Kunz, S. Parisi, E. Lehmann, E. Hartsuiker, B. Fartmann, W. Kramer, J. Kohli, and O. Fleck
The msh2 Gene of Schizosaccharomyces pombe Is Involved in Mismatch Repair, Mating-Type Switching, and Meiotic Chromosome Organization
Mol. Cell. Biol., January 1, 1999; 19(1): 241 - 250.
[Abstract] [Full Text] [PDF]

P. Bertrand, D. X. Tishkoff, N. Filosi, R. Dasgupta, and R. D. Kolodner
Physical interaction between components of DNA mismatch repair and nucleotide excision repair
PNAS, November 24, 1998; 95(24): 14278 - 14283.
[Abstract] [Full Text] [PDF]

B. J. Merrill and C. Holm
The RAD52 Recombinational Repair Pathway is Essential in pol30 (PCNA) Mutants That Accumulate Small Single-Stranded DNA Fragments During DNA Synthesis
Genetics, February 1, 1998; 148(2): 611 - 624.
[Abstract] [Full Text] [PDF]

A. Datta, M. Hendrix, M. Lipsitch, and S. Jinks-Robertson
Dual roles for DNA sequence identity and the mismatch repair system in the regulation of mitotic crossing-over in yeast
PNAS, September 2, 1997; 94(18): 9757 - 9762.
[Abstract] [Full Text] [PDF]

N. Sugawara, F. Paques, M. Colaiacovo, and J. E. Haber
Role of Saccharomyces cerevisiae Msh2 and Msh3 repair proteins in double-strand break-induced recombination
PNAS, August 19, 1997; 94(17): 9214 - 9219.
[Abstract] [Full Text] [PDF]

D. X. Tishkoff, A. L. Boerger, P. Bertrand, N. Filosi, G. M. Gaida, M. F. Kane, and R. D. Kolodner
Identification and characterization of Saccharomyces cerevisiae EXO1, a gene encoding an exonuclease that interacts with MSH2
PNAS, July 8, 1997; 94(14): 7487 - 7492.
[Abstract] [Full Text] [PDF]

N Hunter and R H Borts
Mlh1 is unique among mismatch repair proteins in its ability to promote crossing-over during meiosis.
Genes & Dev., June 15, 1997; 11(12): 1573 - 1582.
[Abstract] [PDF]

				C. Welz-Voegele and S. Jinks-Robertson Sequence Divergence Impedes Crossover More Than Noncrossover Events During Mitotic Gap Repair in Yeast Genetics, July 1, 2008; 179(3): 1251 - 1262. [Abstract] [Full Text] [PDF]

				J. A. Smith, L. A. Bannister, V. Bhattacharjee, Y. Wang, B. C. Waldman, and A. S. Waldman Accurate Homologous Recombination Is a Prominent Double-Strand Break Repair Pathway in Mammalian Chromosomes and Is Modulated by Mismatch Repair Protein Msh2 Mol. Cell. Biol., November 15, 2007; 27(22): 7816 - 7827. [Abstract] [Full Text] [PDF]

				R. L. Barnes and R. McCulloch Trypanosoma brucei homologous recombination is dependent on substrate length and homology, though displays a differential dependence on mismatch repair as substrate length decreases Nucleic Acids Res., May 11, 2007; 35(10): 3478 - 3493. [Abstract] [Full Text] [PDF]

				A. Nicholson, R. M. Fabbri, J. W. Reeves, and G. F. Crouse The Effects of Mismatch Repair and RAD1 Genes on Interchromosomal Crossover Recombination in Saccharomyces cerevisiae Genetics, June 1, 2006; 173(2): 647 - 659. [Abstract] [Full Text] [PDF]

				J. A. Smith, B. C. Waldman, and A. S. Waldman A Role for DNA Mismatch Repair Protein Msh2 in Error-Prone Double-Strand-Break Repair in Mammalian Chromosomes Genetics, May 1, 2005; 170(1): 355 - 363. [Abstract] [Full Text] [PDF]

				L. J. Barber, T. A. Ward, J. A. Hartley, and P. J. McHugh DNA Interstrand Cross-Link Repair in the Saccharomyces cerevisiae Cell Cycle: Overlapping Roles for PSO2 (SNM1) with MutS Factors and EXO1 during S Phase Mol. Cell. Biol., March 15, 2005; 25(6): 2297 - 2309. [Abstract] [Full Text] [PDF]

				K.-C. Li, C.-T. Liu, W. Sun, S. Yuan, and T. Yu A system for enhancing genome-wide coexpression dynamics study PNAS, November 2, 2004; 101(44): 15561 - 15566. [Abstract] [Full Text] [PDF]

				L. D. Langston and L. S. Symington Gene targeting in yeast is initiated by two independent strand invasions PNAS, October 26, 2004; 101(43): 15392 - 15397. [Abstract] [Full Text] [PDF]

				M. U. Keller-Seitz, U. Certa, C. Sengstag, F. E. Wurgler, M. Sun, and M. Fasullo Transcriptional Response of Yeast to Aflatoxin B1: Recombinational Repair Involving RAD51 and RAD1 Mol. Biol. Cell, September 1, 2004; 15(9): 4321 - 4336. [Abstract] [Full Text] [PDF]

				C. E. Schrader, J. Vardo, E. Linehan, M. Z. Twarog, L. J. Niedernhofer, J. H.J. Hoeijmakers, and J. Stavnezer Deletion of the Nucleotide Excision Repair Gene Ercc1 Reduces Immunoglobulin Class Switching and Alters Mutations Near Switch Recombination Junctions J. Exp. Med., August 2, 2004; 200(3): 321 - 330. [Abstract] [Full Text] [PDF]

				J. S. Bell and R. McCulloch Mismatch Repair Regulates Homologous Recombination, but Has Little Influence on Antigenic Variation, in Trypanosoma brucei J. Biol. Chem., November 14, 2003; 278(46): 45182 - 45188. [Abstract] [Full Text] [PDF]

				J.-F. Villemure, C. Abaji, I. Cousineau, and A. Belmaaza MSH2-deficient Human Cells Exhibit a Defect in the Accurate Termination of Homology-directed Repair of DNA Double-Strand Breaks Cancer Res., June 15, 2003; 63(12): 3334 - 3339. [Abstract] [Full Text] [PDF]

				N. J. Morey, P. W. Doetsch, and S. Jinks-Robertson Delineating the Requirements for Spontaneous DNA Damage Resistance Pathways in Genome Maintenance and Viability in Saccharomyces cerevisiae Genetics, June 1, 2003; 164(2): 443 - 455. [Abstract] [Full Text] [PDF]

				A. Galli, T. Cervelli, and R. H. Schiestl Characterization of the Hyperrecombination Phenotype of the pol3-t Mutation of Saccharomyces cerevisiae Genetics, May 1, 2003; 164(1): 65 - 79. [Abstract] [Full Text] [PDF]

				S. Palmer, E. Schildkraut, R. Lazarin, J. Nguyen, and J. A. Nickoloff Gene conversion tracts in Saccharomyces cerevisiae can be extremely short and highly directional Nucleic Acids Res., February 15, 2003; 31(4): 1164 - 1173. [Abstract] [Full Text] [PDF]

				L. S. Symington Role of RAD52 Epistasis Group Genes in Homologous Recombination and Double-Strand Break Repair Microbiol. Mol. Biol. Rev., December 1, 2002; 66(4): 630 - 670. [Abstract] [Full Text] [PDF]

				G. M. Manthey and A. M. Bailis Multiple Pathways Promote Short-Sequence Recombination in Saccharomyces cerevisiae Mol. Cell. Biol., August 1, 2002; 22(15): 5347 - 5356. [Abstract] [Full Text] [PDF]

				H. M. Kearney, D. T. Kirkpatrick, J. L. Gerton, and T. D. Petes Meiotic Recombination Involving Heterozygous Large Insertions in Saccharomyces cerevisiae: Formation and Repair of Large, Unpaired DNA Loops Genetics, August 1, 2001; 158(4): 1457 - 1476. [Abstract] [Full Text] [PDF]

				C. Tornier, S. Bessone, I. Varlet, C. Rudolph, M. Darmon, and O. Fleck Requirement for Msh6, but Not for Swi4 (Msh3), in Msh2-Dependent Repair of Base-Base Mismatches and Mononucleotide Loops in Schizosaccharomyces pombe Genetics, May 1, 2001; 158(1): 65 - 75. [Abstract] [Full Text]

				B. Elliott and M. Jasin Repair of Double-Strand Breaks by Homologous Recombination in Mismatch Repair-Defective Mammalian Cells Mol. Cell. Biol., April 15, 2001; 21(8): 2671 - 2682. [Abstract] [Full Text]

				E. Evans and E. Alani Roles for Mismatch Repair Factors in Regulating Genetic Recombination Mol. Cell. Biol., November 1, 2000; 20(21): 7839 - 7844. [Full Text]

				A. J. R. Bishop, E. J. Louis, and R. H. Borts Minisatellite Variants Generated in Yeast Meiosis Involve DNA Removal During Gene Conversion Genetics, September 1, 2000; 156(1): 7 - 20. [Abstract] [Full Text]

				A. J. Rattray, B. K. Shafer, and D. J. Garfinkel The Saccharomyces cerevisiae DNA Recombination and Repair Functions of the RAD52 Epistasis Group Inhibit Ty1 Transposition Genetics, February 1, 2000; 154(2): 543 - 556. [Abstract] [Full Text]

				N. J. Morey, C. N. Greene, and S. Jinks-Robertson Genetic Analysis of Transcription-Associated Mutation in Saccharomyces cerevisiae Genetics, January 1, 2000; 154(1): 109 - 120. [Abstract] [Full Text]

				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, January 1, 2000; 154(1): 133 - 146. [Abstract] [Full Text]

				T. Nakagawa, A. Datta, and R. D. Kolodner Multiple functions of MutS- and MutL-related heterocomplexes PNAS, December 7, 1999; 96(25): 14186 - 14188. [Full Text] [PDF]

				B. Studamire, G. Price, N. Sugawara, J. E. Haber, and E. Alani Separation-of-Function Mutations in Saccharomyces cerevisiae MSH2 That Confer Mismatch Repair Defects but Do Not Affect Nonhomologous-Tail Removal during Recombination Mol. Cell. Biol., November 1, 1999; 19(11): 7558 - 7567. [Abstract] [Full Text] [PDF]

				O. Inbar and M. Kupiec Homology Search and Choice of Homologous Partner during Mitotic Recombination Mol. Cell. Biol., June 1, 1999; 19(6): 4134 - 4142. [Abstract] [Full Text] [PDF]

				R. L. Swanson, N. J. Morey, P. W. Doetsch, and S. Jinks-Robertson Overlapping Specificities of Base Excision Repair, Nucleotide Excision Repair, Recombination, and Translesion Synthesis Pathways for DNA Base Damage in Saccharomyces cerevisiae Mol. Cell. Biol., April 1, 1999; 19(4): 2929 - 2935. [Abstract] [Full Text] [PDF]

				M. P. Colaiácovo, F. Pâques, and J. E. Haber Removal of One Nonhomologous DNA End During Gene Conversion by a RAD1- and MSH2-Independent Pathway Genetics, April 1, 1999; 151(4): 1409 - 1423. [Abstract] [Full Text]