Roles of RecA homologues Rad51 and Dmc1 during meiotic recombination

RecA protein is involved in homology search and strand exchange processes during recombination. Mitotic cells in eukaryotes express one RecA, Rad51, which is essential for the repair of double-strand breaks (DSBs). Additionally, meiotic cells induce the second RecA, Dmc1. Both Rad51 and Dmc1 are necessary to generate a crossover between homologous chromosomes, which ensures the segregation of the chromosomes at meiotic division I. It is largely unknown how the two RecAs cooperate during meiotic recombination. In this review, recent advances on our knowledge about the roles of Rad51 and Dmc1 during meiosis are summarized and discussed.

[1]  G. Roeder Meiotic chromosomes: it takes two to tango. , 1997, Genes & development.

[2]  R. Camerini-Otero,et al.  The Hop2 protein has a direct role in promoting interhomolog interactions during mouse meiosis. , 2003, Developmental cell.

[3]  S. Prinz,et al.  Isolation of COM1, a new gene required to complete meiotic double-strand break-induced recombination in Saccharomyces cerevisiae. , 1997, Genetics.

[4]  F. Klein,et al.  Mnd1 Is Required for Meiotic Interhomolog Repair , 2004, Current Biology.

[5]  N. Kleckner,et al.  Interhomolog Bias during Meiotic Recombination: Meiotic Functions Promote a Highly Differentiated Interhomolog-Only Pathway , 1997, Cell.

[6]  Roeder Gs Meiotic chromosomes: it takes two to tango , 1997 .

[7]  K. Nairz,et al.  A Central Role for Cohesins in Sister Chromatid Cohesion, Formation of Axial Elements, and Recombination during Yeast Meiosis , 1999, Cell.

[8]  J. Kohli,et al.  Five RecA-like proteins of Schizosaccharomyces pombe are involved in meiotic recombination. , 2003, Genetics.

[9]  J. Buerstedde,et al.  Characterization of the roles of the Saccharomyces cerevisiae RAD54 gene and a homologue of RAD54, RDH54/TID1, in mitosis and meiosis. , 1997, Genetics.

[10]  N. Kleckner,et al.  Meiotic chromosomes: integrating structure and function. , 1999, Annual review of genetics.

[11]  K. Miyagawa,et al.  A role for RAD54B in homologous recombination in human cells , 2002, The EMBO journal.

[12]  H. Nojima,et al.  Dmc1 of Schizosaccharomyces pombe plays a role in meiotic recombination. , 2000, Nucleic acids research.

[13]  Akira Shinohara,et al.  Rad51‐deficient vertebrate cells accumulate chromosomal breaks prior to cell death , 1998, The EMBO journal.

[14]  T. Kodadek,et al.  DMC1 functions in a Saccharomyces cerevisiae meiotic pathway that is largely independent of the RAD51 pathway. , 1997, Genetics.

[15]  L. Symington Role of RAD52 Epistasis Group Genes in Homologous Recombination and Double-Strand Break Repair , 2002, Microbiology and Molecular Biology Reviews.

[16]  S. Forsburg,et al.  Schizosaccharomyces pombe Rdh54 (TID1) acts with Rhp54 (RAD54) to repair meiotic double-strand breaks. , 2003, Molecular biology of the cell.

[17]  S. Kowalczykowski Initiation of genetic recombination and recombination-dependent replication. , 2000, Trends in biochemical sciences.

[18]  E. Revenkova,et al.  Meiotic cohesin REC8 marks the axial elements of rat synaptonemal complexes before cohesins SMC1β and SMC3 , 2003, The Journal of cell biology.

[19]  Daniel G. Anderson,et al.  Reconstitution of an SOS Response Pathway Derepression of Transcription in Response to DNA Breaks , 1998, Cell.

[20]  G. Simchen,et al.  Sister chromatid‐based DNA repair is mediated by RAD54, not by DMC1 or TID1 , 1999, The EMBO journal.

[21]  E. Egelman,et al.  Archaeal RadA protein binds DNA as both helical filaments and octameric rings. , 2001, Journal of molecular biology.

[22]  M. Handel,et al.  Meiotic prophase arrest with failure of chromosome synapsis in mice deficient for Dmc1, a germline-specific RecA homolog. , 1998, Molecular cell.

[23]  K. Ikeo,et al.  Cloning of human, mouse and fission yeast recombination genes homologous to RAD51 and recA , 1993, Nature Genetics.

[24]  Michael G. Sehorn,et al.  Rad51 Recombinase and Recombination Mediators* , 2003, Journal of Biological Chemistry.

[25]  Y. Matsuda,et al.  The mouse RecA-like gene Dmc1 is required for homologous chromosome synapsis during meiosis. , 1998, Molecular cell.

[26]  R. Chanet,et al.  Semidominant suppressors of Srs2 helicase mutations of Saccharomyces cerevisiae map in the RAD51 gene, whose sequence predicts a protein with similarities to procaryotic RecA proteins , 1992, Molecular and cellular biology.

[27]  K. V. SRINATH,et al.  Mechanism of Crossing-over , 1946, Nature.

[28]  K. Nakao,et al.  Targeted disruption of the Rad51 gene leads to lethality in embryonic mice. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[29]  R. Pearlman,et al.  Rad51 and Dmc1 Form Mixed Complexes Associated with Mouse Meiotic Chromosome Cores and Synaptonemal Complexes , 1999, The Journal of cell biology.

[30]  K. Nasmyth,et al.  Un Ménage à Quatre The Molecular Biology of Chromosome Segregation in Meiosis , 2003, Cell.

[31]  A. Nicolas,et al.  Recombination at work for meiosis. , 1998, Current opinion in genetics & development.

[32]  Y. Nishimune,et al.  The mouse and human homologs of DMC1, the yeast meiosis-specific homologous recombination gene, have a common unique form of exon-skipped transcript in meiosis. , 1996, Nucleic acids research.

[33]  G. Roeder,et al.  The Meiosis-Specific Hop2 Protein of S. cerevisiae Ensures Synapsis between Homologous Chromosomes , 1998, Cell.

[34]  Stephen L. Gasior,et al.  Tid1/Rdh54 promotes colocalization of rad51 and dmc1 during meiotic recombination. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[35]  E. Delong,et al.  Diversity of radA Genes from Cultured and UnculturedArchaea: Comparative Analysis of Putative RadA Proteins and Their Use as a Phylogenetic Marker , 1999, Journal of bacteriology.

[36]  H. Klein,et al.  RDH54, a RAD54 homologue in Saccharomyces cerevisiae, is required for mitotic diploid-specific recombination and repair and for meiosis. , 1997, Genetics.

[37]  Samuel Karlin,et al.  Evolutionary Comparisons of RecA-Like Proteins Across All Major Kingdoms of Living Organisms , 1997, Journal of Molecular Evolution.

[38]  A. Shinohara,et al.  Crossover interference in Saccharomyces cerevisiae requires a TID1/RDH54- and DMC1-dependent pathway. , 2003, Genetics.

[39]  J. Haber,et al.  Multiple Pathways of Recombination Induced by Double-Strand Breaks in Saccharomyces cerevisiae , 1999, Microbiology and Molecular Biology Reviews.

[40]  K. Miyagawa,et al.  Human Rad54B is a double-stranded DNA-dependent ATPase and has biochemical properties different from its structural homolog in yeast, Tid1/Rdh54. , 2002, Nucleic acids research.

[41]  N. Kleckner,et al.  DMC1: A meiosis-specific yeast homolog of E. coli recA required for recombination, synaptonemal complex formation, and cell cycle progression , 1992, Cell.

[42]  M. Cox,et al.  RecA protein: structure, function, and role in recombinational DNA repair. , 1997, Progress in nucleic acid research and molecular biology.

[43]  A. Shinohara,et al.  Rad51 protein involved in repair and recombination in S. cerevisiae is a RecA-like protein , 1992, Cell.

[44]  N. Kleckner,et al.  The Single-End Invasion An Asymmetric Intermediate at the Double-Strand Break to Double-Holliday Junction Transition of Meiotic Recombination , 2001, Cell.

[45]  D. K. Bishop,et al.  High copy number suppression of the meiotic arrest caused by a dmc1 mutation: REC114 imposes an early recombination block and RAD54 promotes a DMC1‐independent DSB repair pathway , 1999, Genes to cells : devoted to molecular & cellular mechanisms.

[46]  A. Shinohara,et al.  Localization of RecA-like recombination proteins on chromosomes of the lily at various meiotic stages. , 1995, Genes & development.

[47]  G. Roeder,et al.  Roles for two RecA homologs in promoting meiotic chromosome synapsis. , 1995, Genes & development.

[48]  S. West,et al.  RAD51C Is Required for Holliday Junction Processing in Mammalian Cells , 2004, Science.

[49]  Y. Hiraoka,et al.  A novel meiosis‐specific protein of fission yeast, Meu13p, promotes homologous pairing independently of homologous recombination , 2001, The EMBO journal.

[50]  Eurie L. Hong,et al.  Saccharomyces cerevisiae Dmc1 Protein Promotes Renaturation of Single-strand DNA (ssDNA) and Assimilation of ssDNA into Homologous Super-coiled Duplex DNA* , 2001, The Journal of Biological Chemistry.

[51]  E. Egelman Does a stretched DNA structure dictate the helical geometry of RecA-like filaments? , 2001, Journal of molecular biology.

[52]  R. Kanaar,et al.  Rad54, a Jack of all trades in homologous recombination. , 2003, DNA repair.

[53]  Stephen L. Gasior,et al.  Saccharomyces cerevisiae recA homologues RAD51 and DMC1 have both distinct and overlapping roles in meiotic recombination , 1997, Genes to cells : devoted to molecular & cellular mechanisms.

[54]  S. Keeney,et al.  Mechanism and control of meiotic recombination initiation. , 2001, Current topics in developmental biology.

[55]  J. Derisi,et al.  Mnd1p: An evolutionarily conserved protein required for meiotic recombination , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[56]  S. West,et al.  Human Dmc1 protein binds DNA as an octameric ring. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[57]  Attila Tóth,et al.  A screen for genes required for meiosis and spore formation based on whole-genome expression , 2001, Current Biology.

[58]  E. Egelman,et al.  Similarity of the yeast RAD51 filament to the bacterial RecA filament. , 1993, Science.

[59]  R. Gupta,et al.  The synaptic activity of HsDmc1, a human recombination protein specific to meiosis , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[60]  P. Hasty,et al.  A mutation in mouse rad51 results in an early embryonic lethal that is suppressed by a mutation in p53 , 1996, Molecular and cellular biology.

[61]  G. Roeder,et al.  The importance of genetic recombination for fidelity of chromosome pairing in meiosis. , 2003, Developmental cell.

[62]  P. Sung Catalysis of ATP-dependent homologous DNA pairing and strand exchange by yeast RAD51 protein. , 1994, Science.

[63]  G. Roeder,et al.  The yeast med1 mutant undergoes both meiotic homolog nondisjunction and precocious separation of sister chromatids. , 1994, Genetics.

[64]  G. Roeder,et al.  The Mnd1 Protein Forms a Complex with Hop2 To Promote Homologous Chromosome Pairing and Meiotic Double-Strand Break Repair , 2002, Molecular and Cellular Biology.

[65]  D. K. Bishop RecA homologs Dmc1 and Rad51 interact to form multiple nuclear complexes prior to meiotic chromosome synapsis , 1994, Cell.

[66]  P. Sung,et al.  Promotion of Rad51-dependent D-loop formation by yeast recombination factor Rdh54/Tid1. , 2000, Genes & development.

[67]  S. West,et al.  The meiosis‐specific recombinase hDmc1 forms ring structures and interacts with hRad51 , 1999, The EMBO journal.