From meiosis to postmeiotic events: Uncovering the molecular roles of the meiosis-specific recombinase Dmc1

FEBS Journal

Volumn 277, Issue 3, 2010, Pages 590-598

  Kagawa, Wataru ^a   Kurumizaka, Hitoshi ^a  

^a WASEDA UNIVERSITY   (Japan)

Author keywords

Helical filament; Meiotic recombination; Octameric ring; Recombination regulators

Indexed keywords

BRCA2 PROTEIN; CHROMOSOME PROTEIN; DMC1 RECOMBINASE; FUNGAL PROTEIN; HOP2 PROTEIN; MEI5 PROTEIN; MND1 PROTEIN; PROTEIN SUBUNIT; RAD51 PROTEIN; RAD54 PROTEIN; RECA PROTEIN; RECOMBINASE; SAE3 PROTEIN; SFR1 PROTEIN; SWI5 PROTEIN; UNCLASSIFIED DRUG;

DNA POLYMORPHISM; DNA STRAND; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME REGULATION; ENZYME STRUCTURE; GENE CONTROL; GENE INTERACTION; GENE SEGREGATION; GENE STRUCTURE; GENETIC RECOMBINATION; GENETIC VARIABILITY; HOMOLOGOUS RECOMBINATION; HUMAN; MEIOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SHORT SURVEY; SINGLE NUCLEOTIDE POLYMORPHISM; STRUCTURE ANALYSIS;

BRCA2 PROTEIN; CELL CYCLE PROTEINS; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA BREAKS, DOUBLE-STRANDED; DNA, SINGLE-STRANDED; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; MEIOSIS; MODELS, MOLECULAR; NUCLEAR PROTEINS; PROTEIN STRUCTURE, QUATERNARY; RAD51 RECOMBINASE; REC A RECOMBINASES; RECOMBINASES; RECOMBINATION, GENETIC; SACCHAROMYCES CEREVISIAE PROTEINS; SCHIZOSACCHAROMYCES POMBE PROTEINS; TRANS-ACTIVATORS;

EID: 75149155682     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2009.07503.x     Document Type: Short Survey

References (70)

1. Hassold T Hunt P (2001) To err (meiotically) is human: the genesis of human aneuploidy. Nat Rev Genet 2, 280 291.
2. Chen Z, Yang H Pavletich NP (2008) Mechanism of homologous recombination from the RecA-ssDNA/dsDNA structures. Nature 453, 489 494.
3. Krogh BO Symington LS (2004) Recombination proteins in yeast. Annu Rev Genet 38, 233 271.
4. Baumann P West SC (1998) Role of the human RAD51 protein in homologous recombination and double-stranded-break repair. Trends Biochem Sci 23, 247 251.
5. Bishop DK, Park D, Xu L Kleckner N (1992) DMC1: a meiosis-specific yeast homolog of E. coli recA required for recombination, synaptonemal complex formation, and cell cycle progression. Cell 69, 439 456.
6. Pittman DL, Cobb J, Schimenti KJ, Wilson LA, Cooper DM, Brignull E, Handel MA Schimenti JC (1998) Meiotic prophase arrest with failure of chromosome synapsis in mice deficient for Dmc1, a germline-specific RecA homolog. Mol Cell 1, 697 705.
7. Yoshida K, Kondoh G, Matsuda Y, Habu T, Nishimune Y Morita T (1998) The mouse RecA-like gene Dmc1 is required for homologous chromosome synapsis during meiosis. Mol Cell 1, 707 718.
8. Roeder GS (1997) Meiotic chromosomes: it takes two to tango. Genes Dev 11, 2600 2621.
9. Masson JY, Davies AA, Hajibagheri N, Van Dyck E, Benson FE, Stasiak AZ, Stasiak A West SC (1999) The meiosis-specific recombinase hDmc1 forms ring structures and interacts with hRad51. EMBO J 18, 6552 6560.
10. Passy SI, Yu X, Li Z, Radding CM, Masson JY, West SC Egelman EH (1999) Human Dmc1 protein binds DNA as an octameric ring. Proc Natl Acad Sci USA 96, 10684 10688.
11. Chang YC, Lo YH, Lee MH, Leng CH, Hu SM, Chang CS Wang TF (2005) Molecular visualization of the yeast Dmc1 protein ring and Dmc1-ssDNA nucleoprotein complex. Biochemistry 44, 6052 6058.
12. Sauvageau S, Stasiak AZ, Banville I, Ploquin M, Stasiak A Masson JY (2005) Fission yeast rad51 and dmc1, two efficient DNA recombinases forming helical nucleoprotein filaments. Mol Cell Biol 25, 4377 4387.
13. Shin DS, Pellegrini L, Daniels DS, Yelent B, Craig L, Bates D, Yu DS, Shivji MK, Hitomi C, Arvai AS et al. (2003) Full-length archaeal Rad51 structure and mutants: mechanisms for RAD51 assembly and control by BRCA2. EMBO J 22, 4566 4576.
14. Yang S, Yu X, Seitz EM, Kowalczykowski SC Egelman EH (2001) Archaeal RadA protein binds DNA as both helical filaments and octameric rings. J Mol Biol 314, 1077 1085.
15. Yu X Egelman EH (1997) The RecA hexamer is a structural homologue of ring helicases. Nat Struct Biol 4, 101 104.
16. Benson FE, Stasiak A West SC (1994) Purification and characterization of the human Rad51 protein, an analogue of E. coli RecA. EMBO J 13, 5764 5771.
17. Egelman EH Stasiak A (1986) Structure of helical RecA-DNA complexes. Complexes formed in the presence of ATP-gamma-S or ATP. J Mol Biol 191, 677 697.
18. Komori K, Miyata T, DiRuggiero J, Holley-Shanks R, Hayashi I, Cann IK, Mayanagi K, Shinagawa H Ishino Y (2000) Both RadA and RadB are involved in homologous recombination in Pyrococcus furiosus. J Biol Chem 275, 33782 33790.
19. Ogawa T, Yu X, Shinohara A Egelman EH (1993) Similarity of the yeast RAD51 filament to the bacterial RecA filament. Science 259, 1896 1899.
20. Wu Y, He Y, Moya IA, Qian X Luo Y (2004) Crystal structure of archaeal recombinase RADA: a snapshot of its extended conformation. Mol Cell 15, 423 435.
21. Kinebuchi T, Kagawa W, Enomoto R, Tanaka K, Miyagawa K, Shibata T, Kurumizaka H Yokoyama S (2004) Structural basis for octameric ring formation and DNA interaction of the human homologous-pairing protein Dmc1. Mol Cell 14, 363 374.
22. Sehorn MG Sung P (2004) Meiotic recombination: an affair of two recombinases. Cell Cycle 3, 1375 1377.
23. Bugreev DV, Golub EI, Stasiak AZ, Stasiak A Mazin AV (2005) Activation of human meiosis-specific recombinase Dmc1 by Ca2+. J Biol Chem 280, 26886 26895.
24. Lee MH, Chang YC, Hong EL, Grubb J, Chang CS, Bishop DK Wang TF (2005) Calcium ion promotes yeast Dmc1 activity via formation of long and fine helical filaments with single-stranded DNA. J Biol Chem 280, 40980 40984.
25. Sigurdsson S, Trujillo K, Song B, Stratton S Sung P (2001) Basis for avid homologous DNA strand exchange by human Rad51 and RPA. J Biol Chem 276, 8798 8806.
26. Liu Y, Stasiak AZ, Masson JY, McIlwraith MJ, Stasiak A West SC (2004) Conformational changes modulate the activity of human RAD51 protein. J Mol Biol 337, 817 827.
27. Shim KS, Schmutte C, Yoder K Fishel R (2006) Defining the salt effect on human RAD51 activities. DNA Repair (Amst) 5, 718 730.
28. Bugreev DV Mazin AV (2004) Ca2+ activates human homologous recombination protein Rad51 by modulating its ATPase activity. Proc Natl Acad Sci USA 101, 9988 9993.
29. Qian X, He Y, Wu Y Luo Y (2006) Asp302 determines potassium dependence of a RadA recombinase from Methanococcus voltae. J Mol Biol 360, 537 547.
30. Wu Y, Qian X, He Y, Moya IA Luo Y (2005) Crystal structure of an ATPase-active form of Rad51 homolog from Methanococcus voltae. Insights into potassium dependence. J Biol Chem 280, 722 728.
31. Qian X, He Y, Ma X, Fodje MN, Grochulski P Luo Y (2006) Calcium stiffens archaeal Rad51 recombinase from Methanococcus voltae for homologous recombination. J Biol Chem 281, 39380 39387.
32. Kant CR, Rao BJ Sainis JK (2005) DNA binding and pairing activity of OsDmc1, a recombinase from rice. Plant Mol Biol 57, 1 11.
33. Rajanikant C, Kumbhakar M, Pal H, Rao BJ Sainis JK (2006) DNA strand exchange activity of rice recombinase OsDmc1 monitored by fluorescence resonance energy transfer and the role of ATP hydrolysis. FEBS J 273, 1497 1506.
34. Sakane I, Kamataki C, Takizawa Y, Nakashima M, Toki S, Ichikawa H, Ikawa S, Shibata T Kurumizaka H (2008) Filament formation and robust strand exchange activities of the rice DMC1A and DMC1B proteins. Nucleic Acids Res 36, 4266 4276.
35. Chen LT, Ko TP, Chang YC, Lin KA, Chang CS, Wang AH Wang TF (2007) Crystal structure of the left-handed archaeal RadA helical filament: identification of a functional motif for controlling quaternary structures and enzymatic functions of RecA family proteins. Nucleic Acids Res 35, 1787 1801.
36. Cox MM (2007) Motoring along with the bacterial RecA protein. Nat Rev Mol Cell Biol 8, 127 138.
37. Hikiba J, Hirota K, Kagawa W, Ikawa S, Kinebuchi T, Sakane I, Takizawa Y, Yokoyama S, Mandon-Pépin B, Nicolas A et al. (2008) Structural and functional analyses of the DMC1-M200V polymorphism found in the human population. Nucleic Acids Res 36, 4181 4190.
38. Hikiba J, Takizawa Y, Ikawa S, Shibata T Kurumizaka H (2009) Biochemical analysis of the human DMC1-I37N polymorphism. FEBS J 276, 457 465.
39. Mandon-Pépin B, Touraine P, Kuttenn F, Derbois C, Rouxel A, Matsuda F, Nicolas A, Cotinot C Fellous M (2008) Genetic investigation of four meiotic genes in women with premature ovarian failure. Eur J Endocrinol 158, 107 115.
40. Qian X, He Y Luo Y (2007) Binding of a second magnesium is required for ATPase activity of RadA from Methanococcus voltae. Biochemistry 46, 5855 5863.
41. Sheridan SD, Yu X, Roth R, Heuser JE, Sehorn MG, Sung P, Egelman EH Bishop DK (2008) A comparative analysis of Dmc1 and Rad51 nucleoprotein filaments. Nucleic Acids Res 36, 4057 4066.
42. Sung P Klein H (2006) Mechanism of homologous recombination: mediators and helicases take on regulatory functions. Nat Rev Mol Cell Biol 7, 739 750.
43. Leu JY, Chua PR Roeder GS (1998) The meiosis-specific Hop2 protein of S. cerevisiae ensures synapsis between homologous chromosomes. Cell 94, 375 386.
44. Chen YK, Leng CH, Olivares H, Lee MH, Chang YC, Kung WM, Ti SC, Lo YH, Wang AH, Chang CS et al. (2004) Heterodimeric complexes of Hop2 and Mnd1 function with Dmc1 to promote meiotic homolog juxtaposition and strand assimilation. Proc Natl Acad Sci USA 101, 10572 10577.
45. Gerton JL DeRisi JL (2002) Mnd1p: an evolutionarily conserved protein required for meiotic recombination. Proc Natl Acad Sci USA 99, 6895 6900.
46. Henry JM, Camahort R, Rice DA, Florens L, Swanson SK, Washburn MP Gerton JL (2006) Mnd1/Hop2 facilitates Dmc1-dependent interhomolog crossover formation in meiosis of budding yeast. Mol Cell Biol 26, 2913 2923.
47. Petukhova GV, Romanienko PJ Camerini-Otero RD (2003) The Hop2 protein has a direct role in promoting interhomolog interactions during mouse meiosis. Dev Cell 5, 927 936.
48. Tsubouchi H Roeder GS (2002) The Mnd1 protein forms a complex with hop2 to promote homologous chromosome pairing and meiotic double-strand break repair. Mol Cell Biol 22, 3078 3088.
49. Zierhut C, Berlinger M, Rupp C, Shinohara A Klein F (2004) Mnd1 is required for meiotic interhomolog repair. Curr Biol 14, 752 762.
50. Pezza RJ, Voloshin ON, Vanevski F Camerini-Otero RD (2007) Hop2/Mnd1 acts on two critical steps in Dmc1-promoted homologous pairing. Genes Dev 21, 1758 1766.
51. Ploquin M, Petukhova GV, Morneau D, Déry U, Bransi A, Stasiak A, Camerini-Otero RD Masson JY (2007) Stimulation of fission yeast and mouse Hop2-Mnd1 of the Dmc1 and Rad51 recombinases. Nucleic Acids Res 35, 2719 2733.
52. Enomoto R, Kinebuchi T, Sato M, Yagi H, Kurumizaka H Yokoyama S (2006) Stimulation of DNA strand exchange by the human TBPIP/Hop2-Mnd1 complex. J Biol Chem 281, 5575 5581. (Pubitemid 43847654)
53. Pezza RJ, Petukhova GV, Ghirlando R Camerini-Otero RD (2006) Molecular activities of meiosis-specific proteins Hop2, Mnd1, and the Hop2-Mnd1 complex. J Biol Chem 281, 18426 18434.
54. Petukhova GV, Pezza RJ, Vanevski F, Ploquin M, Masson JY Camerini-Otero RD (2005) The Hop2 and Mnd1 proteins act in concert with Rad51 and Dmc1 in meiotic recombination. Nat Struct Mol Biol 12, 449 453.
55. Enomoto R, Kinebuchi T, Sato M, Yagi H, Shibata T, Kurumizaka H Yokoyama S (2004) Positive role of the mammalian TBPIP/HOP2 protein in DMC1-mediated homologous pairing. J Biol Chem 279, 35263 35272.
56. Hayase A, Takagi M, Miyazaki T, Oshiumi H, Shinohara M Shinohara A (2004) A protein complex containing Mei5 and Sae3 promotes the assembly of the meiosis-specific RecA homolog Dmc1. Cell 119, 927 940.
57. Tsubouchi H Roeder GS (2004) The budding yeast mei5 and sae3 proteins act together with dmc1 during meiotic recombination. Genetics 168, 1219 1230.
58. Ferrari SR, Grubb J Bishop DK (2009) The Mei5-Sae3 protein complex mediates Dmc1 activity in Saccharomyces cerevisiae. J Biol Chem 284, 11766 11770.
59. Haruta N, Kurokawa Y, Murayama Y, Akamatsu Y, Unzai S, Tsutsui Y Iwasaki H (2006) The Swi5-Sfr1 complex stimulates Rhp51/Rad51-and Dmc1-mediated DNA strand exchange in vitro. Nat Struct Mol Biol 13, 823 830.
60. Petukhova G, Stratton S Sung P (1998) Catalysis of homologous DNA pairing by yeast Rad51 and Rad54 proteins. Nature 393, 91 94.
61. Petukhova G, Sung P Klein H (2000) Promotion of Rad51-dependent D-loop formation by yeast recombination factor Rdh54/Tid1. Genes Dev 14, 2206 2215.
62. Sigurdsson S, Van Komen S, Petukhova G Sung P (2002) Homologous DNA pairing by human recombination factors Rad51 and Rad54. J Biol Chem 277, 42790 42794.
63. Bugreev DV, Mazina OM Mazin AV (2006) Rad54 protein promotes branch migration of Holliday junctions. Nature 442, 590 593.
64. Sarai N, Kagawa W, Kinebuchi T, Kagawa A, Tanaka K, Miyagawa K, Ikawa S, Shibata T, Kurumizaka H Yokoyama S (2006) Stimulation of Dmc1-mediated DNA strand exchange by the human Rad54B protein. Nucleic Acids Res 34, 4429 4437. (Pubitemid 44567042)
65. Wesoly J, Agarwal S, Sigurdsson S, Bussen W, Van Komen S, Qin J, van Steeg H, van Benthem J, Wassenaar E, Baarends WM et al. (2006) Differential contributions of mammalian Rad54 paralogs to recombination, DNA damage repair, and meiosis. Mol Cell Biol 26, 976 989.
66. Pellegrini L, Yu DS, Lo T, Anand S, Lee M, Blundell TL Venkitaraman AR (2002) Insights into DNA recombination from the structure of a RAD51-BRCA2 complex. Nature 420, 287 293.
67. Yang H, Jeffrey PD, Miller J, Kinnucan E, Sun Y, Thoma NH, Zheng N, Chen PL, Lee WH Pavletich NP (2002) BRCA2 function in DNA binding and recombination from a BRCA2-DSS1-ssDNA structure. Science 297, 1837 1848.
68. Thorslund T, Esashi F West SC (2007) Interactions between human BRCA2 protein and the meiosis-specific recombinase DMC1. EMBO J 26, 2915 2922.
69. Wang TF, Chen LT Wang AH (2008) Right or left turn? RecA family protein filaments promote homologous recombination through clockwise axial rotation Bioessays 30, 48 56.
70. DeLano WL (2008) The PyMOL Molecular Graphics System. DeLano Scientific LLC, Palo Alto, CA.