RAD51 and DMC1 form mixed complexes associated with mouse meiotic chromosome cores and synaptonemal complexes

Journal of Cell Biology

Volumn 147, Issue 2, 1999, Pages 207-219

  Tarsounas, Madalena ^a,c   Morita, Takashi ^b   Pearlman, Ronald E ^a   Moens, Peter B ^a  

^a YORK UNIVERSITY   (Canada)

^b OSAKA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

Author keywords

DMC1; Genetic recombination; Meiosis; RAD51; Synaptonemal complex

Indexed keywords

RECA PROTEIN; RECOMBINASE;

ANIMAL CELL; ARTICLE; CHROMOSOME; COMPLEX FORMATION; CONTROLLED STUDY; GENETIC RECOMBINATION; MEIOSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROPHASE; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SPERMATOCYTE; SYNAPTONEMAL COMPLEX;

ADENOSINE TRIPHOSPHATASES; ANIMALS; CELL CYCLE PROTEINS; DNA-BINDING PROTEINS; IMMUNOHISTOCHEMISTRY; MALE; MEIOSIS; MICE; NUCLEAR PROTEINS; RAD51 RECOMBINASE; RECOMBINATION, GENETIC; SPERMATOCYTES;

ANIMALIA; EUKARYOTA;

EID: 0032699673     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.147.2.207     Document Type: Article

References (79)

1. Albini, S.M., and G.H. Jones. 1987. Synaptonemal complex spreading in Allium cepa and A. fistulosum. The initiation and sequence of pairing. Chromosoma. 95:324-338.
2. Anderson, L.K., and S.M. Stack. 1988. Nodules associated with axial cores and synaptonemal complexes during zygotene in Psilotum nudum. Chromosoma. 97:96-100.
3. Anderson, L.K., H.H. Offenberg, W.H.H.C. Verkuijlen, and C. Heyting. 1997. RecA-like proteins are components of the early meiotic nodules in lily. Proc. Natl. Acad. Sci. USA. 94:6868-6873.
4. Baker, S.M., A.W. Plug, T.A. Prolla, C.E. Bronner, A.C. Harris, X. Yao, D.M. Christie, C. Monell, N. Arnheim, A. Bradley, T. Ashley, and R.M. Liskay. 1996. Involvement of mouse MLH1 in DNA mismatch repair and meiotic crossing over. Nat. Genet. 13:336-342.
5. Barlow, C., S. Hirotsune, R. Paylor, M. Liyanage, M. Eckhaus, F. Collins, Y. Shiloh, J.N. Crawley, T. Ried, D. Tagle, and A. Wynshaw-Boris. 1996. Atm-deficient mice: a paradigm of ataxia telangiectasia. Cell. 86:159-171.
6. Barlow, A.L., F.E. Benson, S.C. West, and M.A. Hulten. 1997a. Distribution of the Rad51 recombinase in human and mouse spermatocytes. EMBO (Eur. Mol. Biol. Organ.) J. 16:5207-5215.
7. Barlow, C., M. Liyanage, P.B. Moens, C.X. Deng, T. Ried, and A. Wynshaw-Boris. 1997b. Partial rescue of the prophase I defects of Atm-deficient mice by p53 and p21 null alleles. Nat. Genet. 17:462-466.
8. Barlow, C., M. Liyanage, P.B. Moens, M. Tarsounas, K. Nagashima, K. Brown, S. Rottinghaus, S.P. Jackson, D. Tagle, T. Ried, and A. Wynshaw-Boris. 1998. Atm deficiency results in severe meiotic disruption as early as leptonema of prophase I. Development. 125:4007-4017.
9. Baumann, P., and S.C. West. 1997. The human Rad51 protein: polarity of strand transfer and stimulation by hRP-A. EMBO (Eur. Mol. Biol. Organ.) J. 16:5198-5206.
10. Baumann, P., and S.C. West. 1998. Role of the human RAD51 protein in homologous recombination and double-stranded-break repair. Trends Biochem. Sci. 23:247-251.
11. Baumann, P., F.E. Benson, and S.C. West. 1996. Human Rad51 protein promotes ATP-dependent homologous pairing and strand transfer reactions in vitro. Cell. 87:757-766.
12. Benson, F.E., A. Stasiak, and S.C. West. 1994. Purification and characterization of the human Rad51 protein, an analogue of E. coli RecA. EMBO (Eur. Mol. Biol. Organ.) J. 13:5764-5771.
13. Bishop, D.K. 1994. RecA homologs Dmcl and Rad51 interact to form multiple nuclear complexes prior to meiotic chromosome synapsis. Cell. 79:1081-1092.
14. Bishop, D.K., D. Park, L. Xu, and N. Kleckner. 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.
15. Bishop, D.K., U. Ear, A. Bhattacharyya, C. Calderone, M. Beckett, R.R. Weichselbaum, and A. Shinohara. 1998. Xrcc3 is required for assembly of Rad51 complexes in vivo. J. Biol. Chem. 273:21482-21488.
16. Chen, J., D.P. Silver, D. Walpita, S.B. Cantor, A.F. Gazdar, G. Tomlinson, F.J. Couch, B.L. Weber, T. Ashley, D.M. Livingston, and R. Scully. 1998. Stable interaction between the products of the BRCA1 and BRCA2 tumor suppressor genes in mitotic and meiotic cells. Mol. Cell. 2:317-328.
17. Critchlow, S.E., and S.P. Jackson. 1998. DNA end-joining: from yeast to man. Trends Biochem. Sci. 23:394-398.
18. Dobson, M.J., R.E. Pearlman, A. Karaiskakis, B. Spyropoulos, and P.B. Moens. 1994. Synaptonemal complex proteins: occurrence, epitope mapping and chromosome disjunction. J. Cell Sci. 107:2749-2760.
19. Donovan, J.W., G.T. Milne, and D.T. Weaver. 1994. Homotypic and heterotypic protein associations control Rad51 function in double-strand break repair. Genes Dev. 8:2552-2562.
20. Dresser, M.E., D.J. Ewing, M.N. Conrad, A.M. Dominguez, R. Barstead, H. Jiang, and T. Kodadek. 1997. DMC1 functions in a Saccharomyces cerevisiae meiotic pathway that is largely independent of the RAD51 pathway. Genetics. 147:533-544.
21. Freire, R., J.R. Murguia, M. Tarsounas, N.F. Lowndes, P.B. Moens, and S.P. Jackson. 1998. Human and mouse homologs of Schizosaccharomyces pombe rad1(+) and Saccharomyces cerevisiae RAD17: linkage to checkpoint control and mammalian meiosis. Genes Dev. 12:2560-2573.
22. Gasior, S.L., A.K. Wong, Y. Kora, A. Shinohara, and D.K. Bishop. 1998. Rad52 associates with RPA and functions with rad55 and rad57 to assemble meiotic recombination complexes. Genes Dev. 12:2208-2221.
23. Grabske, R.J., S. Lake, B.L. Gledhill, and M.L. Meistrich. 1975. Centrifugal elutriation: separation of spermatogenic cells on the basis of sedimentation velocity. J. Cell. Physiol. 86:177-190.
24. Haber, J.E. 1998. The many interfaces of Mre11. Cell. 95:583-586.
25. Habu, T., T. Taki, A. West, Y. Nishimune, and T. Morita. 1996. 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. Nucleic Acids Res. 24:470-477.
26. Heng, H.H., L.C. Tsui, and P.B. Moens. 1994. Organization of heterologous DNA inserts on the mouse meiotic chromosome cores. Chromosoma. 103: 401-407.
27. Heyting, C., A.J.J. Dietrich, E.J.W. Redeker, and A.C.G. Vink. 1985. Structure and composition of synaptonemal complexes isolated from rat spermatocytes. Eur. J. Cell Biol. 36:307-314.
28. Keegan, K.S., D.A. Holtzman, A.W. Plug, E.R. Christenson, E.E. Brainerd, G. Flaggs, N.J. Bentley, E.M. Taylor, M.S. Meyn, S.B. Moss, et al. 1996. The Atr and Atm protein kinases associate with different sites along meiotically pairing chromosomes. Genes Dev. 10:2423-2437.
29. Kleckner, N. 1996. Meiosis: how could it work? Proc. Natl. Acad. Sci. USA. 93: 8167-8174.
30. Kobayashi, T., Y. Hotta, and S. Tabata. 1993. Isolation and characterization of a yeast gene that is homologous with a meiosis-specific cDNA from a plant. Mol. Gen. Genet. 237:225-232.
31. Kovalenko, O.V., A.W. Plug, T. Haaf, D.K. Gonda, T. Ashley, D.C. Ward, C.M. Radding, and E.I. Golub. 1996. Mammalian ubiquitin-conjugating enzyme Ubc9 interacts with Rad51 recombination protein and localizes in synaptonemal complexes. Proc. Nail. Acad. Sci. USA. 93:2958-2963.
32. Kovalenko, O.V., E.I. Golub, P. Bray-Ward, D.C. Ward, and C.M. Radding. 1997. A novel nucleic acid-binding protein that interacts with human RAD51 recombinase. Nucleic Acids Res. 25:4946-4953.
33. Laemmli, U.K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:680-685.
34. Lammers, J.H.M., H.H. Offenberg, M. van Aalderen, A.C.G. Vink, A.J.J. Dietrich, and C. Heyting. 1994. The gene encoding a major component of the lateral elements of synaptonemal complexes of the rat is related to x-linked lymphocyte-regulated genes. Mol. Cell Biol. 14:1137-1146.
35. Lammers, J.H., M. van Aalderen, A.H. Peters, A.A. van Pelt, D.G. de Rooij, P. de Boer, H.H. Offenberg, AJ. Dietrich, and C. Heyting. 1995. A change in the phosphorylation pattern of the 30,000-33,000 Mr synaptonemal complex proteins of the rat between early and mid-pachytene. Chromosoma. 104: 154-163.
36. Li, Z., E.I. Golub, R. Gupta, and C.M. Radding. 1997. Recombination activities of HsDmcl protein, the meiotic human homolog of RecA protein. Proc. Natl. Acad. Sci. USA. 94:11221-11226.
37. Lim, D.S., and P. Hasty. 1996. A mutation in mouse RAD51 results in an early embryonic lethal that is suppressed by a mutation in p53. Mol. Cell. Biol. 16: 7133-7143.
38. 2 terminus of SCP1 to the central element of the synaptonemal complex and evidence for direct interactions between the N-termini of SCP1 molecules organized head-to-head. Exp. Cell Res. 226:11-19.
39. Meistrich, M.L. 1977. Separation of spermatogenic cells and nuclei from rodent testes. Methods Cell Biol. 15:15-54.
40. Meuwissen, R.L.J., H.H. Offenberg, A.J.J. Dietrich, A. Riesewijk, M. van lersel, and C. Heyting. 1992. A coiled-coil related protein specific for synapsed regions of meiotic prophase chromosomes. EMBO (Eur. Mol. Biol. Organ.) J. 11:5091-5100.
41. Moens, P.B. 1969. The fine structure of meiotic chromosome polarization and pairing in Locusta migratoria spermatocytes. Chromosoma. 28:1-25.
42. Moens, P.B., D.J. Chen, Z. Shen, N. Kolas, M. Tarsounas, H. Heng, and B. Spyropoulos. 1997. Rad51 immunocytology in rat and mouse spermatocytes and oocytes. Chromosoma. 106:207-215.
43. Morita, T., Y. Yoshimura, A. Yamamoto, K. Murata, M. Mori, H. Yamamoto, and A.A. Matsushiro. 1993. A mouse homolog of the Escherichia coli recA and Saccharomyces cerevisiae RAD51 genes. Proc. Natl. Acad. Sci. USA. 90: 6577-6580.
44. Offenberg, H.H., J.A. Schalk, R.L. Meuwissen, M. van Aalderen, H.A. Kester, A.J. Dietrich, and C. Heyting. 1998. SCP2: a major protein component of the axial elements of synaptonemal complexes of the rat. Nucleic Acids Res. 26: 2572-2579.
45. Nairz, K., and F. Klein. 1997. mre11S - a yeast mutation that blocks double-strand-break processing and permits nonhomologous synapsis in meiosis. Genes Dev. 11:2272-2290.
46. Pittman, D.L., J. Cobb, K.L. Schimenti, L.A. Wilson, D.M. Cooper, E. Brignull, M.A. Handel, and J.C. Schimenti. 1998. Meiotic prophase arrest with failure of chromosome synapsis in mice deficient for Dmc1, a germline-specific RecA homolog. Mol. Cell. 1:697-705.
47. Raderschall, E., E.I. Golub. and T. Haaf. 1999. Nuclear foci of mammalian recombination proteins are located at single-stranded DNA regions formed after DNA damage. Proc. Natl. Acad. Sci. USA. 96:1921-1926.
48. Rockmill, B., and G.S. Roeder. 1990. Meiosis in asynaptic yeast. Genetics. 126: 563-574.
49. Rockmill, B., and G.S. Roeder. 1994. The yeast med1 mutant undergoes both meiotic homolog non-disjunction and precocious separation of sister chromatids. Genetics. 136:65-74.
50. Rockmill, B., M. Sym, H. Scherthan, and G.S. Roeder. 1995. Roles for two RecA homologs in promoting meiotic chromosome synapsis. Genes Dev. 9:2684-2695.
51. Roeder, S. 1997. Meiotic chromosomes: it takes two to tango. Genes Dev. 11: 2600-2621.
52. Schmekel, K., R.L.J. Meuwissen, A.J.J. Dietrich, A.C.G. Vink, J. van Marie, H. van Veen, and C. Heyting. 1996. Organization of SCP1 protein molecules within synaptonemal complexes of the rat. Exp. Cell Res. 226:20-30.
53. Schwacha, A., and N. Kleckner. 1997. Interhomolog bias during meiotic recombination: meiotic functions promote a highly differentiated interhomolog-only pathway. Cell. 90:1123-1135.
54. Scully, R., J. Chen, A. Plug, Y. Xiao, D. Weaver, J. Feunteun, T. Ashley, and D.M. Livingston. 1997. Association of BRCA1 with Rad51 in mitotic and meiotic cells. Cell. 88:265-275.
55. Shinohara, A., and T. Ogawa. 1995. Homologous recombination and the roles of double-strand breaks. Trends Biochem. Svi. 20:387-391.
56. Shinohara, A., H. Ogawa, and T. Ogawa. 1992. Rad51 protein involved in repair and recombination in S. cerevisiae is a RecA-like protein. Cell. 69:457-470.
57. Shinohara, A., S. Gasior, T. Ogawa, N. Kleckner, and D.K. Bishop. 1997. Saccharomyces cerevisiae recA homologues RAD51 and DMC1 have both distinct and overlapping roles in meiotic recombination. Genes Cells. 2:615-629.
58. Smith, A.V., and G.S. Roeder. 1997. The yeast Red1 protein localizes to the cores of meiotic chromosomes. J. Cell Biol. 136:957-967.
59. Stack, S.M. 1984. Heterochromatin, the synaptonemal complex and crossing over. J. Cell Sci. 71:159-176.
60. Storlazzi, A., L. Xu, A. Schwacha, and N. Kleckner. 1996. Synaptonemal complex (SC) component Zip1 plays a role in meiotic recombination indepen-dent of SC polymerization along the chromosomes. Proc. Natl. Acad. Sci. USA. 93:9043-9048.
61. Story, R.M., D.K. Bishop, N. Kleckner, and T.A. Steitz. 1993. Structural relationship of bacterial RecA proteins to recombination proteins from bacteriophage T4 and yeast. Science. 259:1892-1896.
62. Sung, P., and D.L. Robberson. 1995. DNA strand exchange mediated by a RAD51-ssDNA nucleoprotein filament with polarity opposite to that of RecA. Cell. 82:453-461.
63. Sym, M., and G.S. Roeder. 1994. Crossover interference is abolished in the absence of a synaptonemal complex protein. Cell. 79:283-292.
64. Sym, M., and G.S. Roeder. 1995. Zip1-induced changes in synaptonemal complex structure and polycomplex assembly. J. Cell Biol. 128:455-466.
65. Sym, M., J.A. Engebrecht, and G.S. Roeder. 1993. ZIP1 is a synaptonemal complex protein required for meiotic chromosome synapsis. Cell. 72:365-378.
66. Szostak, J.W., T.L. Orr-Weaver, R.J. Rothstein, and F.W. Stahl. 1983. The double-strand-break repair model for recombination. Cell. 33:25-35.
67. Tarsounas, M., R.E. Pearlman, P.J. Gasser, M.S. Park, and P.B. Moens. 1997. Protein-protein interactions in the synaptonemal complex. Mol. Biol. Cell. 8:1405-1414.
68. Tarsounas, M., R.E. Pearlman, and P.B. Moens. 1999. Meiotic activation of rat pachytene spermatocytes with okadaic acid: the behaviour of synaptonemal complex components SYN1/SCP1 and COR1/SCP3. J. Cell Sci. 112:423-434.
69. Terasawa, M., A. Shinohara, Y. Hotta, H. Ogawa, and T. Ogawa. 1995. Localization of RecA-like recombination proteins on chromosomes of the lily at various meiotic stages. Genes Dev. 9:925-934.
70. Tsuzuki, T., Y. Fujii, K. Sakumi, Y. Tominaga, K. Nakao, M. Sekiguchi, A. Matsushiro, Y. Yoshimura, and T. Morita. 1996. Targeted disruption of the Rad51 gene leads to lethality in embryonic mice. Proc. Natl. Acad. Sci. USA. 93:6236-6240.
71. Tung, K.S., and G.S. Roeder. 1998. Meiotic chromosome morphology and behaviour in zip1 mutants of Saccharomyces cerevisiae. Genetics. 149:817-832.
72. von Wettstein, D., S.W. Rasmussen, and P.B. Holm. 1984. The synaptonemal complex in genetic segregation. Annu. Rev. Genet. 18:331-413.
73. West, S.C. 1992. Enzymes and molecular mechanisms of genetic recombination. Annu. Rev. Biochem. 61:603-640.
74. Yoshida, K., G. Kondoh, Y. Matsuda, T. Habu, Y. Nishimune, and T. Morita. 1998. The mouse RecA-like gene Dmc1 is required for homologous chromosome synapsis during meiosis. Mol. Cell. 1:707-718.
75. Yoshimura, Y., T. Morita, A. Yamamoto, and A. Matsushiro. 1993. Cloning and sequence of the human RecA-like gene cDNA. Nucleic Acids Res. 21: 1665-1669.
76. Yuan, L., J. Pelttari, E. Brundell, B. Bjorkroth, J. Zhao, J.G. Liu, H. Brismar, B. Daneholt, and C. Hoog. 1998. The synaptonemal complex protein SCP3 can form multistranded, cross-striated fibers in vivo. J. Cell Biol. 142:331-339.
77. Xu, Y., T. Ashley, E.E. Brainerd, R.T. Bronson, M.S. Meyn, and D. Baltimore. 1996. Targeted disruption of ATM leads to growth retardation, chromosomal fragmentation during meiosis, immune defects, and thymic lymphoma. Genes Dev. 10:2411-2422.
78. Zickler, D. 1973. Fine structure of chromosome pairing in ten Ascomycetes. Meiotic and premeiotic (mitotic) synaptonemal complexes. Chromosoma. 40:401-416.
79. Zickler, D., P.J. Moreau, A.D. Huynh, and A.M. Slezec. 1992. Correlation between pairing initiation sites, recombination nodules and meiotic recombination in Sordaria macrospora. Genetics. 132:135-48.