The dual role of HOP2 in mammalian meiotic homologous recombination

Nucleic Acids Research

Volumn 42, Issue 4, 2014, Pages 2346-2357

  Pezza, Roberto J ^a,b   Voloshin, Oleg N ^c   Volodin, Alexander A ^c,d   Boateng, Kingsley A ^c   Bellani, Marina A ^e   Mazin, Alexander V ^f   Camerini Otero, R Daniel ^c  

^a OKLAHOMA MEDICAL RESEARCH FOUNDATION   (United States)

^b UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

^d INSTITUTE OF MOLECULAR GENETICS   (Russian Federation)

^e NATIONAL INSTITUTE ON AGING   (United States)

^f DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; DOUBLE STRANDED DNA; PROTEIN DMC1; PROTEIN HOP2; PROTEIN MND1; RAD51 PROTEIN; SINGLE STRANDED DNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BASE MISPAIRING; CATALYSIS; CELL STIMULATION; CHROMOSOME PAIRING; COMPLEX FORMATION; CONTROLLED STUDY; DNA REPAIR; DOUBLE STRANDED DNA BREAK; EMBRYO; EMBRYONIC STEM CELL; GENE DELETION; HOLLIDAY JUNCTION; HOMOLOGOUS RECOMBINATION; IN VITRO STUDY; MALE; MEIOSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DNA BINDING; PROTEIN FUNCTION; SPERMATOCYTE;

ANIMALS; CELL CYCLE PROTEINS; CELL LINE; CHROMOSOME PAIRING; DNA BREAKS, DOUBLE-STRANDED; DNA HELICASES; MEIOSIS; MICE; NUCLEAR PROTEINS; RECOMBINASES; RECOMBINATIONAL DNA REPAIR;

EID: 84895802706     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt1234     Document Type: Article

References (59)

1. San Filippo, J., Sung, P. and Klein, H. (2008) Mechanism of eukaryotic homologous recombination. Annu. Rev. Biochem., 77, 229-257.
2. Haber, J.E. (2000) Partners and pathwaysrepairing a double-strand break. Trends Genet., 16, 259-264.
3. Kleckner, N. (1996) Meiosis: how could it work? Proc. Natl Acad. Sci. USA, 93, 8167-8174.
4. Roeder, G.S. (1997) Meiotic chromosomes: it takes two to tango. Genes Dev., 11, 2600-2621.
5. Hassold, T.J. and Jacobs, P.A. (1984) Trisomy in man. Annu. Rev. Genet., 18, 69-97.
6. Neale, M.J. and Keeney, S. (2006) Clarifying the mechanics of DNA strand exchange in meiotic recombination. Nature, 442, 153-158.
7. Allers, T. and Lichten, M. (2001) Differential timing and control of noncrossover and crossover recombination during meiosis. Cell, 106, 47-57.
8. Hunter, N. and Kleckner, N. (2001) The single-end invasion: an asymmetric intermediate at the double-strand break to double-holliday junction transition of meiotic recombination. Cell, 106, 59-70.
9. Rattray, A.J. and Symington, L.S. (1995) Multiple pathways for homologous recombination in Saccharomyces cerevisiae. Genetics, 139, 45-56.
10. Cromie, G.A., Hyppa, R.W., Taylor, A.F., Zakharyevich, K., Hunter, N. and Smith, G.R. (2006) Single Holliday junctions are intermediates of meiotic recombination. Cell, 127, 1167-1178.
11. Schwacha, A. and Kleckner, N. (1994) Identification of joint molecules that form frequently between homologs but rarely between sister chromatids during yeast meiosis. Cell, 76, 51-63.
12. Zierhut, C., Berlinger, M., Rupp, C., Shinohara, A. and Klein, F. (2004) Mnd1 is required for meiotic interhomolog repair. Curr. Biol., 14, 752-762.
13. Henry, J.M., Camahort, R., Rice, D.A., Florens, L., Swanson, S.K., Washburn, M.P. and Gerton, J.L. (2006) Mnd1/Hop2 facilitates Dmc1-dependent interhomolog crossover formation in meiosis of budding yeast. Mol. Cell. Biol., 26, 2913-2923.
14. Chen, Y.K., Leng, C.H., Olivares, H., Lee, M.H., Chang, Y.C., Kung, W.M., Ti, S.C., Lo, Y.H., Wang, A.H., Chang, C.S. 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.
15. Leu, J.Y., Chua, P.R. and Roeder, G.S. (1998) The meiosis-specific Hop2 protein of S. cerevisiae ensures synapsis between homologous chromosomes. Cell, 94, 375-386.
16. Tsubouchi, H. and Roeder, G.S. (2003) The importance of genetic recombination for fidelity of chromosome pairing in meiosis. Dev. Cell, 5, 915-925.
17. Petukhova, G.V., Romanienko, P.J. and Camerini-Otero, R.D. (2003) The Hop2 protein has a direct role in promoting interhomolog interactions during mouse meiosis. Dev. Cell, 5, 927-936.
18. Petukhova, G.V., Pezza, R.J., Vanevski, F., Ploquin, M., Masson, J.Y. and Camerini-Otero, R.D. (2005) The Hop2 and Mnd1 proteins act in concert with Rad51 and Dmc1 in meiotic recombination. Nat. Struct. Mol. Biol., 12, 449-453.
19. Bannister, L.A., Pezza, R.J., Donaldson, J.R., de Rooij, D.G., Schimenti, K.J., Camerini-Otero, R.D. and Schimenti, J.C. (2007) A dominant, recombination-defective allele of Dmc1 causing male-specific sterility. PLoS Biol., 5, e105.
20. Pezza, R.J., Petukhova, G.V., Ghirlando, R. and Camerini-Otero, R.D. (2006) Molecular activities of meiosis-specific proteins Hop2, Mnd1, and the Hop2-Mnd1 complex. J. Biol. Chem., 281, 18426-18434.
21. Pezza, R.J., Voloshin, O.N., Vanevski, F. and Camerini-Otero, R.D. (2007) Hop2/Mnd1 acts on two critical steps in Dmc1-promoted homologous pairing. Genes Dev., 21, 1758-1766.
22. Pezza, R.J., Camerini-Otero, R.D. and Bianco, P.R. (2010) Hop2-Mnd1 condenses DNA to stimulate the synapsis phase of DNA strand exchange. Biophys J, 99, 3763-3772.
23. Chi, P., San Filippo, J., Sehorn, M.G., Petukhova, G.V. and Sung, P. (2007) Bipartite stimulatory action of the Hop2-Mnd1 complex on the Rad51 recombinase. Genes Dev., 21, 1747-1757.
24. Peters, A.H., Plug, A.W., van Vugt, M.J. and de Boer, P. (1997) A drying-down technique for the spreading of mammalian meiocytes from the male and female germline. Chromosome Res., 5, 66-68.
25. Masson, J.Y., Davies, A.A., Hajibagheri, N., Van Dyck, E., Benson, F.E., Stasiak, A.Z., Stasiak, A. and West, S.C. (1999) The meiosis-specific recombinase hDmc1 forms ring structures and interacts with hRad51. EMBO J., 18, 6552-6560.
26. Mazina, O.M. and Mazin, A.V. (2004) Human Rad54 protein stimulates DNA strand exchange activity of hRad51 protein in the presence of Ca2+. J. Biol. Chem., 279, 52042-52051.
27. Voloshin, O.N., Wang, L. and Camerini-Otero, R.D. (2000) The homologous pairing domain of RecA also mediates the allosteric regulation of DNA binding and ATP hydrolysis: a remarkable concentration of functional residues. J. Mol. Biol., 303, 709-720.
28. Noirot, P., Gupta, R.C., Radding, C.M. and Kolodner, R.D. (2003) Hallmarks of homology recognition by RecA-like recombinases are exhibited by the unrelated Escherichia coli RecT protein. EMBO J., 22, 324-334.
29. Gupta, R.C., Folta-Stogniew, E., O'Malley, S., Takahashi, M. and Radding, C.M. (1999) Rapid exchange of A:T base pairs is essential for recognition of DNA homology by human Rad51 recombination protein. Mol. Cell, 4, 705-714.
30. Gupta, R.C., Golub, E., Bi, B. and Radding, C.M. (2001) The synaptic activity of HsDmc1, a human recombination protein specific to meiosis. Proc. Natl Acad. Sci. USA, 98, 8433-8439.
31. Bugreev, D.V., Pezza, R.J., Mazina, O.M., Voloshin, O.N., Camerini-Otero, R.D. and Mazin, A.V. (2011) The resistance of DMC1 D-loops to dissociation may account for the DMC1 requirement in meiosis. Nat. Struct. Mol. Biol., 18, 56-60.
32. Volodin, A.A., Bocharova, T.N., Smirnova, E.A. and Camerini-Otero, R.D. (2009) Reversibility, equilibration, and fidelity of strand exchange reaction between short oligonucleotides promoted by RecA protein from escherichia coli and human Rad51 and Dmc1 proteins. J. Biol. Chem., 284, 1495-1504.
33. Petronczki, M., Siomos, M.F. and Nasmyth, K. (2003) Un menage a quatre: the molecular biology of chromosome segregation in meiosis. Cell, 112, 423-440.
34. Zickler, D. and Kleckner, N. (1999) Meiotic chromosomes: integrating structure and function. Annu. Rev. Genet., 33, 603-754.
35. Voloshin, O.N., Wang, L. and Camerini-Otero, R.D. (1996) Homologous DNA pairing promoted by a 20-amino acid peptide derived from RecA. Science, 272, 868-872.
36. Camerini-Otero, R.D. and Hsieh, P. (1995) Homologous recombination proteins in prokaryotes and eukaryotes. Annu. Rev. Genet., 29, 509-552.
37. Ogawa, T., Yu, X., Shinohara, A. and Egelman, E.H. (1993) Similarity of the yeast RAD51 filament to the bacterial RecA filament. Science, 259, 1896-1899.
38. Hsieh, P., Camerini-Otero, C.S. and Camerini-Otero, R.D. (1992) The synapsis event in the homologous pairing of DNAs: RecA recognizes and pairs less than one helical repeat of DNA. Proc. Natl Acad. Sci. USA, 89, 6492-6496.
39. Folta-Stogniew, E., O'Malley, S., Gupta, R., Anderson, K.S. and Radding, C.M. (2004) Exchange of DNA base pairs that coincides with recognition of homology promoted by E. coli RecA protein. Mol. Cell, 15, 965-975.
40. Bazemore, L.R., Folta-Stogniew, E., Takahashi, M. and Radding, C.M. (1997) RecA tests homology at both pairing and strand exchange. Proc. Natl Acad. Sci. USA, 94, 11863-11868.
41. Sagi, D., Tlusty, T. and Stavans, J. (2006) High fidelity of RecA-catalyzed recombination: a watchdog of genetic diversity. Nucleic Acids Res., 34, 5021-5031.
42. Rabitsch, K.P., Toth, A., Galova, M., Schleiffer, A., Schaffner, G., Aigner, E., Rupp, C., Penkner, A.M., Moreno-Borchart, A.C., Primig, M. et al. (2001) A screen for genes required for meiosis and spore formation based on whole-genome expression. Curr. Biol., 11, 1001-1009.
43. Gerton, J.L. and DeRisi, J.L. (2002) Mnd1p: an evolutionarily conserved protein required for meiotic recombination. Proc. Natl Acad. Sci. USA, 99, 6895-6900.
44. Tsubouchi, H. and Roeder, G.S. (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.
45. Saito, T.T., Tougan, T., Kasama, T., Okuzaki, D. and Nojima, H. (2004) Mcp7, a meiosis-specific coiled-coil protein of fission yeast, associates with Meu13 and is required for meiotic recombination. Nucleic Acids Res., 32, 3325-3339.
46. Kerzendorfer, C., Vignard, J., Pedrosa-Harand, A., Siwiec, T., Akimcheva, S., Jolivet, S., Sablowski, R., Armstrong, S., Schweizer, D., Mercier, R. et al. (2006) The Arabidopsis thaliana MND1 homologue plays a key role in meiotic homologous pairing, synapsis and recombination. J. Cell Sci., 119, 2486-2496.
47. Panoli, A.P., Ravi, M., Sebastian, J., Nishal, B., Reddy, T.V., Marimuthu, M.P., Subbiah, V., Vijaybhaskar, V. and Siddiqi, I. (2006) AtMND1 is required for homologous pairing during meiosis in Arabidopsis. BMC Mol. Biol., 7, 24.
48. Domenichini, S., Raynaud, C., Ni, D.A., Henry, Y. and Bergounioux, C. (2006) Atmnd1-delta1 is sensitive to gamma-irradiation and defective in meiotic DNA repair. DNA Repair (Amst), 5, 455-464.
49. Enomoto, R., Kinebuchi, T., Sato, M., Yagi, H., Kurumizaka, H. and Yokoyama, S. (2006) Stimulation of DNA strand exchange by the human TBPIP/Hop2-Mnd1 complex. J. Biol. Chem., 281, 5575-5581.
50. Schommer, C., Beven, A., Lawrenson, T., Shaw, P. and Sablowski, R. (2003) AHP2 is required for bivalent formation and for segregation of homologous chromosomes in Arabidopsis meiosis. Plant J., 36, 1-11.
51. Bianco, P.R., Tracy, R.B. and Kowalczykowski, S.C. (1998) DNA strand exchange proteins: a biochemical and physical comparison. Front. Biosci., 3, D570-D603.
52. Cox, M.M. (2003) The bacterial RecA protein as a motor protein. Annu. Rev. Microbiol., 57, 551-577.
53. Passy, S.I., Yu, X., Li, Z., Radding, C.M. and Egelman, E.H. (1999) Rings and filaments of beta protein from bacteriophage lambda suggest a superfamily of recombination proteins. Proc. Natl Acad. Sci. USA, 96, 4279-4284.
54. Kagawa, W., Kurumizaka, H., Ikawa, S., Yokoyama, S. and Shibata, T. (2001) Homologous pairing promoted by the human Rad52 protein. J. Biol. Chem., 276, 35201-35208.
55. Menetski, J.P., Bear, D.G. and Kowalczykowski, S.C. (1990) Stable DNA heteroduplex formation catalyzed by the Escherichia coli RecA protein in the absence of ATP hydrolysis. Proc. Natl Acad. Sci. USA, 87, 21-25.
56. Rosselli, W. and Stasiak, A. (1990) Energetics of RecA-mediated recombination reactions: without ATP hydrolysis RecA can mediate polar strand exchange but is unable to recycle. J. Mol. Biol., 216, 335-352.
57. Sung, P. and Stratton, S.A. (1996) Yeast Rad51 recombinase mediates polar DNA strand exchange in the absence of ATP hydrolysis. J. Biol. Chem., 271, 27983-27986.
58. Hong, E.L., Shinohara, A. and Bishop, D.K. (2001) Saccharomyces cerevisiae Dmc1 protein promotes renaturation of single-strand DNA (ssDNA) and assimilation of ssDNA into homologous super-coiled duplex DNA. J. Biol. Chem., 276, 41906-41912.
59. Turner, J.M., Mahadevaiah, S.K., Fernandez-Capetillo, O., Nussenzweig, A., Xu, X., Deng, C.X. and Burgoyne, P.S. (2005) Silencing of unsynapsed meiotic chromosomes in the mouse. Nat. Genet., 37, 41-47.