The management of DNA double-strand breaks in mitotic G2, and in mammalian meiosis viewed from a mitotic G2 perspective

BioEssays

Volumn 29, Issue 10, 2007, Pages 974-986

  Burgoyne, Paul S ^a   Mahadevaiah, Shantha K ^a   Turner, James M A ^a  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; ATR PROTEIN; CHECKPOINT KINASE 1; CYCLIN DEPENDENT KINASE; CYCLINE; DOUBLE STRANDED DNA; NIBRIN; PHOSPHATASE; PHOSPHATIDYLINOSITOL 3 KINASE; REPLICATION FACTOR C; SERINE; SINGLE STRANDED DNA; THREONINE; TRANSCRIPTION FACTOR ETV6;

BINDING SITE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL DIVISION; DNA REPAIR; DNA REPLICATION; DNA STRAND BREAKAGE; ENZYME ACTIVITY; EUKARYOTIC CELL; GENOME; HOMOLOGOUS RECOMBINATION; MEIOSIS; MITOSIS; NONHUMAN; PACHYTENE; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; REVIEW; SIGNAL TRANSDUCTION; SPERMATOCYTE;

ANIMALS; CELL CYCLE PROTEINS; DNA DAMAGE; DNA REPAIR; DNA-BINDING PROTEINS; G2 PHASE; MAMMALS; MEIOSIS; MITOSIS; MODELS, GENETIC; PROTEIN-SERINE-THREONINE KINASES; TUMOR SUPPRESSOR PROTEINS;

EUKARYOTA; MAMMALIA;

EID: 34948871524     PISSN: 02659247     EISSN: None     Source Type: Journal    
DOI: 10.1002/bies.20639     Document Type: Review

References (120)

1. O'Connell MJ, Cimprich KA. 2005. G2 damage checkpoints: what is the turn-on? J Cell Sci 118:1-6.
2. Gerton JL, Hawley RS. 2005. Homologous chromosome interactions in meiosis: diversity amidst conservation. Nat Rev Genet 6:477-487.
3. Marcon E, Moens PB. 2005. The evolution of meiosis: recruitment and modification of somatic DNA-repair proteins. Bioessays 27:795-808.
4. Weinert TA, Hartwell LH. 1988. The RAD9 gene controls the cell cycle response to DNA damage in Saccharomyces cerevisiae. Science 241:317-322.
5. Zhou BS, Eledge SJ. 2000. The DNA damage response: putting checkpoints in perspective. Nature 408:433-439.
6. Traven A, Heierhorst J. 2005. SQ/TQ cluster domains: concentrated ATM/ATR kinase phosphorylation site regions in DNA-damage-response proteins. Bioessays 27:397-407.
7. Jazayeri A, Falck J, Lukas C, Bartek J, Smith GC, et al. 2006. ATM- and cell cycle-dependent regulation of ATR in response to DNA double-strand breaks. Nat Cell Biol 8:37-45.
8. Nakada D, Hirano Y, Sugimoto K. 2004. Requirement of the Mre11 complex and exonuclease 1 for activation of the Med signaling pathway. Mol Cell Biol 24:10016-10025.
9. Grenon M, Gilbert C, Lowndes NF. 2001. Checkpoint activation in response to double-strand breaks requires the Mre11/Rad50/Xrs2 complex. Nat Cell Biol 3:844-847.
10. Shroff R, Arbel-Eden A, Pilch D, Ira G, Bonner WM, et al. 2004. Distribution and dynamics of chromatin modification induced by a defined DNA double-strand break. Curr Biol 14:1703-1711.
11. Bhaskara V, Dupre A, Lengsfeld B, Hopkins BB, Chan A, et al. 2007. Rad50 adenylate kinase activity regulates DNA tethering by Mre11/Rad50 complexes. Mol Cell 25:647-661.
12. Nakada D, Matsumoto K, Sugimoto K. 2003. ATM-related Tel1 associates with double-strand breaks through an Xrs2-dependent mechanism. Genes Dev 17:1957-1962.
13. Falck J, Coates J, Jackson SP. 2005. Conserved modes of recruitment of ATM, ATR and DNA-PKcs to sites of DNA damage. Nature 434:605-611.
14. Pellegrini M, Celeste A, Difilippantonio S, Guo R, Wang W, et al. 2006. Autophosphorylation at serine 1987 is dispensable for murine Atm activation in vivo. Nature 443:222-225.
15. Dupre A, Boyer-Chatenet L, Gautier J. 2006. Two-step activation of ATM by DNA and the Mre11-Rad50-Nbs1 complex. Nat Struct Mol Biol 13:451-457.
16. Lee JH, Paull TT. 2005. ATM activation by DNA double-strand breaks through the Mre11-Rad50-Nbs1 complex. Science 308:551-554.
17. Krogh BO, Symington LS. 2004. Recombination proteins in yeast. Annu Rev Genet 38:233-271.
18. D'Amours D, Jackson SP. 2002. The Mre11 complex: at the crossroads of dna repair and checkpoint signalling. Nat Rev Mol Cell Biol 3:317-327.
19. Ira G, Pellicioli A, Balijja A, Wang X, Fiorani S, et al. 2004. DNA end resection, homologous recombination and DNA damage checkpoint activation require C DK1. Nature 431:1011-1017.
20. Zou L, Elledge SJ. 2003. Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 300:1542-1548.
21. Wyka IM, Dhar K, Binz SK, Wold MS. 2003. Replication protein A interactions with DNA: differential binding of the core domains and analysis of the DNA interaction surface. Biochemistry 42:12909-12918.
22. Nakada D, Hirano Y, Tanaka Y, Sugimoto K. 2005. Role of the C terminus of Med checkpoint kinase in its localization to sites of DNA damage. Mol Biol Cell 16:5227-5235.
23. Zou L, Liu D, Elledge SJ. 2003. Replication protein A-mediated recruitment and activation of Rad17 complexes. Proc Natl Acad Sci USA 100:13827-13832.
24. Ellison V, Stillman B. 2003. Biochemical characterization of DNA damage checkpoint complexes: clamp loader and clamp complexes with specificity for 5′; recessed DNA. PLoS Biol 1:E33.
25. Bao S, Shen X, Shen K, Liu Y, Wang X. 1998. The mammalian Rad24 Homologous to yeast Saccharomyces cerevisiae Rad24 and Schizosaccharomyces pombe Rad17 is involved in DNA damage checkpoint. Cell Growth & Differentiation 9:961-967.
26. Bao S, Lu T, Wang X, Zheng H, Wang LE, et al. 2004. Disruption of the Rad9/Rad1/Hus1 (9-1-1) complex leads to checkpoint signaling and replication defects. Oncogene 23:5586-5593.
27. Freire R, Murguia JR, Tarsounas M, Lowndes NF, Moens PB, et al. 1998. Human and mouse homologs of Schizosaccharomyces pombe rad1(+) and Saccharomyces cerevisiae RA D17:linkage to checkpoint control and mammalian meiosis. Genes Dev 12:2560-2573.
28. Longhese MP, Paciotti V, Fraschini R, Zaccarini R, Plevani P, et al. 1997. The novel DNA damage checkpoint protein ddc1p is phosphorylated periodically during the cell cycle and in response to DNA damage in budding yeast. Embo J 16:5216-5226.
29. St Onge RP, Besley BD, Pelley JL, Davey S. 2003. A role for the phosphorylation of hRad9 in checkpoint signaling. J Biol Chem 278:26620-26628.
30. Kumagai A, Lee J, Yoo HY, Dunphy WG. 2006. TopBP1 activates the ATR-ATRIP complex. Cell 124:943-955.
31. Majka J, Niedziela-Majka A, Burgers PM. 2006. The Checkpoint Clamp Activates Med Kinase during Initiation of the DNA Damage Checkpoint. Mol Cell 24:891-901.
32. Majka J, Binz SK, Wold MS, Burgers PM. 2006. Replication protein A directs loading of the DNA damage checkpoint clamp to 5′;-DNA junctions. J Biol Chem 281:27855-27861.
33. Wang X, Haber JE. 2004. Role of saccharomyces single-stranded DNA-binding protein RPA in the strand invasion step of double-strand break repair. PLoS Biol 2:E21.
34. Brown EJ, Baltimore D. 2003. Essential and dispensable roles of ATR in cell cycle arrest and genome maintenance. Genes Dev 17:615-628.
35. Shiloh Y. 2003. ATM and related protein kinases: safeguarding genome integrity. Nat Rev Cancer 3:155-168.
36. Cuadrado M, Martinez-Pastor B, Murga M, Toledo LI, Gutierrez-Martinez P, et al. 2006. ATM regulates ATR chromatin loading in response to DNA double-strand breaks. J Exp Med 203:297-303.
37. Li J, Stern DF. 2005. DNA damage regulates Chk2 association with chromatin. J Biol Chem 280:37948-37956.
38. Smits VA, Reaper PM, Jackson SP. 2006. Rapid PIKK-dependent release of Chk1 from chromatin promotes the DNA-damage checkpoint response. Curr Biol 16:150-159.
39. Boutros R, Dozier C, Ducommun B. 2006. The when and wheres of CDC25 phosphatases. Curr Opin Cell Biol 18:185-191.
40. Nyberg KA, Michelson RJ, Putnam CW, Weinert TA. 2002. Toward maintaining the genome: DNA damage and replication checkpoints. Annu Rev Genet 36:617-656.
41. Sanchez Y, Bachant J, Wang H, Hu F, Liu D, et al. 1999. Control of the DNA damage checkpoint by chk1 and rad53 protein kinases through distinct mechanisms. Science 286:1166-1171.
42. Hammet A, Pike BL, McNees CJ, Conlan LA, Tenis N, et al. 2003. FHA domains as phospho-threonine binding modules in cell signaling. IUBMB Life 55:23-27.
43. Fernandez-Capetillo O, Chen HT, Celeste A, Ward I, Romanienko PJ, et al. 2002. DNA damage-induced G2-M checkpoint activation by histone H2AX and 53 BP1. Nat Cell Biol 4:993-997.
44. Glover JN, Williams RS, Lee MS. 2004. Interactions between BRCT repeats and phosphoproteins: tangled up in two. Trends Biochem Sci 29:579-585.
45. Kobayashi J. 2004. Molecular mechanism of the recruitment of NBS1/hMRE11/hRAD50 complex to DNA double-strand breaks: NBS1 binds to gamma-H2AX through FHA/BRCT domain. J Radiat Res (Tokyo) 45:473-478.
46. Becker E, Meyer V, Madaoui H, Guerois R. 2006. Detection of a tandem BRCT in Nbs1 and Xrs2 with functional implications in the DNA damage response. Bioinformatics 22:1289-1292.
47. Bekker-Jensen S, Lukas C, Kitagawa R, Melander F, Kastan MB, et al. 2006. Spatial organization of the mammalian genome surveillance machinery in response to DNA strand breaks. J Cell Biol 173:195-206.
48. Lee MS, Edwards RA, Thede GL, Glover JN. 2005. Structure of the BRCT repeat domain of MDC1 and its specificity for the free COOH-terminal end of the gamma-H2AX histone tail. J Biol Chem 280:32053-32056.
49. Stucki M, Clapperton JA, Mohammad D, Yaffe MB, Smerdon SJ, et al. 2005. MDC1 directly binds phosphorylated histone H2AX to regulate cellular responses to DNA double-strand breaks. Cell 123:1213-1226.
50. Lee AC, Fernandez-Capetillo O, Pisupati V, Jackson SP, Nussenzweig A. 2005. Specific association of mouse MDC1/NFBD1 with NBS1 at sites of DNA-damage. Cell Cycle 4:177-182.
51. Lukas C, Melander F, Stucki M, Falck J, Bekker-Jensen S, et al. 2004. Mdc1 couples DNA double-strand break recognition by Nbs1 with its H2AX-dependent chromatin retention. Embo J 23:2674-2683.
52. Lou Z, Minter-Dykhouse K, Franco S, Gostissa M, Rivera MA, et al. 2006. MDC1 maintains genomic stability by participating in the amplification of ATM-dependent DNA damage signals. Mol Cell 21:187-200.
53. Zhang J, Ma Z, Treszezamsky A, Powell SN. 2005. MDC1 interacts with Rad51 and facilitates homologous recombination. Nat Struct Mol Biol 12:902-909.
54. Celeste A, Fernandez-Capetillo O, Kruhlak MJ, Pilch DR, Staudt DW, et al. 2003. Histone H2AX phosphorylation is dispensable for the initial recognition of DNA breaks. Nat Cell Biol 5:675-679.
55. Naseem R, Sturdy A, Finch D, Jowitt T, Webb M. 2006. Mapping and conformational characterization of the DNA-binding region of the breast cancer susceptibility protein BRCA1. Biochem J 395:529-535.
56. Gatei M, Zhou BB, Hobson K, Scott S, Young D, et al. 2001. Ataxia telangiectasia mutated (ATM) kinase and ATM and Rad3 related kinase mediate phosphorylation of Brca1 at distinct and overlapping sites. In vivo assessment using phospho-specific antibodies. J Biol Chem 276:17276-17280.
57. Ting NS, Lee WH. 2004. The DNA double-strand break response pathway: becoming more BRCAish than ever. DNA Repair (Amst) 3:935-944.
58. Deng CX. 2006. BRC A1:cell cycle checkpoint, genetic instability, DNA damage response and cancer evolution. Nucleic Acids Res 34:1416-1426.
59. Ekblad CM, Friedler A, Veprintsev D, Weinberg RL, Itzhaki LS. 2004. Comparison of BRCT domains of BRCA1 and 53B P1:a biophysical analysis. Protein Sci 13:617-625.
60. Ward I, Kim JE, Minn K, Chini CC, Mer G, et al. 2006. The tandem BRCT domain of 53BP1 is not required for its repair function. J Biol Chem.
61. Alpha-Bazin B, Lorphelin A, Nozerand N, Charier G, Marchetti C, et al. 2005. Boundaries and physical characterization of a new domain shared between mammalian 53BP1 and yeast Rad9 checkpoint proteins. Protein Sci 14:1827-1839.
62. Huyen Y, Zgheib O, Ditullio RA Jr, Gorgoulis VG, Zacharatos P, et al. 2004. Methylated lysine 79 of histone H3 targets 53BP1 to DNA double-strand breaks. Nature 432:406-411.
63. Bekker-Jensen S, Lukas C, Melander F, Bartek J, Lukas J. 2005. Dynamic assembly and sustained retention of 53BP1 at the sites of DNA damage are controlled by Mdd/NF BD1. J Cell Biol 170:201-211.
64. Toh GW, O'Shaughnessy AM, Jimeno S, Dobbie IM, Grenon M, et al. 2006. Histone H2A phosphorylation and H3 methylation are required for a novel Rad9 DSB repair function following checkpoint activation. DNA Repair (Amst) 5:693-703.
65. Naiki T, Wakayama T, Nakada D, Matsumoto K, Sugimoto K. 2004. Association of Rad9 with double-strand breaks through a Mec1-dependent mechanism. Mol Cell Biol 24:3277-3285.
66. Sweeney FD, Yang F, Chi A, Shabanowitz J, Hunt DF, et al. 2005. Saccharomyces cerevisiae Rad9 acts as a Mec1 adaptor to allow Rad53 activation. Curr Biol 15:1364-1375.
67. Page SL, Hawley RS. 2004. The genetics and molecular biology of the synaptonemal complex. Annu Rev Cell Dev Biol 20:525-558.
68. Mahadevaiah SK, Turner JMA, Baudat F, Rogakou EP, de Boer P, et al. 2001. Recombinational DNA double-strand breaks in mice precede synapsis. Nature Genetics 27:271-276.
69. Roeder GS, Bailis JM. 2000. The pachytene checkpoint. Trends in Genetics 16:395-403.
70. Soustelle C, Vedel M, Kolodner R, Nicolas A. 2002. Replication protein A is required for meiotic recombination in Saccharomyces cerevisiae. Genetics 161:535-547.
71. Borde V. 2007. The multiple roles of the Mre11 complex for meiotic recombination. Chromosome Research.
72. Neale MJ, Pan J, Keeney S. 2005. Endonucleolytic processing of covalent protein-linked DNA double-strand breaks. Nature 436:1053-1057.
73. Usui T, Ogawa H, Petrini JH. 2001. A DNA damage response pathway controlled by Tel1 and the Mre11 complex. Mol Cell 7:1255-1266.
74. Hochwagen A, Amon A. 2006. Checking your breaks: surveillance mechanisms of meiotic recombination. Curr Biol 16:R217-228.
75. Shinohara M, Sakai K, Ogawa T, Shinohara A. 2003. The mitotic DNA damage checkpoint proteins Rad17 and Rad24 are required for repair of double-strand breaks during meiosis in yeast. Genetics 164:855-865.
76. Hong EJ, Roeder GS. 2002. A role for Ddc1 in signaling meiotic double-strand breaks at the pachytene checkpoint. Genes Dev 16:363-376.
77. Lydall D, Nikolsky Y, Bishop DK, Weinert T. 1996. A meiotic recombination checkpoint controlled by mitotic checkpoint genes. Nature 383:840-843.
78. Xu L, Weiner BM, Kleckner N. 1997. Meiotic cells monitor the status of the interhomolog recombination complex. Genes & Development 11:106-118.
79. Leu J-Y, Roeder GS. 1999. The pachytene checkpoint in S. cerevisiae depends on Swe1-mediated phophorylation of the cyclin-dependent kinase Cdc28. Molecular Cell 4:805-814.
80. Pak J, Segall J. 2002. Role of Ndt80, Sum1, and Swe1 as targets of the meiotic recombination checkpoint that control exit from pachytene and spore formation in Saccharomyces cerevisiae. Mol Cell Biol 22:6430-6440.
81. Moens PB, Kolas NK, Tarsounas M, Marcon E, Cohen PE, et al. 2002. The time course and chromosomal localization of recombination-related proteins at meiosis in the mouse are compatible with models that can resolve the early DNA-DNA interactions without reciprocal recombination. J Cell Sci 115:1611-1622.
82. Ashley T, Gaeth AP, Creemers LB, Hack AM, de Rooij DG. 2004. Correlation of meiotic events in testis sections and microspreads of mouse spermatocytes relative to the mid-pachytene checkpoint. Chromosoma 113:126-136.
83. Plug AW, Peters AH, Keegan KS, Hoekstra MF, de Boer P, et al. 1998. Changes in protein composition of meiotic nodules during mammalian meiosis. J Cell Sci 111:413-423.
84. Barchi M, Mahadevaiah S, Di Giacomo M, Baudat F, de Rooij DG, et al. 2005. Surveillance of Different Recombination Defects in Mouse Spermatocytes Yields Distinct Responses despite Elimination at an Identical Developmental Stage. Mol Cell Biol 25:7203-7215.
85. Bellani MA, Romanienko PJ, Cairatti DA, Camerini-Otero RD. 2005. SPO11 is required for sex-body formation, and Spo11 heterozygosity rescues the prophase arrest of Atm-/- spermatocytes. J Cell Sci 118:3233-3245.
86. Hamer G, Kal HB, Westphal CH, Ashley T, de Rooij DG. 2004. Ataxia telangiectasia mutated expression and activation in the testis. Biol Reprod 70:1206-1212.
87. Moens PB, Tarsounas M, Morita T, Habu T, Rottinghaus ST, et al. 1999. The association of ATR protein with mouse meiotic chromosome cores. Chromosoma 108:95-102.
88. Plug AW, Peters AH, Xu Y, Keegan KS, Hoekstra MF, et al. 1997. ATM and RPA in meiotic chromosome synapsis and recombination. Nat Genet 17:457-461.
89. Barlow C, Liyanage M, Moens PB, Tarsounas M, Nagashima K, et al. 1998. Atm deficiency results in severe meiotic disruption as early as leptonema of prophase I. Development 125:4007-4017.
90. Keegan KS, Holtzman DA, Plug AW, Christenson ER, Brainerd EE, et al. 1996. The Atr and Atm protein kinases associate with different sites along meiotically pairing chromosomes. Genes & Development 10:2423-2437.
91. Perera D, Perez-Hidalgo L, Moens PB, Reini K, Lakin N, et al. 2004. TopBP1 and ATR colocalization at meiotic chromosomes: role of TopBP1/Cut5 in the meiotic recombination checkpoint. Mol Biol Cell 15:1568-1579.
92. Hang H, Zhang Y, Dunbrack RL Jr, Wang C, Lieberman HB. 2002. Identification and characterization of a paralog of human cell cycle checkpoint gene HUS1. Genomics 79:487-492.
93. Hopkins KM, Wang X, Berlin A, Hang H, Thaker HM, et al. 2003. Expression of mammalian paralogues of HRAD9 and Mrad9 checkpoint control genes in normal and cancerous testicular tissue. Cancer Res 63:5291-5298.
94. Ashley T, Westphal C, Plug-de Maggio A, de Rooij DG. 2004. The mammalian mid-pachytene checkpoint: meiotic arrest in spermatocytes with a mutation in Atm alone or in combination with a Trp53 (p53) or Cdkn1a (p21/cip1) mutation. Cytogenet Genome Res 107: 256-262.
95. Flaggs G, Plug AW, Dunks KM, Mundt KE, Ford JC, et al. 1997. Atm-dependent interactions of a mammalian chk1 homolog with meiotic chromosomes. Curr Biol 7:977-986.
96. Wolgemuth DJ. 2003. Insights into regulation of the mammalian cell cycle from studies on spermatogenesis using genetic approaches in animal models. Cytogenet Genome Res 103:256-266.
97. Inselman A, Handel MA. 2004. Mitogen-activated protein kinase dynamics during the meiotic G2/MI transition of mouse spermatocytes. Biol Reprod 71:570-578.
98. Wiltshire T, Park C, Caldwell KA, Handel MA. 1995. Induced premature G2/M-phase transition in pachytene spermatocytes includes events unique to meiosis. Dev Biol 169:557-567.
99. Ashley T, Walpita D, de Rooij DG. 2001. Localization of two mammalian cyclin dependent kinases during mammalian meiosis. J Cell Sci 114:685-693.
100. Ortega S, Prieto I, Odajima J, Martin A, Dubus P, et al. 2003. Cyclin-dependent kinase 2 is essential for meiosis but not for mitotic cell division in mice. Nat Genet 35:25-31.
101. Dix DJ, Allen JW, Collins BW, Poorman-Allen P, Mori C, et al. 1997. HSP 70-2is required for desynapsis of synaptonemal complexes during meiotic prophase in juvenile and adult mouse spermatocytes. Development 124:4595-4603.
102. Zhu D, Dix DJ, Eddy EM. 1997. HSP 70-2is required for CDC2 kinase activity in meiosis I of mouse spermatocytes. Development 124:3007-3014.
103. Scully R, Chen J, Plug A, Xiao Y, Weaver D, et al. 1997. Association of BRCA1 with Rad51 in mitotic and meiotic cells. Cell 88:265-275.
104. Turner JM, Aprelikova O, Xu X, Wang R, Kim S, et al. 2004. BRCA1, histone H2AX phosphorylation, and male meiotic sex chromosome inactivation. Curr Biol 14:2135-2142.
105. Esashi F, Christ N, Gannon J, Liu Y, Hunt T, et al. 2005. CDK-dependent phosphorylation of BRCA2 as a regulatory mechanism for recombinational repair. Nature 434:598-604.
106. Chen J, Silver DP, Walpita D, Cantor SB, Gazdar AF, et al. 1998. Stable interaction between the products of the BRCA1 and BRCA2 tumor suppressor genes in mitotic and meiotic cells. Mol Cell 2:317-328.
107. Ahmed EA, van der Vaart A, Barten A, Kal HB, Chen J, et al. 2007. Differences in DNA double-strand breaks repair in male germ cell types: Lessons learned from a differential expression of Mdd and 53BP1. DNA Repair (Amst).
108. Ward IM, Minn K, van Deursen J, Chen J. 2003. p53 Binding protein 53BP1 is required for DNA damage responses and tumor suppression in ice. Mol Cell Biol 23:2556-2563.
109. Tarsounas M, Moens PB. 2001. Checkpoint and DNA-repair proteins are associated with the cores of mammalian meiotic chromosomes. Curr Top Dev Biol 51:109-134.
110. Bishop DK, Park D, Xu L, Kleckner N. 1992. DM C1:A meiosis-specific yeast homologue of E.coli recA required for recombination, synaptonemal complex formation, and cell cycle progression. Cell 69:439-456.
111. McKee AH, Kleckner N. 1997. Mutations in Saccharomyces cerevisiae that block meiotic prophase chromosome metabolism and confer cell cycle arrest at pachytene identify two new meiosis-specific genes SAE1 and SAE3. Genetics 146:817-834.
112. Pittman DL, Cobb J, Schimenti KJ, Wilson LA, Cooper DM, et al. 1998. Meiotic prophase arrest with failure of chromosome synapsis in mice deficient for Dmc1, a germline-specific RecA homolog. Mol Cell 1:697-705.
113. Yoshida K, Kondoh G, Matsuda Y, Habu T, Nishimune Y, et al. 1998. The mouse RecA-like gene Dmc1 is required for homologous chromosome synapsis during meiosis. Mol Cell 1:707-718.
114. Di Giacomo M, Barchi M, Baudat F, Edelmann W, Keeney S, et al. 2005. Distinct DNA-damage-dependent and -independent responses drive the loss of oocytes in recombination-defective mouse mutants. Proc Natl Acad Sci USA 102:737-742.
115. Baudat F, Manova K, Yuen JP, Jasin M, Keeney S. 2000. Chromosome synapsis defects and sexually dimorphic meiotic progression in mice lacking Spo11. Mol Cell 6:989-998.
116. Romanienko PJ, Camerini-Otero RD. 2000. The mouse Spo11 gene is required for meiotic chromosome synapsis. Mol Cell 6:975-987.
117. Turner JMA, Burgoyne PS. 2006. Male meiotic sex chromosome inactivation and meiotic silencing. In: Lau Y-FC, Chan WY, editors. Y Chromosome and Male Germ Cell Biology. Hackensack, NJ: World Scientific Publishers.
118. Turner JM, Mahadevaiah SK, Ellis PJ, Mitchell MJ, Burgoyne PS. 2006. Pachytene asynapsis drives meiotic sex chromosome inactivation and leads to substantial postmeiotic repression in spermatids. Dev Cell 10:521-529.
119. Fernandez-Capetillo O, Mahadevaiah SK, Celeste A, Romanienko PJ, Camerini-Otero RD, et al. 2003. H2AX is required for chromatin remodeling and inactivation of sex chromosomes in male mouse meiosis. Dev Cell 4:497-508.
120. Eijpe M, Offenberg H, Goedecke W, Heyting C. 2000. Localisation of RAD50 and MRE11 in spermatocyte nuclei of mouse and rat. Chromosoma 109:123-132.