Meiotic DNA double-strand breaks and chromosome asynapsis in mice are monitored by distinct HORMAD2-independent and -dependent mechanisms

Genes and Development

Volumn 26, Issue 9, 2012, Pages 958-973

  Wojtasz, Lukasz ^a   Cloutier, Jeffrey M ^b   Baumann, Marek ^a   Daniel, Katrin ^a   Varga, János ^c   Fu, Jun ^a   Anastassiadis, Konstantinos ^d   Francis Stewart, A ^a   Reményi, Attila ^c   Turner, James M A ^b   Tóth, Attila ^a  

^a DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^b NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^c EÖTVÖS LORÁND UNIVERSITY   (Hungary)

^d CENTER FOR REGENERATIVE THERAPIES DRESDEN   (Germany)

Author keywords

Aneuploidy; Asynapsis surveillance; ATR; HORMA domain; Meiosis; Meiotic prophase checkpoint

Indexed keywords

ATR PROTEIN; DOUBLE STRANDED DNA; NUCLEAR PROTEIN; NUCLEAR PROTEIN HORMAD1; NUCLEAR PROTEIN HORMAD2; SPO11 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CHROMATIN; CHROMOSOME ABERRATION; CHROMOSOME ASYNAPSIS; CHROMOSOME CHIASM; CHROMOSOME PAIRING; CONTROLLED STUDY; DNA METABOLISM; DOUBLE STRANDED DNA BREAK; GENE SILENCING; MALE; MALE INFERTILITY; MEIOSIS; MOUSE; NONHUMAN; OOCYTE; PRIORITY JOURNAL; PROPHASE; PROTEIN INTERACTION; SEX CHROMOSOME; SYNAPTONEMAL COMPLEX;

ANIMALS; CELL CYCLE PROTEINS; CHROMOSOME PAIRING; DNA BREAKS, DOUBLE-STRANDED; FEMALE; INFERTILITY, MALE; MALE; MEIOSIS; MICE; MICE, MUTANT STRAINS; NUCLEAR PROTEINS; OOCYTES; SYNAPTONEMAL COMPLEX;

MAMMALIA; MUS;

EID: 84860530521     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.187559.112     Document Type: Article

References (52)

1. TIR sex-reversed mouse ovary. Reproduction 135: 241-252.
2. Barchi M, Mahadevaiah S, Di Giacomo M, Baudat F, de Rooij DG, Burgoyne PS, Jasin M, Keeney S. 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.
3. Baudat F, de Massy B. 2007. Regulating double-stranded DNA break repair towards crossover or non-crossover during mammalian meiosis. Chromosome Res 15: 565-577.
4. 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.
5. - spermatocytes. J Cell Sci 118: 3233-3245.
6. Bolcun-Filas E, Costa Y, Speed R, Taggart M, Benavente R, De Rooij DG, Cooke HJ. 2007. SYCE2 is required for synaptonemal complex assembly, double strand break repair, and homologous recombination. J Cell Biol 176: 741-747.
7. Bolcun-Filas E, Hall E, Speed R, Taggart M, Grey C, de Massy B, Benavente R, Cooke HJ. 2009. Mutation of the mouse Syce1 gene disrupts synapsis and suggests a link between synaptonemal complex structural components and DNA repair. PLoS Genet 5. e1000393: doi: 10.1371/journal.pgen.1000393
8. Burgoyne PS, Mahadevaiah SK, Turner JM. 2009. The consequences of asynapsis for mammalian meiosis. Nat Rev Genet 10: 207-216.
9. Calenda A, Allenet B, Escalier D, Bach JF, Garchon HJ. 1994. The meiosis-specific Xmr gene product is homologous to the lymphocyte Xlr protein and is a component of the XY body. EMBO J 1 3: 100-109.
10. Carballo JA, Johnson AL, Sedgwick SG, Cha RS. 2008. Phosphorylation of the axial element protein Hop1 by Mec1/Tell ensures meiotic interhomolog recombination. Cell 132: 758-770.
11. Couteau F, Zetka M. 2005. HTP-1 coordinates synaptonemal complex assembly with homolog alignment during meiosis in C. elegans. Genes Dev 19: 2744-2756.
12. Daniel K, Lange J, Hached K, Fu J, Anastassiadis K, Roig I, Cooke HJ, Stewart AF, Wassmann K, Jasin M, et al. 2011. Meiotic homologue alignment and its quality surveillance are controlled by mouse HORMAD1. Nat Cell Biol 13: 599-610.
13. De Antoni A, Pearson CG, Cimini D, Canman JC, Sala V, Nezi L, Mapelli M, Sironi L, Faretta M, Salmon ED, et al. 2005. The Mad1/Mad2 complex as a template for Mad2 activation in the spindle assembly checkpoint. Curr Biol 15: 214-225.
14. Di Giacomo M, Barchi M, Baudat F, Edelmann W, Keeney S, Jasin M. 2005. Distinct DNA-damage-dependent and -independent responses drive the loss of oocytes in recombination-defective mouse mutants. Proc Natl Acad Sci 102: 737-742.
15. Femandez-Capetillo O, Mahadevaiah SK, Celeste A, Romanienko PJ, Camerini-Otero RD, Bonner WM, Manova K, Burgoyne P, Nussenzweig A. 2003. H2AX is required for chromatin remodeling and inactivation of sex chromosomes in male mouse meiosis. Dev Cell 4: 497-508.
16. Fukuda T, Daniel K, Wojtasz L, Toth A, Hoog C. 2010. A novel mammalian HORMA domain-containing protein, HORMAD1, preferentially associates with unsynapsed meiotic chromosomes. Exp Cell Res 316: 158-171.
17. Fukuda T, Pratto F, Schimenti JC, Turner JM, Camerini-Otero RD, Hoog C. 2012. Phosphorylation of chromosome core components may serve as axis marks for the status of chromosomal events during mammalian meiosis. PLoS Genet 8: e1002485. doi: 10.1371/journal.pgen.1002485
18. Hamer G, Novak I, Kouznetsova A, Hoog C. 2008a. Disruption of pairing and synapsis of chromosomes causes stage-specific apoptosis of male meiotic cells. Theriogenology 69: 333-339.
19. Harmer G, Wang H, Bolcun-Filas E, Cooke HJ, Benavente R, Hoog C. 2008b. Progression of meiotic recombination requires structural maturation of the central element of the synaptonemal complex. J Cell Sci 121: 2445-2451.
20. Hassold T, Hall H, Hunt P. 2007. The origin of human aneuploidy: Where we have been, where we are going. Hum Mol Genet 16: R203-R208. doi: 10.1093/hmg/ddm243
21. Hochwagen A, Amon A. 2006. Checking your breaks: Surveillance mechanisms of meiotic recombination. Curr Biol 16: R217-R228. doi: 10.1016/j.cub.2006.03.009
22. Ichijima Y, Ichijima M, Lou Z, Nussenzweig A, Camerini-Otero RD, Chen J, Andreassen PR, Namekawa SH. 2011. MDC1 directs chromosome-wide silencing of the sex chromosomes in male germ cells. Genes Dev 25: 959-971.
23. Keegan KS, Holtzman DA, Plug AW, Christenson ER, Brainerd EE, Flaggs G, Bentley NJ, Taylor EM, Meyn MS, Moss SB, et al. 1996. The Atr and Atm protein kinases associate with different sites along meiotically pairing chromosomes. Genes Dev 10: 2423-2437.
24. Keeney S, Giroux CN, Kleckner N. 1997. Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell 88: 375-384.
25. Kolas NK, Marcon E, Crackower MA, Hoog C, Penninger JM, Spyropoulos B, Moens PB. 2005. Mutant meiotic chromosome core components in mice can cause apparent sexual dimorphic endpoints at prophase or X-Y defective male-specific sterility. Chromosoma 114: 92-102.
26. Kouznetsova A, Wang H, Bellani M, Camerini-Otero RD, Jessberger R, Hoog C. 2009. BRCA1-mediated chromatin silencing is limited to oocytes with a small number of asynapsed chromosomes. J Cell Sci 122: 2446-2452.
27. Li XC, Schimenti JC. 2007. Mouse pachytene checkpoint 2 (trip13) is required for completing meiotic recombination but not synapsis. PLoS Genet 3: e130. doi: 10.1371/journal.pgen.0030130.
28. MacQueen AJ, Hochwagen A. 2011. Checkpoint mechanisms: The puppet masters of meiotic prophase. Trends Cell Biol 21: 393-400.
29. Mahadevaiah SK, Bourc'his D, de Rooij DG, Bestor TH, Turner JM, Burgoyne PS. 2008. Extensive meiotic asynapsis in mice antagonises meiotic silencing of unsynapsed chromatin and consequently disrupts meiotic sex chromosome inactivation. J Cell Biol 182: 263-276.
30. Mahadevaiah SK, Costa Y, Turner JM. 2009. Using RNA FISH to study gene expression during mammalian meiosis. Methods Mol Biol 558: 433-444.
31. Marcon E, Moens P. 2003. MLH1p and MLH3p localize to precociously induced chiasmata of okadaic-acid-treated mouse spermatocytes. Genetics 165: 2283-2287.
32. Martinez-Perez E, Villeneuve AM. 2005. HTP-1-dependent constraints coordinate homolog pairing and synapsis and promote chiasma formation during C. elegans meiosis. Genes Dev 19: 2727-2743.
33. Moens P., Tarsounas M, Morita T, Habu T, Rottinghaus ST, Freire R, Jackson SP, Barlow C, Wynshaw-Boris A. 1999. The association of ATR protein with mouse meiotic chromosome cores. Chromosoma 108: 95-102.
34. Moens P., Marcon E, Shore JS, Kochakpour N, Spyropoulos B. 2007. Initiation and resolution of interhomolog connections: Crossover and non-crossover sites along mouse synaptonemal complexes. J Cell Sci 120: 1017-1027.
35. Neale MJ, Pan J, Keeney S. 2005. Endonucleolytic processing of covalent protein-linked DNA double-strand breaks. Nature 436: 1053-1057.
36. Page SL, Hawley RS. 2003. Chromosome choreography: The meiotic ballet. Science 301: 785-789.
37. Perera D, Perez-Hidalgo L, Moens P., Reini K, Lakin N, Syvaoja JE, San-Segundo PA, Freire R. 2004. TopBP1 and ATR colocalization at meiotic chromosomes: Role of TopBP1/Cut5 in the meiotic recombination checkpoint. Mol Biol Cell 15: 1568-1579.
38. 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.
39. Plug AW, Peters AH, Keegan KS, Hoekstra MF, de Boer P, Ashley T. 1998. Changes in protein composition of meiotic nodules during mammalian meiosis. J Cell Sci 111: 413-423.
40. Remenyi A, Good MC, Bhattacharyya RP, Lim WA. 2005. The role of docking interactions in mediating signaling input, output, and discrimination in the yeast MAPK network. Mol Cell 20: 951-962.
41. Reynard LN, Turner JM, Cocquet J, Mahadevaiah SK, Toure A, Hoog C, Burgoyne PS. 2007. Expression analysis of the mouse multi-copy X-linked gene Xlr-related, meiosis-regulated (Xmr), reveals that Xmr encodes a spermatid-expressed cytoplasmic protein, SLX/XMR. Biol Reprod 77: 329-335.
42. Roig I, Dowdle JA, Toth A, de Rooij DG, Jasin M, Keeney S. 2010. Mouse TRIP13/PCH2 is required for recombination and normal higher-order chromosome structure during meiosis. PLoS Genet 6: e1001062. doi: 10.1371/journal.pgen.1001062.
43. Romanienko PJ, Camerini-Otero RD. 2000. The mouse Spo11 gene is required for meiotic chromosome synapsis. Mol Cell 6: 975-987.
44. Royo H, Polikiewicz G, Mahadevaiah SK, Prosser H, Mitchell M, Bradley A, de Rooij DG, Burgoyne PS, Turner JM. 2010. Evidence that meiotic sex chromosome inactivation is essential for male fertility. Curr Biol 20: 2117-2123.
45. Shin YH, Choi Y, Erdin SU, Yatsenko SA, Kloc M, Yang F, Wang PJ, Meistrich ML, Rajkovic A. 2010. Hormad1 mutation disrupts synaptonemal complex formation, recombination, and chromosome segregation in mammalian meiosis. PLoS Genet 6 e1001190: doi: 10.1371/journal.pgen.1001190
46. Testa G, Schaft J, van der Hoeven F, Glaser S, Anastassiadis K, Zhang Y, Hermann T, Stremmel W, Stewart AF. 2004. A reliable lacZ expression reporter cassette for multipurpose, knockout-first alleles. Genesis 38: 151-158.
47. Turner JM, Aprelikova O, Xu X, Wang R, Kim S, Chandramouli GV, Barrett JC, Burgoyne PS, Deng CX. 2004. BRCA1, histone H2AX phosphorylation, and male meiotic sex chromosome inactivation. Curr Biol 14: 2135-2142.
48. Turner JM, Mahadevaiah SK, Fernandez-Capetillo O, Nussenzweig A, Xu X, Deng CX, Burgoyne PS. 2005. Silencing of unsynapsed meiotic chromosomes in the mouse. Nat Genet 37: 41-47.
49. 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.
50. Wojtasz L, Daniel K, Roig I, Bolcun-Filas E, Xu H, Boonsanay V, Eckmann CR, Cooke HJ, Jasin M, Keeney S, et al. 2009. Mouse HORMAD1 and HORMAD2, two conserved meiotic chromosomal proteins, are depleted from synapsed chromosome axes with the help of TRIP13 AAA-ATPase. PLoS Genet 5 e1000702: doi: 10.1371/journal.pgen.1000702
51. 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.
52. Zou L, Elledge SJ. 2003. Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 300: 1542-1548.