H2AX is required for chromatin remodeling and inactivation of sex chromosomes in male mouse meiosis

Developmental Cell

Volumn 4, Issue 4, 2003, Pages 497-508

  Fernandez Capetillo, Oscar ^a   Mahadevaiah, Shantha K ^b   Celeste, Arkady ^a   Romanienko, Peter J ^c   Camerini Otero, R Daniel ^c   Bonner, William M ^a   Manova, Katia ^d   Burgoyne, Paul ^b   Nussenzweig, André ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^c NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^d MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; DOUBLE STRANDED DNA; HISTONE H2A;

ANIMAL CELL; CHROMATIN; CHROMOSOME CONDENSATION; CHROMOSOME INACTIVATION; CHROMOSOME PAIRING; CONTROLLED STUDY; DNA REPAIR; DNA STRAND BREAKAGE; GENE REPRESSION; GENE SILENCING; GENETIC RECOMBINATION; MALE; MEIOSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROPHASE; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; REVIEW; SEX CHROMOSOME; SPERMATOCYTE; TRANSCRIPTION REGULATION; X CHROMOSOME; Y CHROMOSOME;

ANIMALIA; MAMMALIA;

EID: 0346634937     PISSN: 15345807     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1534-5807(03)00093-5     Document Type: Article

References (65)

1. Abraham R.T. Cell cycle checkpoint signaling through the ATM and ATR kinases Genes Dev. 15 2001 2177 2196
2. Ayoub N. Richler C. Wahrman J. Xist RNA is associated with the transcriptionally inactive XY body in mammalian male meiosis Chromosoma 106 1997 1 10
3. Baarends W.M. Hoogerbrugge J.W. Roest H.P. Ooms M. Vreeburg J. Hoeijmakers J.H. Grootegoed J.A. Histone ubiquitination and chromatin remodeling in mouse spermatogenesis Dev. Biol. 207 1999 322 333
4. Bassing C.H. Chua K.F. Sekiguchi J. Suh H. Whitlow S.R. Fleming J.C. Monroe B.C. Ciccone D.N. Yan C. Vlasakova K. et al. Increased ionizing radiation sensitivity and genomic instability in the absence of histone H2AX Proc. Natl. Acad. Sci. USA 99 2002 8173 8178
5. Baudat F. Manova K. Yuen J.P. Jasin M. Keeney S. Chromosome synapsis defects and sexually dimorphic meiotic progression in mice lacking Spo11 Mol. Cell 6 2000 989 998
6. Bauer U.M. Schneider-Hirsch S. Reinhardt S. Benavente R. Maelicke A. The murine nuclear orphan receptor GCNF is expressed in the XY body of primary spermatocytes FEBS Lett. 439 1998 208 214
7. Burgoyne P.S. Mahadevaiah S.K. Sutcliffe M.J. Palmer S.J. Fertility in mice requires X-Y pairing and a Y-chromosomal "spermiogenesis" gene mapping to the long arm Cell 71 1992a 391 398
8. Burgoyne P.S. Sutcliffe M.J. Mahadevaiah S.K. The role of unpaired sex chromosomes in spermatogenic failure Andrologia 24 1992 17 20 b
9. Calenda A. Allenet B. Escalier D. Bach J.F. Garchon H.J. The meiosis-specific Xmr gene product is homologous to the lymphocyte Xlr protein and is a component of the XY body EMBO J. 13 1994 100 109
10. Celeste A. Petersen S. Romanienko P.J. Fernandez-Capetillo O. Chen H.T. Sedelnikova O.A. Reina-San-Martin B. Coppola V. Meffre E. Difilippantonio M.J. et al. Genomic instability in mice lacking histone H2AX Science 296 2002 922 927
11. Csankovszki G. Panning B. Bates B. Pehrson J.R. Jaenisch R. Conditional deletion of Xist disrupts histone macroH2A localization but not maintenance of X inactivation Nat. Genet. 22 1999 323 324
12. Downs J.A. Lowndes N.F. Jackson S.P. A role for Saccharomyces cerevisiae histone H2A in DNA repair Nature 408 2000 1001 1004
13. Drabent B. Bode C. Bramlage B. Doenecke D. Expression of the mouse testicular histone gene H1t during spermatogenesis Histochem. Cell Biol. 106 1996 247 251
14. Escalier D. Garchon H.J. XMR is associated with the asynapsed segments of sex chromosomes in the XY body of mouse primary spermatocytes Chromosoma 109 2000 259 265
15. Goetz P. Chandley A.C. Speed R.M. Morphological and temporal sequence of meiotic prophase development at puberty in the male mouse J. Cell Sci. 65 1984 249 263
16. Hoyer-Fender S. Costanzi C. Pehrson J.R. Histone macroH2A1.2 is concentrated in the XY-body by the early pachytene stage of spermatogenesis Exp. Cell Res. 258 2000 254 260
17. Jablonka E. Lamb M.J. Meiotic pairing constraints and the activity of sex chromosomes J. Theor. Biol. 133 1988 23 36
18. Keegan K.S. Holtzman D.A. Plug A.W. Christenson E.R. Brainerd E.E. Flaggs G. Bentley N.J. Taylor E.M. Meyn M.S. Moss S.B. et al. The Atr and Atm protein kinases associate with different sites along meiotically pairing chromosomes Genes Dev. 10 1996 2423 2437
19. Keeney S. Mechanism and control of meiotic recombination initiation Curr. Top. Dev. Biol. 52 2001 1 53
20. Kralewski M. Novello A. Benavente R. A novel Mr 77,000 protein of the XY body of mammalian spermatocytes: its localization in normal animals and in Searle's translocation carriers Chromosoma 106 1997 160 167
21. Lenhossek M. Untersuchungen uber spermatogenese Arch. Mikrosk. Anat. Entwicklungsmech 51 1898 215 318
22. Liyanage M. Coleman A. du Manoir S. Veldman T. McCormack S. Dickson R.B. Barlow C. Wynshaw-Boris A. Janz S. Wienberg J. et al. Multicolour spectral karyotyping of mouse chromosomes Nat. Genet. 14 1996 312 315
23. Mahadevaiah S.K. Odorisio T. Elliott D.J. Rattigan A. Szot M. Laval S.H. Washburn L.L. McCarrey J.R. Cattanach B.M. Lovell-Badge R. Burgoyne P.S. Mouse homologues of the human AZF candidate gene RBM are expressed in spermatogonia and spermatids and map to a Y chromosome deletion interval associated with a high incidence of sperm abnormalities Hum. Mol. Genet. 7 1998 715 727
24. Mahadevaiah S.K. Turner J.M. Baudat F. Rogakou E.P. de Boer P. Blanco-Rodriguez J. Jasin M. Keeney S. Bonner W.M. Burgoyne P.S. Recombinational DNA double-strand breaks in mice precede synapsis Nat. Genet. 27 2001 271 276
25. Manova K. Tomihara-Newberger C. Wang S. Godelman A. Kalantry S. Witty-Blease K. De Leon V. Chen W.S. Lacy E. Bachvarova R.F. Apoptosis in mouse embryos: elevated levels in pregastrulae and in the distal anterior region of gastrulae of normal and mutant mice Dev. Dyn. 213 1998 293 308
26. Mazeyrat S. Saut N. Grigoriev V. Mahadevaiah S.K. Ojarikre O.A. Rattigan A. Bishop C. Eicher E.M. Mitchell M.J. Burgoyne P.S. A Y-encoded subunit of the translation initiation factor Eif2 is essential for mouse spermatogenesis Nat. Genet. 29 2001 49 53
27. McCarrey J.R. Dilworth D.D. Expression of Xist in mouse germ cells correlates with X-chromosome inactivation Nat. Genet. 2 1992 200 203
28. McCarrey J.R. Watson C. Atencio J. Ostermeier G.C. Marahrens Y. Jaenisch R. Krawetz S.A. X-chromosome inactivation during spermatogenesis is regulated by an Xist/Tsix-independent mechanism in the mouse Genesis 34 2002 257 266
29. McKee B.D. Handel M. Sex chromosomes, recombination, and chromatin conformation Chromosoma 102 1993 71 80
30. Miklos G.L. Sex-chromosome pairing and male fertility Cytogenet. Cell Genet. 13 1974 558 577
31. Moens P.B. Chen D.J. Shen Z. Kolas N. Tarsounas M. Heng H.H. Spyropoulos B. Rad51 immunocytology in rat and mouse spermatocytes and oocytes Chromosoma 106 1997 207 215
32. Moens P.B. Tarsounas M. Morita T. Habu T. Rottinghaus S.T. Freire R. Jackson S.P. Barlow C. Wynshaw-Boris A. The association of ATR protein with mouse meiotic chromosome cores Chromosoma 108 1999 95 102
33. Monesi V. Synthetic activities during spermatogenesis in the mouse RNA and protein Exp. Cell Res. 39 1965 197 224
34. Motzkus D. Singh P.B. Hoyer-Fender S. M31, a murine homolog of Drosophila HP1, is concentrated in the XY body during spermatogenesis Cytogenet. Cell Genet. 86 1999 83 88
35. Nebel B.R. Amarose A.P. Hackett E.M. Calender of gametogenic development in the prepubertal male mouse Science 134 1961 832 833
36. O'Carroll D. Scherthan H. Peters A.H. Opravil S. Haynes A.R. Laible G. Rea S. Schmid M. Lebersorger A. Jerratsch M. et al. Isolation and characterization of Suv39h2, a second histone H3 methyltransferase gene that displays testis-specific expression Mol. Cell. Biol. 20 2000 9423 9433
37. Odartchenko N. Pavillard M. Late DNA replication in male mouse meiotic chromosomes Science 167 1970 1133 1134
38. Odorisio T. Mahadevaiah S.K. McCarrey J.R. Burgoyne P.S. Transcriptional analysis of the candidate spermatogenesis gene Ube1y and of the closely related Ube1x shows that they are coexpressed in spermatogonia and spermatids but are repressed in pachytene spermatocytes Dev. Biol. 180 1996 336 343
39. Odorisio T. Rodriguez T.A. Evans E.P. Clarke A.R. Burgoyne P.S. The meiotic checkpoint monitoring synapsis eliminates spermatocytes via p53-independent apoptosis Nat. Genet. 18 1998 257 261
40. Painter T.S. Studies in mammalian spermatogenesis III. The fate of the chromatin-nucleolus in the opossum J. Exp. Zool. 39 1924 197
41. Parraga M. del Mazo J. XYbp, a novel RING-finger protein, is a component of the XY body of spermatocytes and centrosomes Mech. Dev. 90 2000 95 101
42. Perry J. Palmer S. Gabriel A. Ashworth A. A short pseudoautosomal region in laboratory mice Genome Res. 11 2001 1826 1832
43. Pittman D.L. Cobb J. Schimenti K.J. Wilson L.A. Cooper D.M. Brignull E. Handel M.A. Schimenti J.C. Meiotic prophase arrest with failure of chromosome synapsis in mice deficient for Dmc1, a germline-specific RecA homolog Mol. Cell 1 1998 697 705
44. Prophet, E.B. (1994). Laboratory Methods in Histotechnology, Third Edition (Washington, D.C.; American Registry of Pathology). i
45. Raman R. Das P. Mammalian sex chromosomes. III. Activity of pseudoautosomal steroid sulfatase enzyme during spermatogenesis in Mus musculus Somat. Cell Mol. Genet. 17 1991 429 433
46. Rappold G.A. The pseudoautosomal regions of the human sex chromosomes Hum. Genet. 92 1993 315 324
47. Redon C. Pilch D. Rogakou E. Sedelnikova O. Newrock K. Bonner W. Histone H2A variants H2AX and H2AZ Curr. Opin. Genet. Dev. 12 2002 162 169
48. Richler C. Ast G. Goitein R. Wahrman J. Sperling R. Sperling J. Splicing components are excluded from the transcriptionally inactive XY body in male meiotic nuclei Mol. Biol. Cell 5 1994 1341 1352
49. Richler C. Dhara S.K. Wahrman J. Histone macroH2A1.2 is concentrated in the XY compartment of mammalian male meiotic nuclei Cytogenet. Cell Genet. 89 2000 118 120
50. Roeder G.S. Bailis J.M. The pachytene checkpoint Trends Genet. 16 2000 395 403
51. Romanienko P.J. Camerini-Otero R.D. The mouse Spo11 gene is required for meiotic chromosome synapsis Mol. Cell 6 2000 975 987
52. Scully R. Chen J. Plug A. Xiao Y. Weaver D. Feunteun J. Ashley T. Livingston D.M. Association of BRCA1 with Rad51 in mitotic and meiotic cells Cell 88 1997 265 275
53. Singer-Sam J. Robinson M.O. Bellve A.R. Simon M.I. Riggs A.D. Measurement by quantitative PCR of changes in HPRT, PGK-1, PGK-2, APRT, MTase, and Zfy gene transcripts during mouse spermatogenesis Nucleic Acids Res. 18 1990 1255 1259
54. Smith A. Benavente R. Meiosis-specific protein selectively associated with sex chromosomes of rat pachytene spermatocytes Proc. Natl. Acad. Sci. USA 89 1992 6938 6942
55. Smith A. Benavente R. An Mr 51,000 protein of mammalian spermatogenic cells that is common to the whole XY body and centromeric heterochromatin of autosomes Chromosoma 103 1995 591 596
56. Solari A. The behavior of the XY pair in mammals Int. Rev. Cytol. 38 1974 273 317
57. Strahl B.D. Allis C.D. The language of covalent histone modifications Nature 403 2000 41 45
58. Turner J.M. Burgoyne P.S. Singh P.B. M31 and macroH2A1.2 colocalise at the pseudoautosomal region during mouse meiosis J. Cell Sci. 114 2001 3367 3375
59. Turner J.M. Mahadevaiah S.K. Benavente R. Offenberg H.H. Heyting C. Burgoyne P.S. Analysis of male meiotic "sex body" proteins during XY female meiosis provides new insights into their functions Chromosoma 109 2000 426 432
60. Turner J.M. Mahadevaiah S.K. Elliott D.J. Garchon H.J. Pehrson J.R. Jaenisch R. Burgoyne P.S. Meiotic sex chromosome inactivation in male mice with targeted disruptions of Xist J. Cell Sci. 115 2002 4097 4105
61. Turner, J.M.A. (2000). An investigation into the role of sex chromosome synapsis in meiotic sex chromosome inactivation and fertility. PhD thesis, University College, London.
62. van Gent D.C. Hoeijmakers J.H. Kanaar R. Chromosomal stability and the DNA double-stranded break connection Nat. Rev. Genet. 2 2001 196 206
63. Ward I.M. Chen J. Histone H2AX is phosphorylated in an ATR-dependent manner in response to replicational stress J. Biol. Chem. 276 2001 47759 47762
64. Wiltshire T. Park C. Handel M.A. Chromatin configuration during meiosis I prophase of spermatogenesis Mol. Reprod. Dev. 49 1998 70 80
65. Yoshida K. Kondoh G. Matsuda Y. Habu T. Nishimune Y. Morita T. The mouse RecA-like gene Dmc1 is required for homologous chromosome synapsis during meiosis Mol. Cell 1 1998 707 718