Genetic probing of homologous recombination and non-homologous end joining during meiotic prophase in irradiated mouse spermatocytes

Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis

Volumn 688, Issue 1-2, 2010, Pages 12-18

  Ahmed, Emad A ^a,b   Philippens, Marielle E P ^c   Kal, Henk B ^c   de Rooij, Dirk G ^a,d   de Boer, Peter ^e  

^a UTRECHT UNIVERSITY   (Netherlands)

^b Assiut University   (Egypt)

^c UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^d UNIVERSITY OF AMSTERDAM   (Netherlands)

^e RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

DNA repair; RAD54 RAD54B deficient mice; SCID mice; Spermatogenesis

Indexed keywords

HISTONE H2AX; RAD54 PROTEIN; RAD54B PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CROSSING OVER; DNA REPAIR; DOUBLE STRANDED DNA BREAK; HOMOLOGOUS RECOMBINATION; IRRADIATION; MALE; MEIOSIS; MOUSE; NONHOMOLOGOUS END JOINING; NONHUMAN; PACHYTENE; PRIORITY JOURNAL; PROPHASE; SPERMATID; SPERMATOCYTE; SPERMATOGENESIS;

ANIMALS; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; HISTONES; MALE; MEIOTIC PROPHASE I; MICE; MICE, SCID; NUCLEAR PROTEINS; RECOMBINATION, GENETIC; SPERMATOCYTES;

MUS;

EID: 77952881560     PISSN: 00275107     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mrfmmm.2010.02.004     Document Type: Article

References (36)

1. Rogakou E.P., Boon C., Redon C., Bonner W.M. Megabase chromatin domains involved in DNA double-strand breaks in vivo. J. Cell Biol. 1999, 146:905-916.
2. Fernandez-Capetillo O., Lee A., Nussenzweig M., Nussenzweig A. H2AX: the histone guardian of the genome. DNA Repair 2004, 3:959-967.
3. Pilch D.R., Sedelnikova O.A., Redon C., Celeste A., Nussenzweig A., Bonner W.M. Characteristics of gamma-H2AX foci at DNA double-strand breaks sites. Biochem. Cell Biol. 2003, 81:123-129.
4. Ahmed E.A., van der Vaart A., Barten A., Kal H.B., Chen J., Lou Z., Minter-Dykhouse K., Bartkova J., Bartek J., de Boer P., de Rooij D.G. Differences in DNA double strand breaks repair in male germ cell types: lessons learned from a differential expression of Mdc1 and 53BP1. DNA Repair 2007, 6:1243-1254.
5. Chicheportiche A., Bernardino-Sgherri J., de Massy B., Dutrillaux B. Characterization of Spo11-dependent and independent phospho-H2AX foci during meiotic prophase I in the male mouse. J. Cell Sci. 2007, 120:1733-1742.
6. Derijck A., van der Heijden G., Giele M., Philippens M., de Boer P. DNA double-strand break repair in parental chromatin of mouse zygotes, the first cell cycle as an origin of de novo mutation. Hum. Mol. Genet. 2008, 17:1922-1937.
7. 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 2000, 6:989-998.
8. de Vries F.A., de Boer E., van den Bosch M., Baarends W.M., Ooms M., Yuan L., Liu J.G., van Zeeland A.A., Heyting C., Pastink A. Mouse Sycp1 functions in synaptonemal complex assembly, meiotic recombination, and XY body formation. Genes Dev. 2005, 19:1376-1389.
9. 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. 2001, 27:271-276.
10. Schoenmakers S., Wassenaar E., van Cappellen W.A., Derijck A.A., de Boer P., Laven J.S., Grootegoed J.A., Baarends W.M. Increased frequency of asynapsis and associated meiotic silencing of heterologous chromatin in the presence of irradiation-induced extra DNA double strand breaks. Dev. Biol. 2008, 317:270-281.
11. Matulis S., Handel M.A. Spermatocyte responses in vitro to induced DNA damage. Mol. Reprod. Dev. 2006, 73:1061-1072.
12. Bekker-Jensen S., Lukas C., Kitagawa R., Melander F., Kastan M.B., Bartek J., Lukas J. Spatial organization of the mammalian genome surveillance machinery in response to DNA strand breaks. J. Cell Biol. 2006, 173:195-206.
13. Nazarov I.B., Smirnova A.N., Krutilina R.I., Svetlova M.P., Solovjeva L.V., Nikiforov A.A., Oei S.L., Zalenskaya I.A., Yau P.M., Bradbury E.M., Tomilin N.V. Dephosphorylation of histone gamma-H2AX during repair of DNA double-strand breaks in mammalian cells and its inhibition by calyculin A. Radiat. Res. 2003, 160:309-317.
14. Rothkamm K., Kruger I., Thompson L.H., Lobrich M. Pathways of DNA double-strand break repair during the mammalian cell cycle. Mol. Cell. Biol. 2003, 23:5706-5715.
15. Goedecke W., Eijpe M., Offenberg H.H., van Aalderen M., Heyting C. Mre11 and Ku70 interact in somatic cells, but are differentially expressed in early meiosis. Nat. Genet. 1999, 23:194-198.
16. Hamer G., Roepers-Gajadien H.L., van Duyn-Goedhart A., Gademan I.S., Kal H.B., van Buul P.P., Ashley T., de Rooij D.G. Function of DNA-protein kinase catalytic subunit during the early meiotic prophase without Ku70 and Ku86. Biol. Reprod. 2003, 68:717-721.
17. de Rooij D.G., de Boer P. Specific arrests of spermatogenesis in genetically modified and mutant mice. Cytogenet. Genome Res. 2003, 103:267-276.
18. Ahmed E.A., Philippens M.E.P., Kal H.B., de Boer P., de Rooij D.G. Parp1-XRCC1 and the repair of DNA double strand breaks in mouse round spermatids. Mut. Res. 2010, 683:84-90.
19. DiBiase S.J., Zeng Z.C., Chen R., Hyslop T., Curran W.J., Iliakis G. DNA-dependent protein kinase stimulates an independently active, nonhomologous, end-joining apparatus. Cancer Res. 2000, 60:1245-1253.
20. Iliakis G., Wang H., Perrault A.R., Boecker W., Rosidi B., Windhofer F., Wu W., Guan J., Terzoudi G., Pantelias G. Mechanisms of DNA double strand break repair and chromosome aberration formation. Cytogenet. Genome Res. 2004, 104:14-20.
21. Wang H., Zeng Z.C., Perrault A.R., Cheng X., Qin W., Iliakis G. Genetic evidence for the involvement of DNA ligase IV in the DNA-PK-dependent pathway of non-homologous end joining in mammalian cells. Nucleic Acids Res. 2001, 29:1653-1660.
22. Biedermann K.A., Sun J.R., Giaccia A.J., Tosto L.M., Brown J.M. SCID mutation in mice confers hypersensitivity to ionizing radiation and a deficiency in DNA double-strand break repair. Proc. Natl. Acad. Sci. U.S.A. 1991, 88:1394-1397.
23. Essers J., Hendriks R.W., Swagemakers S.M., Troelstra C., de Wit J., Bootsma D., Hoeijmakers J.H., Kanaar R. Disruption of mouse RAD54 reduces ionizing radiation resistance and homologous recombination. Cell 1997, 89:195-204.
24. Wesoly J., Agarwal S., Sigurdsson S., Bussen W., Van Komen S., Qin J., van Steeg H., van Benthem J., Wassenaar E., Baarends W.M., Ghazvini M., Tafel A.A., Heath H., Galjart N., Essers J., Grootegoed J.A., Arnheim N., Bezzubova O., Buerstedde J.M., Sung P., Kanaar R. Differential contributions of mammalian Rad54 paralogs to recombination, DNA damage repair, and meiosis. Mol. Cell. Biol. 2006, 26:976-989.
25. Peters A.H., Plug A.W., van Vugt M.J., de Boer P. A drying-down technique for the spreading of mammalian meiocytes from the male and female germline. Chromosome Res. 1997, 5:66-68.
26. Baart E.B., de Rooij D.G., Keegan K.S., de Boer P. Distribution of Atr protein in primary spermatocytes of a mouse chromosomal mutant: a comparison of preparation techniques. Chromosoma 2000, 109:139-147.
27. Ashley T., Gaeth A.P., Creemers L.B., Hack A.M., de Rooij D.G. Correlation of meiotic events in testis sections and microspreads of mouse spermatocytes relative to the mid-pachytene checkpoint. Chromosoma 2004, 113:126-136.
28. Sciurano R.B., Rahn M.I., Pigozzi M.I., Olmedo S.B., Solari A.J. An azoospermic man with a double-strand DNA break-processing deficiency in the spermatocyte nuclei: case report. Hum. Reprod. 2006, 21:1194-1203.
29. Allen C., Kurimasa A., Brenneman M.A., Chen D.J., Nickoloff J.A. DNA-dependent protein kinase suppresses double-strand break-induced and spontaneous homologous recombination. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:3758-3763.
30. Fukushima T., Takata M., Morrison C., Araki R., Fujimori A., Abe M., Tatsumi K., Jasin M., Dhar P.K., Sonoda E., Chiba T., Takeda S. Genetic analysis of the DNA-dependent protein kinase reveals an inhibitory role of Ku in late S-G2 phase DNA double-strand break repair. J. Biol. Chem. 2001, 276:44413-44418.
31. Romeijn R.J., Gorski M.M., van Schie M.A., Noordermeer J.N., Mullenders L.H., Ferro W., Pastink A. Lig4 and Rad54 are required for repair of DNA double-strand breaks induced by P-element excision in Drosophila. Genetics 2005, 169:795-806.
32. van Buul P.P., Abramsson-Zetterberg L., Zandman I.M., van Duyn-Goedhart A. Further characterization of the radiosensitivity of the SCID mouse. Int. J. Radiat. Biol. 1998, 74:35-41.
33. Little J.B. Genomic instability and bystander effects: a historical perspective. Oncogene 2003, 22:6978-6987.
34. Matsuda Y., Ohara H., Tobari I. Studies on radiation-induced chromosome aberrations in mouse spermatocytes. II. Dose-response relationships of chromosome aberrations induced at zygotene stage in mouse primary spermatocytes following fast neutron- and 60Co gamma-irradiations. Mutat. Res. 1987, 176:251-257.
35. Walker H.C. Comparative sensitivities of meiotic prophase stages in male mice to chromosome damage by acute X-and chronic gamma-irradiation. Mutat. Res. 1977, 44:427-432.
36. Couëdel C., Mills K.D., Barchi M., Shen L., Olshen A., Johnson R.D., Nussenzweig A., Essers J., Kanaar R., Li G.C., Alt F.W., Jasin M. Collaboration of homologous recombination and nonhomologous end-joining factors for the survival and integrity of mice and cells. Genes Dev. 2004, 18:1293-1304.