Differences in DNA double strand breaks repair in male germ cell types: Lessons learned from a differential expression of Mdc1 and 53BP1

DNA Repair

Volumn 6, Issue 9, 2007, Pages 1243-1254

  Ahmed, Emad A ^a   van der Vaart, Aniek ^a   Barten, Angeliqué ^b   Kal, Henk B ^b   Chen, Junjie ^c   Lou, Zhenkun ^c   Minter Dykhouse, Katherine ^c   Bartkova, Jirina ^d   Bartek, Jiri ^d   de Boer, Peter ^e   de Rooij, Dirk G ^a,b  

^a UTRECHT UNIVERSITY   (Netherlands)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^c MAYO CLINIC   (United States)

^d DANISH CANCER SOCIETY RESEARCH CENTER   (Denmark)

^e RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

53BP1; DNA repair; Mdc1; Meiosis; Rad51; Spermatogenesis

Indexed keywords

ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL CYCLE S PHASE; CELL TYPE; COMPARATIVE STUDY; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; DNA STRAND BREAKAGE; EPITHELIUM; EVOLUTION; GERM CELL; HAPLOIDY; IRRADIATION; MALE; MEIOSIS; MOUSE; NONHUMAN; PACHYTENE; PRIORITY JOURNAL; PROPHASE; PROTEIN EXPRESSION; RADIOSENSITIVITY; SOMATIC CELL; SPERMATID; SPERMATOCYTE; SPERMATOGONIUM;

ANIMALS; DNA; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; DOSE-RESPONSE RELATIONSHIP, RADIATION; FLUORESCENT ANTIBODY TECHNIQUE; GERM CELLS; HISTONES; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MEIOSIS; MICE; MICE, INBRED STRAINS; MICE, KNOCKOUT; PHOSPHOPROTEINS; RAD51 RECOMBINASE; SPERMATOCYTES; SPERMATOGONIA; X-RAYS;

MUS;

EID: 34547800719     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2007.02.011     Document Type: Article

References (41)

1. van Gent D.C., Hoeijmakers J.H., and Kanaar R. Chromosomal stability and the DNA double-stranded break connection. Nat. Rev. Genet. 2 (2001) 196-206
2. Lukas J., Lukas C., and Bartek J. Mammalian cell cycle checkpoints: signalling pathways and their organization in space and time. DNA Rep. 3 (2004) 997-1007
3. Hoeijmakers J.H. Genome maintenance mechanisms for preventing cancer. Nature 411 (2001) 366-374
4. Stucki M., and Jackson S.P. GammaH2AX and MDC1: anchoring the DNA-damage-response machinery to broken chromosomes. DNA Rep. 5 (2006) 534-543
5. Kastan M.B., and Bartek J. Cell cycle checkpoints. Nature 432 (2004) 316-323
6. Stewart G.S., Wang B., Bignell R.C., Taylor A.M., and Elledge S.J. MDC1 is a mediator of the mammalian DNA damage checkpoint. Nature 421 (2003) 961-966
7. Goldberg M., Stucki M., Falck J., D'Amours D., Rahman D., Pappin D., Bartek J., and Jackson S.P. MDC1 is required for the intra-S-phase DNA damage checkpoint. Nature 421 (2003) 952-956
8. Lou Z., Minter-Dykhouse K., Franco S., Gostissa M., Rivera M.A., Celeste A., Manis J.P., van Deursen J., Nussenzweig A., Paull T.T., Alt F.W., and Chen J. MDC1 maintains genomic stability by participating in the amplification of ATM-dependent DNA damage signals. Mol. Cell. 21 (2006) 87-200
9. Wang B., Matsuoka S., Carpenter P.B., and Elledge S.J. 53BP1, a mediator of the DNA damage checkpoint. Science 298 (2002) 1435-1438
10. Xu X., and Stern D.F. NFBD1/MDC1 regulates ionizing radiation-induced focus formation by DNA checkpoint signaling and repair factors. FASEB J. 17 (2003) 1842-1848
11. Lou Z., Chini C.C., Minter-Dykhouse K., and Chen J. Mediator of DNA damage checkpoint protein 1 regulates BRCA1 localization and phosphorylation in DNA damage checkpoint control. J. Biol. Chem. 278 (2003) 13599-13602
12. Lou Z., Chen B.P., Asaithamby A., Minter-Dykhouse K., Chen D.J., and Chen J. MDC1 regulates DNA-PK autophosphorylation in response to DNA damage. J. Biol. Chem. 279 (2004) 46359-46362
13. Bekker-Jensen S., Lukas C., Melander F., Bartek J., and Lukas J. Dynamic assembly and sustained retention of 53BP1 at the sites of DNA damage are controlled by Mdc1/NFBD. J. Cell Biol. 170 (2005) 201-211
14. Nakamura K., Sakai W., Kawamoto T., Bree R.T., Lowndes N.F., Takeda S., and Taniguchi Y. Genetic dissection of vertebrate 53BP1: a major role in non-homologous end joining of DNA double strand breaks. DNA Rep. 6 (2006) 741-749
15. Goedecke W., Eijpe M., Offenberg H.H., van Aalderen M., and Heyting C. Mre11 and Ku70 interact in somatic cells, but are differentially expressed in early meiosis. Nat. Genet. 23 (1999) 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., and de Rooij D.G. Function of DNA-protein kinase catalytic subunit during the early meiotic prophase without Ku70 and Ku86. Biol. Reprod. 68 (2003) 717-721
17. Bartkova J., Bakkenist C.J., Rajpert-De Meyts E., Skakkebaek N.E., Sehested M., Lukas J., Kastan M.B., and Bartek J. ATM activation in normal human tissues and testicular Cancer. Cell Cycle 4 (2005) 838-845
18. Bekker-Jensen S., Lukas C., Kitagawa R., Melander F., Kastan M.B., Bartek J., and Lukas J. Spatial organization of the mammalian genome surveillance machinery in response to DNA strand breaks. J. Cell Biol. 173 (2006) 195-206
19. Russel L.D., Ettlin R.A., Hikim A.P., and Clegg E.D. Histological and Histopathological Evaluation of the Testis (1990), Cache River Press, Clearwater, FL, USA
20. Beumer T.L., Roepers-Gajadien H.L., Gademan I.S., van Buul P.P., Gil-Gomez G., Rutgers D.H., and de Rooij D.G. The role of the tumor suppressor p53 in spermatogenesis. Cell Death Diff. 5 (1998) 669-677
21. Xu B., O'Donnell A.H., Kim S.T., and Kastan M. Phosphorylation of serine 1387 in Brca1 is specifically required for the Atm-mediated S-phase checkpoint after ionizing radiation. Cancer Res. 62 (2002) 4588-4591
22. Moses M.J. New cytogenetic studies on mammalian meiosis. In: Serio M., and Martini L. (Eds). Animal Model in Human Reproduction (1980), Raven, New York 169-190
23. Van der Meer Y., Huiskamp R., Davids J., van der Tweel I., and de Rooij D.G. The sensitivity of quiescent and proliferating mouse spermatogonial stem cells to X-irradiation. Radiat. Res. 130 (1992) 289-295
24. Yamamoto T., Hikino T., Nakayama Y., and Abe S. Newt RAD51: cloning of cDNA and analysis of gene expression during spermatogenesis. Dev. Growth Differ. 41 (1999) 401-406
25. Hamer G., Roepers-Gajadien H.L., van Duyn-Goedhart A., Gademan I.S., Kal H.B., van Buul P.P., and de Rooij D.G. DNA double-strand breaks & γ-H2AX signaling in the testis. Biol. Reprod. 68 (2003) 628-634
26. Riballo E., Kuhne M., Rief N., Doherty A., Smith G.C., Recio M.J., Reis C., Dahm K., Fricke A., Krempler A., Parker A.R., Jackson S.P., Gennery A., Jeggo P.A., and Lobrich M. A pathway of double-strand break rejoining dependent upon ATM, Artemis, and proteins locating to gamma-H2AX foci. Mol. Cell. 13 (2004) 715-724
27. Beumer T.L., Roepers-Gajadien H.L., Gademan L.S., Rutgers D.H., and de Rooij D.G. P21(Cip1/WAF1) expression in the mouse testis before and after X irradiation. Mol. Reprod. Dev. 47 (1997) 240-247
28. Van der Meer Y., Huiskamp R., Davids J.A., and de Rooij D.G. Differential effects of fractionated X irradiation on mouse spermatogonial stem cells. Radiat. Res. 135 (1993) 222-228
29. Mahadevaiah S.K., Turner J.M., Baudat F., Rogakou E.P., de Boer P., Blanco-Rodriguez J., Jasin M., Keeney S., Bonner W.M., and Burgoyne P.S. Recombinational DNA double-strand breaks in mice precede synapsis. Nat. Genet. 27 (2001) 271-276
30. de Vries S.S., Baart E.B., Dekker M., Siezen A., de Rooij D.G., de Boer P., and te Riele H. Mouse MutS-like protein Msh5 is required for proper chromosome synapsis in male and female meiosis. Genes Dev. 13 (1999) 523-531
31. de Rooij D.G., and de Boer P. Specific arrests of spermatogenesis in genetically modified and mutant mice. Cytogenet. Genome Res. 103 (2003) 267-276
32. Barchi M., Mahadevaiah S., Di Giacomo M., Baudat F., de Rooij D.G., Burgoyne P.S., Jasin M., and Keeney S. Surveillance of different recombination defects in mouse spermatocytes yields distinct responses despite elimination at an identical developmental stage. Mol. Cell Biol. 25 (2005) 7203-7215
33. Mutsuda Y., and Tobari I. Studies on radiation-induced chromosome aberrations in mouse spermatocytes I Stage specificity and dose-response relationships of chromosome aberrations induced in mouse primary spermatocytes following X-irradiation. Mut. Res. 176 (1987) 243-250
34. Ward I.M., Minn K., van Deursen J., and Chen J. p53 binding protein 53BP1 is required for DNA damage responses and tumor suppression in mice. Mol. Cell Biol. 23 (2003) 2556-2563
35. Huyen Y., Zgheib O., Ditullio Jr. R.A., Gorgoulis V.G., Zacharatos P., Petty T.J., Sheston E.A., Mellert H.S., Stavridi E.S., and Halazonetis T.D. Methylated lysine 79 of histone H3 targets 53BP1 to DNA double-strand breaks. Nature 432 (2004) 406-411
36. Takata M., Sasaki M.S., Sonoda E., Morrison C., Hashimoto M., Utsumi H., Yamaguchi-Iwai Y., Shinohara A., and Takeda S. Homologous recombination and non-homologous end-joining pathways of DNA double-strand break repair have overlapping roles in the maintenance of chromosomal integrity in vertebrate cells. EMBO J. 17 (1998) 5497-5508
37. Matulis S., and Handel M.A. Spermatocyte responses in vitro to induced DNA. Mol. Reprod. Dev. 73 (2005) 1061-1072
38. Hamer G., Kal H.B., Westphal C.H., Ashley T., and de Rooij D.G. Ataxia telangiectasia mutated expression and activation in the testis. Biol. Reprod. 70 (2004) 1206-1212
39. Russell W.L., Bangham J.W., and Russell L.B. Differential response of mouse male germ-cell stages to radiation-induced specific-locus and dominant mutations. Genetics 148 (1998) 1567-1578
40. Tusell L., Latre L., Ponsa I., Miro R., Egozcue J., and Genesca A. Capping of radiation-induced DNA breaks in mouse early embryos. J. Radiat. Res. (Tokyo) 45 (2004) 415-422
41. Marchetti F., and Wyrobek A.J. Mechanisms and consequences of paternally transmitted chromosomal abnormalities. Birth Defects Res. C. Embryo Today 75 (2005) 112-129