BRIT1/MCPH1 is essential for mitotic and meiotic recombination DNA repair and maintaining genomic stability in mice

PLoS Genetics

Volumn 6, Issue 1, 2010, Pages

  Liang, Yulong ^a   Gao, Hong ^a   Lin, Shiaw Yih ^b   Peng, Guang ^b   Huang, Xingxu ^a,c   Zhang, Pumin ^a   Goss, John A ^a   Brunicardi, Francis C ^a   Multani, Asha S ^b   Chang, Sandy ^b   Li, Kaiyi ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^c NANJING UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BRIT1 PROTEIN; DOUBLE STRANDED DNA; PROTEIN; UNCLASSIFIED DRUG; MCPH1 PROTEIN, MOUSE; NONHISTONE PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER INHIBITION; CHROMOSOME PAIRING; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; DNA STRAND BREAKAGE; FIBROBLAST; GAMMA IRRADIATION; GENETIC STABILITY; GENOMIC INSTABILITY; HYPERSENSITIVITY; IN VITRO STUDY; INFERTILITY; MALE; MEIOSIS; MITOSIS; MOUSE; MOUSE EMBRYO; NONHUMAN; PROPHASE; PROTEIN DOMAIN; SIGNAL TRANSDUCTION; SPERMATOCYTE; T LYMPHOCYTE; ANIMAL; GENETIC RECOMBINATION; GENETICS; METABOLISM; MOUSE MUTANT;

MUS; SYNAPSIS;

ANIMALS; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA REPAIR; GENOMIC INSTABILITY; MEIOSIS; MICE; MICE, KNOCKOUT; MITOSIS; RECOMBINATION, GENETIC;

EID: 76749170775     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1000826     Document Type: Article

References (51)

1. Pastink A, Eeken JC, Lohman PH (2001) Genomic integrity and the repair of double-strand DNA breaks. Mutat Res 480-481: 37-50.
2. Franco S, Alt FW, Manis JP (2006) Pathways that suppress programmed DNA breaks from progressing to chromosomal breaks and translocations. DNA Repair 5: 1030-1041.
3. Pandita TK, Hittelman WN (1992) The contribution of DNA and chromosome repair deficiencies to the radiosensitivity of ataxia-telangiectasia. Radiat Res 131: 214-223.
4. Kuzminov A (1995) Collapse and repair of replication forks in Escherichia coli. Mol Microbiol 16: 373-384.
5. Richardson C, Horikoshi N, Pandita TK (2004) The role of the DNA doublestrand break response network in meiosis. DNA Repair 3: 1149-1164.
6. Rooney S, Chaudhuri J, FW Alt. (2004) The role of the non-homologous endjoining pathway in lymphocyte development. Immunol Rev 200: 115-131.
7. Zhou BB, Elledge SJ (2000) The DNA damage response: putting checkpoints in perspective. Nature 408: 433-439.
8. Rouse J, Jackson SP (2002) Interfaces between the detection, signaling, and repair of DNA damage. Science 297: 547-551.
9. 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.
10. Paull TT, Rogakou EP, Yamazaki V, Kirchgessner CU, Gellert M, et al. (2000) A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage. Curr Biol 10: 886-895.
11. Chapman JR, Jackson SP (2008) Phospho-dependent interactions between NBS1 and MDC1 mediate chromatin retention of the MRN complex at sites of DNA damage. EMBO Rep 9: 795-801.
12. Schultz LB, Chehab NH, Malikzay A, Halazonetis TD (2000) p53 binding protein 1 (53BP1) is an early participant in the cellular response to DNA doublestrand breaks. J Cell Biol 151: 1381-1390.
13. Rappold I, Iwabuchi K, Date T, Chen J (2001) Tumor suppressor p53 binding protein 1 (53BP1) is involved in DNA damage-signaling pathways. J Cell Biol 153: 613-620.
14. Sung P, Krejci L, Van Komen S, Sehorn MG (2003) Rad51 recombinase and recombination mediators. J Biol Chem 278: 42729-42732.
15. Scully R, Chen J, Ochs RL, Keegan K, Hoekstra M, et al. (1997) Dynamic changes of BRCA1 subnuclear location and phosphorylation state are initiated by DNA damage. Cell 90: 425-435.
16. Thorslund T, West SC (2007) BRCA2: a universal recombinase regulator. Oncogene 26: 7720-7730.
17. Lin SY, Rai R, Li K, Xu ZX, Elledge SJ (2005) BRIT1/MCPH1 is a DNA damage responsive protein that regulates the Brca1-Chk1 pathway, implicating checkpoint dysfunction in microcephaly. Proc Natl Acad Sci USA 102: 15105-15109.
18. Rai R, Dai H, Multani AS, Li K, Chin K, et al. (2006) BRIT1 regulates early DNA damage response, chromosomal integrity, and cancer. Cancer Cell 10: 145-157.
19. Jackson AP, Eastwood H, Bell SM, Adu J, Toomes C, et al. (2002) Identification of microcephalin, a protein implicated in determining the size of the human brain. Am J Hum Genet 71: 136-142.
20. Xu X, Lee J, Stern DF (2004) Microcephalin is a DNA damage response protein involved in regulation of CHK1 and BRCA1. J Biol Chem 279: 34091-34094.
21. Alderton GK, Galbiati L, Griffith E, Surinya KH, Neitzel H, et al. (2006) Regulation of mitotic entry by microcephalin and its overlap with ATR signalling. Nat Cell Biol 8: 725-733.
22. Sonoda E, Sasaki MS, Morrison C, Yamaguchi-Iwai Y, Takata M, et al. (1999) Sister chromatid exchanges are mediated by homologous recombination in vertebrate cells. Mol Cell Biol 19: 5166-5169.
23. González-Barrera S, Cortés-Ledesma F, Wellinger RE, Aguilera A (2003) Equal sister chromatid exchange is a major mechanism of double-strand break repair in yeast. Mol Cell 11: 1661-1671.
24. Wood JL, Liang Y, Li K, Chen J (2008) Microcephalin/MCPH1 associates with the Condensin II complex to function in homologous recombination repair. J Biol Chem 283: 29586-29592.
25. Peng G, Yim EK, Dai H, Jackson AP, Burgt I, et al. (2009) BRIT1/MCPH1 links chromatin remodelling to DNA damage response. Nat Cell Biol 11: 865-872.
26. Bellvé AR, Cavicchia JC, Millette CF, O'Brien DA, Bhatnagar YM, et al. (1977) Spermatogenic cells of the prepuberal mouse. Isolation and morphological characterization. J Cell Biol 74: 68-85.
27. Zhao GQ, Garbers DL (2002) Male germ cell specification and differentiation. Dev Cell 2: 537-547.
28. Dobson MJ, Pearlman RE, Karaiskakis A, Spyropoulos B, Moens PB (1994) Synaptonemal complex proteins: occurrence, epitope mapping and chromosome disjunction. J Cell Sci 107: 2749-2760.
29. Schalk JA, Dietrich AJ, Vink AC, Offenberg HH, van Aalderen M, et al. (1998) Localization of SCP2 and SCP3 protein molecules within synaptonemal complexes of the rat. Chromosoma 107: 540-548.
30. Dietrich AJ, Mulder RJ (1983) A light- and electron microscopic analysis of meiotic prophase in female mice. Chromosoma 88: 377-385.
31. de Vries FA, de Boer E, van den Bosch BM, Baarends WM, Ooms M, et al. (2005) Mouse Sycp1 functions in synaptonemal complex assembly, meiotic recombination, and XY body formation. Genes Dev 19: 1376-1389.
32. 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.
33. Fernandez-Capetillo O, Lee A, Nussenzweig M, Nussenzweig A (2004) H2AX: the histone guardian of the genome. DNA Repair 3: 959-967.
34. Kinner A, Wu W, Staudt C, Iliakis G (2008) Gamma-H2AX in recognition and signaling of DNA double-strand breaks in the context of chromatin. Nucleic Acids Res 36: 5678-5694.
35. Keeney S (2001) Mechanism and control of meiotic recombination initiation. Curr Top Dev Biol 52: 1-53.
36. Mahadevaiah SK, Turner JM, Baudat F, Rogakou EP, de Boer P, et al. (2001) Recombinational DNA double-strand breaks in mice precede synapsis. Nat Genet 27: 271-276.
37. Ogawa T, Yu X, Shinohara A, Egelman EH (1993) Similarity of the yeast RAD51 filament to the bacterial RecA filament. Science 259: 1896-1899.
38. Tarsounas M, Morita T, Pearlman RE, Moens PB (1999) RAD51 and DMC1 form mixed complexes associated with mouse meiotic chromosome cores and synaptonemal complexes. J Cell Biol 147: 207-220.
39. Wu X, Mondal G, Wang X, Wu J, Yang L, et al. (2009) Microcephalin regulates BRCA2 and Rad51-associated DNA double-strand break repair. Cancer Res 69: 5531-5536.
40. Xu Y, Ashley T, Brainerd EE, Bronson RT, Meyn MS, et al. (1996) Targeted disruption of ATM leads to growth retardation, chromosomal fragmentation during meiosis, immune defects, and thymic lymphoma. Genes Dev 10: 2411-2422.
41. Celeste A, Petersen S, Romanienko PJ, Fernandez-Capetillo O, Chen HT, et al. (2002) Genomic instability in mice lacking histone H2AX. Science 296: 922-927.
42. 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.
43. Yang SZ, Lin FT, Lin WC (2008) MCPH1/BRIT1 cooperates with E2F1 in the activation of checkpoint, DNA repair and apoptosis. EMBO Rep 9: 907-915.
44. Sharan SK, Pyle A, Coppola V, Babus J, Swaminathan S, et al. (2004) BRCA2 deficiency in mice leads to meiotic impairment and infertility. Development 131: 131-142.
45. 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.
46. 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.
47. Li K, Ramirez MA, Rose E, Beaudet AL (2002) A gene fusion method to screen for regulatory effects on gene expression: application to the LDL receptor. Hum Mol Genet 11: 3257-3265.
48. Ward IM, Minn K, van Deursen J, Chen J (2003) p53 Binding protein 53BP1 is required for DNA damage responses and tumor suppression in mice. Mol Cell Biol 23: 2556-2563.
49. Mei J, Huang X, Zhang P (2001) Securin is not required for cellular viability, but is required for normal growth of mouse embryonic fibroblasts. Curr Biol 11: 1197-1201.
50. Peters AH, Plug AW, van Vugt MJ, de Boer P (1997) A drying-down technique for the spreading of mammalian meiocytes from the male and female germline. Chromosome Res 5: 66-68.
51. Baart EB, de Rooij DG, Keegan KS, de Boer P (2000) Distribution of Atr protein in primary spermatocytes of a mouse chromosomal mutant: a comparison of preparation techniques. Chromosoma 109: 139-147.