Mouse Rad9b is essential for embryonic development and promotes resistance to DNA damage

Developmental Dynamics

Volumn 239, Issue 11, 2010, Pages 2837-2850

  Leloup, Corinne ^a   Hopkins, Kevin M ^a   Wang, Xiangyuan ^b   Zhu, Aiping ^a   Wolgemuth, Debra J ^b   Lieberman, Howard B ^a,c  

^a Columbia University ^*  (United States)

^b NewYork Presbyterian Hospital   (United States)

^c NONE   (United States)

Author keywords

Cell cycle; DNA damage sensitivity; Embryonic development; Mrad9; Mrad9b

Indexed keywords

MITOMYCIN C; NUCLEIC ACID BINDING PROTEIN; PROTEIN RAD9B; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL VIABILITY; CONTROLLED STUDY; DNA DAMAGE; DRUG SENSITIVITY; EMBRYO DEVELOPMENT; EMBRYONIC STEM CELL; FEMALE; FIBROBLAST; GAMMA RADIATION; GENE DELETION; GENE EXPRESSION; GENE TARGETING; GENOMIC INSTABILITY; HETEROZYGOTE; MALE; MOUSE; MOUSE MUTANT; NERVOUS SYSTEM DEVELOPMENT; NEURAL TUBE; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; PROTEIN FUNCTION; RADIOSENSITIVITY;

ANIMALS; BLOTTING, NORTHERN; BLOTTING, SOUTHERN; CELL CYCLE; CELL CYCLE PROTEINS; CELL PROLIFERATION; CELL SURVIVAL; DNA DAMAGE; EMBRYO, MAMMALIAN; EMBRYONIC DEVELOPMENT; EMBRYONIC STEM CELLS; FEMALE; FLOW CYTOMETRY; G2 PHASE; IN SITU HYBRIDIZATION; MALE; MICE; MICE, INBRED C57BL; MITOSIS; POLYMERASE CHAIN REACTION; SISTER CHROMATID EXCHANGE;

MUS;

EID: 77958604345     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.22415     Document Type: Article

References (60)

1. Budzowska M, Jaspers I, Essers J, de Waard H, van Drunen E, Hanada K, Beverloo B, Hendriks RW, de Klein A, Kanaar R, Hoeijmakers JH, Maas A. 2004. Mutation of the mouse Rad17 gene leads to embryonic lethality and reveals a role in DNA damage-dependent recombination. EMBO J 23: 3548-3558.
2. Cang Y, Zhang J, Nicholas SA, Bastien J, Li B, Zhou P, Goff SP. 2006. Deletion of DDB1 in mouse brain and lens leads to p53-dependent elimination of proliferating cells. Cell 127: 929-940.
3. Chapman DL, Wolgemuth DJ. 1994. Expression of proliferating cell nuclear antigen in the mouse germ line and surrounding somatic cells suggests both proliferation-dependent and -independent modes of function. Int J Dev Biol 38: 491-497.
4. de Waard H, Sonneveld E, de Wit J, Esveldt-van Lange R, Hoeijmakers JH, Vrieling H, van der Horst GT. 2008. Cell-type-specific consequences of nucleotide excision repair deficiencies: Embryonic stem cells versus fibroblasts. DNA Repair (Amst) 7: 1659-1669.
5. Dianov GL, Parsons JL. 2007. Co-ordination of DNA single strand break repair. DNA Repair (Amst) 6: 454-460.
6. Dufault VM, Oestreich AJ, Vroman BT, Karnitz LM. 2003. Identification and characterization of RAD9B, a paralog of the RAD9 checkpoint gene. Genomics 82: 644-651.
7. Fenech M. 2000. The in vitro micronucleus technique. Mutat Res 455: 81-95.
8. Frank KM, Sekiguchi JM, Seidl KJ, Swat W, Rathbun GA, Cheng HL, Davidson L, Kangaloo L, Alt FW. 1998. Late embryonic lethality and impaired V(D)J recombination in mice lacking DNA ligase IV. Nature 396: 173-177.
9. Friedberg EC, Meira LB. 2006. Database of mouse strains carrying targeted mutations in genes affecting biological responses to DNA damage Version 7. DNA Repair (Amst) 5: 189-209.
10. Fuertes MA, Alonso C, Perez JM. 2003. Biochemical modulation of Cisplatin mechanisms of action: enhancement of antitumor activity and circumvention of drug resistance. Chem Rev 103: 645-662.
11. Gao Y, Sun Y, Frank KM, Dikkes P, Fujiwara Y, Seidl KJ, Sekiguchi JM, Rathbun GA, Swat W, Wang J, Bronson RT, Malynn BA, Bryans M, Zhu C, Chaudhuri J, Davidson L, Ferrini R, Stamato T, Orkin SH, Greenberg ME, Alt FW. 1998. A critical role for DNA end-joining proteins in both lymphogenesis and neurogenesis. Cell 95: 891-902.
12. Gowen LC, Johnson BL, Latour AM, Sulik KK, Koller BH. 1996. Brca1 deficiency results in early embryonic lethality characterized by neuroepithelial abnormalities. Nat Genet 12: 191-194.
13. Gu Y, Jin S, Gao Y, Weaver DT, Alt FW. 1997. Ku70-deficient embryonic stem cells have increased ionizing radiosensitivity, defective DNA end-binding activity, and inability to support V(D)J recombination. Proc Natl Acad Sci USA 94: 8076-8081.
14. Hakem R, de la Pompa JL, Sirard C, Mo R, Woo M, Hakem A, Wakeham A, Potter J, Reitmair A, Billia F, Firpo E, Hui CC, Roberts J, Rossant J, Mak TW. 1996. The tumor suppressor gene Brca1 is required for embryonic cellular proliferation in the mouse. Cell 85: 1009-1023.
15. Hanawalt PC, Spivak G. 2008. Transcription-coupled DNA repair: two decades of progress and surprises. Nat Rev Mol Cell Biol 9: 958-970.
16. Hanks MC, Loomis CA, Harris E, Tong CX, Anson-Cartwright L, Auerbach A, Joyner A. 1998. Drosophila engrailed can substitute for mouse Engrailed1 function in mid-hindbrain, but not limb development. Development 125: 4521-4530.
17. Harris MJ, Juriloff DM. 1999. Mini-review: toward understanding mechanisms of genetic neural tube defects in mice. Teratology 60: 292-305.
18. Helt CE, Wang W, Keng PC, Bambara RA. 2005. Evidence that DNA damage detection machinery participates in DNA repair. Cell Cycle 4: 529-532.
19. Herrera RE, Sah VP, Williams BO, Makela TP, Weinberg RA, Jacks T. 1996. Altered cell cycle kinetics, gene expression, and G1 restriction point regulation in Rb-deficient fibroblasts. Mol Cell Biol 16: 2402-2407.
20. Hogan B. BR, Costantini F., Lacy E. 1994. Manipulating the mouse embryo. A laboratory manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
21. Hopkins KM, Wang X, Berlin A, Hang H, Thaker HM, Lieberman HB. 2003. Expression of mammalian paralogues of HRAD9 and Mrad9 checkpoint control genes in normal and cancerous testicular tissue. Cancer Res 63: 5291-5298.
22. Hopkins KM, Auerbach W, Wang XY, Hande MP, Hang H, Wolgemuth DJ, Joyner AL, Lieberman HB. 2004. Deletion of mouse rad9 causes abnormal cellular responses to DNA damage, genomic instability, and embryonic lethality. Mol Cell Biol 24: 7235-7248.
23. Hu Z, Liu Y, Zhang C, Zhao Y, He W, Han L, Yang L, Hopkins KM, Yang X, Lieberman HB, Hang H. 2008. Targeted deletion of Rad9 in mouse skin keratinocytes enhances genotoxin-induced tumor development. Cancer Res 68: 5552-5561.
24. Jeggo P, Lobrich M. 2006. Radiation-induced DNA damage responses. Radiat Prot Dosimetry 122: 124-127.
25. Johnston DS, Wright WW, Dicandeloro P, Wilson E, Kopf GS, Jelinsky SA. 2008. Stage-specific gene expression is a fundamental characteristic of rat spermatogenic cells and Sertoli cells. Proc Natl Acad Sci USA 105: 8315-8320.
26. Joyner AL. 2000. Gene targeting: a practical approach, 2d ed. New York: IRL Press.
27. Kaufman MH. 1995. The atlas of mouse development. New York: Academic Press Limited.
28. Larminat F, Cambois G, Zdzienicka MZ, Defais M. 1998. Lack of correlation between repair of DNA interstrand cross-links and hypersensitivity of hamster cells towards mitomycin C and cisplatin. FEBS Lett 437: 97-100.
29. Lieberman HB. 2006. Rad9, an evolutionarily conserved gene with multiple functions for preserving genomic integrity. J Cell Biochem 97: 690-697.
30. Lim DS, Hasty P. 1996. A mutation in mouse rad51 results in an early embryonic lethal that is suppressed by a mutation in p53. Mol Cell Biol 16: 7133-7143.
31. Liu CY, Flesken-Nikitin A, Li S, Zeng Y, Lee WH. 1996. Inactivation of the mouse Brca1 gene leads to failure in the morphogenesis of the egg cylinder in early postimplantation development. Genes Dev 10: 1835-1843.
32. Liu Q, Guntuku S, Cui XS, Matsuoka S, Cortez D, Tamai K, Luo G, Carattini-Rivera S, DeMayo F, Bradley A, Donehower LA, Elledge SJ. 2000. Chk1 is an essential kinase that is regulated by Atr and required for the G(2)/M DNA damage checkpoint. Genes Dev 14: 1448-1459.
33. Loeb LA, Harris CC. 2008. Advances in chemical carcinogenesis: a historical review and prospective. Cancer Res 68: 6863-6872.
34. Ludwig T, Chapman DL, Papaioannou VE, Efstratiadis A. 1997. Targeted mutations of breast cancer susceptibility gene homologs in mice: lethal phenotypes of Brca1, Brca2, Brca1/Brca2, Brca1/p53, and Brca2/p53 nullizygous embryos. Genes Dev 11: 1226-1241.
35. Luo G, Yao MS, Bender CF, Mills M, Bladl AR, Bradley A, Petrini JH. 1999. Disruption of mRad50 causes embryonic stem cell lethality, abnormal embryonic development, and sensitivity to ionizing radiation. Proc Natl Acad Sci USA 96: 7376-7381.
36. McHugh PJ, Spanswick VJ, Hartley JA. 2001. Repair of DNA interstrand crosslinks: molecular mechanisms and clinical relevance. Lancet Oncol 2: 483-490.
37. Menon SG, Sarsour EH, Spitz DR, Higashikubo R, Sturm M, Zhang H, Goswami PC. 2003. Redox regulation of the G1 to S phase transition in the mouse embryo fibroblast cell cycle. Cancer Res 63: 2109-2117.
38. Ng JM, Vrieling H, Sugasawa K, Ooms MP, Grootegoed JA, Vreeburg JT, Visser P, Beems RB, Gorgels TG, Hanaoka F, Hoeijmakers JH, van der Horst GT. 2002. Developmental defects and male sterility in mice lacking the ubiquitin-like DNA repair gene mHR23B. Mol Cell Biol 22: 1233-1245.
39. Niida H, Nakanishi M. 2006. DNA damage checkpoints in mammals. Mutagenesis 21: 3-9.
40. Nussenzweig A, Chen C, da Costa Soares V, Sanchez M, Sokol K, Nussenzweig MC, Li GC. 1996. Requirement for Ku80 in growth and immunoglobulin V(D)J recombination. Nature 382: 551-555.
41. Orii KE, Lee Y, Kondo N, McKinnon PJ. 2006. Selective utilization of nonhomologous end-joining and homologous recombination DNA repair pathways during nervous system development. Proc Natl Acad Sci USA 103: 10017-10022.
42. Palom Y, Suresh Kumar G, Tang LQ, Paz MM, Musser SM, Rockwell S, Tomasz M. 2002. Relative toxicities of DNA cross-links and monoadducts: new insights from studies of decarbamoyl mitomycin C and mitomycin C. Chem Res Toxicol 15: 1398-1406.
43. Pandita RK, Sharma GG, Laszlo A, Hopkins KM, Davey S, Chakhparonian M, Gupta A, Wellinger RJ, Zhang J, Powell SN, Roti Roti JL, Lieberman HB, Pandita TK. 2006. Mammalian Rad9 plays a role in telomere stability, S- and G2-phase-specific cell survival, and homologous recombinational repair. Mol Cell Biol 26: 1850-1864.
44. Pietenpol JA, Stewart ZA. 2002. Cell cycle checkpoint signaling: cell cycle arrest versus apoptosis. Toxicology 181-182: 475-481.
45. Rabik CA, Dolan ME. 2007. Molecular mechanisms of resistance and toxicity associated with platinating agents. Cancer Treat Rev 33: 9-23.
46. Robertson AB, Klungland A, Rognes T, Leiros I. 2009. Base excision repair: the long and short of it. Cell Mol Life Sci 66: 981-983.
47. Sah VP, Attardi LD, Mulligan GJ, Williams BO, Bronson RT, Jacks T. 1995. A subset of p53-deficient embryos exhibit exencephaly. Nat Genet 10: 175-180.
48. Sega GA. 1984. A review of the genetic effects of ethyl methanesulfonate. Mutat Res 134: 113-142.
49. Sharan SK, Morimatsu M, Albrecht U, Lim DS, Regel E, Dinh C, Sands A, Eichele G, Hasty P, Bradley A. 1997. Embryonic lethality and radiation hypersensitivity mediated by Rad51 in mice lacking Brca2. Nature 386: 804-810.
50. Sobol RW, Horton JK, Kuhn R, Gu H, Singhal RK, Prasad R, Rajewsky K, Wilson SH. 1996. Requirement of mammalian DNA polymerase-beta in base-excision repair. Nature 379: 183-186.
51. Suzuki A, de la Pompa JL, Hakem R, Elia A, Yoshida R, Mo R, Nishina H, Chuang T, Wakeham A, Itie A, Koo W, Billia P, Ho A, Fukumoto M, Hui CC, Mak TW. 1997. Brca2 is required for embryonic cellular proliferation in the mouse. Genes Dev 11: 1242-1252.
52. Tebbs RS, Flannery ML, Meneses JJ, Hartmann A, Tucker JD, Thompson LH, Cleaver JE, Pedersen RA. 1999. Requirement for the Xrcc1 DNA base excision repair gene during early mouse development. Dev Biol 208: 513-529.
53. Warren AJ, Ihnat MA, Ogdon SE, Rowell EE, Hamilton JW. 1998. Binding of nuclear proteins associated with mammalian DNA repair to the mitomycin C-DNA interstrand crosslink. Environ Mol Mutagen 31: 70-81.
54. Weiss RS, Enoch T, Leder P. 2000. Inactivation of mouse Hus1 results in genomic instability and impaired responses to genotoxic stress. Genes Dev 14: 1886-1898.
55. Xiao Y, Weaver DT. 1997. Conditional gene targeted deletion by Cre recombinase demonstrates the requirement for the double-strand break repair Mre11 protein in murine embryonic stem cells. Nucleic Acids Res 25: 2985-2991.
56. Yin Y, Zhu A, Jin YJ, Liu YX, Zhang X, Hopkins KM, Lieberman HB. 2004. Human RAD9 checkpoint control/proapoptotic protein can activate transcription of p21. Proc Natl Acad Sci USA 101: 8864-8869.
57. Zha S, Alt FW, Cheng HL, Brush JW, Li G. 2007. Defective DNA repair and increased genomic instability in Cernunnos-XLF-deficient murine ES cells. Proc Natl Acad Sci USA 104: 4518-4523.
58. Zhong Q, Boyer TG, Chen PL, Lee WH. 2002. Deficient nonhomologous end-joining activity in cell-free extracts from Brca1-null fibroblasts. Cancer Res 62: 3966-3970.
59. Zhu A, Zhang CX, Lieberman HB. 2008. Rad9 has a functional role in human prostate carcinogenesis. Cancer Res 68: 1267-1274.
60. Zhu J, Petersen S, Tessarollo L, Nussenzweig A. 2001. Targeted disruption of the Nijmegen breakage syndrome gene NBS1 leads to early embryonic lethality in mice. Curr Biol 11: 105-109.