Enhanced genomic instability and defective postreplication repair in RAD18 knockout mouse embryonic stem cells

Molecular and Cellular Biology

Volumn 23, Issue 2, 2003, Pages 474-481

  Tateishi, Satoshi ^a   Niwa, Hitoshi ^b   Miyazaki, Jun Ichi ^c   Fujimoto, Shiho ^a   Inoue, Hirokazu ^d   Yamaizumi, Masaru ^a  

^a KUMAMOTO UNIVERSITY   (Japan)

^b RIKEN Center for Biosystems Dynamics Research   (Japan)

^c OSAKA UNIVERSITY MEDICAL SCHOOL   (Japan)

^d SAITAMA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

MUTANT PROTEIN; PROTEIN RAD18; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL GROWTH; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; EMBRYO; EMBRYO CELL; GENE CONSTRUCT; GENE EXPRESSION; GENE FREQUENCY; GENE MUTATION; GENE TARGETING; GENETIC STABILITY; GENETIC TRANSFORMATION; GROWTH RATE; KNOCKOUT MOUSE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SEQUENCE HOMOLOGY; SISTER CHROMATID EXCHANGE; STEM CELL; WILD TYPE;

AMINO ACID MOTIFS; ANIMALS; COS CELLS; DNA; DNA DAMAGE; DNA REPAIR; DNA, COMPLEMENTARY; DNA-BINDING PROTEINS; DOSE-RESPONSE RELATIONSHIP, DRUG; GLUTATHIONE TRANSFERASE; HUMANS; IMMUNOHISTOCHEMISTRY; LIGASES; MICE; MICE, KNOCKOUT; MODELS, GENETIC; MUTAGENS; MUTATION; PLASMIDS; PRECIPITIN TESTS; RECOMBINATION, GENETIC; SACCHAROMYCES CEREVISIAE PROTEINS; SISTER CHROMATID EXCHANGE; STEM CELLS; TIME FACTORS; TRANSFECTION; UBIQUITIN-CONJUGATING ENZYMES; ULTRAVIOLET RAYS; X-RAYS;

ANIMALIA; EUKARYOTA; STROPHANTHUS GRATUS; TRIXIS;

EID: 0037218854     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.23.2.474-481.2003     Document Type: Article

References (43)

1. Aboussekhra, A., R. Chanet, Z. Zgaga, C. Cassier-Chauvat, M. Heude, and F. Fabre. 1989. RADH, a gene of Saccharomyces cerevisiae encoding a putative DNA helicase involved in DNA repair. Characteristics of radH mutants and sequence of the gene. Nucleic Acids Res. 17:7211-7219.
2. Araki, K., T. Imaizumi, K. Okuyama, Y. Oike, and K. Yamamura. 1997. Efficiency of recombination by Cre transient expression in embryonic stem cells: comparison of various promoters. J. Biochem. 122:977-982.
3. Araki, K., T. Imaizumi, T. Sekimoto, K. Yoshinobu, J. Yoshimuta, M. Akizuki, K. Miura, M. Araki, and K. Yamamura. 1999. Exchangeable gene trap using the Cre/mutated lox system. Cell Mol. Biol. 45:737-750.
4. Armstrong, J. D., D. N. Chadee, and B. A. Kunz. 1994. Roles for the yeast RAD18 and RAD52 DNA repair genes in UV mutagenesis. Mutat. Res. 315:281-293.
5. Baarends, W. M., R. van der Laan, and J. A. Grootegoed. 2000. Specific aspects of the ubiquitin system in spermatogenesis. J. Endocrinol. Investig. 23:597-604.
6. Bailly, V., J. Lamb, P. Sung, S. Prakash, and L. Prakash. 1994. Specific complex formation between yeast RAD6 and RAD18 proteins: A potential mechanism for targeting RAD6 ubiquitin-conjugating activity to DNA damage sites. Genes Dev. 8:811-820.
7. Bailly, V., S. Prakash, and L. Prakash. 1997. Domains required for dimerization of yeast Rad6 ubiquitin-conjugating enzyme and Rad18 DNA binding protein. Mol. Cell. Biol. 17:4536-4543.
8. Broomfield, S., T. Hryciw, and W. Xiao. 2001. DNA postreplication repair and mutagenesis in Saccharomyces cerevisiae. Mutat. Res. 486:167-184.
9. Cox, M. M., M. F. Goodman, K. N. Kreuzer, D. J. Sherratt, S. J. Sandler, and K. J. Marians. 2000. The importance of repairing stalled replication forks. Nature 404:37-41.
10. Friedberg, E. C., and V. L. Gerlach. 1999. Novel DNA polymerases offer clues to the molecular basis of mutagenesis. Cell 98:413-416.
11. Friedberg, E. C., G. C. Walker, and W. Siede. 1995. DNA Repair and Mutagenesis. ASM Press, Washington, D.C.
12. Friedl, A. A., B. Liefshitz, R. Steinlauf, and M. Kuplec. 2001. Deletion of the SRS2 gene suppresses elevated recombination and DNA damage sensitivity in rad5 and rad18 mutants of Saccharomyces cerevisiae. Mutat. Res. 486:137-146.
13. Geigl, E. M., and F. Eckardt-Schupp. 1991. Repair of gamma ray-induced S1 nuclease hypersensitive sites in yeast depends on homologous mitotic recombination and a RAD18-dependent function. Curr. Genet. 20:33-37.
14. Haber, J. E. 1999. DNA recombination: The replication connection. Trends Biochem. Sci. 24:271-275.
15. Hynes, R. H., and B. A. Kunz. 1981. DNA repair and mutagenesis, p. 371-414. In J. N. Strathern, E. W. Jones, and J. R. Broach (ed.), The Molecular Biology of the Yeast Saccharomyces, vol. 1. Cold Spring Harbor Laboratory Press, Plainview, N.Y.
16. Johnson, R, E., C. M. Kondratick, S. Prakash, and L. Prakash. 1999. hRAD30 mutations in the variant form of xeroderma pigmentosum. Science 285:263-265.
17. Koken, M. H., P. Reynolds, I. Jaspers-Dekker, L. Prakash, S. Prakash, D. Bootsma, and J. H. Hoeijmakers. 1991. Structural and functional conservation of two human homologs of the yeast DNA repair gene RAD6. Proc. Natl. Acad. Sci. USA 88:8865-8869.
18. Kowalczykowski, S. C. 2000. Initiation of genetic recombination and recombination-dependent replication. Trends Biochem. Sci, 25:156-165.
19. Kunz, B. A., A. F. Straffon, and E. J. Vonarx. 2000. DNA damage-induced mutation: Tolerance via translesion synthesis. Mutat. Res. 451:169-185.
20. Kuzminov, A. 2001. DNA replication meets genetic exchange: Chromosomal damage and its repair by homologous recombination. Proc. Natl. Acad. Sci. USA 98:8461-8468.
21. 3H)ouabain and Na pump turnover rates in monolayer cultures of Girardi heart cells. J. Physiol. 213: 57-58.
22. Lawrence, C. W. 1982. Mutagenesis in Saccharomyces cerevisiae. Adv. Genet. 21:173-254.
23. Lawrence, C. W., and R. Christensen. 1976. UV mutagenesis in radiation-sensitive strains of yeast. Genetics 82:207-232.
24. Lehman, A. R., S. Kirk-Bell, C. F. Arlett, M. C. Paterson, P. H. Lohman, E. A. de Weerd-Kastelein, and D. Bootsma. 1975. Xeroderma pigmentosum cells with normal levels of excision repair have a defect in DNA synthesis after UV-irradiation. Proc. Natl. Acad. Sci. USA 72:219-223.
25. Liefshitz, B., R. Steinlauf, A. Friedl, F. Eckardt-Schupp, and M. Kupiec. 1998. Genetic interactions between mutants of the 'error-prone' repair group of Saccharomyces cerevisiae and their effect on recombination and mutagenesis. Mutat. Res. 407:135-145.
26. Masutani, C., R. Kusumoto, A. Yamada, N. Dohmae, M. Yokoi, M. Yuasa, M. Araki, S. Iwai, K. Takio, and F, Hanaoka. 1999. The XPV (xeroderma pigmentosum variant) gene encodes human DNA polymerase η. Nature 399:700-704.
27. McDonald, J. P., A. S. Levine, and R. Woodgate. 1997. The Saccharomyces cerevisiae RAD30 gene, a homologue of Escherichia coli dinB and umuC, is DNA damage inducible and functions in a novel error-free postreplication repair mechanism. Genetics 147:1557-1568.
28. Mowat, M. R., W. J. Jachymczyk, P. J. Hastings, and R. C. von Borstel. 1983. Repair of gamma-ray induced DNA strand breaks in the radiation-sensitive mutant rad18-2 of Saccharomyces cerevisiae. Mol. Gen. Genet. 189:256-262.
29. Nelson, J. R., C. W. Lawrence, and D. C. Hinkle. 1996. Thymine-thymine dimer bypass by yeast DNA polymerase ζ. Science 272:1646-1649.
30. Nichols, J., B. Zevnik, K. Anastassiadis, H. Niwa, D. Klewe-Nebenius, I. Chambers, H. Scholer, and A. Smith. 1998. Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell 95:379-391.
31. Perry, P., and S. Wolff. 1974. New Giemsa method for the differential staining of sister chromatids. Nature 251:156-158.
32. Prakash, L. 1981. Characterization of postreplication repair in Saccharomyces cerevisiae and effects of rad6, rad18, rev3 and rad52 mutations. Mol. Gen. Genet. 184:471-478.
33. Prakash, S., P. Sung, and L. Prakash. 1993. DNA repair genes and proteins of Saccharomyces cerevisiae. Annu. Rev. Genet. 27:33-70.
34. Roest, H. P., J. van Klaveren, J. de Wit, C. G. van Gurp, M. H. Koken, M. Vermey, J. H. van Roijen, J. W. Hoogerbrugge, J. T. Vreeburg, W. M. Baarends, D. Bootsma, J. A. Grootegoed, and J. H. Hoeijmakers. 1996. Inactivation of the HR6B ubiquitin-conjugating DNA repair enzyme in mice causes male sterility associated with chromatin modification. Cell 868:799-810.
35. Rong, L., and H. L. Klein. 1993. Purification and characterization of the SRS2 DNA helicase of the yeast Saccharomyces cerevisiae. J. Biol. Chem. 268:1252-1259.
36. Schiestl, R. H., R. D. Gietz, P. J. Hastings, and U. Wintersberger. 1990, Interchromosomal and intrachromosomal recombination in rad 18 mutants of Saccharomyces cerevisiae. Mol. Gen. Genet. 222:25-32.
37. Schiestl, R. H., S. Prakash, and L. Prakash. 1990. The Srs2 suppressor of rad6 mutations of Saccharomyces cerevisiae acts by channeling DNA lesions into the RAD52 DNA repair pathway. Genetics 124:817-831.
38. Sonoda, E., Sasaki, C. Morrison, Y. Yamaguchi-Iwai, M. Takata, and S. Takeda. 1999. Sister chromatid exchanges are mediated by homologous recombination in vertebrate cells. Mol. Cell. Biol. 19:5166-5169.
39. Tateishi, S., Y. Sakuraba, S. Masuyama, H. Inoue, and M. Yamaizumi. 2000. Dysfunction of human Rad18 results in defective postreplication repair and hypersensitivity to multiple mutagens. Proc. Natl. Acad. Sci. USA 97:7927-7932.
40. Tomita, H., T. Soshi, and H. Inoue. 1993. The Neurospora uvs-2 gene encodes a protein which has homology to yeast RAD18, with unique zinc finger motifs. Mol. Gen. Genet. 238:225-233. (Erratum, Mol. Gen. Genet. 242:743, 1994.)
41. van der Laan, R., H. P. Roest, J. W. Hoogerbrugge, E. M. Smit, R. Slater, W. M. Baarends, J. H. Hoeijmakers, and J. A. Grootegoed. 2000. Characterization of mRAD18Sc, a mouse homolog of the yeast postreplication repair gene RAD18. Genomics 69:86-94.
42. Walker, G. C. 1998. Skiing the black diamond slope: Progress on the biochemistry of translesion DNA synthesis. Proc. Natl. Acad. Sci. USA 95: 10348-10350.
43. Wang, W., M. Seki, Y. Narita, E. Sonoda, S. Takeda, K. Yamada, T. Masuko, T. Katada, and T. Enomoto. 2000. Possible association of BLM in decreasing DNA double strand breaks during DNA replication. EMBO J. 19:3428-3435.