A missense mutation in Rev7 disrupts formation of Pol, impairing mouse development and repair of Genotoxic Agent-induced DNA Lesions

Journal of Biological Chemistry

Volumn 289, Issue 6, 2014, Pages 3811-3824

  Khalaj, Maryam ^a,c   Abbasi, Abdolrahim ^a,c   Yamanishi, Hiroshi ^a   Akiyama, Kouyou ^b   Wakitani, Shuso ^a   Kikuchi, Sotaro ^d   Hirose, Michiko ^e   Yuzuriha, Misako ^e   Magari, Masaki ^a   Degheidy, Heba A ^f   Abe, Kuniya ^e   Ogura, Atsuo ^e   Hashimoto, Hiroshi ^d,g   Kunieda, Tetsuo ^b  

^a Graduate School of Natural Science and Technology   (Japan)

^b OKAYAMA UNIVERSITY   (Japan)

^c NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^d YOKOHAMA CITY UNIVERSITY   (Japan)

^e RIKEN BIORESOURCE CENTER   (Japan)

^f CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

^g UNIVERSITY OF SHIZUOKA   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROLIFERATION; DNA POLYMERASE; EMBRYO; MOUSE GENETICS; MUTANT;

ANIMALS; APOPTOSIS; CELL CYCLE CHECKPOINTS; CELL PROLIFERATION; DNA DAMAGE; DNA POLYMERASE II; DNA-DIRECTED DNA POLYMERASE; FEMALE; GERM CELLS; MAD2 PROTEINS; MALE; MICE; MICE, MUTANT STRAINS; MITOMYCIN; MUTATION, MISSENSE; NUCLEIC ACID SYNTHESIS INHIBITORS; S PHASE; SPINDLE APPARATUS;

EID: 84893708527     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.514752     Document Type: Article

References (60)

1. Lange, S. S., Takata, K., and Wood, R. D. (2011) DNA polymerases and cancer. Nat. Rev. Cancer 11, 96-110
2. Loeb, L. A., and Monnat, R. J., Jr. (2008) DNA polymerases and human disease. Nat. Rev. Genet. 9, 594-604
3. Saribasak, H., Maul, R. W., Cao, Z., Yang, W. W., Schenten, D., Kracker, S., and Gearhart, P. J. (2012) DNA polymerase-generates tandem mutations in immunoglobulin variable regions. J. Exp. Med. 209, 1075-1081
4. Daly, J., Bebenek, K., Watt, D. L., Richter, K., Jiang, C., Zhao, M. L., Ray, M., McGregor, W. G., Kunkel, T. A., and Diaz, M. (2012) Altered Ig hypermutation pattern and frequency in complementary mouse models of DNA polymerase-Activity. J. Immunol. 188, 5528-5537
5. Friedberg, E. C., Lehmann, A. R., and Fuchs, R. P. (2005) Trading places. How do DNA polymerases switch during translesion DNA synthesis? Mol. Cell 18, 499-505
6. Gan, G. N., Wittschieben, J. P., Wittschieben, B. O., and Wood, R. D. (2008) DNA polymerase-(pol) in higher eukaryotes. Cell Res. 18, 174-183
7. Aravind, L., and Koonin, E. V. (1998) The HORMA domain. A common structural denominator in mitotic checkpoints, chromosome synapsis, and DNA repair. Trends Biochem. Sci. 23, 284-286
8. Takata, K., and Wood, R. D. (2009) Bypass specialists operate together. EMBO J. 28, 313-314
9. Gibbs, P. E., McGregor, W. G., Maher, V. M., Nisson, P., and Lawrence, C. W. (1998) A human homolog of the Saccharomyces cerevisiae REV3 gene, which encodes the catalytic subunit of DNA polymerase-. Proc. Natl. Acad. Sci. U.S.A. 95, 6876-6880
10. Morrison, A., Christensen, R. B., Alley, J., Beck, A. K., Bernstine, E. G., Lemontt, J. F., and Lawrence, C. W. (1989) REV3, a Saccharomyces cerevisiae gene whose function is required for induced mutagenesis, is predicted to encode a nonessential DNA polymerase. J. Bacteriol. 171, 5659-5667
11. Okada, T., Sonoda, E., Yoshimura, M., Kawano, Y., Saya, H., Kohzaki, M., and Takeda, S. (2005) Multiple roles of vertebrate REV genes in DNA repair and recombination. Mol. Cell. Biol. 25, 6103-6111
12. Sharma, S., Hicks, J. K., Chute, C. L., Brennan, J. R., Ahn, J. Y., Glover, T. W., and Canman, C. E. (2012) REV1 and polymerase-facilitate homologous recombination repair. Nucleic Acids Res. 40, 682-691
13. Wittschieben, J. P., Reshmi, S. C., Gollin, S. M., and Wood, R. D. (2006) Loss of DNA polymerase-causes chromosomal instability in mammalian cells. Cancer Res. 66, 134-142
14. Esposito, G., Godindagger, I., Klein, U., Yaspo, M. L., Cumano, A., and Rajewsky, K. (2000) Disruption of the Rev3l-encoded catalytic subunit of polymerase-in mice results in early embryonic lethality. Curr. Biol. 10, 1221-1224
15. Wittschieben, J., Shivji, M. K., Lalani, E., Jacobs, M. A., Marini, F., Gearhart, P. J., Rosewell, I., Stamp, G., and Wood, R. D. (2000) Disruption of the developmentally regulated Rev3l gene causes embryonic lethality. Curr. Biol. 10, 1217-1220
16. Bemark, M., Khamlichi, A. A., Davies, S. L., and Neuberger, M. S. (2000) Disruption of mouse polymerase-(Rev3) leads to embryonic lethality and impairs blastocyst development in vitro. Curr. Biol. 10, 1213-1216
17. Schenten, D., Kracker, S., Esposito, G., Franco, S., Klein, U., Murphy, M., Alt, F. W., and Rajewsky, K. (2009) Pol-Ablation in B cells impairs the germinal center reaction, class switch recombination, DNA break repair, and genome stability. J. Exp. Med. 206, 477-490
18. Wittschieben, J. P., Patil, V., Glushets, V., Robinson, L. J., Kusewitt, D. F., and Wood, R. D. (2010) Loss of DNA polymerase-enhances spontaneous tumorigenesis. Cancer Res. 70, 2770-2778
19. Lange, S. S., Wittschieben, J. P., and Wood, R. D. (2012) DNA polymerase-is required for proliferation of normal mammalian cells. Nucleic Acids Res. 40, 4473-4482
20. Rimkus, C., Friederichs, J., Rosenberg, R., Holzmann, B., Siewert, J. R., and Janssen, K. P. (2007) Expression of the mitotic checkpoint gene MAD2L2 has prognostic significance in colon cancer. Int. J. Cancer 120, 207-211
21. Pfleger, C. M., Salic, A., Lee, E., and Kirschner, M. W. (2001) Inhibition of Cdh1-APC by the MAD2-related protein MAD2L2. A novel mechanism for regulating Cdh1. Genes Dev. 15, 1759-1764
22. Chen, J., and Fang, G. (2001) MAD2B is an inhibitor of the anaphasepromoting complex. Genes Dev. 15, 1765-1770
23. Iwai, H., Kim, M., Yoshikawa, Y., Ashida, H., Ogawa, M., Fujita, Y., Muller, D., Kirikae, T., Jackson, P. K., Kotani, S., and Sasakawa, C. (2007) A bacte-rial effector targets Mad2L2, an APC inhibitor, to modulate host cell cycling. Cell 130, 611-623
24. Lessard, C., Lothrop, H., Schimenti, J. C., and Handel, M. A. (2007) Mutagenesis-generated mouse models of human infertility with abnormal sperm. Hum. Reprod. 22, 159-166
25. Abbasi, A. R., Khalaj, M., Tsuji, T., Tanahara, M., Uchida, K., Sugimoto, Y., and Kunieda, T. (2009) A mutation of the WFDC1 gene is responsible for multiple ocular defects in cattle. Genomics. 94, 55-62
26. Couronne, O., Poliakov, A., Bray, N., Ishkhanov, T., Ryaboy, D., Rubin, E., Pachter, L., and Dubchak, I. (2003) Strategies and tools for whole-genome alignments. Genome. Res. 13, 73-80
27. Perry, A. C., Wakayama, T., Kishikawa, H., Kasai, T., Okabe, M., Toyoda, Y., and Yanagimachi, R. (1999) Mammalian transgenesis by intracytoplasmic sperm injection. Science 284, 1180-1183
28. Lawson, K. A., Dunn, N. R., Roelen, B. A., Zeinstra, L. M., Davis, A. M., Wright, C. V., Korving, J. P., and Hogan, B. L. (1999) Bmp4 is required for the generation of primordial germ cells in the mouse embryo. Genes Dev. 13, 424-436
29. Ginsburg, M., Snow, M. H., and McLaren, A. (1990) Primordial germ cells in the mouse embryo during gastrulation. Development 110, 521-528
30. Abe, K., Hashiyama, M., Macgregor, G., and Yamamura, K. i. (1996) Purification of primordial germ cells from TNAP-geo mouse embryos using FACS-gal. Dev. Biol. 180, 468-472
31. Hara, K., Shimizu, T., Unzai, S., Akashi, S., Sato, M., and Hashimoto, H. (2009) Purification, crystallization, and initial X-ray diffraction study of human REV7 in complex with a REV3 fragment. Acta Crystallogr. Sect. F. Struct. Biol. Cryst. Commun. 65, 1302-1305
32. Hara, K., Hashimoto, H., Murakumo, Y., Kobayashi, S., Kogame, T., Unzai, S., Akashi, S., Takeda, S., Shimizu, T., and Sato, M. (2010) Crystal structure of human REV7 in complex with a human REV3 fragment and structural implication of the interaction between DNA polymerase-And REV1. J. Biol. Chem. 285, 12299-12307
33. Huang, X., and Darzynkiewicz, Z. (2006) Cytometric assessment of histone H2AX phosphorylation. A reporter of DNA damage. Methods Mol. Biol. 314, 73-80
34. Lawson, K. A., and Hage, W. J. (1994) Clonal analysis of the origin of primordial germ cells in the mouse. Ciba Found. Symp. 182, 68-84
35. Saeki, A., Tamura, S., Ito, N., Kiso, S., Matsuda, Y., Yabuuchi, I., Kawata, S., and Matsuzawa, Y. (2002) Frequent impairment of the spindle assembly checkpoint in hepatocellular carcinoma. Cancer 94, 2047-2054
36. Hicks, J. K., Chute, C. L., Paulsen, M. T., Ragland, R. L., Howlett, N. G., Guéranger, Q., Glover, T. W., and Canman, C. E. (2010) Differential roles for DNA polymerases eta,-, and REV1 in lesion bypass of intrastrand versus interstrand DNA cross-links. Mol. Cell. Biol. 30, 1217-1230
37. Cheung, H. W., Chun, A. C., Wang, Q., Deng, W., Hu, L., Guan, X. Y., Nicholls, J. M., Ling, M. T., Chuan Wong, Y., Tsao, S. W., Jin, D. Y., and Wang, X. (2006) Inactivation of human MAD2B in nasopharyngeal carcinoma cells leads to chemosensitization to DNA-damaging agents. Cancer Res. 66, 4357-4367
38. Kratz, K., Schöpf, B., Kaden, S., Sendoel, A., Eberhard, R., Lademann, C., Cannavó, E., Sartori, A. A., Hengartner, M. O., and Jiricny, J. (2010) Deficiency of FANCD2-Associated nuclease KIAA1018/FAN1 sensitizes cells to interstrand crosslinking agents. Cell 142, 77-88
39. de Feraudy, S., Revet, I., Bezrookove, V., Feeney, L., and Cleaver J. E. (2010) A minority of foci or pan-nuclear apoptotic staining of-H2AX in the S phase after UV damage contain DNA double-strand breaks. Proc. Natl. Acad. Sci. U.S.A. 107, 6870-6875
40. Murakumo, Y., Ogura, Y., Ishii, H., Numata, S., Ichihara, M., Croce, C. M., Fishel, R., and Takahashi, M. (2001) Interactions in the error-prone postreplication repair proteins hREV1, hREV3, and hREV7. J. Biol. Chem. 276, 35644-35651
41. Deans, A. J., and West, S. C. (2011) DNA interstrand crosslink repair and cancer. Nat. Rev. Cancer 11, 467-480
42. Ho, T. V., and Schärer, O. D. (2010) Translesion DNA synthesis polymerases in DNA interstrand crosslink repair. Environ. Mol. Mutagen. 51, 552-566
43. Wang, W. (2007) Emergence of a DNA-damage response network consisting of Fanconi anaemia and BRCA proteins. Nat. Rev. Genet. 8, 735-748
44. Räschle, M., Knipscheer, P., Knipsheer, P., Enoiu, M., Angelov, T., Sun, J., Griffith, J. D., Ellenberger, T. E., Schärer, O. D., and Walter, J. C. (2008) Mechanism of replication-coupled DNA interstrand crosslink repair. Cell 134, 969-980
45. Chun, A. C., and Jin, D. Y. (2010) Ubiquitin-dependent regulation of translesion polymerases. Biochem. Soc. Trans. 38, 110-115
46. Williams, H. L., Gottesman, M. E., and Gautier, J. (2012) Replicationindependent repair of DNA interstrand crosslinks. Mol. Cell 47, 140-147
47. Moldovan, G. L., and D'Andrea, A. D. (2009) How the fanconi anemia pathway guards the genome. Annu. Rev. Genet. 43, 223-249
48. Chen, M., Tomkins, D. J., Auerbach, W., McKerlie, C., Youssoufian, H., Liu, L., Gan, O., Carreau, M., Auerbach, A., Groves, T., Guidos, C. J., Freedman, M. H., Cross, J., Percy, D. H., Dick, J. E., Joyner, A. L., and Buchwald, M. (1996) Inactivation of Fac in mice produces inducible chromosomal instability and reduced fertility reminiscent of Fanconi anaemia. Nat. Genet. 12, 448-451
49. Wong, J. C., Alon, N., Mckerlie, C., Huang, J. R., Meyn, M. S., and Buchwald, M. (2003) Targeted disruption of exons 1 to 6 of the Fanconi Anemia groupAgene leads to growth retardation, strain-specific microphthalmia, meiotic defects, and primordial germ cell hypoplasia. Hum. Mol. Genet. 12, 2063-2076
50. Nadler, J. J., and Braun, R. E. (2000) Fanconi anemia complementation group C is required for proliferation of murine primordial germ cells. Genesis 27, 117-123
51. Agoulnik, A. I., Lu, B., Zhu, Q., Truong, C., Ty, M. T., Arango, N., Chada, K. K., and Bishop, C. E. (2002) A novel gene, Pog, is necessary for primordial germ cell proliferation in the mouse and underlies the germ cell deficient mutation, gcd. Hum. Mol. Genet. 11, 3047-3053
52. Kim, J. M., Parmar, K., Huang, M., Weinstock, D. M., Ruit, C. A., Kutok, J. L., and D'Andrea, A. D. (2009) Inactivation of murine Usp1 results in genomic instability and a Fanconi anemia phenotype. Dev. Cell 16, 314-320
53. Shima, N., Munroe, R. J., and Schimenti, J. C. (2004) The mouse genomic instability mutation chaos1 is an allele of Polq that exhibits genetic interaction with Atm. Mol. Cell. Biol. 24, 10381-10389
54. Desiderio, S. V., Yancopoulos, G. D., Paskind, M., Thomas, E., Boss, M. A., Landau, N., Alt, F. W., and Baltimore, D. (1984) Insertion ofNregions into heavy-chain genes is correlated with expression of terminal deoxytransferase in B cells. Nature 311, 752-755
55. Bertocci, B., De Smet A., Berek, C., Weill, J. C., and Reynaud, C. A. (2003) Immunoglobulin light chain gene rearrangement is impaired in mice deficient for DNA polymerase mu. Immunity 19, 203-211
56. Delbos, F., De Smet A., Faili, A., Aoufouchi, S., Weill, J. C., and Reynaud, C. A. (2005) Contribution of DNA polymerase eta to immunoglobulin gene hypermutation in the mouse. J. Exp. Med. 201, 1191-1196
57. McDonald, J. P., Frank, E. G., Plosky, B. S., Rogozin, I. B., Masutani, C., Hanaoka, F., Woodgate, R., and Gearhart, P. J. (2003) 129-derived strains of mice are deficient in DNA polymerase-And have normal immunoglobulin hypermutation. J. Exp. Med. 198, 635-643
58. Schenten, D., Gerlach, V. L., Guo, C., Velasco-Miguel, S., Hladik, C. L., White, C. L., Friedberg, E. C., Rajewsky, K., and Esposito, G. (2002) DNA polymerase deficiency does not affect somatic hypermutation in mice. Eur. J. Immunol. 32, 3152-3160
59. Watanabe, N., Mii, S., Asai, N., Asai, M., Niimi, K., Ushida, K., Kato, T., Enomoto, A., Ishii, H., Takahashi, M., and Murakumo, Y. (2013) The REV7 subunit of DNA polymerase-is essential for primordial germ cell maintenance in the mouse. J. Biol. Chem. 288, 10459-10471
60. Lange, S. S., Bedford, E., Reh, S., Wittschieben J. P., Carbajal, S., Kusewitt, D. F., DiGiovanni, J., and Wood, R. D. (2013) Dual role for mammalian DNA polymerase-in maintaining genome stability and proliferative responses. Proc. Natl. Acad. Sci. U.S.A. 110, E687-E696