The REV7 subunit of DNA polymerase ζ is essential for primordial germ cell maintenance in the mouse

Journal of Biological Chemistry

Volumn 288, Issue 15, 2013, Pages 10459-10471

  Watanabe, Naoki ^a   Mii, Shinji ^a   Asai, Naoya ^a   Asai, Masato ^a   Niimi, Kaoru ^a   Ushida, Kaori ^a   Kato, Takuya ^a   Enomoto, Atsushi ^a   Ishii, Hideshi ^b   Takahashi, Masahide ^a   Murakumo, Yoshiki ^a,c  

^a NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c KITASATO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

APOPTOTIC CELL DEATH; APOPTOTIC CELLS; CELL CYCLE REGULATION; DNA POLYMERASE; GROWTH RETARDATION; HISTONE METHYLATION; NORTHERN BLOT ANALYSIS; PRIMORDIAL GERM CELL;

ALKYLATION; CELL DEATH; CELL PROLIFERATION; DAMAGE DETECTION; DNA; GENE EXPRESSION; PROTEINS; REPAIR;

MAMMALS;

DNA POLYMERASE; DNA POLYMERASE ZETA; OCTAMER TRANSCRIPTION FACTOR 4; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; PROTEIN REV7; TRANSCRIPTION FACTOR NANOG; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APLASIA; APOPTOSIS; ARTICLE; CELL MATURATION; CELL MIGRATION; CELL PROLIFERATION; DNA DAMAGE; DNA METHYLATION; EMBRYO; ENZYME ACTIVITY; FEMALE; FOREBRAIN; GENE; GROWTH RETARDATION; MALE; MOUSE; NANOG GENE; NONHUMAN; OCT4 GENE; OVARY; PHENOTYPE; PRIMORDIAL GERM CELL; PRIORITY JOURNAL; REV7 GENE; TESTIS;

ANIMALS; APOPTOSIS; CELL CYCLE PROTEINS; CELL MOVEMENT; DNA DAMAGE; DNA-DIRECTED DNA POLYMERASE; EMBRYO, MAMMALIAN; FEMALE; GERM CELLS; HOMEODOMAIN PROTEINS; HUMANS; MALE; MICE; MICE, KNOCKOUT; NUCLEAR PROTEINS; OCTAMER TRANSCRIPTION FACTOR-3;

MAMMALIA; MUS;

EID: 84876240946     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.421966     Document Type: Article

References (64)

1. Saga, Y. (2008) Mouse germ cell development during embryogenesis. Curr. Opin. Genet. Dev. 18, 337-341
2. Saitou, M. (2009) Germ cell specification in mice. Curr. Opin. Genet. Dev. 19, 386-395
3. Ewen, K. A., and Koopman, P. (2010) Mouse germ cell development. From specification to sex determination. Mol. Cell. Endocrinol. 323, 76-93
4. Matsui, Y. (2010) Epigenetic profiles in primordial germ cells. Global modulation and fine tuning of the epigenome for acquisition of totipotency. J. Androl. 31, 61-65
5. Ohinata, Y., Payer, B., O'Carroll, D., Ancelin, K., Ono, Y., Sano, M., Barton, S. C., Obukhanych, T., Nussenzweig, M., Tarakhovsky, A., Saitou, M., and Surani, M. A. (2005) Blimp1 is a critical determinant of the germ cell lineage in mice. Nature 436, 207-213
6. Kurimoto, K., Yabuta, Y., Ohinata, Y., Shigeta, M., Yamanaka, K., and Saitou, M. (2008) Complex genome-wide transcription dynamics orchestrated by Blimp1 for the specification of the germ cell lineage in mice. Genes Dev. 22, 1617-1635
7. Yamaji, M., Seki, Y., Kurimoto, K., Yabuta, Y., Yuasa, M., Shigeta, M., Yamanaka, K., Ohinata, Y., and Saitou, M. (2008) Critical function of Prdm14 for the establishment of the germ cell lineage in mice. Nat. Genet. 40, 1016-1022
8. Tsuda, M., Sasaoka, Y., Kiso, M., Abe, K., Haraguchi, S., Kobayashi, S., and Saga, Y. (2003) Conserved role of nanos proteins in germ cell development. Science 301, 1239-1241
9. Runyan, C., Schaible, K., Molyneaux, K., Wang, Z., Levin, L., and Wylie, C. (2006) Steel factor controls midline cell death of primordial germ cells and is essential for their normal proliferation and migration. Development 133, 4861-4869
10. Beck, A. R., Miller, I. J., Anderson, P., and Streuli, M. (1998) RNA-binding protein TIAR is essential for primordial germ cell development. Proc. Natl. Acad. Sci. U.S.A. 95, 2331-2336
11. Kehler, J., Tolkunova, E., Koschorz, B., Pesce, M., Gentile, L., Boiani, M., Lomelí, H., Nagy, A., McLaughlin, K. J., Schöler, H. R., and Tomilin, A. (2004) Oct4 is required for primordial germ cell survival. EMBO Rep. 5, 1078-1083
12. Youngren, K. K., Coveney, D., Peng, X., Bhattacharya, C., Schmidt, L. S., Nickerson, M. L., Lamb, B. T., Deng, J. M., Behringer, R. R., Capel, B., Rubin, E. M., Nadeau, J. H., and Matin, A. (2005) The Ter mutation in the dead end gene causes germ cell loss and testicular germ cell tumours. Nature 435, 360-364
13. Mitsui, K., Tokuzawa, Y., Itoh, H., Segawa, K., Murakami, M., Takahashi, K., Maruyama, M., Maeda, M., and Yamanaka, S. (2003) The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell 113, 631-642
14. Seki, Y., Hayashi, K., Itoh, K., Mizugaki, M., Saitou, M., and Matsui, Y. (2005) Extensive and orderly reprogramming of genome-wide chromatin modifications associated with specification and early development of germ cells in mice. Dev. Biol. 278, 440-458
15. Seki, Y., Yamaji, M., Yabuta, Y., Sano, M., Shigeta, M., Matsui, Y., Saga, Y., Tachibana, M., Shinkai, Y., and Saitou, M. (2007) Cellular dynamics associated with the genome-wide epigenetic reprogramming in migrating primordial germ cells in mice. Development 134, 2627-2638
16. Schmahl, J., Eicher, E. M., Washburn, L. L., and Capel, B. (2000) Sry induces cell proliferation in the mouse gonad. Development 127, 65-73
17. Nelson, J. R., Lawrence, C. W., and Hinkle, D. C. (1996) Thymine-thymine dimer bypass by yeast DNA polymerase . Science 272, 1646-1649
18. Guo, C., Kosarek-Stancel, J. N., Tang, T. S., and Friedberg, E. C. (2009) Y-family DNA polymerases in mammalian cells. Cell. Mol. Life Sci. 66, 2363-2381
19. Murakumo, Y., Roth, T., Ishii, H., Rasio, D., Numata, S., Croce, C. M., and Fishel, R. (2000) A human REV7 homolog that interacts with the polymerase catalytic subunit hREV3 and the spindle assembly checkpoint protein hMAD2. J. Biol. Chem. 275, 4391-4397
20. 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
21. Masuda, Y., Ohmae, M., Masuda, K., and Kamiya, K. (2003) Structure and enzymatic properties of a stable complex of the human REV1 and REV7 proteins. J. Biol. Chem. 278, 12356-12360
22. 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
23. McNally, K., Neal, J. A., McManus, T. P., McCormick, J. J., and Maher, V. M. (2008) hRev7, putative subunit of hPol, plays a critical role in survival, induction of mutations, and progression through S-phase, of UV254nm-irradiated human fibroblasts. DNA Repair 7, 597-604
24. 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
25. 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
26. Cahill, D. P., da Costa, L. T., Carson-Walter, E. B., Kinzler, K. W., Vogelstein, B., and Lengauer, C. (1999) Characterization of MAD2B and other mitotic spindle checkpoint genes. Genomics 58, 181-187
27. Chen, J., and Fang, G. (2001) MAD2B is an inhibitor of the anaphasepromoting complex. Genes Dev. 15, 1765-1770
28. 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
29. 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 bacterial effector targets Mad2L2, an APC inhibitor, to modulate host cell cycling. Cell 130, 611-623
30. Zhang, L., Yang, S. H., and Sharrocks, A. D. (2007) Rev7/MAD2B links c-Jun N-terminal protein kinase pathway signaling to activation of the transcription factor Elk-1. Mol. Cell. Biol. 27, 2861-2869
31. Hong, C. F., Chou, Y. T., Lin, Y. S., and Wu, C. W. (2009) MAD2B, a novel TCF4-binding protein, modulates TCF4-mediated epithelial-mesenchymal transdifferentiation. J. Biol. Chem. 284, 19613-19622
32. Weterman, M. A., van Groningen, J. J., Tertoolen, L., and van Kessel, A. G. (2001) Impairment of MAD2B-PRCC interaction in mitotic checkpoint defective t(X;1)-positive renal cell carcinomas. Proc. Natl. Acad. Sci. U.S.A. 98, 13808-13813
33. Li, L., Shi, Y., Wu, H., Wan, B., Li, P., Zhou, L., Shi, H., and Huo, K. (2007) Hepatocellular carcinoma-associated gene 2 interacts with MAD2L2. Mol. Cell. Biochem. 304, 297-304
34. 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
35. Matsunami, H., and Takeichi, M. (1995) Fetal brain subdivisions defined by R- and E-cadherin expressions: evidence for the role of cadherin activity in region-specific, cell-cell adhesion. Dev. Biol. 172, 466-478
36. Chen, T., Du, J., and Lu, G. (2012) Cell growth arrest and apoptosis induced by Oct4 or Nanog knockdown in mouse embryonic stem cells. A possible role of Trp53. Mol. Biol. Rep. 39, 1855-1861
37. Anderson, R., Fässler, R., Georges-Labouesse, E., Hynes, R. O., Bader, B. L., Kreidberg, J. A., Schaible, K., Heasman, J., and Wylie, C. (1999) Mouse primordial germ cells lacking 1 integrins enter the germline but fail to migrate normally to the gonads. Development 126, 1655-1664
38. Wilkinson, D. G., and Nieto, M. A. (1993) Detection of messenger RNA by in situ hybridization to tissue sections and whole mounts. Methods Enzymol. 225, 361-373
39. Matzuk, M. M., and Lamb, D. J. (2002) Genetic dissection of mammalian fertility pathways. Nat. Cell Biol. 4, s41-49
40. Ombelet, W., Cooke, I., Dyer, S., Serour, G., and Devroey, P. (2008) Infertility and the provision of infertility medical services in developing countries. Hum. Reprod. Update 14, 605-621
41. Ferlin, A., Arredi, B., and Foresta, C. (2006) Genetic causes of male infertility. Reprod. Toxicol. 22, 133-141
42. Saitou, M., and Yamaji, M. (2010) Germ cell specification in mice. Signal- ing, transcription regulation, and epigenetic consequences. Reproduction 139, 931-942
43. Schöler, H. R., Dressler, G. R., Balling, R., Rohdewohld, H., and Gruss, P. (1990) Oct-4, a germline-specific transcription factor mapping to the mouse t-complex. EMBO J. 9, 2185-2195
44. Yeom, Y. I., Fuhrmann, G., Ovitt, C. E., Brehm, A., Ohbo, K., Gross, M., Hübner, K., and Schöler, H. R. (1996) Germline regulatory element of Oct-4 specific for the totipotent cycle of embryonal cells. Development 122, 881-894
45. Chambers, I., Colby, D., Robertson, M., Nichols, J., Lee, S., Tweedie, S., and Smith, A. (2003) Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell 113, 643-655
46. Burcham, P. C. (1999) Internal hazards. Baseline DNA damage by endogenous products of normal metabolism. Mutat. Res. 443, 11-36
47. Wink, D. A., Kasprzak, K. S., Maragos, C. M., Elespuru, R. K., Misra, M., Dunams, T. M., Cebula, T. A., Koch, W. H., Andrews, A. W., and Allen, J. S. (1991) DNA deaminating ability and genotoxicity of nitric oxide and its progenitors. Science 254, 1001-1003
48. Jaroudi, S., and SenGupta, S. (2007) DNA repair in mammalian embryos. Mutat. Res. 635, 53-77
49. Vinson, R. K., and Hales, B. F. (2002) DNA repair during organogenesis. Mutat. Res. 509, 79-91
50. Waters, L. S., Minesinger, B. K., Wiltrout, M. E., D'Souza, S., Woodruff, R. V., and Walker, G. C. (2009) Eukaryotic translesion polymerases and their roles and regulation in DNA damage tolerance. Microbiol. Mol. Biol. Rev. 73, 134-154
51. 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
52. 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
53. 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
54. Van Sloun, P. P., Varlet, I., Sonneveld, E., Boei, J. J., Romeijn, R. J., Eeken, J. C., and De Wind N. (2002) Involvement of mouse Rev3 in tolerance of endogenous and exogenous DNA damage. Mol. Cell. Biol. 22, 2159-2169
55. Sun, J., Yomogida, K., Sakao, S., Yamamoto, H., Yoshida, K., Watanabe, K., Morita, T., Araki, K., Yamamura, K., and Tateishi, S. (2009) Rad18 is required for long-term maintenance of spermatogenesis in mouse testes. Mech. Dev. 126, 173-183
56. Ng, J. M., Vrieling, H., Sugasawa, K., Ooms, M. P., Grootegoed, J. A., Vreeburg, J. T., Visser, P., Beems, R. B., Gorgels, T. G., Hanaoka, F., Hoeijmakers, J. H., and van der Horst, G. T. (2002) Developmental defects and male sterility in mice lacking the ubiquitin-likeDNArepair gene mHR23B. Mol. Cell. Biol. 22, 1233-1245
57. Hsia, K. T., Millar, M. R., King, S., Selfridge, J., Redhead, N. J., Melton, D. W., and Saunders, P. T. (2003) DNA repair gene Ercc1 is essential for normal spermatogenesis and oogenesis and for functional integrity of germ cell DNA in the mouse. Development 130, 369-378
58. Nakane, H., Hirota, S., Brooks, P. J., Nakabeppu, Y., Nakatsu, Y., Nishimune, Y., Iino, A., and Tanaka, K. (2008) Impaired spermatogenesis and elevated spontaneous tumorigenesis in xeroderma pigmentosum group A gene (Xpa)-deficient mice. DNA Repair 7, 1938-1950
59. Li, M., York, J. P., and Zhang, P. (2007) Loss of Cdc20 causes a securin-dependent metaphase arrest in two-cell mouse embryos. Mol. Cell. Biol. 27, 3481-3488
60. García-Higuera, I., Manchado, E., Dubus, P., Cañamero, M., Méndez, J., Moreno, S., and Malumbres, M. (2008) Genomic stability and tumour suppression by the APC/C cofactor Cdh1. Nat. Cell. Biol. 10, 802-811
61. Dobles, M., Liberal, V., Scott, M. L., Benezra, R., and Sorger, P. K. (2000) Chromosome missegregation and apoptosis in mice lacking the mitotic checkpoint protein Mad2. Cell 101, 635-645
62. Cesari, F., Brecht, S., Vintersten, K., Vuong, L.G., Hofmann, M., Klingel, K., Schnorr, J. J., Arsenian, S., Schild, H., Herdegen, T., Wiebel, F. F., and Nordheim, A. (2004) Mice deficient for the Ets transcription factor Elk-1 show normal immune responses and mildly impaired neuronal gene activation. Mol. Cell. Biol. 24, 294-305
63. Korinek, V., Barker, N., Moerer, P., van Donselaar, E., Huls, G., Peters, P. J., and Clevers H. (1998) Depletion of epithelial stem-cell compartments in the small intestine of mice lacking Tcf-4. Nat. Genet. 19, 379-383
64. Mazan-Mamczarz, K., Lal, A., Martindale, J. L., Kawai, T., and Gorospe, M. (2006) Translational repression by RNA-binding protein TIAR. Mol. Cell. Biol. 26, 2716-2727