Maternal BCAS2 protects genomic integrity in mouse early embryonic development

Development (Cambridge)

Volumn 142, Issue 22, 2015, Pages 3943-3953

  Xu, Qianhua ^a,b   Wang, Fengchao ^c   Xiang, Yunlong ^a   Zhang, Xiaoxin ^a   Zhao, Zhen Ao ^a   Gao, Zheng ^a,b   Liu, Wenbo ^a   Lu, Xukun ^a,b   Liu, Yusheng ^a   Yu, Xing Jiang ^a   Wang, Haibin ^a   Huang, Jun ^d   Yi, Zhaohong ^e   Gao, Shaorong ^f   Li, Lei ^a  

^a INSTITUTE OF ZOOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c NATIONAL INSTITUTE OF BIOLOGICAL SCIENCES   (China)

^d ZHEJIANG UNIVERSITY   (China)

^e BEIJING UNIVERSITY OF AGRICULTURE   (China)

^f TONGJI UNIVERSITY   (China)

Author keywords

BCAS2; DNA damage; Genomic integrity; Maternal effect genes; Mouse early embryonic development

Indexed keywords

BREAST CARCINOMA AMPLIFIED SEQUENCE 2; PROTEIN; REPLICATION PROTEIN A1; REPLICATION PROTEIN A2; UNCLASSIFIED DRUG; BCAS2 PROTEIN, MOUSE; MULTIPROTEIN COMPLEX; NUCLEAR MATRIX PROTEIN; PRP19P PROTEIN, MOUSE; REPLICATION FACTOR A; RPA1 PROTEIN, MOUSE; TUMOR PROTEIN;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; EMBRYO; EMBRYO DEVELOPMENT; FEMALE; GENE MUTATION; GENETIC STABILITY; GENOME; MICRONUCLEUS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; ZYGOTE; ANIMAL; FERTILITY; FLUORESCENCE MICROSCOPY; GENE TARGETING; GENETICS; GENOMIC INSTABILITY; METABOLISM; PHYSIOLOGY; PREGNANCY; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUNEL ASSAY; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; DNA REPAIR; EMBRYONIC DEVELOPMENT; FEMALE; FERTILITY; GENE TARGETING; GENOMIC INSTABILITY; IN SITU NICK-END LABELING; MICE; MICROSCOPY, FLUORESCENCE; MULTIPROTEIN COMPLEXES; NEOPLASM PROTEINS; NUCLEAR MATRIX-ASSOCIATED PROTEINS; PREGNANCY; REAL-TIME POLYMERASE CHAIN REACTION; REPLICATION PROTEIN A; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 84947465824     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.129841     Document Type: Article

References (63)

1. Abe, K.-I., Yamamoto, R., Franke, V., Cao, M., Suzuki, Y., Suzuki, M. G., Vlahovicek, K., Svoboda, P., Schultz, R. M. and Aoki, F. (2015). The first murine zygotic transcription is promiscuous and uncoupled from splicing and 3 processing. EMBO J. 34, 1523-1537.
2. Adiga, S. K., Toyoshima, M., Shiraishi, K., Shimura, T., Takeda, J., Taga, M., Nagai, H., Kumar, P. and Niwa, O. (2007). p21 provides stage specific DNA damage control to preimplantation embryos. Oncogene 26, 6141-6149.
3. Ajuh, P., Kuster, B., Panov, K., Zomerdijk, J. C. B. M., Mann, M. and Lamond, A. I. (2000). Functional analysis of the human CDC5L complex and identification of its components by mass spectrometry. EMBO J. 19, 6569-6581.
4. Anantha, R. W., Vassin, V. M. and Borowiec, J. A. (2007). Sequential and synergistic modification of human RPA stimulates chromosomal DNA repair. J. Biol. Chem. 282, 35910-35923.
5. Anciano Granadillo, V. J., Earley, J. N., Shuck, S. C., Georgiadis, M. M., Fitch, R. W. and Turchi, J. J. (2010). Targeting the OB-folds of replication protein A with small molecules. J. Nucleic Acids 2010, 304035.
6. Arias-Lopez, C., Lazaro-Trueba, I., Kerr, P., Lord, C. J., Dexter, T., Iravani, M., Ashworth, A. and Silva, A. (2006). P53 modulates homologous recombination by transcriptional regulation of the RAD51 gene. EMBO Rep. 7, 219-224.
7. Artus, J. and Cohen-Tannoudji, M. (2008). Cell cycle regulation during early mouse embryogenesis. Mol. Cell. Endocrinol. 282, 78-86.
8. Ashley, A. K., Shrivastav, M., Nie, J., Amerin, C., Troksa, K., Glanzer, J. G., Liu, S., Opiyo, S. O., Dimitrova, D. D., Le, P. et al. (2014). DNA-PK phosphorylation of RPA32 Ser4/Ser8 regulates replication stress checkpoint activation, fork restart, homologous recombination and mitotic catastrophe. DNA Repair 21, 131-139.
9. Block, W. D., Yu, Y. and Lees-Miller, S. P. (2004). Phosphatidyl inositol 3-kinase- like serine/threonine protein kinases (PIKKs) are required for DNA damage-induced phosphorylation of the 32 kDa subunit of replication protein A at threonine 21. Nucleic Acids Res. 32, 997-1005.
10. Bradley, M. O. and Taylor, V. I. (1981). DNA double-strand breaks induced in normal human cells during the repair of ultraviolet light damage. Proc. Natl. Acad. Sci. USA 78, 3619-3623.
11. Brandriff, B. and Pedersen, R. A. (1981). Repair of the ultraviolet-irradiated male genome in fertilized mouse eggs. Science 211, 1431-1433.
12. Brown, E. J. and Baltimore, D. (2000). ATR disruption leads to chromosomal fragmentation and early embryonic lethality. Genes Dev. 14, 397-402.
13. Brugarolas, J., Chandrasekaran, C., Gordon, J. I., Beach, D., Jacks, T. and Hannon, G. J. (1995). Radiation-induced cell-cycle arrest compromised by P21 deficiency. Nature 377, 552-557.
14. Bultman, S. J., Gebuhr, T. C., Pan, H., Svoboda, P., Schultz, R. M. and Magnuson, T. (2006). Maternal BRG1 regulates zygotic genome activation in the mouse. Genes Dev. 20, 1744-1754.
15. Ciccia, A. and Elledge, S. J. (2010). The DNA damage response: making it safe to play with knives. Mol. Cell 40, 179-204.
16. El-Deiry, W. S., Kern, S. E., Pietenpol, J. A., Kinzler, K. W. and Vogelstein, B. (1992). Definition of a consensus binding site for P53. Nat. Genet. 1, 45-49.
17. Espinosa, J. M., Verdun, R. E. and Emerson, B. M. (2003). P53 functions through stress- and promoter-specific recruitment of transcription initiation components before and after DNA damage. Mol. Cell 12, 1015-1027.
18. Fanning, E., Klimovich, V. and Nager, A. R. (2006). A dynamic model for Replication Protein A (RPA) function in DNA processing pathways. Nucleic Acids Res. 34, 4126-4137.
19. Ferreira, J. and Carmo-Fonseca, M. (1997). Genome replication in early mouse embryos follows a defined temporal and spatial order. J. Cell Sci. 110, 889-897.
20. Fraser, L. R. and Drury, L. M. (1975). Relationship between sperm concentration and fertilization in vitro of mouse eggs. Biol. Reprod. 13, 513-518.
21. Friedberg, E. C. and Meira, L. B. (2006). Database of mouse strains carrying targeted mutations in genes affecting biological responses to DNA damage Version 7. DNA Repair 5, 189-209.
22. Generoso, W. M., Cain, K. T., Krishna, M. and Huff, S. W. (1979). Genetic lesions induced by chemicals in spermatozoa and spermatids of mice are repaired in the egg. Proc. Natl. Acad. Sci. USA 76, 435-437.
23. Goto, H., Tomono, Y., Ajiro, K., Kosako, H., Fujita, M., Sakurai, M., Okawa, K., Iwamatsu, A., Okigaki, T., Takahashi, T. et al. (1999). Identification of a novel phosphorylation site on histone H3 coupled with mitotic chromosome condensation. J. Biol. Chem. 274, 25543-25549.
24. Grinfeld, S. and Jacquet, P. (1987). An unusual radiation-induced G2 arrest in the zygote of the BALB/c mouse strain. Int. J. Radiat. Biol. 51, 353-363.
25. Hajkova, P., Jeffries, S. J., Lee, C., Miller, N., Jackson, S. P. and Surani, M. A. (2010). Genome-wide reprogramming in the mouse germ line entails the base excision repair pathway. Science 329, 78-82.
26. Jazayeri, A., Falck, J., Lukas, C., Bartek, J., Smith, G. C. M., Lukas, J. and Jackson, S. P. (2006). ATM- and cell cycle-dependent regulation of ATR in response to DNA double-strand breaks. Nat. Cell Biol. 8, 37-45.
27. Kojima, Y., Tam, O. H. and Tam, P. P. L. (2014). Timing of developmental events in the early mouse embryo. Semin. Cell Dev. Biol. 34, 65-75.
28. Kuo, P.-C., Tsao, Y.-P., Chang, H.-W., Chen, P.-H., Huang, C.-W., Lin, S.-T., Weng, Y.-T., Tsai, T.-C., Shieh, S.-Y. and Chen, S.-L. (2009). Breast cancer amplified sequence 2, a novel negative regulator of the p53 tumor suppressor. Cancer Res. 69, 8877-8885.
29. Larson, J. S., Stringer, S. L. and Stringer, J. R. (2004). Impact of mismatch repair deficiency on genomic stability in the maternal germline and during early embryonic development. Mutat. Res. 556, 45-53.
30. Levine, A. J. (1997). p53, the cellular gatekeeper for growth and division. Cell 88, 323-331.
31. Lewandoski, M., Wassarman, K. M. and Martin, G. R. (1997). Zp3-cre, a transgenic mouse line for the activation or inactivation of loxP-flanked target genes specifically in the female germ line. Curr. Biol. 7, 148-151.
32. Li, L., Zheng, P. and Dean, J. (2010). Maternal control of early mouse development. Development 137, 859-870.
33. Liu, Q. H., Guntuku, S., Cui, X. S., Matsuoka, S., Cortez, D., Tamai, K., Luo, G. B., Carattini-Rivera, S., DeMayo, F., Bradley, A. et al. (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.
34. Liu, S., Opiyo, S. O., Manthey, K., Glanzer, J. G., Ashley, A. K., Amerin, C., Troksa, K., Shrivastav, M., Nickoloff, J. A. and Oakley, G. G. (2012). Distinct roles for DNA-PK, ATM and ATR in RPA phosphorylation and checkpoint activation in response to replication stress. Nucleic Acids Res. 40, 10780-10794.
35. Luo, G., Yao, M. S., Bender, C. F., Mills, M., Bladl, A. R., Bradley, A. and Petrini, J. H. J. (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. Macleod, K. F., Sherry, N., Hannon, G., Beach, D., Tokino, T., Kinzler, K., Vogelstein, B. and Jacks, T. (1995). P53-dependent and independent expression of P21 during cell growth, differentiation, and DNA damage. Genes Dev. 9, 935-944.
37. Marangos, P. and Carroll, J. (2012). Oocytes progress beyond prophase in the presence of DNA damage. Curr. Biol. 22, 989-994.
38. Marechal, A., Li, J.-M., Ji, X. Y., Wu, C.-S., Yazinski, S. A., Nguyen, H. D., Liu, S., Jimenez, A. E., Jin, J. and Zou, L. (2014). PRP19 transforms into a sensor of RPA-ssDNA after DNA damage and drives ATR activation via a ubiquitin- mediated circuitry. Mol. Cell 53, 235-246.
39. Masui, Y. and Pedersen, R. A. (1975). Ultraviolet light-induced unscheduled DNA synthesis in mouse oocytes during meiotic maturation. Nature 257, 705-706.
40. Miyashita, T. and Reed, J. C. (1995). Tumor suppressor P53 is a direct transcriptional activator of the human Bax gene. Cell 80, 293-299.
41. Nagasaki, K., Maass, N., Manabe, T., Hanzawa, H., Tsukada, T., Kikuchi, K. and Yamaguchi, K. (1999). Identification of a novel gene, DAM1, amplified at chromosome 1p13.3-21 region in human breast cancer cell lines. Cancer Lett. 140, 219-226.
42. Oakley, G. G., Patrick, S. M., Yao, J., Carty, M. P., Turchi, J. J. and Dixon, K. (2003). RPA phosphorylation in mitosis alters DNA binding and protein-protein lnteractions. Biochemistry 42, 3255-3264.
43. O’Connell, M. J., Raleigh, J. M., Verkade, H. M. and Nurse, P. (1997). Chk1 is a wee1 kinase in the G(2) DNA damage checkpoint inhibiting cdc2 by Y15 phosphorylation. EMBO J. 16, 545-554.
44. O’Driscoll, M. and Jeggo, P. A. (2006). The role of double-strand break repair - insights from human genetics. Nat. Rev. Genet. 7, 45-54.
45. Olson, E., Nievera, C. J., Klimovich, V., Fanning, E. and Wu, X. (2006). RPA2 is a direct downstream target for ATR to regulate the S-phase checkpoint. J. Biol. Chem. 281, 39517-39533.
46. Posfai, E., Kunzmann, R., Brochard, V., Salvaing, J., Cabuy, E., Roloff, T. C., Liu, Z., Tardat, M., van Lohuizen, M., Vidal, M. et al. (2012). Polycomb function during oogenesis is required for mouse embryonic development. Genes Dev. 26, 920-932.
47. Rodriguez, C. I., Buchholz, F., Galloway, J., Sequerra, R., Kasper, J., Ayala, R., Stewart, A. F. and Dymecki, S. M. (2000). High-efficiency deleter mice show that FLPe is an alternative to Cre-loxP. Nat. Genet. 25, 139-140.
48. Roest, H. P., Baarends, W. M., de Wit, J., van Klaveren, J. W., Wassenaar, E., Hoogerbrugge, J. W., van Cappellen, W. A., Hoeijmakers, J. H. J. and Grootegoed, J. A. (2004). The ubiquitin-conjugating DNA repair enzyme HR6A is a maternal factor essential for early embryonic development in mice. Mol. Cell. Biol. 24, 5485-5495.
49. Sanchez, Y., Wong, C., Thoma, R. S., Richman, R., Wu, Z., Piwnica-Worms, H. and Elledge, S. J. (1997). Conservation of the Chk1 checkpoint pathway in mammals: linkage of DNA damage to Cdk regulation through Cdc25. Science 277, 1497-1501.
50. Shi, W., Feng, Z., Zhang, J., Gonzalez-Suarez, I., Vanderwaal, R. P., Wu, X., Powell, S. N., Roti, J. L. R., Gonzalo, S. and Zhang, J. (2010). The role of RPA2 phosphorylation in homologous recombination in response to replication arrest. Carcinogenesis 31, 994-1002.
51. Shiloh, Y. (2001). ATM and ATR: networking cellular responses to DNA damage. Curr. Opin. Genet. Dev. 11, 71-77.
52. Shuck, S. C. and Turchi, J. J. (2010). Targeted inhibition of Replication Protein A reveals cytotoxic activity, synergy with chemotherapeutic DNA-damaging agents, and insight into cellular function. Cancer Res. 70, 3189-3198.
53. Siafakas, A. R. and Richardson, D. R. (2009). Growth arrest and DNA damage-45 alpha (GADD45 alpha). Int. J. Biochem. Cell Biol. 41, 986-989.
54. Takai, H., Tominaga, K., Motoyama, N., Minamishima, Y. A., Nagahama, H., Tsukiyama, T., Ikeda, K., Nakayama, K., Nakanishi, M. and Nakayama, K. (2000). Aberrant cell cycle checkpoint function and early embryonic death in Chk1 (-/-) mice. Genes Dev. 14, 1439-1447.
55. Toyoshima, M., Shimura, T., Adiga, S.-K., Taga, M., Shiraishi, K., Inoue, M., Yuan, Z.-M. and Niwa, O. (2005). Transcription-independent suppression of DNA synthesis by p53 in sperm-irradiated mouse zygotes. Oncogene 24, 3229-3235.
56. Wan, L. and Huang, J. (2014). The PSO4 protein complex associates with Replication Protein A (RPA) and modulates the activation of Ataxia Telangiectasia-mutated and Rad3-related (ATR). J. Biol. Chem. 289, 6619-6626.
57. Wang, H. Y., Guan, J., Wang, H. C., Perrault, A. R., Wang, Y. and Iliakis, G. (2001). Replication protein A2 phosphorylation after DNA damage by the coordinated action of ataxia telangiectasia-mutated and DNA-dependent protein kinase. Cancer Res. 61, 8554-8563.
58. Wang, Y., Putnam, C. D., Kane, M. F., Zhang, W., Edelmann, L., Russell, R., Carrion, D. V., Chin, L., Kucherlapati, R., Kolodner, R. D. et al. (2005). Mutation in Rpa1 results in defective DNA double-strand break repair, chromosomal instability and cancer in mice. Nat. Genet. 37, 750-755.
59. Wossidlo, M., Arand, J., Sebastiano, V., Lepikhov, K., Boiani, M., Reinhardt, R., Scholer, H. and Walter, J. (2010). Dynamic link of DNA demethylation, DNA strand breaks and repair in mouse zygotes. EMBO J. 29, 1877-1888.
60. Wu, X., Viveiros, M. M., Eppig, J. J., Bai, Y., Fitzpatrick, S. L. and Matzuk, M. M. (2003). Zygote arrest 1 (Zar1) is a novel maternal-effect gene critical for the oocyte-to-embryo transition. Nat. Genet. 33, 187-191.
61. Zeng, F. and Schultz, R. M. (2005). RNA transcript profiling during zygotic gene activation in the preimplantation mouse embryo. Dev. Biol. 283, 40-57.
62. Zeng, F., Baldwin, D. A. and Schultz, R. M. (2004). Transcript profiling during preimplantation mouse development. Dev. Biol. 272, 483-496.
63. Zou, L. and Elledge, S. J. (2003). Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 300, 1542-1548.