Inactivation of CtIP leads to early embryonic lethality mediated by G 1 restraint and to tumorigenesis by haploid insufficiency

Molecular and Cellular Biology

Volumn 25, Issue 9, 2005, Pages 3535-3542

  Chen, Phang Lang ^a   Liu, Feng ^a   Cai, Suna ^a   Lin, Xiaoqin ^a   Li, Aihua ^a   Chen, Yumay ^b   Gu, Bingnan ^a   Lee, Eva Y H P ^a   Lee, Wen Hwa ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN CTIP; PROTEIN DERIVATIVE; PROTEIN P21; RETINOBLASTOMA PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BLASTOCYST; CARCINOGENESIS; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; CELL DEATH; CONTROLLED STUDY; EMBRYO; EMBRYO DEATH; EMBRYO DEVELOPMENT; EXON; FIBROBLAST; GENE FREQUENCY; GENE INSERTION; HAPLOIDY; HUMAN; HUMAN CELL; LETHALITY; LIFESPAN; LYMPHOMA; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; WILD TYPE;

ANIMALS; BLASTOCYST; CARRIER PROTEINS; CELL CYCLE PROTEINS; EMBRYO; EMBRYONIC DEVELOPMENT; FIBROBLASTS; G1 PHASE; GENE SILENCING; GENES, LETHAL; HAPLOIDY; HETEROZYGOTE; HUMANS; MICE; MICE, KNOCKOUT; NEOPLASMS, MULTIPLE PRIMARY; RETINOBLASTOMA PROTEIN; RNA, SMALL INTERFERING; TUMOR SUPPRESSOR PROTEINS;

EID: 17644375501     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.25.9.3535-3542.2005     Document Type: Article

References (47)

1. Bell, S. P., and A. Dutta. 2002. DNA replication in eukaryotic cells. Annu. Rev. Biochem. 71:333-374.
2. Boyd, J. M., T. Subramanian, U. Schaeper, M. La Regina, S. Bayley, and G. Chinnadurai. 1993. A region in the C-terminus of adenovirus 2/5 E1a protein is required for association with a cellular phos-phoprotein and important for the negative modulation of T24-ras mediated transformation, tumorigenesis and metastasis. EMBO J. 12:469-478.
3. Chinnadurai, G. 2002. CtBP family proteins: more than transcriptional corepressors. BioEssays 25:9-12.
4. Classon, M., and E. Harlow. 2002. The retinoblastoma tumour suppressor in development and cancer. Nat. Rev. Cancer 2:910-917.
5. Collins, N., R. A. Pootl, I. Kukimoto, C. García-Jiménezl, G. Dellaire, and P. D. Varga-Weiszl. 2002. An ACF1-ISWI chromatin-remodeling complex is required for DNA replication through heterochromatin. Nat. Genet. 32:627-632.
6. Decesse, J. T., S. Medjkane, M. B. Datto, and C. E. Cremisi. 2001. RB regulates transcription of the p21/WAF1/CIP1 gene. Oncogene 20:962-971.
7. Dubin, M. J., P. H. Stokes, E. Y. Sum, R. S. Williams, V. A. Valova, P. J. Robinson, G. J. Lindeman, J. N. Glover, J. E. Visvader, and J. M. Matthews. 2004. Dimerization of CtIP, a BRCA1- and CtBP-interacting protein, is mediated by an N-terminal coiled-coil motif. J. Biol. Chem. 279:26932-26938.
8. Fusco, C., A. Reymond, and A. S. Zervos. 1998. Molecular cloning and characterization of a novel retinoblastoma-binding protein. Genomics 51:351-358.
9. Georgopoulos, K., M. Bigby, J. H. Wang, A. Molnar, P. Wu, S. Winandy, and A. Sharpe. 1994. The Ikaros gene is required for the development of all lymphoid lineages. Cell 79:143-156.
10. Gomez-del Arco, P., K. Maki, and K. Georgopoulos. 2004. Phosphorylation controls Ikaros's ability to negatively regulate the G1-S transition. Mol. Cell. Biol. 24:2797-2807.
11. 1 phase of the cell cycle. Cell 67:293-302.
12. Hakem, R., J. L. de la Pompa, C. Sirard, R. Mo, M. Woo, A. Hakem, A. Wakeham, J. Potter, A. Reitmair, F. Billia, E. Firpo, C. C. Hui, J. Roberts, J. Rossant, and T. W. Mak. 1996. The tumor suppressor gene Brca1 is required for embryonic cellular proliferation in the mouse. Cell 85:1009-1023.
13. He, T. C., S. Zhou, L. T. da Costa, J. Yu, K. W. Kinzler, and B. Vogelstein. 1998. A simplified system for generating recombinant adenoviruses. Proc. Natl. Acad. Sci. USA 95:2509-2514.
14. Hildebrand, J. D., and P. Soriano. 2002. Overlapping and unique roles for C-terminal binding protein 1 (CtBP1) and CtBP2 during mouse development. Mol. Cell. Biol. 22:5296-5307.
15. Hoek, M., and B. Stillman. 2003. Chromatin assembly factor 1 is essential and couples chromatin assembly to DNA replication in vivo. Proc. Natl. Acad. Sci. USA 188:12183-12188.
16. Inoue, K., F. Zindy, D. H. Randle, J. E. Rehg, and C. J. Sherr. 2001. Dmp1 is haplo-insufficient for tumor suppression and modifies the frequencies of Arf and p53 mutations in Myc-induced lymphomas. Genes Dev. 15:2934-2939.
17. Jiang, Z., and E. Zacksenhaus. 2002. Activation of retinoblastoma protein in mammary gland leads to ductal growth suppression, precocious differentiation, and adenocarcinoma. J. Cell Biol. 156:185-198.
18. Knudson, A. G. J. 1971. Mutation and cancer: statistical study of retinoblastoma. Proc. Natl. Acad. Sci. USA 68:820-823.
19. Koipally, J., and K. Georgopoulos. 2002. Ikaros-CtIP interactions do not require C-terminal binding protein and participate in a deacetylase-independent mode of repression. J. Biol. Chem. 277:23143-23149.
20. Koipally, J., A. Renold, J. Kim, and K. Georgopoulos. 1999. Repression by Ikaros and Aiolos is mediated through histone deacetylase complexes. EMBO J. 18:3090-3100.
21. Lee, E. Y., C. Y. Chang, N. Hu, Y. C. Wang, C. C. Lai, K. Herrup, W. H. Lee, and A. Bradley. 1992. Mice deficient for Rb are nonviable and show defects in neurogenesis and haematopoiesis. Nature 359:288-294.
22. Li, S., P. L. Chen, T. Subramanian, G. Chinnadurai, G. Tomlinson, C. K. Osborne, Z. D. Sharp, and W. H. Lee. 1999. Binding of CtIP to the BRCT repeats of BRCA1 involved in the transcription regulation of p21 is disrupted upon DNA damage. J. Biol. Chem. 274:11334-11338.
23. Li, S., N. S. Ting, L. Zheng, P. L. Chen, Y. Ziv, Y. Shiloh, E. Y. Lee, and W. H. Lee. 2000. Functional link of BRCA1 and ataxia telangiectasia gene product in DNA damage response. Nature 406:210-215.
24. Liu, C. Y., A. Flesken-Nikitin, S. Li, Y. Zeng, and W. H. Lee. 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.
25. Markey, M. P., S. P. Angus, M. W. Strobeck, S. L. Williams, R. W. Gunawardena, B. J. Aronow, and E. S. Knudsen. 2002. Unbiased analysis of RB-mediated transcriptional repression identifies novel targets and distinctions from E2F action. Cancer Res. 62:6587-6597.
26. McNairn, A. J., and D. M. Gilbert. 2003. Epigenomic replication: linking epigenetics to DNA replication. BioEssays 25:647-656.
27. Meloni, A. R., E. J. Smith, and J. R. Nevins. 1999. A mechanism for Rb/p130-mediated transcription repression involving recruitment of the CtBP corepressor. Proc. Natl. Acad. Sci. USA 96:9574-9579.
28. Peng, A., and P. L. Chen. 2003. NFBD1, like 53BP1, is an early and redundant transducer mediating Chk2 phosphorylation in response to DNA damage. J. Biol. Chem. 278:8873-8876.
29. Pennaneach, V., I. Salles-Passador, A. Munshi, H. Brickner, K. Regazzoni, F. Dick, N. Dyson, T. T. Chen, J. Y. Wang, R. Fotedar, and A. Fotedar. 2001. The large subunit of replication factor C promotes cell survival after DNA damage in an LxCxE motif- and Rb-dependent manner. Mol. Cell 7:715-727.
30. Rebollo, A., and C. Schmitt. 2003. Ikaros, Aiolos and Helios: transcription regulators and lymphoid malignancies. Immunol. Cell Biol. 81:171-175.
31. Riley, D. J., E. Y. Lee, and W. H. Lee. 1994. The retinoblastoma protein: more than a tumor suppressor. Annu. Rev. Cell Biol. 10:1-29.
32. Robertson, K. D., S. Ait-Si-Ali, T. Yokochi, P. A. Wade, P. L. Jones, and A. P. Wolffe. 2000. DNMT1 forms a complex with Rb, E2F1 and HDAC1 and represses transcription from E2F-responsive promoters. Nat. Genet. 25:338-342.
33. Schaeper, U., J. M. Boyd, S. Verma, E. Uhlmann, T. Subramanian, and G. Chinnadurai. 1995. Molecular cloning and characterization of a cellular phosphoprotein that interacts with a conserved C-terminal domain of adenovirus E1A involved in negative modulation of oncogenic transformation. Proc. Natl. Acad. Sci. USA 92:10467-10471.
34. Schaeper, U., T. Subramanian, L. Lim, J. M. Boyd, and G. Chinnadurai. 1998. Interaction between a cellular protein that binds to the C-terminal region of adenovirus E1A (CtBP) and a novel cellular protein is disrupted by E1A through a conserved PLDLS motif. J. Biol. Chem. 273:8549-8552.
35. Sheahan, S., C. O. Bellamy, L. Treanor, D. J. Harrison, and S. Prost. 2004. Additive effect of p53, p21 and Rb deletion in triple knockout primary hepatocytes. Oncogene 23:1489-1497.
36. Sterner, J. M., S. Dew-Knight, C. Musahl, S. Kornbluth, and J. M. Horowitz. 1998. Negative regulation of DNA replication by the retinoblastoma protein is mediated by its association with MCM7. Mol. Cell. Biol. 18:2748-2757.
37. Sui, G., C. Soohoo, B. Affar el, F. Gay, Y. Shi, W. C. Forrester, and Y. Shi. 2002. A DNA vector-based RNAi technology to suppress gene expression in mammalian cells. Proc. Natl. Acad. Sci. USA 99:5515-5520.
38. Sum, E. Y., B. Peng, X. Yu, J. Chen, J. Byrne, G. J. Lindeman, and J. E. Visvader. 2002. The LIM domain protein LMO4 interacts with the cofactor CtIP and the tumor suppressor BRCA1 and inhibits BRCA1 activity. J. Biol. Chem. 277:7849-7856.
39. Takemura, M., T. Kitagawa, S. Izuta, J. Wasa, A. Takai, T. Akiyama, and S. Yoshida. 1997. Phosphorylated retinoblastoma protein stimulates DNA polymerase alpha. Oncogene 15:2483-2492.
40. Tang, B., E. P. Bottinger, S. B. Jakowlew, K. M. Bagnall, J. Mariano, M. R. Anver, J. J. Letterio, and L. M. Wakefield. 1998. Transforming growth factor-beta1 is a new form of tumor suppressor with true haploid insufficiency. Nat. Med. 4:802-807.
41. Wang, J. H., A. Nichogiannopoulou, L. Wu, L. Sun, A. H. Sharpe, M. Bigby, and K. Georgopoulos. 1996. Selective defects in the development of the fetal and adult lymphoid system in mice with an Ikaros null mutation. Immunity 5:537-549.
42. Wong, A. K., P. A. Ormonde, R. Pero, Y. Chen, L. Lian, G. Salada, S. Berry, Q. Lawrence, P. Dayananth, P. Ha, S. V. Tavtigian, D. H. Teng, and P. L. Bartel. 1998. Characterization of a carboxy-terminal BRCA1 interacting protein. Oncogene 17:2279-2285.
43. Xu, X., K. U. Wagner, D. Larson, Z. Weaver, C. Li, T. Ried, L. Hennighausen, A. Wynshaw-Boris, and C. X. Deng. 1999. Conditional mutation of Brcal in mammary epithelial cells results in blunted ductal morphogenesis and tumour formation. Nat. Genet. 22:37-43.
44. Ye, X., A. A. Franco, H. Santos, D. M. Nelson, P. D. Kaufman, and P. D. Adams. 2003. Defective S phase chromatin assembly causes DNA damage, activation of the S phase checkpoint, and S phase arrest. Mol. Cell 11:341-351.
45. Yu, X., and R. Baer. 2000. Nuclear localization and cell cycle-specific expression of CtIP, a protein that associates with the BRCA1 tumor suppressor. J. Biol. Chem. 275:18541-18549.
46. Yu, X., L. C. Wu, A. M. Bowcock, A. Aronheim, and R. Baer. 1998. The C-terminal (BRCT) domains of BRCA1 interact in vivo with CtIP, a protein implicated in the CtBP pathway of transcriptional repression. J. Biol. Chem. 273:25388-25392.
47. Zheng, L., and W.-H. Lee. 2002. Retinoblastoma tumor suppressor and genome stability. Adv. Cancer Res. 85:13-50.