C-terminal binding proteins: Emerging roles in cell survival and tumorigenesis

Apoptosis

Volumn 11, Issue 6, 2006, Pages 879-888

  Bergman, L M ^a,b   Blaydes, J P ^a  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^b SOUTHAMPTON GENERAL HOSPITAL   (United Kingdom)

Author keywords

Apoptosis; Cancer; CtBP; Golgi; Transcriptional repression

Indexed keywords

BINDING PROTEIN; GROWTH FACTOR RECEPTOR; HORMONE RECEPTOR; ONCOPROTEIN; PROTEIN P53; TRANSCRIPTION FACTOR; TRANSFORMING GROWTH FACTOR BETA; WNT1 PROTEIN;

APOPTOSIS; CARBOXY TERMINAL SEQUENCE; CARCINOGENESIS; CELL CYCLE; CELL DEATH; CELL DIFFERENTIATION; CELL NUCLEUS; CELL SURVIVAL; CYTOPLASM; GENE CONTROL; GENE EXPRESSION; GENE STRUCTURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; STRESS;

ALCOHOL OXIDOREDUCTASES; ANIMALS; APOPTOSIS; CELL SURVIVAL; DNA-BINDING PROTEINS; HUMANS; NEOPLASMS;

ADENOVIRIDAE;

EID: 33745031855     PISSN: 13608185     EISSN: 1573675X     Source Type: Journal    
DOI: 10.1007/s10495-006-6651-4     Document Type: Review

References (117)

1. Sang N, Caro J, Giordano A. Adenoviral E1A: Everlasting tool, versatile applications, continuous contributions and new hypotheses. Front Biosci 2002; 7: d407-13.
2. Endter C, Dobner T. Cell transformation by human adenoviruses. Curr Top Microbiol Immunol 2004; 273: 163-214.
3. Schneider JF, Fisher F, Goding CR, Jones NC. Mutational analysis of the adenovirus E1a gene: The role of transcriptional regulation in transformation. Embo J 1987; 6: 2053-2060.
4. Whyte P, Williamson NM, Harlow E. Cellular targets for transformation by the adenovirus E1A proteins. Cell 1989; 56: 67-75.
5. Subramanian T, La Regina M, Chinnadurai G. Enhanced ras oncogene mediated cell transformation and tumorigenesis by adenovirus 2 mutants lacking the C-terminal region of E1a protein. Oncogene 1989; 4: 415-420.
6. Subramanian T, Malstrom SE, Chinnadurai G. Requirement of the C-terminal region of adenovirus E1a for cell transformation in cooperation with E1b. Oncogene 1991; 6: 1171-1173.
7. Chinnadurai G. Modulation of oncogenic transformation by the human adenovirus E1A C-terminal region. Curr Top Microbiol Immunol 2004; 273: 139-161.
8. Boyd JM, Subramanian T, Schaeper U, et al. A region in the C-terminus of adenovirus 2/5 E1a protein is required for association with a cellular phosphoprotein and important for the negative modulation of T24-ras mediated transformation, tumorigenesis and metastasis. Embo J 1993; 12: 469-478.
9. Schaeper U, Boyd JM, Verma S, et al. 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 1995; 92: 10467-10471.
10. Katsanis N, Fisher EM. A novel C-terminal binding protein (CTBP2) is closely related to CTBP1, an adenovirus E1A-binding protein, and maps to human chromosome 21q21.3. Genomics 1998; 47: 294-299.
11. Touitou R, Hickabottom M, Parker G, et al. Physical and functional interactions between the corepressor CtBP and the Epstein-Barr virus nuclear antigen EBNA3C. J Virol 2001; 75: 7749-7755.
12. Hickabottom M, Parker GA, Freemont P, et al. Two nonconsensus sites in the Epstein-Barr virus oncoprotein EBNA3A cooperate to bind the co-repressor carboxyl-terminal-binding protein (CtBP). J Biol Chem 2002; 277: 47197-47204.
13. Nibu Y, Zhang H, Bajor E, et al. dCtBP mediates transcriptional repression by Knirps, Kruppel and Snail in the Drosophila embryo. Embo J 1998; 17: 7009-7020.
14. Poortinga G, Watanabe M, Parkhurst SM. Drosophila CtBP: A Hairy-interacting protein required for embryonic segmentation and hairy-mediated transcriptional repression. Embo J 1998; 17: 2067-2078.
15. Nibu Y, Zhang H, Levine M. Interaction of short-range repressors with Drosophila CtBP in the embryo. Science 1998; 280: 101-104.
16. Chinnadurai G. CtBP, an unconventional transcriptional corepressor in development and oncogenesis. Mol Cell 2002; 9: 213-214.
17. Turner J, Crossley M. The CtBP family: Enigmatic and enzymatic transcriptional co-repressors. Bioessays 2001; 23: 683-690.
18. Furusawa T, Moribe H, Kondoh H, Higashi Y. Identification of CtBP1 and CtBP2 as corepressors of zinc finger-homeodomain factor deltaEF1. Mol Cell Biol 1999; 19: 8581-8590.
19. Hildebrand JD, Soriano P. Overlapping and unique roles for C-terminal binding protein 1 (CtBP1) and CtBP2 during mouse development. Mol Cell Biol 2002; 22: 5296-5307.
20. Sewalt RG, Gunster MJ, van der Vlag J, et al. C-Terminal binding protein is a transcriptional repressor that interacts with a specific class of vertebrate Polycomb proteins. Mol Cell Biol 1999; 19: 777-787.
21. Schmitz F, Konigstorfer A, Sudhof TC. RIBEYE, a component of synaptic ribbons: A protein's journey through evolution provides insight into synaptic ribbon function. Neuron 2000; 28: 857-872.
22. Piatigorsky J. Dual use of the transcriptional repressor (CtBP2)/ribbon synapse (RIBEYE) gene: how prevalent are multifunctional genes? Trends Neucrosci 2001; 24: 555-557.
23. Spano S, Silletta MG, Colanzi A, et al. Molecular cloning and functional characterization of brefeldin A-ADP-ribosylated substrate. A novel protein involved in the maintenance of the Golgi structure. J Biol Chem 1999; 274: 17705-17710.
24. Monleon I, Iturralde M, Martinez-Lorenzo MJ, et al. Lack of Fas/CD95 surface expression in highly proliferative leukemic cell lines correlates with loss of CtBP/BARS and redirection of the protein toward giant lysosomal structures. Cell Growth Differ 2002; 13: 315-324.
25. Lin X, Sun B, Liang M, et al. Opposed regulation of corepressor CtBP by SUMOylation and PDZ binding. Mol Cell 2003; 11: 1389-1396.
26. Kumar V, Carlson JE, Ohgi KA, et al. Transcription corepressor CtBP is an NAD(+)-regulated dehydrogenase. Mol Cell 2002; 10: 857-869.
27. Balasubramanian P, Zhao LJ, Chinnadurai G. Nicotinamide adenine dinucleotide stimulates oligomerization, interaction with adenovirus E1A and an intrinsic dehydrogenase activity of CtBP. FEBS Lett 2003; 537: 157-160.
28. Nardini M, Spano S, Cericola C, et al. CtBP/BARS: a dual-function protein involved in transcription co-repression and Golgi membrane fission. Embo J 2003; 22: 3122-3130.
29. Thio SS, Bonventre JV, Hsu SI. The CtBP2 co-repressor is regulated by NADH-dependent dimerization and possesses a novel N-terminal repression domain. Nucleic Acids Res 2004; 32: 1836-1847.
30. Zhang Q, Piston DW, Goodman RH. Regulation of corepressor function by nuclear NADH. Science 2002; 295: 1895-1897.
31. Fjeld CC, Birdsong WT, Goodman RH. Differential binding of NAD+ and NADH allows the transcriptional corepressor carboxyl-terminal binding protein to serve as a metabolic sensor. Proc Natl Acad Sci USA 2003; 100: 9202-9207.
32. Criqui-Filipe P, Ducret C, Maira SM, Wasylyk B. Net, a negative Ras-switchable TCF, contains a second inhibition domain, the CID, that mediates repression through interactions with CtBP and de-acetylation. Embo J 1999; 18: 3392-3403.
33. Sollerbrant K, Chinnadurai G, Svensson C. The CtBP binding domain in the adenovirus E1A protein controls CR1-dependent transactivation. Nucleic Acids Res 1996; 24: 2578-2584.
34. Turner J, Crossley M. Cloning and characterization of mCtBP2, a co-repressor that associates with basic Kruppel-like factor and other mammalian transcriptional regulators. Embo J 1998; 17: 5129-5140.
35. Koipally J, Georgopoulos K. Ikaros interactions with CtBP reveal a repression mechanism that is independent of histone deacetylase activity. J Biol Chem 2000; 275: 19594-19602.
36. Vo N, Fjeld C, Goodman RH. Acetylation of nuclear hormone receptor-interacting protein RIP140 regulates binding of the transcriptional corepressor CtBP. Mol Cell Biol 2001; 21: 6181-6188.
37. Molloy DP, Barral PM, Bremner KH, et al. Structural determinants outside the PXDLS sequence affect the interaction of adenovirus E1A, C-terminal interacting protein and Drosophila repressors with C-terminal binding protein. Biochim Biophys Acta 2001; 1546: 55-70.
38. Postigo AA, Dean DC. ZEB represses transcription through interaction with the corepressor CtBP. Proc Natl Acad Sci USA 1999; 96: 6683-6688.
39. Grooteclaes ML, Frisch SM. Evidence for a function of CtBP in epithelial gene regulation and anoikis. Oncogene 2000; 19: 3823-3828.
40. Frisch SM. Tumor suppression activity of adenovirus E1a protein: Anoikis and the epithelial phenotype. Adv Cancer Res 2001; 80: 39-49.
41. Peinado H, Portillo F, Cano A. Transcriptional regulation of cadherins during development and carcinogenesis. Int J Dev Biol 2004; 48: 365-375.
42. Tripathi MK, Misra S, Khedkar SV, et al. Regulation of BRCA2 Gene Expression by the SLUG Repressor Protein in Human Breast Cells. J Biol Chem 2005; 280: 17163-17171.
43. Shi Y, Sawada J, Sui G, et al. Coordinated histone modifications mediated by a CtBP co-repressor complex. Nature 2003; 422: 735-738.
44. Zhang CL, McKinsey TA, Lu JR, Olson EN. Association of COOH-terminal-binding protein (CtBP) and MEF2-interacting transcription repressor (MITR) contributes to transcriptional repression of the MEF2 transcription factor. J Biol Chem 2001; 276: 35-39.
45. Meloni AR, Smith EJ, Nevins JR. A mechanism for Rb/p130-mediated transcription repression involving recruitment of the CtBP corepressor. Proc Natl Acad Sci USA 1999; 96: 9574-9579.
46. Srinivasan L, Atchison ML. YY1 DNA binding and PcG recruitment requires CtBP. Genes Dev 2004; 18: 2596-2601.
47. Levine SS, King IF, Kingston RE. Division of labor in polycomb group repression. Trends Biochem Sci 2004; 29: 478-485.
48. Kim JH, Cho EJ, Kim ST, Youn HD. CtBP represses p300-mediated transcriptional activation by direct association with its bromodomain. Nat Struct Mol Biol 2005.
49. Weigert R, Silletta MG, Spano S, et al. CtBP/BARS induces fission of Golgi membranes by acylating lysophosphatidic acid. Nature 1999; 402: 429-433.
50. Hidalgo Carcedo C, Bonazzi M, Spano S, et al. Mitotic Golgi partitioning is driven by the membrane-fissioning protein CtBP3/BARS. Science 2004; 305: 93-96.
51. Diao A, Lowe M. Cell biology. The Golgi goes fission. Science 2004; 305: 48-49.
52. Bonazzi M, Spano S, Turacchio G, et al. CtBP3/BARS drives membrane fission in dynamin-independent transport pathways. Nat Cell Biol 2005.
53. Brannon M, Brown JD, Bates R, et al. XCtBP is a XTcf-3 co-repressor with roles throughout Xenopus development. Development 1999; 126: 3159-3170.
54. Grooteclaes M, Deveraux Q, Hildebrand J, et al. C-terminal-binding protein corepresses epithelial and proapoptotic gene expression programs. Proc Natl Acad Sci USA 2003; 100: 4568-4573.
55. Zhang Q, Yoshimatsu Y, Hildebrand J, et al. Homeodomain interacting protein kinase 2 promotes apoptosis by downregulating the transcriptional corepressor CtBP. Cell 2003; 115: 177-186.
56. Frisch SM. E1a induces the expression of epithelial characteristics. J Cell Biol 1994; 127: 1085-1096.
57. Gooding JM, Yap KL, Ikura M. The cadherin-catenin complex as a focal point of cell adhesion and signalling: New insights from three-dimensional structures. Bioessays 2004; 26: 497-511.
58. Patel SD, Chen CP, Bahna F, et al. Cadherin-mediated cell-cell adhesion: Sticking together as a family. Curr Opin Struct Biol 2003; 13: 690-698.
59. Hay ED. The mesenchymal cell, its role in the embryo, and the remarkable signaling mechanisms that create it. Dev Dyn 2005; 233: 706-720.
60. Wheeler JM. Epigenetics, mismatch repair genes and colorectal cancer. Ann R Coll Surg Engl 2005; 87: 15-20.
61. Wang HD, Ren J, Zhang L. CDH1 germline mutation in hereditary gastric carcinoma. World J Gastroenterol 2004; 10: 3088-3093.
62. Chen XF, Zhang HT, Qi QY, et al. Expression of E-cadherin and nm23 is associated with the clinicopathological factors of human non-small cell lung cancer in China. Lung Cancer 2005; 48: 69-76.
63. Syrigos KN, Karapanagiotou E, Harrington KJ. The clinical significance of molecular markers to bladder cancer. Hybrid Hybridomics 2004; 23: 335-342.
64. Nair KS, Naidoo R, Chetty R. Expression of cell adhesion molecules in oesophageal carcinoma and its prognostic value. J Clin Pathol 2005; 58: 343-351.
65. Quinn DI, Henshall SM, Sutherland RL. Molecular markers of prostate cancer outcome. Eur J Cancer 2005; 41: 858-887.
66. Simpson PT, Reis-Filho JS, Gale T, Lakhani SR. Molecular evolution of breast cancer. J Pathol 2005; 205: 248-254.
67. Vega S, Morales AV, Ocana OH, et al. Snail blocks the cell cycle and confers resistance to cell death. Genes Dev 2004; 18: 1131-1143.
68. Hennig G, Behrens J, Truss M, et al. Progression of carcinoma cells is associated with alterations in chromatin structure and factor binding at the E-caclhenn promoter in vivo. Oncogene 1995; 11: 475-484.
69. Hemavathy K, Hu X, Ashraf SI, et al. The repressor function of snail is required for Drosophila gastrulation and is not replaceable by Escargot or Worniu. Dev Biol 2004; 269: 411-420.
70. Sugimachi K, Tanaka S, Kameyama T, et al. Transcriptional repressor snail and progression of human hepatocellular carcinoma. Clin Cancer Res 2003; 9: 2657-2664.
71. Blanco MJ, Moreno-Bueno G, Sarrio D, et al. Correlation of Snail expression with histological grade and lymph node status in breast carcinomas. Oncogene 2002; 21: 3241-3246.
72. Elloul S, Elstrand MB, Nesland JM, et al. Snail, Slug, and Smad-interacting protein 1 as novel parameters of disease aggressiveness in metastatic ovarian and breast carcinoma. Cancer 2005; 103: 1631-1643.
73. Moody SE, Perez D, Pan TC, et al. The transcriptional repressor Snail promotes mammary tumor recurrence. Cancer Cell 2005; 8: 197-209.
74. Alpatov R, Munguba GC, Caton P, et al. Nuclear speckle-associated protein Pnn/DRS binds to the transcriptional corepressor CtBP and relieves CtBP-mediated repression of the E-cadherin gene. Mol Cell Biol 2004; 24: 10223-10235.
75. Doucas H, Garcea G, Neal CP, et al. Changes in the Wnt signalling pathway in gastrointestinal cancers and their prognostic significance. Eur J Cancer 2005; 41: 365-379.
76. Chen T, Yang I, Irby R, et al. Regulation of caspase expression and apoptosis by adenomatous polyposis coll. Cancer Res 2003; 63: 4368-4374.
77. Hamada F, Bienz M. The APC tumor suppressor binds to C-terminal binding protein to divert nuclear beta-catenin from TCF. Dev Cell 2004; 7: 677-685.
78. Sood R, Talwar-Trikha A, Chakrabarti SR, Nucifora G. MDS1/EVI1 enhances TGF-beta1 signaling and strengthens its growth-inhibitory effect but the leukemia-associated fusion protein AML1/MDS1/EVI1, product of the t(3;21), abrogates growth-inhibition in response to TGF-beta1. Leukemia 1999; 13: 348-357.
79. Hirai H, Izutsu K, Kurokawa M, Mitani K. Oncogenic mechanisms of Evi-1 protein. Cancer Chemother Pharmacol 2001; 48 (Suppl 1): S35-S40.
80. Izutsu K, Kurokawa M, Imai Y, et al. The corepressor CtBP interacts with Evi-1 to repress transforming growth factor beta signaling. Blood 2001; 97: 2815-2822.
81. Palmer S, Brouillet JP, Kilbey A, et al. Evi-1 transforming and repressor activities are mediated by CtBP co-repressor proteins. J Biol Chem 2001; 276: 25834-25840.
82. Alliston T, Ko TC, Cao Y, et al. Repression of BMP and activin-inducible transcription by Evi-1. J Biol Chem 2005.
83. Siegel PM, Massague J. Cytostatic and apoptotic actions of TGF-beta in homeostasis and cancer. Nat Rev Cancer 2003; 3: 807-821.
84. Mitani K. Molecular mechanisms of leukemogenesis by AML1/EVI-1. Oncogene 2004; 23: 4263-4269.
85. Melhuish TA, Wotton D. The interaction of the carboxyl terminus-binding protein with the Smad corepressor TGIF is disrupted by a holoprosencephaly mutation in TGIF. J Biol Chem 2000; 275: 39762-39766.
86. Lin X, Liang YY, Sun B, et al. Smad6 recruits transcription corepressor CtBP to repress bone morphogenetic protein-induced transcription. Mol Cell Biol 2003; 23: 9081-9093.
87. Parrinello S, Lin CQ, Murata K, et al. Id-1, ITF-2, and Id-2 comprise a network of helix-loop-helix proteins that regulate mammary epithelial cell proliferation, differentiation, and apoptosis. J Biol Chem 2001; 276: 39213-39219.
88. Wong YC, Wang X, Ling MT. Id-1 expression and cell survival. Apoptosis 2004; 9: 279-289.
89. Postigo AA, Depp JL, Taylor JJ, Kroll KL. Regulation of Smad signaling through a differential recruitment of coactivators and corepressors by ZEB proteins. Embo J 2003; 22: 2453-2462.
90. Steel JH, White R, Parker MG. Role of the RIP140 corepressor in ovulation and adipose biology. J Endocrinol 2005; 185: 1-9.
91. Castet A, Boulahtouf A, Versini G, et al. Multiple domains of the Receptor-Interacting Protein 140 contribute to transcription inhibition. Nucleic Acids Res 2004; 32: 1957-1966.
92. Schaeper U, Subramanian T, Lim L, et al. 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 1998; 273: 8549-8552.
93. Koipally J, Georgopoulos K. Ikaros-CtIP interactions do not require C-terminal binding protein and participate in a deacetylase-independent mode of repression. J Biol Chem 2002; 277: 23143-23149.
94. Chen PL, Liu F, Cai S, et al. Inactivation of CtIP Leads to Early Embryonic Lethality Mediated by G1 Restraint and to Tumorigenesis by Haploid Insufficiency. Mol Cell Biol 2005; 25: 3535-3542.
95. Wong AK, Ormonde PA, Pero R, et al. Characterization of a carboxy-terminal BRCA1 interacting protein. Oncogene 1998; 17: 2279-2285.
96. Yu X, Wu LC, Bowcock AM, et al. 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 1998; 273: 25388-25392.
97. Yoshida K, Miki Y. Role of BRCA1 and BRCA2 as regulators of DNA repair, transcription, and cell cycle in response to DNA damage. Cancer Sci 2004; 95: 866-871.
98. Powell SN, Kachnic LA. Roles of BRCA1 and BRCA2 in homologous recombination, DNA replication fidelity and the cellular response to ionizing radiation. Oncogene 2003; 22: 5784-5791.
99. Li S, Chen PL, Subramanian T, et al. Binding of CtIP to the BRCT repeats of BRCA1 involved in the transcription regulation of p21 is disrupted upon DNA damage. J Biol Chem 1999; 274: 11334-11338.
100. Li S, Ting NS, Zheng L, et al. Functional link of BRCA1 and ataxia telangiectasia gene product in DNA damage response. Nature 2000; 406: 210-215.
101. Yu X, Baer R. Nuclear localization and cell cycle-specific expression of CtIP, a protein that associates with the BRCA1 tumor suppressor. J Biol Chem 2000; 275: 18541-18549.
102. Wu-Baer F, Baer R. Effect of DNA damage on a BRCA1 complex. Nature 2001; 414: 36.
103. Yu X, Chen J. DNA damage-induced cell cycle checkpoint control requires CtIP, a phosphorylation-dependent binding partner of BRCA1 C-terminal domains. Mol Cell Biol 2004; 24: 9478-9486.
104. Vogelstein B, Lane D, Levine AJ. Surfing the p53 network. Nature 2000; 408: 307-310.
105. Mirnezami AH, Campbell SJ, Darley M, et al. Hdm2 recruits a hypoxia-sensitive corepressor to negatively regulate p53-dependent transcription. Curr Biol 2003; 13: 1234-1239.
106. Momand J, Wu HH, Dasgupta G. MDM2-master regulator of the p53 tumor suppressor protein. Gene 2000; 242: 15-29.
107. Kim YH, Choi CY, Lee SJ, et al. Homeodomain-interacting protein kinases, a novel family of co-repressors for homeodomain transcription factors. J Biol Chem 1998; 273: 25875-25879.
108. D'Orazi G, Cecchinelli B, Bruno T, et al. Homeodomain-interacting protein kinase-2 phosphorylates p53 at Ser 46 and mediates apoptosis. Nat Cell Biol 2002; 4: 11-19.
109. Hofmann TG, Moller A, Sirma H, et al. Regulation of p53 activity by its interaction with homeodomain-interacting protein kinase-2. Nat Cell Biol 2002; 4: 1-10.
110. Zhang Q, Nottke A, Goodman RH. Homeodomain-interacting protein kinase-2 mediates CtBP phosphorylation and degradation in UV-triggered apoptosis. Proc Natl Acad Sci USA 2005; 102: 2802-2807.
111. Riefler GM, Firestein BL. Binding of neuronal nitric-oxide synthase (nNOS) to carboxyl-terminal-binding protein (CtBP) changes the localization of CtBP from the nucleus to the cytosol: A novel function for targeting by the PDZ domain of nNOS. J Biol Chem 2001; 276: 48262-48268.
112. Kagey MH, Melhuish TA, Wotton D. The polycomb protein Pc2 is a SUMO E3. Cell 2003; 113: 127-137.
113. Barnes CJ, Vadlamudi RK, Mishra SK, et al. Functional inactivation of a transcriptional corepressor by a signaling kinase. Nat Struct Biol 2003; 10: 622-628.
114. Poser I, Golob M, Weidner M, et al. Down-regulation of COOH-terminal binding protein expression in malignant melanomas leads to induction of MIA expression. Cancer Res 2002; 62: 5962-5966.
115. Poser I, Bosserhoff AK. Transcription factors involved in development and progression of malignant melanoma. Histol Histopathol 2004; 19: 173-188.
116. Lui WO, Foukakis T, Liden J, et al. Expression profiling reveals a distinct transcription signature in follicular thyroid carcinomas with a PAX8-PPAR(gamma) fusion oncogene. Oncogene 2005; 24: 1467-1476.
117. Johansson C, Zhao H, Bajak E, et al. Impact of the interaction between adenovirus E1A and CtBP on host cell gene expression. Virus Res 2005.