Nicotinamide adenine dinucleotide-induced multimerization of the co-repressor CtBP1 relies on a switching tryptophan

Journal of Biological Chemistry

Volumn 288, Issue 39, 2013, Pages 27836-27848

  Madison, Dana L ^a   Wirz, Jacqueline A ^b   Siess, Don ^a   Lundblad, James R ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEINS; BIOCHEMICAL ACTIVITY; COREPRESSORS; MULTIMERIZATION; NICOTINAMIDE ADENINE; ONCOGENESIS; TETRAMERIC; TRANSCRIPTIONAL REPRESSION;

GENE EXPRESSION;

AMINO ACIDS;

BINDING PROTEIN; C TERMINAL BINDING PROTEIN 1; NICOTINAMIDE ADENINE DINUCLEOTIDE; OXIDOREDUCTASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; TRYPTOPHAN; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CELL NUCLEUS; CONTROLLED STUDY; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN MOTIF; PROTEIN MULTIMERIZATION;

C-TERMINAL-BINDING PROTEIN; COREPRESSOR TRANSCRIPTION; DEHYDROGENASE; NAD; PROTEIN-PROTEIN INTERACTIONS; TRANSCRIPTION;

ALCOHOL OXIDOREDUCTASES; AMINO ACID MOTIFS; BINDING SITES; CELL LINE, TUMOR; CHROMATOGRAPHY, GEL; CROSS-LINKING REAGENTS; DNA-BINDING PROTEINS; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MUTAGENESIS; NAD; NUCLEOTIDES; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; TRYPTOPHAN; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 84884775407     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.493569     Document Type: Article

References (38)

1. Schaeper, U., Boyd, J.M., Verma, S., Uhlmann, E., Subramanian, T., and Chinnadurai, G. (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. U.S.A. 92, 10467-10471
2. Chinnadurai, G. (2002) CtBP. Unconventional transcriptional co-repressor in development and oncogenesis. Mol. Cell 9, 213-224
3. Hildebrand, J. D., and Soriano, P. (2002) Overlapping and unique roles for C-terminal binding protein 1 (CtBP1) and CtBP2 during mouse development. Mol. Cell. Biol. 2, 5296-5307
4. Postigo, A. A., Depp, J. L., Taylor, J. J., and Kroll, K. L. (2003) Regulation of Smad signaling through a differential recruitment of coactivators and corepressors by ZEB proteins. EMBO J. 22, 2453-2462
5. Nibu, Y., Zhang, H., and Levine, M. (1998) Interaction of short range repressors with Drosophila CtBP in the embryo. Science 280, 101-104
6. Chinnadurai, G. (2007) Transcriptional regulation by C-terminal binding proteins. Int. J. Biochem. Cell Biol. 39, 1593-1607
7. Zhang, Q., Piston, D. W., and Goodman, R. H. (2002) Regulation of corepressor function by nuclear NADH. Science 295, 1895-1897
8. Lin, X., Sun, B., Liang, M., Liang, Y.Y., Gast, A., Hildebrand, J., Brunicardi, F. C., Melchior, F., and Feng, X. H. (2003) Opposed regulation of corepressor CtBP by SUMOylation and PDZ binding. Mol. Cell 11, 1389-1396
9. Frisch, S. M., Reich, R., Collier, I. E., Genrich, L. T., Martin, G., and Goldberg, G. I. (1990) Adenovirus E1A represses protease gene expression and inhibits metastasis of human tumor cells. Oncogene 5, 75-83
10. Nadauld, L. D., Phelps, R., Moore, B. C., Eisinger, A., Sandoval, I. T., Chidester, S., Peterson, P. W., Manos, E. J., Sklow, B., Burt, R. W., and Jones, D. A. (2006) Adenomatous polyposis coli control of C-terminal binding protein-1 stability regulates expression of intestinal retinol dehydrogenases. J. Biol. Chem. 281, 37828-37835
11. Thillainadesan, G., Isovic, M., Loney, E., Andrews, J., Tini, M., and Torchia, J. (2008) Genome analysis identifies the p15ink4b tumour suppressor as a direct target of the ZNF217/Corest complex. Mol. Cell. Biol. 28, 6066-6077
12. Shi, Y., Sawada, J., Sui, G., Affar el, B., Whetstine, J. R., Lan, F., Ogawa, H., Luke, M.P., Nakatani, Y., and Shi, Y. (2003) Coordinated histone modifications mediated by a CtBP corepressor complex. Nature 422, 735-738
13. Ueda, J., Tachibana, M., Ikura, T., and Shinkai, Y. (2006) Zinc finger protein Wiz links G9a/GLP histone methyltransferases to the co-repressor molecule CtBP. J. Biol. Chem. 281, 20120-20128
14. Kumar, V., Carlson, J. E., Ohgi, K. A., Edwards, T. A., Rose, D. W., Escalante, C. R., Rosenfeld, M. G., and Aggarwal, A. K. (2002) Transcription corepressor CtBP is an NADβ-regulated dehydrogenase. Mol. Cell 10, 857-869
15. Balasubramanian, P., Zhao, L. J., and Chinnadurai, G. (2003) Nicotinamide adenine dinucleotide stimulates oligomerization, interaction with adenovirus E1A and an intrinsic dehydrogenase activity of CtBP. FEBS Lett. 537, 157-160
16. Nardini, M., Spanò, S., Cericola, C., Pesce, A., Massaro, A., Millo, E., Luini, A., Corda, D., and Bolognesi, M. (2003) CtBP/BARS. A dual-function protein involved in transcription corepression and Golgi membrane fission. EMBO J. 22, 3122-3130
17. Zhang, Y. W., and Arnosti, D. N. (2011) Conserved catalytic and C-terminal regulatory domains of the C-terminal binding protein corepressor fine-tune the transcriptional response in development. Mol. Cell. Biol. 31, 375-384
18. Bhambhani, C., Chang, J. L., Akey, D. L., and Cadigan, K. M. (2011) The oligomeric state of CtBP determines its role as a transcriptional co-activator and co-repressor of Wingless targets. EMBO J. 30, 2031-2043
19. Molloy, D. P., Milner, A. E., Yakub, I. K., Chinnadurai, G., Gallimore, P. H., Grand, R. J. (1998) Structural determinants present in the C-terminal binding protein binding site of adenovirus early region 1A proteins. J. Biol. Chem. 273, 20867-20876
20. Quinlan, K. G., Verger, A., Kwok, A., Lee, S. H., Perdomo, J., Nardini, M., Bolognesi, M., and Crossley, M. (2006) Role of the C-terminal binding protein PXDLS motif binding cleft in protein interactions and transcriptional repression. Mol. Cell. Biol. 26, 8202-8213
21. Madison, D.L., and Lundblad, J.R. (2010) C-terminal binding protein and poly(ADP)ribose polymerase 1 contribute to repression of the p21waf1/cip1 promoter. Oncogene 29, 6027-6039
22. Madison, D. L., Yaciuk, P., Kwok, R. P., and Lundblad, J. R. (2002) Acetylation of the adenovirus-transforming protein E1A determines nuclear localization by disrupting association with importin-. J. Biol. Chem. 277, 38755-38763
23. Sun, P., Enslen, H., Myung, P. S., and Maurer, R. A. (1994) Differential activation of CREB by Ca2+/calmodulin-dependent protein kinases type II and type IV involves phosphorylation of a site that negatively regulates activity. Genes Dev. 8, 2527-2539
24. Grant, G.A., Hu, Z., and Xu, X. L. (2002) Cofactor binding to Escherichia coli D-3-phosphoglycerate dehydrogenase induces multiple conformations which alter effector binding. J. Biol. Chem. 277, 39548-39553
25. Birktoft, J. J., and Banaszak, L. J. (1983) The presence of a histidine-aspartic acid pair in the active site of 2-hydroxyacid dehydrogenases. X-ray refinement of cytoplasmic malate dehydrogenase. J. Biol. Chem. 258, 472-482
26. Thio, S. S., Bonventre, J. V., and Hsu, S. I. (2004) The CtBP2 corepressor is regulated by NADH-dependent dimerization and possesses a novel N-terminal repression domain. Nucleic Acids Res. 32, 1836-1847
27. Kuppuswamy, M., Vijayalingam, S., Zhao, L. J., Zhou, Y., Subramanian, T., Ryerse, J., and Chinnadurai, G. (2008) Role of the PLDLS-binding cleft region of CtBP1 in recruitment of core and auxiliary components of the corepressor complex. Mol. Cell. Biol. 28, 269-281
28. Mani-Telang, P., Sutrias-Grau, M., Williams, G., and Arnosti, D. N. (2007) Role of NAD binding and catalytic residues in the C-terminal binding co-repressor. FEBS Lett. 581, 5241-5246
29. Phippen, T. M., Sweigart, A. L., Moniwa, M., Krumm, A., Davie, J. R., and Parkhurst, S. M. (2000) Drosophila C-terminal binding protein functions as a context dependent transcriptional co-factor and interferes with both mad and groucho transcriptional repression. J. Biol. Chem. 275, 37628-37637
30. Zhao, L. J., Kuppuswamy, M., Vijayalingam, S., and Chinnadurai, G. (2009) Interaction of ZEB and histone deacetylase with the PLDLS binding cleft region of monomeric C-terminal binding protein. BMC Mol. Biol. 10, 89
31. Nardini, M., Valente, C., Ricagno, S., Luini, A., Corda, D., and Bolognesi, M. (2009) CtBP1/BARS Gly1723Glu mutant structure. Impairing NAD(H)-binding and dimerization. Biochem. Biophys. Res. Commun. 381, 70-74
32. Fjeld, C. C., Birdsong, W. T., and Goodman, R. H. (2003) Differential binding of NAD and NADH allows the transcriptional corepressor carboxyl-terminal binding protein to serve as a metabolic sensor. Proc. Natl. Acad. Sci. U.S.A. 100, 9202-9207
33. Grooteclaes, M., Deveraux, Q., Hildebrand, J., Zhang, Q., Goodman, R. H., and Frisch, S. M. (2003) C-terminal-binding protein corepresses epithelial and proapoptotic gene expression programs. Proc. Natl. Acad. Sci. U.S.A. 100, 4568-4573
34. Grant, G. A., Xu, X. L., and Hu, Z. (2000) Removal of the tryptophan side chain 139 in Escherichia coli D-3-phosphoglycerate dehydrogenase produces a dimeric enzyme without cooperative effects. Arch. Biochem. Biophys. 375, 171-174
35. Straza, M. W., Paliwal, S., Kovi, R. C., Rajeshkumar, B., Trenh, P., Parker, D., Whalen, G. F., Lyle, S., Schiffer, C. A., and Grossman, S. R. (2010) Therapeutic targeting of C-terminal binding protein in human cancer. Cell Cycle 9, 3740-3750
36. Di, L. J., Byun, J. S., Wong, M. M., Wakano, C., Taylor, T., Bilke, S., Baek, S., Hunter, K., Yang, H., Lee, M., Zvosec, C., Khramtsova, G., Cheng, F., Perou, C. M., Miller, C. R., Raab, R., Olopade, O. I., and Gardner, K. (2013) Genome-wide profiles of CtBP link metabolism with genome stability and epithelial reprogramming in breast cancer. Nat. Commun. 4, 1449
37. Lundblad, J. R. (2006) Structural determinants of CtBP function. in CtBP Family Proteins (Chinnadurai, G., ed) pp. 83-92, Landes Bioscience and Springer Science-Business Media, New York
38. Yamada, K., Hara, N., Shibata, T., Osago, H., and Tsuchiya, M. (2006) The simultaneous measurement of nicotinamide adenine dinucleotide and related compounds by liquid chromatography/electrospray ionization tandem mass spectrometry. Anal. Biochem. 352, 282-285