Corepressor CtBP and nuclear speckle protein Pnn/DRS differentially modulate transcription and splicing of the E-cadherin gene

Molecular and Cellular Biology

Volumn 28, Issue 5, 2008, Pages 1584-1595

  Alpatov, Roman ^a   Shi, Yujiang ^b   Munguba, Gustavo C ^a   Moghimi, Babak ^a   Joo, Jeong Hoon ^a   Bungert, Jorg ^a   Sugrue, Stephen P ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA BINDING PROTEIN; NUCLEAR PROTEIN; PROTEIN CTBP; PROTEIN PNN; UNCLASSIFIED DRUG; UVOMORULIN; ALCOHOL DEHYDROGENASE; C TERMINAL BINDING PROTEIN; C-TERMINAL BINDING PROTEIN; CADHERIN; CELL ADHESION MOLECULE; COMPLEMENTARY DNA; GREEN FLUORESCENT PROTEIN; HEMAGGLUTININ; HYBRID PROTEIN; LUCIFERASE; MESSENGER RNA; PNN PROTEIN, HUMAN; REPRESSOR PROTEIN; RNA POLYMERASE II;

ARTICLE; CARCINOGENESIS; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; GENE TARGETING; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; RNA PROCESSING; RNA SPLICING; TRANSCRIPTION REGULATION; TUMOR SUPPRESSOR GENE; BIOLOGICAL MODEL; CELL LINE; CHROMATIN IMMUNOPRECIPITATION; CYTOLOGY; GENE EXPRESSION REGULATION; GENE VECTOR; GENETIC TRANSFECTION; GENETICS; HELA CELL; KIDNEY; METABOLISM; PROMOTER REGION; REPORTER GENE; RNA INTERFERENCE; SERODIAGNOSIS;

ALCOHOL OXIDOREDUCTASES; CADHERINS; CELL ADHESION MOLECULES; CELL LINE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN IMMUNOPRECIPITATION; DNA, COMPLEMENTARY; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION; GENES, REPORTER; GENETIC VECTORS; GREEN FLUORESCENT PROTEINS; HELA CELLS; HEMAGGLUTININS; HUMANS; KIDNEY; LUCIFERASES; MODELS, BIOLOGICAL; NUCLEAR PROTEINS; PRECIPITIN TESTS; PROMOTER REGIONS (GENETICS); PROTEIN BINDING; RECOMBINANT FUSION PROTEINS; REPRESSOR PROTEINS; RNA INTERFERENCE; RNA POLYMERASE II; RNA SPLICING; RNA, MESSENGER; TRANSCRIPTION, GENETIC; TRANSFECTION;

EID: 40749155486     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00421-07     Document Type: Article

References (64)

1. Alpatov, R., G. C. Munguba, P. Caton, J. H. Joo, Y. Shi, M. E. Hunt, and S. P. Sugrue. 2004. 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. 24:10223-10235.
2. Auboeuf, D., D. H. Dowhan, X. Li, K. Larkin, L. Ko, S. M. Berget, and B. W. O'Malley. 2004. CoAA, a nuclear receptor coactivator protein at the interface of transcriptional coactivation and RNA splicing. Mol. Cell. Biol. 24:442-453.
3. Auboeuf, D., A. Honig, S. M. Berget, and B. W. O'Malley. 2002. Coordinate regulation of transcription and splicing by steroid receptor coregulators. Science 298:416-419.
4. Balasubramanian, P., L. J. Zhao, and G. Chinnadurai. 2003. Nicotinamide adenine dinucleotide stimulates oligomerization, interaction with adenovirus E1A and an intrinsic dehydrogenase activity of CtBP. FEBS Lett. 537:157-160.
5. Batsche, E., M. Yaniv, and C. Muchardt. 2006. The human SWI/SNF subunit Brm is a regulator of alternative splicing. Nat. Struct. Mol. Biol. 13:22-29.
6. Cheng, C., and P. A. Sharp. 2006. Regulation of CD44 alternative splicing by SRm160 and its potential role in tumor cell invasion. Mol. Cell. Biol. 26:362-370.
7. Chinnadurai, G. 2002. CtBP, an unconventional transcriptional corepressor in development and oncogenesis. Mol. Cell 9:213-224.
8. Comijn, J., G. Berx, P. Vermassen, K. Verschueren, L. van Grunsven, E. Bruyneel, M. Mareel, D. Huylebroeck, and F. van Roy. 2001. The two-handed E box binding zinc finger protein SIP1 downregulates E-cadherin and induces invasion. Mol. Cell 7:1267-1278.
9. Cramer, P., J. F. Caceres, D. Cazalla, S. Kadener, A. F. Muro, F. E. Baralle, and A. R. Kornblihtt. 1999. Coupling of transcription with alternative splicing: RNA pol II promoters modulate SF2/ASF and 9G8 effects on an exonic splicing enhancer. Mol. Cell 4:251-258.
10. Cramer, P., C. G. Pesce, F. E. Baralle, and A. R. Kornblihtt. 1997. Functional association between promoter structure and transcript alternative splicing. Proc. Natl. Acad. Sci. USA 94:11456-11460.
11. Cramer, P., A. Srebrow, S. Kadener, S. Werbajh, M. de la Mata, G. Melen, G. Nogues, and A. R. Kornblihtt. 2001. Coordination between transcription and pre-mRNA processing. FEBS Lett. 498:179-182.
12. Dowhan, D. H., E. P. Hong, D. Auboeuf, A. P. Dennis, M. M. Wilson, S. M. Berget, and B. W. O'Malley. 2005. Steroid hormone receptor coactivation and alternative RNA splicing by U2AF65-related proteins CAPERalpha and CAPERbeta. Mol. Cell 17:429-439.
13. Fjeld, C. C., W. T. Birdsong, and R. H. Goodman. 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. USA 100:9202-9207.
14. Grimes, J. A., S. J. Nielsen, E. Battaglioli, E. A. Miska, J. C. Speh, D. L. Berry, F. Atouf, B. C. Holdener, G. Mandel, and T. Kouzarides. 2000. The co-repressor mSin3A is a functional component of the REST-CoREST repressor complex. J. Biol. Chem. 275:9461-9467.
15. Grooteclaes, M., Q. Deveraux, J. Hildebrand, Q. Zhang, R. H. Goodman, and S. M. Frisch. 2003. C-terminal-binding protein corepresses epithelial and proapoptotic gene expression programs. Proc. Natl. Acad. Sci. USA 100:4568-4573.
16. Grooteclaes, M. L., and S. M. Frisch. 2000. Evidence for a function of CtBP in epithelial gene regulation and anoikis. Oncogene 19:3823-3828.
17. 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.
18. Hirose, Y., and J. L. Manley. 2000. RNA polymerase II and the integration of nuclear events. Genes Dev. 14:1415-1429.
19. Izutsu, K., M. Kurokawa, Y. Imai, K. Maki, K. Mitani, and H. Hirai. 2001. The corepressor CtBP interacts with Evi-1 to repress transforming growth factor beta signaling. Blood 97:2815-2822.
20. Joo, J. H., R. Alpatov, G. C. Munguba, M. R. Jackson, M. E. Hunt, and S. P. Sugrue. 2005. Reduction of Pnn by RNAi induces loss of cell-cell adhesion between human corneal epithelial cells. Mol. Vis. 11:133-142.
21. Joo, J. H., Y. J. Lee, G. C. Munguba, S. Park, T. J. Taxter, M. Y. Elsagga, M. R. Jackson, S. P. Oh, and S. P. Sugrue. 2007. Role of Pinin in neural crest, dorsal dermis, and axial skeleton development and its involvement in the regulation of Tcf/Lef activity in mice. Dev. Dyn. 236:2147-2158.
22. Kim, J. H., E. J. Cho, S. T. Kim, and H. D. Youn. 2005. CtBP represses p300-mediated transcriptional activation by direct association with its bromodomain. Nat. Struct. Mol. Biol. 12:423-428.
23. Koipally, J., and K. Georgopoulos. 2000. Ikaros interactions with CtBP reveal a repression mechanism that is independent of histone deacetylase activity. J. Biol. Chem. 275:19594-19602.
24. Kornblihtt, A. R. 2005. Promoter usage and alternative splicing. Curr. Opin. Cell Biol. 17:262-268.
25. Kornblihtt, A. R. 2006. Chromatin, transcript elongation and alternative splicing. Nat. Struct. Mol. Biol. 13:5-7.
26. Kumar, V., J. E. Carlson, K. A. Ohgi, T. A. Edwards, D. W. Rose, C. R. Escalante, M. G. Rosenfeld, and A. K. Aggarwal. 2002. Transcription corepressor CtBP is an NAD(+)-regulated dehydrogenase. Mol. Cell 10:857-869.
27. Li, C., R. I. Lin, M. C. Lai, P. Ouyang, and W. Y. Tarn. 2003. Nuclear Pnn/DRS protein binds to spliced mRNPs and participates in mRNA processing and export via interaction with RNPS1. Mol. Cell. Biol. 23:7363-7376.
28. Maniatis, T., and R. Reed. 2002. An extensive network of coupling among gene expression machines. Nature 416:499-506.
29. Melhuish, T. A., and D. Wotton. 2000. The interaction of the carboxyl terminus-binding protein with the Smad corepressor TGIF is disrupted by a holoprosencephaly mutation in TGIF. J. Biol. Chem. 275:39762-39766.
30. 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.
31. Moisan, A., C. Larochelle, B. Guillemette, and L. Gaudreau. 2004. BRCA1 can modulate RNA polymerase II carboxy-terminal domain phosphorylation levels. Mol. Cell. Biol. 24:6947-6956.
32. Nardini, M., S. Spano, C. Cericola, A. Pesce, A. Massaro, E. Millo, A. Luini, D. Corda, and M. Bolognesi. 2003. CtBP/BARS: a dual-function protein involved in transcription co-repression and Golgi membrane fission. EMBO J. 22:3122-3130.
33. Nitta, E., K. Izutsu, Y. Yamaguchi, Y. Imai, S. Ogawa, S. Chiba, M. Kurokawa, and H. Hirai. 2005. Oligomerization of Evi-1 regulated by the PR domain contributes to recruitment of corepressor CtBP. Oncogene 24:6165-6173.
34. Ogawa, H., K. Ishiguro, S. Gaubatz, D. M. Livingston, and Y. Nakatani. 2002. A complex with chromatin modifiers that occupies E2F- and Mycresponsive genes in G0 cells. Science 296:1132-1136.
35. Ouyang, P., and S. P. Sugrue. 1996. Characterization of pinin, a novel protein associated with the desmosome-intermediate filament complex. J. Cell Biol. 135:1027-1042.
36. Ouyang, P., and S. P. Sugrue. 1992. Identification of an epithelial protein related to the desmosome and intermediate filament network. J. Cell Biol. 118:1477-1488.
37. Pagani, F., C. Stuani, E. Zuccato, A. R. Kornblihtt, and F. E. Baralle. 2003. Promoter architecture modulates CFTR exon 9 skipping. J. Biol. Chem. 278:1511-1517.
38. Peinado, H., E. Ballestar, M. Esteller, and A. Cano. 2004. Snail mediates E-cadherin repression by the recruitment of the Sin3A/histone deacetylase 1 (HDAC1)/HDAC2 complex. Mol. Cell. Biol. 24:306-319.
39. Phippen, T. M., A. L. Sweigart, M. Moniwa, A. Krumm, J. R. Davie, and S. M. Parkhurst. 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.
40. Postigo, A. A., and D. C. Dean. 2000. Differential expression and function of members of the zfh-1 family of zinc finger/homeodomain repressors. Proc. Natl. Acad. Sci. USA 97:6391-6396.
41. Postigo, A. A., and D. C. Dean. 1999. ZEB represses transcription through interaction with the corepressor CtBP. Proc. Natl. Acad. Sci. USA 96:6683-6688.
42. Proudfoot, N. J., A. Furger, and M. J. Dye. 2002. Integrating mRNA processing with transcription. Cell 108:501-512.
43. Reed, R. 2003. Coupling transcription, splicing and mRNA export. Curr. Opin. Cell Biol. 15:326-331.
44. Sakashita, E., S. Tatsumi, D. Werner, H. Endo, and A. Mayeda. 2004. Human RNPS1 and its associated factors: a versatile alternative pre-mRNA splicing regulator in vivo. Mol. Cell. Biol. 24:1174-1187.
45. Sato, S., C. Tomomori-Sato, T. J. Parmely, L. Florens, B. Zybailov, S. K. Swanson, C. A. Banks, J. Jin, Y. Cai, M. P. Washburn, J. W. Conaway, and R. C. Conaway. 2004. A set of consensus mammalian mediator subunits identified by multidimensional protein identification technology. Mol. Cell 14:685-691.
46. Sewalt, R. G. A. B., M. J. Gunster, J. van der Vlag, D. P. E. Satijn, and A. P. Otte. 1999. C-terminal binding protein is a transcriptional repressor that interacts with a specific class of vertebrate Polycomb proteins. Mol. Cell. Biol. 19:777-787.
47. Shi, J., and S. P. Sugrue. 2000. Dissection of protein linkage between keratins and pinin, a protein with dual location at desmosome- intermediate filament complex and in the nucleus. J. Biol. Chem. 275:14910-14915.
48. Shi, Y., M. N. Simmons, T. Seki, S. P. Oh, and S. P. Sugrue. 2001. Change in gene expression subsequent to induction of Pnn/DRS/memA: increase in p21(cip1/waf1). Oncogene 20:4007-4018.
49. Shi, Y., F. Lan, C. Matson, P. Mulligan, J. R. Whetstine, P. A. Cole, and R. A. Casero. 2004. Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 119:941-953.
50. Shi, Y., P. Ouyang, and S. P. Sugrue. 2000. Characterization of the gene encoding pinin/DRS/memA and evidence for its potential tumor suppressor function. Oncogene 19:289-297.
51. Shi, Y., J. Sawada, G. Sui, B. el Affar, J. R. Whetstine, F. Lan, H. Ogawa, M. P. Luke, and Y. Nakatani. 2003. Coordinated histone modifications mediated by a CtBP co-repressor complex. Nature 422:735-738.
52. Shi, Y., M. Tabesh, and S. P. Sugrue. 2000. Role of cell adhesion-associated protein, pinin (DRS/memA), in corneal epithelial migration. Investig. Ophthalmol. Vis. Sci. 41:1337-1345.
53. Smith, M. J., S. Kulkarni, and T. Pawson. 2004. FF domains of CA150 bind transcription and splicing factors through multiple weak interactions. Mol. Cell. Biol. 24:9274-9285.
54. Srinivasan, L., and M. L. Atchison. 2004. YY1 DNA binding and PcG recruitment requires CtBP. Genes Dev. 18:2596-2601.
55. Sutrias-Grau, M., and D. N. Arnosti. 2004. CtBP contributes quantitatively to Knirps repression activity in an NAD binding-dependent manner. Mol. Cell. Biol. 24:5953-5966.
56. Tasic, B., C. E. Nabholz, K. K. Baldwin, Y. Kim, E. H. Rueckert, S. A. Ribich, P. Cramer, Q. Wu, R. Axel, and T. Maniatis. 2002. Promoter choice determines splice site selection in protocadherin alpha and gamma pre-mRNA splicing. Mol. Cell 10:21-33.
57. Thio, S. S., J. V. Bonventre, and S. I. Hsu. 2004. The CtBP2 co-repressor is regulated by NADH-dependent dimerization and possesses a novel N-terminal repression domain. Nucleic Acids Res. 32:1836-1847.
58. Wang, P., P. J. Lou, S. Leu, and P. Ouyang. 2002. Modulation of alternative pre-mRNA splicing in vivo by pinin. Biochem. Biophys. Res. Commun. 294:448-455.
59. Wysocka, J., T. A. Milne, and C. D. Allis. 2005. Taking LSD1 to a new high. Cell 122:654-658.
60. Zhang, C., D. R. Dowd, A. Staal, C. Gu, J. B. Lian, A. J. van Wijnen, G. S. Stein, and P. N. MacDonald. 2003. Nuclear coactivator-62 kDa/Ski-interacting protein is a nuclear matrix-associated coactivator that may couple vitamin D receptor-mediated transcription and RNA splicing. J. Biol. Chem. 278:35325-35336.
61. Zhang, Q., D. W. Piston, and R. H. Goodman. 2002. Regulation of corepressor function by nuclear NADH. Science 295:1895-1897.
62. Zhang, Q., S. Wang, A. Nottke, J. V. Rocheleau, D. W. Piston, and R. H. Goodman. 2006. Redox sensor CtBP mediates hypoxia-induced tumor cell migration. Proc. Natl. Acad. Sci. USA 103:9029-9033.
63. Zimowska, G., J. Shi, G. Munguba, M. R. Jackson, R. Alpatov, M. N. Simmons, Y. Shi, and S. P. Sugrue. 2003. Pinin/DRS/memA interacts with SRp75, SRm300 and SRrp130 in corneal epithelial cells. Investig. Ophthalmol. Vis. Sci. 44:4715-4723.
64. Zorio, D. A., and D. L. Bentley. 2004. The link between mRNA processing and transcription: communication works both ways. Exp. Cell Res. 296:91-97.