Transforming growth factor-β/SMAD target gene SKIL is negatively regulated by the transcriptional cofactor complex SNON-SMAD4

Journal of Biological Chemistry

Volumn 287, Issue 32, 2012, Pages 26764-26776

  Tecalco Cruz, Angeles C ^a   Sosa Garrocho, Marcela ^a   Vázquez Victorio, Genaro ^a   Ortiz García, Layla ^a   Domínguez Hüttinger, Elisa ^a   Macías Silva, Marina ^a  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

BIOINFORMATICS ANALYSIS; CANCER CELLS; COFACTOR COMPLEXES; CORE PROMOTERS; COREPRESSORS; FOUR-GROUP; GENE ENCODES; GENE PROMOTER; HISTONE DEACETYLASES; MOLECULAR MECHANISM; NEGATIVE FEEDBACK LOOP; PROTEASOMES; PROTEIN LEVEL; RESPONSE ELEMENTS; TARGET GENES; TRANSCRIPTION START SITE; TRANSFORMING GROWTH FACTORS;

BIOINFORMATICS; CLONING; DEGRADATION; ENZYME INHIBITION; GENES; PROTEINS;

TRANSCRIPTION;

HISTONE DEACETYLASE; PROTEIN SNON; SMAD PROTEIN; SMAD4 PROTEIN; TRANSCRIPTION FACTOR; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; DNA RESPONSIVE ELEMENT; EMBRYO; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; MOLECULAR CLONING; NEGATIVE FEEDBACK; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PROTEIN INTERACTION; SKIL GENE; TRANSCRIPTION INITIATION SITE; UPREGULATION;

CELL LINE, TUMOR; CHROMATIN IMMUNOPRECIPITATION; GENE EXPRESSION REGULATION; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PROMOTER REGIONS, GENETIC; PROTO-ONCOGENE PROTEINS; SMAD4 PROTEIN; TRANSCRIPTION, GENETIC; TRANSFORMING GROWTH FACTOR BETA;

EID: 84864550426     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.386599     Document Type: Article

References (58)

1. Shi, Y., and Massagué, J. (2003) Mechanisms of TGF-β signaling from cell membrane to the nucleus. Cell 113, 685-700 (Pubitemid 36724933)
2. Attisano, L., and Wrana, J. L. (2002) Signal transduction by the TGF-βsuperfamily. Science 296, 1646-1647
3. Macías-Silva, M., Abdollah, S., Hoodless, P. A., Pirone, R., Attisano, L., and Wrana, J. L. (1996) MADR2 is a substrate of the TGFβ receptor and its phosphorylation is required for nuclear accumulation and signaling. Cell 87, 1215-1224 (Pubitemid 27010105)
4. Massagué, J., Seoane, J., and Wotton, D. (2005) Smad transcription factors. Genes Dev. 19, 2783-2810 (Pubitemid 41739965)
5. Luo, K. (2004) Ski and SnoN: negative regulators of TGF-β signaling. Curr. Opin. Genet. Dev. 14, 65-70
6. Liu, X., Sun, Y., Weinberg, R. A., and Lodish, H. F. (2001) Ski/Sno and TGF-β signaling. Cytokine Growth Factor Rev. 12, 1-8
7. Cohen, S. B., Zheng, G., Heyman, H. C., and Stavnezer, E. (1999) Heterodimers of the SnoN and Ski oncoproteins form preferentially over homodimers and are more potent transforming agents. Nucleic Acids Res. 27, 1006-1014 (Pubitemid 29209503)
8. Heyman, H. C., and Stavnezer, E. (1994) A carboxyl-terminal region of the ski oncoprotein mediates homodimerization as well as heterodimerization with the related protein SnoN. J. Biol. Chem. 269, 26996-27003 (Pubitemid 24332902)
9. Sun, Y., Liu, X., Eaton, E. N., Lane, W. S., Lodish, H. F., and Weinberg, R. A. (1999) Interaction of the Ski oncoprotein with Smad3 regulates TGF-βsignaling. Mol. Cell 4, 499-509 (Pubitemid 29531130)
10. Shinagawa, T., Dong, H. D., Xu, M., Maekawa, T., and Ishii, S. (2000) The sno gene, which encodes a component of the histone deacetylase complex, acts as a tumor suppressor in mice. EMBO J. 19, 2280-2291 (Pubitemid 30259009)
11. Lin, X., Chen, Y.-G., and Feng, X.-H. (2008) in The TGF-β Family (Derynck, R., and Miyazono, K., eds) pp. 287-332, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
12. Denissova, N. G., and Liu, F. (2004) Repression of endogenous Smad7 by Ski. J. Biol. Chem. 279, 28143-28148 (Pubitemid 38900088)
13. Briones-Orta, M. A., Sosa-Garrocho, M., Moreno-Alvarez, P., Fonseca-Sánchez, M. A., and Macías-Silva, M. (2006) SnoN co-repressor binds and represses smad7 gene promoter. Biochem. Biophys. Res. Commun. 341, 889-894 (Pubitemid 43177572)
14. Krakowski, A. R., Laboureau, J., Mauviel, A., Bissell, M. J., and Luo, K. (2005) Cytoplasmic SnoN in normal tissues and nonmalignant cells antagonizes TGF-β signaling by sequestration of the Smad proteins. Proc. Natl. Acad. Sci. U.S.A. 102, 12437-12442 (Pubitemid 41266377)
15. Sun, Y., Liu, X., Ng-Eaton, E., Lodish, H. F., and Weinberg, R. A. (1999) SnoN and Ski protooncoproteins are rapidly degraded in response to transforming growth factor β signaling. Proc. Natl. Acad. Sci. U.S.A. 96, 12442-12447 (Pubitemid 29513521)
16. Vázquez-Macías, A., Ruíz-Mendoza, A. B., Fonseca-Sánchez, M. A., Briones-Orta, M. A., and Macías-Silva, M. (2005) Downregulation of Ski and SnoN co-repressors by anisomycin. FEBS Lett. 579, 3701-3706
17. Stroschein, S. L., Bonni, S., Wrana, J. L., and Luo, K. (2001) Smad3 recruits the anaphase-promoting complex for ubiquitination and degradation of SnoN. Genes Dev. 15, 2822-2836 (Pubitemid 33042053)
18. Izzi, L., and Attisano, L. (2004) Regulation of the TGFβ signalling pathway by ubiquitin-mediated degradation. Oncogene 23, 2071-2078 (Pubitemid 38496736)
19. Wan, Y., Liu, X., and Kirschner, M. W. (2001) The anaphase-promoting complex mediates TGF-β signaling by targeting SnoN for destruction. Mol. Cell 8, 1027-1039 (Pubitemid 34031805)
20. Bonni, S., Wang, H. R., Causing, C. G., Kavsak, P., Stroschein, S. L., Luo, K., and Wrana, J. L. (2001) TGF-β induces assembly of a Smad2-Smurf2 ubiquitin ligase complex that targets SnoN for degradation. Nat. Cell Biol. 3, 587-595 (Pubitemid 32536856)
21. Levy, L., Howell, M., Das, D., Harkin, S., Episkopou, V., and Hill, C. S. (2007) Arkadia activates Smad3/Smad4-dependent transcription by triggering signal-induced SnoN degradation. Mol. Cell. Biol. 27, 6068-6083 (Pubitemid 47326695)
22. Nagano, Y., Mavrakis, K. J., Lee, K. L., Fujii, T., Koinuma, D., Sase, H., Yuki, K., Isogaya, K., Saitoh, M., Imamura, T., Episkopou, V., Miyazono, K., and Miyazawa, K. (2007) Arkadia induces degradation of SnoN and c-Ski to enhance transforming growth factor-β signaling. J. Biol. Chem. 282, 20492-20501 (Pubitemid 47100041)
23. Stroschein, S. L., Wang, W., Zhou, S., Zhou, Q., and Luo, K. (1999) Negative feedback regulation of TGF-β signaling by the SnoN oncoprotein. Science 286, 771-774
24. Pearson-White, S., and McDuffie, M. (2003) Defective T-cell activation is associated with augmented transforming growth factor β sensitivity in mice with mutations in the Sno gene. Mol. Cell. Biol. 23, 5446-5459 (Pubitemid 36950898)
25. Zhu, Q., Pearson-White, S., and Luo, K. (2005) Requirement for the SnoN oncoprotein in transforming growth factor β-induced oncogenic transformation of fibroblast cells. Mol. Cell. Biol. 25, 10731-10744 (Pubitemid 41747119)
26. Zhu, Q., Krakowski, A. R., Dunham, E. E., Wang, L., Bandyopadhyay, A., Berdeaux, R., Martin, G. S., Sun, L., and Luo, K. (2007) Dual role of SnoN in mammalian tumorigenesis. Mol. Cell. Biol. 27, 324-339 (Pubitemid 46013254)
27. Edmiston, J. S., Yeudall, W. A., Chung, T. D., and Lebman, D. A. (2005) Inability of transforming growth factor-β to cause SnoN degradation leads to resistance to transforming growth factor-β-induced growth arrest in esophageal cancer cells. Cancer Res. 65, 4782-4788 (Pubitemid 40740816)
28. Macias-Silva, M., Li, W., Leu, J. I., Crissey, M. A., and Taub, R. (2002) Up-regulated transcriptional repressors SnoN and Ski bind Smad proteins to antagonize transforming growth factor-β signals during liver regeneration. J. Biol. Chem. 277, 28483-28490 (Pubitemid 41079273)
29. Tan, R., Zhang, J., Tan, X., Zhang, X., Yang, J., and Liu, Y. (2006) Down-regulation of SnoN expression in obstructive nephropathy is mediated by an enhanced ubiquitin-dependent degradation. J. Am. Soc. Nephrol. 17, 2781-2791 (Pubitemid 44484668)
30. Yang, J., Zhang, X., Li, Y., and Liu, Y. (2003) Downregulation of Smad transcriptional corepressors SnoN and Ski in the fibrotic kidney: an amplification mechanism for TGF-β1 signaling. J. Am. Soc. Nephrol. 14, 3167-3177 (Pubitemid 38312571)
31. Padua, D., Zhang, X. H., Wang, Q., Nadal, C., Gerald, W. L., Gomis, R. R., and Massagué, J. (2008) TGFβ primes breast tumors for lung metastasis seeding through angiopoietin-like 4. Cell 133, 66-77 (Pubitemid 351442989)
32. Furlan-Magaril, M., Rincón-Arano, H., and Recillas-Targa, F. (2009) in Methods in Molecular Biology: DNA-Protein Interactions (Moss, T., and Leblanc, B., eds) Vol. 543, pp. 253-266, Humana Press, Totowa, NJ
33. Izzi, L., Silvestri, C., von Both, I., Labbé, E., Zakin, L., Wrana, J. L., and Attisano, L. (2007) Foxh1 recruits Gsc to negatively regulate Mixl1 expression during early mouse development. EMBO J. 26, 3132-3143 (Pubitemid 47057493)
34. Nomura, N., Sasamoto, S., Ishii, S., Date, T., Matsui, M., and Ishizaki, R. (1989) Isolation of human cDNA clones of ski and the ski-related gene, sno. Nucleic Acids Res. 17, 5489-5500 (Pubitemid 19187099)
35. Pearson-White, S., and Crittenden, R. (1997) Proto-oncogene Sno expression, alternative isoforms and immediate early serum response. Nucleic Acids Res. 25, 2930-2937 (Pubitemid 27299813)
36. Nomura, T., Khan, M. M., Kaul, S. C., Dong, H. D., Wadhwa, R., Colmenares, C., Kohno, I., and Ishii, S. (1999) Ski is a component of the histone deacetylase complex required for transcriptional repression by Mad and thyroid hormone receptor. Genes Dev. 13, 412-423 (Pubitemid 29108757)
37. Kokura, K., Kaul, S. C., Wadhwa, R., Nomura, T., Khan, M. M., Shinagawa, T., Yasukawa, T., Colmenares, C., and Ishii S. (2001) The Ski protein family is required for MeCP2-mediated transcriptional repression. J. Biol. Chem. 276, 34115-34121
38. Nagase, T., Nomura, N., and Ishii, S. (1993) Complex formation between proteins encoded by the ski gene family. J. Biol. Chem. 268, 13710-13716 (Pubitemid 23307805)
39. Wilkinson, D. S., Ogden, S. K., Stratton, S. A., Piechan, J. L., Nguyen, T. T., Smulian, G. A., and Barton, M. C. (2005) A direct intersection between p53 and transforming growth factor β pathways targets chromatin modification and transcription repression of the α-fetoprotein gene. Mol. Cell. Biol. 25, 1200-1212 (Pubitemid 40165825)
40. Macías-Silva, M., Vázquez-Victorio, G., and Hernández-Damián, J. (2010) Anisomycin is a multifunctional drug: More than just a protein synthesis inhibitor. Curr. Chem. Biol. 4, 124-132
41. He, J., Tegen, S. B., Krawitz, A. R., Martin, G. S., and Luo, K. (2003) The transforming activity of Ski and SnoN is dependent on their ability to repress the activity of Smad proteins. J. Biol. Chem. 278, 30540-30547 (Pubitemid 36994558)
42. Wu, J. W., Krawitz, A. R., Chai, J., Li, W., Zhang, F., Luo, K., and Shi, Y. (2002) Structural mechanism of Smad4 recognition by the nuclear oncoprotein Ski: insights on Ski-mediated repression of TGF-β signaling. Cell 111, 357-367 (Pubitemid 35341390)
43. Levy, L., and Hill, C. S. (2005) Smad4 dependency defines two classes of transforming growth factor β (TGF-β) target genes and distinguishes TGF-β-induced epithelial-mesenchymal transition from its antiproliferative and migratory responses. Mol. Cell. Biol. 25, 8108-8125 (Pubitemid 41263004)
44. Koinuma, D., Tsutsumi, S., Kamimura, N., Imamura, T., Aburatani, H., and Miyazono, K. (2009) Promoter-wide analysis of Smad4 binding sites in human epithelial cells. Cancer Sci. 100, 2133-2142
45. Imoto, I., Pimkhaokham, A., Fukuda, Y., Yang, Z. Q., Shimada, Y., Nomura, N., Hirai, H., Imamura, M., and Inazawa, J. (2001)SNOis a probable target for gene amplification at 3q26 in squamous-cell carcinomas of the esophagus. Biochem. Biophys. Res. Commun. 286, 559-565 (Pubitemid 32912983)
46. Tan, R., Zhang, X., Yang, J., Li, Y., and Liu, Y. (2007) Molecular basis for the cell type specific induction of SnoN expression by hepatocyte growth factor. J. Am. Soc. Nephrol. 18, 2340-2349 (Pubitemid 47203850)
47. Xi, Q., He, W., Zhang, X. H., Le, H. V., and Massagué, J. (2008) Genome-wide impact of the BRG1 SWI/SNF chromatin remodeler on the transforming growth factor β transcriptional program. J. Biol. Chem. 283, 1146-1155
48. Benchabane, H., and Wrana, J. L. (2003) GATA- and Smad1-dependent enhancers in the Smad7 gene differentially interpret bone morphogenetic protein concentrations. Mol. Cell. Biol. 23, 6646-6661 (Pubitemid 37075774)
49. Briones-Orta, M. A., Tecalco-Cruz, A. C., Sosa-Garrocho, M., Caligaris, C., and Macías-Silva, M. (2011) Inhibitory Smad7: emerging roles in health and disease. Curr. Mol. Pharmacol. 4, 141-153
50. Kalari, K. R., Casavant, M., Bair, T. B., Keen, H. L., Comeron, J. M., Casavant, T. L., and Scheetz, T. E. (2006) First exons and introns-a survey of GC content and gene structure in the human genome. In Silico Biol. 6, 237-242 (Pubitemid 44508933)
51. Sandelin, A., Carninci, P., Lenhard, B., Ponjavic, J., Hayashizaki, Y., and Hume, D. A. (2007) Mammalian RNA polymerase II core promoters: insights from genome-wide studies. Nat. Rev. Genet. 8, 424-436 (Pubitemid 46789243)
52. Tabata, T., Kokura, K., Ten, Dijke P., and Ishii, S. (2009) Ski co-repressor complexes maintain the basal repressed state of the TGF-beta target gene, SMAD7, via HDAC3 and PRMT5. Genes Cells 14, 17-28
53. Ikushima, H., and Miyazono, K. (2010) Cellular context-dependent "colors"of transforming growth factor-β signaling. Cancer Sci. 101, 306-312
54. Ijichi, H., Otsuka, M., Tateishi, K., Ikenoue, T., Kawakami, T., Kanai, F., Arakawa, Y., Seki, N., Shimizu, K., Miyazono, K., Kawabe, T., and Omata, M. (2004) Smad4-independent regulation of p21/WAF1 by transforming growth factor-β. Oncogene 23, 1043-1051 (Pubitemid 38269958)
55. Zhao, S., Ammanamanchi, S., Brattain, M., Cao, L., Thangasamy, A., Wang, J., and Freeman, J. W. (2008) Smad4-dependent TGF-β signaling suppresses RON receptor tyrosine kinase-dependent motility and invasion of pancreatic cancer cells. J. Biol. Chem. 283, 11293-11301
56. Müller, N., Reinacher-Schick, A., Baldus, S., van Hengel, J., Berx, G., Baar, A., van Roy, F., Schmiegel, W., and Schwarte-Waldhoff, I. (2002) Smad4 induces the tumor suppressor E-cadherin and P-cadherin in colon carcinoma cells. Oncogene 21, 6049-6058
57. Hesling, C., Fattet, L., Teyre, G., Jury, D., Gonzalo, P., Lopez, J., Vanbelle, C., Morel, A. P., Gillet, G., Mikaelian, I., and Rimokh, R. (2011) Antagonistic regulation of EMT by TIF1γ and Smad4 in mammary epithelial cells. EMBO Rep. 12, 665-672
58. Yang, G., and Yang, X. (2010) Smad4-mediated TGF-β signaling in tumorigenesis. Int. J. Biol. Sci. 6, 1-8