VHL promotes E2 box-dependent E-cadherin transcription by HIF-mediated regulation of SIP1 and snail

Molecular and Cellular Biology

Volumn 27, Issue 1, 2007, Pages 157-169

  Evans, Andrew J ^a,b   Russell, Ryan C ^a   Roche, Olga ^a   Burry, T Nadine ^a   Fish, Jason E ^a   Chow, Vinca W K ^a   Kim, William Y ^c   Saravanan, Arthy ^b   Maynard, Mindy A ^a   Gervais, Michelle L ^a   Sufan, Roxana I ^a   Roberts, Andrew M ^a   Wilson, Leigh A ^a   Betten, Mark ^d   Vandewalle, Cindy ^e   Berx, Geert ^e   Marsden, Philip A ^a,f   Irwin, Meredith S ^a,g   Teh, Bin T ^d   Jewett, Michael A S ^b   Ohh, Michael ^a   more..

^a UNIVERSITY OF TORONTO   (Canada)

^b PRINCESS MARGARET HOSPITAL   (Canada)

^c UNIVERSITY OF NORTH CAROLINA   (United States)

^d VAN ANDEL RESEARCH INSTITUTE   (United States)

^e GHENT UNIVERSITY   (Belgium)

^f ST MICHAEL'S HOSPITAL   (Canada)

^g HOSPITAL FOR SICK CHILDREN   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CELL ADHESION MOLECULE; GENE PRODUCT; HYPOXIA INDUCIBLE FACTOR; MUTANT PROTEIN; OXYGEN; RNA POLYMERASE II; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SIP1; TRANSCRIPTION FACTOR SNAIL; TUMOR SUPPRESSOR PROTEIN; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; UVOMORULIN; VON HIPPEL LINDAU PROTEIN;

ALPHA CHAIN; ARTICLE; CELL JUNCTION; CLEAR CELL CARCINOMA; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVE SITE; ENZYME SUBSTRATE; EPITHELIUM CELL; GENE EXPRESSION REGULATION; GENE LOSS; GENE OVEREXPRESSION; GENE REPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN TISSUE; HYPOXIA; KIDNEY CARCINOMA; KIDNEY EPITHELIUM; KNOCKOUT GENE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; RNA INTERFERENCE; TRANSCRIPTION REGULATION; UBIQUITINATION; UPREGULATION;

CADHERINS; CELL LINE, TUMOR; EPITHELIAL CELLS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; KIDNEY; NERVE TISSUE PROTEINS; PROMOTER REGIONS (GENETICS); RNA INTERFERENCE; RNA POLYMERASE II; RNA, SMALL INTERFERING; RNA-BINDING PROTEINS; SUBCELLULAR FRACTIONS; TRANSCRIPTION FACTORS; VON HIPPEL-LINDAU TUMOR SUPPRESSOR PROTEIN;

GASTROPODA; PYRONIA TITHONUS;

EID: 33845724527     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00892-06     Document Type: Article

References (68)

1. Affymetrix. 2003. GeneChip expression analysis technical manual. Affymetrix, Santa Clara, CA.
2. Ananth, S., B. Knebelmann, W. Gruning, M. Dhanabal, G. Walz, I. Stillman, and V. Sukhatme. 1999. Transforming growth factor beta1 is a target for the von Hippel-Lindau tumor suppressor and a critical growth factor for clear cell renal carcinoma. Cancer Res. 59:2210-2216.
3. Baba, M., S. Hirai, S. Kawakami, T. Kishida, N. Sakai, S. Kaneko, M. Yao, T. Shuin, Y. Kubota, M. Hosaka, and S. Ohno. 2001. Tumor suppressor protein VHL is induced at high cell density and mediates contact inhibition of cell growth. Oncogene 20:2727-2736.
4. Baba, M., S. Hirai, H. Yamada-Okabe, K. Hamada, H. Tahuchi, K. Kobayashi, K. Kondo, M. Yoshida, A. Yamashita, T. Kishida, N. Nakaigawa, Y. Nagashima, Y. Kubota, M. Yao, and S. Ohno. 2003. Loss of von Hippel-Lindau protein causes cell density dependent deregulation of CyclinD1 expression through hypoxia-inducible factor. Oncogene 22:2728-2738.
5. Batlle, E., E. Sancho, C. Franci, D. Dominguez, M. Monfar, J. Baulida, and A. Garcia De Herreros. 2000. The transcription factor snail is a repressor of E-cadherin gene expression in epithelial tumour cells. Nat. Cell Biol. 2:84-89.
6. Behrens, J., O. Lowrick, L. Klein-Hitpass, and W. Birchmeier. 1991. The E-cadherin promoter: functional analysis of a GC-rich region and an epithelial cell-specific palindromic regulatory element. Proc. Natl. Acad. Sci. USA 88:11495-11499.
7. Berx, G., A. M. Cleton-Jansen, F. Nollet, W. J. de Leeuw, M. van de Vijver, C. Cornelisse, and F. van Roy. 1995. E-cadherin is a tumour/invasion suppressor gene mutated in human lobular breast cancers. EMBO J. 14:6107-6115.
8. Berx, G., A. M. Cleton-Jansen, K. Strumane, W. J. de Leeuw, F. Nollet, F. van Roy, and C. Cornelisse. 1996. E-cadherin is inactivated in a majority of invasive human lobular breast cancers by truncation mutations throughout its extracellular domain. Oncogene 13:1919-1925.
9. Brugarolas, J. B., F. Vazquez, A. Reddy, W. R. Sellers, and W. G. Kaelin, Jr. 2003. TSC2 regulates VEGF through mTOR-dependent and -independent pathways. Cancer Cell 4:147-158.
10. Cano, A., M. A. Perez-Moreno, I. Rodrigo, A. Locascio, M. J. Blanco, M. G. del Barrio, F. Portillo, and M. A. Nieto. 2000. The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat. Cell Biol. 2:76-83.
11. Clifford, S. C., M. E. Cockman, A. C. Smallwood, D. R. Mole, E. R. Woodward, P. H. Maxwell, P. J. Ratcliffe, and E. R. Maher. 2001. Contrasting effects on HIF-1α regulation by disease-causing pVHL mutations correlate with patterns of tumourigenesis in von Hippel-Lindau disease. Hum. Mol. Genet. 10:1029-1038.
12. Cohen, H. T., and F. J. McGovern. 2005. Renal-cell carcinoma. N. Engl. J. Med. 353:2477-2490.
13. 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.
14. Davidowitz, E. J., A. R. Schoenfeld, and R. D. Burk. 2001. VHL induces renal cell differentiation and growth arrest through integration of cell-cell and cell-extracellular matrix signaling. Mol. Cell. Biol. 21:865-874.
15. Eble, J. N., G. Sauter, J. I. Epstein, and I. A. Sesterhenn. 2004. World Health Organization classification of tumors: pathology and genetics of tumors of the urinary system and male genital organs. IRAC Press, Lyon, France.
16. Esteban, M. A., M. G. B. Tran, S. K. Harten, P. Hill, M. C. Castellanos, A. Chandra, R. Raval, T. S. O'Brien, and P. H. Maxwell. 2006. Regulation of E-cadherin expression by VHL and hypoxia-inducible factor. Cancer Res. 66:3567-3575.
17. Fish, J. E., C. C. Matouk, A. Rachlis, S. Lin, S. C. Tai, C. D'Abreo, and P. A. Marsden. 2005. The expression of endothelial nitric-oxide synthase is controlled by a cell-specific histone code. J. Biol. Chem. 280:24824-24838.
18. Furge, K. A., K. A. Lucas, M. Takahashi, J. Sugimura, E. J. Kort, H. O. Kanayama, S. Kagawa, P. Hoekstra, J. Curry, X. J. Yang, and B. T. Teh. 2004. Robust classification of renal cell carcinoma based on gene expression data and predicted cytogenetic profiles. Cancer Res. 64:4117-4121.
19. Graff, J. R., J. G. Herman, R. G. Lapidus, H. Chopra, R. Xu, D. F. Jarrard, W. B. Isaacs, P. M. Pitha, N. E. Davidson, and S. B. Baylin. 1995. E-cadherin expression is silenced by DNA hypermethylation in human breast and prostate carcinomas. Cancer Res. 55:5195-5199.
20. Groulx, I., and S. Lee. 2002. Oxygen-dependent ubiquitination and degradation of hypoxia-inducible factor requires nuclear-cytoplasmic trafficking of the von Hippel-Lindau tumor suppressor protein. Mol. Cell. Biol. 22:5319-5336.
21. Hoffman, M. A., M. Ohh, H. Yang, J. M. Klco, M. Ivan, and W. G. Kaelin, Jr. 2001. von Hippel-Lindau protein mutants linked to type 2C VHL disease preserve the ability to downregulate HIF. Hum. Mol. Genet. 10:1019-1027.
22. Hynes, R. 1992. Integrins: versatility, modulation, and signalling in cell adhesion. Cell 69:11-25.
23. Imai, T., A. Horiuchi, C. Wang, K. Oka, S. Ohira, T. Nikaido, and I. Konishi. 2003. Hypoxia attenuates the expression of E-cadherin via up-regulation of SNAIL in ovarian carcinoma cells. Am. J. Pathol. 163:1437-1447.
24. Ivan, M., K. Kondo, H. Yang, W. Kim, J. Valiando, M. Ohh, A. Salic, J. M. Asara, W. S. Lane, and W. G. Kaelin, Jr. 2001. HIFα targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing. Science 292:464-468.
25. Ivanov, S., I. Kuzmin, M.-H. Wei, S. Pack, L. Geil, B. Johnson, E. Stanbridge, and M. Lerman. 1998. Down-regulation of transmembrane carbonic anhydrases in renal cell carcinoma cell lines by wild-type von Hippel-Lindau transgenes. Proc. Natl. Acad. Sci. USA 95:12596-12601.
26. Jaakkola, P., D. R. Mole, Y. M. Tian, M. I. Wilson, J. Gielbert, S. J. Gaskell, A. Kriegsheim, H. F. Hebestreit, M. Mukherji, C. J. Schofield, P. H. Maxwell, C. W. Pugh, and P. J. Ratcliffe. 2001. Targeting of HIF-α to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science 292:468-472.
27. Jamora, C., P. Lee, P. Kocieniewski, M. Azhar, R. Hosokawa, Y. Chai, and E. Fuchs. 2005. A signaling pathway involving TGF-beta2 and snail in hair follicle morphogenesis. PLOS Biol. 3:e11.
28. Ji, X., A. S. Woodard, D. L. Rimm, and E. R. Fearon. 1997. Transcriptional defects underlie loss of E-cadherin expression in breast cancer. Cell Growth Differ. 8:773-778.
29. Kaelin, W. G., Jr. 2002. Molecular basis of the VHL hereditary cancer syndrome. Nat. Rev. Cancer 2:673-682.
30. Kibel, A., O. Iliopoulos, J. D. DeCaprio, and W. G. Kaelin. 1995. Binding of the von Hippel-Lindau tumor suppressor protein to elongin B and C. Science 269:1444-1446.
31. Kondo, K., W. Y. Kim, M. Lechpammer, and W. G. Kaelin, Jr. 2003. Inhibition of HIF2alpha is sufficient to suppress pVHL-defective tumor growth. PLOS Biol. 1:e83.
32. Kondo, K., J. Klco, E. Nakamura, M. Lechpammer, and W. G. Kaelin, Jr. 2002. Inhibition of HIF is necessary for tumor suppression by the von Hippel-Lindau protein. Cancer Cell 1:237-246.
33. Koochekpour, S., M. Jeffers, P. Wang, C. Gong, G. Taylor, L. Roessler, R. Stearman, J. Vasselli, W. Stetler-Stevenson, W. J. Kaelin, W. Linehan, R. Klausner, J. Gnarra, and G. Vande Woude. 1999. The von Hippel-Lindau tumor suppressor gene inhibits hepatocyte growth factor/scatter factor-induced invasion and branching morphogenesis in renal carcinoma cells. Mol. Cell. Biol. 19:5902-5912.
34. Krishnamachary, B., D. Zagzag, H. Nagasawa, K. Rainey, H. Okuyama, J. H. Baek, and G. L. Semenza. 2006. Hypoxia-inducible factor-1-dependent repression of E-cadherin in von Hippel-Lindau tumor suppressor-null renal cell carcinoma mediated by TCF3, ZFHX1A, and ZFHX1B. Cancer Res. 66:2725-2731.
35. Kurban, G., V. Hudon, E. Duplan, M. Ohh, and A. Pause. 2006. Characterization of a von Hippel Lindau pathway involved in extracellular matrix remodeling, cell invasion, and angiogenesis. Cancer Res. 66:1313-1319.
36. Laughner, E., P. Taghavi, K. Chiles, P. C. Mahon, and G. L. Semenza. 2001. HER2 (neu) signaling increases the rate of hypoxia-inducible factor 1alpha (HIF-1α) synthesis: novel mechanism for HIF-1-mediated vascular endothelial growth factor expression. Mol. Cell. Biol. 21:3995-4004.
37. Lee, S., D. Y. T. Chen, J. S. Humphrey, J. R. Gnarra, W. M. Linehan, and R. D. Klausner. 1996. Nuclear/cytoplasmic localization of the von Hippel-Lindau tumor suppressor gene product is determined by cell density. Proc. Natl. Acad. Sci. USA 93:1770-1775.
38. Lieubeau-Teillet, B., J. Rak, S. Jothy, O. Iliopoulos, W. Kaelin, and R. Kerbel. 1998. von Hippel-Lindau gene-mediated growth suppression and induction of differentiation in renal cell carcinoma cells grown as multicellular tumor spheroids. Cancer Res. 58:4957-4962.
39. Lonergan, K. M., O. Iliopoulos, M. Ohh, T. Kamura, R. C. Conaway, J. W. Conaway, and W. G. Kaelin. 1998. Regulation of hypoxia-inducible mRNAs by the von Hippel-Lindau protein requires binding to complexes containing elongins B/C and Cul2. Mol. Cell. Biol. 18:732-741.
40. Luecke, H. F., and K. R. Yamamoto. 2005. The glucocorticoid receptor blocks P-TEFb recruitment by NF-κB to effect promoter-specific transcriptional repression. Genes Dev. 19:1116-1127.
41. Maranchie, J. K., J. R. Vasselli, J. Riss, J. S. Bonifacino, W. M. Linehan, and R. D. Klausner. 2002. The contribution of VHL substrate binding and HIF1-α to the phenotype of VHL loss in renal cell carcinoma. Cancer Cell 1:247-255.
42. Martinez-Zaguilan, R., E. A. Seftor, R. E. Seftor, Y. W. Chu, R. J. Gillies, and M. J. Hendrix. 1996. Acidic pH enhances the invasive behavior of human melanoma cells. Clin. Exp. Metastasis 14:176-186.
43. Maxwell, P., M. Weisner, G.-W. Chang, S. Clifford, E. Vaux, C. Pugh, E. Maher, and P. Ratcliffe. 1999. The von Hippel-Lindau gene product is necessary for oxygen-dependent proteolysis of hypoxia-inducible factor α subunits. Nature 399:271-275.
44. Mohan, S., and R. D. Burk. 2003. von Hippel-Lindau protein complex is regulated by cell density. Oncogene 22:5270-5280.
45. Morell-Quadreny, L., J. Rubio, J. A. Lopez-Guerrero, J. Casanova, D. Ramos, I. Iborra, E. Solsona, and A. Llombart-Bosch. 2003. Disruption of basement membrane, extracellular matrix metalloproteinases and E-cadherin in renal-cell carcinoma. Anticancer Res. 23:5005-5010.
46. Nelson, W. J., and R. Nusse. 2004. Convergence of Wnt, beta-catenin, and cadherin pathways. Science 303:1483-1487.
47. Nishi, H., T. Nakada, M. Hokamura, Y. Osakabe, O. Itokazu, L. E. Huang, and K. Isaka. 2004. Hypoxia-inducible factor-1 transactivates transforming growth factor-β3 in trophoblast. Endocrinology 145:4113-4118.
48. Ohh, M., and W. G. Kaelin, Jr. 2003. VHL and kidney cancer. Methods Mol. Biol. 222:167-183.
49. Ohh, M., C. W. Park, M. Ivan, M. A. Hoffman, T.-Y. Kim, L. E. Huang, V. Chau, and W. G. Kaelin. 2000. Ubiquitination of HIF requires direct binding to the von Hippel-Lindau protein beta domain. Nat. Cell Biol. 2:423-427.
50. Ohh, M., R. L. Yauch, K. M. Lonergan, J. M. Whaley, A. O. Stemmer-Rachamimov, D. N. Louis, B. J. Gavin, N. Kley, W. G. Kaelin, O. Iliopoulos, and W. G. Kaelin. 1998. The von Hippel-Lindau tumor suppressor protein is required for proper assembly of an extracellular fibronectin matrix. Mol. Cell 1:959-968.
51. Pasqualini, R., S. Bourdoulous, E. Koivunen, V. Woods, Jr., and E. Ruoslahti. 1996. A polymeric form of fibronectin has antimetastatic effects against multiple tumor types. Nat. Med. 2:1197-1203.
52. 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.
53. Rankin, E. B., D. F. Higgins, J. A. Walisser, R. S. Johnson, C. A. Bradfield, and V. H. Haase. 2005. Inactivation of the arylhydrocarbon receptor nuclear translocator (Arnt) suppresses von Hippel-Lindau disease-associated vascular tumors in mice. Mol. Cell. Biol. 25:3163-3172.
54. Rankin, E. B., J. E. Tomaszewski, and V. H. Haase. 2006. Renal cyst development in mice with conditional inactivation of the von Hippel-Lindau tumor suppressor. Cancer Res. 66:2576-2583.
55. Ravi, R., B. Mookerjee, Z. M. Bhujwalla, C. H. Sutter, D. Artemov, Q. Zeng, L. E. Dillehay, A. Madan, G. L. Semenza, and A. Bedi. 2000. Regulation of tumor angiogenesis by p53-induced degradation of hypoxia-inducible factor 1α. Genes Dev. 14:34-44.
56. Ruoslahti, E. 1992. Control of the cell motility and tumour invasion by extracellular matrix interactions. Br. J. Cancer 66:239-242.
57. Scheid, A., R. H. Wenger, L. Schaffer, I. Camenisch, O. Distler, A. Ferenc, H. Cristina, H. E. Ryan, R. S. Johnson, K. F. Wagner, U. G. Stauffer, C. Bauer, M. Gassmann, and M. Meuli. 2002. Physiologically low oxygen concentrations in fetal skin regulate hypoxia-inducible factor 1 and transforming growth factor-β3. FASEB J. 16:411-413.
58. Shimazui, T., L. A. Giroldi, P. P. Bringuier, E. Oosterwjjk, and J. A. Schalken. 1996. Complex cadherin expression in renal cell carcinoma. Cancer Res. 56:3234-3237.
59. Sly, W. S., and P. Y. Hu. 1995. Human carbonic anhydrases and carbonic anhydrase deficiencies. Annu. Rev. Biochem. 64:375-401.
60. Spagnoli, F. M., C. Cicchini, M. Tripodi, and M. C. Weiss. 2000. Inhibition of MMH (Met murine hepatocyte) cell differentiation by TGF(beta) is abrogated by pre-treatment with the heritable differentiation effector FGF1. J. Cell Sci. 113:3639-3647.
61. Staller, P., J. Sulitkova, J. Lisztwan, H. Moch, E. J. Oakeley, and W. Krek. 2003. Chemokine receptor CXCR4 downregulated by von Hippel-Lindau tumour suppressor pVHL. Nature 425:307-311.
62. Stickle, N. H., J. Chung, J. M. Klco, R. P. Hill, W. G. Kaelin, Jr., and M. Ohh. 2004. pVHL modification by NEDD8 is required for fibronectin matrix assembly and suppression of tumor development. Mol. Cell. Biol. 24:3251-3261.
63. Takahashi, M., D. R. Rhodes, K. A. Purge, H. Kanayama, S. Kagawa, B. B. Haab, and B. T. Teh. 2001. Gene expression profiling of clear cell renal cell carcinoma: gene identification and prognostic classification. Proc. Natl. Acad. Sci. USA 98:9754-9759.
64. Vandewalle, C., J. Comijn, B. De Craene, P. Vermassen, E. Bruyneel, H. Andersen, E. Tulchinsky, F. Van Roy, and G. Berx. 2005. S1P1/ZEB2 induces EMT by repressing genes of different epithelial cell-cell junctions. Nucleic Acids Res. 33:6566-6578.
65. Yoshiura, K., Y. Kanai, A. Ochiai, Y. Shimoyama, T. Sugimura, and S. Hirohashi. 1995. Silencing of the E-cadherin invasion-suppressor gene by CpG methylation in human carcinomas. Proc. Natl. Acad. Sci. USA 92:7416-7419.
66. Zagzag, D., B. Krishnamachary, H. Yee, H. Okuyama, L. Chiriboga, M. A. Ali, J. Melamed, and G. L. Semenza. 2005. Stromal cell-derived factor-1alpha and CXCR4 expression in hemangioblastoma and clear cell-renal cell carcinoma: von Hippel-Lindau loss-of-function induces expression of a ligand and its receptor. Cancer Res. 65:6178-6188.
67. Zhang, H., H. O. Akman, E. L. Smith, J. Zhao, J. E. Murphy-Ullrich, and O. A. Batuman. 2003. Cellular response to hypoxia involves signaling via Smad proteins. Blood 101:2253-2260.
68. Zundel, W., C. Schindler, D. Haas-Kogan, A. Koong, F. Kaper, E. Chen, A. Gottschalk, H. Ryan, R. Johnson, A. Jefferson, D. Stokoe, and A. Giaccia. 2000. Loss of PTEN facilitates HIF-1-mediated gene expression. Genes Dev. 14:391-396.