The von Hippel-Lindau tumor suppressor gene product interacts with Sp1 to repress vascular endothelial growth factor promoter activity

Molecular and Cellular Biology

Volumn 17, Issue 9, 1997, Pages 5629-5639

  Mukhopadhyay, Debabrata ^a,b   Knebelmann, Bertrand ^a   Cohen, Herbert T ^a   Ananth, Subbian ^a   Sukhatme, Vikas P ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENE PRODUCT; TRANSCRIPTION FACTOR SP1; VASCULOTROPIN;

ARTICLE; CHROMOSOME 3P; CLEAR CELL CARCINOMA; CONTROLLED STUDY; DROSOPHILA; GENE MUTATION; HUMAN; HUMAN CELL; KIDNEY CARCINOMA; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; TUMOR SUPPRESSOR GENE; VON HIPPEL LINDAU DISEASE;

EID: 0030834249     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.17.9.5629     Document Type: Article

References (76)

1. Ackerman, S. L., A. G. Minden, G. T. Williams, C. Bobonis, and C.-Y. Yeung. 1991. Functional significance of an overlapping consensus binding motif for Sp1 and Zif268 in the murine adenosine deaminase gene promoter. Proc. Natl. Acad. Sci. USA 88:7523-7527.
2. Alemany, J., T. Borras, and F. De Pablo. 1990. Transcriptional stimulation of the 51-crystallin gene by insulin-like growth factor I and insulin requires DNA cis elements in chicken. Proc. Natl. Acad. Sci. USA 87:3353-3357.
3. Aso, T., W. S. Lane, J. W. Conaway, and R. C. Conaway. 1995. Elongin (SIII): a multisuhunit regulator of elongation by RNA polymerase II. Science 269: 1439-1443.
4. Borellini, F., and R. I. Glazer. 1993. Induction of Sp1-p53 DNA-binding heterocomplexes during granulocyte/macrophage colony-stimulating factor-dependent proliferation in human crythroleukemia cell line TF-1. J. Biol. Chem. 268:7923-7928.
5. Borellini, F., Y. F. He, A. Aquino, G. Yu, S. F. Joseph, and R. I. Glazer. 1991. Increased DNA binding and transcriptional activity associated with transcription factor Sp1 in K562 cells transfected with the myeloid-specific c-fes tyrosine kinase gene. J. Biol. Chem. 266:15850-15854.
6. Brown, L. F., B. Berse, R. W. Jackman, K. Tognazzi, E. J. Manseau, H. F. Dvorak, and D. R. Senger. 1993. Increased expression of vascular permeability factor (vascular endothelial growth factor) and its receptors in kidney and bladder carcinomas. Am. J. Pathol. 143:1255-1262.
7. Cao, X., R. Mahendran, G. R. Guy, and Y. H. Tan. 1993. Detection and characterization of cellular EGR-1 binding to its recognition site. J. Biol. Chem. 268:16949-16957.
8. Chen, F., T. Kishida, and M. Yao, et al. 1995. Germline mutations in the von Hippel-Lindau disease tumor suppressor gene: correlations with phenotype. Hum. Mutat. 5:66-75.
9. Chen, L. I., T. Nishinaka, K. Kwan, I. Kitabayashi, K. Yokoyama, Y.-H. F. Fu, S. Grunwald, and R. Chiu. 1994. The retinoblastoma gene product RB stimulates Sp1-mediated transcription by liberating Sp1 from a negative regulator. Mol. Cell. Biol. 14:4380-4389.
10. Chomczynski, P., and N. Sacchi. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162:156-159.
11. Cohen, H. T., S. A. Bossone, G. Zhu, G. A. McDonald, and V. P. Sukhatme. 1997. Sp1 is a critical regulator of the Wilms' tumor-1 gene. J. Biol. Chem. 272:2901-2913.
12. 11a. Cohen, H. T., and V. P. Sukhatme. Unpublished data.
13. Courey, A. J., and R. Tjian. 1988. Analysis of Sp1 in vivo reveals multiple transcriptional domains, including a novel glutamine-rich activation motif. Cell 55:887-898.
14. Crossey, P. A., F. M. Richards, K. Foster, J. S. Green, A. Prowse, F. Latif, M. I. Lerman, B. Zbar, N. A. Affara, M. A. Ferguson-Smith, and E. R. Maher. 1994. Identification of intragenic mutations in the von Hippel-Lindau disease tumour suppressor gene and correlation with disease phenotype. Hum. Mol. Genet. 3:1303-1308.
15. Datta, P. K., P. Raychaudhuri, and S. Bagchi. 1995. Association of p107 with Sp1: genetically separable regions of p107 are involved in regulation of E2F- and Sp1-dependent transcription. Mol. Cell. Biol. 15:5444-5452.
16. Dawson, P. A., S. L. Hofmann, D. R. van der Westhuyzen, T. C. Sudhof, M. S. Brown, and J. L. Goldstein. 1988. Sterol-dependent repression of low density lipoprotein receptor promoter mediated by 16-base pair sequence adjacent to binding site for transcription factor Sp1. J. Biol. Chem. 263:3372-3379.
17. Dignam, J. D., R. M. Lebovitz, and R. G. Roeder. 1983. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11:1475.
18. Duan, D. R., J. S. Humphrey, D. Y. T. Chen, Y. Weng, J. Sukegawa, S. Lee, J. R. Gnarra, W. M. Linehan, and R. D. Klausner. 1995. Characterization of the VHL tumor suppressor gene product: localization, complex formation, and the effect of natural inactivating mutations. Proc. Natl. Acad. Sci. USA 92:6459-6463.
19. Duan, D. R., A. Pause, W. H. Burgess, T. Aso, D. Y. T. Chen, K. P. Garrett, R. C. Conaway, J. W. Conaway, W. M. Linehan, and R. D. Klausner. 1995. Inhibition of transcription elongation by the VHL tumor suppressor protein. Science 269:1402-1406.
20. Feng, Y., L. E. Gunter, E. L. Organ, and D. R. Cavener. 1991. Translation initiation in Drosophila melanogaster is reduced by mutations upstream of the AUG initiator codon. Mol. Cell. Biol. 11:2149-2153.
21. Foster, K., A. Prowse, A. van den Berg, S. Fleming, M. M. F. Hulsbeek, P. A. Crossey, F. M. Richards. P. Cairns, N. A. Affara, M. A. Ferguson-Smith, C. H. C. M. Buys, and E. R. Maher. 1994. Somatic mutations of the von Hippel-Lindau disease tumour suppressor gene in non-familial clear cell renal carcinoma. Hum. Mol. Genet. 3:2169-2173.
22. Gnarra, J. R., K. Tory, Y. Weng, et al. 1994. Mutations of the VHL tumour suppressor gene in renal carcinoma. Nat. Genet. 7:85-90.
23. Gnarra, J. R., S. Zhou, M. J. Merrill, J. R. Wagner, A. Krumm, E. Papavassiliou, E. H. Oldfield, R. D. Klausner, and W. M. Linehan. 1996. Posttranscriptional regulation of vascular endothelial growth factor mRNA by the product of the VHL tumor suppressor gene. Proc. Natl. Acad. Sci. USA 93:10589-10594.
24. Gorman, C. M., L. F. Moffat, and B. H. Howard. 1982. Recombinant genomes which express chloramphenicol acetyltransferase in mammalian cells. Mol. Cell. Biol. 2:1044-1051.
25. Greenberg, M. E. 1988. Identification of newly transcribed RNA. In F. M. Ausubel, R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl (ed.), Current protocols in molecular biology, p. 4.10.1-4.10.8. John Wiley, New York, N.Y.
26. Gu, B., R. Kuddus, and N. A. DeLuca. 1995. Repression of activator-mediated transcription by herpes simplex virus 1CP4 via a mechanism involving interactions with the basal transcription factors TATA-binding protein and TFIIB. Mol. Cell. Biol. 15:3618-3626.
27. Gu, B., R. Rivera-Gonzalez, C. A. Smith, and N. A. DeLuca. 1993. Herpes simplex virus infected cell polypeptide 4 preferentially represses Sp1-activated over basal transcription from its own promoter. Proc. Natl. Acad. Sci. USA 90:9528-9532.
28. Gualberto, A., and A. S. J. Baldwin. 1995. p53 and Sp1 interact and cooperate in the tumor necrosis factor-induced transcriptional activation of the HIV-1 long terminal repeat. J. Biol. Chem. 270:19680-19683.
29. Hagen, G., S. Muller, M. Beato, and G. Suske. 1994. Sp1-mediated transcriptional activation is repressed by Sp3. EMBO J. 13:3843-3851.
30. Haley, J. D., and M. D. Waterfield. 1991. Contributory effects of de novo transcription and premature transcript termination in the regulation of human epidermal growth factor receptor proto-oncogene RNA synthesis. J. Biol. Chem. 266:1746-1753.
31. Hamanaka, R., K. Kohno, T. Seguchi, K. Okamura, A. Morimoto, M. Ono, J. Ogata, and M. Kuwano. 1992. Induction of low density lipoprotein receptor and a transcription factor SP-1 by tumor necrosis factor in human microvascular endothelial cells. J. Biol. Chem. 267:13160-13165.
32. Hung, H.-L., and K. A. High. 1996. Liver-enriched transcription factor HNF-4 and ubiquitous factor NF-Y are critical for expression of blood coagulation factor X. J. Biol. Chem. 271:2323-2331.
33. Iliopoulos, O., A. Kibel, S. Gray, and W. G. J. Kaelin. 1995. Tumour suppression by the human von Hippel-Lindau gene product. Nat. Med. 1:822-826.
34. Iliopoulos, O., A. P. Levy, C. Jiang, W. G. Kaelin, Jr., and M. A. Goldberg. 1996. Negative regulation of hypoxia-inducible genes by the von Hippel-Lindau protein. Proc. Natl. Acad. Sci. USA 93:10595-10599.
35. Inagaki, Y., S. Truter, and F. Ramirez. 1994. Transforming growth factor-β stimulates α2(I) collagen gene expression through a cis-acting element that contains an Sp1-binding site. J. Biol. Chem. 269:14828-14834.
36. Jackson, S. P., J. J. MacDonald, S. Lees-Miller, and R. Tjian. 1990. GC box binding induces phosphorylation of Sp1 by a DNA-dependent protein kinase. Cell 63:155-165.
37. Jackson, S. P., and R. Tjian. 1989. Purification and analysis of RNA polymerase II transcription factors by using wheat germ agglutinin affinity chromatography. Proc. Natl. Acad. Sci. USA 86:1781-1785.
38. Jensen, D. E., C. B. Rich, A. J. Terpstra, S. R. Farmer, and J. A. Foster. 1995. Transcriptional regulation of the elastin gene by insulin-like growth factor-1 involves disruption of Sp1 binding. J. Biol. Chem. 270:6555-6563.
39. Karlseder, J., H. Rotheneder, and E. Wintersberger. 1996. Interaction of Sp1 with the growth- and cell cycle-regulated transcription factor E2F. Mol. Cell. Biol. 16:1659-1667.
40. Kessler, P. M., S. P. Vasavada, R. R. Rackley, T. Stackhouse, F.-M. Duh, F. Latif, M. I. Lerman, B. Zbar, and B. R. G. Williams. 1995. Expression of the von Hippel-Lindau tumor suppressor gene, VHL, in human fetal kidney and during mouse embryogenesis. Mol. Med. 1:457-466.
41. Kibel, A., O. Iliopoulos, J. A. DeCaprio, and W. G. J. Kaelin. 1995. Binding of the von Hippel-Lindau tumor suppressor protein to elongin B and C. Science 269:1444-1446.
42. Kishida, T., T. M. Stackhouse, F. Chen, M. I. Lennan, and B. Zbar. 1995. Cellular proteins that bind the von Hippel-Lindau disease gene product: mapping of binding domains and the effect of missense mutations. Cancer Res. 55:4544-4548.
43. Kitadai, Y., W. Yasui, H. Yokozaki, H. Kuniyasu, K. Haruma, G. Kajiyama, and E. Tahara. 1992. The level of a transcription factor Sp1 is correlated with the expression of EGF receptor in human gastric carcinomas. Biochem. Biophys. Res. Commun. 189:1342-1348.
44. Latif, F., K. Tory, and J. Gnarra, et al. 1993. Identification of the von Hippel-Lindau disease tumor suppressor gene. Science 260:1317-1320.
45. Lee, J.-S., K. M. Galvin, and Y. Shi. 1993. Evidence for physical interaction between the zinc-finger transcription factors YY1 and Sp1. Proc. Natl. Acad. Sci. USA 90:6145-6149.
46. Leggett, R. W., S. A. Armstrong, D. Barry, and C. R. Mueller. 1995. Sp1 is phosphorylated and its DNA binding activity down-regulated upon terminal differentiation of the liver. J. Biol. Chem. 270:25879-25884.
47. Li, J., M. A. Perrella, J.-C. Tsai, S.-F. Yet, C.-M. Hsieh, M. Yoshizumi, C. Patterson, W. O. Endege, F. Zhou, and M.-E. Lee. 1995. Induction of vascular endothelial growth factor gene expression by interleukin-1β in rat aortic smooth muscle cells. J. Biol. Chem. 270:308-312.
48. Li, R., J. D. Knight, S. P. Jackson, R. Tjian, and M. R. Botchan. 1991. Direct interaction between Sp1 and the BPV enhancer E2 protein mediates synergistic activation of transcription. Cell 65:493-505.
49. Lin, S.-Y., A. R. Black, D. Kostic, S. Pajovic, C. N. Hoover, and J. C. Azizkhan. 1996. Cell cycle-regulated association of E2F1 and Sp1 is related to their functional interaction. Mol. Cell. Biol. 16:1668-1675.
50. Liu, Y., S. R. Cox, T. Morita, and S. Kourembanas. 1995. Hypoxia regulates vascular endothelial growth factor gene expression in endothelial cells: identification of a 5′ enhancer. Circ. Res. 77:638-643.
51. Maher, E. R., J. R. Yates, R. Harries, C. Benjamin, R. Harris, A. T. Moore, and M. A. Ferguson-Smith. 1990. Clinical features and natural history of von Hippel Lindau disease. Q. J. Med. 77:1151-1163.
52. Merika, M., and S. H. Orkin. 1995. Functional synergy and physical interactions of the erythroid transcription factor GATA-1 with the Krüppel family proteins Sp1 and EKLF. Mol. Cell. Biol. 15:2437-2447.
53. Miltenberger, R. J., P. J. Farnham, D. E. Smith, J. M. Stommel, and M. M. Cornwell. 1995. v-Raf activates transcription of growth-responsive promoters via GC-rich sequences that hind the transcription factor SP1. Cell Growth Differ. 6:549-556.
54. Mukhopadhyay, D., L. Tsiokas, and V. P. Sukhatme. 1995. Wild type p53 and v-Src exert opposing influences on human vascular endothelial growth factor gene expression. Cancer Res. 55:6161-6165.
55. Murata, Y., H. G. Kim, K. T. Rogers, A. J. Udvadia, and J. M. Horowitz. 1994. Negative regulation of Sp1 trans-activation is correlated with the binding of cellular proteins to the amino terminus of the Sp1 trans-activation domain. J. Biol. Chem. 269:20674-20681.
56. Nehls, M. C., R. A. Rippe, L. Veloz, and D. A. Brenner. 1991. Transcription factors nuclear factor I and Sp1 interact with the murine collagen α1(I) promoter. Mol. Cell. Biol. 11:4065-4073.
57. Perkins, N. D., A. B. Agranoff, E. Pascal, and G. J. Nabel. 1994. An interaction between the DNA-binding domains of RelA(p65) and Sp1 mediates human immunodeficiency virus gene activation. Mol. Cell. Biol. 14:6570-6583.
58. Rahman, A., A. Esmail, and F. Saatcioglu. 1995. A unique thyroid hormone response element in the human immunodeficiency virus type 1 long terminal repeat that overlaps the Sp1 binding sites. J. Biol. Chem. 270:31059-31064.
59. Saffer, J. D., S. P. Jackson, and M. B. Annarella. 1991. Developmental expression of Sp1 in the mouse. Mol. Cell. Biol. 11:2189-2199.
60. Saffer, J. D., S. P. Jackson, and S. J. Thurston. 1990. SV40 stimulates expression of the trans-acting factor Sp1 at the mRNA level. Genes Dev. 4:659-666.
61. Schaufele, F., B. L. West, and T. L. Reudelhuber. 1990. Overlapping Pit-1 and Sp1 binding sites are both essential to full rat growth hormone gene promoter activity despite mutually exclusive Pit-1 and Sp1 binding. J. Biol. Chem. 265:17189-17196.
62. Selo, E., B. Lewis, and T. Shenk. 1993. Interaction between transcription factors Sp1 and YY1. Nature 365:462.
63. Siemeister, G., K. Weindel, K. Mohrs, B. Barleon, G. Martiny-Baron, and D. Marme. 1996. Reversion of deregulated expression of vascular endothelial growth factor in human renal carcinoma cells by von Hippel-Lindau tumor suppressor protein. Cancer Res. 56:2299-2301.
64. Sif, S., A. J. Capobianco, and T. D. Gilmore. 1993. The v-Rel oncoprotein increases expression from Sp1 site-containing promoters in chicken embryo fibroblasts. Oncogene 8:2501-2509.
65. Srivastava, K. K., E. E. Cable, and H. L. Bonkovsky. 1993. Purifying nascent mRNA from nuclear run-on assays using guanidinium isothiocyanate. BioTechniques 15:226-227.
66. Suzuki, M., C. Kuroda, E. Oda, S. Tsunoda, T. Nakamura, T. Nakajima, and K. Oda. 1995. G10BP, an E1A-inducible negative regulator of Sp1, represses transcription of the rat fibronectin gene. Mol. Cell. Biol. 15:5423-5433.
67. Swevers, L., L. Cherbas, P. Cherbas, and K. Iatrou. 1996. Bombyx EcR (BmEcR) and Bombyx USP (BmCF1) combine to form a functional ecdysone receptor. Insect Biochem. Mol. Biol. 26:217-221.
68. Takahashi, A., H. Sasaki, S. J. Kim, K.-I. Tobisu, T. Kakizoe, T. Tsukamoto, Y. Kumamoto, T. Sugimura, and M. Terada. 1994. Markedly increased amounts of messenger RNAs for vascular endothelial growth factor and placenta growth factor in renal cell carcinoma associated with angiogenesis. Cancer Res. 54:4233-4237.
69. Tischer, E., R. Mitchell, T. Hartman, M. Silva, D. Gospodarowicz, J. C. Fiddes, and J. A. Abraham. 1991. The human gene for vascular endothelial growth factor. J. Biol. Chem. 266:11947-11954.
70. Tsuchiya, H., T. Iseda, and O. Hino. 1996. Identification of a novel protein (VBP-1) binding to the von Hippel-Lindau (VHL) tumor suppressor gene product. Cancer Res. 56:2881-2885.
71. Warren, R. S., H. Yuan, M. R. Matli, N. Ferrara, and D. B. Donner. 1996. Induction of vascular endothelial growth factor by insulin-like growth factor 1 in colorectal carcinoma. J. Biol. Chem. 271:29483-29488.
72. Weidner, U., S. Peter, T. Strohmeyer, R. Hussnatter, R. Ackermann, and H. Sies. 1990. Inverse relationship of epidermal growth factor receptor and HER2/neu gene expression in human renal cell carcinoma. Cancer Res. 50:4504-4509.
73. Wizigmann-Voos, S., G. Breier, W. Risau, and K. H. Plate. 1995. Up-regulation of vascular endothelial growth factor and its receptors in von Hippel-Lindau disease-associated and sporadic hemangioblastomas. Cancer Res. 55:1358-1364.
74. Xu, J., K. L. Thompson, L. B. Shephard, L. G. Hudson, and G. N. Gill. 1993. T3 receptor suppression of Sp1-dependcnt transcription from the epidermal growth factor receptor promoter via overlapping DNA-binding sites. J. Biol. Chem. 268:16065-16073.
75. Yao, M., T. Shuin, H. Misaki, and Y. Kubota. 1988. Enhanced expression of c-myc and epidermal growth factor receptor (C-erbB-1) genes in primary human renal cancer. Cancer Res. 48:6753-6757.
76. Zhu, L., S. van den Heuvel, K. Helin, A. Fattaey, M. Ewen, D. Livingston, N. Dyson, and E. Harlow. 1993. Inhibition of cell proliferation by p107, a relative of the retinoblastoma protein. Genes Dev. 7:1111-1125.