Repression of the insulin receptor promoter by the tumor suppressor gene product p53: A possible mechanism for receptor overexpression in breast cancer

Cancer Research

Volumn 56, Issue 12, 1996, Pages 2781-2788

  Webster, Nicholas J G ^a,b   Resnik, Jamie L ^a,b   Reichart, Donna B ^a,b   Strauss, Brian ^a   Haas, Martin ^a   Seely, B Lynn ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INSULIN; INSULIN RECEPTOR; PROTEIN P53; SOMATOMEDIN C; SOMATOMEDIN C RECEPTOR;

ARTICLE; BREAST CARCINOGENESIS; BREAST CARCINOMA; GENE EXPRESSION REGULATION; GROWTH REGULATION; HORMONE RECEPTOR INTERACTION; HUMAN; HUMAN TISSUE; PRIORITY JOURNAL; PROMOTER REGION; TUMOR GROWTH; TUMOR SUPPRESSOR GENE;

ANIMALS; BASE SEQUENCE; BINDING, COMPETITIVE; BREAST NEOPLASMS; CCAAT-ENHANCER-BINDING PROTEINS; DNA-BINDING PROTEINS; FEMALE; GENES, REPORTER; HUMANS; INSULIN; INSULIN-LIKE GROWTH FACTOR I; MICE; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; PROMOTER REGIONS (GENETICS); RECEPTOR, IGF TYPE 1; RECEPTOR, INSULIN; SP1 TRANSCRIPTION FACTOR; TRANSFECTION; TUMOR SUPPRESSOR PROTEIN P53;

EID: 0029885334     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (64)

1. McClain, D A., Maegawa, H , Lee, J., Dull, T. J., Ulrich, A., and Olefsky, J. M. A mutant insulin receptor with defective tyrosine kinase displays no biologic activity and does not undergo endocytosis. J Biol Chem., 262 14663-14671, 1987.
2. Yeh, T. C , and Roth, R. A Insulin receptor signaling in Madin-Darby canine kidney cells overexpressing the human insulin receptor. Diabetes, 43: 1297-1303, 1994.
3. Hofmann, C , Goldfine, I. D., and Whittaker, J. The metabolic and mitogenic effects of both insulin and insulin-like growth factor are enhanced by transfection of insulin receptors into NIH3T3 fibroblasts J. Biol. Chem., 264: 8606-8611, 1989.
4. Frittitta, L., Vigneri, R., Stampfer, M. R . and Goldfine, I D Insulin receptor overexpression in 184B5 human mammary epithelial cells induces a ligand-dependent transformed phenotype J Cell Biochem., 57. 666-669, 1995.
5. Giorgino, F., Belfiore, A., Milazzo, G., Costantino, A , Maddux, B., Whittaker, J., Goldfine, I. D , and Vigneri, R. Overexpression of insulin receptors in fibroblast and ovary cells induces a ligand-mediated transformed phenotype Mol. Endocrinol., 5 452-459, 1991
6. Le Marchand, L., Kolonel, L. N., Earle, M. E., and Mi, M. P Body size at different periods of life and breast cancer risk. Am J. Epidemiol, 128. 137-152, 1988.
7. Schapira, D. V., Kumar, N. B., Lyman, G. H., and Cox, C E. Abdominal obesity and breast cancer risk. Ann. Intern. Med . 112: 182-186, 1990.
8. Pathak, D. R. and Whittemore, A. S Combined effects of body size, parity, and menstrual events on breast cancer incidence in seven countries Am J. Epidemiol. 135: 153-168, 1992
9. Bulun, S. E , Mahendroo, M. S , and Simpson, E. R Aromatase gene expression in adipose tissue: relationship to breast cancer. J. Steroid. Biochem Mol. Biol., 49, 319-326, 1994
10. Siiteri, P K Review of studies on estrogen biosynthesis in the human. Cancer Res., 42: 3269s-3273s, 1982.
11. Miller, W. R., Hawkins, R. A., and Forrest, A. P. Significance of aromatase activity in human breast cancer. Cancer Res., 42: 3365s-3368s, 1982.
12. DeFronzo, R. A., and Ferrannini, E. Insulin resistance. A multifaceted syndrome responsible for NIDDM, obesity, hypertension, dyslipidemia, and atherosclerotic cardiovascular disease. Diabetes Care, 14: 173-194, 1991.
13. Bonadonna, R. C., Groop, L., Kraemer, N., Ferrannini, E., Del Prato, S., and DeFronzo, R. A. Obesity and insulin resistance in humans: a dose-response study. Metabolism, 39. 452-459, 1990.
14. Nolan, J. J , Freidenberg, G., Henry, R., Reichart, D., and Olefsky, J. M. Role of human skeletal muscle insulin receptor kinase in the in vivo insulin resistance of noninsulin-dependent diabetes mellitus and obesity. J. Clin. Endocrinol. Metab., 78: 471-477, 1994.
15. Heuson, J. C., and Legros, N Influence of insulin deprivation on growth of the 7,12-dimethylbenz(a)anthracene-induced mammary carcinoma in rats subjected to alloxan diabetes and food restriction. Cancer Res., 32: 226-232, 1972.
16. Heuson, J C., Legros, N., and Heimann, R. Influence of insulin administration on growth of the 7,12-dimethylbenz(a)anthracene-induced mammary carcinoma in intact, oophorectomized, and hypophysectomized rats. Cancer Res., 32:233-238, 1972.
17. Heuson, J. C , and Legros, N. Effect of insulin and of alloxan diabetes on growth of the rat mammary carcinoma in vivo. Eur. J. Cancer, 6: 349-351, 1970.
18. Jorgensen, L. N., Didenksen, L. H., and Drejer, K. Carcinogenic effect of the human insulin analogue B10Asp in female rats. Diabetes, 41 (Suppl.1): 143A, 1992
19. Milazzo, G., Giorgino, F., Damante, G., Sung, C., Stampfer, M R., Vigneri, R., Goldfine, I. D., and Belfiore, A. Insulin receptor expression and function in human breast cancer cell lines. Cancer Res., 52: 3924-3930, 1992.
20. Papa, V., Gliozzo, B., Clark, G M., McGuire, W. L., Moore, D., Fujita-Yamaguchi, Y., Vigneri, R., Goldfine, I. D., and Pezzino, V. Insulin-like growth factor-I receptors are overexpressed and predict a low risk in human breast cancer. Cancer Res., 53, 3736-3740, 1993.
21. Papa, V , Pezzino, V , Costantino, A , Belfiore, A., Giuffrida, D., Frittitta, L , Vannelli, G. B., Brand, R., Goldfine, I D., and Vigneri, R. Elevated insulin receptor content in human breast cancer. J. Clin. Invest., 86: 1503-1510, 1990.
22. Peyrat, J. P., and Bonneterre, J. Type 1 IGF receptor in human breast diseases. Breast Cancer Res. Treat., 22: 59-67, 1992.
23. Peyrat, J. P., Bonneterre, J., Vennin, P. H., Jammes, H., Beuscart, R., Hecquet, B., Djiane, J., Lefebvre, J., and Demaille, A. Insulin-like growth factor 1 receptors (IGF1-R) and IGF1 in human breast tumors. J. Steroid Biochem. Mol. Biol., 37. 823-827, 1990.
24. Cullen, K. J., Yee, D., Sly, W S., Perdue, J., Hampton, B., Lippman, M E, and Rosen. N. Insulin-like growth factor receptor expression and function in human breast cancer. Cancer Res., 50: 48-53, 1990.
25. Sell, C., Dumenil, G., Deveaud, C., Miura, M., Coppola, D., DeAngelis, T., Rubin, R., Efstratiadis, A., and Baserga, R. Effect of a null mutation of the insulin-like growth factor I receptor gene on growth and transformation of mouse embryo fibroblasts Mol. Cell. Biol. 14: 3604-3612, 1994
26. Sell, C., Ptasznik, A., Chang, C. D., Swantek, J., Cristofalo, V. J., and Baserga, R. IGF-1 receptor levels and the proliferation of young and senescent human fibroblasts. Biochem. Biophys Res. Commun., 194: 259-265, 1993.
27. Baserga, R. The insulin-like growth factor I receptor, a key to tumor growth? Cancer Res , 55: 249-252, 1995
28. Coppola, D., Ferber, A., Miura, M , Sell, C., D'Ambrosio, C., Rubin, R., and Baserga, R. A functional insulin-like growth factor I receptor is required for the mitogenic and transforming activities of the epidermal growth factor receptor. Mol Cell Biol., 14. 4588-4595, 1994.
29. Osborne, C. K., Clemmons, D. R., and Arteaga, C L. Regulation of breast cancer growth by insulin-like growth factors J Steroid Biochem. Mol. Biol., 37, 805-809, 1990
30. Davidoff, A. M., Humphrey, P. A., Iglehart, J D., and Marks, J R. Genetic basis for p53 overexpression in human breast cancer. Proc Natl. Acad. Sci. USA. 88: 5006-5010, 1991.
31. Borresen, A. L , Hovig, E., Smith-Sorensen, B , Malkin, D., Lystad, S., Andersen, T I., Nesland, J. M., Isselbacher, K. J., and Friend, S H. Constant denaturant gel electrophoresis as a rapid screening technique for p53 mutations Proc. Natl Acad. Sci USA, 88: 8405-8409, 1991.
32. Mazars, R. Spinardi, L., BenCheikh, M , Simony-Lafontaine, J., Jeanteur, P., and Theillet, C. p53 mutations occur in aggressive breast cancer. Cancer Res., 52: 3918-3923, 1992.
33. Runnebaum, I B., Nagarajan, M., Bowman, M., Soto, D , and Sukumar, S. Mutations in p53 as potential molecular markers for human breast cancer. Proc. Natl. Acad Sci. USA, 88 10657-10661, 1991
34. Milner, J , and Medcalf, E A. Cotranslation of activated mutant p53 with wild type drives the wild-type p53 protein into the mutant conformation. Cell, 65, 765-774, 1991.
35. Horak, E., Smith, K., Bromley, L., LeJeune, S., Greenall, M., Lane, D., and Harris, A. L. Mutant p53, EGF receptor and c-erbB-2 expression in human breast cancer. Oncogene, 6: 2277-2284, 1991.
36. Lane, D. P On the expression of the p53 protein in human cancer Mol Biol. Rep , 19: 23-29, 1994
37. Kastan, M. B., Canman, C. E., and Leonard, C. J. p53, cell cycle control and apoptosis, implications for cancer. Cancer Metastasis Rev., 14: 3-15, 1995.
38. Zambetti, G. P., Bargonetti, J., Walker, K., Prives, C., and Levins, A. J. Wild-type p53 mediates positive regulation of gene expression through a specific DNA sequence element. Genes Dev., 6: 1143-1152, 1992.
39. Kern, S. E., Pietenpol, J. A., Thiagalingam, S , Seymour, A., Kinder, K. W., and Vogelstein, B. Oncogenic forms of p53 inhibit p53-regulated gene expression. Science (Washington DC), 256: 827-830, 1992.
40. Mack, D. H., Vartikar, J., Pipas, J M., and Laimins, L. A. Specific repression of TATA-mediated but not initiator-mediated transcription by wild-type p53 Nature (Lond.), 363, 281-283, 1993.
41. Agoff, S. N , Hou, J., Linzer, D. I., and Wu, B. Regulation of the human hsp70 promoter by p53. Science (Washington DC), 259; 84-87, 1993.
42. McKeon, C., Moncada, V., Pham, T., Salvatore, P , Kadowaki, T., Accili, D., and Taylor, S. I. Structural and functional analysis of the insulin receptor promoter. Mol. Endocrinol., 4; 647-656, 1990.
43. Mamula, P. W , Wong, K. Y., Maddux, B. A., McDonald, A. R., and Goldfine, I. D. Sequence and analysis of promoter region of human insulin-receptor gene. Diabetes, 37: 1241-1246, 1988.
44. Tewari, D S , Cook, D. M , and Taub, R. Characterization of the promoter region and 3′ end of the human insulin receptor gene. J. Biol. Chem., 264: 16238-16245, 1989
45. Cameron, K. E , Resnik, J., and Webster, N. J Transcriptional regulation of the human insulin receptor promoter. J. Biol. Chem. 267: 17375-17383, 1992.
46. Levy, J. R., and Hug, V. Nuclear protein-binding analysis of a GC-rich insulin-receptor promoter regulatory region. Diabetes, 42, 66-73, 1993.
47. Lee, J. K., Tam, J. W , Tsai, M. J., and Tsai, S. Y. Identification of cis- and trans-acting factors regulating the expression of the human insulin receptor gene. J. Biol. Chem., 267: 4638-4645, 1992.
48. Webster, N. J. G., Kong, Y., Cameron, K E., and Resnik, J. L. An upstream element from the human insulin receptor gene promoter contains binding sites for C/EBPβ and NF-1 Diabetes, 43: 305-312, 1994.
49. McKeon, C., and Pham, T. Transactivation of the human insulin receptor gene by the CAAT/enhancer binding protein. Biochem. Biophys. Res. Commun., 174: 721-728, 1991.
50. Brunetti, A., Foti, D , and Goldfine, I. D. Identification of unique nuclear regulatory proteins for the insulin receptor gene, which appear during myocyte and adipocyte differentiation. J. Clin. Invest., 92: 1288-1295, 1993
51. Werner, H , Rauscher, F J., III, Sukhatme, V. P., Drummond, I. A., Roberts, C. T., Jr., and LeRoith, D. Transcriptional repression of the insulin-like growth factor I receptor (IGF-I-R) gene by the tumor suppressor WT1 involves binding to sequences both upstream and downstream of the IGF-I-R gene transcription start site. J. Biol. Chem., 269: 12577-12582, 1994.
52. Beitner-Johnson, D., Werner, H , Roberts, C T J., and LeRoith, D. Regulation of insulin-like growth factor I receptor gene expression by Sp1: physical and functional interactions of Sp1 at GC boxes and at a CT element. Mol. Endocrinol., 9: 1147-1156, 1995.
53. Borellini, F., and Glazer, R. I. Induction of Sp1-p53 DNA-binding heterocomplexes during granulocyte/macrophage colony-stimulating factor-dependent proliferation in human erythroleukemia cell line TF-1. J Biol. Chem., 268: 7923-7928, 1993.
54. Margulies, L., and Sehgal, P B. Modulation of the human interleukin-6 promoter (IL-6) and transcription factor C/EBP beta (NF-IL6) activity by p53 species. J. Biol. Chem., 268: 15096-15100, 1993.
55. Lin, F-T., and Lane, M. D. CCAAT/enhancer binding protein α is sufficient to initiate the 3T3-L1 adipocyte differentiation program. Proc. Natl. Acad. Sci. USA, 91: 8757-8761, 1994.
56. Yeh, W. C., Cao, Z, Classon, M., and McKnight, S. L Cascade regulation of terminal adipocyte differentiation by three members of the C/EBP family of leucine zipper proteins. Genes Dev , 9: 168-181, 1995.
57. Akira, S , Isshiki, H., Sugita, T., Tanabe, O., Kinoshita, S., Nishio, Y., Nakajima, T., Hirano, T., and Kishimoto, T. A nuclear factor for IL-6 expression (NF-IL6) is a member of a C/EBP family. EMBO J., 9. 1897-1906, 1990
58. Yin, T., Yasukawa, K., Taga, T., Kishimoto, T., and Yang, Y-C. Identification of a 130-kilodalton tyrosine-phosphorylated protein induced by interleukin-11 as JAK2 tyrosme kinase, which associates with gp130 signal transducer. Exp. Hematol., 22: 467-472, 1994.
59. Faraham, P. J , and Schimke, R. T. In vitro transcription and delimitation of promoter elements of the murine dihydrofolate reductase gene. Mol. Cell. Biol., 6, 2392-2401, 1986
60. Kim, H S., Lee, I. K , and Tsai, S. Y. Ela activation of insulin receptor gene expression is mediated by Sp1-binding sites Mol. Endocrinol., 9: 178-186, 1995.
61. Blake, M C., and Azizkhan, J C. Transcription factor E2F is required for efficient expression of the hamster dihydrofolate reductase gene in vitro and in vivo. Mol. Cell. Biol., 9 4994-5002, 1989.
62. Morris, G. F , and Mathews, M. B The adeaovirus E1A transforming protein activate the proliferating cell nuclear antigen promoter via an activating transcription factor site. J. Virol., 65, 6397-6406, 1991.
63. Yew, P. R., and Berk, A. J. Inhibition of p53 transactivation required for transformation by adenovirus early 1B protein Nature (Lond.), 357: 82-85, 1992.
64. Yew, P R., Liu, X , and Berk, A. J. Adenovirus E1B oncoprotein tethers a transcriptional repression domain to p53. Genes Dev , 8: 190-202, 1994.