Heregulin induces transcriptional activation of the progesterone receptor by a mechanism that requires functional ErbB-2 and mitogen-activated protein kinase activation in breast cancer cells

Molecular and Cellular Biology

Volumn 23, Issue 3, 2003, Pages 1095-1111

  Labriola, Leticia ^a   Salatino, Mariana ^a   Proietti, Cecilia J ^a   Pecei, Adalí ^b   Coso, Omar A ^b   Kornblihtt, Alberto R ^b   Charreau, Eduardo H ^a,b   Elizalde, Patricia V ^a  

^a INST DE BIOL Y MED EXPERIMENTAL   (Argentina)

^b UNIVERSIDAD DE BUENOS AIRES   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; ANTISENSE OLIGODEOXYNUCLEOTIDE; EPIDERMAL GROWTH FACTOR RECEPTOR 2; GESTAGEN; MEDROXYPROGESTERONE ACETATE; MIFEPRISTONE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; NEU DIFFERENTIATION FACTOR; PROGESTERONE; PROGESTERONE RECEPTOR; PROTEIN; TYROSINE KINASE RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; AUTORADIOGRAPHY; BINDING SITE; BREAST ADENOCARCINOMA; BREAST CANCER; CANCER CELL CULTURE; CARCINOGENESIS; CELL NUCLEUS; CONTROLLED STUDY; DNA PROTEIN COMPLEX; DOWN REGULATION; ENZYME ACTIVATION; ENZYME ACTIVITY; GENETIC TRANSFECTION; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; TRANSACTIVATION; TRANSCRIPTION INITIATION;

ANIMALS; BREAST NEOPLASMS; CELL DIVISION; CELL NUCLEUS; ENZYME INHIBITORS; FEMALE; FLAVONOIDS; GENES, ERBB-2; HORMONE ANTAGONISTS; HUMANS; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; MICE, INBRED BALB C; MIFEPRISTONE; MITOGEN-ACTIVATED PROTEIN KINASES; NEUREGULIN-1; PHOSPHORYLATION; RECEPTOR, ERBB-2; RECEPTORS, PROGESTERONE; RNA, MESSENGER; RNA, NEOPLASM; TRANS-ACTIVATION (GENETICS); TUMOR CELLS, CULTURED;

ANIMALIA; EUKARYOTA; FELIS CATUS; MURINAE;

EID: 0037305884     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.23.3.1095-1111.2003     Document Type: Article

References (77)

1. Aronica, S. M., and B. S. Katzenellenbogen. 1991. Progesterone receptor regulation in uterine cells: stimulation by estrogen, cyclic adenosine 3′,5′-monophosphate, and insulin-like growth factor I and suppression by antiestrogens and protein kinase inhibitors. Endocrinology 128:2045-2052.
2. MAPK and is involved in phosphatidylinositol 3-kinase signaling in Xenopus oocytes. J. Biol. Chem. 276:37708-37714.
3. Bai, W., B. G. Rowan, V. E. Allgood, B. W. O'Malley, and N. L. Weigel. 1997. Differential phosphorylation of chicken progesterone receptor in hormone-dependent and ligand-independent activation. J. Biol. Chem. 272:10457-10463.
4. Balañá, M. E., L. Labriola, M. Salatino, F. Movsichoff, G. Peters, E. H. Charreau, and P. V. Elizalde. 2001. Activation of ErbB-2 via a hierarchical interaction between ErbB-2 and type I insulin-like growth factor receptor in mammary tumor cells. Oncogene 20:34-47.
5. Balañá, M. E., R. Lupu, L. Labriola, E. H. Charreau, and P. V. Elizalde. 1999. Interactions between progestins and heregulin (HRG) signaling pathways: HRG acts as mediator of progestins proliferative effects in mouse mammary adenocarcinomas. Oncogene 18:6370-6379.
6. Baserga, R. 1995. The insulin-like growth factor I receptor: a key to tumor growth. Cancer Res. 55:249-252.
7. Beck, C. A., N. L. Weigel, and D. P. Edwards. 1992. Effect of hormone and cellular modulators of protein phosphorylation on transcriptional activity, DNA binding, and phosphorylation of human progesterone receptors. Mol. Endocrinol. 6:607-620.
8. Beerli, R. R., D. Graus-Porta, K. Woods-Cook, X. Chen, Y. Yarden, and N. E. Hynes. 1995. Neu differentiation factor activation of ErbB-3 and ErbB-4 is cell specific and displays a differential requirement for ErbB-2. Mol. Cell. Biol. 15:6496-6505.
9. Boonjarantanakornkit, V., M. Porter Scott, V. Ribon, L. Sherman, S. M. Anderson, J. L. Maller, W. T. Miller, and D. P. Edwards. 2001. Progesterone receptor contains a proline-rich motif that directly interacts with SH3 domains and activates c-SRC family tyrosine kinases. Mol. Cell 8:269-280.
10. Braunsberg, H., N. G. Coldham, R. E. Learke, S. K. Cowan, and W. Wong. 1987. Actions of progestogen on human breast cancer cells: mechanisms of growth stimulation and inhibition. Eur. J. Cancer Clin. Oncol. 23:563-571.
11. Bunone, G., P. A. Briand, R. J. Miksicek, and D. Picard. 1996, Activation of the unliganded estrogen receptor by EGF involves the MAP kinase pathway and direct phosphorylation. EMBO J. 15:2174-2183.
12. Cho, H., S. M. Aronica, and B. S. Katzenellenbogen. 1994. Regulation of progesterone receptor gene expression in MCF-7 breast cancer cells: a comparison of the effects of cyclic adenosine 3′,5′-monophosphate, estradiol, insulin growth factor I, and serum factors. Endocrinology 134:658-664.
13. Clarke, C. L., and R. L. Sutherland. 1990. Progestin regulation of cellular proliferation. Endocrinol. Rev. 11:266-302.
14. Clemm, D. L., L. Sherman, V. Boonyaratanakornkit, W. T. Schrader, N. L. Weigel, and D. P. Edwards. 2000. Differential hormone-dependent phosphorylation of progesterone receptor A and B forms revealed by a phosphoserine site-specific monoclonal antibody. Mol. Endocrinol. 14:52-65.
15. Cohen, G. B., R. Ren, and D. Baltimore. 1995. Modular binding domains in signal transduction proteins. Cell 80:237-248.
16. Colomer, R., R. Lupu, S. S. Bacus, and E. P. Gelmann. 1994. ErbB-2 antisense oligonucleotides inhibit the proliferation of breast carcinoma cells with erbB-2 oncogene amplification. Br. J. Cancer 70:819-825.
17. Coso, O. A., S. Montaner, C. Fromm, J. C. Lacal, R. Prywes, H. Teramoto, and J. S. Gutkind. 1997. Signaling from G protein-coupled receptors to the c-Jun promoter involves the MEF2 transcription factor. J. Biol. Chem. 272: 20691-20697.
18. Curtis, S. W., T. Washburn, C. Sewall, R. Di Augustine, J. Lindzey, J. F. Couse, and K. S. Korach. 1996. Physiological coupling of growth factor and steroid receptor signaling pathways: estrogen receptor knockout mice lack estrogen-like response to epidermal growth factor. Proc. Natl. Acad. Sci. USA 93:12626-12630.
19. Denner, L. A., N. L., Weigel, B. L. Maxwell, W. T. Schrader, and B. W. O'Malley. 1990. Regulation of progesterone receptor-mediated transcription by phosphorylation. Science 250:1740-1743.
20. Denner, L. A., N. L. Weigel, W. T. Schrader, and B. W. O'Malley. 1989. Hormone-dependent regulation of chicken progesterone receptor deoxyribonucleic acid binding and phosphorylation. Endocrinology 125:3051-3058.
21. Dran, G., I. A. Luthy, A. A. Molinolo, F. Montecchia, E. H. Charreau, C. D. Pasqualini, and C. Lanari. 1995. Effect of medroxyprogesterone acetate (MPA) and serum factors on cell proliferation in primary cultures of an MPA-induced mammary adenocarcinoma. Breast Cancer Res. Treatment 35:173-186.
22. Edwards, D. P., N. L. Weigel, S. K. Nordeen, and C. A. Beck. 1993. Modulators of cellular protein phosphorylation alter the trans-activation function of human progesterone receptor and the biological activity of progesterone antagonists. Breast Cancer Res. Treatment 27:41-56.
23. Egan, S. E., and R. A. Weinberg. 1993. The pathway to signal achievement. Nature 365:781-783.
24. El-Ashry, D., S. A. Oñate, S. K. Nordeen, and D. P. Edwards. 1989. Human progesterone receptor complexed with the antagonist RU486 binds to hormone response elements in a structurally altered form. Mol. Endocrinol. 3:1545-1558.
25. Fiddes, R. J., P. W. Janes, S. P. Silversten, R. L. Sutherland, E. A. Musgrove, and R. J. Daly. 1998. Inhibition of the MAP kinase cascade blocks heregulin-induced cell cycle progression in T-47D human breast cancer cells. Oncogene 16:2803-2813.
26. Gass, E. K., S. A. Leonhardt, S. K. Nordeen, and D. P. Edwards. 1998. The antagonists RU486 and ZK98299 stimulate progesterone receptor binding to deoxyribonucleic acid in vitro and in vivo but have distinct effects on receptor conformation. Endocrinology 139:1905-1919.
27. Graus-Porta, D., R. R. Beerli, and N. E. Hynes. 1995. Single-chain antibody-mediated intracellular retention of ErbB-2 impairs Neu differentiation factor and epidermal growth factor signaling. Mol. Cell. Biol. 15:1182-1191.
28. Graus-Porta, D., R. R. Beerli, J. M. Daly, and N. E. Hynes. 1997. ErbB-2, the preferred heterodimerization partner of all ErbB receptors, is a mediator of lateral signaling. EMBO J. 16:1647-1655.
29. Groshong, S. D., G. L. Owen, B. Grimison, I. E. Schauer, M. C. Todd, T. A. Langan, R. A. Sclafani, C. A. Lange, and K. B. Horwitz. 1997. Biphasic regulation of breast cancer cell growth by progesterone: role of the cyclin-dependent kinase inhibitor, p21 and p27 (kip1). Mol. Endocrinol. 11:1593-1607.
30. Horwitz, K. B., and P. S. Alexander. 1983. In situ photolinked nuclear progesterone receptors of human breast cancer cells: subunit molecular weights after transformation and translocation. Endocrinology 113:2195-2201.
31. Ignar-Trowbridge, D. M., C. T. Teng, K. A. Ross, M. G. Parker, K. S. Korach, and J. A. McLachlan. 1993. Peptide growth factors elicit estrogen-dependent transcriptional activation of an estrogen-responsive element. Mol. Endocrinol. 7:992-998.
32. Ignar-Trowbridge, D. M., K. G. Nelson, M. C. Bidwell, S. W. Curtis, T. F. Washburn, J. A. McLachlan, and K. S. Korach. 1992. Coupling of dual signaling pathways: epidermal growth factor action involves the estrogen receptor. Proc. Natl. Acad. Sci. USA 89:4658-4662.
33. Kato, S., H. Endoh, Y. Masuhiro, T. Kitamoto, S. Uchiyama, H. Sasaki, S. Masushige, Y. Gotoh, E. Nishida, H. Kawashima, D. Metzger, and P. Chambon. 1995. Activation of the estrogen receptor through phosphorylation by mitogen-activated protein kinase. Science 270:1491-1494.
34. Kavanaugh, W. M., and L. T. Williams. 1994. An alternative to SH2 domains for binding tyrosine phosphorylated proteins. Science 266:1862-1865.
35. Kiss, R., R. J. Paridaens, J. C. Heuson, and A. J. Danguy. 1986. Effect of progesterone on cell proliferation on the MXT mouse hormone-sensitive mammary neoplasm. J. Natl. Cancer Inst. 77:173-178.
36. Knotts, T. A., R. O. Orkiszewski, R. G. Cook, D. P. Edwards, and N. L. Weigel. 2001. Identification of a phosphorylation site in the hinge region of the human progesterone receptor and additional amino-terminal phosphorylation sites. J. Biol. Chem. 276:8475-8483.
37. Kraus, M. H., W. Issing, T. Miki, N. C. Popescu, and S. A. Aaronson. 1989. Isolation and characterization of ERBB3, a third member of the ERBB/epidermal growth factor receptor family: evidence for overexpression in a subset of human mammary tumors. Proc. Natl. Acad. Sci. USA 86:9193-9197.
38. Lanari, C., E. Kordon, A. A. Molinolo, C. D. Pasqualini, and E. H. Charreau. 1989. Mammary adenocaminomas induced by medroxyprogesterone acetate: hormone dependence and EGF receptors of BALB/c in vivo sublines. Int. J. Cancer 43:845-850.
39. Lange, C. A., J. K. Richer, T. Shen, and K. B. Horwitz. 1998. Convergence of progesterone and epidermal growth factor signaling in breast cancer. J. Biol. Chem. 273:31308-31316.
40. Lange, C. A., T. Shen, and K. B. Horwitz. 2000. Phosphorylation of human progesterone receptors at serine-294 by mitogen-activated protein kinase signals their degradation by the 26S proteosome. Proc. Natl. Acad. Sci. USA 97:1032-1037.
41. Lewis, G. D., J. A. Lofgren, A. E. McMurtrey, A. Nuijens, B. M. Fendly, K. D. Bauer, and M. X. Sliwkowski. 1996. Growth regulation of human breast and ovarian tumor cells by heregulin: evidences for the requirement of ErbB-2 as a critical component in mediating heregulin responsivness. Cancer Res. 56:1457-1465.
42. Lowenstein, E. J., R. J. Daly, A. G. Batzer, W. Li, B. Margolis, R. Lammers, A. Ullrich, E. Y. Skolnik, D. Bar-Sagi, and J. Schlessinger. 1992. The SH2 and SH3 domain-containing protein GrbB-2 links receptor tyrosine kinases to ras signaling. Cell 70:431-442.
43. Manni, A., B. Badger, C. Wright, J. R. Ahmed, and L. M. Demers. 1987. Effects of progestins on growth of experimental breast cancer in culture: interaction with estradiol and prolactin and involvement of the polyamine pathway. Cancer Res. 47:3066-3071.
44. Marte, B. M., D. Graus-Porta, M. Jescke, D. Favor, N. E. Hynes, and D. Taverna. 1995. NDF/heregulin activates MAP kinase and p70/p85 S6 kinase during proliferation or differentiation of mammary epithelial cells. Oncogene 10:167-175.
45. Migliaccio, A., D. Piccolo, G. Castoria, M. Di Domenico, A. Bilancio, M. Lombardi, W. Gong, M. Beato, and F. Auricchio. 1998. Activation of the Src/p21 ras/Erk pathway by progesterone receptor via cross-talk with estrogen receptor. EMBO J. 17:2008-2018.
46. Mockus, M. B., and K. B. Horwitz. 1983. Progesterone receptors in human breast cancer: stoichiometric translocation and nuclear receptor processing. J. Biol. Chem. 258:4778-4783.
47. Molinolo, A. A., C. Lanari, E. H. Charreau, N. Sanjuan, and C. D. Pasqualini. 1987. Mouse mammary tumors induced by medroxiprogesterone acetate: immunochemistry and hormonal receptors. J. Natl. Cancer. Inst. 79:1341-1350.
48. Montecchia, M. F., C. Lamb, A. A. Molinolo, I. A. Luthy, P. Pazos, E. H. Charreau, S. Vanzulli, and C. Lanari. 1999. Progesterone receptor involvement in independent tumor growth in MPA-induced murine mammary adenocarcinomas. J. Steroid Biochem. Mol. Biol. 68:11-21.
49. Mullik, A., and B. S. Katzenellenbogen. 1986. Progesterone receptor synthesis and degradation in MCF-7 human breast cancer cells as studied by dense amino acid incorporation. J. Biol. Chem. 261:13236-13243.
50. Pelicci, G., L. Lanfrancone, F. Grignani, J. McGlade, F. Cavallo, G. Forni, I. Nicoletti, F. Grignani, T. Pawson, and P. G. Pelicci. 1992. A novel transforming protein (SHC) and SH2 domain is implicated in mitogenic signal transduction. Cell 70:93-104.
51. Pietras, R. J., J. Arboleda, D. M. Reese, N. Wongvipat, M. D. Pegram, L. Ramos, C. M. Groman, M. G. Parker, M. X. Slikowski, and D. J. Slamon. 1995. Her-2 tyrosine kinase pathway targets estrogen receptor and promotes hormone-independent growth in human breast cancer cells. Oncogene 10: 2435-2446.
52. Pinkas-Kramaski, R., I. Alroy, and Y. Yarden. 1997. Human epidermal growth factor receptor cDNA sequence and aberrant expression of the amplified gene in A431 epidermoid carcinoma cells. J. Mamm. Gland Biol. Neoplasia 2:97-107.
53. Plowman, G. D., G. S. Whitney, M. G. Neubauer, J. M. Green, V. L. McDonald, G. J. Todaro, and M. Shoyab. 1990. Molecular cloning and expression of an additional epidermal growth factor receptor-related gene. Proc. Natl. Acad. Sci. USA 87:4905-4909.
54. erbB-4, a fourth member of the epidermal growth factor receptor family. Proc. Natl. Acad. Sci. USA 90:1746-1750.
55. Poletti, A., and N. L. Weigel. 1993. Identification of a hormone-dependent phosphorylation site adjacent to the DNA-binding domain of the chicken progesterone receptor. Mol. Endocrinol. 7:241-246.
56. Power, R. F., S. K. Mani, J. Codina, O. M. Conneely, and B. W. O'Malley. 1991. Dopaminergic and ligand-independent activation of steroid hormone receptors. Science 254:1636-1939.
57. Read, L. D., C. E. Snider, J. S. Miller, G. L. Green, and B. S. Katzenellenbogen. 1988. Ligand-modulated region of progesterone receptor messenger ribonucleic acid and protein in human breast cancer cell lines. Mol. Endocrinol. 2:263-271.
58. Richer, J. K., C. A. Lange, N. G. Manning, G. Owen, R. Powell, and K. B. Horwitz. 1998. Convergence of progesterone with growth factor and cytokine signaling in breast cancer. J. Biol. Chem. 273:31317-31326.
59. Riese, D. J., II, and D. F. Stern. 1998. Specificity within the EGF family/ErbB receptor family signaling network. Bioessays 20:41-48.
60. Saceda, M., T. Grunt, R. Colomer, M. Lippman, R. Lupu, and M. Martin. 1996. Regulation of estrogen receptor concentration and activity by an erbB/HER ligand in breast carcinoma cell lines. Endocrinology 137:4322-4330.
61. Sartorius, C. A., M. Y. Melville, A. R. Hovland, L. Tung, G. S. Takimoto, and K. B. Horwitz. 1994. A third transactivation function (AF3) of human progesterone receptors locate in the unique N-terminal segment of the B-isoform. Mol. Endocrinol. 8:1347-1360.
62. Sarup, J. C., K. V. S. Rao, and C. F. Fox. 1988. Decreased progesterone binding and attenuated progesterone action in cultured human breast carcinoma cells treated with epidermal growth factor. Cancer Res. 48:50711-55078.
63. Sepp-Lorenzino, L., I. Eberhard, Z. Ma, C. Cho, H. Serve, F. Liu, N. Rosen, and R. Lupu. 1996. Signal transduction pathways induced by heregulin in MDA-MB-453 breast cancer cells. Oncogene 12:1679-1687.
64. Shen, T., K. B. Horwitz, and C. A. Lange. 2001. Transcriptional hyperactivity of human progesterone receptors is coupled to their ligand-dependent down-regulation by mitogen-activated protein kinase-dependent phosphorylation of serine 294. Mol. Cell. Biol. 21:6122-6131.
65. Shyamala, G., W. Schneider, and W. Schott. 1990. Developmental regulation of murine mammary progesterone receptor gene expression. Endocrinology 126:2882-2889.
66. Takimoto, G. S., A. R. Hovland, D. M. Tasset, M. Y. Melville, L. Tung, and K. B. Horwitz. 1996. Role of phosphorylation in DNA binding and transcriptional functions of human progesterone receptors. J. Biol. Chem. 271:13308-13316.
67. Takimoto, G. S., D. M. Tasset, A. C. Eppert, and K. B. Horwitz. 1992. Hormone-induced progesterone receptor phosphorylation consists of sequential DNA-independent and DNA-dependent stages: analysis with zinc finger mutants and the progesterone antagonist ZK98299. Proc. Natl. Acad. Sci. USA 89:3050-3054.
68. Tzahar, E., H. Waterman, X. Chen, G. Levkowitz, D. Karunagaran, S. Lavi, B. J. Ratzkin, and Y. Yarden. 1996. A hierarchical network of interreceptor interactions determines signal transduction by Neu differentiation factor/neuregulin and epidermal growth factor. Mol. Cell. Biol. 16:5276-5287.
69. Ullrich, A., L. Coussens, J. S. Hayflick, T. J. Dull, A. Gray, A. W. Tam, J. Lee, Y. Yarden, T. A. Liebermann, J. Schlessinger, J. Downward, E. L. V. Mayes, N. Whittle, M. D. Waterfield, and P. H. Seeburh. 1984. Human epidermal growth factor receptor cDNA sequence and aberrant expression of the amplified gene in A431 epidermoid carcinoma cells. Nature 309:418-425.
70. Wei, L. L., N. L. Krett, M. D. Francis, D. F. Gordon, W. M. Wood, B. W. O'Malley, and K. B. Horwitz. 1988. Multiple human progesterone receptor messenger ribonucleic acids and their autoregulation by progestin agonist and antagonists in breast cancer cells. Mol. Endocrinol. 2:62-72.
71. Wei, L. L., P. L. Sheridan, N. L. Krett, M. D. Francis, D. O. Toft, D. P. Edwards, and K. B. Horwitz. 1987. Immunologic analysis of human breast cancer progesterone receptors: structure, phosphorylation, and processing. Biochemistry 26:6262-6272.
72. Weigel, N. L. 1996. Steroid hormone receptors and their regulation by phosphorylation. Biochem. J. 319:657-667.
73. Yamamoto, T., S. Ikawa, and T. Akiyama. 1986. An erbB-related gene, c-erbB-2, encodes a possible receptor protein similar to the epidermoid growth factor receptor. Nature 319:230-234.
74. Zhang, Y., C. A. Beck, A. Poletti, D. P. Edwards, and N. L. Weigel. 1994. Identification of phosphorylation sites unique to the B form of human progesterone receptor. J. Biol. Chem. 269:31034-31040.
75. Zhang, Y., C. A. Beck, A. Poletti, D. P. Edwards, and N. L. Weigel. 1995. Identification of a group of Ser-Pro motif hormone-inducible phosphorylation sites in the human progesterone receptor. Mol. Endocrinol. 9:1029-1040.
76. Zhang, Y., C. A. Beck, A. Poletti, J. P. Clement IV, P. Prendergast, T. Yip, T. W. Hutchens, D. P. Edwards, and N. L. Weigel. 1997. Phosphorylation of human progesterone receptor by cyclin-dependent kinase 2 on three sites that are authentic basal phosphorylation sites in vivo. Mol. Endocrinol. 11:823-832.
77. Zhang, Y., W. Bai, V. E. Allgood, and N. L. Weigel. 1994. Multiple signaling pathways activate the chicken progesterone receptor. Mol. Endocrinol. 8:577-584.