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PMID: 9524123 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Activation of the Src/p21ras/Erk pathway by progesterone receptor via cross-talk with estrogen receptor.

The EMBO journal ·Vol. 17 ·No. 7 ·1998-04-01 ·Pages 2008-18

Migliaccio A, Piccolo D, Castoria G, Di Domenico M, Bilancio A, Lombardi M, Gong W, Beato M, Auricchio F

Abstract

The molecular mechanisms by which ovarian hormones stimulate growth of breast tumors are unclear. It has been reported previously that estrogens activate the signal-transducing Src/p21(ras)/Erk pathway in human breast cancer cells via an interaction of estrogen receptor (ER) with c-Src. We now show that progestins stimulate human breast cancer T47D cell proliferation and induce a similar rapid and transient activation of the pathway which, surprisingly, is blocked not only by anti-progestins but also by anti-estrogens. In Cos-7 cells transfected with the B isoform of progesterone receptor (PRB), progestin activation of the MAP kinase pathway depends on co-transfection of ER. A transcriptionally inactive PRB mutant also activates the signaling pathway, demonstrating that this activity is independent of transcriptional effects. PRB does not interact with c-Src but associates via the N-terminal 168 amino acids with ER. This association is required for the signaling pathway activation by progestins. We propose that ER transmits to the Src/p21(ras)/Erk pathway signals received from the agonist-activated PRB. These findings reveal a hitherto unrecognized cross-talk between ovarian hormones which could be crucial for their growth-promoting effects on cancer cells.

MeSH Terms
Animals Breast Neoplasms/metabolism COS Cells CSK Tyrosine-Protein Kinase Carcinoma/metabolism Enzyme Activation Enzyme Inhibitors/pharmacology Epidermal Growth Factor/pharmacology Estradiol/pharmacology Gene Expression Regulation Guanosine Triphosphate/metabolism Hormone Antagonists/pharmacology Humans Mitogen-Activated Protein Kinase 1/physiology Point Mutation Promegestone/pharmacology Protein-Tyrosine Kinases/antagonists & inhibitors,metabolism Proto-Oncogene Proteins p21(ras)/metabolism Receptors, Estrogen/genetics,metabolism Receptors, Progesterone/genetics,metabolism Signal Transduction/physiology Tamoxifen/pharmacology Transcriptional Activation Tumor Cells, Cultured src-Family Kinases
Chemicals
Enzyme Inhibitors Hormone Antagonists Receptors, Estrogen Receptors, Progesterone progesterone receptor B Tamoxifen Estradiol Epidermal Growth Factor Guanosine Triphosphate Promegestone Protein-Tyrosine Kinases CSK Tyrosine-Protein Kinase src-Family Kinases CSK protein, human Mitogen-Activated Protein Kinase 1 HRAS protein, human Proto-Oncogene Proteins p21(ras)
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Migliaccio A
Istituto di Patologia Generale e Oncologia, Facoltà di Medicina e Chirurgia, II Università di Napoli, Largo S.Aniello a Caponapoli, 2, 80138 Napoli, Italy.
Piccolo D
Castoria G
Di Domenico M
Bilancio A
Lombardi M
Gong W
Beato M
Auricchio F
References (65)
65 references, click to expand
  1. Progesterone and 17 alpha-hydroxyprogesterone. Novel stimulators of calcium influx in human sperm.
    J Biol Chem. 1990 Jan 25;265(3):1376-80 PMID: 2104840
  2. Two distinct estrogen-regulated promoters generate transcripts encoding the two functionally different human progesterone receptor forms A and B.
    EMBO J. 1990 May;9(5):1603-14 PMID: 2328727
  3. Progestin regulation of cellular proliferation.
    Endocr Rev. 1990 May;11(2):266-301 PMID: 2114281
  4. Use and specificity of genistein as inhibitor of protein-tyrosine kinases.
    Methods Enzymol. 1991;201:362-70 PMID: 1658553
  5. Dopaminergic and ligand-independent activation of steroid hormone receptors.
    Science. 1991 Dec 13;254(5038):1636-9 PMID: 1749936
  6. Coupling of dual signaling pathways: epidermal growth factor action involves the estrogen receptor.
    Proc Natl Acad Sci U S A. 1992 May 15;89(10):4658-62 PMID: 1584801
  7. Growth factor signaling by receptor tyrosine kinases.
    Neuron. 1992 Sep;9(3):383-91 PMID: 1326293
  8. Growth factor, steroid, and steroid antagonist regulation of cyclin gene expression associated with changes in T-47D human breast cancer cell cycle progression.
    Mol Cell Biol. 1993 Jun;13(6):3577-87 PMID: 8497271
  9. Raf-1 protein kinase is important for progesterone-induced Xenopus oocyte maturation and acts downstream of mos.
    Mol Cell Biol. 1993 Jul;13(7):4197-202 PMID: 8321223
  10. The mitogen-activated protein kinase signal transduction pathway.
    J Biol Chem. 1993 Jul 15;268(20):14553-6 PMID: 8325833
  11. Estrogen regulation of proto-oncogenes coding for nuclear proteins.
    Crit Rev Oncog. 1993;4(4):361-88 PMID: 8353138
  12. How receptor tyrosine kinases activate Ras.
    Trends Biochem Sci. 1993 Aug;18(8):273-5 PMID: 8236435
  13. Alteration of reproductive function but not prenatal sexual development after insertional disruption of the mouse estrogen receptor gene.
    Proc Natl Acad Sci U S A. 1993 Dec 1;90(23):11162-6 PMID: 8248223
  14. Activation of the c-Src tyrosine kinase is required for the induction of mammary tumors in transgenic mice.
    Genes Dev. 1994 Jan;8(1):23-32 PMID: 7507074
  15. Oncogenic activity of cyclin D1 revealed through cooperation with Ha-ras: link between cell cycle control and malignant transformation.
    Oncogene. 1994 Jan;9(1):323-6 PMID: 8302597
  16. Inducible regulatory elements in the human cyclin D1 promoter.
    Oncogene. 1994 Apr;9(4):1295-304 PMID: 8134134
  17. JNK1: a protein kinase stimulated by UV light and Ha-Ras that binds and phosphorylates the c-Jun activation domain.
    Cell. 1994 Mar 25;76(6):1025-37 PMID: 8137421
  18. New T47D breast cancer cell lines for the independent study of progesterone B- and A-receptors: only antiprogestin-occupied B-receptors are switched to transcriptional agonists by cAMP.
    Cancer Res. 1994 Jul 15;54(14):3868-77 PMID: 8033109
  19. Multiple signaling pathways activate the chicken progesterone receptor.
    Mol Endocrinol. 1994 May;8(5):577-84 PMID: 8058067
  20. Cyclin D1 induction in breast cancer cells shortens G1 and is sufficient for cells arrested in G1 to complete the cell cycle.
    Proc Natl Acad Sci U S A. 1994 Aug 16;91(17):8022-6 PMID: 8058751
  21. c-Fos transcriptional activity stimulated by H-Ras-activated protein kinase distinct from JNK and ERK.
    Nature. 1994 Sep 8;371(6493):171-5 PMID: 8072547
  22. Estrogen action via the cAMP signaling pathway: stimulation of adenylate cyclase and cAMP-regulated gene transcription.
    Proc Natl Acad Sci U S A. 1994 Aug 30;91(18):8517-21 PMID: 8078914
  23. Induction of cyclin D1 overexpression by activated ras.
    Oncogene. 1994 Dec;9(12):3627-33 PMID: 7970723
  24. Insights from the study of animals lacking functional estrogen receptor.
    Science. 1994 Dec 2;266(5190):1524-7 PMID: 7985022
  25. Membrane estrogen receptors identified by multiple antibody labeling and impeded-ligand binding.
    FASEB J. 1995 Mar;9(5):404-10 PMID: 7896011
  26. Nongenomic steroid action: independent targeting of a plasma membrane calcium channel and a tyrosine kinase.
    Biochem Biophys Res Commun. 1995 May 16;210(2):518-23 PMID: 7755629
  27. The role of estradiol receptor in the proliferative activity of vanadate on MCF-7 cells.
    Cell Growth Differ. 1995 Feb;6(2):105-13 PMID: 7756169
  28. HER-2 tyrosine kinase pathway targets estrogen receptor and promotes hormone-independent growth in human breast cancer cells.
    Oncogene. 1995 Jun 15;10(12):2435-46 PMID: 7784095
  29. Cyclin D1 provides a link between development and oncogenesis in the retina and breast.
    Cell. 1995 Aug 25;82(4):621-30 PMID: 7664341
  30. Transforming p21ras mutants and c-Ets-2 activate the cyclin D1 promoter through distinguishable regions.
    J Biol Chem. 1995 Oct 6;270(40):23589-97 PMID: 7559524
  31. Mice lacking cyclin D1 are small and show defects in eye and mammary gland development.
    Genes Dev. 1995 Oct 1;9(19):2364-72 PMID: 7557388
  32. Mice lacking progesterone receptor exhibit pleiotropic reproductive abnormalities.
    Genes Dev. 1995 Sep 15;9(18):2266-78 PMID: 7557380
  33. Expression of the cyclin-dependent kinase inhibitors p16INK4, p15INK4B and p21WAF1/CIP1 in human breast cancer.
    Int J Cancer. 1995 Nov 15;63(4):584-91 PMID: 7591270
  34. Activation of the estrogen receptor through phosphorylation by mitogen-activated protein kinase.
    Science. 1995 Dec 1;270(5241):1491-4 PMID: 7491495
  35. Steroid hormone receptors: many actors in search of a plot.
    Cell. 1995 Dec 15;83(6):851-7 PMID: 8521509
  36. Growth factors in breast cancer.
    Endocr Rev. 1995 Oct;16(5):559-89 PMID: 8529572
  37. Discovery of a novel, potent, and Src family-selective tyrosine kinase inhibitor. Study of Lck- and FynT-dependent T cell activation.
    J Biol Chem. 1996 Jan 12;271(2):695-701 PMID: 8557675
  38. Tyrosine kinase/p21ras/MAP-kinase pathway activation by estradiol-receptor complex in MCF-7 cells.
    EMBO J. 1996 Mar 15;15(6):1292-300 PMID: 8635462
  39. 17beta-Estradiol induces cyclin D1 gene transcription, p36D1-p34cdk4 complex activation and p105Rb phosphorylation during mitogenic stimulation of G(1)-arrested human breast cancer cells.
    Oncogene. 1996 Jun 6;12(11):2315-24 PMID: 8649771
  40. Cyclin D1 expression is regulated positively by the p42/p44MAPK and negatively by the p38/HOGMAPK pathway.
    J Biol Chem. 1996 Aug 23;271(34):20608-16 PMID: 8702807
  41. Estradiol activation of human colon carcinoma-derived Caco-2 cell growth.
    Cancer Res. 1996 Oct 1;56(19):4516-21 PMID: 8813150
  42. Convergence of mitogenic signalling cascades from diverse classes of receptors at the cyclin D-cyclin-dependent kinase-pRb-controlled G1 checkpoint.
    Mol Cell Biol. 1996 Dec;16(12):6917-25 PMID: 8943347
  43. Estrogen-induced activation of Cdk4 and Cdk2 during G1-S phase progression is accompanied by increased cyclin D1 expression and decreased cyclin-dependent kinase inhibitor association with cyclin E-Cdk2.
    J Biol Chem. 1997 Apr 18;272(16):10882-94 PMID: 9099745
  44. Induction of cell proliferation in quiescent NIH 3T3 cells by oncogenic c-Raf-1.
    Mol Cell Biol. 1997 May;17(5):2576-86 PMID: 9111327
  45. Mammary gland development is mediated by both stromal and epithelial progesterone receptors.
    Mol Endocrinol. 1997 Jun;11(6):801-11 PMID: 9171243
  46. Crosslinking of progesterone receptor to DNA using tuneable nanosecond, picosecond and femtosecond UV laser pulses.
    Nucleic Acids Res. 1997 Jun 15;25(12):2478-84 PMID: 9171102
  47. Rapid activation of MAP kinase by estrogen in the bone cell line.
    Biochem Biophys Res Commun. 1997 Jun 9;235(1):99-102 PMID: 9196043
  48. Estrogen-dependent cyclin E-cdk2 activation through p21 redistribution.
    Mol Cell Biol. 1997 Jul;17(7):4059-69 PMID: 9199341
  49. Rapid membrane effects of steroids in neuroblastoma cells: effects of estrogen on mitogen activated protein kinase signalling cascade and c-fos immediate early gene transcription.
    Endocrinology. 1997 Sep;138(9):4030-3 PMID: 9275096
  50. Point mutation in the ligand-binding domain of the progesterone receptor generates a transdominant negative phenotype.
    Mol Endocrinol. 1997 Sep;11(10):1476-85 PMID: 9280063
  51. Effect of perinatal oestrogen on the pretreatment required for mouse mammary lobular formation in vitro.
    J Endocrinol. 1978 Apr;77(1):1-10 PMID: 641427
  52. Estrogens stimulate cell proliferation and induce secretory proteins in a human breast cancer cell line (T47D).
    J Clin Endocrinol Metab. 1982 Aug;55(2):276-83 PMID: 7045150
  53. Phenol red in tissue culture media is a weak estrogen: implications concerning the study of estrogen-responsive cells in culture.
    Proc Natl Acad Sci U S A. 1986 Apr;83(8):2496-500 PMID: 3458212
  54. Effect of progesterone on cell proliferation in the MXT mouse hormone-sensitive mammary neoplasm.
    J Natl Cancer Inst. 1986 Jul;77(1):173-8 PMID: 3459912
  55. Oral contraceptives and breast cancer. In vitro effect of contraceptive steroids on human mammary cell growth.
    Cancer. 1987 Jan 15;59(2):281-7 PMID: 3802015
  56. Effects of progestins on growth of experimental breast cancer in culture: interaction with estradiol and prolactin and involvement of the polyamine pathway.
    Cancer Res. 1987 Jun 15;47(12):3066-71 PMID: 3107802
  57. Progestin effects on growth in the human breast cancer cell line T-47D--possible therapeutic implications.
    Biochem Biophys Res Commun. 1987 Jun 15;145(2):706-11 PMID: 3593365
  58. Antiestrogens inhibit the mitogenic effect of growth factors on breast cancer cells in the total absence of estrogens.
    Biochem Biophys Res Commun. 1987 Aug 14;146(3):1502-8 PMID: 3304294
  59. Actions of a progestogen on human breast cancer cells: mechanisms of growth stimulation and inhibition.
    Eur J Cancer Clin Oncol. 1987 May;23(5):563-71 PMID: 2958286
  60. Functional domains of the human estrogen receptor.
    Cell. 1987 Dec 24;51(6):941-51 PMID: 3690665
  61. The product of the mos proto-oncogene as a candidate "initiator" for oocyte maturation.
    Science. 1989 Aug 11;245(4918):643-6 PMID: 2474853
  62. The cloned human oestrogen receptor contains a mutation which alters its hormone binding properties.
    EMBO J. 1989 Jul;8(7):1981-6 PMID: 2792078
  63. The human estrogen receptor has two independent nonacidic transcriptional activation functions.
    Cell. 1989 Nov 3;59(3):477-87 PMID: 2805068
  64. Mechanisms of growth control in normal and malignant breast epithelium.
    Recent Prog Horm Res. 1989;45:383-435; discussion 435-40 PMID: 2682845
  65. A functional cell surface type receptor is required for the early action of 1,25-dihydroxyvitamin D3 on the phosphoinositide metabolism in rat enterocytes.
    J Biol Chem. 1989 Dec 5;264(34):20403-6 PMID: 2555357
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
1998-04-01
Pages
2008-18
Language
English
Region
England
NLM ID
8208664
PMCID
PMC1170546
Subset
IM
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