Regulation of gene expression by progesterone in cancer cells: Effects on cyclin D1, EGFR and VEGF

Mini-Reviews in Medicinal Chemistry

Volumn 13, Issue 5, 2013, Pages 635-642

  Hernández Hernández, Olivia Tania ^a   Camacho Arroyo, Ignacio ^a  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

Cancer; Cyclin D1; Epidermal growth factor receptor; Progesterone; Progesterone receptor; Vascular endothelial growth factor

Indexed keywords

CALCIUM; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIN D1; EPIDERMAL GROWTH FACTOR RECEPTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MEDROXYPROGESTERONE ACETATE; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITIDE; PHOSPHATIDYLINOSITOL 3 KINASE; PROGESTERONE; PROTEIN KINASE B; PROTEIN KINASE C; PROTEIN TYROSINE KINASE; RAF PROTEIN; RAS PROTEIN; VASCULOTROPIN;

ANGIOGENESIS; BREAST CANCER; CELL CYCLE; CELL PROLIFERATION; DRUG MECHANISM; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION; HUMAN; METASTASIS; NEOPLASM; NONHUMAN; PROTEIN BINDING; REVIEW; SIGNAL TRANSDUCTION;

BREAST NEOPLASMS; CYCLIN D1; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; PROGESTERONE; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTORS, PROGESTERONE; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84877838121     PISSN: 13895575     EISSN: 18755607     Source Type: Journal    
DOI: 10.2174/1389557511313050002     Document Type: Review

References (57)

1. Bain, D.L.; Heneghan, A.F.; Connaghan-Jones, K.D.; Miura, M.T. Nuclear receptor structure: implications for function. Annu. Rev. Physiol., 2007, 69, 201-220.
2. Boonyaratanakornkit, V.; Bi, Y.; Rudd, M.; Edwards, D.P. The role and mechanism of progesterone receptor activation of extra-nuclear signaling pathways in regulating gene transcription and cell cycle progression. Steroids, 2008, 73(9-10), 922-928.
3. Faivre, E.J.; Daniel, A.R.; Hillard, C.J.; Lange, C.A. Progesterone receptor rapid signaling mediates serine 345 phosphorylation and tethering to specificity protein 1 transcription factors. Mol. Endocrinol., 2008, 22(4), 823-837.
4. Caldwell, J.D.; Suleman, F.; Chou, S.H.; Shapiro, R.A.; Herbert, Z.; Jirikowski, G.F. Emerging roles of steroid-binding globulins. Horm. Metab. Res., 2006, 38(4), 206-218.
5. Cabrera-Munoz, E.; Hernandez-Hernandez, O.T.; Camacho-Arroyo, I. Role of progesterone receptor in human astrocytomas growth. Curr. Top. Med. Chem., 2011, 11(13), 1663-1667.
6. Conneely, O.M.; Jericevic, B.M.; Lydon, J.P. Progesterone receptors in mammary gland development and tumorigenesis. J. Mammary Gland Biol. Neoplasia, 2003, 8(2), 205-214.
7. Chlebowski, R.T.; Hendrix, S.L.; Langer, R.D.; Stefanick, M.L.; Gass, M.; Lane, D.; Rodabough, R.J.; Gilligan, M.A.; Cyr MG, Thomson, C.A. Khandekar, J.; Petrovitch, H.; McTiernan, A. Influence of estrogen plus progestin on breast cancer and mammography in healthy postmenopausal women: the Women's Health Initiative Randomized Trial. Jama, 2003, 289(24), 3243-3253.
8. Edwards, D.P. Regulation of signal transduction pathways by estrogen and progesterone. Annu. Rev. Physiol., 2005, 67, 335-376.
9. Spicer, D.V.; Pike, M.C. Sex steroids and breast cancer prevention. J. Natl. Cancer Inst. Monogr., 1994, (16), 139-147.
10. Musgrove, E.A.; Sutherland, R.L. Steroids, growth factors, and cell cycle controls in breast cancer. Cancer Treat. Res., 1991, 53, 305-331.
11. Graham, J.D.; Clarke, C.L. Physiological action of progesterone in target tissues. Endocr. Rev., 1997, 18(4), 502-519.
12. Wu, J.; Richer, J.; Horwitz, K.B.; Hyder, S.M. Progestin-dependent induction of vascular endothelial growth factor in human breast cancer cells: preferential regulation by progesterone receptor B. Cancer Res., 2004, 64(6), 2238-2244.
13. Dressing, G.E.; Alyea, R.; Pang, Y.; Thomas, P. Membrane progesterone receptors (mPRs) mediate progestin induced antimorbidity in breast cancer cells and are expressed in human breast tumors. Horm. Cancer, 2012, 3(3), 101-112.
14. Peluso, J.J.; DeCerbo, J.; Lodde, V. Evidence for a genomic mechanism of action for progesterone receptor membrane component-1. Steroids, 2012, 77(10), 1007-1012.
15. Thomas, P. Characteristics of membrane progestin receptor alpha (mPRalpha) and progesterone membrane receptor component 1 (PGMRC1) and their roles in mediating rapid progestin actions. Front. Neuroendocrinol., 2008, 29(2), 292-312.
16. Zuo, L.; Li, W.; You, S. Progesterone reverses the mesenchymal phenotypes of basal phenotype breast cancer cells via a membrane progesterone receptor mediated pathway. Breast Cancer Res, 2010, 12(3), R34.
17. Causey, M.W.; Huston, L.J.; Harold, D.M.; Charaba, C.J.; Ippolito, D.L.; Hoffer, Z.S.; Brown, T.A.; Stallings, J.D. Transcriptionalanalysis of novel hormone receptors PGRMC1 and PGRMC2 as potential biomarkers of breast adenocarcinoma staging. J Surg Res, 2011, 171(2), 615-622.
18. Kastner, P.; Krust, A.; Turcotte, B.; Stropp, U.; Tora, L.; Gronemeyer, H.; Chambon, P. Two distinct estrogen-regulated promoters generate transcripts encoding the two functionally different human progesterone receptor forms A and B. Embo. J., 1990, 9(5), 1603-1614.
19. Sartorius, C.A.; Melville, M.Y.; Hovland, A.R.; Tung, L.; Takimoto, G.S.; Horwitz, K.B. A third transactivation function (AF3) of human progesterone receptors located in the unique N-terminal segment of the B-isoform. Mol. Endocrinol., 1994, 8(10), 1347-1360.
20. Tung, L.; Mohamed, M.K.; Hoeffler, J.P.; Takimoto, G.S.; Horwitz, K.B. Antagonist-occupied human progesterone B-receptors activate transcription without binding to progesterone response elements and are dominantly inhibited by A-receptors. Mol. Endocrinol., 1993, 7(10), 1256-1265.
21. Cabrera-Munoz, E.; Hernandez-Hernandez, O.T.; Camacho-Arroyo I. Role of Estradiol and Progesterone in HIV susceptibility and diases progression Mini Rev. Med. Chem., 2012, 12(7), 1-6.
22. Faivre, E.J.; Lange, C.A. Progesterone receptors upregulate Wnt-1 to induce epidermal growth factor receptor transactivation and c-Src-dependent sustained activation of Erk1/2 mitogen-activated protein kinase in breast cancer cells. Mol. Cell. Biol., 2007, 27(2), 466-480.
23. Lange, C.A.; Shen, T.; Horwitz, K.B. Phosphorylation of human progesterone receptors at serine-294 by mitogen-activated protein kinase signals their degradation by the 26S proteasome. Proc. Natl. Acad. Sci. U S A, 2000, 97(3), 1032-1037.
24. Proietti, C.; Salatino, M.; Rosemblit, C.; Carnevale R.; Pecci, A.; Kornblihtt, A.R.; Molinolo, A.A.; Frahm, I.; Charreau, E.H.; Schillaci, R.; Elizalde, P.V. Progestins induce transcriptional activation of signal transducer and activator of transcription 3 (Stat3) via a Jak-and Src-dependent mechanism in breast cancer cells. Mol. Cell Biol., 2005, 25(12), 4826-4840.
25. Migliaccio, A.; Piccolo, D.; Castoria, G.; Di Domenico M.; Bilancio, A.; Lombardi, M.; Gong, W.; Beato, M.; Auricchio, F. Activation of the Src/p21ras/Erk pathway by progesterone receptor via cross-talk with estrogen receptor. Embo. J., 1998, 17(7), 2008-2018.
26. Boonyaratanakornkit, V.; Scott, M.P.; Ribon, V.; Sherman, L.; Anderson, S.M.; Maller, J.L.; Miller, W.T.; Edwards, D.P. Progesterone receptor contains a proline-rich motif that directly interacts with SH3 domains and activates c-Src family tyrosine kinases. Mol. Cell, 2001, 8(2), 269-280.
27. McGowan, E.M.; Russell, A.J.; Boonyaratanakornkit, V.; Saunders, D.N.; Lehrbach, G.M.; Sergio, C.M.; Musgrove, E.A.; Edwards, D.P.; Sutherland, R.L. Progestins reinitiate cell cycle progression in antiestrogen-arrested breast cancer cells through the B-isoform of progesterone receptor. Cancer Res., 2007, 67(18), 8942-8951.
28. McGowan, E.M.; Clarke, C.L. Effect of overexpression of progesterone receptor A on endogenous progestin-sensitive endpoints in breast cancer cells. Mol. Endocrinol., 1999, 13(10), 1657-1671.
29. Gonzalez-Aguero, G.; Ondarza, R.; Gamboa-Dominguez, A.; Cerbon, M.A.; Camacho-Arroyo, I. Progesterone receptor isoforms expression pattern in human astrocytomas. Brain Res. Bull, 2001, 56(1), 43-48.
30. Gonzalez-Aguero, G.; Gutierrez, A.A.; Gonzalez-Espinosa, D.; Solano, J.D.; Morales, R.; Gonzalez-Arenas, A.; Cabrera-Munoz, E.; Camacho-Arroyo, I. Progesterone effects on cell growth of U373 and D54 human astrocytoma cell lines. Endocrine, 2007, 32(2), 129-135.
31. Cabrera-Munoz, E.; Gonzalez-Arenas, A.; Saqui-Salces, M.; Camacho, J.; Larrea, F.; Garcia-Becerra, R.; Camacho-Arroyo, I. Regulation of progesterone receptor isoforms content in human astrocytoma cell lines. J. Steroid Biochem. Mol. Biol., 2009, 113(1-2), 80-84.
32. Moore, M.R.; Conover, J.L.; Franks, K.M. Progestin effects on long-term growth, death, and Bcl-xL in breast cancer cells. Biochem. Biophys. Res. Commun., 2000, 277(3), 650-654.
33. Thuneke, I.; Schulte, H.M.; Bamberger, A.M. Biphasic effect of medroxyprogesterone-acetate (MPA) treatment on proliferation and cyclin D1 gene transcription in T47D breast cancer cells. Breast Cancer Res. Treat., 2000, 63(3), 243-248.
34. Lew, D.J.; Dulic, V.; Reed, S.I. Isolation of three novel human cyclins by rescue of G1 cyclin (Cln) function in yeast. Cell, 1991, 66(6), 1197-1206.
35. Fu, M.; Wang, C.; Li, Z.; Sakamaki, T.; Pestell, R.G. Minireview: Cyclin D1: normal and abnormal functions. Endocrinology, 2004, 145(12), 5439-5447.
36. Hernandez-Hernandez, O.T.; Gonzalez-Garcia, T.K.; Camacho-Arroyo, I. Progesterone receptor and SRC-1 participate in the regulation of VEGF, EGFR and Cyclin D1 expression in human astrocytoma cell lines. J. Steroid Biochem. Mol Biol., 2012, 132, 127-134.
37. Musgrove, E.A.; Hamilton, J.A.; Lee, C.S.; Sweeney, K.J.; Watts, C.K.; Sutherland, R.L. 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, 13(6), 3577-3587.
38. Boonyaratanakornkit, V.; McGowan, E.; Sherman, L.; Mancini, M.A.; Cheskis, B.J.; Edwards, D.P. The role of extranuclear signaling actions of progesterone receptor in mediating progesterone regulation of gene expression and the cell cycle. Mol. Endocrinol., 2007, 21(2), 359-375.
39. Cicatiello, L.; Addeo, R.; Sasso, A.; Altucci, L.; Petrizzi, V.B.; Borgo, R.; Cancemi, M.; Caporali, S.; Caristi, S.; Scafoglio, C. Estrogens and progesterone promote persistent CCND1 gene activation during G1 by inducing transcriptional derepression via c-Jun/c-Fos/estrogen receptor (progesterone receptor) complex assembly to a distal regulatory element and recruitment of cyclin D1 to its own gene promoter. Mol. Cell Biol., 2004, 24(16), 7260-7274.
40. Giulianelli, S.; Vaque, J.P.; Soldati, R.; Wargon, V.; Vanzulli, S.I.; Martins, R.; Zeitlin, E.; Molinolo, A.A.; Helguero, L.A.; Lamb, C.A. Estrogen receptor alpha mediates progestin-induced mammary tumor growth by interacting with progesterone receptors at the cyclin D1/MYC promoters. Cancer Res., 2012, 72(9), 2416-2427.
41. Daniel, A.R.; Faivre, E.J.; Lange, C.A. Phosphorylation-dependent antagonism of sumoylation derepresses progesterone receptor action in breast cancer cells. Mol. Endocrinol., 2007, 21(12), 2890-2906.
42. Ashktorab, H.; Daremipouran, M.; Wilson, M.; Siddiqi, S.; Lee, E.L.; Rakhshani, N.; Malekzadeh, R.; Johnson, A.C.; Hewitt, S.M.; Smoot, D.T. Transactivation of the EGFR by AP-1 is induced by Helicobacter pylori in gastric cancer. Am. J. Gastroenterol., 2007, 102(10), 2135-2146.
43. Halatsch, M.E.; Schmidt, U.; Behnke-Mursch, J.; Unterberg, A.; Wirtz, C.R. Epidermal growth factor receptor inhibition for the treatment of glioblastoma multiforme and other malignant brain tumours. Cancer Treat. Rev., 2006, 32(2), 74-89.
44. Hudson, L.G.; Thompson, K.L.; Xu, J.; Gill, G.N. Identification and characterization of a regulated promoter element in the epidermal growth factor receptor gene. Proc. Natl. Acad. Sci. U S A, 1990, 87(19), 7536-7540.
45. Gee, J.M.; Harper, M.E.; Hutcheson, I.R.; Madden, T.A.; Barrow, D.; Knowlden, J.M.; McClelland, R.A.; Jordan, N.; Wakeling, A.E.; Nicholson, R.I. The antiepidermal growth factor receptor agent gefitinib (ZD1839/Iressa) improves antihormone response and prevents development of resistance in breast cancer in vitro. Endocrinology, 2003, 144(11), 5105-5117.
46. Kariagina, A.; Xie, J.; Leipprandt, J.R.; Haslam, S.Z. Amphiregulin mediates estrogen, progesterone, and EGFR signaling in the normal rat mammary gland and in hormone-dependent rat mammary cancers. Horm. Cancer, 2010, 1(5), 229-244.
47. Ferrara, N. Role of vascular endothelial growth factor in physiologic and pathologic angiogenesis: therapeutic implications. Semin. Oncol., 2002, 29(6 Suppl. 16), 10-14.
48. Bergers, G.; Benjamin, L.E. Tumorigenesis and the angiogenic switch. Nat. Rev. Cancer, 2003, 3(6), 401-410.
49. Mueller, M.D.; Vigne, J.L.; Pritts, E.A.; Chao, V.; Dreher, E.; Taylor, R.N. Progestins activate vascular endothelial growth factor gene transcription in endometrial adenocarcinoma cells. Fertil Steril, 2003, 79(2), 386-392.
50. Liang, Y.; Hyder, S.M. Proliferation of endothelial and tumor epithelial cells by progestin-induced vascular endothelial growth factor from human breast cancer cells: paracrine and autocrine effects. Endocrinology, 2005, 146(8), 3632-3641.
51. Tung, L., Abdel-Hafiz, H., Shen, T., Harvel, D.M., Nitao, L.K., Richer, J.K., Sartorius, C.A., Takimoto, G.S., Horwitz, K.B.Progesterone receptors (PR)-B and-A regulate transcription by different mechanisms: AF-3 exerts regulatory control over coactivator binding to PR-B. Mol. Endocrinol., 2006, 20(11), 2656-2670.
52. Tischer, E.; Mitchell, R.; Hartman, T.; Silva, M.; Gospodarowicz, D.; Fiddes, J.C.; Abraham, J.A. The human gene for vascular endothelial growth factor. Multiple protein forms are encoded through alternative exon splicing. J. Biol. Chem., 1991, 266(18), 11947-11954.
53. Neubauer, H.; Adam, G.; Seeger, H.; Mueck, A.O.; Solomayer, E., Wallwiener, D.; Cahill, M.A.; Fehm, T. Membrane-initiated effects of progesterone on proliferation and activation of VEGF in breast cancer cells. Climacteric 2009, 12(3), 230-239.
54. Lacroix, M.; Leclercq, G. Relevance of breast cancer cell lines as models for breast tumours: an update. Breast Cancer Res. Treat., 2004, 83(3), 249-289.
55. Charafe-Jauffret, E.; Ginestier, C.; Monville, F.; Finetti, P.; Adelaide, J.; Cervera, N.; Fekairi S.; Xerri L.; Jacquemier J.; Birnbaum D. Gene expression profiling of breast cell lines identifies potential new basal markers. Oncogene, 2006, 25(15), 2273-2284.
56. Sallinen, S.L.; Sallinen, P.K.; Kononen, J.T.; Syrjakoski, K.M.; Nupponen, N.N.; Rantala, I.S.; Helen, P.T.; Helin, H.J.; Haapasalo, H.K. Cyclin D1 expression in astrocytomas is associated with cell proliferation activity and patient prognosis. J. Pathol., 1999, 188(3), 89-293.
57. Godard, S.; Getz G.; Delorenzi, M.; Farmer, P.; Kobayashi, H.; Desbaillets, I.; Nozaki, M.; Diserens, A.C.; Hamou, M.F.; Dietrich, P.Y. Classification of human astrocytic gliomas on the basis of gene expression: a correlated group of genes with angiogenic activity emerges as a strong predictor of subtypes. Cancer Res., 2003, 63(20), 6613-6625.