Progesterone promotes focal adhesion formation and migration in breast cancer cells through induction of protease-activated receptor-1

Journal of Endocrinology

Volumn 214, Issue 2, 2012, Pages 165-175

  Diaz, Jorge ^a,e   Aranda, Evelyn ^a   Henriquez, Soledad ^a   Quezada, Marisol ^a   Espinoza, Estefanía ^a   Bravo, Maria Loreto ^a   Oliva, Bárbara ^a   Lange, Soledad ^b   Villalon, Manuel ^a   Jones, Marius ^c   Brosens, Jan J ^c   Kato, Sumie ^a,b   Cuello, Mauricio A ^b   Knutson, Todd P ^d   Lange, Carol A ^d   Leyton, Lisette ^e   Owen, Gareth I ^a,f  

^a Center for Advanced Studies in Ecology and Biodiversity   (Chile)

^b PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^c UNIVERSITY OF WARWICK   (United Kingdom)

^d UNIVERSITY OF MINNESOTA   (United States)

^e UNIVERSITY OF CHILE   (Chile)

^f Biomedical Research Consortium (BMRC) Chile   (Chile)

Author keywords

[No Author keywords available]

Indexed keywords

FOCAL ADHESION KINASE; MESSENGER RNA; PROGESTERONE; PROGESTERONE RECEPTOR; PROLINE RICH PROTEIN; PROTEINASE ACTIVATED RECEPTOR 1;

ARTICLE; BLOOD CLOTTING; BREAST CANCER; CANCER CELL; CANCER CELL CULTURE; CANCER RISK; CELL ADHESION; CELL MIGRATION; CONTROLLED STUDY; ENZYME INDUCTION; FOCAL ADHESION; GENE EXPRESSION; HUMAN; HUMAN TISSUE; PRIORITY JOURNAL; PROLINE RICH PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; UPREGULATION;

BREAST NEOPLASMS; CARCINOMA; CELL LINE, TUMOR; CELL MOVEMENT; DRUG EVALUATION, PRECLINICAL; FEMALE; FOCAL ADHESIONS; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, ERBB-1; HUMANS; MAP KINASE KINASE 1; POSTMENOPAUSE; PROGESTERONE; PROTO-ONCOGENE PROTEINS PP60(C-SRC); RECEPTOR, PAR-1; SIGNAL TRANSDUCTION; UP-REGULATION;

EID: 84866289319     PISSN: 00220795     EISSN: 14796805     Source Type: Journal    
DOI: 10.1530/JOE-11-0310     Document Type: Article

References (59)

1. Abreu MT, Hughes WE, Mele K, Lyons RJ, Rickwood D, Browne BC, Bennett HL, Vallotton P, Brummer T and Daly RJ. 2011 Gab2 regulates cytoskeletal organization and migration of mammary epithelial cells by modulating RhoA activation. Molecular Biology of the Cell 22 105-116.
2. Albrektsen T, Sorensen BB, Hjorto GM, Fleckner J, Rao LV and Petersen LC. 2007 Transcriptional program induced by factor VIIa-tissue factor, PAR1 and PAR2 in MDA-MB-231 cells. Journal of Thrombosis and Haemostasis 5 1588-1597.
3. Avalos AM, Arthur WT, Schneider P, Quest AF, Burridge K and Leyton L. 2004 Aggregation of integrins and RhoA activation are required for Thy-1-induced morphological changes in astrocytes. Journal of Biological Chemistry 279 39139-39145.
4. Beral V. 2003 Breast cancer and hormone-replacement therapy in the Million Women Study. Lancet 362 419-427.
5. Boonyaratanakornkit V, Scott MP, Ribon V, Sherman L, Anderson SM, Maller JL, Miller WT and Edwards DP. 2001 Progesterone receptor contains a proline-rich motif that directly interacts with SH3 domains and activates c-Src family tyrosine kinases. Molecular Cell 8 269-280.
6. Bray JD, Jelinsky S, Ghatge R, Bray JA, Tunkey C, Saraf K, Jacobsen BM, Richer JK, Brown EL, Winneker RC et al. 2005 Quantitative analysis of gene regulation by seven clinically relevant progestins suggests a highly similar mechanism of action through progesterone receptors in T47D breast cancer cells. Journal of Steroid Biochemistry and Molecular Biology 97 328-341.
7. Burridge K and Chrzanowska-Wodnicka M. 1996 Focal adhesions, contractility, and signaling. Annual Review of Cell and Developmental Biology 12 463-518.
8. Carragher NO and Frame MC. 2004 Focal adhesion and actin dynamics: a place where kinases and proteases meet to promote invasion. Trends in Cell Biology 14 241-249.
9. Carvajal A, Espinoza N, Kato S, Pinto M, Sadarangani A, Monso C, Aranda E, Villalon M, Richer JK, Horwitz KB et al. 2005 Progesterone pre-treatment potentiates EGF pathway signaling in the breast cancer cell line ZR-75. Breast Cancer Research and Treatment 94 171-183.
10. Critchley DR. 2000 Focal adhesions - the cytoskeletal connection. Current Opinion in Cell Biology 12 133-139.
11. Critchley HO, Kelly RW, Baird DT and Brenner RM. 2006 Regulation of human endometrial function: mechanisms relevant to uterine bleeding. Reproductive Biology and Endocrinology 4 (Suppl 1) S5.
12. Daniel AR and Lange CA. 2009 Protein kinases mediate ligand-independent derepression of sumoylated progesterone receptors in breast cancer cells. PNAS 106 14287-14292.
13. Daniel AR, Faivre EJ and Lange CA. 2007 Phosphorylation-dependent antagonism of sumoylation derepresses progesterone receptor action in breast cancer cells. Molecular Endocrinology 21 2890-2906.
14. Duarte M, Kolev V, Soldi R, Kirov A, Graziani I, Oliveira SM, Kacer D, Friesel R, Maciag T and Prudovsky I. 2006 Thrombin induces rapid PAR1-mediated non-classical FGF1 release. Biochemical and Biophysical Research Communications 350 604-609.
15. Engel LW, Young NA, Tralka TS, Lippman ME, O'Brien SJ and Joyce MJ. 1978 Establishment and characterization of three new continuous cell lines derived from human breast carcinomas. Cancer Research 38 3352-3364.
16. Even-Ram S, Uziely B, Cohen P, Grisaru-Granovsky S, Maoz M, Ginzburg Y, Reich R, Vlodavsky I and Bar-Shavit R. 1998 Thrombin receptor overexpression in malignant and physiological invasion processes. Nature Medicine 4 909-914.
17. Even-Ram SC, Maoz M, Pokroy E, Reich R, Katz BZ, Gutwein P, Altevogt P and Bar-Shavit R. 2001 Tumor cell invasion is promoted by activation of protease activated receptor-1 in cooperation with the alpha vbeta 5 integrin. Journal of Biological Chemistry 276 10952-10962.
18. Faivre EJ and Lange CA. 2007 Progesterone receptors upregulate Wnt-1 to induce epidermal growth factor receptor transactivation and c-Srcdependent sustained activation of Erk1/2 mitogen-activated protein kinase in breast cancer cells. Molecular and Cellular Biology 27 466-480.
19. Faivre E, Skildum A, Pierson-Mullany L and Lange CA. 2005 Integration of progesterone receptor mediated rapid signaling and nuclear actions in breast cancer cell models: Role of mitogen-activated protein kinases and cell cycle regulators. Steroids 70 418-426.
20. Faivre EJ, Daniel AR, Hillard CJ and Lange CA. 2008 Progesterone receptor rapid signaling mediates serine 345 phosphorylation and tethering to specificity protein 1 transcription factors. Molecular Endocrinology 22 823-837.
21. Fu XD, Giretti MS, Baldacci C, Garibaldi S, Flamini M, Sanchez AM, Gadducci A, Genazzani AR and Simoncini T. 2008 Extra-nuclear signaling of progesterone receptor to breast cancer cell movement and invasion through the actin cytoskeleton. PLoS ONE 3 e2790.
22. Grisaru-Granovsky S, Salah Z, Maoz M, Pruss D, Beller U and Bar-Shavit R. 2005 Differential expression of protease activated receptor 1 (Par1) and pY397FAK in benign and malignant human ovarian tissue samples. International Journal of Cancer 113 372-378.
23. Guan JL. 2010 Integrin signaling through FAK in the regulation of mammary stem cells and breast cancer. IUBMB Life 62 268-276.
24. Hague S, Oehler MK, MacKenzie IZ, Bicknell R and Rees MC. 2002 Protease activated receptor-1 is down regulated by levonorgestrel in endometrial stromal cells. Angiogenesis 5 93-98.
25. Henriquez S, Calderon C, Quezada M, Oliva B, Bravo ML, Aranda E, Kato S, Cuello MA, Gutierrez J, Quest AF et al. 2011 Progesterone utilizes distinct membrane pools of tissue factor to increase coagulation and invasion and these effects are inhibited by TFPI. Journal of Cellular Physiology 226 3278-3285.
26. Herkert O, Kuhl H, Sandow J, Busse R and Schini-Kerth VB. 2001 Sex steroids used in hormonal treatment increase vascular procoagulant activity by inducing thrombin receptor (PAR-1) expression: role of the glucocorticoid receptor. Circulation 104 2826-2831.
27. Hirano K. 2007 The roles of proteinase-activated receptors in the vascular physiology and pathophysiology. Arteriosclerosis, Thrombosis, and Vascular Biology 27 27-36.
28. Horwitz KB, Mockus MB and Lessey BA 1982 Variant T47D human breast cancer cells with high progesterone-receptor levels despite estrogen and antiestrogen resistance. Cell 28 633-642.
29. Horwitz KB, Sheridan PL, Wei LL and Krett NL 1990 Human progesterone receptors: synthesis, structure, and phosphorylation. Progress in Clinical and Biological Research 322 41-52.
30. Kato S, Pinto M, Carvajal A, Espinoza N, Monso C, Bravo L, Villalon M, Cuello M, Quest AF, Suenaga A et al. 2005a Tissue factor is regulated by epidermal growth factor in normal and malignant human endometrial epithelial cells. Thrombosis and Haemostasis 94 444-453.
31. Kato S, Pinto M, Carvajal A, Espinoza N,Monso C, Sadarangani A, VillalonM, Brosens JJ,White JO, Richer JK et al. 2005b Progesterone increases tissue factor gene expression, procoagulant activity, and invasion in the breast cancer cell line ZR-75-1. Journal of Clinical Endocrinology and Metabolism 90 1181-1188.
32. Kelly P, Stemmle LN, Madden JF, Fields TA, Daaka Y and Casey PJ 2006 A role for the G12 family of heterotrimeric G proteins in prostate cancer invasion. Journal of Biological Chemistry 281 26483-26490.
33. Knutson TP, Daniel AR, Fan D, Silverstein KAT, Covington KR, Fuqua SAW and Lange CA 2012 Phosphorylated and SUMO-deficient progesterone receptors drive proliferative gene signatures during breast cancer progression. Breast Cancer Research 14 R95.
34. Landis RC 2007 Protease activated receptors: clinical relevance to hemostasis and inflammation. Hematology/Oncology Clinics of North America 21 103-113.
35. Lange CA 2008 Integration of progesterone receptor action with rapid signaling events in breast cancer models. Journal of Steroid Biochemistry and Molecular Biology 108 203-212.
36. Lange CA, Shen T and Horwitz KB 2000 Phosphorylation of human progesterone receptors at serine-294 by mitogen-activated protein kinase signals their degradation by the 26S proteasome. PNAS 97 1032-1037.
37. Leger AJ, Covic L and Kuliopulos A 2006 Protease-activated receptors in cardiovascular diseases. Circulation 114 1070-1077.
38. Leung T, Chen XQ, Manser E and Lim L 1996 The p160 RhoA-binding kinase ROK alpha is a member of a kinase family and is involved in the reorganization of the cytoskeleton. Molecular and Cellular Biology 16 5313-5327.
39. Lin VC, Ng EH, Aw SE, Tan MG and Bay BH 2000 Progesterone induces focal adhesion in breast cancer cells MDA-MB-231 transfected with progesterone receptor complementary DNA. Molecular Endocrinology 14 348-358.
40. Maragoudakis ME, Tsopanoglou NE, Andriopoulou P and Maragoudakis MM 2000 Effects of thrombin/thrombosis in angiogenesis and tumour progression. Matrix Biology 19 345-351.
41. Mitchell SE, Robinson JJ, King ME and Williams LM 2005 Proteinaseactivated receptors in ovine cervical function. Reproduction, Fertility, and Development 17 693-699.
42. Nguyen QD, Faivre S, Bruyneel E, Rivat C, Seto M, Endo T, Mareel M, Emami S and Gespach C 2002 RhoA- and RhoD-dependent regulatory switch of Galpha subunit signaling by PAR-1 receptors in cellular invasion. FASEB Journal 16 565-576.
43. Ossovskaya VS and Bunnett NW 2004 Protease-activated receptors: contribution to physiology and disease. Physiological Reviews 84 579-621.
44. Pellegrin S and Mellor H 2007 Actin stress fibres. Journal of Cell Science 120 3491-3499.
45. Pierson-Mullany LK and Lange CA 2004 Phosphorylation of progesterone receptor serine 400 mediates ligand-independent transcriptional activity in response to activation of cyclin-dependent protein kinase 2. Molecular and Cellular Biology 24 10542-10557.
46. Quezada MDJ,Henriquez S, Bravo ML, Aranda E, Oliva B, VillalonM, Kato S, Cuello MA, Brosens JJ, Lange CA et al. 2010 2-Methoxyestradiol inhibits progesterone mediated tissue factor expression and activity in breast cancer cells. Hormones and Cancer 1 117-126.
47. Rhodes DR, Yu J, Shanker K, Deshpande N, Varambally R, Ghosh D, Barrette T, Pandey A and Chinnaiyan AM 2004 ONCOMINE: a cancer microarray database and integrated data-mining platform. Neoplasia 6 1-6.
48. Rhodes DR, Kalyana-Sundaram S, Mahavisno V, Varambally R, Yu J, Briggs BB, Barrette TR, Anstet MJ, Kincead-Beal C, Kulkarni P et al. 2007 Oncomine 3.0: genes, pathways, and networks in a collection of 18,000 cancer gene expression profiles. Neoplasia 9 166-180.
49. Rickles FR 2006 Mechanisms of cancer-induced thrombosis in cancer. Pathophysiology of Haemostasis and Thrombosis 35 103-110.
50. Ruf W and Mueller BM 2006 Thrombin generation and the pathogenesis of cancer. Seminars in Thrombosis and Hemostasis 32 (Suppl 1) 61-68.
51. Sartorius CA, Groshong SD, Miller LA, Powell RL, Tung L, Takimoto GS and Horwitz KB 1994 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 Research 54 3868-3877.
52. Schaller MD 2008 Calcium-dependent Pyk2 activation: a role for calmodulin? Biochemical Journal 410 e3-e4.
53. Schaller MD, Borgman CA, Cobb BS, Vines RR, Reynolds AB and Parsons JT 1992 pp125FAK a structurally distinctive protein-tyrosine kinase associated with focal adhesions. PNAS 89 5192-5196.
54. Tellez C and Bar-Eli M 2003 Role and regulation of the thrombin receptor (PAR-1) in human melanoma. Oncogene 22 3130-3137.
55. Turm H, Maoz M, Katz V, Yin YJ, Offermanns S and Bar-Shavit R 2010 Protease-activated receptor-1 (PAR1) acts via a novel Galpha13-dishevelled axis to stabilize beta-catenin levels. Journal of Biological Chemistry 285 15137- 15148.
56. Uusitalo-Jarvinen H, Kurokawa T, Mueller BM, Andrade-Gordon P, Friedlander M and Ruf W 2007 Role of protease activated receptor 1 and 2 signaling in hypoxia-induced angiogenesis. Arteriosclerosis, Thrombosis, and Vascular Biology 27 1456-1462.
57. Yin YJ, Salah Z, Grisaru-Granovsky S, Cohen I, Even-Ram SC, Maoz M, Uziely B, Peretz T and Bar-Shavit R 2003 Human protease-activated receptor 1 expression in malignant epithelia: a role in invasiveness. Arteriosclerosis, Thrombosis, and Vascular Biology 23 940-944.
58. Yuan TC and Lin MF 2004 Protease-activated receptor 1: a role in prostate cancer metastasis. Clinical Prostate Cancer 3 189-191.
59. Zhao J and Guan JL 2009 Signal transduction by focal adhesion kinase in cancer. Cancer Metastasis Reviews 28 35-49.