Progesterone receptor isoforms A and B: New insights into the mechanism of progesterone resistance for the treatment of endometrial carcinoma

ecancermedicalscience

Volumn 7, Issue 1, 2013, Pages

  Shao, Ruijin ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

Animal model; Cell cell interaction; Endometrial carcinoma; Progesterone receptor isoforms; Progesterone resistance

Indexed keywords

PROGESTERONE; PROGESTERONE RECEPTOR A; PROGESTERONE RECEPTOR B;

CANCER HORMONE THERAPY; CARCINOMA CELL; DNA METHYLATION; ENDOMETRIUM CARCINOMA; ENDOMETRIUM CELL; HUMAN; NONHUMAN; REVIEW; TUMOR MICROENVIRONMENT;

EID: 84891958352     PISSN: None     EISSN: 17546605     Source Type: Journal    
DOI: 10.3332/ecancer.2013.381     Document Type: Review

References (49)

1. Yang S, Thiel KW and Leslie KK (2011) Progesterone: the ultimate endometrial tumor suppressor Trends Endocrinol Metab 22(4) 145-52 DOI: 10.1016/j.tem.2011.01.005 PMID: 21353793
2. Amant F, Moerman P, Neven P, Timmerman D, Van Limbergen E and Vergote I (2005) Endometrial cancer Lancet 366(9484) 491-505 DOI: 10.1016/S0140-6736(05) 67063-8 PMID: 16084259
3. Jemal A, Siegel R, Xu J and Ward E (2010) Cancer statistics, 2010 CA Cancer J Clin 60(5) 277-300 DOI: 10.3322/caac.20073 PMID: 20610543
4. Lee WL, Lee FK, Su WH, Tsui KH, Kuo CD, Hsieh SL, Wang PH (2012) Hormone therapy for younger patients with endometrial cancer Taiwanese J Obstet Gynecol 51(4) 495-505 DOI: 10.1016/j.tjog.2012.09.003
5. Setiawan VW, Yang HP, Pike MC, McCann SE, Yu H, Xiang YB, Wolk A, Wentzensen N, Weiss NS, Webb PM, et al (2013) Type I and II endometrial cancers: have they different risk factors? J Clin Oncol: Official Journal of the American Society of Clinical Oncology 31(20) 2607-18 DOI: 10.1200/JCO.2012.48. 2596
6. Horn LC, Meinel A, Handzel R and Einenkel J (2007) Histopathology of endometrial hyperplasia and endometrial carcinoma: an update Ann Diagn Pathol 11(4) 297-311 DOI: 10.1016/j.anndiagpath.2007.05.002 PMID: 17630117
7. Ushijima K, Yahata H, Yoshikawa H, Konishi I, Yasugi T, Saito T, Nakanishi T, Sasaki H, Saji F, Iwasaka T, et al (2007) Multicenter phase II study of fertility-sparing treatment with medroxyprogesterone acetate for endometrial carcinoma and atypical hyperplasia in young women J Clin Oncol: Official Journal of the American Society of Clinical Oncology 25(19) 2798-803 DOI: 10.1200/JCO.2006.08.8344
8. Yang S, Thiel KW, De Geest K and Leslie KK (2011) Endometrial cancer: reviving progesterone therapy in the molecular age Discov Med 12(64) 205-12 PMID: 21955848
9. Kim JJ, Kurita T and Bulun SE (2013) Progesterone action in endometrial cancer, endometriosis, uterine fibroids, and breast cancer Endocr Rev 34(1) 130-62 DOI: 10.1210/er.2012-1043 PMID: 23303565 PMCID: 3565104
10. Kim JJ and Chapman-Davis E (2010) Role of progesterone in endometrial cancer Semin Reprod Med 28(1) 81-90 DOI: 10.1055/s-0029-1242998 PMID: 20104432
11. Graham JD and Clarke CL (1997) Physiological action of progesterone in target tissues Endocr Rev 18(4) 502-19 DOI: 10.1210/er.18.4.502 PMID: 9267762
12. Wetendorf M and DeMayo FJ (2012) The progesterone receptor regulates implantation, decidualization, and glandular development via a complex paracrine signaling network Mol Cell Endocrinol 357(1-2) 108-18 DOI: 10.1016/j.mce.2011. 10.028 PMCID: 3443857
13. Kastner P, Krust A, Turcotte B, Stropp U, Tora L, Gronemeyer H and Chambon P (1990) Two distinct estrogen-regulated promoters generate transcripts encoding the two functionally different human progesterone receptor forms A and B EMBO J 9(5) 1603-14 PMID: 2328727 PMCID: 551856
14. Conneely OM, Mulac-Jericevic B, DeMayo F, Lydon JP and O'Malley BW (2002) Reproductive functions of progesterone receptors Recent Prog Horm Res 57 339-55 DOI: 10.1210/rp.57.1.339 PMID: 12017551
15. Shao R, Weijdegard B, Ljungstrom K, Friberg A, Zhu C, Wang X, Zhu Y, Fernandez-Rodriguez J, Egecioglu E, Rung E, et al (2006) Nuclear progesterone receptor A and B isoforms in mouse fallopian tube and uterus: implications for expression, regulation, and cellular function Am J Physiol Endocrinol Metab 291(1) E59-72 DOI: 10.1152/ajpendo.00582.2005 PMID: 16449295
16. Critchley HO and Saunders PT (2009) Hormone receptor dynamics in a receptive human endometrium. Reprod Sci 16(2) 191-9 DOI: 10.1177/ 1933719108331121 PMID: 19208787
17. Mote PA, Balleine RL, McGowan EM and Clarke CL (1999) Colocalization of progesterone receptors A and B by dual immunofluorescent histochemistry in human endometrium during the menstrual cycle J Clin Endocrinol Metab 84(8) 2963-71 DOI: 10.1210/jc.84.8.2963 PMID: 10443705
18. Shao R, Wang X, Weijdegard B, Norstrom A, Fernandez-Rodriguez J, Brannstrom M and Billig H (2012) Coordinate regulation of heterogeneous nuclear ribonucleoprotein dynamics by steroid hormones in the human Fallopian tube and endometrium in vivo and in vitro Am J Physiol Endocrinol Metab 302(10) E1269-82 DOI: 10.1152/ajpendo.00673.2011 PMID: 22436695
19. Sakaguchi H, Fujimoto J, Hong BL, Nakagawa Y and Tamaya T (2004) Drastic decrease of progesterone receptor form B but not A mRNA reflects poor patient prognosis in endometrial cancers Gynecol Oncol 93(2) 394-99 DOI: 10.1016/j.ygyno.2004.01.042 PMID: 15099952
20. Saito S, Ito K, Nagase S, Suzuki T, Akahira J, Okamura K, Yaegashi N and Sasano H (2006) Progesterone receptor isoforms as a prognostic marker in human endometrial carcinoma Cancer Sci 97(12) 1308-14 DOI: 10.1111/j.1349-7006.2006. 00332.x PMID: 16999816
21. Jongen V, Briet J, de Jong R, ten Hoor K, Boezen M, van der Zee A, Nijman H and Hollema H (2009) Expression of estrogen receptor-alpha and -beta and progesterone receptor-A and -B in a large cohort of patients with endometrioid endometrial cancer Gynecol Oncol 112(3) 537-42 DOI: 10.1016/j.ygyno.2008.10.032
22. Kumar NS, Richer J, Owen G, Litman E, Horwitz KB and Leslie KK (1998) Selective down-regulation of progesterone receptor isoform B in poorly differentiated human endometrial cancer cells: implications for unopposed estrogen action Cancer Res 58(9) 1860-5 PMID: 9581825
23. Arnett-Mansfield RL, DeFazio A, Mote PA and Clarke CL (2004) Subnuclear distribution of progesterone receptors A and B in normal and malignant endometrium J Clin Endocrinol Metab 89(3) 1429-1442. DOI: 10.1210/jc.2003-031111 PMID: 15001645
24. Miyamoto T, Watanabe J, Hata H, Jobo T, Kawaguchi M, Hattori M, Saito M and Kuramoto H (2004) Significance of progesterone receptor-A and -B expressions in endometrial adenocarcinoma J Steroid Biochem Mol Biol 92(3) 111-8 DOI: 10.1016/j.jsbmb.2004.07.007 PMID: 15555905
25. Mortel R, Zaino R and Satyaswaroop PG (1984) Heterogeneity and progesterone-receptor distribution in endometrial adenocarcinoma Cancer 53(1) 1136
26. Arnett-Mansfield RL, deFazio A, Wain GV, Jaworski RC, Byth K, Mote PA and Clarke CL (2001) Relative expression of progesterone receptors A and B in endometrioid cancers of the endometrium Cancer Res 61(11) 4576-82 PMID: 11389093
27. Xiong Y, Dowdy SC, Gonzalez Bosquet J, Zhao Y, Eberhardt NL, Podratz KC and Jiang SW (2005) Epigenetic-mediated upregulation of progesterone receptor B gene in endometrial cancer cell lines Gynecologic oncology 99(1) 135-41 DOI: 10.1016/j.ygyno.2005.05.035 PMID: 16024066
28. Sasaki M, Dharia A, Oh BR, Tanaka Y, Fujimoto S and Dahiya R (2001) Progesterone receptor B gene inactivation and CpG hypermethylation in human uterine endometrial cancer Cancer Res 61(1) 97-102 PMID: 11196205
29. Ren Y, Liu X, Ma D, Feng Y and Zhong N (2007) Down-regulation of the progesterone receptor by the methylation of progesterone receptor gene in endometrial cancer cells Cancer Genet Cytogenet 175(2) 107-16 DOI: 10.1016/j.cancergencyto.2007.02.002 PMID: 17556066
30. Yang S, Xiao X, Jia Y, Liu X, Zhang Y, Devor EJ, Meng X, Thiel KW and Leslie KK (2013) Epigenetic modification restores functional PR expression in endometrial cancer cells Curr Pharm Des in press
31. Westin SN and Broaddus RR (2012) Personalized therapy in endometrial cancer: challenges and opportunities Cancer Biology Therapy 13(1) 1-13 DOI: 10.4161/cbt.13.1.18438 PMCID: 3335980
32. Neubauer NL, Ward EC, Patel P, Lu Z, Lee I, Blok LJ, Hanifi-Moghaddam P, Schink J and Kim JJ (2011) Progesterone receptor-B induction of BIRC3 protects endometrial cancer cells from AP1-59-mediated apoptosis Hormones Cancer 2(3) 170-81 DOI: 10.1007/s12672-011-0065-7 PMID: 21760855 PMCID: 3133609
33. Dai D, Wolf DM, Litman ES, White MJ and Leslie KK (2002) Progesterone inhibits human endometrial cancer cell growth and invasiveness: down-regulation of cellular adhesion molecules through progesterone B receptors Cancer Res 62(3) 881-6 PMID: 11830547
34. Ward EC, Hoekstra AV, Blok LJ, Hanifi-Moghaddam P, Lurain JR, Singh DK, Buttin BM, Schink JC and Kim JJ (2008) The regulation and function of the forkhead transcription factor, Forkhead box O1, is dependent on the progesterone receptor in endometrial carcinoma Endocrinology 149(4) 1942-50 DOI: 10.1210/en.2007-0756
35. Utsunomiya H, Suzuki T, Ito K, Moriya T, Konno R, Sato S, Yaegashi N, Okamura K and Sasano H (2003) The correlation between the response to progestogen treatment and the expression of progesterone receptor B and 17beta-hydroxysteroid dehydrogenase type 2 in human endometrial carcinoma Clin Endocrinol (Oxf) 58(6) 696-703 DOI: 10.1046/j.1365-2265.2003.01766.x
36. Tlsty TD and Coussens LM (2006) Tumor stroma and regulation of cancer development Annu Rev Pathol 1 119-50 DOI: 10.1146/annurev.pathol.1.110304.100224
37. Lin J, Li R and Zhou J (2003) The influence of insulin on secretion of IGF-I and IGFBP-I in cultures of human endometrial stromal cells Chin Med J 116(2) 301-304 PMID: 12775252
38. Wang HS and Chard T (1999) IGFs and IGF-binding proteins in the regulation of human ovarian and endometrial function J Endocrinol 161(1) 1-13 DOI: 10.1677/joe.0.1610001 PMID: 10194523
39. Kaaks R, Lukanova A and Kurzer MS (2002) Obesity, endogenous hormones, and endometrial cancer risk: a synthetic review Cancer Epidemiol Biomarkers Prev 11(12) 1531-43 PMID: 12496040
40. Cunha GR, Cooke PS and Kurita T (2004) Role of stromal-epithelial interactions in hormonal responses Arch Histol Cytol 67(5) 417-34 DOI: 10.1679/aohc.67.417
41. Daikoku T, Hirota Y, Tranguch S, Joshi AR, DeMayo FJ, Lydon JP, Ellenson LH and Dey SK (2008) Conditional loss of uterine Pten unfailingly and rapidly induces endometrial cancer in mice Cancer Res 68(14) 5619-27 DOI: 10.1158/0008-5472.CAN-08-1274 PMID: 18632614 PMCID: 2824329
42. Carracedo A and Pandolfi PP (2008) The PTEN-PI3K pathway: of feedbacks and cross-talks Oncogene 27(41) 5527-41 DOI: 10.1038/onc.2008.247 PMID: 18794886
43. Carracedo A, Alimonti A and Pandolfi PP (2011) PTEN level in tumor suppression: how much is too little? Cancer Res 71(3) 629-33 DOI: 10.1158/0008-5472.CAN-10-2488 PMID: 21266353 PMCID: 3249925
44. Janzen DM, Rosales MA, Paik DY, Lee DS, Smith DA, Witte ON, Iruela-Arispe ML and Memarzadeh S (2013) Progesterone receptor signaling in the microenvironment of endometrial cancer influences its response to hormonal therapy Cancer Res 73(15) 4697-710 DOI: 10.1158/0008-5472.CAN-13-0930 PMID: 23744837 PMCID: 3752407
45. Kraus WL and Katzenellenbogen BS (1993) Regulation of progesterone receptor gene expression and growth in the rat uterus: modulation of estrogen actions by progesterone and sex steroid hormone antagonists. Endocrinology 132(6) 2371-9 DOI: 10.1210/en.132.6.2371 PMID: 8504742
46. Leonhardt SA, Altmann M and Edwards DP (1998) Agonist and antagonists induce homodimerization and mixed ligand heterodimerization of human progesterone receptors in vivo by a mammalian two-hybrid assay Mol Endocrinol 12(12) 1914-30 DOI: 10.1210/me.12.12.1914 PMID: 9849965
47. Li X and O'Malley BW (2003) Unfolding the action of progesterone receptors J Biol Chem 278(41) 39261-4 DOI: 10.1074/jbc.R300024200 PMID: 12893816
48. Smid-Koopman E, Kuhne LC, Hanekamp EE, Gielen SC, De Ruiter PE, Grootegoed JA, Helmerhorst TJ, Burger CW, Brinkmann AO, Huikeshoven FJ, et al (2005) Progesterone-induced inhibition of growth and differential regulation of gene expression in PRA- and/or PRB-expressing endometrial cancer cell lines J Soc Gynecol Investig 12(4) 285-92 DOI: 10.1016/j.jsgi.2005.01.003 PMID: 15866122
49. Aghajanova L, Velarde MC and Giudice LC (2010) Altered gene expression profiling in endometrium: evidence for progesterone resistance Semin Reprod Med 28(1) 51-8 DOI: 10.1055/s-0029-1242994 PMID: 20104428