Decreased progesterone receptor isoform expression in luteal phase fallopian tube epithelium and high-grade serous carcinoma

Endocrine-Related Cancer

Volumn 18, Issue 2, 2011, Pages 221-234

  Tone, Alicia A ^a,b,c   Virtanen, Carl ^d   Shaw, Patricia A ^b,c   Brown, Theodore J ^a,c  

^a MOUNT SINAI HOSPITAL   (Canada)

^b Department of Laboratory Medicine and Pathobiology ^*  (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d UNIVERSITY HEALTH NETWORK   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BRCA1 PROTEIN; BRCA2 PROTEIN; PROGESTERONE RECEPTOR A; PROGESTERONE RECEPTOR B;

ARTICLE; CARCINOMA; GENE EXPRESSION PROFILING; GENE MUTATION; HIGH GRADE SEROUS CARCINOMA; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LUTEAL PHASE; UTERINE TUBE;

CYSTADENOCARCINOMA, SEROUS; EPITHELIUM; FALLOPIAN TUBES; FEMALE; GENE EXPRESSION PROFILING; GENES, BRCA1; GENES, BRCA2; GENETIC PREDISPOSITION TO DISEASE; HUMANS; IMMUNOHISTOCHEMISTRY; LUTEAL PHASE; PROTEIN ISOFORMS; RECEPTORS, PROGESTERONE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER;

EID: 79953218350     PISSN: 13510088     EISSN: 14796821     Source Type: Journal    
DOI: 10.1530/ERC-10-0235     Document Type: Article

References (49)

1. Aghmesheh M, Edwards L, Clarke CL, Byth K, Katzenellenbogen BS, Russell PJ, Friedlander M, Tucker KM & de Fazio A 2005 Expression of steroid hormone receptors in BRCA1-associated ovarian carcinomas. Gynecologic Oncology 97 16-25. (doi:10.1016/j.ygyno.2004.12.030)
2. Akahira J, Inoue T, Suzuki T, Ito K, Konno R, Sato S, Moriya T, Okamura K, Yajima A & Sasano H 2000 Progesterone receptor isoforms A and B in human epithelial ovarian carcinoma: immunohistochemical and RT-PCR studies. British Journal of Cancer 83 1488-1494. (doi:10.1054/bjoc.2000.1463)
3. Akahira J, Suzuki T, Ito K, Kaneko C, Darnel AD, Moriya T , Okamura K, Yaegashi N & Sasano H 2002 Differential expression of progesterone receptor isoforms A and B in the normal ovary, and in benign, borderline, and malignant ovarian tumors. Japanese Journal of Cancer Research 93 807-815. (doi:10.1111/j.1349-7006.2002.tb01323.x)
4. Ariga N, Suzuki T, Moriya T, Kimura M, Inoue T, Ohuchi N & Sasano H 2001 Progesterone receptor A and B isoforms in the human breast and its disorders. Japanese Journal of Cancer Research 92 302-308. (doi:10.1111/j.1349- 7006.2001.tb01095.x)
5. Boonyaratanakornkit V, Bi Y, Rudd M & Edwards DP 2008 The role and mechanism of progesterone receptor activation of extra-nuclear signaling pathways in regulating gene transcription and cell cycle progression. Steroids 73 922-928. (doi:10.1016/j.steroids.2008.01.010)
6. Briton-Jones C, Lok IH, Cheung CK, Po AL, Chiu TT & Haines C 2005 Ratio of mRNA expression of progesterone receptor isoforms AB is to B in human oviduct mucosal cells during the ovulatory cycle. Journal of Assisted Reproduction and Genetics 22 429-435. (doi:10.1007/s10815-005-7203-5)
7. Cass I, Holschneider C, Datta N, Barbuto D, Walts AE & Karlan BY 2005 BRCA-mutation-associated fallopian tube carcinoma: a distinct clinical phenotype? Obstetrics and Gynecology 106 1327-1334. (doi:10.1097/01.AOG. 0000187892.78392.3f)
8. Colgan TJ, Murphy J, Cole DE, Narod S & Rosen B 2001 Occult carcinoma in prophylactic oophorectomy specimens: prevalence and association with BRCA germline mutation status. American Journal of Surgical Pathology 25 1283-1289. (doi:10.1097/00000478-200110000-00009)
9. Crow J, Amso NN, Lewin J & Shaw RW 1994 Morphology and ultrastructure of fallopian tube epithelium at different stages of the menstrual cycle and menopause. Human Reproduction 9 2224-2233.
10. Crum CP, Drapkin R, Miron A, Ince TA, Muto M, Kindelberger DW & Lee Y 2007 The distal fallopian tube: a new model for pelvic serous carcinogenesis. Current Opinion in Obstetrics & Gynecology 19 3-9. (doi:10.1097/GCO. 0b013e328011a21f)
11. Denner LA, Weigel NL, Maxwell BL, Schrader WT & O'Malley BW 1990 Regulation of progesterone receptor-mediated transcription by phosphorylation. Science 250 1740-1743. (doi:10.1126/science.2176746)
12. Fan S, Ma YX, Wang C, Yuan RQ, Meng Q, Wang JA, Erdos M, Goldberg ID, Webb P, Kushner PJ et al. 2002 p300 modulates the BRCA1 inhibition of estrogen receptor activity. Cancer Research 62 141-151. (Pubitemid 34073998)
13. Finch A, Shaw P, Rosen B, Murphy J, Narod SA & Colgan TJ 2006 Clinical and pathologic findings of prophylactic salpingo-oophorectomies in 159 BRCA1 and BRCA2 carriers. Gynecologic Oncology 100 58-64. (doi:10.1016/j.ygyno. 2005.06.065)
14. Folkins AK, Jarboe EA, Saleemuddin A, Lee Y, Callahan MJ, Drapkin R, Garber JE, Muto MG, Tworoger S & Crum CP 2008 A candidate precursor to pelvic serous cancer (p53 signature) and its prevalence in ovaries and fallopian tubes fromwomenwith BRCAmutations. Gynecologic Oncology 109 168-173. (doi:10.1016/j.ygyno.2008.01.012)
15. Gabra H, Langdon SP, Watson JE, Hawkins RA, Cohen BB, Taylor L, Mackay J, Steel CM, Leonard RC & Smyth JF 1995 Loss of heterozygosity at 11q22 correlates with low progesterone receptor content in epithelial ovarian cancer. Clinical Cancer Research 1 945-953.
16. Gellersen B, Fernandes MS & Brosens JJ 2009 Non-genomic progesterone actions in female reproduction. Human Reproduction Update 15 119-138. (doi:10.1093/humupd/dmn044)
17. Gien LT, Rosen B, Panzarella T, Chapman W & Dodge JE 2008 A comparison of outcomes between endometrioid and serous carcinomas of the ovary: are they different cancers? In 4th Canadian Conference on Ovarian Cancer Research Montreal, Quebec, Canada.
18. Graham JD, Yeates C, Balleine RL, Harvey SS, Milliken JS, Bilous AM & Clarke CL 1995 Characterization of progesterone receptor A and B expression in human breast cancer. Cancer Research 55 5063-5068.
19. Helm G, Batra S & Owman C 1987 Cytoplasmic and nuclear progesterone receptors in human fallopian tube and their relationship to plasma steroids during the menstrual cycle. International Journal of Fertility 32 162-166. (Pubitemid 17066386)
20. Jacobsen BM, Schittone SA, Richer JK & Horwitz KB 2005 Progesterone-independent effects of human progesterone receptors (PRs) in estrogen receptor-positive breast cancer: PR isoform-specific gene regulation and tumor biology. Molecular Endocrinology 19 574-587. (doi:10.1210/me.2004- 0287)
21. Kindelberger DW, Lee Y, Miron A, Hirsch MS, Feltmate C, Medeiros F, Callahan MJ, Garner EO, Gordon RW, Birch C et al. 2007 Intraepithelial carcinoma of the fimbria and pelvic serous carcinoma: evidence for a causal relationship. American Journal of Surgical Pathology 31 161-169. (doi:10.1097/01.pas. 0000213335.40358.47)
22. Lange CA, Shen T & 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. (doi:10.1073/pnas.97.3.1032)
23. Lau KM, Mok SC & Ho SM 1999 Expression of human estrogen receptor-α and -β, progesterone receptor, and androgen receptor mRNA in normal and malignant ovarian epithelial cells. PNAS 96 5722-5727. (doi:10.1073/pnas.96.10.5722)
24. Launonen V, Stenback F, Puistola U, Bloigu R, Huusko P, Kytola S, Kauppila A & Winqvist R 1998 Chromosome 11q22.3-q25 LOH in ovarian cancer: association with a more aggressive disease course and involved subregions. Gynecologic Oncology 71 299-304. (doi:10.1006/gyno.1998.5186)
25. Lee P, Rosen DG, Zhu C, Silva EG & Liu J 2005 Expression of progesterone receptor is a favorable prognostic marker in ovarian cancer. Gynecologic Oncology 96 671-677. (doi:10.1016/j.ygyno.2004.11.010)
26. Lee Y, Miron A, Drapkin R, Nucci MR, Medeiros F, Saleemuddin A, Garber J, Birch C, Mou H, Gordon RW et al. 2007 A candidate precursor to serous carcinoma that originates in the distal fallopian tube. Journal of Pathology 211 26-35. (doi:10.1002/path.2091)
27. Leo JC & Lin VC 2008 The activities of progesterone receptor isoform A and B are differentially modulated by their ligands in a gene-selective manner. International Journal of Cancer 122 230-243. (doi:10.1002/ijc.23081)
28. Leonhardt SA, Boonyaratanakornkit V & Edwards DP 2003 Progesterone receptor transcription and non-transcription signaling mechanisms. Steroids 68 761-770. (doi:10.1016/S0039-128X(03)00129-6)
29. Ma Y, Katiyar P, Jones LP, Fan S, Zhang Y, Furth PA & Rosen EM 2006 The breast cancer susceptibility gene BRCA1 regulates progesterone receptor signaling in mammary epithelial cells. Molecular Endocrinology 20 14-34. (doi:10.1210/me.2004-0488)
30. May T, Virtanen C, Sharma M, Milea A, Begley H, Rosen B, Murphy KJ, Brown TJ & Shaw PA 2010 Low malignant potential tumors with micropapillary features are molecularly similar to low-grade serous carcinoma of the ovary. Gynecologic Oncology 117 9-17. (doi:10.1016/j.ygyno.2010.01.006)
31. Medeiros F, Muto MG, Lee Y, Elvin JA, Callahan MJ, Feltmate C, Garber JE, Cramer DW & Crum CP 2006 The tubal fimbria is a preferred site for early adenocarcinoma in women with familial ovarian cancer syndrome. American Journal of Surgical Pathology 30 230-236. (doi:10.1097/01.pas.0000180854.28831.77)
32. Mote PA, Johnston JF, Manninen T, Tuohimaa P & Clarke CL 2001 Detection of progesterone receptor forms A and B by immunohistochemical analysis. Journal of Clinical Pathology 54 624-630. (doi:10.1136/jcp.54.8.624)
33. Mote PA, Bartow S, Tran N & Clarke CL 2002 Loss of co-ordinate expression of progesterone receptors A and B is an early event in breast carcinogenesis. Breast Cancer Research and Treatment 72 163-172. (doi:10.1023/A:1014820500738)
34. Mote PA, Leary JA, Avery KA, Sandelin K, Chenevix-Trench G, Kirk JA & Clarke CL 2004 Germ-line mutations in BRCA1 or BRCA2 in the normal breast are associated with altered expression of estrogen-responsive proteins and the predominance of progesterone receptor A. Genes, Chromosomes and Cancer 39 236-248. (doi:10.1002/gcc.10321)
35. Mulac-Jericevic B & Conneely OM 2004 Reproductive tissue selective actions of progesterone receptors. Reproduction 128 139-146. (doi:10.1530/rep.1.00189)
36. Piek JM, van Diest PJ, Zweemer RP, Jansen JW, Poort-Keesom RJ, Menko FH, Gille JJ, Jongsma AP, Pals G, Kenemans P et al. 2001 Dysplastic changes in prophylactically removed fallopian tubes of women predisposed to developing ovarian cancer. Journal of Pathology 195 451-456. (doi:10.1002/path.1000)
37. Piek JM, Verheijen RH, Menko FH, Jongsma AP, Weegenaar J, Gille JJ, Pals G, Kenemans P & van Diest PJ 2003 Expression of differentiation and proliferation related proteins in epithelium of prophylactically removed ovaries from women with a hereditary female adnexal cancer predisposition. Histopathology 43 26-32. (doi:10.1046/j.1365-2559.2003.01654.x)
38. Pierson-Mullany LK & 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. (doi:10.1128/MCB.24.24.10542-10557.2004)
39. Pino AM, Devoto L, Davila M & Soto E 1984 Changes during the menstrual cycle in cytosolic and nuclear concentrations of progestagen receptor in the human fallopian tube. Journal of Reproduction and Fertility 70 481-485. (doi:10.1530/jrf.0.0700481)
40. 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. American Journal of Physiology. Endocrinology and Metabolism 291 E59-E72. (doi:10.1152/ajpendo.00582.2005)
41. Shaw PA, Rouzbahman M, Pizer ES, Pintilie M & Begley H 2009 Candidate serous cancer precursors in fallopian tube epithelium of BRCA1/2 mutation carriers. Modern Pathology 22 1133-1138. (doi:10.1038/modpathol.2009.89)
42. Shih IM & Kurman RJ 2004 Ovarian tumorigenesis: a proposed model based on morphological and molecular genetic analysis. American Journal of Pathology 164 1511-1518. (doi:10.1016/S0002-9440(10)63708-X)
43. Singer G, Kurman RJ, Chang HW, Cho SK & Shih IM 2002 Diverse tumorigenic pathways in ovarian serous carcinoma. American Journal of Pathology 160 1223-1228. (doi:10.1016/S0002-9440(10)62549-7)
44. Talamo TS, Bender BL, Ellis LD & Scioscia EA 1982 Adenocarcinoma of the fallopian tube. An ultrastructural study. Virchows Archive. A: Pathological Anatomy and Histology 397 363-368. (doi:10.1007/BF00496577)
45. Tibshirani R, Hastie T, Narasimhan B & Chu G 2002 Diagnosis of multiple cancer types by shrunken centroids of gene expression. PNAS 99 6567-6572. (doi:10.1073/pnas.082099299)
46. Tone AA, Begley H, Sharma M, Murphy J, Rosen B, Brown TJ & Shaw PA 2008 Gene expression profiles of luteal phase fallopian tube epithelium from BRCA mutation carriers resemble high-grade serous carcinoma. Clinical Cancer Research 14 4067-4078. (doi:10.1158/1078-0432.CCR-07-4959)
47. Vegeto E, Shahbaz MM, Wen DX, Goldman ME, O'Malley BW & McDonnell DP 1993 Human progesterone receptor A form is a cell- and promoter-specific repressor of human progesterone receptor B function. Molecular Endocrinology 7 1244-1255. (doi:10.1210/me.7.10.1244)
48. Verhage HG, Akbar M & Jaffe RC 1980 Cyclic changes in cytosol progesterone receptor of human fallopian tube. Journal of Clinical Endocrinology and Metabolism 51 776-780. (doi:10.1210/jcem-51-4-776)
49. Zheng L, Annab LA, Afshari CA, Lee WH & Boyer TG 2001 BRCA1 mediates ligand-independent transcriptional repression of the estrogen receptor. PNAS 98 9587-9592. (doi:10.1073/pnas.171174298)