Proliferation and ovarian hormone signaling are impaired in normal breast tissues from women with BRCA1 mutations: Benefit of a progesterone receptor modulator treatment as a breast cancer preventive strategy in women with inherited BRCA1 mutations

Oncotarget

Volumn 7, Issue 29, 2016, Pages 45317-45330

  Communal, Laudine ^a   Vilasco, Myriam ^a   Hugon Rodin, Justine ^a   Courtin, Aurélie ^a   Mourra, Najat ^b   Lahlou, Najiba ^a   Le Guillou, Morwenna ^c   de Jotemps, Muriel Perrault ^d   Chauvet, Marie Pierre ^e   Chaouat, Marc ^a   Pujol, Pascal ^f   Feunteun, Jean ^c   Delaloge, Suzette ^g   Forgez, Patricia ^a   Gompel, Anne ^a  

^a UNIVERSITÉ PARIS DESCARTES   (France)

^b HÔPITAL SAINT ANTOINE   (France)

^c UNIVERSITÉ PARIS SACLAY   (France)

^d Clinique Hartmann   (France)

^e CENTRE OSCAR LAMBRET   (France)

^f MONTPELLIER UNIVERSITY HOSPITAL   (France)

^g INSTITUT GUSTAVE ROUSSY   (France)

Author keywords

BRCA1; Breast cancer; Ovarian hormones; Prevention; Ulipristal acetate

Indexed keywords

BRCA1 PROTEIN; ESTRADIOL; ESTROGEN RECEPTOR; FATTY ACID SYNTHASE; HORMONE RECEPTOR; ISOPROTEIN; KI 67 ANTIGEN; PROGESTERONE; PROGESTERONE RECEPTOR; PROGESTERONE RECEPTOR B; PROGESTERONE RECEPTOR MODULATOR; ULIPRISTAL; PREGNANE DERIVATIVE;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST CANCER; CANCER PREVENTION; CELL PROLIFERATION; COHORT ANALYSIS; CONTROLLED STUDY; FEMALE; GENE TARGETING; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; MAJOR CLINICAL STUDY; MOUSE; MUTATIONAL ANALYSIS; NONHUMAN; PROTEIN DEPLETION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TREATMENT RESPONSE; TUMOR XENOGRAFT; ANIMAL; ANTAGONISTS AND INHIBITORS; BREAST; BREAST TUMOR; DRUG SCREENING; GENETICS; MIDDLE AGED; MUTATION; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE; TUMOR SUPPRESSOR GENE;

ADULT; ANIMALS; BREAST; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL PROLIFERATION; ESTRADIOL; FEMALE; GENES, BRCA1; HUMANS; MICE; MIDDLE AGED; MUTATION; NORPREGNADIENES; RECEPTORS, ESTROGEN; RECEPTORS, PROGESTERONE; SIGNAL TRANSDUCTION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84979941674     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.9638     Document Type: Article

References (64)

1. Silver DP, Livingston DM. Mechanisms of BRCA1 tumor suppression. Cancer discovery. 2012; 2:679-684.
2. Boulton SJ. Cellular functions of the BRCA tumoursuppressor proteins. Biochemical Society transactions. 2006; 34:633-645.
3. Mavaddat N, Peock S, Frost D, Ellis S, Platte R, Fineberg E, Evans DG, Izatt L, Eeles RA, Adlard J, Davidson R, Eccles D, Cole T, et al. Cancer risks for BRCA1 and BRCA2 mutation carriers: results from prospective analysis of EMBRACE. Journal of the National Cancer Institute. 2013; 105:812-822.
4. King MC, Marks JH, Mandell JB. Breast and ovarian cancer risks due to inherited mutations in BRCA1 and BRCA2. Science. 2003; 302:643-646.
5. Lecarpentier J, Nogues C, Mouret-Fourme E, Buecher B, Gauthier-Villars M, Stoppa-Lyonnet D, Bonadona V, Fricker JP, Berthet P, Caron O, Coupier I, Pujol P, Faivre L, et al. Breast cancer risk associated with oestrogen exposure and truncating mutation location in BRCA1/2 carriers. Cancer epidemiology, biomarkers & prevention. 2015; 24:698-707.
6. Pan H, He Z, Ling L, Ding Q, Chen L, Zha X, Zhou W, Liu X, Wang S. Reproductive factors and breast cancer risk among BRCA1 or BRCA2 mutation carriers: results from ten studies. Cancer epidemiology. 2014; 38:1-8.
7. Rebbeck TR, Kauff ND, Domchek SM. Meta-analysis of risk reduction estimates associated with risk-reducing salpingo-oophorectomy in BRCA1 or BRCA2 mutation carriers. Journal of the National Cancer Institute. 2009; 101:80-87.
8. Noruzinia M, Coupier I, Pujol P. Is BRCA1/BRCA2-related breast carcinogenesis estrogen dependent? Cancer. 2005; 104:1567-1574.
9. Eisen A, Lubinski J, Klijn J, Moller P, Lynch HT, Offit K, Weber B, Rebbeck T, Neuhausen SL, Ghadirian P, Foulkes WD, Gershoni-Baruch R, Friedman E, et al. Breast cancer risk following bilateral oophorectomy in BRCA1 and BRCA2 mutation carriers: an international case-control study. Journal of clinical oncology. 2005; 23:7491-7496.
10. Fan S, Ma YX, Wang C, Yuan RQ, Meng Q, Wang JA, Erdos M, Goldberg ID, Webb P, Kushner PJ, Pestell RG, Rosen EM. Role of direct interaction in BRCA1 inhibition of estrogen receptor activity. Oncogene. 2001; 20:77-87.
11. Wang C, Fan S, Li Z, Fu M, Rao M, Ma Y, Lisanti MP, Albanese C, Katzenellenbogen BS, Kushner PJ, Weber B, Rosen EM, Pestell RG. Cyclin D1 antagonizes BRCA1 repression of estrogen receptor alpha activity. Cancer research. 2005; 65:6557-6567.
12. Hosey AM, Gorski JJ, Murray MM, Quinn JE, Chung WY, Stewart GE, James CR, Farragher SM, Mulligan JM, Scott AN, Dervan PA, Johnston PG, Couch FJ, et al. Molecular basis for estrogen receptor alpha deficiency in BRCA1-linked breast cancer. Journal of the National Cancer Institute. 2007; 99:1683-1694.
13. Jeffy BD, Hockings JK, Kemp MQ, Morgan SS, Hager JA, Beliakoff J, Whitesell LJ, Bowden GT, Romagnolo DF. An estrogen receptor-alpha/p300 complex activates the BRCA-1 promoter at an AP-1 site that binds Jun/Fos transcription factors: repressive effects of p53 on BRCA-1 transcription. Neoplasia. 2005; 7:873-882.
14. Ma Y, Katiyar P, Jones LP, Fan S, Zhang Y, Furth PA, Rosen EM. The breast cancer susceptibility gene BRCA1 regulates progesterone receptor signaling in mammary epithelial cells. Mol Endocrinol. 2006; 20:14-34.
15. Katiyar P, Ma Y, Riegel A, Fan S, Rosen EM. Mechanism of BRCA1-mediated inhibition of progesterone receptor transcriptional activity. Mol Endocrinol. 2009; 23:1135-1146.
16. Mote PA, Leary JA, Avery KA, Sandelin K, Chenevix-Trench G, Kirk JA, Clarke CL. 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 & cancer. 2004; 39:236-248.
17. Prest SJ, May FE, Westley BR. The estrogen-regulated protein, TFF1, stimulates migration of human breast cancer cells. FASEB journal. 2002; 16:592-594.
18. Poole AJ, Li Y, Kim Y, Lin SC, Lee WH, Lee EY. Prevention of Brca1-mediated mammary tumorigenesis in mice by a progesterone antagonist. Science. 2006; 314:1467-1470.
19. King MC, Wieand S, Hale K, Lee M, Walsh T, Owens K, Tait J, Ford L, Dunn BK, Costantino J, Wickerham L, Wolmark N, Fisher B. Tamoxifen and breast cancer incidence among women with inherited mutations in BRCA1 and BRCA2: National Surgical Adjuvant Breast and Bowel Project (NSABP-P1) Breast Cancer Prevention Trial. JAMA. 2001; 286:2251-2256.
20. Eisinger F, Nogues C, Guinebretiere JM, Peyrat JP, Bardou VJ, Noguchi T, Vennin P, Sauvan R, Lidereau R, Birnbaum D, Jacquemier J, Sobol H. Novel indications for BRCA1 screening using individual clinical and morphological features. International journal of cancer. 1999; 84:263-267.
21. Fisher B, Costantino JP, Wickerham DL, Redmond CK, Kavanah M, Cronin WM, Vogel V, Robidoux A, Dimitrov N, Atkins J, Daly M, Wieand S, Tan-Chiu E, et al. Tamoxifen for prevention of breast cancer: report of the National Surgical Adjuvant Breast and Bowel Project P-1 Study. Journal of the National Cancer Institute. 1998; 90:1371-1388.
22. Vogel VG, Costantino JP, Wickerham DL, Cronin WM, Cecchini RS, Atkins JN, Bevers TB, Fehrenbacher L, Pajon ER, Jr., Wade JL, 3rd, Robidoux A, Margolese RG, James J, et al. Effects of tamoxifen vs raloxifene on the risk of developing invasive breast cancer and other disease outcomes: the NSABP Study of Tamoxifen and Raloxifene (STAR) P-2 trial. JAMA: the journal of the American Medical Association. 2006; 295:2727-2741.
23. Vogel VG, Costantino JP, Wickerham DL, Cronin WM, Cecchini RS, Atkins JN, Bevers TB, Fehrenbacher L, Pajon ER, Wade JL, 3rd, Robidoux A, Margolese RG, James J, et al. Update of the National Surgical Adjuvant Breast and Bowel Project Study of Tamoxifen and Raloxifene (STAR) P-2 Trial: Preventing breast cancer. Cancer Prev Res (Phila). 2010; 3:696-706.
24. Phillips KA, Milne RL, Rookus MA, Daly MB, Antoniou AC, Peock S, Frost D, Easton DF, Ellis S, Friedlander ML, Buys SS, Andrieu N, Nogues C, et al. Tamoxifen and risk of contralateral breast cancer for BRCA1 and BRCA2 mutation carriers. Journal of clinical oncology. 2013; 31:3091-3099.
25. Goss PE, Ingle JN, Ales-Martinez JE, Cheung AM, Chlebowski RT, Wactawski-Wende J, McTiernan A, Robbins J, Johnson KC, Martin LW, Winquist E, Sarto GE, Garber JE, et al. Exemestane for breast-cancer prevention in postmenopausal women. The New England journal of medicine. 2011; 364:2381-2391.
26. Trefoux Bourdet A, Luton D, Koskas M. Clinical utility of ulipristal acetate for the treatment of uterine fibroids: current evidence. International journal of women's health. 2015; 7:321-330.
27. Glasier A. The rationale for use of Ulipristal Acetate as first line in emergency contraception: biological and clinical evidence. Gynecological endocrinology. 2014; 30:688-690.
28. Communal L, Vilasco M, Hugon-Rodin J, Courtin A, Mourra N, Lahlou N, Dumont S, Chaouat M, Forgez P, Gompel A. Ulipristal acetate does not impact human normal breast tissue. Hum Reprod. 2012; 27:2785-2798.
29. Nieman LK, Blocker W, Nansel T, Mahoney S, Reynolds J, Blithe D, Wesley R, Armstrong A. Efficacy and tolerability of CDB-2914 treatment for symptomatic uterine fibroids: a randomized, double-blind, placebo-controlled, phase IIb study. Fertility and sterility. 2011; 95:767-772 e761-762.
30. Donnez J, Hudecek R, Donnez O, Matule D, Arhendt H, Zatik J, Kasilovskiene Z, Dumitrascu MC, Fernandez H, Barlow DH, Bouchard P, Fauser BC, Bestel E, et al. Efficacy and safety of repeated use of ulipristal acetate in uterine fibroids. Fertility and sterility. 2014.
31. McGowan EM, Clarke CL. Effect of overexpression of progesterone receptor A on endogenous progestin-sensitive endpoints in breast cancer cells. Mol Endocrinol. 1999; 13:1657-1671.
32. Giangrande PH, Kimbrel EA, Edwards DP, McDonnell DP. The opposing transcriptional activities of the two isoforms of the human progesterone receptor are due to differential cofactor binding. Molecular and cellular biology. 2000; 20:3102-3115.
33. Rochefort H, Chalbos D. The role of sex steroid receptors on lipogenesis in breast and prostate carcinogenesis: a viewpoint. Hormones & cancer. 2010; 1:63-70.
34. Kuhajda FP. Fatty acid synthase and cancer: new application of an old pathway. Cancer research. 2006; 66:5977-5980.
35. Joyeux C, Chalbos D, Rochefort H. Effects of progestins and menstrual cycle on fatty acid synthetase and progesterone receptor in human mammary glands. The Journal of clinical endocrinology and metabolism. 1990; 70:1438-1444.
36. Chalbos D, Joyeux C, Galtier F, Escot C, Chambon M, Maudelonde T, Rochefort H. Regulation of fatty acid synthetase by progesterone in normal and tumoral human mammary glands. Revista espanola de fisiologia. 1990; 46:43-46.
37. Courtin A, Communal L, Vilasco M, Cimino D, Mourra N, de Bortoli M, Taverna D, Faussat AM, Chaouat M, Forgez P, Gompel A. Glucocorticoid receptor activity discriminates between progesterone and medroxyprogesterone acetate effects in breast cells. Breast cancer research and treatment. 2012; 131:49-63.
38. Rennstam K, Ringberg A, Cunliffe HE, Olsson H, Landberg G, Hedenfalk I. Genomic alterations in histopathologically normal breast tissue from BRCA1 mutation carriers may be caused by BRCA1 haploinsufficiency. Genes, chromosomes & cancer. 2010; 49:78-90.
39. Pathania S, Bade S, Le Guillou M, Burke K, Reed R, Bowman-Colin C, Su Y, Ting DT, Polyak K, Richardson AL, Feunteun J, Garber JE, Livingston DM. BRCA1 haploinsufficiency for replication stress suppression in primary cells. Nature communications. 2014; 5:5496.
40. Lim E, Vaillant F, Wu D, Forrest NC, Pal B, Hart AH, Asselin-Labat ML, Gyorki DE, Ward T, Partanen A, Feleppa F, Huschtscha LI, Thorne HJ, et al. Aberrant luminal progenitors as the candidate target population for basal tumor development in BRCA1 mutation carriers. Nature medicine. 2009; 15:907-913.
41. Mohammed H, Russell IA, Stark R, Rueda OM, Hickey TE, Tarulli GA, Serandour AA, Birrell SN, Bruna A, Saadi A, Menon S, Hadfield J, Pugh M, et al. Progesterone receptor modulates ERalpha action in breast cancer. Nature. 2015; 523:313-317.
42. Wargon V, Riggio M, Giulianelli S, Sequeira GR, Rojas P, May M, Polo ML, Gorostiaga MA, Jacobsen B, Molinolo A, Novaro V, Lanari C. Progestin and antiprogestin responsiveness in breast cancer is driven by the PRA/PRB ratio via AIB1 or SMRT recruitment to the CCND1 and MYC promoters. International journal of cancer. 2015; 136:2680-2692.
43. Layde PM, Webster LA, Baughman AL, Wingo PA, Rubin GL, Ory HW. The independent associations of parity, age at first full term pregnancy, and duration of breastfeeding with the risk of breast cancer. Cancer and Steroid Hormone Study Group. Journal of clinical epidemiology. 1989; 42:963-973.
44. Russo J, Moral R, Balogh GA, Mailo D, Russo IH. The protective role of pregnancy in breast cancer. Breast cancer research. 2005; 7:131-142.
45. Hinkula M, Pukkala E, Kyyronen P, Kauppila A. Grand multiparity and the risk of breast cancer: populationbased study in Finland. Cancer causes & control. 2001; 12:491-500.
46. Xu L, Zhao Y, Chen Z, Wang Y, Chen L, Wang S. Tamoxifen and risk of contralateral breast cancer among women with inherited mutations in BRCA1 and BRCA2: a meta-analysis. Breast Cancer. 2015.
47. Widschwendter M, Rosenthal AN, Philpott S, Rizzuto I, Fraser L, Hayward J, Intermaggio MP, Edlund CK, Ramus SJ, Gayther SA, Dubeau L, Fourkala EO, Zaikin A, et al. The sex hormone system in carriers of BRCA1/2 mutations: a case-control study. The Lancet Oncology. 2013; 14:1226-1232.
48. Jones LP, Tilli MT, Assefnia S, Torre K, Halama ED, Parrish A, Rosen EM, Furth PA. Activation of estrogen signaling pathways collaborates with loss of Brca1 to promote development of ERalpha-negative and ERalphapositive mammary preneoplasia and cancer. Oncogene. 2008; 27:794-802.
49. Lee EY. Promotion of BRCA1-associated triple-negative breast cancer by ovarian hormones. Current opinion in obstetrics & gynecology. 2008; 20:68-73.
50. Bramley M, Clarke RB, Howell A, Evans DG, Armer T, Baildam AD, Anderson E. Effects of oestrogens and antioestrogens on normal breast tissue from women bearing BRCA1 and BRCA2 mutations. British journal of cancer. 2006; 94:1021-1028.
51. Mote PA, Bartow S, Tran N, Clarke CL. Loss of co-ordinate expression of progesterone receptors A and B is an early event in breast carcinogenesis. Breast cancer research and treatment. 2002; 72:163-172.
52. Mote PA, Graham JD, Clarke CL. Progesterone receptor isoforms in normal and malignant breast. Ernst Schering Foundation symposium proceedings. 2007; 77-107.
53. Hagan CR, Lange CA. Molecular determinants of contextdependent progesterone receptor action in breast cancer. BMC medicine. 2014; 12:32.
54. Vazquez-Martinez ER, Mendoza-Garces L, Vergara-Castaneda E, Cerbon M. Epigenetic regulation of Progesterone Receptor isoforms: from classical models to the sexual brain. Molecular and cellular endocrinology. 2014; 392:115-124.
55. Khan JA, Amazit L, Bellance C, Guiochon-Mantel A, Lombes M, Loosfelt H. p38 and p42/44 MAPKs differentially regulate progesterone receptor A and B isoform stabilization. Mol Endocrinol. 2011; 25:1710-1724.
56. Vilasco M, Communal L, Hugon-Rodin J, Penault-Llorca F, Mourra N, Wu Z, Forgez P, Gompel A. Loss of glucocorticoid receptor activation is a hallmark of BRCA1-mutated breast tissue. Breast cancer research and treatment. 2013; 142:283-296.
57. Yan Y, Haas JP, Kim M, Sgagias MK, Cowan KH. BRCA1-induced apoptosis involves inactivation of ERK1/2 activities. The Journal of biological chemistry. 2002; 277:33422-33430.
58. Kotsopoulos J, Lubinski J, Moller P, Lynch HT, Singer CF, Eng C, Neuhausen SL, Karlan B, Kim-Sing C, Huzarski T, Gronwald J, McCuaig J, Senter L, et al. Timing of oral contraceptive use and the risk of breast cancer in BRCA1 mutation carriers. Breast cancer research and treatment. 2014; 143:579-586.
59. Brohet RM, Goldgar DE, Easton DF, Antoniou AC, Andrieu N, Chang-Claude J, Peock S, Eeles RA, Cook M, Chu C, Nogues C, Lasset C, Berthet P, et al. Oral contraceptives and breast cancer risk in the international BRCA1/2 carrier cohort study: a report from EMBRACE, GENEPSO, GEO-HEBON, and the IBCCS Collaborating Group. Journal of clinical oncology. 2007; 25:3831-3836.
60. Rebbeck TR, Friebel T, Wagner T, Lynch HT, Garber JE, Daly MB, Isaacs C, Olopade OI, Neuhausen SL, van't Veer L, Eeles R, Evans DG, Tomlinson G, et al. Effect of short-term hormone replacement therapy on breast cancer risk reduction after bilateral prophylactic oophorectomy in BRCA1 and BRCA2 mutation carriers: the PROSE Study Group. Journal of clinical oncology. 2005; 23:7804-7810.
61. Eisen A, Lubinski J, Gronwald J, Moller P, Lynch HT, Klijn J, Kim-Sing C, Neuhausen SL, Gilbert L, Ghadirian P, Manoukian S, Rennert G, Friedman E, et al. Hormone therapy and the risk of breast cancer in BRCA1 mutation carriers. Journal of the National Cancer Institute. 2008; 100:1361-1367.
62. Kotsopoulos J, Huzarski T, Gronwald J, Moller P, Lynch HT, Neuhausen SL, Senter L, Demsky R, Foulkes WD, Eng C, Karlan B, Tung N, Singer CF, et al. Hormone replacement therapy after menopause and risk of breast cancer in BRCA1 mutation carriers: a case-control study. Breast cancer research and treatment. 2016; 155:365-373.
63. Molyneux G, Geyer FC, Magnay FA, McCarthy A, Kendrick H, Natrajan R, Mackay A, Grigoriadis A, Tutt A, Ashworth A, Reis-Filho JS, Smalley MJ. BRCA1 basal-like breast cancers originate from luminal epithelial progenitors and not from basal stem cells. Cell stem cell. 2010; 7:403-417.
64. Pohl O, Zobrist RH, Gotteland JP. The clinical pharmacology and pharmacokinetics of ulipristal acetate for the treatment of uterine fibroids. Reprod Sci. 2015; 22:476-483.