Progesterone and progesterone receptors in breast cancer: past, present, and future

Cover Page

Cite item

Full Text

Abstract

 The history of progesterone and progesterone receptors (PR) in breast cancer is as great, as controversial. In this review, we summarize the early history of PR research in breast cancer, debunk the myth that progesterone causes cancer, discuss recent discoveries in PR regulating cellular heterogeneity, attempt to reconcile theories that PR play “good” and “bad” role in tumorigenesis, and discuss new directions that may help elucidate the role of this puzzling hormone and its receptors. 

About the authors

M. V. Rodionova

V.I. Kulakov National Medical Research Center of Obstetrics, Gynecology, and Perinatology, Ministry of Health of Russia

Author for correspondence.
ORCID iD: 0000-0002-0658-1454

4 Akademika Oparina St., Moscow 117198, Russia

Russian Federation

V. V. Rodionov

V.I. Kulakov National Medical Research Center of Obstetrics, Gynecology, and Perinatology, Ministry of Health of Russia

Email: dr.valery.rodionov@gmail.com
ORCID iD: 0000-0003-0096-7126

Valeriy Vitalyevich Rodionov 

4 Akademika Oparina St., Moscow 117198, Russia

Russian Federation

V. V. Kometova

V.I. Kulakov National Medical Research Center of Obstetrics, Gynecology, and Perinatology, Ministry of Health of Russia

ORCID iD: 0000-0001-9666-6875

4 Akademika Oparina St., Moscow 117198, Russia

Russian Federation

A. A. Smetnik

V.I. Kulakov National Medical Research Center of Obstetrics, Gynecology, and Perinatology, Ministry of Health of Russia

ORCID iD: 0000-0002-0627-3902

4 Akademika Oparina St., Moscow 117198, Russia

Russian Federation

I. V. Kolyadina

V.I. Kulakov National Medical Research Center of Obstetrics, Gynecology, and Perinatology, Ministry of Health of Russia;
Russian Medical Academy of Postgraduate Education, Ministry of Health of Russia

ORCID iD: 0000-0002-1124-6802

4 Akademika Oparina St., Moscow 117198, Russia

Build. 1, 2/1 Barrikadnaya St., Moscow 125993, Russia

Russian Federation

O. V. Burmenskaya

V.I. Kulakov National Medical Research Center of Obstetrics, Gynecology, and Perinatology, Ministry of Health of Russia

ORCID iD: 0000-0003-2842-3980

4 Akademika Oparina St., Moscow 117198, Russia

Russian Federation

V. K. Bozhenko

V.I. Kulakov National Medical Research Center of Obstetrics, Gynecology, and Perinatology, Ministry of Health of Russia;
Russian Scientific Center of Roentgenradiology, Ministry of Health of Russia

ORCID iD: 0000-0001-8351-8152

4 Akademika Oparina St., Moscow 117198, Russia

86 Profsoyuznaya St., Moscow 117997, Russia

Russian Federation

Yu. V. Bikeev

V.I. Kulakov National Medical Research Center of Obstetrics, Gynecology, and Perinatology, Ministry of Health of Russia

ORCID iD: 0009-0000-3757-5025

4 Akademika Oparina St., Moscow 117198, Russia

Russian Federation

L. M. Mikhaleva

A.P. Avtsyn Research Institute of Human Morphology

ORCID iD: 0000-0003-2052-914X

3 Tsyurupy St., Moscow 117418, Russia

Russian Federation

L. A. Ashrafyan

V.I. Kulakov National Medical Research Center of Obstetrics, Gynecology, and Perinatology, Ministry of Health of Russia

ORCID iD: 0000-0001-6396-4948

4 Akademika Oparina St., Moscow 117198, Russia

Russian Federation

References

  1. Giatti S., Romano S., Pesaresi M. et al. Neuroactive steroids and the peripheral nervous system: An update. Steroids 2015;103:23–30. doi: 10.1016/j.steroids.2015.03.014
  2. Africander D., Storbeck K.H. Steroid metabolism in breast cancer: Where are we and what are we missing? Mol Cell Endocrinol 2018;466:86–97. doi: 10.1016/j.mce.2017.05.016
  3. Bitsadze V.O., Akinshina S.V., Khizroeva D.Kh. et al. Pathogenetic rationale for the use of natural progesterone in obstetric practice. Akusherstvo, ginekologiya i reproduktsiya = Obstetrics, Gynecology and Reproduction 2014;2:79–88. (In Russ.).
  4. Kastner P., Krust A., Turcotte B. et al. Two distinct estrogenregulated promoters generate transcripts encoding the two functionally different human progesterone receptor forms A and B. EMBO J 1990;9:1603–14. doi: 10.1002/j.1460-2075.1990.tb08280.x
  5. Mangelsdorf D.J., Thummel C., Beato M. et al. The nuclear receptor superfamily: The second decade. Cell 1995;83:835–9. doi: 10.1016/0092-8674(95)90199-x
  6. Takimoto G.S., Tung L., Abdel-Hafiz H. et al. Functional properties of the N-terminal region of progesterone receptors and their mechanistic relationship to structure. J Steroid Biochem Mol Biol 2003;85:209–19. doi: 10.1016/s0960-0760(03)00197-3
  7. Hilton H.N., Graham J.D., Kantimm S. et al. Progesterone and estrogen receptors segregate into different cell subpopulations in the normal human breast. Mol Cell Endocrinol 2012;361:191–201. doi: 10.1016/j.mce.2012.04.010
  8. Graham J.D., Roman S.D., McGowan E. et al. Preferential stimulation of human progesterone receptor B expression by estrogen in T-47D human breast cancer cells. J Biol Chemistry 1995;270:30693–700. doi: 10.1074/jbc.270.51.30693
  9. Hopp T.A., Weiss H.L., Hilsenbeck S.G. et al. Breast cancer patients with progesterone receptor PR-A-rich tumors have poorer disease-free survival rates. Clin Cancer Res 2004;10:2751–60. doi: 10.1158/1078-0432
  10. Rojas P.A., May M., Sequeira G.R. et al. Progesterone receptor isoform ratio: A breast cancer prognostic and predictive factor for antiprogestin responsiveness. J Natl Cancer Inst 2017;109(7):djw317. doi: 10.1093/jnci/djw317
  11. Axlund S.D., Sartorius C.A. Progesterone regulation of stem and progenitor cells in normal and malignant breast. Mol Cell Endocrinol 2012;357:71–9. doi: 10.1016/j.mce.2011.09.021
  12. Finlay-Schultz J., Sartorius C.A. Steroid hormones, steroid receptors, and breast cancer stem cells. J Mammary Gland Biol Neoplasia 2015;20:39–50. doi: 10.1007/s10911-015-9340-5
  13. Cenciarini M.E., Proietti C.J. Molecular mechanisms underlying progesterone receptor action in breast cancer: Insights into cell proliferation and stem cell regulation. Steroids 2019;152:108503. doi: 10.1016/j.steroids.2019.108503
  14. Beatson G.T. On the treatment of inoperable cases of carcinoma of the mamma: Suggestions for a new method of treatment with illustrative cases. Lancet 1896;2:104–7.
  15. Dao T.L. Ablation therapy for hormone-dependent tumors. Ann Rev Med 1972;23:1–18. doi: 10.1146/annurev.me.23.020172.000245
  16. Glascock R.F., Hoekstra W.G. Selective accumulation of tritiumlabelled hexoestrol by the reproductive organs of immature female goats and sheep. Biochem J 1959;72:673–682. doi: 10.1042/bj0720673
  17. Jensen E.V., Jacobson H.I. Fate of seroid estrogens in target tissues. In: Biologic Activities of Streoids in Relation to Cancer. Academic Press, 1960. Pp. 161–174.
  18. King R.J., Gordon J., Cowan D.M., Inman D.R. The intranuclear localization of [6,7-3H]-oestradiol-17-beta in dimethylbenzanthracene-induced rat mammary adenocarcinoma and other tissues. J Endocrinology 1966;36:139–50. doi: 10.1677/joe.0.0360139
  19. Soule H.D., Vazguez J., Long A. et al. A human cell line from a pleural effusion derived from a breast carcinoma. J Natl Cancer Inst 1973;51:1409–16. doi: 10.1093/jnci/51.5.1409
  20. McGuire W.L. Estrogen receptors in human breast cancer. J Clin Invest 1973;52:73–7. doi: 10.1172/JCI107175
  21. McGuire W.L., Horwitz K.B., Chamness G.C., Zava D.T. A physiological role for estrogen and progesterone in breast cancer. J Steroid Biochem 1976;7:875–82. doi: 10.1016/0022-4731(76)90005-4
  22. McGuire W.L., Chamness G.C. Studies on the estrogen receptor in breast cancer. Adv Exp Med Biol 1973;36:113–36. doi: 10.1007/978-1-4684-3237-4_7
  23. Huggins C., Moon R.C., Morii S. Extinction of experimental mammary cancer. I. Estradiol-17beta and progesterone. PNAS 1962;48:379–86. doi: 10.1073/pnas.48.3.379
  24. O’Malley B.W., Sherman M.R., Toft D.O. Progesterone “receptors” in the cytoplasm and nucleus of chick oviduct target tissue. PNAS 1970;67:501–8. doi: 10.1073/pnas.67.2.501
  25. Schrader W.T. Molecular structure and analysis of progesterone receptors. In: Receptors and Hormone Action. Academic Press, 1978. Pp. 189–224.
  26. Philibert D., Raynaud J.P. Binding of progesterone and R 5020, a highly potent progestin, to human endometrium and myometrium. Contraception 1974;10:457–66. doi: 10.1016/0010-7824(74)90112-7
  27. Horwitz K.B., McGuire W.L. Specific progesterone receptors in human breast cancer. Steroids 1975b;25:497–505. doi: 10.1016/0039-128x(75)90027-6
  28. Horwitz K.B., Costlow M.E., McGuire W.L. MCF-7; a human breast cancer cell line with estrogen, androgen, progesterone, and glucocorticoid receptors. Steroids 1975;26:785–95. doi: 10.1016/0039-128x(75)90110-5
  29. Freifeld M.L., Feil P.D., Bardin C.W. The in vivo regulation of the progesterone “receptor” in guinea pig uterus: dependence on estrogen and progesterone. Steroids 1974;23:93–103. doi: 10.1016/0039-128x(74)90143-3
  30. Horwitz K.B., McGuire W.L. Predicting response to endocrine therapy in human breast cancer: A hypothesis. Science 1975;189:726, 727. doi: 10.1126/science.168640
  31. McGuire W.L., Horwitz K.B., Pearson O.H., Segaloff A. Current status of estrogen and progesterone receptors in breast cancer. Cancer 1977;39(6 Suppl):2934–47. doi: 10.1002/1097-0142(197706)39:6<2934::aidcncr2820390680>3.0.co;2-p
  32. Osborne C.K. Steroid hormone receptors in breast cancer management. Breast Cancer Res Treat 1998;51:227–38. doi: 10.1023/a:1006132427948
  33. Olivotto I.A., Truong P.T., Speers C.H. et al. Time to stop progesterone receptor testing in breast cancer management. J Clin Oncol 2004;22(9):1769–70. doi: 10.1200/JCO.2004.99.251
  34. Colomer R., Beltran M., Dorcas J. et al. It is not time to stop progesterone receptor testing in breast cancer. J Clin Oncol 2005;23(16):3868–9. doi: 10.1200/JCO.2005.05.203
  35. Braun L., Mietzsch F., Seibold P. et al. Intrinsic breast cancer subtypes defined by estrogen receptor signalling-prognostic relevance of progesterone receptor loss. Mod Pathol 2013;26(9):1161–71. doi: 10.1038/modpathol.2013.60
  36. Prat A., Cheang M.C., Martín M. et al. Prognostic significance of progesterone receptor-positive tumor cells within immunohistochemically defined luminal A breast cancer. J Clin Oncol 2013;31(2):203–9. doi: 10.1200/JCO.2012.43.4134
  37. Perou C.M., Sorlie T., Eisen M.B. et al. Molecular portraits of human breast tumors. Nature 2000;406:747–52. doi: 10.1038/35021093
  38. Allison K.H., Hammond M.E.H., Dowsett M. et al. Estrogen and progesterone receptor testing in breast cancer: ASCO/CAP Guideline Update. J Clin Oncol 2020;38(12):1346–66. doi: 10.1200/JCO.19.02309
  39. Kunc M., Biernat W., Senkus-Konefka E. Estrogen receptornegative progesterone receptor-positive breast cancer – “Nobody’s land” or just an artifact? Cancer Treat Rev 2018;67:78–87. doi: 10.1016/j.ctrv.2018.05.005
  40. Beltjens F., Molly D., Bertaut A. et al. ER–/PR+ breast cancer: A distinct entity, which is morphologically and molecularly close to triple-negative breast cancer. Int J Cancer 2021;149(1):200–13. doi: 10.1002/ijc.33539
  41. Li Z., Tu Y., Wu Q. et al. Clinical characteristics and outcomes of single versus double hormone receptor-positive breast cancer in 2 large databases. Clin Breast Cancer 2020;20(2):e151–63. doi: 10.1016/j.clbc.2019.07.002
  42. Li Y., Yang D., Yin X. et al. Clinicopathological characteristics and breast cancer-specific survival of patients with single hormone receptor-positive breast cancer. JAMA Netw Open 2020;3(1):e1918160. doi: 10.1001/jamanetworkopen.2019.18160
  43. Zattarin E., Leporati R., Ligorio F. et al. Hormone receptor loss in breast cancer: Molecular mechanisms, clinical settings, and therapeutic implications. Cells 2020;9(12):2644. doi: 10.3390/cells9122644
  44. Creighton C.J., Kent Osborne C., van de Vijver M.J. et al. Molecular profiles of progesterone receptor loss in human breast tumors. Breast Cancer Res Treat 2009;114(2):287–99. doi: 10.1007/s10549-008-0017-2
  45. Thakkar J.P., Mehta D.G. A review of an unfavorable subset of breast cancer: Estrogen receptor positive progesterone receptor negative. Oncologist 2011;16(3):276–85. doi: 10.1634/theoncologist.2010-0302
  46. Fahlén M., Zhang H., Löfgren L. et al. Expression of progesterone and androgen receptors in the breast of premenopausal women, considering menstrual phase. Anticancer Res 2018;38(3):1499–510. doi: 10.21873/anticanres.12377
  47. Ruan Z.X., Su Y., Gu K. et al. Association of hormone-related characteristics and breast cancer risk by estrogen receptor/progesterone receptor status in the shanghai breast cancer study. Am J Epidemiol 2011;174(6):661–71. doi: 10.1093/aje/kwr145
  48. Fournier A., Fabre A., Mesrine S. et al. Use of different postmenopausal hormone therapies and risk of histologyand hormone receptor-defined invasive breast cancer. J Clin Oncol 2008;26(8):1260–8. doi: 10.1200/JCO.2007.13.4338
  49. Nevels R.M., Gontkovsky S.T., Williams B.E. Paroxetine – the antidepressant from hell? Probably not, but caution required. Psychopharmacol Bull 2016;46(1):77–104.
  50. Dembinski R., Prasath V., Bohnak C. et al. Estrogen receptor positive and progesterone receptor negative breast cancer: The role of hormone therapy. Horm Cancer 2020;11(3–4):148–54. doi: 10.1007/s12672-020-00387-1
  51. Larsson S.C., Bergkvist L., Wolk A. Long-term meat intake and risk of breast cancer by oestrogen and progesterone receptor status in a cohort of Swedish women. Eur J Cancer 2009;45(17):3042–6. doi: 10.1016/j.ejca.2009.04.035
  52. Loi S., Haibe-Kains B., Desmedt C. et al. Definition of clinically distinct molecular subtypes in estrogen receptor-positive breast carcinomas through genomic grade. J Clin Oncol 2007;25(10):1239–46. doi: 10.1200/JCO.2006.07.1522
  53. Yu K.D., Liu G.Y., Di G.H. et al. Progesterone receptor status provides predictive value for adjuvant endocrine therapy in older estrogen receptor-positive breast cancer patients. Breast 2007;16(3):307–15. doi: 10.1016/j.breast.2006.12.011
  54. Salmen J., Neugebauer J., Fasching P.A. et al. Pooled analysis of the prognostic relevance of progesterone receptor status in five German cohort studies. Breast Cancer Res Treat 2014;148(1):143–51. doi: 10.1007/s10549-014-3130-4
  55. Dunnwald L.K., Rossing M.A., Li C.I. Hormone receptor status, tumor characteristics, and prognosis: A prospective cohort of breast cancer patients. Breast Cancer Res 2007;9:R6. doi: 10.1186/bcr1639
  56. Petruolo O.A., Pilewskie M., Patil S. et al. Standard pathologic features can be used to identify a subset of estrogen receptorpositive, HER2 negative patients likely to benefit from neoadjuvant chemotherapy. Ann Surg Oncol 2017;24(9):2556–62. doi: 10.1245/s10434-017-5898-z
  57. Li Y., Yang D., Yin X. et al. Clinicopathological characteristics and breast cancer-specific survival of patients with single hormone receptor-positive breast cancer. JAMA Netw Open 2020;3(1):e1918160. doi: 10.1001/jamanetworkopen.2019.18160
  58. Van Mackelenbergh M.T., Denkert C., Nekljudova V. et al. Outcome after neoadjuvant chemotherapy in estrogen receptorpositive and progesterone receptor-negative breast cancer patients: A pooled analysis of individual patient data from ten prospectively randomized controlled neoadjuvant trials. Breast Cancer Res Treat 2018;167(1):59–71. doi: 10.1007/s10549-017-4480-5
  59. Davey M.G., Ryan É.J., Folan P.J. et al. The impact of progesterone receptor negativity on oncological outcomes in oestrogen-receptor-positive breast cancer. BJS Open 2021;5(3):zrab040. doi: 10.1093/bjsopen/zrab040
  60. Perez-Garcia J.M., Saura C., Munoz C. et al. Role of progesterone receptor status (PR) as predictive factor of pathologic complete response (pCR) to neoadjuvant chemotherapy (NACT) in breast cancer patients. JCO 2010;28:628. doi: 10.1200/jco.2010.28.15_suppl.628
  61. Dowsett M., Cuzick J., Wale C. et al. Role of progesterone receptor status (PR) as predictive factor of pathologic complete response (pCR) to neoadjuvant chemotherapy (NACT) in breast cancer patients. Retrospective analysis of time to recurrence in the ATAC trial according to hormone receptor status: An hypothesisgenerating study. J Clin Oncol 2005;23(30):7512–7. doi: 10.1200/JCO.2005.01.4829
  62. Early Breast Cancer Trialists’ Collaborative Group (EBCTCG), Davies C., Godwin J. et al. Relevance of breast cancer hormone receptors and other factors to the efficacy of adjuvant tamoxifen: Patient-level meta-analysis of randomised trials. Lancet 2011;378(9793):771–84. doi: 10.1016/S0140-6736(11)60993-8
  63. Nadal R., Fernandez A., Sanchez-Rovira P. et al. Biomarkers characterization of circulating tumour cells in breast cancer patients. Breast Cancer Res 2012;14(3):R71. doi: 10.1186/bcr3180
  64. Ahn S., Kim H.J., Kim M. et al. Negative conversion of progesterone receptor status after primary systemic therapy is associated with poor clinical outcome in patients with breast cancer. Cancer Res Treat 2018;50(4):1418–32. doi: 10.4143/crt.2017.552
  65. Ellis M.J., Tao Y., Luo J. et al. Outcome prediction for estrogen receptor-positive breast cancer based on postneoadjuvant endocrine therapy tumor characteristics. J Natl Cancer Inst 2008;100(19):1380–8. doi: 10.1093/jnci/djn309
  66. Milosevic J., Klinge J., Borg A.L. et al. Clinical instability of breast cancer markers is reflected in long-term in vitro estrogen deprivation studies. BMC Cancer 2013;13:473. doi: 10.1186/1471-2407-13-473
  67. Gambrell R.D.Jr., Bagnell C.A., Greenblatt R.B. Role of estrogens and progesterone in the etiology and prevention of endometrial cancer: Review. Am J Obstet Gynecol 1983;146:696–707. doi: 10.1016/0002-9378(83)91014-1
  68. Chlebowski R.T., Anderson G.L., Gass M. et al. Estrogen plus progestin and breast cancer incidence and mortality in postmenopausal women. JAMA 2010;304:1684–92. doi: 10.1001/jama.2010.1500
  69. Beral V., Reeves G., Bull D. et al. Breast cancer risk in relation to the interval between menopause and starting hormone therapy. J Natl Cancer Inst 2011;103:296–305. doi: 10.1093/jnci/djq527
  70. Collaborative Group on Hormonal Factors in Breast Cancer. Type and timing of menopausal hormone therapy and breast cancer risk: Individual participant meta-analysis of the worldwide epidemiological evidence. Lancet 2019;394(10204):1159–68. doi: 10.1016/S0140-6736(19)31709-X
  71. Piette P. The history of natural progesterone, the never-ending story. Climacteric 2018;21:308–14. doi: 10.1080/13697137.2018.1462792
  72. Carroll J.S., Hickey T.E., Tarulli G.A. et al. Deciphering the divergent roles of progestogens in breast cancer. Cancer 2017;17:54–64. doi: 10.1038/nrc.2016.116
  73. Boyd S. On oophorectomy in cancer of the breast. BMJ 1900;2:1161–87. doi: 10.1136/bmj.2.2077.1161
  74. Palmieri C., Patten D.K., Januszewski A. et al. Breast cancer: Current and future endocrine therapies. Mol Cell Endocrinol 2014;382:695–723. doi: 10.1016/j.mce.2013.08.001
  75. Pan H., Gray R., Braybrooke J. et al. 20-year risks of breast cancer recurrence after stopping endocrine therapy at 5 years. N Engl J Med 2017;377:1836–46. doi: 10.1056/NEJMoa1701830
  76. Turner N.C., Slamon D.J., Ro J. et al. Overall survival with palbociclib and fulvestrant in advanced breast cancer. N Engl J Med 2018;379:1926–36. doi: 10.1056/NEJMoa1810527
  77. Henderson I.C., Canellos G.P. Cancer of the breast: The past decade (first of two parts). N Engl J Med 1980;302:17–30. doi: 10.1056/NEJM198001033020104
  78. Santen R.J., Manni A., Harvey H., Redmond C. Endocrine treatment of breast cancer in women. Endocrine Rev 1990;11: 221–65. doi: 10.1210/edrv-11-2-221
  79. Walter K.R., Goodman M.L., Singhal H. et al. Interferonstimulated genes are transcriptionally repressed by PR in breast cancer. Mol Cancer Res 2017;15:1331–40. doi: 10.1158/1541-7786.MCR-17-0180
  80. Goodman M.L., Trinca G.M., Walter K.R. et al. Progesterone receptor attenuates STAT1-mediated IFN signaling in breast cancer. J Immunol 2019;202:3076–86. doi: 10.4049/jimmunol.1801152
  81. Klijn J.G., de Jong F.H., Bakker G.H. et al. Antiprogestins, a new form of endocrine therapy for human breast cancer. Cancer Res 1989;49(11):2851–6.
  82. Perrault D., Eisenhauer E.A., Pritchard K.I. et al. Phase II study of the progesterone antagonist mifepristone in patients with untreated metastatic breast carcinoma: A National Cancer Institute of Canada Clinical Trials Group study. J Clin Oncol 1996;14(10):2709–12. doi: 10.1200/JCO.1996.14.10.2709
  83. Romieu G., Maudelonde T., Ulmann A. et al. The antiprogestin RU486 in advanced breast cancer: Preliminary clinical trial. Bull Cancer 1987;74:455–61.
  84. Robertson J.F., Willsher P.C., Winterbottom L. et al. Onapristone, a progesterone receptor antagonist, as first-line therapy in primary breast cancer. Eur J Cancer 1999;35(2):214–8. doi: 10.1016/s0959-8049(98)00388-8
  85. Jonat W., Bachelot T., Ruhstaller T. et al. Randomized phase II study of lonaprisan as second-line therapy for progesterone receptor-positive breast cancer. Ann Oncol 2013;24:2543–48. doi: 10.1093/annonc/mdt216
  86. Klijn J.G., Setyono-Han B., Foekens J.A. Progesterone antagonists and progesterone receptor modulators in the treatment of breast cancer. Steroids 2000;65(10–11):825–30. doi: 10.1016/s0039-128x(00)00195-1
  87. Lee O., Sullivan M.E., Xu Y. et al. Selective progesterone receptor modulators in early-stage breast cancer: A randomized, placebocontrolled phase II window-of-opportunity trial using telapristone acetate. Clin Cancer Res 2020;26(1):25–34. doi: 10.1158/1078-0432
  88. Elía A., Saldain L., Vanzulli S.I. et al. Beneficial effects of mifepristone treatment in patients with breast cancer selected by the progesterone receptor isoform ratio: Results from the MIPRA Trial. Clin Cancer Res 2023;29(5):866–77. doi: 10.1158/1078-0432.CCR-22-2060
  89. Chen N., Saha P., Rampurwala M.M. et al. A randomized phase II trial of nab-paclitaxel with or without mifepristone for advanced triple-negative breast cancer. JCO 2023;41:e13103. doi: 10.1200/JCO.2023.41.16_suppl.e13103.
  90. Chen N., Michaels E., Saha P. et al. Phase II study of pembrolizumab plus mifepristone in patients with advanced HER2-negative breast cancer. JCO 2023;41:1095. doi: 10.1200/JCO.2023.41.16_suppl.1095
  91. Traina T.A., Chen Y., Khoury K. et al. TBCRC 058: A randomized phase II study of enzalutamide, enzalutamide with mifepristone, and treatment of physician’s choice in patients with androgen receptor-positive metastatic triple-negative or estrogen receptor-low breast cancer (NCT06099769 BCRC 058: A randomized phase II study of enzalutamide, enzalutamide with mifepristone, and treatment of physician’s choice in patients with androgen receptor-positive metastatic triple-negative or estrogen receptor-low breast cancer (NCT06099769). JCO 2024;42:1138. doi: 10.1200/JCO.2024.42.16_suppl.TPS1138
  92. Stringer Е.М., Saha P., Swoboda A. et al. A phase I trial of mifepristone (M), carboplatin (C), and gemcitabine (G) in advanced breast and ovarian cancer. JCO 2017;35:1083. doi: 10.1200/JCO.2017.35.15_suppl.1083
  93. Bellet M., Morales S., Gasol A. et al. Primary results of ONAWA (SOLTI-1802) trial: A window of opportunity trial of onapristone in postmenopausal women with progesterone receptor-positive/ HER2-negative early breast cancer (EBC). Cancer Res 2022;82(4 Suppl):P1-07-02. doi: 10.1158/1538-7445.SABCS21-P1-07-02

Supplementary files

Supplementary Files
Action
1. JATS XML
Download

Copyright (c) 2024


СМИ зарегистрировано Федеральной службой по надзору в сфере связи, информационных технологий и массовых коммуникаций (Роскомнадзор).
Регистрационный номер и дата принятия решения о регистрации СМИ: серия ПИ № ФС 77 - 36991 от  21.07.2009.