Progesterone receptor-B enhances estrogen responsiveness of breast cancer cells via scaffolding PELP1-and estrogen receptor-containing transcription complexes

Oncogene

Volumn 34, Issue 4, 2015, Pages 506-515

  Daniel, A R ^a   Gaviglio, A L ^a   Knutson, T P ^a   Ostrander, J H ^b   D'Assoro, A B ^c   Ravindranathan, P ^d   Peng, Y ^d   Raj, G V ^d   Yee, D ^a   Lange, C A ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

^b UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^c MAYO GRADUATE SCHOOL   (United States)

^d UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

breast cancer; cathepsin D; estrogen receptor; IGF1R; PELP1; progesterone receptor

Indexed keywords

CATHEPSIN D; COREPRESSOR PROTEIN; CTSD PROTEIN, HUMAN; DNA; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR ALPHA, HUMAN; PELP1 PROTEIN, HUMAN; PHOSPHATIDYLINOSITOL 3 KINASE; PROGESTERONE RECEPTOR; PROGESTERONE RECEPTOR B; SOMATOMEDIN C; SOMATOMEDIN C RECEPTOR; TAMOXIFEN; TRANSCRIPTION FACTOR;

BREAST NEOPLASMS; CELL PROLIFERATION; CHEMISTRY; DRUG EFFECTS; FEMALE; GENETIC TRANSCRIPTION; GENETICS; HUMAN; MCF 7 CELL LINE; METABOLISM; PATHOLOGY; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; SIGNAL TRANSDUCTION;

BREAST NEOPLASMS; CATHEPSIN D; CELL PROLIFERATION; CO-REPRESSOR PROTEINS; DNA; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; FEMALE; HUMANS; INSULIN-LIKE GROWTH FACTOR I; MCF-7 CELLS; PHOSPHATIDYLINOSITOL 3-KINASES; PROTEIN STRUCTURE, TERTIARY; RECEPTOR CROSS-TALK; RECEPTOR, IGF TYPE 1; RECEPTORS, PROGESTERONE; TAMOXIFEN; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 85028266773     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2013.579     Document Type: Article

References (50)

1. Early Breast Cancer Trialists' Collaborative Group (EBCTCG). Effects of chemotherapy and hormonal therapy for early breast cancer on recurrence and 15-year survival: an overview of the randomised trials. Lancet 2005; 365: 1687-1717.
2. Davies C, Godwin J, Gray R, Clarke M, Cutter D, Darby S 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: 771-784.
3. Musgrove EA, Sutherland RL. Biological determinants of endocrine resistance in breast cancer. Nat Rev Cancer 2009; 9: 631-643.
4. de Leeuw R, Neefjes J, Michalides R. A role for estrogen receptor phosphorylation in the resistance to tamoxifen. Int J Breast Cancer 2011; 2011: 232435.
5. Vallabhaneni S, Nair BC, Cortez V, Challa R, Chakravarty D, Tekmal RR et al. Significance of ER-Src axis in hormonal therapy resistance. Breast Cancer Res Treat 2011; 130: 377-385.
6. Ballare C, Uhrig M, Bechtold T, Sancho E, Di Domenico M, Migliaccio A et al. Two domains of the progesterone receptor interact with the estrogen receptor and are required for progesterone activation of the c-Src/Erk pathway in mammalian cells. Mol Cell Biol 2003; 23: 1994-2008.
7. Shimizu T, Krebs S, Bauersachs S, Blum H, Wolf E, Miyamoto A. Actions and interactions of progesterone and estrogen on transcriptome profiles of the bovine endometrium. Physiol Genom 2010; 42A: 290-300.
8. Daniel AR, Hagan CR, Lange CA. Progesterone receptor action: defining a role in breast cancer. Expert Rev Endocrinol Metab 2011; 6: 359-369.
9. Proietti CJ, Rosemblit C, Beguelin W, Rivas MA, Diaz Flaque MC, Charreau EH et al. Activation of Stat3 by heregulin/ErbB-2 through the co-option of progesterone receptor signaling drives breast cancer growth. Mol Cell Biol 2009; 29: 1249-1265.
10. Daniel AR, Lange CA. Protein kinases mediate ligand-independent derepression of sumoylated progesterone receptors in breast cancer cells. Proc Natl Acad Sci USA 2009; 106: 14287-14292.
11. Hagan CR, Regan TM, Dressing GE, Lange CA. Ck2-dependent phosphorylation of progesterone receptors (PR) on Ser81 regulates PR-B isoform-specific target gene expression in breast cancer cells. Mol Cell Biol 2011; 31: 2439-2452.
12. Knutson TP, Daniel AR, Fan D, Silverstein KA, Covington KR, Fuqua SA et al. Phosphorylated and sumoylation-deficient progesterone receptors drive proliferative gene signatures during breast cancer progression. Breast Cancer Res 2012; 14: R95.
13. Gupta A, Mehta R, Alimirah F, Peng X, Murillo G, Wiehle R et al. Efficacy and mechanism of action of Proellex, an antiprogestin in aromatase overexpressing and Letrozole resistant T47D breast cancer cells. J Steroid Biochem Mol Biol 2013; 133: 30-42.
14. Giulianelli S, Vaque JP, Soldati R, Wargon V, Vanzulli SI, Martins R et al. Estrogen receptor alpha mediates progestin-induced mammary tumor growth by interacting with progesterone receptors at the cyclin D1/MYC promoters. Cancer Res 2012; 72: 2416-2427.
15. Hilton HN, Graham JD, Kantimm S, Santucci N, Cloosterman D, Huschtscha LI et al. Progesterone and estrogen receptors segregate into different cell subpopulations in the normal human breast. Mol Cell Endocrinol 2012; 361: 191-201.
16. Zukiwski AA. Independent characterization by duel staining of progesterone receptor (PR) and estrogen receptor (ER) in breast cancer (BC). Abstract No. 596 from the ASCO (American Society for Clinical Oncology) Meeting. Chicago, IL, 2013.
17. Brisken C, O'Malley B. Hormone action in the mammary gland. Cold Spring Harb Perspect Biol 2010; 2: a003178.
18. Faivre EJ, Lange CA. Progesterone receptors upregulate Wnt-1 to induce epidermal growth factor receptor transactivation and c-Src-dependent sustained activation of Erk1/2 mitogen-activated protein kinase in breast cancer cells. Mol Cell Biol 2007; 27: 466-480.
19. Boonyaratanakornkit V, Scott MP, Ribon V, Sherman L, Anderson SM, Maller JL et al. Progesterone receptor contains a proline-rich motif that directly interacts with SH3 domains and activates c-Src family tyrosine kinases. Mol Cell 2001; 8: 269-280.
20. Fagan DH, Yee D. Crosstalk between IGF1R and estrogen receptor signaling in breast cancer. J Mammary Gland Biol Neoplasia 2008; 13: 423-429.
21. Smid M, Wang Y, Zhang Y, Sieuwerts AM, Yu J, Klijn JG et al. Subtypes of breast cancer show preferential site of relapse. Cancer Res 2008; 68: 3108-3114.
22. Massarweh S, Osborne CK, Creighton CJ, Qin L, Tsimelzon A, Huang S et al. Tamoxifen resistance in breast tumors is driven by growth factor receptor signaling with repression of classic estrogen receptor genomic function. Cancer Res 2008; 68: 826-833.
23. Riggins RB, Lan JP, Zhu Y, Klimach U, Zwart A, Cavalli LR et al. ERRgamma mediates tamoxifen resistance in novel models of invasive lobular breast cancer. Cancer Res 2008; 68: 8908-8917.
24. Doane AS, Danso M, Lal P, Donaton M, Zhang L, Hudis C et al. An estrogen receptor-negative breast cancer subset characterized by a hormonally regulated transcriptional program and response to androgen. Oncogene 2006; 25: 3994-4008.
25. Chia SK, Bramwell VH, Tu D, Shepherd LE, Jiang S, Vickery T et al. A 50-gene intrinsic subtype classifier for prognosis and prediction of benefit from adjuvant tamoxifen. Clin Cancer Res 2012; 18: 4465-4472.
26. Becker MA, Ibrahim YH, Cui X, Lee AV, Yee D. The IGF pathway regulates ERalpha through a S6K1-dependent mechanism in breast cancer cells. Mol Endocrinol 2011; 25: 516-528.
27. Gao J, Aksoy BA, Dogrusoz U, Dresdner G, Gross B, Sumer SO et al. Integrative analysis of complex cancer genomics and clinical profiles using the cBioPortal. Sci Signal 2013; 6: p51.
28. 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 Res Treat 2002; 72: 163-172.
29. Bretschneider N, Kangaspeska S, Seifert M, Reid G, Gannon F, Denger S. E2-mediated cathepsin D (CTSD) activation involves looping of distal enhancer elements. Mol Oncol 2008; 2: 182-190.
30. Shang Y, Hu X, DiRenzo J, Lazar MA, Brown M. Cofactor dynamics and sufficiency in estrogen receptor-regulated transcription. Cell 2000; 103: 843-852.
31. Daniel AR, Knutson TP, Lange CA. Signaling inputs to progesterone receptor gene regulation and promoter selectivity. Mol Cell Endocrinol 2009; 308: 47-52.
32. Chakravarty D, Tekmal RR, Vadlamudi RK. PELP1: a novel therapeutic target for hormonal cancers. IUBMB Life 2010; 62: 162-169.
33. Cheskis BJ, Greger J, Cooch N, McNally C, McLarney S, Lam HS et al. MNAR plays an important role in ERa activation of Src/MAPK and PI3K/Akt signaling pathways. Steroids 2008; 73: 901-905.
34. Vadlamudi RK, Manavathi B, Balasenthil S, Nair SS, Yang Z, Sahin AA et al. Functional implications of altered subcellular localization of PELP1 in breast cancer cells. Cancer Res 2005; 65: 7724-7732.
35. Fox EM, Bernaciak TM, Wen J, Weaver AM, Shupnik MA, Silva CM. Signal transducer and activator of transcription 5b, c-Src, and epidermal growth factor receptor signaling play integral roles in estrogen-stimulated proliferation of estrogen receptor-positive breast cancer cells. Mol Endocrinol 2008; 22: 1781-1796.
36. Leontovich AA, Zhang S, Quatraro C, Iankov I, Veroux PF, Gambino MW et al. Raf-1 oncogenic signaling is linked to activation of mesenchymal to epithelial transition pathway in metastatic breast cancer cells. Int J Oncol 2012; 40: 1858-1864.
37. Byron SA, Horwitz KB, Richer JK, Lange CA, Zhang X, Yee D. Insulin receptor substrates mediate distinct biological responses to insulin-like growth factor receptor activation in breast cancer cells. Br J Cancer 2006; 95: 1220-1228.
38. Zhang Y, P Janet, Z Chen, JS David, N Steven. Progesterone receptor binds to an estrogen response element, and antagonizes estrogen receptor-mediated gene induction. The role of DNA as a functional ligand. Keystone Symposia on Molecular and Cellular Biology 2008 Abstract Book. 7 March 2008.
39. Tang Q, Chen Y, Meyer C, Geistlinger T, Lupien M, Wang Q et al. A comprehensive view of nuclear receptor cancer cistromes. Cancer Res 2011; 71: 6940-6947.
40. Fox EM, Arteaga CL, Miller TW. Abrogating endocrine resistance by targeting ERalpha and PI3K in breast cancer. Front Oncol 2012; 2: 145.
41. Baselga J. Targeting the phosphoinositide-3 (PI3) kinase pathway in breast cancer. Oncologist 2011; 16(Suppl 1): 12-19.
42. Likhite VS, Stossi F, Kim K, Katzenellenbogen BS, Katzenellenbogen JA. Kinasespecific phosphorylation of the estrogen receptor changes receptor interactions with ligand, deoxyribonucleic acid, and coregulators associated with alterations in estrogen and tamoxifen activity. Mol Endocrinol 2006; 20: 3120-3132.
43. Riggins RB, Schrecengost RS, Guerrero MS, Bouton AH. Pathways to tamoxifen resistance. Cancer Lett 2007; 256: 1-24.
44. Casa AJ, Dearth RK, Litzenburger BC, Lee AV, Cui X. The type I insulin-like growth factor receptor pathway: a key player in cancer therapeutic resistance. Front Biosci 2008; 13: 3273-3287.
45. Fagan DH, Uselman RR, Sachdev D, Yee D. Acquired resistance to tamoxifen is associated with loss of the type I insulin-like growth factor receptor: implications for breast cancer treatment. Cancer Res 2012; 72: 3372-3380.
46. Aupperlee MD, Haslam SZ. Differential hormonal regulation and function of progesterone receptor isoforms in normal adult mouse mammary gland. Endocrinology 2007; 148: 2290-2300.
47. Encarnacion CA, Ciocca DR, McGuire WL, Clark GM, Fuqua SA, Osborne CK. Measurement of steroid hormone receptors in breast cancer patients on tamoxifen. Breast Cancer Res Treat 1993; 26: 237-246.
48. Johnston SR, Saccani-Jotti G, Smith IE, Salter J, Newby J, Coppen M et al. Changes in estrogen receptor, progesterone receptor, and pS2 expression in tamoxifenresistant human breast cancer. Cancer Res 1995; 55: 3331-3338.
49. Lanari C, Wargon V, Rojas P, Molinolo AA. Antiprogestins in breast cancer treatment: are we ready? Endocr Relat Cancer 2012; 19: R35-R50.
50. Sachdev D, Li SL, Hartell JS, Fujita-Yamaguchi Y, Miller JS, Yee D. A chimeric humanized single-chain antibody against the type I insulin-like growth factor (IGF) receptor renders breast cancer cells refractory to the mitogenic effects of IGF-I. Cancer Res 2003; 63: 627-635.