Hypermethylation of the progesterone receptor A in constitutive antiprogestin-resistant mouse mammary carcinomas

Breast Cancer Research and Treatment

Volumn 126, Issue 2, 2011, Pages 319-332

  Wargon, Victoria ^a   Fernandez, Sandra V ^b   Goin, Mercedes ^c   Giulianelli, Sebastián ^a   Russo, Jose ^b   Lanari, Claudia ^a  

^a Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

^b FOX CHASE CANCER CENTER   (United States)

^c INST DE BIOL Y MED EXPERIMENTAL   (Argentina)

Author keywords

DNA methylation; DNMT inhibitors; Hormone resistance; Mammary carcinomas; Progesterone receptors

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; DNA METHYLTRANSFERASE 1; DNA METHYLTRANSFERASE 3B; GLUCOCORTICOID RECEPTOR; MIFEPRISTONE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROGESTERONE RECEPTOR A; PROTEIN P16; RETINOBLASTOMA PROTEIN; RETINOIC ACID RECEPTOR BETA; UVOMORULIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BREAST CANCER; CANCER RESISTANCE; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; EXON; FEMALE; FIBROBLAST; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION;

ANIMALS; APOPTOSIS; AZACITIDINE; CELL CULTURE TECHNIQUES; CELL LINE, TUMOR; COCULTURE TECHNIQUES; DNA METHYLATION; DNA MODIFICATION METHYLASES; DRUG RESISTANCE, NEOPLASM; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE SILENCING; HORMONE ANTAGONISTS; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; MICE, INBRED BALB C; MIFEPRISTONE; MITOSIS; NEOPLASM TRANSPLANTATION; PROMOTER REGIONS, GENETIC; RECEPTORS, GLUCOCORTICOID; RECEPTORS, PROGESTERONE; TRANSPLANTATION, HETEROLOGOUS; TUMOR BURDEN;

EID: 79958709933     PISSN: 01676806     EISSN: 15737217     Source Type: Journal    
DOI: 10.1007/s10549-010-0908-x     Document Type: Article

References (57)

1. Santen RJ, Manni A, Harvey H, Redmond C (1990) Endocrine treatment of breast cancer in women. Endocr Rev 11:221-265 (Pubitemid 20182870)
2. Normanno N, Di Maio M, De Maio E, De Luca A, de Matteis A, Giordano A, Perrone F (2005) Mechanisms of endocrine resistance and novel therapeutic strategies in breast cancer. Endocr Relat Cancer 12:721-747 (Pubitemid 41815773)
3. Kastner P, Krust A, Turcotte B, Stropp U, Tora L, Gronemeyer H, Chambon P (1990) Two distinct estrogen-regulated promoters generate transcripts encoding the two functionally different human progesterone receptor forms A and B. EMBO J 9:1603-1614
4. Kraus WL, 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 132:2371-2379 (Pubitemid 23156884)
5. Richer JK, Jacobsen BM, Manning NG, Abel MG, Wolf DM, Horwitz KB (2002) Differential gene regulation by the two progesterone receptor isoforms in human breast cancer cells. J Biol Chem 277:5209-5218 (Pubitemid 34968565)
6. Hopp TA, Weiss HL, Hilsenbeck SG, Cui Y, Allred DC, Horwitz KB, Fuqua SA (2004) Breast cancer patients with progesterone receptor PR-A-rich tumors have poorer disease-free survival rates. Clin Cancer Res 10:2751-2760 (Pubitemid 38509151)
7. Long BJ, Jelovac D, Handratta V, Thiantanawat A, MacPherson N, Ragaz J, Goloubeva OG, Brodie AM (2004) Therapeutic strategies using the aromatase inhibitor letrozole and tamoxifen in a breast cancer model. J Natl Cancer Inst 96:456-465 (Pubitemid 38443649)
8. Macedo LF, Sabnis GJ, Goloubeva OG, Brodie A (2008) Combination of anastrozole with fulvestrant in the intratumoral aromatase xenograft model. Cancer Res 68:3516-3522
9. Lanari C, Molinolo AA, Pasqualini CD (1986) Induction of mammary adenocarcinomas by medroxyprogesterone acetate in BALB/c female mice. Cancer Lett 33:215-223 (Pubitemid 17194510)
10. Molinolo AA, Lanari C, Charreau EH, Sanjuan N, Pasqualini CD (1987) Mouse mammary tumors induced by medroxyprogesterone acetate: immunohistochemistry and hormonal receptors. J Natl Cancer Inst 79:1341-1350 (Pubitemid 18036740)
11. Lanari C, Lamb CA, Fabris VT, Helguero LA, Soldati R, Bottino MC, Giulianelli S, Cerliani JP, Wargon V, Molinolo A (2009) The MPA mouse breast cancer model: evidence for a role of progesterone receptors in breast cancer. Endocr Relat Cancer 16:333-350
12. Helguero LA, Viegas M, Asaithamby A, Shyamala G, Lanari C, Molinolo AA (2003) Progesterone receptor expression in medroxyprogesterone acetate-induced murine mammary carcinomas and response to endocrine treatment. Breast Cancer Res Treat 79:379-390 (Pubitemid 36750945)
13. Wargon V, Helguero LA, Bolado J, Rojas P, Novaro V, Molinolo A, Lanari C (2009) Reversal of antiprogestin resistance and progesterone receptor isoform ratio in acquired resistant mammary carcinomas. Breast Cancer Res Treat 116:449-460
14. Momparler RL, Bovenzi V (2000) DNA methylation and cancer. J Cell Physiol 183:145-154 (Pubitemid 30185933)
15. Palii SS, Van Emburgh BO, Sankpal UT, Brown KD, Robertson KD (2008) DNA methylation inhibitor 5-Aza-2'-deoxycytidine induces reversible genome-wide DNA damage that is distinctly influenced by DNA methyltransferases 1 and 3B. Mol Cell Biol 28:752-771
16. Brinkman JA, El Ashry D (2009) ER re-expression and re-sensitization to endocrine therapies in ER-negative breast cancers. J Mammary Gland Biol Neoplasia 14:67-78
17. Jones PA, Baylin SB (2002) The fundamental role of epigenetic events in cancer. Nat Rev Genet 3:415-428 (Pubitemid 34587077)
18. Roll JD, Rivenbark AG, Jones WD, Coleman WB (2008) DNMT3b overexpression contributes to a hypermethylator phenotype in human breast cancer cell lines. Mol Cancer 7:15
19. Ferguson AT, Lapidus RG, Baylin SB, Davidson NE (1995) Demethylation of the estrogen receptor gene in estrogen receptornegative breast cancer cells can reactivate estrogen receptor gene expression. Cancer Res 55:2279-2283
20. Ferguson DJ, Anderson TJ (1981) Morphological evaluation of cell turnover in relation to the menstrual cycle in the "resting" human breast. Br J Cancer 44:177-181 (Pubitemid 11039573)
21. Lapidus RG, Ferguson AT, Ottaviano YL, Parl FF, Smith HS, Weitzman SA, Baylin SB, Issa JP, Davidson NE (1996) Methylation of estrogen and progesterone receptor gene 5' CpG islands correlates with lack of estrogen and progesterone receptor gene expression in breast tumors. Clin Cancer Res 2:805-810
22. Nass SJ, Herman JG, Gabrielson E, Iversen PW, Parl FF, Davidson NE, Graff JR (2000) Aberrant methylation of the estrogen receptor and E-cadherin 5' CpG islands increases with malignant progression in human breast cancer. Cancer Res 60:4346-4348 (Pubitemid 32103608)
23. Bird AP (1986) CpG-rich islands and the function of DNA methylation. Nature 321:209-213 (Pubitemid 16016411)
24. Lapidus RG, Nass SJ, Davidson NE (1998) The loss of estrogen and progesterone receptor gene expression in human breast cancer. J Mammary Gland Biol Neoplasia 3:85-94 (Pubitemid 128513222)
25. Ottaviano YL, Issa JP, Parl FF, Smith HS, Baylin SB, Davidson NE (1994) Methylation of the estrogen receptor gene CpG island marks loss of estrogen receptor expression in human breast cancer cells. Cancer Res 54:2552-2555 (Pubitemid 24173735)
26. Yang X, Yan L, Davidson NE (2001) DNA methylation in breast cancer. Endocr Relat Cancer 8:115-127 (Pubitemid 32641353)
27. Institute of Laboratory Animal Resources CoLSNRC (1996) Guide for the care and use of laboratory animals. National Academy Press, Washington, DC
28. Vanzulli S, Efeyan A, Benavides F, Helguero L, Peters G, Shen J, Conti CJ, Lanari C, Molinolo A (2002) p21, p27 and p53 in estrogen and antiprogestin-induced tumor regression of experimental mouse mammary ductal carcinomas. Carcinogenesis 23:749-757 (Pubitemid 34567513)
29. Frommer M, McDonald LE, Millar DS, Collis CM, Watt F, Grigg GW, Molloy PL, Paul CL (1992) A genomic sequencing protocol that yields a positive display of 5-methylcytosine residues in individual DNA strands. Proc Natl Acad Sci USA 89:1827-1831
30. Hagihara K, Wu-Peng XS, Funabashi T, Kato J, Pfaff DW (1994) Nucleic acid sequence and DNase hypersensitive sites of the 5' region of the mouse progesterone receptor gene. Biochem Biophys Res Commun 205:1093-1101
31. Lanari C, Luthy I, Lamb CA, Fabris V, Pagano E, Helguero LA, Sanjuan N, Merani S, Molinolo AA (2001) Five novel hormone-responsive cell lines derived from murine mammary ductal carcinomas: in vivo and in vitro effects of estrogens and progestins. Cancer Res 61:293-302 (Pubitemid 32095730)
32. Giulianelli S, Cerliani JP, Lamb CA, Fabris VT, Bottino MC, Gorostiaga MA, Novaro V, Gongora A, Baldi A, Molinolo A, Lanari C (2008) Carcinoma-associated fibroblasts activate progesterone receptors and induce hormone independent mammary tumor growth: A role for the FGF-2/FGFR-2 axis. Int J Cancer 123:2518-2531
33. Lamb C, Simian M, Molinolo A, Pazos P, Lanari C (1999) Regulation of cell growth of a progestin-dependent murine mammary carcinoma in vitro: progesterone receptor involvement in serum or growth factor-induced cell proliferation. J Steroid Biochem Mol Biol 70:133-142 (Pubitemid 29528423)
34. Mirza S, Sharma G, Prasad CP, Parshad R, Srivastava A, Gupta SD, Ralhan R (2007) Promoter hypermethylation of TMS1, BRCA1, ERalpha and PRB in serum and tumor DNA of invasive ductal breast carcinoma patients. Life Sci 81:280-287 (Pubitemid 47030571)
35. Leu YW, Yan PS, Fan M, Jin VX, Liu JC, Curran EM, Welshons WV, Wei SH, Davuluri RV, Plass C, Nephew KP, Huang TH (2004) Loss of estrogen receptor signaling triggers epigenetic silencing of downstream targets in breast cancer. Cancer Res 64:8184-8192 (Pubitemid 39491754)
36. Vasilatos SN, Broadwater G, Barry WT, Baker JC Jr, Lem S, Dietze EC, Bean GR, Bryson AD, Pilie PG, Goldenberg V, Skaar D, Paisie C, Torres-Hernandez A, Grant TL, Wilke LG, Ibarra-Drendall C, Ostrander JH, D'Amato NC, Zalles C, Jirtle R, Weaver VM, Seewaldt VL (2009) CpG island tumor suppressor promoter methylation in non-BRCA-associated early mammary carcinogenesis. Cancer Epidemiol Biomarkers Prev 18:901-914
37. Ferguson AT, Lapidus RG, Davidson NE (1998) Demethylation of the progesterone receptor CpG island is not required for progesterone receptor gene expression. Oncogene 17:577-583 (Pubitemid 28401026)
38. Sharma D, Saxena NK, Davidson NE, Vertino PM (2006) Restoration of tamoxifen sensitivity in estrogen receptor-negative breast cancer cells: tamoxifen-bound reactivated ER recruits distinctive corepressor complexes. Cancer Res 66:6370-6378
39. Fan J, Yin WJ, Lu JS, Wang L, Wu J, Wu FY, Di GH, Shen ZZ, Shao ZM (2008) ER alpha negative breast cancer cells restore response to endocrine therapy by combination treatment with both HDAC inhibitor and DNMT inhibitor. J Cancer Res Clin Oncol 134:883-890
40. Pazos P, Lanari C, Meiss R, Charreau EH, Pasqualini CD (1992) Mammary carcinogenesis induced by N-methyl-N-nitrosourea (MNU) and medroxyprogesterone acetate (MPA) in BALB/c mice. Breast Cancer Res Treat 20:133-138
41. Russo IH, Gimotty P, Dupuis M, Russo J (1989) Effect of medroxyprogesterone acetate on the response of the rat mammary gland to carcinogenesis. Br J Cancer 59:210-216 (Pubitemid 19072719)
42. Aldaz CM, Liao QY, Paladugu A, Rehm S, Wang H (1996) Allelotypic and cytogenetic characterization of chemically induced mouse mammary tumors: high frequency of chromosome 4 loss of heterozygosity at advanced stages of progression. Mol Carcinog 17:126-133 (Pubitemid 26408187)
43. Horwitz KB, Tung L, Takimoto GS (1996) Novel mechanisms of antiprogestin action. Acta Oncol 35:129-140 (Pubitemid 26155137)
44. Hyder SM, Murthy L, Stancel GM (1998) Progestin regulation of vascular endothelial growth factor in human breast cancer cells. Cancer Res 58:392-395 (Pubitemid 28087395)
45. Goepfert TM, McCarthy M, Kittrell FS, Stephens C, Ullrich RL, Brinkley BR, Medina D (2000) Progesterone facilitates chromosome instability (aneuploidy) in p53 null normal mammary epithelial cells. FASEB J 14:2221-2229
46. Lydon JP, Ge G, Kittrell FS, Medina D, O'Malley BW (1999) Murine mammary gland carcinogenesis is critically dependent on progesterone receptor function. Cancer Res 59:4276-4284 (Pubitemid 29418743)
47. Women's Health Initiative (2002) Risks and benefits of estrogen plus progestin in healthy postmenopausal women principal results From the Women's Health Initiative randomized controlled trial. JAMA 288:321-333
48. Beral V (2003) Breast cancer and hormone-replacement therapy in the Million Women Study. Lancet 362:419-427 (Pubitemid 36999703)
49. Klijn JG, Setyono-Han B, Foekens JA (2000) Progesterone antagonists and progesterone receptor modulators in the treatment of breast cancer. Steroids 65:825-830
50. Moore MR (2004) A rationale for inhibiting progesterone-related pathways to combat breast cancer. Curr Cancer Drug Targets 4:183-189 (Pubitemid 38332555)
51. Gaddy VT, Barrett JT, Delk JN, Kallab AM, Porter AG, Schoenlein PV (2004) Mifepristone induces growth arrest, cas-pase activation, and apoptosis of estrogen receptor-expressing, antiestrogen-resistant breast cancer cells. Clin Cancer Res 10:5215-5225 (Pubitemid 39099796)
52. Horwitz KB (1992) The molecular biology of RU486. Is there a role for antiprogestins in the treatment of breast cancer? Endocr Rev 13:146-163
53. Montecchia MF, Lamb C, Molinolo AA, Luthy IA, Pazos P, Charreau E, Vanzulli S, Lanari C (1999) Progesterone receptor involvement in independent tumor growth in MPA-induced murine mammary adenocarcinomas. J Steroid Biochem Mol Biol 68:11-21 (Pubitemid 29130381)
54. Lamb CA, Helguero LA, Giulianelli S, Soldati R, Vanzulli SI, Molinolo A, Lanari C (2005) Antisense oligonucleotides targeting the progesterone receptor inhibit hormone-independent breast cancer growth in mice. Breast Cancer Res 7:R1111-R1121
55. Lyko F, Brown R (2005) DNA methyltransferase inhibitors and the development of epigenetic cancer therapies. J Natl Cancer Inst 97:1498-1506 (Pubitemid 41631949)
56. O'Brien CS, Howell SJ, Farnie G, Clarke RB (2009) Resistance to endocrine therapy: are breast cancer stem cells the culprits? J Mammary Gland Biol Neoplasia 14:45-54
57. Lin HJ, Zuo T, Lin CH, Kuo CT, Liyanarachchi S, Sun S, Shen R, Deatherage DE, Potter D, Asamoto L, Lin S, Yan PS, Cheng AL, Ostrowski MC, Huang TH (2008) Breast cancer-associated fibroblasts confer AKT1-mediated epigenetic silencing of Cystatin M in epithelial cells. Cancer Res 68:10257-10266