Chemopreventive effect of ERβ-Selective agonist on intestinal tumorigenesis in ApcMin/+ Mice

Molecular Carcinogenesis

Volumn 50, Issue 5, 2011, Pages 359-369

  Giroux, Véronique ^a   Bernatchez, Gérald ^a   Carrier, Julie C ^a  

^a UNIVERSITY OF SHERBROOKE   (Canada)

Author keywords

Colon cancer; Estrogen receptor beta; TGF

Indexed keywords

APC PROTEIN; BROXURIDINE; CASPASE 3; DIARYLPROPIONITRILE; ESTROGEN RECEPTOR BETA; HORMONE RECEPTOR STIMULATING AGENT; PROTEIN P27; SMAD2 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA1; TRANSFORMING GROWTH FACTOR BETA3;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER RISK; CARCINOGENESIS; COLON MUCOSA; CONTROLLED STUDY; FEMALE; INTESTINE TUMOR; JEJUNUM; MALE; MOUSE; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; QUANTITATIVE ANALYSIS; TREATMENT DURATION;

MUS;

EID: 79953773923     PISSN: 08991987     EISSN: 10982744     Source Type: Journal    
DOI: 10.1002/mc.20719     Document Type: Article

References (58)

1. Potter JD. Colorectal cancer: Molecules and populations. J Natl Cancer Inst 1999; 91: 916-932.
2. Chlebowski RT, Wactawski-Wende J, Ritenbaugh C, et al. Estrogen plus progestin and colorectal cancer in postmenopausal women. N Engl J Med 2004; 350: 991-1004.
3. Smirnoff P, Liel Y, Gnainsky J, Shany S, Schwartz B. The protective effect of estrogen against chemically induced murine colon carcinogenesis is associated with decreased CpG island methylation and increased mRNA and protein expression of the colonic vitamin D receptor. Oncol Res 1999; 11: 255-264.
4. Weyant MJ, Carothers AM, Mahmoud NN, et al. Reciprocal expression of ERalpha and ERbeta is associated with estrogen-mediated modulation of intestinal tumorigenesis. Cancer Res 2001; 61: 2547-2551.
5. Javid SH, Moran AE, Carothers AM, Redston M, Bertagnolli MM. Modulation of tumor formation and intestinal cell migration by estrogens in the apc(min/+) mouse model of colorectal cancer. Carcinogenesis 2005; 26: 587-595.
6. Pearce ST, Jordan VC. The biological role of estrogen receptors alpha and beta in cancer. Crit Rev Oncol Hematol 2004; 50: 3-22.
7. Nilsson S, Makela S, Treuter E, et al. Mechanisms of estrogen action. Physiol Rev 2001; 81: 1535-1565.
8. Couse JF, Korach KS. Estrogen receptor null mice: What have we learned and where will they lead us? Endocr Rev 1999; 20: 358-417.
9. Campbell-Thompson M, Reyher KK, Wilkinson LB. Immunolocalization of estrogen receptor alpha and beta in gastric epithelium and enteric neurons. J Endocrinol 2001; 171: 65-73.
10. Foley EF, Jazaeri AA, Shupnik MA, Jazaeri O, Rice LW. Selective loss of estrogen receptor beta in malignant human colon. Cancer Res 2000; 60: 245-248.
11. Konstantinopoulos PA, Kominea A, Vandoros G, et al. Oestrogen receptor beta (ERbeta) is abundantly expressed in normal colonic mucosa, but declines in colon adenocarcinoma paralleling the tumour's dedifferentiation. Eur J Cancer 2003; 39: 1251-1258.
12. Bardin A, Boulle N, Lazennec G, Vignon F, Pujol P. Loss of ERbeta expression as a common step in estrogen-dependent tumor progression. Endocr Relat Cancer 2004; 11: 537-551.
13. Jassam N, Bell SM, Speirs V, Quirke P. Loss of expression of oestrogen receptor beta in colon cancer and its association with dukes' staging. Oncol Rep 2005; 14: 17-21.
14. Lazennec G, Bresson D, Lucas A, Chauveau C, Vignon F. ER beta inhibits proliferation and invasion of breast cancer cells. Endocrinology 2001; 142: 4120-4130.
15. Bardin A, Hoffmann P, Boulle N, et al. Involvement of estrogen receptor beta in ovarian carcinogenesis. Cancer Res 2004; 64: 5861-5869.
16. Cheng J, Lee EJ, Madison LD, Lazennec G. Expression of estrogen receptor beta in prostate carcinoma cells inhibits invasion and proliferation and triggers apoptosis. FEBS Lett 2004; 566: 169-172.
17. Martineti V, Picariello L, Tognarini I, et al. ERbeta is a potent inhibitor of cell proliferation in the HCT8 human colon cancer cell line through regulation of cell cycle components. Endocr Relat Cancer 2005; 12: 455-469.
18. Harris HA. Estrogen receptor-beta: Recent lessons from in vivo studies. Mol Endocrinol 2007; 21: 1-13.
19. Moser AR, Pitot HC, Dove WF. A dominant mutation that predisposes to multiple intestinal neoplasia in the mouse. Science 1990; 247: 322-324.
20. Powell SM, Zilz N, Beazer-Barclay Y, et al. APC mutations occur early during colorectal tumorigenesis. Nature 1992; 359: 235-237.
21. Nishisho I, Nakamura Y, Miyoshi Y, et al. Mutations of chromosome 5q21 genes in FAP and colorectal cancer patients. Science 1991; 253: 665-669.
22. Su LK, Kinzler KW, Vogelstein B, et al. Multiple intestinal neoplasia caused by a mutation in the murine homolog of the APC gene. Science 1992; 256: 668-670.
23. Corpet DE, Pierre F. Point: From animal models to prevention of colon cancer. systematic review of chemoprevention in min mice and choice of the model system. Cancer Epidemiol Biomarkers Prev 2003; 12: 391-400.
24. min/+ mice. Int J Cancer 2008; 123: 303-311.
25. Takaku K, Oshima M, Miyoshi H, Matsui M, Seldin MF, Taketo MM. Intestinal tumorigenesis in compound mutant mice of both Dpc4 (Smad4) and apc genes. Cell 1998; 92: 645-656.
26. Munoz NM, Upton M, Rojas A, et al. Transforming growth factor beta receptor type II inactivation induces the malignant transformation of intestinal neoplasms initiated by apc mutation. Cancer Res 2006; 66: 9837-9844.
27. Perreault N, Beaulieu JF. Primary cultures of fully differentiated and pure human intestinal epithelial cells. Exp Cell Res 1998; 245: 34-42.
28. Harris HA, Katzenellenbogen JA, Katzenellenbogen BS. Characterization of the biological roles of the estrogen receptors, ERalpha and ERbeta, in estrogen target tissues in vivo through the use of an ERalpha-selective ligand. Endocrinology 2002; 143: 4172-4177.
29. Meyers MJ, Sun J, Carlson KE, Marriner GA, Katzenellenbogen BS, Katzenellenbogen JA. Estrogen receptor-beta potency-selective ligands: Structure-activity relationship studies of diarylpropionitriles and their acetylene and polar analogues. J Med Chem 2001; 44: 4230-4251.
30. Seoane J. Escaping from the TGFbeta anti-proliferative control. Carcinogenesis 2006; 27: 2148-2156.
31. Yue J, Mulder KM. Transforming growth factor-beta signal transduction in epithelial cells. Pharmacol Ther 2001; 91: 1-34.
32. Inoue S, Ogawa S, Horie K, et al. An estrogen receptor beta isoform that lacks exon 5 has dominant negative activity on both ERalpha and ERbeta. Biochem Biophys Res Commun 2000; 279: 814-819.
33. Lee HK, Choi YS, Park YA, Jeong S. Modulation of oncogenic transcription and alternative splicing by beta-catenin and an RNA aptamer in colon cancer cells. Cancer Res 2006; 66: 10560-10566.
34. Wada-Hiraike O, Imamov O, Hiraike H, et al. Role of estrogen receptor beta in colonic epithelium. Proc Natl Acad Sci USA 2006; 103: 2959-2964.
35. Weige CC, Allred KF, Allred CD. Estradiol alters cell growth in nonmalignant colonocytes and reduces the formation of preneoplastic lesions in the colon. Cancer Res 2009; 69: 9118-9124.
36. Cho NL, Javid SH, Carothers AM, Redston M, Bertagnolli MM. Estrogen receptors alpha and beta are inhibitory modifiers of apc-dependent tumorigenesis in the proximal colon of min/+ mice. Cancer Res 2007; 67: 2366-2372.
37. Cleveland AG, Oikarinen SI, Bynote KK, et al. Disruption of estrogen receptor signaling enhances intestinal neoplasia in ApcMin/+ mice. Carcinogenesis 2009; 30: 1581-1590.
38. Saleiro D, Murillo G, Lubahn DB, Kopelovich L, Korach KS, Mehta RG. Enhanced induction of mucin-depleted foci in estrogen receptor {beta} knockout mice. Cancer Prev Res (Phila) 2010; 3: 1198-1204.
39. Paruthiyil S, Parmar H, Kerekatte V, Cunha GR, Firestone GL, Leitman DC. Estrogen receptor beta inhibits human breast cancer cell proliferation and tumor formation by causing a G2 cell cycle arrest. Cancer Res 2004; 64: 423-428.
40. Strom A, Hartman J, Foster JS, Kietz S, Wimalasena J, Gustafsson JA. Estrogen receptor beta inhibits 17beta-estradiol-stimulated proliferation of the breast cancer cell line T47D. Proc Natl Acad Sci USA 2004; 101: 1566-1571.
41. Helguero LA, Faulds MH, Gustafsson JA, Haldosen LA. Estrogen receptors alfa (ERalpha) and beta (ERbeta) differentially regulate proliferation and apoptosis of the normal murine mammary epithelial cell line HC11. Oncogene 2005; 24: 6605-6616.
42. Pravettoni A, Mornati O, Martini PG, et al. Estrogen receptor beta (ERbeta) and inhibition of prostate cancer cell proliferation: Studies on the possible mechanism of action in DU145 cells. Mol Cell Endocrinol 2007; 263: 46-54.
43. Motylewska E, Stasikowska O, Melen-Mucha G. The inhibitory effect of diarylpropionitrile, a selective agonist of estrogen receptor beta, on the growth of MC38 colon cancer line. Cancer Lett 2009; 276: 68-73.
44. Qiu Y, Waters CE, Lewis AE, Langman MJ, Eggo MC. Oestrogen-induced apoptosis in colonocytes expressing oestrogen receptor beta. J Endocrinol 2002; 174: 369-377.
45. Marino M, Galluzzo P, Leone S, Acconcia F, Ascenzi P. Nitric oxide impairs the 17beta-estradiol-induced apoptosis in human colon adenocarcinoma cells. Endocr Relat Cancer 2006; 13: 559-569.
46. Chang EC, Frasor J, Komm B, Katzenellenbogen BS. Impact of estrogen receptor beta on gene networks regulated by estrogen receptor alpha in breast cancer cells. Endocrinology 2006; 147: 4831-4842.
47. Monroe DG, Getz BJ, Johnsen SA, Riggs BL, Khosla S, Spelsberg TC. Estrogen receptor isoform-specific regulation of endogenous gene expression in human osteoblastic cell lines expressing either ERalpha or ERbeta. J Cell Biochem 2003; 90: 315-326.
48. Monroe DG, Secreto FJ, Subramaniam M, Getz BJ, Khosla S, Spelsberg TC. Estrogen receptor alpha and beta heterodimers exert unique effects on estrogen- and tamoxifen-dependent gene expression in human U2OS osteosarcoma cells. Mol Endocrinol 2005; 19: 1555-1568.
49. Dunker N, Schmitt K, Schuster N, Krieglstein K. The role of transforming growth factor beta-2, beta-3 in mediating apoptosis in the murine intestinal mucosa. Gastroenterology 2002; 122: 1364-1375.
50. Yang NN, Venugopalan M, Hardikar S, Glasebrook A. Identification of an estrogen response element activated by metabolites of 17beta-estradiol and raloxifene. Science 1996; 273: 1222-1225.
51. Harrington WR, Sheng S, Barnett DH, Petz LN, Katzenellenbogen JA, Katzenellenbogen BS. Activities of estrogen receptor alpha- and beta-selective ligands at diverse estrogen responsive gene sites mediating transactivation or transrepression. Mol Cell Endocrinol 2003; 206: 13-22.
52. Yu Z, Tang Y, Hu D, Li J. Inhibitory effect of genistein on mouse colon cancer MC-26 cells involved TGF-beta1/Smad pathway. Biochem Biophys Res Commun 2005; 333: 827-832.
53. Suenaga F, Hatsushika K, Takano S, et al. A possible link between resveratrol and TGF-beta: Resveratrol induction of TGF-beta expression and signaling. FEBS Lett 2008; 582: 586-590.
54. Matsuda T, Yamamoto T, Muraguchi A, Saatcioglu F. Cross-talk between transforming growth factor-beta and estrogen receptor signaling through Smad3. J Biol Chem 2001; 276: 42908-42914.
55. Florenes VA, Bhattacharya N, Bani MR, Ben-David Y, Kerbel RS, Slingerland JM. TGF-beta mediated G1 arrest in a human melanoma cell line lacking p15INK4B: Evidence for cooperation between p21Cip1/WAF1 and p27Kip1. Oncogene 1996; 13: 2447-2457.
56. Yue J, Buard A, Mulder KM. Blockade of TGFbeta3 up-regulation of p27Kip1 and p21Cip1 by expression of RasN17 in epithelial cells. Oncogene 1998; 17: 47-55.
57. Mal A, Poon RY, Howe PH, Toyoshima H, Hunter T, Harter ML. Inactivation of p27Kip1 by the viral E1A oncoprotein in TGFbeta-treated cells. Nature 1996; 380: 262-265.
58. Philipp-Staheli J, Kim KH, Payne SR, et al. Pathway-specific tumor suppression. reduction of p27 accelerates gastrointestinal tumorigenesis in apc mutant mice, but not in Smad3 mutant mice. Cancer Cell 2002; 1: 355-368.