Oestrogen and colorectal cancer: Mechanisms and controversies

International Journal of Colorectal Disease

Volumn 28, Issue 6, 2013, Pages 737-749

  Foster, Paul A ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

17 hydroxysteroid dehydrogenase; Colorectal cancer; Oestrogen; Oestrogen receptor; Oestrone sulphotransferase; Organic anion transporter proteins; Steroid sulphatase

Indexed keywords

ESTRADIOL; ESTROGEN; ESTROGEN DERIVATIVE; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; ESTRONE; ESTRONE SULFOTRANSFERASE; GESTAGEN; MEDROXYPROGESTERONE ACETATE; ORGANIC ANION TRANSPORTER; STERYL SULFATASE; SULFOTRANSFERASE; TESTOSTERONE 17BETA DEHYDROGENASE; UNCLASSIFIED DRUG;

ABLATION THERAPY; APOPTOSIS; CANCER CELL; CANCER GROWTH; CANCER INCIDENCE; CANCER INHIBITION; CANCER PROGNOSIS; CANCER RISK; CANCER SURVIVAL; CELL PROLIFERATION; CHEMICAL ANALYSIS; CHEMICAL STRUCTURE; COLORECTAL CANCER; DIET SUPPLEMENTATION; ENZYME ACTIVITY; ESTROGEN METABOLISM; HORMONE SUBSTITUTION; HUMAN; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; POSTMENOPAUSE; PREMENOPAUSE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; RISK REDUCTION; SEX DIFFERENCE; TREATMENT RESPONSE;

17-HYDROXYSTEROID DEHYDROGENASES; ANIMALS; AROMATASE; COLON; COLORECTAL NEOPLASMS; ESTROGENS; HUMANS; STERYL-SULFATASE;

EID: 84878530393     PISSN: 01791958     EISSN: 14321262     Source Type: Journal    
DOI: 10.1007/s00384-012-1628-y     Document Type: Review

References (126)

1. Brewster DH, Black RJ (2010) UK cancer survival statistics: survival is multifactorial. Br Med J 341:c5133
2. Coleman M, Babb P, Damiecki P (1999) Cancer survival trends in England and Wales, 1971-1995: deprivation and NHS region. Office of National Statistics, Vol. 1999 TSO
3. American Cancer Facts and Figures 2011 http://www.cancer.org/Research/ CancerFactsFigures/CancerFactsFigures/cancer-facts-figures-2011
4. GLOBOCAN Project World Health Organisation 2008 http://globocan.iarc.fr/
5. Pisani P, Parkin DM, Bray F, Ferlay J (1999) Estimates of the worldwide mortality from 25 cancers in 1990. Int J Cancer 83:18-29
6. Brenner H, Bouvier AM, Foschi R, Hackl M, Larsen IK, Lemmens V, Mangone L, Francisci S (2012) Progress of colorectal cancer survival in Europe, from the late 1980s to the early 21st century: the EUROCARE study. Int J Cancer 131:1649-1658
7. Lacassagne A (1955) Endocrine factors concerned in the genesis of experimental mammary carcinoma. J Endocrinol 13:9-18
8. Fraumeni JF Jr, Lloyd JW, Smith EM, Wagoner JK (1969) Cancer mortality among nuns: role of marital status in aetiology of neoplastic disease in women. J Natl Cancer Inst 42:455-468
9. McMichael AJ, Potter JD (1980) Reproduction, endogenous and exogenous sex steroids, and colon cancer: a review and hypothesis. J Natl Cancer Inst 65:1201-1207
10. Weiss NS, Daling JR, Chow WH (1981) Incidence of cancer of the large bowel in women in relation to reproductive and hormonal factors. J Natl Cancer Inst 67:57-60
11. Potter JD, McMichael AJ (1983) Large bowel cancer in women in relation to reproductive and hormonal factors: a case-control study. J Natl Cancer Inst 71:703-709
12. Howe GR, Craib KJ, Miller AB (1985) Age at first pregnancy and risk of colorectal cancer: a case-control study. J Natl Cancer Inst 74:1155-1159
13. Furner SE, Davis FG, Nelson RL, Haenszel W (1989) A case-control study of large bowel cancer and hormone exposure in women. Cancer Res 49:4936-4940
14. Chute CG, Willett WC, Colditz GA, Stampfer MJ, Rosner B, Speizer FE (1991) A prospective study of reproductive history and exogenous estrogens on the risk of colorectal cancer in women. Epidemiology 2:201-207
15. Wu AH, Paganini-Hill A, Ross RK, Henderson BE (1987) Alcohol, physical activity and other risk factors for colorectal cancer: a prospective study. Br J Cancer 55:687-694
16. Gerhardsson de Verdier M, London S (1992) Reproductive factors, exogenous female hormones, and colorectal cancer by subsite. Cancer Causes Control 3:355-360
17. Calle EE, Miracle-McMahill HL, Thun MJ, Heath CW Jr (1995) Estrogen replacement therapy and risk of fatal colon cancer in a prospective cohort of postmenopausal women. J Natl Cancer Inst 87:517-523
18. Newcomb PA, Storer BE (1995) Postmenopausal hormone use and risk of large bowel cancer. J Natl Cancer Inst 87:1067-1071
19. Rossouw JE, Anderson GL, Prentice RL, LaCroix AZ, Kooperberg C, Stefanick ML, Jackson RD, Beresford SA, Howard BV, Johnson KC et al (2002) Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results from the Women's Health Initiative randomized control trial. JAMA 288:321-333
20. Chlebowski RT, Wactawski-Wende J, Ritenbaugh C, Hubbell FA, Ascensao J, Rodabough RJ, Rosenberg CA, Taylor VM, Harris R, Chen C et al (2004) Estrogen plus progestin and colorectal cancer in postmenopausal women. N Engl J Med 350:991-1004
21. Ritenbaugh C, Stanford JL, Wu L, Shikany JM, Schoen RE, Stefanick ML, Taylor V, Garland C, Frank G, Lane D et al (2008) Conjugated equine estrogens and colorectal cancer incidence and survival: the Women's Health Initiative randomized clinical trial. Cancer Epidemiol Biomarkers Prev 17:2609-2618
22. Gunter MJ, Hoover DR, Yu H, Wassertheil-Smoller S, Rohan TE, Manson JE, Howard BV, Wylie-Rosett J, Anderson JL, Ho GY et al (2008) Insulin, insulin-like growth factor-1, endogenous estradiol, and risk of colorectal cancer in postmenopausal women. Cancer Res 68:329-337
23. Clandenen TV, Koenig KL, Shore RE, Levitz M, Arslan AA, Zeleniuch-Jacquotte A (2009) Postmenopausal levels of endogenous sex hormones and risk of colorectal cancer. Cancer Epidemiol Biomarkers Prev 18:275-281
24. Zervoudakis A, Strickler HD, Park Y, Xue X, Hollenbeck A, Schatzkin A, Gunter MJ (2011) Reproductive history and risk of colorectal cancer in postmenopausal women. J Natl Cancer Inst 103:826-834
25. Lin JK, Cheung WY, Lai JY-C, Giovannucci EL (2012) The effect of estrogen vs. combined estrogen progestogen therapy on the risk of colorectal cancer. Int J Cancer 130:419-430
26. Reed MJ, Murray MAF (1979) The oestrogens. Academic, London, pp 263-266
27. Hobkirk R (1993) Steroid sulfation. Trends Endocrinol Metab 4:69-74
28. Falany JL, Falany CN (1996) Expression of cytosolic sulfotransferases in normal mammary epithelial cells and breast cancer cell lines. Cancer Res 56:1551-1555
29. Falany JL, Macrina N, Falany CN (2002) Regulation of MCF-7 breast cancer cell growth by beta-estradiol sulfation. Breast Cancer Res Treat 74:16776
30. Stott CA (2002) Sulfonation and molecular action. Endocr Rev 23:703-732
31. Noel CT, Reed MJ, Jacobs HS, James VHL (1981) The plasma concentration of oestrone sulphate in postmenopausal women: lack of diurnal variation, effect of ovariectomy, age and weight. J Steroid Biochem 14:1101-1105
32. Pasqualini JR, Chetrite G, Blacker C, Feinstein MC, Delalonde L, Talbi M, Maloche C (1996) Concentration of estrone, estradiol, and estrone sulfate and evaluation of sulfatase and aromatase activities in pre- and post-menopausal breast cancer patients. J Clin Endocrinol Metab 81:1460-1464
33. Ruder HJ, Loriaux DL, Lipsett MB (1972) Estrone sulfate: production rate and metabolism in man. J Clin Investig 51:1020-1033
34. Reed MJ, Purohit A (1994) Design of enzyme inhibitors as drugs, vol. 2. Oxford University Press, pp 481-494
35. Reed MJ, Purohit A, Woo LWL, Potter BVL (1996) The development of steroid sulphatase inhibitors. Endocr Relat Cancer 3:9-23
36. English MA, Kane KF, Cruickshank N, Langman MJ, Stewart PM, Hewison M (1999) Loss of estrogen inactivation in colonic cancer. J Clin Endocrinol Metab 84:2080-2085
37. English MA, Hughes SV, Kane KF, Langman MJ, Stewart PM, Hewsion M (2000) Oestrogen inactivation in the colon: analysis of the expression and regulation of 17beta-hydroxysteroid dehydrogenase isozymes in normal colon and colonic cancer. Br J Cancer 83:550-558
38. Day JM, Foster PA, Tutill HJ, Parsons MF, Newman SP, Chander SK, Allan GM, Lawrence HR, Vicker N, Potter BVL et al (2008) 17beta-hydroxysteroid dehydrogenase type 1, and not type 12, is a target for endocrine therapy of hormone-dependent breast cancer. Int J Cancer 122:1931-1940
39. Oduwole OO, Isomaa VV, Nokelainen PA, Stenback F, Vihko PT (2002) Down-regulation of estrogen metabolising 17beta-hydroxysteroid dehydrogenase type 2 expression correlates inversely with Ki67 proliferation marker in colon-cancer development. Int J Cancer 97:1-6
40. English MA, Stewart PM, Hewison M (2001) Estrogen metabolism and malignancy: analysis of the expression and function of 17b-hydroxysteroid dehydrogenases in colonic cancer. Mol Cell Endocrinol 171:53-60
41. Oduwole OO, M kinen MJ, Isomaa VV, Pulkka A, Jernvall P, Karttunen TJ, Vihko PT (2003) 17beta-hydroxysteroid dehydrogenase type 2: independent prognostic significance and evidence of estrogen protection in female patients with colon cancer. J Steroid Biochem Mol Biol 87:133-140
42. Fiorelli G, Picariello L, Martineti V, Tonelli F, Brandi ML (1999) Estrogen synthesis in human colon cancer epithelial cells. J Steroid Biochem Mol Biol 71:223-230
43. Wilkins HR, Doucet K, Duke V, Morra A, Johnson N (2010) Estrogen prevents sustained COLO-205 human colon cancer cell growth by inducing apoptosis, decreasing c-myb protein, and decreasing transcription of the anti-apoptotic protein bcl-2. Tumour Biol 31:16-22
44. Bernstein C, Bernstein H, Garewal H, Dinning P, Jabi R, Sampliner RE, McCuskey MK, Panda M, Roe DJ, Heureux LL, Payne C (1999) A bile acid-induced apoptosis assay for colon cancer risk and associated quality control studies. Cancer Res 59:2353-2357
45. Slattery ML, Potter JD, Curtin K, Edwards S, Ma KN, Anderson K, Schaffer D, Samowitz WS (2001) Estrogens reduce and withdrawal of estrogens increase risk of microsatellite instability-positive colon cancer. Cancer Res 61:126-130
46. Kuiper GG, Enmark E, Pelto-Huikko M, Nilsson S, Gustafsson JA (1996) Cloning of a novel receptor expressed in rat prostate and ovary. Proc Natl Acad Sci 93:5925-5930
47. Reed MJ, Purohit A, Woo LW, Newman SP, Potter BVL (2005) Steroid sulfatase: molecular biology, regulation, and inhibition. Endocr Rev 26:171-202
48. Foster PA, Chander SK, Parson MF, Newman SP, Woo LWL, Potter BVL, Reed MJ, Purohit A (2008) Efficacy of three potent steroid sulfatase inhibitors: pre-clinical investigations for their use in the treatment of hormone-dependent breast cancer. Breast Cancer Res Treat 111:129-138
49. Foster PA, Woo LWL, Potter BVL, Reed MJ, Purohit A (2008) The use of steroid sulfatase inhibitors as a novel therapeutic strategy against hormone-dependent endometrial cancer. Endocrinology 149:4035-4042
50. Stanway SJ, Purohit A, Woo LWL, Sufi S, Vigushin D, Ward R, Wilson RH, Stanczyk FZ, Dobbs N, Kulinskaya E et al (2006) Phase I study of STX64 (667 Coumate) in breast cancer patients: the first study of a steroid sulfatase inhibitor. Clin Cancer Res 12:1585-1592
51. Foster PA, Newman SP, Chander SK, Stengel C, Jhalli R, Woo LWL, Potter BVL, Reed MJ, Purohit A (2006) In vivo efficacy of STX213, a second generation steroid sulfatase inhibitors, for hormone dependent breast cancer therapy. Clin Cancer Res 12:5543-5549
52. Monroe DG, Chang PL (1987) Tissue specific expression of human arylsulfatase-C isozymes and steroid sulfatase. Am J Hum Genet 40:102-114
53. Her C, Szumlanski C, Aksoy IA, Weinshilboum RM (1996) Human jejunal estrogen sulfotransferase and dehydroepiandrosterone sulfotransferase: immunochemical characterization of individual variation. Drug Metab Dispos 24:1328-1335
54. Sato R, Suzuki T, Katayose Y, Miura K, Shiiba K, Tateno H, Miki Y, Akahira J, Kamogawa Y, Nagasaki S et al (2009) Steroid sulfatase and estrogen sulfotransferase in colon carcinoma: regulators of intratumoral estrogen concentrations and potent prognostic factors. Cancer Res 69:914-922
55. Lee W, Belkhiri A, Lockhart AC, Merchant N, Glaeser H, Harris I, Washington MK, Brunt EM, Zaika A, Kim RB, El-Rifai W (2008) Overexpression of OATP1B3 confers apoptotic resistance in colon cancer. Cancer Res 68:10315-10323
56. Pressler H, Sissung TM, Vanzon D, Price DK, Figg WD (2011) Expression of OATP family members in hormone-related cancers: potential markers of progression. Public Libr Sci ONE 5:e20372
57. McGuire JL, Lisk RD (1968) Estrogen receptors in the intact rat. Proc Natl Acad Sci 61:497-503
58. Enmark E, Pelto-Huikko M, Grandien K, Langercrantz S, Lagercrantz J, Fried G, Nordenskjold M, Gustafsson JA (1997) Human estrogen receptor beta-gene structure, chromosomal location, and expression pattern. J Clin Endocrinol Metab 82:4258-4265
59. Jiang H, Teng R, Wang Q, Zhang X, Wang H, Wang Z, Cao T, Leng L (2008) Transcriptional analysis of estrogen receptor alpha variant mRNAs in colorectal cancers and their matched normal colorectal tissues. J Steroid Biochem Mol Biol 112:20-24
60. Jiang HP, Teng RY, Wang Q, Zhang X, Wang HH, Cao J, Teng LS (2008) Estrogen receptor alpha variant ERalpha46 mediates growth inhibition and apoptosis of human HT-29 colon adenoarcoma cells in the prescence of 17beta-oestradiol. Chin Med J (Engl) 121:1025-1031
61. Wang NA, Malcomson RD, Jodrell DI, Groome NP, Harrison DJ, Sanders PT (2005) ERbeta isoform expression in colorectal carcinoma: an in vivo and in vitro study of clinicopathological and molecular correlates. J Pathol 207:53-60
62. Wang ZY, Zhang XT, Shen P, Loggie BW, Chang YC, Deuel TF (2006) A variant of estrogen receptor-α, hER-α36: transduction of estrogen- and antiestrogen-dependent membrane-initiated mitogenic signalling. Proc Natl Acad Sci 103:9063-9068
63. Flouriot G, Brand H, Denger S, Metivier R, Kos M, Reid G, Sonntag-Buck V, Gannon F (2000) Identification of a new isoform of the human estrogen receptor-alpha (hER-alpha) that is encoded by distinct transcripts and that is able to repress hER-alpha activation function 1. EMBO J 19:4688-4700
64. Shi L, Dong B, Li Z, Lu Y, Ouyang T, Li J, Wang T, Fan Z, Lin B, Wang Z, Xie Y (2009) Expression of ER- > {alpha}36, a novel variant of estrogen receptor {alpha}, and resistance to tamoxifen treatment in breast cancer. J Clin Oncol 27:3423-3429
65. Deng H, Huang X, Fan J, Wang L, Xai Q, Yang X, Wang Z, Liu L (2010) A variant of estrogen receptor-alpha, ER-alpha36 is expressed in human gastric cancer is highly correlated with lymph node metastasis. Oncol Rep 24:171-176
66. Tu BB, Lin SL, Yan LY, Wang ZL, Sun QY, Qiao J (2011) ER-α36, a novel variant of estrogen receptor α, is involved in EGRF-related carcinogenesis in endometrial cancer. Am J Obstet Gynecol 205:227.e1-227.e6
67. Lin J, Zee RY, Liu KY, Zhang SM, Lee IM, Manson JE, Giovannucci E, Buring JE, Cook NR (2010) Genetic variation in sex-steroid receptors and synthesizing enzymes and colorectal cancer risk in women. Cancer Causes Control 21:897-908
68. Miceli C, Cocciadiferro L, Fregapane M, Zarcone M, Montalto G, Polito LM, Agostara B, Granta OM, Carruba G (2011) Expression of wild-type and variant estrogen receptor alpha in liver carcinogenesis and tumour progression. OMICS 15:313-317
69. Campbell-Thompson ML (1997) Estrogen receptor alpha and beta expression in upper gastrointestinal tract with regulation of trefoil factor family 2 mRNA levels in ovariectomized rats. Biochem Biophys Res Commun 240:478-483
70. Papaxoninis K, Triantafyllou K, Sasco AJ, Nicolopoulou-Stamati P, Ladas SD (2010) Subsite-specific differences of estrogen receptor beta expression in the normal colonic epithelium: implications for carcinogenesis and colorectal cancer epidemiology. Eur J Gastroenterol Hepatol 22:614-619
71. Campbell-Thompson M, Lynch IJ, Bhardwaj B (2001) Expression of estrogen receptor (ER) subtypes and ERbeta isoforms in colon cancer. Cancer Res 61:632-640
72. Nüssler NC, Reinbacher K, Shanny N, Schirmeier A, Glanemann M, Neuhaus P, Nussler AK, Kirschner M (2008) Sex-specific differences in the expression levels of estrogen receptor subtypes in colorectal cancer. Gend Med 5:209-217
73. Bardin A, Boulle N, Lazennec G, Vignon F, Pujol P (2004) Loss of ERbeta as a common step in estrogen-dependent tumor progression. Endocr Relat Cancer 11:537-551
74. Foley EF, Jazaeri AA, Shupnik MA, Jazaeri O, Rice LW (2000) Selective loss of estrogen receptor beta in malignant colon cancer. Cancer Res 60:245-248
75. Konstantinopoulos PA, Kominea A, Vandoros G, Sykiotis GP, Andricopoulos P, Varakis I, Sotiropoulou-Bonikou G, Papavassiliou AG (2003) Oestrogen receptor beta (ERbeta) is abundantly expressed in normal colonic mucosa, but declines in colon adenocarcinoma paralleling the tumour's dedifferentiation. Eur J Cancer 39:1251-1258
76. Jassam N, Bell SM, Speirs V, Quirke P (2005) Loss of expression of oestrogen receptor beta in colon cancer and its association with Dukes' staging. Oncol Rep 14:17-21
77. Castiglione F, Taddei A, Degl'Innocenti DR, Buccoliero AM, Bechi P, Garbini F, Chiara FG, Moncini D, Cavallina G, Marascio L et al (2008) Expression of estrogen receptor beta in colon cancer progression. Diagn Mol Pathol 17:231-236
78. Fang YJ, Lu ZH, Wang F, Wu XJ, Li LR, Zhang LY, Pan ZZ, Wan DS (2010) Prognostic impact of ERβ and MMP7 expression on overall survival in colon cancer. Tumour Biol 31:651-658
79. Di Domenico M, Castoria G, Bilancio A, Migliaccio A, Auricchio F (1996) Estradiol activation of human colon carcinoma-derived Caco-2 cell growth. Cancer Res 56:4516-4521
80. Xu X, Thomson ML (1994) Estrogen receptor-mediated direct stimulation of colon cancer cell growth in vitro. Mol Cell Endocrinol 105:197-201
81. Issa JP, Ottaviano YL, Celano P, Hamilton SR, Davidson NE, Baylin SB (1994) Methylation of the oestrogen receptor CpG island links aging and neoplasia in human colon. Nat Genet 7:536-540
82. Arai N, Ström A, Rafter JJ, Gustafsson JA (2000) Estrogen receptor beta mRNA in colon cancer cells: growth effects of estrogen and genistein. Biochem Biophys Res Commun 270:425-431
83. Qui Y, Waters CE, Lewis AE, Langman MJ, Eggo MC (2002) Oestrogen-induced apoptosis in colonocytes expressing oestrogen receptor beta. J Endocrinol 174:369-377
84. Koehler KF, Helquero LA, Haldosén LA, Warner M, Gustafsson JA (2005) Reflections on the discovery and significance of estrogen receptor beta. Endocr Rev 26:465-478
85. Pettersson K, Grandien K, Kuiper GG, Gustafsson JA (1997) Mouse estrogen receptor β forms estrogen response element-binding heterodimers with estrogen receptor α. Mol Endocrinol 11:1486-1496
86. Imamov O, Shim GJ, Warner M, Gustafsson JA (2005) Estrogen receptor beta in health and disease. Biol Reprod 73:866-871
87. Couse JF, Korach KS (1999) Estrogen receptor null mice: what have we learned and where will they lead us? Endocr Rev 20:358-417
88. Hsu HH, Cheng SF, Wu CC, Chu CH, Weng YJ, Lin CS, Lee SD, Wu HC, Huang CY, Kuo WW (2006) Apoptotic effects of over-expressed estrogen receptor-beta on LoVo colon cancer cell is mediated by p53 signalings in a ligand-dependent manner. Chin J Physiol 49:110-116
89. Marino M, Gulluzzo P, Leone S, Acconcia F, Ascenzi P (2006) Nitric oxide impairs the 17beta-estradiol-induced apoptosis in human colon adenocarcinoma cells. Endocr Relat Cancer 13:559-569
90. Hartman J, Edvardsson K, Lindberg K, Zhao C, Williams C, Ström A, Gustafsson JA (2009) Tumor repressive functions of estrogen receptor beta in SW480 colon cancer cells. Cancer Res 69:6100-6106
91. Loda M, Cukor B, Tam SW, Lavin P, Fiorentino M, Draetta GF, Jessup JM, Pagano M (1997) Increased proteasome-dependent degradation of the cyclin-dependent kinase inhibitor p27 in aggressive colorectal carcinomas. Nat Med 3:231-234
92. Petrova TV, Nykänen A, Norrmén C, Ivanov KI, Andersson LC, Haglund C, Puolakkainen P, Wempe F, von Melchner H, Gradwohl G (2008) Transcription factor PROX1 induces colon cancer progression by promoting the transition from benign to highly dysplastic phenotype. Cancer Cell 13:407-419
93. Edvardsson K, Ström A, Jonsson P, Gustafsson JA, Williams C (2011) Estrogen receptor β induced anti-inflammatory and antitumorogenic networks in colon cancer cells. Mol Endocrinol 25:969-979
94. Izbicki JR, Schmitz R, Hoppen OH, Izbicki W, Troidl H (1984) Effects of steroid hormone therapy on primary xenotransplanted human colorectal adenocarcinomas. J Cancer Res Clin Oncol 108:345-350
95. Stebbings WS, Vinson GP, Farthing MJ, Balkwill F, Wood RF (1989) Effect of steroid hormones on human colorectal adenocarcinoma xenografts, of known steroid-receptor status, in nude mice. J Cancer Res Clin Oncol 115:439-444
96. Narayan S, Rajakumar G, Prouix H, Singh P (1992) Estradiol is trophic for colon cancer in mice: effect of ornithine decarboxylase and c-myc messenger RNA. Gastroenterology 103:1823-1832
97. Singh P, Reubi JC, Rajakumar G, Guo YS, Prioux H, Chicone L (1993) In vivo mitogenic effects of estradiol on colon cancers: role of gastrin and gastrin receptors. J Steroid Biochem Mol Biol 46:49-60
98. Kuruppa D, Christophi C, Bertram JF, O'Brien PE (1998) Tamoxifen inhibits colorectal cancer metastases in the liver: a study in a murine model. J Gastroenterol Hepatol 13:521-527
99. Shen LZ, Hua YB, Yu XM, Xu Q, Chen T, Wang JH, Wu WX (2005) Tamoxifen can reverse multidrug resistance of colorectal carcinoma in vivo. World J Gastroenterol 11:1060-1064
100. Wada-Hiraike O, Warner M, Gustafsson JA (2006) New developments in oestrogen signalling in colonic epithelium. Biochem Soc Trans 34:1114-1116
101. Saleiro D, Murillo G, Lubahan DB, Kopelovich L, Korach KS, Mehta RG (2010) Enhanced induction of mucin-depleted foci in estrogen receptor beta knockout mice. Cancer Prev Res 3:1198-1204
102. Weige CC, Allred KF, Allred CD (2009) Estradiol alters cell growth in non-malignant colonocytes and reduces the formation of preneoplastic legions in the colon. Cancer Res 69:9118-9124
103. Cho NL, Javid SH, Carothers AM, Redston M, Bertagnolli MM (2007) Estrogen receptors alpha and beta are inhibitory modifiers of Apc-dependent tumorigenesis in the proximal colon of Min-/+ mice. Cancer Res 67:2366-2372
104. Giroux V, Lemay F, Bernatchez G, Robitaille Y, Carrier JC (2008) Estrogen receptor beta deficiency enhances small interstinal tumorigenesis in ApcMin-/+ mice. Int J Cancer 123:303-311
105. Motylewska E, Stasikowska O, Mełeń-Mucha G (2009) The inhibitory effect of diarylpropionitrile, a selective agonist of estrogen receptor beta, on the growth of MC38 colon cancer line. Cancer Lett 276:68-73
106. Weyant MJ, Carothers AM, Mahmoud NN, Bradlow HL, Remotti H, Bilinski RT, Bertagnolli MM (2001) Reciprocol expression of ERalpha and ERbeta is associated with estrogen-mediated modulation of intestinal tumorigenesis. Cancer Res 61:2547-2551
107. Javid SH, Moran AE, Carothers AM, Redston M, Bertagnolli MM (2005) Modulation of tumour formation and intestinal cell migration by estrogens in the Apc(Min/+) mouse model of colorectal cancer. Carcinogenesis 26:587-595
108. Barone M, Lofano K, De Tullio N, Licino R, Albano F, Di Leo A (2006) Dietary, endocrine, and metabolic factors in the development of colorectal cancer. J Gastrointest Cancer 43:13-19
109. Manno M, Cotterchio M, Boucher B, Gallinger S, Okay A, Harper P (2006) Dietary phytoestrogen intake is associated with reduced colorectal cancer risk. J Nutr 136:3046-3053
110. Day JM, Tutill HJ, Purohit A, Reed MJ (2008) Design and validation of specific inhibitors of 17beta-hydroxysteroid dehydrogenases for therapeutic application in breast and prostate cancer, and in endometriosis. Endocr Relat Cancer 15:665-692
111. Foster PA, Reed MJ, Purohit A (2008) Recent developments of steroid sulfatase inhibitors as anti-cancer agents. Anti Cancer Agents Med Chem 8:732-738
112. Stanway SJ, Delavault P, Purohit A, Woo LW, Thurieau C, Potter BV, Reed MJ (2007) Steroid sulfatase: a new target for the endocrine therapy of breast cancer. Oncologist 12:370-374
113. Hogan AM, Collins D, Sheehan K, Zierau O, Baird AW, Winter DC (2010) Rapid effects of phytoestrogens on human colonic smooth muscle are mediated by oestrogen receptor beta. Mol Cell Endocrinol 320:106-110
114. Braniste V, Leveque M, Buisson-Brenac C, Bueno L, Fioramonti J, Houdeau E (2009) Oestradiol decreased colonic permeability through oestrogen receptor beta-mediated up-regulation of occludin and junctional adhesion molecule-A in epithelial cells. J Physiol 587:3317-3328
115. Harris HA, Albert LM, Leathurby Y, Malamas MS, Mewshaw RE, Miller CP, Kharode YP, Marzolf J, Komm BS, Winneker RC et al (2003) Evaluation of estrogen receptor-beta agonists in animal models of human disease. Endocrinology 144:4241-4249
116. Malamas MS, Manas ES, McDevitt RE, Gunawan I, Xu ZB, Collini MD, Miller CP, Dinh T, Henderson RA, Keith JC Jr, Harris HA (2004) Design and synthesis of aryl diphenolic azoles as potent and selective estrogen receptor-beta ligands. J Med Chem 47:5021-5040
117. Mersereau JE, Levy N, Staub RE, Baggett S, Zogovic T, Chow S, Ricke WA, Tagliaferri M, Cohen I, Bjeldanes LF, Leitman DC (2008) Liquiritigenin is a plant-derived highly selective estrogen receptor beta agonist. Mol Cell Endocrinol 283:49-57
118. Paruthiyil S, Cvoro A, Zhao X, Wu Z, Sui Y, Staub RE, Baggett S, Herber CB, Griffin C, Tagliaferri M et al (2009) Drug and cell-type specific regulation of genes with different classes of estrogen receptor beta-selective agonists. Public Libr Sci ONE 4:e6271
119. Satoh T, Matsui M, Tamura H (2000) Sulfotransferases in a human colon carcinoma cell line, Caco-2. Biol Pharm Bull 23:810-814
120. Fiorelli G, Picariello L, Martineti V, Tognarini I, Tonelli F, Brandi ML (2002) Estrogen metabolism in human colorectal cancer cells. J Steroid Biochem Mol Biol 81:281-289
121. Nakayama Y, Sakamoto H, Satoh K, Yamamoto T (2000) Tamoxifen and gonadal steroids inhibit colon cancer growth in association with inhibition of thymidylate synthase, survivin and telomerase expression through estrogen receptor beta mediated system. Cancer Lett 161:63-71
122. Hennessy BA, Harvey BJ, Healy V (2005) 17beta-estradiol rapidly stimulates c-fos expression via the MAPK pathway in T84 cells. Mol Cell Endocrinol 229:39-47
123. Messa C, Notarnicola M, Russo F, Cavallini A, Pallottini V, Trentalance A, Bifulco M, Laezza C, Gabriella Caruso M (2005) Estrogenic regulation of cholesterol biosynthesis and cell growth in DLD-1 human colon cancer cells. Scand J Gastroenterol 40:1454-1461
124. Martineti V, Picariello L, Tognarini I, Carbonell Sala S, Gozzini A, Azzari C, Mavilia C, Tanini A, Falchetti A, Fiorelli G et al (2005) 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 12:455-69
125. Lai TY, Chen LM, Lin JY, Tzang BS, Lin JA, Tsai CH, Lin YM, Huang CY, Liu CJ, Hsu HH (2010) 17beta-estradiol inhibits prostaglandin E2-induced COX-2 expressions and cell migration by suppressing Akt and ERK1/2 signaling pathways in human LoVo colon cancer cells. Mol Cell Biochem 342:63-70
126. Bulzomi P, Galluzzo P, Bolli A, Leone S, Acconcia F, Marino M (2012) The pro-apoptotic effect of quercetin in cancer cell lines requires ERβ-dependent signals. J Cell Physiol 227:1891-1898.