Raloxifene and antiestrogenic gonadorelin inhibits intestinal tumorigenesis by modulating immune cells and decreasing stem-like cells

Cancer Prevention Research

Volumn 7, Issue 3, 2014, Pages 300-309

  Janakiram, Naveena B ^a   Mohammed, Altaf ^a   Brewer, Misty ^a   Bryant, Taylor ^a   Biddick, Laura ^a   Lightfoot, Stan ^a   Pathuri, Gopal ^a,b   Gali, Hariprasad ^b   Rao, Chinthalapally V ^a  

^a UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF OKLAHOMA HEALTH SCIENCES CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; CD24 ANTIGEN; CHEMOKINE; CYCLIN D1; CYCLINE; CYCLOOXYGENASE 2; EPITHELIAL CELL ADHESION MOLECULE; ESTROGEN; ESTROGEN RECEPTOR BETA; GONADORELIN; HERMES ANTIGEN; INDUCIBLE NITRIC OXIDE SYNTHASE; LAMININ 1; LAMININ 1 BETA; NATURAL KILLER CELL RECEPTOR; RALOXIFENE; UNCLASSIFIED DRUG; ANTIESTROGEN; APC PROTEIN; SELECTIVE ESTROGEN RECEPTOR MODULATOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN EXPRESSION; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CANCER INHIBITION; CARCINOGENESIS; COLON TUMOR; CONTROLLED STUDY; DIET; IMMUNOCOMPETENT CELL; IMMUNOMODULATION; MOUSE; NATURAL KILLER CELL; NONHUMAN; POLYP; PRIORITY JOURNAL; PROTEIN EXPRESSION; SMALL INTESTINE TUMOR; STEM CELL; TUMOR VOLUME; UPREGULATION; ANIMAL; C57BL MOUSE; CELL COUNT; CELLULAR IMMUNITY; CYTOLOGY; DRUG EFFECTS; FEMALE; GENETICS; HEMATOPOIETIC STEM CELL; IMMUNOLOGY; INTESTINAL NEOPLASMS; INTESTINE; MALE; PATHOLOGY; TRANSGENIC MOUSE;

ADENOMATOUS POLYPOSIS COLI PROTEIN; ANIMALS; CARCINOGENESIS; CELL COUNT; ESTROGEN ANTAGONISTS; FEMALE; GONADOTROPIN-RELEASING HORMONE; HEMATOPOIETIC STEM CELLS; IMMUNITY, CELLULAR; INTESTINAL NEOPLASMS; INTESTINES; KILLER CELLS, NATURAL; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; RALOXIFENE; SELECTIVE ESTROGEN RECEPTOR MODULATORS;

EID: 84897136044     PISSN: 19406207     EISSN: 19406215     Source Type: Journal    
DOI: 10.1158/1940-6207.CAPR-13-0345     Document Type: Article

References (38)

1. http://www.cancer.org/cancer/colonandrectumcancer/detailedguide/ colorectal-cancer-key-statistics.
2. http://www.cancer.gov/cancertopics/pdq/screening/colorectal/ Health-Professional/page1.
3. Siegel RL, Ahmedin J, Ward EM. Increase in incidence of colorectal cancer among young men and women in the United States. Cancer Epidemiol Biomarkers Prev 2009;8:1695-8.
4. Ferlitsch M, Reinhart K, Pramhas S, Wiener C, Gal O, Bannert C, et al. Sex-specific prevalence of adenomas, advanced adenomas, and colorectal cancer in individuals undergoing screening colonoscopy. JAMA 2011;306:1352-8.
5. Chlebowski RT, Wactawski-Wende J, Ritenbaugh C, Hubbell FA, Ascensao J, Rodabough RJ, et al. Estrogen plus progestin and colorectal cancer in postmenopausal women. N Engl J Med 2004;350:991-1004. (Pubitemid 38269276)
6. Rossouw JE, Anderson GL, Prentice RL, LaCroix AZ, Kooperberg C, Stefanick ML, et al. Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results From the Women's Health Initiative randomized controlled trial. JAMA 2002;288:321-33. (Pubitemid 34761611)
7. Anderson GL, Limacher M, Assaf AR, Bassford T, Beresford SA, Black H, et al. Effects of conjugated equine estrogen in postmenopausal women with hysterectomy: the Women's Health Initiative randomized controlled trial. JAMA 2004;291:1701-12. (Pubitemid 38489892)
8. Ritenbaugh C, Stanford JL, Wu L, Shikany JM, Schoen RE, Stefanick ML, et al. Conjugated equine estrogens and colorectal cancer incidence and survival: the Women's Health Initiative randomized clinical trial. Cancer Epidemiol Biomarkers Prev 2008;17:2609-18.
9. Gunter MJ, Hoover DR, Yu H, Wassertheil-Smoller S, Rohan TE, Manson JE, et al. Insulin, insulin-like growth factor-I, endogenous estradiol, and risk of colorectal cancer in postmenopausal women. Cancer Res 2008;68:329-37. (Pubitemid 351380136)
10. Clendenen TV, Koenig KL, Shore RE, Levitz M, Arslan AA, Zeleniuch-Jacquotte A. Postmenopausal levels of endogenous sex hormones and risk of colorectal cancer. Cancer Epidemiol Biomarkers Prev 2009;18:275-81.
11. McMichael AJ, Potter JD. Reproduction, endogenous and exogenous sex hormones, and colon cancer: reviewand hypothesis. J Natl Cancer Inst 1980;65:1201-7. (Pubitemid 11196006)
12. Narayan S, Rajakumar G, Prouix H, Singh P. Estradiol is trophic for colon cancer in mice: effect on ornithine decarboxylase and c-myc messenger RNA. Gastroenterology 1992;103:1823-32.
13. Singh S, Paraskeva C, Gallimore PH, Sheppard MC, Langman MJ. Differential growth response to estrogen of premalignant and malignant colonic cell lines. Anticancer Res 1994;14:1037-41. (Pubitemid 24272564)
14. Di Domenico M, Castoria G, Bilancio A, Migliaccio A, Auricchio F. Estradiol activation of human colon carcinoma-derived Caco-2 cell growth. Cancer Res 1996;56:4516-21. (Pubitemid 26330464)
15. Hennessy BA, Harvey BJ, Healy V. 17β-Estradiol rapidly stimulates cfos expression via the MAPK pathway in T84 cells. Mol Cell Endocrinol 2005;229:39-47. (Pubitemid 40018081)
16. Janakiram NB, Steele VE, Rao CV. Estrogen receptor-β as a potential target for colon cancer prevention: chemoprevention of azoxy-methane-induced colon carcinogenesis by raloxifene in F344 rats. Cancer Prev Res 2005;2:52-9.
17. Dunn GP, Bruce AT, Ikeda H, Old LJ, Schreiber RD. Cancer immunoediting: from immunosurveillance to tumor escape. Nat Immunol 2002;3:991-8. (Pubitemid 35363648)
18. Janakiram NB, Mohammed A, Qian L, Choi CI, Steele VE, Rao CV. Chemopreventive effects of RXR-selective rexinoid bexarotene on intestinal neoplasia of Apc(Min/+) mice. Neoplasia 2012;14:159-68.
19. http://www.ema.europa.eu/docs/en-GB/document-library/Maximum-Residue- Limits---Report/2009/11/WC500014361.pdf.
20. Eliassen AH, Hankinson SE. Endogenous hormone levels and risk of breast, endometrial and ovarian cancers: prospective studies. Adv Exp Med Biol 2008;630:148-65.
21. Cavalieri EL, Rogan EG. Depurinating estrogen-DNA adducts in the etiology and prevention of breast and other human cancers. Future Oncol 2010;6:75-91.
22. Márquez-Garbán DC, Chen HW, Goodglick L, Fishbein MC, Pietras RJ. Targeting aromatase and estrogen signaling in human non-small cell lung cancer. Ann N Y Acad Sci 2009;1155:194-205.
23. Siegfried JM, Hershberger PA, Stabile LP. Estrogen receptor signaling in lung cancer. Semin Oncol 2009;36:524-31.
24. Di Leo A, Messa C, Cavallini A, Linsalata M. Estrogens and colorectal cancer. Curr Drug Targets Immune Endocr Metabol Disord 2001;1:1-12.
25. Wada-Hiraike O, Imamov O, Hiraike H, Hultenby K, Schwend T, Omoto Y, et al. Role of estrogen receptor β in colonic epithelium. Proc Natl Acad Sci U S A 2006;103:2959-64.
26. Half E, Arber N. Colon cancer: preventive agents and the present status of chemoprevention. Expert Opin Pharmacother 2009;10:211-9.
27. Clevers H. Wnt breakers in colon cancer. Cancer Cell 2004;5:5-6. (Pubitemid 38121590)
28. Fu M, Wang C, Li Z, Sakamaki T, Pestell RG. Minireview: cyclin D1: normal and abnormal functions. Endocrinology 2004;145:5439-47. (Pubitemid 39564581)
29. Heijmans J, Wielenga MCB, Rosekrans SL, Lidth de Jeude JFV, Roelofs J, Groothuis P, et al. Oestrogens promote tumorigenesis in a mouse model for colitis-associated cancer. Gut 2013;63:310-6; doi 10, 1136/gutjnl-304216.
30. Couse JF, Yates MM, Deroo BJ, Korach KS. Estrogen receptor-β is critical to granulosa cell differentiation and the ovulatory response to gonadotropins. Endocrinology 2005;146:3247-62. (Pubitemid 41058094)
31. Janakiram NB, Mohammed A, Rao CV. Role of lipoxins, resolvins, and other bioactive lipids in colon and pancreatic cancer. Cancer Metastasis Rev 2011;30:507-23.
32. Janakiram NB, Rao CV. iNOS-selective inhibitors for cancer prevention: promise and progress. Future Med Chem 2012;4:2193-04.
33. Coelho AL, Schaller MA, Benjamim CF, Orlofsky AZ, Hogaboam CM, Kunkel SL. The chemokine CCL6 promotes innate immunity via immune cell activation and recruitment. J Immunol 2007;179:5474-82.
34. Klatte T, Seligson DB, Leppert JT, Riggs SB, Yu H, Zomorodian N, et al. The chemokine receptor CXCR3 is an independent prognostic factor in patients with localized clear cell renal cell carcinoma. J Urol 2008;179:61-6. (Pubitemid 350216740)
35. Coca S, Perez-Piqueras J, Martinez D, Colmenarejo A, Saez MA, Vallejo C, et al. The prognostic significance of intratumoral natural killer cells in patients with colorectal carcinoma. Cancer 1997;79:2320-8. (Pubitemid 27251014)
36. Seaman WE, Gindhart TD. Effect of estrogen on natural killer cells. Arthritis Rheum 1979;22:1234-40. (Pubitemid 10163788)
37. Rossi P, Lindgren JA, Kullman C, Jondal M. Products of the lipoxygenase pathway in human natural killer cell cytotoxicity. Cell Immunol 1985;93:1-8. (Pubitemid 15021229)
38. Fillmore CM, Gupta PB, Rudnick JA, Caballero S, Keller PJ, Lander ES, et al. Estrogen expands breast cancer stem-like cells through paracrine FGF/Tbx3 signaling. PNAS 2010;107:21737-42.