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 colonie vitamin D receptor

Oncology Research

Volumn 11, Issue 6, 1999, Pages 255-264

  Smirnoff, Patricia ^a   Liel, Yair ^a   Gnainsky, Julia ^a   Shany, Shraga ^a   Schwartz, Betty ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

Colorectal cancer; Dna methylation; Estrogen; Steroid receptors; Vitamin d

Indexed keywords

CALCITRIOL RECEPTOR; CARCINOGEN; DIMETHYLHYDRAZINE; ESTRADIOL; ESTROGEN; MESSENGER RNA; PARATHYROID HORMONE;

ANIMAL; ARTICLE; BLOOD; CHEMICALLY INDUCED DISORDER; COLON TUMOR; CPG ISLAND; DNA METHYLATION; DRUG EFFECT; FEMALE; METABOLISM; ORGAN SIZE; OVARIECTOMY; PHYSIOLOGY; RAT; UTERUS;

ANIMALS; CARCINOGENS; COLONIC NEOPLASMS; CPG ISLANDS; DIMETHYLHYDRAZINES; DNA METHYLATION; ESTRADIOL; ESTROGENS; FEMALE; ORGAN SIZE; OVARIECTOMY; PARATHYROID HORMONE; RATS; RECEPTORS, CALCITRIOL; RNA, MESSENGER; UTERUS;

EID: 0033250830     PISSN: 09650407     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (67)

1. Francavilla, A.; Di Léo, A.; Polimeno, L.; Conte, D.; Barone, M.; Fanizza, G.; Chiumarulo, C.; Rizzo, G.; Rubino, M. Nuclear and cytosolic estrogen receptors in human colon carcinoma and in surrounding noncancerous colonie tissue. Gastroenterology 93:1301-1306; 1987.
2. Utsumi, Y.; Nakamura, T.; Nagasue, N.; Kubota, H.; Harada, T.; Morikawa, S. Effect of 17β-estradiol on the growth of an estrogen receptor-positive human esophageal carcinoma cell line. Cancer 67:2284-2289; 1991.
3. Meggouh, F.; Lointier, P.; Saez, S. Sex steroid and 1,25-dihydroxyvitamin Dj receptors in human colorcctal adenocarcinoma and normal mucosa. Cancer Res 51:1227-1233; 1991.
4. Hendrickse, C. W.; Jones, C. E.; Donovan, I. A.; Neoptolemos, J. P.; Baker, P. R. Oestrogen and progesterone receptors in colorectal cancer and human colonie cancer cell lines. Br. J. Surg. 80: 636-640; 1993.
5. Singh, S.; Sheppard, M. C.; Langman, M. J. Sex differences in the incidence of colorectal cancer: An exploration of oestrogen and progesterone receptors. Gut 34:611-615; 1993.
6. Theisinger, B.; Guthke, R.; Blin, N.; Welter, C.; Scitz, G. Influence of steroid hormones on pS2/BCEI gene expression in xenografted colon tumors. In Vivo 7:411-414; 1993.
7. Luqmani, Y. A.; Ryall, G.; Shousha, S.; Coombes, R. C. An immunohistochemical survey of pS2 expression in human epithelial cancers. Int. J. Cancer 50:302-304; 1992.
8. Welter, C.; Scitz, G.; Blin, N. Expression of the breast cancerassociated protein pS2 in adenosquamous carcinomas of the gastrointestinal tract. Acta Oncol. 32:315-317; 1993.
9. Welter, C.; Theisinger, B.; Rio, M. C.; Scitz, G.; Schuder, G.; Blin, N. Expression pattern of breast-cancer-associated protein pS2/BCEI in colorectal tumors. Int. J. Cancer 56:52-55; 1994.
10. Takeda, H.; Yamakawa, M.; Takahashi, T.; Imai, Y.; Ishikawa, M. An immunohistochemical study with an estrogen receptor-related protein (ER-D5) in human colorectal cancer. Cancer 69:907-912; 1992.
11. Di Leo, A.; Linsalata, M.; Cavallini, A.; Messa, C.; Russo, F. Sex steroid hormone receptors, epidermal growth factor receptor, and polyamines in human colorectal cancer. Dis. Colon Rectum 35: 305-309; 1992.
12. Dawson, P. M.; Shousha, S.; Blair, S. D.; Carter, G. D.; Jones, J.; Alaghband Zadeh, J.; Theodorou, N. A. Oestrogen receptors in colorectal carcinoma. J. Clin. Pathol. 43:149-151; 1990.
13. Issa, J. P.; Ottaviano, Y. L.; Celano, P.; Hamilton, S. R.; Davidson, N. E.; Baylin, S. B. Melhylation of the oestrogen receptor CpG island links aging and neoplasia in human colon. Nat. Genet. 7:536-540; 1994.
14. Chute, C. G.; Willett, W. C.; Colditz, G. A.; Stampfer, M. J.; Rosner, B.; Speizer, F. E. A prospective study of reproductive history and exogenous estrogens on the risk of colorectal cancer in women. Epidemiology 2:201-207; 1991.
15. Newcomb, P. A.; Storer, B. E. Postmenopausal hormone use and risk of large bowel cancer. J. Nail. Cancer Inst. 87:1067-1071; 1995.
16. Grodstcin, F.; Martinez, E.; Platz, E. A.; Giovannucci, E.; Colditz, G. A.; Kautzky, M.; Fuchs, C.; Stampfer, M. J. Postmenopausal hormone use and risk for colorectal cancer and adenoma. Ann. Intern. Med. 128:705-712; 1998.
17. Dos Santos Suva, I.; Swerdlow, A. J. Sex differences in time trends of colorectal cancer in England and Wales: The possible effect of female hormonal factors. Br. J. Cancer 73:692-697; 1996.
18. Gerhardsson de Verdier, M.; London, S. Reproductive factors, exogenous female hormones, and colorectal cancer by subsite. Cancer Causes Control 3:355-360; 1992.
19. Jacobs, E. J.; White, E.; Weiss, N. S. Exogenous hormones, reproductive history, and colon cancer (Seattle, Washington, USA). Cancer Causes Control 5:359-366; 1994.
20. Calle, E. E.; Miracle McMahill, H. L.; Thun, M. J.; Heath, C. W., Jr. Estrogen replacement therapy and risk of fatal colon cancer in a prospective cohort of postmenopausal women. J. Nail. Cancer Inst. 87:517-523; 1995.
21. Delhougne, B.; Deneux, C; Abs, R.; Chanson, P.; Fierens, H.; Laurentpuig, P.; Duysburgh, L; Stevenaert, A.; Tabarin, A.; Delwaide, J.; Schaison, G.; Belaiche, J.; Beckers, A. The prevalence of colonie polyps in acromegaly: A colonoscopic and pathological study in 103 patients. J. Clin. Endocrinol. Metab. 80:3223-3226; 1995.
22. Garland, C.; Shekelle, R. B.; Barrett-Connor, E.; Criqui, M. H.; Rossof, A. H.; Paul, O. Dietary vitamin D and calcium and risk of colorectal cancer: A 19 year prospective study in men. Lancet 1:307-309; 1985.
23. Garland, C. F.; Garland, F. C.; Gorham, E. D. Can colon cancer incidence and death rates be reduced with calcium and vitamin D. Am. J. Clin. Nutr. 54:193S-201S; 1991.
24. Eisman, J.; Barkla, D. H.; Tutton, P. J. M. Suppression of in-vivo growth of human cancer solid tumor xenograft by 1,25-dihydroxyvitamin Dj. Cancer Res. 47:21-25; 1987.
25. Tanaka, Y.; Wu, A. Y.; Ikekawa, N.; Iseki, K.; Kawai, M.; Kobayashi, Y. Inhibition of HT-29 human colon cancer growth under the renal capsule of severe combined immunodeficient mice by an analogue of 1,25-dihydroxyvitamin D3, DD-003. Cancer Res. 54: 5148-5153; 1994.
26. Thomas, M. G.; Tebbut, S.; Williamson, R. C. N. l,25(OH)Dj inhibits crypt cell proliferation in human colorectal mucosa. In: Norman, A. W.; Bouillon, R.; Thomasset, M., eds. Proceedings of 8lh Workshop on Vitamin D. Berlin/New York: Walter de Gruyter; 1991:453-454.
27. Brasitus, T. A.; Sitrin, M. D. Chemoprevention of colon cancer by vitamin D3 and its metabolites/analogs. In: Feldman, D.; Glorieux, F. H.; Pike, J. W., eds. Vitamin D. San Diego: Academic Press; 1997:1141-1154.
28. Hewison, M.; O'Riordan, L. Immunomodulatory and cell differentiation effects of vitamin D. In: Feldman, D.; Glorieux, F. H.; Pike, J. W., eds. Vitamin D. San Diego: Academic Press; 1997: 447-462.
29. Walters, M. R. An estrogen-stimulated l ,25-dihydroxyvitamin D3 receptor in rat uterus. Biophys. Biochem. Res. Commun. 103: 721-726; 1981.
30. Levy, J.; Zuili, L; Yankowitz, N.; Shany, S. Induction of cytosolic receptors for 1,25 dihydroxyvitamin D3 in the immature rat uterus by oestradiol. J. Endocrinol. 100:265-269; 1984.
31. Davoodi, F.; Brenner, R. V.; Evans, S. R.; Schumaker, L. M.; Shabahang, M.; Nauta, R. J.; Buras, R. R. Modulation of vitamin D receptor and estrogen receptor by l,25(OH)2-vitamin Dj in T47D human breast cancer cells. J. Steroid Biochem. Mol. Biol. 54: 147-153;1995.
32. Liel, Y.; Kraus, S.; Levy, J.; Shany, S. Evidence that estrogens modulate activity and increase the number of 1,25-dihydroxyvitamin Dj receptors in osteoblast-Iike cells (ROS 17/2.8). Endocrinology 130:2597-2601; 1992.
33. Liel, Y.; Shany, S.; Smirnoff, P.; Schwanz, B. Estrogen increases 1,25-dihydroxyviatmin D receptors expression and bioresponse in the rat duodenal mucosa. Endocrinology 140:280-285; 1999.
34. Schwanz, B.; Avivi, C.; Lamprecht, S. A. Isolation and characterization of normal and neoplastic colonie epithelial cell populations. Gastroenterology 100:692-702; 1991.
35. Adams, J. S.; Singer, F. R.; Gacad, M. A.; Sharma, O. P.; Hayes, M. J.; Vouros, P.; Holick, M. F. Isolation and structural identification of 1,25-dihydroxy vitamin D3 produced by cultured alveolar macrophages in sarcoidosis. J. Clin. Endocrinol. Metab. 60:969-966; 1985.
36. Reinhard!, T. A.; Horst, R. L.; Orf, J. W.; Hollis, B. .W. A microassay for l,25(OH)2Dj not requiring HPLC. Applications to clinical studies. J. Clin. Endocrinol. Metab. 58:91-98; 1984..
37. Shany, S.; Rapoport, J.; Zuili, L; Yankowitz, N.; Chaimovitz, C. Enhancement of 24,25-dihydroxyvitamin D levels in patients treated with continuous ambulatory peritoneal dialysis. Nephron 42:141-145; 1986.
38. Kirschbaum, B. Use of the bicinchoninic acid assay in measuring urinary proteins. Clin. Chem. 32:572; 1986.
39. Chomczynski, P.; Sacchi, N. Single-step method of RNA isolation by acid guanidinium miocyanate-phenol-chloroform extraction. Anal. Biochem. 162:156-159; 1987.
40. lida, K.; Taniguchi, S.; Kurokawa, K. Distribution of 1,25-dihydroxyvitamin D3 receptor and 25-hydroxyvitamin Dj-24-hydroxylase mRNA expression along rat nephron segments. Biochem. Biophys. Res. Commun. 194:659-664; 1993.
41. Michalowsky, L. A.; Jones, P. A. Gene structure and transcription in mouse cells with extensively demethylated DNA. Mol. Cell. Biol. 9:885-892; 1989.
42. Burmester, J. K.; Wiese, R. J.; Maeda, N.; DcLuca, H. F. Structure and regulation of the rat 1,25-dihydroxyvitamin Dj receptor. Proc. Natl. Acad. Sci. USA 85:9499-9502; 1988.
43. Hoff, M. B.; Chang, W. W. L.; Mak, K. M. Effect of estrogen on cell proliferation in colonie mucosa of the mouse. Virchow Arch. Cell Pathol. 35:263-273; 1981.
44. Lointier, P.; Wildrick, D. M.; Boman, B. M. The effects of steroid hormones on a human colon cancer cell line in vitro. Anticancer Res. 12:1327-1330; 1992.
45. Turusov, V. S.; Morozova, O. V.; Samoilov, D. V. Estrogen modification of 1,2-dimcthylhydrazine carcinogenesis in C3HA mice. Cancer Lett. 83:51-58; 1994.
46. Gershbein, L. L. Action of estrogen and adrenocorticoids on adenocarcinoma induction by 1,2-dimethylhydrazine in male rats. Res. Commun. Chem. Pathol. Pharmacol. 81:117-120; 1993.
47. McMichael, A. J.; Potter, J. D. Reproduction, endogenous and exogenous sex hormones, and colon cancer: A review and hypothesis. J. Natl. Cancer Inst. 65:1201-1207; 1980.
48. Koch, M.; McPherson, T. A.; Egedahl, R. D. Effect of sex and reproductive history on the survival of patients with colorectal cancer. J. Chron. Dis. 35:69-72; 1982.
49. La Vecchia, C.; Franceschi, S. Reproductive factors and colorectal cancer. Cancer Causes Control 2:193-200; 1991.
50. Chu, K. C.; Tarone, R. E.; Chow, W. H.; Hankey, B. F.; Ries, L. A. Temporal patterns in colorectal cancer incidence, survival, and mortality from 1950 through 1990. J. Natl. Cancer Inst. 86:997-1006; 1994.
51. Martinez, M. E.; Willett, W. C. Calcium, vitamin D, and colorectal cancer: A review of the epidemiologic evidence. Cancer Epidemiol. Biomarker Prev. 7:163-168; 1998.
52. Fernandez, E.; LaVecchia, C.; Braga, C.; Talamini, R.; Negri, E.; Parazzini, F.; Franceschi, S. Hormone replacement therapy and risk of colon and rectal cancer. Cancer Epidemiol. Biomarker Prev. 7:329-333; 1998.
53. Fernandez, E.; LaVecchia, C; Franceschi, S.; Braga, C.; Talamini, R.; Negri, E.; Parazzini. F. Oral contraceptive use and risk of colorectal cancer. Epidemiology 9:295-300; 1998.
54. Counts, J. L.; Goodman, J. I. Alterations in DNA methylation may play a variety of roles in carcinogenesis. Cell 83:13-15; 1995.
55. Zingg, J. M.; Jones, P. A. Genetic and epigenetic aspects of DNA methylation on genome expression, evolution, mutation and carcinogenesis. Carcinogenesis 18:869-882; 1997.
56. Wiencke, J. K.; Zheng, S.; Lafuente, A.; Lafuente, M. J.; Grudzen, C.; Wrensch, M. R.; Make, R.; Ballesta, A.; Trias, M. Aberrant methylation of p 16 INK 4 a in anatomic and gender-specific subtypes of sporadic colorectal cancer. Cancer Epidemiol. Biomarkers Prev. 8:501-506; 1999.
57. Herfart, K. K.; Brent, T. P.; Danam, R. P.; Remack, J. S.; Kodner, I. J.; Wells, S. A.; Goodfellow, P. J. A specific CpG methylation pattern of the MGMT promoter region is associated with reduced MGMT expression in primary colorectal cancers. Mol. Carcinog. 24:90-98; 1999.
58. Herman, J. G.; Umar, A.; Polyak, K.; Graff, J. R.; Ahuja, N.; Issa, J. P.; Markowitz, S.; Wilsson, J. K.; Hamilton, S. R.; Kinzler, K. W.; Kane, M. F.; Kolodner, R. D.; Vogelstein, B.; Kunkel, T. A.; Baylin, S. B. Incidence of functional consequences of hMLHl promoter hypermethylation in colorectal carcinoma. Proc. Natl. Acad. Sci. USA 95:6870-6875; 1998.
59. Boffa, L. C.; Bolognesi, C. In vitro DNA and nuclear proteins alkylationby 1,2-dimethylhydrazine. Mutât. Res. 173:157-162; 1986.
60. Pereira, M. A.; Lin, L. H.; Herren, S. L. Role of O6-methylation in the initiation of GGTase positive foci. Chem. Biol. Interact. 43(3):313-322; 1983.
61. Brambilla, G.; Cavanna, M.; Parodi, S.; Sciaba, L.; Pino, A.; Robbianno, L. DNA damage in liver, colon, stomach, lung and kidney of BALB/c mice treated with dimethylhydrazine. Int. J. Cancer 15:22(2):174-180; 1978.
62. Rossiello, M. R.; Rao, P. M.; Rajalakshmi, S.; Sarma, D. S. R. Similar patterns of hypomethylation in the β-hydroxy-β-methylglutaryl coenzyme A reductase gene in hepatic nodules induced by different carcinogens. Mol. Carcinog. 24:90-98; 1999.
63. Belleli, A.; Shany, S.; Levy, J.; Guberman, R.; Lamprecht, S. A. A protective role of 1,25-dihydroxyvytamin D, in chemically induced rat colon carcinogenesis. Carcinogenesis 13:2293-2298; 1992.
64. Duncan, W. E.; Glass, A. R.; Wray, H. L. Estrogen regulation of the nuclear 1,25-dihydroxyvitamin D3 receptor in rat liver and kidney. Endocrinology 129:2318-2324; 1991.
65. Dokoh, S.; Donaldson, C. A.; Haussier, M. R. Influence of 1,25dihydroxyvitamin D, on cultured osteogenic sarcoma cells: Correlation with the 1,25-dihydroxyvitamin D3 receptors. Cancer Res. 44:2103-2109; 1984.
66. Liel, Y.; Shany, S.; Schwanz, B. Estrogen increases the number and bioresponse of 1,25-dihydroxy vitamin D receptors in the rat colon. Possible implications for the pathogenesis of colon cancer. In: 79th Annual Meeting of the Endocrine Society. Minneapolis, MN; 1997:P3-19 [abstract].
67. Censure, R. C.; Antrobus, S. D.; Fox, J.; Okwueze, M.; Talton, S. Y.; Walters, M. R. Homologous up-regulation of vitamin D receptors is tissue specific in the rat. J. Bone Miner. Res. 13:454-463; 1998.