Frequent HOXA11 and THBS2 promoter methylation, and a methylator phenotype in endometrial adenocarcinoma

Clinical Cancer Research

Volumn 9, Issue 6, 2003, Pages 2277-2287

  Whitcomb, Bradford P ^a   Mutch, David G ^a   Herzog, Thomas J ^a   Rader, Janet S ^a   Gibb, Randall K ^a   Goodfellow, Paul J ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENE PRODUCT; PROTEIN CDKN2A; PROTEIN CTNNB1; PROTEIN HOXA11; PROTEIN MLH1; PROTEIN THBS1; PROTEIN THBS2; PROTEIN VDR; TUMOR PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CALCULATION; CANCER RECURRENCE; CANCER STAGING; CELL LINE; CONTROLLED STUDY; CORRELATION ANALYSIS; DISEASE ASSOCIATION; DNA DETERMINATION; DNA METHYLATION; EARLY DIAGNOSIS; ENDOMETRIUM CARCINOMA; FEMALE; FISHER EXACT TEST; HISTOPATHOLOGY; HUMAN; HUMAN CELL; METHYLATION INDEX; METHYLATOR PHENOTYPE; NUCLEOTIDE SEQUENCE; PHENOTYPE; PHENOTYPIC VARIATION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN METHYLATION; STATISTICAL ANALYSIS; STATISTICAL SIGNIFICANCE; STUDENT T TEST; TREATMENT OUTCOME;

ADENOCARCINOMA; BETA CATENIN; CELL LINE, TUMOR; CYTOSKELETAL PROTEINS; DNA METHYLATION; ENDOMETRIAL NEOPLASMS; FEMALE; GENES, P16; HOMEODOMAIN PROTEINS; HUMANS; PHENOTYPE; PROMOTER REGIONS (GENETICS); THROMBOSPONDIN 1; THROMBOSPONDINS; TRANS-ACTIVATORS;

EID: 0037838407     PISSN: 10780432     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (75)

1. Jemal, A., Thomas, A., Murray, T., and Thun, M. Cancer statistics, 2002. CA Cancer J. Clin., 52: 23-47, 2002.
2. Pecorelli, S. FIGO Annual report on the results of treatment in gynecological cancer. J. Epidemiol. Biostat., 3: 1-168, 1998.
3. Creutzberg, C. L., van Putten, W. L., Koper, P. C., Lybeert, M. L., Jobsen, J. J., Warlam-Rodenhuis, C. C., De Winter, K. A., Lutgens, L. C., van den Bergh, A. C., van de Steen-Banasik, E., Beerman, H., and van Lent, M. Surgery and postoperative radiotherapy versus surgery alone for patients with stage-1 endometrial carcinoma: multicentre randomised trial. PORTEC Study Group. Post Operative Radiation Therapy in Endometrial Carcinoma. Lancet, 355: 1404-1411, 2000.
4. Jereczek-Fossa, B., Badzio, A., and Jassem, J. Surgery followed by radiotherapy in endometrial cancer: analysis of survival and patterns of failure. Int. J. Gynecol. Cancer, 9: 285-294, 1999.
5. Sasaki, M., Kotcherguina, L., Dharia, A., Fujimoto, S., and Dahiya, R. Cytosine-phosphoguanine methylation of estrogen receptors in endometrial cancer. Cancer Res., 61: 3262-3266, 2001.
6. Sasaki, M., Oh, B. R., Dharia, A., Fujimoto, S., and Dahiya, R. Inactivation of the human androgen receptor gene is associated with CpG hypermethylation in uterine endometrial cancer. Mol. Carcinog., 29: 59-66, 2000.
7. Enomoto, T., Fujita, M., Inoue, M., Rice, J. M., Nakajima, R., Tanizawa, O., and Nomura, T. Alterations of the p53 tumor suppressor gene and its association with activation of the c-K-ras-2 protooncogene in premalignant and malignant lesions of the human uterine endometrium. Cancer Res., 53: 1883-1888, 1993.
8. Honda, T., Kato, H., Imamura, T., Gima, T., Nishida, J. I., Sasaki, M., Hoshi, K., Sato, A., and Wake, N. Involvement of p53 gene mutations in human endometrial carcinomas. Int. J. Cancer, 53: 963-967, 1993.
9. Risinger, J. I., Berchuck, A., Kohler, M. F., Watson, P., Lynch, H. T., and Boyd, J. Genetic instability of microsatellites in endometrial carcinoma. Cancer Res., 53: 5100-5103, 1993.
10. Kobayashi, K., Sagae, S., Nishioka, Y., Tokino, T., and Kudo, R. Mutations of the β-catenin gene in endometrial carcinomas. Jpn. J. Cancer Res., 90: 55-59, 1999.
11. Fukuchi, T., Sakamoto, M., Tsuda, H., Maruyama, K., Nozawa, S., and Hirohashi, S. β-Catenin mutation in carcinoma of the uterine endometrium. Cancer Res., 58: 3526-3528, 1998.
12. Simpkins, S. B., Bocker, T., Swisher, E. M., Mutch, D. G., Gersell, D. J., Kovatich, A. J., Palazzo, J. P., Fishel, R., and Goodfellow, P. J. MLH1 promoter methylation and gene silencing is the primary cause of microsatellite instability in sporadic endometrial cancers. Hum. Mol. Genet., 8: 661-666, 1999.
13. Swisher, E. M., Peiffer-Schneider, S., Mutch, D. G., Herzog, T. J., Rader, J. S., Elbendary, A., and Goodfellow, P. J. Differences in patterns of TP53 and KRAS2 mutations in a large series of endometrial carcinomas with or without microsatellite instability. Cancer (Phila.), 85: 119-126, 1999.
14. Sasaki, H., Nishii, H., Takahashi, H., Tada, A., Furusato, M., Terashima, Y., Siegal, G. P., Parker, S. L., Kohler, M. F., Berchuck, A., and Boyd, J. Mutation of the Ki-ras protooncogene in human endometrial hyperplasia and carcinoma. Cancer Res., 53: 1906-1910, 1993.
15. Kong, D., Suzuki, A., Zou, T-T., Sakurada, A., Kemp, L. W., Wakatsuki, S., Yokoyama, T., Yamakawa, H., Furukawa, T., Sato, M., Ohuchi, N., Sato, S., Yin, J., Wang, S., Abraham, J. M., Souza, R. F., Smolinski, K. N., Meltzer, S. J., and Horii, A. PTEN1 is frequently mutated in primary endometrial carcinomas. Nat. Genet., 17: 143-144, 1997.
16. DiSaia, P. J., and Creasman, W. T. Clinical Gynecologic Oncology, 6th edition. St. Louis: Mosby, Inc., 2002.
17. Kodama, S., Kase, H., Tanaka, K., and Matsui, K. Multivariate analysis of prognostic factors in patients with endometrial cancer. Int. J. Gynaecol. Obstet., 53: 23-30, 1996.
18. Tsuruchi, N., Kaku, T., Kamura, T., Tsukamoto, N., Tsuneyoshi, M., Akazawa, K., and Nakano, H. The prognostic significance of lymphovascular space invasion in endometrial cancer when conventional hemotoxylin and eosin staining is compared to immunohistochemical staining. Gynecol. Oncol., 57: 307-312, 1995.
19. Jhala, D. N., Atkinson, B. F., Balsara, G. R., Hernandez, E., and Jhala, N. C. Role of DNA ploidy analysis in endometrial adenocarcinoma. Ann. Diag. Pathol., 5: 267-273, 2001.
20. Grulich, D., Hagen, A., and Morack, G. Prognostic factors and results of treatment in endometrial carcinoma. Zentralbl. Gynakol., 118: 154-163, 1996.
21. Seki, N., Kodama, J., Hashimoto, I., Hongo, A., Yoshinouchi, M., and Kudo, T. Thrombospondin-1 and -2 messenger RNA expression in normal and neoplastic endometrial tissues: correlation with angiogenesis and prognosis. Int. J. Oncol., 19: 305-310, 2001.
22. Coronado, P. J., Vidart, J. A., Lopez-asenjo, J. A., Fasero, M., Furio-bacete, V., Magrina, J., Escudero, M., and Taketani, Y. P53 overexpression predicts endometrial carcinoma recurrence better than HER-2/neu overexpression. Eur. J. Obstet. Gynecol. Reprod. Biol., 98: 103-108, 2001.
23. Fiumicino, S., Ercoli, A., Ferrandina, G., Hess, P., Raspaglio, G., Genuardi, M., Rovella, V., Bellacosa, A., Cicchillitti, L., Mancuso, S., Bignami, M., and Scambia, G. Microsatellite instability is an independent indicator of recurrence in sporadic stage I-II endometrial adenocarcinoma. J. Clin. Oncol., 19: 1008-1014, 2001.
24. Geisler, J. P., Geisler, H. E., Wiemann, M. C., Zhou, Z., Miller, G. A., and Crabtree, W. p53 expression as a prognostic indicator of 5-year survival in endometrial cancer. Gynecol Oncol, 74: 468-471, 1999.
25. Basil, J. B., Goodfellow, P. J., Rader, J. S., Mutch, D. G., and Herzog, T. J. Clinical significance of microsatellite instability in endometrial cancer. Cancer (Phila.), 89: 1758-1764, 2000.
26. Peiro, G., Diebold, J., Mayr, D., Baretton, G. B., Kimmig, R., Schmidt, M., and Lohrs, U. Prognostic relevance of hMLH1, hMSH2, and BAX protein expression in endometrial carcinoma. Mod. Pathol., 14: 777-783, 2001.
27. Jones, P. A. DNA methylation errors and cancer. Cancer Res., 56: 2463-2467, 1996.
28. Goelz, S. E., Vogelstein, B., Hamilton, S. R., and Feinberg, A. P. Hypomethylation of DNA from benign and malignant human colon neoplasms. Science (Wash. DC), 228: 187-190, 1985.
29. Baylin, S. B., Herman, J. G., Graff, J. R., Vertino, P. M., and Issa, J. P. Alterations in DNA methylation: a fundamental aspect of neoplasia. Adv. Cancer Res., 72: 141-196, 1998.
30. Herman, J. G., and Baylin, S. B. Promoter-region hypermethylation and gene silencing in human cancer. Curr. Top. Microbiol. Immunol., 249: 35-54, 2000.
31. Bird, A. P. CpG-rich islands and the function of DNA methylation. Nature (Lond.), 321: 209-213, 1986.
32. Maruyama, R., Toyooka, S., Toyooka, K. O., Harada, K., Virmani, A. K., Zochbauer-Muller, S., Farinas, A. J., Vakar-Lopez, F., Minna, J. D., Sagalowsky, A., Czerniak, B., Gazdar, A. F., Anant, S., Lee, R. M., Kennedy, S., Viskochil, D., and Davidson, N. O. Aberrant promoter methylation profile of bladder cancer and its relationship to clinicopathological features. Cancer Res., 61: 8659-8663, 2001.
33. Maruyama, R., Toyooka, S., Toyooka, K. O., Virmani, A. K., Zochbauer-Muller, S., Farinas, A. J., Minna, J. D., McConnell, J., Frenkel, E. P., and Gazdar, A. F. Aberrant promoter methylation profile of prostate cancers and its relationship to clinicopathological features. Clin. Cancer Res., 8: 514-519, 2002.
34. Toyota, M., Ahuja, N., Ohe-Toyota, M., Herman, J. G., Baylin, S. B., and Issa, J. P. CpG island methylator phenotype in colorectal cancer. Proc. Natl. Acad. Sci. USA, 96: 8681-8686, 1999.
35. Toyota, M., Ahuja, N., Suzuki, H., Itoh, F., Ohe-Toyota, M., Imai, K., Baylin, S. B., and Issa, J. P. Aberrant methylation in gastric cancer associated with the CpG island methylator phenotype. Cancer Res., 59: 5438-5442, 1999.
36. Toyota, M., and Issa, J. P. CpG island methylator phenotypes in aging and cancer. Semin. Cancer Biol., 9: 349-357, 1999.
37. Strathdee, G., Appleton, K., Illand, M., Millan, D. W., Sargent, J., Paul, J., and Brown, R. Primary ovarian carcinomas display multiple methylator phenotypes involving know tumor suppressor genes. Am. J. Pathol., 158: 1121-1127, 2001.
38. Toyota, M., Ohe-Toyota, M., Ahuja, N., and Issa, J. J. Distinct genetic profiles in colorectal tumors with or without the CpGisland methylator phenotype. Proc. Natl. Acad. Sci. USA, 97: 710-715, 2000.
39. Ueki, T., Toyota, M., Sohn, T., Yeo, C. J., Issa, J. P., Hruban, R. H., and Goggins, M. Hypermethylation of multiple genes in pancreatic adenocarcinoma. Cancer Res., 60: 1835-1839, 2000.
40. Esteller, M., Corn, P. G., Baylin, S. B., and Herman, J. G. A gene hypermethylation profile of human cancer. Cancer Res., 61: 3225-3229, 2001.
41. Kwong, J., Lo, K. W., To, K. F., Teo, P. M., Johnson, P. J., and Huang, D. P. Promoter hypermethylation of multiple genes in nasopharyngeal carcinoma. Clin. Cancer Res., 8: 131-137, 2002.
42. Esteller, M., Catasus, L., Matias-Guiu, X., Mutter, G. L., Prat, J., Baylin, S. B., and Herman, J. G. hMLH1 promoter hypermethylation is an early event in human endometrial tumorigenesis. Am. J. Pathol., 155: 1767-1772, 1999.
43. Wong, Y. F., Chung, T. K., Cheung, T. H., Nobori, T., Yu, A. L., Yu, J., Batova, A., Lai, K. W., and Chang, A. M. Methylation of p16INK4A in primary gynecologic malignancy. Cancer Lett., 136: 231-235, 1999.
44. Gargett, C. E., and Rogers, P. A. Human endometrial angiogenesis. Reproduction, 121: 181-186, 2001.
45. Iruela-Arispe, M. L., Porter, P., Bornstein, P., and Sage, E. H. Thrombospondin-1, an inhibitor of angiogenesis, is regulated by progesterone in the human endometrium. J. Clin. Investig., 97: 403-412, 1996.
46. Gendron, R. L., Paradis, H., Hsieh-Li, H. M., Lee, D. W., Potter, S. S., and Markoff, E. Abnormal uterine stromal and glandular function associated with maternal reproductive defects in Hoxa-11 null mice. Biol. Reprod., 56: 1097-1105, 1997.
47. Hsieh-Li, H. M., Witte, D. P., Weinstein, M., Branford, W., H., L., Small, K., and Potter, S. S. Hoxa 11 structure, extensive antisense transcription, and function in male and female fertility. Development, 121: 1373-1385, 1995.
48. van den Bemd, G. J., and Chang, G. T. Vitamin D and vitamin D analogs in cancer treatment. Curr. Drug Targets, 3: 85-94, 2002.
49. Yabushita, H., Hirata, M., Noguchi, M., and Nakanishi, M. Vitamin D receptor in endometrial carcinoma and the differentiation-inducing effect of 1, 25-dihydroxyvitamin D3 on endometrial carcinoma cell lines. J. Obstet. Gynaecol. Res., 22: 529-539, 1996.
50. Powell, M. A., Mutch, D. G., Rader, J. S., Herzog, T. J., Huang, T. H., and Goodfellow, P. J. Ribosomal DNA methylation in patients with endometrial carcinoma. Cancer (Phila.), 94: 2941-2952, 2002.
51. Horowitz, N., Pinto, K., Mutch, D., Herzog, T., Rader, J., Gibb, R., Bocker Edmonston, T., and Goodfellow, P. Microsatellite Instability. MLH1 promoter methylation and loss of mismatch repair in endometrial cancer and concomitant atypical hyperplasia. Gynecol. Oncol., 86: 62-68, 2002.
52. Xiong, Z., and Laird, P. W. COBRA: a sensitive and quantitative DNA methylation assay. Nucleic Acids Res., 25: 2532-2534, 1997.
53. Yamamoto, H., Min, Y., Itoh, F., Imsumran, A., Horiuchi, S., Yoshida, M., Iku, S., Fukushima, H., and Imai, K. Differential involvement of the hypermethylator phenotype in hereditary and sporadic colorectal cancers with high-frequency microsatellite instability. Genes Chromosomes Cancer, 33: 322-325, 2002.
54. Miyakura, Y., Sugano, K., Konishi, F., Ichikawa, A., Maekawa, M., Shitoh, K., Igarashi, S., Kotake, K., Koyama, Y., and Nagai, H. Extensive methylation of hMLH1 promoter region predominates in proximal colon cancer with microsatellite instability. Gastroenterology, 121: 1300-1309, 2001.
55. Herman, J. G., Graff, J. R., Myohanen, S., Nelkin, B. D., and Baylin, S. B. Methylation-specific PCR: a novel PCR assay for methylation status of CpG islands. Proc. Natl. Acad. Sci. USA, 93: 9821-9826, 1996.
56. Esteller, M., Tortola, S., Toyota, M., Capella, G., Peinado, M. A., Baylin, S. B., and Herman, J. G. Hypermethylation-associated inactivation of p14(ARF) is independent of p16(INK4a) methylation and p53 mutational status. Cancer Res., 60: 129-133, 2000.
57. Tsuda, H., Yamamoto, K., Inoue, T., Uchiyama, I., and Umesaki, N. The role of p16-cyclin d/CDK-pRb pathway in the tumorigenesis of endometriod-type endometrial carcinoma. Br. J. Cancer, 82: 675-682, 2000.
58. Chao, H., Sun, J., and Lu, S. Methylation and expression of the p16 gene in endometrial carcinoma. Zhonghua Zhong Liu Za Zhi, 22: 228-231, 2000.
59. Nakashima, R., Fujita, M., Enomoto, T., Haba, T., Yoshino, K., Wada, H., Kurachi, H., Sasaki, M., Wakasa, K., Inoue, M., Buzard, G., and Murata, Y. Alteration of p16 and p15 genes in human uterine tumors. Br. J. Cancer, 80: 458-467, 1999.
60. Salvesen, H. B., Das, S., and Akslen, L. A. Loss of nuclear p16 protein expression is not associated with promoter methylation but defines a subgroup of aggressive endometrial carcinomas with poor prognosis. Clin. Cancer Res., 6: 153-159, 2000.
61. Li, Q., Ahuja, N., Burger, P. C., and Issa, J. P. Methylation and silencing of the Thrombospondin-1 promoter in human cancer. Oncogene, 18: 3284-3289, 1999.
62. Ahuja, N., Mohan, A. L., Li, Q., Stolker, J. M., Herman, J. G., Hamilton, S. R., Baylin, S. B., and Issa, J-P. J. Association between CpG island methylation and microsatellite instability in colorectal cancer. Cancer Res., 57: 3370-3374, 1997.
63. Salvesen, H. B., and Akslen, L. A. Significance of tumour-associated macrophages, vascular endothelial growth factor and Thrombospondin-1 expression for tumour angiogenesis and prognosis in endometrial carcinomas. Int. J. Cancer, 84: 538-543, 1999.
64. Palacios, J., Catasus, L., Moreno-Bueno, G., Matias-Guiu, X., Prat, J., and Gamallo, C. β- and γ-catenin expression in endometrial carcinoma. Relationship with clinicopathological features and microsatellite instability. Virchows Arch., 438: 464-469, 2001.
65. Jones, M., and Nakamura, Y. Deletion mapping of chromosome 3p in female genital tract malignancies using microsatellite polymorphisms. Oncogene, 7: 1631-1634, 1992.
66. Jones, M. H., Koi, S., Fujimoto, I., Hasumi, K., Kato, K., and Nakamura, Y. Allelotype of uterine cancer by analysis of RFLP and microsatellite polymorphisms: Frequent loss of heterozygosity on chromosome amrs 3p, 9q, 10q, and 17p. Genes Chromosomes Cancer, 9: 119-123, 1994.
67. Arlt, M. F., Herzog, T. J., Mutch, D. G., and Goodfellow, P. J. Loss of heterozygosity of chromosome 3p sequence is an infrequent event in endometrial cancer. Gynecol. Oncol., 60: 308-312, 1996.
68. Eads, C., Lord, R., Wickramasinghe, K., Long, T., Kurumboor, S., Bernstein, L., Peters, J., DeMeester, S., DeMeester, T., Skinner, K., and Laird, P. Epigenetic patterns in the progression of esophageal adenocarcinoma. Cancer Res., 61: 3410-3418, 2001.
69. Smirnoff, P., Liel, Y., Gnainsky, J., Shany, S., and 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., 11: 255-264, 1999.
70. Taylor, H. S., Vanden Heuvel, G. B., and Igarashi, P. A conserved Hox axis in the mouse and human female reproductive system: late establishment and persistent adult expression of the Hoxa cluster genes. Biol. Reprod., 57: 1338-1345, 1997.
71. Taylor, H. S., Igarashi, P., Olive, D. L., and Arici, A. Sex steroids mediate HOXA11 expression in the human peri-implantation endometrium. J. Clin. Endocrinol. Metab., 84: 1129-1135, 1999.
72. Taylor, H. S., Bagot, C., Kardana, A., Olive, D., and Arici, A. HOX gene expression is altered in the endometrium of women with endometriosis. Hum. Reprod., 14: 1328-1331, 1999.
73. Ma, L., Benson, G. V., Lim, H., Dey, S. K., and Maas, R. L. Abdominal B (AbdB) Hoxa genes: regulation in adult uterus by estrogen and prosterine and repression in Mullerian duct by the synthetic estrogen diethylstilbestrol (DES). Dev. Biol., 197: 141-154, 1998.
74. Li, S., Ma, L., Chiang, T., Burow, M., Newbold, R. R., Negishi, M., Barrett, J. C., and McLachlan, J. A. Promoter CpG methylation of Hox-a10 and Hox-a11 in mouse uterus not altered upon neonatal diethylstilbestrol exposure. Mol. Carcinog., 32: 213-219, 2001.
75. Newbold, R. R., Bullock, B. C., and McLachlan, J. A. Uterine adenocarcinoma in mice following developmental treatment with estrogens: a model for hormonal carcinogenesis. Cancer Res., 50: 7677-7681, 1990.