Inhibition of the interferon-γ/signal transducers and activators of transcription (STAT) pathway by hypermethylation at a STAT-binding site in the p21(WAF1) promoter region

Cancer Research

Volumn 60, Issue 12, 2000, Pages 3290-3298

  Chen, Bin ^a,b   He, Ling ^b   Savell, Van H ^b   Jenkins, Jesse J ^c   Parham, David M ^b  

^a CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

^b ARKANSAS CHILDREN S HOSPITAL   (United States)

^c ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; CYCLIN DEPENDENT KINASE INHIBITOR; GAMMA INTERFERON; MESSENGER RNA; PROTEIN P21; STAT PROTEIN;

ARTICLE; CELL GROWTH; CONTROLLED STUDY; ELECTROPHORETIC MOBILITY; GROWTH INHIBITION; HUMAN; HUMAN CELL; METHYLATION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; RHABDOMYOSARCOMA; SIGNAL TRANSDUCTION; SOUTHERN BLOTTING;

ANTIMETABOLITES, ANTINEOPLASTIC; AZACITIDINE; BLOTTING, SOUTHERN; CELL DIVISION; CPG ISLANDS; CYCLIN-DEPENDENT KINASE INHIBITOR P21; CYCLINS; DNA METHYLATION; DNA MUTATIONAL ANALYSIS; DNA-BINDING PROTEINS; DOSE-RESPONSE RELATIONSHIP, DRUG; GENES, REPORTER; HUMANS; INTERFERON TYPE II; LUCIFERASES; MUSCLE NEOPLASMS; MUSCLE, SKELETAL; POLYMORPHISM, GENETIC; PROMOTER REGIONS (GENETICS); RESPONSE ELEMENTS; RHABDOMYOSARCOMA; SIGNAL TRANSDUCTION; STAT1 TRANSCRIPTION FACTOR; TIME FACTORS; TRANS-ACTIVATORS; TRANSFECTION; TUMOR CELLS, CULTURED; UP-REGULATION;

EID: 0034046395     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (54)

1. el-Deiry, W. S., Tokino, T., Velculescu, V. E., Levy, D. B., Parsons, R., Trent, J. M., Lin, D., Mercer, W. E., Kinzler, K. W., and Vogelstein, B. WAF1, a potential mediator of p53 tumor suppression. Cell, 75: 817-825, 1993.
2. Harper, J. W., Adami, G. R., Wei, N., Keyomarsi, K., and Elledge, S. J. The p21 Cdk-interacting protein Cip1 is a potent inhibitor of G1 cyclin-dependent kinases. Cell, 75: 805-816, 1993.
3. Gu, Y., Turck, C. W., and Morgan, D. O. Inhibition of CDK2 activity in vivo by an associated 20K regulatory subunit. Nature (Lond.), 366: 707-710, 1993.
4. Hunter, T. Braking the cycle. Cell, 75: 839-841, 1993.
5. Sherr, C. J., and Roberts, J. M. Inhibitors of mammalian G1 cyclin-dependent kinases. Genes Dev., 9: 1149-1163, 1995.
6. 1 arrest and apoptosis. Cancer Res., 54: 1169-1174, 1994.
7. Darnell, J. E., Jr. STATs and gene regulation. Science (Washington DC), 277: 1630-1635, 1997.
8. Horvath, C. M., Wen, Z., and Darnell, J. E., Jr. A STAT protein domain that determines DNA sequence recognition suggests a novel DNA-binding domain. Genes Dev., 9: 984-994, 1995.
9. Chin, Y. E., Kitagawa, M., Su, W. C., You, Z. H., Iwamoto, Y., and Fu, X. Y. Cell growth arrest and induction of cyclin-dependent kinase inhibitor p21 WAF1/CIP1 mediated by STAT1. Science (Washington DC), 272: 719-722, 1996.
10. Bromberg, J. F., Horvath, C. M., Wen, Z., Schreiber, R. D., and Darnell, J. E., Jr. Transcriptionally active Stat1 is required for the antiproliferative effects of both interferon alpha and interferon γ. Proc. Natl. Acad. Sci. USA, 93: 7673-7678, 1996.
11. Chin, Y. E., Kitagawa, M., Kuida, K., Flavell, R. A., and Fu, X. Y. Activation of the STAT signaling pathway can cause expression of caspase 1 and apoptosis. Mol. Cell. Biol., 17: 5328-5337, 1997.
12. Xu, X., Fu, X. Y., Plate, J., and Chong, A. S. IFN-γ induces cell growth inhibition by Fas-mediated apoptosis: requirement of STAT1 protein for up-regulation of Fas and FasL expression. Cancer Res., 58: 2832-2837, 1998.
13. Parham, D. M. The molecular biology of childhood rhabdomyosarcoma. Semin. Diag. Pathol., 11: 39-46, 1994.
14. Parham, D. M., Webber, B., Holt, H., Williams, W. K., and Maurer, H. Immunohistochemical study of childhood rhabdomyosarcomas and related neoplasms. Results of an Intergroup Rhabdomyosarcoma study project. Cancer (Phila.), 67: 3072-3080, 1991.
15. Otten, A. D., Firpo, E. J., Gerber, A. N., Brody, L. L., Roberts, J. M., and Tapscott, S. J. Inactivation of MyoD-mediated expression of p21 in tumor cell lines. Cell Growth Differ., 8: 1151-1160, 1997.
16. Knudsen, E. S., Pazzagli, C., Born, T. L., Bertolaet, B. L., Knudsen, K. E., Arden, K. C., Henry, R. R., and Feramisco, J. R. Elevated cyclins and cyclin-dependent kinase activity in the rhabdomyosarcoma cell line RD. Cancer Res., 58: 2042-2049, 1998.
17. Smith, S. S. Biological implications of the mechanism of action of human DNA (cytosine-5)methyltransferase. Prog. Nucleic Acid Res. Mol. Biol., 49: 65-111, 1994.
18. Li, E., Beard, C., Forster, A. C., Bestor, T. H., and Jaenisch, R. DNA methylation, genomic imprinting, and mammalian development. Cold Spring Harbor Symp. Quant. Biol., 58: 297-305, 1993.
19. Razin, A., and Kafri, T. DNA methylation from embryo to adult. Prog. Nucleic Acid Res. Mol. Biol., 48: 53-81, 1994.
20. Li, E., Beard, C., and Jaenisch, R. Role for DNA methylation in genomic imprinting. Nature (Lond.), 366: 362-365, 1993.
21. Li, E., Bestor, T. H., and Jaenisch, R. Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell, 69: 915-926, 1992.
22. Tate, P. H., and Bird, A. P. Effects of DNA methylation on DNA-binding proteins and gene expression. Curr. Opin. Genet. Dev., 3: 226-231, 1993.
23. Gama-Sosa, M. A., Slagel, V. A., Trewyn, R. W., Oxenhandler, R., Kuo, K. C., Gehrke, C. W., and Ehrlich, M. The 5-methylcytosine content of DNA from human tumors. Nucleic Acids Res., 11: 6883-6894, 1983.
24. Flatau, E., Bogenmann, E., and Jones, P. A. Variable 5-methylcytosine levels in human tumor cell lines and fresh pediatric tumor explants. Cancer Res., 43: 4901-4905, 1983.
25. 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.
26. Merlo, A., Herman, J. G., Mao, L., Lee, D. J., Gabrielson, E., Burger, P. C., Baylin, S. B., Sidransky, D., and Baylin, S. B. 5′ CpG island methylation is associated with transcriptional silencing of the tumour suppressor p16/CDKN2/MTS1 in human cancers. Nat. Med., 1: 686-692, 1995.
27. Herman, J. G., Merlo, A., Mao, L., Lapidus, R. G., Issa, J. P., Davidson, N. E., Sidransky, D., Baylin, S. B., and Sidransky, D. Inactivation of the CDKN2/p16/MTS1 gene is frequently associated with aberrant DNA methylation in all common human cancers. Cancer Res., 55: 4525-4530, 1995.
28. Ng, M. H., Chung, Y. F., Lo, K. W., Wickham, N. W., Lee, J. C., and Huang, D. P. Frequent hypermethylation of p16 and p15 genes in multiple myeloma. Blood, 89: 2500-2506, 1997.
29. Herman, J. G. Jen, J., Merlo, A., and Baylin, S. B. Hypermethylation-associated inactivation indicates a tumor suppressor role for p15INK4B. Cancer Res., 56: 722-727, 1996.
30. Gartel, A. L., and Tyner, A. L. Transcriptional regulation of the p21(WAF1/CIP1) gene. Exp. Cell Res., 246: 280-289, 1999.
31. Shiohara, M., el-Deiry, W. S., Wada, M., Nakamaki, T., Takeuchi, S., Yang, R., Chen, D. L., Vogelstein, B., Koeffler, H. P., and Chen, D. L. Absence of WAF1 mutations in a variety of human malignancies. Blood, 84: 3781-3784, 1994.
32. Chen, B., Dias, P., Jenkins, J. J., 3rd, Savell, V. H., and Parham, D. M. Methylation alterations of the MyoD1 upstream region are predictive of subclassification of human rhabdomyosarcomas. Am. J. Pathol. 152: 1071-1079, 1998.
33. Chen, B., Liu, X., Savell, V. H., Dilday, B. R., Johnson, M. W., Jenkins, J. J., and Parham, D. M. Increased DNA methyltransferase expression in rhabdomyosarcomas. Int. J. Cancer, 83: 10-14, 1999.
34. Barletta, J. M., Rainier, S., and Feinberg, A. P. Reversal of loss of imprinting in tumor cells by 5-aza-2′-deoxycytidine. Cancer Res., 57: 48-50, 1997.
35. Bender, C. M., Pao, M. M., and Jones, P. A. Inhibition of DNA methylation by 5-aza-2′-deoxycytidine suppresses the growth of human tumor cell lines. Cancer Res., 58: 95-101, 1998.
36. Chen, B., Johanson, L., Wiest, J. S., Anderson, M. W., and You, M. The second intron of the K-ras gene contains regulatory elements associated with mouse lung tumor susceptibility. Proc. Natl. Acad. Sci. USA, 91: 1589-1593, 1994.
37. Mancini, D. N., Rodenhiser, D. I., Ainsworth, P. J., O'Malley, F. P., Singh, S. M., Xing, W., and Archer, T. K. CpG methylation within the 5′ regulatory region of the BRCA1 gene is tumor specific and includes a putative CREB binding site. Oncogene, 16: 1161-1169, 1998.
38. Wagner, B. J., Hayes, T. E., Hoban, C. J., and Cochran, B. H. The SIF binding element confers sis/PDGF inducibility onto the c-fos promoter. EMBO J., 9: 4477-4484, 1990.
39. Halevy, O., Novitch, B. G., Spicer, D. B., Skapek, S. X., Rhee, J., Hannon, G. J., Beach, D., and Lassar, A. B. Correlation of terminal cell cycle arrest of skeletal muscle with induction of p21 by MyoD. Science (Washington DC), 267: 1018-1021, 1995.
40. Parker, S. B., Eichele, G., Zhang, P., Rawls, A., Sands, A. T., Bradley, A., Olson, E. N., Harper, J. W., and Elledge, S. J. p53-independent expression of p21Cip1 in muscle and other terminally differentiating cells. Science (Washington DC), 267: 1024-1027, 1995.
41. Tate, P. H., and Bird, A. P. Effects of DNA methylation on DNA-binding proteins and gene expression. Curr. Opin. Genet. Dev., 3: 226-231, 1993.
42. Herman, J. G., Latif, F., Weng, Y., Lerman, M. I., Zbar, B., Liu, S., Samid, D., Duan, D. R., Gnarra, J. R., Linehan, W. M., and Baylin, S. B. Silencing of the VHL tumor-suppressor gene by DNA methylation in renal carcinoma. Proc. Natl. Acad. Sci. USA, 91: 9700-9704, 1994.
43. Young, H. A., Ghosh, P., Ye, J., Lederer, J., Lichtman, A., Gerard, J. R., Penix, L., Wilson, C. B., Melvin, A. J., McGurn, M. E., Lewis, D. B., and Taub, D. D. Differentiation of the T helper phenotypes by analysis of the methylation state of the IFN-γ gene. J. Immunol., 153: 3603-3610, 1994.
44. Melvin, A. J., McGurn, M. E., Bort, S. J., Gibson, C., and Lewis, D. B. Hypomethylation of the interferon-γ gene correlates with its expression by primary T-lineage cells. Eur. J. Immunol., 25: 426-430, 1995.
45. Mancini, D. N., Singh, S. M., Archer, T. K., and Rodenhiser, D. I. Site-specific DNA methylation in the neurofibromatosis (NF1) promoter interferes with binding of CREB and SP1 transcription factors. Oncogene, 18: 4108-4119, 1999.
46. Ohtani-Fujita, N., Fujita, T., Aoike, A., Osifchin, N. E., Robbins, P. D., Sakai, T., and Fujita, T. CpG methylation inactivates the promoter activity of the human retinoblastoma tumor-suppressor gene. Oncogene, 8: 1063-1067, 1993.
47. Xiong, Y., Hannon, G. J., Zhang, H., Casso, D., Kobayashi, R., and Beach, D. p21 is a universal inhibitor of cyclin kinases. Nature (Lond.), 366: 701-704, 1993.
48. Chuang, L. S., Ian, H. I., Koh, T. W., Ng, H. H., Xu, G., and Li, B. F. Human DNA-(cytosine-5) methyltransferase-PCNA complex as a target for p21WAF1. Science (Washington DC), 277: 1996-2000, 1997.
49. Vidal, M. J., Loganzo, F., Jr., de Oliveira, A. R., Hayward, N. K., and Albino, A. P. Mutations and defective expression of the WAF1 p21 tumour-suppressor gene in malignant melanomas. Melanoma Res., 5: 243-250, 1995.
50. Maelandsmo, G. M., Holm, R., Fodstad, O., Kerbel, R. S., and Florenes, V. A. Cyclin kinase inhibitor p21WAF1/CIP1 in malignant melanoma: reduced expression in metastatic lesions. Am. J. Pathol., 149: 1813-1822, 1996.
51. Topley, G. I., Okuyama, R., Gonzales, J. G., Conti, C., and Dotto, G. P. p21(WAF1/Cip1) functions as a suppressor of malignant skin tumor formation and a determinant of keratinocyte stem-cell potential. Proc. Natl. Acad. Sci. USA, 96: 9089-9094, 1999.
52. Ozcelik, H., Mousses, S., and Andrulis, I. L. Low levels of expression of an inhibitor of cyclin-dependent kinases (CIP1/WAF1) in primary breast carcinomas with p53 mutations. Clin. Cancer Res., 1: 907-912, 1995.
53. Furutani, M., Arii, S., Tanaka, H., Mise, M., Niwano, M., Harada, T., Higashitsuji, H., Imamura, M., and Fujita, J. Decreased expression and rare somatic mutation of the CIP1/WAF1 gene in human hepatocellular carcinoma. Cancer Lett., 111: 191-197, 1997.
54. Nye, J. A., Petersen, J. M., Gunther, C. V., Jonsen, M. D., and Graves, B. J. Interaction of murine ets-1 with GGA-binding sites establishes the ETS domain as a new DNA-binding motif. Genes Dev., 6: 975-990, 1992.