Infection with human immunodeficiency virus type 1 upregulates DNA methyltransferase, resulting in de novo methylation of the gamma interferon (IFN-γ) promoter and subsequent downregulation of IFN-γ production

Molecular and Cellular Biology

Volumn 18, Issue 9, 1998, Pages 5166-5177

  Mikovits, Judy A ^a   Young, Howard A ^a   Vertino, Paula ^b   Issa, Jean Pierre J ^b   Pitha, Paula M ^b   Turcoski Corrales, Susan ^c   Taub, Dennis D ^d   Petrow, Cari L ^a   Baylin, Stephen B ^b   Ruscetti, Francis W ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b DEPARTMENT OF PATHOLOGY   (United States)

^c CENTER FOR BIOLOGICS EVALUATION AND RESEARCH   (United States)

^d NATIONAL INSTITUTE ON AGING   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DINUCLEOTIDE; GAMMA INTERFERON; INTERLEUKIN 12; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; DNA METHYLATION; DOWN REGULATION; ENZYME ACTIVITY; GENE EXPRESSION; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE RESPONSE; PRIORITY JOURNAL; PROMOTER REGION; RECEPTOR UPREGULATION;

HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; RNA VIRUSES; UNIDENTIFIED RETROVIRUS;

EID: 0031811880     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/mcb.18.9.5166     Document Type: Article

References (87)

1. 2 accumulation by a mechanism which differs from DNA damage checkpoint control. J. Virol. 70:2324-2331.
2. Baylin, S. B. 1992. Abnormal regional hypermethylation in cancer cells. AIDS Res. Hum. Retroviruses 8:811-820
3. Baylin, S. B., M. Makos, J. J. Wu, R. W. Yen, A. deBustros, P. Vertino, and B. D. Nelkin. 1991. Abnormal patterns of DNA methylation in human neoplasia: potential consequences for tumor progression. Cancer Cells 3:383-390.
4. Bednarik, D. P., J. A. Cook, and P. M. Pitha. 1989. Inactivation of HIV LTR by DNA CpG methylation. EMBO J. 1:1157-1164.
5. Belinsky, S. L., K. J. Nikula, S. B. Baylin, and J.-P. J. Issa. 1996. Increased cytosine DNA-methyltransferase activity is target-cell-specific and an early event in lung cancer. Proc. Natl. Acad. Sci. USA 93:4045-4050.
6. Bemeniste, O., B. Vaslin, R. Le grand, A. Cheret, F. Matheux, F. Theodoro, M. P. Cranage, and D. Dormont. 1996. Comparative interleukin (IL)-2/ Interferon (IFN)-γ and IL-4/IL-10 responds during acute infection of macaques inoculated with attenuated nef-truncated or pathogenic SIVmac251 virus. Proc. Natl. Acad. Sci. USA 93:3658-3663.
7. Bestor, T., A. Laudana, R. Mattaliano, and V. Ingram. 1988. Cloning and sequencing of a cDNA encoding DNA methyltransferase of mouse cells: the carboxyl-terminal domain of the mammalian enzymes is related to bacterial restriction methyltransferases. J. Mol. Biol. 203:971-983.
8. H1 cell development. J. Immunol. 157:1350-1358.
9. Brown, T. 1994. Analysis of DNA sequences by blotting and hybridization, p. 2.91-2.10.16. In F. A. Ausubel. R. Brent. R. E. Kingston, D. D. Moore. J. G. Seidman, J. A. Smith, and K. Struhl (ed.), Current protocols in molecular biology. Greene Publishing and Wiley Interscience. New York, N.Y.
10. Chakrabarti, L., M.-C. Cumont, L. Montagnier, and B. Hurtrel. 1994. Variable course of primary simian immunodeficiency virus infection in lymph nodes: relation to disease progression. J. Virol. 68:6634-6642.
11. Chehimi, J., S. E. Stair, I. Frank, A. D'Andrea, X. Ma, R. R. Macgregor, J. Sennelier, and G. Trinchieri. 1994. Impaired IL-12 production in human immunodeficiency virus infected patients. J. Exp. Med. 179:1361-1367.
12. Clark, S. J., J. Harrison, and M. Frommer. 1995. CpNpG methylation in mammalian cells. Nat. Genet. 10:20-26.
13. Clerici, M., F. T. Hakim, D. J. Venzon, S. Blatt, C. W. Hendrix, T. A. Wynn, and G. M. Shearer. 1993. Changes in interleukin-2 and interleukin-4 production in asymptomatic, human immunodeficiency virus-seropositive individuals. J. Clin. Invest. 91:759-765.
14. Conner, R. I., B. K. Chen, S. Choe, and N. R. Landau. 1995. Vpr is required for efficient replication of human immunodeficiency virus type-1 in mono- nuclear phagocytes. Virology 206:935-944.
15. de Bustros, A., B. D. Nelkin, A. Silverman, G. Ehrlich, B. Poiesz, and S. B. Baylin. 1988. The short arm of chromosome 11 is a "hot spot" for hypermethylation in human neoplasia. Proc. Natl. Acad. Sci. USA 85:5693-5697.
16. Derse, D. D., J. A. Mikovits, M. Polianova, B. K. Felber, and F. W. Ruscetti. 1995. Virions released from cells transfected with a molecular clone of human T-cell leukemia virus type 1 give rise to primary and secondary infections of T cells. J. Virol. 69:1907-1912.
17. El-Deiry, W. S., B. D. Nelkin, P. Celano, R. W. Yen, J. P. Falco, S. R. Hamilton, and S. B. Baylin. 1991. High expression of the DNA methyltrans- ferase gene characterizes human neoplastic cells and progression stages of colon cancer. Proc. Natl. Acad. Sci. USA 88:3470-3474.
18. Embretson, J., M. Zupancic, J. Beneke, M. Till, S. Wolinsky, J. L. Ribas, A. Burke, and A. T. Haase. 1993. Analysis of human immunodeficiency virus- infected tissues by amplification and in situ hybridization reveals latent and permissive infections at single-cell resolution. Proc. Natl. Acad. Sci. USA 90:357-361.
19. Emilie, D., M. Peuchmaur, M. C. Maillot, M. C. Crevon, N. Brousse, J. F. Delfraissy, J. Dormont, and P. Galanaud. 1990. Production of interleukins in human immunodeficiency virus-1-replicating lymph nodes. J. Clin. Invest. 86:148-159.
20. Fan, J., P. Li, T.-W. Kok, and C. J. Burrell. 1997. AZT blocks down- regulation of IL-2 and IFN-γ gene expression in HIV acutely infected cells. Arch. Virol. 142:1035-1043.
21. Farrar, W. L., F. W. Ruscetti, and H. A. Young. 1985. 5-Azacytidine treatment of a murine cytotoxic T cell line alters gamma interferon gene induction by interleukin 2. J. Immunol. 138:1551-1554.
22. Feinberg, A. P., C. W. Gehrke, K. C. Kuo, and M. Ehrlich. 1988. Reduced genomic 5-methylcytosine content in human colonic neoplasia. Cancer Res. 48:1159-1161.
23. Fitch, F., and T. Gajewski. 1991. Production of T-cell clones, p. 3.13.1-3.13.9. In J. Coligan, A. Kruisbeck, D. Marguiles, E. Shevach, and W. Stober (ed.), Current protocols in immunology. J. Wiley and Sons, New York, N.Y.
24. Fitzpatrick, D. R., D. Macaranas, K. Shirley, and A. Kelso. 1997. Clonal analysis of demethylation patterns in the interferon-gamma promoter following CD8+ T cell activation. J. Interferon Cytokine Res. 17(Suppl. 2):S82.
25. Gazzinelli, R. T., S. Bala, R. Stevens, M. Baseler, M. Kubin, G. Trinchieri, and A. Sher. 1995. HIV infection suppresses type 1 lymphokine and IL-12 responses to Toxoplasma gondii but fails to inhibit the synthesis of other parasite-induced monokines. J. Immunol. 155:1565-1571.
26. Gendelman, H., J. Orenstein, M. Martin, C. Ferrua, R. Mitra, T. Phipps, L. Wahl, H. C. Lane, and A. Fauci. 1988. Efficient isolation and propagation of human immunodeficiency virus on colony stimulating factor 1-treated monocytes. J. Exp. Med. 167:1428-1441.
27. Goelz, S. E., B. Vogelstein, S. R. Hamilton, and A. P. Feinberg. 1985. Hypomethylation of DNA from benign and malignant human colon neoplasms. Science 228:187-190.
28. Graziosi, C., K. R. Gantt, M. Vaccarezza, J. F. Demarest, M. Daucher, M. S. Saag, G. M. Shaw, T. C. Quinn, O. J. Cohen, C. C. Welbon, G. Pantaleo, and A. S. Fauci. 1996. Kinetics of Cytokine expression during primary human immunodeficiency virus type 1 infection. Proc. Natl. Acad. Sci. USA 93: 4386-4391.
29. Greger, V., E. Passarge, W. Hopping, E. Messmer, and Bκ. Horsthemki. 1989. Epigenetic changes may contribute to the formation and spontaneous re- gression of retinoblastoma. Hum. Genet, 83:155-158.
30. Groux, H., G. Torpier, D. Monte, Y. Mouton, A. Capron, and J. C. Ameisen. 1992. Activation-induced death by apoptosis in CD4+ T cells from human immunodeficiency virus-infected asymptomatic individuals. J. Exp. Med 175:331-336.
31. Gunthert, U., M. Schweiger, M. Stupp, and W. Doerfler. 1976. DNA methylation in adenovirus, adenovirus-transformed cells, and host cells. Proc. Natl. Acad. Sci. USA 73:3923-3927.
32. Hardy, K. J., B. M. Peterlin, R. E. Atchison, and J. D. Stobo. 1985. Regulation of expression of the human interferon gene. Proc. Natl. Acad. Sci USA 82:8173-8177.
33. cdc2 activity. J. Virol 69:6705-6711.
34. INK4B1. Cancer Res. 56:722-727.
35. Herman, J. G., F. Latif, Y. Weng, M. I. Lerman, B. Zbar, S. Liu, D. Sa Mid, D.-H. Duan, J. R. Gnarra, W. M. Linehan, and S. B. Baylin. 1994. Silencing of the VHL tumor-suppressor gene by DNA methylation in renal cell carcinoma. Proc. Natl. Acad. Sci. USA 91:9700-9704.
36. Herman, J. G., A. Merlo, L. Mao, R. G. Lapidus, J.-P. J. Issa, N. E. Davidson, D. Sidransky, and S. B. Baylin. 1995. Inactivation of the CDKN2/p16/ MTS1 gene is frequently associated with aberrant DNA methylation in all common human cancers. Cancer Res. 55:4525-4530.
37. Hollsberg, P., and D. A. Hatter. 1993. Pathogenesis of diseases induced by human lymphotropic virus type 1 infection. N. Engl. J. Med. 328:1173-1182.
38. Hyjek, E., H. W. Lischner, T. Hyslop, J. Bartkowiak, M. Kubin, G. Trincfcieri, and D. Kozbor. 1995. Cytokine patterns during progression to AIDS in children with perinatal HIV infection. J. Immunol. 155:4060-4067.
39. Iguchi-Ariga, S. M. M., and W. Schaffner. 1989. CpG methylation of the cAMP responsive enhancer/promoter TGACGTCA abolishes specific factor binding as well as transcriptional activation. Genes Dev. 3:612-619.
40. Issa, J. P., P. M. Vertino, J. Wu, S. Sazawal, P. Celano, B. D. Nelkin, S. R. Hamilton, and S. B. Baylin. 1993. Increased cytosine DNA-methyltransferase activity during colon cancer progression. J. Natl. Cancer Inst. 85:1235- 1240.
41. Jahner, D., and R. Jaenisch. 1985. Retrovirus-induced de novo methylation of flanking host sequences correlates with gene inactivity. Nature (London) 315:594-597.
42. Jones, P. A., and J. D. Buckley. 1990. The role of DNA methylation in cancer. Adv. Cancer Res. 54:1-23.
43. Jurriaans, S., B. Van Gemen, G. J. Weverling, D. Van Strijp, P. Nara, R. Coutinho, M. Koot, H. Schuitemaker, and J. Goudsmit. 1994. The natural history of HIV-1 infection: virus load and virus phenotype independent determinants of clinical course? Virology 204:223-233.
44. Kautiainen, T. L., and P. A. Jones. 1986. DNA methyltransferase levels in tumorigenic and nontumorigenic cells in culture. J. Biol. Chem. 261:1594- 1598.
45. Kumar, S., X. Cheng, S. Klimasauskas, S. Mi, J. Posfai, R. J. Roberts, and G. G. Wilson. 1994. The DNA (cytosine-5) methyltransferases. Nucleic Acids Res. 22:1-10.
46. Laird, P. W., and R. Jaenisch. 1994. DNA methylation and cancer. Hum Mol. Genet. 3:1487-1495.
47. Lee, P. J., L. L. Washer, D. J. Law, C. R. Boland, I. L. Horon, and A. P. Feinberg. 1996. Limited up-regulation of DNA methyltransferase in human colon cancer reflecting increased cell proliferation. Proc. Natl. Acad. Sci. USA 93:10366-10370.
48. Leonhardt, H., and T. H. Bestor. 1993. Structure, function and regulation of mammalian DNA methyltransferase, p. 109-119. In J. P. Jost and H. P. Saluz (ed.), DNA methylation: molecular biology and biological significance. Birkhauser Verlag, Basel, Switzerland.
49. Levy, J. 1993. HIV pathogenesis and long term survival. AIDS 7:1401-1410
50. Li, E., T. H. Bestor, and R. Jaenisch. 1992. Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 69:915-926.
51. Ma, X., J. M. Chow, G. Gri, G. Carra, F. Gerosa, S. F. Wolf, R. Dzialo, and G. Trinchieri. 1996. The interleukin 12 p 40 gene promoter is primed by interferon γ in monocytic cells. J. Exp. Med. 183:147-157.
52. Masucci, M. G., B. Salazzar-Contreras, E. Ragnar, K. Falk, J. Minarovits, I. Ernberg, and G. Klein. 1989. 5-Azacytidine upregulates the expression of Epstein-Barr virus nuclear antigen 2 (EBNA-2) through EBNA-6 and latent membrane protein in Burkitt's lymphoma line Real. J. Virol. 63:3135-3141.
53. Melvin, M. J., M. E. McGurn, S. J. Bort, C. Gibson, and D. B. Lewis. 1995. Hypomethylation of the interferon gamma gene correlates with its expression by primary T-lineage cells. Eur. J. Immunol. 25:426-430.
54. Merlo, A., J. G. Herman, L. Mao, D. J. Lee, E. Gabrielson, P. C. Burger, S. B. Baylin, and D. Sidransky. 1995. 5′ CpG island methylation is associated with transcriptional silencing of the tumor suppressor p16/CDKN2/MTS1 in human cancers. Nat. Med. 1:686-692.
55. Meyaard, L., E. Hovenkamp, R. P. M. Keet, B. Hooibrink, I. H. De Jong S. A. Otto, and F. Miedema. 1996. Single-cell analysis of IL-4 and IFN-γ production by T cells from HIV-infected individuals. J. Immunol. 157:2712-2718.
56. Meyaard, L., S. Otto, B. Hooibrink, and F. Miedema. 1994. Quantitative analysis of CD4+ T cell function in the course of human immunodeficiency virus infection. J. Clin. Invest. 94:1947-1952.
57. Meyaard, L., S. A. Otto, R. R. Jonker, M. J. Mijnster, R. P. M. Keet, and F. Miedema. 1992. Programmed cell death of T cells in HIV-1 infection. Science 257:217-219.
58. Mikovits, J. A., N. C. Lohrey, R. Schuloff. J. Courtless, and F. W. Ruscetti. 1992. Immune activation of HIV expression from latently infected monocytes from asymptomatic seropositive patients. J. Clin. Invest. 90:1486-1491.
59. Mikovits, J. A., Raziuddin, M. Gonda, M. Ruta, N. Lohrey, H.-F. Kung, and F. W. Ruscetti. 1990. Negative regulation of HIV replication in monocytes: distinctions between restricted and latent expression in THP-1 cells. J. Exp. Med. 171:1705-1720.
60. H2 cells: different patterns of lymphokine secretion lead to different functional properties. Annu. Rev. Immunol. 7:145-173.
61. Murray, H. W., D. A. Scavuzzo, C. D. Kelly, B. Y. Rubin, and R. B. Roberts. 1988. T4+ cell production of IFN-γ and the clinical spectrum of patients at risk for and with acquired immunodeficiency syndrome. Arch. Intern. Med. 148:1613-1620.
62. Navikas, V., J. Link, B. Wahren, C. Persson, and H. Link. 1994. Increased levels of Interferon-gamma (IFN-gamma), IL-4 and transforming growth factor-β (TGF-β) mRNA expressing blood mononuclear cells in human HIV infection. Clin. Exp. Immunoi. 96:59-65.
63. Ohtani-Fujita, N., T. Fujita, A. Aoike, N. E. Osifchin, P. D. Robbins, and T. Sakai. 1993. CpG methylation inactivates the promoter activity of the human retinoblastoma tumor-suppressor gene. Oncogene 8:1063-1067.
64. Pang, Y., Y. Norihisa, D. Benjamin, R. R. S. Kantor, and H. A. Young. 1992. Interferon-γ gene expression in human B-cell lines: induction by interleukin-2, protein kinase C activators, and possible effect of hypomethylation on gene regulation. Blood 80:724-732.
65. Penix, L., W. M. Weaver, Y. Pang, H. A. Young, and C. B. Wilson. 1993. Two essential regulatory elements in the human IFN-γ promoter confer specific expression in T-cells. J. Exp. Med. 178:1483-1496.
66. Penix, L. A., M. T. Sweetser, W. M. Weaver, J. P. Hoeffler, T. K. Kerppola, and C. B. Wilson. 1996. The regulatory element of the interferon-γ promoter mediates selective expression in T cells. J. Biol. Chem. 271:31964-31972.
67. Poli, P., and A. S. Fauci. 1995. Role of cytokines in the pathogenesis of human immunodeficiency virus infection, p. 421-450. In B. Aggarwaral and R. Puri (ed.), Human cytokines: their role in disease and therapy. Blackwell Science, Cambridge, Mass.
68. Rideout, W. M., III, G. A. Coetzee, A. F. Olumi, and P. A. Jones. 1990. 5-MethyIcytosine as an endogenous mutagen in the human LDL receptor and p53 genes. Science 249:1288-1290.
69. Saggioro, D., M. Forino, and L. Chieco-Bianchi. 1991. Transcriptional block of HTLV-1 LTR by sequence-specific methylation. Virology 182:68-75.
70. Saggioro, D., M. Panozzo, and L. Chieco-Bianchi. 1990. Human T-lymphotropic virus type I transcriptional regulation by methylation. Cancer Res. 50:4968-4973.
71. Schmutte, C., A. S. Yang, T. T. Nguyen, R. W. Beart, and P. A. Jones. 1996. Mechanisms for the involvement of DNA methylation in colon carcinogenesis. Cancer Res. 56:2375-2381.
72. Shearer, G. M., and M. Clerici. 1991. Early T-helper cell defects in HIV infection. AIDS 5:245-253.
73. Shen, J. C., W. M. Rideout, and P. A. Jones. 1992. High frequency mutagenesis by a DNA methyltransferase. Cell 71:1073-1080.
74. Vertino, P. M., J.-P. Issa, O. M. Pereira-Smith, and S. B. Baylin. 1994. Stabilization of DNA methyltransferase levels and CpG island hypermethylation precede SV40 induced immortalization of human fibroblasts. Cell Growth Differ. 5:1395-1402.
75. Vertino, P. M., R.-W. C. Yen, J. Gao, and S. B. Baylin. 1996. De novo methylation of CpG island sequences in human fibroblasts overexpressing DNA (cytosine-5-methyltransferase). Mol. Cell. Biol. 16:4555-4565.
76. Vykarnam, A., P. Matear, A. Meager, G. Kelly, B. Stanley, I. Weller, and P. Beverley. 1991. Altered production of tumor necrosis factors alpha and beta and interferon-gamma by HIV-1 infected individuals. Clin. Exp. Immunol. 84:109-115.
77. Weinberg, J. B., T. J. Matthews, B. R. Cullen, and M. H. Malim. 1991. Productive human immunodeficiency virus type 1 (HIV-1) infection of non- proliferating human monocytes. J. Exp. Med. 174:1477-1482.
78. Wu, J., J. G. Herman, G. Wilson, R. Y. Lee, R.-W. C. Yen, M. Mabry, A. de Bustros, B. D. Nelkin, and S. B. Baylin. 1996. Expression of prokaryotic Hha I DNA methyltransferase is lethal and transforming to eukaryotic cells. Cancer Res. 56:616-622.
79. Wu, J., J.-P. Issa, J. G. Herman, D. E. Bassett, Jr., B. D. Nelkin, and S. B. Baylin. 1993. Expression of an exogenous eukaryotic DNA methyltransferase gene induces transformation of NIH 3T3 cells. Proc. Natl. Acad. Sci. USA 90:8891-8895.
80. Ye, J., J. Ortaldo, K. Conlon, R. Winkler-Pickett, and H. Young. 1995. Cellular and molecular mechanisms of IFN production induced by IL-2 and IL-12. J. Leukocyte Biol. 58:225-233.
81. Yeivin, A., and A. Razin. 1993. Gene methylation patterns and expression, p. 523-568. In J. P. Host and H. P. Saluz (ed.), DNA methylation: molecular biology and biological significance. Birkhauser Verlag, Basel, Switzerland.
82. Yen, R.-W. C., P. M. Vertino, B. D. Nelkin, J. J. Yu, W. El-Deiry, A. Cumaraswamy, G. G. Lennon, B. J. Trask, P. Celano, and S. B. Baylin. 1992. Isolation and characterization of the cDNA encoding human DNA methyl- transferase. Nucleic Acids Res. 20:2287-2291.
83. Yisraeli, J., and M. Szyf. 1984. DNA methylation and gene expression, p. 353-378. In A. Razin, H. Cedar, and A. D. Riggs (ed.), DNA methylation: biochemistry and biological significance. Springer-Verlag, New York, N.Y.
84. Young, H. A., P. Ghosh, J. Ye, J. Lederer, A. Lichtman, J. Gerard, L. Penix, C. B. Wilson, A. J. Melvin, M. E. McGurn, D. B. Lewis, and D. D. Taub. 1994. Differentiation of the T helper phenotypes by analysis of the methylation state of the IFN-γ gene in immune cell regulation. J. Immunol. 153:3603- 3610.
85. Young, H. A., and P. Ghosh. 1997. Molecular regulation of cytokine gene expression: interferon-γ as a model system. Prog. Nucleic Acid Res. Mol. Biol. 56:109-127.
86. Youssoufian, H., S. M. Hammer, M. S. Hirsch, and C. Mulder. 1982. Methylation of the viral genome in an in vitro model of herpes simplex virus latency. Proc. Natl. Acad. Sci. USA 79:2207-2210.
87. Zhang, M., J. Gong, D. V. Iyer, B. E. Jones, R. L. Modlin, and P. F. Barnes. 1994. T cell cytokine responses in persons with tuberculosis and human immunodeficiency virus infection. J. Clin. Invest. 94:2435-2441.