Actinomycin D induces high-level resistance to thymidine analogs in replication of human immunodeficiency virus type 1 by interfering with host cell thymidine kinase expression

Journal of Virology

Volumn 77, Issue 2, 2003, Pages 1011-1020

  Imamichi, Tomozumi ^a   Murphy, Michael A ^a   Adelsberger, Joseph W ^a   Yang, Jun ^a   Watkins, Catherine M ^a   Berg, Steve C ^a   Baseler, Michael W ^a   Lempicki, Richard A ^a   Guo, Jianhui ^b   Levin, Judith G ^b   Lane, H Clifford ^c  

^a NATIONAL CANCER INSTITUTE   (United States)

^b EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^c NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DACTINOMYCIN; NUCLEOSIDE DERIVATIVE; PROTEINASE INHIBITOR; RNA DIRECTED DNA POLYMERASE INHIBITOR; STAVUDINE; THYMIDINE DERIVATIVE; THYMIDINE KINASE; ZIDOVUDINE;

ARTICLE; CONTROLLED STUDY; DRUG EFFECT; DRUG SENSITIVITY; HOST CELL; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; VIRUS REPLICATION;

ANTI-HIV AGENTS; BASE SEQUENCE; CELL LINE; DACTINOMYCIN; DNA PRIMERS; DRUG RESISTANCE, VIRAL; HIV-1; HUMANS; THYMIDINE; THYMIDINE KINASE; VIRUS REPLICATION;

EID: 0037229062     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.77.2.1011-1020.2003     Document Type: Article

References (63)

1. Adachi, A., H. E. Gendelman, S. Koenig, T. Folks, R. Willey, A. Rabson, and M. A. Martin. 1986. Production of acquired immunodeficiency syndrome-associated retrovirus in human and nonhuman cells transfected with an infectious molecular clone. J. Virol. 59:284-291.
2. AIDS Clinical Trials Group. 1997. Virology Manual for HIV Laboratories. Division of AIDS, National Institute of Allergy and Infectious Diseases. Bethesda, Md. [Online.] http://www.niaid.nih.gov./daids/vir_manual.
3. Beyl, W., K. Nehring, L. Gürtler, J. Eberle, and F. Deinhardt. 1987. AIDS verursacht dutch HIV-2. Münch. Med. Wochenschr. 129:895-896.
4. Boehnlein, E., M. Siekevitz, D. W. Ballard, J. W. Lowenthal, L. Rimsky, H. Bogerd, J. Hoffman, Y. Wano, B. R. Franza, and W. C. Greene. 1988. Stimulation of the HIV-1 enhancer by the HTLV-1 tax gene product involves the action of inducible cellular proteins. J. Virol. 63:1578-1586.
5. Bonin, L. R., and J. K. McDougall. 1997. Human cytomegalovirus IE2 86-kilodalton protein binds p53 but does not abrogate Gt checkpoint function. J. Virol 71:5861-5870.
6. Cassé, C., F. Giannoni, V. T. Nguyen, M.-F. Dubois, and O. Bensaude. 1999. The transcriptional inhibitors, actinomycin D and α-amanitin activate the HIV-1 promoter and favor phosphorylation of the RNA polymerase II C-terminal domain. J. Biol. Chem. 274:16097-16106.
7. Chen, F. M. 1988. Binding specificities of actinomycin D to self-complementary tetranucleotide sequences -XGCY-. Biochemistry 27:6393-6397.
8. Chen, I. S. Y., and H. M. Temin. 1982. Establishment of infection by spleen necrosis virus: Inhibition in stationary cells and the role of secondary infection. J. Virol. 41:183-191.
9. Cheng, H., J. Tarnok, and W. Parks. 1998. Human immunodeficiency virus type 1 genome activation induced by human T-cell leukemia virus type 1 Tax protein is through cooperation of NF-κB and Tat. J. Virol. 72:6911-6916.
10. Davis, W. R., S. Gabbara, D. Hupe, and J. A. Peliska. 1998. Actinomycin D inhibition of DNA strand transfer reactions catalyzed by HIV-1 reverse transcriptase and nucleocapsid protein. Biochemistry 37:14213-14221.
11. Dhib-Jalbut, S., P. M. Hoffman, T. Yamabe, D. Sun, J. Xia, H. Eisenberg, G. Berger, and F. W. Ruscetti. 1994. Extracellular human T-cell lymphotropic virus type I Tax protein induces cytokine production in adult human microglial cells. Ann. Neurol. 36:787-790.
12. Farber, S. 1966. Chemotherapy in the treatment of leukemia and Wilms' tumor. JAMA 198:826-836.
13. Fritsch, E. F., and H. M. Temin. 1977. Inhibition of viral DNA synthesis in stationary chicken embryo fibroblasts infected with avian retroviruses. J. Virol. 24:461-469.
14. Furman, P. A., J. A. Fyfe, M. H. Clair, Sr., K. Weinhold, J. L. Rideout, G. A. Freeman, S. N. Lehrman, D. P. Bolognesi, S. Broder, H. Mitsuya, and D. W. Barry. 1986. Phosphorylation of 3′-azido-3′-deoxythymidine and selective interaction of the 5′-triphosphate with human immunodeficiency virus reverse transcriptase. Proc. Natl. Acad. Sci. USA 83:8333-8337.
15. Gabbara, S., W. R. Davis, L. Hupe, D. Hupe, and J. A. Peliska. 1999. Inhibitors of DNA strand transfer reactions catalyzed by HIV-1 reverse transcriptase. Biochemistry 38:13070-13076.
16. Goodisman, J., R. Rehfuss, B. Ward, and J. C. Dabrowiak. 1992. Site-specific binding constants for actinomycin D on DNA determined from footprinting studies. Biochemistry 31:1046-1058.
17. Guo, J., T. Wu, J. Bess, L. E. Henderson, and J. G. Levin. 1998. Actinomycin D inhibits human immunodeficiency virus type 1 minus-strand transfer in in vitro and endogenous reverse transcriptase assays. J. Virol. 72:6716-6724.
18. Haertle, T., C. J. Carrera, D. B. Wasson, L. C. Sowers, D. -D. Richman, and D. A. Carson. 1988. Metabolism and anti-human immunodeficiency virus-1 activity of 2-halo-2′,3′-dideoxyadenosine derivatives. J. Biol. Chem. 263:5870-5875.
19. Harada, S., Y. Koyanagi, and N. Yamamoto. 1985. Infection of HTLV-III/LAV in HTLV-carrying cells MT-2 and MT-4 and application in a plaque assay. Science 229:563-566.
20. Harel, J., E. Rassart, and P. Jolicoeur. 1981. Cell cycle dependence of synthesis of unintegrated viral DNA in mouse cells newly infected with murine leukemia virus. Virology 110:202-207.
21. Hollsberg, P., and D. A. Hafler. 1993. Pathogenesis of diseases induced by human lymphotropic virus type I infection. N. Engl. J. Med. 328:1173-1182.
22. Hsu, T. W., and J. M. Taylor. 1982. Effect of aphidicolin on avian sarcoma virus replication. J. Virol. 44:493-498.
23. Humphries, E. H., and H. M. Temin. 1974. Requirement for cell division for initiation of transcription of Rous sarcoma virus RNA. J. Virol. 14:531-546.
24. Imamichi, T., S. C. Berg, H. Imamichi, J. C. Lopez, J. A. Metcalf, J. Fallon, and H. C. Lane. 2000. Relative replication fitness of a high-level 3′-azido-3′-deoxythimidine-resistant variant of human immunodeficiency virus type-1 possessing an amino acid deletion at codon 67 and a novel substitution (Thr to Gly) at codon 69. J. Virol. 74:10958-10964.
25. Imamichi, T., T. Sinha, H. Imamichi, Y. M. Zhang, J. A. Metcalf, J. Falloon, and H. C. Lane. 2000. High-level resistance to 3′-azido-3′-deoxythimidine due to a deletion in the reverse transcriptase gene of human immunodeficiency virus type 1. J. Virol.74:1023-1028.
26. Jeeninga, R. E., H. T. Huthoff, A. P. Gultyaev, and B. Berkhout. 1998. The mechanism of actinomycin D-mediated inhibition of HIV-1 reverse transcription. Nucleic Acids Res. 26:5472-5479.
27. Kamitori, S., and F. Takusagawa. 1992. Crystal structure of the 2:1 complex between d(GAAGCTTC) and the anticancer drug actinomycin D. J. Mol. Biol. 225:445-456.
28. Kauffman, M. G., and T. J. Kelly. 1991. Cell cycle regulation of thymidine kinase: Residues near the carboxyl terminus are essential for the specific degradation of the enzyme at mitosis. Mol. Cell. Biol. 11:2538-2546.
29. 1 arrest in MCF-7 cells. Carcinogenesis 21:1611-1618.
30. Kim, E.-Y., M. A. Winters, R. M. Kagan, and T. C. Merigan. 2001. Functional correlates of insertion mutations in the protease gene of human immunodeficiency virus type 1 isolates from patients. J. Virol. 75:11227-11233.
31. Koyanagi, Y., Y. Hinuma, J. Schneider, T. Chosa, G. Hunsmann, N. Kobayashi, M. Hatanaka, and N. Yamamoto. 1984. Expression of HTLV-specific polypeptides in various human T-cell lines. Med. Microbiol. Immunol. 173:127-140.
32. Larder, B. A., G. Darby, and D. D. Richman. 1989. HIV with reduced sensitivity to zidovudine (AZT) isolated during prolonged therapy. Science 243:1731-1734.
33. Lewis, J. L., Jr. 1972. Chemotherapy of gestational choriocarcinoma. Cancer 30:1517-1521.
34. Lindholm, P. F., S. J. Marriott, S. D. Gitlin, C. A. Bohan, and J. N. Brady. 1990. Induction of nuclear NF-κB DNA binding activity after exposure of lymphoid cells to soluble Tax1 protein. New Biol. 2:1034-1043.
35. + cell line H9. AIDS Res. Hum. Retrovir. 5:253-255.
36. Marriott, S. J., P. F. Lindholm, R. L. Reid, and J. N. Brady. 1991. Soluble HTLV-1 Tax1 protein stimulates proliferation of human peripheral blood lymphocytes. New Biol. 3:678-686.
37. Meuth, M. 1989. The molecular basis of mutations induced by deoxyribonucleoside triphosphate pool imbalances in mammalian cells. Exp. Cell. Res. 181:305-316.
38. Myers, G., B. Korber, S. Wain-Hobson, K.-T. Jeang, L. E. Henderson, and G. N. Pavlakis. 1994. Human Retroviruses and AIDS. Los Alamos National Laboratory, Los Alamos, N.Mex.
39. Nguyen, V. T., T. Kiss, A. A. Michels, and O. Bensaude. 2001. 7SK small nuclear RNA binds to and inhibits the activity of CDK9/cyclin T complexes. Nature 414:322-325.
40. Oliver, F. J., M. K. Collins, and A. Lopez-Rivas. 1997. Overexpression of a heterologous thymidine kinase delays apoptosis induced by factor deprivation and inhibitors of deoxynucleotide metabolism. J. Biol. Chem. 272:10624-10630.
41. Pauwels, R., E. De Clercq, J. Desmyter, J. Balzarini, P. Goubau, P. Herdewijn, H. Vanderhaeghe, and M. Vandeputte. 1987. Sensitive and rapid assay on MT-4 cells for detection of antiviral compounds against the AIDS virus. J. Virol. Methods 16:171-185.
42. Perrin, L., and A. Telenti. 1998. HIV treatment failure: Testing for HIV resistance in clinical practice. Science 280:1871-1873.
43. Perry, R. P., and D. E. Kelley. 1970. Inhibition of RNA synthesis by actinomycin D: Characteristic dose-response of different RNA species. J. Cell. Physiol. 76:127-139.
44. Popovic, M., E. Read-Connole, and R. C. Gallo. 1984. T4 positive human neoplastic cell lines susceptible to and permissive for HTLV-III. Lancet II:1472-1473.
45. Popovic, M., M. G. Sarngadharan, E. Read, and R. C. Gallo. 1984. Detection, isolation, and continuous production of cytopathic retroviruses (HTLV-III) from patients with AIDS and pre-AIDS. Science 224:497-500.
46. Rabson, A. B., and B. J. Graves. 1997. Synthesis and processing of viral RNA, p. 205-261. In J. M. Coffin, S. H. Hughes, and H. E. Varmus (ed.), Retroviruses. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
47. Rill, R. L., and K. H. Hecker. 1996. Sequence-specific actinomycin D binding to single-stranded DNA inhibits HIV reverse transcriptase and other polymerases. Biochemistry 35:3525-3533.
48. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular Cloning: A Laboratory Manual, 2nd Ed., p. 18.38. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
49. Schinazi, R. F., B. A. Larder, and J. W. Mellors. 2000. Mutations in retroviral genes associated with drug resistance. Int. Antivir. News 8:65-91.
50. Sherley, J. L., and J. K. Thomas. 1988. Regulation of human thymidine kinase during the cell cycle. J. Biol. Chem. 263:8350-8358.
51. Shibata, R., M. D. Hoggan, C. Broscius, G. Englund, T. S. Theodore, A. Buckler-White, L. O. Arthur, Z. Israel, A. Schultz, H. C. Lane, and M. A. Martin. 1995. Isolation and characterization of a synctium-inducing, macrophage/T-cell line-tropic human immunodeficiency virus type 1 isolate that readily infects chimpanzee cells in vitro and in vivo. J. Virol. 69:4453-4462.
52. Sobell, H. M. 1985. Actinomycin and DNA transcription. Proc. Natl. Acad. Sci. USA 82:5328-5331.
53. Stewart, C. J., M. Ito, and S. E. Conrad. 1987. Evidence for transcriptional and post-transcriptional control of the cellular thymidine kinase gene. Mol. Cell. Biol. 7:1156-1163.
54. Takusagawa, F., K. T. Takusagawa, R. G. Carlson, and R. F. Weaver. 1997. Selectivity of F8-actinomycin D for RNA:DNA hybrids and its anti-leukemia activity. Bioorg. Med. Chem. 5:1197-1207.
55. Telesnitsky, A., and S. P. Goff. 1997. Reverse transcriptase and the generation of retroviral DNA, p. 121-160. In J. M. Coffin, S. H. Hughes, and H. E. Varmus (ed.), Retroviruses. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
56. Varmus, H. E., T. Padgett, S. Heasley, G. Simon, and J. M. Bishop. 1977. Cellular functions are required for synthesis and integration of avian sarcoma virus-specific DNA. Cell 11:307-319.
57. Wadkins, R. M., and T. M. Jovin. 1991. Actinomycin D and 7-aminoactinomycin D binding to single-stranded DNA. Biochemistry. 30:9469-9478.
58. Wadkins, R. M., E. A. Jares-Erijman, R. Klement, A. Rudiger, and T. M. Jovin. 1996. Actinomycin D binding to single-stranded DNA: Sequence specificity and hemi-intercalation model from fluorescence and 1H NMR spectroscopy. J. Mol. Biol. 262:53-68.
59. Waring, M. J. 1981. DNA modification and cancer. Annu. Rev. Biochem. 50:159-192.
60. Winters, M. A., J. M. Schapiro, J. Lawrence, and T. C. Merigan. 1998. Human immunodeficiency virus type 1 protease genotypes and in vitro protease inhibitor susceptibilities of isolates from individuals who were switched to other protease inhibitors after long-term saquinavir treatment. J. Virol. 72:5303-5306.
61. Yang, Z., Q. Zhu, K. Luo, and Q. Zhou. 2001. The 7SK small nuclear RNA inhibits the CDK9/cyclin T1 kinase to control transcription. Nature 414:317-322.
62. Zack, J. A., A. J. Cann, J. P. Lugo, and I. S. Y. Chen. 1988. HIV-1 production from infected peripheral blood T cells after HTLV-I induced mitogenic stimulation. Science 240:1026-1029.
63. Zhang, Y.-M., H. Imamichi, T. Imamichi, H. C. Lane, J. Falloon, M. B. Vasudevachari, and N. P. Salzman. 1997. Drug resistance during indinavir therapy is caused by mutations in the protease gene and in its Gag substrate cleavage sites. J. Virol. 71:6662-6670.