Oncogenic potential of TAR RNA binding protein TRBP and its regulatory interaction with RNA-dependent protein kinase PKR

EMBO Journal

Volumn 16, Issue 3, 1997, Pages 611-624

  Benkirane, Monsef ^a   Neuveut, Christine ^a   Chun, Rene F ^a   Smith, Stephen M ^a   Samuel, Charles E ^b   Gatignol, Anne ^c   Jeang, Kuan Teh ^a  

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

^b UNIVERSITY OF CALIFORNIA   (United States)

^c INSTITUT COCHIN   (France)

Author keywords

Interferon; Regulation; RNA binding protein; Transformation; Translation

Indexed keywords

PROTEIN SERINE THREONINE KINASE; RNA BINDING PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIVIRAL ACTIVITY; ARTICLE; AUTOPHOSPHORYLATION; CELL PROLIFERATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; MITOSIS INHIBITION; MOLECULAR INTERACTION; MOUSE; NONHUMAN; ONCOGENE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN SYNTHESIS; VIRUS CELL TRANSFORMATION;

3T3 CELLS; ANIMALS; BLOTTING, WESTERN; CELL DIVISION; EIF-2 KINASE; GENE EXPRESSION REGULATION, VIRAL; HELA CELLS; HIV-1; HUMANS; INTERFERON-ALPHA; MICE; MICE, NUDE; NEOPLASMS, EXPERIMENTAL; PHOSPHORYLATION; PRECIPITIN TESTS; PROTEIN-SERINE-THREONINE KINASES; RNA, DOUBLE-STRANDED; RNA-BINDING PROTEINS; TRANSFORMATION, GENETIC;

ANIMALIA; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 0031014063     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/16.3.611     Document Type: Article

References (75)

1. Adachi, A., Gendelman, S., Folks, T., Willey, R., Rabson, A. and Martin, M.A. (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. Agy, M.B., Acker, L.R., Sherbert, C.H. and Katze, M.G. (1995) Interferon treatment inhibits virus replication in HIV-1- and SIV-infected CD4+ T-cell lines by distinct mechanisms: evidence for decreased stability and aberrant processing of HIV-1 proteins. Virology, 214, 379-386.
3. Barber, G.N., Thompson, S., Lee, T.G., Strom, T., Jagus, R., Darveau, A. and Katze, M.G. (1994) The 58-kilodalton inhibitor of the interferon-induced double-stranded RNA-activated protein kinase is a tetratricopeptide repeat protein with oncogenic properties. Proc. Natl Acad. Sci. USA, 91, 4278-4282.
4. Barber, G.N., Wambach, M., Thompson, S., Jagus, R. and Katze, M.G. (1995) Mutant of the RNA-dependent protein kinase (PKR) lacking dsRNA binding domain I can act as transdominant inhibitor and induce malignant transformation. Mol. Cell. Biol., 15, 3138-3146.
5. Black, T.L., Safer, B., Hovanessian, A. and Katze, M.G. (1989) The cellular 68,000 kD protein kinase is highly autophosphorylated and activated yet significantly degraded during poliovirus infection: implications for translational regulation. J. Virol., 63, 2244-2251.
6. Blair, E.D., Roberts, C.M., Snowden, B.W., Gatignol, A., Benkirane, M. and Jeang, K.-T. (1995) Expression of TAR RNA-binding protein in baculovirus and co-immunoprecipitation with insect cell protein kinase. J. Biomed. Sci., 2, 322-329.
7. Chen, J.J., Throop, M.S., Gehrke, L., Kuo, I., Pal, J.K., Brodsky, M. and London, I.M. (1991) Cloning of the cDNA of the heme-regulated eukaryotic initiation factor 2α (eIF-2α) kinase of rabbit reticulocytes: homology to yeast GCN2 protein kinase and human double-stranded RNA-dependent eIF-2α kinase. Proc. Natl Acad. Sci. USA, 88, 7729-7733.
8. Chong, K.L., Feng, L., Schappert, K., Meurs, E., Donahue, T.F., Friesen, J.D., Hovanessian, A.G. and Williams, B.R. (1992) Human p68 kinase exhibits growth suppression in yeast and homology to the translational regulator GCN2. EMBO J., 11, 1553-1562.
9. Clemens, M.J. (1996) Protein kinases that phosphorylate eIF-2α and eIF-2β, and their role in eukaryotic cell translational control. In Clemens, M.J. (ed.), Translational Control. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp. 139-172.
10. Coccia, E.M., Kryst, B. and Hovannessian, A.G. (1994) Specific inhibition of viral protein synthesis in HIV-infected cells in response to interferon treatment. J. Biol. Chem., 269, 23087-23094.
11. Cosentino, G.P., Venkatesan, S., Serluca, F.C., Green, S.R., Mathews, M.B. and Sonenberg, N. (1995) Double-stranded-RNA-dependent protein kinase and TAR RNA-binding protein form homo- and heterodimers in vivo. Proc. Natl Acad. Sci. USA, 92, 9445-9449.
12. Davies, M.V., Elroy-Stein, O., Jagus, R., Moss, B. and Kaufman, R.J. (1992) The vaccinia virus K3L gene product potentiates translation by inhibiting double-stranded-RNA-activated protein kinase and phosphorylation of the alpha subunit of eukaryotic initiation factor 2. J. Virol., 66, 1943-1950.
13. Der, S.D. and Lau, A.S. (1995) Involvement of the double-stranded-RNA-dependent kinase PKR in interferon expression and interferon-mediated antiviral activity. Proc. Natl Acad. Sci. USA, 92, 8841-8845.
14. Dever, T.E., Chen, J.J., Barber, J.N., Cigan, A.M., Feng, L., Donahue, T.F., London, I.M., Katze, M.G. and Hinnebusch, A.G. (1993) Mammalian eukaryotic initiation 2a kinase functionally substitute for GCN 2 protein kinase in the GCN 4 translational control mechanism of yeast. Proc. Natl Acad. Sci. USA, 90, 4616-4620.
15. Donze, O., Jagus, R., Koromilas, A.E., Hershey, J.W.B. and Sonenberg, N. (1995) Abrogation of translation initiation factor elF-2 phosphorylation causes malignant transformation of NIH3T3 cells. EMBO J., 14, 3828-3834.
16. Dubois, M.F. and Hovanessian, A.G. (1990) Modified subcellular localization of interferon-induced p68 kinase during encephalo-myocarditis virus infection. Virology, 179, 591-598.
17. Edery, I., Petryshyn, R. and Sonenberg, N. (1989) Activation of double-stranded RNA-dependent kinase (dsI) by the TAR region of HIV-1 mRNA: a novel translational control mechanism. Cell, 56, 303-312.
18. Edlin, B.R., Marty, H., Pitha, P.M., Whaling, S.M., King, D.M., Bitran, J.D. and Weinstein, R.A. (1992) In-vitro resistence to zidovudine and alpha-interferon in HIV-1 isolates from patients: correlations with treatment duration and response. Ann. Internal Med., 117, 457-460.
19. Francis, M.L., Meltzer, M.S. and Gendelman, H.E. (1992) Interferons in the persistence, pathogenesis and treatment of HIV-1 infection. AIDS Res. Hum. Retrovirus, 8, 199-207.
20. Gatignol, A., Kumar, A., Rabson, A. and Jeang, K.-T. (1989) Identification of cellular proteins that bind to the human immunodeficiency virus type 1 trans-activation-responsive TAR element RNA. Proc. Natl Acad. Sci. USA, 86, 7828-7832.
21. Gatignol, A., Buckler-White, A., Berkhout, B. and Jeang, K.-T. (1991) Characterization of human TAR RNA-binding protein that activates the HIV-1LTR. Science, 251, 1597-1600.
22. Gatignol, A., Buckler, C. and Jeang, K.-T. (1993) Relatedness of an RNA-binding motif in human immunodeficiency virus type 1 TAR RNA-binding protein TRBP to human P1/dsI kinase and Drosophila Staufen. Mol. Cell. Biol., 13, 2193-2202.
23. Hershey, J.W.B. (1991) Translational control in mammalian cells. Annu. Rev. Biochem., 60, 717-755.
24. Hovanessian, A.G. (1989) The double stranded RNA-activated protein kinase induced by interferon: dsRNA-PK. J. Interferon Res., 9, 641-647.
25. Hovanessian, A.G., Galabru, J., Meurs, E., Buffet-Janvresse, C., Svab, J. and Robert, N. (1987) Rapid decrease in levels of the double-stranded RNA-dependent protein kinase during virus infections. Virology, 159, 126-136.
26. Huang, L., Joshi, A., Willey, R., Ornstein, J. and Jeang, K.-T. (1994) Human immunodeficiency viruses regulated by alternative trans-activators: genetic evidence for a novel non-transcriptional function of Tat in virion infectivity. EMBO J., 13, 2886-2896.
27. Hunter, T. (1995) Protein kinases and phosphatases: the Yin and Yang of protein phosphorylation and signaling. Cell, 80, 225-236.
28. Imani, F. and Jacobs, B.L. (1988) Inhibitory activity for the imerferon-induced protein kinase is associated with the reovirus serotype 1 sigma 3 protein. Proc. Natl Acad. Sci. USA, 85, 7887-7891.
29. Jeang, K.-T., Chun, R., Lin, N.H., Gatignol, A., Glabe, C.G. and Fan, H. (1993) In vivo and in vitro binding of human immunodeficiency virus type 1 Tat protein and Sp1 transcription factor. J. Virol., 67, 6224-6233.
30. Joshi, A. and Jeang, K.-T. (1993) Reduction in growth temperature minimizes instability of large plasmids containing HIV-1 proviral genomes. BioTechniques, 14, 880-886.
31. Judware, R. and Petryshyn, R. (1991) Mechanism of action of cellular inhibitor of the dsRNA-dependent protein kinase from 3T3-F442A cells. J. Biol. Chem., 267, 21685-21690.
32. Katze, M.G. (1992) The war against the interferon-induced dsRNA-activated protein kinase. J. Interferon Res., 12, 241-248.
33. Kaufman, R.J. (1994) Control of gene expression at the level of translation initiation. Curr. Opin. Biotechnol., 5, 550-557.
34. Kitajewski, J., Schneider, R.J., Safer, B., Munemitsu, S.M., Samuel, C.E., Thimmappaya, B. and Shenk, T. (1986) Adenovirus VAI RNA antagonizes the antiviral action of Interferon by preventing activation of the interferon-induced elf-2 alpha kinase. Cell, 45, 195-200.
35. Koromilas, A.E., Roy, S., Barber, G.N., Katze, M.G. and Sonenberg, N. (1992) Malignant transformation by a mutant of the IFN-induced dsRNA-dependent protein kinase. Science, 257, 1685-1689.
36. Kozak, C.A., Gatignol, A., Graham, K., Jeang, K.-T. and McBride, O.W. (1995) Genetic mapping in human and mouse of the locus encoding TRBP, a protein that binds the TAR region of the human immunodeficiency virus (HIV-1). Genomics, 25, 66-72.
37. Kumar, A., Haque, J., Lacoste, J., Hiscott, J. and Williams, B.R.G. (1994) Double-stranded RNA-dependent protein kinase activates transcription factor NF-κB by phosphorylating IκB. Proc. Natl Acad. Sci. USA, 91, 6288-6292.
38. Lee, S.B. and Esteban, M. (1994) The interferon-induced double stranded RNA-activated protein kinase induces appoptosis. Virology, 199, 491-496.
39. Lee, S.B., Melkova, Z., Yan, W., William, B.R., Hovanessian, A.G. and Esteban, M. (1993) The interferon-induced double-stranded RNA-activated human p68 protein kinase potently inhibits protein synthesis in cultured cells. Virology, 192, 380-385.
40. Lee, T.G. and Katz, M.G. (1994) Cellular inhibitors of the interferon-induced, dsRNA-activated protein kinase. Prog. Mol. Subcell. Biol., 14, 48-65.
41. r 68,000 from influenza virus-infected cells. Proc. Natl Acad. Sci. USA, 87, 6208-6212.
42. Lee, T.G., Tomita, J., Hovanessian, A.G. and Katze, M.G. (1992) Characterization and regulation of the 58,000-Dalton cellular inhibitor of the interferon-induced, dsRNA-activated protein kinase. J. Biol. Chem., 267, 14238-14243.
43. Lee, T.G., Tong, N., Thompson, S., Miller, J. and Katze, M.G. (1994) The 58,000-Dalton cellular inhibitor of the interferon-induced double-stranded RNA-activated protein kinase (PKR) is a member of the tetratricopeptide repeat family of proteins. Mol. Cell. Biol., 14, 2331-2342.
44. Lengyel, P. (1993) Tumor suppressor genes: news about the interferon connection. Proc. Natl Acad. Sci. USA, 90, 5893-5895.
45. Maitra, R.K., McMilan, N.A.J., Desai, S., McSwiggen, J., Hovanessian, A.G., Sen, G., William, B.R.G. and Silverman, R.H. (1994) HIV-1 TAR RNA has an intrinsic ability to activate interferon-inducible enzymes. Virology, 204, 823-827.
46. 1 and TAR RNAs. Virology, 206, 511-519.
47. McCormack, S.J., Thomis, D.C. and Samuel, C.E. (1992) Mechanism of interferon action: identification of RNA binding domains within the N-terminal region of the human RNA-depdendent P1-eIF-2α protein kinase. Virology, 188, 47-56.
48. McCormack, S.J., Ortega, L.G., Doohan, J.P. and Samuel, C.E. (1994) Mechanism of interferon action: motif I of the interferon-induced. RNA-dependent protein kinase (PKR) is sufficient to mediate RNA-binding activity. Virology, 198, 92-99.
49. McMillan, N.A.J. et al. (1995a) HIV-1 Tat RNA directly interacts with the interferon-induced, double-stranded RNA-dependent kinase, PKR. Virology, 213, 413-424.
50. McMillan, N.A.J., Carpick, B.W., Hollis, B., Toone, M.W., Zamanian-Daryoush, M. and Williams, B.R.G. (1995b) Mutational analysis of the double-stranded RNA (dsRNA) binding domain of the dsRNA-activated protein kinase. PKR. J. Biol. Chem., 270, 2601-2606.
51. Meurs, E., Chong, K., Galabru, J., Thomas, N.S.B., Kerr, I.M., William, B.R.G. and Hovanessian, A.G. (1990) Molecular cloning and characterization of the human double-stranded RNA-activated protein kinase induced by interferon. Cell, 62, 379-390.
52. Meurs, E., Watanabe, Y., Kadereit, S., Barber, G.N., Katze, M.G., Chong, K., Williams, B.R.G. and Hovanessian, A.G. (1992) Constitutive expression of human double-stranded RNA-activated p68 kinase in murine cells mediates phosphorylation of eukaryotic initiation factor 2 and partial resistance to encephalomyocarditis virus grouth. J. Virol., 66, 5805-5814.
53. Meurs, E., Galabru, J., Barber, G.N., Katze, M.G. and Hovanessian, A.G. (1993) Tumor suppressor function of the interferon-induced double-stranded RNA-activated protein kinase. Proc. Natl Acad. Sci. USA, 90, 232-236.
54. Mundschau, L.J. and Faller, D.V. (1992) Oncogenic ras induces an inhibitor of double-stranded RNA-dependent eukaryotic initiation factor 2a-kinase activation. J. Biol. Chem., 267, 23092-23098.
55. O'Malley, R.P., Mariano, T.M., Siekierka, J. and Mathews, M.B. (1986) A mechanism for the control of protein synthesis by adenovirus VA RNAI. Cell, 44, 391-400.
56. Ortega, L.G., Mccotter, M.D., Henry, G.L., Mccormack, S.J., Thomis, D.C. and Samuel, C.E. (1996) Biochemical and genetic evidence for the intermolecular association of the RNA-dependent protein kinase PKR from human cells. Virology, 215, 31-39.
57. Park, H. et al. (1994) TAR RNA-binding protein is an inhibitor of the interferon-induced protein kinase PKR. Proc. Natl Acad. Sci. USA, 91, 4713-4717.
58. Patel, R.C., Statnton, P., McMillan, N.M.J., Williams, B.R.G. and Sen, G.C. (1995) The interferon-induced double-stranded RNA-activated protein kinase self-associates in vitro and in vivo. Proc. Natl Acad. Sci. USA, 92, 8283-8287.
59. Petryshyn, R., Chen, J.J. and London, I.M. (1984) Growth-related expression of a double-stranded RNA-dependent protein kinase in NIH 3T3 cells. J. Biol. Chem., 259, 14736-14742.
60. Petryshyn, R., Chen, J.J. and London, I.M. (1988) Detection of activated double-stranded RNA-dependent protein kinase in 3T3-F442A cells. Proc. Natl Acad. Sci. USA, 85, 1427-1431.
61. Pitha, P.M. (1994) Multiple effects of interferon on the replication of human immunodeficiency virus type 1. Antiviral Res., 24, 205-219.
62. Ramaiah, K., Davies, M.V., Chen, J.J. and Kaufman, R.J. (1994) Expression of mutant eukaryotic initiation factor 2α subunit (eIF-2α) reduce inhibition of guanine nucleotide exchange activity of eIF-2β mediated by eIF-2α phosphorylation. Mol. Cell. Biol., 14, 4546-4553.
63. Rowlands, A.G., Panniers, R. and Henshaw, E.C. (1988) The catalytic mechanism of guanine nucleotide exchange factor action and competitive inhibition by phosphorylated eukaryotic initiation factor 2. J. Biol. Chem., 263, 5526-5533.
64. r protein kinase. J. Virol., 65, 632-640.
65. Samuel, C.E. (1991) Antiviral actions of interferon: interferon-regulated cellular proteins and their surprisingly selective antiviral activities. Virology, 183, 1-11.
66. Samuel, C.E. (1993) The eIF-2α protein kinase, regulators of translation in eukaryotes from yeasts to humans. J. Biol. Chem., 268, 7603-7606.
67. SenGupta, D.N. and Silverman, R.H. (1989) Activation of interferon regulated dsRNA dependent enzymes by human immunodeficiency virus 1 leader RNA. Nucleic Acids Res., 17, 969-978.
68. Sonenberg, N. (1990) Measures and countermeasures in the modulation of initiation factor activities by viruses. New Biologist, 2, 402-409.
69. Sonenberg, N. (1993) Translation factors as effectors of cell growth and tumorigenesis. Curr. Opin. Cell Biol., 5, 955-960.
70. Tanaka, H. and Samuel, C.E. (1994) Mechanism of interferon action. Structure of the mouse PKR gene encoding the interferon-inducible RNA-dependent protein kinase. Proc. Natl Acad. Sci. USA, 91, 7995-7999.
71. Thomis, D.C. and Samuel, C.E. (1992a) Mechanism of interferon action. cDNA structure, expression and regulation of the interferon-induced, RNA-dependent P1/eIF-2α protein kinase from human cells. Virology, 188, 33-46.
72. Thomis, D.C. and Samuel, C. (1992b) Mechanism of interferon action: autoregulation of RNA-dependent P1/eIF-2α protein kinase (PKR) expression in transfection of mammalian cells. Proc. Natl Acad. Sci. USA, 89, 10837-10841.
73. Whitaker-Dowling, P.A. and Yoongner, J.S. (1984) Characterization of a specific kinase inhibitory factor produced by vaccinia virus which inhibits the interferon-induced protein kinase. Virology, 137, 171-181.
74. Williams, B.R.G. (1991) Transcriptional regulation of interferon-stimulated genes. Eur. J. Biochem., 200, 1-11.
75. Yang, Y.-L., Reis, L.F.L., Pavlovic, J., Aguzzi, A., Schafer, R., Kumar, A., Williams, B.R.G., Aguet, M. and Weissmann, C. (1995) Deficient signaling in mice devoid of double-stranded RNA-dependent protein kinase. EMBO J., 14, 6095-6106.