The Cellular TAR RNA binding protein, TRBP, promotes HIV-1 replication primarily by inhibiting the activation of double-stranded RNA-dependent kinase PKR

Journal of Virology

Volumn 85, Issue 23, 2011, Pages 12614-12621

  Sanghvi, Viraj R ^a   Steel, Laura F ^a  

^a DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; MICRORNA; PROTEIN KINASE R; TAR DNA BINDING PROTEIN;

ARTICLE; CD4+ T LYMPHOCYTE; CELL CULTURE; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVATION; ENZYME INHIBITION; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; T LYMPHOCYTE; VIRUS IMMUNITY; VIRUS REPLICATION;

BLOTTING, WESTERN; CD4-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; DEAD-BOX RNA HELICASES; EIF-2 KINASE; HELA CELLS; HIV INFECTIONS; HIV-1; HUMANS; JURKAT CELLS; MICRORNAS; PHOSPHORYLATION; PROTEIN BINDING; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RIBONUCLEASE III; RNA, DOUBLE-STRANDED; RNA, MESSENGER; RNA-BINDING PROTEINS; VIRUS REPLICATION;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 81255164734     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.05240-11     Document Type: Article

References (54)

1. Bannwarth, S., et al. 2001. Organization of the human tarbp2 gene reveals two promoters that are repressed in an astrocytic cell line. J. Biol. Chem. 276:48803-48813.
2. Benkirane, M., et al. 1997. Oncogenic potential of TAR RNA binding protein TRBP and its regulatory interaction with RNA-dependent protein kinase PKR. EMBO J. 16:611-624.
3. Bennasser, Y., M. L. Yeung, and K. T. Jeang. 2006. HIV-1 TAR RNA subverts RNA interference in transfected cells through sequestration of TAR RNA-binding protein, TRBP. J. Biol. Chem. 281:27674-27678.
4. Boo, K. H., and J. S. Yang. 2010. Intrinsic cellular defenses against virus infection by antiviral type I interferon. Yonsei Med. J. 51:9-17.
5. Brand, S. R., R. Kobayashi, and M. B. Mathews. 1997. The Tat protein of human immunodeficiency virus type 1 is a substrate and inhibitor of the interferon-induced, virally activated protein kinase, PKR. J. Biol. Chem. 272:8388-8395.
6. Carpick, B. W., et al. 1997. Characterization of the solution complex between the interferon-induced, double-stranded RNA-activated protein kinase and HIV-I trans-activating region RNA. J. Biol. Chem. 272:9510-9516.
7. Chable-Bessia, C., et al. 2009. Suppression of HIV-1 replication by microRNA effectors. Retrovirology 6:26.
8. Chendrimada, T. P., et al. 2005. TRBP recruits the Dicer complex to Ago2 for microRNA processing and gene silencing. Nature 436:740-744.
9. Christensen, H. S., et al. 2007. Small interfering RNAs against the TAR RNA binding protein, TRBP, a Dicer cofactor, inhibit human immunodeficiency virus type 1 long terminal repeat expression and viral production. J. Virol. 81:5121-5131.
10. Clerzius, G., et al. 2009. ADAR1 interacts with PKR during human immunodeficiency virus infection of lymphocytes and contributes to viral replication. J. Virol. 83:10119-10128.
11. Clerzius, G., J. F. Gelinas, and A. Gatignol. 2011. Multiple levels of PKR inhibition during HIV-1 replication. Rev. Med. Virol. 21:42-53.
12. Daher, A., et al. 2009. TRBP control of PACT-induced phosphorylation of protein kinase R is reversed by stress. Mol. Cell. Biol. 29:254-265.
13. Daher, A., et al. 2001. Two dimerization domains in the trans-activation response RNA-binding protein (TRBP) individually reverse the protein kinase R inhibition of HIV-1 long terminal repeat expression. J. Biol. Chem. 276:33899-33905.
14. Dimitrova, D. I., et al. 2005. Lentivirus-mediated transduction of PKR into CD34(+) hematopoietic stem cells inhibits HIV-1 replication in differentiated T cell progeny. J. Interferon Cytokine Res. 25:345-360.
15. Ding, S. W. 2010. RNA-based antiviral immunity. Nat. Rev. Immunol. 10: 632-644.
16. Dorin, D., et al. 2003. The TAR RNA-binding protein, TRBP, stimulates the expression of TAR-containing RNAs in vitro and in vivo independently of its ability to inhibit the dsRNA-dependent kinase PKR. J. Biol. Chem. 278: 4440-4448.
17. Eekels, J. J., D. Geerts, R. E. Jeeninga, and B. Berkhout. 2010. Long-term inhibition of HIV-1 replication with RNA interference against cellular cofactors. Antiviral Res. 89:43-53.
18. Endo-Munoz, L., T. Warby, D. Harrich, and N. A. McMillan. 2005. Phosphorylation of HIV Tat by PKR increases interaction with TAR RNA and enhances transcription. Virol. J. 2:17.
19. Folks, T. M., et al. 1989. Tumor necrosis factor alpha induces expression of human immunodeficiency virus in a chronically infected T-cell clone. Proc. Natl. Acad. Sci. U. S. A. 86:2365-2368.
20. Garcia, M. A., E. F. Meurs, and M. Esteban. 2007. The dsRNA protein kinase PKR: virus and cell control. Biochimie 89:799-811.
21. Gatignol, A., A. Buckler-White, B. Berkhout, and K. T. Jeang. 1991. Characterization of a human TAR RNA-binding protein that activates the HIV-1 LTR. Science 251:1597-1600.
22. Gatignol, A., S. Laine, and G. Clerzius. 2005. Dual role of TRBP in HIV replication and RNA interference: viral diversion of a cellular pathway or evasion from antiviral immunity? Retrovirology 2:65.
23. Geballe, A. P., and M. K. Gray. 1992. Variable inhibition of cell-free translation by HIV-1 transcript leader sequences. Nucleic Acids Res. 20:4291-4297.
24. Gelinas, J. F., G. Clerzius, E. Shaw, and A. Gatignol. 2011. Enhancement of replication of RNA viruses by ADAR1 via RNA editing and inhibition of RNA-activated protein kinase. J. Virol. 85:8460-8466.
25. George, C. X., et al. 2009. Tipping the balance: antagonism of PKR kinase and ADAR1 deaminase functions by virus gene products. J. Interferon Cytokine Res. 29:477-487.
26. Goujon, C., and M. H. Malim. 2010. Characterization of the alpha interferon-induced postentry block to HIV-1 infection in primary human macrophages and T cells. J. Virol. 84:9254-9266.
27. Gunnery, S., A. P. Rice, H. D. Robertson, and M. B. Mathews. 1990. Tatresponsive region RNA of human immunodeficiency virus 1 can prevent activation of the double-stranded-RNA-activated protein kinase. Proc. Natl. Acad. Sci. U. S. A. 87:8687-8691.
28. Haase, A. D., et al. 2005. TRBP, a regulator of cellular PKR and HIV-1 virus expression, interacts with Dicer and functions in RNA silencing. EMBO Rep. 6:961-967.
29. Heinicke, L. A., et al. 2009. RNA dimerization promotes PKR dimerization and activation. J. Mol. Biol. 390:319-338.
30. Huang, J., et al. 2007. Cellular microRNAs contribute to HIV-1 latency in resting primary CD4+ T lymphocytes. Nat. Med. 13:1241-1247.
31. Kim, I., C. W. Liu, and J. D. Puglisi. 2006. Specific recognition of HIV TAR RNA by the dsRNA binding domains (dsRBD1-dsRBD2) of PKR. J. Mol. Biol. 358:430-442.
32. Kimpton, J., and M. Emerman. 1992. Detection of replication-competent and pseudotyped human immunodeficiency virus with a sensitive cell line on the basis of activation of an integrated beta-galactosidase gene. J. Virol. 66:2232-2239.
33. Koromilas, A. E., S. Roy, G. N. Barber, M. G. Katze, and N. Sonenberg. 1992. Malignant transformation by a mutant of the IFN-inducible dsRNA-dependent protein kinase. Science 257:1685-1689.
34. Langland, J. O., J. M. Cameron, M. C. Heck, J. K. Jancovich, and B. L. Jacobs. 2006. Inhibition of PKR by RNA and DNA viruses. Virus Res. 119:100-110.
35. Lee, J. Y., et al. 2004. Merlin, a tumor suppressor, interacts with transactivation-responsive RNA-binding protein and inhibits its oncogenic activity. J. Biol. Chem. 279:30265-30273.
36. Li, S., and A. E. Koromilas. 2001. Dominant negative function by an alternatively spliced form of the interferon-inducible protein kinase PKR. J. Biol. Chem. 276:13881-13890.
37. Li, S., K. Nagai, and A. E. Koromilas. 2000. A diminished activation capacity of the interferon-inducible protein kinase PKR in human T lymphocytes. Eur. J. Biochem. 267:1598-1606.
38. Lin, J., and B. R. Cullen. 2007. Analysis of the interaction of primate retroviruses with the human RNA interference machinery. J. Virol. 81: 12218-12226.
39. Maitra, R. K., et al. 1994. HIV-1 TAR RNA has an intrinsic ability to activate interferon-inducible enzymes. Virology 204:823-827.
40. McMillan, N. A., et al. 1995. HIV-1 Tat directly interacts with the interferoninduced, double-stranded RNA-dependent kinase, PKR. Virology 213:413-424.
41. Nathans, R., et al. 2009. Cellular microRNA and P bodies modulate host-HIV-1 interactions. Mol. Cell 34:696-709.
42. Ong, C. L., et al. 2005. Low TRBP levels support an innate human immunodeficiency virus type 1 resistance in astrocytes by enhancing the PKR antiviral response. J. Virol. 79:12763-12772.
43. Park, H., et al. 1994. TAR RNA-binding protein is an inhibitor of the interferon-induced protein kinase PKR. Proc. Natl. Acad. Sci. U. S. A. 91:4713-4717.
44. Parkin, N. T., et al. 1988. Mutational analysis of the 5?non-coding region of human immunodeficiency virus type 1: effects of secondary structure on translation. EMBO J. 7:2831-2837.
45. Paroo, Z., X. Ye, S. Chen, and Q. Liu. 2009. Phosphorylation of the human microRNA-generating complex mediates MAPK/Erk signaling. Cell 139: 112-122.
46. Roy, S., et al. 1990. Control of the interferon-induced 68-kilodalton protein kinase by the HIV-1 tat gene product. Science 247:1216-1219.
47. Sanghvi, V. R., and L. F. Steel. 2011. Expression of interfering RNAs from an HIV-1 Tat-inducible chimeric promoter. Virus Res. 155:106-111.
48. Sanghvi, V. R., and L. F. Steel. 2011. A re-examination of global suppression of RNA interference by HIV-1. PLoS One 6:e17246.
49. Singh, M., D. Castillo, C. V. Patel, and R. C. Patel. 2011. Stress-induced phosphorylation of PACT reduces its interaction with TRBP and leads to PKR activation. Biochemistry 50:4550-4560.
50. Skalsky, R. L., and B. R. Cullen. 2010. Viruses, microRNAs, and host interactions. Annu. Rev. Microbiol. 64:123-141.
51. Soumelis, V., et al. 2001. Depletion of circulating natural type 1 interferonproducing cells in HIV-infected AIDS patients. Blood 98:906-912.
52. Triboulet, R., et al. 2007. Suppression of microRNA-silencing pathway by HIV-1 during virus replication. Science 315:1579-1582.
53. Umbach, J. L., and B. R. Cullen. 2009. The role of RNAi and microRNAs in animal virus replication and antiviral immunity. Genes Dev. 23:1151-1164.
54. Wek, R. C., H. Y. Jiang, and T. G. Anthony. 2006. Coping with stress: eIF2 kinases and translational control. Biochem. Soc. Trans. 34:7-11.