HIV-1 Rev downregulates Tat expression and viral replication via modulation of NAD(P)H:quinine oxidoreductase 1 (NQO1)

Nature Communications

Volumn 6, Issue , 2015, Pages

  Lata, Sneh ^a   Ali, Amjad ^b   Sood, Vikas ^a,b,c   Raja, Rameez ^b   Banerjea, Akhil C ^b  

^a UNIVERSITY COLLEGE OF MEDICAL SCIENCES   (India)

^b NATIONAL INSTITUTE OF IMMUNOLOGY   (India)

^c TRANSLATIONAL HEALTH SCIENCE AND TECHNOLOGY INSTITUTE   (India)

Author keywords

[No Author keywords available]

Indexed keywords

DICOUMAROL; NAD(P)H:QUININE OXIDOREDUCTASE 1; OXIDOREDUCTASE; PROTEASOME; REV PROTEIN; TRANSACTIVATOR PROTEIN; UNCLASSIFIED DRUG; NQO1 PROTEIN, HUMAN; NUCLEAR EXPORT SIGNAL; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) DEHYDROGENASE (QUINONE);

BIODEGRADATION; ENZYME ACTIVITY; GENE EXPRESSION; INHIBITION; INHIBITOR; PROTEIN; VIRUS;

ARTICLE; CYTOPLASM; DOWN REGULATION; EMBRYO; GENE EXPRESSION; GENETIC TRANSFECTION; HEK293 CELL LINE; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; HUMAN IMMUNODEFICIENCY VIRUS 1; IN VITRO STUDY; NUCLEAR EXPORT SIGNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; UBIQUITINATION; VIRUS REPLICATION; METABOLISM; PHYSIOLOGY;

HUMAN IMMUNODEFICIENCY VIRUS 1;

GENE PRODUCTS, REV; GENE PRODUCTS, TAT; HIV-1; NAD(P)H DEHYDROGENASE (QUINONE); NUCLEAR EXPORT SIGNALS; PROTEOLYSIS; VIRUS REPLICATION;

EID: 84931260280     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms8244     Document Type: Article

References (54)

1. Rana, T. M. & Jeang, K. T. Biochemical and functional interactions between HIV-1 Tat protein and TAR RNA. Arch. Biochem. Biophys. 365, 175-185 (1999).
2. Kjems, J., Frankel, A. D. & Sharp, P. A. Specific regulation of mRNA splicing in vitro by a peptide from HIV-1 Rev. Cell 67, 169-178 (1991).
3. Hope, T. J., McDonald, D., Huang, X. J., Low, J. & Parslow, T. G. Mutational analysis of the human immunodeficiency virus type 1 Rev transactivator: Essential residues near the amino terminus. J. Virol. 64, 5360-5366 (1990).
4. Malim, M. H., Hauber, J., Le, S. Y., Maizel, J. V. & Cullen, B. R. The HIV-1 rev trans-activator acts through a structured target sequence to activate nuclear export of unspliced viral mRNA. Nature 338, 254-257 (1989).
5. Felber, B. K., Drysdale, C. M. & Pavlakis, G. N. Feedback regulation of human immunodeficiency virus type 1 expression by the Rev protein. J. Virol. 64, 3734-3741 (1990).
6. Kalland, K. H., Szilvay, A. M., Brokstad, K. A., Saetrevik, W. & Haukenes, G. The human immunodeficiency virus type 1 Rev protein shuttles between the cytoplasm and nuclear compartments. Mol. Cell. Biol. 14, 7436-7444 (1994).
7. Meyer, B. E. & Malim, M. H. The HIV-1 Rev trans-activator shuttles between the nucleus and the cytoplasm. Genes Dev. 8, 1538-1547 (1994).
8. Richard, N., Iacampo, S. & Cochrane, A. HIV-1 Rev is capable of shuttling between the nucleus and cytoplasm. Virology 204, 123-131 (1994).
9. Stauber, R. H. & Pavlakis, G. N. Intracellular trafficking and interactions of the HIV-1 Tat protein. Virology 252, 126-136 (1998).
10. Fornerod, M., Ohno, M., Yoshida, M. & Mattaj, I. W. CRM1 is an export receptor for leucine-rich nuclear export signals. Cell 90, 1051-1060 (1997).
11. Marcello, A., Zoppe, M. & Giacca, M. Multiple modes of transcriptional regulation by the HIV-1 Tat transactivator. IUBMB Life 51, 175-181 (2001).
12. Emerman, M. & Malim, M. H. HIV-1 regulatory/accessory genes: Keys to unraveling viral and host cell biology. Science 280, 1880-1884 (1998).
13. Sawaya, B. E., Khalili, K., Gordon, J., Taube, R. & Amini, S. Cooperative interaction between HIV-1 regulatory proteins Tat and Vpr modulates transcription of the viral genome. J. Biol. Chem. 275, 35209-35214 (2000).
14. Wang, J. et al. The HIV-1 Vif protein mediates degradation of Vpr and reduces Vpr-induced cell cycle arrest. DNA Cell Biol. 27, 267-277 (2008).
15. Joseph, A. M., Ladha, J. S., Mojamdar, M. & Mitra, D. Human immunodeficiency virus-1 Nef protein interacts with Tat and enhances HIV-1 gene expression. FEBS Lett. 548, 37-42 (2003).
16. Hershko, A. Roles of ubiquitin-mediated proteolysis in cell cycle control. Curr. Opin. Cell Biol. 9, 788-799 (1997).
17. Ciechanover, A. Intracellular protein degradation: From a vague idea thru the lysosome and the ubiquitin-proteasome system and onto human diseases and drug targeting. Cell Death Differ. 12, 1178-1190 (2005).
18. Voges, D., Zwickl, P. & Baumeister, W. The 26S proteasome: A molecular machine designed for controlled proteolysis. Annu. Rev. Biochem. 68, 1015-1068 (1999).
19. Gsponer, J., Futschik, M. E., Teichmann, S. A. & Babu, M. M. Tight regulation of unstructured proteins: From transcript synthesis to protein degradation. Science 322, 1365-1368 (2008).
20. Asher, G., Reuven, N. & Shaul, Y. 20S proteasomes and protein degradation "by default". Bioessays 28, 844-849 (2006).
21. Davies, K. J. Degradation of oxidized proteins by the 20S proteasome. Biochimie 83, 301-310 (2001).
22. Baugh, J. M., Viktorova, E. G. & Pilipenko, E. V. Proteasomes can degrade a significant proportion of cellular proteins independent of ubiquitination. J. Mol. Biol. 386, 814-827 (2009).
23. Asher, G., Tsvetkov, P., Kahana, C. & Shaul, Y. A mechanism of ubiquitinindependent proteasomal degradation of the tumor suppressors p53 and p73. Genes Dev. 19, 316-321 (2005).
24. Wiggins, C. M. et al. BIMEL, an intrinsically disordered protein, is degraded by 20S proteasomes in the absence of poly-ubiquitylation. J. Cell Sci. 124, 969-977 (2011).
25. Asher, G., Bercovich, Z., Tsvetkov, P., Shaul, Y. & Kahana, C. 20S proteasomal degradation of ornithine decarboxylase is regulated by NQO1. Mol. Cell 17, 645-655 (2005).
26. Adamovich, Y. et al. The protein level of PGC-1a, a key metabolic regulator, is controlled by NADH-NQO1. Mol. Cell. Biol. 3, 2603-2613 (2013).
27. Moscovitz, O. et al. A mutually inhibitory feedback loop between the 20S proteasome and its regulator, NQO1. Mol. Cell 47, 76-86 (2012).
28. Henning, M. S., Morham, S. G., Goff, S. P. & Naghavi, M. H. PDZD8 is a novel Gag-interacting factor that promotes retroviral infection. J. Virol. 84, 8990-8995 (2010).
29. Brès, V. et al. A non-proteolytic role for ubiquitin in Tat-mediated transactivation of the HIV-1 promoter. Nat. Cell Biol. 5, 754-761 (2003).
30. Verma, S., Ali, A., Arora, S. & Banerjea, A. C. Inhibition of b-TrcP-dependent ubiquitination of p53 by HIV-1 Vpu promotes p53-mediated apoptosis in human T cells. Blood 117, 6600-6607 (2011).
31. Lim, K. L. et al. Parkin mediates nonclassical, proteasomal-independent ubiquitination of synphilin-1: Implications for Lewy body formation. J. Neurosci. 25, 2002-2009 (2005).
32. Yang, Y. et al. Inhibitors of ubiquitin-activating enzyme (E1), a new class of potential cancer therapeutics. Cancer Res. 67, 9472-9481 (2007).
33. Ponia, S. S., Arora, S., Kumar, B. & Banerjea, A. C. Arginine rich short linear motif of HIV-1 regulatory proteins inhibits Dicer dependent RNA interference. Retrovirology 10, 97 (2013).
34. Meredith, L. W., Sivakumaran, H., Major, L., Suhrbier, A. & Harrich., D. Potent inhibition of HIV-1 replication by a Tat mutant. PLoS ONE 4, e7769 (2009).
35. Shojania, S. & O'Neil, J. D. Intrinsic disorder and function of the HIV-1 Tat protein. Protein Pept. Lett. 17, 999-1011 (2010).
36. Platt, E. J., Wehrly, K., Kuhmann, S. E., Chesebro, B. & Kabat, D. Effects of CCR5 and CD4 cell surface concentrations on infections by macrophagetropic isolates of human immunodeficiency virus type 1. J. Virol. 4, 2855-2864 (1998).
37. Hamy, F. et al. Blocking HIV replication by targeting Tat protein. Chem. Biol. 7, 669-676 (2000).
38. Perez, V. L. et al. An HIV-1-infected T cell clone defective in IL-2 production and Ca2 mobilization after CD3 stimulation. J. Immunol. 147, 3145-3148 (1991).
39. Fernández Larrosa, P. N. et al. Apoptosis resistance in HIV-1 persistentlyinfected cells is independent of active viral replication and involves modulation of the apoptotic mitochondrial pathway. Retrovirology 5, 19 (2008).
40. Riccardi, C. & Nicoletti, I. Analysis of apoptosis by propidium iodide staining and flow cytometry. Nat. Protoc. 1, 1458-1461 (2006).
41. Freeman, W. M., Walker, S. J. & Vrana, K. E. Quantitative RT-PCR: Pitfalls and potential. Biotechniques 26, 112-122 124-125 (1999).
42. Singh, D. K., Islam, M. N., Choudhury, N. R., Karjee, S. & Mukherjee, S. K. The 32 kDa subunit of replication protein A (RPA) participates in the DNA replication of Mung bean yellow mosaic India virus (MYMIV) by interacting with the viral Rep protein. Nucleic Acids Res. 35, 755-770 (2007).
43. Verma, S., Ronsard, L., Kapoor, R. & Banerjea, A. C. Genetic characterization of natural variants of Vpu from HIV-1 infected individuals from Northern India and their impact on virus release and cell death. PLoS ONE 8, e59283 (2013).
44. He, J. et al. Human immunodeficiency virus type 1 viral protein R (Vpr) arrests cells in the G2 phase of the cell cycle by inhibiting p34cdc2 activity. J. Virol. 69, 6705-6711 (1995).
45. Fiume, G. et al. Human immunodeficiency virus-1 Tat activates NF-kB via physical interaction with IkB-a and p65. Nucleic Acids Res. 40, 3548-3562 (2012).
46. Mousseau, G. et al. An analog of the natural steroidal alkaloid cortistatin A potently suppresses Tat-dependent HIV transcription. Cell Host Microbe 12, 97-108 (2012).
47. Cujec, T. P. et al. The HIV transactivator TAT binds to the CDK-activating kinase and activates the phosphorylation of the carboxy-terminal domain of RNA polymerase II. Genes Dev. 11, 2645-2657 (1997).
48. Lu, R. et al. Class II integrase mutants with changes in putative nuclear localization signals are primarily blocked at a postnuclear entry step of human immunodeficiency virus type 1 replication. J. Virol. 78, 12735-12746 (2004).
49. Ward, A. M., Rekosh, D. & Hammarskjold, M. L. Trafficking through the Rev/RRE pathway is essential for efficient inhibition of human immunodeficiency virus type 1 by an antisense RNA derived from the envelope gene. J. Virol. 83, 940-952 (2009).
50. Klave, B. & Berkhout, B. Comparison of the 50 and 30 LTR promoter function in the human immunodeficiency virus. J. Virol. 68, 3830-3840 (1994).
51. Adachi, A. et al. Production of acquired immunodeficiency syndromeassociated retrovirus in human and nonhuman cells transfected with an infectious molecular clone. J. Virol. 59, 284-291 (1986).
52. Chang, L.-J., Urlacher, V., Iwakuma, T., Cui, Y. & Zucali, J. Efficacy and safety analyses of a recombinant human immunodeficiency virus type 1 derived vector system. Gene Ther. 6, 715-728 (1999).
53. Gao, F. et al. Codon usage optimization of HIV type 1 subtype C gag, pol, env, and nef genes: In vitro expression and immune responses in DNA-vaccinated mice. AIDS Res. Hum. Retroviruses 19, 817-823 (2003).
54. Xirodimas, D. P., Stephen, C. W. & Lane, D. P. Cocopartmentalization of p53 and Mdm-2 is a major determinant for Mdm-2-mediated degradation of p53. Exp. Cell Res. 270, 66-77 (2001).