HIV Vpu interferes with NF-κB activity but not with interferon regulatory factor 3

Journal of Virology

Volumn 89, Issue 19, 2015, Pages 9781-9790

  Manganaro, Lara ^a   de Castro, Elisa ^a   Maestre, Ana M ^a   Olivieri, Kevin ^b   García Sastre, Adolfo ^a   Fernandez Sesma, Ana ^a   Simon, Viviana ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b BURNHAM INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON REGULATORY FACTOR 3; VPU PROTEIN; GREEN FLUORESCENT PROTEIN; HUMAN IMMUNODEFICIENCY VIRUS PROTEIN; LUCIFERASE; PRIMER DNA; VIRAL PROTEIN; VPU PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS 1;

ARTICLE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; EMBRYO; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; INNATE IMMUNITY; MACROPHAGE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; GENETICS; HEK293 CELL LINE; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOBLOTTING; IMMUNOLOGY; METABOLISM; PLASMID; VIROLOGY;

CD4-POSITIVE T-LYMPHOCYTES; DNA PRIMERS; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; GREEN FLUORESCENT PROTEINS; HEK293 CELLS; HIV-1; HUMAN IMMUNODEFICIENCY VIRUS PROTEINS; HUMANS; IMMUNOBLOTTING; INTERFERON REGULATORY FACTOR-3; LUCIFERASES; NF-KAPPA B; PLASMIDS; SIGNAL TRANSDUCTION; VIRAL REGULATORY AND ACCESSORY PROTEINS;

EID: 84940981926     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01596-15     Document Type: Article

References (67)

1. Kumar H, Kawai T, Akira S. 2011. Pathogen recognition by the innate immune system. Int Rev Immunol 30:16-34. http://dx.doi.org/10.3109/08830185.2010.529976.
2. Newton K, Dixit VM. 2012. Signaling in innate immunity and inflammation. Cold Spring Harb Perspect Biol 4:a006049. http://dx.doi.org/10.1101/cshperspect.a006049.
3. Ranjan P, Bowzard JB, Schwerzmann JW, Jeisy-Scott V, Fujita T, Sambhara S. 2009. Cytoplasmic nucleic acid sensors in antiviral immunity. Trends Mol Med 15:359-368. http://dx.doi.org/10.1016/j.molmed.2009.06.003.
4. Iwasaki A, Medzhitov R. 2010. Regulation of adaptive immunity by the innate immune system. Science 327:291-295. http://dx.doi.org/10.1126/science.1183021.
5. Iannello A, Debbeche O, Martin E, Attalah LH, Samarani S, Ahmad A. 2006. Viral strategies for evading antiviral cellular immune responses of the host. J Leukoc Biol 79:16-35.
6. Landau NR. 2014. The innate immune response to HIV-1: to sense or not to sense. DNA Cell Biol 33:271-274. http://dx.doi.org/10.1089/dna.2014.2378.
7. Roy N, Pacini G, Berlioz-Torrent C, Janvier K. 2014. Mechanisms underlying HIV-1 Vpu-mediated viral egress. Front Microbiol 5:177. http://dx.doi.org/10.3389/fmicb.2014.00177.
8. Neil SJ, Zang T, Bieniasz PD. 2008. Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature 451:425-430. http://dx.doi.org/10.1038/nature06553.
9. Van Damme N, GoffD, Katsura C, Jorgenson RL, Mitchell R, Johnson MC, Stephens EB, Guatelli J. 2008. The interferon-induced protein BST-2 restricts HIV-1 release and is downregulated from the cell surface by the viral Vpu protein. Cell Host Microbe 3:245-252. http://dx.doi.org/10.1016/j.chom.2008.03.001.
10. Galao RP, Le Tortorec A, Pickering S, Kueck T, Neil SJ. 2012. Innate sensing of HIV-1 assembly by Tetherin induces NF-κB-dependent proinflammatory responses. Cell Host Microbe 12:633-644. http://dx.doi.org/10.1016/j.chom.2012.10.007.
11. Tokarev A, Suarez M, Kwan W, Fitzpatrick K, Singh R, Guatelli J. 2013. Stimulation of NF-κB activity by the HIV restriction factor BST2. J Virol 87:2046-2057. http://dx.doi.org/10.1128/JVI.02272-12.
12. Bour S, Perrin C, Akari H, Strebel K. 2001. The human immunodeficiency virus type 1 Vpu protein inhibits NF-κB activation by interfering with beta TrCP-mediated degradation of IκB. J Biol Chem 276:15920-15928. http://dx.doi.org/10.1074/jbc. M010533200.
13. Willey RL, Maldarelli F, Martin MA, Strebel K. 1992. Human immunodeficiency virus type 1 Vpu protein induces rapid degradation of CD4. J Virol 66:7193-7200.
14. Moll M, Andersson SK, Smed-Sorensen A, Sandberg JK. 2010. Inhibition of lipid antigen presentation in dendritic cells by HIV-1 Vpu interference with CD1d recycling from endosomal compartments. Blood 116: 1876-1884. http://dx.doi.org/10.1182/blood-2009-09-243667.
15. Shah AH, Sowrirajan B, Davis ZB, Ward JP, Campbell EM, Planelles V, Barker E. 2010. Degranulation of natural killer cells following interaction with HIV-1-infected cells is hindered by downmodulation of NTB-A by Vpu. Cell Host Microbe 8:397-409. http://dx.doi.org/10.1016/j.chom.2010.10.008.
16. Doehle BP, Chang K, Fleming L, McNevin J, Hladik F, McElrath MJ, Gale M, Jr. 2012. Vpu-deficient HIV strains stimulate innate immune signaling responses in target cells. J Virol 86:8499-8506. http://dx.doi.org/10.1128/JVI.00424-12.
17. Doehle BP, Chang K, Rustagi A, McNevin J, McElrath MJ, Gale M, Jr. 2012. Vpu mediates depletion of interferon regulatory factor 3 during HIV infection by a lysosome-dependent mechanism. J Virol 86:8367-8374. http://dx.doi.org/10.1128/JVI.00423-12.
18. Hotter D, KirchhoffF, Sauter D. 2013. HIV-1 Vpu does not degrade interferon regulatory factor 3. J Virol 87:7160-7165. http://dx.doi.org/10.1128/JVI.00526-13.
19. Park SY, Waheed AA, Zhang ZR, Freed EO, Bonifacino JS. 2014. HIV-1 Vpu accessory protein induces caspase-mediated cleavage of IRF3 transcription factor. J Biol Chem 289:35102-35110. http://dx.doi.org/10.1074/jbc. M114.597062.
20. Versteeg GA, Rajsbaum R, Sanchez-Aparicio MT, Maestre AM, Valdiviezo J, Shi M, Inn KS, Fernandez-Sesma A, Jung J, Garcia-Sastre A. 2013. The E3-ligase TRIM family of proteins regulates signaling pathways triggered by innate immune pattern-recognition receptors. Immunity 38: 384-398. http://dx.doi.org/10.1016/j.immuni.2012.11.013.
21. Rajsbaum R, Versteeg GA, Schmid S, Maestre AM, Belicha-Villanueva A, Martinez-Romero C, Patel JR, Morrison J, Pisanelli G, Miorin L, Laurent-Rolle M, Moulton HM, Stein DA, Fernandez-Sesma A, ten Oever BR, Garcia-Sastre A. 2014. Unanchored K48-linked polyubiquitin synthesized by the E3-ubiquitin ligase TRIM6 stimulates the interferon-IKKekinase-mediated antiviral response. Immunity 40:880-895. http://dx.doi.org/10.1016/j.immuni.2014.04.018.
22. Nistal-Villan E, Gack MU, Martinez-Delgado G, Maharaj NP, Inn KS, Yang H, Wang R, Aggarwal AK, Jung JU, Garcia-Sastre A. 2010. Negative role of RIG-I serine 8 phosphorylation in the regulation of interferon-beta production. J Biol Chem 285:20252-20261. http://dx.doi.org/10.1074/jbc. M109.089912.
23. Lahm HW, Stein S. 1985. Characterization of recombinant human interleukin-2 with micromethods. J chromatography 326:357-361. http://dx.doi.org/10.1016/S0021-9673(01)87461-6.
24. Aguirre S, Maestre AM, Pagni S, Patel JR, Savage T, Gutman D, Maringer K, Bernal-Rubio D, Shabman RS, Simon V, Rodriguez-Madoz JR, Mulder LC, Barber GN, Fernandez-Sesma A. 2012. DENV inhibits type I IFN production in infected cells by cleaving human STING. PLoS Pathog 8:e1002934. http://dx.doi.org/10.1371/journal.ppat.1002934.
25. Husain M, Gusella GL, Klotman ME, Gelman IH, Ross MD, Schwartz EJ, Cara A, Klotman PE. 2002. HIV-1 Nef induces proliferation and anchorage-independent growth in podocytes. JAmSoc Nephrol 13:1806-1815. http://dx.doi.org/10.1097/01.ASN.0000019642.55998.69.
26. Sauter D, Hue S, Petit SJ, Plantier JC, Towers GJ, KirchhoffF, Gupta RK. 2011. HIV-1 Group P is unable to antagonize human tetherin by Vpu, Env, or Nef. Retrovirology 8:103. http://dx.doi.org/10.1186/1742-4690-8-103.
27. Gack MU, Shin YC, Joo CH, Urano T, Liang C, Sun L, Takeuchi O, Akira S, Chen Z, Inoue S, Jung JU. 2007. TRIM25 RING-finger E3 ubiquitin ligase is essential for RIG-I-mediated antiviral activity. Nature 446:916-920. http://dx.doi.org/10.1038/nature05732.
28. Yoneyama M, Suhara W, Fukuhara Y, Fukuda M, Nishida E, Fujita T. 1998. Direct triggering of the type I interferon system by virus infection: activation of a transcription factor complex containing IRF-3 and CBP/p300. EMBO J 17:1087-1095. http://dx.doi.org/10.1093/emboj/17.4.1087.
29. Peden K, Emerman M, Montagnier L. 1991. Changes in growth properties on passage in tissue culture of viruses derived from infectious molecular clones of HIV-1LAI, HIV-1MAL, and HIV-1ELI. Virology 185:661-672. http://dx.doi.org/10.1016/0042-6822(91)90537-L.
30. Munch J, Rajan D, Schindler M, Specht A, Rucker E, Novembre FJ, Nerrienet E, Muller-Trutwin MC, Peeters M, Hahn BH, KirchhoffF. 2007. Nef-mediated enhancement of virion infectivity and stimulation of viral replication are fundamental properties of primate lentiviruses. J Virol 81:13852-13864. http://dx.doi.org/10.1128/JVI.00904-07.
31. Cohen GB, Gandhi RT, Davis DM, Mandelboim O, Chen BK, Strominger JL, Baltimore D. 1999. The selective downregulation of class I major histocompatibility complex proteins by HIV-1 protects HIV-infected cells from NK cells. Immunity 10:661-671. http://dx.doi.org/10.1016/S1074-7613(00)80065-5.
32. Chakrabarti LA, Ivanovic T, Cheng-Mayer C. 2002. Properties of the surface envelope glycoprotein associated with virulence of simian-human immunodeficiency virus SHIV(SF33A) molecular clones. J Virol 76: 1588-1599. http://dx.doi.org/10.1128/JVI.76.4.1588-1599.2002.
33. Goujon C, Jarrosson-Wuilleme L, Bernaud J, Rigal D, Darlix JL, Cimarelli A. 2006. With a little help from a friend: increasing HIV transduction of monocyte-derived dendritic cells with virion-like particles of SIV(MAC). Gene Ther 13:991-994. http://dx.doi.org/10.1038/sj.gt.3302753.
34. Negre D, Mangeot PE, Duisit G, Blanchard S, Vidalain PO, Leissner P, Winter AJ, Rabourdin-Combe C, Mehtali M, Moullier P, Darlix JL, Cosset FL. 2000. Characterization of novel safe lentiviral vectors derived from simian immunodeficiency virus (SIVmac251) that efficiently transduce mature human dendritic cells. Gene Ther 7:1613-1623. http://dx.doi.org/10.1038/sj.gt.3301292.
35. Yee JK, Friedmann T, Burns JC. 1994. Generation of high-titer pseudotyped retroviral vectors with very broad host range. Methods Cell Biol 43(Pt A):99-112.
36. Boussif O, Lezoualc'h F, Zanta MA, Mergny MD, Scherman D, Demeneix B, Behr JP. 1995. A versatile vector for gene and oligonucleotide transfer into cells in culture and in vivo: polyethylenimine. Proc Natl Acad Sci U S A 92:7297-7301. http://dx.doi.org/10.1073/pnas.92.16.7297.
37. Ooms M, Majdak S, Seibert CW, Harari A, Simon V. 2010. The localization of APOBEC3H variants in HIV-1 virions determines their antiviral activity. J Virol 84:7961-7969. http://dx.doi.org/10.1128/JVI.00754-10.
38. Platt EJ, Bilska M, Kozak SL, Kabat D, Montefiori DC. 2009. Evidence that ecotropic murine leukemia virus contamination in TZM-bl cells does not affect the outcome of neutralizing antibody assays with human immunodeficiency virus type 1. J Virol 83:8289-8292. http://dx.doi.org/10.1128/JVI.00709-09.
39. Platt EJ, Wehrly K, Kuhmann SE, Chesebro B, Kabat D. 1998. Effects of CCR5 and CD4 cell surface concentrations on infections by macrophagetropic isolates of human immunodeficiency virus type 1. J Virol 72:2855-2864.
40. Takeuchi Y, McClure MO, Pizzato M. 2008. Identification of gammaretroviruses constitutively released from cell lines used for human immunodeficiency virus research. J Virol 82:12585-12588. http://dx.doi.org/10.1128/JVI.01726-08.
41. Wei X, Decker JM, Liu H, Zhang Z, Arani RB, Kilby JM, Saag MS, Wu X, Shaw GM, Kappes JC. 2002. Emergence of resistant human immunodeficiency virus type 1 in patients receiving fusion inhibitor (T-20) monotherapy. Antimicrob Agents Chemother 46:1896-1905. http://dx.doi.org/10.1128/AAC.46.6.1896-1905.2002.
42. Derdeyn CA, Decker JM, Sfakianos JN, Wu X, O'Brien WA, Ratner L, Kappes JC, Shaw GM, Hunter E. 2000. Sensitivity of human immunodeficiency virus type 1 to the fusion inhibitor T-20 is modulated by coreceptor specificity defined by the V3 loop of gp120. J Virol 74:8358-8367. http://dx.doi.org/10.1128/JVI.74.18.8358-8367.2000.
43. Yoneyama M, Kikuchi M, Natsukawa T, Shinobu N, Imaizumi T, Miyagishi M, Taira K, Akira S, Fujita T. 2004. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat Immunol 5:730-737. http://dx.doi.org/10.1038/ni1087.
44. Papkalla A, Munch J, Otto C, KirchhoffF. 2002. Nef enhances human immunodeficiency virus type 1 infectivity and replication independently of viral coreceptor tropism. J Virol 76:8455-8459. http://dx.doi.org/10.1128/JVI.76.16.8455-8459.2002.
45. Harari A, Ooms M, Mulder LC, Simon V. 2009. Polymorphisms and splice variants influence the antiretroviral activity of human APOBEC3H. J Virol 83:295-303. http://dx.doi.org/10.1128/JVI.01665-08.
46. Hrecka K, Hao C, Gierszewska M, Swanson SK, Kesik-Brodacka M, Srivastava S, Florens L, Washburn MP, Skowronski J. 2011. Vpx relieves inhibition of HIV-1 infection of macrophages mediated by the SAMHD1 protein. Nature 474:658-661. http://dx.doi.org/10.1038/nature10195.
47. Laguette N, Sobhian B, Casartelli N, Ringeard M, Chable-Bessia C, Segeral E, Yatim A, Emiliani S, Schwartz O, Benkirane M. 2011. SAMHD1 is the dendritic-and myeloid-cell-specific HIV-1 restriction factor counteracted by Vpx. Nature 474:654-657. http://dx.doi.org/10.1038/nature10117.
48. Manel N, Hogstad B, Wang Y, Levy DE, Unutmaz D, Littman DR. 2010. Acryptic sensor for HIV-1 activates antiviral innate immunity in dendritic cells. Nature 467:214-217. http://dx.doi.org/10.1038/nature09337.
49. Mascola JR, Louder MK, Winter C, Prabhakara R, De Rosa SC, Douek DC, Hill BJ, Gabuzda D, Roederer M. 2002. Human immunodeficiency virus type 1 neutralization measured by flow cytometric quantitation of single-round infection of primary human T cells. J Virol 76:4810-4821. http://dx.doi.org/10.1128/JVI.76.10.4810-4821.2002.
50. Snyder A, Alsauskas ZC, Leventhal JS, Rosenstiel PE, Gong P, Chan JJ, Barley K, He JC, Klotman ME, Ross MJ, Klotman PE. 2010. HIV-1 viral protein r induces ERK and caspase-8-dependent apoptosis in renal tubular epithelial cells. AIDS 24:1107-1119. http://dx.doi.org/10.1097/QAD.0b013e328337b0ab.
51. Fujita T, Shibuya H, Hotta H, Yamanishi K, Taniguchi T. 1987. Interferon-beta gene regulation: tandemly repeated sequences of a synthetic 6-bp oligomer function as a virus-inducible enhancer. Cell 49:357-367. http://dx.doi.org/10.1016/0092-8674(87)90288-1.
52. Sharma S, ten Oever BR, Grandvaux N, Zhou GP, Lin R, Hiscott J. 2003. Triggering the interferon antiviral response through an IKK-related pathway. Science 300:1148-1151. http://dx.doi.org/10.1126/science.1081315.
53. Uchil PD, Hinz A, Siegel S, Coenen-Stass A, Pertel T, Luban J, Mothes W. 2013. TRIM protein-mediated regulation of inflammatory and innate immune signaling and its association with antiretroviral activity. J Virol 87:257-272. http://dx.doi.org/10.1128/JVI.01804-12.
54. Sauter D, Hotter D, Van Driessche B, Sturzel CM, Kluge SF, Wildum S, Yu H, Baumann B, Wirth T, Plantier JC, Leoz M, Hahn BH, Van Lint C, KirchhoffF. 2015. Differential regulation of NF-κB-mediated proviral and antiviral host gene expression by primate lentiviral Nef and Vpu proteins. Cell Reports 10:586-599. http://dx.doi.org/10.1016/j.celrep.2014.12.047.
55. Beg AA, Finco TS, Nantermet PV, Baldwin AS, Jr. 1993. Tumor necrosis factor and interleukin-1 lead to phosphorylation and loss of IκBα: a mechanism for NF-κB activation. Mol Cell Biol 13:3301-3310.
56. Blanchet FP, Mitchell JP, Piguet V. 2012. beta-TrCP dependency of HIV-1 Vpu-induced downregulation of CD4 and BST-2/tetherin. Curr HIV Res 10:307-314. http://dx.doi.org/10.2174/157016212800792441.
57. Margottin F, Bour SP, Durand H, Selig L, Benichou S, Richard V, Thomas D, Strebel K, Benarous R. 1998. A novel human WD protein, h-beta TrCp, that interacts with HIV-1 Vpu connects CD4 to the ER degradation pathway through an F-box motif. Mol Cell 1:565-574. http://dx.doi.org/10.1016/S1097-2765(00)80056-8.
58. Mangeat B, Gers-Huber G, Lehmann M, Zufferey M, Luban J, Piguet V. 2009. HIV-1 Vpu neutralizes the antiviral factor Tetherin/BST-2 by binding it and directing its beta-TrCP2-dependent degradation. PLoS Pathog 5:e1000574. http://dx.doi.org/10.1371/journal.ppat.1000574.
59. Besnard-Guerin C, Belaidouni N, Lassot I, Segeral E, Jobart A, Marchal C, Benarous R. 2004. HIV-1 Vpu sequesters β-transducin repeatcontaining protein (βTrCP) in the cytoplasm and provokes the accumulation of beta-catenin and other SCFβTrCP substrates. J Biol Chem 279: 788-795. http://dx.doi.org/10.1074/jbc. M308068200.
60. Beg AA, Baldwin AS, Jr. 1993. The IκB proteins: multifunctional regulators of Rel/NF-κB transcription factors. Genes Dev 7:2064-2070. http://dx.doi.org/10.1101/gad.7.11.2064.
61. Brown K, Park S, Kanno T, Franzoso G, Siebenlist U. 1993. Mutual regulation of the transcriptional activator NF-κB and its inhibitor, IκBα. Proc Natl Acad Sci U S A 90:2532-2536. http://dx.doi.org/10.1073/pnas.90.6.2532.
62. Henkel T, Machleidt T, Alkalay I, Kronke M, Ben-Neriah Y, Baeuerle PA. 1993. Rapid proteolysis of IκBα is necessary for activation of transcription factor NF-κB. Nature 365:182-185.
63. Altfeld M, Gale M, Jr. 2015. Innate immunity against HIV-1 infection. Nat Immunol 16:554-562. http://dx.doi.org/10.1038/ni.3157.
64. Simon V, Bloch N, Landau NR. 2015. Intrinsic host restrictions to HIV-1 and mechanisms of viral escape. Nat Immunol 16:546-553. http://dx.doi.org/10.1038/ni.3156.
65. Cummins NW, Badley AD. 2010. Mechanisms of HIV-associated lymphocyte apoptosis: 2010. Cell Death Dis 1:e99. http://dx.doi.org/10.1038/cddis.2010.77.
66. Harman AN, Nasr N, Feetham A, Galoyan A, Alshehri AA, Rambukwelle D, Botting RA, Hiener BM, Diefenbach E, Diefenbach RJ, Kim M, Mansell A, Cunningham AL. 2015. HIV blocks interferon induction in human dendritic cells and macrophages by dysregulation of TBK1. J Virol 89:6575-6584. http://dx.doi.org/10.1128/JVI.00889-15.
67. Chan JK, Greene WC. 2012. Dynamic roles for NF-κB in HTLV-1 and HIV-1 retroviral pathogenesis. Immunol Rev 246:286-310. http://dx.doi.org/10.1111/j.1600-065X.2012.01094.x.