Vpu Downmodulates Two Distinct Targets, Tetherin and Gibbon Ape Leukemia Virus Envelope, through Shared Features in the Vpu Cytoplasmic Tail

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Lucas, Tiffany M ^a   Janaka, Sanath K ^a   Stephens, Edward B ^b   Johnson, Marc C ^a  

^a University of Missouri   (United States)

^b UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; GIBBON APE LEUKEMIA VIRUS ENVELOPE PROTEIN; MEMBRANE PROTEIN; TETHERIN; UNCLASSIFIED DRUG; VIRUS ENVELOPE PROTEIN; VPU PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; CYTOPLASMIC TAIL; DOWN REGULATION; HINGE REGION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN STRUCTURE; PROTEIN TARGETING; STRUCTURE ACTIVITY RELATION; VIRUS PARTICLE;

AMINO ACID SEQUENCE; ANTIGENS, CD; CYTOPLASM; FLOW CYTOMETRY; GPI-LINKED PROTEINS; HEK293 CELLS; HIV-1; HUMAN IMMUNODEFICIENCY VIRUS PROTEINS; HUMANS; LEUKEMIA VIRUS, GIBBON APE; MOLECULAR SEQUENCE DATA; MUTANT PROTEINS; PROTEIN INTERACTION DOMAINS AND MOTIFS; RECOMBINANT FUSION PROTEINS; VIRAL REGULATORY AND ACCESSORY PROTEINS; VIRION; VIRUS ASSEMBLY; VIRUS REPLICATION;

GIBBON APE LEUKEMIA VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84871261826     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0051741     Document Type: Article

References (55)

1. Janaka SK, Lucas TM, Johnson MC, (2011) Sequences in gibbon ape leukemia virus envelope that confer sensitivity to HIV-1 accessory protein Vpu. Journal of Virology 85: 11945-11954.
2. Lucas TM, Lyddon TD, Cannon PM, Johnson MC, (2010) Pseudotyping incompatibility between HIV-1 and gibbon ape leukemia virus Env is modulated by Vpu. Journal of Virology 84: 2666-2674.
3. Christodoulopoulos I, Droniou-Bonzom ME, Oldenburg JE, Cannon PM, (2010) Vpu-dependent block to incorporation of GaLV Env into lentiviral vectors. Retrovirology 7: 4.
4. Bour S, Perrin C, Akari H, Strebel K, (2001) The Human Immunodeficiency Virus Type 1 Vpu Protein Inhibits NF-κB Activation by Interfering with βTrCP-mediated Degradation of IκB. Journal of Biological Chemistry 276: 15920-15928.
5. Bour S, Schubert U, Strebel K, (1995) The human immunodeficiency virus type 1 Vpu protein specifically binds to the cytoplasmic domain of CD4: Implications for the mechanism of degradation. Journal of Virology 69: 1510-1520.
6. Willey RL, Maldarelli F, Martin MA, Strebel K, (1992) Human immunodeficiency virus type 1 Vpu protein induces rapid degradation of CD4. Journal of Virology 66: 7193-7200.
7. Hussain A, Wesley C, Khalid M, Chaudhry A, Jameel S, (2008) Human Immunodeficiency Virus Type 1 Vpu Protein Interacts with CD74 and Modulates Major Histocompatibility Complex Class II Presentation. Journal of Virology 82: 893-902.
8. Shah AH, Sowrirajan B, Davis ZB, Ward JP, Campbell EM, et al. (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.
9. Neil SJD, Sandrin V, Sundquist WI, Bieniasz PD, (2007) An Interferon-±-Induced Tethering Mechanism Inhibits HIV-1 and Ebola Virus Particle Release but Is Counteracted by the HIV-1 Vpu Protein. Cell host & microbe 2: 193-203.
10. Bour S, Strebel K, (2003) The HIV-1 Vpu protein: A multifunctional enhancer of viral particle release. Microbes and Infection 5: 1029-1039.
11. Nomaguchi M, Fujita M, Adachi A, (2008) Role of HIV-1 Vpu protein for virus spread and pathogenesis. Microbes and Infection 10: 960-967.
12. Guatelli JC, (2009) Interactions of viral protein U (Vpu) with cellular factors. pp. 27-45.
13. Ruiz A, Guatelli JC, Stephens EB, (2010) The Vpu protein: New concepts in virus release and CD4 down-modulation. Current HIV Research 8: 240-252.
14. Willey RL, Buckler-White A, Strebel K, (1994) Sequences present in the cytoplasmic domain of CD4 are necessary and sufficient to confer sensitivity to the human immunodeficiency virus type 1 Vpu protein. Journal of Virology 68: 1207-1212.
15. Chen MY, Maldarelli F, Karczewski MK, Willey RL, Strebel K, (1993) Human immunodeficiency virus type 1 Vpu protein induces degradation of CD4 in vitro: The cytoplasmic domain of CD4 contributes to Vpu sensitivity. Journal of Virology 67: 3877-3884.
16. Schubert U, Anton LC, Cox JH, Bour S, Bennink JR, et al. (1998) CD4 Glycoprotein Degradation Induced by Human Immunodeficiency Virus Type 1 Vpu Protein Requires the Function of Proteasomes and the Ubiquitin-Conjugating Pathway. J Virol 72: 2280-2288.
17. Margottin F, Bour SP, Durand H, Selig L, Benichou S, et al. (1998) A novel human WD protein, h-βTrCP, that interacts with HIV-1 Vpu connects CD4 to the ER degradation pathway through an F-box motif. Molecular Cell 1: 565-574.
18. Magadán JG, Pérez-Victoria FJ, Sougrat R, Ye Y, Strebel K, et al. (2010) Multilayered mechanism of CD4 downregulation by HIV-1 Vpu involving distinct ER retention and ERAD targeting steps. PLoS Pathogens 6: e1000869.
19. Fujita K, Omura S, Silver J, (1997) Rapid degradation of CD4 in cells expressing human immunodeficiency virus type 1 Env and Vpu is blocked by proteasome inhibitors. Journal of General Virology 78: 619-625.
20. Magadán JG, Bonifacino JS, (2012) Transmembrane Domain Determinants of CD4 Downregulation by HIV-1 Vpu. Journal of Virology 86: 757-772.
21. Tiganos E, Friborg J, Allain B, Daniel NG, Yao XJ, et al. (1998) Structural and functional analysis of the membrane-spanning domain of the human immunodeficiency virus type 1 Vpu protein. Virology 251: 96-107.
22. Hill MS, Ruiz A, Schmitt K, Stephens EB, (2010) Identification of amino acids within the second alpha helical domain of the human immunodeficiency virus type 1 Vpu that are critical for preventing CD4 cell surface expression. Virology 397: 104-112.
23. Ruiz A, Hill MS, Schmitt K, Guatelli J, Stephens EB, (2008) Requirements of the membrane proximal tyrosine and dileucine-based sorting signals for efficient transport of the subtype C Vpu protein to the plasma membrane and in virus release. Virology 378: 58-68.
24. Schubert U, Bour S, Ferrer-Montiel AV, Montal M, Maldarell F, et al. (1996) The two biological activities of human immunodeficiency virus type 1 Vpu protein involve two separable structural domains. Journal of Virology 70: 809-819.
25. Hout DR, Gomez ML, Pacyniak E, Gomez LM, Inbody SH, et al. (2005) Scrambling of the amino acids within the transmembrane domain of Vpu results in a simian-human immunodeficiency virus (SHIVTM) that is less pathogenic for pig-tailed macaques. Virology 339: 56-69.
26. Watanabe R, Leser GP, Lamb RA, (2011) Influenza virus is not restricted by tetherin whereas influenza VLP production is restricted by tetherin. Virology 417: 50-56.
27. Pardieu C, Vigan R, Wilson SJ, Calvi A, Zang T, et al. (2010) The RING-CH Ligase K5 Antagonizes Restriction of KSHV and HIV-1 Particle Release by Mediating Ubiquitin-Dependent Endosomal Degradation of Tetherin. PLoS Pathog 6: e1000843.
28. Neil SJD, Zang T, Bieniasz PD, (2008) Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature 451: 425-430.
29. Dubé M, Paquay C, Roy BB, Bego MG, Mercier J, et al. (2011) HIV-1 Vpu Antagonizes BST-2 by Interfering Mainly with the Trafficking of Newly Synthesized BST-2 to the Cell Surface. Traffic 12: 1714-1729.
30. Schmidt S, Fritz JV, Bitzegeio J, Fackler OT, Keppler OT, (2011) HIV-1 vpu blocks recycling and biosynthetic transport of the intrinsic immunity factor CD317/tetherin to overcome the virion release restriction. mBio 2.
31. Skasko M, Tokarev A, Chen CC, Fischer WB, Pillai SK, et al. (2011) BST-2 is rapidly down-regulated from the cell surface by the HIV-1 protein Vpu: Evidence for a post-ER mechanism of Vpu-action. Virology 411: 65-77.
32. Hauser H, Lopez LA, Yang SJ, Oldenburg JE, Exline CM, et al. (2010) HIV-1 Vpu and HIV-2 Env counteract BST-2/tetherin by sequestration in a perinuclear compartment. Retrovirology 7: 51.
33. Mitchell RS, Katsura C, Skasko MA, Fitzpatrick K, Lau D, et al. (2009) Vpu Antagonizes BST-2-Mediated Restriction of HIV-1 Release via β-TrCP and Endo-Lysosomal Trafficking. PLoS Pathog 5: e1000450.
34. Dubé M, Roy BB, Guiot-Guillain P, Binette J, Mercier J, et al. (2010) Antagonism of tetherin restriction of HIV-1 release by Vpu involves binding and sequestration of the restriction factor in a perinuclear compartment. PLoS Pathogens 6: e1000856.
35. Miyagi E, Andrew AJ, Kao S, Strebel K, (2009) Vpu enhances HIV-1 virus release in the absence of Bst-2 cell surface down-modulation and intracellular depletion. Proceedings of the National Academy of Sciences 106: 2868-2873.
36. Douglas JL, Viswanathan K, McCarroll MN, Gustin JK, Früh K, et al. (2009) Vpu directs the degradation of the human immunodeficiency virus restriction factor BST-2/tetherin via a βTrCP-dependent mechanism. Journal of Virology 83: 7931-7947.
37. Mangeat B, Gers-Huber G, Lehmann M, Zufferey M, Luban J, et al. (2009) HIV-1 Vpu neutralizes the antiviral factor tetherin/BST-2 by binding it and directing its beta-TrCP2-dependent degradation. PLoS Pathogens 5: e1000574.
38. Schubert U, Henklein P, Boldyreff B, Wingender E, Strebel K, et al. (1994) The human immunodeficiency virus type 1 encoded Vpu protein is phosphorylated by casein kinase-2 (CK-2) at positions Ser52 and Ser56 within a predicted alpha-helix-turn-alpha-helix motif. J Mol Biol 236: 16-25.
39. Binette J, Dube M, Mercier J, Halawani D, Latterich M, et al. (2007) Requirements for the selective degradation of CD4 receptor molecules by the human immunodeficiency virus type 1 Vpu protein in the endoplasmic reticulum. Retrovirology 4: 75.
40. Lewis BC, Chinnasamy N, Morgan RA, Varmus HE, (2001) Development of an avian leukosis-sarcoma virus subgroup A pseudotyped lentiviral vector. J Virol 75: 9339-9344.
41. Perez-Caballero D, Zang T, Ebrahimi A, McNatt MW, Gregory DA, et al. (2009) Tetherin Inhibits HIV-1 Release by Directly Tethering Virions to Cells. Cell 139: 499-511.
42. Jorgenson RL, Vogt VM, Johnson MC, (2009) Foreign glycoproteins can be actively recruited to virus assembly sites during pseudotyping. J Virol 83: 4060-4067.
43. Van Damme N, Goff D, Katsura C, Jorgenson RL, Mitchell R, et al. (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.
44. Vigan R, Neil SJD, (2010) Determinants of tetherin antagonism in the transmembrane domain of the human immunodeficiency virus type 1 Vpu protein. Journal of Virology 84: 12958-12970.
45. Skasko M, Wang Y, Tian Y, Tokarev A, Munguia J, et al. (2012) HIV-1 Vpu Protein Antagonizes Innate Restriction Factor BST-2 via Lipid-embedded Helix-Helix Interactions. Journal of Biological Chemistry 287: 58-67.
46. Schubert U, Strebel K, (1994) Differential activities of the human immunodeficiency virus type 1-encoded Vpu protein are regulated by phosphorylation and occur in different cellular compartments. Journal of Virology 68: 2260-2271.
47. Vigan R, Neil SJD, (2011) Separable Determinants of Subcellular Localization and Interaction Account for the Inability of Group O HIV-1 Vpu To Counteract Tetherin. Journal of Virology 85: 9737-9748.
48. Dubé M, Roy BB, Guiot-Guillain P, Mercier J, Binette J, et al. (2009) Suppression of Tetherin-Restricting Activity upon Human Immunodeficiency Virus Type 1 Particle Release Correlates with Localization of Vpu in the trans-Golgi Network. Journal of Virology 83: 4574-4590.
49. Kueck T, Neil SJ, (2012) A cytoplasmic tail determinant in HIV-1 Vpu mediates targeting of tetherin for endosomal degradation and counteracts interferon-induced restriction. PLoS Pathog 8: e1002609.
50. Rong L, Zhang J, Lu J, Pan Q, Lorgeoux RP, et al. (2009) The transmembrane domain of BST-2 determines its sensitivity to down-modulation by human immunodeficiency virus type 1 Vpu. Journal of Virology 83: 7536-7546.
51. Iwabu Y, Fujita H, Kinomoto M, Kaneko K, Ishizaka Y, et al. (2009) HIV-1 accessory protein Vpu internalizes cell-surface BST-2/tetherin through transmembrane interactions leading to lysosomes. Journal of Biological Chemistry 284: 35060-35072.
52. Sauter D, Schindler M, Specht A, Landford WN, Münch J, et al. (2009) Tetherin-Driven Adaptation of Vpu and Nef Function and the Evolution of Pandemic and Nonpandemic HIV-1 Strains. Cell Host and Microbe 6: 409-421.
53. Kobayashi T, Ode H, Yoshida T, Sato K, Gee P, et al. (2011) Identification of amino acids in the human tetherin transmembrane domain responsible for HIV-1 Vpu interaction and susceptibility. Journal of Virology 85: 932-945.
54. Tokarev AA, Munguia J, Guatelli JC, (2011) Serine-threonine ubiquitination mediates downregulation of BST-2/tetherin and relief of restricted virion release by HIV-1 Vpu. Journal of Virology 85: 51-63.
55. Gustin JK, Douglas JL, Bai Y, Moses AV, (2012) Ubiquitination of BST-2 Protein by HIV-1 Vpu Protein Does Not Require Lysine, Serine, or Threonine Residues within the BST-2 Cytoplasmic Domain. Journal of Biological Chemistry 287: 14837-14850.