Involvement of a C-terminal motif in the interference of primate lentiviral Vpu proteins with CD1d-mediated antigen presentation

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Bächle, Susanna M ^a   Sauter, Daniel ^b   Sibitz, Sabrina ^a   Sandberg, Johan K ^a   Kirchhoff, Frank ^b   Moll, Markus ^a  

^a KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^b UNIVERSITY OF ULM   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CD1D ANTIGEN; HUMAN IMMUNODEFICIENCY VIRUS PROTEIN; VIRAL PROTEIN; VPU PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS 1;

AMINO ACID SEQUENCE; ANIMAL; ANTIGEN PRESENTATION; CELL LINE; CHEMISTRY; CONSERVED SEQUENCE; DOWN REGULATION; GENE EXPRESSION; GENETICS; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; MOLECULAR GENETICS; MUTATION; NATURAL KILLER T CELL; POSITION WEIGHT MATRIX; PROTEIN DOMAIN; PROTEIN MOTIF;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; ANTIGEN PRESENTATION; ANTIGENS, CD1D; CELL LINE; CONSERVED SEQUENCE; DOWN-REGULATION; GENE EXPRESSION; HIV-1; HUMAN IMMUNODEFICIENCY VIRUS PROTEINS; HUMANS; LENTIVIRUSES, PRIMATE; LYMPHOCYTE ACTIVATION; MOLECULAR SEQUENCE DATA; MUTATION; NATURAL KILLER T-CELLS; POSITION-SPECIFIC SCORING MATRICES; PROTEIN INTERACTION DOMAINS AND MOTIFS; VIRAL REGULATORY AND ACCESSORY PROTEINS;

EID: 84928138658     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep09675     Document Type: Article

References (58)

1. Jost, S. & Altfeld, M. Control of human viral infections by natural killer cells. Annu Rev Immunol 31, 163-194 (2013).
2. Juno, J. A., Keynan, Y. & Fowke, K. R. Invariant NKT cells: regulation and function during viral infection. PLoS Pathog 8, e1002838 (2012).
3. Sandberg, J. K., Andersson, S. K., Bachle, S. M., Nixon, D. F. & Moll, M. HIV-1 Vpu interference with innate cell-mediated immune mechanisms. Curr HIV Res 10, 327-333 (2012).
4. Neil, S. J., Zang, T. & Bieniasz, P. D. Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature 451, 425-430 (2008).
5. Van Damme, N. et al. 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 (2008).
6. Willey, R. L., Maldarelli, F., Martin, M. A. & Strebel, K. Human immunodeficiency virus type 1 Vpu protein induces rapid degradation of CD4. J Virol 66, 7193-7200 (1992).
7. Matusali, G., Potesta, M., Santoni, A., Cerboni, C. & Doria, M. The human immunodeficiency virus type 1 Nef and Vpu proteins downregulate the natural killer cell-activating ligand PVR. J Virol 86, 4496-4504 (2012).
8. Shah, A. H. et al. 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 (2010).
9. Chen, N. et al. HIV-1 down-regulates the expression of CD1d via Nef. Eur J Immunol 36, 278-286 (2006).
10. Moll, M., Andersson, S. K., Smed-Sorensen, A. & Sandberg, J. K. Inhibition of lipid antigen presentation in dendritic cells by HIV-1 Vpu interference with CD1d recycling from endosomal compartments. Blood 116, 1876-1884 (2010).
11. Brigl, M., Bry, L., Kent, S. C., Gumperz, J. E. & Brenner, M. B. Mechanism of CD1d-restricted natural killer T cell activation during microbial infection. Nat Immunol 4, 1230-1237 (2003).
12. Spada, F. M. et al. Low expression level but potent antigen presenting function of CD1d on monocyte lineage cells. Eur J Immunol 30, 3468-3477 (2000).
13. Brennan, P. J. et al. Invariant natural killer T cells recognize lipid self antigen induced by microbial danger signals. Nat Immunol 12, 1202-1211 (2011).
14. Zeissig, S. et al. Hepatitis B virus-induced lipid alterations contribute to natural killer T cell-dependent protective immunity. Nat Med 18, 1060-1068 (2012).
15. Brugger, B. et al. Human immunodeficiency virus type 1 Nef protein modulates the lipid composition of virions and host cell membrane microdomains. Retrovirology 4, 70 (2007).
16. Dube, M., Bego, M. G., Paquay, C. & Cohen, E. A. Modulation of HIV-1-host interaction: role of the Vpu accessory protein. Retrovirology 7, 114 (2010).
17. Schubert, U. et al. The two biological activities of human immunodeficiency virus type 1 Vpu protein involve two separable structural domains. J Virol 70, 809-819 (1996).
18. Paul, M. & Jabbar, M. A. Phosphorylation of both phosphoacceptor sites in the HIV-1 Vpu cytoplasmic domain is essential for Vpu-mediated ER degradation of CD4. Virology 232, 207-216 (1997).
19. Sauter, D. et al. Human tetherin exerts strong selection pressure on the HIV-1 group N Vpu protein. PLoS Pathog 8, e1003093 (2012).
20. Sharp, P. M. & Hahn, B. H. The evolution of HIV-1 and the origin of AIDS. Philos Trans R Soc Lond B Biol Sci 365, 2487-2494 (2010).
21. Sauter, D. et al. HIV-1 Group P is unable to antagonize human tetherin by Vpu, Env or Nef. Retrovirology 8, 103 (2011).
22. Sauter, D. et al. Tetherin-driven adaptation of Vpu and Nef function and the evolution of pandemic and nonpandemic HIV-1 strains. Cell Host Microbe 6, 409-421 (2009).
23. Bricard, G. et al. Alpha-galactosylceramide analogs with weak agonist activity for human iNKT cells define new candidate anti-inflammatory agents. PLoS One 5, e14374 (2010).
24. Bolduan, S. et al. HIV-1 Vpu affects the anterograde transport and the glycosylation pattern of NTB-A. Virology 440, 190-203 (2013).
25. Hill, M. S., Ruiz, A., Schmitt, K. & Stephens, E. B. 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 (2010).
26. Kueck, T. & Neil, S. J. A cytoplasmic tail determinant in HIV-1 Vpu mediates targeting of tetherin for endosomal degradation and counteracts interferon-induced restriction. PLoS Pathog 8, e1002609 (2012).
27. Pacyniak, E. et al. Identification of a region within the cytoplasmic domain of the subtype B Vpu protein of human immunodeficiency virus type 1 (HIV-1) that is responsible for retention in the golgi complex and its absence in the Vpu protein from a subtype C HIV-1. AIDS Res Hum Retroviruses 21, 379-394 (2005).
28. Jia, X. et al. Structural basis of HIV-1 Vpu-mediated BST2 antagonism via hijacking of the clathrin adaptor protein complex 1. Elife 3, e02362 (2014).
29. Bell, C. M. et al. Molecular characterization of the HIV type 1 subtype C accessory genes vif, vpr, and vpu. AIDS Res Hum Retroviruses 23, 322-330 (2007).
30. McCormick-Davis, C., Dalton, S. B., Singh, D. K. & Stephens, E. B. Comparison of Vpu sequences from diverse geographical isolates of HIV type 1 identifies the presence of highly variable domains, additional invariant amino acids, and a signature sequence motif common to subtype C isolates. AIDS Res Hum Retroviruses 16, 1089-1095 (2000).
31. Leonard, J. A., Filzen, T., Carter, C. C., Schaefer, M. & Collins, K. L. HIV-1 Nef disrupts intracellular trafficking of major histocompatibility complex class I, CD4, CD8, and CD28 by distinct pathways that share common elements. J Virol 85, 6867-6881 (2011).
32. Douglas, J. L., Bai, Y., Gustin, J. K. & Moses, A. V. A comparative mutational analysis of HIV-1 Vpu subtypes B and C for the identification of determinants required to counteract BST-2/Tetherin and enhance viral egress. Virology 441, 182-196 (2013).
33. Ruiz, A., Hill, M. S., Schmitt, K., Guatelli, J. & Stephens, E. B. 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 (2008).
34. Kirchhoff, F. Immune evasion and counteraction of restriction factors by HIV-1 and other primate lentiviruses. Cell Host Microbe 8, 55-67 (2010).
35. Lawson, V. Turned on by danger: activation of CD1d-restricted invariant natural killer T cells. Immunology 137, 20-27 (2012).
36. Snyder-Cappione, J. E. et al. A comprehensive ex vivo functional analysis of human NKT cells reveals production of MIP1-alpha and MIP1-beta, a lack of IL-17, and a Th1-bias in males. PLoS One 5, e15412 (2010).
37. Aldrovandi, G. M. & Zack, J. A. Replication and pathogenicity of human immunodeficiency virus type 1 accessory gene mutants in SCID-hu mice. J Virol 70, 1505-1511 (1996).
38. Dave, V. P., Hajjar, F., Dieng, M. M., Haddad, E. & Cohen, E. A. Efficient BST2 antagonism by Vpu is critical for early HIV-1 dissemination in humanized mice. Retrovirology 10, 128 (2013).
39. Sato, K. et al. Vpu augments the initial burst phase of HIV-1 propagation and downregulates BST2 and CD4 in humanized mice. J Virol 86, 5000-5013 (2012).
40. Hill, M. S. et al.Modulation of the severe CD41 T-cell loss caused by a pathogenic simian-human immunodeficiency virus by replacement of the subtype B vpu with the vpu from a subtype C HIV-1 clinical isolate. Virology 371, 86-97 (2008).
41. Ruiz, A., Schmitt, K., Culley, N. & Stephens, E. B. Simian-Human immunodeficiency viruses expressing chimeric subtype B/C Vpu proteins demonstrate the importance of the amino terminal and transmembrane domains in the rate of CD4(1) T cell loss in macaques. Virology 435, 395-405 (2013).
42. Mann, J. K. et al. Ability of HIV-1 Nef to downregulate CD4 and HLA class I differs among viral subtypes. Retrovirology 10, 100 (2013).
43. Abraha, A. et al. CCR5- and CXCR4-tropic subtype C human immunodeficiency virus type 1 isolates have a lower level of pathogenic fitness than other dominant group M subtypes: implications for the epidemic. J Virol 83, 5592-5605 (2009).
44. Arien, K. K. et al. The replicative fitness of primary human immunodeficiency virus type 1 (HIV-1) group M, HIV-1 group O, and HIV-2 isolates. J Virol 79, 8979-8990 (2005).
45. Ball, S. C. et al. Comparing the ex vivo fitness of CCR5-tropic human immunodeficiency virus type 1 isolates of subtypes B and C. J Virol 77, 1021-1038 (2003).
46. Dube, M. et al. Antagonism of tetherin restriction of HIV-1 release by Vpu involves binding and sequestration of the restriction factor in a perinuclear compartment. PLoS Pathog 6, e1000856 (2010).
47. Collins, D. R. & Collins, K. L. HIV-1 Accessory Proteins Adapt Cellular Adaptors to Facilitate Immune Evasion. PLoS Pathog 10, e1003851 (2014).
48. Tokarev, A. & Guatelli, J. Misdirection of membrane trafficking by HIV-1 Vpu and Nef: Keys to viral virulence and persistence. Cell Logist 1, 90-102 (2011).
49. Dube, M. et al. Suppression of Tetherin-restricting activity upon human immunodeficiency virus type 1 particle release correlates with localization of Vpu in the trans-Golgi network. J Virol 83, 4574-4590 (2009).
50. Jafari, M., Guatelli, J. & Lewinski, M. K. Activities of Transmitted/Founder and Chronic Clade B HIV-1 Vpu and a C-terminal Polymorphism Specifically Affecting Virion Release. J Virol 88, 5062-5078 (2014).
51. Singh, S. K. et al. Mapping the interaction between the cytoplasmic domains of HIV-1 viral protein U and human CD4 with NMR spectroscopy. FEBS J 279, 3705-3714 (2012).
52. Wittlich, M., Koenig, B. W., Stoldt, M., Schmidt, H. & Willbold, D. NMR structural characterization of HIV-1 virus protein U cytoplasmic domain in the presence of dodecylphosphatidylcholine micelles. FEBS J 276, 6560-6575 (2009).
53. Leeansyah, E. et al. Activation, exhaustion, and persistent decline of the antimicrobial MR1-restricted MAIT-cell population in chronic HIV-1 infection. Blood 121, 1124-1135 (2013).
54. Andersson, S. K., Paquin-Proulx, D., Kroll, M., Sandberg, J. K. & Moll, M. Technical advance. Measurement of iNKT cell responses at the single-cell level against rare HIV-1-infected dendritic cells in a mixed culture. J Leukoc Biol 93, 449-455 (2013).
55. Smed-Sorensen, A. et al. IgG regulates the CD1 expression profile and lipid antigen-presenting function in human dendritic cells via FcgammaRIIa. Blood 111, 5037-5046 (2008).
56. Waterhouse, A. M., Procter, J. B., Martin, D. M., Clamp, M. & Barton, G. J. Jalview Version 2 - a multiple sequence alignment editor and analysis workbench. Bioinformatics 25, 1189-1191 (2009).
57. Crooks, G. E., Hon, G., Chandonia, J. M. & Brenner, S. E. WebLogo: a sequence logo generator. Genome Res 14, 1188-1190 (2004).
58. Schneider, T. D. & Stephens, R. M. Sequence logos: a new way to display consensus sequences. Nucleic Acids Res 18, 6097-6100 (1990).