Tetherin restricts productive HIV-1 cell-to-cell transmission

PLoS Pathogens

Volumn 6, Issue 6, 2010, Pages

  Casartelli, Nicoletta ^a   Sourisseau, Marion ^a   Feldmann, Jerome ^a   Guivel Benhassine, Florence ^a   Mallet, Adeline ^b   Marcelin, Anne Geneviève ^c   Guatelli, John ^d   Schwartz, Olivier ^a  

^a CNRS   (France)

^b INSTITUT PASTEUR   (France)

^c SORBONNE UNIVERSITÉ   (France)

^d UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAG PROTEIN; MEMBRANE PROTEIN; NEVIRAPINE; PROTEIN TETHERIN; UNCLASSIFIED DRUG; VPU PROTEIN; BST2 PROTEIN, HUMAN; HUMAN IMMUNODEFICIENCY VIRUS PROTEIN; LEUKOCYTE ANTIGEN; VIRUS PROTEIN; VPU PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS 1;

ARTICLE; CELL TO CELL TRANSMISSION; COCULTURE; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; LYMPHOCYTE; NONHUMAN; SURFACE PROPERTY; VIRION; VIRUS TRANSMISSION; WILD TYPE; CELL COMMUNICATION; CELL CULTURE; CELL FUSION; DISEASE TRANSMISSION; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; METABOLISM; T LYMPHOCYTE; VIRUS REPLICATION; WESTERN BLOTTING;

HUMAN IMMUNODEFICIENCY VIRUS 1;

ANTIGENS, CD; BLOTTING, WESTERN; CELL COMMUNICATION; CELL FUSION; CELLS, CULTURED; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GENE PRODUCTS, GAG; HIV INFECTIONS; HIV-1; HUMAN IMMUNODEFICIENCY VIRUS PROTEINS; HUMANS; MEMBRANE GLYCOPROTEINS; T-LYMPHOCYTES; VIRAL REGULATORY AND ACCESSORY PROTEINS; VIRION; VIRUS REPLICATION;

EID: 77954668607     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000955     Document Type: Article

References (49)

1. Sattentau Q (2008) Avoiding the void: cell-to-cell spread of human viruses. Nat Rev Microbiol 6: 815-826.
2. Chen P, Hubner W, Spinelli MA, Chen BK (2007) Predominant mode of human immunodeficiency virus transfer between T cells is mediated by sustained Env-dependent neutralization-resistant virological synapses. J Virol 81: 12582-12595.
3. Rudnicka D, Feldmann J, Porrot F, Wietgrefe S, Guadagnini S, et al. (2009) Simultaneous cell-to-cell transmission of human immunodeficiency virus to multiple targets through polysynapses. J Virol 83: 6234-6246.
4. Sherer NM, Lehmann MJ, Jimenez-Soto LF, Horensavitz C, Pypaert M, et al. (2007) Retroviruses can establish filopodial bridges for efficient cell-to-cell transmission. Nat Cell Biol 9: 310-315.
5. Sowinski S, Jolly C, Berninghausen O, Purbhoo MA, Chauveau A, et al. (2008) Membrane nanotubes physically connect T cells over long distances presenting a novel route for HIV-1 transmission. Nat Cell Biol 10: 211-219.
6. Pais-Correia AM, Sachse M, Guadagnini S, Robbiati V, Lasserre R, et al. (2009) Biofilm-like extracellular viral assemblies mediate HTLV-1 cell-to-cell transmission at virological synapses. Nat Med.
7. Ruggiero E, Bona R, Muratori C, Federico M (2008) Virological consequences of early events following cell-cell contact between human immunodeficiency virus type 1-infected and uninfected CD4+ cells. J Virol 82: 7773-7789.
8. Hubner W, McNerney GP, Chen P, Dale BM, Gordon RE, et al. (2009) Quantitative 3D video microscopy of HIV transfer across T cell virological synapses. Science 323: 1743-1747.
9. Bosch B, Grigorov B, Senserrich J, Clotet B, Darlix JL, et al. (2008) A clathrin-dynamin-dependent endocytic pathway for the uptake of HIV-1 by direct T cell-T cell transmission. Antiviral Res 80: 185-193.
10. Vendrame D, Sourisseau M, Perrin V, Schwartz O, Mammano F. (2009) Partial Inhibition of HIV Replication by Type-I Interferons: Impact of Cell-to-Cell Viral Transfer. J Virol.
11. Neil SJ, Zang T, Bieniasz PD (2008) Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature 451: 425-430.
12. 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.
13. Jouvenet N, Neil SJ, Zhadina M, Zang T, Kratovac Z, et al. (2009) Broad-spectrum inhibition of retroviral and filoviral particle release by tetherin. J Virol 83: 1837-1844.
14. Sakuma T, Noda T, Urata S, Kawaoka Y, Yasuda J (2009) Inhibition of Lassa and Marburg virus production by tetherin. J Virol 83: 2382-2385.
15. Groom HC, Yap MW, Galao RP, Neil SJ, Bishop KN (2010) Susceptibility of xenotropic murine leukemia virus-related virus (XMRV) to retroviral restriction factors. Proc Natl Acad Sci U S A 107: 5166-5171.
16. Arnaud F, Black S, Murphy L, Griffiths D, Neil SJ, et al. (2010) Interplay Between Ovine Bone Marrow Stromal Cell Antigen 2 (BST2)/Tetherin and Endogenous Retroviruses. J Virol.
17. Mattiuzzo G, Ivol S, Takeuchi Y (2010) Regulation of porcine endogenous retrovirus release by porcine and human tetherins. J Virol 84: 2618-2622.
18. Gupta RK, Hue S, Schaller T, Verschoor E, Pillay D, et al. (2009) Mutation of a single residue renders human tetherin resistant to HIV-1 Vpu-mediated depletion. PLoS Pathog 5: e1000443.
19. Douglas JL, Viswanathan K, McCarroll MN, Gustin JK, Fruh K, et al. (2009) Vpu directs the degradation of the human immunodeficiency virus restriction factor BST-2/Tetherin via a {beta}TrCP-dependent mechanism. J Virol 83: 7931-7947.
20. Mitchell RS, Katsura C, Skasko MA, Fitzpatrick K, Lau D, et al. (2009) Vpu antagonizes BST-2-mediated restriction of HIV-1 release via beta-TrCP and endo-lysosomal trafficking. PLoS Pathog 5: e1000450.
21. Goffinet C, Allespach I, Homann S, Tervo HM, Habermann A, et al. (2009) HIV-1 antagonism of CD317 is species specific and involves Vpu-mediated proteasomal degradation of the restriction factor. Cell Host Microbe 5: 285- 297.
22. 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 Pathog 5: e1000574.
23. 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. J Biol Chem.
24. Gupta RK, Mlcochova P, Pelchen-Matthews A, Petit SJ, Mattiuzzo G, et al. (2009) Simian immunodeficiency virus envelope glycoprotein counteracts tetherin/BST-2/CD317 by intracellular sequestration. Proc Natl Acad Sci U S A.
25. Jia B, Serra-Moreno R, Neidermyer W, Rahmberg A, Mackey J, et al. (2009) Species-specific activity of SIV Nef and HIV-1 Vpu in overcoming restriction by tetherin/BST2. PLoS Pathog 5: e1000429.
26. Lim ES, Emerman M (2009) Simian immunodeficiency virus SIVagm from African green monkeys does not antagonize endogenous levels of african green monkey tetherin/BST-2. J Virol 83: 11673-11681.
27. Zhang F, Wilson SJ, Landford WC, Virgen B, Gregory D, et al. (2009) Nef proteins from simian immunodeficiency viruses are tetherin antagonists. Cell Host Microbe 6: 54-67.
28. Sauter D, Schindler M, Specht A, Landford WN, Munch J, et al. (2009) Tetherin-Driven Adaptation of Vpu and Nef Function and the Evolution of Pandemic and Nonpandemic HIV-1 Strains. Cell Host Microbe 6: 409-421.
29. McNatt MW, Zang T, Hatziioannou T, Bartlett M, Fofana IB, et al. (2009) Species-specific activity of HIV-1 Vpu and positive selection of tetherin transmembrane domain variants. PLoS Pathog 5: e1000300.
30. 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.
31. Fitzpatrick K, Skasko M, Deerinck TJ, Crum J, Ellisman MH, et al. (2010) Direct restriction of virus release and incorporation of the interferon-induced protein BST-2 into HIV-1 particles. PLoS Pathog 6: e1000701.
32. Rollason R, Korolchuk V, Hamilton C, Schu P, Banting G (2007) Clathrin-mediated endocytosis of a lipid-raft-associated protein is mediated through a dual tyrosine motif. J Cell Sci 120: 3850-3858.
33. Rollason R, Korolchuk V, Hamilton C, Jepson M, Banting G (2009) A CD317/ tetherin-RICH2 complex plays a critical role in the organization of the subapical actin cytoskeleton in polarized epithelial cells. J Cell Biol 184: 721-736.
34. Andrew AJ, Miyagi E, Kao S, Strebel K (2009) The formation of cysteine-linked dimers of BST-2/tetherin is important for inhibition of HIV-1 virus release but not for sensitivity to Vpu. Retrovirology 6: 80.
35. Nguyen DH, Hildreth JE (2000) Evidence for budding of human immunodeficiency virus type 1 selectively from glycolipid-enriched membrane lipid rafts. J Virol 74: 3264-3272.
36. Ono A, Freed EO (2001) Plasma membrane rafts play a critical role in HIV-1 assembly and release. Proc Natl Acad Sci U S A 98: 13925-13930.
37. Miyakawa K, Ryo A, Murakami T, Ohba K, Yamaoka S, et al. (2009) BCA2/ Rabring7 promotes tetherin-dependent HIV-1 restriction. PLoS Pathog 5: e1000700.
38. Neil SJ, Eastman SW, Jouvenet N, Bieniasz PD (2006) HIV-1 Vpu promotes release and prevents endocytosis of nascent retrovirus particles from the plasma membrane. PLoS Pathog 2: e39.
39. Sourisseau M, Sol-Foulon N, Porrot F, Blanchet F, Schwartz O (2007) Inefficient human immunodeficiency virus replication in mobile lymphocytes. J Virol 81: 1000-1012.
40. Cavrois M, De Noronha C, Greene WC (2002) A sensitive and specific enzyme-based assay detecting HIV-1 virion fusion in primary T lymphocytes. Nat Biotechnol 20: 1151-1154.
41. Bergeron L, Sullivan N, Sodroski J (1992) Target cell-specific determinants of membrane fusion within the Human Immunodeficiency virus type 1 gp120 third variable region and gp41 amino terminus. J Virol 66: 2389-2397.
42. Nobile C, Petit C, Moris A, Skrabal K, Abastado JP, et al. (2005) Covert human immunodeficiency virus replication in dendritic cells and in DC-SIGN-expressing cells promotes long-term transmission to lymphocytes. J Virol 79: 5386-5399.
43. Puigdomenech I, Massanella M, Cabrera C, Clotet B, Blanco J (2009) On the steps of cell-to-cell HIV transmission between CD4 T cells. Retrovirology 6: 89.
44. Miyauchi K, Kim Y, Latinovic O, Morozov V, Melikyan GB (2009) HIV enters cells via endocytosis and dynamin-dependent fusion with endosomes. Cell 137: 433-444.
45. Gummuluru S, Kinsey CM, Emerman M (2000) An in vitro rapid-turnover assay for human immunodeficiency virus type 1 replication selects for cell-to-cell spread of virus. J Virol 74: 10882-10891.
46. Schubert U, Clouse KA, Strebel K (1995) Augmentation of virus secretion by the human immunodeficiency virus type 1 Vpu protein is cell type independent and occurs in cultured human primary macrophages and lymphocytes. J Virol 69: 7699-7711.
47. Muller B, Daecke J, Fackler OT, Dittmar MT, Zentgraf H, et al. (2004) Construction and characterization of a fluorescently labeled infectious human immunodeficiency virus type 1 derivative. J Virol 78: 10803-10813.
48. Avettand-Fenoel V, Prazuck T, Hocqueloux L, Melard A, Michau C, et al. (2008) HIV-DNA in rectal cells is well correlated with HIV-DNA in blood in different groups of patients, including long-term non-progressors. Aids 22: 1880-1882.
49. Sol-Foulon N, Sourisseau M, Porrot F, Thoulouze MI, Trouillet C, et al. (2007) ZAP-70 kinase regulates HIV cell-to-cell spread and virological synapse formation. Embo J 26: 516-526.