The molecular basis of HIV entry

Cellular Microbiology

Volumn 14, Issue 8, 2012, Pages 1183-1192

  Klasse, Per Johan ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; CAVEOLIN; CD4 ANTIGEN; CHEMOKINE RECEPTOR CCR5; CHEMOKINE RECEPTOR CXCR4; CLATHRIN; EPIDERMAL GROWTH FACTOR RECEPTOR; EPITOPE; GAG PROTEIN; GLYCOPROTEIN GP 120; GLYCOPROTEIN GP 160; GLYCOPROTEIN GP 41; HUMAN IMMUNODEFICIENCY VIRUS FUSION INHIBITOR; HYBRID PROTEIN; INTERCELLULAR ADHESION MOLECULE 1; LIGAND; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; MANNOSE; MEMBRANE PHOSPHOLIPID; NEUTRALIZING ANTIBODY; PROTEINASE; T LYMPHOCYTE RECEPTOR; TYROSINE;

CELL COMPARTMENTALIZATION; CELL HETEROGENEITY; DENDRITIC CELL; DEPOLYMERIZATION; ELECTRON TOMOGRAPHY; ENDOCYTOSIS; ENZYME INHIBITION; GLYCOSYLATION; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; LYMPHOCYTE; MACROPHAGE; MOLECULAR BIOLOGY; NONHUMAN; PINOCYTOSIS; PREVALENCE; PRIORITY JOURNAL; PROTEIN DEGRADATION; REVIEW; STOICHIOMETRY; SYNAPSE; T LYMPHOCYTE; VACCINATION; VIRAL GENE DELIVERY SYSTEM; VIRION; VIRUS CORE; VIRUS ENTRY; VIRUS GENOME; VIRUS REPLICATION; VIRUS TRANSMISSION;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; HIV; HIV INFECTIONS; HOST-PATHOGEN INTERACTIONS; HUMAN IMMUNODEFICIENCY VIRUS PROTEINS; HUMANS; MEMBRANE FUSION; VIRION; VIRUS ATTACHMENT; VIRUS INTERNALIZATION;

EID: 84864001990     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2012.01812.x     Document Type: Review

References (61)

1. Abela, I.A., Berlinger, L., Schanz, M., Reynell, L., Gunthard, H.F., Rusert, P., and Trkola, A. (2012) Cell-cell transmission enables HIV-1 to evade inhibition by potent CD4bs directed antibodies. PLoS Pathog 8: e1002634.
2. Alkhatib, G., Combadiere, C., Broder, C.C., Feng, Y., Kennedy, P.E., Murphy, P.M., and Berger, E.A. (1996) CC CKR5: a RANTES, MIP-1alpha, MIP-1beta receptor as a fusion cofactor for macrophage-tropic HIV-1. Science 272: 1955-1958.
3. Anastassopoulou, C.G., Ketas, T.J., Klasse, P.J., and Moore, J.P. (2009) Resistance to CCR5 inhibitors caused by sequence changes in the fusion peptide of HIV-1 gp41. Proc Natl Acad Sci USA 106: 5318-5323.
4. Baribaud, F., Edwards, T.G., Sharron, M., Brelot, A., Heveker, N., Price, K., etal. (2001) Antigenically distinct conformations of CXCR4. J Virol 75: 8957-8967.
5. Berro, R., Sanders, R.W., Lu, M., Klasse, P.J., and Moore, J.P. (2009) Two HIV-1 variants resistant to small molecule CCR5 inhibitors differ in how they use CCR5 for entry. PLoS Pathog 5: e1000548.
6. Berro, R., Klasse, P.J., Lascano, D., Flegler, A., Nagashima, K.A., Sanders, R.W., etal. (2011) Multiple CCR5 conformations on the cell surface are used differentially by human immunodeficiency viruses resistant or sensitive to CCR5 inhibitors. J Virol 85: 8227-8240.
7. Bhakta, S.J., Shang, L., Prince, J.L., Claiborne, D.T., and Hunter, E. (2011) Mutagenesis of tyrosine and di-leucine motifs in the HIV-1 envelope cytoplasmic domain results in a loss of Env-mediated fusion and infectivity. Retrovirology 8: 37.
8. Carter, G.C., Bernstone, L., Baskaran, D., and James, W. (2011) HIV-1 infects macrophages by exploiting an endocytic route dependent on dynamin, Rac1 and Pak1. Virology 409: 234-250.
9. Daecke, J., Fackler, O.T., Dittmar, M.T., and Krausslich, H.G. (2005) Involvement of clathrin-mediated endocytosis in human immunodeficiency virus type 1 entry. J Virol 79: 1581-1594.
10. Dale, B.M., McNerney, G.P., Thompson, D.L., Hubner, W., de Los Reyes, K., Chuang, F.Y., etal. (2011) Cell-to-cell transfer of HIV-1 via virological synapses leads to endosomal virion maturation that activates viral membrane fusion. Cell Host Microbe 10: 551-562.
11. Davis, M.R., Jiang, J., Zhou, J., Freed, E.O., and Aiken, C. (2006) A mutation in the human immunodeficiency virus type 1 Gag protein destabilizes the interaction of the envelope protein subunits gp120 and gp41. J Virol 80: 2405-2417.
12. Farzan, M., Mirzabekov, T., Kolchinsky, P., Wyatt, R., Cayabyab, M., Gerard, N.P., etal. (1999) Tyrosine sulfation of the amino terminus of CCR5 facilitates HIV-1 entry. Cell 96: 667-676.
13. Feldmann, J., and Schwartz, O. (2010) HIV-1 virological synapse: live imaging of transmission. Viruses 2: 1666-1680.
14. Geijtenbeek, T.B., Torensma, R., van Vliet, S.J., van Duijnhoven, G.C., Adema, G.J., van Kooyk, Y., and Figdor, C.G. (2000) Identification of DC-SIGN, a novel dendritic cell-specific ICAM-3 receptor that supports primary immune responses. Cell 100: 575-585.
15. Grewe, C., Beck, A., and Gelderblom, H.R. (1990) HIV: early virus-cell interactions. J Acquir Immune Defic Syndr 3: 965-974.
16. Grivel, J.C., Shattock, R.J., and Margolis, L.B. (2011) Selective transmission of R5 HIV-1 variants: where is the gatekeeper? J Transl Med 9 (Suppl. 1): S6.
17. Grove, J., and Marsh, M. (2011) The cell biology of receptor-mediated virus entry. J Cell Biol 195: 1071-1082.
18. Gustchina, E., Li, M., Louis, J.M., Anderson, D.E., Lloyd, J., Frisch, C., etal. (2010) Structural basis of HIV-1 neutralization by affinity matured Fabs directed against the internal trimeric coiled-coil of gp41. PLoS Pathog 6: e1001182.
19. Haase, A.T. (2010) Targeting early infection to prevent HIV-1 mucosal transmission. Nature 464: 217-223.
20. Hartley, O., Klasse, P.J., Sattentau, Q.J., and Moore, J.P. (2005) V3: HIV's switch-hitter. AIDS Res Hum Retroviruses 21: 171-189.
21. Huang, C.C., Tang, M., Zhang, M.Y., Majeed, S., Montabana, E., Stanfield, R.L., etal. (2005) Structure of a V3-containing HIV-1 gp120 core. Science 310: 1025-1028.
22. Jiang, J., and Aiken, C. (2006) Maturation of the viral core enhances the fusion of HIV-1 particles with primary human T cells and monocyte-derived macrophages. Virology 346: 460-468.
23. Ketas, T.J., Holuigue, S., Matthews, K., Moore, J.P., and Klasse, P.J. (2012) Env-glycoprotein heterogeneity as a source of apparent synergy and enhanced cooperativity in inhibition of HIV-1 infection by neutralizing antibodies and entry inhibitors. Virology 422: 22-36.
24. Klasse, P.J. (2007) Modeling how many envelope glycoprotein trimers per virion participate in human immunodeficiency virus infectivity and its neutralization by antibody. Virology 369: 245-262.
25. Klasse, P.J., and Moore, J.P. (1996) Quantitative model of antibody- and soluble CD4-mediated neutralization of primary isolates and T-cell line-adapted strains of human immunodeficiency virus type 1. J Virol 70: 3668-3677.
26. Klasse, P.J., and Sattentau, Q.J. (2002) Occupancy and mechanism in antibody-mediated neutralization of animal viruses. J Gen Virol 83: 2091-2108.
27. Klasse, P.J., Shattock, R., and Moore, J.P. (2008) Antiretroviral drug-based microbicides to prevent HIV-1 sexual transmission. Annu Rev Med 59: 455-471.
28. von Kleist, L., Stahlschmidt, W., Bulut, H., Gromova, K., Puchkov, D., Robertson, M.J., etal. (2011) Role of the clathrin terminal domain in regulating coated pit dynamics revealed by small molecule inhibition. Cell 146: 471-484.
29. Kwong, P.D., Doyle, M.L., Casper, D.J., Cicala, C., Leavitt, S.A., Majeed, S., etal. (2002) HIV-1 evades antibody-mediated neutralization through conformational masking of receptor-binding sites. Nature 420: 678-682.
30. Leaman, D.P., Kinkead, H., and Zwick, M.B. (2010) In-solution virus capture assay helps deconstruct heterogeneous antibody recognition of human immunodeficiency virus type 1. J Virol 84: 3382-3395.
31. Lee, B., Sharron, M., Blanpain, C., Doranz, B.J., Vakili, J., Setoh, P., etal. (1999) Epitope mapping of CCR5 reveals multiple conformational states and distinct but overlapping structures involved in chemokine and coreceptor function. J Biol Chem 274: 9617-9626.
32. Liu, J., Bartesaghi, A., Borgnia, M.J., Sapiro, G., and Subramaniam, S. (2008) Molecular architecture of native HIV-1 gp120 trimers. Nature 455: 109-113.
33. McClure, M.O., Marsh, M., and Weiss, R.A. (1988) Human immunodeficiency virus infection of CD4-bearing cells occurs by a pH-independent mechanism. EMBO J 7: 513-518.
34. Maddon, P.J., McDougal, J.S., Clapham, P.R., Dalgleish, A.G., Jamal, S., Weiss, R.A., and Axel, R. (1988) HIV infection does not require endocytosis of its receptor, CD4. Cell 54: 865-874.
35. Magnus, C., and Regoes, R.R. (2012) Analysis of the subunit stoichiometries in viral entry. PLoS ONE 7: e33441.
36. Magnus, C., Rusert, P., Bonhoeffer, S., Trkola, A., and Regoes, R.R. (2009) Estimating the stoichiometry of human immunodeficiency virus entry. J Virol 83: 1523-1531.
37. Marechal, V., Clavel, F., Heard, J.M., and Schwartz, O. (1998) Cytosolic Gag p24 as an index of productive entry of human immunodeficiency virus type 1. J Virol 72: 2208-2212.
38. Marechal, V., Prevost, M.C., Petit, C., Perret, E., Heard, J.M., and Schwartz, O. (2001) Human immunodeficiency virus type 1 entry into macrophages mediated by macropinocytosis. J Virol 75: 11166-11177.
39. Martin, N., Welsch, S., Jolly, C., Briggs, J.A., Vaux, D., and Sattentau, Q.J. (2010) Virological synapse-mediated spread of human immunodeficiency virus type 1 between T cells is sensitive to entry inhibition. J Virol 84: 3516-3527.
40. Melikyan, G.B. (2008) Common principles and intermediates of viral protein-mediated fusion: the HIV-1 paradigm. Retrovirology 5: 111.
41. Miyauchi, K., Kim, Y., Latinovic, O., Morozov, V., and Melikyan, G.B. (2009) HIV enters cells via endocytosis and dynamin-dependent fusion with endosomes. Cell 137: 433-444.
42. Moore, J.P., and Doms, R.W. (2003) The entry of entry inhibitors: a fusion of science and medicine. Proc Natl Acad Sci USA 100: 10598-10602.
43. Moore, P.L., Crooks, E.T., Porter, L., Zhu, P., Cayanan, C.S., Grise, H., etal. (2006) Nature of nonfunctional envelope proteins on the surface of human immunodeficiency virus type 1. J Virol 80: 2515-2528.
44. Munoz-Barroso, I., Salzwedel, K., Hunter, E., and Blumenthal, R. (1999) Role of the membrane-proximal domain in the initial stages of human immunodeficiency virus type 1 envelope glycoprotein-mediated membrane fusion. J Virol 73: 6089-6092.
45. Pauza, C.D., and Price, T.M. (1988) Human immunodeficiency virus infection of T cells and monocytes proceeds via receptor-mediated endocytosis. J Cell Biol 107: 959-968.
46. Pejchal, R., and Wilson, I.A. (2010) Structure-based vaccine design in HIV: blind men and the elephant? Curr Pharm Des 16: 3744-3753.
47. Pelchen-Matthews, A., Clapham, P., and Marsh, M. (1995) Role of CD4 endocytosis in human immunodeficiency virus infection. J Virol 69: 8164-8168.
48. Piguet, V., and Sattentau, Q. (2004) Dangerous liaisons at the virological synapse. J Clin Invest 114: 605-610.
49. Platt, E.J., Durnin, J.P., Shinde, U., and Kabat, D. (2007) An allosteric rheostat in HIV-1 gp120 reduces CCR5 stoichiometry required for membrane fusion and overcomes diverse entry limitations. J Mol Biol 374: 64-79.
50. Poignard, P., Moulard, M., Golez, E., Vivona, V., Franti, M., Venturini, S., etal. (2003) Heterogeneity of envelope molecules expressed on primary human immunodeficiency virus type 1 particles as probed by the binding of neutralizing and nonneutralizing antibodies. J Virol 77: 353-365.
51. Sabin, C., Corti, D., Buzon, V., Seaman, M.S., Lutje Hulsik, D., Hinz, A., etal. (2010) Crystal structure and size-dependent neutralization properties of HK20, a human monoclonal antibody binding to the highly conserved heptad repeat 1 of gp41. PLoS Pathog 6: e1001195.
52. Sattentau, Q.J., and Weiss, R.A. (1988) The CD4 antigen: physiological ligand and HIV receptor. Cell 52: 631-633.
53. Schaeffer, E., Soros, V.B., and Greene, W.C. (2004) Compensatory link between fusion and endocytosis of human immunodeficiency virus type 1 in human CD4 T lymphocytes. J Virol 78: 1375-1383.
54. Seibert, C., Cadene, M., Sanfiz, A., Chait, B.T., and Sakmar, T.P. (2002) Tyrosine sulfation of CCR5 N-terminal peptide by tyrosylprotein sulfotransferases 1 and 2 follows a discrete pattern and temporal sequence. Proc Natl Acad Sci USA 99: 11031-11036.
55. Sougrat, R., Bartesaghi, A., Lifson, J.D., Bennett, A.E., Bess, J.W., Zabransky, D.J., and Subramaniam, S. (2007) Electron tomography of the contact between T cells and SIV/HIV-1: implications for viral entry. PLoS Pathog 3: e63.
56. Stein, B.S., Gowda, S.D., Lifson, J.D., Penhallow, R.C., Bensch, K.G., and Engleman, E.G. (1987) pH-independent HIV entry into CD4-positive T cells via virus envelope fusion to the plasma membrane. Cell 49: 659-668.
57. Ugolini, S., Mondor, I., Parren, P.W., Burton, D.R., Tilley, S.A., Klasse, P.J., and Sattentau, Q.J. (1997) Inhibition of virus attachment to CD4+ target cells is a major mechanism of T cell line-adapted HIV-1 neutralization. J Exp Med 186: 1287-1298.
58. de la Vega, M., Marin, M., Kondo, N., Miyauchi, K., Kim, Y., Epand, R.F., etal. (2011) Inhibition of HIV-1 endocytosis allows lipid mixing at the plasma membrane, but not complete fusion. Retrovirology 8: 99.
59. Yamamoto, T., Tsunetsugu-Yokota, Y., Mitsuki, Y.Y., Mizukoshi, F., Tsuchiya, T., Terahara, K., etal. (2009) Selective transmission of R5 HIV-1 over X4 HIV-1 at the dendritic cell-T cell infectious synapse is determined by the T cell activation state. PLoS Pathog 5: e1000279.
60. Yang, X., Kurteva, S., Ren, X., Lee, S., and Sodroski, J. (2005) Stoichiometry of envelope glycoprotein trimers in the entry of human immunodeficiency virus type 1. J Virol 79: 12132-12147.
61. Yang, X., Kurteva, S., Ren, X., Lee, S., and Sodroski, J. (2006) Subunit stoichiometry of human immunodeficiency virus type 1 envelope glycoprotein trimers during virus entry into host cells. J Virol 80: 4388-4395.