Real-time analysis of human immunodeficiency virus type 1 Env-mediated membrane fusion by fluorescence resonance energy transfer

Microbes and Infection

Volumn 8, Issue 2, 2006, Pages 520-532

  Furuta, Rika A ^a   Nishikawa, Masao ^a   Fujisawa, Jun Ichi ^a  

^a KANSAI MEDICAL UNIVERSITY   (Japan)

Author keywords

FRET; HIV 1; Membrane fusion; Real time imaging

Indexed keywords

CD4 ANTIGEN; CHEMOKINE RECEPTOR ANTAGONIST; CHEMOKINE RECEPTOR CCR5; CYAN FLUORESCENT PROTEIN; ENFUVIRTIDE; GLYCOPROTEIN GP 120; GLYCOPROTEIN GP 41; HYBRID PROTEIN; N [4 [[[6,7 DIHYDRO 2 (4 METHYLPHENYL) 5H BENZOCYCLOHEPTEN 8 YL]CARBONYL]AMINO]BENZYL] N,N DIMETHYL 2H TETRAHYDROPYRAN 4 AMINIUM CHLORIDE; RECOMBINANT PROTEIN; VIRUS ENVELOPE PROTEIN; VIRUS RECEPTOR; YELLOW FLUORESCENT PROTEIN;

ARTICLE; CELL FUSION; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; CYTOPLASM; EMBRYO; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; MEMBRANE FUSION; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; RECEPTOR UPREGULATION; VIRUS ENVELOPE;

ANTIGENS, CD4; BACTERIAL PROTEINS; CELL FUSION; CELL LINE; FLUORESCENCE RESONANCE ENERGY TRANSFER; FLUORESCENT DYES; GENE PRODUCTS, ENV; GREEN FLUORESCENT PROTEINS; HIV-1; HUMANS; LUMINESCENT PROTEINS; MEMBRANE FUSION; MICROSCOPY, CONFOCAL; RECEPTORS, CCR5; RECOMBINANT FUSION PROTEINS;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 32244442746     PISSN: 12864579     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.micinf.2005.08.004     Document Type: Article

References (69)

1. M. Kowalski, J. Potz, L. Basiripour, T. Dorfman, W.C. Goh, E. Terwilliger, A. Dayton, C. Rosen, W. Haseltine, and J. Sodroski Functional regions of the envelope glycoprotein of human immunodeficiency virus type 1 Science 237 1987 1351 1355
2. G. Alkhatib, C. Combadiere, C.C. Broder, Y. Feng, P.E. Kennedy, P.M. Murphy, and E.A. Berger CC CKR5: a RANTES, MIP-1alpha, MIP-1beta receptor as a fusion cofactor for macrophage-tropic HIV-1 Science 272 1996 1955 1958
3. H. Choe, M. Farzan, Y. Sun, N. Sullivan, B. Rollins, P.D. Ponath, L. Wu, C.R. Mackay, G. LaRosa, W. Newman, N. Gerard, C. Gerard, and J. Sodroski The beta-chemokine receptors CCR3 and CCR5 facilitate infection by primary HIV-1 isolates Cell 85 1996 1135 1148
4. H. Deng, R. Liu, W. Ellmeier, S. Choe, D. Unutmaz, M. Burkhart, P. Di Marzio, S. Marmon, R.E. Sutton, C.M. Hill, C.B. Davis, S.C. Peiper, T.J. Schall, D.R. Littman, and N.R. Landau Identification of a major co-receptor for primary isolates of HIV-1 Nature 381 1996 661 666
5. T. Dragic, V. Litwin, G.P. Allaway, S.R. Martin, Y. Huang, K.A. Nagashima, C. Cayanan, P.J. Maddon, R.A. Koup, J.P. Moore, and W.A. Paxton HIV-1 entry into CD4+ cells is mediated by the chemokine receptor CC-CKR-5 Nature 381 1996 667 673
6. Y. Feng, C.C. Broder, P.E. Kennedy, and E.A. Berger HIV-1 entry cofactor: functional cDNA cloning of a seven-transmembrane, G protein-coupled receptor Science 272 1996 872 877
7. D.C. Chan, and P.S. Kim HIV entry and its inhibition Cell 93 1998 681 684
8. W. Weissenhorn, A. Dessen, S.C. Harrison, J.J. Skehel, and D.C. Wiley Atomic structure of the ectodomain from HIV-1 gp41 Nature 387 1997 426 430
9. K. Tan, J. Liu, J. Wang, S. Shen, and M. Lu Atomic structure of a thermostable subdomain of HIV-1 gp41 Proc. Natl. Acad. Sci. USA 94 1997 12303 12308
10. S. Frey, M. Marsh, S. Gunther, A. Pelchen-Matthews, P. Stephens, S. Ortlepp, and T. Stegmann Temperature dependence of cell-cell fusion induced by the envelope glycoprotein of human immunodeficiency virus type 1 J. Virol. 69 1995 1462 1472
11. S. Genoud, F. Kajumo, Y. Guo, D. Thompson, and T. Dragic CCR5-Mediated human immunodeficiency virus entry depends on an amino-terminal gp120-binding site and on the conformational integrity of all four extracellular domains J. Virol. 73 1999 1645 1648
12. S.P. Layne, M.J. Merges, M. Dembo, J.L. Spouge, and P.L. Nara HIV requires multiple gp120 molecules for CD4-mediated infection Nature 346 1990 277 279
13. P.D. Kwong, R. Wyatt, J. Robinson, R.W. Sweet, J. Sodroski, and W.A. Hendrickson Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human antibody Nature 393 1998 648 659
14. D.C. Chan, D. Fass, J.M. Berger, and P.S. Kim Core structure of gp41 from the HIV envelope glycoprotein Cell 89 1997 263 273
15. C.K. Lapham, J. Ouyang, B. Chandrasekhar, N.Y. Nguyen, D.S. Dimitrov, and H. Golding Evidence for cell-surface association between fusin and the CD4-gp120 complex in human cell lines Science 274 1996 602 605
16. R.A. Furuta, C.T. Wild, Y. Weng, and C.D. Weiss Capture of an early fusion-active conformation of HIV-1 gp41 Nat. Struct. Biol. 5 1998 276 279
17. Q.J. Sattentau, and J.P. Moore Conformational changes induced in the human immunodeficiency virus envelope glycoprotein by soluble CD4 binding J. Exp. Med. 174 1991 407 415
18. Q.J. Sattentau, J.P. Moore, F. Vignaux, F. Traincard, and P. Poignard Conformational changes induced in the envelope glycoproteins of the human and simian immunodeficiency viruses by soluble receptor binding J. Virol. 67 1993 7383 7393
19. L. Wu, N.P. Gerard, R. Wyatt, H. Choe, C. Parolin, N. Ruffing, A. Borsetti, A.A. Cardoso, E. Desjardin, W. Newman, C. Gerard, and J. Sodroski CD4-induced interaction of primary HIV-1 gp120 glycoproteins with the chemokine receptor CCR-5 Nature 384 1996 179 183
20. Y. He, R. Vassell, M. Zaitseva, N. Nguyen, Z. Yang, Y. Weng, and C.D. Weiss Peptides trap the human immunodeficiency virus type 1 envelope glycoprotein fusion intermediate at two sites J. Virol. 77 2003 1666 1671
21. J. Bentz, and A. Mittal Architecture of the influenza hemagglutinin membrane fusion site Biochim. Biophys. Acta 1614 2003 24 35
22. M. Greenberg, N. Cammack, M. Salgo, and L. Smiley HIV fusion and its inhibition in antiretroviral therapy Rev. Med. Virol. 14 2004 321 337
23. R.M. Clegg, A.I. Murchie, A. Zechel, C. Carlberg, S. Diekmann, and D.M. Lilley Fluorescence resonance energy transfer analysis of the structure of the four-way DNA junction Biochemistry 31 1992 4846 4856
24. R.M. Clegg Fluorescence resonance energy transfer X. Wana B. Herman Fluorescence Imaging Spectroscopy and Microscopy, Chemical Analysis series:V 1996 Wiley New York 179 252 (B)
25. 2+ based on green fluorescent proteins and calmodulin Nature 388 1997 882 887
26. R. Onuki, A. Nagasaki, H. Kawasaki, T. Baba, T.Q. Uyeda, and K. Taira Confirmation by FRET in individual living cells of the absence of significant amyloid beta-mediated caspase 8 activation Proc. Natl. Acad. Sci. USA 99 2002 14716 14721
27. X. Jiang, and A. Sorkin Coordinated traffic of Grb2 and Ras during epidermal growth factor receptor endocytosis visualized in living cells Mol. Biol. Cell 13 2002 1522 1535
28. M.C. Overton, and K.J. Blumer G-protein-coupled receptors function as oligomers in vivo Curr. Biol. 10 2000 341 344
29. K.Q. Luo, V.C. Yu, Y. Pu, and D.C. Chang Application of the fluorescence resonance energy transfer method for studying the dynamics of caspase-3 activation during UV-induced apoptosis in living HeLa cells Biochem. Biophys. Res. Commun. 283 2001 1054 1060
30. K. Herrick-Davis, E. Grinde, and J.E. Mazurkiewicz Biochemical and biophysical characterization of serotonin 5-HT2C receptor homodimers on the plasma membrane of living cells Biochemistry 43 2004 13963 13971
31. S. Damjanovich, L. Bene, J. Matko, A. Alileche, C.K. Goldman, S. Sharrow, and T.A. Waldmann Preassembly of interleukin 2 (IL-2) receptor subunits on resting Kit 225 K6 T cells and their modulation by IL-2, IL-7, and IL-15: a fluorescence resonance energy transfer study Proc. Natl. Acad. Sci. USA 94 1997 13134 13139
32. A.K. Kenworthy, N. Petranova, and M. Edidin High-resolution FRET microscopy of cholera toxin B-subunit and GPI-anchored proteins in cell plasma membranes Mol. Biol. Cell 11 2000 1645 1655
33. L.G. Tertoolen, C. Blanchetot, G. Jiang, J. Overvoorde, T.W. Gadella Jr., T. Hunter, and J. den Hertog Dimerization of receptor protein-tyrosine phosphatase alpha in living cells BMC Cell Biol. 2 2001 8
34. J.F. Mercier, A. Salahpour, S. Angers, A. Breit, and M. Bouvier Quantitative assessment of beta 1- and beta 2-adrenergic receptor homo- and heterodimerization by bioluminescence resonance energy transfer J. Biol. Chem. 277 2002 44925 44931
35. F. Verrier, A.M. Borman, D. Brand, and M. Girard Role of the HIV type 1 glycoprotein 120 V3 loop in determining coreceptor usage AIDS Res. Hum. Retroviruses 15 1999 731 743
36. M.W. Cho, M.K. Lee, M.C. Carney, J.F. Berson, R.W. Doms, and M.A. Martin Identification of determinants on a dualtropic human immunodeficiency virus type 1 envelope glycoprotein that confer usage of CXCR4 J. Virol. 72 1998 2509 2515
37. F. Cocchi, A.L. DeVico, A. Garzino-Demo, A. Cara, R.C. Gallo, and P. Lusso The V3 domain of the HIV-1 gp120 envelope glycoprotein is critical for chemokine-mediated blockade of infection Nat. Med. 2 1996 1244 1247
38. J.R. Trujillo, W.K. Wang, T.H. Lee, and M. Essex Identification of the envelope V3 loop as a determinant of a CD4-negative neuronal cell tropism for HIV-1 Virology 217 1996 613 617
39. B.K. Chen, K. Saksela, R. Andino, and D. Baltimore Distinct modes of human immunodeficiency virus type 1 proviral latency revealed by superinfection of nonproductively infected cell lines with recombinant luciferase-encoding viruses J. Virol. 68 1994 654 660
40. R.I. Connor, B.K. Chen, S. Choe, and N.R. Landau Vpr is required for efficient replication of human immunodeficiency virus type-1 in mononuclear phagocytes Virology 206 1995 935 944
41. C.D. Weiss, S.W. Barnett, N. Cacalano, N. Killeen, D.R. Littman, and J.M. White Studies of HIV-1 envelope glycoprotein-mediated fusion using a simple fluorescence assay AIDS 10 1996 241 246
42. A.K. Kenworthy Imaging protein-protein interactions using fluorescence resonance energy transfer microscopy Methods 24 2001 289 296
43. T.S. Karpova, C.T. Baumann, L. He, X. Wu, A. Grammer, P. Lipsky, G.L. Hager, and J.G. McNally Fluorescence resonance energy transfer from cyan to yellow fluorescent protein detected by acceptor photobleaching using confocal microscopy and a single laser J. Microsc. 209 2003 56 70
44. C.A. Rosen Regulation of HIV gene expression by RNA-protein interactions Trends Genet. 7 1991 9 14
45. B.R. Cullen RNA-sequence-mediated gene regulation in HIV-1 Infect. Agents Dis. 3 1994 68 76
46. P.D. Kwong, S.E. Ryu, W.A. Hendrickson, R. Axel, R.M. Sweet, G. Folena-Wasserman, P. Hensley, and R.W. Sweet Molecular characteristics of recombinant human CD4 as deduced from polymorphic crystals Proc. Natl. Acad. Sci. USA 87 1990 6423 6427
47. M.G. Paterlini Structure modeling of the chemokine receptor CCR5: implications for ligand binding and selectivity Biophys. J. 83 2002 3012 3031
48. S.E. Kuhmann, and J.P. Moore HIV-1 entry inhibitor entrances Trends Pharmacol. Sci. 25 2004 117 120
49. L. Wu, G. LaRosa, N. Kassam, C.J. Gordon, H. Heath, N. Ruffing, H. Chen, J. Humblias, M. Samson, M. Parmentier, J.P. Moore, and C.R. Mackay Interaction of chemokine receptor CCR5 with its ligands: multiple domains for HIV-1 gp120 binding and a single domain for chemokine binding J. Exp. Med. 186 1997 1373 1381
50. M. Baba, O. Nishimura, N. Kanzaki, M. Okamoto, H. Sawada, Y. Iizawa, M. Shiraishi, Y. Aramaki, K. Okonogi, Y. Ogawa, K. Meguro, and M. Fujino A small-molecule, nonpeptide CCR5 antagonist with highly potent and selective anti-HIV-1 activity Proc. Natl. Acad. Sci. USA 96 1999 5698 5703
51. C.T. Wild, D.C. Shugars, T.K. Greenwell, C.B. McDanal, and T.J. Matthews Peptides corresponding to a predictive alpha-helical domain of human immunodeficiency virus type 1 gp41 are potent inhibitors of virus infection Proc. Natl. Acad. Sci. USA 91 1994 9770 9774
52. J.D. Reeves, S.A. Gallo, N. Ahmad, J.L. Miamidian, P.E. Harvey, M. Sharron, S. Pohlmann, J.N. Sfakianos, C.A. Derdeyn, R. Blumenthal, E. Hunter, and R.W. Doms Sensitivity of HIV-1 to entry inhibitors correlates with envelope/coreceptor affinity, receptor density, and fusion kinetics Proc. Natl. Acad. Sci. USA 99 2002 16249 16254
53. H. Golding, M. Zaitseva, E. de Rosny, L.R. King, J. Manischewitz, I. Sidorov, M.K. Gorny, S. Zolla-Pazner, D.S. Dimitrov, and C.D. Weiss Dissection of human immunodeficiency virus type 1 entry with neutralizing antibodies to gp41 fusion intermediates J. Virol. 76 2002 6780 6790
54. G.B. Melikyan, R.M. Markosyan, H. Hemmati, M.K. Delmedico, D.M. Lambert, and F.S. Cohen Evidence that the transition of HIV-1 gp41 into a six-helix bundle, not the bundle configuration, induces membrane fusion J. Cell Biol. 151 2000 413 423
55. S.A. Gallo, A. Puri, and R. Blumenthal HIV-1 gp41 six-helix bundle formation occurs rapidly after the engagement of gp120 by CXCR4 in the HIV-1 Env-mediated fusion process Biochemistry 40 2001 12231 12236
56. T.L. Hoffman, C.C. LaBranche, W. Zhang, G. Canziani, J. Robinson, I. Chaiken, J.A. Hoxie, and R.W. Doms Stable exposure of the coreceptor-binding site in a CD4-independent HIV-1 envelope protein Proc. Natl. Acad. Sci. USA 96 1999 6359 6364
57. C.C. LaBranche, T.L. Hoffman, J. Romano, B.S. Haggarty, T.G. Edwards, T.J. Matthews, R.W. Doms, and J.A. Hoxie Determinants of CD4 independence for a human immunodeficiency virus type 1 variant map outside regions required for coreceptor specificity J. Virol. 73 1999 10310 10319
58. T.G. Edwards, S. Wyss, J.D. Reeves, S. Zolla-Pazner, J.A. Hoxie, R.W. Doms, and F. Baribaud Truncation of the cytoplasmic domain induces exposure of conserved regions in the ectodomain of human immunodeficiency virus type 1 envelope protein J. Virol. 76 2002 2683 2691
59. M. Boge, S. Wyss, J.S. Bonifacino, and M. Thali A membrane-proximal tyrosine-based signal mediates internalization of the HIV-1 envelope glycoprotein via interaction with the AP-2 clathrin adaptor J. Biol. Chem. 273 1998 15773 15778
60. G.W. Lynch, A.J. Sloane, V. Raso, A. Lai, and A.L. Cunningham Direct evidence for native CD4 oligomers in lymphoid and monocytoid cells Eur. J. Immunol. 29 1999 2590 2602
61. G.W. Lynch, E.K. Slaytor, F.D. Elliott, A. Saurajen, S.G. Turville, A.J. Sloane, P.U. Cameron, A.L. Cunningham, and G.M. Halliday CD4 is expressed by epidermal Langerhans' cells predominantly as covalent dimers Exp. Dermatol. 12 2003 700 711
62. G.J. Babcock, M. Farzan, and J. Sodroski Ligand-independent dimerization of CXCR4, a principal HIV-1 coreceptor J. Biol. Chem. 278 2003 3378 3385
63. G.W. Gordon, G. Berry, X.H. Liang, B. Levine, and B. Herman Quantitative fluorescence resonance energy transfer measurements using fluorescence microscopy Biophys. J. 74 1998 2702 2713
64. T. Dragic, A. Trkola, D.A. Thompson, E.G. Cormier, F.A. Kajumo, E. Maxwell, S.W. Lin, W. Ying, S.O. Smith, T.P. Sakmar, and J.P. Moore A binding pocket for a small molecule inhibitor of HIV-1 entry within the transmembrane helices of CCR5 Proc. Natl. Acad. Sci. USA 97 2000 5639 5644
65. Y. Kliger, and Y. Shai Inhibition of HIV-1 entry before gp41 folds into its fusion-active conformation J. Mol. Biol. 295 2000 163 168
66. W. Yuan, S. Craig, Z. Si, M. Farzan, and J. Sodroski CD4-induced T-20 binding to human immunodeficiency virus type 1 gp120 blocks interaction with the CXCR4 coreceptor J. Virol. 78 2004 5448 5457
67. S. Liu, H. Lu, J. Niu, Y. Xu, S. Wu, and S. Jiang Different from the HIV fusion inhibitor C34, the anti-HIV drug fuzeon (T-20) inhibits HIV-1 entry by targeting multiple sites in gp41 and gp120 J. Biol. Chem. 2005
68. M. Lu, S.C. Blacklow, and P.S. Kim A trimeric structural domain of the HIV-1 transmembrane glycoprotein Nat. Struct. Biol. 2 1995 1075 1082
69. H. Murakoshi, R. Iino, T. Kobayashi, T. Fujiwara, C. Ohshima, A. Yoshimura, and A. Kusumi Single-molecule imaging analysis of Ras activation in living cells Proc. Natl. Acad. Sci. USA 101 2004 7317 7322