Evidence That the Transition of HIV-1 Gp41 into a Six-Helix Bundle, Not the Bundle Configuration, Induces Membrane Fusion

doi:10.1083/jcb.151.2.413

Published online 16 October 2000. doi:10.1083/jcb.151.2.413

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© The Rockefeller University Press, 0021-9525/2000//413 $5.00
The Journal of Cell Biology, Volume 151, Number 2, , 2000 413-424

Original Article

Evidence That the Transition of HIV-1 Gp41 into a Six-Helix Bundle, Not the Bundle Configuration, Induces Membrane Fusion

Grigory B. Melikyan^a, Ruben M. Markosyan^a, Hila Hemmati^a, Mary K. Delmedico^b, Dennis M. Lambert^b, and Fredric S. Cohen^a

^a Department of Molecular Biophysics and Physiology, Rush Medical College, Chicago, Illinois 60612
^b Trimeris Inc., Durham, North Carolina 27707
Department of Molecular Biophysics and Physiology, Rush Medical College, 1653 W. Congress Parkway, Chicago, IL 60612.(312) 942-8711(312) 942-6753

Many viral fusion proteins exhibit a six-helix bundle as a corestructure. HIV Env–induced fusion was studied to resolvewhether membrane merger was due to the transition into the bundleconfiguration or occurred after bundle formation. Suboptimaltemperature was used to arrest fusion at an intermediate stage.When bundle formation was prevented by adding inhibitory peptidesat this stage, membranes did not merge upon raising temperature.Inversely, when membrane merger was prevented by incorporatinglysophosphatidylcholine (LPC) into cell membranes at the intermediate,the bundle did not form upon optimizing temperature. In theabsence of LPC, the six-helix bundle did not form when the temperatureof the intermediate was raised for times too short to promotefusion. Kinetic measures showed that after the temperature pulse,cells had not advanced further toward fusion. The latter resultsindicate that bundle formation is the rate-limiting step betweenthe arrested intermediate and fusion. Electrical measures showedthat the HIV Env–induced pore is initially large and growsrapidly. It is proposed that bundle formation and fusion areeach contingent on the other and that movement of Env duringits transition into the six-helix bundle directly induces thelipid rearrangements of membrane fusion. Because peptide inhibitionshowed that, at the intermediate stage, the heptad repeats ofgp41 have become stably exposed, creation of the intermediatecould be of importance in drug and/or vaccine development.

Key Words: fusion pore • fusion intermediates • inhibitory peptides • fusion kinetics • hemifusion

The online version of this article contains supplemental material.

Abbreviations used in this paper: CMAC, 7-amino-4-chloromethylcoumarin;CXCR4, chemokine receptor; DiI, 1,1'-dioctadecyl-3,3,3',3'-tetramethylindocarbocyanineperchlorate; HA, hemagglutinin; HR, heptad repeat; IR, infrared;LAS, lipid-arrested stage; LPC, lysophosphatidylcholine; OA,oleic acid; SNARE, soluble N-ethylmaleimide–sensitivefactor attachment protein receptor; TAS, temperature-arrestedstage; TM, transmembrane.

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Corcoran, J. A., Duncan, R. (2004). Reptilian Reovirus Utilizes a Small Type III Protein with an External Myristylated Amino Terminus To Mediate Cell-Cell Fusion. J. Virol. 78: 4342-4351 [Abstract] [Full Text]
Gibbons, D. L., Reilly, B., Ahn, A., Vaney, M.-C., Vigouroux, A., Rey, F. A., Kielian, M. (2004). Purification and Crystallization Reveal Two Types of Interactions of the Fusion Protein Homotrimer of Semliki Forest Virus. J. Virol. 78: 3514-3523 [Abstract] [Full Text]
Melikyan, G. B., Barnard, R. J. O., Markosyan, R. M., Young, J. A. T., Cohen, F. S. (2004). Low pH Is Required for Avian Sarcoma and Leukosis Virus Env-Induced Hemifusion and Fusion Pore Formation but Not for Pore Growth. J. Virol. 78: 3753-3762 [Abstract] [Full Text]
Thorp, E. B., Gallagher, T. M. (2004). Requirements for CEACAMs and Cholesterol during Murine Coronavirus Cell Entry. J. Virol. 78: 2682-2692 [Abstract] [Full Text]
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Smith, J. G., Mothes, W., Blacklow, S. C., Cunningham, J. M. (2004). The Mature Avian Leukosis Virus Subgroup A Envelope Glycoprotein Is Metastable, and Refolding Induced by the Synergistic Effects of Receptor Binding and Low pH Is Coupled to Infection. J. Virol. 78: 1403-1410 [Abstract] [Full Text]
Egelhofer, M., Brandenburg, G., Martinius, H., Schult-Dietrich, P., Melikyan, G., Kunert, R., Baum, C., Choi, I., Alexandrov, A., von Laer, D. (2004). Inhibition of Human Immunodeficiency Virus Type 1 Entry in Cells Expressing gp41-Derived Peptides. J. Virol. 78: 568-575 [Abstract] [Full Text]
Qian, Z., Albritton, L. M. (2004). An Aromatic Side Chain Is Required at Residue 8 of SU for Fusion of Ecotropic Murine Leukemia Virus. J. Virol. 78: 508-512 [Abstract] [Full Text]
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Russell, C. J., Kantor, K. L., Jardetzky, T. S., Lamb, R. A. (2003). A dual-functional paramyxovirus F protein regulatory switch segment: activation and membrane fusion. JCB 163: 363-374 [Abstract] [Full Text]
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Moore, J. P., Doms, R. W. (2003). The entry of entry inhibitors: A fusion of science and medicine. Proc. Natl. Acad. Sci. USA 100: 10598-10602 [Abstract] [Full Text]
Bosch, B. J., van der Zee, R., de Haan, C. A. M., Rottier, P. J. M. (2003). The Coronavirus Spike Protein Is a Class I Virus Fusion Protein: Structural and Functional Characterization of the Fusion Core Complex. J. Virol. 77: 8801-8811 [Abstract] [Full Text]
Lin, X., Derdeyn, C. A., Blumenthal, R., West, J., Hunter, E. (2003). Progressive Truncations C Terminal to the Membrane-Spanning Domain of Simian Immunodeficiency Virus Env Reduce Fusogenicity and Increase Concentration Dependence of Env for Fusion. J. Virol. 77: 7067-7077 [Abstract] [Full Text]
Binley, J. M., Cayanan, C. S., Wiley, C., Schulke, N., Olson, W. C., Burton, D. R. (2003). Redox-Triggered Infection by Disulfide-Shackled Human Immunodeficiency Virus Type 1 Pseudovirions. J. Virol. 77: 5678-5684 [Abstract] [Full Text]
Abrahamyan, L. G., Markosyan, R. M., Moore, J. P., Cohen, F. S., Melikyan, G. B. (2003). Human Immunodeficiency Virus Type 1 Env with an Intersubunit Disulfide Bond Engages Coreceptors but Requires Bond Reduction after Engagement To Induce Fusion. J. Virol. 77: 5829-5836 [Abstract] [Full Text]
Douglas, J. L., Panis, M. L., Ho, E., Lin, K.-Y., Krawczyk, S. H., Grant, D. M., Cai, R., Swaminathan, S., Cihlar, T. (2003). Inhibition of Respiratory Syncytial Virus Fusion by the Small Molecule VP-14637 via Specific Interactions with F Protein. J. Virol. 77: 5054-5064 [Abstract] [Full Text]
Root, M. J., Hamer, D. H. (2003). Targeting therapeutics to an exposed and conserved binding element of the HIV-1 fusion protein. Proc. Natl. Acad. Sci. USA 100: 5016-5021 [Abstract] [Full Text]