Home LiteratureArticle Details
PMID: 16103167 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, U.S. Gov't, P.H.S.

Ternary complex formation of human immunodeficiency virus type 1 Env, CD4, and chemokine receptor captured as an intermediate of membrane fusion.

Journal of virology ·Vol. 79 ·No. 17 ·2005-09-00 ·Pages 11161-9

Mkrtchyan SR, Markosyan RM, Eadon MT, Moore JP, Melikyan GB, Cohen FS

Abstract

Human immunodeficiency virus (HIV) Env-induced fusion is highly temperature dependent. When effector and target cells were coincubated at 37 degrees C, there was a kinetic delay before fusion commenced. When effector and target cells were coincubated for varied times at 23 degrees C, a temperature that does not permit fusion, a temperature-arrested stage was created. Raising temperature to 37 degrees C from the 23 degrees C intermediate eliminated the kinetic delay. Inhibitors (T22, AMD3100, and Sch-C) that block fusion by binding chemokine receptors were added after creating the intermediate so as to assess the extent of engagement between gp120 and chemokine receptors at that stage. For both CXCR4 and CCR5 as coreceptors, increasingly long times of coincubation at 23 degrees C reduced the efficacy of the coreceptor-binding inhibitors in blocking fusion. This implies that an increasing number of ternary Env/CD4/coreceptor complexes form over time at 23 degrees C. It also shows that ternary complex formation has a lower temperature threshold than the downstream steps that include Env folding into a six-helix bundle; this provides an experimental means to separate coreceptor binding by gp120 from the subsequent refolding of gp41 into a six-helix bundle structure. As the time of cell coincubation at 23 degrees C was prolonged, more cells quickly fused upon the raising of the temperature to 37 degrees C, and the increase quantitatively correlated with the greater percentage of fusion that was resistant to drugs. Therefore the pronounced kinetic delay in HIV Env-induced fusion is caused predominantly by the time needed for ternary complexes to form.

MeSH Terms
CD4 Antigens/metabolism Cell Line HIV Envelope Protein gp120/metabolism HIV Envelope Protein gp41/metabolism HIV-1/physiology Humans Membrane Fusion/physiology Receptors, Chemokine/metabolism Temperature Time Factors Virus Replication
Chemicals
CD4 Antigens HIV Envelope Protein gp120 HIV Envelope Protein gp41 Receptors, Chemokine
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Mkrtchyan Samvel R
Department of Molecular Biophysics and Physiology, Rush University Medical Center, Chicago, IL 60612, USA.
Markosyan Ruben M
Eadon Michael T
Moore John P
Melikyan Gregory B
Cohen Fredric S
References (45)
45 references, click to expand
  1. Altering expression levels of human immunodeficiency virus type 1 gp120-gp41 affects efficiency but not kinetics of cell-cell fusion.
    J Virol. 2002 Apr;76(7):3522-33 PMID: 11884576
  2. The CCR5 receptor-based mechanism of action of 873140, a potent allosteric noncompetitive HIV entry inhibitor.
    Mol Pharmacol. 2005 Apr;67(4):1268-82 PMID: 15644495
  3. Dissection of human immunodeficiency virus type 1 entry with neutralizing antibodies to gp41 fusion intermediates.
    J Virol. 2002 Jul;76(13):6780-90 PMID: 12050391
  4. HIV-1 envelope proteins complete their folding into six-helix bundles immediately after fusion pore formation.
    Mol Biol Cell. 2003 Mar;14(3):926-38 PMID: 12631714
  5. Analysis of the mechanism by which the small-molecule CCR5 antagonists SCH-351125 and SCH-350581 inhibit human immunodeficiency virus type 1 entry.
    J Virol. 2003 May;77(9):5201-8 PMID: 12692222
  6. Human immunodeficiency virus type 1 Env with an intersubunit disulfide bond engages coreceptors but requires bond reduction after engagement to induce fusion.
    J Virol. 2003 May;77(10):5829-36 PMID: 12719576
  7. Mutations at the CXCR4 interaction sites for AMD3100 influence anti-CXCR4 antibody binding and HIV-1 entry.
    FEBS Lett. 2003 Jul 10;546(2-3):300-6 PMID: 12832058
  8. Lipid bilayer simulations of CXCR4 with inverse agonists and weak partial agonists.
    J Biol Chem. 2003 Nov 21;278(47):47136-44 PMID: 12958314
  9. Electron tomography analysis of envelope glycoprotein trimers on HIV and simian immunodeficiency virus virions.
    Proc Natl Acad Sci U S A. 2003 Dec 23;100(26):15812-7 PMID: 14668432
  10. Molecular mechanism of AMD3100 antagonism in the CXCR4 receptor: transfer of binding site to the CXCR3 receptor.
    J Biol Chem. 2004 Jan 23;279(4):3033-41 PMID: 14585837
  11. Genetic and phenotypic analyses of human immunodeficiency virus type 1 escape from a small-molecule CCR5 inhibitor.
    J Virol. 2004 Mar;78(6):2790-807 PMID: 14990699
  12. The differential sensitivity of human and rhesus macaque CCR5 to small-molecule inhibitors of human immunodeficiency virus type 1 entry is explained by a single amino acid difference and suggests a mechanism of action for these inhibitors.
    J Virol. 2004 Apr;78(8):4134-44 PMID: 15047829
  13. The T4 gene encodes the AIDS virus receptor and is expressed in the immune system and the brain.
    Cell. 1986 Nov 7;47(3):333-48 PMID: 3094962
  14. A human lymphoid recombinant cell line with functional human immunodeficiency virus type 1 envelope.
    AIDS Res Hum Retroviruses. 1993 Jan;9(1):23-32 PMID: 8094000
  15. Highly potent and selective inhibition of human immunodeficiency virus by the bicyclam derivative JM3100.
    Antimicrob Agents Chemother. 1994 Apr;38(4):668-74 PMID: 7913308
  16. Temperature dependence of cell-cell fusion induced by the envelope glycoprotein of human immunodeficiency virus type 1.
    J Virol. 1995 Mar;69(3):1462-72 PMID: 7853478
  17. The fusion kinetics of influenza hemagglutinin expressing cells to planar bilayer membranes is affected by HA density and host cell surface.
    J Gen Physiol. 1995 Nov;106(5):783-802 PMID: 8648292
  18. CD4, CXCR-4, and CCR-5 dependencies for infections by primary patient and laboratory-adapted isolates of human immunodeficiency virus type 1.
    J Virol. 1997 Feb;71(2):873-82 PMID: 8995603
  19. Multiple extracellular domains of CCR-5 contribute to human immunodeficiency virus type 1 entry and fusion.
    J Virol. 1997 Jul;71(7):5003-11 PMID: 9188565
  20. Identification of a chemokine receptor encoded by human cytomegalovirus as a cofactor for HIV-1 entry.
    Science. 1997 Jun 20;276(5320):1874-8 PMID: 9188536
  21. Effects of CCR5 and CD4 cell surface concentrations on infections by macrophagetropic isolates of human immunodeficiency virus type 1.
    J Virol. 1998 Apr;72(4):2855-64 PMID: 9525605
  22. Use of a gp120 binding assay to dissect the requirements and kinetics of human immunodeficiency virus fusion events.
    J Virol. 1999 Dec;73(12):10346-58 PMID: 10559353
  23. A binding pocket for a small molecule inhibitor of HIV-1 entry within the transmembrane helices of CCR5.
    Proc Natl Acad Sci U S A. 2000 May 9;97(10):5639-44 PMID: 10779565
  24. Varying effects of temperature, Ca(2+) and cytochalasin on fusion activity mediated by human immunodeficiency virus type 1 and type 2 glycoproteins.
    FEBS Lett. 2000 Jun 2;474(2-3):246-51 PMID: 10838094
  25. Critical role of enhanced CD4 affinity in laboratory adaptation of human immunodeficiency virus type 1.
    AIDS Res Hum Retroviruses. 2000 Jun 10;16(9):871-82 PMID: 10875613
  26. Cooperation of multiple CCR5 coreceptors is required for infections by human immunodeficiency virus type 1.
    J Virol. 2000 Aug;74(15):7005-15 PMID: 10888639
  27. A biosensor assay for studying ligand-membrane receptor interactions: binding of antibodies and HIV-1 Env to chemokine receptors.
    Proc Natl Acad Sci U S A. 2000 Oct 10;97(21):11215-20 PMID: 11005830
  28. Evidence that the transition of HIV-1 gp41 into a six-helix bundle, not the bundle configuration, induces membrane fusion.
    J Cell Biol. 2000 Oct 16;151(2):413-23 PMID: 11038187
  29. Molecular interactions of cyclam and bicyclam non-peptide antagonists with the CXCR4 chemokine receptor.
    J Biol Chem. 2001 Apr 27;276(17):14153-60 PMID: 11154697
  30. HIV fusion and its inhibition.
    Antiviral Res. 2001 May;50(2):95-115 PMID: 11369431
  31. 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. 2001 Oct 16;40(41):12231-6 PMID: 11591141
  32. SCH-C (SCH 351125), an orally bioavailable, small molecule antagonist of the chemokine receptor CCR5, is a potent inhibitor of HIV-1 infection in vitro and in vivo.
    Proc Natl Acad Sci U S A. 2001 Oct 23;98(22):12718-23 PMID: 11606733
  33. Mechanisms of viral membrane fusion and its inhibition.
    Annu Rev Biochem. 2001;70:777-810 PMID: 11395423
  34. Capture of an early fusion-active conformation of HIV-1 gp41.
    Nat Struct Biol. 1998 Apr;5(4):276-9 PMID: 9546217
  35. Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human antibody.
    Nature. 1998 Jun 18;393(6686):648-59 PMID: 9641677
  36. Determinants for sensitivity of human immunodeficiency virus coreceptor CXCR4 to the bicyclam AMD3100.
    J Virol. 1998 Aug;72(8):6381-8 PMID: 9658078
  37. 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. 1999 Feb;73(2):1645-8 PMID: 9882373
  38. T134, a small-molecule CXCR4 inhibitor, has no cross-drug resistance with AMD3100, a CXCR4 antagonist with a different structure.
    J Virol. 1999 Feb;73(2):1719-23 PMID: 9882387
  39. Epitope mapping of CCR5 reveals multiple conformational states and distinct but overlapping structures involved in chemokine and coreceptor function.
    J Biol Chem. 1999 Apr 2;274(14):9617-26 PMID: 10092648
  40. Differential inhibition of human immunodeficiency virus type 1 fusion, gp120 binding, and CC-chemokine activity by monoclonal antibodies to CCR5.
    J Virol. 1999 May;73(5):4145-55 PMID: 10196311
  41. Quantification of CD4, CCR5, and CXCR4 levels on lymphocyte subsets, dendritic cells, and differentially conditioned monocyte-derived macrophages.
    Proc Natl Acad Sci U S A. 1999 Apr 27;96(9):5215-20 PMID: 10220446
  42. The cytoplasmic tail slows the folding of human immunodeficiency virus type 1 Env from a late prebundle configuration into the six-helix bundle.
    J Virol. 2005 Jan;79(1):106-15 PMID: 15596806
  43. Structure of an unliganded simian immunodeficiency virus gp120 core.
    Nature. 2005 Feb 24;433(7028):834-41 PMID: 15729334
  44. Stoichiometry of antibody neutralization of human immunodeficiency virus type 1.
    J Virol. 2005 Mar;79(6):3500-8 PMID: 15731244
  45. Envelope glycoprotein incorporation, not shedding of surface envelope glycoprotein (gp120/SU), Is the primary determinant of SU content of purified human immunodeficiency virus type 1 and simian immunodeficiency virus.
    J Virol. 2002 Jun;76(11):5315-25 PMID: 11991960
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
0022-538X
Published
2005-09-00
Pages
11161-9
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC1193594
Subset
IM
Grants
NIGMS NIH HHS · GM54787 · United States
NIGMS NIH HHS · R01 GM027367 · United States
NIGMS NIH HHS · R29 GM054787 · United States
NIAID NIH HHS · AI41420 · United States
NIGMS NIH HHS · GM27367 · United States
NIGMS NIH HHS · R01 GM054787 · United States
NIAID NIH HHS · R01 AI041420 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com