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PMID: 10775580 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

The human immunodeficiency virus type 1 gp120 V2 domain mediates gp41-independent intersubunit contacts.

Journal of virology ·Vol. 74 ·No. 10 ·2000-05-00 ·Pages 4448-55

Center RJ, Earl PL, Lebowitz J, Schuck P, Moss B

Abstract

The envelope protein of human immunodeficiency virus type 1 HIV-1 undergoes proteolytic cleavage in the Golgi complex to produce subunits designated gp120 and gp41, which remain noncovalently associated. While gp41 has a well-characterized oligomeric structure, the maintenance of gp41-independent gp120 intersubunit contacts remains a contentious issue. Using recombinant vaccinia virus to achieve high-level expression of gp120 in mammalian cells combined with gel filtration analysis, we were able to isolate a discrete oligomeric form of gp120. Oligomerization of gp120 occurred intracellularly between 30 and 120 min after synthesis. Analysis by sedimentation equilibrium unequivocally identified the oligomeric species as a dimer. In order to identify the domains involved in the intersubunit contact, we expressed a series of gp120 proteins lacking various domains and assessed the effects of mutation on oligomeric structure. Deletion of the V1 or V3 loops had little effect on the relative amounts of monomer and dimer in comparison to wild-type gp120. In contrast, deletion of either all or part of the V2 loop drastically reduced dimer formation, indicating that this domain is required for intersubunit contact formation. Consistent with this, the V2 loop of the dimer was less accessible than that of the monomer to a specific monoclonal antibody. Previous studies have shown that while the V2 loop is not an absolute requirement for viral entry, the absence of this domain reduces viral resistance to neutralization by monoclonal antibodies or sera. We propose that the quaternary structure of gp120 may contribute to resistance to neutralization by limiting the exposure of conserved epitopes.

MeSH Terms
Cell Line Centrifugation, Density Gradient Chromatography, Gel Dimerization Epitopes Genetic Vectors HIV Envelope Protein gp120/chemistry,genetics,metabolism HIV Envelope Protein gp41/chemistry,genetics,metabolism HIV-1/genetics,metabolism Humans Protein Structure, Tertiary Vaccinia virus/genetics,metabolism
Chemicals
Epitopes HIV Envelope Protein gp120 HIV Envelope Protein gp41
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Center R J
Laboratory of Viral Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland 20892, USA.
Earl P L
Lebowitz J
Schuck P
Moss B
References (51)
51 references, click to expand
  1. Structural modulations of the envelope gp120 glycoprotein of human immunodeficiency virus type 1 upon oligomerization and differential V3 loop epitope exposure of isolates displaying distinct tropism upon virion-soluble receptor binding.
    J Virol. 1995 Oct;69(10):6191-8 PMID: 7545244
  2. Modern applications of analytical ultracentrifugation.
    Annu Rev Biophys Biomol Struct. 1999;28:75-100 PMID: 10410796
  3. Complete nucleotide sequence of the AIDS virus, HTLV-III.
    Nature. 1985 Jan 24-30;313(6000):277-84 PMID: 2578615
  4. Oligomeric structure of gp41, the transmembrane protein of human immunodeficiency virus type 1.
    J Virol. 1989 Jun;63(6):2674-9 PMID: 2786089
  5. Studies with crosslinking reagents on the oligomeric structure of the env glycoprotein of HIV.
    Virology. 1989 Sep;172(1):367-9 PMID: 2672564
  6. Oligomeric structure of the human immunodeficiency virus type 1 envelope glycoprotein.
    Proc Natl Acad Sci U S A. 1990 Jan;87(2):648-52 PMID: 2300552
  7. Intracellular processing of the gp160 HIV-1 envelope precursor. Endoproteolytic cleavage occurs in a cis or medial compartment of the Golgi complex.
    J Biol Chem. 1990 Feb 15;265(5):2640-9 PMID: 2406237
  8. Assignment of intrachain disulfide bonds and characterization of potential glycosylation sites of the type 1 recombinant human immunodeficiency virus envelope glycoprotein (gp120) expressed in Chinese hamster ovary cells.
    J Biol Chem. 1990 Jun 25;265(18):10373-82 PMID: 2355006
  9. Oligomeric organization of gp120 on infectious human immunodeficiency virus type 1 particles.
    J Virol. 1990 Nov;64(11):5674-7 PMID: 2214033
  10. The human immunodeficiency virus type 1 envelope glycoprotein precursor acquires aberrant intermolecular disulfide bonds that may prevent normal proteolytic processing.
    Virology. 1990 Dec;179(2):827-33 PMID: 2238472
  11. Biological and immunological properties of human immunodeficiency virus type 1 envelope glycoprotein: analysis of proteins with truncations and deletions expressed by recombinant vaccinia viruses.
    J Virol. 1991 Jan;65(1):31-41 PMID: 1985202
  12. Folding, interaction with GRP78-BiP, assembly, and transport of the human immunodeficiency virus type 1 envelope protein.
    J Virol. 1991 Apr;65(4):2047-55 PMID: 1900540
  13. Human immunodeficiency virus type 1 gp120 envelope glycoprotein regions important for association with the gp41 transmembrane glycoprotein.
    J Virol. 1991 Apr;65(4):2119-23 PMID: 2002555
  14. gp160, the envelope glycoprotein of human immunodeficiency virus type 1, is a dimer of 125-kilodalton subunits stabilized through interactions between their gp41 domains.
    J Virol. 1991 Jul;65(7):3797-803 PMID: 2041094
  15. The assembly of the HIV-1 env glycoprotein into dimers and tetramers.
    Adv Exp Med Biol. 1991;300:203-19; discussion 220-1 PMID: 1781345
  16. Functional and immunologic characterization of human immunodeficiency virus type 1 envelope glycoproteins containing deletions of the major variable regions.
    J Virol. 1993 Aug;67(8):4557-65 PMID: 8331723
  17. Mutational analysis of the assembly domain of the HIV-1 envelope glycoprotein.
    AIDS Res Hum Retroviruses. 1993 Jul;9(7):589-94 PMID: 8369163
  18. Probing the structure of the V2 domain of human immunodeficiency virus type 1 surface glycoprotein gp120 with a panel of eight monoclonal antibodies: human immune response to the V1 and V2 domains.
    J Virol. 1993 Oct;67(10):6136-51 PMID: 7690418
  19. Probing the structure of the human immunodeficiency virus surface glycoprotein gp120 with a panel of monoclonal antibodies.
    J Virol. 1994 Jan;68(1):469-84 PMID: 7504741
  20. Recognition properties of a panel of human recombinant Fab fragments to the CD4 binding site of gp120 that show differing abilities to neutralize human immunodeficiency virus type 1.
    J Virol. 1994 Aug;68(8):4821-8 PMID: 7518527
  21. Identification and characterization of monoclonal antibodies specific for polymorphic antigenic determinants within the V2 region of the human immunodeficiency virus type 1 envelope glycoprotein.
    J Virol. 1995 Jan;69(1):222-30 PMID: 7527084
  22. Oligomeric rearrangement of tick-borne encephalitis virus envelope proteins induced by an acidic pH.
    J Virol. 1995 Feb;69(2):695-700 PMID: 7529335
  23. Replicative function and neutralization sensitivity of envelope glycoproteins from primary and T-cell line-passaged human immunodeficiency virus type 1 isolates.
    J Virol. 1995 Jul;69(7):4413-22 PMID: 7769703
  24. Human immunodeficiency virus type 1 neutralization is determined by epitope exposure on the gp120 oligomer.
    J Exp Med. 1995 Jul 1;182(1):185-96 PMID: 7540648
  25. Involvement of the V1/V2 variable loop structure in the exposure of human immunodeficiency virus type 1 gp120 epitopes induced by receptor binding.
    J Virol. 1995 Sep;69(9):5723-33 PMID: 7543586
  26. Evidence for cell-surface association between fusin and the CD4-gp120 complex in human cell lines.
    Science. 1996 Oct 25;274(5287):602-5 PMID: 8849450
  27. CD4-induced interaction of primary HIV-1 gp120 glycoproteins with the chemokine receptor CCR-5.
    Nature. 1996 Nov 14;384(6605):179-83 PMID: 8906795
  28. CD4-dependent, antibody-sensitive interactions between HIV-1 and its co-receptor CCR-5.
    Nature. 1996 Nov 14;384(6605):184-7 PMID: 8906796
  29. Crystal structures of a single coiled-coil peptide in two oligomeric states reveal the basis for structural polymorphism.
    Nat Struct Biol. 1996 Dec;3(12):1002-9 PMID: 8946853
  30. Partial characterization of the C-terminal non-collagenous domain (NC1) of collagen type X.
    Biochem J. 1996 Dec 1;320 ( Pt 2):479-85 PMID: 8973556
  31. Human immunodeficiency virus type 1 envelope glycoprotein oligomerization requires the gp41 amphipathic alpha-helical/leucine zipper-like sequence.
    J Virol. 1997 Mar;71(3):2041-9 PMID: 9032336
  32. Neutralization of the human immunodeficiency virus type 1 primary isolate JR-FL by human monoclonal antibodies correlates with antibody binding to the oligomeric form of the envelope glycoprotein complex.
    J Virol. 1997 Apr;71(4):2779-85 PMID: 9060632
  33. Core structure of gp41 from the HIV envelope glycoprotein.
    Cell. 1997 Apr 18;89(2):263-73 PMID: 9108481
  34. Binding of antibodies to virion-associated gp120 molecules of primary-like human immunodeficiency virus type 1 (HIV-1) isolates: effect on HIV-1 infection of macrophages and peripheral blood mononuclear cells.
    Virology. 1997 Mar 17;229(2):360-9 PMID: 9126249
  35. Atomic structure of the ectodomain from HIV-1 gp41.
    Nature. 1997 May 22;387(6631):426-30 PMID: 9163431
  36. Involvement of the HIV-1 external envelope glycoprotein 120 (gp120) C2 region in gp120 oligomerization.
    Biochim Biophys Acta. 1997 Jul 18;1340(2):277-82 PMID: 9252114
  37. Analysis of the interaction of the human immunodeficiency virus type 1 gp120 envelope glycoprotein with the gp41 transmembrane glycoprotein.
    J Virol. 1997 Dec;71(12):9722-31 PMID: 9371638
  38. Replication and neutralization of human immunodeficiency virus type 1 lacking the V1 and V2 variable loops of the gp120 envelope glycoprotein.
    J Virol. 1997 Dec;71(12):9808-12 PMID: 9371651
  39. Compact, synthetic, vaccinia virus early/late promoter for protein expression.
    Biotechniques. 1997 Dec;23(6):1094-7 PMID: 9421642
  40. Dilation of the human immunodeficiency virus-1 envelope glycoprotein fusion pore revealed by the inhibitory action of a synthetic peptide from gp41.
    J Cell Biol. 1998 Jan 26;140(2):315-23 PMID: 9442107
  41. Capture of an early fusion-active conformation of HIV-1 gp41.
    Nat Struct Biol. 1998 Apr;5(4):276-9 PMID: 9546217
  42. Neutralization of human immunodeficiency virus type 1 by antibody to gp120 is determined primarily by occupancy of sites on the virion irrespective of epitope specificity.
    J Virol. 1998 May;72(5):3512-9 PMID: 9557629
  43. CD4-Induced conformational changes in the human immunodeficiency virus type 1 gp120 glycoprotein: consequences for virus entry and neutralization.
    J Virol. 1998 Jun;72(6):4694-703 PMID: 9573233
  44. Interactions of polyclonal and monoclonal anti-glycoprotein 120 antibodies with oligomeric glycoprotein 120-glycoprotein 41 complexes of a primary HIV type 1 isolate: relationship to neutralization.
    AIDS Res Hum Retroviruses. 1998 May 1;14(7):591-7 PMID: 9591713
  45. A conserved HIV gp120 glycoprotein structure involved in chemokine receptor binding.
    Science. 1998 Jun 19;280(5371):1949-53 PMID: 9632396
  46. 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
  47. The antigenic structure of the HIV gp120 envelope glycoprotein.
    Nature. 1998 Jun 18;393(6686):705-11 PMID: 9641684
  48. An envelope modification that renders a primary, neutralization-resistant clade B human immunodeficiency virus type 1 isolate highly susceptible to neutralization by sera from other clades.
    J Virol. 1998 Oct;72(10):7840-5 PMID: 9733820
  49. Characterization of conformation-dependent anti-gp120 murine monoclonal antibodies produced by immunization with monomeric and oligomeric human immunodeficiency virus type 1 envelope proteins.
    Virology. 1999 Feb 15;254(2):257-67 PMID: 9986792
  50. Analytical band centrifugation of proteins and protein complexes.
    Biochem Soc Trans. 1998 Nov;26(4):745-9 PMID: 10047819
  51. Ultracentrifugal analysis of molecular mass of glycoproteins of unknown or ill-defined carbohydrate composition.
    Methods Enzymol. 2000;321:136-49 PMID: 10909055
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
0022-538X
Published
2000-05-00
Pages
4448-55
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC111965
Subset
IM
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