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PMID: 11134289 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Organization of immature human immunodeficiency virus type 1.

Journal of virology ·Vol. 75 ·No. 2 ·2001-01-00 ·Pages 759-71

Wilk T, Gross I, Gowen BE, Rutten T, de Haas F, Welker R, Kräusslich HG, Boulanger P, Fuller SD

Abstract

Immature retrovirus particles contain radially arranged Gag polyproteins in which the N termini lie at the membrane and the C termini extend toward the particle's center. We related image features to the polyprotein domain structure by combining mutagenesis with cryoelectron microscopy and image analysis. The matrix (MA) domain appears as a thin layer tightly associated with the inner face of the viral membrane, separated from the capsid (CA) layer by a low-density region corresponding to its C terminus. Deletion of the entire p6 domain has no effect on the width or spacing of the density layers, suggesting that p6 is not ordered in immature human immunodeficiency virus type 1 (HIV-1). In vitro assembly of a recombinant Gag polyprotein containing only capsid (CA) and nucleocapsid (NC) domains results in the formation of nonenveloped spherical particles which display two layers with density matching that of the CA-NC portion of immature HIV-1 Gag particles. Authentic, immature HIV-1 displays additional surface features and an increased density between the lipid bilayers which reflect the presence of gp41. The other internal features match those of virus-like particles.

MeSH Terms
Capsid/chemistry Cell Membrane/metabolism Cryoelectron Microscopy Gene Deletion Gene Products, gag/chemistry,genetics,metabolism HIV-1/chemistry,genetics,physiology,ultrastructure Humans Image Processing, Computer-Assisted Lipid Bilayers Nucleocapsid/chemistry Protein Structure, Tertiary Recombinant Proteins/metabolism Viral Matrix Proteins/chemistry,genetics Virion/chemistry,ultrastructure Virus Assembly gag Gene Products, Human Immunodeficiency Virus
Chemicals
Gene Products, gag Lipid Bilayers Recombinant Proteins Viral Matrix Proteins gag Gene Products, Human Immunodeficiency Virus p6 gag protein, Human immunodeficiency virus 1
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Wilk T
The Structural Biology Programme, European Molecular Biology Laboratory, D69012 Heidelberg, Federal Republic of Germany.
Gross I
Gowen B E
Rutten T
de Haas F
Welker R
Kräusslich H G
Boulanger P
Fuller S D
References (46)
46 references, click to expand
  1. Cryo-electron microscopy reveals the functional organization of an enveloped virus, Semliki Forest virus.
    Mol Cell. 2000 Feb;5(2):255-66 PMID: 10882067
  2. Localization of actin in Moloney murine leukemia virus by immunoelectron microscopy.
    Virology. 1999 Jul 20;260(1):23-34 PMID: 10405353
  3. Production of acquired immunodeficiency syndrome-associated retrovirus in human and nonhuman cells transfected with an infectious molecular clone.
    J Virol. 1986 Aug;59(2):284-91 PMID: 3016298
  4. Fine structure of human immunodeficiency virus (HIV) and immunolocalization of structural proteins.
    Virology. 1987 Jan;156(1):171-6 PMID: 3643678
  5. Standardized and simplified nomenclature for proteins common to all retroviruses.
    J Virol. 1988 May;62(5):1808-9 PMID: 3357211
  6. Theoretically determined three-dimensional structures for amphipathic segments of the HIV-1 gp41 envelope protein.
    AIDS Res Hum Retroviruses. 1989 Feb;5(1):7-22 PMID: 2541749
  7. Assembly and release of HIV-1 precursor Pr55gag virus-like particles from recombinant baculovirus-infected insect cells.
    Cell. 1989 Oct 6;59(1):103-12 PMID: 2676191
  8. The GAG precursor of simian immunodeficiency virus assembles into virus-like particles.
    EMBO J. 1989 Sep;8(9):2653-60 PMID: 2684654
  9. Production of human immunodeficiency virus (HIV)-like particles from cells infected with recombinant vaccinia viruses carrying the gag gene of HIV.
    Virology. 1990 Mar;175(1):139-48 PMID: 1689917
  10. Human immunodeficiency virus as a prototypic complex retrovirus.
    J Virol. 1991 Mar;65(3):1053-6 PMID: 1995941
  11. Effect of mutations affecting the p6 gag protein on human immunodeficiency virus particle release.
    Proc Natl Acad Sci U S A. 1991 Apr 15;88(8):3195-9 PMID: 2014240
  12. Functional domains of HIV-1 gag-polyprotein expressed in baculovirus-infected cells.
    Virology. 1991 Sep;184(1):417-22 PMID: 1871977
  13. Assembly and morphology of HIV: potential effect of structure on viral function.
    AIDS. 1991 Jun;5(6):617-37 PMID: 1652977
  14. Expression and extracellular release of human immunodeficiency virus type 1 Gag precursors by recombinant baculovirus-infected cells.
    J Virol. 1992 May;66(5):3230-5 PMID: 1560545
  15. Mechanism of action of regulatory proteins encoded by complex retroviruses.
    Microbiol Rev. 1992 Sep;56(3):375-94 PMID: 1406488
  16. A large deletion in the matrix domain of the human immunodeficiency virus gag gene redirects virus particle assembly from the plasma membrane to the endoplasmic reticulum.
    J Virol. 1993 Aug;67(8):4972-80 PMID: 8331736
  17. Structural and functional studies in vitro on the p6 protein from the HIV-1 gag open reading frame.
    Biochim Biophys Acta. 1993 Sep 8;1182(2):157-61 PMID: 8357847
  18. Fullerene-like organization of HIV gag-protein shell in virus-like particles produced by recombinant baculovirus.
    Virology. 1994 Jan;198(1):288-96 PMID: 8259664
  19. Further evidence of icosahedral symmetry in human and simian immunodeficiency virus.
    AIDS Res Hum Retroviruses. 1993 Oct;9(10):929-38 PMID: 8280478
  20. A morphological and immunolabelling study of freeze-substituted human and simian immunodeficiency viruses.
    Micron. 1994;25(2):119-28 PMID: 8055244
  21. Determination of the size of HIV using adenovirus type 2 as an internal length marker.
    J Virol Methods. 1994 Jun;48(1):43-52 PMID: 7962259
  22. Comparative morphology of Gag protein structures produced by mutants of the gag gene of human immunodeficiency virus type 1.
    J Gen Virol. 1994 Nov;75 ( Pt 11):2985-97 PMID: 7964608
  23. The p2 domain of human immunodeficiency virus type 1 Gag regulates sequential proteolytic processing and is required to produce fully infectious virions.
    J Virol. 1994 Dec;68(12):8017-27 PMID: 7966591
  24. Sequence requirements for encapsidation of deletion mutants and chimeras of human immunodeficiency virus type 1 Gag precursor into retrovirus-like particles.
    J Virol. 1995 Apr;69(4):2366-77 PMID: 7884882
  25. The human and simian immunodeficiency virus envelope glycoprotein transmembrane subunits are palmitoylated.
    Proc Natl Acad Sci U S A. 1995 Oct 10;92(21):9871-5 PMID: 7568235
  26. p6Gag is required for particle production from full-length human immunodeficiency virus type 1 molecular clones expressing protease.
    J Virol. 1995 Nov;69(11):6810-8 PMID: 7474093
  27. Crystal structure of SIV matrix antigen and implications for virus assembly.
    Nature. 1995 Dec 14;378(6558):743-7 PMID: 7501025
  28. Crystal structures of the trimeric human immunodeficiency virus type 1 matrix protein: implications for membrane association and assembly.
    Proc Natl Acad Sci U S A. 1996 Apr 2;93(7):3099-104 PMID: 8610175
  29. Glycoprotein incorporation and HIV-1 infectivity despite exchange of the gp160 membrane-spanning domain.
    Virology. 1996 Apr 1;218(1):269-74 PMID: 8615034
  30. High-resolution icosahedral reconstruction: fulfilling the promise of cryo-electron microscopy.
    Structure. 1997 Jun 15;5(6):741-50 PMID: 9261076
  31. Cryo-electron microscopy reveals ordered domains in the immature HIV-1 particle.
    Curr Biol. 1997 Oct 1;7(10):729-38 PMID: 9368755
  32. A putative alpha-helical structure which overlaps the capsid-p2 boundary in the human immunodeficiency virus type 1 Gag precursor is crucial for viral particle assembly.
    J Virol. 1998 Mar;72(3):2072-8 PMID: 9499062
  33. Particle size determinants in the human immunodeficiency virus type 1 Gag protein.
    J Virol. 1998 Jun;72(6):4667-77 PMID: 9573230
  34. Supramolecular organization of immature and mature murine leukemia virus revealed by electron cryo-microscopy: implications for retroviral assembly mechanisms.
    Proc Natl Acad Sci U S A. 1998 Jun 23;95(13):7299-304 PMID: 9636143
  35. Morphopoietic determinants of HIV-1 Gag particles assembled in baculovirus-infected cells.
    Virology. 1998 Aug 1;247(2):160-9 PMID: 9705909
  36. HIV-1 gag proteins: diverse functions in the virus life cycle.
    Virology. 1998 Nov 10;251(1):1-15 PMID: 9813197
  37. Further evidence for hexagonal organization of HIV gag protein in prebudding assemblies and immature virus-like particles.
    J Struct Biol. 1998 Oct;123(2):143-9 PMID: 9843668
  38. Actin associates with the nucleocapsid domain of the human immunodeficiency virus Gag polyprotein.
    J Virol. 1999 Mar;73(3):1931-40 PMID: 9971772
  39. Identification of retroviral late domains as determinants of particle size.
    J Virol. 1999 Mar;73(3):2309-20 PMID: 9971814
  40. In vitro assembly properties of wild-type and cyclophilin-binding defective human immunodeficiency virus capsid proteins in the presence and absence of cyclophilin A.
    Virology. 1999 Apr 25;257(1):247-60 PMID: 10208938
  41. Adding the third dimension to virus life cycles: three-dimensional reconstruction of icosahedral viruses from cryo-electron micrographs.
    Microbiol Mol Biol Rev. 1999 Dec;63(4):862-922, table of contents PMID: 10585969
  42. A symmetry mismatch at the site of RNA packaging in the polymerase complex of dsRNA bacteriophage phi6.
    J Mol Biol. 1999 Nov 26;294(2):357-72 PMID: 10610764
  43. A conformational switch controlling HIV-1 morphogenesis.
    EMBO J. 2000 Jan 4;19(1):103-13 PMID: 10619849
  44. The intact retroviral Env glycoprotein of human foamy virus is a trimer.
    J Virol. 2000 Mar;74(6):2885-7 PMID: 10684305
  45. Towards the structure of the human immunodeficiency virus: divide and conquer.
    Curr Opin Struct Biol. 1999 Apr;9(2):231-43 PMID: 10322217
  46. Size, shape and surface structure of mouse mammary tumour virus (MTV). Brief report.
    Arch Gesamte Virusforsch. 1973;41(3):284-9 PMID: 4125536
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
0022-538X
Published
2001-01-00
Pages
759-71
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC113972
Subset
IM
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