Home LiteratureArticle Details
PMID: 14990685 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Budding of PPxY-containing rhabdoviruses is not dependent on host proteins TGS101 and VPS4A.

Journal of virology ·Vol. 78 ·No. 6 ·2004-03-00 ·Pages 2657-65

Irie T, Licata JM, McGettigan JP, Schnell MJ, Harty RN

Abstract

Viral matrix proteins of several enveloped RNA viruses play important roles in virus assembly and budding and are by themselves able to bud from the cell surface in the form of lipid-enveloped, virus-like particles (VLPs). Three motifs (PT/SAP, PPxY, and YxxL) have been identified as late budding domains (L-domains) responsible for efficient budding. L-domains can functionally interact with cellular proteins involved in vacuolar sorting (VPS4A and TSG101) and endocytic pathways (Nedd4), suggesting involvement of these pathways in virus budding. Ebola virus VP40 has overlapping PTAP and PPEY motifs, which can functionally interact with TSG101 and Nedd4, respectively. As for vesicular stomatitis virus (VSV), a PPPY motif within M protein can interact with Nedd4. In addition, M protein has a PSAP sequence downstream of the PPPY motif, but the function of PSAP in budding is not clear. In this study, we compared L-domain functions between Ebola virus and VSV by constructing a chimeric M protein (M40), in which the PPPY motif of VSV M is replaced by the L domains of VP40. The budding efficiency of M40 was 10-fold higher than that of wild-type (wt) M protein. Overexpression of a dominant negative mutant of VPS4A or depletion of cellular TSG101 reduced the budding of only M40-containing VLPs but not that of wt M VLPs or live VSV. These findings suggest that the PSAP motif of M protein is not critical for budding and that there are fundamental differences between PTAP-containing viruses (Ebola virus and human immunodeficiency virus type 1) and PPPY-containing viruses (VSV and rabies virus) regarding their dependence on specific host factors for efficient budding.

MeSH Terms
Adenosine Triphosphatases/genetics,metabolism Amino Acid Motifs Animals COS Cells Cell Line DNA-Binding Proteins/genetics,metabolism Ebolavirus/chemistry,growth & development Endosomal Sorting Complexes Required for Transport Humans Nucleoproteins/chemistry,metabolism Recombinant Fusion Proteins/genetics,metabolism Transcription Factors/genetics,metabolism Vesicular stomatitis Indiana virus/chemistry,growth & development Viral Core Proteins/chemistry,metabolism Viral Matrix Proteins/chemistry,genetics,metabolism Virion/metabolism Virus Assembly
Chemicals
DNA-Binding Proteins Endosomal Sorting Complexes Required for Transport M protein, Vesicular stomatitis virus Nucleoproteins Recombinant Fusion Proteins Transcription Factors Tsg101 protein Viral Core Proteins Viral Matrix Proteins nucleoprotein VP40, Ebola virus Adenosine Triphosphatases
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Irie Takashi
Department of Pathobiology, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, Pennsylvania 19104, USA.
Licata Jillian M
McGettigan James P
Schnell Matthias J
Harty Ronald N
References (60)
60 references, click to expand
  1. Evidence for budding of human immunodeficiency virus type 1 selectively from glycolipid-enriched membrane lipid rafts.
    J Virol. 2000 Apr;74(7):3264-72 PMID: 10708443
  2. Recombinant rabies virus as potential live-viral vaccines for HIV-1.
    Proc Natl Acad Sci U S A. 2000 Mar 28;97(7):3544-9 PMID: 10706640
  3. Infectivity of Moloney murine leukemia virus defective in late assembly events is restored by late assembly domains of other retroviruses.
    J Virol. 2000 Aug;74(16):7250-60 PMID: 10906179
  4. Mutations in the PPPY motif of vesicular stomatitis virus matrix protein reduce virus budding by inhibiting a late step in virion release.
    J Virol. 2000 Nov;74(21):9818-27 PMID: 11024108
  5. Proteasome inhibition interferes with gag polyprotein processing, release, and maturation of HIV-1 and HIV-2.
    Proc Natl Acad Sci U S A. 2000 Nov 21;97(24):13057-62 PMID: 11087859
  6. A role for ubiquitin ligase recruitment in retrovirus release.
    Proc Natl Acad Sci U S A. 2000 Nov 21;97(24):13063-8 PMID: 11087860
  7. Ubiquitin is part of the retrovirus budding machinery.
    Proc Natl Acad Sci U S A. 2000 Nov 21;97(24):13069-74 PMID: 11087861
  8. A PPxY motif within the VP40 protein of Ebola virus interacts physically and functionally with a ubiquitin ligase: implications for filovirus budding.
    Proc Natl Acad Sci U S A. 2000 Dec 5;97(25):13871-6 PMID: 11095724
  9. Ubiquitination of HIV-1 and MuLV Gag.
    Virology. 2000 Dec 5;278(1):111-21 PMID: 11112487
  10. Mammalian tumor susceptibility gene 101 (TSG101) and the yeast homologue, Vps23p, both function in late endosomal trafficking.
    Traffic. 2000 Mar;1(3):248-58 PMID: 11208108
  11. TSG101/mammalian VPS23 and mammalian VPS28 interact directly and are recruited to VPS4-induced endosomes.
    J Biol Chem. 2001 Apr 13;276(15):11735-42 PMID: 11134028
  12. Vesicular release of ebola virus matrix protein VP40.
    Virology. 2001 Apr 25;283(1):1-6 PMID: 11312656
  13. Ebola virus VP40-induced particle formation and association with the lipid bilayer.
    J Virol. 2001 Jun;75(11):5205-14 PMID: 11333902
  14. Tsg101, a homologue of ubiquitin-conjugating (E2) enzymes, binds the L domain in HIV type 1 Pr55(Gag).
    Proc Natl Acad Sci U S A. 2001 Jul 3;98(14):7724-9 PMID: 11427703
  15. Expression and immunogenicity of human immunodeficiency virus type 1 Gag expressed by a replication-competent rhabdovirus-based vaccine vector.
    J Virol. 2001 Sep;75(18):8724-32 PMID: 11507217
  16. Ubiquitin-dependent sorting into the multivesicular body pathway requires the function of a conserved endosomal protein sorting complex, ESCRT-I.
    Cell. 2001 Jul 27;106(2):145-55 PMID: 11511343
  17. Proteins related to the Nedd4 family of ubiquitin protein ligases interact with the L domain of Rous sarcoma virus and are required for gag budding from cells.
    Proc Natl Acad Sci U S A. 2001 Sep 25;98(20):11199-204 PMID: 11562473
  18. Tsg101 and the vacuolar protein sorting pathway are essential for HIV-1 budding.
    Cell. 2001 Oct 5;107(1):55-65 PMID: 11595185
  19. Rhabdoviruses and the cellular ubiquitin-proteasome system: a budding interaction.
    J Virol. 2001 Nov;75(22):10623-9 PMID: 11602704
  20. HIV-1 and Ebola virus encode small peptide motifs that recruit Tsg101 to sites of particle assembly to facilitate egress.
    Nat Med. 2001 Dec;7(12):1313-9 PMID: 11726971
  21. The late domain of human immunodeficiency virus type 1 p6 promotes virus release in a cell type-dependent manner.
    J Virol. 2002 Jan;76(1):105-17 PMID: 11739676
  22. Functional replacement and positional dependence of homologous and heterologous L domains in equine infectious anemia virus replication.
    J Virol. 2002 Feb;76(4):1569-77 PMID: 11799151
  23. Equine infectious anemia virus and the ubiquitin-proteasome system.
    J Virol. 2002 Mar;76(6):3038-44 PMID: 11861870
  24. Lipid raft microdomains: a gateway for compartmentalized trafficking of Ebola and Marburg viruses.
    J Exp Med. 2002 Mar 4;195(5):593-602 PMID: 11877482
  25. Viral late domains.
    J Virol. 2002 May;76(10):4679-87 PMID: 11967285
  26. Functional involvement of a novel Nedd4-like ubiquitin ligase on retrovirus budding.
    EMBO Rep. 2002 Jul;3(7):636-40 PMID: 12101095
  27. An ESCRT into the endosome.
    Mol Cell. 2002 Aug;10(2):215-6 PMID: 12191463
  28. Escrt-III: an endosome-associated heterooligomeric protein complex required for mvb sorting.
    Dev Cell. 2002 Aug;3(2):271-82 PMID: 12194857
  29. Endosome-associated complex, ESCRT-II, recruits transport machinery for protein sorting at the multivesicular body.
    Dev Cell. 2002 Aug;3(2):283-9 PMID: 12194858
  30. The PPPY motif of human T-cell leukemia virus type 1 Gag protein is required early in the budding process.
    J Virol. 2002 Oct;76(19):10024-9 PMID: 12208980
  31. Structure of the Tsg101 UEV domain in complex with the PTAP motif of the HIV-1 p6 protein.
    Nat Struct Biol. 2002 Nov;9(11):812-7 PMID: 12379843
  32. Overlapping motifs (PTAP and PPEY) within the Ebola virus VP40 protein function independently as late budding domains: involvement of host proteins TSG101 and VPS-4.
    J Virol. 2003 Feb;77(3):1812-9 PMID: 12525615
  33. Ebola virus matrix protein VP40 interaction with human cellular factors Tsg101 and Nedd4.
    J Mol Biol. 2003 Feb 14;326(2):493-502 PMID: 12559917
  34. Retroviruses have differing requirements for proteasome function in the budding process.
    J Virol. 2003 Mar;77(6):3384-93 PMID: 12610113
  35. Organization of the vesicular stomatitis virus glycoprotein into membrane microdomains occurs independently of intracellular viral components.
    J Virol. 2003 Apr;77(7):3985-92 PMID: 12634358
  36. Role of ESCRT-I in retroviral budding.
    J Virol. 2003 Apr;77(8):4794-804 PMID: 12663786
  37. Defects in human immunodeficiency virus budding and endosomal sorting induced by TSG101 overexpression.
    J Virol. 2003 Jun;77(11):6507-19 PMID: 12743307
  38. Basic residues of the helix six domain of influenza virus M1 involved in nuclear translocation of M1 can be replaced by PTAP and YPDL late assembly domain motifs.
    J Virol. 2003 Jun;77(12):7078-92 PMID: 12768027
  39. Equine infectious anemia virus utilizes host vesicular protein sorting machinery during particle release.
    J Virol. 2003 Aug;77(15):8440-7 PMID: 12857913
  40. Protein sorting into multivesicular endosomes.
    Curr Opin Cell Biol. 2003 Aug;15(4):446-55 PMID: 12892785
  41. The Mason-Pfizer monkey virus PPPY and PSAP motifs both contribute to virus release.
    J Virol. 2003 Sep;77(17):9474-85 PMID: 12915562
  42. Nedd4 regulates egress of Ebola virus-like particles from host cells.
    J Virol. 2003 Sep;77(18):9987-92 PMID: 12941909
  43. Lassa virus Z protein is a matrix protein and sufficient for the release of virus-like particles [corrected].
    J Virol. 2003 Oct;77(19):10700-5 PMID: 12970458
  44. AIP1/ALIX is a binding partner for HIV-1 p6 and EIAV p9 functioning in virus budding.
    Cell. 2003 Sep 19;114(6):689-99 PMID: 14505569
  45. The protein network of HIV budding.
    Cell. 2003 Sep 19;114(6):701-13 PMID: 14505570
  46. Divergent retroviral late-budding domains recruit vacuolar protein sorting factors by using alternative adaptor proteins.
    Proc Natl Acad Sci U S A. 2003 Oct 14;100(21):12414-9 PMID: 14519844
  47. Viral liposomes released from insect cells infected with recombinant baculovirus expressing the matrix protein of vesicular stomatitis virus.
    J Virol. 1993 Jul;67(7):4415-20 PMID: 8389938
  48. Membrane vesiculation function and exocytosis of wild-type and mutant matrix proteins of vesicular stomatitis virus.
    J Virol. 1995 May;69(5):3156-60 PMID: 7707543
  49. 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
  50. Fine mapping and characterization of the Rous sarcoma virus Pr76gag late assembly domain.
    J Virol. 1996 Aug;70(8):5695-700 PMID: 8764091
  51. Endosomal transport function in yeast requires a novel AAA-type ATPase, Vps4p.
    EMBO J. 1997 Apr 15;16(8):1820-31 PMID: 9155008
  52. Equine infectious anemia virus utilizes a YXXL motif within the late assembly domain of the Gag p9 protein.
    J Virol. 1997 Sep;71(9):6541-6 PMID: 9261374
  53. Ubiquitin is covalently attached to the p6Gag proteins of human immunodeficiency virus type 1 and simian immunodeficiency virus and to the p12Gag protein of Moloney murine leukemia virus.
    J Virol. 1998 Apr;72(4):2962-8 PMID: 9525617
  54. The Vps4p AAA ATPase regulates membrane association of a Vps protein complex required for normal endosome function.
    EMBO J. 1998 Jun 1;17(11):2982-93 PMID: 9606181
  55. Molecular events in the assembly of retrovirus particles.
    Adv Exp Med Biol. 1998;440:329-39 PMID: 9782300
  56. Equine infectious anemia virus Gag polyprotein late domain specifically recruits cellular AP-2 adapter protein complexes during virion assembly.
    J Virol. 1998 Dec;72(12):10218-21 PMID: 9811764
  57. Influenza viruses select ordered lipid domains during budding from the plasma membrane.
    J Biol Chem. 1999 Jan 22;274(4):2038-44 PMID: 9890962
  58. A proline-rich motif within the matrix protein of vesicular stomatitis virus and rabies virus interacts with WW domains of cellular proteins: implications for viral budding.
    J Virol. 1999 Apr;73(4):2921-9 PMID: 10074141
  59. Late domain function identified in the vesicular stomatitis virus M protein by use of rhabdovirus-retrovirus chimeras.
    J Virol. 1999 Apr;73(4):3359-65 PMID: 10074190
  60. Mutations altering the moloney murine leukemia virus p12 Gag protein affect virion production and early events of the virus life cycle.
    EMBO J. 1999 Sep 1;18(17):4700-10 PMID: 10469649
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
0022-538X
Published
2004-03-00
Pages
2657-65
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC353768
Subset
IM
Grants
NIAID NIH HHS · T32 AI007324 · United States
NIAID NIH HHS · AI49153 · United States
NIAID NIH HHS · R21 AI049153 · United States
NIAID NIH HHS · T32-AI007324 · United States
NIAID NIH HHS · R01 AI049153 · United States
NIAID NIH HHS · AI46499 · United States
NIAID NIH HHS · R01 AI046499 · United States
NIAID NIH HHS · AI53393 · United States
Corrections
ErratumIn
-
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