Home LiteratureArticle Details
PMID: 17538020 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

The clathrin adaptor complex AP-1 binds HIV-1 and MLV Gag and facilitates their budding.

Molecular biology of the cell ·Vol. 18 ·No. 8 ·2007-08-00 ·Pages 3193-203

Camus G, Segura-Morales C, Molle D, Lopez-Vergès S, Begon-Pescia C, Cazevieille C, Schu P, Bertrand E, Berlioz-Torrent C, Basyuk E

Abstract

Retroviral assembly is driven by Gag, and nascent viral particles escape cells by recruiting the machinery that forms intralumenal vesicles of multivesicular bodies. In this study, we show that the clathrin adaptor complex AP-1 is involved in retroviral release. The absence of AP-1mu obtained by genetic knock-out or by RNA interference reduces budding of murine leukemia virus (MLV) and HIV-1, leading to a delay of viral propagation in cell culture. In contrast, overexpression of AP-1mu enhances release of HIV-1 Gag. We show that the AP-1 complex facilitates retroviral budding through a direct interaction between the matrix and AP-1mu. Less MLV Gag is found associated with late endosomes in cells lacking AP-1, and our results suggest that AP-1 and AP-3 could function on the same pathway that leads to Gag release. In addition, we find that AP-1 interacts with Tsg101 and Nedd4.1, two cellular proteins known to be involved in HIV-1 and MLV budding. We propose that AP-1 promotes Gag release by transporting it to intracellular sites of active budding, and/or by facilitating its interactions with other cellular partners.

MeSH Terms
Adaptor Protein Complex 1/metabolism Adaptor Protein Complex 3/metabolism Adaptor Protein Complex mu Subunits/metabolism Animals Carrier Proteins/metabolism DNA-Binding Proteins/metabolism Endosomal Sorting Complexes Required for Transport Gene Products, gag/metabolism HIV-1/physiology,ultrastructure HeLa Cells Humans Leukemia Virus, Murine/physiology Mice Mutation/genetics Protein Binding Protein Transport Rats Transcription Factors/metabolism Two-Hybrid System Techniques Virus Replication
Chemicals
Adaptor Protein Complex 1 Adaptor Protein Complex 3 Adaptor Protein Complex mu Subunits Carrier Proteins DNA-Binding Proteins Endosomal Sorting Complexes Required for Transport Gene Products, gag Transcription Factors Tsg101 protein
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Camus Grégory
Institut Cochin, Université Paris Descartes, Centre National de la Recherche Scientifique (UMR 8104), Paris, France.
Segura-Morales Carolina
Molle Dorothee
Lopez-Vergès Sandra
Begon-Pescia Christina
Cazevieille Chantal
Schu Peter
Bertrand Edouard
Berlioz-Torrent Clarisse
Basyuk Eugenia
References (77)
77 references, click to expand
  1. Mechanism of Nef-induced CD4 endocytosis: Nef connects CD4 with the mu chain of adaptor complexes.
    EMBO J. 1998 May 1;17(9):2472-81 PMID: 9564030
  2. Efficient HIV-1 replication can occur in the absence of the viral matrix protein.
    EMBO J. 1998 May 1;17(9):2699-708 PMID: 9564051
  3. Nef interacts with the mu subunit of clathrin adaptor complexes and reveals a cryptic sorting signal in MHC I molecules.
    Immunity. 1998 Apr;8(4):483-95 PMID: 9586638
  4. A dileucine motif in HIV-1 Nef acts as an internalization signal for CD4 downregulation and binds the AP-1 clathrin adaptor.
    Curr Biol. 1998 Nov 5;8(22):1235-8 PMID: 9811606
  5. A dileucine motif in HIV-1 Nef is essential for sorting into clathrin-coated pits and for downregulation of CD4.
    Curr Biol. 1998 Nov 5;8(22):1239-42 PMID: 9811611
  6. Interactions of the cytoplasmic domains of human and simian retroviral transmembrane proteins with components of the clathrin adaptor complexes modulate intracellular and cell surface expression of envelope glycoproteins.
    J Virol. 1999 Feb;73(2):1350-61 PMID: 9882340
  7. Differential use of two AP-3-mediated pathways by lysosomal membrane proteins.
    Traffic. 2004 Dec;5(12):946-62 PMID: 15522097
  8. Retrovirus budding.
    Virus Res. 2004 Dec;106(2):87-102 PMID: 15567490
  9. HECT ubiquitin ligases link viral and cellular PPXY motifs to the vacuolar protein-sorting pathway.
    J Cell Biol. 2005 Jan 3;168(1):89-101 PMID: 15623582
  10. The trans-Golgi network-associated human ubiquitin-protein ligase POSH is essential for HIV type 1 production.
    Proc Natl Acad Sci U S A. 2005 Feb 1;102(5):1478-83 PMID: 15659549
  11. AP-1 and AP-3 facilitate lysosomal targeting of Batten disease protein CLN3 via its dileucine motif.
    J Biol Chem. 2005 Mar 18;280(11):10277-83 PMID: 15598649
  12. AP-3 directs the intracellular trafficking of HIV-1 Gag and plays a key role in particle assembly.
    Cell. 2005 Mar 11;120(5):663-74 PMID: 15766529
  13. Tsg101 and Alix interact with murine leukemia virus Gag and cooperate with Nedd4 ubiquitin ligases during budding.
    J Biol Chem. 2005 Jul 22;280(29):27004-12 PMID: 15908698
  14. The protein network of HIV budding.
    Cell. 2003 Sep 19;114(6):701-13 PMID: 14505570
  15. 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
  16. Regulation of membrane protein transport by ubiquitin and ubiquitin-binding proteins.
    Annu Rev Cell Dev Biol. 2003;19:141-72 PMID: 14570567
  17. Sorting it out: AP-2 and alternate clathrin adaptors in endocytic cargo selection.
    J Cell Biol. 2003 Oct 27;163(2):203-8 PMID: 14581447
  18. PPPYVEPTAP motif is the late domain of human T-cell leukemia virus type 1 Gag and mediates its functional interaction with cellular proteins Nedd4 and Tsg101 [corrected].
    J Virol. 2003 Nov;77(22):11882-95 PMID: 14581525
  19. Visualization of retroviral replication in living cells reveals budding into multivesicular bodies.
    Traffic. 2003 Nov;4(11):785-801 PMID: 14617360
  20. HIV-1 egress is gated through late endosomal membranes.
    Traffic. 2003 Dec;4(12):902-10 PMID: 14617353
  21. Recognition of dileucine-based sorting signals from HIV-1 Nef and LIMP-II by the AP-1 gamma-sigma1 and AP-3 delta-sigma3 hemicomplexes.
    J Cell Biol. 2003 Dec 22;163(6):1281-90 PMID: 14691137
  22. Cell-type-dependent targeting of human immunodeficiency virus type 1 assembly to the plasma membrane and the multivesicular body.
    J Virol. 2004 Feb;78(3):1552-63 PMID: 14722309
  23. Role of LBPA and Alix in multivesicular liposome formation and endosome organization.
    Science. 2004 Jan 23;303(5657):531-4 PMID: 14739459
  24. The Nedd4 family of E3 ubiquitin ligases: functional diversity within a common modular architecture.
    Oncogene. 2004 Mar 15;23(11):1972-84 PMID: 15021885
  25. Role of protein ubiquitylation in regulating endocytosis of receptor tyrosine kinases.
    Oncogene. 2004 Mar 15;23(11):2057-70 PMID: 15021893
  26. An AP-1/clathrin coat plays a novel and essential role in forming the Weibel-Palade bodies of endothelial cells.
    J Cell Biol. 2005 Aug 15;170(4):627-36 PMID: 16087708
  27. Role of the endocytic machinery in the sorting of lysosome-associated membrane proteins.
    Mol Biol Cell. 2005 Sep;16(9):4231-42 PMID: 15987739
  28. Functions of adaptor protein (AP)-3 and AP-1 in tyrosinase sorting from endosomes to melanosomes.
    Mol Biol Cell. 2005 Nov;16(11):5356-72 PMID: 16162817
  29. Interaction of HIV-1 Gag with the clathrin-associated adaptor AP-2.
    Virology. 2005 Nov 25;342(2):190-200 PMID: 16139856
  30. EGF stimulates annexin 1-dependent inward vesiculation in a multivesicular endosome subpopulation.
    EMBO J. 2006 Jan 11;25(1):1-12 PMID: 16052208
  31. An essential role for SNX1 in lysosomal sorting of protease-activated receptor-1: evidence for retromer-, Hrs-, and Tsg101-independent functions of sorting nexins.
    Mol Biol Cell. 2006 Mar;17(3):1228-38 PMID: 16407403
  32. A lumenal domain-dependent pathway for sorting to intralumenal vesicles of multivesicular endosomes involved in organelle morphogenesis.
    Dev Cell. 2006 Mar;10(3):343-54 PMID: 16516837
  33. Identification of an intracellular trafficking and assembly pathway for HIV-1 gag.
    Traffic. 2006 Jun;7(6):731-45 PMID: 16683918
  34. The ESCRT complexes: structure and mechanism of a membrane-trafficking network.
    Annu Rev Biophys Biomol Struct. 2006;35:277-98 PMID: 16689637
  35. Regulation of functional diversity within the Nedd4 family by accessory and adaptor proteins.
    Bioessays. 2006 Jun;28(6):617-28 PMID: 16700065
  36. Assembly of infectious HIV-1 in human epithelial and T-lymphoblastic cell lines.
    J Mol Biol. 2006 Jun 16;359(4):848-62 PMID: 16682056
  37. Endosomal and non-endosomal functions of ESCRT proteins.
    Trends Cell Biol. 2006 Jun;16(6):317-26 PMID: 16716591
  38. Clathrin-associated adaptor protein complexes.
    J Cell Sci. 2006 Sep 15;119(Pt 18):3719-21 PMID: 16959901
  39. 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
  40. Role of adaptor complex AP-3 in targeting wild-type and mutated CD63 to lysosomes.
    Mol Biol Cell. 2002 Mar;13(3):1071-82 PMID: 11907283
  41. Viral late domains.
    J Virol. 2002 May;76(10):4679-87 PMID: 11967285
  42. Functional involvement of a novel Nedd4-like ubiquitin ligase on retrovirus budding.
    EMBO Rep. 2002 Jul;3(7):636-40 PMID: 12101095
  43. Escrt-III: an endosome-associated heterooligomeric protein complex required for mvb sorting.
    Dev Cell. 2002 Aug;3(2):271-82 PMID: 12194857
  44. 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
  45. Cooperation of GGAs and AP-1 in packaging MPRs at the trans-Golgi network.
    Science. 2002 Sep 6;297(5587):1700-3 PMID: 12215646
  46. Human macrophages accumulate HIV-1 particles in MHC II compartments.
    Traffic. 2002 Oct;3(10):718-29 PMID: 12230470
  47. AP-1A and AP-3A lysosomal sorting functions.
    Traffic. 2002 Oct;3(10):752-61 PMID: 12230473
  48. Visualization of TGN to endosome trafficking through fluorescently labeled MPR and AP-1 in living cells.
    Mol Biol Cell. 2003 Jan;14(1):142-55 PMID: 12529433
  49. Morphology and dynamics of clathrin/GGA1-coated carriers budding from the trans-Golgi network.
    Mol Biol Cell. 2003 Apr;14(4):1545-57 PMID: 12686608
  50. Human ESCRT-II complex and its role in human immunodeficiency virus type 1 release.
    J Virol. 2006 Oct;80(19):9465-80 PMID: 16973552
  51. Vesicle formation at the plasma membrane and trans-Golgi network: the same but different.
    Science. 2006 Sep 15;313(5793):1591-4 PMID: 16973870
  52. Gamma-adaptin, a novel ubiquitin-interacting adaptor, and Nedd4 ubiquitin ligase control hepatitis B virus maturation.
    J Biol Chem. 2006 Sep 29;281(39):29297-308 PMID: 16867982
  53. Tail-interacting protein TIP47 is a connector between Gag and Env and is required for Env incorporation into HIV-1 virions.
    Proc Natl Acad Sci U S A. 2006 Oct 3;103(40):14947-52 PMID: 17003132
  54. The conserved dileucine- and tyrosine-based motifs in MLV and MPMV envelope glycoproteins are both important to regulate a common Env intracellular trafficking.
    Retrovirology. 2006;3:62 PMID: 16978406
  55. Plasma membrane is the site of productive HIV-1 particle assembly.
    PLoS Biol. 2006 Dec;4(12):e435 PMID: 17147474
  56. HIV-1 buds predominantly at the plasma membrane of primary human macrophages.
    PLoS Pathog. 2007 Mar;3(3):e36 PMID: 17381240
  57. mu1A-adaptin-deficient mice: lethality, loss of AP-1 binding and rerouting of mannose 6-phosphate receptors.
    EMBO J. 2000 May 15;19(10):2193-203 PMID: 10811610
  58. 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
  59. The highly conserved C-terminal dileucine motif in the cytosolic domain of the human immunodeficiency virus type 1 envelope glycoprotein is critical for its association with the AP-1 clathrin adaptor [correction of adapter].
    J Virol. 2001 Mar;75(6):2982-92 PMID: 11222723
  60. 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
  61. 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
  62. Tsg101 and the vacuolar protein sorting pathway are essential for HIV-1 budding.
    Cell. 2001 Oct 5;107(1):55-65 PMID: 11595185
  63. Targeting of the human immunodeficiency virus type 1 envelope to the trans-Golgi network through binding to TIP47 is required for env incorporation into virions and infectivity.
    J Virol. 2003 Jun;77(12):6931-45 PMID: 12768012
  64. Retroviral genomic RNAs are transported to the plasma membrane by endosomal vesicles.
    Dev Cell. 2003 Jul;5(1):161-74 PMID: 12852860
  65. Infectious HIV-1 assembles in late endosomes in primary macrophages.
    J Cell Biol. 2003 Aug 4;162(3):443-55 PMID: 12885763
  66. The Mason-Pfizer monkey virus PPPY and PSAP motifs both contribute to virus release.
    J Virol. 2003 Sep;77(17):9474-85 PMID: 12915562
  67. The M-PMV cytoplasmic targeting-retention signal directs nascent Gag polypeptides to a pericentriolar region of the cell.
    Traffic. 2003 Oct;4(10):660-70 PMID: 12956869
  68. M-PMV capsid transport is mediated by Env/Gag interactions at the pericentriolar recycling endosome.
    Traffic. 2003 Oct;4(10):671-80 PMID: 12956870
  69. 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
  70. Localization of the AP-3 adaptor complex defines a novel endosomal exit site for lysosomal membrane proteins.
    J Cell Biol. 2004 Mar 29;164(7):1065-76 PMID: 15051738
  71. Late assembly motifs of human T-cell leukemia virus type 1 and their relative roles in particle release.
    J Virol. 2004 Jun;78(12):6636-48 PMID: 15163754
  72. Retrovirus budding.
    Annu Rev Cell Dev Biol. 2004;20:395-425 PMID: 15473846
  73. 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
  74. The GAG precursor of simian immunodeficiency virus assembles into virus-like particles.
    EMBO J. 1989 Sep;8(9):2653-60 PMID: 2684654
  75. Alteration of intracellular traffic by monensin; mechanism, specificity and relationship to toxicity.
    Biochim Biophys Acta. 1990 May 7;1031(2):225-46 PMID: 2160275
  76. WW domains and retrovirus budding.
    Nature. 1996 Jun 27;381(6585):744-5 PMID: 8657277
  77. Interaction of endocytic signals from the HIV-1 envelope glycoprotein complex with members of the adaptor medium chain family.
    Virology. 1997 Nov 24;238(2):305-15 PMID: 9400603
Article Info
Journal
Molecular biology of the cell
Abbr.
Mol Biol Cell
ISSN
1059-1524
Published
2007-08-00
Epub
2007-00-30
Pages
3193-203
Language
English
Region
United States
NLM ID
9201390
PMCID
PMC1949356
Subset
IM
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