Home LiteratureArticle Details
PMID: 11222723 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

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].

Journal of virology ·Vol. 75 ·No. 6 ·2001-03-00 ·Pages 2982-92

Wyss S, Berlioz-Torrent C, Boge M, Blot G, Höning S, Benarous R, Thali M

Abstract

Short amino acid sequences in the cytosolic domains of transmembrane proteins are recognized by specialized adaptor [corrected] proteins which are part of coated vesicles utilized to transport membrane proteins between the trans-Golgi network (TGN) and the plasma membrane (forward and backward). Previously, we and others reported that the membrane-proximal tyrosine residues Y712 (human immunodeficiency virus [HIV]) and Y721 (simian immunodeficiency virus [SIV]) in the envelope glycoprotein (Env) of the primate lentiviruses are crucial for the association of Env with clathrin-associated adaptor [corrected] complex AP-2. The same tyrosine-based endocytosis motifs in the cytosolic domains (EnvCD) of transmembrane gp41 of HIV type 1 (HIV-1) and SIV, respectively, were also shown to modulate the interaction with TGN- and endosome-based clathrin-associated complex AP-1. Our findings suggested that EnvCD binding to AP-1, unlike the association of EnvCD with AP-2, is dependent largely on residues other than Y712 and Y721. Here, we tested if motifs downstream of Y712 affect HIV-1 EnvCD-AP-1 binding and Env trafficking. Mutational analysis revealed that the C-terminal leucine-based motif in Env was crucial for the recruitment of AP-1 in vitro and in Env-expressing cells. In addition to affecting Env-AP-1 association, mutations at the C terminus of Env also altered the subcellular localization of Env, suggesting that proper post-Golgi routing of Env depends on its recruitment of AP-1. Finally, the C-terminal dileucine was shown to assist the membrane-proximal Y712 motif in restricting the cell surface expression of Env.

MeSH Terms
Adaptor Protein Complex delta Subunits Amino Acid Motifs Amino Acid Sequence Gene Expression Regulation, Viral Gene Products, env/chemistry,genetics,metabolism Genes, env HIV-1/chemistry,metabolism HeLa Cells Humans Leucine/chemistry,genetics Membrane Proteins/genetics,metabolism Molecular Sequence Data Mutation Signal Transduction Subcellular Fractions/metabolism Transfection
Chemicals
Adaptor Protein Complex delta Subunits Gene Products, env Membrane Proteins Leucine
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Wyss S
Institute of Microbiology, University of Lausanne, CH-1011 Lausanne, Switzerland.
Berlioz-Torrent C
Boge M
Blot G
Höning S
Benarous R
Thali M
References (50)
50 references, click to expand
  1. Mechanisms of protein sorting and coat assembly: insights from the clathrin-coated vesicle pathway.
    Curr Opin Cell Biol. 1998 Aug;10(4):499-503 PMID: 9719871
  2. Polarized distribution of viral envelope proteins in the plasma membrane of infected epithelial cells.
    Cell. 1980 May;20(1):45-54 PMID: 6248236
  3. Roles for endocytosis in lentiviral replication.
    Trends Cell Biol. 1997 Jan;7(1):1-4 PMID: 17708890
  4. A di-leucine-based motif in the cytoplasmic tail of LIMP-II and tyrosinase mediates selective binding of AP-3.
    EMBO J. 1998 Aug 10;17(5):1304-14 PMID: 9482728
  5. Mannose 6-phosphate receptors regulate the formation of clathrin-coated vesicles in the TGN.
    J Cell Biol. 1997 Apr 21;137(2):335-45 PMID: 9128246
  6. Human immunodeficiency virus type 2 glycoprotein enhancement of particle budding: role of the cytoplasmic domain.
    J Virol. 1996 Apr;70(4):2669-73 PMID: 8642705
  7. Multimerization potential of the cytoplasmic domain of the human immunodeficiency virus type 1 transmembrane glycoprotein gp41.
    J Biol Chem. 2000 May 26;275(21):15809-19 PMID: 10747937
  8. Mu1B, a novel adaptor medium chain expressed in polarized epithelial cells.
    FEBS Lett. 1999 Apr 23;449(2-3):215-20 PMID: 10338135
  9. Regulation and function of the CD3gamma DxxxLL motif: a binding site for adaptor protein-1 and adaptor protein-2 in vitro.
    J Cell Biol. 1997 Jul 28;138(2):271-81 PMID: 9230070
  10. Human immunodeficiency virus type 1 envelope protein endocytosis mediated by a highly conserved intrinsic internalization signal in the cytoplasmic domain of gp41 is suppressed in the presence of the Pr55gag precursor protein.
    J Virol. 1996 Oct;70(10):6547-56 PMID: 8794289
  11. An internalization signal in the simian immunodeficiency virus transmembrane protein cytoplasmic domain modulates expression of envelope glycoproteins on the cell surface.
    J Cell Biol. 1996 Mar;132(5):795-811 PMID: 8603913
  12. Recognition of sorting signals by clathrin adaptors.
    Bioessays. 1999 Jul;21(7):558-67 PMID: 10472183
  13. A membrane-proximal tyrosine-based signal mediates internalization of the HIV-1 envelope glycoprotein via interaction with the AP-2 clathrin adaptor.
    J Biol Chem. 1998 Jun 19;273(25):15773-8 PMID: 9624176
  14. A single amino acid change in the cytoplasmic domain of the simian immunodeficiency virus transmembrane molecule increases envelope glycoprotein expression on infected cells.
    J Virol. 1995 Sep;69(9):5217-27 PMID: 7636963
  15. Protein sorting by tyrosine-based signals: adapting to the Ys and wherefores.
    Trends Cell Biol. 1997 Mar;7(3):124-8 PMID: 17708922
  16. Endocytosis of endogenously synthesized HIV-1 envelope protein. Mechanism and role in processing for association with class II MHC.
    J Immunol. 1995 Jul 1;155(1):473-88 PMID: 7602119
  17. Specific interactions between retrovirus Env and Gag proteins in rat neurons.
    J Virol. 1998 Apr;72(4):2832-45 PMID: 9525603
  18. Catch the mu1B train to the basolateral surface.
    Cell. 1999 Oct 15;99(2):121-2 PMID: 10535730
  19. Localization of furin to the trans-Golgi network and recycling from the cell surface involves Ser and Tyr residues within the cytoplasmic domain.
    J Biol Chem. 1995 Nov 24;270(47):28397-401 PMID: 7499343
  20. In vitro binding of clathrin adaptors to sorting signals correlates with endocytosis and basolateral sorting.
    EMBO J. 1996 Jun 3;15(11):2893-9 PMID: 8654387
  21. Linking cargo to vesicle formation: receptor tail interactions with coat proteins.
    Curr Opin Cell Biol. 1997 Aug;9(4):488-95 PMID: 9261055
  22. 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
  23. Clathrin and adaptors.
    Biochim Biophys Acta. 1998 Aug 14;1404(1-2):173-93 PMID: 9714795
  24. Sorting of furin at the trans-Golgi network. Interaction of the cytoplasmic tail sorting signals with AP-1 Golgi-specific assembly proteins.
    J Biol Chem. 1999 Mar 19;274(12):8199-207 PMID: 10075724
  25. Human immunodeficiency virus type 1 Nef associates with a cellular serine kinase in T lymphocytes.
    Proc Natl Acad Sci U S A. 1994 Feb 15;91(4):1539-43 PMID: 8108442
  26. A role for acidic residues in di-leucine motif-based targeting to the endocytic pathway.
    J Biol Chem. 1995 Aug 25;270(34):19989-97 PMID: 7650016
  27. Dileucine-based sorting signals bind to the beta chain of AP-1 at a site distinct and regulated differently from the tyrosine-based motif-binding site.
    EMBO J. 1998 Apr 15;17(8):2148-55 PMID: 9545228
  28. A novel clathrin adaptor complex mediates basolateral targeting in polarized epithelial cells.
    Cell. 1999 Oct 15;99(2):189-98 PMID: 10535737
  29. Endocytosis and molecular sorting.
    Annu Rev Cell Dev Biol. 1996;12:575-625 PMID: 8970738
  30. 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
  31. Molecular bases for the recognition of tyrosine-based sorting signals.
    J Cell Biol. 1999 May 31;145(5):923-6 PMID: 10352010
  32. The intracytoplasmic domain of gp41 mediates polarized budding of human immunodeficiency virus type 1 in MDCK cells.
    J Virol. 1994 Aug;68(8):4857-61 PMID: 8035484
  33. 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
  34. The membrane-proximal intracytoplasmic tyrosine residue of HIV-1 envelope glycoprotein is critical for basolateral targeting of viral budding in MDCK cells.
    EMBO J. 1997 Feb 17;16(4):695-705 PMID: 9049299
  35. An acidic sequence within the cytoplasmic domain of furin functions as a determinant of trans-Golgi network localization and internalization from the cell surface.
    EMBO J. 1995 Oct 16;14(20):4961-75 PMID: 7588625
  36. Regulation of virus release by the macrophage-tropic human immunodeficiency virus type 1 AD8 isolate is redundant and can be controlled by either Vpu or Env.
    J Virol. 1999 Feb;73(2):887-96 PMID: 9882289
  37. Coats and vesicle budding.
    Trends Cell Biol. 1997 Mar;7(3):99-102 PMID: 17708916
  38. The tyrosine-based lysosomal targeting signal in lamp-1 mediates sorting into Golgi-derived clathrin-coated vesicles.
    EMBO J. 1996 Oct 1;15(19):5230-9 PMID: 8895568
  39. Real-time biospecific interaction analysis using surface plasmon resonance and a sensor chip technology.
    Biotechniques. 1991 Nov;11(5):620-7 PMID: 1804254
  40. Two independent targeting signals in the cytoplasmic domain determine trans-Golgi network localization and endosomal trafficking of the proprotein convertase furin.
    EMBO J. 1995 Jun 1;14(11):2424-35 PMID: 7781597
  41. The simian immunodeficiency virus envelope glycoprotein contains multiple signals that regulate its cell surface expression and endocytosis.
    Traffic. 2000 Aug;1(8):661-74 PMID: 11208154
  42. A novel di-leucine motif and a tyrosine-based motif independently mediate lysosomal targeting and endocytosis of CD3 chains.
    Cell. 1992 Jun 26;69(7):1143-57 PMID: 1535555
  43. Interactions of the AP-1 Golgi adaptor with the polymeric immunoglobulin receptor and their possible role in mediating brefeldin A-sensitive basolateral targeting from the trans-Golgi network.
    J Biol Chem. 1999 Jan 22;274(4):2201-15 PMID: 9890983
  44. Endocytosis in viral replication.
    Traffic. 2000 Jul;1(7):525-32 PMID: 11208139
  45. Intracellular trafficking of furin is modulated by the phosphorylation state of a casein kinase II site in its cytoplasmic tail.
    EMBO J. 1995 Dec 1;14(23):5869-83 PMID: 8846780
  46. Human immunodeficiency virus envelope protein determines the site of virus release in polarized epithelial cells.
    Proc Natl Acad Sci U S A. 1991 May 1;88(9):3987-91 PMID: 2023946
  47. 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
  48. In polarized MDCK cells basolateral vesicles arise from clathrin-gamma-adaptin-coated domains on endosomal tubules.
    J Cell Biol. 1998 May 4;141(3):611-23 PMID: 9566963
  49. 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
  50. Polarized human immunodeficiency virus budding in lymphocytes involves a tyrosine-based signal and favors cell-to-cell viral transmission.
    J Virol. 1999 Jun;73(6):5010-7 PMID: 10233963
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
0022-538X
Published
2001-03-00
Pages
2982-92
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC115924
Subset
IM
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