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PMID: 8794291 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Targeting of glycoprotein I (gE) of varicella-zoster virus to the trans-Golgi network by an AYRV sequence and an acidic amino acid-rich patch in the cytosolic domain of the molecule.

Journal of virology ·Vol. 70 ·No. 10 ·1996-10-00 ·Pages 6563-75

Zhu Z, Hao Y, Gershon MD, Ambron RT, Gershon AA

Abstract

Previous studies suggested that varicella-zoster virus (VZV) envelope glycoproteins (gps) are selectively transported to the trans-Golgi network (TGN) and that the cytosolic domain of gpI (gE) targets it to the TGN. To identify targeting signals in the gpI cytosolic domain, intracellular protein trafficking was studied in transfected cells expressing chimeric proteins in which a full-length or mutated gpI cytosolic domain was fused to the gpI transmembrane domain and interleukin-2 receptor (tac) ectodomain. Expressed protein was visualized with antibodies to tac. A targeting sequence (AYRV) and a second, acidic amino acid-rich region of the gpI cytosolic domain (putative signal patch) were each sufficient to cause expressed protein to colocalize with TGN markers. This targeting was lost when the tyrosine of the AYRV sequence was replaced with glycine or lysine, when arginine was replaced with glutamic acid, or when valine was substituted with lysine. In contrast, tyrosine could be replaced by phenylalanine and valine could be substituted with leucine. Mutation of alanine to aspartic acid or deletion of alanine abolished TGN targeting. Exposure of transfected cells to antibodies to the tac ectodomain revealed that the TCN targeting of expressed tac-gpI chimeric proteins occurred as a result of selective retrieval from the plasmalemma. These data suggest that the AYRV sequence and a second signaling patch in the cytosolic domain of gpI are responsible for its targeting to the TGN. The observations also support the hypothesis that the TGN plays a critical role in the envelopment of VZV.

MeSH Terms
Amino Acid Sequence Cell Line Golgi Apparatus/metabolism,virology Herpesvirus 3, Human/metabolism Humans Molecular Sequence Data Sequence Analysis Viral Envelope Proteins/genetics,metabolism Virus Assembly
Chemicals
Viral Envelope Proteins
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Zhu Z
Department of Anatomy and Cell Biology, Columbia University College of Physicians and Surgeons, New York, New York, USA.
Hao Y
Gershon M D
Ambron R T
Gershon A A
References (29)
29 references, click to expand
  1. Herpesvirus envelopment.
    J Virol. 1968 Jan;2(1):48-55 PMID: 4316013
  2. Electron microscopic observations on the development of herpes simplex virus.
    J Exp Med. 1959 Oct 1;110:643-56 PMID: 14424096
  3. Immunology of the varicella-zoster virus glycoproteins.
    J Infect Dis. 1988 May;157(5):877-81 PMID: 2834465
  4. Molecular trapping of a fluorescent ceramide analogue at the Golgi apparatus of fixed cells: interaction with endogenous lipids provides a trans-Golgi marker for both light and electron microscopy.
    J Cell Biol. 1989 Nov;109(5):2067-79 PMID: 2478562
  5. The overexpressed human 46-kDa mannose 6-phosphate receptor mediates endocytosis and sorting of beta-glucuronidase.
    Proc Natl Acad Sci U S A. 1990 Oct;87(20):8036-40 PMID: 2172972
  6. Cation-dependent mannose 6-phosphate receptor contains two internalization signals in its cytoplasmic domain.
    Proc Natl Acad Sci U S A. 1990 Dec;87(24):10010-4 PMID: 2175900
  7. The recycling itinerary of the 46 kDa mannose 6-phosphate receptor--Golgi to late endosomes--coincides with that of the 215 kDa M6PR.
    Eur J Cell Biol. 1990 Dec;53(2):203-11 PMID: 1964415
  8. Perturbation of the morphology of the trans-Golgi network following Brefeldin A treatment: redistribution of a TGN-specific integral membrane protein, TGN38.
    J Cell Biol. 1992 Jan;116(1):85-94 PMID: 1730751
  9. Glycoproteins of varicella-zoster virus and their herpes simplex virus homologs.
    Rev Infect Dis. 1991 Nov-Dec;13 Suppl 11:S960-3 PMID: 1664135
  10. Identification, molecular characterization and immunolocalization of an isoform of the trans-Golgi-network (TGN)-specific integral membrane protein TGN38.
    Biochem J. 1992 Apr 15;283 ( Pt 2):313-6 PMID: 1575675
  11. A His-Leu-Leu sequence near the carboxyl terminus of the cytoplasmic domain of the cation-dependent mannose 6-phosphate receptor is necessary for the lysosomal enzyme sorting function.
    J Biol Chem. 1992 Aug 25;267(24):17110-5 PMID: 1324923
  12. Localization of TGN38 to the trans-Golgi network: involvement of a cytoplasmic tyrosine-containing sequence.
    J Cell Biol. 1993 Mar;120(5):1123-35 PMID: 8436587
  13. TGN38 is maintained in the trans-Golgi network by a tyrosine-containing motif in the cytoplasmic domain.
    EMBO J. 1993 May;12(5):2219-28 PMID: 8491209
  14. Pseudorabies virus infection of the rat central nervous system: ultrastructural characterization of viral replication, transport, and pathogenesis.
    J Neurosci. 1993 Jun;13(6):2515-39 PMID: 8388923
  15. Tail-specific antibodies that block return of 46,000 M(r) mannose 6-phosphate receptor to the trans-Golgi network.
    J Cell Biol. 1993 Aug;122(3):541-51 PMID: 7687604
  16. The SXYQRL sequence in the cytoplasmic domain of TGN38 plays a major role in trans-Golgi network localization.
    J Biol Chem. 1993 Oct 25;268(30):22853-62 PMID: 8226795
  17. Histochemical localization of copper in the intestine and kidney of macular mice: light and electron microscopic study.
    J Histochem Cytochem. 1993 Oct;41(10):1529-35 PMID: 8245411
  18. An electron microscopic study of TGN38/41 dynamics.
    J Cell Sci Suppl. 1993;17:41-7 PMID: 8144704
  19. The TGN38 glycoprotein contains two non-overlapping signals that mediate localization to the trans-Golgi network.
    J Cell Biol. 1994 Apr;125(2):253-68 PMID: 8163544
  20. Analysis of the co-localization of the insulin-responsive glucose transporter (GLUT4) and the trans Golgi network marker TGN38 within 3T3-L1 adipocytes.
    Biochem J. 1994 Jun 15;300 ( Pt 3):743-9 PMID: 8010955
  21. The cytoplasmic domain mediates localization of furin to the trans-Golgi network en route to the endosomal/lysosomal system.
    J Cell Biol. 1994 Sep;126(5):1157-72 PMID: 7914893
  22. Intracellular transport of newly synthesized varicella-zoster virus: final envelopment in the trans-Golgi network.
    J Virol. 1994 Oct;68(10):6372-90 PMID: 8083976
  23. 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
  24. Characterization of the exon structure of the Menkes disease gene using vectorette PCR.
    Genomics. 1995 Apr 10;26(3):437-42 PMID: 7607665
  25. 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
  26. Envelopment of varicella-zoster virus: targeting of viral glycoproteins to the trans-Golgi network.
    J Virol. 1995 Dec;69(12):7951-9 PMID: 7494308
  27. 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
  28. Cytoplasmic coat proteins involved in endosome function.
    Cell. 1995 Dec 1;83(5):703-13 PMID: 8521487
  29. The complete DNA sequence of varicella-zoster virus.
    J Gen Virol. 1986 Sep;67 ( Pt 9):1759-816 PMID: 3018124
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
0022-538X
Published
1996-10-00
Pages
6563-75
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC190697
Subset
IM
Grants
NIAID NIH HHS · AI 127187 · United States
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