Home LiteratureArticle Details
PMID: 8970961 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Accessory human cytomegalovirus glycoprotein US9 in the unique short component of the viral genome promotes cell-to-cell transmission of virus in polarized epithelial cells.

Journal of virology ·Vol. 70 ·No. 12 ·1996-12-00 ·Pages 8402-10

Maidji E, Tugizov S, Jones T, Zheng Z, Pereira L

Abstract

Human cytomegalovirus (CMV) encodes accessory glycoproteins that are dispensable for virus growth in nonpolarized cells in culture. We report that CMV deletion mutants lacking the gene for accessory glycoprotein US9 in the unique short component of the viral genome are impaired in plaque formation in polarized human retinal pigment epithelial (ARPE-19) cells. Comparison of CMV deletion mutants in US9 with herpes simplex virus type 1 deletion mutants lacking glycoproteins gE and gI showed that both of these mutants are impaired in altering junctional complexes and increasing paracellular permeability in polarized ARPE-19 cells cultured on permeable filter supports. Results of functional studies indicate that CMV US9 and homologs of gE have analogous roles in promoting virus spread across lateral membranes of polarized epithelial cells.

MeSH Terms
Animals Cell Line Cytomegalovirus/genetics,metabolism Dogs Gene Deletion Glycoproteins/genetics,metabolism Herpesvirus 1, Human/genetics,metabolism Humans Pigment Epithelium of Eye/cytology,metabolism Viral Envelope Proteins/genetics,metabolism Viral Proteins/genetics,metabolism
Chemicals
Glycoproteins Viral Envelope Proteins Viral Proteins glycoprotein E, herpes simplex virus type 1
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Maidji E
Department of Stomatology, School of Dentistry, University of California San Francisco, 94143-0512, USA.
Tugizov S
Jones T
Zheng Z
Pereira L
References (65)
65 references, click to expand
  1. Bacterial pathogens caught in the actin.
    Curr Biol. 1992 Dec;2(12):649-51 PMID: 15336017
  2. A cytomegalovirus protein with properties of herpes simplex virus ICP8: partial purification of the polypeptide and map position of the gene.
    J Virol. 1987 Oct;61(10):3143-51 PMID: 3041036
  3. Accessory cholera enterotoxin (Ace), the third toxin of a Vibrio cholerae virulence cassette.
    Proc Natl Acad Sci U S A. 1993 Jun 1;90(11):5267-71 PMID: 8389476
  4. Sequence analysis of the 4.7-kb BamHI-EcoRI fragment of the equine herpesvirus type-1 short unique region.
    Gene. 1991 May 30;101(2):203-8 PMID: 1647359
  5. Cytomegalovirus replication in human retinal pigment epithelial cells. Altered expression of viral early proteins.
    Invest Ophthalmol Vis Sci. 1996 Apr;37(5):814-25 PMID: 8603866
  6. Cytomegalovirus infection in patients with AIDS.
    J Infect Dis. 1988 Aug;158(2):449-56 PMID: 2841381
  7. A 15-kilobase-pair region of the human cytomegalovirus genome which includes US1 through US13 is dispensable for growth in cell culture.
    J Virol. 1991 Oct;65(10):5184-9 PMID: 1654438
  8. Cytoskeletal disruption during human cytomegalovirus infection of human lung fibroblasts.
    Eur J Cell Biol. 1986 Aug;41(2):304-12 PMID: 3019700
  9. Domains of herpes simplex virus I glycoprotein B that function in virus penetration, cell-to-cell spread, and cell fusion.
    Virology. 1992 Jan;186(1):99-112 PMID: 1370130
  10. Specific pseudorabies virus infection of the rat visual system requires both gI and gp63 glycoproteins.
    J Virol. 1993 Jul;67(7):3786-97 PMID: 8389905
  11. The human cytomegalovirus US11 gene product dislocates MHC class I heavy chains from the endoplasmic reticulum to the cytosol.
    Cell. 1996 Mar 8;84(5):769-79 PMID: 8625414
  12. The structure and isomerization of herpes simplex virus genomes.
    Cell. 1979 Mar;16(3):481-94 PMID: 222462
  13. Role of apical and basolateral membranes in replication of human cytomegalovirus in polarized retinal pigment epithelial cells.
    J Gen Virol. 1996 Jan;77 ( Pt 1):61-74 PMID: 8558129
  14. Glycoproteins E and I facilitate neuron-to-neuron spread of herpes simplex virus.
    J Virol. 1995 Nov;69(11):7087-98 PMID: 7474128
  15. Zonula occludens toxin modulates tight junctions through protein kinase C-dependent actin reorganization, in vitro.
    J Clin Invest. 1995 Aug;96(2):710-20 PMID: 7635964
  16. Emergence of a new cholera pandemic: molecular analysis of virulence determinants in Vibrio cholerae O139 and development of a live vaccine prototype.
    J Infect Dis. 1994 Aug;170(2):278-83 PMID: 8035010
  17. Golgi-derived vesicles from developing epithelial cells bind actin filaments and possess myosin-I as a cytoplasmically oriented peripheral membrane protein.
    J Cell Biol. 1993 Jan;120(1):117-27 PMID: 8416982
  18. Cytomegalovirus replication in cultured human retinal pigment epithelial cells.
    Curr Eye Res. 1989 Aug;8(8):835-9 PMID: 2551575
  19. Rapid degradation of the heavy chain of class I major histocompatibility complex antigens in the endoplasmic reticulum of human cytomegalovirus-infected cells.
    J Virol. 1994 Dec;68(12):7933-43 PMID: 7966584
  20. Organization and function of the cytoskeleton in polarized epithelial cells: a component of the protein sorting machinery.
    Curr Opin Cell Biol. 1994 Feb;6(1):16-24 PMID: 8167021
  21. Two alpha-herpesvirus strains are transported differentially in the rodent visual system.
    Neuron. 1991 Jun;6(6):957-69 PMID: 1711350
  22. Actin cytoskeleton. Missing link for intracellular bacterial motility?
    Curr Biol. 1995 Aug 1;5(8):837-40 PMID: 7583135
  23. Polarity of epithelial and neuronal cells.
    Annu Rev Cell Biol. 1992;8:395-427 PMID: 1476804
  24. An analysis of the in vitro and in vivo phenotypes of mutants of herpes simplex virus type 1 lacking glycoproteins gG, gE, gI or the putative gJ.
    J Gen Virol. 1994 Jun;75 ( Pt 6):1245-58 PMID: 8207391
  25. Epithelial cell adhesion and development of cell surface polarity: possible mechanisms for modulation of cadherin function, organization and distribution.
    J Cell Sci Suppl. 1993;17:139-45 PMID: 8144690
  26. Complex between glycoproteins gI and gp63 of pseudorabies virus: its effect on virus replication.
    J Virol. 1988 Dec;62(12):4622-6 PMID: 2460638
  27. Herpes simplex virus glycoproteins E and I facilitate cell-to-cell spread in vivo and across junctions of cultured cells.
    J Virol. 1994 Feb;68(2):834-45 PMID: 8289387
  28. Multiple independent loci within the human cytomegalovirus unique short region down-regulate expression of major histocompatibility complex class I heavy chains.
    J Virol. 1995 Aug;69(8):4830-41 PMID: 7609050
  29. Actin-dependent organelle movement in squid axoplasm.
    Nature. 1992 Apr 23;356(6371):722-5 PMID: 1570018
  30. The DNA sequence of human herpesvirus-6: structure, coding content, and genome evolution.
    Virology. 1995 May 10;209(1):29-51 PMID: 7747482
  31. Vibrio cholerae produces a second enterotoxin, which affects intestinal tight junctions.
    Proc Natl Acad Sci U S A. 1991 Jun 15;88(12):5242-6 PMID: 2052603
  32. ARPE-19, a human retinal pigment epithelial cell line with differentiated properties.
    Exp Eye Res. 1996 Feb;62(2):155-69 PMID: 8698076
  33. Receptor properties of two varicella-zoster virus glycoproteins, gpI and gpIV, homologous to herpes simplex virus gE and gI.
    J Virol. 1992 Jun;66(6):3643-51 PMID: 1316474
  34. Fine mapping of transcripts expressed from the US6 gene family of human cytomegalovirus strain AD169.
    J Virol. 1991 Apr;65(4):2024-36 PMID: 1848316
  35. Structure, biochemistry, and assembly of epithelial tight junctions.
    Am J Physiol. 1987 Dec;253(6 Pt 1):C749-58 PMID: 3322036
  36. The UL10 gene of herpes simplex virus 1 encodes a novel viral glycoprotein, gM, which is present in the virion and in the plasma membrane of infected cells.
    J Virol. 1993 Mar;67(3):1441-52 PMID: 7679747
  37. The complete DNA sequence and the genetic organization of the short unique region (US) of the bovine herpesvirus type 1 (ST strain).
    Virology. 1994 Mar;199(2):409-21 PMID: 8122370
  38. Use of lambda gt11 to isolate genes for two pseudorabies virus glycoproteins with homology to herpes simplex virus and varicella-zoster virus glycoproteins.
    J Virol. 1986 Oct;60(1):185-93 PMID: 3018284
  39. Identification of a herpes simplex virus 1 glycoprotein gene within a gene cluster dispensable for growth in cell culture.
    Proc Natl Acad Sci U S A. 1987 Jun;84(12):4303-7 PMID: 3035578
  40. Role of a structural glycoprotein of pseudorabies in virus virulence.
    J Virol. 1987 Dec;61(12):4030-2 PMID: 2824832
  41. Actin-based bacterial motility.
    Curr Opin Cell Biol. 1995 Feb;7(1):94-101 PMID: 7755995
  42. Precise localization of genes on large animal virus genomes: use of lambda gt11 and monoclonal antibodies to map the gene for a cytomegalovirus protein family.
    Proc Natl Acad Sci U S A. 1985 Feb;82(4):1266-70 PMID: 2983334
  43. Monoclonal antibodies to human cytomegalovirus: three surface membrane proteins with unique immunological and electrophoretic properties specify cross-reactive determinants.
    Infect Immun. 1982 Jun;36(3):924-32 PMID: 6178693
  44. Glycoprotein B of human cytomegalovirus promotes virion penetration into cells, transmission of infection from cell to cell, and fusion of infected cells.
    Virology. 1993 Nov;197(1):143-58 PMID: 7692667
  45. Gene encoding zonula occludens toxin (zot) does not occur independently from cholera enterotoxin genes (ctx) in Vibrio cholerae.
    J Clin Microbiol. 1993 Mar;31(3):732-3 PMID: 8458975
  46. Complementation analysis of pseudorabies virus gE and gI mutants in retinal ganglion cell neurotropism.
    J Virol. 1994 Aug;68(8):5275-9 PMID: 8035525
  47. DNA sequence and expression of the B95-8 Epstein-Barr virus genome.
    Nature. 1984 Jul 19-25;310(5974):207-11 PMID: 6087149
  48. Analysis of the protein-coding content of the sequence of human cytomegalovirus strain AD169.
    Curr Top Microbiol Immunol. 1990;154:125-69 PMID: 2161319
  49. Replacement mutagenesis of the human cytomegalovirus genome: US10 and US11 gene products are nonessential.
    J Virol. 1991 Nov;65(11):5860-72 PMID: 1656074
  50. A cluster of dispensable genes within the human cytomegalovirus genome short component: IRS1, US1 through US5, and the US6 family.
    J Virol. 1992 Apr;66(4):2541-6 PMID: 1312642
  51. Function of glycoprotein B homologues of the family herpesviridae.
    Infect Agents Dis. 1994 Feb;3(1):9-28 PMID: 7952927
  52. The complete DNA sequence of varicella-zoster virus.
    J Gen Virol. 1986 Sep;67 ( Pt 9):1759-816 PMID: 3018124
  53. Safety, immunogenicity, and efficacy of live attenuated Vibrio cholerae O139 vaccine prototype.
    Lancet. 1995 Apr 15;345(8955):949-52 PMID: 7715293
  54. Construction and characterization of deletion mutants of pseudorabies virus: a new generation of 'live' vaccines.
    J Gen Virol. 1987 Feb;68 ( Pt 2):523-34 PMID: 3029289
  55. Intragenomic linear amplification of human herpesvirus 6B oriLyt suggests acquisition of oriLyt by transposition.
    J Virol. 1995 Jan;69(1):589-96 PMID: 7983761
  56. Pseudorabies virus envelope glycoprotein gI influences both neurotropism and virulence during infection of the rat visual system.
    J Virol. 1992 May;66(5):3032-41 PMID: 1313916
  57. Deletion mutants in human cytomegalovirus glycoprotein US9 are impaired in cell-cell transmission and in altering tight junctions of polarized human retinal pigment epithelial cells.
    Scand J Infect Dis Suppl. 1995;99:82-7 PMID: 8668948
  58. Herpes simplex virus immunoglobulin G Fc receptor activity depends on a complex of two viral glycoproteins, gE and gI.
    J Virol. 1988 Apr;62(4):1347-54 PMID: 2831396
  59. Cloning of a gene (zot) encoding a new toxin produced by Vibrio cholerae.
    Infect Immun. 1992 Feb;60(2):428-34 PMID: 1730472
  60. Effects of cytochalasin D on occluding junctions of intestinal absorptive cells: further evidence that the cytoskeleton may influence paracellular permeability and junctional charge selectivity.
    J Cell Biol. 1986 Jun;102(6):2125-36 PMID: 3711143
  61. Sequence determination and genetic content of the short unique region in the genome of herpes simplex virus type 1.
    J Mol Biol. 1985 Jan 5;181(1):1-13 PMID: 2984429
  62. A focal adhesion factor directly linking intracellularly motile Listeria monocytogenes and Listeria ivanovii to the actin-based cytoskeleton of mammalian cells.
    EMBO J. 1995 Apr 3;14(7):1314-21 PMID: 7729410
  63. Clustering of genes dispensable for growth in culture in the S component of the HSV-1 genome.
    Science. 1987 May 1;236(4801):573-6 PMID: 3033823
  64. Infection of polarized MDCK cells with herpes simplex virus 1: two asymmetrically distributed cell receptors interact with different viral proteins.
    Proc Natl Acad Sci U S A. 1991 Jun 15;88(12):5087-91 PMID: 1647025
  65. Actin-based motility of vaccinia virus.
    Nature. 1995 Dec 7;378(6557):636-8 PMID: 8524400
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
0022-538X
DOI
10.1128/JVI.70.12.8402-8410.1996
Published
1996-12-00
Pages
8402-10
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC190929
Subset
IM
Grants
NEI NIH HHS · EY10138 · United States
NEI NIH HHS · EY11223 · United States
External Links
PubMed source DOI: 10.1128/JVI.70.12.8402-8410.1996 PMC Full Text View journal details
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

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2