Home LiteratureArticle Details
PMID: 9573219 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

The Us9 gene product of pseudorabies virus, an alphaherpesvirus, is a phosphorylated, tail-anchored type II membrane protein.

Journal of virology ·Vol. 72 ·No. 6 ·1998-06-00 ·Pages 4560-70

Brideau AD, Banfield BW, Enquist LW

Abstract

The Us9 gene is highly conserved among the alphaherpesviruses sequenced to date, yet its function remains unknown. In this report, we demonstrate that the pseudorabies virus (PRV) Us9 protein is present in infected cell lysates as several phosphorylated polypeptides ranging from 17 to 20 kDa. Synthesis is first detected at 6 h postinfection and is sensitive to the DNA synthesis inhibitor phosphonoacetic acid. Unlike the herpes simplex virus type 1 Us9 homolog, which was reported to be associated with nucleocapsids in the nuclei of infected cells (M. C. Frame, D. J. McGeoch, F. J. Rixon, A. C. Orr, and H. S. Marsden, Virology 150:321-332, 1986), PRV Us9 localizes to the secretory pathway (predominately to the Golgi apparatus) and not to the nucleus. By fusing the enhanced green fluorescent protein (EGFP) reporter molecule to the carboxy terminus of Us9, we demonstrated that Us9 not only is capable of targeting a Us9-EGFP fusion protein to the Golgi compartment but also is able to direct efficient incorporation of such chimeric molecules into infectious viral particles. Moreover, through protease digestion experiments with Us9-EGFP-containing viral particles, we demonstrated that the Us9 protein is inserted into the viral envelope as a type II, tail-anchored membrane protein.

MeSH Terms
Amino Acid Sequence Animals Cell Line Cloning, Molecular Herpesvirus 1, Suid/metabolism Intracellular Signaling Peptides and Proteins Lipoproteins/genetics,metabolism Membrane Proteins/genetics,metabolism Molecular Sequence Data Phosphoproteins/genetics,metabolism Phosphorylation Transfection Viral Proteins/genetics,metabolism
Chemicals
Intracellular Signaling Peptides and Proteins Lipoproteins Membrane Proteins Phosphoproteins US9 protein, Suid herpesvirus 1 Viral Proteins
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Brideau A D
Department of Molecular Biology, Princeton University, Princeton, New Jersey 08544, USA.
Banfield B W
Enquist L W
References (67)
67 references, click to expand
  1. A novel 115-kD peripheral membrane protein is required for intercisternal transport in the Golgi stack.
    J Cell Biol. 1992 Sep;118(5):1015-26 PMID: 1512287
  2. The abundance of the herpes simplex virus type 1 UL37 tegument protein in virus particles is closely controlled.
    J Gen Virol. 1997 Jan;78 ( Pt 1):189-94 PMID: 9010303
  3. Neurotropic properties of pseudorabies virus: uptake and transneuronal passage in the rat central nervous system.
    J Neurosci. 1990 Jun;10(6):1974-94 PMID: 2162388
  4. Structural and functional properties of the membrane binding segment of cytochrome b5.
    J Biol Chem. 1978 Nov 25;253(22):8203-9 PMID: 711746
  5. Deletions in vaccine strains of pseudorabies virus and their effect on synthesis of glycoprotein gp63.
    J Virol. 1986 Dec;60(3):1166-9 PMID: 3023669
  6. Respiratory syncytial virus envelope glycoprotein (G) has a novel structure.
    Nucleic Acids Res. 1985 Nov 11;13(21):7795-812 PMID: 4069997
  7. Characterization of pseudorabies virus mutants expressing carboxy-terminal truncations of gE: evidence for envelope incorporation, virulence, and neurotropism domains.
    J Virol. 1997 Sep;71(9):6455-64 PMID: 9261363
  8. Deletion of glycoprotein gE reduces the propagation of pseudorabies virus in the nervous system of mice after intranasal inoculation.
    Virology. 1996 May 1;219(1):279-84 PMID: 8623540
  9. Isolation and characterization of cDNA clones corresponding to transcripts from the BamHI H and F regions of the Epstein-Barr virus genome.
    J Virol. 1987 Sep;61(9):2902-9 PMID: 3039177
  10. The DNA sequence of equine herpesvirus-1.
    Virology. 1992 Jul;189(1):304-16 PMID: 1318606
  11. 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
  12. Nucleotide sequence analysis of a homologue of herpes simplex virus type 1 gene US9 found in the genome of simian herpes B virus.
    J Gen Virol. 1992 Jan;73 ( Pt 1):195-9 PMID: 1309859
  13. A C-terminally-anchored Golgi protein is inserted into the endoplasmic reticulum and then transported to the Golgi apparatus.
    Proc Natl Acad Sci U S A. 1995 May 23;92(11):5102-5 PMID: 7761455
  14. Pseudorabies virus infections in explants of porcine nasal mucosa.
    Res Vet Sci. 1991 Jan;50(1):45-53 PMID: 1646473
  15. Monensin inhibits the processing of herpes simplex virus glycoproteins, their transport to the cell surface, and the egress of virions from infected cells.
    J Virol. 1982 Sep;43(3):1102-12 PMID: 6292453
  16. Transport route for synaptobrevin via a novel pathway of insertion into the endoplasmic reticulum membrane.
    EMBO J. 1995 Jan 16;14(2):217-23 PMID: 7835332
  17. Genetic basis of the neurovirulence of pseudorabies virus.
    J Virol. 1984 Oct;52(1):198-205 PMID: 6090697
  18. Identification of two genes in the unique short region of pseudorabies virus; comparison with herpes simplex virus and varicella-zoster virus.
    J Gen Virol. 1990 Aug;71 ( Pt 8):1747-55 PMID: 2167928
  19. Ultrastructural analysis of the replication cycle of pseudorabies virus in cell culture: a reassessment.
    J Virol. 1997 Mar;71(3):2072-82 PMID: 9032339
  20. Envelopment of varicella-zoster virus: targeting of viral glycoproteins to the trans-Golgi network.
    J Virol. 1995 Dec;69(12):7951-9 PMID: 7494308
  21. The equine herpesvirus type 1 (EHV-1) homolog of herpes simplex virus type 1 US9 and the nature of a major deletion within the unique short segment of the EHV-1 KyA strain genome.
    Virology. 1992 Sep;190(1):307-15 PMID: 1326805
  22. Analysis of pseudorabies virus glycoprotein gIII localization and modification by using novel infectious viral mutants carrying unique EcoRI sites.
    J Virol. 1987 Oct;61(10):2962-72 PMID: 3041015
  23. Two alpha-herpesvirus strains are transported differentially in the rodent visual system.
    Neuron. 1991 Jun;6(6):957-69 PMID: 1711350
  24. Point mutations define a sequence flanking the AUG initiator codon that modulates translation by eukaryotic ribosomes.
    Cell. 1986 Jan 31;44(2):283-92 PMID: 3943125
  25. Host cell-specific growth advantage of pseudorabies virus with a deletion in the genome sequences encoding a structural glycoprotein.
    J Virol. 1988 Jan;62(1):12-9 PMID: 2824839
  26. The membrane-embedded segment of cytochrome b5 as studied by cross-linking with photoactivatable phospholipids. II. The nontransferable form.
    J Biol Chem. 1983 Aug 10;258(15):9136-42 PMID: 6874681
  27. Us9, a stable lysine-less herpes simplex virus 1 protein, is ubiquitinated before packaging into virions and associates with proteasomes.
    Proc Natl Acad Sci U S A. 1997 Dec 9;94(25):13973-8 PMID: 9391137
  28. Role of cytoplasmic vacuoles in varicella-zoster virus glycoprotein trafficking and virion envelopment.
    J Virol. 1988 Aug;62(8):2701-11 PMID: 2839696
  29. Morphogenesis of three pseudorabies virus strains in porcine nasal mucosa.
    Intervirology. 1991;32(6):327-37 PMID: 1657823
  30. A small open reading frame in pseudorabies virus and implications for evolutionary relationships between herpesviruses.
    Virology. 1987 Jul;159(1):193-5 PMID: 3037781
  31. Pseudorabies virus avirulent strains fail to express a major glycoprotein.
    J Virol. 1985 Oct;56(1):307-11 PMID: 2411950
  32. Characterization of foot-and-mouth disease virus gene products with antisera against bacterially synthesized fusion proteins.
    J Virol. 1986 Mar;57(3):983-91 PMID: 3005640
  33. Dissemination of wild-type and gC-, gE-and gI-deleted mutants of Aujeszky's disease virus in the maxillary nerve and trigeminal ganglion of pigs after intranasal inoculation.
    J Gen Virol. 1995 Aug;76 ( Pt 8):2063-6 PMID: 7636488
  34. Extracellular vaccinia virus envelope glycoprotein encoded by the A33R gene.
    J Virol. 1996 Jun;70(6):3753-62 PMID: 8648710
  35. Characterization of the genome of equine herpesvirus 1 subtype 2.
    J Gen Virol. 1988 Jul;69 ( Pt 7):1575-90 PMID: 2839595
  36. Transcriptional analysis of the short segment of the feline herpesvirus type 1 genome and insertional mutagenesis of a unique reading frame.
    Virology. 1995 Apr 20;208(2):704-11 PMID: 7747442
  37. Herpesvirus (pseudorabies virus) latency in swine: occurrence and physical state of viral DNA in neural tissues.
    Virology. 1986 Dec;155(2):600-13 PMID: 3024403
  38. Herpes simplex virus 2 UL45 is a type II membrane protein.
    J Virol. 1998 May;72(5):4430-3 PMID: 9557736
  39. The complete DNA sequence of the long unique region in the genome of herpes simplex virus type 1.
    J Gen Virol. 1988 Jul;69 ( Pt 7):1531-74 PMID: 2839594
  40. 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
  41. Retrieval of human cytomegalovirus glycoprotein B from the infected cell surface for virus envelopment.
    Arch Virol. 1996;141(3-4):557-72 PMID: 8645095
  42. Herpes-type virus of the frog renal adenocarcinoma. I. Virus development in tumor transplants maintained at low temperature.
    J Virol. 1969 Jul;4(1):75-93 PMID: 5808113
  43. Pseudorabies virus recombinants expressing functional virulence determinants gE and gI from bovine herpesvirus 1.1.
    J Virol. 1997 Apr;71(4):2731-9 PMID: 9060626
  44. Nucleotide sequence of the G protein gene of human respiratory syncytial virus reveals an unusual type of viral membrane protein.
    Proc Natl Acad Sci U S A. 1985 Jun;82(12):4075-9 PMID: 3858865
  45. Assembly of Bcl-2 into microsomal and outer mitochondrial membranes.
    J Biol Chem. 1994 Apr 1;269(13):9842-9 PMID: 8144576
  46. The scanning model for translation: an update.
    J Cell Biol. 1989 Feb;108(2):229-41 PMID: 2645293
  47. A simple and efficient method for direct cloning of PCR products using ddT-tailed vectors.
    Nucleic Acids Res. 1991 Mar 11;19(5):1156 PMID: 2020554
  48. Effect of brefeldin A on alphaherpesvirus membrane protein glycosylation and virus egress.
    J Virol. 1991 Mar;65(3):1066-81 PMID: 1847436
  49. The 10K virion phosphoprotein encoded by gene US9 from herpes simplex virus type 1.
    Virology. 1986 Apr 30;150(2):321-32 PMID: 3008413
  50. Deletions in the genomes of pseudorabies virus vaccine strains and existence of four isomers of the genomes.
    J Virol. 1984 Mar;49(3):970-9 PMID: 6321776
  51. Structure of the neuraminidase gene in human influenza virus A/PR/8/34.
    Nature. 1981 Mar 19;290(5803):213-7 PMID: 7010182
  52. Deleting valine-125 and cysteine-126 in glycoprotein gI of pseudorabies virus strain NIA-3 decreases plaque size and reduces virulence in mice.
    Arch Virol. 1993;131(3-4):251-64 PMID: 8394068
  53. The complete DNA sequence of varicella-zoster virus.
    J Gen Virol. 1986 Sep;67 ( Pt 9):1759-816 PMID: 3018124
  54. Vaccinia virus gene A36R encodes a M(r) 43-50 K protein on the surface of extracellular enveloped virus.
    Virology. 1994 Oct;204(1):376-90 PMID: 8091668
  55. A 12-residue-long polyleucine tail is sufficient to anchor synaptobrevin to the endoplasmic reticulum membrane.
    J Biol Chem. 1996 Mar 29;271(13):7583-6 PMID: 8631791
  56. The US 9, 10, 11, and 12 genes of herpes simplex virus type 1 are of no importance for its neurovirulence and latency in mice.
    Virology. 1993 May;194(1):419-23 PMID: 8386887
  57. A class of membrane proteins with a C-terminal anchor.
    Trends Cell Biol. 1993 Mar;3(3):72-5 PMID: 14731773
  58. 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
  59. Rapid redistribution of Golgi proteins into the ER in cells treated with brefeldin A: evidence for membrane cycling from Golgi to ER.
    Cell. 1989 Mar 10;56(5):801-13 PMID: 2647301
  60. The pseudorabies virus gII gene is closely related to the gB glycoprotein gene of herpes simplex virus.
    J Virol. 1987 Sep;61(9):2691-701 PMID: 3039163
  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. Microtubule-dependent retrograde transport of proteins into the ER in the presence of brefeldin A suggests an ER recycling pathway.
    Cell. 1990 Mar 9;60(5):821-36 PMID: 2178778
  63. Phosphorylation of the herpes simplex virus type 1 tegument protein VP22.
    Virology. 1996 Dec 1;226(1):140-5 PMID: 8941333
  64. A new technique for the assay of infectivity of human adenovirus 5 DNA.
    Virology. 1973 Apr;52(2):456-67 PMID: 4705382
  65. Post-translational modification of the tegument proteins (VP13 and VP14) of herpes simplex virus type 1 by glycosylation and phosphorylation.
    J Gen Virol. 1991 Nov;72 ( Pt 11):2771-5 PMID: 1658203
  66. An endoplasmic reticulum-retained herpes simplex virus glycoprotein H is absent from secreted virions: evidence for reenvelopment during egress.
    J Virol. 1996 Jul;70(7):4311-6 PMID: 8676453
  67. Contribution of single genes within the unique short region of Aujeszky's disease virus (suid herpesvirus type 1) to virulence, pathogenesis and immunogenicity.
    J Gen Virol. 1992 Feb;73 ( Pt 2):243-51 PMID: 1311354
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
0022-538X
Published
1998-06-00
Pages
4560-70
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC109967
Subset
IM
Grants
PHS HHS · 1RO133506 · United States
NIGMS NIH HHS · 5T32GM07312 · United States
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: [email protected]