Identification and characterization of the herpes simplex virus type 2 gene encoding the essential capsid protein ICP32/VP19c.
Abstract
We describe the characterization of the herpes simplex virus type 2 (HSV-2) gene encoding infected cell protein 32 (ICP32) and virion protein 19c (VP19c). We also demonstrate that the HSV-1 UL38/ORF.553 open reading frame (ORF), which has been shown to specify a viral protein essential for capsid formation (B. Pertuiset, M. Boccara, J. Cebrian, N. Berthelot, S. Chousterman, F. Puvian-Dutilleul, J. Sisman, and P. Sheldrick, J. Virol. 63: 2169-2179, 1989), must encode the cognate HSV type 1 (HSV-1) ICP32/VP19c protein. The region of the HSV-2 genome deduced to contain the gene specifying ICP32/VP19c was isolated and subcloned, and the nucleotide sequence of 2,158 base pairs of HSV-2 DNA mapping immediately upstream of the gene encoding the large subunit of the viral ribonucleotide reductase was determined. This region of the HSV-2 genome contains a large ORF capable of encoding two related 50,538- and 49,472-molecular-weight polypeptides. Direct evidence that this ORF encodes HSV-2 ICP32/VP19c was provided by immunoblotting experiments that utilized antisera directed against synthetic oligopeptides corresponding to internal portions of the predicted polypeptides encoded by the HSV-2 ORF or antisera directed against a TrpE/HSV-2 ORF fusion protein. The type-common immunoreactivity of the two antisera and comparison of the primary amino acid sequences of the predicted products of the HSV-2 ORF and the equivalent genomic region of HSV-1 provided evidence that the HSV-1 UL38 ORF encodes the HSV-1 ICP32/VP19c. Analysis of the expression of the HSV-1 and HSV-2 ICP32/VP19c cognate proteins indicated that there may be differences in their modes of synthesis. Comparison of the predicted structure of the HSV-2 ICP32/VP19c protein with the structures of related proteins encoded by other herpes viruses suggested that the internal capsid architecture of the herpes family of viruses varies substantially.
Full text
Full text is available as a scanned copy of the original print version. Get a printable copy (PDF file) of the complete article (2.7M), or click on a page image below to browse page by page. Links to PubMed are also available for Selected References.
Images in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Ackermann M, Sarmiento M, Roizman B. Application of antibody to synthetic peptides for characterization of the intact and truncated alpha 22 protein specified by herpes simplex virus 1 and the R325 alpha 22- deletion mutant. J Virol. 1985 Oct;56(1):207–215. [PMC free article] [PubMed] [Google Scholar]
- Arsenakis M, Campadelli-Fiume G, Lombardo MT, Roizman B. The glycoprotein C gene of herpes simplex virus 1 resident in clonal L cell lines manifests two regulatory domains conferring a dominant B and a subordinate gamma 2 regulation. Virology. 1988 Feb;162(2):300–310. [PubMed] [Google Scholar]
- Baer R, Bankier AT, Biggin MD, Deininger PL, Farrell PJ, Gibson TJ, Hatfull G, Hudson GS, Satchwell SC, Séguin C, et al. DNA sequence and expression of the B95-8 Epstein-Barr virus genome. Nature. 1984 Jul 19;310(5974):207–211. [PubMed] [Google Scholar]
- Batterson W, Furlong D, Roizman B. Molecular genetics of herpes simplex virus. VIII. further characterization of a temperature-sensitive mutant defective in release of viral DNA and in other stages of the viral reproductive cycle. J Virol. 1983 Jan;45(1):397–407. [PMC free article] [PubMed] [Google Scholar]
- Batterson W, Roizman B. Characterization of the herpes simplex virion-associated factor responsible for the induction of alpha genes. J Virol. 1983 May;46(2):371–377. [PMC free article] [PubMed] [Google Scholar]
- Bejcek B, Conley AJ. A transforming plasmid from HSV-2 transformed cells contains rat DNA homologous to the HSV-1 and HSV-2 genomes. Virology. 1986 Oct 15;154(1):41–55. [PubMed] [Google Scholar]
- Biggin MD, Gibson TJ, Hong GF. Buffer gradient gels and 35S label as an aid to rapid DNA sequence determination. Proc Natl Acad Sci U S A. 1983 Jul;80(13):3963–3965. [PMC free article] [PubMed] [Google Scholar]
- Braun DK, Batterson W, Roizman B. Identification and genetic mapping of a herpes simplex virus capsid protein that binds DNA. J Virol. 1984 May;50(2):645–648. [PMC free article] [PubMed] [Google Scholar]
- Braun DK, Roizman B, Pereira L. Characterization of post-translational products of herpes simplex virus gene 35 proteins binding to the surfaces of full capsids but not empty capsids. J Virol. 1984 Jan;49(1):142–153. [PMC free article] [PubMed] [Google Scholar]
- Chase JW, Williams KR. Single-stranded DNA binding proteins required for DNA replication. Annu Rev Biochem. 1986;55:103–136. [PubMed] [Google Scholar]
- Chee M, Rudolph SA, Plachter B, Barrell B, Jahn G. Identification of the major capsid protein gene of human cytomegalovirus. J Virol. 1989 Mar;63(3):1345–1353. [PMC free article] [PubMed] [Google Scholar]
- Chou J, Roizman B. The terminal a sequence of the herpes simplex virus genome contains the promoter of a gene located in the repeat sequences of the L component. J Virol. 1986 Feb;57(2):629–637. [PMC free article] [PubMed] [Google Scholar]
- Chou PY, Fasman GD. Prediction of protein conformation. Biochemistry. 1974 Jan 15;13(2):222–245. [PubMed] [Google Scholar]
- Cohen FE, Abarbanel RM, Kuntz ID, Fletterick RJ. Secondary structure assignment for alpha/beta proteins by a combinatorial approach. Biochemistry. 1983 Oct 11;22(21):4894–4904. [PubMed] [Google Scholar]
- Cohen GH, Ponce de Leon M, Diggelmann H, Lawrence WC, Vernon SK, Eisenberg RJ. Structural analysis of the capsid polypeptides of herpes simplex virus types 1 and 2. J Virol. 1980 May;34(2):521–531. [PMC free article] [PubMed] [Google Scholar]
- Corey L, Whitley RJ, Stone EF, Mohan K. Difference between herpes simplex virus type 1 and type 2 neonatal encephalitis in neurological outcome. Lancet. 1988 Jan 2;1(8575-6):1–4. [PubMed] [Google Scholar]
- Davison AJ, Scott JE. The complete DNA sequence of varicella-zoster virus. J Gen Virol. 1986 Sep;67(Pt 9):1759–1816. [PubMed] [Google Scholar]
- Davison AJ, Scott JE. DNA sequence of the major capsid protein gene of herpes simplex virus type 1. J Gen Virol. 1986 Oct;67(Pt 10):2279–2286. [PubMed] [Google Scholar]
- Ejercito PM, Kieff ED, Roizman B. Characterization of herpes simplex virus strains differing in their effects on social behaviour of infected cells. J Gen Virol. 1968 May;2(3):357–364. [PubMed] [Google Scholar]
- Frenkel N, Jacob RJ, Honess RW, Hayward GS, Locker H, Roizman B. Anatomy of herpes simplex virus DNA. III. Characterization of defective DNA molecules and biological properties of virus populations containing them. J Virol. 1975 Jul;16(1):153–167. [PMC free article] [PubMed] [Google Scholar]
- Furlong D. Direct evidence for 6-fold symmetry of the herpesvirus hexon capsomere. Proc Natl Acad Sci U S A. 1978 Jun;75(6):2764–2766. [PMC free article] [PubMed] [Google Scholar]
- Galloway DA, Nelson JA, McDougall JK. Small fragments of herpesvirus DNA with transforming activity contain insertion sequence-like structures. Proc Natl Acad Sci U S A. 1984 Aug;81(15):4736–4740. [PMC free article] [PubMed] [Google Scholar]
- Geballe AP, Leach FS, Mocarski ES. Regulation of cytomegalovirus late gene expression: gamma genes are controlled by posttranscriptional events. J Virol. 1986 Mar;57(3):864–874. [PMC free article] [PubMed] [Google Scholar]
- Gibson W, Roizman B. Proteins specified by herpes simplex virus. 8. Characterization and composition of multiple capsid forms of subtypes 1 and 2. J Virol. 1972 Nov;10(5):1044–1052. [PMC free article] [PubMed] [Google Scholar]
- Gompels UA, Craxton MA, Honess RW. Conservation of glycoprotein H (gH) in herpesviruses: nucleotide sequence of the gH gene from herpesvirus saimiri. J Gen Virol. 1988 Nov;69(Pt 11):2819–2829. [PubMed] [Google Scholar]
- Heine JW, Honess RW, Cassai E, Roizman B. Proteins specified by herpes simplex virus. XII. The virion polypeptides of type 1 strains. J Virol. 1974 Sep;14(3):640–651. [PMC free article] [PubMed] [Google Scholar]
- Holland LE, Anderson KP, Shipman C, Jr, Wagner EK. Viral DNA synthesis is required for the efficient expression of specific herpes simplex virus type 1 mRNA species. Virology. 1980 Feb;101(1):10–24. [PubMed] [Google Scholar]
- Homa FL, Glorioso JC, Levine M. A specific 15-bp TATA box promoter element is required for expression of a herpes simplex virus type 1 late gene. Genes Dev. 1988 Jan;2(1):40–53. [PubMed] [Google Scholar]
- Homa FL, Otal TM, Glorioso JC, Levine M. Transcriptional control signals of a herpes simplex virus type 1 late (gamma 2) gene lie within bases -34 to +124 relative to the 5' terminus of the mRNA. Mol Cell Biol. 1986 Nov;6(11):3652–3666. [PMC free article] [PubMed] [Google Scholar]
- Honess RW. Herpes simplex and 'the herpes complex': diverse observations and a unifying hypothesis. The eighth Fleming lecture. J Gen Virol. 1984 Dec;65(Pt 12):2077–2107. [PubMed] [Google Scholar]
- Honess RW, Roizman B. Proteins specified by herpes simplex virus. XI. Identification and relative molar rates of synthesis of structural and nonstructural herpes virus polypeptides in the infected cell. J Virol. 1973 Dec;12(6):1347–1365. [PMC free article] [PubMed] [Google Scholar]
- Honess RW, Roizman B. Regulation of herpesvirus macromolecular synthesis. I. Cascade regulation of the synthesis of three groups of viral proteins. J Virol. 1974 Jul;14(1):8–19. [PMC free article] [PubMed] [Google Scholar]
- Honess RW, Roizman B. Regulation of herpesvirus macromolecular synthesis: sequential transition of polypeptide synthesis requires functional viral polypeptides. Proc Natl Acad Sci U S A. 1975 Apr;72(4):1276–1280. [PMC free article] [PubMed] [Google Scholar]
- Hopp TP, Woods KR. Prediction of protein antigenic determinants from amino acid sequences. Proc Natl Acad Sci U S A. 1981 Jun;78(6):3824–3828. [PMC free article] [PubMed] [Google Scholar]
- Jacobson JG, Martin SL, Coen DM. A conserved open reading frame that overlaps the herpes simplex virus thymidine kinase gene is important for viral growth in cell culture. J Virol. 1989 Apr;63(4):1839–1843. [PMC free article] [PubMed] [Google Scholar]
- Jariwalla RJ, Tanczos B, Jones C, Ortiz J, Salimi-Lopez S. DNA amplification and neoplastic transformation mediated by a herpes simplex DNA fragment containing cell-related sequences. Proc Natl Acad Sci U S A. 1986 Mar;83(6):1738–1742. [PMC free article] [PubMed] [Google Scholar]
- Johnson PA, Everett RD. The control of herpes simplex virus type-1 late gene transcription: a 'TATA-box'/cap site region is sufficient for fully efficient regulated activity. Nucleic Acids Res. 1986 Nov 11;14(21):8247–8264. [PMC free article] [PubMed] [Google Scholar]
- Kieff E, Hoyer B, Bachenheimer S, Roizman B. Genetic relatedness of type 1 and type 2 herpes simplex viruses. J Virol. 1972 May;9(5):738–745. [PMC free article] [PubMed] [Google Scholar]
- Knipe DM, Batterson W, Nosal C, Roizman B, Buchan A. Molecular genetics of herpes simplex virus. VI. Characterization of a temperature-sensitive mutant defective in the expression of all early viral gene products. J Virol. 1981 May;38(2):539–547. [PMC free article] [PubMed] [Google Scholar]
- Kozak M. Comparison of initiation of protein synthesis in procaryotes, eucaryotes, and organelles. Microbiol Rev. 1983 Mar;47(1):1–45. [PMC free article] [PubMed] [Google Scholar]
- Kozak M. Point mutations close to the AUG initiator codon affect the efficiency of translation of rat preproinsulin in vivo. Nature. 1984 Mar 15;308(5956):241–246. [PubMed] [Google Scholar]
- Kozak M. Point mutations define a sequence flanking the AUG initiator codon that modulates translation by eukaryotic ribosomes. Cell. 1986 Jan 31;44(2):283–292. [PubMed] [Google Scholar]
- Kyte J, Doolittle RF. A simple method for displaying the hydropathic character of a protein. J Mol Biol. 1982 May 5;157(1):105–132. [PubMed] [Google Scholar]
- Lipman DJ, Pearson WR. Rapid and sensitive protein similarity searches. Science. 1985 Mar 22;227(4693):1435–1441. [PubMed] [Google Scholar]
- Longnecker R, Chatterjee S, Whitley RJ, Roizman B. 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):4303–4307. [PMC free article] [PubMed] [Google Scholar]
- Longnecker R, Roizman B. Clustering of genes dispensable for growth in culture in the S component of the HSV-1 genome. Science. 1987 May 1;236(4801):573–576. [PubMed] [Google Scholar]
- Mavromara-Nazos P, Roizman B. Activation of herpes simplex virus 1 gamma 2 genes by viral DNA replication. Virology. 1987 Dec;161(2):593–598. [PubMed] [Google Scholar]
- McGeoch DJ, Dalrymple MA, Davison AJ, Dolan A, Frame MC, McNab D, Perry LJ, Scott JE, Taylor P. 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):1531–1574. [PubMed] [Google Scholar]
- McGeoch DJ, Moss HW, McNab D, Frame MC. DNA sequence and genetic content of the HindIII l region in the short unique component of the herpes simplex virus type 2 genome: identification of the gene encoding glycoprotein G, and evolutionary comparisons. J Gen Virol. 1987 Jan;68(Pt 1):19–38. [PubMed] [Google Scholar]
- McLauchlan J, Gaffney D, Whitton JL, Clements JB. The consensus sequence YGTGTTYY located downstream from the AATAAA signal is required for efficient formation of mRNA 3' termini. Nucleic Acids Res. 1985 Feb 25;13(4):1347–1368. [PMC free article] [PubMed] [Google Scholar]
- Messing J. New M13 vectors for cloning. Methods Enzymol. 1983;101:20–78. [PubMed] [Google Scholar]
- Mizusawa S, Nishimura S, Seela F. Improvement of the dideoxy chain termination method of DNA sequencing by use of deoxy-7-deazaguanosine triphosphate in place of dGTP. Nucleic Acids Res. 1986 Feb 11;14(3):1319–1324. [PMC free article] [PubMed] [Google Scholar]
- Morse LS, Pereira L, Roizman B, Schaffer PA. Anatomy of herpes simplex virus (HSV) DNA. X. Mapping of viral genes by analysis of polypeptides and functions specified by HSV-1 X HSV-2 recombinants. J Virol. 1978 May;26(2):389–410. [PMC free article] [PubMed] [Google Scholar]
- Pearson RE, Bejcek B, Conley AJ. A physical domain of herpes simplex virus ICP8 is expressed and active in Escherichia coli. J Virol. 1985 Feb;53(2):360–365. [PMC free article] [PubMed] [Google Scholar]
- Pertuiset B, Boccara M, Cebrian J, Berthelot N, Chousterman S, Puvion-Dutilleul F, Sisman J, Sheldrick P. Physical mapping and nucleotide sequence of a herpes simplex virus type 1 gene required for capsid assembly. J Virol. 1989 May;63(5):2169–2179. [PMC free article] [PubMed] [Google Scholar]
- Proudfoot NJ, Brownlee GG. 3' non-coding region sequences in eukaryotic messenger RNA. Nature. 1976 Sep 16;263(5574):211–214. [PubMed] [Google Scholar]
- Reyes GR, LaFemina R, Hayward SD, Hayward GS. Morphological transformation by DNA fragments of human herpesviruses: evidence for two distinct transforming regions in herpes simplex virus types 1 and 2 and lack of correlation with biochemical transfer of the thymidine kinase gene. Cold Spring Harb Symp Quant Biol. 1980;44(Pt 1):629–641. [PubMed] [Google Scholar]
- Robson B, Platt E, Finn PW, Millard P, Gibrat JF, Garnier J. Prediction of the conformation and antigenic determinants of the V-sis viral oncogene product homologous with human platelet-derived growth factor. Int J Pept Protein Res. 1985 Jan;25(1):1–8. [PubMed] [Google Scholar]
- Roizman B, Norrild B, Chan C, Pereira L. Identification and preliminary mapping with monoclonal antibodies of a herpes simplex virus 2 glycoprotein lacking a known type 1 counterpart. Virology. 1984 Feb;133(1):242–247. [PubMed] [Google Scholar]
- Roizman B, Spear PG. Preparation of herpes simplex virus of high titer. J Virol. 1968 Jan;2(1):83–84. [PMC free article] [PubMed] [Google Scholar]
- Sanger F, Nicklen S, Coulson AR. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. [PMC free article] [PubMed] [Google Scholar]
- Schrag JD, Prasad BV, Rixon FJ, Chiu W. Three-dimensional structure of the HSV1 nucleocapsid. Cell. 1989 Feb 24;56(4):651–660. [PubMed] [Google Scholar]
- Sherman G, Bachenheimer SL. Characterization of intranuclear capsids made by ts morphogenic mutants of HSV-1. Virology. 1988 Apr;163(2):471–480. [PubMed] [Google Scholar]
- Shillitoe EJ. Examination of herpes virus DNA sequences for patterns that resemble transposable elements. J Oral Pathol. 1988 Jan;17(1):21–25. [PubMed] [Google Scholar]
- Silver S, Roizman B. gamma 2-Thymidine kinase chimeras are identically transcribed but regulated a gamma 2 genes in herpes simplex virus genomes and as beta genes in cell genomes. Mol Cell Biol. 1985 Mar;5(3):518–528. [PMC free article] [PubMed] [Google Scholar]
- Staden R. An interactive graphics program for comparing and aligning nucleic acid and amino acid sequences. Nucleic Acids Res. 1982 May 11;10(9):2951–2961. [PMC free article] [PubMed] [Google Scholar]
- Staden R. Measurements of the effects that coding for a protein has on a DNA sequence and their use for finding genes. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 2):551–567. [PMC free article] [PubMed] [Google Scholar]
- Steven AC, Roberts CR, Hay J, Bisher ME, Pun T, Trus BL. Hexavalent capsomers of herpes simplex virus type 2: symmetry, shape, dimensions, and oligomeric status. J Virol. 1986 Feb;57(2):578–584. [PMC free article] [PubMed] [Google Scholar]
- Swain MA, Galloway DA. Herpes simplex virus specifies two subunits of ribonucleotide reductase encoded by 3'-coterminal transcripts. J Virol. 1986 Mar;57(3):802–808. [PMC free article] [PubMed] [Google Scholar]
- Tabor S, Richardson CC. DNA sequence analysis with a modified bacteriophage T7 DNA polymerase. Proc Natl Acad Sci U S A. 1987 Jul;84(14):4767–4771. [PMC free article] [PubMed] [Google Scholar]
- Tollefson AE, Wold WS. Identification and gene mapping of a 14,700-molecular-weight protein encoded by region E3 of group C adenoviruses. J Virol. 1988 Jan;62(1):33–39. [PMC free article] [PubMed] [Google Scholar]
- Vernon SK, Ponce de Leon M, Cohen GH, Eisenberg RJ, Rubin BA. Morphological components of herpesvirus. III. Localization of herpes simplex virus type 1 nucleocapsid polypeptides by immune electron microscopy. J Gen Virol. 1981 May;54(Pt 1):39–46. [PubMed] [Google Scholar]
- Voss JH, Roizman B. Properties of two 5'-coterminal RNAs transcribed part way and across the S component origin of DNA synthesis of the herpes simplex virus 1 genome. Proc Natl Acad Sci U S A. 1988 Nov;85(22):8454–8458. [PMC free article] [PubMed] [Google Scholar]
- Weyer U, Doerfler W. Species dependence of the major late promoter in adenovirus type 12 DNA. EMBO J. 1985 Nov;4(11):3015–3019. [PMC free article] [PubMed] [Google Scholar]
- Wilbur WJ, Lipman DJ. Rapid similarity searches of nucleic acid and protein data banks. Proc Natl Acad Sci U S A. 1983 Feb;80(3):726–730. [PMC free article] [PubMed] [Google Scholar]
- Wolf H, Roizman B. The regulations of gamma (structural) polypeptide synthesis in herpes simplex virus types 1 and 2 infected cells. IARC Sci Publ. 1978;(24 Pt 1):327–336. [PubMed] [Google Scholar]
- Zweig M, Heilman CJ, Jr, Hampar B. Identification of disulfide-linked protein complexes in the nucleocapsids of herpes simplex virus type 2. Virology. 1979 Apr 30;94(2):442–450. [PubMed] [Google Scholar]


