Skip to main content
PMC home page
Nucleic Acids Research logoLink to Nucleic Acids Research
. 1984 Mar 12;12(5):2473–2487. doi: 10.1093/nar/12.5.2473

A 3' co-terminal family of mRNAs from the herpes simplex virus type 1 short region: two overlapping reading frames encode unrelated polypeptide one of which has highly reiterated amino acid sequence.

F J Rixon, D J McGeoch
PMCID: PMC318677  PMID: 6324121

Abstract

We have used DNA sequencing, mRNA mapping and in vitro translation to characterise three partially overlapping genes in the genome of herpes simplex virus (HSV) type 1. These genes specify three mRNAs with distinct 5' termini but a common 3' terminus, the longest of which is immediate-early (IE) mRNA-5. The 12,000 MW (12K) IE polypeptide encoded by IEmRNA-5 is translated from an 88 codon open reading frame, leaving a 1200 base 3' non-translated region. The second mRNA (mRNA-B) is initiated within the coding sequence of IEmRNA-5, and encodes a 21K polypeptide. The 12K and 21K polypeptide coding regions do not overlap. The third mRNA (mRNA-C) is initiated within the coding region of mRNA-B, and encodes a 33K polypeptide. The reading frame for 33K has a 110 codon out-of-frame overlap with the 21K reading frame. This is the first instance of overlapping genes described for HSV. The 21K polypeptide is thought to be a DNA binding protein and is remarkable for an array of 24 tandem repeats of the sequence X/Pro/Arg (where X represents predominantly Glu, Asp, Thr, Ser or Val) in its C-terminal portion. This array, which occupies most of the region of overlap with 33K, can vary in repeat number between virus strains.

Full text

PDF
2484

Images in this article

2477Image
on p.2477
2479Image
on p.2479
2482Image
on p.2482

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Anderson K. P., Costa R. H., Holland L. E., Wagner E. K. Characterization of herpes simplex virus type 1 RNA present in the absence of de novo protein synthesis. J Virol. 1980 Apr;34(1):9–27. doi: 10.1128/jvi.34.1.9-27.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bayliss G. J., Marsden H. S., Hay J. Herpes simplex virus proteins: DNA-binding proteins in infected cells and in the virus structure. Virology. 1975 Nov;68(1):124–134. doi: 10.1016/0042-6822(75)90154-3. [DOI] [PubMed] [Google Scholar]
  3. Clements J. B., McLauchlan J., McGeoch D. J. Orientation of herpes simplex virus type 1 immediate early mRNA's. Nucleic Acids Res. 1979 Sep 11;7(1):77–91. doi: 10.1093/nar/7.1.77. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Clements J. B., Watson R. J., Wilkie N. M. Temporal regulation of herpes simplex virus type 1 transcription: location of transcripts on the viral genome. Cell. 1977 Sep;12(1):275–285. doi: 10.1016/0092-8674(77)90205-7. [DOI] [PubMed] [Google Scholar]
  5. Costa R. H., Draper K. G., Banks L., Powell K. L., Cohen G., Eisenberg R., Wagner E. K. High-resolution characterization of herpes simplex virus type 1 transcripts encoding alkaline exonuclease and a 50,000-dalton protein tentatively identified as a capsid protein. J Virol. 1983 Dec;48(3):591–603. doi: 10.1128/jvi.48.3.591-603.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Davison A. J., Wilkie N. M. Nucleotide sequences of the joint between the L and S segments of herpes simplex virus types 1 and 2. J Gen Virol. 1981 Aug;55(Pt 2):315–331. doi: 10.1099/0022-1317-55-2-315. [DOI] [PubMed] [Google Scholar]
  7. Fitzgerald M., Shenk T. The sequence 5'-AAUAAA-3'forms parts of the recognition site for polyadenylation of late SV40 mRNAs. Cell. 1981 Apr;24(1):251–260. doi: 10.1016/0092-8674(81)90521-3. [DOI] [PubMed] [Google Scholar]
  8. Gannon F., O'Hare K., Perrin F., LePennec J. P., Benoist C., Cochet M., Breathnach R., Royal A., Garapin A., Cami B. Organisation and sequences at the 5' end of a cloned complete ovalbumin gene. Nature. 1979 Mar 29;278(5703):428–434. doi: 10.1038/278428a0. [DOI] [PubMed] [Google Scholar]
  9. Garfinkel M. D., Pruitt R. E., Meyerowitz E. M. DNA sequences, gene regulation and modular protein evolution in the Drosophila 68C glue gene cluster. J Mol Biol. 1983 Aug 25;168(4):765–789. doi: 10.1016/s0022-2836(83)80074-6. [DOI] [PubMed] [Google Scholar]
  10. Godson G. N., Ellis J., Svec P., Schlesinger D. H., Nussenzweig V. Identification and chemical synthesis of a tandemly repeated immunogenic region of Plasmodium knowlesi circumsporozoite protein. Nature. 1983 Sep 1;305(5929):29–33. doi: 10.1038/305029a0. [DOI] [PubMed] [Google Scholar]
  11. Hall L. M., Draper K. G., Frink R. J., Costa R. H., Wagner E. K. Herpes simplex virus mRNA species mapping in EcoRI fragment I. J Virol. 1982 Aug;43(2):594–607. doi: 10.1128/jvi.43.2.594-607.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Jones P. C., Roizman B. Regulation of herpesvirus macromolecular synthesis. VIII. The transcription program consists of three phases during which both extent of transcription and accumulation of RNA in the cytoplasm are regulated. J Virol. 1979 Aug;31(2):299–314. doi: 10.1128/jvi.31.2.299-314.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Kozak M. Possible role of flanking nucleotides in recognition of the AUG initiator codon by eukaryotic ribosomes. Nucleic Acids Res. 1981 Oct 24;9(20):5233–5252. doi: 10.1093/nar/9.20.5233. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kumar A., Lindberg U. Characterization of messenger ribonucleoprotein and messenger RNA from KB cells. Proc Natl Acad Sci U S A. 1972 Mar;69(3):681–685. doi: 10.1073/pnas.69.3.681. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Lee G. T., Para M. F., Spear P. G. Location of the structural genes for glycoproteins gD and gE and for other polypeptides in the S component of herpes simplex virus type 1 DNA. J Virol. 1982 Jul;43(1):41–49. doi: 10.1128/jvi.43.1.41-49.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Marsden H. S., Lang J., Davison A. J., Hope R. G., MacDonald D. M. Genomic location and lack of phosphorylation of the HSV immediate-early polypeptide IE 12. J Gen Virol. 1982 Sep;62(Pt 1):17–27. doi: 10.1099/0022-1317-62-1-17. [DOI] [PubMed] [Google Scholar]
  17. Marsden H. S., Stow N. D., Preston V. G., Timbury M. C., Wilkie N. M. Physical mapping of herpes simplex virus-induced polypeptides. J Virol. 1978 Nov;28(2):624–642. doi: 10.1128/jvi.28.2.624-642.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. McLauchlan J., Clements J. B. Organization of the herpes simplex virus type 1 transcription unit encoding two early proteins with molecular weights of 140000 and 40000. J Gen Virol. 1983 May;64(Pt 5):997–1006. doi: 10.1099/0022-1317-64-5-997. [DOI] [PubMed] [Google Scholar]
  19. Messing J., Vieira J. A new pair of M13 vectors for selecting either DNA strand of double-digest restriction fragments. Gene. 1982 Oct;19(3):269–276. doi: 10.1016/0378-1119(82)90016-6. [DOI] [PubMed] [Google Scholar]
  20. Morse L. S., Buchman T. G., Roizman B., Schaffer P. A. Anatomy of herpes simplex virus DNA. IX. Apparent exclusion of some parental DNA arrangements in the generation of intertypic (HSV-1 X HSV-2) recombinants. J Virol. 1977 Oct;24(1):231–248. doi: 10.1128/jvi.24.1.231-248.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Murchie M. J., McGeoch D. J. DNA sequence analysis of an immediate-early gene region of the herpes simplex virus type 1 genome (map coordinates 0.950 to 0.978). J Gen Virol. 1982 Sep;62(Pt 1):1–15. doi: 10.1099/0022-1317-62-1-1. [DOI] [PubMed] [Google Scholar]
  22. Preston C. M. Control of herpes simplex virus type 1 mRNA synthesis in cells infected with wild-type virus or the temperature-sensitive mutant tsK. J Virol. 1979 Jan;29(1):275–284. doi: 10.1128/jvi.29.1.275-284.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Preston C. M., McGeoch D. J. Identification and mapping of two polypeptides encoded within the herpes simplex virus type 1 thymidine kinase gene sequences. J Virol. 1981 May;38(2):593–605. doi: 10.1128/jvi.38.2.593-605.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Rixon F. J., Campbell M. E., Clements J. B. The immediate-early mRNA that encodes the regulatory polypeptide Vmw 175 of herpes simplex virus type 1 is unspliced. EMBO J. 1982;1(10):1273–1277. doi: 10.1002/j.1460-2075.1982.tb00024.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Rixon F. J., Clements J. B. Detailed structural analysis of two spliced HSV-1 immediate-early mRNAs. Nucleic Acids Res. 1982 Apr 10;10(7):2241–2256. doi: 10.1093/nar/10.7.2241. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Sanger F., Coulson A. R., Barrell B. G., Smith A. J., Roe B. A. Cloning in single-stranded bacteriophage as an aid to rapid DNA sequencing. J Mol Biol. 1980 Oct 25;143(2):161–178. doi: 10.1016/0022-2836(80)90196-5. [DOI] [PubMed] [Google Scholar]
  27. Sheldrick P., Berthelot N. Inverted repetitions in the chromosome of herpes simplex virus. Cold Spring Harb Symp Quant Biol. 1975;39(Pt 2):667–678. doi: 10.1101/sqb.1974.039.01.080. [DOI] [PubMed] [Google Scholar]
  28. Soeda E., Arrand J. R., Smolar N., Walsh J. E., Griffin B. E. Coding potential and regulatory signals of the polyoma virus genome. Nature. 1980 Jan 31;283(5746):445–453. doi: 10.1038/283445a0. [DOI] [PubMed] [Google Scholar]
  29. Swanstrom R. I., Wagner E. K. Regulation of synthesis of herpes simplex type 1 virus mRNA during productive infection. Virology. 1974 Aug;60(2):522–533. doi: 10.1016/0042-6822(74)90346-8. [DOI] [PubMed] [Google Scholar]
  30. Twigg A. J., Sherratt D. Trans-complementable copy-number mutants of plasmid ColE1. Nature. 1980 Jan 10;283(5743):216–218. doi: 10.1038/283216a0. [DOI] [PubMed] [Google Scholar]
  31. Wadsworth S., Hayward G. S., Roizman B. Anatomy of herpes simplex virus DNA. V. Terminally repetitive sequences. J Virol. 1976 Feb;17(2):503–512. doi: 10.1128/jvi.17.2.503-512.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Warren K. G., Koprowski H., Lonsdale D. M., Brown S. M., Subak-Sharpe J. H. The polypeptide and the DNA restriction enzyme profiles of spontaneous isolates of herpes simplex virus type 1 from explants of human trigeminal, superior cervical and vagus ganglia. J Gen Virol. 1979 Apr;43(1):151–171. doi: 10.1099/0022-1317-43-1-151. [DOI] [PubMed] [Google Scholar]
  33. Watson R. J., Colberg-Poley A. M., Marcus-Sekura C. J., Carter B. J., Enquist L. W. Characterization of the herpes simplex virus type 1 glycoprotein D mRNA and expression of this protein in Xenopus oocytes. Nucleic Acids Res. 1983 Mar 11;11(5):1507–1522. doi: 10.1093/nar/11.5.1507. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Watson R. J., Preston C. M., Clements J. B. Separation and characterization of herpes simplex virus type 1 immediate-early mRNA's. J Virol. 1979 Jul;31(1):42–52. doi: 10.1128/jvi.31.1.42-52.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Watson R. J., Sullivan M., Vande Woude G. F. Structures of two spliced herpes simplex virus type 1 immediate-early mRNA's which map at the junctions of the unique and reiterated regions of the virus DNA S component. J Virol. 1981 Jan;37(1):431–444. doi: 10.1128/jvi.37.1.431-444.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Watson R. J., Umene K., Enquist L. W. Reiterated sequences within the intron of an immediate-early gene of herpes simplex virus type 1. Nucleic Acids Res. 1981 Aug 25;9(16):4189–4199. doi: 10.1093/nar/9.16.4189. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Watson R. J., Vande Woude G. F. DNA sequence of an immediate-early gene (IEmRNA-5) of herpes simplex virus type I. Nucleic Acids Res. 1982 Feb 11;10(3):979–991. doi: 10.1093/nar/10.3.979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Whitton J. L., Rixon F. J., Easton A. J., Clements J. B. Immediate-early mRNA-2 of herpes simplex viruses types 1 and 2 is unspliced: conserved sequences around the 5' and 3' termini correspond to transcription regulatory signals. Nucleic Acids Res. 1983 Sep 24;11(18):6271–6287. doi: 10.1093/nar/11.18.6271. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Wozney J., Hanahan D., Tate V., Boedtker H., Doty P. Structure of the pro alpha 2 (I) collagen gene. Nature. 1981 Nov 12;294(5837):129–135. doi: 10.1038/294129a0. [DOI] [PubMed] [Google Scholar]

Articles from Nucleic Acids Research are provided here courtesy of Oxford University Press

RESOURCES