Skip to main content
Journal of Virology logoLink to Journal of Virology
. 1987 Jan;61(1):35–41. doi: 10.1128/jvi.61.1.35-41.1987

5'-terminal sequences influence the segregation of ground squirrel hepatitis virus RNAs into polyribosomes and viral core particles.

G H Enders, D Ganem, H E Varmus
PMCID: PMC255195  PMID: 2431165

Abstract

To determine which of the major ground squirrel hepatitis virus RNAs serve as mRNAs and which serve as templates for reverse transcription of the genome, we analyzed the subcellular distribution of these RNAs in livers of infected ground squirrels. Both major classes of viral RNA, the 2.3- and 3.5-kilobase (kb) classes, are unspliced, are polyadenylated at a common position, and display heterogeneous 5' ends that can encode proteins with different amino termini (G.H. Enders, D. Ganem, and H. Varmus, Cell 42:297-308, 1985). Both of the 2.3-kb RNAs, which encode surface antigens, appear to be predominantly associated with polyribosomes. Of the three 3.5-kb RNAs, the two longer, which can encode a protein initiated from the first methionine codon in the core antigen gene, appear to be predominantly associated with polyribosomes, and a minority of the shortest 3.5-kb RNAs, which can encode a protein initiated from the second methionine in the core antigen gene, appears to be associated with polyribosomes. This last RNA is instead found predominantly within viral core particles, consistent with evidence that indirectly implicates it in two steps of viral DNA synthesis (C. Seeger, D. Ganem, and H.E. Varmus, Science 232:477-484, 1986). None of the other viral RNAs is detectably packaged into cores. These findings provide independent evidence that the shortest 3.5-kb RNA is the template for synthesis of the viral genome and reveal a novel selectivity in viral RNA packaging.

Full text

PDF
41

Images in this article

Selected References

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

  1. Adelman M. R., Sabatini D. D., Blobel G. Ribosome-membrane interaction. Nondestructive disassembly of rat liver rough microsomes into ribosomal and membranous components. J Cell Biol. 1973 Jan;56(1):206–229. doi: 10.1083/jcb.56.1.206. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Beasley R. P., Hwang L. Y., Lin C. C., Chien C. S. Hepatocellular carcinoma and hepatitis B virus. A prospective study of 22 707 men in Taiwan. Lancet. 1981 Nov 21;2(8256):1129–1133. doi: 10.1016/s0140-6736(81)90585-7. [DOI] [PubMed] [Google Scholar]
  3. Büscher M., Reiser W., Will H., Schaller H. Transcripts and the putative RNA pregenome of duck hepatitis B virus: implications for reverse transcription. Cell. 1985 Mar;40(3):717–724. doi: 10.1016/0092-8674(85)90220-x. [DOI] [PubMed] [Google Scholar]
  4. Enders G. H., Ganem D., Varmus H. Mapping the major transcripts of ground squirrel hepatitis virus: the presumptive template for reverse transcriptase is terminally redundant. Cell. 1985 Aug;42(1):297–308. doi: 10.1016/s0092-8674(85)80125-2. [DOI] [PubMed] [Google Scholar]
  5. Feitelson M. A., Marion P. L., Robinson W. S. Core particles of hepatitis B virus and ground squirrel hepatitis virus. I. Relationship between hepatitis B core antigen- and ground squirrel hepatitis core antigen-associated polypeptides by sodium dodecyl sulfate-polyacrylamide gel electrophoresis and tryptic peptide mapping. J Virol. 1982 Aug;43(2):687–696. doi: 10.1128/jvi.43.2.687-696.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Ganem D., Greenbaum L., Varmus H. E. Virion DNA of ground squirrel hepatitis virus: structural analysis and molecular cloning. J Virol. 1982 Oct;44(1):374–383. doi: 10.1128/jvi.44.1.374-383.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Ganem D. Persistent infection of humans with hepatitis B virus: mechanisms and consequences. Rev Infect Dis. 1982 Sep-Oct;4(5):1026–1047. doi: 10.1093/clinids/4.5.1026. [DOI] [PubMed] [Google Scholar]
  8. Gerlich W. H., Robinson W. S. Hepatitis B virus contains protein attached to the 5' terminus of its complete DNA strand. Cell. 1980 Oct;21(3):801–809. doi: 10.1016/0092-8674(80)90443-2. [DOI] [PubMed] [Google Scholar]
  9. Jacks T., Varmus H. E. Expression of the Rous sarcoma virus pol gene by ribosomal frameshifting. Science. 1985 Dec 13;230(4731):1237–1242. doi: 10.1126/science.2416054. [DOI] [PubMed] [Google Scholar]
  10. Katze M. G., Chen Y. T., Krug R. M. Nuclear-cytoplasmic transport and VAI RNA-independent translation of influenza viral messenger RNAs in late adenovirus-infected cells. Cell. 1984 Jun;37(2):483–490. doi: 10.1016/0092-8674(84)90378-7. [DOI] [PubMed] [Google Scholar]
  11. Lien J. M., Aldrich C. E., Mason W. S. Evidence that a capped oligoribonucleotide is the primer for duck hepatitis B virus plus-strand DNA synthesis. J Virol. 1986 Jan;57(1):229–236. doi: 10.1128/jvi.57.1.229-236.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Mann R., Baltimore D. Varying the position of a retrovirus packaging sequence results in the encapsidation of both unspliced and spliced RNAs. J Virol. 1985 May;54(2):401–407. doi: 10.1128/jvi.54.2.401-407.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Miller R. H., Marion P. L., Robinson W. S. Hepatitis B viral DNA-RNA hybrid molecules in particles from infected liver are converted to viral DNA molecules during an endogenous DNA polymerase reaction. Virology. 1984 Nov;139(1):64–72. doi: 10.1016/0042-6822(84)90330-1. [DOI] [PubMed] [Google Scholar]
  14. Miller R. H., Tran C. T., Robinson W. S. Hepatitis B virus particles of plasma and liver contain viral DNA-RNA hybrid molecules. Virology. 1984 Nov;139(1):53–63. doi: 10.1016/0042-6822(84)90329-5. [DOI] [PubMed] [Google Scholar]
  15. Möröy T., Etiemble J., Trépo C., Tiollais P., Buendia M. A. Transcription of woodchuck hepatitis virus in the chronically infected liver. EMBO J. 1985 Jun;4(6):1507–1514. doi: 10.1002/j.1460-2075.1985.tb03810.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Ohori H., Yamaki M., Onodera S., Yamada E., Ishida N. Antigenic conversion from HBcAg to HBeAg by degradation of hepatitis B core particles. Intervirology. 1980;13(2):74–82. doi: 10.1159/000149110. [DOI] [PubMed] [Google Scholar]
  17. Ou J. H., Laub O., Rutter W. J. Hepatitis B virus gene function: the precore region targets the core antigen to cellular membranes and causes the secretion of the e antigen. Proc Natl Acad Sci U S A. 1986 Mar;83(6):1578–1582. doi: 10.1073/pnas.83.6.1578. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Persing D. H., Varmus H. E., Ganem D. Antibodies to pre-S and X determinants arise during natural infection with ground squirrel hepatitis virus. J Virol. 1986 Oct;60(1):177–184. doi: 10.1128/jvi.60.1.177-184.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Roossinck M. J., Jameel S., Loukin S. H., Siddiqui A. Expression of hepatitis B viral core region in mammalian cells. Mol Cell Biol. 1986 May;6(5):1393–1400. doi: 10.1128/mcb.6.5.1393. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Seeger C., Ganem D., Varmus H. E. Biochemical and genetic evidence for the hepatitis B virus replication strategy. Science. 1986 Apr 25;232(4749):477–484. doi: 10.1126/science.3961490. [DOI] [PubMed] [Google Scholar]
  21. Seeger C., Ganem D., Varmus H. E. Nucleotide sequence of an infectious molecularly cloned genome of ground squirrel hepatitis virus. J Virol. 1984 Aug;51(2):367–375. doi: 10.1128/jvi.51.2.367-375.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Standring D. N., Rutter W. J., Varmus H. E., Ganem D. Transcription of the hepatitis B surface antigen gene in cultured murine cells initiates within the presurface region. J Virol. 1984 May;50(2):563–571. doi: 10.1128/jvi.50.2.563-571.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Summers J., Mason W. S. Replication of the genome of a hepatitis B--like virus by reverse transcription of an RNA intermediate. Cell. 1982 Jun;29(2):403–415. doi: 10.1016/0092-8674(82)90157-x. [DOI] [PubMed] [Google Scholar]
  24. Thomas P. S. Hybridization of denatured RNA and small DNA fragments transferred to nitrocellulose. Proc Natl Acad Sci U S A. 1980 Sep;77(9):5201–5205. doi: 10.1073/pnas.77.9.5201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Watanabe S., Temin H. M. Encapsidation sequences for spleen necrosis virus, an avian retrovirus, are between the 5' long terminal repeat and the start of the gag gene. Proc Natl Acad Sci U S A. 1982 Oct;79(19):5986–5990. doi: 10.1073/pnas.79.19.5986. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Virology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES