Skip to main content
NCBI home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1986 Apr;83(8):2531–2535. doi: 10.1073/pnas.83.8.2531

Common evolutionary origin of hepatitis B virus and retroviruses.

R H Miller, W S Robinson
PMCID: PMC323332  PMID: 3458214

Abstract

Hepatitis B virus (HBV), although classified as a double-stranded DNA virus, has been shown recently to replicate by reverse transcription of an RNA intermediate. Also, the putative viral polymerase has been found to share amino acid homology with reverse transcriptase of retroviruses. Using computer-assisted DNA and protein sequence analyses, we examined the genomes of 13 hepadnavirus isolates (nine human, two duck, one woodchuck, and one ground squirrel) and found that other conserved regions of the hepadnavirus genome share homology to corresponding regions of the genomes of type C retroviruses and retrovirus-like endogenous human DNA elements. Specifically, the most highly conserved sequence of the HBV genome, positioned at or near the initiation site for first-strand HBV DNA synthesis, is homologous over 67 nucleotides to the U5 region, a comparable region in retrovirus long terminal repeats. Within a highly conserved (i.e., 90%) 16-nucleotide sequence a heptanucleotide sequence CCTTGGG is 97% homologous between 27 virus isolates. Also, we found that the highly conserved HBV core, or nucleocapsid, protein shares 41% homology over 98 amino acids with the carboxyl-terminal region of the p30 gag nucleocapsid protein of type C retroviruses. In both cases, as with the previously reported polymerase homology, HBV is most homologous to the murine leukemia/sarcoma retroviruses. Further analysis revealed additional similarities between hepadnavirus and retroviral genomes. Taken together, our results suggest that HBV and retroviruses have a common evolutionary origin, with HBV arising through a process of deletion from a retrovirus, or retrovirus-like, progenitor.

Full text

PDF
2531

Selected References

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

  1. Adachi A., Sakai K., Kitamura N., Nakanishi S., Niwa O., Matsuyama M., Ishimoto A. Characterization of the env gene and long terminal repeat of molecularly cloned Friend mink cell focus-inducing virus DNA. J Virol. 1984 Jun;50(3):813–821. doi: 10.1128/jvi.50.3.813-821.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bichko V., Pushko P., Dreilina D., Pumpen P., Gren E. Subtype ayw variant of hepatitis B virus. DNA primary structure analysis. FEBS Lett. 1985 Jun 3;185(1):208–212. doi: 10.1016/0014-5793(85)80771-7. [DOI] [PubMed] [Google Scholar]
  3. Birnstiel M. L., Busslinger M., Strub K. Transcription termination and 3' processing: the end is in site! Cell. 1985 Jun;41(2):349–359. doi: 10.1016/s0092-8674(85)80007-6. [DOI] [PubMed] [Google Scholar]
  4. Bonner T. I., Birkenmeier E. H., Gonda M. A., Mark G. E., Searfoss G. H., Todaro G. J. Molecular cloning of a family of retroviral sequences found in chimpanzee but not human DNA. J Virol. 1982 Sep;43(3):914–924. doi: 10.1128/jvi.43.3.914-924.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bonner T. I., O'Connell C., Cohen M. Cloned endogenous retroviral sequences from human DNA. Proc Natl Acad Sci U S A. 1982 Aug;79(15):4709–4713. doi: 10.1073/pnas.79.15.4709. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Brutlag D. L., Clayton J., Friedland P., Kedes L. H. SEQ: a nucleotide sequence analysis and recombination system. Nucleic Acids Res. 1982 Jan 11;10(1):279–294. doi: 10.1093/nar/10.1.279. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. 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]
  8. Chen H. R., Barker W. C. Nucleotide sequences of the retroviral long terminal repeats and their adjacent regions. Nucleic Acids Res. 1984 Feb 24;12(4):1767–1778. doi: 10.1093/nar/12.4.1767. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Cohen M., Rein A., Stephens R. M., O'Connell C., Gilden R. V., Shure M., Nicolson M. O., McAllister R. M., Davidson N. Baboon endogenous virus genome: molecular cloning and structural characterization of nondefective viral genomes from DNA of a baboon cell strain. Proc Natl Acad Sci U S A. 1981 Aug;78(8):5207–5211. doi: 10.1073/pnas.78.8.5207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Fiers W., Contreras R., Haegemann G., Rogiers R., Van de Voorde A., Van Heuverswyn H., Van Herreweghe J., Volckaert G., Ysebaert M. Complete nucleotide sequence of SV40 DNA. Nature. 1978 May 11;273(5658):113–120. doi: 10.1038/273113a0. [DOI] [PubMed] [Google Scholar]
  11. Fujiyama A., Miyanohara A., Nozaki C., Yoneyama T., Ohtomo N., Matsubara K. Cloning and structural analyses of hepatitis B virus DNAs, subtype adr. Nucleic Acids Res. 1983 Jul 11;11(13):4601–4610. doi: 10.1093/nar/11.13.4601. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Galibert F., Chen T. N., Mandart E. Nucleotide sequence of a cloned woodchuck hepatitis virus genome: comparison with the hepatitis B virus sequence. J Virol. 1982 Jan;41(1):51–65. doi: 10.1128/jvi.41.1.51-65.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Galibert F., Mandart E., Fitoussi F., Tiollais P., Charnay P. Nucleotide sequence of the hepatitis B virus genome (subtype ayw) cloned in E. coli. Nature. 1979 Oct 25;281(5733):646–650. doi: 10.1038/281646a0. [DOI] [PubMed] [Google Scholar]
  14. Gelmann E. P., Petri E., Cetta A., Wong-Staal F. Deletions of specific regions of the simian sarcoma-associated virus genome are found in defective viruses and in the simian sarcoma virus. J Virol. 1982 Feb;41(2):593–604. doi: 10.1128/jvi.41.2.593-604.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Goff S. P. The genetics of murine leukemia viruses. Curr Top Microbiol Immunol. 1984;112:45–71. doi: 10.1007/978-3-642-69677-0_3. [DOI] [PubMed] [Google Scholar]
  16. Hunter E., Bhown A. S., Bennett J. C. Amino-terminal amino acid sequence of the major structural polypeptides of avian retroviruses: sequence homology between reticuloendotheliosis virus p30 and p30s of mammalian retroviruses. Proc Natl Acad Sci U S A. 1978 Jun;75(6):2708–2712. doi: 10.1073/pnas.75.6.2708. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Ju G., Skalka A. M. Nucleotide sequence analysis of the long terminal repeat (LTR) of avian retroviruses: structural similarities with transposable elements. Cell. 1980 Nov;22(2 Pt 2):379–386. doi: 10.1016/0092-8674(80)90348-7. [DOI] [PubMed] [Google Scholar]
  18. Kobayashi M., Koike K. Complete nucleotide sequence of hepatitis B virus DNA of subtype adr and its conserved gene organization. Gene. 1984 Oct;30(1-3):227–232. doi: 10.1016/0378-1119(84)90124-0. [DOI] [PubMed] [Google Scholar]
  19. Mandart E., Kay A., Galibert F. Nucleotide sequence of a cloned duck hepatitis B virus genome: comparison with woodchuck and human hepatitis B virus sequences. J Virol. 1984 Mar;49(3):782–792. doi: 10.1128/jvi.49.3.782-792.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Molnar-Kimber K. L., Summers J. W., Mason W. S. Mapping of the cohesive overlap of duck hepatitis B virus DNA and of the site of initiation of reverse transcription. J Virol. 1984 Jul;51(1):181–191. doi: 10.1128/jvi.51.1.181-191.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. 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]
  22. Needleman S. B., Wunsch C. D. A general method applicable to the search for similarities in the amino acid sequence of two proteins. J Mol Biol. 1970 Mar;48(3):443–453. doi: 10.1016/0022-2836(70)90057-4. [DOI] [PubMed] [Google Scholar]
  23. Nikbakht K. N., Ou C. Y., Boone L. R., Glover P. L., Yang W. K. Nucleotide sequence analysis of endogenous murine leukemia virus-related proviral clones reveals primer-binding sites for glutamine tRNA. J Virol. 1985 Jun;54(3):889–893. doi: 10.1128/jvi.54.3.889-893.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. O'Connell C. D., Cohen M. The long terminal repeat sequences of a novel human endogenous retrovirus. Science. 1984 Dec 7;226(4679):1204–1206. doi: 10.1126/science.6505687. [DOI] [PubMed] [Google Scholar]
  25. O'Connell C., O'Brien S., Nash W. G., Cohen M. ERV3, a full-length human endogenous provirus: chromosomal localization and evolutionary relationships. Virology. 1984 Oct 30;138(2):225–235. doi: 10.1016/0042-6822(84)90347-7. [DOI] [PubMed] [Google Scholar]
  26. O'Rear J. J., Temin H. M. Spontaneous changes in nucleotide sequence in proviruses of spleen necrosis virus, an avian retrovirus. Proc Natl Acad Sci U S A. 1982 Feb;79(4):1230–1234. doi: 10.1073/pnas.79.4.1230. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Ohno S. Segmental homology and internal repetitiousness identified in putative nucleic acid polymerase and human hepatitis B surface antigen of human hepatitis B virus. Proc Natl Acad Sci U S A. 1984 Jun;81(12):3781–3785. doi: 10.1073/pnas.81.12.3781. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Ono Y., Onda H., Sasada R., Igarashi K., Sugino Y., Nishioka K. The complete nucleotide sequences of the cloned hepatitis B virus DNA; subtype adr and adw. Nucleic Acids Res. 1983 Mar 25;11(6):1747–1757. doi: 10.1093/nar/11.6.1747. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Oroszlan S., Barbacid M., Copeland T. D., Aaronson S. A., Gilden R. V. Chemical and Immunological characterization of the major structural protein (p28) of MMC-1, a rhesus monkey endogenous type C virus: homology with the major structural protein of avian reticuloendotheliosis virus. J Virol. 1981 Sep;39(3):845–854. doi: 10.1128/jvi.39.3.845-854.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Oroszlan S., Copeland T. D., Gilden R. V., Todaro G. J. Structural homology of the major internal proteins of endogeneous type C viruses of two distantly related species of Old World monkeys: Macaca arctoides and Colobus polykomos. Virology. 1981 Dec;115(2):262–271. doi: 10.1016/0042-6822(81)90109-4. [DOI] [PubMed] [Google Scholar]
  31. Panganiban A. T., Temin H. M. The terminal nucleotides of retrovirus DNA are required for integration but not virus production. Nature. 1983 Nov 10;306(5939):155–160. doi: 10.1038/306155a0. [DOI] [PubMed] [Google Scholar]
  32. Pasek M., Goto T., Gilbert W., Zink B., Schaller H., MacKay P., Leadbetter G., Murray K. Hepatitis B virus genes and their expression in E. coli. Nature. 1979 Dec 6;282(5739):575–579. doi: 10.1038/282575a0. [DOI] [PubMed] [Google Scholar]
  33. Patarca R., Haseltine W. A. Sequence similarity among retroviruses--erratum. Nature. 1984 Jun 21;309(5970):728–728. doi: 10.1038/309728b0. [DOI] [PubMed] [Google Scholar]
  34. Paulson K. E., Deka N., Schmid C. W., Misra R., Schindler C. W., Rush M. G., Kadyk L., Leinwand L. A transposon-like element in human DNA. Nature. 1985 Jul 25;316(6026):359–361. doi: 10.1038/316359a0. [DOI] [PubMed] [Google Scholar]
  35. Reddy E. P., Smith M. J., Aaronson S. A. Complete nucleotide sequence and organization of the Moloney murine sarcoma virus genome. Science. 1981 Oct 23;214(4519):445–450. doi: 10.1126/science.6170110. [DOI] [PubMed] [Google Scholar]
  36. Repaske R., O'Neill R. R., Steele P. E., Martin M. A. Characterization and partial nucleotide sequence of endogenous type C retrovirus segments in human chromosomal DNA. Proc Natl Acad Sci U S A. 1983 Feb;80(3):678–682. doi: 10.1073/pnas.80.3.678. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Repaske R., Steele P. E., O'Neill R. R., Rabson A. B., Martin M. A. Nucleotide sequence of a full-length human endogenous retroviral segment. J Virol. 1985 Jun;54(3):764–772. doi: 10.1128/jvi.54.3.764-772.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Rosenthal N., Kress M., Gruss P., Khoury G. BK viral enhancer element and a human cellular homolog. Science. 1983 Nov 18;222(4625):749–755. doi: 10.1126/science.6314501. [DOI] [PubMed] [Google Scholar]
  39. Schwartz D. E., Tizard R., Gilbert W. Nucleotide sequence of Rous sarcoma virus. Cell. 1983 Mar;32(3):853–869. doi: 10.1016/0092-8674(83)90071-5. [DOI] [PubMed] [Google Scholar]
  40. 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]
  41. Shaul Y., Rutter W. J., Laub O. A human hepatitis B viral enhancer element. EMBO J. 1985 Feb;4(2):427–430. doi: 10.1002/j.1460-2075.1985.tb03646.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Shinnick T. M., Lerner R. A., Sutcliffe J. G. Nucleotide sequence of Moloney murine leukaemia virus. Nature. 1981 Oct 15;293(5833):543–548. doi: 10.1038/293543a0. [DOI] [PubMed] [Google Scholar]
  43. Shoemaker C., Goff S., Gilboa E., Paskind M., Mitra S. W., Baltimore D. Structure of a cloned circular Moloney murine leukemia virus DNA molecule containing an inverted segment: implications for retrovirus integration. Proc Natl Acad Sci U S A. 1980 Jul;77(7):3932–3936. doi: 10.1073/pnas.77.7.3932. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Shoemaker C., Hoffman J., Goff S. P., Baltimore D. Intramolecular integration within Moloney murine leukemia virus DNA. J Virol. 1981 Oct;40(1):164–172. doi: 10.1128/jvi.40.1.164-172.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Sprengel R., Kuhn C., Will H., Schaller H. Comparative sequence analysis of duck and human hepatitis B virus genomes. J Med Virol. 1985 Apr;15(4):323–333. doi: 10.1002/jmv.1890150402. [DOI] [PubMed] [Google Scholar]
  46. 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]
  47. Tamura T. A. Provirus of M7 baboon endogenous virus: nucleotide sequence of the gag-pol region. J Virol. 1983 Jul;47(1):137–145. doi: 10.1128/jvi.47.1.137-145.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Tamura T., Takano T. Long terminal repeat (LTR)-derived recombination of retroviral DNA: sequence analyses of an aberrant clone of baboon endogenous virus DNA which carries an inversion from the LTR to the gag region. Nucleic Acids Res. 1982 Sep 11;10(17):5333–5343. doi: 10.1093/nar/10.17.5333. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Tiollais P., Pourcel C., Dejean A. The hepatitis B virus. Nature. 1985 Oct 10;317(6037):489–495. doi: 10.1038/317489a0. [DOI] [PubMed] [Google Scholar]
  50. Toh H., Hayashida H., Miyata T. Sequence homology between retroviral reverse transcriptase and putative polymerases of hepatitis B virus and cauliflower mosaic virus. 1983 Oct 27-Nov 2Nature. 305(5937):827–829. doi: 10.1038/305827a0. [DOI] [PubMed] [Google Scholar]
  51. Van Beveren C., van Straaten F., Galleshaw J. A., Verma I. M. Nucleotide sequence of the genome of a murine sarcoma virus. Cell. 1981 Nov;27(1 Pt 2):97–108. doi: 10.1016/0092-8674(81)90364-0. [DOI] [PubMed] [Google Scholar]
  52. Wain-Hobson S., Nussinov R., Brown R. J., Sussman J. L. Preferential codon usage in genes. Gene. 1981 May;13(4):355–364. doi: 10.1016/0378-1119(81)90015-9. [DOI] [PubMed] [Google Scholar]
  53. Wain-Hobson S., Sonigo P., Danos O., Cole S., Alizon M. Nucleotide sequence of the AIDS virus, LAV. Cell. 1985 Jan;40(1):9–17. doi: 10.1016/0092-8674(85)90303-4. [DOI] [PubMed] [Google Scholar]
  54. Wilbur W. J., Lipman D. J. Rapid similarity searches of nucleic acid and protein data banks. Proc Natl Acad Sci U S A. 1983 Feb;80(3):726–730. doi: 10.1073/pnas.80.3.726. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES