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Recombination between sequences of hepatitis B virus from different genotypes

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Abstract

A comparison of 25 hepatitis B virus (HBV) isolates for which complete genome sequences are available revealed two that occupied different positions in phylogenetic trees reconstructed from different open reading frames. Further analysis indicated that this incongruence was the result of recombination between viruses of different genomic and antigenic types. Both putative recombinants originated from geographic regions where multiple genotypes are known to cocirculate. A search of the sequence databases showed evidence of similar intergenotypic recombinants. These observations indicate that recombination between divergent strains may represent an important source of genetic variation in HBV.

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References

  • Bancroft WH, Mundon FK, Russel PK (1972) Detection of additional antigenic determinants of hepatitis B antigen. J Immunol 109:842–848

    Google Scholar 

  • Bichko V, Pushko P, Dreilina D, Pumpen P, Gren E (1985) Subtype ayw variant of hepatitis B virus. DNA primary structure analysis. FEBS Lett 185:208–212

    Google Scholar 

  • Buendia MA, Paterlini P, Tiollas P, Brechot C (1993) Hepatitis B virus: liver cancer. In: Zuckerman AJ, Thomas HC (eds) Viral hepatitis. Churchill Livingstone, Edinburgh, pp 137–164

    Google Scholar 

  • Carman WF, Hadziyannis S, Karayiannis P (1991) Association of the precore variant of HBV with acute and fulminant hepatitis B infection. In: Hollinger FB, Lemon SM, Mangolis HS (eds) Viral hepatitis and liver disease. Williams and Wilkins, Baltimore, pp 216–219

    Google Scholar 

  • Carman WF, Thomas HK, Domingo E (1993a) Viral genetic variation: hepatitis B virus as a clinical example. Lancet 341:349–353

    Google Scholar 

  • Carman WF, Thomas HC, Zuckerman AJ, Harrison T (1993b) Hepatitis B virus: molecular variants. In: Zuckerman AJ, Thomas HC (eds) Viral hepatitis. Churchill Livingstone, Edinburgh, pp 115–136

    Google Scholar 

  • Estacio RC, Chavez CC, Okamoto H, Lingao AL, Reyes MT, Domingo E, Mayumi M (1988) Nucleotide sequence of a hepatitis B virus genome of subtype adw isolated from a Philippino: comparison with the reported three genomes of the same subtype. J Gastroenterol Hepatol 3:215–222

    Google Scholar 

  • Felsenstein J (1993) PHYLIP (phylogeny inference package) version 3.5c. Distributed by the author. Department of Genetics, University of Washington, Seattle, USA

    Google Scholar 

  • Fujiyama A, Miyanohara A, Nozaki C, Yoneyama T, Ohtomo N, Matsubara K (1983) Cloning and structural analyses of hepatitis B virus DNAs, subtype adr. Nucleic Acids Res 11:4601–4610

    Google Scholar 

  • Galibert F, Mandart E, Fitoussi F, Tiollais P, Charnay P (1979) Nucleotide sequence of the hepatitis B virus genome (subtype ayw) cloned in E. coli. Nature 281:646–650

    Google Scholar 

  • Georgi-Geisberger P, Berns H, Loncarevic IF, Yu ZY, Tang ZY, Zentgraf H, Scroder CH (1992) Mutations on free and integrated hepatitis B Virus DNA in a hepatocellular carcinoma: footprints of homologous recombination. Oncology 49:386–395

    Google Scholar 

  • Harrison TJ, Hopes EA, Oon CJ, Zanetta AR, Zuckerman AJ (1991) Independent emergence of a vaccine induced escape mutant of hepatitis B virus. J Hepatol 13:105–107

    Google Scholar 

  • Hasegawa K, Huang JK, Rogers SA, Blum HE, Liang TJ (1994) Enhanced replication of a hepatitis B virus mutant associated with an epidemic of fulminant hepatitis. J Virol 68:1651–1659

    Google Scholar 

  • Higgins DG, Bleasby AJ, Fuchs R (1992) CLUSTALV: improved software for multiple sequence alignment. Comput Appl Biosci 8:189–191

    Google Scholar 

  • Hino O, Tabata S, Hotta Y (1991) Evidence for increased in vitro recombination with insertion of human hepatitis B virus DNA. Proc. Natl Acad Sci USA 88:9248–9252

    Google Scholar 

  • Kim KT, Hyun SW, Kim YS, Rho HM (1988) Complete nucleotide sequence of hepatitis B virus (subtype adr). Korean J Biochem 21:319–331

    Google Scholar 

  • Kobayashi M, Koike K (1984) Complete nucleotide sequence of hepatitis B virus DNA of subtype adr and its conserved gene organization. Gene 30:227–232

    Google Scholar 

  • Koechel H (1990) Unpublished. Direct submission to the EMBL/GenBank/DDBJ databases

  • Kosaka Y, Takase K, Kojima M (1991) Fulminant hepatitis B: induction by hepatitis B virus mutants defective in the precore region and incapable of encoding e antigen. Gastroenterology 324:1087–1094

    Google Scholar 

  • Lai ME, Mazzoleni AP, Melis A, Balestrieri A (1992) Unpublished. Direct submission to the EMBL/GenBank/DDBJ databases

  • Lai ME, Melis A, Mazzoleni AP, Farci P, Balestrieri A (1991) Sequence analysis of hepatitis B virus genome of a new mutant of ayw subtype isolated in Sardinia. Nucleic Acids Res 19:5078

    Google Scholar 

  • Le Bouvier GL (1971) The heterogeneity of the Australia antigen. J Infect Dis 123:671–675

    Google Scholar 

  • Maynard Smith J (1992) Analyzing the mosaic structure of genes. J Mol Evol 34:126–129

    Google Scholar 

  • Meisel H, Jantschak J, Tars K, Prosch S, Pushko P, Pumpen P (1993) Unpublished. Direct submission to the EMBL/GenBank/DDBJ databases

  • Mukaide M, Kumazawa T, Hoshi A, Kawaguchi R, Hikiji K (1992) The complete nucleotide sequence of Hepatitis B virus, subtype adr (SRADR) and phylogenetic analysis. Nucleic Acids Res 20:6105

    Google Scholar 

  • Naumann H, Schaefer S, Yoshida CFT, Gaspar AML, Repp R, Gerlich WH (1993) Identification of a new hepatitis B virus (HBV) genotype from Brazil that expresses HBV surface antigen subtype adw4. J Gen Virol 74:1627–1632

    Google Scholar 

  • Norder H, Hammas B, Lofdahl S, Courouce A, Magnius L (1992) Comparison of the amino acid sequences of nine different serotypes of hepatitis B surface antigen and genomic classification of the corresponding hepatitis B virus strains. J Gen Virol 73:1201–1208

    Google Scholar 

  • Norder H, Courouce AM, Magnius LO (1994) Complete genomes, phylogenetic relatedness, and structural proteins of six strains of the hepatitis B virus, four of which represented two new genotypes. Virology 198:489–503

    Google Scholar 

  • Norder H, Hammas B, Lee SD, Bile K, Courouce A, Mushahwar I, Magnius LO (1993) Genetic relatedness of hepatitis B viral strains of diverse geographical origin and natural variations in the primary structure of the surface antigen. J Gen Virol 74:1341–1348

    Google Scholar 

  • Ogata N, Miller RH, Ishak KG, Purcell RH (1993) The complete nucleotide sequence of a pre-core mutant of hepatitis B virus implicated in fulminant hepatitis and its biological characterization in chimpanzees. Virology 194:263–276

    Google Scholar 

  • Okamoto H, Imai M, Shimozaki M, Hoshi Y, Iizuka H, Gotanda T, Tsuda F, Miyakawa Y, Mayumi M (1986) Nucleotide sequence of a cloned hepatitis B virus genome, subtype ayr: comparison with genomes of the other three subtypes. J Gen Virol 67:2305–2314

    Google Scholar 

  • Okamoto H, Tsuda F, Sakugawa H, Sastrosoewignjo RI, Imai M, Miyakawa Y, Mayumi M (1988) Typing hepatitis B virus by homology in nucleotide sequence: comparison of surface antigen subtypes. J Gen Virol 69:2575–2583

    Google Scholar 

  • Omata M, Ehata T, Yokosuka O, Hosoda K, Ohto M (1991) Mutations in the precore region of hepatitis B virus DNA in patients with fulminant and severe hepatitis. New Engl J Med 324:1699–1704

    Google Scholar 

  • Ono Y, Onda H, Sasada R, Igarashi K, Sugino Y, Nishioka K (1983) The complete nucleotide sequences of the cloned hepatitis B virus DNA; subtype adr and adw. Nucleic Acids Res 11:1747–1757

    Google Scholar 

  • Renbao G, Meijin C, Lueping S, Suwen Q, Zaiping L (1987) The complete nucleotide sequence of the cloned DNA of hepatitis B virus subtype adr in pADR-1. Sci Sin 30:507–521

    Google Scholar 

  • Rho HM, Kim KT, Hyun SW, Kim YS (1989) The nucleotide sequence and reading frames of a mutant hepatitis B virus subtype adr. Nucleic Acids Res 17:2124

    Google Scholar 

  • Robertson DK, Hahn BH, Sharp PM (1995a) Recombination in AIDS viruses. J Mol Evol 40:249–259

    Google Scholar 

  • Robertson DL, Sharp PM, McCuthan FE, Hahn BH (1995b) Recombination in HIV-1. Nature 374:124–126

    Google Scholar 

  • Satrosoewignjo RI, Omi S, Okamoto H, Mayumi M, Rustam M, Sujudi X (1987) The complete nucleotide sequence of HBV DNA clone of subtype adw (pMND122) from Menado in Sulawesi Island, Indonesia. ICMR Ann 7:51–60

    Google Scholar 

  • Sherlock S (1993) Clinical features of hepatitis. In: Zuckerman AJ, Thomas HC (eds) Viral hepatitis. Churchill Livingstone, Edinburgh, pp 1–17

    Google Scholar 

  • Tong SP, Li JS, Vitvitski L, Trepo C (1990) Active hepatitis B virus replication in the presence of anti-HBe is associated with viral variants containing an inactive pre-C region. Virology 176:596–603

    Google Scholar 

  • Valenzuela P, Quiroga M, Zalvidar J, Gray P, Rutter WJ (1980) The nucleotide sequence of the hepatitis B viral genome and the identification of the major viral genes. In: Fields BN, Jaenisch R, Fox CF (eds) Animal virus genetics. Academic Press, New York, pp 57–70

    Google Scholar 

  • Wallace LA, Carman WF (1994) Clinical implications of hepatitis B virus envelope protein variation. Int J Clin Lab Res 24:80–85

    Google Scholar 

  • Yamamoto K, Hosikita M, Tsuda F, Itoh K, Akahane Y, Yotsumoto S, Okamoto H, Miyakawa Y, Mayumi M (1994) Naturally occurring escape mutants of hepatitis B virus with various mutations in the S gene in carriers seropositive for antibody to hepatitis B surface antigen. J Virol 68:2671–2676

    Google Scholar 

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  1. Wellcome Centre for the Epidemiology of Infectious Disease, Department of Zoology, University of Oxford, South Parks Road, OX1 3PS, Oxford, UK

    Paul L. Bollyky, Andrew Rambaut, Paul H. Harvey & Edward C. Holmes

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  1. Paul L. Bollyky
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  2. Andrew Rambaut
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  3. Paul H. Harvey
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  4. Edward C. Holmes
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Bollyky, P.L., Rambaut, A., Harvey, P.H. et al. Recombination between sequences of hepatitis B virus from different genotypes. J Mol Evol 42, 97–102 (1996). https://doi.org/10.1007/BF02198834

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  • DOI: https://doi.org/10.1007/BF02198834

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