Bioinformatic analysis of the hepadnavirus e-antigen and its precursor identifies remarkable sequence conservation in all orthohepadnaviruses

Journal of Medical Virology

Volumn 82, Issue 1, 2010, Pages 104-115

  Revill, Peter ^a   Yuen, Lilly ^a   Walsh, Renae ^a   Perrault, Marie ^a,c   Locarnini, Stephen ^a   Kramvis, Anna ^b  

^a VICTORIAN INFECTIOUS DISEASES REFERENCE LABORATORY   (Australia)

^b UNIVERSITY OF THE WITWATERSRAND   (South Africa)

^c UNIVERSITÉ DE LYON   (France)

Author keywords

Bioinformatics; Genotype; HBeAg; HBV; Mutation; Precore protein

Indexed keywords

EPITOPE; HEPATITIS B(E) ANTIGEN; HEPATITIS E ANTIGEN;

AMINO TERMINAL SEQUENCE; ARTICLE; BIOINFORMATICS; CELLULAR IMMUNITY; GENE SEQUENCE; GENETIC CONSERVATION; GENOTYPE; GEOGRAPHIC ORIGIN; HEPADNAVIRUS; HEPATITIS B VIRUS; HUMORAL IMMUNITY; IMMUNOMODULATION; IMMUNOREGULATION; INNATE IMMUNITY; NONHUMAN; NUCLEOTIDE SEQUENCE; ORTHOHEPADNAVIRUS; PERSISTENT VIRUS INFECTION; PROTEIN EXPRESSION; T LYMPHOCYTE; VIRUS ASSEMBLY; VIRUS NUCLEOCAPSID; VIRUS REPLICATION;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; COMPUTATIONAL BIOLOGY; CONSERVED SEQUENCE; GENOTYPE; HEPADNAVIRIDAE; HEPATITIS B E ANTIGENS; MOLECULAR SEQUENCE DATA; MUTATION; ORTHOHEPADNAVIRUS; PROTEIN PRECURSORS; SEQUENCE ALIGNMENT;

HEPADNAVIRIDAE; HEPATITIS B VIRUS; MAMMALIA;

EID: 74849108037     PISSN: 01466615     EISSN: 10969071     Source Type: Journal    
DOI: 10.1002/jmv.21645     Document Type: Article

References (66)

1. Arauz-Ruiz P, Norder H, Robertson BH, Magnius LO. 2002. Genotype H: A new Amerindian genotype of hepatitis B virus revealed in Central America. J Gen Virol 83:2059-2073.
2. Beck J, Nassal M. 2007. Hepatitis B virus replication. World J Gastroenterol 13:48-64.
3. Belnap DM, Watts NR, Conway JF, Cheng N, Stahl SJ, Wingfield PT, Steven AC. 2003. Diversity of core antigen epitopes of hepatitis B virus. Proc Natl Acad Sci USA 100:10884-10889.
4. Billaud JN, Peterson D, Schodel F, Chen A, Sallberg M, Garduno F, Goldstein P, McDowell W, Hughes J, Jones J, Milich D. 2005. Comparative antigenicity and immunogenicity of hepadnavirus core proteins. J Virol 79:13641-13655.
5. Bruss V,Gerlich WH. 1988. Formation of transmembraneous hepatitis B e-antigen by cotranslational in vitro processing of the viral precore protein. Virology 163:268-275.
6. Carman WF, Jacyna MR, Hadziyannis S, Karayiannis P, McGarvey MJ, Makris A, Thomas HC. 1989. Mutation preventing formation of hepatitis B e antigen in patients with chronic hepatitis B infection. Lancet 2:588-591.
7. Chang C, Enders G, Sprengel R, Peters N, Varmus HE, GanemD. 1987. Expression of the precore region of an avian hepatitis B virus is not required for viral replication. J Virol 61:3322-3325.
8. Chen HS, Kew MC, Hornbuckle WE, Tennant BC, Cote PJ, Gerin JL, Purcell RH, Miller RH. 1992. The precore gene of the woodchuck hepatitis virus genome is not essential for viral replication in the natural host. J Virol 66:5682-5684.
9. Chen MT, Billaud JN, Sallberg M, Guidotti LG, Chisari FV, Jones J, Hughes J, Milich DR. 2004. A function of the hepatitis B virus precore protein is to regulate the immune response to the core antigen. Proc Natl Acad Sci USA 101:14913-14918.
10. Chen M, Sallberg M, Hughes J, Jones J, Guidotti LG, Chisari FV, Billaud JN, Milich DR. 2005. Immune tolerance split between hepatitis B virus precore and core proteins. J Virol 79:3016-3027.
11. Chen CY, Crowther C, Kew MC, Kramvis A. 2008. A valine to phenylalanine mutation in the precore region of hepatitis B virus causes intracellular retention and impaired secretion of HBeantigen. Hepatol Res 38:580-592.
12. Chu CJ, Keeffe EB, Han SH, Perrillo RP, Min AD, Soldevila-Pico C, Carey W, Brown RS, Jr., Luketic VA, Terrault N, Lok AS. 2003. Hepatitis B virus genotypes in the United States: Results of a nationwide study. Gastroenterology 125:444-451.
13. Eckhardt SG, Milich DR, McLachlan A. 1991. Hepatitis B virus core antigen has two nuclear localization sequences in the arginine-rich carboxyl terminus. J Virol 65:575-582.
14. Ferrari C, Bertoletti A, Penna A, Cavalli A, Valli A, Missale G, Pilli M, Fowler P, Giuberti T, Chisari FV, Fiaccadori, F. 1991. Identification of immunodominant T cell epitopes of the hepatitis B virus nucleocapsid antigen. J Clin Invest 88:214-222.
15. Garcia PD, Ou JH, Rutter WJ, Walter P. 1988. Targeting of the hepatitis B virus precore protein to the endoplasmic reticulum membrane: After signal peptide cleavage translocation can be aborted and the product released into the cytoplasm. J Cell Biol 106:1093-1104.
16. Hall T. 1999. BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp 41:95-98.
17. Huang CF, Lin SS, Ho YC, Chen FL, Yang CC. 2006. The immune response induced by hepatitis B virus principal antigens. Cell Mol Immunol 3:97-106.
18. Huy TT, Ushijima H, Quang VX, Win KM, Luengrojanakul P, Kikuchi K, Sata T, Abe K. 2004. Genotype C of hepatitis B virus can be classified into at least two subgroups. J Gen Virol 85:283-292.
19. Huy TT, UshijimaH, Sata T, Abe K. 2006. Genomic characterization of HBV genotype F in Bolivia: Genotype F subgenotypes correlate with geographic distribution and T(1858) variant. Arch Virol 151:589-597.
20. Ito K, Kim KH, Lok AS, Tong S. 2009. Characterization of genotype specific carboxyl terminal cleavage sites of hepatitis B virus e antigen precursor and identification of furin as the candidate enzyme. J Virol 83:3507-3517.
21. Junker-Niepmann M, Bartenschlager R, Schaller H. 1990. A short cisacting sequence is required for hepatitis B virus pregenome encapsidation and sufficient for packaging of foreign RNA. EMBO J 9:3389-3396.
22. Kao JH. 2002. Hepatitis B viral genotypes: Clinical relevance and molecular characteristics. J Gastroenterol Hepatol 17:643-650.
23. Kimbi GC, Kramvis A, Kew MC. 2004. Distinctive sequence characteristics of subgenotype A1 isolates of hepatitis B virus from South Africa. J Gen Virol 85:1211-1220.
24. KramvisA,Kew MC. 1998. Structure and function of the encapsidation signal of hepadnaviridae. J Viral Hepat 5:357-367.
25. Kramvis A, Kew MC. 2005. Relationship of genotypes of hepatitis B virus to mutations, disease progression and response to antiviral therapy. J Viral Hepat 12:456-464.
26. Kramvis A, Kew MC. 2007. Molecular characterization of subgenotype A1 (subgroup Aa) of hepatitis B virus. Hepatol Res 37:S27-S32.
27. Kramvis A, Bukofzer S, Kew MC, Song E. 1997. Nucleic acid sequence analysis of the precore region of hepatitis B virus from sera of southern African black adult carriers of the virus. Hepatology 25:235-240.
28. Kramvis A, Kew MC, Bukofzer S. 1998. Hepatitis B virus precore mutants in serum and liver of Southern African Blacks with hepatocellular carcinoma. J Hepatol 28:132-141.
29. Kramvis A, Weitzmann L, Owiredu WK, KewMC. 2002. Analysis of the complete genome of subgroup A' hepatitis B virus isolates from South Africa. J Gen Virol 83:835-839.
30. Kramvis A, Kew M, Francois G. 2005. Hepatitis B virus genotypes. Vaccine 23:2409-2423.
31. Kramvis A, ArakawaK,Yu MC, Nogueira R, StramDO,KewMC. 2008. Relationship of serological subtype, basic core promoter and precore mutations to genotypes/subgenotypes of hepatitis B virus. J Med Virol 80:27-46.
32. Laine S, Salhi S, Rossignol JM. 2002. Overexpression and purification of the hepatitis B e antigen precursor. J Virol Methods 103: 67-74.
33. Laine S, Thouard A, Derancourt J, Kress M, Sitterlin D, Rossignol JM. 2003. In vitro and in vivo interactions between the hepatitis B virus protein P22 and the cellular protein gC1qR. J Virol 77:12875-12880.
34. Lok AS, Akarca U, Greene S. 1994. Mutations in the pre-core region of hepatitis B virus serve to enhance the stability of the secondary structure of the pre-genome encapsidation signal. Proc Natl Acad Sci USA 91:4077-4081.
35. Mangisa NP, Smuts HE, Kramvis A, Linley CW, Skelton M, Tucker TJ, De La MHP, Kahn D, Jilbert AR, Kew MC. 2004. Molecular characterization of duck hepatitis B virus isolates from South African ducks. Virus Genes 28:179-186.
36. Mbayed VA, Barbini L, Lopez JL, Campos RH. 2001. Phylogenetic analysis of the hepatitis B virus (HBV) genotype F including Argentine isolates. Arch Virol 146:1803-1810.
37. Messageot F, Carlier D, Rossignol JM. 1998. The C terminus of the hepatitis B virus e antigen precursor is required for a tunicamycinsensitive step that promotes efficient secretion of the antigen. J Biol Chem 273:18594-18598.
38. Messageot F, Salhi S,Eon P, Rossignol JM. 2003. Proteolytic processing of the hepatitis B virus e antigen precursor. Cleavage at two furin consensus sequences. J Biol Chem 278:891-895.
39. Milich D, Liang TJ. 2003. Exploring the biological basis of hepatitis B e antigen in hepatitis B virus infection. Hepatology (Baltimore, MD) 38:1075-1086.
40. Milich DR, McLachlan A, Moriarty A, Thornton GB. 1987. Immune response to hepatitis B virus core antigen (HBcAg): Localization of T cell recognition sites within HBcAg/HBeAg. J Immunol (Baltimore, MD) 139:1223-1231.
41. Milich DR, Jones JE, Hughes JL, Price J, Raney AK, McLachlan A. 1990. Is a function of the secreted hepatitis B e antigen to induce immunologic tolerance in utero? Proc Natl Acad Sci USA 87:6599-6603.
42. Milich DR, Chen MK, Hughes JL, Jones JE. 1998. The secreted hepatitis B precore antigen can modulate the immune response to the nucleocapsid: A mechanism for persistence. J Immunol 160:2013-2021.
43. Norder H, Courouce AM, Magnius LO. 1992. Molecular basis of hepatitis B virus serotype variations within the four major subtypes. J Gen Virol 73:3141-3145.
44. Norder H, Courouce AM, Coursaget P, Echevarria JM, Lee SD, Mushahwar IK, Robertson BH, Locarnini S, Magnius LO. 2004. Genetic diversity of hepatitis B virus strains derived worldwide: Genotypes, subgenotypes, and HBsAg subtypes. Intervirology 47:289-309.
45. 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.
46. Okamoto H, Yotsumoto S, Akahane Y, Yamanaka T,Miyazaki Y, Sugai Y, Tsuda F, Tanaka T, Miyakawa Y, Mayumi M. 1990. Hepatitis B viruses with precore region defects prevail in persistently infected hosts along with seroconversion to the antibody against e antigen. J Virol 64:1298-1303.
47. OsiowyC,Giles E, Tanaka Y, MizokamiM,Minuk GY. 2006. Molecular evolution of hepatitis B virus over 25 years. J Virol 80:10307-10314.
48. Ou JH, Laub O, Rutter WJ. 1986. 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 USA 83:1578-1582.
49. Riordan SM, Skinner N, Nagree A, McCallum H, McIver CJ, Kurtovic J, Hamilton JA, Bengmark S, Williams R, Visvanathan K. 2003. Peripheral blood mononuclear cell expression of toll-like receptors and relation to cytokine levels in cirrhosis. Hepatology 37:1154-1164.
50. Salhi S, Messageot F, Carlier D, Jean-Jean O, Rossignol JM. 2001. Identification of a cellular protein specifically interacting with the precursor of the hepatitis B e antigen. J Viral Hepat 8:169-173.
51. Schaefer S. 2007. Hepatitis B virus taxonomy and hepatitis B virus genotypes. World J Gastroenterol 13:14-21.
52. Schlicht HJ, Salfeld J, Schaller H. 1987. The duck hepatitisBvirus pre-C region encodes a signal sequence which is essential for synthesis and secretion of processed core proteins but not for virus formation. J Virol 61:3701-3709.
53. Schodel F, Peterson D, Zheng J, Jones JE, Hughes JL, Milich DR. 1993. Structure of hepatitis B virus core and e-antigen. A single precore amino acid prevents nucleocapsid assembly. J Biol Chem 268:1332-1337.
54. Seeger C, BaldwinB,Hornbuckle WE, Yeager AE, Tennant BC, Cote P, Ferrell L, Ganem D, Varmus HE. 1991. Woodchuck hepatitis virus is a more efficient oncogenic agent than ground squirrel hepatitis virus in a common host. J Virol 65:1673-1679.
55. Standring DN, Ou JH, Masiarz FR, Rutter WJ. 1988. A signal peptide encoded within the precore region of hepatitis B virus directs the secretion of a heterogeneous population of e antigens in Xenopus oocytes. Proc Natl Acad Sci USA 85:8405-8409.
56. Starkman SE, MacDonald DM, Lewis JC, Holmes EC, Simmonds P. 2003. Geographic and species association of hepatitis B virus genotypes in non-human primates. Virology 314:381-393.
57. Sugauchi F, Kumada H, Sakugawa H, Komatsu M, Niitsuma H, Watanabe H, Akahane Y, Tokita H, Kato T, Tanaka Y, Orito E, Ueda R, Miyakawa Y, MizokamiM. 2004. Two subtypes of genotype B (Ba and Bj) of hepatitis B virus in Japan. Clin Infect Dis 38:1222-1228.
58. Summers J, Mason WS. 1982. Replication of the genome of a hepatitis B-like virus by reverse transcription of an RNA intermediate. Cell 29:403-415.
59. Takahashi K, Machida A, Funatsu G, Nomura M, Usuda S, Aoyagi S, Tachibana K, Miyamoto H, Imai M, Nakamura T, Miyakawa Y, Mayumi M. 1983. Immunochemical structure of hepatitis B e antigen in the serum. J Immunol 130:2903-2907.
60. Takahashi K, Mishiro S, Prince AM. 2001. Novel hepatitis B virus strain from a chimpanzee of Central Africa (Pan troglodytes troglodytes) with an unusual antigenicity of the core protein. Intervirology 44:321-326.
61. Tanaka Y, Orito E, Yuen MF, MukaideM, Sugauchi F, Ito K, Ozasa A, Sakamoto T,Kurbanov F, Lai CL, MizokamiM. 2005. Two subtypes (subgenotypes) of hepatitis B virus genotype C: A novel subtyping assay based on restriction fragment length polymorphism. Hepatol Res 33:216-224.
62. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. 1997. The CLUSTAL-X windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876-4882.
63. Tong S. 2007. Impact of viral genotypes and naturally occurring mutations on biological properties of hepatitis B virus. Hepatol Res 37:S3-S8.
64. Visvanathan K, Skinner NA, Thompson AJ, Riordan SM, Sozzi V, Edwards R, Rodgers S, Kurtovic J, Chang J, Lewin S, Desmond P, Locarnini S. 2007. Regulation of Toll-like receptor-2 expression in chronic hepatitis B by the precore protein. Hepatology 45:102-110.
65. Wasenauer G, Kock J, Schlicht HJ. 1992. A cysteine and a hydrophobic sequence in the noncleaved portion of the pre-C leader peptide determine the biophysical properties of the secretory core protein (HBe protein) of human hepatitis B virus. J Virol 66:5338-5346.
66. Yang CY, Kuo TH, Ting LP. 2006. Human hepatitis B viral e antigen interacts with cellular interleukin-1 receptor accessory protein and triggers interleukin-1 response. J Biol Chem 281:34525-34536.