Top

Published in:

Open Access 01-12-2013 | Review

Medical Virology of Hepatitis B: how it began and where we are now

Author: Wolfram H Gerlich

Published in: Virology Journal | Issue 1/2013

Abstract

Infection with hepatitis B virus (HBV) may lead to acute or chronic hepatitis. HBV infections were previously much more frequent but there are still 240 million chronic HBV carriers today and ca. 620,000 die per year from the late sequelae liver cirrhosis or hepatocellular carcinoma. Hepatitis B was recognized as a disease in ancient times, but its etiologic agent was only recently identified. The first clue in unraveling this mystery was the discovery of an enigmatic serum protein named Australia antigen 50 years ago by Baruch Blumberg. Some years later this was recognized to be the HBV surface antigen (HBsAg). Detection of HBsAg allowed for the first time screening of inapparently infected blood donors for a dangerous pathogen. The need to diagnose clinically silent HBV infections was a strong driving force in the development of modern virus diagnostics. HBsAg was the first infection marker to be assayed with a highly sensitive radio immune assay. HBV itself was among the first viruses to be detected by assay of its DNA genome and IgM antibodies against the HBV core antigen were the first to be selectively detected by the anti-μ capture assay. The cloning and sequencing of the HBV genome in 1978 paved the way to understand the viral life cycle, and allowed development of efficient vaccines and drugs. Today’s hepatitis B vaccine was the first vaccine produced by gene technology. Among the problems that still remain today are the inability to achieve a complete cure of chronic HBV infections, the recognition of occult HBV infections, their potential reactivation and the incomplete protection against escape mutants and heterologous HBV genotypes by HBV vaccines.

Available only for authorised users

Blumberg BS: Hepatitis B - The hunt for a killer virus. 2002, Princeton: Princeton University Press

Lürmann A: Eine Icterusepidemie. Ber Klin Wochenschr. 1885, 22: 20-23.

MacCallum FO: 1971 International symposium on viral hepatitis. Historical perspectives. Can Med Assoc J. 1972, 106 (Suppl): 423-426.PubMedPubMedCentral

Seeff LB, Beebe GW, Hoofnagle JH, Norman JE, Buskell-Bales Z, Waggoner JG, Kaplowitz N, Koff RS, Petrini JL, Schiff ER, et al: A serologic follow-up of the 1942 epidemic of post-vaccination hepatitis in the United States Army. N Engl J Med. 1987, 316: 965-970. 10.1056/NEJM198704163161601.PubMed

Barker LF, Murray R: Relationship of virus dose to incubation time of clinical hepatitis and time of appearance of hepatitis–associated antigen. Am J Med Sci. 1972, 263: 27-33. 10.1097/00000441-197201000-00005.PubMed

Krugman S, Giles JP, Hammond J: Infectious hepatitis. Evidence for two distinctive clinical, epidemiological, and immunological types of infection. JAMA. 1967, 200: 365-373. 10.1001/jama.1967.03120180053006.PubMed

Prince AM: Relation of Australia and SH antigens. Lancet. 1968, 2 (7565): 462-463.PubMed

Ling CM, Overby LR: Prevalence of hepatitis B virus antigen as revealed by direct radioimmune assay with 125 I-antibody. J Immunol. 1972, 109: 834-841.PubMed

Le Bouvier GL, McCollum RW, Hierholzer WJ, Irwin GR, Krugman S, Giles JP: Subtypes of Australia antigen and hepatitis-B virus. JAMA. 1972, 222: 928-930. 10.1001/jama.1972.03210080020005.PubMed

10.

Bancroft WH, Mundon FK, Russell PK: Detection of additional antigenic determinants of hepatitis B antigen. J Immunol. 1972, 109: 842-848.PubMed

11.

Millman I, Loeb LA, Bayer ME, Blumberg BS: Australia antigen (a hepatitis-associated antigen): purification and physical properties. J Exp Med. 1970, 131: 1190-1199. 10.1084/jem.131.6.1190.PubMedPubMedCentral

12.

Gerlich W, May G: Hepatitis-associated antigen: purification and properties. Zentralbl Bakteriol Orig A. 1973, 224: 49-60. GermanPubMed

13.

Griffith JS: Self-replication and scrapie. Nature. 1967, 215: 1043-1044. 10.1038/2151043a0.PubMed

14.

Dane DS, Cameron CH, Briggs M: Virus-like particles in serum of patients with Australia-antigen-associated hepatitis. Lancet. 1970, 1 (7649): 695-698.PubMed

15.

Almeida JD, Rubenstein D, Stott EJ: New antigen-antibody system in Australia-antigen-positive hepatitis. Lancet. 1971, 2 (7736): 1225-1227.PubMed

16.

Seitz S, Urban S, Antoni C, Böttcher B: Cryo-electron microscopy of hepatitis B virions reveals variability in envelope capsid interactions. EMBO J. 2007, 26: 4160-4167. 10.1038/sj.emboj.7601841.PubMedPubMedCentral

17.

Hirschman SZ, Vernace SJ, Schaffner F: D.N.A. polymerase in preparations containing Australia antigen. Lancet. 1971, 1 (7709): 1099-1103.PubMed

18.

Kaplan PM, Greenman RL, Gerin JL, Purcell RH, Robinson WS: DNA polymerase associated with human hepatitis B antigen. J Virol. 1973, 12: 995-1005.PubMedPubMedCentral

19.

Robinson WS, Clayton DA, Greenman RL: DNA of a human hepatitis B virus candidate. J Virol. 1974, 14: 384-391.PubMedPubMedCentral

20.

Berg P, Baltimore D, Brenner S, Roblin RO, Singer MF: Summary statement of the Asilomar conference on recombinant DNA molecules. Proc Natl Acad Sci USA. 1975, 72: 1981-1984. 10.1073/pnas.72.6.1981.PubMedPubMedCentral

21.

Charnay P, Pourcel C, Louise A, Fritsch A, Tiollais P: Cloning in Escherichia coli and physical structure of hepatitis B virion DNA. Proc Natl Acad Sci USA. 1979, 76: 2222-2226. 10.1073/pnas.76.5.2222.PubMedPubMedCentral

22.

Valenzuela P, Gray P, Quiroga M, Zaldivar J, Goodman HM, Rutter WJ: Nucleotide sequence of the gene coding for the major protein of hepatitis B virus surface antigen. Nature. 1979, 280: 815-819. 10.1038/280815a0.PubMed

23.

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, 282: 575-579. 10.1038/282575a0.PubMed

24.

Wittkop L, Schwarz A, Cassany A, Grün-Bernhard S, Delaleau M, Rabe B, Cazenave C, Gerlich W, Glebe D, Kann M: Inhibition of protein kinase C phosphorylation of hepatitis B virus capsids inhibits virion formation and causes intracellular capsid accumulation. Cell Microbiol. 2010, 12: 962-975. 10.1111/j.1462-5822.2010.01444.x.PubMed

25.

Will H, Cattaneo R, Koch HG, Darai G, Schaller H, Schellekens H, van Eerd PM, Deinhardt F: Cloned HBV DNA causes hepatitis in chimpanzees. Nature. 1982, 299: 740-742. 10.1038/299740a0.PubMed

26.

Hoofnagle JH, Gerety RJ, Barker LF: Antibody to hepatitis-B-virus core in man. Lancet. 1973, 2 (7834): 869-873.PubMed

27.

Hoofnagle JH, Seeff LB, Bales ZB, Zimmerman HJ: Type B hepatitis after transfusion with blood containing antibody to hepatitis B core antigen. N Engl J Med. 1978, 298: 1379-1383. 10.1056/NEJM197806222982502.PubMed

28.

Galbraith RM, Eddleston AL, Williams R, Zuckerman AJ: Fulminant hepatic failure in leukaemia and choriocarcinoma related to withdrawal of cytotoxic drug therapy. Lancet. 1975, 2 (7934): 528-530.PubMed

29.

Flehmig B, Ranke M, Berthold H, Gerth HJ: A solid-phase radioimmunoassay for detection of IgM antibodies to hepatitis A virus. J Infect Dis. 1979, 140: 169-175. 10.1093/infdis/140.2.169.PubMed

30.

Gerlich WH, Lüer W: Selective detection of IgM-antibody against core antigen of the hepatitis B virus by a modified enzyme immune assay. J Med Virol. 1979, 4: 227-238. 10.1002/jmv.1890040308.PubMed

31.

Gerlich WH, Uy A, Lambrecht F, Thomssen R: Cutoff levels of immunoglobulin M antibody against viral core antigen for differentiation of acute, chronic, and past hepatitis B virus infections. J Clin Microbiol. 1986, 24: 288-293.PubMedPubMedCentral

32.

Milich DR, McLachlan A: The nucleocapsid of hepatitis B virus is both a T-cell-independent and a T-cell-dependent antigen. Science. 1986, 234: 1398-1401. 10.1126/science.3491425.PubMed

33.

Magnius LO, Espmark A: A new antigen complex co-occurring with Australia antigen. Acta Pathol Microbiol Scand B Microbiol Immunol. 1972, 80: 335-337.PubMed

34.

Standring DN, Ou JH, Masiarz FR, Rutter WJ: 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. 1988, 85: 8405-8409. 10.1073/pnas.85.22.8405.PubMedPubMedCentral

35.

Bruss V, Gerlich WH: Formation of transmembraneous hepatitis B e-antigen by cotranslational in vitro processing of the viral precore protein. Virology. 1988, 163: 268-275. 10.1016/0042-6822(88)90266-8.PubMed

36.

Carman WF, Jacyna MR, Hadziyannis S, Karayiannis P, McGarvey MJ, Makris A, Thomas HC: Mutation preventing formation of hepatitis B e antigen in patients with chronic hepatitis B infection. Lancet. 1989, 2 (8663): 588-591.PubMed

37.

Milich DR, Chen MK, Hughes JL, Jones JE: The secreted hepatitis B precore antigen can modulate the immune response to the nucleocapsid: a mechanism for persistence. J Immunol. 1998, 160: 2013-2021.PubMed

38.

Maynard JE, Berquist KR, Krushak DH, Purcell RH: Experimental infection of chimpanzees with the virus of hepatitis B. Nature. 1972, 237: 514-515. 10.1038/237514a0.PubMed

39.

Petersen J, Dandri M, Gupta S, Rogler CE: Liver repopulation with xenogenic hepatocytes in B and T cell-deficient mice leads to chronic hepadnavirus infection and clonal growth of hepatocellular carcinoma. Proc Natl Acad Sci USA. 1998, 95: 310-315. 10.1073/pnas.95.1.310.PubMedPubMedCentral

40.

Köck J, Nassal M, MacNelly S, Baumert TF, Blum HE, von Weizsäcker F: Efficient infection of primary tupaia hepatocytes with purified human and woolly monkey hepatitis B virus. J Virol. 2001, 75: 5084-5089. 10.1128/JVI.75.11.5084-5089.2001.PubMedPubMedCentral

41.

Glebe D, Urban S, Knoop EV, Çag N, Krass P, Grün S, Bulavaite A, Sasnauskas K, Gerlich WH: Mapping of the hepatitis B virus attachment site by infection-inhibiting preS1 lipopeptides using Tupaia hepatocytes. Gastroenterology. 2005, 129: 234-245. 10.1053/j.gastro.2005.03.090.PubMed

42.

Gripon P, Rumin S, Urban S, Le Seyec J, Glaise D, Cannie I, Guyomard C, Lucas J, Trepo C, Guguen-Guillouzo C: Infection of a human hepatoma cell line by hepatitis B virus. Proc Natl Acad Sci USA. 2002, 99: 15655-15660. 10.1073/pnas.232137699.PubMedPubMedCentral

43.

Quint WG, Heijtink RA, Schirm J, Gerlich WH, Niesters HG: Reliability of methods for hepatitis B virus DNA detection. J Clin Microbiol. 1995, 33: 225-228.PubMedPubMedCentral

44.

Gerlich WH, Robinson WS: Hepatitis B virus contains protein attached to the 5’ terminus of its complete DNA strand. Cell. 1980, 21: 801-809. 10.1016/0092-8674(80)90443-2.PubMed

45.

Saldanha J, Gerlich W, Lelie N, Dawson P, Heermann K, Heath A, WHO Collaborative Study Group: An international collaborative study to establish a World Health Organization international standard for hepatitis B virus DNA nucleic acid amplification techniques. Vox Sang. 2001, 80: 63-71. 10.1046/j.1423-0410.2001.00003.x.PubMed

46.

Tabuchi A, Tanaka J, Katayama K, Mizui M, Matsukura H, Yugi H, Shimada T, Miyakawa Y, Yoshizawa H: Titration of hepatitis B virus infectivity in the sera of pre-acute and late acute phases of HBV infection: transmission experiments to chimeric mice with human liver repopulated hepatocytes. J Med Virol. 2008, 80: 2064-2068. 10.1002/jmv.21320.PubMed

47.

Allain JP, Mihaljevic I, Gonzalez-Fraile MI, Gubbe K, Holm-Harritshøj L, Garcia JM, Brojer E, Erikstrup C, Saniewski M, Wernish L, Bianco L, Ullum H, Candotti D, Lelie N, Gerlich WH, Chudy M: Infectivity of blood products from donors with occult hepatitis B virus infection. Transfusion. 2013, doi: 10.1111/trf.12096. [Epub ahead of print]

48.

Gunson RN, Shouval D, Roggendorf M, Zaaijer H, Nicholas H, Holzmann H, de Schryver A, Reynders D, Connell J, Gerlich WH, Marinho RT, Tsantoulas D, Rigopoulou E, Rosenheim M, Valla D, Puro V, Struwe J, Tedder R, Aitken C, Alter M, Schalm SW, Carman WF, European Consensus Group: Hepatitis B virus (HBV) and hepatitis C virus (HCV) infections in health care workers (HCWs): guidelines for prevention of transmission of HBV and HCV from HCW to patients. J Clin Virol. 2003, 27: 213-230. 10.1016/S1386-6532(03)00087-8.PubMed

49.

Couroucé-Pauty AM, Soulier JP: Further data on HBs antigen subtypes - geographical distribution. Vox Sang. 1974, 27: 533-549. 10.1111/j.1423-0410.1974.tb02451.x.PubMed

50.

Okamoto H, Tsuda F, Sakugawa H, Sastrosoewignjo RI, Imai M, Miyakawa Y, Mayumi M: Typing hepatitis B virus by homology in nucleotide sequence: comparison of surface antigen subtypes. J Gen Virol. 1988, 69: 2575-2583. 10.1099/0022-1317-69-10-2575.PubMed

51.

Norder H, Couroucé AM, Coursaget P, Echevarria JM, Lee SD, Mushahwar IK, Robertson BH, Locarnini S, Magnius LO: Genetic diversity of hepatitis B virus strains derived worldwide: genotypes, subgenotypes, and HBsAg subtypes. Intervirology. 2004, 47: 289-309. 10.1159/000080872.PubMed

52.

Andernach IE, Nolte C, Pape JW, Muller CP: Slave trade and hepatitis B virus genotypes and subgenotypes in Haiti and Africa. Emerg Infect Dis. 2009, 15: 1222-1228. 10.3201/eid1508.081642.PubMedPubMedCentral

53.

Kramvis A, Kew MC: Molecular characterization of subgenotype A1 (subgroup Aa) of hepatitis B virus. Hepatol Res. 2007, 37 (Suppl 1): S27-S32.PubMed

54.

Davies J, Littlejohn M, Locarnini SA, Whiting S, Hajkowicz K, Cowie BC, Bowden DS, Tong SY, Davis JS: The molecular epidemiology of Hepatitis B in the Indigenous people of northern Australia. J Gastroenterol Hepatol. 2013, 10.1111/jgh.12177. [Epub ahead of print]

55.

Paraskevis D, Magiorkinis G, Magiorkinis E, Ho SY, Belshaw R, Allain JP, Hatzakis A: Dating the origin and dispersal of hepatitis B virus infection in humans and primates. Hepatology. 2013, 57: 908-916. 10.1002/hep.26079.PubMed

56.

Shi W, Zhu C, Zheng W, Zheng W, Ling C, et al: Subgenotyping of genotype C hepatitis B virus: correcting misclassifications and identifying a novel subgenotype. PLoS ONE. 2012, 7 (10): e47271-10.1371/journal.pone.0047271.PubMedPubMedCentral

57.

Mason WS, Gerlich WH, Taylor JM, Kann M, Loeb D, Sureau S, Magnius L, Norder H: Virus taxonomy, ninth report of the international committee on taxonomy of viruses. Family Hepadnaviridae. 2012, Amsterdam: Elsevier, 445-455.

58.

Lanford RE, Chavez D, Brasky KM, Burns RB, Rico-Hesse R: Isolation of a hepadnavirus from the woolly monkey, a new world primate. Proc Natl Acad Sci USA. 1998, 95: 5757-5761. 10.1073/pnas.95.10.5757.PubMedPubMedCentral

59.

Dreesman JM, Baillot A, Hamschmidt L, Monazahian M, Wend UC, Gerlich WH: Outbreak of hepatitis B in a nursing home associated with capillary blood sampling. Epidemiol. Infect. 2006, 26: 1102-1113.

60.

Guidotti LG, Chisari FV: Immunobiology and pathogenesis of viral hepatitis. Annu Rev Pathol. 2006, 1: 23-61. 10.1146/annurev.pathol.1.110304.100230.PubMed

61.

Raimondo G, Allain JP, Brunetto MR, Buendia MA, Chen DS, Colombo M, Craxì A, Donato F, Ferrari C, Gaeta GB, Gerlich WH, Levrero M, Locarnini S, Michalak T, Mondelli MU, Pawlotsky JM, Pollicino T, Prati D, Puoti M, Samuel D, Shouval D, Smedile A, Squadrito G, Trépo C, Villa E, Will H, Zanetti AR, Zoulim F: Statements from the Taormina expert meeting on occult hepatitis B virus infection. J Hepatol. 2008, 49: 652-657. 10.1016/j.jhep.2008.07.014.PubMed

62.

Westhoff TH, Jochimsen F, Schmittel A, Stöffler-Meilicke M, Schäfer JH, Zidek W, Gerlich WH, Thiel E: Fatal hepatitis B virus reactivation by an escape mutant following rituximab therapy. Blood. 1930, 2003: 102-

63.

Blaich A, Manz M, Dumoulin A, Schüttler CG, Hirsch HH, Gerlich WH, Frei R: Reactivation of hepatitis B virus with mutated HBsAg in a liver transplant recipient receiving a graft from an anti-HBs and anti-HBc positive donor. Transfusion. 2012, 52: 1999-2006. 10.1111/j.1537-2995.2011.03537.x.PubMedPubMedCentral

64.

Turelli P, Mangeat B, Jost S, Vianin S, Trono D: Inhibition of hepatitis B virus replication by APOBEC3G. Science. 2004, 303: 1829-10.1126/science.1092066.PubMed

65.

Szmuness W: Hepatocellular carcinoma and the hepatitis B virus: evidence for a causal association. Prog Med Virol. 1978, 24: 40-69.PubMed

66.

Beasley RP, Hwang LY, Lin CC, Chien CS: Hepatocellular carcinoma and hepatitis B virus. A prospective study of 22 707 men in Taiwan. Lancet. 1981, 2 (8256): 1129-1133.PubMed

67.

Alexander JJ, Bey EM, Geddes EW, Lecatsas G: Establishment of a continuously growing cell line from primary carcinoma of the liver. S Afr Med J. 1976, 50: 2124-2128.PubMed

68.

Edman JC, Gray P, Valenzuela P, Rall LB, Rutter WJ: Integration of hepatitis B virus sequences and their expression in a human hepatoma cell. Nature. 1980, 286: 535-538. 10.1038/286535a0.PubMed

69.

Kekulé AS, Lauer U, Meyer M, Caselmann WH, Hofschneider PH, Koshy R: The preS2/S region of integrated hepatitis B virus DNA encodes a transcriptional transactivator. Nature. 1990, 343: 457-461. 10.1038/343457a0.PubMed

70.

Höhne M, Schaefer S, Seifer M, Feitelson MA, Paul D, Gerlich WH: Malignant transformation of immortalized transgenic hepatocytes after transfection with hepatitis B virus DNA. EMBO Journal. 1990, 9: 1137-1145.PubMedPubMedCentral

71.

Lucifora J, Arzberger S, Durantel D, Belloni L, Strubin M, Levrero M, Zoulim F, Hantz O, Protzer U: Hepatitis B virus X protein is essential to initiate and maintain virus replication after infection. J Hepatol. 2011, 55: 996-1003. 10.1016/j.jhep.2011.02.015.PubMed

72.

Dejean A, Bougueleret L, Grzeschik KH, Tiollais P: Hepatitis B virus DNA integration in a sequence homologous to v-erb-A and steroid receptor genes in a hepatocellular carcinoma. Nature. 1986, 322: 70-72. 10.1038/322070a0.PubMed

73.

Mason WS, Liu C, Aldrich CE, Litwin S, Yeh MM: Clonal expansion of normal-appearing human hepatocytes during chronic hepatitis B virus infection. J Virol. 2010, 84: 8308-8315. 10.1128/JVI.00833-10.PubMedPubMedCentral

74.

Chen CJ, Yang HI, Su J, Jen CL, You SL, Lu SN, Huang GT, Iloeje UH: REVEAL-HBV Study Group: Risk of hepatocellular carcinoma across a biological gradient of serum hepatitis B virus DNA level. JAMA. 2006, 295: 65-73. 10.1001/jama.295.1.65.PubMed

75.

Summers J, Smolec JM, Snyder R: A virus similar to human hepatitis B virus associated with hepatitis and hepatoma in woodchucks. Proc Natl Acad Sci USA. 1978, 75: 4533-4537. 10.1073/pnas.75.9.4533.PubMedPubMedCentral

76.

Marion PL, Oshiro LS, Regnery DC, Scullard GH, Robinson WS: A virus in Beechey ground squirrels that is related to hepatitis B virus of humans. Proc Natl Acad Sci USA. 1980, 77: 2941-2945. 10.1073/pnas.77.5.2941.PubMedPubMedCentral

77.

Fourel G, Trepo C, Bougueleret L, Henglein B, Ponzetto A, Tiollais P, Buendia MA: Frequent activation of N-myc genes by hepadnavirus insertion in woodchuck liver tumours. Nature. 1990, 347: 294-298. 10.1038/347294a0.PubMed

78.

Mason WS, Seal G, Summers J: Virus of Pekin ducks with structural and biological relatedness to human hepatitis B virus. J Virol. 1980, 36: 829-836.PubMedPubMedCentral

79.

Sprengel R, Kaleta EF, Will H: Isolation and characterization of a hepatitis B virus endemic in herons. J Virol. 1988, 62: 3832-3839.PubMedPubMedCentral

80.

Suh A, Brosius J, Schmitz J, Kriegs JO: The genome of a mesozoic paleovirus reveals the evolution of hepatitis B viruses. Nature Communications. 2013, 4: 1791-PubMed

81.

Summers J, Mason WS: Replication of the genome of a hepatitis B-like virus by reverse transcription of an RNA intermediate. Cell. 1982, 29: 403-415. 10.1016/0092-8674(82)90157-X.PubMed

82.

Nassal M: Hepatitis B viruses: reverse transcription a different way. Virus Res. 2008, 134: 235-249. 10.1016/j.virusres.2007.12.024.PubMed

83.

Rabe B, Vlachou A, Panté N, Helenius A, Kann M: Nuclear import of hepatitis B virus capsids and release of the viral genome. Proc Natl Acad Sci USA. 2003, 100: 9849-9854. 10.1073/pnas.1730940100.PubMedPubMedCentral

84.

Gerelsaikhan T, Tavis JE, Bruss V: Hepatitis B virus nucleocapsid envelopment does not occur without genomic DNA synthesis. J Virol. 1996, 70: 4269-4274.PubMedPubMedCentral

85.

Bruss V, Lu X, Thomssen R, Gerlich WH: Post-translational alterations in transmembrane topology of the hepatitis B virus large envelope protein. EMBO J. 1994, 13: 2273-2279.PubMedPubMedCentral

86.

Lambert C, Döring T, Prange R: Hepatitis B virus maturation is sensitive to functional inhibition of ESCRT-III, Vps4, and gamma 2-adaptin. J Virol. 2007, 81: 9050-9060. 10.1128/JVI.00479-07.PubMedPubMedCentral

87.

Sells MA, Chen ML, Acs G: Production of hepatitis B virus particles in Hep G2 cells transfected with cloned hepatitis B virus DNA. Proc Natl Acad Sci USA. 1987, 84: 1005-1009. 10.1073/pnas.84.4.1005.PubMedPubMedCentral

88.

Zahn P, Allain JP: Hepatitis C virus and hepatitis B virus bind to heparin: purification of largely IgG-free virions from infected plasma by heparin chromatography. J Gen Virol. 2005, 86: 677-685. 10.1099/vir.0.80614-0.PubMed

89.

Sureau C, Salisse J: A conformational heparan sulfate binding site essential to infectivity overlaps with the conserved hepatitis B virus a-determinant. Hepatology. 2013, 57: 985-994. 10.1002/hep.26125.PubMed

90.

Heermann KH, Goldmann U, Schwartz W, Seyffarth T, Baumgarten H, Gerlich WH: Large surface proteins of hepatitis B virus containing the pre-s sequence. J Virol. 1984, 52: 396-402.PubMedPubMedCentral

91.

Neurath AR, Kent SB, Strick N, Parker K: Identification and chemical synthesis of a host cell receptor binding site on hepatitis B virus. Cell. 1986, 46: 429-436. 10.1016/0092-8674(86)90663-X.PubMed

92.

Ishikawa T, Ganem D: The pre-S domain of the large viral envelope protein determines host range in avian hepatitis B viruses. Proc Natl Acad Sci USA. 1995, 92: 6259-6263. 10.1073/pnas.92.14.6259.PubMedPubMedCentral

93.

Eng FJ, Novikova EG, Kuroki K, Ganem D, Fricker LD: Gp180, a protein that binds duck hepatitis B virus particles, has metallocarboxypeptidase D-like enzymatic activity. J Biol Chem. 1998, 273: 8382-8388. 10.1074/jbc.273.14.8382.PubMed

94.

Glebe D, Aliakbari M, Krass P, Knoop EV, Valerius KP, Gerlich WH: Pre-s1 antigen-dependent infection of Tupaia hepatocyte cultures with human hepatitis B virus. J Virol. 2003, 77: 9511-9521. 10.1128/JVI.77.17.9511-9521.2003.PubMedPubMedCentral

95.

Yan H, Zhong G, Xu G, He W, Jing Z, Gao Z, Huang Y, Qi Y, Peng B, Wang H, Fu L, Song M, Chen P, Gao W, Ren B, Sun Y, Cai T, Feng X, Sui J, Li W: Sodium taurocholate cotransporting polypeptide is a functional receptor for human hepatitis B and D virus. Elife. 2012, 1: e00049-10.7554/eLife.00049.PubMedPubMedCentral

96.

Greenberg HB, Pollard RB, Lutwick LI, Gregory PB, Robinson WS, Merigan TC: Effect of human leukocyte interferon on hepatitis B virus infection in patients with chronic active hepatitis. N Engl J Med. 1976, 295: 517-522. 10.1056/NEJM197609022951001.PubMed

97.

Petersen J, Buti M: Considerations for the long-term treatment of chronic hepatitis B with nucleos(t)ide analogs. Expert Rev Gastroenterol Hepato. 2012, 6: 683-693. 10.1586/egh.12.52.

98.

Gerlich W, Stamm B, Thomssen R: Prognostic significance of quantitative HBsAg determination in acute hepatitis B. Partial report of a cooperative clinical study of the DFG-focus of “virus hepatitis”. Verh Dtsch Ges Inn Med. 1977, 83: 554-557. GermanPubMed

99.

Doong SL, Tsai CH, Schinazi RF, Liotta DC, Cheng YC: Inhibition of the replication of hepatitis B virus in vitro by 2′,3′-dideoxy-3′-thiacytidine and related analogues. Proc Natl Acad Sci USA. 1991, 88: 8495-8499. 10.1073/pnas.88.19.8495.PubMedPubMedCentral

100.

Benhamou Y, Dohin E, Lunel-Fabiani F, Poynard T, Huraux JM, Katlama C, Opolon P, Gentilini M: Efficacy of lamivudine on replication of hepatitis B virus in HIV-infected patients. Lancet. 1995, 345 (8946): 396-397. 10.1016/S0140-6736(95)90388-7.PubMed

101.

Dienstag JL, Perrillo RP, Schiff ER, Bartholomew M, Vicary C, Rubin M: A preliminary trial of lamivudine for chronic hepatitis B infection. N Engl J Med. 1995, 333: 1657-1661. 10.1056/NEJM199512213332501.PubMed

102.

Torresi J, Locarnini S: Antiviral chemotherapy for the treatment of hepatitis B virus infections. Gastroenterology. 2000, 118 (Suppl 1): S83-S103.PubMed

103.

Warner N, Locarnini S: The antiviral drug selected hepatitis B virus rtA181T/sW172* mutant has a dominant negative secretion defect and alters the typical profile of viral rebound. Hepatology. 2008, 48: 88-98. 10.1002/hep.22295.PubMed

104.

van Bömmel F, Wünsche T, Mauss S, Reinke P, Bergk A, Schürmann D, Wiedenmann B, Berg T: Comparison of adefovir and tenofovir in the treatment of lamivudine-resistant hepatitis B virus infection. Hepatology. 2004, 40: 1421-1425. 10.1002/hep.20464.PubMed

105.

Han GR, Cao MK, Zhao W, Jiang HX, Wang CM, Bai SF, Yue X, Wang GJ, Tang X, Fang ZX: A prospective and open-label study for the efficacy and safety of telbivudine in pregnancy for the prevention of perinatal transmission of hepatitis B virus infection. J Hepatol. 2011, 55: 1215-1221. 10.1016/j.jhep.2011.02.032.PubMed

106.

Volz T, Allweiss L, Barek MB M, Warlich M, Lohse AW, Pollok JM, Alexandrov A, Urban S, Petersen J, Lütgehetmann M, Dandri M: The entry inhibitor Myrcludex-B efficiently blocks intrahepatic virus spreading in humanized mice previously infected with hepatitis B virus. J Hepatol. 2013, 58: 861-867. 10.1016/j.jhep.2012.12.008.PubMed

107.

Kosinska AD, Zhang E, Johrden L, Liu J, Seiz PL, Zhang X, Ma Z, Kemper T, Fiedler M, Glebe D, Wildner O, Dittmer U, Lu M, Roggendorf M: Combination of DNA prime - adenovirus boost immunization with entecavir elicits sustained control of chronic hepatitis B in the woodchuck model. PLoS Pathog. 2013, 9: e1003391-10.1371/journal.ppat.1003391.PubMedPubMedCentral

108.

Beasley RP, Hwang LY, Lin CC, Stevens CE, Wang KY, Sun TS, Hsieh FJ, Szmuness W: Hepatitis B immune globulin (HBIG) efficacy in the interruption of perinatal transmission of hepatitis B virus carrier state. Initial report of a randomised double-blind placebo-controlled trial. Lancet. 1981, 2 (8243): 388-393.PubMed

109.

Krugman S, Giles JP, Hammond J: Viral hepatitis, type B (MS-2 strain). Studies on active immunization. JAMA. 1971, 217: 41-45. 10.1001/jama.1971.03190010023005.PubMed

110.

Purcell RH, Gerin JL: Hepatitis B subunit vaccine: a preliminary report of safety and efficacy tests in chimpanzees. Am J Med Sci. 1975, 270: 395-399. 10.1097/00000441-197509000-00024.PubMed

111.

Maupas P, Goudeau A, Coursaget P, Drucker J, Bagros P: Immunisation against hepatitis B in man. Lancet. 1976, 1 (7974): 1367-1370.PubMed

112.

Szmuness W, Stevens CE, Harley EJ, Zang EA, Oleszko WR, William DC, Sadovsky R, Morrison JM, Kellner A: Hepatitis B vaccine: demonstration of efficacy in a controlled clinical trial in a high-risk population in the United States. N Engl J Med. 1980, 303: 833-841. 10.1056/NEJM198010093031501.PubMed

113.

Peterson DL, Roberts IM, Vyas GN: Partial amino acid sequence of two major component polypeptides of hepatitis B surface antigen. Proc Natl Acad Sci USA. 1977, 74: 1530-1534. 10.1073/pnas.74.4.1530.PubMedPubMedCentral

114.

Valenzuela P, Medina A, Rutter WJ, Ammerer G, Hall BD: Synthesis and assembly of hepatitis B virus surface antigen particles in yeast. Nature. 1982, 298: 347-350. 10.1038/298347a0.PubMed

115.

Harford N, Cabezon T, Crabeel M, Simoen E, Rutgers A, De Wilde M: Expression of hepatitis B surface antigen in yeast. Dev Biol Stand. 1983, 54: 125-130.PubMed

116.

McAleer WJ, Buynak EB, Maigetter RZ, Wampler DE, Miller WJ, Hilleman MR: Human hepatitis B vaccine from recombinant yeast. Nature. 1984, 307: 178-180. 10.1038/307178a0.PubMed

117.

Poovorawan Y, Sanpavat S, Pongpunlert W, Chumdermpadetsuk S, Sentrakul P, Safary A: Protective efficacy of a recombinant DNA hepatitis B vaccine in neonates of HBe antigen-positive mothers. JAMA. 1989, 261: 3278-3281. 10.1001/jama.1989.03420220092033.PubMed

118.

Lavanchy D: Viral hepatitis: global goals for vaccination. J Clin Virol. 2012, 55: 296-302. 10.1016/j.jcv.2012.08.022.PubMed

119.

Chang MH, You SL, Chen CJ, Liu CJ, Lee CM, Lin SM, Chu HC, Wu TC, Yang SS, Kuo HS, Chen DS, Taiwan Hepatoma Study Group: Decreased incidence of hepatocellular carcinoma in hepatitis B vaccinees: a 20-year follow-up study. J Natl Cancer Inst. 2009, 101: 1348-1355. 10.1093/jnci/djp288.PubMed

120.

Su WJ, Liu CC, Liu DP, Chen SF, Huang JJ, Chan TC, Chang MH: Effect of age on the incidence of acute hepatitis B after 25 years of a universal newborn hepatitis B immunization program in Taiwan. J Infect Dis. 2012, 205: 757-762. 10.1093/infdis/jir852.PubMed

121.

Poovorawan Y, Chongsrisawat V, Theamboonlers A, Leroux-Roels G, Kuriyakose S, Leyssen M, Jacquet J-M: Evidence of protection against clinical and chronic hepatitis B infection 20 years after infant vaccination in a high endemicity region. J Viral Hepat. 2011, 18: 369-375. 10.1111/j.1365-2893.2010.01312.x.PubMedPubMedCentral

122.

Coates T, Wilson R, Patrick G, André F, Watson V: Hepatitis B vaccines: assessment of the seroprotective efficacy of two recombinant DNA vaccines. Clin Ther. 2001, 23: 392-403. 10.1016/S0149-2918(01)80044-8.PubMed

123.

Wolters B, Junge U, Dziuba S, Roggendorf M: Immunogenicity of combined hepatitis A and B vaccine in elderly persons. Vaccine. 2003, 21: 3623-3628. 10.1016/S0264-410X(03)00399-2.PubMed

124.

Hsu HY, Chang MH, Ni YH, Chiang CL, Chen HL, Wu JF, Chen PJ: No increase in prevalence of hepatitis B surface antigen mutant in a population of children and adolescents who were fully covered by universal infant immunization. J Infect Dis. 2010, 201: 1192-1200. 10.1086/651378.PubMed

125.

Stramer SL, Wend U, Candotti D, Foster GA, Hollinger FB, Dodd RY, Allain J-P, Gerlich W: Nucleic acid testing to detect HBV infection in blood donors. New Engl J Med. 2011, 364: 236-247. 10.1056/NEJMoa1007644.PubMed

126.

Feeney SA, McCaughey C, Watt AP, El Agnaf MR, McDougal N, Morris K, Wend UC, Gerlich WH, Coyle PV: Reactivation of occult hepatitis B virus infection following cytotoxic lymphoma therapy in an anti-HBc negative patient. J Med Virol. 2013, 85: 597-601. 10.1002/jmv.23513.PubMed

127.

Bremer CM, Sominskaya I, Skrastina D, Pumpens P, El Wahed AA, Beutling U, Frank R, Fritz HJ, Hunsmann G, Gerlich WH, Glebe D: N-terminal myristoylation-dependent masking of neutralizing epitopes in the preS1 attachment site of hepatitis B virus. J Hepatol. 2011, 55: 29-37. 10.1016/j.jhep.2010.10.019.PubMed

128.

Chen D-S: Toward elimination and eradication of hepatitis B. J Gastroenterol Hepatol. 2010, 25: 11-25.

129.

Zuckerman JN, Zuckerman AJ: Recombinant hepatitis B triple antigen vaccine: Hepacare. Expert Rev Vaccines. 2002, 1: 141-144. 10.1586/14760584.1.2.141.PubMed

130.

Shouval D: Hepatitis B, vaccines. J Hepatol. 2003, 39 (Suppl 1): S70-S76.PubMed

131.

Rendi-Wagner P, Shouval D, Genton B, Lurie Y, Rümke H, Boland G, Cerny A, Heim M, Bach D, Schroeder M, Kollaritsch H: Comparative immunogenicity of a PreS/S hepatitis B vaccine in non- and low responders to conventional vaccine. Vaccine. 2006, 24: 2781-2789. 10.1016/j.vaccine.2006.01.007.PubMed

132.

Niedre-Otomere B, Bogdanova A, Skrastina D, Zajakina A, Bruvere R, Ose V, Gerlich WH, Garoff H, Pumpens P, Glebe D, Kozlovska T: Recombinant Semliki forest virus vectors encoding hepatitis B virus small surface and pre-S1 antigens induce broadly reactive neutralizing antibodies. J Viral Hepatitis. 2012, 19: 664-673. 10.1111/j.1365-2893.2012.01594.x.

Title: Medical Virology of Hepatitis B: how it began and where we are now
Author: Wolfram H Gerlich
Publication date: 01-12-2013
Publisher: BioMed Central
Published in: Virology Journal / Issue 1/2013
Electronic ISSN: 1743-422X
DOI: https://doi.org/10.1186/1743-422X-10-239

ACC 2024 Congress Coverage

Heart Failure Video

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Medical Virology of Hepatitis B: how it began and where we are now

Abstract

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 1/2013

Roles and functions of HIV-1 Tat protein in the CNS: an overview

MicroRNA-145 regulates oncolytic herpes simplex virus-1 for selective killing of human non-small cell lung cancer cells

Analysis of whole genome sequences of 16 strains of rubella virus from the United States, 1961–2009

Characterization of Farmington virus, a novel virus from birds that is distantly related to members of the family Rhabdoviridae

Complete genome sequencing and analysis of six enterovirus 71 strains with different clinical phenotypes

A cell based high-throughput screening approach for the discovery of new inhibitors of respiratory syncytial virus

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page