Abstract
Hepadnaviruses are DNA viruses that replicate through reverse transcription of an RNA pregenome. Viral DNA synthesis takes place inside viral nucleocapsids, formed by core protein dimers. Previous studies have identified carboxy-terminal truncations of the core protein that affect viral DNA maturation. Here, we describe the effect of small amino-terminal insertions into the duck hepatitis B virus (DHBV) core protein on viral DNA replication. All insertion mutants formed replication-competent nucleocapsids. Elongation of viral DNA, however, appeared to be incomplete. Increasing the number of additional amino acids and introducing negatively charged residues further reduced the observed size of mature viral DNA species. Mutant core proteins did not inhibit the viral polymerase. Instead, viral DNA synthesis destabilized mutant nucleocapsids, rendering mature viral DNA selectively sensitive to nuclease action. Interestingly, the phenotype of two previously described carboxy-terminal DHBV core protein deletion mutants was found to be based on the same mechanism. These data suggest that (i) the amino- as well as the carboxy-terminal portion of the DHBV core protein plays a critical role in nucleocapsid stabilization, and (ii) the hepadnavirus polymerase can perform partial second-strand DNA synthesis in the absence of intact viral nucleocapsids.
MeSH Terms
Amino Acid Sequence
Animals
Cell Line
Chickens
DNA, Viral/biosynthesis,genetics,metabolism
Hepatitis B Virus, Duck/genetics,physiology
Molecular Sequence Data
Mutagenesis, Insertional
Nucleocapsid/biosynthesis,chemistry,genetics
Sequence Deletion
Viral Core Proteins/chemistry,genetics,metabolism
Virus Replication
Chemicals
DNA, Viral
Viral Core Proteins
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Köck J
Department of Medicine II, University of Freiburg, Freiburg, Germany.
Wieland S
Blum H E
von Weizsäcker F
References (32)
32 references, click to expand
-
A protease-sensitive hinge linking the two domains of the hepatitis B virus core protein is exposed on the viral capsid surface.
J Virol. 1994 Sep;68(9):5548-55
PMID: 7520091
-
Three-dimensional structure of hepatitis B virus core particles determined by electron cryomicroscopy.
Cell. 1994 Jun 17;77(6):943-50
PMID: 8004680
-
Nucleotide priming and reverse transcriptase activity of hepatitis B virus polymerase expressed in insect cells.
J Virol. 1995 Jul;69(7):4431-9
PMID: 7539509
-
Recent studies on replication of hepatitis B virus.
J Hepatol. 1995;22(1 Suppl):9-13
PMID: 7602085
-
Evolutionary conservation in the hepatitis B virus core structure: comparison of human and duck cores.
Structure. 1995 Oct 15;3(10):1009-19
PMID: 8589996
-
Inhibition of viral replication by genetically engineered mutants of the duck hepatitis B virus core protein.
Hepatology. 1996 Aug;24(2):294-9
PMID: 8690395
-
Determination of the fold of the core protein of hepatitis B virus by electron cryomicroscopy.
Nature. 1997 Mar 6;386(6620):88-91
PMID: 9052786
-
Visualization of a 4-helix bundle in the hepatitis B virus capsid by cryo-electron microscopy.
Nature. 1997 Mar 6;386(6620):91-4
PMID: 9052787
-
cis-Acting sequences in addition to donor and acceptor sites are required for template switching during synthesis of plus-strand DNA for duck hepatitis B virus.
J Virol. 1997 Jul;71(7):5336-44
PMID: 9188603
-
Why are hepadnaviruses DNA and not RNA viruses?
Trends Microbiol. 1997 Nov;5(11):447-50
PMID: 9402701
-
Virus-like particles in serum of patients with Australia-antigen-associated hepatitis.
Lancet. 1970 Apr 4;1(7649):695-8
PMID: 4190997
-
A virus similar to human hepatitis B virus associated with hepatitis and hepatoma in woodchucks.
Proc Natl Acad Sci U S A. 1978 Sep;75(9):4533-7
PMID: 212758
-
Virus of Pekin ducks with structural and biological relatedness to human hepatitis B virus.
J Virol. 1980 Dec;36(3):829-36
PMID: 7463557
-
Replication of the genome of a hepatitis B--like virus by reverse transcription of an RNA intermediate.
Cell. 1982 Jun;29(2):403-15
PMID: 6180831
-
Biochemical and genetic evidence for the hepatitis B virus replication strategy.
Science. 1986 Apr 25;232(4749):477-84
PMID: 3961490
-
Establishment and characterization of a chicken hepatocellular carcinoma cell line, LMH.
Cancer Res. 1987 Aug 15;47(16):4460-4
PMID: 3607775
-
The molecular biology of the hepatitis B viruses.
Annu Rev Biochem. 1987;56:651-93
PMID: 3039907
-
The duck hepatitis B virus core protein contains a highly phosphorylated C terminus that is essential for replication but not for RNA packaging.
J Virol. 1989 Jul;63(7):2995-3000
PMID: 2724419
-
A recombinant hepatitis B core antigen polypeptide with the protamine-like domain deleted self-assembles into capsid particles but fails to bind nucleic acids.
J Virol. 1989 Nov;63(11):4645-52
PMID: 2677399
-
Efficient duck hepatitis B virus production by an avian liver tumor cell line.
J Virol. 1990 Jul;64(7):3249-58
PMID: 2352324
-
Hepatitis B virus nucleocapsid assembly: primary structure requirements in the core protein.
J Virol. 1990 Jul;64(7):3319-30
PMID: 2191149
-
A domain of the hepadnavirus capsid protein is specifically required for DNA maturation and virus assembly.
J Virol. 1991 May;65(5):2511-7
PMID: 2016770
-
The effect of the structure of the terminal regions of the hepatitis B virus gene C polypeptide on the formation of core antigen (HBcAg) particles.
Biomed Sci. 1991;2(3):257-65
PMID: 1751758
-
The arginine-rich domain of the hepatitis B virus core protein is required for pregenome encapsidation and productive viral positive-strand DNA synthesis but not for virus assembly.
J Virol. 1992 Jul;66(7):4107-16
PMID: 1602535
-
RNA- and DNA-binding activities in hepatitis B virus capsid protein: a model for their roles in viral replication.
J Virol. 1992 Sep;66(9):5232-41
PMID: 1501273
-
The reverse transcriptase of hepatitis B virus acts as a protein primer for viral DNA synthesis.
Cell. 1992 Nov 13;71(4):663-70
PMID: 1384989
-
Hepatitis B virus capsid particles are assembled from core-protein dimer precursors.
Proc Natl Acad Sci U S A. 1992 Nov 1;89(21):10046-50
PMID: 1438193
-
Expression of functional hepatitis B virus polymerase in yeast reveals it to be the sole viral protein required for correct initiation of reverse transcription.
Proc Natl Acad Sci U S A. 1993 May 1;90(9):4107-11
PMID: 7683422
-
Carboxy-terminal truncations of the HBV core protein affect capsid formation and the apparent size of encapsidated HBV RNA.
Virology. 1993 Jun;194(2):597-607
PMID: 7684872
-
Recombinant human hepatitis B virus reverse transcriptase is active in the absence of the nucleocapsid or the viral replication origin, DR1.
J Virol. 1993 Aug;67(8):4513-20
PMID: 7687299
-
Hepatitis B virus replication.
Trends Microbiol. 1993 Sep;1(6):221-8
PMID: 8137119
-
Identification of two separable modules in the duck hepatitis B virus core protein.
J Virol. 1995 Apr;69(4):2704-7
PMID: 7884928