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Origin and Structure Similarity with the Central Domain of DNA Glycosylase

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Origin and Structure Similarity with the Central Domain of DNA Glycosylase Protein X of Hepatitis B Virus: Origin and Structure Similarity with the Central Domain of DNA Glycosylase Formijn J. van Hemert1*, Maarten A. A. van de Klundert3, Vladimir V. Lukashov1*, Neeltje A. Kootstra3, Ben Berkhout1, Hans L. Zaaijer2,3 1 Laboratory of Experimental Virology, Department of Medical Microbiology, Center for Infection and Immunity Amsterdam (CINIMA), Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands, 2 Laboratory Clinical Virology, Department of Medical Microbiology, Center for Infection and Immunity Amsterdam (CINIMA), Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands, 3 Laboratory of Experimental Immunology, Department of Medical Microbiology, Center for Infection and Immunity Amsterdam (CINIMA), Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands Abstract Orthohepadnavirus (mammalian hosts) and avihepadnavirus (avian hosts) constitute the family of Hepadnaviridae and differ by their capability and inability for expression of protein X, respectively. Origin and functions of X are unclear. The evolutionary analysis at issue of X indicates that present strains of orthohepadnavirus started to diverge about 25,000 years ago, simultaneously with the onset of avihepadnavirus diversification. These evolutionary events were preceded by a much longer period during which orthohepadnavirus developed a functional protein X while avihepadnavirus evolved without X. An in silico generated 3D-model of orthohepadnaviral X protein displayed considerable similarity to the tertiary structure of DNA glycosylases (key enzymes of base excision DNA repair pathways). Similarity is confined to the central domain of MUG proteins with the typical DNA-binding facilities but without the capability of DNA glycosylase enzymatic activity. The hypothetical translation product of a vestigial X reading frame in the genome of duck hepadnavirus could also been folded into a DNA glycosylase-like 3D-structure. In conclusion, the most recent common ancestor of ortho- and avihepadnavirus carried an X sequence with orthology to the central domain of DNA glycosylase. Citation: van Hemert FJ, van de Klundert MAA, Lukashov VV, Kootstra NA, Berkhout B, et al. (2011) Protein X of Hepatitis B Virus: Origin and Structure Similarity with the Central Domain of DNA Glycosylase. PLoS ONE 6(8): e23392. doi:10.1371/journal.pone.0023392 Editor: Jean-Pierre Vartanian, Institut Pasteur, France Received May 11, 2011; Accepted July 15, 2011; Published August 5, 2011 Copyright: ß 2011 van Hemert et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: The authors have no support or funding to report. Competing Interests: The authors have declared that no competing interests exist. * E-mail: [email protected] (FJvH); [email protected] (VVL) Introduction DDB1 (Damaged DNA Binding Protein1), in which case protein X redirects the ubiquitin ligase activity of CUL4-DDB1 E3 The hepatitis B virus (HBV) particle contains a partially double complexes, which are intimately involved in the intracellular stranded DNA genome of about 3200 base pairs [1,2] with four regulation of DNA replication and repair, transcription and signal partially overlapping reading frames encoding the C, S and X transduction [13]. The X protein is well conserved among proteins and the error-prone viral reverse transcriptase or (mammalian) orthohepadnavirus, but absent in avihepadnavirus. polymerase [3,4]. Besides human HBV, the subfamily of Similarity of X with host cellular proteins appeared to be below or Orthohepadnaviridae includes similar virus strains isolated from near the threshold level of detection and a crystal model of its 3D- gorilla, orangutan, chimpanzee, gibbon, woolly monkey, chuck structure is currently not available. and squirrel species. Infections by Avihepadnaviridae have been Here, we present an in silico generated model of the X tertiary demonstrated in duck, goose, heron and stork species. About 300 structure. The X model of choice is the best of the 5 alternative million patients worldwide carry a chronic HBV infection [5], structures constructed by the modeling software. In docking which causes the death of over one million persons annually by experiments of the X structures with HBXIP or DDB1 into liver failure or hepatocellular carcinoma [6]. Transgenic mice heterodimers, X model 1 outperforms most other models expressing the X protein in liver were prone to develop regarding the interface stability of these complexes. Amino acid hepatocellular carcinoma [7]. However, the cellular pathways residues in X proven to be critical for dimer formation with along which X induces hepatocellular carcinoma are fragmentary HBXIP are among the contact residues of the interface. In documented [8]. The X protein is 154 amino acids in size and heterodimers of DDB1 with full-length protein X, the interfaces displays direct or indirect interaction with host factors, thus contain most of the H-box a-helical X residues that were described modulating a plethora of cellular processes. Protein X interferes to be involved in a DDB1/H-box oligopeptide complex [13]. We with transcription, signal transduction, cell cycle progress, protein have queried the PDB database for proteins displaying similarity degradation, apoptosis and chromosomal stability [9–11]. More with the X 3D-structure and found a striking similarity of X with specifically, heterodimer complex formation of X with its cellular members of the MUG family of DNA glycosylases, which are the target protein (HBX interacting protein, HBXIP) has been key enzymes of the BER (base excision repair) pathway [14]. Even demonstrated, triggering deregulation of centrosome dynamics the hypothetical translation product of a vestigial X reading frame and mitotic spindle formation [12]. Another interaction involves in duck hepadnavirus - after restoration of stopcodons into coding PLoS ONE | www.plosone.org 1 August 2011 | Volume 6 | Issue 8 | e23392 3D-Structure Similarity of HBx with DNA Glycosylase triplets [15] - showed a 3D-structure with significant similarity to (http://cbsuapps.tc.cornell.edu/beast.aspx) for phylogenetic re- MUG proteins. Protein-DNA docking experiments indicated a construction and tMRCA (time of the most recent common binding capability of X protein to an oligodeoxynucleotide that ancestor) estimation. An uncorrelated lognormal relaxed molec- has been analyzed by X-ray in complex with E. coli MUG DNA ular clock was assumed to act via the JTT amino acid replacement glycosylase [16,17]. From the evolutionary point of view, model [25] with gamma and invariant site heterogeneity. A orthohepadnavirus and avihepadnavirus share a common protein constant population size was chosen as a demographic model. X ancestor with orthology to DNA glycosylase. Identical analyses were done in parallel over a sufficient period of time to achieve convergence of Monte Carlo Markov chains. Materials and Methods Relevant XML files are added as Supporting Information Files. DNA glycosylases are indicated by their PDB entry (lower case) The NCBI reference set served as a source of human HBV with the chain identifier (upper case). The actual GenBank sequences. Hepadnavirus sequences of non-human hosts (other accession numbers are mentioned in table and figures. TimeTree primates, woolly monkey, chuck, squirrel and birds) were [26] estimates of species divergence were used to calibrate BEAST downloaded from GenBank. X protein sequences were derived analyses for the determination of the rate of amino acid by translation of the appropriate reading frame in complete viral replacements in animal DNA glycosylases. 3D-models were genomes. An ancestral and a consensus sequence of human HBV generated by submission to the i-TASSER server [27] and X protein was constructed from the same collection by means of visualized by means of RasTop 2.2 (http://sourceforge.net/ the ANCESCON server [18] and by BioEdit [19], respectively. An projects/rastop). Application of parent or template structures HBV genotype D consensus sequence was available [20]. (server-detected or custom-supplied) is mentioned in the text. Sequences with relatively high similarity were aligned by ClustalW Protein-protein docking was achieved by ClusPro 1.0 [28] and by [21] or by PROBCONS [22] in case of low similarity. Alignments ClusPro 2.0, presently available as PIPER [29]. The usage of were combined by the profile-to-profile option of MUSCLE [23] ALASCAN [30] for the identification of protein-protein interfaces and subjected to rounds of manual refinement particularly at gap and the calculation of interface stability has been described borders. The BEAST suite consisting of the modules Beauti, Beast, previously [31]. Distances between amino acid residues were Logcombiner, TreeAnnotator v1.4.8, Tracer v1.4.1 and FigTree estimated by means of Chimera v1.6 [32]. Protein-DNA docking v1.2.3 [24] was used locally and distantly on the BEAST server of was performed by means of PatchDock [33] and HEX [34]. the Computational Biology Service Unit at Cornell University Protein-DNA interfaces were analyzed by means of ProTorP [35]. Figure 1. Phylogeny and divergence time estimates of hepadnaviral protein X. (A) Virus strains are indicated by the common name of their hosts and the GenBank accession identifier. The evolutionary
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