Dating the origin and dispersal of hepatitis B virus infection in humans and primates

Paraskevis, Dimitrios; Magiorkinis, Gkikas; Magiorkinis, Emmanouil; Ho, Simon Y. W.; Belshaw, Robert; Allain, Jean‐Pierre; Hatzakis, Angelos

doi:10.1002/hep.26079

Cited by 142 publications

(183 citation statements)

References 42 publications

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“…The colonization-adaptation trade-off (CAT) model reconciles the high short-term and apparently low long-term HBV evolutionary rates reported in the literature (2,4,5,23,24). In chronic HBV, limited host immunity against HBV at an early stage (the immune tolerance or noninflammatory phase) (8,11) might favor viruses with a high replication ability (represented by the blank area in the upper circles in Fig.…”

Section: Discussionsupporting

confidence: 54%

“…The time-dependent HBV substitution rate may shed light on the evolutionary origin of HBV, which is still controversial, because the substitution rates required for HBV/human codivergence are an order of magnitude lower than those estimated based on extant sequences (3,4,23,25,26). Figure 2A We applied these equations to test if the divergence of the HBV-F/H genotypes from American Indians corresponded to their first colonization of the Americas.…”

Section: Discussionmentioning

confidence: 99%

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New Insights into the Evolutionary Rate of Hepatitis B Virus at Different Biological Scales

Lin

Liu

Chien

et al. 2015

J Virol

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The evolutionary rates of hepatitis B virus (HBV) estimated using contemporary sequences are 10 2 to 10 4 times higher than those derived from archaeological and genetic evidence. This discrepancy makes the origin of HBV and the time scale of its spread, both of which are critical for studying the burden of HBV pathogenicity, largely unresolved. To evaluate whether the dual demands (i.e., adaptation within hosts and colonization between hosts) of the viral life cycle affect this conundrum, the HBV quasispecies dynamics within and among hosts from a family consisting of a grandmother, her 5 children, and her 2 granddaughters, all of whom presumably acquired chronic HBV through mother-to-infant transmission, were examined by PCR cloning and next-generation sequencing methods. We found that the evolutionary rate of HBV between hosts was considerably lower than that within hosts. Moreover, the between-host substitution rates of HBV decreased as transmission numbers between individuals increased. Both observations were due primarily to changes at nonsynonymous rather than synonymous sites. There were significantly more multiple substitutions than expected for random mutation processes, and 97% of substitutions were changed from common to rare amino acid residues in the database. Continual switching between colonization and adaptation resulted in a rapid accumulation of mutations at a limited number of positions, which quickly became saturated, whereas substitutions at the remaining regions occurred at a much lower rate. Our study may help to explain the time-dependent HBV substitution rates reported in the literature and provide new insights into the origin of the virus. IMPORTANCEIt is known that the estimated hepatitis B virus (HBV) substitution rate is time dependent, but the reason behind this observation is still elusive. We hypothesize that owing to the small genome size of HBV, transmission between hosts and adaptation within hosts must exhibit high levels of fitness trade-offs for the virus. By studying the HBV quasispecies dynamics for a chain of sequentially infected transmissions within a family, we found the HBV substitution rate between patients to be negatively correlated with the number of transmissions. Continual switching between hosts resulted in a rapid accumulation of mutations at a limited number of genomic sites, which quickly became saturated in the short term. Nevertheless, substitutions at the remaining regions occurred at a much lower rate. Therefore, the HBV substitution rate decreased as the divergence time increased. H epatitis B virus (HBV) is one of the most common infectious agents in the world. According to the World Health Organization (WHO), more than a third of the world's population (2 billion people) has been infected with HBV, and 240 million people among them are chronic carriers (1). Despite its importance, the evolutionary origins of HBV and the time scale of its spread remain elusive. For example, if the evolutionary history of HBV is calibrated using phylodynamic ph...

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Section: Discussionsupporting

confidence: 54%

Section: Discussionmentioning

confidence: 99%

New Insights into the Evolutionary Rate of Hepatitis B Virus at Different Biological Scales

Lin

Liu

Chien

et al. 2015

J Virol

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“…In this study, we demonstrated that WMHBV, like human HBV, uses Tupaia NTCP as a cellular receptor for entry into PTHs. Given that among all of the primate HBV family members, WMHBV is phylogenetically the most distant from human HBV (12,28), and both WMHBV and HBV utilize Tupaia NTCP to infect PTHs, it is conceivable that NTCP likely serves as a common cellular receptor for the entry of all known primate hepadnaviruses into host cells.…”

Section: Fig 4 Inhibition Of Wmhbv Infection In Pths By Tsntcp-bindinmentioning

confidence: 99%

Sodium Taurocholate Cotransporting Polypeptide Mediates Woolly Monkey Hepatitis B Virus Infection of Tupaia Hepatocytes

Zhong

Yan

Wang

et al. 2013

J Virol

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dPrimary Tupaia hepatocytes (PTHs) are susceptible to woolly monkey hepatitis B virus (WMHBV) infection, but the identity of the cellular receptor(s) mediating WMHBV infection of PTHs remains unclear. Recently, sodium taurocholate cotransporting polypeptide (NTCP) was identified as a functional receptor for human hepatitis B virus (HBV) infection of primary human and Tupaia hepatocytes. In this study, a synthetic pre-S1 peptide from WMHBV was found to bind specifically to cells expressing Tupaia NTCP (tsNTCP) and it efficiently blocked WMHBV entry into PTHs; silencing of tsNTCP in PTHs significantly inhibited WMHBV infection. Ectopic expression of tsNTCP rendered HepG2 cells susceptible to WMHBV infection. These data demonstrate that tsNTCP is a functional receptor for WMHBV infection of PTHs. The result also indicates that NTCP's orthologs likely act as a common cellular receptor for all known primate hepadnaviruses. Human hepatitis B virus (HBV) is a leading cause of liver diseases ranging from acute hepatitis to chronic hepatitis, cirrhosis, and hepatocellular carcinoma. With approximately 240 million cases of chronic infection worldwide, HBV is responsible for about 600,000 deaths annually (1). Despite its enormous medical and social relevance, progress in HBV research has been impeded by the lack of understanding of HBV entry by which the virus specifically infects human liver cells. Recently we found that sodium taurocholate cotransporting polypeptide (NTCP; also known as SLC10A1 [solute carrier family 10 member 1]), a hepatic sodium/bile acid symporter presumed to span the cellular membrane up to 10 times with small extracellular loops (2-5), is a functional receptor for human HBV and hepatitis D virus (HDV) infections of human and Tupaia hepatocytes (6). The pre-S1 domain of the HBV large envelope protein (L protein) is the key determinant of interaction with the cellular receptor NTCP (6). Furthermore, the critical receptor-binding motif in the pre-S1 domain of human HBV (7-10) is conserved among all hepadnaviruses from humans and nonhuman primates, including chimpanzees, gorillas, orangutans, gibbons, and woolly monkeys (Fig. 1A). Therefore, it is tempting to speculate that NTCP may play an important role in the entry of all known primate hepadnaviruses into host cells.Woolly monkey HBV (WMHBV) is the only hepadnavirus of a nonhuman primate with an established infectious clone and has been studied in some detail (10-18). It was originally isolated from a woolly monkey (Lagothrix lagotricha) with fulminant hepatitis. It has the same genetic organization as and shares 78% sequence identity with human HBV (12). Both the woolly monkey and a closely related New World monkey, the spider monkey (Ateles geoffroyi), are susceptible to WMHBV infection, while chimpanzees are minimally susceptible (11,12). In cell cultures, WMHBV or WMHBV envelope pseudotyped HDV could consistently infect spider monkey and, with much lower efficiency, chimpanzee and human hepatocytes (10,14,15). Similar to HBV, WMHBV infects hepat...

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“…The current paper reports the demographic, epidemiological, and clinical characteristics of 170 HBsAg-positive 2 Hepat Mon. 2017; 17(8):e13260.…”

Section: Study Populationmentioning

confidence: 99%

Hepatitis B Virus Genotypes, Epidemiological Characteristics, and Clinical Presentation of HBV Chronic Infection in Immigrant Populations Living in Southern Italy

Sagnelli

Alessio²,

Gualdieri³

et al. 2017

Hepat Mon

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Background: Information on hepatitis B virus (HBV) genotypes in immigrant populations living in Italy is scanty. Objectives: The current study aimed at assessing the epidemiological and clinical need to detect HBV genotypes in immigrants with HBV infection. Methods: A multicenter screening was performed in 5 first-level care facilities centers in Southern Italy to identify migrants with HBV infection. Hepatitis B surface antigen (HBsAg)-positive subjects were further investigated at a tertiary unit of infectious diseases. Results: Of the 1727 investigated immigrants, 170 (9.8%) were HBsAg-positive. These 170 subjects, prevalently males (86.5%), aged 31.0

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Dating the origin and dispersal of hepatitis B virus infection in humans and primates

Cited by 142 publications

References 42 publications

New Insights into the Evolutionary Rate of Hepatitis B Virus at Different Biological Scales

New Insights into the Evolutionary Rate of Hepatitis B Virus at Different Biological Scales

Sodium Taurocholate Cotransporting Polypeptide Mediates Woolly Monkey Hepatitis B Virus Infection of Tupaia Hepatocytes

Hepatitis B Virus Genotypes, Epidemiological Characteristics, and Clinical Presentation of HBV Chronic Infection in Immigrant Populations Living in Southern Italy

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