Skip to main content
Top
Published in: Archives of Virology 10/2017

01-10-2017 | Review

Modulation of Wnt signaling pathway by hepatitis B virus

Authors: Muhammad Daud, Muhammad Adeel Rana, Tayyab Husnain, Bushra Ijaz

Published in: Archives of Virology | Issue 10/2017

Login to get access

Abstract

Hepatitis B virus (HBV) has a global distribution and is one of the leading causes of hepatocellular carcinoma. The precise mechanism of pathogenicity of HBV-associated hepatocellular carcinoma (HCC) is not yet fully understood. Viral-related proteins are known to take control of several cellular pathways like Wnt/β-catenin, TGF-β, Raf/MAPK and ROS for the virus’s own replication. This affects cellular persistence, multiplication, migration, alteration and genomic instability. The Wnt/FZD/β-catenin signaling pathway plays a significant role in the pathology and physiology of the liver and has been identified as a main factor in HCC development. The role of β-catenin is linked mainly to the canonical pathway of the signaling system. Progression of liver diseases is known to be accompanied by disturbances in β-catenin expression (mainly overexpression), with its cytoplasmic or nuclear translocation. In recent years, studies have documented that the HBV X protein and hepatitis B surface antigen (HBsAg) can act as pathogenic factors that are involved in the modulation and induction of canonical Wnt signaling pathway. In the present review we explore the interaction of HBV genome products with components of the Wnt/β–catenin signaling pathway that results in the enhancement of the pathway and leads to hepatocarcinogenesis.
Literature
4.
go back to reference Milich D, Liang TJ (2003) Exploring the biological basis of hepatitis B e antigen in hepatitis B virus infection. Hepatology 38(5):1075–1086CrossRefPubMed Milich D, Liang TJ (2003) Exploring the biological basis of hepatitis B e antigen in hepatitis B virus infection. Hepatology 38(5):1075–1086CrossRefPubMed
5.
go back to reference Han Y et al (2013) Regulation of B7-H1 expression on peripheral monocytes and IFN-γ secretion in T lymphocytes by HBeAg. Cell Immunol 283(1):25–30CrossRefPubMed Han Y et al (2013) Regulation of B7-H1 expression on peripheral monocytes and IFN-γ secretion in T lymphocytes by HBeAg. Cell Immunol 283(1):25–30CrossRefPubMed
9.
go back to reference Murakami S (2001) Hepatitis B virus X protein: a multifunctional viral regulator. J Gastroenterol 36(10):651–660CrossRefPubMed Murakami S (2001) Hepatitis B virus X protein: a multifunctional viral regulator. J Gastroenterol 36(10):651–660CrossRefPubMed
10.
go back to reference Feitelson MA, Duan L-X (1997) Hepatitis B virus X antigen in the pathogenesis of chronic infections and the development of hepatocellular carcinoma. Am J Pathol 150(4):1141PubMedPubMedCentral Feitelson MA, Duan L-X (1997) Hepatitis B virus X antigen in the pathogenesis of chronic infections and the development of hepatocellular carcinoma. Am J Pathol 150(4):1141PubMedPubMedCentral
11.
12.
16.
go back to reference Chen GF, Wang C, Lau G (2017) Treatment of chronic hepatitis B infection-2017. Liver Int 37(S1):59–66CrossRefPubMed Chen GF, Wang C, Lau G (2017) Treatment of chronic hepatitis B infection-2017. Liver Int 37(S1):59–66CrossRefPubMed
17.
go back to reference Bejsovec A (2006) Flying at the head of the pack: Wnt biology in Drosophila. Oncogene 25(57):7442–7449CrossRefPubMed Bejsovec A (2006) Flying at the head of the pack: Wnt biology in Drosophila. Oncogene 25(57):7442–7449CrossRefPubMed
18.
go back to reference Brunt LH et al (2017) Wnt Signalling controls the response to mechanical loading during zebrafish joint development. 115105 (bioRxiv2017) Brunt LH et al (2017) Wnt Signalling controls the response to mechanical loading during zebrafish joint development. 115105 (bioRxiv2017)
19.
20.
go back to reference Kumawat K, Gosens R (2016) WNT-5A: signaling and functions in health and disease. Cell Mol Life Sci 73(3):567–587CrossRefPubMed Kumawat K, Gosens R (2016) WNT-5A: signaling and functions in health and disease. Cell Mol Life Sci 73(3):567–587CrossRefPubMed
22.
go back to reference Mulligan KA, Cheyette BN (2016) Neurodevelopmental perspectives on Wnt signaling in psychiatry. Mol Neuropsychiatry 2(4):219–246CrossRef Mulligan KA, Cheyette BN (2016) Neurodevelopmental perspectives on Wnt signaling in psychiatry. Mol Neuropsychiatry 2(4):219–246CrossRef
24.
go back to reference Takahashi H et al (2017) Possible role of nuclear β-catenin in resistance to preoperative chemoradiotherapy in locally advanced rectal cancer. Histol. doi:10.1111/his.13227 Takahashi H et al (2017) Possible role of nuclear β-catenin in resistance to preoperative chemoradiotherapy in locally advanced rectal cancer. Histol. doi:10.​1111/​his.​13227
26.
27.
go back to reference Hart M et al (1999) The F-box protein β-TrCP associates with phosphorylated β-catenin and regulates its activity in the cell. Curr Biol 9(4):207–211CrossRefPubMed Hart M et al (1999) The F-box protein β-TrCP associates with phosphorylated β-catenin and regulates its activity in the cell. Curr Biol 9(4):207–211CrossRefPubMed
28.
go back to reference Kimelman D, Xu W (2006) β-Catenin destruction complex: insights and questions from a structural perspective. Oncogene 25(57):7482–7491CrossRefPubMed Kimelman D, Xu W (2006) β-Catenin destruction complex: insights and questions from a structural perspective. Oncogene 25(57):7482–7491CrossRefPubMed
29.
30.
go back to reference Liu C et al (2002) Control of β-catenin phosphorylation/degradation by a dual-kinase mechanism. Cell 108(6):837–847CrossRefPubMed Liu C et al (2002) Control of β-catenin phosphorylation/degradation by a dual-kinase mechanism. Cell 108(6):837–847CrossRefPubMed
31.
go back to reference Price MA (2006) CKI, there’s more than one: casein kinase I family members in Wnt and Hedgehog signaling. Genes Dev 20(4):399–410CrossRefPubMed Price MA (2006) CKI, there’s more than one: casein kinase I family members in Wnt and Hedgehog signaling. Genes Dev 20(4):399–410CrossRefPubMed
32.
go back to reference Ozawa M, Baribault H, Kemler R (1989) The cytoplasmic domain of the cell adhesion molecule uvomorulin associates with three independent proteins structurally related in different species. EMBO J 8(6):1711PubMedPubMedCentral Ozawa M, Baribault H, Kemler R (1989) The cytoplasmic domain of the cell adhesion molecule uvomorulin associates with three independent proteins structurally related in different species. EMBO J 8(6):1711PubMedPubMedCentral
33.
go back to reference Pez F et al (2013) Wnt signaling and hepatocarcinogenesis: molecular targets for the development of innovative anticancer drugs. J Hepatol 59(5):1107–1117CrossRefPubMed Pez F et al (2013) Wnt signaling and hepatocarcinogenesis: molecular targets for the development of innovative anticancer drugs. J Hepatol 59(5):1107–1117CrossRefPubMed
34.
go back to reference Laurent-Puig P, Zucman-Rossi J (2006) Genetics of hepatocellular tumors. Oncogene 25(27):3778–3786CrossRefPubMed Laurent-Puig P, Zucman-Rossi J (2006) Genetics of hepatocellular tumors. Oncogene 25(27):3778–3786CrossRefPubMed
36.
go back to reference Levrero M, Zucman-Rossi J (2016) Mechanisms of HBV-induced hepatocellular carcinoma. J Hepatol 64(1):S84–S101CrossRefPubMed Levrero M, Zucman-Rossi J (2016) Mechanisms of HBV-induced hepatocellular carcinoma. J Hepatol 64(1):S84–S101CrossRefPubMed
37.
go back to reference Huang H et al (1999) β-catenin mutations are frequent in human hepatocellular carcinomas associated with hepatitis C virus infection. Am J Pathol 155(6):1795–1801CrossRefPubMedPubMedCentral Huang H et al (1999) β-catenin mutations are frequent in human hepatocellular carcinomas associated with hepatitis C virus infection. Am J Pathol 155(6):1795–1801CrossRefPubMedPubMedCentral
38.
go back to reference Hsu H-C et al (2000) β-catenin mutations are associated with a subset of low-stage hepatocellular carcinoma negative for hepatitis B virus and with favorable prognosis. Am J Pathol 157(3):763–770CrossRefPubMedPubMedCentral Hsu H-C et al (2000) β-catenin mutations are associated with a subset of low-stage hepatocellular carcinoma negative for hepatitis B virus and with favorable prognosis. Am J Pathol 157(3):763–770CrossRefPubMedPubMedCentral
39.
go back to reference Wong CM, Fan ST, Ng IO (2001) β-catenin mutation and overexpression in hepatocellular carcinoma. Cancer 92(1):136–145CrossRefPubMed Wong CM, Fan ST, Ng IO (2001) β-catenin mutation and overexpression in hepatocellular carcinoma. Cancer 92(1):136–145CrossRefPubMed
40.
go back to reference Zucman-Rossi J et al (2007) Differential effects of inactivated Axin1 and activated β-catenin mutations in human hepatocellular carcinomas. Oncogene 26(5):774–780CrossRefPubMed Zucman-Rossi J et al (2007) Differential effects of inactivated Axin1 and activated β-catenin mutations in human hepatocellular carcinomas. Oncogene 26(5):774–780CrossRefPubMed
42.
go back to reference Austinat M et al (2008) Correlation between beta-catenin mutations and expression of Wnt-signaling target genes in hepatocellular carcinoma. Mol Cancer 7(1):21CrossRefPubMedPubMedCentral Austinat M et al (2008) Correlation between beta-catenin mutations and expression of Wnt-signaling target genes in hepatocellular carcinoma. Mol Cancer 7(1):21CrossRefPubMedPubMedCentral
43.
go back to reference Tornesello ML et al (2013) Mutations in TP53, CTNNB1 and PIK3CA genes in hepatocellular carcinoma associated with hepatitis B and hepatitis C virus infections. Genomics 102(2):74–83CrossRefPubMed Tornesello ML et al (2013) Mutations in TP53, CTNNB1 and PIK3CA genes in hepatocellular carcinoma associated with hepatitis B and hepatitis C virus infections. Genomics 102(2):74–83CrossRefPubMed
44.
45.
go back to reference Yost C et al (1996) The axis-inducing activity, stability, and subcellular distribution of beta-catenin is regulated in Xenopus embryos by glycogen synthase kinase 3. Genes Dev 10(12):1443–1454CrossRefPubMed Yost C et al (1996) The axis-inducing activity, stability, and subcellular distribution of beta-catenin is regulated in Xenopus embryos by glycogen synthase kinase 3. Genes Dev 10(12):1443–1454CrossRefPubMed
46.
go back to reference Park JY et al (2005) Mutations of β-catenin and AXIN I genes are a late event in human hepatocellular carcinogenesis. Liver Int 25(1):70–76CrossRefPubMed Park JY et al (2005) Mutations of β-catenin and AXIN I genes are a late event in human hepatocellular carcinogenesis. Liver Int 25(1):70–76CrossRefPubMed
47.
go back to reference Jain S et al (2011) Methylation of the CpG sites only on the sense strand of the APC gene is specific for hepatocellular carcinoma. PLoS One 6(11):e26799CrossRefPubMedPubMedCentral Jain S et al (2011) Methylation of the CpG sites only on the sense strand of the APC gene is specific for hepatocellular carcinoma. PLoS One 6(11):e26799CrossRefPubMedPubMedCentral
48.
go back to reference Lee H-H et al (2009) Wnt-1 protein as a prognostic biomarker for hepatitis B-related and hepatitis C-related hepatocellular carcinoma after surgery. Cancer Epidemiol Biomark Prevent 18(5):1562–1569CrossRef Lee H-H et al (2009) Wnt-1 protein as a prognostic biomarker for hepatitis B-related and hepatitis C-related hepatocellular carcinoma after surgery. Cancer Epidemiol Biomark Prevent 18(5):1562–1569CrossRef
49.
go back to reference Cha MY et al (2004) Hepatitis B virus X protein is essential for the activation of Wnt/β-catenin signaling in hepatoma cells. Hepatology 39(6):1683–1693CrossRefPubMed Cha MY et al (2004) Hepatitis B virus X protein is essential for the activation of Wnt/β-catenin signaling in hepatoma cells. Hepatology 39(6):1683–1693CrossRefPubMed
50.
go back to reference Kim M et al (2008) Functional interaction between Wnt3 and Frizzled-7 leads to activation of the Wnt/β-catenin signaling pathway in hepatocellular carcinoma cells. J Hepatol 48(5):780–791CrossRefPubMedPubMedCentral Kim M et al (2008) Functional interaction between Wnt3 and Frizzled-7 leads to activation of the Wnt/β-catenin signaling pathway in hepatocellular carcinoma cells. J Hepatol 48(5):780–791CrossRefPubMedPubMedCentral
51.
go back to reference Lin X et al (2013) Differential expression of Wnt pathway genes in sporadic hepatocellular carcinomas infected with hepatitis B virus identified with OligoGE arrays. Hepatitis Mon 13(1):e6192 Lin X et al (2013) Differential expression of Wnt pathway genes in sporadic hepatocellular carcinomas infected with hepatitis B virus identified with OligoGE arrays. Hepatitis Mon 13(1):e6192
52.
go back to reference Tamori A et al (2005) Alteration of gene expression in human hepatocellular carcinoma with integrated hepatitis B virus DNA. Clin Cancer Res 11(16):5821–5826CrossRefPubMed Tamori A et al (2005) Alteration of gene expression in human hepatocellular carcinoma with integrated hepatitis B virus DNA. Clin Cancer Res 11(16):5821–5826CrossRefPubMed
53.
go back to reference Boyault S et al (2007) Transcriptome classification of HCC is related to gene alterations and to new therapeutic targets. Hepatology 45(1):42–52CrossRefPubMed Boyault S et al (2007) Transcriptome classification of HCC is related to gene alterations and to new therapeutic targets. Hepatology 45(1):42–52CrossRefPubMed
55.
go back to reference Lee J-O et al (2005) Hepatitis B virus X protein represses E-cadherin expression via activation of DNA methyltransferase 1. Oncogene 24(44):6617–6625CrossRefPubMed Lee J-O et al (2005) Hepatitis B virus X protein represses E-cadherin expression via activation of DNA methyltransferase 1. Oncogene 24(44):6617–6625CrossRefPubMed
57.
go back to reference Lara-Pezzi E et al (2001) The hepatitis B virus HBx protein induces adherens junction disruption in a src-dependent manner. Oncogene 20(26):3323–3331CrossRefPubMed Lara-Pezzi E et al (2001) The hepatitis B virus HBx protein induces adherens junction disruption in a src-dependent manner. Oncogene 20(26):3323–3331CrossRefPubMed
58.
go back to reference Xie Q et al (2014) Epigenetic silencing of SFRP1 and SFRP5 by hepatitis B virus X protein enhances hepatoma cell tumorigenicity through Wnt signaling pathway. Int J Cancer 135(3):635–646CrossRefPubMed Xie Q et al (2014) Epigenetic silencing of SFRP1 and SFRP5 by hepatitis B virus X protein enhances hepatoma cell tumorigenicity through Wnt signaling pathway. Int J Cancer 135(3):635–646CrossRefPubMed
59.
go back to reference Takagi H et al (2008) Frequent epigenetic inactivation of SFRP genes in hepatocellular carcinoma. J Gastroenterol 43(5):378–389CrossRefPubMed Takagi H et al (2008) Frequent epigenetic inactivation of SFRP genes in hepatocellular carcinoma. J Gastroenterol 43(5):378–389CrossRefPubMed
60.
go back to reference Hsieh A et al (2011) Hepatitis B viral X protein interacts with tumor suppressor adenomatous polyposis coli to activate Wnt/β-catenin signaling. Cancer Lett 300(2):162–172CrossRefPubMed Hsieh A et al (2011) Hepatitis B viral X protein interacts with tumor suppressor adenomatous polyposis coli to activate Wnt/β-catenin signaling. Cancer Lett 300(2):162–172CrossRefPubMed
61.
62.
go back to reference Kuo C-Y et al (2008) HBx inhibits the growth of CCL13-HBX-stable cells via the GSK-3/-catenin cascade. Intervirology 51(2):130–136CrossRefPubMed Kuo C-Y et al (2008) HBx inhibits the growth of CCL13-HBX-stable cells via the GSK-3/-catenin cascade. Intervirology 51(2):130–136CrossRefPubMed
63.
go back to reference Peifer M, Polakis P (2000) Wnt signaling in oncogenesis and embryogenesis—a look outside the nucleus. Science 287(5458):1606–1609CrossRefPubMed Peifer M, Polakis P (2000) Wnt signaling in oncogenesis and embryogenesis—a look outside the nucleus. Science 287(5458):1606–1609CrossRefPubMed
64.
go back to reference Wang Q et al (2012) A mutant of hepatitis B virus X protein (HBxΔ127) promotes cell growth through a positive feedback loop involving 5-lipoxygenase and fatty acid synthase. Neoplasia 12(2):103-IN3 Wang Q et al (2012) A mutant of hepatitis B virus X protein (HBxΔ127) promotes cell growth through a positive feedback loop involving 5-lipoxygenase and fatty acid synthase. Neoplasia 12(2):103-IN3
65.
go back to reference Jung JK et al (2007) Hepatitis B virus X protein differentially affects the ubiquitin-mediated proteasomal degradation of β-catenin depending on the status of cellular p53. J Gen Virol 88(8):2144–2154CrossRefPubMed Jung JK et al (2007) Hepatitis B virus X protein differentially affects the ubiquitin-mediated proteasomal degradation of β-catenin depending on the status of cellular p53. J Gen Virol 88(8):2144–2154CrossRefPubMed
66.
go back to reference Ostuni A et al (2013) The hepatitis B x antigen anti-apoptotic effector URG7 is localized to the endoplasmic reticulum membrane. FEBS Lett 587(18):3058–3062CrossRefPubMed Ostuni A et al (2013) The hepatitis B x antigen anti-apoptotic effector URG7 is localized to the endoplasmic reticulum membrane. FEBS Lett 587(18):3058–3062CrossRefPubMed
67.
go back to reference Lian Z et al (2006) Enhanced cell survival of Hep3B cells by the hepatitis B × antigen effector, URG11, is associated with upregulation of β-catenin. Hepatology 43(3):415–424CrossRefPubMed Lian Z et al (2006) Enhanced cell survival of Hep3B cells by the hepatitis B × antigen effector, URG11, is associated with upregulation of β-catenin. Hepatology 43(3):415–424CrossRefPubMed
68.
go back to reference Pan J et al (2007) The hepatitis B x antigen effector, URG7, blocks tumour necrosis factor α-mediated apoptosis by activation of phosphoinositol 3-kinase and β-catenin. J Gen Virol 88(12):3275–3285CrossRefPubMed Pan J et al (2007) The hepatitis B x antigen effector, URG7, blocks tumour necrosis factor α-mediated apoptosis by activation of phosphoinositol 3-kinase and β-catenin. J Gen Virol 88(12):3275–3285CrossRefPubMed
69.
go back to reference Sun Q et al (2014) Notch1 promotes hepatitis B virus X protein-induced hepatocarcinogenesis via Wnt/β-catenin pathway. Int J Oncol 45(4):1638–1648CrossRefPubMed Sun Q et al (2014) Notch1 promotes hepatitis B virus X protein-induced hepatocarcinogenesis via Wnt/β-catenin pathway. Int J Oncol 45(4):1638–1648CrossRefPubMed
71.
go back to reference Lee S et al (2016) Hepatitis B virus X protein enhances Myc stability by inhibiting SCFSkp2 ubiquitin E3 ligase-mediated Myc ubiquitination and contributes to oncogenesis. Oncogene 35(14):1857–1867CrossRefPubMed Lee S et al (2016) Hepatitis B virus X protein enhances Myc stability by inhibiting SCFSkp2 ubiquitin E3 ligase-mediated Myc ubiquitination and contributes to oncogenesis. Oncogene 35(14):1857–1867CrossRefPubMed
73.
go back to reference Tian X et al (2007) Gene-expression profiles of a hepatitis B small surface antigen-secreting cell line reveal upregulation of lymphoid enhancer-binding factor 1. J Gen Virol 88(11):2966–2976CrossRefPubMed Tian X et al (2007) Gene-expression profiles of a hepatitis B small surface antigen-secreting cell line reveal upregulation of lymphoid enhancer-binding factor 1. J Gen Virol 88(11):2966–2976CrossRefPubMed
74.
go back to reference Tian X et al (2009) Role of hepatitis B surface antigen in the development of hepatocellular carcinoma: regulation of lymphoid enhancer-binding factor 1. J Exp Clin Cancer Res 28(1):1CrossRef Tian X et al (2009) Role of hepatitis B surface antigen in the development of hepatocellular carcinoma: regulation of lymphoid enhancer-binding factor 1. J Exp Clin Cancer Res 28(1):1CrossRef
76.
go back to reference Sasai N et al (2004) The neurotrophin-receptor-related protein NRH1 is essential for convergent extension movements. Nat Cell Biol 6(8):741–748CrossRefPubMed Sasai N et al (2004) The neurotrophin-receptor-related protein NRH1 is essential for convergent extension movements. Nat Cell Biol 6(8):741–748CrossRefPubMed
77.
go back to reference Lu W et al (2004) Mammalian Ryk is a Wnt coreceptor required for stimulation of neurite outgrowth. Cell 119(1):97–108CrossRefPubMed Lu W et al (2004) Mammalian Ryk is a Wnt coreceptor required for stimulation of neurite outgrowth. Cell 119(1):97–108CrossRefPubMed
78.
go back to reference Lu X et al (2004) PTK7/CCK-4 is a novel regulator of planar cell polarity in vertebrates. Nature 430(6995):93–98CrossRefPubMed Lu X et al (2004) PTK7/CCK-4 is a novel regulator of planar cell polarity in vertebrates. Nature 430(6995):93–98CrossRefPubMed
79.
go back to reference Nishita M et al (2006) Filopodia formation mediated by receptor tyrosine kinase Ror2 is required for Wnt5a-induced cell migration. J Cell Biol 175(4):555–562CrossRefPubMedPubMedCentral Nishita M et al (2006) Filopodia formation mediated by receptor tyrosine kinase Ror2 is required for Wnt5a-induced cell migration. J Cell Biol 175(4):555–562CrossRefPubMedPubMedCentral
80.
go back to reference He X et al (2004) LDL receptor-related proteins 5 and 6 in Wnt/β-catenin signaling: arrows point the way. Development 131(8):1663–1677CrossRefPubMed He X et al (2004) LDL receptor-related proteins 5 and 6 in Wnt/β-catenin signaling: arrows point the way. Development 131(8):1663–1677CrossRefPubMed
81.
go back to reference Wallingford JB, Habas R (2005) The developmental biology of dishevelled: an enigmatic protein governing cell fate and cell polarity. Development 132(20):4421–4436CrossRefPubMed Wallingford JB, Habas R (2005) The developmental biology of dishevelled: an enigmatic protein governing cell fate and cell polarity. Development 132(20):4421–4436CrossRefPubMed
82.
83.
go back to reference Semenov M, He X (2003) Secreted antagonists/modulators of Wnt signaling. In: Kuhl M (ed) Wnt Signaling in Development, pp 16–25 Semenov M, He X (2003) Secreted antagonists/modulators of Wnt signaling. In: Kuhl M (ed) Wnt Signaling in Development, pp 16–25
84.
go back to reference Park E et al (2006) Role of PKA as a negative regulator of PCP signaling pathway during Xenopus gastrulation movements. Dev Biol 292(2):344–357CrossRefPubMed Park E et al (2006) Role of PKA as a negative regulator of PCP signaling pathway during Xenopus gastrulation movements. Dev Biol 292(2):344–357CrossRefPubMed
85.
go back to reference Herbst A et al (2014) Comprehensive analysis of β-catenin target genes in colorectal carcinoma cell lines with deregulated Wnt/β-catenin signaling. BMC Genom 15(1):74CrossRef Herbst A et al (2014) Comprehensive analysis of β-catenin target genes in colorectal carcinoma cell lines with deregulated Wnt/β-catenin signaling. BMC Genom 15(1):74CrossRef
Metadata
Title
Modulation of Wnt signaling pathway by hepatitis B virus
Authors
Muhammad Daud
Muhammad Adeel Rana
Tayyab Husnain
Bushra Ijaz
Publication date
01-10-2017
Publisher
Springer Vienna
Published in
Archives of Virology / Issue 10/2017
Print ISSN: 0304-8608
Electronic ISSN: 1432-8798
DOI
https://doi.org/10.1007/s00705-017-3462-6

Other articles of this Issue 10/2017

Archives of Virology 10/2017 Go to the issue