Sodium taurocholate cotransporting polypeptide is the limiting host factor of hepatitis B virus infection in macaque and pig hepatocytes

Hepatology

Volumn 66, Issue 3, 2017, Pages 703-716

  Lempp, Florian A ^a,b   Wiedtke, Ellen ^a   Qu, Bingqian ^a   Roques, Pierre ^c,d   Chemin, Isabelle ^e   Vondran, Florian W R ^f,g   Le Grand, Roger ^c,d   Grimm, Dirk ^a   Urban, Stephan ^a,b  

^a UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^b German Centre for Infection Research   (Germany)

^c INSTITUT DE RADIOPROTECTION ET DE SÛRETÉ NUCLÉAIRE   (France)

^d UNIVERSITÉ PARIS SACLAY   (France)

^e CENTRE DE RECHERCHE EN CANCÉROLOGIE DE LYON   (France)

^f HANNOVER MEDICAL SCHOOL   (Germany)

^g German Centre for Infection Research (DZIF) Partner Site Hannover Braunschweig   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENO ASSOCIATED VIRUS VECTOR; ANTIVIRUS AGENT; CIRCULAR DNA; MYRCLUDEX B; SODIUM BILE ACID COTRANSPORTER; TAUROCHOLIC ACID; UNCLASSIFIED DRUG; COTRANSPORTER; HOST FACTOR 1; ORGANIC ANION TRANSPORTER; SODIUM-BILE ACID COTRANSPORTER; VIRUS RECEPTOR;

ADENO ASSOCIATED VIRUS 8; ANIMAL CELL; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; DELTA AGENT HEPATITIS; DISEASE PREDISPOSITION; DOG; EXPERIMENTAL ANIMAL; GENE EXPRESSION; HEPATITIS B; HEPATITIS B VIRUS; HEPATITIS DELTA VIRUS; HEPATOCELLULAR CARCINOMA CELL LINE; HUMAN; HUMAN CELL; HUMAN TISSUE; LIVER CELL; MACACA FASCICULARIS; MOUSE; NONHUMAN; PIG; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; RAT; RHESUS MONKEY; TRANSGENE; VIRUS REPLICATION; ANIMAL; C57BL MOUSE; CELL CULTURE; COMPARATIVE STUDY; DISEASE MODEL; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; METABOLISM; PATHOPHYSIOLOGY; RANDOMIZATION; SIGNAL TRANSDUCTION; SPECIES DIFFERENCE; VIROLOGY; WISTAR RAT;

ANIMALS; CELLS, CULTURED; DISEASE MODELS, ANIMAL; DOGS; GENE EXPRESSION REGULATION, VIRAL; HEPATITIS B; HEPATITIS B VIRUS; HEPATOCYTES; HOST FACTOR 1 PROTEIN; MACACA MULATTA; MICE; MICE, INBRED C57BL; ORGANIC ANION TRANSPORTERS, SODIUM-DEPENDENT; RANDOM ALLOCATION; RATS; RATS, WISTAR; RECEPTORS, VIRUS; SIGNAL TRANSDUCTION; SPECIES SPECIFICITY; SWINE; SYMPORTERS; TAUROCHOLIC ACID; TRANSFECTION; VIRUS REPLICATION;

EID: 85022323650     PISSN: 02709139     EISSN: 15273350     Source Type: Journal    
DOI: 10.1002/hep.29112     Document Type: Article

References (40)

1. Trepo C, Chan HL, Lok A. Hepatitis B virus infection. Lancet 2014;384:2053-2063.
2. Littlejohn M, Locarnini S, Yuen L. Origins and evolution of hepatitis B virus and hepatitis D virus. Cold Spring Harb Perspect Med 2016;6:a021360.
3. Lempp FA, Ni Y, Urban S. Hepatitis delta virus: insights into a peculiar pathogen and novel treatment options. Nat Rev Gastroenterol Hepatol 2016;13:580-589.
4. Liang TJ, Block TM, McMahon BJ, Ghany MG, Urban S, Guo JT, et al. Present and future therapies of hepatitis B: From discovery to cure. Hepatology 2015;62:1893-1908.
5. Ni Y, Lempp FA, Mehrle S, Nkongolo S, Kaufman C, Falth M, et al. Hepatitis B and D viruses exploit sodium taurocholate co-transporting polypeptide for species-specific entry into hepatocytes. Gastroenterology 2014;146:1070-1083.
6. Yan H, Zhong G, Xu G, He W, Jing Z, Gao Z, et al. Sodium taurocholate cotransporting polypeptide is a functional receptor for human hepatitis B and D virus. Elife 2012;1:e00049.
7. Mason WS. Animal models and the molecular biology of hepadnavirus infection. Cold Spring Harb Perspect Med 2015;5.
8. Winer BY, Ding Q, Gaska J, Ploss A. In vivo models of hepatitis B and C virus infection. FEBS Lett 2016;590:1987-1999.
9. Guidotti LG, Rochford R, Chung J, Shapiro M, Purcell R, Chisari FV. Viral clearance without destruction of infected cells during acute HBV infection. Science 1999;284:825-829.
10. Collins FS. NIH will no longer support biomedical research on chimpanzees. https://www.nih.gov/about-nih/who-we-are/nih-director/statements/nih-will-no-longer-support-biomedical-research-chimpanzees. Published November 17, 2015. Accessed on 29th November 2016.
11. He W, Ren B, Mao F, Jing Z, Li Y, Liu Y, et al. Hepatitis D virus infection of mice expressing human sodium taurocholate co-transporting polypeptide. PLoS Pathog 2015;11:e1004840.
12. He W, Cao Z, Mao F, Ren B, Li Y, Li D, et al. Modification of three amino acids in sodium taurocholate cotransporting polypeptide renders mice susceptible to infection with hepatitis D virus in vivo. J Virol 2016;90:8866-8874.
13. Guidotti LG, Matzke B, Schaller H, Chisari FV. High-level hepatitis B virus replication in transgenic mice. J Virol 1995;69:6158-6169.
14. Bogomolov P, Alexandrov A, Voronkova N, Macievich M, Kokina K, Petrachenkova M, et al. Treatment of chronic hepatitis D with the entry inhibitor myrcludex B: first results of a phase Ib/IIa study. J Hepatol 2016;65:490-498.
15. Meier A, Mehrle S, Weiss TS, Mier W, Urban S. Myristoylated PreS1-domain of the hepatitis B virus L-protein mediates specific binding to differentiated hepatocytes. Hepatology 2013;58:31-42.
16. Schieck A, Schulze A, Gahler C, Muller T, Haberkorn U, Alexandrov A, et al. Hepatitis B virus hepatotropism is mediated by specific receptor recognition in the liver and not restricted to susceptible hosts. Hepatology 2013;58:43-53.
17. Yan H, Peng B, He W, Zhong G, Qi Y, Ren B, et al. Molecular determinants of hepatitis B and D virus entry restriction in mouse sodium taurocholate cotransporting polypeptide. J Virol 2013;87:7977-7991.
18. Lempp FA, Mutz P, Lipps C, Wirth D, Bartenschlager R, Urban S. Evidence that hepatitis B virus replication in mouse cells is limited by the lack of a host cell dependency factor. J Hepatol 2016;64:556-564.
19. Vondran FW, Katenz E, Schwartlander R, Morgul MH, Raschzok N, Gong X, et al. Isolation of primary human hepatocytes after partial hepatectomy: criteria for identification of the most promising liver specimen. Artif Organs 2008;32:205-213.
20. Lucifora J, Vincent IE, Berthillon P, Dupinay T, Michelet M, Protzer U, et al. Hepatitis B virus replication in primary macaque hepatocytes: crossing the species barrier toward a new small primate model. Hepatology 2010;51:1954-1960.
21. Cattaneo R, Will H, Darai G, Pfaff E, Schaller H. Detection of an element of the SV40 late promoter in vectors used for expression studies in COS cells. EMBO J 1983;2:511-514.
22. Nkongolo S, Ni Y, Lempp FA, Kaufman C, Lindner T, Esser-Nobis K, et al. Cyclosporin A inhibits hepatitis B and hepatitis D virus entry by cyclophilin-independent interference with the NTCP receptor. J Hepatol 2014;60:723-731.
23. Schulze A, Mills K, Weiss TS, Urban S. Hepatocyte polarization is essential for the productive entry of the hepatitis B virus. Hepatology 2012;55:373-383.
24. Xia Y, Carpentier A, Cheng X, Block PD, Zhao Y, Zhang Z, et al. Human stem cell-derived hepatocytes as a model for hepatitis B virus infection, spreading and virus-host interactions. J Hepatol 2017;66:494-503.
25. Wang J, Shen T, Huang X, Kumar GR, Chen X, Zeng Z, et al. Serum hepatitis B virus RNA is encapsidated pregenome RNA that may be associated with persistence of viral infection and rebound. J Hepatol 2016;65:700-710.
26. Lempp FA, Qu B, Wang YX, Urban S. Hepatitis B virus infection of a mouse hepatic cell line reconstituted with human sodium taurocholate cotransporting polypeptide. J Virol 2016;90:4827-4831.
27. Walter E, Keist R, Niederost B, Pult I, Blum HE. Hepatitis B virus infection of tupaia hepatocytes in vitro and in vivo. Hepatology 1996;24:1-5.
28. Li H, Zhuang Q, Wang Y, Zhang T, Zhao J, Zhang Y, et al. HBV life cycle is restricted in mouse hepatocytes expressing human NTCP. Cell Mol Immunol 2014;11:175-183.
29. Cui X, Guo JT, Hu J. Hepatitis B virus covalently closed circular DNA formation in immortalized mouse hepatocytes associated with nucleocapsid destabilization. J Virol 2015;89:9021-9028.
30. Giersch K, Helbig M, Volz T, Allweiss L, Mancke LV, Lohse AW, et al. Persistent hepatitis D virus mono-infection in humanized mice is efficiently converted by hepatitis B virus to a productive co-infection. J Hepatol 2014;60:538-544.
31. Barker LF, Chisari FV, McGrath PP, Dalgard DW, Kirschstein RL, Almeida JD, et al. Transmission of type B viral hepatitis to chimpanzees. J Infect Dis 1973;127:648-662.
32. Maynard JE, Berquist KR, Krushak DH, Purcell RH. Experimental infection of chimpanzees with the virus of hepatitis B. Nature 1972;237:514-515.
33. Dupinay T, Gheit T, Roques P, Cova L, Chevallier-Queyron P, Tasahsu SI, et al. Discovery of naturally occurring transmissible chronic hepatitis B virus infection among Macaca fascicularis from Mauritius Island. Hepatology 2013;58:1610-1620.
34. Bell P, Wang L, Gao G, Haskins ME, Tarantal AF, McCarter RJ, et al. Inverse zonation of hepatocyte transduction with AAV vectors between mice and non-human primates. Mol Genet Metab 2011;104:395-403.
35. Nathwani AC, Rosales C, McIntosh J, Rastegarlari G, Nathwani D, Raj D, et al. Long-term safety and efficacy following systemic administration of a self-complementary AAV vector encoding human FIX pseudotyped with serotype 5 and 8 capsid proteins. Mol Ther 2011;19:876-885.
36. Fontanellas A, Hervas-Stubbs S, Mauleon I, Dubrot J, Mancheno U, Collantes M, et al. Intensive pharmacological immunosuppression allows for repetitive liver gene transfer with recombinant adenovirus in nonhuman primates. Mol Ther 2010;18:754-765.
37. Asabe S, Wieland SF, Chattopadhyay PK, Roederer M, Engle RE, Purcell RH, et al. The size of the viral inoculum contributes to the outcome of hepatitis B virus infection. J Virol 2009;83:9652-9662.
38. Li W, She R, Liu L, You H, Yin J. Prevalence of a virus similar to human hepatitis B virus in swine. Virol J 2010;7:60.
39. Vieira YR, Silva MF, Santos DR, Vieira AA, Ciacci-Zanella JR, Barquero G, et al. Serological and molecular evidence of hepadnavirus infection in swine. Ann Agric Environ Med 2015;22:11-16.
40. Schlosser J, Eiden M, Vina-Rodriguez A, Fast C, Dremsek P, Lange E, et al. Natural and experimental hepatitis E virus genotype 3-infection in European wild boar is transmissible to domestic pigs. Vet Res 2014;45:121.