The first transmembrane domain of the hepatitis B virus large envelope protein is crucial for infectivity

Journal of Virology

Volumn 83, Issue 22, 2009, Pages 11819-11829

  Lepère Douard, Charlotte ^a,b   Trotard, Maud ^a,b   Le Seyec, Jacques ^a,b   Gripon, Philippe ^a,b  

^a INSERM   (France)

^b UNIVERSITÉ DE RENNES 1   (France)

Author keywords

[No Author keywords available]

Indexed keywords

DIHYDROLIPOAMIDE DEHYDROGENASE; ENVELOPE PROTEIN; M PROTEIN; MEMBRANE PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CELL SURFACE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; GENE FUSION; HEPATITIS B VIRUS; HUMAN; HUMAN CELL; MUTAGENESIS; MUTATIONAL ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; VIRUS INFECTION; VIRUS INFECTIVITY; VIRUS NUCLEOCAPSID;

CELL LINE, TUMOR; HEPATITIS B; HEPATITIS B E ANTIGENS; HEPATITIS B SURFACE ANTIGENS; HEPATITIS B VIRUS; HUMANS; MUTAGENESIS, SITE-DIRECTED; VIRAL ENVELOPE PROTEINS;

HEPATITIS B VIRUS;

EID: 70350333409     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01026-09     Document Type: Article

References (56)

1. Abou-Jaoude, G., and C. Sureau. 2007. Entry of hepatitis delta virus requires the conserved cysteine residues of the hepatitis B virus envelope protein antigenic loop and is blocked by inhibitors of thiol-disulfide exchange. J. Virol. 81:13057-13066. (Pubitemid 350156944)
2. Berting, A., C. Fischer, S. Schaefer, W. Garten, H. D. Klenk, and W. H. Gerlich. 2000. Hemifusion activity of a chimeric influenza virus hemagglutinin with a putative fusion peptide from hepatitis B virus. Virus Res. 68: 35-49. (Pubitemid 30621409)
3. Blanchet, M., and C. Sureau. 2006. Analysis of the cytosolic domains of the hepatitis B virus envelope proteins for their function in viral particle assembly and infectivity. J. Virol. 80:11935-11945. (Pubitemid 44904343)
4. Blanchet, M., and C. Sureau. 2007. Infectivity determinants of the hepatitis B virus pre-S domain are confined to the N-terminal 75 amino acid residues. J. Virol. 81:5841-5849. (Pubitemid 46847021)
5. Bruss, V. 1997. A short linear sequence in the pre-S domain of the large hepatitis B virus envelope protein required for virion formation. J. Virol. 71:9350-9357. (Pubitemid 27492377)
6. Bruss, V. 2007. Hepatitis B virus morphogenesis. World J. Gastroenterol. 13:65-73.
7. Bruss, V., and D. Ganem. 1991. Mutational analysis of hepatitis B surface antigen particle assembly and secretion. J. Virol. 65:3813-3820.
8. Bruss, V., and D. Ganem. 1991. The role of envelope proteins in hepatitis B virus assembly. Proc. Natl. Acad. Sci. USA 88:1059-1063.
9. Bruss, V., J. Hagelsten, E. Gerhardt, and P. R. Galle. 1996. Myristylation of the large surface protein is required for hepatitis B virus in vitro infectivity. Virology 218:396-399. (Pubitemid 26164741)
10. Bruss, V., and R. Thomssen. 1994. Mapping a region of the large envelope protein required for hepatitis B virion maturation. J. Virol. 68:1643-1650. (Pubitemid 24065730)
11. Bruss, V., and K. Vieluf. 1995. Functions of the internal pre-S domain of the large surface protein in hepatitis B virus particle morphogenesis. J. Virol. 69:6652-6657.
12. Chen, R. W., H. Piiparinen, M. Seppanen, P. Koskela, S. Sarna, and M. Lappalainen. 2001. Real-time PCR for detection and quantitation of hepatitis B virus DNA. J. Med. Virol. 65:250-256.
13. Chojnacki, J., D. A. Anderson, and E. V. Grgacic. 2005. A hydrophobic domain in the large envelope protein is essential for fusion of duck hepatitis B virus at the late endosome. J. Virol. 79:14945-14955. (Pubitemid 41636291)
14. Chouteau, P., J. Le Seyec, I. Cannie, M. Nassal, C. Guguen-Guillouzo, and P. Gripon. 2001. A short N-proximal region in the large envelope protein harbors a determinant that contributes to the species specificity of human hepatitis B virus. J. Virol. 75:11565-11572. (Pubitemid 33063248)
15. Dubois, M. F., C. Pourcel, S. Rousset, C. Chany, and P. Tiollais. 1980. Excretion of hepatitis B surface antigen particles from mouse cells transformed with cloned viral DNA. Proc. Natl. Acad. Sci. USA 77:4549-4553.
16. Eble, B. E., V. R. Lingappa, and D. Ganem. 1986. Hepatitis B surface antigen: an unusual secreted protein initially synthesized as a transmembrane polypeptide. Mol. Cell. Biol. 6:1454-1463.
17. Eble, B. E., V. R. Lingappa, and D. Ganem. 1990. The N-terminal (pre-S2) domain of a hepatitis B virus surface glycoprotein is translocated across membranes by downstream signal sequences. J. Virol. 64:1414-1419.
18. Eble, B. E., D. R. MacRae, V. R. Lingappa, and D. Ganem. 1987. Multiple topogenic sequences determine the transmembrane orientation of the hepatitis B surface antigen. Mol. Cell. Biol. 7:3591-3601.
19. Engelke, M., K. Mills, S. Seitz, P. Simon, P. Gripon, M. Schnolzer, and S. Urban. 2006. Characterization of a hepatitis B and hepatitis delta virus receptor binding site. Hepatology 43:750-760.
20. Fernholz, D., P. R. Galle, M. Stemler, M. Brunetto, F. Bonino, and H. Will. 1993. Infectious hepatitis-B virus variant defective in pre-S2 protein expression in a chronic carrier. Virology 194:137-148. (Pubitemid 23211746)
21. Fernholz, D., M. Stemler, M. Brunetto, F. Bonino, and H. Will. 1991. Replicating and virion secreting hepatitis B mutant virus unable to produce preS2 protein. J. Hepatol. 13(Suppl. 4):S102-S104.
22. Glebe, D., M. Aliakbari, P. Krass, E. V. Knoop, K. P. Valerius, and W. H. Gerlich. 2003. Pre-s1 antigen-dependent infection of Tupaia hepatocyte cultures with human hepatitis B virus. J. Virol. 77:9511-9521.
23. Glebe, D., and S. Urban. 2007. Viral and cellular determinants involved in hepadnaviral entry. World J. Gastroenterol. 13:22-38.
24. Grgacic, E. V., and H. Schaller. 2000. A metastable form of the large envelope protein of duck hepatitis B virus: low-pH release results in a transition to a hydrophobic, potentially fusogenic conformation. J. Virol. 74:5116-5122.
25. Gripon, P., I. Cannie, and S. Urban. 2005. Efficient inhibition of hepatitis B virus infection by acylated peptides derived from the large viral surface protein. J. Virol. 79:1613-1622. (Pubitemid 40459108)
26. Gripon, P., C. Diot, and C. Guguen-Guillouzo. 1993. Reproducible high level infection of cultured adult human hepatocytes by hepatitis-B virus: effect of polyethylene glycol on adsorption and penetration. Virology 192:534-540. (Pubitemid 23232026)
27. Gripon, P., J. Le Seyec, S. Rumin, and C. Guguen-Guillouzo. 1995. Myristylation of the hepatitis B virus large surface protein is essential for viral infectivity. Virology 213:292-299.
28. Gripon, P., S. Rumin, S. Urban, J. Le Seyec, D. Glaise, I. Cannie, C. Guyomard, J. Lucas, C. Trepo, and C. Guguen-Guillouzo. 2002. Infection of a human hepatoma cell line by hepatitis B virus. Proc. Natl. Acad. Sci. USA 99:15655-15660.
29. Guarnieri, M., K. H. Kim, G. Bang, J. Li, Y. Zhou, X. Tang, J. Wands, and S. Tong. 2006. Point mutations upstream of hepatitis B virus core gene affect DNA replication at the step of core protein expression. J. Virol. 80:587-595. (Pubitemid 43062871)
30. Huovila, A. P., A. M. Eder, and S. D. Fuller. 1992. Hepatitis B surface antigen assembles in a post-ER, pre-Golgi compartment. J. Cell Biol. 118: 1305-1320.
31. Jaoude, G. A., and C. Sureau. 2005. Role of the antigenic loop of the hepatitis B virus envelope proteins in infectivity of hepatitis delta virus. J. Virol. 79:10460-10466.
32. Kuroki, K., R. Russnak, and D. Ganem. 1989. Novel N-terminal amino acid sequence required for retention of a hepatitis B virus glycoprotein in the endoplasmic reticulum. Mol. Cell. Biol. 9:4459-4466.
33. Lambert, C., and R. Prange. 2001. Dual topology of the hepatitis B virus large envelope protein: determinants influencing post-translational pre-S translocation. J. Biol. Chem. 276:22265-22272.
34. Leemans, W. F., H. L. Janssen, and R. A. de Man. 2007. Future prospectives for the management of chronic hepatitis B. World J. Gastroenterol. 13:2554-2567.
35. Lepere, C., M. Regeard, J. Le Seyec, and P. Gripon. 2007. The translocation motif of hepatitis B virus envelope proteins is dispensable for infectivity. J. Virol. 81:7816-7818. (Pubitemid 47047869)
36. Le Seyec, J., P. Chouteau, I. Cannie, C. Guguen-Guillouzo, and P. Gripon. 1999. Infection process of the hepatitis B virus depends on the presence of a defined sequence in the pre-S1 domain. J. Virol. 73:2052-2057. (Pubitemid 29098108)
37. Le Seyec, J., P. Chouteau, I. Cannie, C. Guguen-Guillouzo, and P. Gripon. 1998. Role of the pre-S2 domain of the large envelope protein in hepatitis B virus assembly and infectivity. J. Virol. 72:5573-5578. (Pubitemid 28283341)
38. Liu, J., and B. Rost. 2003. NORSp: predictions of long regions without regular secondary structure. Nucleic Acids Res. 31:3833-3835. (Pubitemid 37442259)
39. Lu, X., T. M. Block, and W. H. Gerlich. 1996. Protease-induced infectivity of hepatitis B virus for a human hepatoblastoma cell line. J. Virol. 70:2277-2285. (Pubitemid 26087590)
40. Nassal, M. 1996. Hepatitis B virus morphogenesis. Curr. Top. Microbiol. Immunol. 214:297-337.
41. Ou, J. H., and W. J. Rutter. 1987. Regulation of secretion of the hepatitis B virus major surface antigen by the preS-1 protein. J. Virol. 61:782-786. (Pubitemid 17040206)
42. Patient, R., C. Hourioux, P. Y. Sizaret, S. Trassard, C. Sureau, and P. Roingeard. 2007. Hepatitis B virus subviral envelope particle morphogenesis and intracellular trafficking. J. Virol. 81:3842-3851. (Pubitemid 46586881)
43. Patzer, E. J., G. R. Nakamura, C. C. Simonsen, A. D. Levinson, and R. Brands. 1986. Intracellular assembly and packaging of hepatitis B surface antigen particles occur in the endoplasmic reticulum. J. Virol. 58:884-892.
44. Persing, D. H., H. E. Varmus, and D. Ganem. 1986. Inhibition of secretion of hepatitis B surface antigen by a related presurface polypeptide. Science 234:1388-1391. (Pubitemid 17210217)
45. Petersen, J., M. Dandri, W. Mier, M. Lutgehetmann, T. Volz, F. von Weizsacker, U. Haberkorn, L. Fischer, J. M. Pollok, B. Erbes, S. Seitz, and S. Urban. 2008. Prevention of hepatitis B virus infection in vivo by entry inhibitors derived from the large envelope protein. Nat. Biotechnol. 26:335-341.
46. Poisson, F., A. Severac, C. Hourioux, A. Goudeau, and P. Roingeard. 1997. Both pre-S1 and S domains of hepatitis B virus envelope proteins interact with the core particle. Virology 228:115-120. (Pubitemid 27238827)
47. Prange, R., R. Nagel, and R. E. Streeck. 1992. Deletions in the hepatitis B virus small envelope protein: effect on assembly and secretion of surface antigen particles. J. Virol. 66:5832-5841.
48. Prange, R., and R. E. Streeck. 1995. Novel transmembrane topology of the hepatitis B virus envelope proteins. EMBO J. 14:247-256.
49. Rodriguez-Crespo, I., J. Gomez-Gutierrez, J. A. Encinar, J. M. Gonzalez- Ros, J. P. Albar, D. L. Peterson, and F. Gavilanes. 1996. Structural properties of the putative fusion peptide of hepatitis B virus upon interaction with phospholipids. Circular dichroism and Fourier-transform infrared spectroscopy studies. Eur. J. Biochem. 242:243-248.
50. Rodriguez-Crespo, I., J. Gomez-Gutierrez, M. Nieto, D. L. Peterson, and F. Gavilanes. 1994. Prediction of a putative fusion peptide in the S protein of hepatitis B virus. J. Gen. Virol. 75:637-639.
51. Rodriguez-Crespo, I., E. Nunez, J. Gomez-Gutierrez, B. Yelamos, J. P. Albar, D. L. Peterson, and F. Gavilanes. 1995. Phospholipid interactions of the putative fusion peptide of hepatitis B virus surface antigen S protein. J. Gen. Virol. 76:301-308.
52. Rost, B., P. Fariselli, and R. Casadio. 1996. Topology prediction for helical transmembrane proteins at 86% accuracy. Protein Sci. 5:1704-1718. (Pubitemid 26257233)
53. Salisse, J., and C. Sureau. 2009. A function essential to viral entry underlies the hepatitis B virus "a" determinant. J. Virol. 83:9321-9328.
54. Schulze, A., P. Gripon, and S. Urban. 2007. Hepatitis B virus infection initiates with a large surface protein-dependent binding to heparan sulfate proteoglycans. Hepatology 46:1759-1768.
55. Tillmann, H. L. 2007. Antiviral therapy and resistance with hepatitis B virus infection. World J. Gastroenterol. 13:125-140.
56. World Health Organization. 2002. Hepatitis B. Department of Communicable Diseases Surveillance and Response, World Health Organization, Geneva, Switzerland. http://www.who.int/csr/disease/hepatitis/HepatitisB -whocdscsrlyo2002-2.pdf.