A Novel Monoclonal Anti-CD81 Antibody Produced by Genetic Immunization Efficiently Inhibits Hepatitis C Virus Cell-Cell Transmission

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Fofana, Isabel ^a,b   Xiao, Fei ^a,b   Thumann, Christine ^a,b   Turek, Marine ^a,b   Zona, Laetitia ^a,b   Tawar, Rajiv G ^a,b   Grunert, Fritz ^c   Thompson, John ^c   Zeisel, Mirjam B ^a,b   Baumert, Thomas F ^a,b,d  

^a INSERM   (France)

^b UNIVERSITÉ DE STRASBOURG   (France)

^c Aldevron GmbH   (Germany)

^d UNIVERSITY HOSPITAL OF STRASBOURG   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CD81 ANTIGEN; COMPLEMENTARY DNA; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY JS81; MONOCLONAL ANTIBODY QV 6A8 F2 C4; NEUTRALIZING ANTIBODY; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIVIRAL ACTIVITY; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG PROTEIN BINDING; DRUG TARGETING; FEMALE; GENETIC IMMUNIZATION; GENOTYPE; HEPATITIS C; HUMAN; HUMAN CELL; IC 50; INFECTION PREVENTION; NONHUMAN; TOXICITY TESTING; VIRUS CELL INTERACTION; VIRUS ENTRY; VIRUS ENVELOPE; VIRUS TRANSMISSION;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODIES, NEUTRALIZING; ANTIGENS, CD81; CELL MEMBRANE; HEPACIVIRUS; HEPATITIS C; HEPATITIS C ANTIBODIES; HUMANS; IMMUNIZATION; RATS; RATS, WISTAR; VIRAL ENVELOPE PROTEINS; VIRUS INTERNALIZATION;

EID: 84877957589     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0064221     Document Type: Article

References (53)

1. Sarrazin C, Zeuzem S, (2010) Resistance to direct antiviral agents in patients with hepatitis C virus infection. Gastroenterology 138: 447-462.
2. Brown RS, (2005) Hepatitis C and liver transplantation. Nature 436: 973-978.
3. Watt K, Veldt B, Charlton M, (2009) A practical guide to the management of HCV infection following liver transplantation. Am J Transplant 9: 1707-1713.
4. Crespo G, Marino Z, Navasa M, Forns X, (2012) Viral hepatitis in liver transplantation. Gastroenterology 142: 1373-1383 e1371.
5. Charlton M, (2011) Telaprevir, boceprevir, cytochrome P450 and immunosuppressive agents-a potentially lethal cocktail. Hepatology 54: 3-5.
6. Zeisel MB, Fofana I, Fafi-Kremer S, Baumert TF, (2011) Hepatitis C virus entry into hepatocytes: molecular mechanisms and targets for antiviral therapies. J Hepatol 54: 566-576.
7. Zeisel MB, Lupberger J, Fofana I, Baumert TF, (2013) Host-targeting agents for prevention and treatment of chronic hepatitis C- perspectives and challenges. J Hepatol 58: 375-384.
8. Fafi-Kremer S, Fofana I, Soulier E, Carolla P, Meuleman P, et al. (2010) Enhanced viral entry and escape from antibody-mediated neutralization are key determinants for hepatitis C virus re-infection in liver transplantation. J Exp Med 207: 2019-2031.
9. Fofana I, Krieger SE, Grunert F, Glauben S, Xiao F, et al. (2010) Monoclonal anti-claudin 1 antibodies for prevention of hepatitis C virus infection. Gastroenterology 139: 953-954, 953-964, 964.e951-954.
10. Timpe JM, Stamataki Z, Jennings A, Hu K, Farquhar MJ, et al. (2008) Hepatitis C virus cell-cell transmission in hepatoma cells in the presence of neutralizing antibodies. Hepatology 47: 17-24.
11. Pileri P, Uematsu Y, Campagnoli S, Galli G, Falugi F, et al. (1998) Binding of hepatitis C virus to CD81. Science 282: 938-941.
12. Lindenbach BD, Evans MJ, Syder AJ, Wolk B, Tellinghuisen TL, et al. (2005) Complete replication of hepatitis C virus in cell culture. Science 309: 623-626.
13. Flint M, von Hahn T, Zhang J, Farquhar M, Jones CT, et al. (2006) Diverse CD81 proteins support hepatitis C virus infection. J Virol 80: 11331-11342.
14. Bartosch B, Vitelli A, Granier C, Goujon C, Dubuisson J, et al. (2003) Cell entry of hepatitis C virus requires a set of co-receptors that include the CD81 tetraspanin and the SR-B1 scavenger receptor. J Biol Chem 278: 41624-41630.
15. Zhang J, Randall G, Higginbottom A, Monk P, Rice CM, et al. (2004) CD81 is required for hepatitis C virus glycoprotein-mediated viral infection. J Virol 78: 1448-1455.
16. Koutsoudakis G, Herrmann E, Kallis S, Bartenschlager R, Pietschmann T, (2007) The level of CD81 cell surface expression is a key determinant for productive entry of Hepatitis C Virus into host cells. J Virol 81: 588-598.
17. Akazawa D, Date T, Morikawa K, Murayama A, Miyamoto M, et al. (2007) CD81 expression is important for heterogeneous HCV permissiveness of Huh7 cell clones. J Virol 81: 5036-5045.
18. Koutsoudakis G, Kaul A, Steinmann E, Kallis S, Lohmann V, et al. (2006) Characterization of the early steps of hepatitis C virus infection by using luciferase reporter viruses. J Virol 80: 5308-5320.
19. Evans MJ, von Hahn T, Tscherne DM, Syder AJ, Panis M, et al. (2007) Claudin-1 is a hepatitis C virus co-receptor required for a late step in entry. Nature 446: 801-805.
20. Farquhar MJ, Hu K, Harris HJ, Davis C, Brimacombe CL, et al. (2012) Hepatitis C virus induces CD81 and claudin-1 endocytosis. J Virol 86: 4305-4316.
21. Harris HJ, Farquhar MJ, Mee CJ, Davis C, Reynolds GM, et al. (2008) CD81 and claudin 1 coreceptor association: role in hepatitis C virus entry. J Virol 82: 5007-5020.
22. Harris HJ, Davis C, Mullins JG, Hu K, Goodall M, et al. (2010) Claudin association with CD81 defines hepatitis C virus entry. J Biol Chem 285: 21092-21102.
23. Farquhar MJ, Harris HJ, Diskar M, Jones S, Mee CJ, et al. (2008) Protein kinase A-dependent step(s) in hepatitis C virus entry and infectivity. J Virol 82: 8797-8811.
24. Krieger SE, Zeisel MB, Davis C, Thumann C, Harris HJ, et al. (2010) Inhibition of hepatitis C virus infection by anti-claudin-1 antibodies is mediated by neutralization of E2-CD81-claudin-1 associations. Hepatology 51: 1144-1157.
25. Lupberger J, Zeisel MB, Xiao F, Thumann C, Fofana I, et al. (2011) EGFR and EphA2 are hepatitis C virus host entry factors and targets for antiviral therapy. Nat Med 17: 589-595.
26. Ploss A, Evans MJ, Gaysinskaya VA, Panis M, You H, et al. (2009) Human occludin is a hepatitis C virus entry factor required for infection of mouse cells. Nature 457: 882-886.
27. Dorner M, Horwitz JA, Robbins JB, Barry WT, Feng Q, et al. (2011) A genetically humanized mouse model for hepatitis C virus infection. Nature 474: 208-211.
28. Bitzegeio J, Bankwitz D, Hueging K, Haid S, Brohm C, et al. (2010) Adaptation of hepatitis C virus to mouse CD81 permits infection of mouse cells in the absence of human entry factors. PLoS Pathog 6: e1000978.
29. Meuleman P, Hesselgesser J, Paulson M, Vanwolleghem T, Desombere I, et al. (2008) Anti-CD81 antibodies can prevent a hepatitis C virus infection in vivo. Hepatology 48: 1761-1768.
30. Wakita T, Pietschmann T, Kato T, Date T, Miyamoto M, et al. (2005) Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat Med 11: 791-796.
31. Zhong J, Gastaminza P, Cheng G, Kapadia S, Kato T, et al. (2005) Robust hepatitis C virus infection in vitro. Proc Natl Acad Sci U S A 102: 9294-9299.
32. Brimacombe CL, Grove J, Meredith LW, Hu K, Syder AJ, et al. (2011) Neutralizing antibody-resistant hepatitis C virus cell-to-cell transmission. J Virol 85: 596-605.
33. Sainz B Jr, Barretto N, Martin DN, Hiraga N, Imamura M, et al. (2012) Identification of the Niemann-Pick C1-like 1 cholesterol absorption receptor as a new hepatitis C virus entry factor. Nat Med 18: 281-285.
34. Witteveldt J, Evans MJ, Bitzegeio J, Koutsoudakis G, Owsianka AM, et al. (2009) CD81 is dispensable for hepatitis C virus cell-to-cell transmission in hepatoma cells. J Gen Virol 90: 48-58.
35. Jones CT, Catanese MT, Law LM, Khetani SR, Syder AJ, et al. (2010) Real-time imaging of hepatitis C virus infection using a fluorescent cell-based reporter system. Nat Biotechnol 28: 167-171.
36. Pestka JM, Zeisel MB, Blaser E, Schurmann P, Bartosch B, et al. (2007) Rapid induction of virus-neutralizing antibodies and viral clearance in a single-source outbreak of hepatitis C. Proc Natl Acad Sci U S A 104: 6025-6030.
37. Mee CJ, Harris HJ, Farquhar MJ, Wilson G, Reynolds G, et al. (2009) Polarization restricts hepatitis C virus entry into HepG2 hepatoma cells. J Virol 83: 6211-6221.
38. Zahid MN, Turek M, Xiao F, Dao Thi VL, Guerin M, et al. (2013) The postbinding activity of scavenger receptor class B type I mediates initiation of hepatitis C virus infection and viral dissemination. Hepatology 57: 492-504.
39. Haberstroh A, Schnober EK, Zeisel MB, Carolla P, Barth H, et al. (2008) Neutralizing host responses in hepatitis C virus infection target viral entry at postbinding steps and membrane fusion. Gastroenterology 135: 1719-1728.
40. Da Costa D, Turek M, Felmlee DJ, Girardi E, Pfeffer S, et al. (2012) Reconstitution of the entire hepatitis C virus life cycle in nonhepatic cells. J Virol 86: 11919-11925.
41. Bartosch B, Dubuisson J, Cosset FL, (2003) Infectious hepatitis C virus pseudo-particles containing functional E1-E2 envelope protein complexes. J Exp Med 197: 633-642.
42. Zhu H, Wong-Staal F, Lee H, Syder A, McKelvy J, et al. (2012) Evaluation of ITX 5061, a scavenger receptor B1 antagonist: resistance selection and activity in combination with other hepatitis C virus antivirals. J Infect Dis 205: 656-662.
43. Zhao L, Wientjes MG, Au JL, (2004) Evaluation of combination chemotherapy: integration of nonlinear regression, curve shift, isobologram, and combination index analyses. Clin Cancer Res 10: 7994-8004.
44. Bertaux C, Dragic T, (2006) Different domains of CD81 mediate distinct stages of hepatitis C virus pseudoparticle entry. J Virol 80: 4940-4948.
45. Zeisel MB, Koutsoudakis G, Schnober EK, Haberstroh A, Blum HE, et al. (2007) Scavenger receptor BI is a key host factor for Hepatitis C virus infection required for an entry step closely linked to CD81. Hepatology 46: 1722-1731.
46. Fofana I, Fafi-Kremer S, Carolla P, Fauvelle C, Zahid MN, et al. (2012) Mutations that alter use of hepatitis C virus cell entry factors mediate escape from neutralizing antibodies. Gastroenterology 143: 223-233 e229.
47. Boyle JS, Silva A, Brady JL, Lew AM, (1997) DNA immunization: induction of higher avidity antibody and effect of route on T cell cytotoxicity. Proc Natl Acad Sci U S A 94: 14626-14631.
48. Flint M, Maidens CM, Loomis-Price LD, Shotton C, Dubuisson J, et al. (1999) Characterization of hepatitis C virus E2 glycoprotein interaction with a putative cellular receptor CD81. J Virol 73: 6235-6244.
49. Owsianka A, Clayton RF, Loomis-Price LD, McKeating JA, Patel AH, (2001) Functional analysis of hepatitis C virus E2 glycoproteins and virus-like particles reveals structural dissimilarities between different forms of E2. J Gen Virol 82: 1877-1883.
50. Patel AH, Wood J, Penin F, Dubuisson J, McKeating JA, (2000) Construction and characterization of chimeric hepatitis C virus E2 glycoproteins: analysis of regions critical for glycoprotein aggregation and CD81 binding. J Gen Virol 81: 2873-2883.
51. Schwarz AK, Grove J, Hu K, Mee CJ, Balfe P, et al. (2009) Hepatoma cell density promotes claudin-1 and scavenger receptor BI expression and hepatitis C virus internalization. J Virol 83: 12407-12414.
52. Meuleman P, Catanese MT, Verhoye L, Desombere I, Farhoudi A, et al. (2012) A human monoclonal antibody targeting scavenger receptor class B type I precludes hepatitis C virus infection and viral spread in vitro and in vivo. Hepatology 55: 364-372.
53. Lacek K, Vercauteren K, Grzyb K, Naddeo M, Verhoye L, et al. (2012) Novel human SR-BI antibodies prevent infection and dissemination of HCV in vitro and in humanized mice. J Hepatol 57: 17-23.