A prime-boost strategy using virus-like particles pseudotyped for HCV proteins triggers broadly neutralizing antibodies in macaques

Science Translational Medicine

Volumn 3, Issue 94, 2011, Pages

  Garrone, Pierre ^a,i   Fluckiger, Anne Catherine ^a   Mangeot, Philippe E ^a   Gauthier, Emmanuel ^b   Dupeyrot Lacas, Pia ^a   Mancip, Jimmy ^a   Cangialosi, Arnaud ^a   Du Chéné, Isaure ^a   LeGrand, Roger ^c   Mangeot, Isabelle ^c   Lavillette, Dimitri ^b   Bellier, Bertrand ^d,e,f   Cosset, François Loic ^b   Tangy, Frederic ^e   Klatzmann, David ^d,e,f,g   Dalba, Charlotte ^a,h  

^a Epixis SA   (France)

^b UNIVERSITÉ LYON 1   (France)

^c CRSSA   (France)

^d SORBONNE UNIVERSITÉ   (France)

^e CNRS   (France)

^f Sorbonne Université   (France)

^g PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^h EPIXIS SA   (France)

ⁱ Vivalis   (France)

Author keywords

[No Author keywords available]

Indexed keywords

GAG PROTEIN; GLYCOPROTEIN E1; GLYCOPROTEIN E2; NEUTRALIZING ANTIBODY; PROTEIN ANTIBODY; VIRUS LIKE PARTICLE VACCINE; VIRUS PROTEIN; HEPATITIS C ANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY RESPONSE; ANTIBODY TITER; ARTICLE; CONTROLLED STUDY; FEMALE; GENOTYPE; HEPATITIS C; HEPATITIS C VIRUS; IMMUNE RESPONSE; INFECTION PREVENTION; MACACA; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; VACCINATION; VACCINE PRODUCTION; VALIDATION PROCESS; VIRUS LIKE AGENT; VIRUS NEUTRALIZATION; VIRUS REPLICATION; ANIMAL; BIOSYNTHESIS; CROSS REACTION; IMMUNOLOGY; MOLECULAR GENETICS; VALIDATION STUDY; VIRION;

ANIMALS; ANTIBODIES, NEUTRALIZING; CROSS REACTIONS; HEPACIVIRUS; HEPATITIS C ANTIBODIES; MACACA; MICE; MOLECULAR SEQUENCE DATA; VIRAL PROTEINS; VIRION;

EID: 79961221361     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.3002330     Document Type: Article

References (54)

1. J. R. Mascola, D. C. Montefiori, The role of antibodies in HIV vaccines. Annu. Rev. Immunol. 28, 413-444 (2010).
2. F. Stoll-Keller, H. Barth, S. Fafi-Kremer, M. B. Zeisel, T. F. Baumert, Development of hepatitis C virus vaccines: Challenges and progress. Expert Rev. Vaccines 8, 333-345 (2009).
3. M. Law, T. Maruyama, J. Lewis, E. Giang, A. W. Tarr, Z. Stamataki, P. Gastaminza, F. V. Chisari, I. M. Jones, R. I. Fox, J. K. Ball, J. A. McKeating, N. M. Kneteman, D. R. Burton, Broadly neutralizing antibodies protect against hepatitis C virus quasispecies challenge. Nat. Med. 14, 25-27 (2008).
4. A. D. Barrett, D. E. Teuwen, Yellow fever vaccine-How does it work and why do rare cases of serious adverse events take place? Curr. Opin. Immunol. 21, 308-313 (2009).
5. P. Roy, R. Noad, Virus-like particles as a vaccine delivery system: Myths and facts. Adv. Exp. Med. Biol. 655, 145-158 (2009).
6. D. M. Harper, E. L. Franco, C. M. Wheeler, A. B. Moscicki, B. Romanowski, C. M. Roteli-Martins, D. Jenkins, A. Schuind, S. A. Costa Clemens, G. Dubin; HPV Vaccine Study Group, Sustained efficacy up to 4.5 years of a bivalent L1 virus-like particle vaccine against human papillomavirus types 16 and 18: Follow-up from a randomised control trial. Lancet 367, 1247-1255 (2006).
7. W. Akahata, Z. Y. Yang, H. Andersen, S. Sun, H. A. Holdaway, W. P. Kong, M. G. Lewis, S. Higgs, M. G. Rossmann, S. Rao, G. J. Nabel, A virus-like particle vaccine for epidemic Chikungunya virus protects nonhuman primates against infection. Nat. Med. 16, 334-338 (2010).
8. C. Dalba, B. Bellier, N. Kasahara, D. Klatzmann, Replication-competent vectors and empty virus-like particles: New retroviral vector designs for cancer gene therapy or vaccines. Mol. Ther. 15, 457-466 (2007).
9. C. Ludwig, R. Wagner, Virus-like particles - Universal molecular toolboxes. Curr. Opin. Biotechnol. 18, 537-545 (2007).
10. B. Bartosch, J. Bukh, J. C. Meunier, C. Granier, R. E. Engle, W. C. Blackwelder, S. U. Emerson, F. L. Cosset, R. H. Purcell, In vitro assay for neutralizing antibody to hepatitis C virus: Evidence for broadly conserved neutralization epitopes. Proc. Natl. Acad. Sci. U.S.A. 100, 14199-14204 (2003).
11. B. Bartosch, J. Dubuisson, F. L. Cosset, Infectious hepatitis C virus pseudo-particles containing functional E1-E2 envelope protein complexes. J. Exp. Med. 197, 633-642 (2003).
12. D. Desjardins, C. Huret, C. Dalba, F. Kreppel, S. Kochanek, F. L. Cosset, F. Tangy, D. Klatzmann, B. Bellier, Recombinant retrovirus-like particle forming DNA vaccines in prime-boost immunization and their use for hepatitis C virus vaccine development. J. Gene Med. 11, 313-325 (2009).
13. A. Op De Beeck, C. Voisset, B. Bartosch, Y. Ciczora, L. Cocquerel, Z. Keck, S. Foung, F. L. Cosset, J. Dubuisson, Characterization of functional hepatitis C virus envelope glycoproteins. J. Virol. 78, 2994-3002 (2004).
14. G. Leroux-Roels, A. H. Batens, I. Desombere, B. Van Den Steen, C. Vander Stichele, G. Maertens, F. Hulstaert, Immunogenicity and tolerability of intradermal administration of an HCV E1-based vaccine candidate in healthy volunteers and patients with resolved or ongoing chronic HCV infection. Hum. Vaccin. 1, 61-65 (2005).
15. J. C. Meunier, R. S. Russell, V. Goossens, S. Priem, H. Walter, E. Depla, A. Union, K. N. Faulk, J. Bukh, S. U. Emerson, R. H. Purcell, Isolation and characterization of broadly neutralizing human monoclonal antibodies to the E1 glycoprotein of hepatitis C virus. J. Virol. 82, 966-973 (2008).
16. T. Pietschmann, A. Kaul, G. Koutsoudakis, A. Shavinskaya, S. Kallis, E. Steinmann, K. Abid, F. Negro, M. Dreux, F. L. Cosset, R. Bartenschlager, Construction and characterization of infectious intragenotypic and intergenotypic hepatitis C virus chimeras. Proc. Natl. Acad. Sci. U.S.A. 103, 7408-7413 (2006).
17. M. Dreux, T. Pietschmann, C. Granier, C. Voisset, S. Ricard-Blum, P. E. Mangeot, Z. Keck, S. Foung, N. Vu-Dac, J. Dubuisson, R. Bartenschlager, D. Lavillette, F. L. Cosset, High density lipoprotein inhibits hepatitis C virus-neutralizing antibodies by stimulating cell entry via activation of the scavenger receptor BI. J. Biol. Chem. 281, 18285-18295 (2006).
18. G. Leroux-Roels, C. A. Esquivel, R. DeLeys, L. Stuyver, A. Elewaut, J. Philippé, I. Desombere, J. Paradijs, G. Maertens, Lymphoproliferative responses to hepatitis C virus core, E1, E2, and NS3 in patients with chronic hepatitis C infection treated with interferon α. Hepatology 23, 8-16 (1996).
19. J.M. Pestka, M. B. Zeisel, E. Bläser, P. Schürmann, B. Bartosch, F. L. Cosset, A. H. Patel, H. Meisel, J. Baumert, S. Viazov, K. Rispeter, H. E. Blum, M. Roggendorf, T. F. Baumert, 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 (2007).
20. V. Sandrin, F. L. Cosset, Intracellular versus cell surface assembly of retroviral pseudotypes is determined by the cellular localization of the viral glycoprotein, its capacity to interact with Gag, and the expression of the Nef protein. J. Biol. Chem. 281, 528-542 (2006).
21. L. Naldini, U. Blömer, P. Gallay, D. Ory, R. Mulligan, F. H. Gage, I. M. Verma, D. Trono, In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science 272, 263-267 (1996).
22. Y. Yang, E. F. Vanin, M. A. Whitt, M. Fornerod, R. Zwart, R. D. Schneiderman, G. Grosveld, A. W. Nienhuis, Inducible, high-level production of infectious murine leukemia retroviral vector particles pseudotyped with vesicular stomatitis virus G envelope protein. Hum. Gene Ther. 6, 1203-1213 (1995).
23. M. Hsu, J. Zhang, M. Flint, C. Logvinoff, C. Cheng-Mayer, C. M. Rice, J. A. McKeating, Hepatitis C virus glycoproteins mediate pH-dependent cell entry of pseudotyped retroviral particles. Proc. Natl. Acad. Sci. U.S.A. 100, 7271-7276 (2003).
24. P. Bonnafous, M. Perrault, O. Le Bihan, B. Bartosch, D. Lavillette, F. Penin, O. Lambert, E. I. Pécheur, Characterization of hepatitis C virus pseudoparticles by cryo-transmission electron microscopy using functionalized magnetic nanobeads. J. Gen. Virol. 91 (Pt 8), 1919-1930 (2010).
25. J. Dubuisson, H. H. Hsu, R. C. Cheung, H. B. Greenberg, D. G. Russell, C. M. Rice, Formation and intracellular localization of hepatitis C virus envelope glycoprotein complexes expressed by recombinant vaccinia and Sindbis viruses. J. Virol. 68, 6147-6160 (1994).
26. J. Szécsi, B. Boson, P. Johnsson, P. Dupeyrot-Lacas, M. Matrosovich, H. D. Klenk, D. Klatzmann, V. Volchkov, F. L. Cosset, Induction of neutralising antibodies by virus-like particles harbouring surface proteins from highly pathogenic H5N1 and H7N1 influenza viruses. Virol. J. 3, 70 (2006).
27. K. J. Stittelaar, R. L. de Swart, H.W. Vos, G. van Amerongen, N. Sixt, T. F.Wild, A. D. Osterhaus, Priming of measles virus-specific humoral- and cellular-immune responses in macaques by DNA vaccination. Vaccine 20, 2022-2026 (2002).
28. C. Kuiken, P. Simmonds, Nomenclature and numbering of the hepatitis C virus. Methods Mol. Biol. 510, 33-53 (2009).
29. D. Lavillette, A. W. Tarr, C. Voisset, P. Donot, B. Bartosch, C. Bain, A. H. Patel, J. Dubuisson, J. K. Ball, F. L. Cosset, Characterization of host-range and cell entry properties of the major genotypes and subtypes of hepatitis C virus. Hepatology 41, 265-274 (2005).
30. C. Kuiken, M. Mizokami, G. Deleage, K. Yusim, F. Penin, T. Shin-I, C. Charavay, N. Tao, D. Crisan, D. Grando, A. Dalwani, C. Geourjon, A. Agrawal, C. Combet, Hepatitis C databases, principles and utility to researchers. Hepatology 43, 1157-1165 (2006).
31. B. D. Lindenbach, M. J. Evans, A. J. Syder, B. Wolk, T. L. Tellinghuisen, C. C. Liu, T. Maruyama, R. O. Hynes, D. R. Burton, J. A. McKeating, C. M. Rice, Complete replication of hepatitis C virus in cell culture. Science 309, 623-626 (2005).
32. T. Wakita, T. Pietschmann, T. Kato, T. Date, M. Miyamoto, Z. Zhao, K. Murthy, A. Habermann, H. G. Kräusslich, M. Mizokami, R. Bartenschlager, T. J. Liang, Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat. Med. 11, 791-796 (2005).
33. J. Zhong, P. Gastaminza, G. Cheng, S. Kapadia, T. Kato, D. R. Burton, S. F. Wieland, S. L. Uprichard, T. Wakita, F. V. Chisari, Robust hepatitis C virus infection in vitro. Proc. Natl. Acad. Sci. U.S.A. 102, 9294-9299 (2005).
34. L. Arribillaga, A. L. de Cerio, P. Sarobe, N. Casares, M. Gorraiz, A. Vales, O. Bruna-Romero, F. Borrás-Cuesta, G. Paranhos-Baccala, J. Prieto, J. Ruiz, J. J. Lasarte, Vaccination with an adenoviral vector encoding hepatitis C virus (HCV) NS3 protein protects against infection with HCV-recombinant vaccinia virus. Vaccine 21, 202-210 (2002).
35. + T-cell epitopes within hepatitis C virus NS3 and NS4 proteins. J. Virol. 79, 12425-12433 (2005).
36. K. A. Lang, J. Yan, R. Draghia-Akli, A. Khan, D. B. Weiner, Strong HCV NS3- and NS4A-specific cellular immune responses induced in mice and Rhesus macaques by a novel HCV genotype 1a/1b consensus DNA vaccine. Vaccine 26, 6225-6231 (2008).
37. D. Lavillette, Y. Morice, G. Germanidis, P. Donot, A. Soulier, E. Pagkalos, G. Sakellariou, L. Intrator, B. Bartosch, J. M. Pawlotsky, F. L. Cosset, Human serum facilitates hepatitis C virus infection, and neutralizing responses inversely correlate with viral replication kinetics at the acute phase of hepatitis C virus infection. J. Virol. 79, 6023-6034 (2005).
38. C. Logvinoff, M. E. Major, D. Oldach, S. Heyward, A. Talal, P. Balfe, S. M. Feinstone, H. Alter, C. M. Rice, J. A. McKeating, Neutralizing antibody response during acute and chronic hepatitis C virus infection. Proc. Natl. Acad. Sci. U.S.A. 101, 10149-10154 (2004).
39. A. S. Fauci, M. I. Johnston, C. W. Dieffenbach, D. R. Burton, S. M. Hammer, J. A. Hoxie, M. Martin, J. Overbaugh, D. I. Watkins, A. Mahmoud, W. C. Greene, HIV vaccine research: The way forward. Science 321, 530-532 (2008).
40. Y. Shu, S. Winfrey, Z. Y. Yang, L. Xu, S. S. Rao, I. Srivastava, S. W. Barnett, G. J. Nabel, J. R. Mascola, Efficient protein boosting after plasmid DNA or recombinant adenovirus immunization with HIV-1 vaccine constructs. Vaccine 25, 1398-1408 (2007).
41. B. F. Haynes, H. X. Liao, G. D. Tomaras, Is developing an HIV-1 vaccine possible? Curr. Opin. HIV AIDS 5, 362-367 (2010).
42. J. H. Kim, S. Rerks-Ngarm, J. L. Excler, N. L. Michael, HIV vaccines: Lessons learned and the way forward. Curr. Opin. HIV AIDS 5, 428-434 (2010).
43. Z. Stamataki, S. Coates, M. J. Evans, M. Wininger, K. Crawford, C. Dong, Y. L. Fong, D. Chien, S. Abrignani, P. Balfe, C. M. Rice, J. A. McKeating, M. Houghton, Hepatitis C virus envelope glycoprotein immunization of rodents elicits cross-reactive neutralizing antibodies. Vaccine 25, 7773-7784 (2007).
44. Y. Lin, T. Kwon, J. Polo, Y. F. Zhu, S. Coates, K. Crawford, C. Dong, M. Wininger, J. Hall, M. Selby, D. Coit, A. Medina-Selby, C. McCoin, P. Ng, D. Drane, D. Chien, J. Han, M. Vajdy, M. Houghton, Induction of broad CD4+ and CD8+ T-cell responses and cross-neutralizing antibodies against hepatitis C virus by vaccination with Th1-adjuvanted polypeptides followed by defective alphaviral particles expressing envelope glycoproteins gpE1 and gpE2 and nonstructural proteins 3, 4, and 5. J. Virol. 82, 7492-7503 (2008).
45. R. Ray, K. Meyer, A. Banerjee, A. Basu, S. Coates, S. Abrignani, M. Houghton, S. E. Frey, R. B. Belshe, Characterization of antibodies induced by vaccination with hepatitis C virus envelope glycoproteins. J. Infect. Dis. 202, 862-866 (2010).
46. J. K. Yee, T. Friedmann, J. C. Burns, Generation of high-titer pseudotyped retroviral vectors with very broad host range. Methods Cell Biol. 43 (Pt A), 99-112 (1994).
47. C. Combredet, V. Labrousse, L. Mollet, C. Lorin, F. Delebecque, B. Hurtrel, H. McClure, M. B. Feinberg, M. Brahic, F. Tangy, A molecularly cloned Schwarz strain of measles virus vaccine induces strong immune responses in macaques and transgenic mice. J. Virol. 77, 11546-11554 (2003).
48. M. A. Petit, M. Lievre, S. Peyrol, S. De Sequeira, P. Berthillon, R. W. Ruigrok, C. Trépo, Enveloped particles in the serum of chronic hepatitis C patients. Virology 336, 144-153 (2005).
49. B. Horvat, P. Rivailler, G. Varior-Krishnan, A. Cardoso, D. Gerlier, C. Rabourdin-Combe, Transgenic mice expressing human measles virus (MV) receptor CD46 provide cells exhibiting different permissivities to MV infections. J. Virol. 70, 6673-6681 (1996).
50. U. Müller, U. Steinhoff, L. F. Reis, S. Hemmi, J. Pavlovic, R. M. Zinkernagel, M. Aguet, Functional role of type I and type II interferons in antiviral defense. Science 264, 1918-1921 (1994).
51. M. Dreux, F. L. Cosset, Detection of neutralizing antibodies with HCV pseudoparticles (HCVpp). Methods Mol. Biol. 510, 427-438 (2009).
52. H. Nakabayashi, K. Taketa, K. Miyano, T. Yamane, J. Sato, Growth of human hepatoma cells lines with differentiated functions in chemically defined medium. Cancer Res. 42, 3858-3863 (1982).
53. V. Deleersnyder, A. Pillez, C. Wychowski, K. Blight, J. Xu, Y. S. Hahn, C. M. Rice, J. Dubuisson, Formation of native hepatitis C virus glycoprotein complexes. J. Virol. 71, 697-704 (1997).
54. -/-) mice via F. Tangy. Funding: This work was supported by grants from the European Union (LSHB-CT-2004-005246 "COMPUVAC"), the Agence Nationale de Recherches sur le SIDA et les Hepatites Virales, the European Research Council (ERC Advanced Grant No. 233130 "HEPCENT" to F.-L.C.), the FINOVI Foundation, and recurrent funding by Université Pierre et Marie Curie, INSERM, CNRS, École Normale Supérieure de Lyon, and Université Claude Bernard Lyon I. Author contributions: P.G., F.-L.C., F.T., D.K., and C.D. designed and supervised the studies and analyzed the data. P.G., A.-C.F., P.E.M., E.G., P.D.-L., J.M., A.C., and I.D.C. performed the in vitro experiments. E.G., P.D.-L., J.M., A.C., and B.B. performed the in vivo experiments in mouse. R.L. and I.M. performed the in vivo experiments in macaque. P.G., A.-C.F., D.K., and C.D. wrote the paper. Competing interests: Employment: A.C., C.D., I.D.C., P.D.-L., A.-C.F., P.G., J.M., and P.E.M. were employed by Epixis S.A. while engaged in the research project. Personal financial interests: F.-L.C., C.D., D.K., and F.T. own shares in Epixis S.A.; F.-L.C., D.K., and F.T. obtained consultation fees from Epixis S.A. while engaged in the research project; B.B., F.-L.C., C.D., D.K., and F.T. are authors of the following patents related to the technology presented: "Synthetic viruses and uses thereof" (U.S. No. US2004-0071661, EP No. EP1404819), "Infectious HCV pseudo-particles containing functional E1, E2 envelope proteins" (U.S. No. US2006-222661, EP No. EP1537206), "Infectious cDNA of an approved vaccine strain of measles virus - use for immunogenic compositions" (U.S. No. US2005-227224, EP No. EP1513872), and "Recombinant measles virus expressing epitopes of antigens of RNA viruses - use for the preparation of vaccine composition" (U.S. No. US2006-0013826, EP No. EP1516058). The other authors declare that they have no competing interests. Accession numbers: The sequences of the E1E2 proteins of HCV strains H77, CG1b, CON1, JFH-1, UKN2B, and UKN4 can be found as GenBank AF009606, AF333324, AJ238799, AB047639, AY734982, and AY734986, respectively.