Influenza virus-like particle vaccines made in Nicotiana benthamiana elicit durable, poly-functional and cross-reactive T cell responses to influenza HA antigens

Clinical Immunology

Volumn 154, Issue 2, 2014, Pages 164-177

  Landry, Nathalie ^a   Pillet, Stéphane ^a,b   Favre, David ^a   Poulin, Jean François ^a   Trépanier, Sonia ^a   Yassine Diab, Bader ^a   Ward, Brian J ^b  

^a Medicago inc ^*  (Canada)

^b RESEARCH INSTITUTE OF THE MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

Author keywords

Cell mediated immunity; Influenza; Long term memory response; Nicotiana benthamiana; Vaccine; Virus like particle

Indexed keywords

INACTIVATED VACCINE; INFLUENZA VACCINE; INFLUENZA VIRUS HEMAGGLUTININ; PLACEBO; GAMMA INTERFERON; H1 VIRUS LIKE PARTICLE VACCINE; H5 VIRUS LIKE PARTICLE VACCINE; INTERLEUKIN 17; INTERLEUKIN 2; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ADULT; ANTIBODY RESPONSE; ARTICLE; BLOOD SAMPLING; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; FLOW CYTOMETRY; HUMAN; HUMAN TISSUE; HUMORAL IMMUNITY; INFLUENZA; INFLUENZA VACCINATION; INFLUENZA VIRUS A H5N1; LONG TERM MEMORY; MEMORY T LYMPHOCYTE; NICOTIANA BENTHAMIANA; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL (TOPIC); T LYMPHOCYTE; ANTIBODY TITER; CROSS REACTION; IMMUNOGENICITY; INFLUENZA VIRUS A H1N1; MAJOR CLINICAL STUDY; NORMAL HUMAN; PHASE 1 CLINICAL TRIAL; PHASE 2 CLINICAL TRIAL; RANDOMIZED CONTROLLED TRIAL; SEROCONVERSION; VIRUS LIKE AGENT;

CELL-MEDIATED IMMUNITY; INFLUENZA; LONG-TERM MEMORY RESPONSE; NICOTIANA BENTHAMIANA; VACCINE; VIRUS-LIKE PARTICLE;

ADOLESCENT; ADULT; ANTIGENS, VIRAL; BIOLOGICAL MARKERS; FEMALE; HUMANS; IMMUNITY, CELLULAR; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA A VIRUS, H5N1 SUBTYPE; INFLUENZA VACCINES; MALE; T-LYMPHOCYTES; TOBACCO; VACCINES, VIRUS-LIKE PARTICLE; YOUNG ADULT;

EID: 84908368993     PISSN: 15216616     EISSN: 15217035     Source Type: Journal    
DOI: 10.1016/j.clim.2014.08.003     Document Type: Article

References (58)

1. Kim T.S., Sun J., Braciale T.J. T cell responses during influenza infection: getting and keeping control. Trends Immunol. 2011, 32:225-231.
2. Kreijtz J.H., Fouchier R.A., Rimmelzwaan G.F. Immune responses to influenza virus infection. Virus Res. 2011, 162:19-30.
3. McElhaney J.E., Xie D., Hager W.D., Barry M.B., Wang Y., Kleppinger A., et al. T cell responses are better correlates of vaccine protection in the elderly. J. Immunol. 2006, 176:6333-6339.
4. Gras S., Kedzierski L., Valkenburg S.A., Laurie K., Liu Y.C., Denholm J.T., et al. Cross-reactive CD8+ T-cell immunity between the pandemic H1N1-2009 and H1N1-1918 influenza A viruses. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:12599-12604.
5. Wagar L.E., Rosella L., Crowcroft N., Lowcock B., Drohomyrecky P.C., Foisy J., et al. Humoral and cell-mediated immunity to pandemic H1N1 influenza in a Canadian cohort one year post-pandemic: implications for vaccination. PLoS One 2011, 6:e28063.
6. Laurie K.L., Carolan L.A., Middleton D., Lowther S., Kelso A., Barr I.G. Multiple infections with seasonal influenza A virus induce cross-protective immunity against A(H1N1) pandemic influenza virus in a ferret model. J. Infect. Dis. 2010, 202:1011-1020.
7. Weinfurter J.T., Brunner K., Capuano S.V., Li C., Broman K.W., Kawaoka Y., et al. Cross-reactive T cells are involved in rapid clearance of 2009 pandemic H1N1 influenza virus in nonhuman primates. PLoS Pathog. 2011, 7:e1002381.
8. Hillaire M.L., van Trierum S.E., Kreijtz J.H., Bodewes R., Geelhoed-Mieras M.M., Nieuwkoop N.J., et al. Cross-protective immunity against influenza pH1N1 2009 viruses induced by seasonal influenza A (H3N2) virus is mediated by virus-specific T-cells. J. Gen. Virol. 2011, 92:2339-2349.
9. Subbramanian R.A., Basha S., Brady R.C., Hazenfeld S., Shata M.T., Bernstein D.I. Age-related changes in magnitude and diversity of cross-reactive CD4+ T-cell responses to the novel pandemic H1N1 influenza hemagglutinin. Hum. Immunol. 2010, 71:957-963.
10. Baumgartner C.K., Malherbe L.P. Regulation of CD4 T-cell receptor diversity by vaccine adjuvants. Immunology 2010, 130:16-22.
11. Galli G., Medini D., Borgogni E., Zedda L., Bardelli M., Malzone C., et al. Adjuvanted H5N1 vaccine induces early CD4+ T cell response that predicts long-term persistence of protective antibody levels. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:3877-3882.
12. Peek L.J., Middaugh C.R., Berkland C. Nanotechnology in vaccine delivery. Adv. Drug Deliv. Rev. 2008, 60:915-928.
13. De Temmerman M.L., Rejman J., Demeester J., Irvine D.J., Gander B., De Smedt S.C. Particulate vaccines: on the quest for optimal delivery and immune response. Drug Discov. Today 2011, 16:569-582.
14. McNeela E.A., Lavelle E.C. Recent advances in microparticle and nanoparticle delivery vehicles for mucosal vaccination. Curr. Top. Microbiol. Immunol. 2012, 354:75-99.
15. Lacasse P., Denis J., Lapointe R., Leclerc D., Lamarre A. Novel plant virus-based vaccine induces protective cytotoxic T-lymphocyte-mediated antiviral immunity through dendritic cell maturation. J. Virol. 2008, 82:785-794.
16. D'Aoust M.A., Couture M.M., Charland N., Trepanier S., Landry N., Ors F., et al. The production of hemagglutinin-based virus-like particles in plants: a rapid, efficient and safe response to pandemic influenza. Plant Biotechnol. J. 2010, 8:607-619.
17. Hillaire M.L., Osterhaus A.D., Rimmelzwaan G.F. Induction of virus-specific cytotoxic T lymphocytes as a basis for the development of broadly protective influenza vaccines. J. Biomed. Biotechnol. 2011, 2011:939860.
18. Sommerfelt M.A. T-cell-mediated and humoral approaches to universal influenza vaccines. Expert Rev. Vaccines 2011, 10:1359-1361.
19. Stanekova Z., Vareckova E. Conserved epitopes of influenza A virus inducing protective immunity and their prospects for universal vaccine development. Virol. J. 2010, 7:351.
20. Schotsaert M., Saelens X., Leroux-Roels G. Influenza vaccines: T-cell responses deserve more attention. Expert Rev. Vaccines 2012, 11:949-962.
21. Baylor N.W., Houn F. Considerations for licensure of influenza vaccines with pandemic and prepandemic indications. Curr. Top. Microbiol. Immunol. 2009, 333:453-470.
22. Bull M., Lee D., Stucky J., Chiu Y.L., Rubin A., Horton H., et al. Defining blood processing parameters for optimal detection of cryopreserved antigen-specific responses for HIV vaccine trials. J. Immunol. Methods 2007, 322:57-69.
23. Jaimes M.C., Maecker H.T., Yan M., Maino V.C., Hanley M.B., Greer A., et al. Quality assurance of intracellular cytokine staining assays: analysis of multiple rounds of proficiency testing. J. Immunol. Methods 2011, 363:143-157.
24. Makedonas G., Betts M.R. Polyfunctional analysis of human t cell responses: importance in vaccine immunogenicity and natural infection, Springer Semin. Immunopathol. 2006, 28:209-219.
25. Moris P., van der Most R., Leroux-Roels I., Clement F., Drame M., Hanon E., et al. H5N1 influenza vaccine formulated with AS03 A induces strong cross-reactive and polyfunctional CD4 T-cell responses. J. Clin. Immunol. 2011, 31:443-454.
26. Gaundar S.S., Clancy L., Blyth E., Meyer W., Gottlieb D.J. Robust polyfunctional T-helper 1 responses to multiple fungal antigens from a cell population generated using an environmental strain of Aspergillus fumigatus. Cytotherapy 2012, 14:1119-1130.
27. Landry N., Ward B.J., Trepanier S., Montomoli E., Dargis M., Lapini G., et al. Preclinical and clinical development of plant-made virus-like particle vaccine against avian H5N1 influenza. PLoS One 2010, 5:e15559.
28. WHO Manual on animal influenza diagnosis and surveillance 2002 Available from:. http://www.wpro.who.int/NR/rdonlyres/EFD2B9A7-2265-4AD0-BC98-97937B4FA83C/0/manualonanimalaidiagnosisandsurveillance.pdf.
29. Galli G., Hancock K., Hoschler K., DeVos J., Praus M., Bardelli M., et al. Fast rise of broadly cross-reactive antibodies after boosting long-lived human memory B cells primed by an MF59 adjuvanted prepandemic vaccine. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:7962-7967.
30. Betts M.R., Brenchley J.M., Price D.A., De Rosa S.C., Douek D.C., Roederer M., et al. Sensitive and viable identification of antigen-specific CD8+ T cells by a flow cytometric assay for degranulation. J. Immunol. Methods 2003, 281:65-78.
31. Zaritskaya L., Shurin M.R., Sayers T.J., Malyguine A.M. New flow cytometric assays for monitoring cell-mediated cytotoxicity. Expert Rev. Vaccines 2010, 9:601-616.
32. Williams M.A., Bevan M.J. Effector and memory CTL differentiation. Annu. Rev. Immunol. 2007, 25:171-192.
33. Moron G., Dadaglio G., Leclerc C. New tools for antigen delivery to the MHC class I pathway. Trends Immunol. 2004, 25:92-97.
34. Shoham D. Influenza type A virus: an outstandingly protean pathogen and a potent modular weapon. Crit. Rev. Microbiol. 2013, 39:123-138.
35. McKinstry K.K., Dutton R.W., Swain S.L., Strutt T.M. Memory CD4 T cell-mediated immunity against influenza A virus: more than a little helpful. Arch. Immunol. Ther. Exp. (Warsz) 2013, 61:341-353.
36. Kreijtz J.H., Bodewes R., van Amerongen G., Kuiken T., Fouchier R.A., Osterhaus A.D., et al. Primary influenza A virus infection induces cross-protective immunity against a lethal infection with a heterosubtypic virus strain in mice. Vaccine 2007, 25:612-620.
37. Kreijtz J.H., Bodewes R., van den Brand J.M., de Mutsert G., Baas C., van Amerongen G., et al. Infection of mice with a human influenza A/H3N2 virus induces protective immunity against lethal infection with influenza A/H5N1 virus. Vaccine 2009, 27:4983-4989.
38. D'Aoust M.A., Lavoie P.O., Couture M.M., Trepanier S., Guay J.M., Dargis M., et al. Influenza virus-like particles produced by transient expression in Nicotiana benthamiana induce a protective immune response against a lethal viral challenge in mice. Plant Biotechnol. J. 2008, 6:930-940.
39. Lipatov A.S., Hoffmann E., Salomon R., Yen H.L., Webster R.G. Cross-protectiveness and immunogenicity of influenza A/Duck/Singapore/3/97(H5) vaccines against infection with A/Vietnam/1203/04(H5N1) virus in ferrets. J. Infect. Dis. 2006, 194:1040-1043.
40. Wilkinson T.M., Li C.K., Chui C.S., Huang A.K., Perkins M., Liebner J.C., et al. Preexisting influenza-specific CD4+ T cells correlate with disease protection against influenza challenge in humans. Nat. Med. 2012, 18:274-280.
41. Sridhar S., Begom S., Bermingham A., Hoschler K., Adamson W., Carman W., et al. Cellular immune correlates of protection against symptomatic pandemic influenza. Nat. Med. 2013, 19:1305-1312.
42. Duvvuri V.R., Marchand-Austin A., Eshaghi A., Patel S.N., Low D.E., Gubbay J.B. Potential T cell epitopes within swine-origin triple reassortant influenza A (H3N2) variant virus which emerged in 2011: an immunoinformatics study. Vaccine 2012, 30:6054-6063.
43. Duvvuri V.R., Moghadas S.M., Guo H., Duvvuri B., Heffernan J.M., Fisman D.N., et al. Highly conserved cross-reactive CD4+ T-cell HA-epitopes of seasonal and the 2009 pandemic influenza viruses. Influenza Other Respir. Viruses 2010, 4:249-258.
44. Terajima M., Babon J.A., Co M.D., Ennis F.A. Cross-reactive human B cell and T cell epitopes between influenza A and B viruses. Virol. J. 2013, 10:244.
45. Lee L.Y., Ha do L.A., Simmons C., de Jong M.D., Chau N.V., Schumacher R., et al. Memory T cells established by seasonal human influenza A infection cross-react with avian influenza A (H5N1) in healthy individuals. J. Clin. Invest. 2008, 118:3478-3490.
46. Kang S.M., Song J.M., Quan F.S., Compans R.W. Influenza vaccines based on virus-like particles. Virus Res. 2009, 143:140-146.
47. Seder R.A., Darrah P.A., Roederer M. T-cell quality in memory and protection: implications for vaccine design. Nat. Rev. Immunol. 2008, 8:247-258.
48. McHeyzer-Williams L.J., Malherbe L.P., McHeyzer-Williams M.G. Helper T cell-regulated B cell immunity. Curr. Top. Microbiol. Immunol. 2006, 311:59-83.
49. Weaver J.M., Yang H., Roumanes D., Lee F.E., Wu H., Treanor J.J., et al. Increase in IFNgamma(-)IL-2(+) cells in recent human CD4 T cell responses to 2009 pandemic H1N1 influenza. PLoS One 2013, 8:e57275.
50. Kool M., Fierens K., Lambrecht B.N. Alum adjuvant: some of the tricks of the oldest adjuvant. J. Med. Microbiol. 2012, 61:927-934.
51. Keitel W.A., Campbell J.D., Treanor J.J., Walter E.B., Patel S.M., He F., et al. Safety and immunogenicity of an inactivated influenza A/H5N1 vaccine given with or without aluminum hydroxide to healthy adults: results of a phase I-II randomized clinical trial. J. Infect. Dis. 2008, 198:1309-1316.
52. Baz M., Luke C.J., Cheng X., Jin H., Subbarao K. H5N1 vaccines in humans. Virus Res. 2013, 178(1):78-98.
53. Dillon S.B., Demuth S.G., Schneider M.A., Weston C.B., Jones C.S., Young J.F., et al. Induction of protective class I MHC-restricted CTL in mice by a recombinant influenza vaccine in aluminium hydroxide adjuvant. Vaccine 1992, 10:309-318.
54. Hansen B., Belfast M., Soung G., Song L., Egan P.M., Capen R., et al. Effect of the strength of adsorption of hepatitis B surface antigen to aluminum hydroxide adjuvant on the immune response. Vaccine 2009, 27:888-892.
55. Hansen B., Malyala P., Singh M., Sun Y., Srivastava I., Hogenesch H., et al. Effect of the strength of adsorption of HIV 1 SF162dV2gp140 to aluminum-containing adjuvants on the immune response. J. Pharm. Sci. 2011, 100:3245-3250.
56. Hansen B., Sokolovska A., HogenEsch H., Hem S.L. Relationship between the strength of antigen adsorption to an aluminum-containing adjuvant and the immune response. Vaccine 2007, 25:6618-6624.
57. Watkinson A., Soliakov A., Ganesan A., Hirst K., Lebutt C., Fleetwood K., et al. Increasing the potency of an alhydrogel formulated vaccine by minimising antigen-adjuvant interactions. Clin. Vaccine Immunol. 2013, 20(11):1659-1668.
58. Spinozzi F., Porcelli S.A. Recognition of lipids from pollens by CD1-restricted T cells. Immunol. Allergy Clin. N. Am. 2007, 27:79-92.