A study of Chitosan and c-di-GMP as mucosal adjuvants for intranasal influenza H5N1 vaccine

Influenza and other Respiratory Viruses

Volumn 7, Issue 6, 2013, Pages 1181-1193

  Svindland, Signe C ^a   Pedersen, Gabriel K ^a   Pathirana, Rishi D ^a   Bredholt, Geir ^a   Nøstbakken, Jane K ^a   Jul Larsen, Åsne ^a   Guzmán, Carlos A ^b   Montomoli, Emanuele ^c,d   Lapini, Giulia ^c   Piccirella, Simona ^d   Jabbal Gill, Inderjit ^e   Hinchcliffe, Michael ^e   Cox, Rebecca J ^a,f  

^a UNIVERSITY OF BERGEN   (Norway)

^b HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

^c UNIVERSITY OF SIENA   (Italy)

^d VisMederi Srl   (Italy)

^e Archimedes Development Ltd   (United Kingdom)

^f HAUKELAND UNIVERSITY HOSPITAL   (Norway)

Author keywords

C di GMP; Chitosan; H5N1; Influenza; Intranasal; Th17; Vaccine

Indexed keywords

BIS(3',5') CYCLIC DIMERIC GUANOSINE MONOPHOSPHATE; CHISYS; CHITOSAN DERIVATIVE; CHITOSAN GLUTAMATE 213; GAMMA INTERFERON; GUANOSINE PHOSPHATE; INACTIVATED INFLUENZA SUBUNIT VACCINE; INFLUENZA VACCINE; INFLUENZA VIRUS HEMAGGLUTININ; INTERLEUKIN 2; NIBRG 14; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ADJUVANT THERAPY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY RESPONSE; ARTICLE; CD4+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RESPONSE; DOSE RESPONSE; DRUG EFFICACY; FEMALE; HEMAGGLUTINATION INHIBITION; HEMOLYSIS; HUMORAL IMMUNITY; IMMUNE RESPONSE; INFLUENZA A (H5N1); INFLUENZA VACCINATION; INFLUENZA VIRUS A H5N1; MOUSE; MUCOSAL IMMUNITY; NONHUMAN; PRIORITY JOURNAL; TH1 CELL; TH2 CELL; VIRUS HEMAGGLUTINATION;

C-DI-GMP; CHITOSAN; H5N1; INFLUENZA; INTRANASAL; TH17; VACCINE;

ADJUVANTS, IMMUNOLOGIC; ADMINISTRATION, INTRANASAL; ANIMAL EXPERIMENTATION; ANIMALS; ANTIBODIES, VIRAL; CD4-POSITIVE T-LYMPHOCYTES; CHITOSAN; CYCLIC GMP; CYTOKINES; FEMALE; HEMAGGLUTINATION INHIBITION TESTS; INFLUENZA A VIRUS, H5N1 SUBTYPE; INFLUENZA VACCINES; MICE; MICE, INBRED BALB C; VACCINATION;

EID: 84887149479     PISSN: 17502640     EISSN: 17502659     Source Type: Journal    
DOI: 10.1111/irv.12056     Document Type: Article

References (60)

1. Imai M, Watanabe T, Hatta M et al. Experimental adaptation of an influenza H5 HA confers respiratory droplet transmission to a reassortant H5 HA/H1N1 virus in ferrets. Nature 2012; 486:420-428.
2. Herfst S, Schrauwen EJ, Linster M et al. Airborne transmission of influenza A/H5N1 virus between ferrets. Science 2012; 336:1534-1541.
3. Amorij JP, Hinrichs W, Frijlink HW, Wilschut JC, Huckriede A. Needle-free influenza vaccination. Lancet Infect Dis 2010; 10:699-711.
4. Pulendran B, Ahmed R. Immunological mechanisms of vaccination. Nat Immunol 2011; 12:509-517.
5. Bucy RP, Panoskaltsis-Mortari A, Huang GQ et al. Heterogeneity of single cell cytokine gene expression in clonal T cell populations. J Exp Med 1994; 180:1251-1262.
6. Darrah PA, Patel DT, De Luca PM et al. Multifunctional TH1 cells define a correlate of vaccine-mediated protection against Leishmania major. Nat Med 2007; 13:843-850.
7. Mosmann TR, Coffman RL. TH1 and TH2 cells: different patterns of lymphokine secretion lead to different functional properties. Annu Rev Immunol 1989; 7:145-173.
8. McGeachy MJ, Bak-Jensen KS, Chen Y et al. TGF-beta and IL-6 drive the production of IL-17 and IL-10 by T cells and restrain T(H)-17 cell-mediated pathology. Nat Immunol 2007; 8:1390-1397.
9. Aggarwal S, Ghilardi N, Xie MH, De Sauvage FJ, Gurney AL. Interleukin-23 promotes a distinct CD4 T cell activation state characterized by the production of interleukin-17. J Biol Chem 2003; 278:1910-1914.
10. Esplugues E, Huber S, Gagliani N et al. Control of TH17 cells occurs in the small intestine. Nature 2011; 475:514-518.
11. Bermejo-Martin JF, Ortiz de Lejarazu R, Pumarola T et al. Th1 and Th17 hypercytokinemia as early host response signature in severe pandemic influenza. Crit Care 2009; 13:R201.
12. Crowe CR, Chen K, Pociask DA et al. Critical role of IL-17RA in immunopathology of influenza infection. J Immunol 2009; 183:5301-5310.
13. Hamada H, Garcia-Hernandez Mde L, Reome JB et al. Tc17, a unique subset of CD8 T cells that can protect against lethal influenza challenge. J Immunol 2009; 182:3469-3481.
14. Pedersen G, Major D, Roseby S, Wood J, Madhun AS, Cox RJ. Matrix-M adjuvanted virosomal H5N1 vaccine confers protection against lethal viral challenge in a murine model. Influenza Other Respir Viruses 2011; 5:426-437.
15. Moran TM, Park H, Fernandez-Sesma A, Schulman JL. Th2 responses to inactivated influenza virus can Be converted to Th1 responses and facilitate recovery from heterosubtypic virus infection. J Infect Dis 1999; 180:579-585.
16. Kistner O, Crowe BA, Wodal W et al. A whole virus pandemic influenza H1N1 vaccine is highly immunogenic and protective in active immunization and passive protection mouse models. PLoS ONE 2010; 5:e9349.
17. Hovden AO, Cox RJ, Haaheim LR. Whole influenza virus vaccine is more immunogenic than split influenza virus vaccine and induces primarily an IgG2a response in BALB/c mice. Scand J Immunol 2005; 62:36-44.
18. Bungener L, Geeraedts F, Ter Veer W, Medema J, Wilschut J, Huckriede A. Alum boosts TH2-type antibody responses to whole-inactivated virus influenza vaccine in mice but does not confer superior protection. Vaccine 2008; 26:2350-2359.
19. Huber VC, McKeon RM, Brackin MN et al. Distinct contributions of vaccine-induced immunoglobulin G1 (IgG1) and IgG2a antibodies to protective immunity against influenza. Clin Vaccine Immunol 2006; 13:981-990.
20. Soane RJ, Hinchcliffe M, Davis SS, Illum L. Clearance characteristics of chitosan based formulations in the sheep nasal cavity. Int J Pharm 2001; 217:183-191.
21. Soane RJ, Frier M, Perkins AC, Jones NS, Davis SS, Illum L. Evaluation of the clearance characteristics of bioadhesive systems in humans. Int J Pharm 1999; 178:55-65.
22. Smith J, Wood E, Dornish M. Effect of chitosan on epithelial cell tight junctions. Pharm Res 2004; 21:43-49.
23. Baldrick P. The safety of chitosan as a pharmaceutical excipient. Regul Toxicol Pharmacol 2010; 56:290-299.
24. Svindland SC, Jul-Larsen A, Pathirana R et al. The mucosal and systemic immune responses elicited by a chitosan-adjuvanted intranasal influenza H5N1 vaccine. Influenza Other Respi Viruses 2012; 6:90-100.
25. Burdette DL, Monroe KM, Sotelo-Troha K et al. STING is a direct innate immune sensor of cyclic di-GMP. Nature 2011; 478:515-518.
26. Pedersen GK, Ebensen T, Gjeraker IH et al. Evaluation of the Sublingual Route for Administration of Influenza H5N1 virosomes in combination with the bacterial second messenger c-di-GMP. PLoS ONE 2012; 6:90-100.
27. Madhun AS, Haaheim LR, Nostbakken JK et al. Intranasal c-di-GMP-adjuvanted plant-derived H5 influenza vaccine induces multifunctional Th1 CD4+ cells and strong mucosal and systemic antibody responses in mice. Vaccine 2011; 29:4973-4982.
28. Ebensen T, Schulze K, Riese P, Morr M, Guzman CA. The bacterial second messenger cdiGMP exhibits promising activity as a mucosal adjuvant. Clin Vaccine Immunol 2007; 14:952-958.
29. Karaolis DK, Means TK, Yang D et al. Bacterial c-di-GMP is an immunostimulatory molecule. J Immunol 2007; 178:2171-2181.
30. Burdette DL, Monroe KM, Sotelo-Troha K et al. STING is a direct innate immune sensor of cyclic di-GMP. Nature 2011; 478:515-518.
31. Shang G, Zhu D, Li N et al. Crystal structures of STING protein reveal basis for recognition of cyclic di-GMP. Nat Struct Mol Biol 2012; 19:725-727.
32. Ishikawa H, Ma Z, Barber GN. STING regulates intracellular DNA-mediated, type I interferon-dependent innate immunity. Nature 2009; 461:788-792.
33. Schild GC, Pereira MS, Chakraverty P. Single-radial-hemolysis: a new method for the assay of antibody to influenza haemagglutinin. Applications for diagnosis and seroepidemiologic surveillance of influenza. Bull World Health Organ 1975; 52:43-50.
34. Spearman C. The method of 'right and wrong cases' ('constant stimuli') without Gauss's formula. Brit J Psychol 1908; 2:227-242.
35. Karber G. A contribution to the collective treatment of a pharmacological experimental series. Arch Exp Path Pharmak 1931; 162:480-487.
36. Madhun AS, Haaheim LR, Nilsen MV, Cox RJ. Intramuscular Matrix-M-adjuvanted virosomal H5N1 vaccine induces high frequencies of multifunctional Th1 CD4+ cells and strong antibody responses in mice. Vaccine 2009; 27:7367-7376.
37. Cox RJ, Mykkeltvedt E, Robertson J, Haaheim LR. Non-lethal viral challenge of influenza haemagglutinin and nucleoprotein DNA vaccinated mice results in reduced viral replication. Scand J Immunol 2002; 55:14-23.
38. Roederer M, Nozzi JL, Nason MX. SPICE: exploration and analysis of post-cytometric complex multivariate datasets. Cytometry A 2011; 79:167-174.
39. Nauta JJ, Beyer WE, Osterhaus AD. On the relationship between mean antibody level, seroprotection and clinical protection from influenza. Biologicals 2009; 37:216-221.
40. Zygmunt BM, Rharbaoui F, Groebe L, Guzman CA. Intranasal immunization promotes th17 immune responses. J Immunol 2009; 183:6933-6938.
41. Chen LM, Blixt O, Stevens J et al. In vitro evolution of H5N1 avian influenza virus toward human-type receptor specificity. Virology 2011; 422:105-133.
42. Jefferson T, Di Pietrantonj C, Rivetti A, Bawazeer GA, Al-Ansary LA, Ferroni E. Vaccines for preventing influenza in healthy adults. Cochrane Database Syst Rev 2010; CD001269.
43. Osterholm MT, Kelley NS, Sommer A, Belongia EA. Efficacy and effectiveness of influenza vaccines: a systematic review and meta-analysis. Lancet Infect Dis 2011; 12:36-44.
44. Karron RA, Talaat K, Luke C et al. Evaluation of two live attenuated cold-adapted H5N1 influenza virus vaccines in healthy adults. Vaccine 2009; 27:4953-4960.
45. Mutsch M, Zhou W, Rhodes P et al. Use of the inactivated intranasal influenza vaccine and the risk of Bell's palsy in Switzerland. N Engl J Med 2004; 350:896-903.
46. Mannila J, Jarvinen K, Holappa J, Matilainen L, Auriola S, Jarho P. Cyclodextrins and chitosan derivatives in sublingual delivery of low solubility peptides: a study using cyclosporin A, alpha-cyclodextrin and quaternary chitosan N-betainate. Int J Pharm 2009; 381:19-24.
47. Saint-Lu N, Tourdot S, Razafindratsita A et al. Targeting the allergen to oral dendritic cells with mucoadhesive chitosan particles enhances tolerance induction. Allergy 2009; 64:1003-1013.
48. Li H, Willingham SB, Ting JP, Re F. Cutting edge: inflammasome activation by alum and alum's adjuvant effect are mediated by NLRP3. J Immunol 2008; 181:17-21.
49. Mills KH, Cosgrove C, McNeela EA et al. Protective levels of diphtheria-neutralizing antibody induced in healthy volunteers by unilateral priming-boosting intranasal immunization associated with restricted ipsilateral mucosal secretory immunoglobulin a. Infect Immun 2003; 71:726-732.
50. Read RC, Naylor SC, Potter CW et al. Effective nasal influenza vaccine delivery using chitosan. Vaccine 2005; 23:4367-4374.
51. Tamayo R, Pratt JT, Camilli A. Roles of cyclic diguanylate in the regulation of bacterial pathogenesis. Annu Rev Microbiol 2007; 61:131-148.
52. Karaolis DK, Cheng K, Lipsky M et al. 3′, 5′-Cyclic diguanylic acid (c-di-GMP) inhibits basal and growth factor-stimulated human colon cancer cell proliferation. Biochem Biophys Res Commun 2005; 329:40-45.
53. Ebensen T, Libanova R, Schulze K, Yevsa T, Morr M, Guzman CA. Bis-(3′, 5′)-cyclic dimeric adenosine monophosphate: strong Th1/Th2/Th17 promoting mucosal adjuvant. Vaccine 2011; 29:5210-5220.
54. Baudner BC, Giuliani MM, Verhoef JC, Rappuoli R, Junginger HE, Giudice GD. The concomitant use of the LTK63 mucosal adjuvant and of chitosan-based delivery system enhances the immunogenicity and efficacy of intranasally administered vaccines. Vaccine 2003; 21:3837-3844.
55. Wimer-Mackin S, Hinchcliffe M, Petrie CR et al. An intranasal vaccine targeting both the Bacillus anthracis toxin and bacterium provides protection against aerosol spore challenge in rabbits. Vaccine 2006; 24:3953-3963.
56. Illum L, Farraj NF, Davis SS. Chitosan as a novel nasal delivery system for peptide drugs. Pharm Res 1994; 11:1186-1189.
57. Jaffar Z, Ferrini ME, Herritt LA, Roberts K. Cutting edge: lung mucosal Th17-mediated responses induce polymeric Ig receptor expression by the airway epithelium and elevate secretory IgA levels. J Immunol 2009; 182:4507-4511.
58. Datta SK, Sabet M, Nguyen KP et al. Mucosal adjuvant activity of cholera toxin requires Th17 cells and protects against inhalation anthrax. Proc Natl Acad Sci USA 2010; 107:10638-10643.
59. Seder RA, Darrah PA, Roederer M. T-cell quality in memory and protection: implications for vaccine design. Nat Rev Immunol 2008; 8:247-258.
60. Kannanganat S, Ibegbu C, Chennareddi L, Robinson HL, Amara RR. Multiple-cytokine-producing antiviral CD4 T cells are functionally superior to single-cytokine-producing cells. J Virol 2007; 81:8468-8476.