Immunization of young African green monkeys with OprF epitope 8-OprI-type A- and B-flagellin fusion proteins promotes the production of protective antibodies against nonmucoid Pseudomonas aeruginosa

Vaccine

Volumn 27, Issue 48, 2009, Pages 6762-6769

  Weimer, Eric T ^a   Ervin, Sean E ^a   Wozniak, Daniel J ^b   Mizel, Steven B ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

^b THE OHIO STATE UNIVERSITY WEXNER MEDICAL CENTER   (United States)

Author keywords

Flagellin; Nonhuman primates; Pseudomonas aeruginosa; Vaccine

Indexed keywords

ANTIGEN; COMPLEMENT COMPONENT C3; FLAGELLIN ANTIBODY; HYBRID PROTEIN; IMMUNOGLOBULIN G; IMMUNOGLOBULIN G ANTIBODY; OPRF EPITOPE 8; OPRF PROTEIN[311-341]; OPRI A FLAGELLIN FUSION PROTEIN; OPRI ANTIBODY; OPRI B FLAGELLIN FUSION PROTEIN; UNCLASSIFIED DRUG;

ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY PRODUCTION; ANTIBODY RESPONSE; ARTICLE; CERCOPITHECIDAE; CLINICAL EVALUATION; COMPARATIVE STUDY; CONTROLLED STUDY; FEMALE; LUNG; NEWBORN; NONHUMAN; PASSIVE IMMUNIZATION; PLASMA; PRIMATE; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTION;

ANIMALS; ANTIBODIES, BACTERIAL; ANTIBODY SPECIFICITY; BACTERIAL PROTEINS; CERCOPITHECUS AETHIOPS; COMPLEMENT ACTIVATION; COMPLEMENT C3; FEMALE; FLAGELLIN; IMMUNITY, HUMORAL; IMMUNOGLOBULIN G; LIPOPROTEINS; LUNG; MICE; MICE, INBRED BALB C; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; PSEUDOMONAS VACCINES; RECOMBINANT FUSION PROTEINS;

EID: 70350564882     PISSN: 0264410X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.vaccine.2009.08.080     Document Type: Article

References (58)

1. Burns J.L., Gibson R.L., McNamara S., Yim D., Emerson J., Rosenfeld M., et al. Longitudinal assessment of Pseudomonas aeruginosa in young children with cystic fibrosis. J Infect Dis 183 3 (2001) 444-452
2. Li Z., Kosorok M.R., Farrell P.M., Laxova A., West S.E., Green C.G., et al. Longitudinal development of mucoid Pseudomonas aeruginosa infection and lung disease progression in children with cystic fibrosis. JAMA 293 5 (2005) 581-588
3. Tosi M.F., Zakem-Cloud H., Demko C.A., Schreiber J.R., Stern R.C., Konstan M.W., et al. Cross-sectional and longitudinal studies of naturally occurring antibodies to Pseudomonas aeruginosa in cystic fibrosis indicate absence of antibody-mediated protection and decline in opsonic quality after infection. J Infect Dis 172 2 (1995) 453-461
4. Koch C. Early infection and progression of cystic fibrosis lung disease. Pediatr Pulmonol 34 3 (2002) 232-236
5. Doring G., Meisner C., Stern M., and Flagella Vaccine Trial Study Group. A double-blind randomized placebo-controlled phase III study of a Pseudomonas aeruginosa flagella vaccine in cystic fibrosis patients. PNAS 104 26 (2007) 11020-11025
6. Sorichter S., Baumann U., Baumgart A., Walterspacher S., and von Specht B.U. Immune responses in the airways by nasal vaccination with systemic boosting against Pseudomonas aeruginosa in chronic lung disease. Vaccine 27 21 (2009) 2755-2759
7. Cryz Jr. S.J., Lang A., Rudeberg A., Wedgewood J., Que J.U., Furer E., et al. Immunization of cystic fibrosis patients with a Pseudomonas aeruginosa O-polysaccharide-toxin A conjugate vaccine. Behring Inst Mitt 98 (1997) 345-349
8. Lang A.B., Rudeberg A., Schoni M.H., Que J.U., Furer E., and Schaad U.B. Vaccination of cystic fibrosis patients against Pseudomonas aeruginosa reduces the proportion of patients infected and delays time to infection. Pediatr Infect Dis J 23 6 (2004) 504-510
9. Langford D.T., and Hiller J. Prospective, controlled study of a polyvalent pseudomonas vaccine in cystic fibrosis-three year results. Arch Dis Child 59 12 (1984) 1131-1134
10. Zuercher A.W., Horn M.P., Que J.U., Ruedeberg A., Schoeni M.H., Schaad U.B., et al. Antibody responses induced by long-term vaccination with an octovalent conjugate Pseudomonas aeruginosa vaccine in children with cystic fibrosis. FEMS Immunol Med Microbiol 47 2 (2006) 302-308
11. Liu P.V., and Wang S. Three new major somatic antigens of Pseudomonas aeruginosa. J Clin Microbiol 28 5 (1990) 922-925
12. DiGiandomenico A., Rao J., Harcher K., Zaid T.S., Gardner J., Neely A.N., et al. Intranasal immunization with heterologously expressed polysaccharide protects against multiple Pseudomonas aeruginosa infections. PNAS 104 11 (2007) 4624-4629
13. Finke M., Duchene M., Eckhardt A., Domdey H., and von Specht B.U. Protection against experimental Pseudomonas aeruginosa infection by recombinant P. aeruginosa lipoprotein I expressed in Escherichia coli. Infect Immun 58 7 (1990) 2241-2244
14. Arnold H., Bumann D., Felies M., Gewecke B., Sorensen M., Gessner J.E., et al. Enhanced immunogenicity in the murine airway mucosa with an attenuated Salmonella live vaccine expressing OprF-OprI from Pseudomonas aeruginosa. Infect Immun 72 11 (2004) 6546-6553
15. Mansouri E., Gabelsberger J., Knapp B., Hundt E., Lenz U., Hungerer K.D., et al. Safety and immunogenicity of a Pseudomonas aeruginosa hybrid outer membrane protein F-I vaccine in human volunteers. Infect Immun 67 3 (1999) 1461-1470
16. Weimer E.T., Lu H., Kock N.D., Wozniak D.J., and Mizel S.B. A fusion protein vaccine containing OprF epitope 8, OprI, and type A and B flagellin promotes enhanced clearance of nonmucoid Pseudomonas aeruginosa. Infect Immun 77 6 (2009) 2356-2366
17. Knapp B., Hundt E., Lenz U., Hungerer K.D., Gabelsberger J., Domdey H., et al. A recombinant hybrid outer membrane protein for vaccination against Pseudomonas aeruginosa. Vaccine 17 13-14 (1999) 1663-1666
18. Mansouri E., Blome-Eberwein S., Gabelsberger J., Germann G., and von Specht B.U. Clinical study to assess the immunogenicity and safety of a recombinant Pseudomonas aeruginosa OprF-OprI vaccine in burn patients. FEMS Immunol Med Microbiol 37 2-3 (2003) 161-166
19. Worgall S., Krause A., Qiu J., Joh J., Hackett N.R., and Crystal R.G. Protective immunity to Pseudomonas aeruginosa induced with a capsid-modified adenovirus expressing P. aeruginosa OprF. J Virol 81 24 (2007) 13801-13808
20. Worgall S., Krause A., Rivara M., Joh J., Hackett N.R., and Crystal R.G. Protection against P. aeruginosa with an adenovirus vector containing an OprF epitope in the capsid. J Clin Invest 115 5 (2005) 1281-1289
21. Eckhardt A., Heiss M.M., Ehret W., Permanetter W., Duchene M., Domdey H., et al. Evaluation of protective mAbs against Pseudomonas aeruginosa outer membrane protein I by C1q binding assay. Zentralbl Bakteriol 275 1 (1991) 100-111
22. Pier G.B., Saunders J.M., Ames P., Edwards M.S., Auerbach H., Goldfarb J., et al. Opsonophagocytic killing antibody to Pseudomonas aeruginosa mucoid exopolysaccharide in older noncolonized patients with cystic fibrosis. N Engl J Med 317 13 (1987) 793-798
23. Pollack M., Koles N.L., Preston M.J., Brown B.J., and Pier G.B. Functional properties of isotype-switched immunoglobulin M (IgM) and IgG monoclonal antibodies to Pseudomonas aeruginosa lipopolysaccharide. Infect Immun 63 11 (1995) 4481-4488
24. von Specht B.U., Christian Lucking H., Blum B., Schmitt A., Dieter Hungerer K., and Domdey H. Safety and immunogenicity of a Pseudomonas aeruginosa outer membrane protein I vaccine in human volunteers. Vaccine 14 12 (1996) 1111-1117
25. Eichler I., Joris L., Hsu Y.P., Van Wye J., Bram R., and Moss R. Nonopsonic antibodies in cystic fibrosis. Pseudomonas aeruginosa lipopolysaccharide-specific immunoglobulin G antibodies from infected patient sera inhibit neutrophil oxidative responses. J Clin Invest 84 6 (1989) 1794-1804
26. Moss R.B., Hsu Y.P., Sullivan M.M., and Lewiston N.J. Altered antibody isotype in cystic fibrosis: possible role in opsonic deficiency. Pediatr Res 20 5 (1986) 453-459
27. Bates J.T., Honko A.N., Graff A.H., Kock N.D., and Mizel S.B. Mucosal adjuvant activity of flagellin in aged mice. Mech Ageing Dev 129 5 (2008) 271-281
28. Honko A.N., Sriranganathan N., Lees C.J., and Mizel S.B. Flagellin is an effective adjuvant for immunization against lethal respiratory challenge with Yersinia pestis. Infect Immun 74 2 (2006) 1113-1120
29. Mizel S.B., Graff A.H., and Sriranganathan N. A fusion protein, flagellin/F1/V, is an effective plague vaccine in mice and two species of nonhuman primates. ClinVaccine Immunol (2008) CVI
30. Pino O., Martin M., and Michalek S.M. Cellular mechanisms of the adjuvant activity of the flagellin component FljB of Salmonella enterica Serovar Typhimurium to potentiate mucosal and systemic responses. Infect Immun 73 10 (2005) 6763-6770
31. Cuadros C., Lopez-Hernandez F.J., Dominguez A.L., McClelland M., and Lustgarten J. Flagellin fusion proteins as adjuvants or vaccines induce specific immune responses. Infect Immun 72 5 (2004) 2810-2816
32. Cunningham A.F., Khan M., Ball J., Toellner K.M., Serre K., Mohr E., et al. Responses to the soluble flagellar protein FliC are Th2, while those to FliC on Salmonella are Th1. Eur J Immunol 34 11 (2004) 2986-2995
33. McDonald W.F., Huleatt J.W., Foellmer H.G., Hewitt D., Tang J., Desai P., et al. A West Nile virus recombinant protein vaccine that coactivates innate and adaptive immunity. J Infect Dis 195 11 (2007) 1607-1617
34. McEwen J., Levi R., Horwitz R.J., and Arnon R. Synthetic recombinant vaccine expressing influenza haemagglutinin epitope in Salmonella flagellin leads to partial protection in mice. Vaccine 10 6 (1992) 405-411
35. McSorley S.J., Ehst B.D., Yu Y., and Gewirtz A.T. Bacterial flagellin is an effective adjuvant for CD4+ T cells in vivo. J Immunol 169 7 (2002) 3914-3919
36. Schwarz K., Storni T., Manolova V., Didlerlaurent A., Sirard J.C., Rothlisberger P., et al. Role of toll-like receptors in costimulating cytotoxic T cell responses. Eur J Immunol 33 6 (2003) 1465-1470
37. Strindelius L., Filler M., and Sjoholm I. Mucosal immunization with purified flagellin from Salmonella induces systemic and mucosal immune responses in C3H/HeJ mice. Vaccine 22 27-28 (2004) 3797-3808
38. Honko A.N., and Mizel S.B. Mucosal administration of flagellin induces innate immunity in the mouse lung. Infect Immun 72 11 (2004) 6676-6679
39. Ben Yedidia T., Tarrab-Hazdai R., Schechtman D., and Arnon R. Intranasal administration of synthetic recombinant peptide-based vaccine protects mice from infection by Schistosoma mansoni. Infect. Immun. 67 9 (1999) 4360-4366
40. Huleatt J.W., Jacobs A.R., Tang J., Desai P., Kopp E.D., Huang Y., et al. Vaccination with recombinant fusion proteins incorporating Toll-like receptor ligands induces rapid cellular and humoral immunity. Vaccine 25 4 (2007) 763-775
41. Drenkard E., and Ausubel F.M. Pseudomonas biofilm formation and antibiotic resistance are linked to phenotypic variation. Nature 416 6882 (2002) 740-743
42. Friedman L., and Kolter R. Two genetic loci produce distinct carbohydrate-rich structural components of the Pseudomonas aeruginosa biofilm matrix. J Bacteriol 186 14 (2004) 4457-4465
43. Hoiby N. Understanding bacterial biofilms in patients with cystic fibrosis: current and innovative approaches to potential therapies. J Cyst Fibros 1 4 (2002) 249-254
44. Meluleni G.J., Grout M., Evans D.J., and Pier G.B. Mucoid Pseudomonas aeruginosa growing in a biofilm in vitro are killed by opsonic antibodies to the mucoid exopolysaccharide capsule but not by antibodies produced during chronic lung infection in cystic fibrosis patients. J Immunol 155 4 (1995) 2029-2038
45. Abman S.H., Ogle J.W., Harbeck R.J., Butler-Simon N., Hammond K.B., and Accurso F.J. Early bacteriologic, immunologic, and clinical courses of young infants with cystic fibrosis identified by neonatal screening. J Pediatr 119 2 (1991) 211-217
46. Toder D.S. Gene replacement in Pseudomonas aeruginosa. Methods Enzymol 235 (1994) 466-474
47. Macdonald R.A., Hosking C.S., and Jones C.L. The measurement of relative antibody affinity by ELISA using thiocyanate elution. J Immunol Methods 106 2 (1988) 191-194
48. Tam M., Jackson Snipes G., and Stevenson M.M. Characterization of chronic bronchopulmonary Pseudomonas aeruginosa infection in resistant and susceptible inbred mouse strains. Am J Respir Cell Mol Biol 20 4 (1999) 710-719
49. Worgall S., Kikuchi T., Singh R., Martushova K., Lande L., and Crystal R.G. Protection against pulmonary infection with Pseudomonas aeruginosa following immunization with P. aeruginosa-pulsed dendritic cells. Infect Immun 69 7 (2001) 4521-4527
50. Garrett E.S., Perlegas D., and Wozniak D.J. Negative control of flagellum synthesis in Pseudomonas aeruginosa is modulated by the alternative sigma factor AlgT (AlgU). J Bacteriol 181 23 (1999) 7401-7404
51. Pennington J.E., Reynolds H.Y., Wood R.E., Robinson R.A., and Levine A.S. Use of a Pseudomonas aeruginosa vaccine in patients with acute leukemia and cystic fibrosis. Am J Med 58 5 (1975) 629-636
52. Wood R.E., Pennington J.E., and Reynolds H.Y. Intranasal administration of a Pseudomonas lipopolysaccharide vaccine in cystic fibrosis patients. Pediatr Infect Dis 2 5 (1983) 367-369
53. Zuercher A.W., Horn M.P., Wu H., Song Z., bundgaard C.J., Johansen H.K., et al. Intranasal immunisation with conjugate vaccine protects mice from systemic and respiratory tract infection with Pseudomonas aeruginosa. Vaccine 24 20 (2006) 4333-4342
54. Heijerman H. Infection and inflammation in cystic fibrosis: a short review. J Cyst Fibros 4 Suppl. 2 (2005) 3-5
55. Costerton J.W. Cystic fibrosis pathogenesis and the role of biofilms in persistent infection. Trends Microbiol 9 2 (2001) 50-52
56. Govan J.R., and Deretic V. Microbial pathogenesis in cystic fibrosis: mucoid Pseudomonas aeruginosa and Burkholderia cepacia. Microbiol Rev 60 3 (1996) 539-574
57. Chmiel J., Berger M., and Konstan M. The role of inflammation in the pathophysiology of CF lung disease. Clin Rev Allergy Immunol 23 1 (2002) 5-27
58. Bates J.T., Uematsu S., Akira S., and Mizel S.B. J Immunol 182 12 (2009) 7539-7547