Mucosal immunization with the Moraxella catarrhalis porin M35 induces enhanced bacterial clearance from the lung: A possible role for opsonophagocytosis

Frontiers in Immunology

Volumn 2, Issue MAY, 2011, Pages

  Easton, Donna M ^a,b   Cripps, Allan W ^a,c   Foxwell, A Ruth ^a   Kyd, Jennelle M ^d  

^a UNIVERSITY OF CANBERRA   (Australia)

^b UNIVERSITY OF QUEENSLAND   (Australia)

^c GRIFFITH UNIVERSITY   (Australia)

^d CENTRAL QUEENSLAND UNIVERSITY   (Australia)

Author keywords

Moraxella catarrhalis; Mucosal immunization; Opsonophagocytosis; Porin; Respiratory tract

Indexed keywords

EID: 84874089214     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2011.00013     Document Type: Article

References (47)

1. Aase, A., Bjune, G., Hoiby, E. A., Rosenqvist, E., Pedersen, A. K., and Michaelsen, T. E. (1995). Comparison among opsonic activity, anti-meningococcal immunoglobulin G response, and serum bactericidal activity against meningococci in sera from vaccines after immunization with a serogroup B outer membrane vesicle vaccine. Infect. Immun. 63, 3531-3536.
2. Armbruster, C. E., Hong, W., Pang, B., Weimer, K. E., Juneau, R. A., Turner, J., and Swords, W. E. (2010). Indirect pathogenicity of Haemophilus influenzae and Moraxella catarrhalis in polymicrobial otitis media occurs via interspecies quorum signaling. MBio 1, e00102-e00110.
3. Bash, M. C., Lesiak, K. B., Banks, S. D., and Frasch, C. E. (1995). Analysis of Neisseria meningitidis class 3 outer membrane protein gene variable regions and type identification using genetic techniques. Infect. Immun. 63, 1484-1490.
4. Buret, A., Dunkley, M. L., Pang, G., Clancy, R. L., and Cripps, A. W. (1994). Pulmonary immunity to Pseudomonas aeruginosa in intestinally immunized rats roles of alveolar macrophages, tumor necrosis factor alpha, and interleukin-1 alpha. Infect. Immun. 62, 5335-5343.
5. Clancy, R., and Dunkley, M. (2011). Acute exacerbations in COPD and their control with oral immunization with non-typeable Haemophilus influenzae. Front. Immun. 2:7. doi: 10.3389/fimmu.2011.00007
6. Daoud, A., Abuekteish, F., and Masaadeh, H. (1996). Neonatal meningitis due to Moraxella catarrhalis and review of the literature. Ann. Trop. Paediatr. 16, 199-201.
7. Delvig, A. A., Michaelsen, T. E., Aase, A., Hoiby, E. A., and Rosen-qvist, E. (1997a). Vaccine-induced IgG antibodies to the linear epi-tope on the PorB outer membrane protein promote opsonophagocy-tosis of Neisseria meningitidis by human neutrophils. Clin. Immunol. Immunopathol. 84, 27-35.
8. Delvig, A. A., Rosenqvist, E., Oftung, F., and Robinson, J. H. (1997b). T-Cell epitope mapping the PorB protein of serogroup B Neisseria meningitidis in B10 congenic strains of mice. Clin. Immunol. Immunopathol. 85, 134-142.
9. Delvig, A. A., Wedege, E., Caugant, D. A., Dalseg, R., Kolberg, J., Acht-man, M., and Rosenqvist, E. (1995). A linear B-cell epitope on the class 3 outer-membrane protein of Neisseria meningitidis recognized after vaccination with the Norwegian group B outer-membrane vesicle vaccine. Microbiology 141 (Pt 7), 1593-1600.
10. Delvig, A. A., Wedege, E., Michaelsen, T. E., Hoiby, E. A., Brandtzaeg, P., and Rosenqvist, E. (1996). Immune responses to linear epitopes on the PorB protein of Neisseria meningitidis in patients with systemic meningococcal disease. Microbiology 142(Pt 9), 2491-2498.
11. Duim, B., Dankert, J., Jansen, H. M., and van Alphen, L. (1993). Genetic analysis of the diversity in outer membrane protein P2 of non-encapsulated Haemophilus influenzae. Microb. Pathog. 14, 451-462.
12. Dunkley, M., Pabst, R., and Cripps, A. (1995). An important role for intestinally derived T cells in respiratory defence. Immunol. Today 16, 231-236.
13. Easton, D. M., Smith, A., Gallego, S. G., Foxwell, A. R., Cripps, A. W., and Kyd, J. M. (2005). Characterization of a novel porin protein from Moraxella catarrhalis and identification of an immunodomi-nant surface loop. J. Bacteriol. 187, 6528-6535.
14. Faden, H., Hong, J. J., and Pahade, N. (1994). Immune response to Moraxella catarrhalis in children with otitis media: opsonophago-cytosis with antigen-coated latex beads. Ann. Otol. Rhinol. Laryngol. 103, 522-524.
15. Foxwell, A. R., Kyd, J. M., and Cripps, A. W. (2001). Programmed inflammatory processes induced by mucosal immunisation. Vaccine 19, 2522-2526.
16. Haase, E. M., Campagnari, A. A., Sarwar, J., Shero, M., Wirth, M., Cumming, C. U., and Murphy, T. F. (1991). Strain-specific and immunodomi-nant surface epitopes of the P2 porin protein of nontypeable Haemophilus influenzae. Infect. Immun. 59, 1278-1284.
17. Hol, C., Verduin, C. M., Van Dijke, E. E., Verhoef, J., Fleer, A., and van Dijk, H. (1995). Complement resistance is a virulence factor of Branhamella (Moraxella) catarrhalis. FEMS Immunol. Med. Microbiol. 11, 207-211.
18. Hu, W. G., Berry, J., Chen, J., and Gu, X. X. (2004). Exploration of Moraxella catarrhalis outer membrane proteins, CD and UspA, as new carriers for lipooligosaccharide-based conjugates. FEMS Immunol. Med. Microbiol. 41, 109-115.
19. Jetter, M., Heiniger, N., Spaniol, V., Troller, R., Schaller, A., and Aebi, C. (2009). Outer membrane porin M35 of Moraxella catarrhalis mediates susceptibility to aminopeni-cillins. BMC Microbiol. 9, 188. doi: 10.1186/471-2180-9-188.
20. Jomaa, M., Yuste, J., Paton, J. C., Jones, C., Dougan, G., and Brown, J. S. (2005a). Antibodies to the iron uptake ABC transporter lipopro-teins PiaA and PiuA promote opsonophagocytosis of Streptococcus pneumoniae. Infect. Immun. 73, 6852-6859.
21. Jomaa, M., Kyd, J. M., and Cripps, A. W. (2005b). Mucosal immunisation with novel Streptococcus pneumoniae protein antigens enhances bacterial clearance in an acute mouse lung infection model. FEMS Immunol. Med. Microbiol. 44, 59-67.
22. Karalus, R., and Campagnari, A. (2000). Moraxella catarrhalis: a review of an important human mucosal pathogen. Microbes Infect. 2, 547-559.
23. Khader, S. A., Gaffen, S. L., and Kolls, J. K. (2009). Th17 cells at the crossroads of innate and adaptive immunity against infectious diseases at the mucosa. Mucosal Immunol. 2, 403-411.
24. Krishnamurthy A., McGrath, J., Cripps, A. W., and Kyd, J. M. (2009). The incidence of Streptococcus pneumoniae otitis media is affected by the polymicrobial environment particularly Moraxella catarrhalis in a mouse nasal colonisation model. Microbes Infect. 11, 545-553.
25. Kyd, J., John, A., Cripps, A., and Murphy, T. F. (1999). Investigation of mucosal immunisation in pulmonary clearance of Moraxella (Branhamella) catarrhalis. Vaccine 18, 398-406.
26. Kyd, J. M., Cripps, A. W., and Murphy, T. F. (1998). Outer-membrane antigen expression by Moraxella (Branhamella) catarrhalis influences pulmonary clearance. J. Med. Microbiol. 47, 159-168.
27. Martinez, J. E., Romero-Steiner, S., Pilishvili, T., Barnard, S., Schinsky, J., Goldblatt, D., and Carlone, G. M. (1999). A flow cytomet-ric opsonophagocytic assay for measurement of functional antibodies elicited after vaccination with the 23-valent pneumo-coccal polysaccharide vaccine. Clin. Diagn. Lab. Immunol. 6, 581-586.
28. Massa, H. M., Cripps, A. W., and Lehmann, D. (2009). Otitis media: viruses, bacteria, biofilms and vaccines. Med. J. Aust. 191, S44-S49.
29. Mawas, F., Ho, M. M., and Corbel, M. J. (2009). Current progress with Moraxella catarrhalis antigens as vaccine candidates. Expert Rev. Vaccines 8, 77-90.
30. Mes, T. H., and van Putten, J. P. (2007). Positively selected codons in immune-exposed loops of the vaccine candidate OMP-P1 of Haemophilus influenzae. J. Mol. Evol. 64, 411-422.
31. Meyer, G. A., Shope, T. R., Waecker, N. J. Jr., and Lanningham, F. H. (1995). Moraxella (Branhamella) catarrhalis bacteremia in children. A report of two patients and review of the literature. Clin. Pediatr. (Phila) 34, 146-150.
32. Murphy, T. F. (1996). Branhamella catarrhalis: epidemiology, surface antigenic structure, and immune response. Microbiol. Rev. 60, 267-279.
33. Murphy, T. F. (2005). Vaccine development for non-typeable Haemophilus influenzae and Moraxella catarrhalis: progress and challenges. Expert Rev. Vaccines 4, 843-853.
34. Murphy, T. F. (2009). Vaccine development for Moraxella catarrhalis: rationale, approaches and challenges. Expert Rev. Vaccines 8, 655-658.
35. Murphy, T. F., Kirkham, C., Liu, D. E, and Sethi, S. (2003). Human immune response to outer membrane protein CD of Moraxella catarrhalis in adults with chronic obstructive pulmonary disease. Infect. Immun. 71, 1288-1294.
36. Murphy, T. F., Kyd, J. M., John, A., Kirkham, C., and Cripps, A. W. (1998). Enhancement of pulmonary clearance of Moraxella (Branhamella) catarrhalis following immunization with outer membrane protein CD in a mouse model. J. Infect. Dis. 178, 1667-1675.
37. Novotny, L. A., and Bakaletz, L. O. (2003). The fourth surface-exposed region of the outer membrane protein P5-homologous adhesin of nontypable Haemophilus influenzae is an immunodominant but nonpro-tective decoying epitope. J. Immunol. 171, 1978-1983.
38. Otczyk, D. C., and Cripps, A. W. (2010). Mucosal immunization: A realistic alternative. Hum. Vaccin. 6, 978-1006.
39. Schirmer, T. (1998). General and specific porins from bacterial outer membranes. J. Struct. Biol. 121, 101-109.
40. Seshadri, K., Garemyr, R., Wallin, E., von Heijne, G., and Elofsson, A. (1998). Architecture of beta-barrel membrane proteins: analysis of trimeric porins. Protein Sci. 7, 2026-2032.
41. Tan, T. T., Christensen, J. J., Dziegiel, M. H., Forsgren, A., and Ries-beck, K. (2006). Comparison of the serological responses to Moraxella catarrhalis immunoglob-ulin D-binding outer membrane protein and the ubiquitous surface proteins A1 and A2. Infect. Immun. 74, 6377-6386.
42. Verduin, C. M., Hol, C., Fleer, A., van Dijk, H., and van Belkum, A. (2002). Moraxella catarrhalis: from emerging to established pathogen. Clin. Microbiol. Rev. 15, 125-144.
43. Verduin, C. M., Hol, C., Van Dijke, E., Faber, J. A., Jansze, M., Verhoef, J., andVanDijk, H. (1995). Assessment of complement-mediated killing of Moraxella (Branhamella) catarrhalis isolates by a simple method. Clin. Diagn. Lab. Immunol. 2, 365-368.
44. Watanabe, Y. (2002). Characterization of the refolding and reassembly of an integral membrane protein OmpF porin by low-angle laser light scattering photometry coupled with high-performance gel chro-matography. J. Chromatogr. A 961, 137-146.
45. Williams, K. M., Bigley, E. C. III, and Raybourne, R. B. (2000). Identification of murine B-cell and T-cell epitopes of Escherichia coli outer membrane protein F with synthetic polypeptides. Infect. Immun. 68, 2535-2545.
46. Yamashita, E., Zhalnina, M. V., Zakharov, S. D., Sharma, O., and Cramer, W A. (2008). Crystal structures of the OmpF porin: function in a colicin translocon. EMBO J. 27, 2171-2180.
47. Yi, K., and Murphy, T. F. (1997). Importance of an immunodomi-nant surface-exposed loop on outer membrane protein P2 of non-typeable Haemophilus influenzae. Infect. Immun. 65, 150-155.