Protection against development of otitis media induced by nontypeable Haemophilus influenzae by both active and passive immunization in a chinchilla model of virus-bacterium superinfection

Infection and Immunity

Volumn 67, Issue 6, 1999, Pages 2746-2762

  Bakaletz, Lauren O ^a,c   Kennedy, Bobbie Jo ^a   Novotny, Laura A ^a   Duquesne, Guy ^b   Cohen, Joe ^b   Lobet, Yves ^b  

^a OHIO STATE UNIVERSITY   (United States)

^b GLAXOSMITHKLINE BIOLOGICALS   (Belgium)

^c THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALUMINUM POTASSIUM SULFATE; ANTIGEN; CHIMERIC PROTEIN; FIBRIN; FREUND ADJUVANT; LIPOPROTEIN; MEMBRANE PROTEIN; PHOSPHORYL LIPID A;

ACTIVE IMMUNIZATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY TITER; ARTICLE; BACTERIAL COLONIZATION; CHINCHILLA; DISEASE SEVERITY; HAEMOPHILUS INFLUENZAE; IMMUNOBLOTTING; INTRANASAL DRUG ADMINISTRATION; NONHUMAN; OTITIS MEDIA; PASSIVE IMMUNIZATION; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SUPERINFECTION;

EID: 0033021078     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/iai.67.6.2746-2762.1999     Document Type: Article

References (75)

1. Akkoyunlu, M., and A. Forsgren. 1996. Local and systemic antibody levels against protein D of Haemophilus influenzae following immunization and infection in rats. APMIS 104:709-717.
2. Akkoyunlu, M., H. Janson, M. Ruan, and A. Forsgren. 1996. Biological activity of serum antibodies to a nonacylated form of lipoprotein D of Haemophilus influenzae. Infect. Immun. 64:4586-4592.
3. Akkoyunlu, M., A. Melhus, C. Capiau, O. Van Opstal, and A. Forsgren. 1997. The acylated form of protein D of Haemophilus influenzae is more immunogenic than the nonacylated form and elicits an adjuvant effect when it is used as a carrier conjugated to polyribosyl ribitol phosphate. Infect. Immun. 65:5010-5016.
4. Akkoyunlu, M., M. Ruan, and A. Forsgren. 1991. Distribution of protein D and immunoglobulin D-binding protein, in Haemophilus strains. Infect. Immun. 59:1231-1238.
5. Bakaletz, L. O., and S. J. Barenkamp. 1994. Localization of high molecular weight adhesion proteins of nontypable Haemophilus influenzae by immunoelectron microscopy. Infect. Immun. 62:4460-4468.
6. Bakaletz, L. O., R. L. Daniels, and D. J. Lim. 1993. Modeling adenovirus type 1-induced otitis media in the chinchilla: effect on ciliary activity and fluid transport function of eustachian tube mucosal epithelium. J. Infect. Dis. 168:865-872.
7. Bakaletz, L. O., and K. A. Holmes. 1997. Evidence for transudation of specific antibody into the middle ears of parenterally immunized chinchillas after an upper respiratory tract infection with adenovirus. Clin Diagn. Lab. Immunol. 4:223-225.
8. Bakaletz, L. O., E. R. Leake, J. M. Billy, and P. T. P. Kaumaya. 1997. Relative immunogenicity and efficacy of two synthetic chimeric peptides of flimbrin as vaccinogens against nasopharyngeal colonization by nontypeable Haemophilus influenzae in the chinchilla. Vaccine 15:955-961.
9. Bakaletz, L. O., D. M. Murwin, and J. M. Billy. 1995. Adenovirus serotype 1 does not act synergistically with Moraxella (Branhamella) catarrhalis to induce otitis media in the chinchilla. Infect. Immun. 63:4188-4190.
10. Bakaletz, L. O., B. M. Tallan, W. J. Andrzejewski, T. F. DeMaria, and D. J. Lim. 1989. Immunological responsiveness of chinchillas to outer membrane and isolated fimbrial proteins of nontypable Haemophilus influenzae. Infect. Immun. 57:3226-3229.
11. Bakaletz, L. O., B. M. Tallan, T. Hoepf, T. F. DeMaria, H. G. Birck, and D. J. Lim. 1988. Frequency of fimbriation of nontypable Haemophilus influenzae and its ability to adhere to chinchilla and human respiratory epithelium. Infect. Immun. 56:331-335.
12. Barenkamp, S. J. 1986. Protection by serum antibodies in experimental nontypeable Haemophilus influenzae otitis media. Infect. Immun. 52:572-580.
13. Barenkamp, S. J. 1996. Immunization with high-molecular-weight adhesion proteins of nontypeable Haemophilus influenzae modifies experimental otitis media in chinchillas. Infect. Immun. 64:1246-1251.
14. Bernstein, J. M., P. M. Bronson, and M. E. Wilson. 1997. Immunoglobulin G subclass response to major outer membrane proteins of nontypeable Haemophilus influenzae in children with acute otitis media. Otolaryngol. Head Neck Surg. 116:363-371.
15. Bernstein, J. M., H. S. Faden, and P. L. Ogra. 1991. Nasopharyngeal colonization by nontypeable Haemophilus influenzae in children: the effect of serum bactericidal antibody. Otolaryngol. Head Neck Surg. 105:406-410.
16. Bernstein, J. M., F. F. Howard, D. M. Dryja, and J. Wactawski-Wende. 1993. Micro-ecology of the nasopharyngeal bacterial flora in otitis-prone and non-otitis-prone children. Acta Otolaryngol. 113:88-92.
17. DeMaria, T. F., M. A. Apicella, W. A. Nichols, and E. R. Leake. 1997. Evaluation of the virulence of nontypeable Haemophilus influenzae lipooligosaccharide htrB and rfaD mutants in the chinchilla model of otitis media. Infect. Immun. 65:4431-4435.
18. DeMaria, T. F., D. M. Murwin, and E. R. Leake. 1996. Immunization with outer membrane protein P6 from nontypeable Haemophilia influenzae induces bactericidal antibody and affords protection in the chinchilla model of otitis media. Infect. Immun. 64:5187-5192.
19. De Mot, R., and J. Vanderleyden. 1994. The C-terminal sequence conservation between OmpA-related outer membrane proteins and MotB suggests a common function in both Gram-positive and Gram-negative bacteria, possibly the interaction of these domains with peptidoglycan. Mol. Microbiol. 12:333-334.
20. Dulm, B., L. D. Bowler, P. P. Eijk, H. M. Jansen, J. Dankert, and L. van Alphen. 1997. Molecular variation in the major outer membrane protein P5 gene of nonencapsulated Haemophilus influenzae during chronic infections. Infect. Immun. 65:1351-1356.
21. Dulm, B., P. Ruiter, L. D. Bowler, J. Dankert, and L. van Alphen. 1997. Sequence variation in the hpd gene of nonencapsulated Haemophilus influenzae isolated from patients with chronic bronchitis. Gene 191:57-60.
22. Faden, H., J. Bernstein, L. Brodsky, J. Stanievich, D. Krystofik, C. Shuff, J. J. Hong, and P. L. Ogra. 1989. Otitis media in children. The systemic immune response to nontypeable Haemophilus influenzae. J. Infect. Dis. 160:999-1004.
23. Freijd, A., S. Bygdeman, and B. Rynnel-Dagöö. 1984. The nasopharyngeal microflora of otitis-prone children, with emphasis on H. influenzae. Acta Otolaryngol. 97:117-126.
24. Giebink, G. S., K. A. Heller, and E. R. Harford. 1982. Tympanometric configurations and middle ear findings in experimental otitis media. Ann. Otol. Rhinol. Laryngol. 91:20-24.
25. Gomez-Duarte, O. G., M. Dehio, C. A. Guzman, G. S. Chhatwal, C. Dehio, and T. F. Meyer. 1997. Binding of vitronectin to opa-expressing Neisseria gonorrhoeae mediates invasion of HeLa cells. Infect. Immun. 65:3857-3866.
26. Green, B. A., M. E. Vazquez, G. W. Zlotnick, G. Quigley-Reape, J. D. Swarts, I. Green, J. L. Cowell, C. D. Bluestone, and W. J. Doyle. 1993. Evaluation of mixtures of purified Haemophilus influenzae outer membrane proteins in protection against challenge with nontypeable H. influenzae in the chinchilla otitis media model. Infect. Immun. 61:1950-1957.
27. Gross, M., and R. W. Sweet. 1985. Purification and characterization of human H-ras proteins expressed in Escherichia coli. Mol. Cell. Biol. 5:1015-1024.
28. Gu, X. X., J. Sun, S. Jin, S. J. Barenkamp, D. J. Lim, J. B. Robbins, and J. Battey. 1997. Detoxified lipooligosaccharide from nontypeable Haemophilus influenzae conjugated to proteins confers protection against otitis media in chinchillas. Infect. Immun. 65:4488-4493.
29. Gu, X. X., C. M. Tsai, T. Ueyama, S. J. Barenkamp, J. B. Robbins, and D. J. Lim. 1996. Synthesis, characterization, and immunologic properties of detoxified lipooligosaccharide from nontypeable Haemophilus influenzae conjugated to proteins. Infect. Immun. 64:4047-4053.
30. Haase, E. M., A. A. Campagnari, J. Sarwar, M. Shero, M. Wirth, C. U. Cumming, and T. Murphy. 1991. Strain-specific and immunodominant surface epitopes of the P2 porin protein of nontypeable Haemophilus influenzae. Infect. Immun. 59:1278-1284.
31. Hotomi, M., T. Saito, and N. Yamanaka. 1998. Specific mucosal immunity and enhanced nasopharyngeal clearance of nontypeable Haemophilus influenzae after intranasal immunization with outer membrane protein P6 and cholera toxin. Vaccine 16:1950-1956.
32. Janson, H., L. O. Hedén, and A. Forsgren. 1992. Protein D, the immunoglobulin D-binding protein of Haemophilus influenzae, is a lipoprotein. Infect. Immun. 60:1336-1342.
33. Janson, H., L. O. Hedén, A. Grubb, M. Ruan, and A. Forsgren. 1991. Protein D and immunoglobulin D-binding protein of Haemophilus influenzae: cloning, nucleotide sequence, and expression in Escherichia coli. Infect. Immun. 59:119-125.
34. Janson, H., A. Melhus, A. Hermansson, and A. Forsgren. 1994. Protein D, the glycerophosphodiester phosphodiesterase from Haemophilus influenzae with affinity for human immunoglobulin D, influences virulence in a rat otitis model. Infect. Immun. 62:4848-4854.
35. Janson, H., M. Ruan, and A. Forsgren. 1993. Limited diversity of the protein D gene (hpd) among encapsulated and nonencapsulated Haemophilus influenzae strains. Infect. Immun. 61:4546-4552.
36. Jiang, Z., N. Nagata, E. Molina, L. O. Bakaletz, H. Hawkins, and J. A. Patel. 1999. Fimbriae-mediated enhanced attachment of nontypeable Haemophilus influenzae to respiratory syncytial virus-infected respiratory epithelial cells. Infect. Immun. 67:187-192.
37. Karasic, R. B., D. J. Beste, S. C. M. To, W. J. Doyle, S. W. Wood, M. J. Carter, A. C. C. To, and C. C. Brinton. 1989. Evaluation of pilus vaccines for prevention of experimental otitis media caused by nontypeable Haemophilus influenzae. Pediatr. Infect. Dis. J. 8:S062-S065.
38. 4, p. 883-885. In J. A. Smith and J. E. Rivier (ed.), Peptides: chemistry and biology. ESCOM, Leiden, The Netherlands.
39. Kaumaya, P. T. P., S. Kobs-Conrad, Y. H. Seo, H. Lee, A. M. VanBuskirk, N. Feng, J. F. Sheridan, and V. Stevens. 1993. Peptide vaccines incorporating a "promiscuous" T-cell epitope bypass certain haplotype restricted immune responses and provide broad spectrum immunogenicity. J. Mol. Recognit. 6:81-94.
40. Kobs-Conrad, S., A. Gerdau, and P. T. P. Kaumaya. 1992. Multivalent B-cell and T-cell epitope vaccine design, p. 886-888. In J. A. Smith and J. E. Rivier (ed.), Peptides: chemistry and biology. ESCOM, Leiden, The Netherlands.
41. Kyd, J. M., and A. W. Cripps. 1996. Modulation of antigen-specific T and B cell responses influence bacterial clearance of nontypeable Haemophilus influenzae from the lung in a rat model. Vaccine 14:1471-1478.
42. Kyd, J. M., M. L. Dunkley, and A. W. Cripps. 1995. Enhanced respiratory clearance of nontypeable Haemophilus influenzae following mucosal immunization with P6 in a rat model. Infect. Immun. 63:2931-2940.
43. Lairmore, M. D., A. M. Di George, S. F. Conrad, A. V. Trevino, R. B. Lal, and P. T. P. Kaumaya. 1995. Human T-lymphotropic virus type 1 peptides in chimeric and multivalent constructs with promiscuous T-cell epitopes enhance immunogenicity and overcome genetic restriction. J. Virol. 69:6077-6089.
44. Loosmore, S. M., Y. P. Yang, R. Oomen, J. M. Shortreed, D. C. Coleman, and M. H. Klein. 1998. The Haemophilus influenzae HtrA protein is a protective antigen. Infect. Immun. 66:899-906.
45. Margolis, R. H., L. L. Hunter, J. R. Rykken, and G. S. Giebink. 1993. Effects of otitis media on extended high-frequency hearing in children. Ann. Otol. Rhinol. Laryngol. 102:1-5.
46. Miyamoto, N., and L. O. Bakaletz. 1996. Selective adherence of nontypeable Haemophilus influenzae (NTHi) to mucus or epithelial cells in the chinchilla eustachian tube and middle ear. Microb. Pathog. 21:343-356.
47. Miyamoto, N., and L. O. Bakaletz. 1997. Kinetics of the ascension of NTHi from the nasopharynx to the middle ear coincident with adenovirus-induced compromise in the chinchilla. Microb. Pathog. 23:119-126.
48. Morona, R., M. Klose, and U. Henning. 1984. Escherichia coti K-12 outer membrane protein (OmpA) as a bacteriophage receptor: analysis of mutant genes expressing altered proteins. J. Bacteriol. 159:570-578.
49. Mott, J. E., and R. A. Grant. 1985. Maximizing gene expression from plasmid vectors containing the lambda PL promoter: strategies for overproducing transcription termination factor rho. Proc. Natl. Acad. Sci. USA 82:88-92.
50. Movva, N. R., K. Nakamura, and M. Inouye. 1980. Gene structure of the OmpA protein, a major surface protein of Escherichia coll required for cell-cell interaction. J. Mol. Biol. 143:317-328.
51. Munson, R. S., Jr., S. Grass, and R. West. 1993. Molecular cloning and sequence of the gene for outer membrane protein P5 of Haemophilus influenzae. Infect. Immun. 61:4017-4020.
52. Munson, R. S., Jr., and K. Sasaki. 1993. Protein D, a putative immunoglobulin D-binding protein produced by Haemophilus influenzae, is glycerophosphodiester phosphodiesterase. J. Bacteriol. 175:4569-4571.
53. Pelton, S. I., G. Bolduc, S. Guiati, Y. Liu, and P. A. Rice. 1990. Protection from experimental otitis media in chinchillas due to nontypeable Haemophilus influenzae following immunization with outer membrane protein 1 (P1), abstr. 610, p. 188. In Program and abstracts of the 30th Interscience Conference on Antimicrobial Agents and Chemotherapy. American Society for Microbiology, Washington, D.C.
54. Perkins, A., H. Jonsdottir, H. Briem, E. Griffiths, D. Plikaytis, and E. A. Hoiby. 1998. Immunogenicity of two efficacious outer membrane protein-based serogroup meningococcal vaccines among young adults in Iceland. J. Infect. Dis. 177:683-691.
55. Prasadarao, N. V., C. A. Wass, and K. S. Kim. 1996. Endothelial cell GlcNAc-β-14GlcNac epitopes for outer membrane protein A enhance traversal of Escherichia coli across the blood-brain barrier. Infect. Immun. 64:154-160.
56. Prasadarao, N. V., C. A. Wass, J. N. Weiser, M. F. Stins, S. H. Huang, and K. S. Kim. 1996. Outer membrane protein A of Escherichia coli contributes to invasion of brain microvascular endothelial cells. Infect. Immun. 64:146-153.
57. Reddy, M. S., J. M. Bernstein, T. F. Murphy, and H. S. Faden. 1996. Binding between outer membrane proteins of nontypeable Haemophilus influenzae and human nasopharyngeal mucin. Infect. Immun. 64:1477-1479.
58. Reddy, M. S., T. F. Murphy, H. S. Faden, and J. M. Bernstein. 1997. Middle ear mucin glycoprotein: purification and interaction with nontypeable Haemophilus influenzae and Moraxella catarrhalis. Otolaryngol. Head Neck Surg. 116:175-180.
59. Robbins, J. B., R. Schneerson, and S. C. Szu. 1995. Perspective: hypothesis -serum IgG antibody is sufficient to confer protection against infectious diseases by inactivating the inoculum. J. Infect. Dis. 171:1387-1398.
60. Rabbins, J. B., R. Schneerson, and S. C. Szu. 1996. Hypothesis: how licensed vaccines confer protective immunity. Adv. Exp. Med. Biol. 397:169-182.
61. Rosenfeld, R. M., W. J. Doyle, J. M. Griffiss, and B. W. Gibson. 1992. Third-generation cephalosporins in the treatment of acute pneumococcal otitis media: an animal study. Arch. Otolaryngol. Head Neck Surg. 118:49-52.
62. Sasaki, K., and R. S. Munson, Jr. 1993. Protein D of Haemophilus influenzae is not a universal immunoglobulin D-binding protein. Infect. Immun. 61: 3026-3031.
63. Schneerson, R., A. Fattom, S. C. Szu, D. Bryla, J. T. Ulrich, J. A. Rudbach, G. Schiffman, and J. B. Rabbins. 1991. Evaluation of monophosphoryl lipid A (MPL) as an adjuvant: Enhancement of the serum antibody response in mice to polysaccharide-protein conjugates by concurrent injection with MPL. J. Immunol. 147:2136-2140.
64. Shurin, P. A., J. M. Rehmus, C. E. Johnson, C. D. Marchant, S. A. Carlin, D. M. Super, G. F. Van Hare, P. K. Jones, D. M. Ambrosino, and G. R. Siber. 1993. Bacterial polysaccharide immune globulin for prophylaxis of acute otitis media in high-risk children. J. Pediatr. 123:801-810.
65. Siber, G. R., D. Leombruno, J. Leszczynski, J. McIver, D. Bodkin, R. Gonin, C. M. Thompson, E. E. Walsh, P. A. Piedra, V. G. Hemming, and G. A. Prince. 1994. Comparison of antibody concentrations and protective activity of respiratory syncytial virus immune globulin and conventional immune globulin. J. Infect. Dis. 169:1368-1373.
66. Sirakova, T., P. E. Kolattukudy, D. M. Murwin, J. M. Billy, E. R. Leake, D. J. Lim, T. F. DeMaria, and L. O. Bakaletz. 1994. The role of fimbriae expressed by nontypable Haemophilus influenzae (NTHi) in the pathogenesis of and protection against otitis media and the relatedness of the fimbrin subunit to outer membrane protein A. Infect. Immun. 62:2002-2020.
67. Snapper, C. M., F. R. Rosas, L. Jin, C. Wortham, M. R. Kehry, and J. J. Mond. 1995. Bacterial lipoproteins may substitute for cytokines in the humoral immune response to T cell-independent type II antigens. J. Immunol. 155:5582-5589.
68. Song, X. M., A. Forsgren, and H. Janson. 1995. The gene encoding protein D (hpd) is highly conserved among Haemophilus influenzae type b and non-typeable strains. Infect. Immun. 63:696-699.
69. Sperandio, V., C. Bailey, J. A. Giron, V. J. DiRita, W. D. Silveira, A. L. Vettore, and J. B. Kaper. 1996. Cloning and characterization of the gene encoding the OmpU outer membrane protein of Vibrio cholerae. Infect. Immun. 64:5406-5409.
70. Sperandio, V., J. A. Giron, W. D. Silveira, and J. B. Kaper. 1995. The OmpU outer membrane protein, a potential adherence factor of Vibrio cholerae. Infect. Immun. 63:4433-4438.
71. Spinola, S. M. G. E. Griffiths, K. L. Shanks, and M. S. Blake. 1993. The major outer membrane protein of Haemophilus ducreyi is a member of the OmpA family of proteins. Infect. Immun. 61:1346-1351.
72. Suzuki, K., and L. O. Bakaletz. 1994. Synergistic effect of adenovirus type 1 and nontypeable Haemophilus influenzae in a chinchilla model of experimental otitis media. Infect. Immun. 62:1710-1718.
73. Virji, M., K. Makepeace, D. J. P. Ferguson, M. Achtman, and E. R. Moxon. 1993. Meningococcal Opa and Ope proteins: their role in colonization and invasion of human epithelial and endothelial cells. Mol. Microbiol. 10:499-510.
74. Weiser, J. N., and E. C. Gotschlich. 1991. Outer membrane protein A (Omp A) contributes to serum resistance and pathogenicity of Escherichia coli K-1. Infect. Immun. 59:2252-2258.
75. Willems, J. L., J. Kamerbeek, A. W. Geuijen, J. Top, H. Gielen, W. Gaastra, and F. R. Mooi. 1998. The efficacy of a whole cell pertussis vaccine and fimbriae against Bordetella pertussis and Bordetella parapertussis infections in a respiratory mouse model. Vaccine 16:410-416.