Reduced severity of middle ear infection caused by nontypeable Haemophilus influenzae lacking the hemoglobin/hemoglobin-haptoglobin binding proteins (Hgp) in a chinchilla model of otitis media

Microbial Pathogenesis

Volumn 36, Issue 1, 2004, Pages 25-33

  Morton, Daniel J ^a   Bakaletz, Lauren O ^b   Jurcisek, Joseph A ^b   VanWagoner, Timothy M ^a   Seale, Thomas W ^a   Whitby, Paul W ^a   Stull, Terrence L ^a  

^a UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

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

Author keywords

Chinchilla model; Haemophilus influenzae; Heme; Hemoglobin haptoglobin; Otitis media; Pathogenesis

Indexed keywords

BINDING PROTEIN; HAPTOGLOBIN; HEMOGLOBIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL COUNT; BACTERIAL INFECTION; BACTERIAL STRAIN; BACTERIUM MUTANT; CHINCHILLA; CONTROLLED STUDY; DISEASE DURATION; DISEASE MODEL; EXPERIMENTAL ANIMAL; HAEMOPHILUS INFLUENZAE; KNOCKOUT GENE; MIDDLE EAR EFFUSION; NONHUMAN; OTITIS MEDIA; OTOSCOPY; PRIORITY JOURNAL; PROTEIN BINDING; STRAIN DIFFERENCE; TYMPANOMETRY; VIDEORECORDING; WILD TYPE;

BACTERIA (MICROORGANISMS); CHINCHILLA LANIGERA; CHINCHILLIDAE; HAEMOPHILUS; HAEMOPHILUS INFLUENZAE;

EID: 0345688136     PISSN: 08824010     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.micpath.2003.08.007     Document Type: Article

References (46)

1. Turk D.C. The pathogenicity of Haemophilus influenzae. J Med Microbiol. 18:1984;1-16.
2. Infante-Rivard C., Fernandez A. Otitis media in children: frequency, risk factors, and research avenues. Epidemiol Rev. 15:1993;444-465.
3. Hendley J.O. Otitis media. N Engl J Med. 347:2002;1169-1174.
4. Bluestone C.D., Klein J.O., Rosenfeld R.M., Berman S., Casselbrant M.L., Chonmaitree T., Giebink G.S., Grote J.J., Ingvarsson L.B., Linder T., Lous J., Maw A.R., Paradise J.L., Sando I., Stool S.E., Takasaka T. Recent advances in otitis media. 9. Treatment, complications, and sequelae. Ann Otol Rhinol Laryngol. 111:2002;102-124.
5. Paradise J.L., Dollaghan C.A., Campbell T.F., Feldman H.M., Bernard B.S., Colborn D.K., Rockette H.E., Janosky J.E., Pitcairn D.L., Sabo D.L., Kurs-Lasky M., Smith C.G. Language, speech sound production, and cognition in three-year-old children in relation to otitis media in their first three years of life. Pediatrics. 105:2000;1119-1130.
6. Giebink G.S., Mills E.L., Huff J.S., Edelman C.K., Weber M.L., Juhn S.K., Quie P.G. The microbiology of serous and mucoid otitis media. Pediatrics. 63:1979;915-919.
7. Kilpi T., Herva E., Kaijalainen T., Syrjänen R., Takala A.K. Bacteriology of acute otitis media in a cohort of Finnish children followed for the first two years of life. Pediatr Infect Dis J. 20:2001;654-662.
8. White D.C., Granick S. Hemin biosynthesis in Haemophilus. J Bacteriol. 85:1963;842-850.
9. Schlor S., Herbert M., Rodenburg M., Blass J., Reidl J. Characterization of ferrochelatase (hemH) mutations in Haemophilus influenzae. Infect Immun. 68:2000;3007-3009.
10. Griffiths E. Iron in biological systems. Bullen J.J., Griffiths E. Iron and infection: molecular, physiological and clinical aspects. 1999;1-26 Wiley, New York, NY.
11. Ward C.G., Bullen J.J. Clinical and physiological aspects. Bullen J.J., Griffiths E. Iron and infection: molecular, physiological and clinical aspects. 1999;369-450 Wiley, New York, NY.
12. Evans R.W., Crawley J.B., Joannou C.L., Sharma N.D. Iron proteins. Bullen J.J., Griffiths E. Iron and infection: molecular, physiological and clinical aspects. 1999;27-86 Wiley, New York, NY.
13. Stull T.L. Protein sources of heme for Haemophilus influenzae. Infect Immun. 55:1987;148-153.
14. Morton D.J., Williams P. Utilization of transferrin-bound iron by Haemophilus species of human and porcine origins. FEMS Microbiol Lett. 53:1989;123-127.
15. Schryvers A.B., Gray-Owen S. Iron acquisition in Haemophilus influenzae: receptors for human transferrin. J Infect Dis. 165:(Suppl 1):1992;S103-S104.
16. Morton D.J., Stull T.L. Haemophilus. Crosa J.H., Payne S.M. Iron transport in bacteria: molecular genetics, biochemistry, microbial pathogenesis and ecology. 2004;American Society for Microbiology, Washington, DC. in press.
17. Cope L.D., Yogev R., Muller-Eberhard U., Hansen E.J. A gene cluster involved in the utilization of both free heme and heme:hemopexin by Haemophilus influenzae type b. J Bacteriol. 177:1995;2644-2653.
18. Cope L.D., Love R.P., Guinn S.E., Gilep A., Usanov S., Estabrook R.W., Hrkal Z., Hansen E.J. Involvement of HxuC outer membrane protein in utilization of hemoglobin by Haemophilus influenzae. Infect Immun. 69:2001;2353-2363.
19. Gray-Owen S.D., Schryvers A.B. Bacterial transferrin and lactoferrin receptors. Trends Microbiol. 4:1996;185-191.
20. Jin H., Ren Z., Whitby P.W., Morton D.J., Stull T.L. Characterization of hgpA, a gene encoding a hemoglobin/hemoglobin-haptoglobin binding protein of Haemophilus influenzae. Microbiology. 145:1999;905-914.
21. Ren Z., Jin H., Morton D.J., Stull T.L. hgpB, a gene encoding a second Haemophilus influenzae hemoglobin- and hemoglobin-haptoglobin-binding protein. Infect Immun. 66:1998;4733-4741.
22. Ren Z., Jin H., Whitby P.W., Morton D.J., Stull T.L. Role of CCAA nucleotide repeats in regulation of hemoglobin and hemoglobin-haptoglobin binding protein genes of Haemophilus influenzae. J Bacteriol. 181:1999;5865-5870.
23. Morton D.J., Whitby P.W., Jin H., Ren Z., Stull T.L. Effect of multiple mutations in the hemoglobin- and hemoglobin-haptoglobin-binding proteins, HgpA, HgpB, and HgpC of Haemophilus influenzae type b. Infect Immun. 67:1999;2729-2739.
24. Morton D.J., Stull T.L. Distribution of a family of Haemophilus influenzae genes containing CCAA nucleotide repeating units. FEMS Microbiol Lett. 174:1999;303-309.
25. Cope L.D., Hrkal Z., Hansen E.J. Detection of phase variation in expression of proteins involved in hemoglobin and hemoglobin-haptoglobin binding by nontypeable Haemophilus influenzae. Infect Immun. 68:2000;4092-4101.
26. Bakaletz L.O., Kennedy B.-J., Novotnoy L.A., Duquesne G., Cohen J., Lobet Y. 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. Infect Immun. 67:1999;2746-2762.
27. Hanson M.S., Pelzel S.E., Latimer J., Muller-Eberhard U., Hansen E.J. Identification of a genetic locus of Haemophilus influenzae type b necessary for the binding and utilization of heme bound to human hemopexin. Proc Natl Acad Sci USA. 89:1992;1973-1977.
28. Jarosik G.P., Sanders J.D., Cope L.D., Muller-Eberhard U., Hansen E.J. A functional tonB gene is required for both utilization of heme and virulence expression by Haemophilus influenzae type b. Infect Immun. 62:1994;2470-2477.
29. Mogi G., Honjo S. Middle ear effusion. Analysis of protein components. Ann Otol Rhinol Laryngol. 81:1972;99-105.
30. Van de Calseyde P., Blaton V., Ampe W., Goethals H., Peeters H. The protein pattern of middle ear effusion in serous otitis media behind an intact drum. Acta Otolaryngol. 71:1971;153-158.
31. Juhn S.K., Huff J.S., Paparella M.M. Biochemical analyses of middle ear effusions. Ann Otol Rhinol Laryngol. 80:1971;347-353.
32. Sorensen C.H., Moller H. Lactoferrin, secretory IgA, and albumin in upper airway secretions from children with secretory otitis media. Lim D.J., Bluestone C.D., Klein J.O., Nelson J.D., Ogra P.L. Recent advances in otitis media. 1993;424-426 Decker Periodicals, Hamilton, Ontario.
33. Hiraide F., Inouye T., Miyakogawa N. Experimental cholesterol granuloma. Histopathological and histochemical studies. J Laryngol Otol. 96:1982;491-501.
34. Paparella M.M., Hiraide F., Juhn S.K., Kaneko Y. Cellular events involved in middle ear fluid production. Ann Otol Rhinol Laryngol. 79:1970;766-779.
35. Kaneko Y., Paparella M.M. Middle ear epithelium in the presence of experimental effusion. Acta Otolaryngol. 72:1971;206-214.
36. Broides A., Leibovitz E., Dagan R., Press J., Raiz S., Kafka M., Leiberman A., Yermiahu T. Cytology of middle ear fluid during acute otitis media. Pediatr Infect Dis J. 21:2002;57-61.
37. Nonomura N., Giebink G.S., Juhn S.K., Harada T., Aeppli D. Pathophysiology of Streptococcus pneumoniae otitis media: kinetics of the middle ear biochemical and cytologic host responses. Ann Otol Rhinol Laryngol. 100:1991;236-243.
38. Giebink G.S., Juhn S.K., Weber M.L., Le C.T. The bacteriology and cytology of chronic otitis media with effusion. Pediatr Infect Dis. 1:1982;98-103.
39. Giebink G.S., Carlson B.A., Hetherington S.V., Hostetter M.K., Le C.T., Juhn S.K. Bacterial and polymorphonuclear leukocyte contribution to middle ear inflammation in chronic otitis media with effusion. Ann Otol Rhinol Laryngol. 94:1985;398-402.
40. Ponka P. Cell biology of heme. Am J Med Sci. 318:1999;241-256.
41. Whitby P.W., Sim K.E., Morton D.J., Patel J.A., Stull T.L. Transcription of genes encoding iron and heme acquisition proteins of Haemophilus influenzae during acute otitis media. Infect Immun. 65:1997;4696-4700.
42. Morton D.J., Musser J.M., Stull T.L. Expression of the Haemophilus influenzae transferrin receptor is repressible by hemin but not elemental iron alone. Infect Immun. 61:1993;4033-4037.
43. Kennedy B.J., Novotnoy L.A., Jurcisek J.A., Lobet Y., Bakaletz L.O. Passive transfer of antiserum specific for immunogens derived from a nontypeable Haemophilus influenzae adhesin and lipoprotein D prevents otitis media after heterologous challenge. Infect Immun. 68:2000;2756-2765.
44. Suzuki K., Bakaletz L.O. Synergistic effect of adenovirus type 1 and nontypeable Haemophilus influenzae in a chinchilla model of experimental otitis media. Infect Immun. 62:1994;1710-1718.
45. Gromkova R.C., Rowji P.B., Koornhof H.J. Induction of competence in nonencapsulated and encapsulated strains of Haemophilus influenzae. Curr Microbiol. 19:1989;241-245.
46. Bakaletz L.O., Leake E.R., Billy J.M., Kaumaya P.T.P. Relative immunogenicity and efficacy of two synthetic chimeric peptides of fimbrin as vaccinogens against nasopharyngeal colonization by nontypeable Haemophilus influenzae in the chinchilla. Vaccine. 15:1997;955-961.