The heme-binding protein (HbpA) of Haemophilus influenzae as a virulence determinant

International Journal of Medical Microbiology

Volumn 299, Issue 7, 2009, Pages 479-488

  Morton, Daniel J ^a   Seale, Thomas W ^a   Bakaletz, Lauren O ^b   Jurcisek, Joseph A ^b   Smith, Ann ^c   VanWagoner, Timothy M ^a,d   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)

^c UNIVERSITY OF MISSOURI KANSAS CITY   (United States)

^d OKLAHOMA CHRISTIAN UNIVERSITY   (United States)

Author keywords

Haemophilus influenzae; Heme; Virulence

Indexed keywords

ALBUMIN; HEME; HEME BINDING PROTEIN A; HEMOPEXIN; HEMOPROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTEREMIA; BACTERIAL GROWTH; BACTERIAL VIRULENCE; CHINCHILLA; CONTROLLED STUDY; FEMALE; GENE INSERTION; GENE MUTATION; HAEMOPHILUS INFLUENZAE; HAEMOPHILUS INFLUENZAE TYPE A; HAEMOPHILUS INFLUENZAE TYPE B; HAEMOPHILUS MENINGITIS; NONHUMAN; OTITIS MEDIA; PATHOGENESIS; PROTEIN FUNCTION; RAT; VIRUS STRAIN; WILD TYPE;

ANIMALS; ANIMALS, NEWBORN; BACTEREMIA; BACTERIAL PROTEINS; CARRIER PROTEINS; CHINCHILLA; DISEASE MODELS, ANIMAL; FEMALE; HAEMOPHILUS INFLUENZAE; HEME; HUMANS; LIPOPROTEINS; MUTAGENESIS, INSERTIONAL; OTITIS MEDIA; PREGNANCY; RATS; VIRULENCE;

EID: 70349147003     PISSN: 14384221     EISSN: 16180607     Source Type: Journal    
DOI: 10.1016/j.ijmm.2009.03.004     Document Type: Article

References (45)

1. Bakaletz L.O., Kennedy B.-J., Novotnoy L.A., Duquesne G., Cohen J., and 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
2. Bakaletz L.O., Leake E.R., Billy J.M., and 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
3. Cope L.D., Yogev R., Muller-Eberhard U., and 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
4. Evans R.W., Crawley J.B., Joannou C.L., and Sharma N.D. Iron proteins. In: Bullen J.J., and Griffiths E. (Eds). Iron and Infection: Molecular, Physiological and Clinical Aspects (1999), Wiley, Inc., New York 27-86
5. Fleischmann R.D., Adams M.D., White O., Clayton R.A., Kirkness E.F., Kerlavage A.R., Bult C.J., Tomb J., Dougherty B.A., Merrick J.M., McKenney K., Sutton G., FitzHugh W., Fields C., Gocayne J.D., Scott J., Shirley R., Liu L., Glodek A., Kelley J.M., Weidman J.F., Phillips C.A., Spriggs T., Hedblom E., Cotton M.D., Utterback R.C., Hanna M.C., Nguyen D.T., Saudek D.M., Brandon R.C., Fine L.D., Fritchman J.L., Fuhrmann J.L., Geoghagen N.S.M., Gnehm C.L., McDonald L.A., Small K.V., Fraser C.M., Smith H.O., and Venter J.C. Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science 269 (1995) 496-512
6. Gitiban N., Jurcisek J.A., Harris R.H., Mertz S.E., Durbin R.K., Bakaletz L.O., and Durbin J.E. Chinchilla and murine models of upper respiratory tract infections with respiratory syncytial virus. J. Virol. 79 (2005) 6035-6042
7. Griffiths E. Iron in biological systems. In: Bullen J.J., and Griffiths E. (Eds). Iron and Infection: Molecular, Physiological and Clinical Aspects (1999), Wiley, Inc., New York 1-26
8. Hanson M.S., and Hansen E.J. Molecular cloning, partial purification, and characterization of a haemin-binding lipoprotein from Haemophilus influenzae type b. Mol. Microbiol. 5 (1991) 267-278
9. Hanson M.S., Slaughter C., and Hansen E.J. The hbpA gene of Haemophilus influenzae type b encodes a heme-binding lipoprotein conserved among heme-dependent Haemophilus species. Infect. Immun. 60 (1992) 2257-2266
10. Harrison A., Dyer D.W., Gillaspy A., Ray W.C., Mungur R., Carson M.B., Zhong H., Gipson J., Gipson M., Johnson L.S., Lewis L., Bakaletz L.O., and Munson Jr. R.S. Genomic sequence of an otitis media isolate of nontypeable Haemophilus influenzae: comparative study with H. influenzae serotype d, strain KW20. J. Bacteriol. 187 (2005) 4627-4636
11. Jett B.D., Hatter K.L., Huycke M.M., and Gilmore M.S. Simplified agar plate method for quantifying viable bacteria. Biotechniques 23 (1997) 648-650
12. Kelly D.F., Moxon E.R., and Pollard A.J. Haemophilus influenzae type b conjugate vaccines. Immunology 113 (2004) 163-174
13. Kennedy B.J., Novotnoy L.A., Jurcisek J.A., Lobet Y., and 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
14. Mason, K.M., Bakaletz, L.O., 2008. The Sap transporter is critical to survival strategies by nontypeable Haemophilus influenzae (NTHi). Abstracts of the 108th General Meeting of the American Society of Microbiology, Boston, MA, June 1-5, 2008.
15. Mason K.M., Bruggeman M.E., Munson R.S., and Bakaletz L.O. The non-typeable Haemophilus influenzae Sap transporter provides a mechanism of antimicrobial peptide resistance and SapD-dependent potassium acquisition. Mol. Microbiol. 62 (2006) 1357-1372
16. Moldenhauer H., and Rose H. Entwicklung der Serumeiweiße von Ratten im ersten Monat nach der Geburt. Acta Biol. Med. Ger. 25 (1970) 469-472
17. Morton D.J., Bakaletz L.O., Jurcisek J.A., VanWagoner T.M., Seale T.W., Whitby P.W., and Stull T.L. 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. Microb. Pathog. 36 (2004) 25-33
18. Morton D.J., Madore L.L., Smith A., VanWagoner T.M., Seale T.W., Whitby P.W., and Stull T.L. The heme-binding lipoprotein (HbpA) of Haemophilus influenzae: role in heme utilization. FEMS Microbiol. Lett. 253 (2005) 193-199
19. Morton D.J., Seale T.W., Madore L.L., VanWagoner T.M., Whitby P.W., and Stull T.L. The haem-haemopexin utilization gene cluster (hxuCBA) as a virulence factor of Haemophilus influenzae. Microbiology 153 (2007) 215-224
20. Morton D.J., Smith A., Ren Z., Madore L.L., VanWagoner T.M., Seale T.W., Whitby P.W., and Stull T.L. Identification of a haem-utilization protein (Hup) in Haemophilus influenzae. Microbiology 150 (2004) 3923-3933
21. Morton D.J., Smith A., VanWagoner T.M., Seale T.W., Whitby P.W., and Stull T.L. Lipoprotein e (P4) of Haemophilus influenzae: role in heme utilization and pathogenesis. Microbes Infect. 9 (2007) 932-939
22. Morton, D.J., Stull, T.L., 2004. Haemophilus. In: Crosa, J.H., Mey, A.R., Payne, S.M. (Eds.), Iron Transport in Bacteria. American Society for Microbiology, Washington, DC, pp. 273-292.
23. Morton D.J., VanWagoner T.M., Seale T.W., Whitby P.W., and Stull T.L. Differential utilization by Haemophilus influenzae of hemoglobin complexed to the three human haptoglobin phenotypes. FEMS Immunol. Med. Microbiol. 46 (2006) 426-432
24. Morton D.J., VanWagoner T.M., Seale T.W., Whitby P.W., and Stull T.L. Utilization of myoglobin as a heme source by Haemophilus influenzae requires binding of myoglobin to haptoglobin. FEMS Microbiol. Lett. 258 (2006) 235-240
25. Morton D.J., VanWagoner T.M., Seale T.W., Whitby P.W., and Stull T.L. Catalase as a source of both X- and V-factor for Haemophilus influenzae. FEMS Microbiol. Lett. 279 (2008) 157-161
26. Morton D.J., Whitby P.W., Jin H., Ren Z., and 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
27. Morton D.J., and Williams P. Utilization of transferrin-bound iron by Haemophilus species of human and porcine origins. FEMS Microbiol. Lett. 53 (1989) 123-127
28. Musser J.M., Barenkamp S.J., Granoff D.M., and Selander R.K. Genetic relationships of serologically nontypable and serotype b strains of Haemophilus influenzae. Infect. Immun. 52 (1986) 183-191
29. Panek H., and O'Brian M.R. A whole genome view of prokaryotic haem biosynthesis. Microbiology 148 (2002) 2273-2282
30. Peters T. All About Albumin: Biochemistry, Genetics, and Medical Applications (1996), Academic Press, San Diego, CA
31. Poje G., and Redfield R.J. General methods for culturing Haemophilus influenzae. Methods Mol. Med. 71 (2003) 51-56
32. Rosadini C.V., Wong S.M., and Akerley B.J. The periplasmic disulfide oxidoreductase DsbA contributes to Haemophilus influenzae pathogenesis. Infect. Immun. 76 (2008) 1498-1508
33. Seale T.W., Morton D.J., Whitby P.W., Wolf R., Kosanke S.D., VanWagoner T.M., and Stull T.L. Complex role of hemoglobin and hemoglobin-haptoglobin binding proteins in Haemophilus influenzae virulence in the infant rat model of invasive infection. Infect. Immun. 74 (2006) 6213-6225
34. Smith A. Intracellular distribution of haem after uptake by different receptors. Haem-haemopexin and haem-asialo-haemopexin. Biochem. J. 231 (1985) 663-669
35. Smith A., and Morgan W.T. Hemopexin-mediated heme uptake by liver. Characterization of the interaction of heme-hemopexin with isolated rabbit liver plasma membranes. J. Biol. Chem. 259 (1984) 12049-12053
36. Smith A.L., Smith D.H., Averill D.R., Marino J., and Moxon E.R. Production of Haemophilus influenzae b meningitis in infant rats by intraperitoneal inoculation. Infect. Immun. 8 (1973) 278-290
37. Stull T.L. Protein sources of heme for Haemophilus influenzae. Infect. Immun. 55 (1987) 148-153
38. Suzuki K., and 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
39. Turk D.C. The pathogenicity of Haemophilus influenzae. J. Med. Microbiol. 18 (1984) 1-16
40. VanWagoner, T.M., Morton, D.J., Whitby, P.W., Seale, T.W., Stull, T.L., 2007. Identification of an ABC transport system involved in heme uptake in type b capsulated Haemophilus influenzae. Abstracts of the 107th General Meeting of the American Society of Microbiology, Toronto, Canada, May 21-25, 2007.
41. Ward C.G., and Bullen J.J. Clinical and physiological aspects. In: Bullen J.J., and Griffiths E. (Eds). Iron and Infection: Molecular, Physiological and Clinical Aspects (1999), Wiley, Inc., New York 369-450
42. Whitby P.W., Seale T.W., VanWagoner T.M., Morton D.J., and Stull T.L. The iron/heme regulated genes of Haemophilus influenzae: comparative transcriptional profiling as a tool to define the species core modulon. BMC Genomics 10 (2009) 6
43. Whitby P.W., VanWagoner T.M., Seale T.W., Morton D.J., and Stull T.L. Transcriptional profile of Haemophilus influenzae: effects of iron and heme. J. Bacteriol. 188 (2006) 5640-5645
44. Whitby P.W., Morton D.J., and Stull T.L. Construction of antibiotic resistance cassettes with multiple paired restriction sites for insertional mutagenesis of Haemophilus influenzae. FEMS Microbiol. Lett. 158 (1998) 57-60
45. White D.C., and Granick S. Hemin biosynthesis in Haemophilus. J. Bacteriol. 85 (1963) 842-850