Complex role of hemoglobin and hemoglobin-haptoglobin binding proteins in Haemophilus influenzae virulence in the infant rat model of invasive infection

Infection and Immunity

Volumn 74, Issue 11, 2006, Pages 6213-6225

  Seale, Thomas W ^a   Morton, Daniel J ^a   Whitby, Paul W ^a   Wolf, Roman ^a   Kosanke, Stanley D ^a   Vanwagoner, Timothy M ^a   Stull, Terrence L ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

HAPTOGLOBIN; HEMOGLOBIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTEREMIA; BACTERIAL COUNT; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM ISOLATE; BACTERIUM MUTANT; CHINCHILLA; CONTROLLED STUDY; DISEASE DURATION; GENE DELETION; GENE DISRUPTION; GENE FUNCTION; HAEMOPHILUS INFLUENZAE; HGP GENE; HISTOPATHOLOGY; HXUC GENE; MENINGITIS; NEWBORN; NEWBORN INFECTION; NONHUMAN; OPERON; OTITIS MEDIA; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT;

ANIMALS; ANIMALS, NEWBORN; BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL PROTEINS; CARRIER PROTEINS; DISEASE MODELS, ANIMAL; FEMALE; HAEMOPHILUS INFECTIONS; HAEMOPHILUS INFLUENZAE; HAPTOGLOBINS; HEMOGLOBINS; RATS; RATS, SPRAGUE-DAWLEY; VIRULENCE;

EID: 33750469363     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.00744-06     Document Type: Article

References (70)

1. Alper, C. M., A. Andalibi, L. O. Bakaletz, C. Buchman, P. Caye-Thomasen, S. O. Hellstrom, P. Herman, A. Hermansson, B. Hussl, Y. Iino, H. Kawauchi, M. M. Paparella, I. Sando, J. D. Swarts, and T. Takasaka. 2002. Recent advances in otitis media. 4. Anatomy, cell biology, pathology, and animal models. Ann. Otol. Rhmol. Laryngol. 111(Suppl. 188):36-51.
2. Alrawi, A. M., K. C. Chern, V. Cevallos, T. Lietman, J. P. Whitcher, T. P. Margolis, and E. T. Cunningham. 2002. Biotypes and serotypes of Haemophilus influenzae ocular isolates. Br. J. Opthalmol. 86:276-277.
3. Bajanca, P., M. Canica, and The Multicenter Study Group. 2004. Emergence of nonencapsulated and encapsulated non-b-type invasive Haemophilus influenzae isolates in Portugal (1989-2001). J. Clin. Microbiol. 42:807-810.
4. Casey, J. R., and M. E. Pichichero. 2004. Changes in frequency and pathogens causing acute otitis media in 1995-2003. Pediatr. Infect. Dis. J. 23:824-828.
5. Cope, L. D., Z. Hrkal, and E. J. Hansen. 2000. Detection of phase variation in expression of proteins involved in hemoglobin and hemoglobin-haptoglobin binding by nontypeable Haemophilus influenzae. Infect. Immun. 68:4092-4101.
6. Cope, L. D., R. P. Love, S. E. Guinn, A. Gilep, S. Usanov, R. W. Estabrook, Z. Hrkal, and E. J. Hansen. 2001. Involvement of HxuC outer membrane protein in utilization of hemoglobin by Haemophilus influenzae. Infect. Immun. 69:2353-2363.
7. Cope, L. D., S. E. Thomas, Z. Hrkal, and E. J. Hansen. 1998. Binding of heme-hemopexin complexes by soluble HxuA protein allows utilization of this complexed heme by Haemophilus influenzae. Infect. Immun. 66:4511-4516.
8. Cope, L. D., S. E. Thomas, J. L. Latimer, C. A. Slaughter, U. Muller-Eberhard, and E. J. Hansen. 1994. The 100 kDa haem:haemopexin-binding protein of Haemophilus influenzae: structure and localization. Mol. Microbiol. 13:863-873.
9. Cope, L. D., R. Yogev, U. Muller-Eberhard, and E. J. Hansen. 1995. A gene cluster involved in the utilization of both free heme and heme:hemopexin by Haemophilus influenzae type b. J. Bacteriol. 177:2644-2653.
10. Cox, A. J., M. L. Hunt, J. D. Boyce, and B. Adler. 2003. Functional characterization of HgbB, a new hemoglobin binding protein of Pasteurella multocida. Microb. Pathog. 34:287-296.
11. Delers, F., C. Lombart, M. Domingo, and S. Musquera. 1981. A novel and specific method for the purification of hemoglobin-binding proteins. Anal. Biochem. 118:353-357.
12. Dewhirst, F. E., B. J. Paster, I. Olsen, and G. J. Fraser. 1992. Phylogeny of 54 representative strains of species in the family Pasteurellaceae as determined by comparison of 16S rRNA sequences. J. Bacteriol. 174:2002-2013.
13. Dubuque, S. H., B. Dvorak, S. S. Woodward, R. S. McCuskey, and P. J. Kling. 2002. Iron-deficient erythropoiesis in neonatal rats. Biol. Neonate 81:51-57.
14. Eaton, J. W., P. Brandt, J. R. Mahoney, and J. T. Lee Jr. 1982. Haptoglobin: a natural bacteriostat. Science 215:691-693.
15. Evans, N. M., D. D. Smith, and A. J. Wicken. 1974. Haemin and nicotinamide adenine dinucleotide requirements of Haemophilus influenzae and Haemophilus parainfluenzae. J. Med. Microbiol. 7:359-365.
16. Evans, R. W., J. B. Crawley, C. L. Joannou, and N. D. Sharma. 1999. Iron proteins, p. 27-86. In J. J. Bullen and E. Griffiths (ed.), Iron and infection: molecular, physiological and clinical aspects. John Wiley & Sons, Inc., New York, N. Y.
17. Garcia-Rodriguez, J. A., and M. J. Fresnadillo Martinez. 2002. Dynamics of nasopharyngeal colonization by potential respiratory pathogens. J. Antimicrob. Chemother. 50(Suppl. S2):59-73.
18. Genco, C. A., and D. W. Dixon. 2001. Emerging strategies in microbial haem capture. Mol. Microbiol. 39:1-11.
19. Glibetic, M., D. Bogojevic, S. Matic, and L. Sevaljevic. 1992. The expression of liver acute-phase protein genes during rat development and in response to inflammation of the dam. Differentiation 50:35-40.
20. Goldstein, L. A., and E. C. Heath. 1984. Nucleotide sequence of rat haptoglobin cDNA. Characterization of the αβ-subunit junction region of prohaptoglobin. J. Biol. Chem. 259:9212-9217.
21. Granert, C., H. Abdalla, L. Lindquist, A. Diab, M. Bahkiet, K. J. Tracey, and J. Andersson. 2000. Suppression of macrophage activation with CNI-1493 increases survival in infant rats with systemic Haemophilus influenzae infection. Infect. Immun. 68:5329-5334.
22. Gromkova, R. C., P. B. Rowji, and H. J. Koornhof. 1989. Induction of competence in nonencapsulated and encapsulated strains of Haemophilus influenzae. Curr. Microbiol. 19:241-245.
23. Harlow, E., and D. Lane. 1999. Immunoblotting, p. 267-309. In Using antibodies; a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
24. Harris, R. H., D. Wilk, C. L. Bevins, R. S. Munson, Jr., and L. O. Bakaletz. 2004. Identification and characterization of a mucosal antimicrobial peptide expressed by the chinchilla (Chinchilla lanigera) airway. J. Biol. Chem. 279:20250-20256.
25. Harrison, A., D. W. Dyer, A. Gillaspy, W. C. Ray, R. Mungur, M. B. Carson, H. Zhong, J. Gipson, M. Gipson, L. S. Johnson, L. Lewis, L. O. Bakaletz, and R. S. Munson, Jr. 2005. Genomic sequence of an otitis media isolate of nontypeable Haemophilus influenzae: comparative study with H. influenzae serotype d, strain KW20. J. Bacteriol. 187:4627-4636.
26. Herbert, M., A. Kraiss, A. K. Hilpert, S. Schlor, and J. Reidl. 2003. Aerobic growth deficient Haemophilus influenzae mutants are non-virulent: implications on metabolism. Int. J. Med. Microbiol. 293:145-152.
27. Huang, G., J. Ouyang, J. R. Delanghe, W. R. Baeyens, and Z. Dai. 2004. Chemiluminescent image detection of haptoglobin phenotyping after polyacrylamide gel electrophoresis. Anal. Chem. 76:2997-3004.
28. Jerse, A. E., E. T. Crow, A. N. Bordner, I. Rahman, C. N. Cornelissen, T. R. Moench, and K. Mehrazar. 2002. Growth of Neisseria gonorrhoeae in the female mouse genital tract does not require the gonococcal transferrin or hemoglobin receptors and may be enhanced by commensal lactobacilli. Infect. Immun. 70:2549-2558.
29. Jett, B. D., K. L. Hatter, M. M. Huycke, and M. S. Gilmore. 1997. Simplified agar plate method for quantifying viable bacteria. BioTechniques 23:648-650.
30. Jin, H., Z. Ren, J. M. Pozsgay, C. Elkins, P. W. Whitby, D. J. Morton, and T. L. Stull. 1996. Cloning of a DNA fragment encoding a heme-repressible hemoglobin-binding outer membrane protein from Haemophilus influenzae. Infect. Immun. 64:3134-3141.
31. Jin, H., Z. Ren, P. W. Whitby, D. J. Morton, and T. L. Stull. 1999. Characterization of hgpA, a gene encoding a hemoglobin/hemoglobin-haptoglobin binding protein of Haemophilus influenzae. Microbiology 145:905-914.
32. Kanakoudi, F., V. Drossou, V. Tzimouli, E. Diamanti, T. Konstantinidis, A. Germenis, and G. Kremenopoulos. 1995. Serum concentrations of 10 acute-phase proteins in healthy term and preterm infants from birth to age 6 months. Clin. Chem. 41:605-608.
33. Knutson, M., and M. Wessling-Resnick. 2003. Iron metabolism in the reticuloendothelial system. Crit. Rev. Biochem. Mol. Biol. 38:61-88.
34. Koedel, U., and H. W. Pfister. 1999. Models of experimental bacterial meningitis. Role and limitations. Infect. Dis. Clin. N. Am. 13:549-577, vi.
35. Langlois, M. R., and J. R. Delanghe. 1996. Biological and clinical significance of haptoglobin polymorphism in humans. Clin. Chem. 42:1589-1600.
36. Leong, W. I., C. L. Bowlus, J. Tallkvist, and B. Lonnerdal. 2003. Iron supplementation during infancy-effects on expression of iron transporters, iron absorption, and iron utilization in rat pups. Am. J. Clin. Nutr. 78:1203-1211.
37. Moldenhauer, H., and H. Rose. 1970. Entwicklung der serumeiweisse von ratten im ersten monat nach der geburt. Acta Biol. Med. Ger. 25:469-472.
38. Morton, D. J., L. O. Bakaletz, J. A. Jurcisek, T. M. VanWagoner, T. W. Seale, P. W. Whitby, and T. L. Stull. 2004. 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. 36:25-33.
39. Morton, D. J., A. Smith, L. L. Madore, T. M. VanWagoner, T. W. Seale, P. W. Whitby, and T. L. Stull. 2004. Identification of a haem utilization protein (Hup) in Haemophilus influenzae. Microbiology 150:3923-3933.
40. Morton, D. J., and T. L. Stull. 2004. Haemophilus, p. 273-292. In J. H. Crosa, A. R. Mey, and S. M. Payne (ed.), Iron transport in bacteria. American Society for Microbiology, Washington, D.C.
41. Morton, D. J., T. M. VanWagoner, T. W. Seale, P. W. Whitby, and T. L. Stull. 2006. Differential utilization by Haemophilus influenzae of hemoglobin complexed to the three human haptoglobin phenotypes. FEMS Immunol. Med. Microbiol. 46:426-432.
42. Morton, D. J., T. M. VanWagoner, T. W. Seale, P. W. Whitby, and T. L. Stull. 2006. Utilization of myoglobin as a heme source by Haemophilus influenzae requires binding of myoglobin to haptoglobin. FEMS Microbiol. Lett. 258:235-240.
43. Morton, D. J., P. W. Whitby, H. Jin, Z. Ren, and T. L. Stull. 1999. Effect of multiple mutations in the hemoglobin- and hemoglobin-haptoglobin- binding proteins, HgpA, HgpB, and HgpC of Haemophilus influenzae type b. Infect. Immun. 67:2729-2739.
44. Morton, D. J., and P. Williams. 1989. Utilization of transferrin-bound iron by Haemophilus species of human and porcine origins. FEMS Microbiol. Lett. 53:123-127.
45. Motley, S. T., B. J. Morrow, X. Liu, I. L. Dodge, A. Vitiello, C. K. Ward, and K. J. Shaw. 2004. Simultaneous analysis of host and pathogen interactions during an in vivo infection reveals local induction of host acute phase response proteins, a novel bacterial stress response, and evidence of a host-imposed metal ion limited environment. Cell Microbiol. 6:849-865.
46. Moxon, E. R., A. L. Smith, D. R. Averill, and D. H. Smith. 1974. Haemophilus influenzae meningitis in infant rats after intranasal inoculation. J. Infect. Dis. 129:154-162.
47. Murphy, T. F., L. O. Bakaletz, J. M. Kyd, B. Watson, and D. L. Klein. 2005. Vaccines for otitis media: proposals for overcoming obstacles to progress. Vaccine 23:2696-2702.
48. Murphy, T. F., A. L. Brauer, A. T. Schiffmacher, and S. Sethi. 2004. Persistent colonization by Haemophilus influenzae in chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med. 170:266-272.
49. Musser, J. M., S. J. Barenkamp, D. M. Granoff, and R. K. Selander. 1986. Genetic relationships of serologically nontypable and serotype b strains of Haemophilus influenzae. Infect. Immun. 52:183-191.
50. Myerowitz, R. L., R. Klaw, and B. L. Johnson. 1976. Experimental endogenous endophthalmitis caused by Haemophilus influenzae type b. Infect. Immun. 14:1043-1051.
51. Nikkila, H., J. D. Gitlin, and U. Muller-Eberhard. 1991. Rat hemopexin. Molecular cloning, primary structural characterization, and analysis of gene expression. Biochemistry 30:823-829.
52. Orihuela, C. J., J. N. Radin, J. E. Sublett, G. Gao, D. Kaushal, and E. I. Tuomanen. 2004. Microarray analysis of pneumococcal gene expression during invasive disease. Infect. Immun. 72:5582-5596.
53. Panek, H., and M. R. O'Brian. 2002. A whole genome view of prokaryotic haem biosynthesis. Microbiology 148:2273-2282.
54. Peltola, H. 2000. Worldwide Haemophilus influenzae type b disease at the beginning of the 21st century: global analysis of the disease burden 25 years after the use of the polysaccharide vaccine and a decade after the advent of conjugates. Clin. Microbiol. Rev. 13:302-317.
55. Pidcock, K. A., J. A. Wooten, B. A. Daley, and T. L. Stull. 1988. Iron acquisition by Haemophilus influenzae. Infect. Immun. 56:721-725.
56. Poolman, J. T., L. Bakaletz, A. Cripps, P. A. Denoel, A. Forsgren, J. Kyd, and Y. Lobet. 2000. Developing a nontypeable Haemophilus influenzae (NTHi) vaccine. Vaccine 19 (Suppl. 1):S108-S115.
57. Ren, Z., H. Jin, D. J. Morton, and T. L. Stull. 1998. hgpB, a gene encoding a second Haemophilus influenzae hemoglobin- and hemoglobin-haptoglobin- binding protein. Infect. Immun. 66:4733-4741.
58. Ribeiro, G. S., J. N. Reis, S. M. Cordeiro, J. B. Lima, E. L. Gouveia, M. Petersen, K. Salgado, H. R. Silva, R. C. Zanella, S. C. Almeida, M. C. Brandileone, M. G. Reis, and A. I. Ko. 2003. Prevention of Haemophilus influenzae type b (Hib) meningitis and emergence of serotype replacement with type a strains after introduction of Hib immunization in Brazil. J. Infect. Dis. 187:109-116.
59. Schaible, U. E., and S. H. Kaufmann. 2004. Iron and microbial infection. Nat. Rev. Microbiol. 2:946-953.
60. Schryvers, A. B. 1989. Identification of the transferrin- and lactoferrin-binding proteins in Haemophilus influenzae. J. Med. Microbiol. 29:121-130.
61. Smith, A. L., D. H. Smith, D. R. Averill, J. Marino, and E. R. Moxon. 1973. Production of Haemophilus influenzae b meningitis in infant rats by intraperitoneal inoculation. Infect. Immun. 8:278-290.
62. Stevens, M. K., S. Porcella, J. Klesney-Tait, S. Lumbley, S. E. Thomas, M. V. Norgard, J. D. Radolf, and E. J. Hansen. 1996. A hemoglobin-binding outer membrane protein is involved in virulence expression by Haemophilus ducreyi in an animal model. Infect. Immun. 64:1724-1735.
63. Stull, T. L. 1987. Protein sources of heme for Haemophilus influenzae. Infect. Immun. 55:148-153.
64. Turk, D. C. 1984. The pathogenicity of Haemophilus influenzae. J. Med. Microbiol. 18:1-16.
65. Vogel, L., F. Geluk, H. Jansen, J. Dankert, and L. van Alphen. 1997. Human lactoferrin receptor activity in non-encapsulated Haemophilus influenzae. FEMS Microbiol. Lett. 156:165-170.
66. Watson, M. E., Jr., J. Jarisch, and A. L. Smith. 2004. Inactivation of deoxyadenosine methyltransferase (dam) attenuates Haemophilus influenzae virulence. Mol. Microbiol. 53:651-664.
67. Watt, J. P., O. S. Levine, and M. Santosham. 2003. Global reduction of Hib disease: what are the next steps? Proceedings of the meeting Scottsdale, Arizona, September 22-25, 2002. J. Pediatr. 143:5163-5187.
68. Whitby, P. W., K. E. Sim, D. J. Morton, J. A. Patel, and T. L. Stull. 1997. Transcription of genes encoding iron and heme acquisition proteins of Haemophilus influenzae during acute otitis media. Infect. Immun. 65:4696-4700.
69. Williams, P., D. J. Morton, K. J. Towner, P. Stevenson, and E. Griffiths. 1990. Utilization of enterobactin and other exogenous iron sources by Haemophilus influenzae, H. parainfluenzae and H. paraphrophilus. J. Gen. Microbiol. 136:2343-2350.
70. Wong, J. C. Y., J. Holland, T. Parsons, A. Smith, and P. Williams. 1994. Identification and characterization of an iron-regulated hemopexin receptor in Haemophilus influenzae type b. Infect. Immun. 62:48-59.