Cloning of a DNA fragment encoding a heme-repressible hemoglobin- binding outer membrane protein from Haemophilus influenzae

Infection and Immunity

Volumn 64, Issue 8, 1996, Pages 3134-3141

  Jin, Hongfan ^a   Ren, Zhen ^a   Pozsgay, Judith M ^b   Elkins, Christopher ^c   Whitby, Paul W ^a   Morton, Daniel J ^a   Stull, Terrence L ^a,d  

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

^b DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^d CHO 2B300 ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA FRAGMENT; HAPTOGLOBIN; HEME; HEMOGLOBIN; OUTER MEMBRANE PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL GENE; BACTERIAL MENINGITIS; BACTERIAL PNEUMONIA; EPIGLOTTITIS; ESCHERICHIA COLI; HAEMOPHILUS INFLUENZAE; MOLECULAR CLONING; NONHUMAN; OTITIS MEDIA; PRIORITY JOURNAL; PROTEIN ISOLATION;

EID: 0030056385     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/iai.64.8.3134-3141.1996     Document Type: Article

References (58)

1. Adhikari, P., S. D. Kirby, A. J. Nowalk, K. L. Veraldi, A. B. Schryvers, and T. A. Mietzner. 1995. Biochemical characterization of a Haemophilus influenzae periplasmic iron transport operon. J. Biol. Chem. 270:25142-25149.
2. Anderson, J. E., P. F. Sparling, and C. N. Cornelissen. 1994. Gonococcal transferrin-hinding protein 2 facilitates but is not essential for transferrin utilization. J. Bacteriol. 176:3162-3170.
3. Bezkorovainy, A. 1987. Iron proteins, p. 27-68. In J. J. Bullen and E. Griffiths (ed.), Iron and infection: molecular, physiological and clinical aspects. John Wiley & Sons, New York.
4. 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.
5. 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.
6. Cornelissen, C. N., G. D. Biswas, J. Tsai, D. K. Paruchuri, S. A. Thompson, and P. F. Sparling. 1992. Gonococcal transferrin-binding protein 1 is required for transferrin utilization and is homologous to TonB-dependent outer membrane receptors. J. Bacteriol. 174:5788-5797.
7. Cornelissen, C. N., and P. F. Sparling. 1994. Iron piracy: acquisition of transferrin-bound iron by bacterial pathogens. Mol. Microbiol. 14:843-850.
8. Elkins, C. 1995. Identification and purification of a conserved heme-regulated hemoglobin-binding outer membrane protein from Haemophilus ducreyi. Infect. Immun. 63:1241-1245.
9. Elkins, C., C. J. Chen, and C. E. Thomas. 1995. Characterization of the hgbA locus encoding a hemoglobin receptor from Haemophilus ducreyi. Infect. Immun. 63:2194-2200.
10. Eskola, J., H. Kayhty, H. Peltola, V. Karanko, P. H. Makela, J. Samuelson, and L. K. Gordon. 1985. Antibody levels achieved in infants by course of Haemophilus influenzae type b polysaccharide/diphtheria toxoid conjugate vaccine. Lancet i:1184-1186.
11. 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.
12. Falla, T. J., S. R. Dobson, D. W. Crook, W. A. Kraak, W. W. Nichols, E. C. Anderson, J. Z. Jordens, M. P. Slack, E. Mayon-White, and E. R. Moxon. 1993. Population-based study of non-typable Haemophilus influenzae invasive disease in children and neonates. Lancet 341:851-854.
13. Fleischmann, R. D., M. D. Adams, O. White, R. A. Clayton, E. F. Kirkness, A. R. Kerlavage, C. J. Bult, J. Tomb, B. A. Dougherty, J. M. Merrick, K. McKenney, G. Sutton, W. FitzHugh, C. Fields, J. D. Gocayne, J. Scott, R. Shirley, L. Liu, A. Glodek, J. M. Kelley, J. F. Weidman, C. A. Phillips, T. Spriggs, E. Hedblom, M. D. Cotton, R. C. Utterback, M. C. Hanna, D. T. Nguyen, D. M. Saudek, R. C. Brandon, L. D. Fine, J. L. Fritchman, J. L. Fuhrmann, N. S. M. Geoghagen, C. L. Gnehm, L. A. McDonald, K. V. Small, C. M. Fraser, H. O. Smith, and J. C. Venter. 1995. Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science. 269:496-512.
14. 13a.Fowler, A. Personal communication.
15. Frangipane, M. E., D. J. Morton, J. A. Wooten, J. M. Pozsgay, and T. L. Stull. 1994. Binding of human hemoglobin by Haemophilus influenzae. FEMS Microbiol. Lett. 118:243-248.
16. Gilsdorf, J. R., K. McCrea, and L. Forney. 1990. Conserved and nonconserved epitopes among Haemophilus tnfluenzae type b pili. Infect. Immun. 58:2252-2257.
17. Gray-Owen, S. D., S. Loosmore, and A. B. Schryvers. 1995. Identification and characterization of genes encoding the human transferrin-binding proteins from Haemophilus influenzae. Infect. Immun. 63:1201-1210.
18. Gray-Owen, S. D., and A. B. Schryvers. 1995. Characterization of transferrin-binding proteins 1 and 2 in invasive type b and nontypeable strains of Haemophilus influenzae. Infect. Immun. 63:3809-3815.
19. Griffiths, E. 1987. Iron in biological systems, p. 1-26. In J. J. Bullen and E. Griffiths (ed.), Iron and infection: molecular, physiological and clinical aspects. John Wiley & Sons, New York.
20. Hanson, M. S., and E. J. Hansen. 1991. Molecular cloning, partial purification, and characterization of a haemin-binding lipoprotein from Haemophilus influenzae type b. Mol. Microbiol. 5:267-278.
21. Hanson, M. S., S. E. Pelzel, J. Latimer, U. Muller-Eberhard, and E. J. Hansen. 1992. 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. 89:1973-1977.
22. Hanson, M. S., C. Slaughter, and E. J. Hansen. 1992. The hbpA gene of Haemophilus influenzae type b encodes a heme-binding lipoprotein conserved among heme-dependent Haemophilus species. Infect. Immun. 60: 2257-2266.
23. Hardie, K. R., R. A. Adams, and K. J. Towner. 1993. Transferrin-binding ability of invasive and commensal isolates of Haemophilus spp. J. Med. Microbiol. 39:218-224.
24. Jarosik, G. P., J. D. Sanders, L. D. Cope, U. Muller-Eberhard, and E. J. Hansen. 1994. A functional tonB gene is required for both utilization of heme and virulence expression by Haemophilus influenzae type b. Infect. Immun. 62:2470-2477.
25. Kostman, J. R., B. L. Sherry, C. L. Flinger, S. Egaas, P. Sheeran, L. Baken, J. E. Bauwens, C. Clausen, D. M. Sherer, J. J. Plorde, T. L. Stull, and P. M. Mendelmen. 1993. Invasive Haemophilus influenzae infections in older children and adults in Seattle. Clin. Infect. Dis. 17:389-396.
26. 24a.Keyte, J. Personal communication.
27. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (London) 227:680-685.
28. Lee, B. C. 1992. Isolation of an outer membrane hemin-binding protein of Haemophilus influenzae type b. Infect. Immun. 60:810-816.
29. Lee, B. C. 1995. Quelling the red menace: haem capture by bacteria. Mol. Microbiol. 18:383-390.
30. Lee, B. C., and P. Hill. 1992. Identification of an outer-membrane haemoglobin-binding protein in Neisseria meningitidis. J. Gen. Microbiol. 138:2647-2656.
31. Legrain, M., V. Mazarin, S. W. Irwin, B. Bouchon, M. J. Quentin-Millet, E. Jacobs, and A. B. Schryvers. 1993. Cloning and characterization of Neisseria meningitidis genes encoding the transferrin-binding proteins Tbp1 and Tbp2. Gene 130:73-80.
32. Lewis, L. A., and D. W. Dyer. 1995. Identification of an iron-regulated outer membrane protein of Neisseria meningitidis involved in the utilization of hemoglobin complexed to haptoglobin. J. Bacteriol. 177:1299-1306.
33. Litwin, C. M., and S. B. Calderwood. 1993. Role of iron in regulation of virulence genes. Clin. Microbiol. Rev. 6:137-149.
34. Madorne, D. V., C. L. Johnson, D. C. Phipps, Pennridge Pediatric Associates, L. A. Popejoy, R. Eby, and D. H. Smith. 1990. Safety and immunologic response to Haemophilus influenzae type b oligosaccharide-CRM197 conjugate vaccine in 1 to 6-month-old infants. Pediatrics 85:331-337.
35. Moos, M. 1993. Isolation of proteins for microsequence analysis, p. 8.71-8.712. In J. E. Coligan, A. M. Kruisbeck, D. H. Margulies, E. M. Shevach, and W. Strober (ed.), Current protocols in immunology. John Wiley & Sons, New York.
36. Morton, D. J., J. M. Musser, and T. L. Stull. 1993. Expression of the Haemophilus influenzae transferrin receptor is repressible by hemin but not elemental iron alone. Infect. Immun. 61:4033-4037.
37. 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.
38. Morton, D. J., and P. Williams. 1990. Siderophore-independent acquisition of transferrin-bound iron by Haemophilus influenzae type b. J. Gen. Microbiol. 136:927-933.
39. Moxon, E. R., and K. A. Vaughan. 1981. Type b capsular polysaccharide as a virulence determinant of Haemophilus influenzae: studies using clinical isolates and laboratory transformants. J. Infect. Dis. 143:517-524.
40. Murphy, T. V., K. E. White, and P. Pastor. 1993. Declining incidence of Haemophilus influenzae type b disease since introduction of vaccination. JAMA 269:246-248.
41. Musser, J. M., S. J. Barenkamp, D. M. Granoff, and R. K. Selander. 1986. Genetic relationships of serologically nontypable and serotype b strains of Haemophilia influenzae. Infect. Immun. 52:183-191.
42. Otto, B. R., A. M. Verweij-van Vught, and D. M. MacLaren. 1992. Transferrins and heme-compounds as iron sources for pathogenic bacteria. Crit. Rev. Microbiol. 18:217-233.
43. Pidcock, K. A., J. A. Wooten, B. A. Daley, and T. L. Stull. 1988. Iron acquisition by Haemophilus inftuenzae. Infect. Immun. 56:721-725.
44. Postle, K. 1990. TonB and the gram-negative dilemma. Mol. Microbiol. 4:2019-2025.
45. Roberts, M., T. L. Stull, and A. L. Smith. 1981. Comparative virulence of Haemophilus influenzae with a type b or type d capsule. Infect. Immun. 32:518-524.
46. Sambrook, T., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
47. Schaffer, S., K. Hantke, and V. Braun. 1985. Nucleotide sequence of the iron regulatory gene fur. Mol. Gen. Genet. 200:110-113.
48. Shapiro, E. D., L. S. Capobianco, A. T. Berg, and M. Q. Zitt. 1989. The immunogenicity of Haemophilus influenzae type b polysaccharide-Neisseria meningitidis group B outer membrane protein complex vaccine in infants and young children. J. Infect. Dis. 160:1064-1066.
49. Stojiljkovic, I., V. Hwa, L. de Saint Martin, P. O'Gaora, X. Nassif, F. Heffron, and M. So. 1995. The Neisseria meningitidis haemoglobin receptor: its role in iron utilization and virulence. Mol. Microbiol. 15:531-541.
50. Stull, T. L. 1987. Protein sources of heme for Haemophilus influenzae. Infect. Immun. 55:148-153.
51. Stull, T. L., K. Mack, J. E. Haas, J. Smit, and A. L. Smith. 1985. A comparison of techniques for isolation of the outer membrane proteins of Haemophilus influenzae type b. Anal. Biochem. 150:471-480.
52. Szabo, M., D. Maskell, P. Butler, J. Love, and R. Moxon. 1992. Use of chromosomal gene fusions to investigate the role of repetitive DNA in regulation of genes involved in lipopolysaccharide biosynthesis in Haemophilus influenzae. J. Bacteriol. 174:7245-7252.
53. Teele, D. W., J. O. Klein, V. Rosner, and The Greater Boston Otitis Media Study Group. 1989. Epidemiology of otitis media during the first seven years of life in children in greater Boston: a prospective, cohort study. J. Infect. Dis. 160:83-94.
54. Turk, D. C. 1984. The pathogenicity of Haemophilus influenzae. J. Med. Microbiol. 18:1-16.
55. Wallace, R. J., D. M. Musher, and R. J. Martin. 1978. Haemophilus influenzae pneumonia in adults. Am. J. Med. 64:87-93.
56. Wenger, J. D., R. Pierce, K. Deaver, R. Fraklin, G. Bosley, N. Pigott, and C. V. Broome. 1992. Invasive Haemophilus influenzae disease: a population-based evaluation of the role of capsular polysaccharide serotype. J. Infect. Dis. 165:S34-S35.
57. 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.
58. Wong, J. C. Y., R. Patel, D. Kendall, P. W. Whitby, A. Smith, J. Holland, and P. Williams. 1995. Affinity, conservation, and surface exposure of hemopexin-binding proteins in Haemophilus influenzae. Infect. Immun. 63: 2327-2333.