Heme utilization by nontypeable haemophilus influenzae is essential and dependent on sap transporter function

Journal of Bacteriology

Volumn 193, Issue 10, 2011, Pages 2527-2535

  Mason, Kevin M ^a   Raffel, Forrest K ^a   Ray, William C ^b   Bakaletz, Lauren O ^a  

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

^b BATTELLE MEMORIAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BETA DEFENSIN 2; BETA DEFENSIN 3; CATHELICIDIN ANTIMICROBIAL PEPTIDE LL 37; HEME; HEME BINDING LIPOPROTEIN; LIPOPROTEIN; MELITTIN; MEMBRANE PROTEIN; NEUTROPHIL PROTEIN 1; PERMEASE; SAPA PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; ATOMIC EMISSION SPECTROMETRY; CHEMOLUMINESCENCE; CONTROLLED STUDY; CYTOPLASM; GENE DELETION; GENE MUTATION; HAEMOPHILUS INFLUENZAE; NONHUMAN; NONTYPEABLE HAEMOPHILUS INFLUENZAE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN TRANSPORT;

ALPHA-DEFENSINS; ANTIMICROBIAL CATIONIC PEPTIDES; BACTERIAL PROTEINS; BETA-DEFENSINS; HAEMOPHILUS INFLUENZAE; HEME; HUMANS; MELITTEN; MEMBRANE TRANSPORT PROTEINS; MODELS, MOLECULAR; PROTEIN BINDING; VIRULENCE FACTORS;

BACTERIA (MICROORGANISMS); HAEMOPHILUS; HAEMOPHILUS INFLUENZAE;

EID: 79956142965     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.01313-10     Document Type: Article

References (47)

1. Abouhamad, W. N., M. Manson, M. M. Gibson, and C. F. Higgins. 1991. Peptide transport and chemotaxis in Escherichia coli and Salmonella typhimurium: characterization of the dipeptide permease (Dpp) and the dipeptide-binding protein. Mol. Microbiol. 5:1035-1047.
2. Berntsson, R. P., et al. 2009. The structural basis for peptide selection by the transport receptor OppA. EMBO J. 28:1332-1340.
3. Bracken, C. S., M. T. Baer, A. Abdur-Rashid, W. Helms, and I. Stojiljkovic. 1999. Use of heme-protein complexes by the Yersinia enterocolitica HemR receptor: histidine residues are essential for receptor function. J. Bacteriol. 181:6063-6072.
4. Brogden, K. A. 2005. Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat. Rev. Microbiol. 3:238-250.
5. Burkhard, K. A., and A. Wilks. 2008. Functional characterization of the Shigella dysenteriae heme ABC transporter. Biochemistry 47:7977-7979.
6. Cope, L. D., et al. 1994. The 100 kDa haem:haemopexin-binding protein of Haemophilus influenzae: structure and localization. Mol. Microbiol. 13:863-873.
7. Dunten, P., and S. L. Mowbray. 1995. Crystal structure of the dipeptide binding protein from Escherichia coli involved in active transport and chemotaxis. Protein Sci. 4:2327-2334.
8. Dunten, P., and S. L. Mowbray. 1995. Modeling of the structure of the Haemophilus influenzae heme-binding protein suggests a mode of heme interaction. Protein Sci. 4:2335-2340.
9. Ganz, T. 2004. Antimicrobial polypeptides. J. Leukoc. Biol. 75:34-38.
10. 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.
11. 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.
12. G from Escherichia coli K-12. Microbiology 147:2991-3003.
13. Harrison, A., et al. 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.
14. Harrison, A., et al. 2007. The OxyR regulon in nontypeable Haemophilus influenzae. J. Bacteriol. 189:1004-1012.
15. Higgins, C. F. 2001. ABC transporters: physiology, structure and mechanism-an overview. Res. Microbiol. 152:205-210.
16. Kaur, A. P., I. B. Lansky, and A. Wilks. 2009. The role of the cytoplasmic heme-binding protein (PhuS) of Pseudomonas aeruginosa in intracellular heme trafficking and iron homeostasis. J. Biol. Chem. 284:56-66.
17. Klein, J. O. 1997. Role of nontypeable Haemophilus influenzae in pediatric respiratory tract infections. Pediatr. Infect. Dis. J. 16:S5-S8.
18. Létoffé, S., P. Delepelaire, and C. Wandersman. 2008. Functional differences between heme permeases: Serratia marcescens HemTUV permease exhibits a narrower substrate specificity (restricted to heme) than the Escherichia coli DppABCDF peptide-heme permease. J. Bacteriol. 190:1866-1870.
19. Létoffé, S., P. Delepelaire, and C. Wandersman. 2006. The housekeeping dipeptide permease is the Escherichia coli heme transporter and functions with two optional peptide binding proteins. Proc. Natl. Acad. Sci. U. S. A. 103:12891-12896.
20. Maciver, I., et al. 1996. Identification of an outer membrane protein involved in utilization of hemoglobin-haptoglobin complexes by nontypeable Haemophilus influenzae. Infect. Immun. 64:3703-3712.
21. Markel, T. A., et al. 2007. The struggle for iron: gastrointestinal microbes modulate the host immune response during infection. J. Leukoc. Biol. 81: 393-400.
22. Mason, K. M., M. E. Bruggeman, R. S. Munson, and L. O. Bakaletz. 2006. The non-typeable Haemophilus influenzae Sap transporter provides a mechanism of antimicrobial peptide resistance and SapD-dependent potassium acquisition. Mol. Microbiol. 62:1357-1372.
23. Mason, K. M., R. S. Munson, Jr., and L. O. Bakaletz. 2005. A mutation in the sap operon attenuates survival of nontypeable Haemophilus influenzae in a chinchilla model of otitis media. Infect. Immun. 73:599-608.
24. Mason, K. M., R. S. Munson, Jr., and L. O. Bakaletz. 2003. Nontypeable Haemophilus influenzae gene expression induced in vivo in a chinchilla model of otitis media. Infect. Immun. 71:3454-3462.
25. Morton, D. J., et al. 2004. Reduced severity of middle ear infection caused by nontypeable Haemophilus influenzae lacking the hemoglobin/hemoglobinhaptoglobin binding proteins (Hgp) in a chinchilla model of otitis media. Microb. Pathog. 36:25-33.
26. Morton, D. J., et al. 2005. The heme-binding lipoprotein (HbpA) of Haemophilus influenzae: role in heme utilization. FEMS Microbiol. Lett. 253: 193-199.
27. Morton, D. J., et al. 2009. The heme-binding protein (HbpA) of Haemophilus influenzae as a virulence determinant. Int. J. Med. Microbiol. 299:479-488.
28. Morton, D. J., T. W. Seale, T. M. Vanwagoner, P. W. Whitby, and T. L. Stull. 2009. The dppBCDF gene cluster of Haemophilus influenzae: role in heme utilization. BMC Res. Notes 2:166.
29. Morton, D. J., et al. 2004. Identification of a haem-utilization protein (Hup) in Haemophilus influenzae. Microbiology 150:3923-3933.
30. Murphy, T. F. 2003. Respiratory infections caused by non-typeable Haemophilus influenzae. Curr. Opin. Infect. Dis. 16:129-134.
31. Nizet, V. 2006. Antimicrobial peptide resistance mechanisms of human bacterial pathogens. Curr. Issues Mol. Biol. 8:11-26.
32. Occhino, D. A., E. E. Wyckoff, D. P. Henderson, T. J. Wrona, and S. M. Payne. 1998. Vibrio cholerae iron transport: haem transport genes are linked to one of two sets of tonB, exbB, exbD genes. Mol. Microbiol. 29:1493-1507.
33. Parra-Lopez, C., M. T. Baer, and E. A. Groisman. 1993. Molecular genetic analysis of a locus required for resistance to antimicrobial peptides in Salmonella typhimurium. EMBO J. 12:4053-4062.
34. Parra-Lopez, C., R. Lin, A. Aspedon, and E. A. Groisman. 1994. A Salmonella protein that is required for resistance to antimicrobial peptides and transport of potassium. EMBO J. 13:3964-3972.
35. Peschel, A. 2002. How do bacteria resist human antimicrobial peptides? Trends Microbiol. 10:179-186.
36. Poolman, B., et al. 2005. Functional analysis of detergent-solubilized and membrane-reconstituted ATP-binding cassette transporters. Methods Enzymol. 400:429-459.
37. Ren, Z., H. Jin, D. J. Morton, and T. L. Stull. 1998. hgpB, a gene encoding a second Haemophilus influenzae hemoglobin- and hemoglobin-haptoglobinbinding protein. Infect. Immun. 66:4733-4741.
38. Román, F., R. Canton, M. Perez-Vazquez, F. Baquero, and J. Campos. 2004. Dynamics of long-term colonization of respiratory tract by Haemophilus influenzae in cystic fibrosis patients shows a marked increase in hypermutable strains. J. Clin. Microbiol. 42:1450-1459.
39. Saier, M. H., Jr. 2000. A functional-phylogenetic classification system for transmembrane solute transporters. Microbiol. Mol. Biol. Rev. 64:354-411.
40. Sethi, S., and T. F. Murphy. 2001. Bacterial infection in chronic obstructive pulmonary disease in 2000: a state-of-the-art review. Clin. Microbiol. Rev. 14:336-363.
41. Shepherd, M., M. D. Heath, and R. K. Poole. 2007. NikA binds heme: a new role for an Escherichia coli periplasmic nickel-binding protein. Biochemistry 46:5030-5037.
42. St. Geme, J. W., III. 2000. The pathogenesis of nontypable Haemophilus influenzae otitis media. Vaccine 19(Suppl. 1):S41-S50.
43. Stojiljkovic, I., and K. Hantke. 1994. Transport of haemin across the cytoplasmic membrane through a haemin-specific periplasmic binding-proteindependent transport system in Yersinia enterocolitica. Mol. Microbiol. 13: 719-732.
44. Stojiljkovic, I., and D. Perkins-Balding. 2002. Processing of heme and hemecontaining proteins by bacteria. DNA Cell Biol. 21:281-295.
45. Thompson, J. M., H. A. Jones, and R. D. Perry. 1999. Molecular characterization of the hemin uptake locus (hmu) from Yersinia pestis and analysis of hmu mutants for hemin and hemoprotein utilization. Infect. Immun. 67: 3879-3892.
46. Tracy, E., F. Ye, B. D. Baker, and R. S. Munson, Jr. 2008. Construction of non-polar mutants in Haemophilus influenzae using FLP recombinase technology. BMC Mol. Biol. 9:101.
47. Vergauwen, B., J. Elegheert, A. Dansercoer, B. Devreese, and S. N. Savvides. 2010. Glutathione import in Haemophilus influenzae Rd is primed by the periplasmic heme-binding protein HbpA. Proc. Natl. Acad. Sci. U. S. A. 107:13270-13275.