The non-typeable Haemophilus influenzae Sap transporter provides a mechanism of antimicrobial peptide resistance and SapD-dependent potassium acquisition

Molecular Microbiology

Volumn 62, Issue 5, 2006, Pages 1357-1372

  Mason, Kevin M ^a   Bruggeman, Molly E ^a   Munson, Robert S ^a   Bakaletz, Lauren O ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA DEFENSIN 1; BINDING PROTEIN; POLYPEPTIDE ANTIBIOTIC AGENT; PROTEIN; RECOMBINANT PROTEIN; SENSITIVITY TO ANTIMICROBIAL PEPTIDE A; SENSITIVITY TO ANTIMICROBIAL PEPTIDE D; UNCLASSIFIED DRUG;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GROWTH; BACTERIAL SURVIVAL; CHINCHILLA; CONTROLLED STUDY; GENE ACTIVITY; GENE EXPRESSION REGULATION; GENE MUTATION; GENETIC COMPLEMENTATION; HAEMOPHILUS INFLUENZAE; NONHUMAN; OPERON; OTITIS MEDIA; POTASSIUM TRANSPORT; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FUNCTION; UPREGULATION;

ANIMALS; ANTI-BACTERIAL AGENTS; ATP-BINDING CASSETTE TRANSPORTERS; BIOLOGICAL TRANSPORT, ACTIVE; CHINCHILLA; DRUG RESISTANCE, BACTERIAL; HAEMOPHILUS INFECTIONS; HAEMOPHILUS INFLUENZAE; MICROBIAL SENSITIVITY TESTS; MULTIGENE FAMILY; POTASSIUM CHANNELS;

BACTERIA (MICROORGANISMS); HAEMOPHILUS INFLUENZAE;

EID: 33750707543     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2006.05460.x     Document Type: Article

References (85)

1. Abouhamad, W.N., Manson, M., Gibson, M.M., and Higgins, C.F. (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. Aspedon, A., and Groisman, E.A. (1996) The antibacterial action of protamine: evidence for disruption of cytoplasmic membrane energization in Salmonella typhimurium. Microbiology 142: 3389-3397.
3. Bader, M.W., Sanowar, S., Daley, M.E., Schneider, A.R., Cho, U., Xu, W., et al. (2005) Recognition of antimicrobial peptides by a bacterial sensor kinase. Cell 122: 461-472.
4. Bakaletz, L.O. (2002) Otitis media. In Polymicrobial Diseases. Brogden, K.A., Guthmiller, J.M. (eds). Washington DC: American Society for Microbiology Press, pp. 259-298.
5. Bakaletz, L.O., Leake, E.R., Billy, J.M., and Kaumaya, P.T. (1997) 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: 955-961.
6. Bakaletz, L.O., Baker, B.D., Jurcisek, J.A., Harrison, A., Novotny, L.A., Bookwalter, J.E., et al. (2005) Demonstration of Type IV pilus expression and a twitching phenotype by Haemophilus influenzae. Infect Immun 73: 1635-1643.
7. Bakker, E.P., and Harold, F.M. (1980) Energy coupling to potassium transport in Streptococcus faecalis. Interplay of ATP and the protonmotive force. J Biol Chem 255: 433-440.
8. Bakker, E.P., and Mangerich, W.E. (1981) Interconversion of components of the bacterial proton motive force by electrogenic potassium transport. J Bacteriol 147: 820-826.
9. Bayer, A.S., Prasad, R., Chandra, J., Koul, A., Smriti, M., Varma, A., et al. (2000) In vitro resistance of Staphylococcus aureus to thrombin-induced platelet microbicidal protein is associated with alterations in cytoplasmic membrane fluidity. Infect Immun 68: 3548-3553.
10. Bengoechea, J.A., and Skurnik, M. (2000) Temperature-regulated efflux pump/potassium antiporter system mediates resistance to cationic antimicrobial peptides in Yersinia. Mol Microbiol 37: 67-80.
11. +-transport protein TrkA of Escherichia coli is a peripheral membrane protein that requires other trk gene products for attachment to the cytoplasmic membrane. J Biol Chem 264: 16403-16410.
12. Coleman, H.N., Daines, D.A., Jarisch, J., and Smith, A.L. (2003) Chemically defined media for growth of Haemophilus influenzae strains. J Clin Microbiol 41: 4408-4410.
13. Csonka, L.N. (1989) Physiological and genetic responses of bacteria to osmotic stress. Microbiol Rev 53: 121-147.
14. Derzelle, S., Turlin, E., Duchaud, E., Pages, S., Kunst, F., Givaudan, A., and Danchin, A. (2004) The PhoP-PhoQ two-component regulatory system of Photorhabdus luminescens is essential for virulence in insects. J Bacteriol 186: 1270-1279.
15. Dosch, D.C., Helmer, G.L., Sutton, S.H., Salvacion, F.F., and Epstein, W. (1991) Genetic analysis of potassium transport loci in Escherichia coli: evidence for three constitutive systems mediating uptake potassium. J Bacteriol 173: 687-696.
16. Douglas, R.M., Ritchie, G.Y., Munro, A.W., McLaggan, D., and Booth, I.R. (1994) The K(+)-efflux system, KefC. Escherichia coli: genetic evidence for oligomeric structure. Mol Membr Biol 11: 55-61.
17. Ernst, R.K., Yi, E.C., Guo, L., Lim, K.B., Burns, J.L., Hackett, M., and Miller, S.I. (1999) Specific lipopolysaccharide found in cystic fibrosis airway Pseudomonas aeruginosa. Science 286: 1561-1565.
18. Fields, P.I., Groisman, E.A., and Heffron, F. (1989) A Salmonella locus that controls resistance to microbicidal proteins from phagocytic cells. Science 243: 1059-1062.
19. Freer, E., Moreno, E., Moriyon, I., Pizarro-Cerda, J., Weintraub, A., and Gorvel, J.P. (1996) Brucella-Salmonella lipopolysaccharide chimeras are less permeable to hydrophobic probes and more sensitive to cationic peptides and EDTA than are their native Brucella sp. counterparts. J Bacteriol 178: 5867-5876.
20. Groisman, E.A., Parra-Lopez, C., Salcedo, M., Lipps, C.J., and Heffron, F. (1992) Resistance to host antimicrobial peptides is necessary for Salmonella virulence. Proc Natl Acad Sci USA 89: 11939-11943.
21. Guina, T., Yi, E.C., Wang, H., Hackett, M., and Miller, S.I. (2000) A PhoP-regulated outer membrane protease of Salmonella enterica serovar typhimurium promotes resistance to alpha-helical antimicrobial peptides. J Bacteriol 182: 4077-4086.
22. Gunn, J.S., Lim, K.B., Krueger, J., Kim, K., Guo, L., Hackett, M., and Miller, S.I. (1998) PmrA-PmrB-regulated genes necessary for 4-aminoarabinose lipid A modification and polymyxin resistance. Mol Microbiol 27: 1171-1182.
23. Guo, L., Lim, K.B., Gunn, J.S., Bainbridge, B., Darveau, R.P., Hackett, M., and Miller, S.I. (1997) Regulation of lipid A modifications by Salmonella typhimurium virulence genes phoP-phoQ. Science 276: 250-253.
24. Guo, L., Lim, K.B., Poduje, C.M., Daniel, M., Gunn, J.S., Hackett, M., and Miller, S.I. (1998) Lipid A acylation and bacterial resistance against vertebrate antimicrobial peptides. Cell 95: 189-198.
25. Hancock, R.E., and Chapple, D.S. (1999) Peptide antibiotics. Antimicrob Agents Chemother 43: 1317-1323.
26. G from Escherichia coli K-12. Microbiology 147: 2991-3003.
27. Harris, R.H., Wilk, D., Bevins, C.L., Munson, R.S., Jr, and Bakaletz, L.O. (2004) Identification and characterization of a mucosal antimicrobial peptide expressed by the chinchilla (Chinchilla lanigera) airway. J Biol Chem 279: 20250-20256.
28. Harrison, A., Dyer, D.W., Gillaspy, A., Ray, W.C., Mungur, R., Carson, M.B., 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.
29. Heikkinen, T., and Chonmaitree, T. (2003) Importance of respiratory viruses in acute otitis media. Clin Microbiol Rev 16: 230-241.
30. Higgins, C.F. (1992) ABC transporters: from microorganisms to man. Annu Rev Cell Biol 8: 67-113.
31. Hiles, I.D., Gallagher, M.P., Jamieson, D.J., and Higgins, C.F. (1987) Molecular characterization of the oligopeptide permease of Salmonella typhimurium. J Mol Biol 195: 125-142.
32. Hoffmann, J.A., Kafatos, F.C., Janeway, C.A., and Ezekowitz, R.A. (1999) Phylogenetic perspectives in innate immunity. Science 284: 1313-1318.
33. Infante-Rivard, C., and Fernandez, A. (1993) Otitis media in children: frequency, risk factors, and research avenues. Epidemiol Rev 15: 444-465.
34. Karlsson, R., Michaelsson, A., and Mattsson, L. (1991) Kinetic analysis of monoclonal antibody-antigen interactions with a new biosensor based analytical system. J Immunol Meth 145: 229-240.
35. Kennedy, B.J., Novotny, L.A., Jurcisek, J.A., Lobet, Y., and Bakaletz, L.O. (2000) 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: 2756-2765.
36. Kilpi, T., Herva, E., Kaijalainen, T., Syrjanen, R., and Takala, A.K. (2001) Bacteriology of acute otitis media in a cohort of Finnish children followed for the first two years of life. Pediatr Infect Dis J 20: 654-662.
37. Kim, H.J., Kim, S.S., Lee, M.H., Lee, B.J., and Ryu, P.D. (2004) Role of C-terminal heptapeptide in pore-forming activity of antimicrobial agent, gaegurin 4. J Pept Res 64: 151-158.
38. Klein, J.O. (1997) Role of nontypeable Haemophilus influenzae in pediatric respiratory tract infections. Pediatr Infect Dis J 16: S5-S8.
39. T. J Bacteriol 187: 1036-1043.
40. Lee, H.Y., Andalibi, A., Webster, P., Moon, S.K., Teufert, K., Kang, S.H., et al. (2004) Antimicrobial activity of innate immune molecules against Streptococcus pneumoniae, Moraxella catarrhalis and nontypeable Haemophilus influenzae. BMC Infect Dis 4: 12.
41. Lee, S.H., Kim, J.E., Lim, H.H., Lee, H.M., and Choi, J.O. (2002) Antimicrobial defensin peptides of the human nasal mucosa. Ann Otol Rhinol Laryngol 111: 135-141.
42. Lopez-Solanilla, E., Garcia-Olmedo, F., and Rodriguez-Palenzuela, P. (1998) Inactivation of the sapA to sapF locus of Erwinia chrysanthemi reveals common features in plant and animal bacterial pathogenesis. Plant Cell 10: 917-924.
43. McCoy, A.J., Liu, H., Falla, T.J., and Gunn, J.S. (2001) Identification of Proteus mirabilis mutants with increased sensitivity to antimicrobial peptides. Antimicrob Agents Chemother 45: 2030-2037.
44. Martinez de Tejada, G., Pizarro-Cerda, J., Moreno, E., and Moriyon, I. (1995) The outer membranes of Brucella spp. are resistant to bactericidal cationic peptides. Infect Immun 63: 3054-3061.
45. Mason, K.M., Munson, R.S., Jr, and Bakaletz, L.O. (2003) Nontypeable Haemophilus influenzae gene expression induced in vivo in a chinchilla model of otitis media. Infect Immun 71: 3454-3462.
46. Mason, K.M., Munson, R.S., Jr, and Bakaletz, L.O. (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.
47. Matsuda, N., Kobayashi, H., Katoh, H., Ogawa, T., Futatsugi, L., Nakamura, T., et al. (2004) Na+-dependent K+ uptake Ktr system from the cyanobacterium Synechocystis sp. PCC 6803 and its role in the early phases of cell adaptation to hyperosmotic shock. J Biol Chem 279: 54952-54962.
48. Matsuzaki, K., Fukui, M., Fujii, N., and Miyajima, K. (1991) Interactions of an antimicrobial peptide, tachyplesin I, with lipid membranes. Biochim Biophys Acta 1070: 259-264.
49. Matsuzaki, K., Sugishita, K., Harada, M., Fujii, N., and Miyajima, K. (1997) Interactions of an antimicrobial peptide, magainin 2, with outer and inner membranes of Gram-negative bacteria. Biochim Biophys Acta 1327: 119-130.
50. Matsuzaki, K., Sugishita, K., and Miyajima, K. (1999) Interactions of an antimicrobial peptide, magainin 2, with lipopolysaccharide-containing liposomes as a model for outer membranes of Gram-negative bacteria. FEBS Lett 449: 221-224.
51. Meury, J., and Robin, A. (1990) Glutathione-gated K+ channels of Escherichia coli carry out K+ efflux controlled by the redox state of the cell. Arch Microbiol 154: 475-482.
52. Moon, S.K., Lee, H.Y., Li, J.D., Nagura, M., Kang, S.H., Chun, Y.M., et al. (2002) Activation of a Src-dependent Raf-MEK1/2-ERK signaling pathway is required for IL-1alpha-induced upregulation of beta-defensin 2 in human middle ear epithelial cells. Biochim Biophys Acta 1590: 41-51.
53. Moss, J.E., Fisher, P.E., Vick, B., Groisman, E.A., and Zychlinsky, A. (2000) The regulatory protein PhoP controls susceptibility to the host inflammatory response in Shigella flexneri. Cell Microbiol 2: 443-452.
54. Munson, R.S., Jr, Harrison, A., Gillaspy, A., Ray, W.C., Carson, M., Armbruster, D., et al. (2004) Partial analysis of the genomes of two nontypeable Haemophilus influenzae otitis media isolates. Infect Immun 72: 3002-3010.
55. Murphy, T.F. (2003) Respiratory infections caused by nontypeable Haemophilus influenzae. Curr Opin Infect Dis 16: 129-134.
56. +-uptake system of Vibrio alginolyticus. Microbiology 144: 2281-2289.
57. + efflux systems. J Biol Chem 274: 9524-9530.
58. Novotny, L.A., Jurcisek, J.A., Pichichero, M.E., and Bakaletz, L.O. (2000) Epitope mapping of the outer membrane protein P5-homologous fimbrin adhesin of nontypeable Haemophilus influenzae. Infect Immun 68: 2119-2128.
59. Ohmizo, C., Yata, M., and Katsu, T. (2004) Bacterial cytoplasmic membrane permeability assay using ion-selective electrodes. J Microbiol Meth 59: 173-179.
60. Parra-Lopez, C., Baer, M.T., and Groisman, E.A. (1993) Molecular genetic analysis of a locus required for resistance to antimicrobial peptides in Salmonella typhimurium. EMBO J 12: 4053-4062.
61. Parra-Lopez, C., Lin, R., Aspedon, A., and Groisman, E.A. (1994) A Salmonella protein that is required for resistance to antimicrobial peptides and transport of potassium. EMBO J 13: 3964-3972.
62. Paustian, M.L., May, B.J., Cao, D., Boley, D., and Kapur, V. (2002) Transcriptional response of Pasteurella multocida to defined iron sources. J Bacteriol 184: 6714-6720.
63. Perego, M., and Hoch, J.A. (1991) Negative regulation of Bacillus subtilis sporulation by the spo0E gene product. J Bacteriol 173: 2514-2520.
64. Peschel, A. (2002) How do bacteria resist human antimicrobial peptides? Trends Microbiol 10: 179-186.
65. Peschel, A., Otto, M., Jack, R.W., Kalbacher, H., Jung, G., and Gotz, F. (1999) Inactivation of the dlt operon in Staphylococcus aureus confers sensitivity to defensins, protegrins, and other antimicrobial peptides. J Biol Chem 274: 8405-8410.
66. Porter, E.M., Poles, M.A., Lee, J.S., Naitoh, J., Bevins, C.L., and Ganz, T. (1998) Isolation of human intestinal defensins from ileal neobladder urine. FEBS Lett 434: 272-276.
67. Rebeil, R., Ernst, R.K., Gowen, B.B., Miller, S.I., and Hinnebusch, B.J. (2004) Variation in lipid A structure in the pathogenic yersiniae. Mol Microbiol 52: 1363-1373.
68. + transport in Escherichia coli K-12. J Biol Chem 252: 1394-1401.
69. Rhoads, D.B., Waters, F.B., and Epstein, W. (1976) Cation transport in Escherichia coli. VIII. Potassium transport mutants. J Gen Physiol 67: 325-341.
70. Richey, B., Cayley, D.S., Mossing, M.C., Kolka, C., Anderson, C.F., Farrar, T.C., and Record, M.T., Jr (1987) Variability of the intracellular ionic environment of Escherichia coli. Differences between in vitro and in vivo effects of ion concentrations on protein-DNA interactions and gene expression. J Biol Chem 262: 7157-7164.
71. Roman, F., Canton, R., Perez-Vazquez, M., Baquero, F., and Campos, J. (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.
72. St Geme, J.W., 3rd (2000) The pathogenesis of nontypable Haemophilus influenzae otitis media. Vaccine 19 (Suppl. 1): S41-S50.
73. Schibli, D.J., Hunter, H.N., Aseyev, V., Starner, T.D., Wiencek, J.M., McCray, P.B., Jr, et al. (2002) The solution structures of the human beta-defensins lead to a better understanding of the potent bactericidal activity of HBD3 against Staphylococcus aureus. J Biol Chem 277: 8279-8289.
74. Schlosser, A., Meldorf, M., Stumpe, S., Bakker, E.P., and Epstein, W. (1995) TrkH and its homolog, TrkG, determine the specificity and kinetics of cation transport by the Trk system of Escherichia coli. J Bacteriol 177: 1908-1910.
75. Sethi, S., and Murphy, T.F. (2001) Bacterial infection in chronic obstructive pulmonary disease in 2000: a state-of-the-art review. Clin Microbiol Rev 14: 336-363.
76. Shafer, W.M., Qu, X., Waring, A.J., and Lehrer, R.I. (1998) Modulation of Neisseria gonorrhoeae susceptibility to vertebrate antibacterial peptides due to a member of the resistance/nodulation/division efflux pump family. Proc Natl Acad Sci USA 95: 1829-1833.
77. Sirakova, T., Kolattukudy, P.E., Murwin, D., Billy, J., Leake, E., Lim, D., et al. (1994) Role of fimbriae expressed by nontypeable Haemophilus influenzae in pathogenesis of and protection against otitis media and relatedness of the fimbrin subunit to outer membrane protein A. Infect Immun 62: 2002-2020.
78. + uptake via the Trk system in Escherichia coli: the role of ATP. J Gen Microbiol 131: 77-85.
79. +-uptake capacity and of extracytoplasmic protease activity for protamine resistance of Escherichia coli. Arch Microbiol 167: 126-136.
80. Stumpe, S., Schmid, R., Stephens, D.L., Georgiou, G., and Bakker, E.P. (1998) Identification of OmpT as the protease that hydrolyzes the antimicrobial peptide protamine before it enters growing cells of Escherichia coli. J Bacteriol 180: 4002-4006.
81. Suzuki, K., and Bakaletz, L.O. (1994) Synergistic effect of adenovirus type 1 and nontypeable Haemophilus influenzae in a chinchilla model of experimental otitis media. Infect Immun 62: 1710-1718.
82. Tholema, N., Bakker, E.P., Suzuki, A., and Nakamura, T. (1999) Change to alanine of one out of four selectivity filter glycines in KtrB causes a two orders of magnitude decrease in the affinities for both K+ and Na+ of the Na+ dependent K+ uptake system KtrAB from Vibrio alginolyticus. FEBS Lett 450: 217-220.
83. Tholema, N., Vor der Bruggen, M., Maser, P., Nakamura, T., Schroeder, J.I., Kobayashi, H., et al. (2005) All four putative selectivity filter glycine residues in KtrB are essential for high affinity and selective K+ uptake by the KtrAB system from Vibrio alginolyticus. J Biol Chem 280: 41146-41154.
84. Wang, M.S., Pang, J.S., and Selsted, M.E. (1997) Semidry electroblotting of peptides and proteins from acid-urea polyacrylamide gels. Anal Biochem 253: 225-230.
85. White, S.H., Wimley, W.C., and Selsted, M.E. (1995) Structure, function, and membrane integration of defensins. Curr Opin Struct Biol 5: 521-527.