Sap transporter mediated import and subsequent degradation of antimicrobial peptides in Haemophilus

PLoS Pathogens

Volumn 7, Issue 11, 2011, Pages

  Shelton, Catherine L ^a   Raffel, Forrest K ^a   Beatty, Wandy L ^b   Johnson, Sara M ^a   Mason, Kevin M ^a,c  

^a THE RESEARCH INSTITUTE AT NATIONWIDE CHILDREN S HOSPITAL   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; NEUTRALIZING ANTIBODY; PEPTIDASE; PERIPLASMIC BINDING PROTEIN; POLYPEPTIDE ANTIBIOTIC AGENT; SAP TRANSPORTER; UNCLASSIFIED DRUG; ANTIMICROBIAL CATIONIC PEPTIDE; BACTERIAL PROTEIN;

ANIMAL CELL; ARTICLE; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; CONTROLLED STUDY; CYTOPLASM; DRUG DEGRADATION; DRUG TRANSPORT; ENZYME ACTIVITY; HAEMOPHILUS INFLUENZAE; HOST RESISTANCE; NONHUMAN; PROTEIN LOCALIZATION; ANIMAL; CHINCHILLA; HAEMOPHILUS INFECTION; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PROTEIN BINDING;

BACTERIA (MICROORGANISMS); HAEMOPHILUS; HAEMOPHILUS INFLUENZAE;

ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; ATP-BINDING CASSETTE TRANSPORTERS; BACTERIAL PROTEINS; CHINCHILLA; HAEMOPHILUS INFECTIONS; HAEMOPHILUS INFLUENZAE; PROTEIN BINDING;

EID: 81755183017     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002360     Document Type: Article

References (61)

1. Brogden KA, (2005) Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat Rev Microbiol 3: 238-250.
2. Sitaram N, Nagaraj R, (2002) Host-defense antimicrobial peptides: importance of structure for activity. Curr Pharm Des 8: 727-742.
3. Stolzenberg ED, Anderson GM, Ackermann MR, Whitlock RH, Zasloff M, (1997) Epithelial antibiotic induced in states of disease. Proc Natl Acad Sci U S A 94: 8686-8690.
4. Harder J, Bartels J, Christophers E, Schroder JM, (2001) Isolation and characterization of human beta-defensin-3, a novel human inducible peptide antibiotic. J Biol Chem 276: 5707-5713.
5. Sorensen O, Arnljots K, Cowland JB, Bainton DF, Borregaard N, (1997) The human antibacterial cathelicidin, hCAP-18, is synthesized in myelocytes and metamyelocytes and localized to specific granules in neutrophils. Blood 90: 2796-2803.
6. Bals R, Wang X, Zasloff M, Wilson JM, (1998) The peptide antibiotic LL-37/hCAP-18 is expressed in epithelia of the human lung where it has broad antimicrobial activity at the airway surface. Proc Natl Acad Sci U S A 95: 9541-9546.
7. Salzman NH, Ghosh D, Huttner KM, Paterson Y, Bevins CL, (2003) Protection against enteric salmonellosis in transgenic mice expressing a human intestinal defensin. Nature 422: 522-526.
8. Selsted ME, Ouellette AJ, (2005) Mammalian defensins in the antimicrobial immune response. Nat Immunol 6: 551-557.
9. Lehrer RI, (2004) Paradise lost and paradigm found. Nat Immunol 5: 775-776.
10. Laube DM, Yim S, Ryan LK, Kisich KO, Diamond G, (2006) Antimicrobial peptides in the airway. Curr Top Microbiol Immunol 306: 153-182.
11. Nizet V, Ohtake T, Lauth X, Trowbridge J, Rudisill J, et al. (2001) Innate antimicrobial peptide protects the skin from invasive bacterial infection. Nature 414: 454-457.
12. Peschel A, (2002) How do bacteria resist human antimicrobial peptides? Trends Microbiol 10: 179-186.
13. Ernst RK, Guina T, Miller SI, (2001) Salmonella typhimurium outer membrane remodeling: role in resistance to host innate immunity. Microbes Infect 3: 1327-1334.
14. Kawasaki K, (2006) [Outer membrane remodeling of Salmonella typhimurium and host innate immunity]. Yakugaku Zasshi 126: 1227-1234.
15. Shafer WM, Qu X, Waring AJ, Lehrer RI, (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 U S A 95: 1829-1833.
16. Sieprawska-Lupa M, Mydel P, Krawczyk K, Wojcik K, Puklo M, et al. (2004) Degradation of human antimicrobial peptide LL-37 by Staphylococcus aureus-derived proteinases. Antimicrob Agents Chemother 48: 4673-4679.
17. Islam D, Bandholtz L, Nilsson J, Wigzell H, Christensson B, et al. (2001) Downregulation of bactericidal peptides in enteric infections: a novel immune escape mechanism with bacterial DNA as a potential regulator. Nat Med 7: 180-185.
18. Attia AS, Benson MA, Stauff DL, Torres VJ, Skaar EP, (2010) Membrane damage elicits an immunomodulatory program in Staphylococcus aureus. PLoS Pathog 6: e1000802.
19. Frick IM, Akesson P, Rasmussen M, Schmidtchen A, Bjorck L, (2003) SIC, a secreted protein of Streptococcus pyogenes that inactivates antibacterial peptides. J Biol Chem 278: 16561-16566.
20. Klein JO, (1997) Role of nontypeable Haemophilus influenzae in pediatric respiratory tract infections. Pediatr Infect Dis J 16: S5-8.
21. Kilpi T, Herva E, Kaijalainen T, Syrjanen R, Takala AK, (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.
22. Patel PB, Diaz MC, Bennett JE, Attia MW, (2007) Clinical features of bacterial conjunctivitis in children. Acad Emerg Med 14: 1-5.
23. Brook I, (2002) Bacteriology of acute and chronic frontal sinusitis. Arch Otolaryngol Head Neck Surg 128: 583-585.
24. Sethi S, (2000) Bacterial infection and the pathogenesis of COPD. Chest 117: 286S-291S.
25. Roman F, Canton R, Perez-Vazquez M, Baquero F, 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.
26. Lysenko ES, Gould J, Bals R, Wilson JM, Weiser JN, (2000) Bacterial phosphorylcholine decreases susceptibility to the antimicrobial peptide LL-37/hCAP18 expressed in the upper respiratory tract. Infect Immun 68: 1664-1671.
27. Starner TD, Swords WE, Apicella MA, McCray PB Jr, (2002) Susceptibility of nontypeable Haemophilus influenzae to human beta-defensins is influenced by lipooligosaccharide acylation. Infect Immun 70: 5287-5289.
28. Groisman EA, Parra-Lopez C, Salcedo M, Lipps CJ, Heffron F, (1992) Resistance to host antimicrobial peptides is necessary for Salmonella virulence. Proc Natl Acad Sci U S A 89: 11939-11943.
29. Parra-Lopez C, Baer MT, Groisman EA, (1993) Molecular genetic analysis of a locus required for resistance to antimicrobial peptides in Salmonella typhimurium. Embo J 12: 4053-4062.
30. Parra-Lopez C, Lin R, Aspedon A, Groisman EA, (1994) A Salmonella protein that is required for resistance to antimicrobial peptides and transport of potassium. Embo J 13: 3964-3972.
31. Eswarappa SM, Panguluri KK, Hensel M, Chakravortty D, (2008) The yejABEF operon of Salmonella confers resistance to antimicrobial peptides and contributes to its virulence. Microbiology 154: 666-678.
32. Lopez-Solanilla E, Garcia-Olmedo F, 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.
33. Chen HY, Weng SF, Lin JW, (2000) Identification and analysis of the sap genes from Vibrio fischeri belonging to the ATP-binding cassette gene family required for peptide transport and resistance to antimicrobial peptides. Biochem Biophys Res Commun 269: 743-748.
34. Harms C, Domoto Y, Celik C, Rahe E, Stumpe S, et al. (2001) Identification of the ABC protein SapD as the subunit that confers ATP dependence to the K+-uptake systems Trk(H) and Trk(G) from Escherichia coli K-12. Microbiology 147: 2991-3003.
35. Rodas PI, Contreras I, Mora GC, (2010) Salmonella enterica serovar Typhi has a 4.1 kb genetic island inserted within the sapABCDF operon that causes loss of resistance to the antimicrobial peptide protamine. J Antimicrob Chemother 65: 1624-1630.
36. Mount KL, Townsend CA, Rinker SD, Gu X, Fortney KR, et al. (2010) Haemophilus ducreyi SapA contributes to cathelicidin resistance and virulence in humans. Infect Immun 78: 1176-1184.
37. Mason KM, Bruggeman ME, Munson RS, Bakaletz LO, (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.
38. Mason KM, Munson RS Jr, Bakaletz LO, (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.
39. Mason KM, Raffel FK, Ray WC, Bakaletz LO, (2011) Heme Utilization by Nontypeable Haemophilus influenzae is Essential and Dependent on Sap Transporter Function. J Bacteriol 193: 2527-35.
40. Chromek M, Slamova Z, Bergman P, Kovacs L, Podracka L, et al. (2006) The antimicrobial peptide cathelicidin protects the urinary tract against invasive bacterial infection. Nat Med 12: 636-641.
41. McGillivary G, Mason KM, Jurcisek JA, Peeples ME, Bakaletz LO, (2009) Respiratory syncytial virus-induced dysregulation of expression of a mucosal beta-defensin augments colonization of the upper airway by non-typeable Haemophilus influenzae. Cell Microbiol 11: 1399-1408.
42. McGillivary G, Ray WC, Bevins CL, Munson RS Jr, Bakaletz LO, (2007) A member of the cathelicidin family of antimicrobial peptides is produced in the upper airway of the chinchilla and its mRNA expression is altered by common viral and bacterial co-pathogens of otitis media. Mol Immunol 44: 2446-2458.
43. Lim DJ, Chun YM, Lee HY, Moon SK, Chang KH, et al. (2000) Cell biology of tubotympanum in relation to pathogenesis of otitis media- a review. Vaccine 19 (Suppl 1): S17-25.
44. Gunn JS, Miller SI, (1996) PhoP-PhoQ activates transcription of pmrAB, encoding a two-component regulatory system involved in Salmonella typhimurium antimicrobial peptide resistance. J Bacteriol 178: 6857-6864.
45. McPhee JB, Bains M, Winsor G, Lewenza S, Kwasnicka A, et al. (2006) Contribution of the PhoP-PhoQ and PmrA-PmrB two-component regulatory systems to Mg2+-induced gene regulation in Pseudomonas aeruginosa. J Bacteriol 188: 3995-4006.
46. Bengoechea JA, Skurnik M, (2000) Temperature-regulated efflux pump/potassium antiporter system mediates resistance to cationic antimicrobial peptides in Yersinia. Mol Microbiol 37: 67-80.
47. Rinker SD, Trombley MP, Gu X, Fortney KR, Bauer ME, (2011) Deletion of mtrC in Haemophilus ducreyi increases sensitivity to human antimicrobial peptides and activates the CpxRA regulon. Infect Immun 79: 2324-34.
48. Harris RH, Wilk D, Bevins CL, Munson RS Jr, Bakaletz LO, (2004) Identification and characterization of a mucosal antimicrobial peptide expressed by the chinchilla (Chinchilla lanigera) airway. J Biol Chem 279: 20250-20256.
49. Iimura M, Gallo RL, Hase K, Miyamoto Y, Eckmann L, et al. (2005) Cathelicidin mediates innate intestinal defense against colonization with epithelial adherent bacterial pathogens. J Immunol 174: 4901-4907.
50. Shinnar AE, Butler KL, Park HJ, (2003) Cathelicidin family of antimicrobial peptides: proteolytic processing and protease resistance. Bioorg Chem 31: 425-436.
51. Sugimura K, Higashi N, (1988) A novel outer-membrane-associated protease in Escherichia coli. J Bacteriol 170: 3650-3654.
52. Sodeinde OA, Subrahmanyam YV, Stark K, Quan T, Bao Y, et al. (1992) A surface protease and the invasive character of plague. Science 258: 1004-1007.
53. Guina T, Yi EC, Wang H, Hackett M, Miller SI, (2000) A PhoP-regulated outer membrane protease of Salmonella enterica serovar typhimurium promotes resistance to alpha-helical antimicrobial peptides. J Bacteriol 182: 4077-4086.
54. Yeaman MR, Yount NY, (2003) Mechanisms of antimicrobial peptide action and resistance. Pharmacol Rev 55: 27-55.
55. Botos I, Melnikov EE, Cherry S, Khalatova AG, Rasulova FS, et al. (2004) Crystal structure of the AAA+ alpha domain of E. coli Lon protease at 1.9A resolution. J Struct Biol 146: 113-122.
56. McGillivray SM, Ebrahimi CM, Fisher N, Sabet M, Zhang DX, et al. (2009) ClpX contributes to innate defense peptide resistance and virulence phenotypes of Bacillus anthracis. J Innate Immun 1: 494-506.
57. Hancock RE, (1997) Peptide antibiotics. Lancet 349: 418-422.
58. Harrison A, Dyer DW, Gillaspy A, Ray WC, Mungur R, 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.
59. Harrison A, Ray WC, Baker BD, Armbruster DW, Bakaletz LO, et al. (2007) The OxyR regulon in nontypeable Haemophilus influenzae. J Bacteriol 189: 1004-1012.
60. Tracy E, Ye F, Baker BD, Munson RS Jr, (2008) Construction of non-polar mutants in Haemophilus influenzae using FLP recombinase technology. BMC Mol Biol 9: 101.
61. Wang B, Cleary PP, Xu H, Li JD, (2003) Up-regulation of interleukin-8 by novel small cytoplasmic molecules of nontypeable Haemophilus influenzae via p38 and extracellular signal-regulated kinase pathways. Infect Immun 71: 5523-5530.