Role of Bacterial Surface Structures on the Interaction of Klebsiella pneumoniae with Phagocytes

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  March, Catalina ^a,b   Cano, Victoria ^a,b   Moranta, David ^a,b   Llobet, Enrique ^a,b   Pérez Gutiérrez, Camino ^a,b   Tomás, Juan M ^c   Suárez, Teresa ^d   Garmendia, Junkal ^a,b,e   Bengoechea, José A ^a,b,e  

^a Laboratory Microbial Pathogenesis   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

^c UNIVERSITY OF BARCELONA   (Spain)

^d CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

^e CSIC   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

AMINOARABINOSE; ARABINOSE; BACTERIUM LIPOPOLYSACCHARIDE; LIPID A; OUTER MEMBRANE PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL CELL; BACTERIAL STRAIN; BACTERICIDAL ACTIVITY; BACTERIUM MUTANT; CONTROLLED STUDY; DICTYOSTELIUM DISCOIDEUM; FEMALE; HOST PATHOGEN INTERACTION; KLEBSIELLA PNEUMONIAE INFECTION; LUNG ALVEOLUS MACROPHAGE; MOUSE; NONHUMAN; NUTRIENT CONCENTRATION; ORGANISMAL INTERACTION; PALMITOYLATION; PHAGOCYTE; PHAGOCYTOSIS; PREDATION;

ANIMALS; ARABINOSE; BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL PROTEINS; CARBOHYDRATE SEQUENCE; DICTYOSTELIUM; FEMALE; HOST-PATHOGEN INTERACTIONS; KLEBSIELLA PNEUMONIAE; LIPID A; MACROPHAGES, ALVEOLAR; MICE; MOLECULAR SEQUENCE DATA; MUTATION; O ANTIGENS; PALMITIC ACID; PHAGOCYTES; PHAGOCYTOSIS; PORINS;

EID: 84874066976     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0056847     Document Type: Article

References (63)

1. Bozzaro S, Bucci C, Steinert M, (2008) Phagocytosis and host-pathogen interactions in Dictyostelium with a look at macrophages. Int Rev Cell Mol Biol 271: 253-300.
2. Cardelli J, (2001) Phagocytosis and macropinocytosis in Dictyostelium: phosphoinositide-based processes, biochemically distinct. Traffic 2: 311-320.
3. Cosson P, Soldati T, (2008) Eat, kill or die: when amoeba meets bacteria. Curr Opin Microbiol 11: 271-276.
4. Hilbi H, Weber SS, Ragaz C, Nyfeler Y, Urwyler S, (2007) Environmental predators as models for bacterial pathogenesis. Environ Microbiol 9: 563-575.
5. Eichinger L, Pachebat JA, Glockner G, Rajandream MA, Sucgang R, et al. (2005) The genome of the social amoeba Dictyostelium discoideum. Nature 435: 43-57.
6. Sahly H, Podschun R, (1997) Clinical, bacteriological, and serological aspects of Klebsiella infections and their spondylarthropathic sequelae. Clin Diagn Lab Immunol 4: 393-399.
7. Nordmann P, Cuzon G, Naas T, (2009) The real threat of Klebsiella pneumoniae carbapenemase-producing bacteria. Lancet Infect Dis 9: 228-236.
8. Bagley ST, (1985) Habitat association of Klebsiella species. Infect Control 6: 52-58.
9. Struve C, Krogfelt KA, (2004) Pathogenic potential of environmental Klebsiella pneumoniae isolates. Environ Microbiol 6: 584-590.
10. Broug-Holub E, Toews GB, van Iwaarden JF, Strieter RM, Kunkel SL, et al. (1997) Alveolar macrophages are required for protective pulmonary defenses in murine Klebsiella pneumonia: elimination of alveolar macrophages increases neutrophil recruitment but decreases bacterial clearance and survival. Infect Immun 65: 1139-1146.
11. Cheung DO, Halsey K, Speert DP, (2000) Role of pulmonary alveolar macrophages in defense of the lung against Pseudomonas aeruginosa. Infect Immun 68: 4585-4592.
12. Alvarez D, Merino S, Tomas JM, Benedi VJ, Alberti S, (2000) Capsular polysaccharide is a major complement resistance factor in lipopolysaccharide O side chain-deficient Klebsiella pneumoniae clinical isolates. Infect Immun 68: 953-955.
13. Cortes G, Borrell N, de Astorza B, Gomez C, Sauleda J, et al. (2002) Molecular analysis of the contribution of the capsular polysaccharide and the lipopolysaccharide O side chain to the virulence of Klebsiella pneumoniae in a murine model of pneumonia. Infect Immun 70: 2583-2590.
14. Regueiro V, Campos MA, Pons J, Alberti S, Bengoechea JA, (2006) The uptake of a Klebsiella pneumoniae capsule polysaccharide mutant triggers an inflammatory response by human airway epithelial cells. Microbiology 152: 555-566.
15. Camprubi S, Merino S, Benedi VJ, Tomas JM, (1993) The role of the O-antigen lipopolysaccharide and capsule on an experimental Klebsiella pneumoniae infection of the rat urinary tract. FEMS Microbiol Lett 111: 9-13.
16. Lawlor MS, Hsu J, Rick PD, Miller VL, (2005) Identification of Klebsiella pneumoniae virulence determinants using an intranasal infection model. Mol Microbiol 58: 1054-1073.
17. Benghezal M, Fauvarque MO, Tournebize R, Froquet R, Marchetti A, et al. (2006) Specific host genes required for the killing of Klebsiella bacteria by phagocytes. Cell Microbiol 8: 139-148.
18. Hsieh PF, Lin TL, Yang FL, Wu MC, Pan YJ, et al. (2012) Lipopolysaccharide O1 antigen contributes to the virulence in Klebsiella pneumoniae causing pyogenic liver abscess. PLoS ONE 7: e33155.
19. Pan YJ, Lin TL, Hsu CR, Wang JT, (2011) Use of a Dictyostelium model for isolation of genetic loci associated with phagocytosis and virulence in Klebsiella pneumoniae. Infect Immun 79: 997-1006.
20. Raetz CR, Reynolds CM, Trent MS, Bishop RE, (2007) Lipid A modification systems in gram-negative bacteria. Annu Rev Biochem 76: 295-329.
21. Gunn JS, Lim KB, Krueger J, Kim K, Guo L, et al. (1998) PmrA-PmrB-regulated genes necessary for 4-aminoarabinose lipid A modification and polymyxin resistance. Mol Microbiol 27: 1171-1182.
22. Gunn JS, Ryan SS, Van Velkinburgh JC, Ernst RK, Miller SI, (2000) Genetic and functional analysis of a PmrA-PmrB-regulated locus necessary for lipopolysaccharide modification, antimicrobial peptide resistance, and oral virulence of Salmonella enterica serovar typhimurium. Infect Immun 68: 6139-6146.
23. Guo L, Lim KB, Poduje CM, Daniel M, Gunn JS, et al. (1998) Lipid A acylation and bacterial resistance against vertebrate antimicrobial peptides. Cell 95: 189-98.
24. Lee H, Hsu FF, Turk J, Groisman EA, (2004) The PmrA-regulated pmrC gene mediates phosphoethanolamine modification of lipid A and polymyxin resistance in Salmonella enterica. J Bacteriol 186: 4124-4133.
25. Nizet V, (2006) Antimicrobial peptide resistance mechanisms of human bacterial pathogens. Curr Issues Mol Biol 8: 11-26.
26. Llobet E, Campos MA, Gimenez P, Moranta D, Bengoechea JA, (2011) Analysis of the networks controlling the antimicrobial peptide-dependent induction of Klebsiella pneumoniae virulence factors. Infect Immun 79: 3718-3732.
27. Lin J, Huang S, Zhang Q, (2002) Outer membrane proteins: key players for bacterial adaptation in host niches. Microbes Infect 4: 325-331.
28. Smith SG, Mahon V, Lambert MA, Fagan RP, (2007) A molecular Swiss army knife: OmpA structure, function and expression. FEMS Microbiol Lett 273: 1-11.
29. Hernandez-Alles S, Alberti S, Alvarez D, Domenech-Sanchez A, Martinez-Martinez L, et al. (1999) Porin expression in clinical isolates of Klebsiella pneumoniae. Microbiology 145 (Pt 3): 673-679.
30. Llobet E, March C, Gimenez P, Bengoechea JA, (2009) Klebsiella pneumoniae OmpA confers resistance to antimicrobial peptides. Antimicrob Agents Chemother 53: 298-302.
31. March C, Moranta D, Regueiro V, Llobet E, Tomas A, et al. (2011) Klebsiella pneumoniae outer membrane protein A is required to prevent the activation of airway epithelial cells. J Biol Chem 286: 9956-9967.
32. Link AJ, Phillips D, Church GM, (1997) Methods for generating precise deletions and insertions in the genome of wild-type Escherichia coli: application to open reading frame characterization. J Bacteriol 179: 6228-6237.
33. Moranta D, Regueiro V, March C, Llobet E, Margareto J, et al. (2010) Klebsiella pneumoniae capsule polysaccharide impedes the expression of β-defensins by airway epithelial cells. Infect Immun 78: 1135-1146.
34. Izquierdo L, Coderch N, Pique N, Bedini E, Corsaro MM, et al. (2003) The Klebsiella pneumoniae wabG gene: role in biosynthesis of the core lipopolysaccharide and virulence. J Bacteriol 185: 7213-7221.
35. Regue M, Izquierdo L, Fresno S, Pique N, Corsaro MM, et al. (2005) A second outer-core region in Klebsiella pneumoniae lipopolysaccharide. J Bacteriol 187: 4198-4206.
36. Perez-Gutierrez C, Llobet E, Llompart CM, Reines M, Bengoechea JA, (2010) Role of lipid A acylation in Yersinia enterocolitica virulence. Infect Immun 78: 2768-2781.
37. Choi KH, Gaynor JB, White KG, Lopez C, Bosio CM, et al. (2005) A Tn7-based broad-range bacterial cloning and expression system. Nat Methods 2: 443-448.
38. Dennis JJ, Zylstra GJ, (1998) Plasposons: modular self-cloning minitransposon derivatives for rapid genetic analysis of gram-negative bacterial genomes. Appl Environ Microbiol 64: 2710-2715.
39. Valdivia RH, Falkow S, (1996) Bacterial genetics by flow cytometry: rapid isolation of Salmonella typhimurium acid-inducible promoters by differential fluorescence induction. Mol Microbiol 22: 367-378.
40. Valdivia RH, Falkow S, (1997) Fluorescence-based isolation of bacterial genes expressed within host cells. Science 277: 2007-2011.
41. Marolda CL, Lahiry P, Vines E, Saldias S, Valvano MA, (2006) Micromethods for the characterization of lipid A-core and O-antigen lipopolysaccharide. Methods Mol Biol 347: 237-252.
42. Froquet R, Lelong E, Marchetti A, Cosson P, (2009) Dictyostelium discoideum: a model host to measure bacterial virulence. Nat Protoc 4: 25-30.
43. Sussman R, Sussman M, (1967) Cultivation of Dictyostelium discoideum in axenic medium. Biochem Biophys Res Commun 29: 53-55.
44. Lelong E, Marchetti A, Gueho A, Lima WC, Sattler N, et al. (2011) Role of magnesium and a phagosomal P-type ATPase in intracellular bacterial killing. Cell Microbiol 13: 246-258.
45. Ravanel K, de CB, Cornillon S, Benghezal M, Zulianello L, et al. (2001) Membrane sorting in the endocytic and phagocytic pathway of Dictyostelium discoideum. Eur J Cell Biol 80: 754-764.
46. Fischer M, Haase I, Simmeth E, Gerisch G, Muller-Taubenberger A, (2004) A brilliant monomeric red fluorescent protein to visualize cytoskeleton dynamics in Dictyostelium. FEBS Lett 577: 227-232.
47. Marti-Lliteras P, Regueiro V, Morey P, Hood DW, Saus C, et al. (2009) Non-typable Haemophilus influenzae clearance by alveolar macrophages is impaired by exposure to cigarette smoke. Infect Immun.
48. Kabha K, Nissimov L, Athamna A, Keisari Y, Parolis H, et al. (1995) Relationships among capsular structure, phagocytosis, and mouse virulence in Klebsiella pneumoniae. Infect Immun 63: 847-852.
49. Lin JC, Chang FY, Fung CP, Xu JZ, Cheng HP, et al. (2004) High prevalence of phagocytic-resistant capsular serotypes of Klebsiella pneumoniae in liver abscess. Microbes Infect 6: 1191-1198.
50. Froquet R, Cherix N, Burr SE, Frey J, Vilches S, et al. (2007) Alternative host model to evaluate Aeromonas virulence. Appl Environ Microbiol 73: 5657-5659.
51. Fresno S, Jimenez N, Izquierdo L, Merino S, Corsaro MM, et al. (2006) The ionic interaction of Klebsiella pneumoniae K2 capsule and core lipopolysaccharide. Microbiology 152: 1807-1818.
52. Regue M, Climent N, Abitiu N, Coderch N, Merino S, et al. (2001) Genetic characterization of the Klebsiella pneumoniae waa gene cluster, involved in core lipopolysaccharide biosynthesis. J Bacteriol 183: 3564-3573.
53. Shankar-Sinha S, Valencia GA, Janes BK, Rosenberg JK, Whitfield C, et al. (2004) The Klebsiella pneumoniae O antigen contributes to bacteremia and lethality during murine pneumonia. Infect Immun 72: 1423-1430.
54. Pukatzki S, Ma AT, Sturtevant D, Krastins B, Sarracino D, et al. (2006) Identification of a conserved bacterial protein secretion system in Vibrio cholerae using the Dictyostelium host model system. Proc Natl Acad Sci U S A 103: 1528-1533.
55. de AB, Cortes G, Crespi C, Saus C, Rojo JM, et al. (2004) C3 promotes clearance of Klebsiella pneumoniae by A549 epithelial cells. Infect Immun 72: 1767-1774.
56. Evrard B, Balestrino D, Dosgilbert A, Bouya-Gachancard JL, Charbonnel N, et al. (2010) Roles of capsule and lipopolysaccharide O antigen in interactions of human monocyte-derived dendritic cells and Klebsiella pneumoniae. Infect Immun 78: 210-219.
57. Lugo JZ, Price S, Miller JE, Ben-David I, Merrill VA, et al. (2007) Lipopolysaccharide O-antigen promotes persistent murine bacteremia. Shock 27: 186-191.
58. Skurnik M, Venho R, Bengoechea J-A, Moriyón I, (1999) The lipopolysaccharide outer core of Yersinia enterocolitica serotype O:3 is required for virulence and plays a role in outer membrane integrity. Mol Microbiol 31: 1443-1462.
59. Hansen DS, Mestre F, Alberti S, Hernandez-Alles S, Alvarez D, et al. (1999) Klebsiella pneumoniae lipopolysaccharide O typing: revision of prototype strains and O-group distribution among clinical isolates from different sources and countries. J Clin Microbiol 37: 56-62.
60. Robey M, O'Connell W, Cianciotto NP, (2001) Identification of Legionella pneumophila rcp, a pagP-like gene that confers resistance to cationic antimicrobial peptides and promotes intracellular infection. Infect Immun 69: 4276-4286.
61. Appleyard RK, (1954) Segregation of new lysogenic types during growth of doubly lysogenic strain derived from Escherichia coli K12. Genetics 39: 440-452.
62. Nassif X, Fournier JM, Arondel J, Sansonetti PJ, (1989) Mucoid phenotype of Klebsiella pneumoniae is a plasmid-encoded virulence factor. Infect Immun 57: 546-552.
63. Llobet E, Tomas JM, Bengoechea JA, (2008) Capsule polysaccharide is a bacterial decoy for antimicrobial peptides. Microbiology 154: 3877-3886.