Pseudomonas aeruginosa Pili and Flagella mediate distinct binding and signaling events at the apical and basolateral surface of airway epithelium

PLoS Pathogens

Volumn 8, Issue 4, 2012, Pages

  Bucior, Iwona ^a,b   Pielage, Julia F ^a,b   Engel, Joanne N ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; FIBROBLAST GROWTH FACTOR RECEPTOR; FLAGELLIN; HEPARAN SULFATE; PHOSPHATIDYLINOSITOL 3 KINASE; PILIN; PLATELET DERIVED ENDOTHELIAL CELL GROWTH FACTOR; PROTEIN KINASE B; PROTEIN SHC; VASCULOTROPIN; ADHESIN; EGFR PROTEIN, HUMAN; HEPARIN; PROTEOHEPARAN SULFATE;

APICAL MEMBRANE; ARTICLE; BACTERIAL FLAGELLUM; BACTERIUM ADHERENCE; BACTERIUM PILUS; BASOLATERAL MEMBRANE; BINDING AFFINITY; CELL AGGREGATION; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; GENE SILENCING; GLYCOSYLATION; HOST PATHOGEN INTERACTION; NONHUMAN; PROTEIN BINDING; PROTEIN DEPLETION; PSEUDOMONAS AERUGINOSA; RESPIRATORY EPITHELIUM; CELL LINE; ENZYME ACTIVATION; FIMBRIA; FLAGELLUM; GENETICS; HUMAN; IMMUNOLOGY; LUNG; METABOLISM; MICROBIOLOGY; MUTATION; PSEUDOMONAS INFECTION; RESPIRATORY TRACT MUCOSA;

BACTERIA (MICROORGANISMS); PSEUDOMONAS AERUGINOSA;

ADHESINS, BACTERIAL; BACTERIAL ADHESION; CELL LINE; ENZYME ACTIVATION; FIMBRIAE, BACTERIAL; FLAGELLA; HEPARAN SULFATE PROTEOGLYCANS; HEPARIN; HUMANS; LUNG; MUTATION; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; RECEPTOR, EPIDERMAL GROWTH FACTOR; RESPIRATORY MUCOSA;

EID: 84861213684     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002616     Document Type: Article

References (64)

1. Mandell GL, Bennett JE, Dolin R, (2010) Mandell, Douglas, and Bennett's principles and practice of infectious diseases. 7th ed Philadelphia, PA Churchill Livingstone/Elsevier online resource (2 v. (cl, 4028, xcvii p.)).
2. Giantsou E, Manolas K, (2011) Superinfections in Pseudomonas aeruginosa ventilator-associated pneumonia. Minerva Anestesiol 77: 964-970.
3. Smith EE, Buckley DG, Wu Z, Saenphimmachak C, Hoffman LR, et al. (2006) Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients. Proc Natl Acad Sci U S A 103: 8487-8492.
4. Tramper-Stranders GA, van der Ent CK, Molin S, Yang L, Hansen SK, et al. (2011) Initial Pseudomonas aeruginosa infection in patients with cystic fibrosis: characteristics of eradicated and persistent isolates. Clin Microbiol Infect E-pud ahead of print. doi: 10.1111/j.1469-0691.2011.03627.x.
5. Almagro P, Salvado M, Garcia-Vidal C, Rodriguez-Carballeira M, Cuchi E, et al. (2011) Pseudomonas aeruginosa and Mortality after Hospital Admission for Chronic Obstructive Pulmonary Disease. Respiration E-pub ahead of print. doi: 10.1159/000331224.
6. Salami AK, Olatunji PO, Oluboyo PO, Akanbi AA 2nd, Fawibe EA, (2006) Bacterial pneumonia in the AIDS patients. West Afr J Med 25: 1-5.
7. Godwin TA, (1998) HIV-AIDS case histories: diagnostic problems. Diagnosis: Pseudomonas aeruginosa pneumonia. AIDS Patient Care STDs 12: 573-575.
8. Franzetti F, Grassini A, Piazza M, Degl'innocenti M, Bandera A, et al. (2006) Nosocomial bacterial pneumonia in HIV-infected patients: risk factors for adverse outcome and implications for rational empiric antibiotic therapy. Infection 34: 9-16.
9. Bucior I, Mostov K, Engel JN, (2010) Pseudomonas aeruginosa-mediated damage requires distinct receptors at the apical and basolateral surfaces of the polarized epithelium. Infect Immun 78: 939-953.
10. Engel J, (2007) Pseudomonas aeruginosa internalization by non-phagocytic cells. In: Ramos J-L, Filloux A, editors. Pseudomonas: A model system in Biology New York Springer pp. 343-368.
11. Chi E, Mehl T, Nunn D, Lory S, (1991) Interaction of Pseudomonas aeruginosa with A549 pneumocyte cells. Infect Immun 59: 822-828.
12. Feldman M, Bryan R, Rajan S, Scheffler L, Brunnert S, et al. (1998) Role of flagella in pathogenesis of Pseudomonas aeruginosa pulmonary infection. Infect Immun 66: 43-51.
13. Dasgupta N, Wolfgang MC, Goodman AL, Arora SK, Jyot J, et al. (2003) A four-tiered transcriptional regulatory circuit controls flagellar biogenesis in Pseudomonas aeruginosa. Mol Microbiol 50: 809-824.
14. Balloy V, Verma A, Kuravi S, Si-Tahar M, Chignard M, et al. (2007) The role of flagellin versus motility in acute lung disease caused by Pseudomonas aeruginosa. J Infect Dis 196: 289-296.
15. Arora SK, Bangera M, Lory S, Ramphal R, (2001) A genomic island in Pseudomonas aeruginosa carries the determinants of flagellin glycosylation. Proc Natl Acad Sci U S A 98: 9342-9347.
16. Feuillet V, Medjane S, Mondor I, Demaria O, Pagni PP, et al. (2006) Involvement of Toll-like receptor 5 in the recognition of flagellated bacteria. Proc Natl Acad Sci U S A 103: 12487-12492.
17. Lightfield KL, Persson J, Brubaker SW, Witte CE, von Moltke J, et al. (2008) Critical function for Naip5 in inflammasome activation by a conserved carboxy-terminal domain of flagellin. Nat Immunol 9: 1171-1178.
18. Kofoed EM, Vance RE, (2011) Innate immune recognition of bacterial ligands by NAIPs determines inflammasome specificity. Nature 477: 592-595.
19. Scharfman A, Arora SK, Delmotte P, Van Brussel E, Mazurier J, et al. (2001) Recognition of Lewis×derivatives present on mucins by flagellar components of Pseudomonas aeruginosa. Infect Immun 69: 5243-5248.
20. Mattick JS, (2002) Type iv pili and twitching motility. Annu Rev Microbiol 56: 289-314.
21. Engel JN, (2003) Molecular pathogenesis of acute Pseudomonas aeruginosa infections. In: Hauser A, Rello J, editors. Severe Infections Caused by Pseudomonas aeruginosa New York City Kluwer Academic/Plenum Press pp. 201-230.
22. Saiman L, Prince A, (1993) Pseudomonas aeruginosa pili bind to asialoGM1 which is increased on the surface of cystic fibrosis epithelial cells. J Clin Invest 92: 1875-1880.
23. Comolli JC, Waite LL, Mostov KE, Engel JN, (1999) Pili binding to asialo-GM1 on epithelial cells can mediate cytotoxicity or bacterial internalization by Pseudomonas aeruginosa. Infect Immun 67: 3207-3214.
24. Schroeder TH, Zaidi T, Pier GB, (2001) Lack of adherence of clinical isolates of Pseudomonas aeruginosa to asialo-GM(1) on epithelial cells. Infect Immun 69: 719-729.
25. Emam A, Yu AR, Park HJ, Mahfoud R, Kus J, et al. (2006) Laboratory and clinical Pseudomonas aeruginosa strains do not bind glycosphingolipids in vitro or during type IV pili-mediated initial host cell attachment. Microbiology 152: 2789-2799.
26. Engel J, Balachandran P, (2009) Role of Pseudomonas aeruginosa type III effectors in disease. Curr Opin Microbiol 12: 61-66.
27. Pier GB, (2000) Role of the cystic fibrosis transmembrane conductance regulator in innate immunity to Pseudomonas aeruginosa infections. Proc Natl Acad Sci U S A 97: 8822-8828.
28. Kazmierczak BI, Mostov K, Engel JN, (2004) Epithelial cell polarity alters Rho-GTPase responses to Pseudomonas aeruginosa. Mol Biol Cell 15: 411-419.
29. Esen M, Grassme H, Riethmuller J, Riehle A, Fassbender K, et al. (2001) Invasion of human epithelial cells by Pseudomonas aeruginosa involves src-like tyrosine kinases p60Src and p59Fyn. Infect Immun 69: 281-287.
30. Evans DJ, Frank DW, Finck-Barbançon V, Wu C, Fleiszig SM, (1998) Pseudomonas aeruginosa invasion and cytotoxicity are independent events, both of which involve protein tyrosine kinase activity. Infect Immun 66: 1453-1459.
31. Pielage JF, Powell KR, Kalman D, Engel JN, (2008) RNAi screen reveals an Abl kinase-dependent host cell pathway involved in Pseudomonas aeruginosa internalization. PLoS Pathog 4: e1000031.
32. Abraham SN, Duncan MJ, Li G, Zaas D, (2005) Bacterial penetration of the mucosal barrier by targeting lipid rafts. J Investig Med 53: 318-321.
33. Kierbel A, Gassam A, Mostov K, Engel J, (2005) The Phosphoinositol-3-kinase-Protein kinase B/Akt pathway is critical for Pseudomonas aeruginosa strain PAK internalization. Mol Biol Cell 16: 2577.
34. Li H, Schmid-Bindert G, Wang D, Zhao Y, Yang X, et al. (2011) Blocking the PI3K/AKT and MEK/ERK signaling pathways can overcome Gefitinib-resistance in non-small cell lung cancer cell lines. Adv Med Sci 56: 275-284.
35. Vallet I, Olson JW, Lory S, Lazdunski A, Filloux A, (2001) The chaperone/usher pathways of Pseudomonas aeruginosa: identification of fimbrial gene clusters (cup) and their involvement in biofilm formation. Proc Natl Acad Sci U S A 98: 6911-6916.
36. Chemani C, Imberty A, de Bentzmann S, Pierre M, Wimmerova M, et al. (2009) Role of LecA and LecB lectins in Pseudomonas aeruginosa-induced lung injury and effect of carbohydrate ligands. Infect Immun 77: 2065-2075.
37. Rush JS, Panneerselvam K, Waechter CJ, Freeze HH, (2000) Mannose supplementation corrects GDP-mannose deficiency in cultured fibroblasts from some patients with Congenital Disorders of Glycosylation (CDG). Glycobiology 10: 829-835.
38. Kang PJ, Hauser AR, Apodaca G, Fleiszig SM, Wiener-Kronish J, et al. (1997) Identification of Pseudomonas aeruginosa genes required for epithelial cell injury. Mol Microbiol 24: 1249-1262.
39. Wong WY, Campbell AP, McInnes C, Sykes BD, Paranchych W, et al. (1995) Structure-function analysis of the adherence-binding domain on the pilin of Pseudomonas aeruginosa strains PAK and KB7. Biochemistry 34: 12963-12972.
40. Bucior I, Scheuring S, Engel A, Burger MM, (2004) Carbohydrate-carbohydrate interaction provides adhesion force and specificity for cellular recognition. J Cell Biol 165: 529-537.
41. Fleiszig SM, Evans DJ, Do N, Vallas V, Shin S, et al. (1997) Epithelial cell polarity affects susceptibility to Pseudomonas aeruginosa invasion and cytotoxicity. Infect Immun 65: 2861-2867.
42. Gotoh N, Tojo A, Muroya K, Hashimoto Y, Hattori S, et al. (1994) Epidermal growth factor-receptor mutant lacking the autophosphorylation sites induces phosphorylation of Shc protein and Shc-Grb2/ASH association and retains mitogenic activity. Proc Natl Acad Sci U S A 91: 167-171.
43. Hybiske K, Ichikawa JK, Huang V, Lory SJ, Machen TE, (2004) Cystic fibrosis airway epithelial cell polarity and bacterial flagellin determine host response to Pseudomonas aeruginosa. Cell Microbiol 6: 49-63.
44. Tseng J, Do J, Widdicombe JH, Machen TE, (2006) Innate immune responses of human tracheal epithelium to Pseudomonas aeruginosa flagellin, TNF-alpha, and IL-1beta. Am J Physiol Cell Physiol 290: C678-690.
45. Zhang J, Li H, Wang J, Dong Z, Mian S, et al. (2004) Role of EGFR transactivation in preventing apoptosis in Pseudomonas aeruginosa-infected human corneal epithelial cells. Invest Ophthalmol Vis Sci 45: 2569-2576.
46. Nagy TA, Frey MR, Yan F, Israel DA, Polk DB, et al. (2009) Helicobacter pylori regulates cellular migration and apoptosis by activation of phosphatidylinositol 3-kinase signaling. J Infect Dis 199: 641-651.
47. Keates S, Sougioultzis S, Keates AC, Zhao D, Peek RM Jr, et al. (2001) cag+ Helicobacter pylori induce transactivation of the epidermal growth factor receptor in AGS gastric epithelial cells. J Biol Chem 276: 48127-48134.
48. Seo B, Choy EW, Maudsley S, Miller WE, Wilson BA, et al. (2000) Pasteurella multocida toxin stimulates mitogen-activated protein kinase via G(q/11)-dependent transactivation of the epidermal growth factor receptor. J Biol Chem 275: 2239-2245.
49. Merz AJ, Enns CA, So M, (1999) Type IV pili of pathogenic Neisseriae elicit cortical plaque formation in epithelial cells. Mol Microbiol 32: 1316-1332.
50. Mikami F, Gu H, Jono H, Andalibi A, Kai H, et al. (2005) Epidermal growth factor receptor acts as a negative regulator for bacterium nontypeable Haemophilus influenzae-induced Toll-like receptor 2 expression via an Src-dependent p38 mitogen-activated protein kinase signaling pathway. J Biol Chem 280: 36185-36194.
51. Yan F, Cao H, Chaturvedi R, Krishna U, Hobbs SS, et al. (2009) Epidermal growth factor receptor activation protects gastric epithelial cells from Helicobacter pylori-induced apoptosis. Gastroenterology 136: 1297-1307 e1291-1293.
52. Swanson KV, Griffiss JM, Edwards VL, Stein DC, Song W, (2011) Neisseria gonorrhoeae-induced transactivation of EGFR enhances gonococcal invasion. Cell Microbiol 13: 1078-1090.
53. Gerçeker AA, Zaidi T, Marks P, Golan DE, Pier GB, (2000) Impact of heterogeneity within cultured cells on bacterial invasion: analysis of Pseudomonas aeruginosa and Salmonella enterica serovar typhi entry into MDCK cells by using a green fluorescent protein-labelled cystic fibrosis transmembrane conductance regulator receptor. Infect Immun 68: 861-870.
54. Roger P, Puchelle E, Bajolet-Laudinat O, Tournier JM, Debordeaux C, et al. (1999) Fibronectin and α5β1 integrin mediate binding of Pseudomonas aeruginosa to repairing airway epithelium. Eur Respir J 13: 1301-1309.
55. Gao N, Kumar A, Jyot J, Yu FS, (2010) Flagellin-induced corneal antimicrobial peptide production and wound repair involve a novel NF-kappaB-independent and EGFR-dependent pathway. PLoS One 5: e9351.
56. Koff JL, Shao MX, Ueki IF, Nadel JA, (2008) Multiple TLRs activate EGFR via a signaling cascade to produce innate immune responses in airway epithelium. Am J Physiol Lung Cell Mol Physiol 294: L1068-1075.
57. Zhou K, Kanai R, Lee P, Wang HW, Modis Y, (2011) Toll-like receptor 5 forms asymmetric dimers in the absence of flagellin. J Struct Biol 177: 402-409.
58. Muir A, Soong G, Sokol S, Reddy B, Gomez MI, et al. (2004) Toll-like receptors in normal and cystic fibrosis airway epithelial cells. Am J Respir Cell Mol Biol 30: 777-783.
59. Koff JL, Shao MX, Kim S, Ueki IF, Nadel JA, (2006) Pseudomonas lipopolysaccharide accelerates wound repair via activation of a novel epithelial cell signaling cascade. J Immunol 177: 8693-8700.
60. Song JS, Hyun SW, Lillihoj E, Kim BT, (2001) Mucin secretion in the rat tracheal epithelial cells by epidermal growth factor and Pseudomonas aeruginosa extracts. Korean J Intern Med 16: 167-172.
61. Evans DJ, Kuo TC, Kwong M, Van R, Fleiszig SM, (2002) Mutation of csk, encoding the C-terminal Src kinase, reduces Pseudomonas aeruginosa internalization by mammalian cells and enhances bacterial cytotoxicity. Microb Pathog 33: 135-143.
62. Lepanto P, Bryant DM, Rossello J, Datta A, Mostov KE, et al. (2011) Pseudomonas aeruginosa interacts with epithelial cells rapidly forming aggregates that are internalized by a Lyn-dependent mechanism. Cell Microbiol 13: 1212-1222.
63. Bertrand JJ, West JT, Engel JN, (2010) Genetic analysis of the regulation of type IV pilus function by the Chp chemosensory system of Pseudomonas aeruginosa. J Bacteriol 192: 994-1010.
64. Liu PV, (1966) The roles of various fractions of Pseudomonas aeruginosa in its pathogenesis: Identity of the lethal toxins produced in vitro and in vivo. J Infect Dis 116: 481-489.