Infection of human mucosal tissue by Pseudomonas aeruginosa requires sequential and mutually dependent virulence factors and a novel pilus-associated adhesin

Cellular Microbiology

Volumn 12, Issue 8, 2010, Pages 1158-1173

  Heiniger, Ryan W ^a,d   Winther Larsen, Hanne C ^b,e   Pickles, Raymond J ^a   Koomey, Michael ^b,c   Wolfgang, Matthew C ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b Department of Molecular Biosciences ^*  (Norway)

^c UNIVERSITY OF OSLO   (Norway)

^d JEALOTT S HILL RESEARCH STATION   (United Kingdom)

^e NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; PILUS ASSOCIATED PROTEIN PIIY1; UNCLASSIFIED DRUG; VIRULENCE FACTOR; BACTERIAL TOXIN; FIMBRIA PROTEIN; PILY1 PROTEIN, PSEUDOMONAS AERUGINOSA;

ARTICLE; BACTERIAL GENE; BACTERIUM ADHERENCE; BACTERIUM PILUS; CELL CULTURE; CELL SURFACE; EPITHELIUM CELL; HOST CELL; HUMAN; HUMAN CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; OPERON; OPPORTUNISTIC INFECTION; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTION; RESPIRATORY EPITHELIUM; TISSUE INJURY; BIOLOGICAL MODEL; CYTOCHEMISTRY; FIMBRIA; FLUORESCENCE MICROSCOPY; GENETICS; METABOLISM; MICROBIOLOGY; MICROSCOPY; ORGAN CULTURE TECHNIQUE; PATHOGENICITY; PHYSIOLOGY; RESPIRATORY TRACT MUCOSA;

BACTERIAL ADHESION; BACTERIAL TOXINS; CELLS, CULTURED; EPITHELIAL CELLS; FIMBRIAE PROTEINS; FIMBRIAE, BACTERIAL; HISTOCYTOCHEMISTRY; HUMANS; MICROSCOPY; MICROSCOPY, FLUORESCENCE; MODELS, BIOLOGICAL; ORGAN CULTURE TECHNIQUES; PSEUDOMONAS AERUGINOSA; RESPIRATORY MUCOSA; VIRULENCE FACTORS;

BACTERIA (MICROORGANISMS); PSEUDOMONAS AERUGINOSA;

EID: 77957116883     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2010.01461.x     Document Type: Article

References (69)

1. Alm RA, Mattick JS. Genes involved in the biogenesis and function of type-4 fimbriae in Pseudomonas aeruginosa. Gene 1997, 192:89-98.
2. Alm RA, Hallinan JP, Watson AA, Mattick JS. Fimbrial biogenesis genes of Pseudomonas aeruginosa: pilW and pilX increase the similarity of type 4 fimbriae to the GSP protein-secretion systems and pilY1 encodes a gonococcal PilC homologue. Mol Microbiol 1996, 22:161-173.
3. van Alphen LB, Bleumink-Pluym NM, Rochat KD, van Balkom BW, Wosten MM, van Putten JP. Active migration into the subcellular space precedes Campylobacter jejuni invasion of epithelial cells. Cell Microbiol 2008, 10:53-66.
4. Belete B, Lu H, Wozniak DJ. Pseudomonas aeruginosa AlgR regulates type IV pilus biosynthesis by activating transcription of the fimU-pilVWXY1Y2E operon. J Bacteriol 2008, 190:2023-2030.
5. de Bentzmann S, Roger P, Puchelle E. Pseudomonas aeruginosa adherence to remodelling respiratory epithelium. Eur Respir J 1996, 9:2145-2150.
6. Bloemberg GV, O'Toole GA, Lugtenberg BJ, Kolter R. Green fluorescent protein as a marker for Pseudomonas spp. Appl Environ Microbiol 1997, 63:4543-4551.
7. Bohn YS, Brandes G, Rakhimova E, Horatzek S, Salunkhe P, Munder A. Multiple roles of Pseudomonas aeruginosa TBCF10839 PilY1 in motility, transport and infection. Mol Microbiol 2009, 71:730-747.
8. Bucior I, Mostov K, Engel JN. Pseudomonas aeruginosa-mediated damage requires distinct receptors at the apical and basolateral surfaces of the polarized epithelium. Infect Immun 2010, 78:939-953.
9. Carbonnelle E, Helaine S, Nassif X, Pelicic V. A systematic genetic analysis in Neisseria meningitidis defines the Pil proteins required for assembly, functionality, stabilization and export of type IV pili. Mol Microbiol 2006, 61:1510-1522.
10. Chi E, Mehl T, Nunn D, Lory S. Interaction of Pseudomonas aeruginosa with A549 pneumocyte cells. Infect Immun 1991, 59:822-828.
11. Chiang P, Sampaleanu LM, Ayers M, Pahuta M, Howell PL, Burrows LL. Functional role of conserved residues in the characteristic secretion NTPase motifs of the Pseudomonas aeruginosa type IV pilus motor proteins PilB, PilT and PilU. Microbiology 2008, 154:114-126.
12. Cleary J, Lai LC, Shaw RK, Straatman-Iwanowska A, Donnenberg MS, Frankel G, Knutton S. Enteropathogenic Escherichia coli (EPEC) adhesion to intestinal epithelial cells: role of bundle-forming pili (BFP), EspA filaments and intimin. Microbiology 2004, 150:527-538.
13. Collins RF, Davidsen L, Derrick JP, Ford RC, Tonjum T. Analysis of the PilQ secretin from Neisseria meningitidis by transmission electron microscopy reveals a dodecameric quaternary structure. J Bacteriol 2001, 183:3825-3832.
14. Comolli JC, Hauser AR, Waite L, Whitchurch CB, Mattick JS, Engel JN. Pseudomonas aeruginosa gene products PilT and PilU are required for cytotoxicity in vitro and virulence in a mouse model of acute pneumonia. Infect Immun 1999a, 67:3625-3630.
15. Comolli JC, Waite LL, Mostov KE, Engel JN. Pili binding to asialo-GM1 on epithelial cells can mediate cytotoxicity or bacterial internalization by Pseudomonas aeruginosa. Infect Immun 1999b, 67:3207-3214.
16. Craig L, Taylor RK, Pique ME, Adair BD, Arvai AS, Singh M. Type IV pilin structure and assembly: X-ray and EM analyses of Vibrio cholerae toxin-coregulated pilus and Pseudomonas aeruginosa PAK pilin. Mol Cell 2003, 11:1139-1150.
17. Doig P, Todd T, Sastry PA, Lee KK, Hodges RS, Paranchych W, Irvin RT. Role of pili in adhesion of Pseudomonas aeruginosa to human respiratory epithelial cells. Infect Immun 1988, 56:1641-1646.
18. Doig P, Sastry PA, Hodges RS, Lee KK, Paranchych W, Irvin RT. Inhibition of pilus-mediated adhesion of Pseudomonas aeruginosa to human buccal epithelial cells by monoclonal antibodies directed against pili. Infect Immun 1990, 58:124-130.
19. Driscoll JA, Brody SL, Kollef MH. The epidemiology, pathogenesis and treatment of Pseudomonas aeruginosa infections. Drugs 2007, 67:351-368.
20. Emam A, Yu AR, Park HJ, Mahfoud R, Kus J, Burrows LL, Lingwood CA. Laboratory and clinical Pseudomonas aeruginosa strains do not bind glycosphingolipids in vitro or during type IV pili-mediated initial host cell attachment. Microbiology 2006, 152:2789-2799.
21. Fleiszig SM, Evans DJ, Do N, Vallas V, Shin S, Mostov KE. Epithelial cell polarity affects susceptibility to Pseudomonas aeruginosa invasion and cytotoxicity. Infect Immun 1997, 65:2861-2867.
22. Fulcher ML, Gabriel S, Burns KA, Yankaskas JR, Randell SH. Well-differentiated human airway epithelial cell cultures. Methods Mol Med 2005, 107:183-206.
23. Furste JP, Pansegrau W, Frank R, Blocker H, Scholz P, Bagdasarian M, Lanka E. Molecular cloning of the plasmid RP4 primase region in a multi-host-range tacP expression vector. Gene 1986, 48:119-131.
24. Gaillard JL, Finlay BB. Effect of cell polarization and differentiation on entry of Listeria monocytogenes into the enterocyte-like Caco-2 cell line. Infect Immun 1996, 64:1299-1308.
25. Garau J, Gomez L. Pseudomonas aeruginosa pneumonia. Curr Opin Infect Dis 2003, 16:135-143.
26. Hazes B, Sastry PA, Hayakawa K, Read RJ, Irvin RT. Crystal structure of Pseudomonas aeruginosa PAK pilin suggests a main-chain-dominated mode of receptor binding. J Mol Biol 2000, 299:1005-1017.
27. Helaine S, Dyer DH, Nassif X, Pelicic V, Forest KT. 3D structure/function analysis of PilX reveals how minor pilins can modulate the virulence properties of type IV pili. Proc Natl Acad Sci USA 2007, 104:15888-15893.
28. Hyland RM, Sun J, Griener TP, Mulvey GL, Klassen JS, Donnenberg MS, Armstrong GD. The bundlin pilin protein of enteropathogenic Escherichia coli is an N-acetyllactosamine-specific lectin. Cell Microbiol 2008, 10:177-187.
29. Ichikawa JK, English SB, Wolfgang MC, Jackson R, Butte AJ, Lory S. Genome-wide analysis of host responses to the Pseudomonas aeruginosa type III secretion system yields synergistic effects. Cell Microbiol 2005, 7:1635-1646.
30. Jensen VB, Harty JT, Jones BD. Interactions of the invasive pathogens Salmonella typhimurium, Listeria monocytogenes, and Shigella flexneri with M cells and murine Peyer's patches. Infect Immun 1998, 66:3758-3766.
31. Lee A, Chow D, Haus B, Tseng W, Evans D, Fleiszig S. Airway epithelial tight junctions and binding and cytotoxicity of Pseudomonas aeruginosa. Am J Physiol 1999, 277:L204-L217.
32. Lee KK, Sheth HB, Wong WY, Sherburne R, Paranchych W, Hodges RS. The binding of Pseudomonas aeruginosa pili to glycosphingolipids is a tip-associated event involving the C-terminal region of the structural pilin subunit. Mol Microbiol 1994, 11:705-713.
33. Lizewski SE, Lundberg DS, Schurr MJ. The transcriptional regulator AlgR is essential for Pseudomonas aeruginosa pathogenesis. Infect Immun 2002, 70:6083-6093.
34. Martinez A, Ostrovsky P, Nunn DN. LipC, a second lipase of Pseudomonas aeruginosa, is LipB and Xcp dependent and is transcriptionally regulated by pilus biogenesis components. Mol Microbiol 1999, 34:317-326.
35. Mattick JS. Type IV pili and twitching motility. Annu Rev Microbiol 2002, 56:289-314.
36. Mayhew TM, Myklebust R, Whybrow A, Jenkins R. Epithelial integrity, cell death and cell loss in mammalian small intestine. Histol Histopathol 1999, 14:257-267.
37. Merz AJ, So M, Sheetz MP. Pilus retraction powers bacterial twitching motility. Nature 2000, 407:98-102.
38. Monteville MR, Konkel ME. Fibronectin-facilitated invasion of T84 eukaryotic cells by Campylobacter jejuni occurs preferentially at the basolateral cell surface. Infect Immun 2002, 70:6665-6671.
39. Morand PC, Bille E, Morelle S, Eugene E, Beretti JL, Wolfgang M. Type IV pilus retraction in pathogenic Neisseria is regulated by the PilC proteins. EMBO J 2004, 23:2009-2017.
40. Mounier J, Vasselon T, Hellio R, Lesourd M, Sansonetti PJ. Shigella flexneri enters human colonic Caco-2 epithelial cells through the basolateral pole. Infect Immun 1992, 60:237-248.
41. Nougayrede JP, Fernandes PJ, Donnenberg MS. Adhesion of enteropathogenic Escherichia coli to host cells. Cell Microbiol 2003, 5:359-372.
42. O'Toole GA, Kolter R. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol Microbiol 1998, 30:295-304.
43. Orans J, Johnson MD, Coggan KA, Sperlazza JR, Heiniger RW, Wolfgang MC, Redinbo MR. Crystal structure analysis reveals Pseudomonas PilY1 as an essential calcium-dependent regulator of bacterial surface motility. Proc Natl Acad Sci USA 2010, 107:1065-1070.
44. Pelicic V. Type IV pili: e pluribus unum? Mol Microbiol 2008, 68:827-837.
45. Pentecost M, Otto G, Theriot JA, Amieva MR. Listeria monocytogenes invades the epithelial junctions at sites of cell extrusion. PLoS Pathog 2006, 2:e3.
46. Ramphal R, Small PM, Shands JW, Fischlschweiger W, Small PA. Adherence of Pseudomonas aeruginosa to tracheal cells injured by influenza infection or by endotracheal intubation. Infect Immun 1980, 27:614-619.
47. Rudel T, Scheurerpflug I, Meyer TF. Neisseria PilC protein identified as type-4 pilus tip-located adhesin. Nature 1995a, 373:357-359.
48. Rudel T, Boxberger HJ, Meyer TF. Pilus biogenesis and epithelial cell adherence of Neisseria gonorrhoeae pilC double knock-out mutants. Mol Microbiol 1995b, 17:1057-1071.
49. Sadikot RT, Blackwell TS, Christman JW, Prince AS. Pathogen-host interactions in Pseudomonas aeruginosa pneumonia. Am J Respir Crit Care Med 2005, 171:1209-1223.
50. Schweizer F, Jiao H, Hindsgaul O, Wong WY, Irvin RT. Interaction between the pili of Pseudomonas aeruginosa PAK and its carbohydrate receptor beta-d-GalNAc(1->4)beta-d-Gal analogs. Can J Microbiol 1998, 44:307-311.
51. Sheth HB, Lee KK, Wong WY, Srivastava G, Hindsgaul O, Hodges RS. The pili of Pseudomonas aeruginosa strains PAK and PAO bind specifically to the carbohydrate sequence beta GalNAc(1-4)beta Gal found in glycosphingolipids asialo-GM1 and asialo-GM2. Mol Microbiol 1994, 11:715-723.
52. Skerker JM, Berg HC. Direct observation of extension and retraction of type IV pili. Proc Natl Acad Sci USA 2001, 98:6901-6904.
53. Soong G, Reddy B, Sokol S, Adamo R, Prince A. TLR2 is mobilized into an apical lipid raft receptor complex to signal infection in airway epithelial cells. J Clin Invest 2004, 113:1482-1489.
54. Soong G, Parker D, Magargee M, Prince AS. The type III toxins of Pseudomonas aeruginosa disrupt epithelial barrier function. J Bacteriol 2008, 190:2814-2821.
55. Strom MS, Lory S. Cloning and expression of the pilin gene of Pseudomonas aeruginosa PAK in Escherichia coli. J Bacteriol 1986, 165:367-372.
56. Sundin C, Wolfgang MC, Lory S, Forsberg A, Frithz-Lindsten E. Type IV pili are not specifically required for contact dependent translocation of exoenzymes by Pseudomonas aeruginosa. Microb Pathog 2002, 33:265-277.
57. Taha MK, Morand PC, Pereira Y, Eugene E, Giorgini D, Larribe M, Nassif X. Pilus-mediated adhesion of Neisseria meningitidis: the essential role of cell contact-dependent transcriptional upregulation of the PilC1 protein. Mol Microbiol 1998, 28:1153-1163.
58. Tang H, Kays M, Prince A. Role of Pseudomonas aeruginosa pili in acute pulmonary infection. Infect Immun 1995, 63:1278-1285.
59. Thomas WE, Trintchina E, Forero M, Vogel V, Sokurenko EV. Bacterial adhesion to target cells enhanced by shear force. Cell 2002, 109:913-923.
60. Turner LR, Lara JC, Nunn DN, Lory S. Mutations in the consensus ATP-binding sites of XcpR and PilB eliminate extracellular protein secretion and pilus biogenesis in Pseudomonas aeruginosa. J Bacteriol 1993, 175:4962-4969.
61. Vallis AJ, Yahr TL, Barbieri JT, Frank DW. Regulation of ExoS production and secretion by Pseudomonas aeruginosa in response to tissue culture conditions. Infect Immun 1999, 67:914-920.
62. Whitchurch CB, Hobbs M, Livingston SP, Krishnapillai V, Mattick JS. Characterisation of a Pseudomonas aeruginosa twitching motility gene and evidence for a specialised protein export system widespread in eubacteria. Gene 1991, 101:33-44.
63. Winther-Larsen HC, Wolfgang M, Dunham S, van Putten JP, Dorward D, Lovold C. A conserved set of pilin-like molecules controls type IV pilus dynamics and organelle-associated functions in Neisseria gonorrhoeae. Mol Microbiol 2005, 56:903-917.
64. Winther-Larsen HC, Wolfgang MC, van Putten JP, Roos N, Aas FE, Egge-Jacobsen WM. Pseudomonas aeruginosa type IV pilus expression in Neisseria gonorrhoeae: effects of pilin subunit composition on function and organelle dynamics. J Bacteriol 2007, 189:6676-6685.
65. Wolfgang M, Park HS, Hayes SF, van Putten JP, Koomey M. Suppression of an absolute defect in type IV pilus biogenesis by loss-of-function mutations in pilT, a twitching motility gene in Neisseria gonorrhoeae. Proc Natl Acad Sci USA 1998, 95:14973-14978.
66. Wolfgang M, van Putten JP, Hayes SF, Dorward D, Koomey M. Components and dynamics of fiber formation define a ubiquitous biogenesis pathway for bacterial pili. EMBO J 2000, 19:6408-6418.
67. Wolfgang MC, Lee VT, Gilmore ME, Lory S. Coordinate regulation of bacterial virulence genes by a novel adenylate cyclase-dependent signaling pathway. Dev Cell 2003, 4:253-263.
68. Yu L, Lee KK, Hodges RS, Paranchych W, Irvin RT. Adherence of Pseudomonas aeruginosa and Candida albicans to glycosphingolipid (Asialo-GM1) receptors is achieved by a conserved receptor-binding domain present on their adhesins. Infect Immun 1994, 62:5213-5219.
69. Zolfaghar I, Evans DJ, Fleiszig SM. Twitching motility contributes to the role of pili in corneal infection caused by Pseudomonas aeruginosa. Infect Immun 2003, 71:5389-5393.