Crystallographic analysis of the Pseudomonas aeruginosa strain K122-4 monomeric pilin reveals a conserved receptor-binding architecture

Biochemistry

Volumn 43, Issue 36, 2004, Pages 11427-11435

  Audette, Gerald F ^a   Irvin, Randall T ^a   Hazes, Bart ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY CROSS REACTIVITY; PILIN GENES; PSEUDOMONAS;

ANTIBODIES; CELLS; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; GENES; MICROORGANISMS; VACCINES;

BIOCHEMISTRY;

CROSS REACTING ANTIBODY; EPITOPE; MONOMER; PILIN;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL GENE; BACTERIAL INFECTION; BACTERIUM ADHERENCE; BACTERIUM PILUS; BINDING AFFINITY; BINDING SITE; CROSS REACTION; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; OPPORTUNISTIC INFECTION; PILIN GENE; PRIORITY JOURNAL; PROTEIN CONFORMATION; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS AERUGINOSA K122 4; PSEUDOMONAS TYPE IV PILIN; RECEPTOR BINDING; RECEPTOR BINDING DOMAIN;

BINDING SITES; CONSERVED SEQUENCE; CRYSTALLOGRAPHY, X-RAY; FIMBRIAE PROTEINS; FIMBRIAE, BACTERIAL; MODELS, MOLECULAR; NEISSERIA GONORRHOEAE; PILI, SEX; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; PSEUDOMONAS AERUGINOSA; RECEPTORS, IMMUNOLOGIC; VIBRIO CHOLERAE;

BACTERIA (MICROORGANISMS); PSEUDOMONAS; PSEUDOMONAS AERUGINOSA;

EID: 4444325332     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi048957s     Document Type: Article

References (71)

1. Todd, T. R. J., Franklin, A., Mankinen-Irvin, P., Gurman, G., and Irvin, R. T. (1989) Augmented bacterial adherence to tracheal epithelial cells is associated with Gram-negative pneumonia in an intensive care unit population, Am. Rev. Respir. Dis. 140, 1585-1589.
2. Hoffken, G., and Niederman, M. S. (2002) Nosocomial pneumonia: The importance of a de-escalating strategy for antibiotic treatment of pneumonia in the ICU, Chest 122, 2183-2196.
3. Raymond, D. P., Pelletier, S. J., Evans, H. L., Pruett, T. L., and Sawyer, R. G. (2003) Impact of antibiotic-resistant Gram-negative bacilli infections on outcome of hospitalized patients, Crit. Care Med. 31, 1035-1041.
4. Bang, R. L., Gang, R. K., Sanyal, S. C., Mokaddas, E., and Ebrahim, M. K. (1998) Burn septicaemia: An analysis of 79 patients, Burns 24, 354-361.
5. Bang, R. L., Sharma, P. N., Sanyal, S. C., and Al Najjadah, I. (2002) Septicaemia after burn injury: A comparative study, Burns 28, 746-751.
6. Pruitt, B. A., Jr., McManus, A. T., Kim, S. H., and Goodwin, C. W. (1998) Burn wound infections: Current status, World J. Surg. 22, 135-145.
7. Maschmeyer, G., and Braveny, I. (2000) Review of the incidence and prognosis of Pseudomonas aeruginosa infections in cancer patients in the 1990s, Eur. J. Clin. Microbiol. Infect. Dis. 19, 915-925.
8. Tummler, B., Bosshammer, J., Breitenstein, S., Brockhausen, I., Gudwius, P., Herrmann, C., Heuer, T., Kubesch, P., Mekus, F., Romling, U., Schmidt, K. D., Spangenberg, C., and Walter, S. (1997) Infections with Pseudomonas aeruginosa in patients with cystic fibrosis, Behring Inst. Mitt. 98, 249-255.
9. Brennan, A. L., and Geddes, D. M. (2002) Cystic fibrosis, Curr. Opin. Infect. Dis. 15, 175-182.
10. Manfredi, R., Nanetti, A., Ferri, M., and Chiodo, F. (2000) Pseudomonas spp. complications in patients with HIV disease: An eight-year clinical and microbiological survey, Eur. J. Epidemiol. 16, 111-118.
11. Hancock, R. E. W., and Speert, D. P. (2000) Antibiotic resistance in Pseudomonas aeruginosa: Mechanisms and impact on treatment, Drug Resist. Updates 3, 247-255.
12. Normark, B. H., and Normark, S. (2002) Evolution and spread of antibiotic resistance, J. Intern. Med. 252, 91-106.
13. Hahn, H. P. (1997) The type-4 pilus is the major virulence-associated adhesin of Pseudomonas aeruginosa - a review, Gene 792, 99-108.
14. Strom, M. S., and Lory, S. (1993) Structure-function and biogenesis of the type IV pili, Annu. Rev. Microbiol. 47, 565-596.
15. Merz, A. J., and So, M. (2000) Interactions of pathogenic Neisseriae with epithelial cell membranes, Annu. Rev. Cell Dev. Biol. 16, 423-457.
16. Farinha, M. A., Conway, B. D., Glaiser, L. M., Ellert, N. W., Irvin, R. T., Sherburne, R., and Paranchych, W. (1994) Alteration of the pilin adhesin of Pseudomonas aeruginosa PAO results in normal pilus biogenesis but a loss of adherence to human pneumocyte cells and decreased virulence in mice, Infect. Immun. 62, 4118-4123.
17. Tang, H., Kays, M., and Price, A. (1995) Role of Pseudomonas aeruginosa pili in acute pulmonary infection, Infect. Immun. 63, 1278-1285.
18. Sheth, H. B., Glasier, L. M. G., Willert, N. W., Cachia, P., Kohn, W., Lee, K. K., Paranchych, W., Hodges, R. S., and Irvin, R. T. (1995) Development of an anti-adhesive vaccine for Pseudomonas aeruginosa targeting the C-terminal region of the pilin structural protein, Biomed. Pept. Proteins Nucl. Acids I, 141-148.
19. Cachia, P. J. Glasier, L. M. G., Hodgins, R. R., Wong, W. Y., Irvin, R. T., and Hodges, R. S. (1998) The use of synthetic peptides in the design of a consensus sequence vaccine for Pseudomonas aeruginosa, J. Peptide Res. 52, 289-299.
20. Cachia, P. J., and Hodges, R. S. (2003) Synthetic peptide vaccine and antibody therapeutic development: Prevention and treatment of Pseudomonas aeruginosa, Biopolymers 71, 141-168.
21. Irvin, R. T., Doig, P. C., Sastry, P. A., Heller, B., and Paranchych, W. (1990) Usefulness of equilibrium parameters of adhesion in predicting the outcome of competition for bacterial receptor sites on respiratory epithelial cells by Pseudomonas aeruginosa strains of heterologous pilus type, Microb. Ecol. Health Dis. 3, 39-47.
22. Irvin, R. T. (1993) Attachment and colonization of Pseudomonas aeruginosa: Role of the surface structures, in Pseudomonas aeruginosa as an Opportunistic Pathogen (Campa, M., Bendinelli, M., and Friedman, H., Eds.) pp 19-42, Plenum Press, New York.
23. Doig, P., Todd, T., Sastry, P. A., Lee, K. K., Hodges, R. S., Paranchych, W., and Irvin, R. T. (1988) Role of pili in adhesion of Pseudomonas aeruginosa to human respiratory epithelial cells, Infect. Immun. 56, 1641-1646.
24. Doig, P., Sastry, P. A., Hodges, R. S., Lee, K. K., Paranchych, W., and Irvin, R. T. (1990) Inhibition of pilus-mediated adhesion of Pseudomonas aeruginosa to human buccal epithelial cells by monoclonal antibodies direct against pili, Infect. Immun. 58, 124-130.
25. Irvin, R. T., Doig, P., Lee, K. K., Sastry, P. A., Paranchych, W., Todd, T., and Hodges, R. S. (1989) Characterization of the Pseudomonas aeruginosa pilus adhesin: Confirmation that the pilin structural protein subunit contains a human epithelial cell-binding domain, Infect. Immun. 57, 3720-3726.
26. Lee, K. K., Doig, P., Irvin, R. T., Paranchych, W., and Hodges, R. S. (1989) Mapping the surface regions of Pseudomonas aeruginosa PAK pilin: The importance of the C-terminal region for adherence to human buccal epithelial cells, Mol. Microbiol. 11, 1493-1499.
27. Lee, K. K., Sheth, H. B., Wong, W. Y., Sherburne, R., Paranchych, W., Hodges, R. S., Lingwood, C. A., Krivan, H., and Irvin, R. T. (1994) 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. 11, 705-713.
28. Campbell, A. P., McInnes, C., Hodges, R. S., and Sykes, B. D. (1995) Comparison of NMR solution structures of the receptor binding domains of Pseudomonas aeruginosa pili strains PAO, KB7, and PAK: Implications for receptor binding and synthetic vaccine design, Biochemistry 34, 16255-16268.
29. Campbell, P. A., Wong, W. Y., Houston, M., Jr., Schweizer, F., Cachia, P. J., Irvin, R. T., Hindsgaul, O., Hodges, R. S., and Sykes, B. D. (1997) Interaction of the receptor binding domains of Pseudomonas aeruginosa pili strains PAK, PAO, KB7, and P1 to a cross-reactive antibody and receptor analog: Implications for synthetic vaccine design, J. Mol. Biol. 267, 382-402.
30. Merz, A. J., So, M., and Sheetz, M. P. (2000) Pilus retraction powers bacterial twitching motility, Nature 407, 98-102.
31. Mattick, J. S. (2002) Type IV pili and twitching motility, Annu. Rev. Microbiol. 56, 289-314.
32. O'Toole, G. A., and Kolter, R. (1998) Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development, Mol. Microbiol. 30, 295-304.
33. Stoodley, P., Sauer, K., Davies, D. G., and Costerton, J. W. (2002) Biofilms as complex differentiated communities, Annu. Rev. Microbiol. 56, 187-209.
34. Klausen, M., Heydorn, A., Ragas, P., Lambertsen, L., Aaes- Jørgensen, A., Molin, S., and Tolker-Nielsen, T. (2003) Biofilm formation by Pseudomonas aeruginosa wild type, flagella, and type IV pili mutants, Mol. Microbiol. 48, 1511-1524.
35. Abraham, S. N., Jonsson, A. B., and Normark, S. (1998) Fimbriae-mediated host-pathogen cross-talk, Curr. Opin. Microbiol. 1, 75-81.
36. DiMango, E., Ratner, A. J., Tabibi, S., and Prince, A. (1998) Activation of NF-κB by adherent Pseudomonas aeruginosa in normal and cystic fibrosis respiratory epithelial cells, J. Clin. Invest. 101, 2598-2607.
37. Jendrossek, A., Fillon, A., Belka, C., Müller, I., Puttkammer, B., and Lang, F. (2003) Apoptotic response of Chang cells to infection with Pseudomonas aeruginosa strains PAK and PAO-I: Molecular ordering of the apoptosis signaling cascade and role of type IV pili, Infect. Immun. 71, 2665-2673.
38. Dubnau, D. (1999) DNA uptake in bacteria, Annu. Rev. Microbiol. 53, 217-244.
39. Bradley, D. E., and Pitt, T. L. (1974) Pilus dependence of four Pseudomonas aeruginosa bacteriophages with non-contractile tails, J. Gen. Virol. 24, 1-15.
40. Hazes, B., Sastry, P. A., Hayakawa, K., Read, R. J., and Irvin, R. T. (2000) Crystal structure of Pseudomonas aeruginosa PAK pilin suggests a main-chain-dominated mode of receptor binding, J. Mol. Biol. 299, 1005-1017.
41. Keizer, D. W., Slupsky, C. M., Kalisiak, M., Campbell, A. P., Crump, M. P., Sastry, P. A., Hazes, B., Irvin, R. T., and Sykes, B. D. (2001) Structure of a pilin monomer from Pseudomonas aeruginosa: Implications for the assembly of pili, J. Biol. Chem. 276, 24186-24193.
42. 2, Infect. Immun. 62, 5213-5219.
43. 2, Mol. Microbiol. 11, 715-723.
44. Parge, H. E., Forest, K. T., Hickey, M. J., Christensen, D. A., Getzoff, E. D., and Tainer, J. A. (1995) Structure of the fibre-forming protein pilin at 2.6 Å resolution, Nature 378, 32-38.
45. Craig, L., Taylor, R. K., Pique, M. E., Adair, B. D., Arvai, A. S., Singh, M., Lloyd, S. J., Shin, D. S., Getzoff, E. D., Yeager, M., Forest, K. T., and Tainer, J. A. (2003) Type IV pilin structure and assembly: X-ray and EM analyses of Vibrio cholerae toxin-coregulated pilus and Pseudomonas aeruginosa PAK pilin, Mol. Cell II, 1139-1150.
46. Audette, G. F., Irvin, R. T., and Hazes, B. (2003) Purification, crystallization, and preliminary diffraction studies of the Pseudomonas aeruginosa strain K122-4 monomeric pilin, Acta Crystallogr., Sect. D 59, 1665-1667.
47. Leslie, A. G. W. (1992) Recent changes to the MOSFLM package for processing film and image plate data, Joint CCP4/ESF-EAMCB Newsletter on Protein Crystallogr. 26.
48. CCP4 (1994) The SERC (U.K.) collaborative computing project No. 4: A suite of programs for protein crystallography, Acta Crystallogr., Sect. D 50, 760-763.
49. Navaza, J. (1994) AMoRe: An automated package for molecular replacement, Acta Crystallogr., Sect. A 50, 157-163.
50. Lamzin, V. S., and Wilson, K. W. (1993) Automated refinement of protein models, Acta Crystallogr., Sect. D 49, 129-147.
51. Perrakis, A., Harkiolaki, M., Wilson, K. W., and Lamzin, V. S. (2001) ARP/wARP and molecular replacement, Acta Crystallogr., Sect. D 57, 1445-1450.
52. Read, R. J. (1997) Model phases: Probabilities and bias, Methods Enzymol. 277, 110-128.
53. McRee, D. E. (1999) XtalView/Xfit: A versatile program for manipulating atomic coordinates and electron density, J. Struct. Biol. 125, 156-165.
54. Pasloske, B. L., Sastry, P. A., Finlay, B. B., and Paranchych, W. (1988) Two unusual pilin sequences from different isolates of Pseudomonas aeruginosa, J. Bacteriol. 170, 3738-3741.
55. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method, Acta Crystallogr., Sect. D 53, 240-255.
56. Winn, M. D., Isupov, M. N., and Murshudov, G. N. (2001) Use of TLS parameters to model anisotropic displacements in macromolecular refinement, Acta Crystallogr., Sect. D 57, 122-133.
57. Brünger, A. T. (1992) Free R value: A novel statistical quantity for assessing the accuracy of crystal structures, Nature 355, 472-475.
58. Engh, R. A., and Huber, R. (1991) Accurate bond and angle parameters for X-ray protein-structure refinement, Acta Crystallogr., Sect. A 47, 392-400.
59. Sheldrick, G. M., and Schneider, T. M. (1997) SHELXL: High-resolution refinement, Methods Enzymol. 277, 319-343.
60. Laskowski, R. A., MacArthur, M. W., Moss, D. S., and Thornton, J. M. (1993) PROCHECK: A program to check the stereochemical quality of protein structures, J. Appl. Cryst. 26, 283-291.
61. Ramakrishnan, C., and Ramachandran, G. N. (1965) Stereochemical criteria for polypeptide and protein chain conformations II. Allowed conformations for a pair of peptide units, Biophys. J. 5, 909-933.
62. Craig, L., Pique, M. E., and Tainer, J. A. (2004) Type IV pilus structure and bacterial pathogenicity, Nat. Rev. Microbiol. 2, 363-378.
63. Marvin, D. A., Nadassy, K., Welsh, L. C., and Forest, K. T. (2003) Type-4 bacterial pill: Molecular models and their simulated diffraction patterns, Fibre Diffraction Rev. 11, 87-94.
64. Haas, R., Schwarz, H., and Meyer, T. F. (1987) Release of soluble pilin antigen coupled with gene conversion in Neisseria gonorrhoeae, Proc. Natl. Acad. Sci. U.S.A. 84, 9079-9083.
65. Kus, J. V., Tullis, E., Cvitkovitch, D. G., and Burrows, L. L. (2004) Significant differences in type IV pilin allele distribution among Pseudomonas aeruginosa isolates from cystic fibrosis (CF) versus non-CF patients, Microbiology 150, 1315-1326.
66. McInnes, C., Sonnichsen, F. D., Kay, C. M., Hodges, R. S., and Sykes, B. D. (1993) NMR solution structure and flexibility of a peptide antigen representing the receptor binding domain of Pseudomonas aeruginosa, Biochemistry 31, 13432-13440.
67. Campbell, A. P., Bautista, D. L., Tripet, B., Wong, W. Y., Irvin, R. T., Hodges, R. S., and Sykes, B. D. (1997) Solution secondary structure of a bacterially expressed peptide from the receptor binding domain of Pseudomonas aeruginosa pili strain PAK: A heteronuclear multidimensional NMR study, Biochemistry 36, 12791-12801.
68. Wong, W., Campbell, A. P., McInnes, C., Sykes, B. D., Paranchych, W., Irvin, R. T., and Hodges, R. S. (1995) Structure-function analysis of the adherence-binding domain on the pilin of Pseudomonas aeruginosa strains PAK and KB7, Biochemistry 34, 12963-12972.
69. Suh, J.-Y., Spyracopoulos, L., Keizer, D. W., Irvin, R. T., and Sykes, B. D. (2001) Backbone dynamics of receptor binding and antigenic regions of a Pseudomonas aeruginosa pilin monomer, Biochemistry 40, 3985-3995.
70. Kraulis, J. (1991) MOLSCRIPT: A program to produce both detailed and schematic plots of protein structures, J. Appl. Crystallogr. 24, 946-950.
71. Merritt, E. A., and Bacon, D. J. (1997) Raster3D photorealistic molecular graphics, Methods Enzymol. 277, 505-524.