Functional mapping of PilF and PilQ in the Pseudomonas aeruginosa type IV pilus system

Biochemistry

Volumn 52, Issue 17, 2013, Pages 2914-2923

  Koo, Jason ^a,b   Tang, Tim ^b   Harvey, Hanjeong ^c   Tammam, Stephanie ^a,b   Sampaleanu, Liliana ^a   Burrows, Lori L ^c   Howell, P Lynne ^a,b  

^a HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c MCMASTER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

FUNCTIONAL MAPPING; INNER MEMBRANES; PROTEIN SURFACE; PROTEIN-PROTEIN INTERACTIONS; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS CELLS; SITE DIRECTED MUTAGENESIS; VIRULENCE FACTORS;

BACTERIA; OLIGOMERIZATION; OLIGOMERS; PROTEINS;

MEMBRANES;

BACTERIAL PROTEIN; CHAPERONE; MEMBRANE PROTEIN; MONOMER; PILF PROTEIN; PILQ PROTEIN; SECRETIN; UNCLASSIFIED DRUG;

ARTICLE; BIOGENESIS; CARBOXY TERMINAL SEQUENCE; CELL LYSATE; CONTROLLED STUDY; CYTOPLASM; HYDROPHOBICITY; MOLECULAR MODEL; NONHUMAN; OLIGOMERIZATION; OUTER MEMBRANE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN MOTIF; PSEUDOMONAS AERUGINOSA; SITE DIRECTED MUTAGENESIS; TYPE IV SECRETION SYSTEM;

FIMBRIAE PROTEINS; FIMBRIAE, BACTERIAL; GENETIC COMPLEMENTATION TEST; MODELS, MOLECULAR; MUTAGENESIS; PSEUDOMONAS AERUGINOSA;

PSEUDOMONAS; PSEUDOMONAS AERUGINOSA;

EID: 84877026195     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi3015345     Document Type: Article

References (47)

1. Burrows, L. L. (2005) Weapons of mass retraction Mol. Microbiol. 57, 878-888
2. Chiang, P. and Burrows, L. L. (2003) Biofilm formation by hyperpiliated mutants of Pseudomonas aeruginosa J. Bacteriol. 185, 2374-2378
3. Mattick, J. S. (2002) Type IV pili and twitching motility Annu. Rev. Microbiol. 56, 289-314
4. O'Toole, G. A. and Kolter, R. (1998) Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development Mol. Microbiol. 30, 295-304
5. Saiman, L., Ishimoto, K., Lory, S., and Prince, A. (1990) The effect of piliation and exoproduct expression on the adherence of Pseudomonas aeruginosa to respiratory epithelial monolayers J. Infect. Dis. 161, 541-548
6. Semmler, A. B., Whitchurch, C. B., and Mattick, J. S. (1999) A re-examination of twitching motility in Pseudomonas aeruginosa Microbiology 145 (Part 10) 2863-2873
7. Whitchurch, C. B. and Mattick, J. S. (1994) Characterization of a gene, pilU, required for twitching motility but not phage sensitivity in Pseudomonas aeruginosa Mol. Microbiol. 13, 1079-1091
8. Koo, J., Tammam, S., Ku, S. Y., Sampaleanu, L. M., Burrows, L. L., and Howell, P. L. (2008) PilF is an outer membrane lipoprotein required for multimerization and localization of the Pseudomonas aeruginosa Type IV pilus secretin J. Bacteriol. 190, 6961-6969
9. Berry, J. L., Phelan, M. M., Collins, R. F., Adomavicius, T., Tonjum, T., Frye, S. A., Bird, L., Owens, R., Ford, R. C., Lian, L. Y., and Derrick, J. P. (2012) Structure and Assembly of a Trans-Periplasmic Channel for Type IV Pili in Neisseria meningitidis PLoS Pathog. 8, e1002923
10. Kim, K., Oh, J., Han, D., Kim, E. E., Lee, B., and Kim, Y. (2006) Crystal structure of PilF: Functional implication in the type 4 pilus biogenesis in Pseudomonas aeruginosa Biochem. Biophys. Res. Commun. 340, 1028-1038
11. Trindade, M. B., Job, V., Contreras-Martel, C., Pelicic, V., and Dessen, A. (2008) Structure of a widely conserved type IV pilus biogenesis factor that affects the stability of secretin multimers J. Mol. Biol. 378, 1031-1039
12. Koo, J., Burrows, L. L., and Howell, P. L. (2012) Decoding the roles of pilotins and accessory proteins in secretin escort services FEMS Microbiol. Lett. 328, 1-12
13. Gu, S., Rehman, S., Wang, X., Shevchik, V. E., and Pickersgill, R. W. (2012) Structural and functional insights into the pilotin-secretin complex of the type II secretion system PLoS Pathog. 8, e1002531
14. Okon, M., Moraes, T. F., Lario, P. I., Creagh, A. L., Haynes, C. A., Strynadka, N. C., and McIntosh, L. P. (2008) Structural characterization of the type-III pilot-secretin complex from Shigella flexneri Structure 16, 1544-1554
15. Tosi, T., Nickerson, N. N., Mollica, L., Jensen, M. R., Blackledge, M., Baron, B., England, P., Pugsley, A. P., and Dessen, A. (2011) Pilotin-secretin recognition in the type II secretion system of Klebsiella oxytoca Mol. Microbiol. 82, 1422-1432
16. Burghout, P., Beckers, F., de Wit, E., van Boxtel, R., Cornelis, G. R., Tommassen, J., and Koster, M. (2004) Role of the pilot protein YscW in the biogenesis of the YscC secretin in Yersinia enterocolitica J. Bacteriol. 186, 5366-5375
17. Viarre, V., Cascales, E., Ball, G., Michel, G. P., Filloux, A., and Voulhoux, R. (2009) HxcQ liposecretin is self-piloted to the outer membrane by its N-terminal lipid anchor J. Biol. Chem. 284, 33815-33823
18. Scheufler, C., Brinker, A., Bourenkov, G., Pegoraro, S., Moroder, L., Bartunik, H., Hartl, F. U., and Moarefi, I. (2000) Structure of TPR domain-peptide complexes: Critical elements in the assembly of the Hsp70-Hsp90 multichaperone machine Cell 101, 199-210
19. Zhang, Y. and Chan, D. C. (2007) Structural basis for recruitment of mitochondrial fission complexes by Fis1 Proc. Natl. Acad. Sci. U.S.A. 104, 18526-18530
20. Quinaud, M., Ple, S., Job, V., Contreras-Martel, C., Simorre, J. P., Attree, I., and Dessen, A. (2007) Structure of the heterotrimeric complex that regulates type III secretion needle formation Proc. Natl. Acad. Sci. U.S.A. 104, 7803-7808
21. Lazarus, M. B., Nam, Y., Jiang, J., Sliz, P., and Walker, S. (2011) Structure of human O-GlcNAc transferase and its complex with a peptide substrate Nature 469, 564-567
22. Burkhardt, J., Vonck, J., and Averhoff, B. (2011) Structure and function of PilQ, a secretin of the DNA transporter from the thermophilic bacterium Thermus thermophilus HB27 J. Biol. Chem. 286, 9977-9984
23. Korotkov, K. V., Gonen, T., and Hol, W. G. (2011) Secretins: Dynamic channels for protein transport across membranes Trends Biochem. Sci. 36, 433-443
24. Brillet, K., Journet, L., Celia, H., Paulus, L., Stahl, A., Pattus, F., and Cobessi, D. (2007) A β strand lock exchange for signal transduction in TonB-dependent transducers on the basis of a common structural motif Structure 15, 1383-1391
25. Larsen, R. A., Thomas, M. G., and Postle, K. (1999) Protonmotive force, ExbB and ligand-bound FepA drive conformational changes in TonB Mol. Microbiol. 31, 1809-1824
26. Tarry, M., Jaaskelainen, M., Paino, A., Tuominen, H., Ihalin, R., and Hogbom, M. (2011) The Extra-Membranous Domains of the Competence Protein HofQ Show DNA Binding, Flexibility and a Shared Fold with Type I KH Domains J. Mol. Biol. 409, 642-653
27. Hoang, H. H., Nickerson, N. N., Lee, V. T., Kazimirova, A., Chami, M., Pugsley, A. P., and Lory, S. (2011) Outer membrane targeting of Pseudomonas aeruginosa proteins shows variable dependence on the components of Bam and Lol machineries MBio 2, e00246-11
28. Ayers, M., Sampaleanu, L. M., Tammam, S., Koo, J., Harvey, H., Howell, P. L., and Burrows, L. L. (2009) PilM/N/O/P proteins form an inner membrane complex that affects the stability of the Pseudomonas aeruginosa type IV pilus secretin J. Mol. Biol. 394, 128-142
29. OpenWetWare-contributors (2010) Round-the-horm site-directed mutagenesis, OpenWetWare. http://openwetware.org/index.php?title=%27Round-the-horn-site- directed-mutagenesis&oldid=458415.
30. Schnaitman, C. A. (1971) Effect of ethylenediaminetetraacetic acid, Triton X-100, and lysozyme on the morphology and chemical composition of isolate cell walls of Escherichia coli J. Bacteriol. 108, 553-563
31. Schnaitman, C. A. (1971) Solubilization of the cytoplasmic membrane of Escherichia coli by Triton X-100 J. Bacteriol. 108, 545-552
32. Allan, R. K. and Ratajczak, T. (2011) Versatile TPR domains accommodate different modes of target protein recognition and function Cell Stress Chaperones 16, 353-367
33. Lautrop, H. (1961) Bacterium anitratum transferred to the genus Cytophaga Int. J. Syst. Evol. Microbiol. 11, 107-108
34. Bradley, D. E. (1972) Shortening of Pseudomonas aeruginosa pili after RNA-phage adsorption J. Gen. Microbiol. 72, 303-319
35. Bradley, D. E. (1972) Evidence for the retraction of Pseudomonas aeruginosa RNA phage pili Biochem. Biophys. Res. Commun. 47, 142-149
36. Bradley, D. E. (1974) The adsorption of Pseudomonas aeruginosa pilus-dependent bacteriophages to a host mutant with nonretractile pili Virology 58, 149-163
37. Tammam, S., Sampaleanu, L. M., Koo, J., Manoharan, K., Daubaras, M., Burrows, L. L., and Howell, P. L. PilMNOPQ from the Pseudomonas aeruginosa Type IV Pilus System form a Transenvelope Protein Interaction Network that Interacts with PilA. J. Bacteriol. 2013, not supplied.
38. Korotkov, K. V. and Hol, W. G. (2013) Crystal structure of the pilotin from the enterohemorrhagic Escherichia coli type II secretion system J. Struct. Biol. 10.1016/j.jsb.2013.02.013
39. Szeto, T. H., Dessen, A., and Pelicic, V. (2011) Structure/function analysis of Neisseria meningitidis PilW, a conserved protein playing multiple roles in type IV pilus biology Infect. Immun. 79, 3028-3035
40. Guilvout, I., Chami, M., Berrier, C., Ghazi, A., Engel, A., Pugsley, A. P., and Bayan, N. (2008) In vitro multimerization and membrane insertion of bacterial outer membrane secretin PulD J. Mol. Biol. 382, 13-23
41. Guilvout, I., Chami, M., Engel, A., Pugsley, A. P., and Bayan, N. (2006) Bacterial outer membrane secretin PulD assembles and inserts into the inner membrane in the absence of its pilotin EMBO J. 25, 5241-5249
42. Guilvout, I., Nickerson, N. N., Chami, M., and Pugsley, A. P. (2011) Multimerization-defective variants of dodecameric secretin PulD Res. Microbiol. 162, 180-190
43. Nickerson, N. N., Abby, S. S., Rocha, E. P., Chami, M., and Pugsley, A. P. (2012) A Single Amino Acid Substitution Changes the Self-Assembly Status of a Type IV Piliation Secretin J. Bacteriol. 194, 4951-4958
44. Tammam, S., Sampaleanu, L. M., Koo, J., Sundaram, P., Ayers, M., Andrew Chong, P., Forman-Kay, J. D., Burrows, L. L., and Howell, P. L. (2011) Characterization of the PilN, PilO and PilP type IVa pilus subcomplex Mol. Microbiol. 82, 1496-1514
45. Collin, S., Guilvout, I., Nickerson, N. N., and Pugsley, A. P. (2011) Sorting of an integral outer membrane protein via the lipoprotein-specific Lol pathway and a dedicated lipoprotein pilotin Mol. Microbiol. 80, 655-665
46. Sampaleanu, L. M., Bonanno, J. B., Ayers, M., Koo, J., Tammam, S., Burley, S. K., Almo, S. C., Burrows, L. L., and Howell, P. L. (2009) Periplasmic domains of Pseudomonas aeruginosa PilN and PilO form a stable heterodimeric complex J. Mol. Biol. 394, 143-159
47. Jacobs, M. A., Alwood, A., Thaipisuttikul, I., Spencer, D., Haugen, E., Ernst, S., Will, O., Kaul, R., Raymond, C., Levy, R., Chun-Rong, L., Guenthner, D., Bovee, D., Olson, M. V., and Manoil, C. (2003) Comprehensive transposon mutant library of Pseudomonas aeruginosa Proc. Natl. Acad. Sci. U.S.A. 100, 14339-14344