Modification of Pseudomonas aeruginosa Pa5196 type IV pilins at multiple sites with D-Araf by a novel GT-C family arabinosyltransferase, TfpW

Journal of Bacteriology

Volumn 190, Issue 22, 2008, Pages 7464-7478

  Kus, Julianne V ^a   Kelly, John ^b   Tessier, Luc ^b   Harvey, Hanjeong ^c   Cvitkovitch, Dennis G ^a   Burrows, Lori L ^a,c,d,e  

^a UNIVERSITY OF TORONTO   (Canada)

^b NATIONAL RESEARCH COUNCIL CANADA   (Canada)

^c MCMASTER UNIVERSITY   (Canada)

^d MCMASTER UNIVERSITY   (Canada)

^e MCMASTER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ARABINOSYLTRANSFERASE TFPW; GLYCOSYLTRANSFERASE; PILIN; PILIN TYPE IV; SERINE; THREONINE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL STRAIN; CONTROLLED STUDY; ELECTROSPRAY MASS SPECTROMETRY; ENZYME SPECIFICITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN GLYCOSYLATION; PROTEIN MOTIF; PROTEIN PROCESSING; PSEUDOMONAS AERUGINOSA; SITE DIRECTED MUTAGENESIS;

AMINO ACID SEQUENCE; ARABINOSE; BACTERIAL PROTEINS; BLOTTING, WESTERN; CHROMATOGRAPHY, LIQUID; ELECTROPHORESIS, POLYACRYLAMIDE GEL; FIMBRIAE PROTEINS; GENETIC COMPLEMENTATION TEST; GLYCOSYLATION; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; MUTATION; PENTOSYLTRANSFERASES; PROTEIN PROCESSING, POST-TRANSLATIONAL; PSEUDOMONAS AERUGINOSA; SEQUENCE HOMOLOGY, AMINO ACID; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; SUBSTRATE SPECIFICITY; TANDEM MASS SPECTROMETRY;

MYCOBACTERIUM; NEGIBACTERIA; PILA; PSEUDOMONAS; PSEUDOMONAS AERUGINOSA;

EID: 55549121207     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.01075-08     Document Type: Article

References (64)

1. Aas, F. E., A. Vik, J. Vedde, M. Koomey, and W. Egge-Jacobsen. 2007. Neisseria gonorrhoeae O-linked pilin glycosylation: functional analyses define both the biosynthetic pathway and glycan structure. Mol. Microbiol. 65:607-624.
2. Aas, F. E., W. Egge-Jacobsen, H. C. Winther-Larsen, C. Lovold, P. G. Hitchen, A. Dell, and M. Koomey. 2006. Neisseria gonorrhoeae type IV pili undergo multisite, hierarchical modifications with phosphoethanolamine and phosphocholine requiring an enzyme structurally related to lipopolysaccharide phosphoethanolamine transferases. J. Biol. Chem. 281:27712-27723.
3. Alaimo, C., I. Catrein, L. Morf, C. L. Marolda, N. Callewaert, M. A. Valvano, M. F. Feldman, and M. Aebi. 2006. Two distinct but interchangeable mechanisms for flipping of lipid-linked oligosaccharides. EMBO J. 25:967-976.
4. Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
5. 4a.Asikyan, M. L., J. V. Kus, and L. L. Burrows. 2008. Novel proteins that modulate type IV pilus retraction dynamics in Pseudomonas aeruginosa. J. Bacteriol. 190:7022-7034.
6. Benz, I., and M. A. Schmidt. 2002. Never say never again: protein glycosylation in pathogenic bacteria. Mol. Microbiol. 45:267-276.
7. Berg, S., D. Kaur, M. Jackson, and P. J. Brennan. 2007. The glycosyltransferases of Mycobacterium tuberculosis - roles in the synthesis of arabinogalactan, lipoarabinomannan, and other glycoconjugates. Glycobiology 17:35R-56R.
8. Blatch, G. L., and M. Lassle. 1999. The tetratricopeptide repeat: a structural motif mediating protein-protein interactions. Bioessays 21:932-939.
9. Burrows, L. L. 2005. Weapons of mass retraction. Mol. Microbiol. 57:878-888.
10. Castric, P. 1995. pilO, a gene required for glycosylation of Pseudomonas aeruginosa 1244 pilin. Microbiology 141:1247-1254.
11. Chamot-Rooke, J., B. Rousseau, F. Lanternier, G. Mikaty, E. Mairey, C. Malosse, G. Bouchoux, V. Pelicic, L. Camoin, X. Nassif, and G. Dumenil. 2007. Alternative Neisseria spp. type IV pilin glycosylation with a glyceramido acetamido trideoxyhexose residue. Proc. Natl. Acad. Sci. USA 104:14783-14788.
12. Chenna, R., H. Sugawara, T. Koike, R. Lopez, T. J. Gibson, D. G. Higgins, and J. D. Thompson. 2003. Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res. 31:3497-3500.
13. Chiang, P., and L. L. Burrows. 2003. Biofilm formation by hyperpiliated mutants of Pseudomonas aeruginosa. J. Bacteriol. 185:2374-2378.
14. Choi, K. H., A. Kumar, and H. P. Schweizer. 2006. A 10-min method for preparation of highly electrocompetent Pseudomonas aeruginosa cells: application for DNA fragment transfer between chromosomes and plasmid transformation. J. Microbiol. Methods 64:391-397.
15. Coleman, F. T., S. Mueschenborn, G. Meluleni, C. Ray, V. J. Carey, S. O. Vargas, C. L. Cannon, F. M. Ausubel, and G. B. Pier. 2003. Hypersusceptibility of cystic fibrosis mice to chronic Pseudomonas aeruginosa oropharyngeal colonization and lung infection. Proc. Natl. Acad. Sci. USA 100:1949-1954.
16. Comer, J. E., M. A. Marshall, V. J. Blanch, C. D. Deal, and P. Castric. 2002. Identification of the Pseudomonas aeruginosa 1244 pilin glycosylation site. Infect. Immun. 70:2837-2845.
17. Coon, J. J., B. Ueberheide, J. E. Syka, D. D. Dryhurst, J. Ausio, J. Shabanowitz, and D. F. Hunt. 2005. Protein identification using sequential ion/ion reactions and tandem mass spectrometry. Proc. Natl. Acad. Sci. USA 102:9463-9468.
18. Coutinho, P. M., E. Deleury, G. J. Davies, and B. Henrissat. 2003. An evolving hierarchical family classification for glycosyltransferases. J. Mol. Biol. 328:307-317.
19. Craig, L., M. E. Pique, and J. A. Tainer. 2004. Type IV pilus structure and bacterial pathogenicity. Nat. Rev. Microbiol. 2:363-378.
20. Craig, L., R. K. Taylor, M. E. Pique, B. D. Adair, A. S. Arvai, M. Singh, S. J. Lloyd, D. S. Shin, E. D. Getzoff, M. Yeager, K. T. Forest, and J. A. Tainer. 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 11:1139-1150.
21. DiGiandomenico, A., M. J. Matewish, A. Bisaillon, J. R. Stehle, J. S. Lam, and P. Castric. 2002. Glycosylation of Pseudomonas aeruginosa 1244 pilin: glycan substrate specificity. Mol. Microbiol. 46:519-530.
22. Doig, P., T. Todd, P. A. Sastry, K. K. Lee, R. S. Hodges, W. Paranchych, and R. T. Irvin. 1988. Role of pili in adhesion of Pseudomonas aeruginosa to human respiratory epithelial cells. Infect. Immun. 56:1641-1646.
23. Faridmoayer, A., M. A. Fentabil, D. C. Mills, J. S. Klassen, and M. F. Feldman. 2007. Functional characterization of bacterial oligosaccharyltransferases involved in O-linked protein glycosylation. J. Bacteriol. 189:8088-8098.
24. Gallant, C. V., C. Daniels, J. M. Leung, A. S. Ghosh, K. D. Young, L. P. Kotra, and L. L. Burrows. 2005. Common beta-lactamases inhibit bacterial biofilm formation. Mol. Microbiol. 58:1012-1024.
25. Reference deleted.
26. Giltner, C. L., E. J. van Schaik, G. F. Audette, D. Kao, R. S. Hodges, D. J. Hassett, and R. T. Irvin. 2006. The Pseudomonas aeruginosa type IV pilin receptor binding domain functions as an adhesin for both biotic and abiotic surfaces. Mol. Microbiol. 59:1083-1096.
27. Hahn, H. P. 1997. The type-4 pilus is the major virulence-associated adhesin of Pseudomonas aeruginosa - a review. Gene 192:99-108.
28. Hegge, F. T., P. G. Hitchen, F. E. Aas, H. Kristiansen, C. Lovold, W. Egge-Jacobsen, M. Panico, W. Y. Leong, V. Bull, M. Virji, H. R. Morris, A. Dell, and M. Koomey. 2004. Unique modifications with phosphocholine and phosphoethanolamine define alternate antigenic forms of Neisseria gonorrhoeae type IV pili. Proc. Natl. Acad. Sci. USA 101:10798-10803.
29. Hoang, T. T., R. R. Karkhoff-Schweizer, A. J. Kutchma, and H. P. Schweizer. 1998. A broad-host-range Flp-FRT recombination system for site-specific excision of chromosomally-located DNA sequences: application for isolation of unmarked Pseudomonas aeruginosa mutants. Gene 212:77-86.
30. Hogan, J. M., S. J. Pitteri, P. A. Chrisman, and S. A. McLuckey. 2005. Complementary structural information from a tryptic N-linked glycopeptide via electron transfer ion/ion reactions and collision-induced dissociation. J. Proteome Res. 4:628-632.
31. Horton, R. M., Z. L. Cai, S. N. Ho, and L. R. Pease. 1990. Gene splicing by overlap extension: tailor-made genes using the polymerase chain reaction. BioTechniques 8:528-535.
32. Horzempa, J., J. E. Comer, S. A. Davis, and P. Castric. 2006. Glycosylation substrate specificity of Pseudomonas aeruginosa 1244 pilin. J. Biol. Chem. 281:1128-1136.
33. Kikuchi, N., Y. D. Kwon, M. Gotoh, and H. Narimatsu. 2003. Comparison of glycosyltransferase families using the profile hidden Markov model. Biochem. Biophys. Res. Commun. 310:574-579.
34. Kuo, C., N. Takahashi, A. F. Swanson, Y. Ozeki, and S. Hakomori. 1996. An N-linked high-mannose type oligosaccharide, expressed at the major outer membrane protein of Chlamydia trachomatis, mediates attachment and infectivity of the microorganism to HeLa cells. J. Clin. Investig. 98:2813-2818.
35. Kus, J. V., E. Tullis, D. G. Cvitkovitch, and L. L. Burrows. 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.
36. Lefebre, M. D., and M. A. Valvano. 2002. Construction and evaluation of plasmid vectors optimized for constitutive and regulated gene expression in Burkholderia cepacia complex isolates. Appl. Environ. Microbiol. 68:5956-5964.
37. Lindenthal, C., and E. A. Elsinghorst. 1999. Identification of a glycoprotein produced by enterotoxigenic Escherichia coli. Infect. Immun. 67:4084-4091.
38. Liu, J., and A. Mushegian. 2003. Three monophyletic superfamilies account for the majority of the known glycosyltransferases. Protein Sci. 12:1418-1431.
39. Lu, H. M., S. T. Motley, and S. Lory. 1997. Interactions of the components of the general secretion pathway: role of Pseudomonas aeruginosa type IV pilin subunits in complex formation and extracellular protein secretion. Mol. Microbiol. 25:247-259.
40. Lyczak, J. B., C. L. Cannon, and G. B. Pier. 2000. Establishment of Pseudomonas aeruginosa infection: lessons from a versatile opportunist. Microbes Infect. 2:1051-1060.
41. Marceau, M., and X. Nassif. 1999. Role of glycosylation at Ser63 in production of soluble pilin in pathogenic Neisseria. J. Bacteriol. 181:656-661.
42. Marceau, M., K. Forest, J. L. Beretti, J. Tainer, and X. Nassif. 1998. Consequences of the loss of O-linked glycosylation of meningococcal type IV pilin on piliation and pilus-mediated adhesion. Mol. Microbiol. 27:705-715.
43. Mattick, J. S. 2002. Type IV pili and twitching motility. Annu. Rev. Microbiol. 56:289-314.
44. Murray, T. S., M. Egan, and B. I. Kazmierczak. 2007. Pseudomonas aeruginosa chronic colonization in cystic fibrosis patients. Curr. Opin. Pediatr. 19:83-88.
45. O'Toole, G. A., and R. Kolter. 1998. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol. Microbiol. 30:295-304.
46. Power, P. M., and M. P. Jennings. 2003. The genetics of glycosylation in Gram-negative bacteria. FEMS Microbiol. Lett. 218:211-222.
47. Power, P. M., K. L. Seib, and M. P. Jennings. 2006. Pilin glycosylation in Neisseria meningitidis occurs by a similar pathway to wzy-dependent Oantigen biosynthesis in Escherichia coli. Biochem. Biophys. Res. Commun. 347:904-908.
48. Romling, U., B. Fiedler, J. Bosshammer, D. Grothues, J. Greipel, H. von der Hardt, and B. Tummler. 1994. Epidemiology of chronic Pseudomonas aeruginosa infections in cystic fibrosis. J. Infect. Dis. 170:1616-1621.
49. Saiman, L., and A. Prince. 1993. Pseudomonas aeruginosa pili bind to asialoGM1 which is increased on the surface of cystic fibrosis epithelial cells. J. Clin. Investig. 92:1875-1880.
50. Smedley, J. G., III, E. Jewell, J. Roguskie, J. Horzempa, A. Syboldt, D. B. Stolz, and P. Castric. 2005. Influence of pilin glycosylation on Pseudomonas aeruginosa 1244 pilus function. Infect. Immun. 73:7922-7931.
51. Spangenberg, C., R. Fislage, W. Sierralta, B. Tummler, and U. Romling. 1995. Comparison of type IV-pilin genes of Pseudomonas aeruginosa of various habitats has uncovered a novel unusual sequence. FEMS Microbiol. Lett. 125:265-273.
52. Spyropoulos, I. C., T. D. Liakopoulos, P. G. Bagos, and S. J. Hamodrakas. 2004. TMRPres2D: high quality visual representation of transmembrane protein models. Bioinformatics 20:3258-3260.
53. Stimson, E., M. Virji, S. Barker, M. Panico, I. Blench, J. Saunders, G. Payne, E. R. Moxon, A. Dell, and H. R. Morris. 1996. Discovery of a novel protein modification: alpha-glycerophosphate is a substituent of meningococcal pilin. Biochem. J. 316:29-33.
54. Stimson, E., M. Virji, K. Makepeace, A. Dell, H. R. Morris, G. Payne, J. R. Saunders, M. P. Jennings, S. Barker, and M. Panico. 1995. Meningococcal pilin: a glycoprotein substituted with digalactosyl 2,4-diacetamido-2,4,6-trideoxyhexose. Mol. Microbiol. 17:1201-1214.
55. Strom, M. S., and S. Lory. 1993. Structure-function and biogenesis of the type IV pili. Annu. Rev. Microbiol. 47:565-596.
56. Strom, M. S., and S. Lory. 1986. Cloning and expression of the pilin gene of Pseudomonas aeruginosa PAK in Escherichia coli. J. Bacteriol. 165:367-372.
57. Syka, J. E., J. J. Coon, M. J. Schroeder, J. Shabanowitz, and D. F. Hunt. 2004. Peptide and protein sequence analysis by electron transfer dissociation mass spectrometry. Proc. Natl. Acad. Sci. USA 101:9528-9533.
58. Szymanski, C. M., and B. W. Wren. 2005. Protein glycosylation in bacterial mucosal pathogens. Nat. Rev. Microbiol. 3:225-237.
59. Szymanski, C. M., D. H. Burr, and P. Guerry. 2002. Campylobacter protein glycosylation affects host cell interactions. Infect. Immun. 70:2242-2244.
60. Voisin, S., J. V. Kus, S. Houliston, F. St-Michael, D. Watson, D. G. Cvitkovitch, J. Kelly, J. R. Brisson, and L. L. Burrows. 2007. Glycosylation of Pseudomonas aeruginosa strain Pa5196 type IV pilins with mycobacterium-like α-1,5-linked D-Araf oligosaccharides. J. Bacteriol. 189:151-159.
61. Wall, D., and D. Kaiser. 1999. Type IV pili and cell motility. Mol. Microbiol. 32:1-10.
62. Wang, W., and B. A. Malcolm. 1999. Two-stage PCR protocol allowing introduction of multiple mutations, deletions and insertions using QuikChange site-directed mutagenesis. BioTechniques 26:680-682.
63. Wong, W. Y., A. P. Campbell, C. McInnes, B. D. Sykes, W. Paranchych, R. T. Irvin, and R. S. Hodges. 1995. Structure-function analysis of the adherence-binding domain on the pilin of Pseudomonas aeruginosa strains PAK and KB7. Biochemistry 34:12963-12972.
64. Wuhrer, M., J. C. Stam, F. E. van de Geijn, C. A. Koeleman, C. T. Verrips, R. J. Dolhain, C. H. Hokke, and A. M. Deelder. 2007. Glycosylation profiling of immunoglobulin G (IgG) subclasses from human serum. Proteomics 7:4070-4081.