Structural characterization of CFA/III and longus type IVb Pili from enterotoxigenic Escherichia coli

Journal of Bacteriology

Volumn 194, Issue 10, 2012, Pages 2725-2735

  Kolappan, Subramaniapillai ^a   Roos, Justin ^a   Yuen, Alex S W ^a   Pierce, Owen M ^a   Craig, Lisa ^a  

^a SIMON FRASER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CFA III PROTEIN; CHOLERA TOXIN; COFA PROTEIN; LONGUS TYPE IVB; PILIN; TOXIN COREGULATED PILI; UNCLASSIFIED DRUG;

ALPHA HELIX; ANIMAL CELL; ARTICLE; BACTERIAL STRAIN; BACTERIUM ADHERENCE; BACTERIUM PILUS; COLONY FORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; ELECTRON MICROSCOPY; ENTEROTOXIGENIC ESCHERICHIA COLI; GENE EXPRESSION; HETEROLOGOUS EXPRESSION; NONHUMAN; NUCLEOTIDE SEQUENCE; OPERON; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; VIBRIO CHOLERAE;

AMINO ACID SEQUENCE; ENTEROTOXIGENIC ESCHERICHIA COLI; FIMBRIAE PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN SUBUNITS; VIBRIO CHOLERAE;

ESCHERICHIA COLI; NEGIBACTERIA; VIBRIO CHOLERAE;

EID: 84861408384     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00282-12     Document Type: Article

References (58)

1. Anantha RP, Stone KD, Donnenberg MS. 1998. Role of BfpF, a member of the PilT family of putative nucleotide-binding proteins, in type IV pilus biogenesis and in interactions between enteropathogenic Escherichia coli and host cells. Infect. Immun. 66:122-131.
2. Asikyan ML, Kus JV, Burrows LL. 2008. Novel proteins that modulate type IV pilus retraction dynamics in Pseudomonas aeruginosa. J. Bacteriol. 190:7022-7034.
3. Audette GF, Irvin RT, Hazes B. 2004. Crystallographic analysis of the Pseudomonas aeruginosa strain K122-4 monomeric pilin reveals a conserved receptor-binding architecture. Biochemistry 43:11427-11435.
4. Ayers M, Howell PL, Burrows LL. 2010. Architecture of the type II secretion and type IV pilus machineries. Future Microbiol. 5:1203-1218.
5. Beard MK, et al. 1990. Morphogenetic expression of Moraxella bovis fimbriae (pili) in Pseudomonas aeruginosa. J. Bacteriol. 172:2601-2607.
6. Brunger AT, et al. 1998. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54:905-921.
7. Clavijo AP, Bai J, Gomez-Duarte OG. 2010. The Longus type IV pilus of enterotoxigenic Escherichia coli (ETEC) mediates bacterial selfaggregation and protection from antimicrobial agents. Microb. Pathog. 48:230-238.
8. Craig L, Li J. 2008. Type IV pili: paradoxes in form and function. Curr. Opin. Struct. Biol. 18:267-277.
9. Craig L, Pique ME, Tainer JA. 2004. Type IV pilus structure and bacterial pathogenicity. Nat. Rev. Microbiol. 2:363-378.
10. Craig L, et al. 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.
11. Craig L, et al. 2006. Type IV pilus structure by cryo-electron microscopy and crystallography: implications for pilus assembly and functions. Mol. Cell 23:651-662.
12. Davis IW, et al. 2007. MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res. 35:W375-W383.
13. De Lorenzo V, Timmis K. 1994. Analysis and construction of stable phenotypes in gram-negative bacteria with Tn5- and Tn10-derived minitransposons. Methods Enzymol. 235:386-405.
14. DiRita VJ, Neely M, Taylor RK, Bruss PM. 1996. Differential expression of the ToxR regulon in classical and E1 Tor biotypes of Vibrio cholerae is due to biotype-specific control over toxT expression. Proc. Natl. Acad. Sci. U. S. A. 93:7991-7995.
15. Emsley P, Cowtan K. 2004. COOT: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60:2126-2132.
16. Evans DG, Evans DJ, Jr, Tjoa W. 1977. Hemagglutination of human group A erythrocytes by enterotoxigenic Escherichia coli isolated from adults with diarrhea: correlation with colonization factor. Infect. Immun. 18:330-337.
17. Giron JA, Gomez-Duarte OG, Jarvis KG, Kaper JB. 1997. Longus pilus of enterotoxigenic Escherichia coli and its relatedness to other type-4 pili: a minireview. Gene 192:39-43.
18. Giron JA, Ho AS, Schoolnik GK. 1991. An inducible bundle-forming pilus of enteropathogenic Escherichia coli. Science 254:710-713.
19. Giron JA, Levine MM, Kaper JB. 1994. Longus: a long pilus ultrastructure produced by human enterotoxigenic Escherichia coli. Mol. Microbiol. 12:71-82.
20. Gomez-Duarte OG, et al. 2007. Genetic diversity of the gene cluster encoding Longus, a type IV pilus of enterotoxigenic Escherichia coli. J. Bacteriol. 189:9145-9149.
21. Hartung S, et al. 2011. Ultra-high resolution and full-length pilin structures with insights for filament assembly, pathogenic functions and vaccine potential. J. Biol. Chem. 286:44254-44265.
22. Hazes B, Sastry PA, Hayakawa K, Read RJ, Irvin RT. 2000. Crystal structure of Pseudomonas aeruginosa PAK pilin suggests a main-chaindominated mode of receptor binding. J. Mol. Biol. 299:1005-1017.
23. Honda T, Arita M, Miwatani T. 1984. Characterization of new hydrophobic pili of human enterotoxigenic Escherichia coli: a possible new colonization factor. Infect. Immun. 43:959-965.
24. Honda T, Wetprasit N, Arita M, Miwatani T. 1989. Production and characterization of monoclonal antibodies to a pilus colonization factor (colonization factor antigen III) of human enterotoxigenic Escherichia coli. Infect. Immun. 57:3452-3457.
25. Hyland RM, et al. 2008. The bundlin pilin protein of enteropathogenic Escherichia coli is an N-acetyllactosamine-specific lectin. Cell. Microbiol. 10:177-187.
26. Kirn TJ, Lafferty MJ, Sandoe CM, Taylor RK. 2000. Delineation of pilin domains required for bacterial association into microcolonies and intestinal colonization by Vibrio cholerae. Mol. Microbiol. 35:896-910.
27. Laskowski RA, McArthur MW, Moss DS, Thornton JM. 1993. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26:283-291.
28. Leslie AGW, Brick P, Wonacott A. 1986. Daresbury Laboratory information quarterly for protein crystallography, vol 18, p 33-39. Daresbury Laboratory, Warrinton, United Kingdom.
29. Li J, Egelman E, Craig L. 2012. Structure of the Vibrio cholerae type IVb pilus and stability comparison with the Neisseria gonorrhoeae type IVa pilus. J. Mol. Biol. 418:47-64.
30. Li J, et al. 2008. Vibrio cholerae toxin-coregulated pilus structure analyzed by hydrogen/deuterium exchange mass spectrometry. Structure 16:137-148.
31. Lim MS, et al. 2010. Vibrio cholerae El Tor TcpA crystal structure and mechanism for pilus-mediated microcolony formation. Mol. Microbiol. 77:755-770.
32. Lu Q. 2005. Seamless cloning and gene fusion. Trends Biotechnol. 23: 199-207.
33. Mattick JS, et al. 1987. Morphogenetic expression of Bacteroides nodosus fimbriae in Pseudomonas aeruginosa. J. Bacteriol. 169:33-41.
34. Mazariego-Espinosa K, Cruz A, Ledesma MA, Ochoa SA, Xicohtencatl-Cortes J. 2010. Longus, a type IV pilus of enterotoxigenic Escherichia coli, is involved in adherence to intestinal epithelial cells. J. Bacteriol. 192: 2791-2800.
35. McNamara BP, Donnenberg MS. 2000. Evidence for specificity in type 4 pilus biogenesis by enteropathogenic Escherichia coli. Microbiology 146: 719-729.
36. Murshudov GN, Vagin AA, Dodson EJ. 1997. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53:240-255.
37. Nguyen Y, Jackson SG, Aidoo F, Junop M, Burrows LL. 2010. Structural characterization of novel Pseudomonas aeruginosa type IV pilins. J. Mol. Biol. 395:491-503.
38. Nye MB, Pfau JD, Skorupski K, Taylor RK. 2000. Vibrio cholerae H-NS silences virulence gene expression at multiple steps in the ToxR regulatory cascade. J. Bacteriol. 182:4295-4303.
39. Oron A, Wolfson H, Gunasekaran K, Nussinov R. 2003. Using DelPhi to compute electrostatic potentials and assess their contribution to interactions. Curr. Protoc. Bioinformatics 8:Unit 8.4.
40. Parge HE, et al. 1995. Structure of the fibre-forming protein pilin at 2.6 Å resolution. Nature 378:32-38.
41. Pelicic V. 2008. Type IV pili: e pluribus unum? Mol. Microbiol. 68:827-837
42. Perrakis A, Morris R, Lamzin VS. 1999. Automated protein model building combined with iterative structure refinement. Nat. Struct. Biol. 6:458-463.
43. Pier GB, et al. 1998. Salmonella typhi uses CFTR to enter intestinal epithelial cells. Nature 393:79-82.
44. Qadri F, et al. 2000. Human antibody response to Longus type IV pilus and study of its prevalence among enterotoxigenic Escherichia coli in Bangladesh by using monoclonal antibodies. J. Infect. Dis. 181:2071-2074.
45. Ramboarina S, et al. 2005. Structure of the bundle-forming pilus from enteropathogenic Escherichia coli. J. Biol. Chem. 48:40252-40260.
46. Rodgers K, Arvidson CG, Melville S. 2011. Expression of a Clostridium perfringens type IV pilin by Neisseria gonorrhoeae mediates adherence to muscle cells. Infect. Immun. 79:3096-3105.
47. Salomonsson E, et al. 2009. Functional analyses of pilin-like proteins from Francisella tularensis: complementation of type IV pilus phenotypes in Neisseria gonorrhoeae. Microbiology 155:2546-2559.
48. Skorupski K, Taylor RK. 1996. Positive selection vectors for allelic exchange. Gene 169:47-52.
49. Storoni LC, McCoy AJ, Read RJ. 2004. Likelihood-enhanced fast rotation functions. Acta Crystallogr. D Biol. Crystallogr. 60:432-438.
50. Strom MS, Lory S. 1993. Structure-function and biogenesis of the type IV pili. Annu. Rev. Microbiol. 47:565-596.
51. Taniguchi T, et al. 2001. Gene cluster for assembly of pilus colonization factor antigen III of enterotoxigenic Escherichia coli. Infect. Immun. 69: 5864-5873.
52. Taniguchi T, Fujino Y, Yamamoto K, Miwatani T, Honda T. 1995. Sequencing of the gene encoding the major pilin of pilus colonization factor antigen III (CFA/III) of human enterotoxigenic Escherichia coli and evidence that CFA/III is related to type IV pili. Infect. Immun. 63:724-728.
53. Taylor RK, Miller VL, Furlong DB, Mekalanos JJ. 1987. Use of phoA gene fusions to identify a pilus colonization factor coordinately regulated with cholera toxin. Proc. Natl. Acad. Sci. U. S. A. 84:2833-2837.
54. Tsui IS, Yip CM, Hackett J, Morris C. 2003. The type IVB pili of Salmonella enterica serovar Typhi bind to the cystic fibrosis transmembrane conductance regulator. Infect. Immun. 71:6049-6050.
55. Vaguine AA, Richelle J, Wodak SJ. 1999. SFCHECK: a unified set of procedures for evaluating the quality of macromolecular structure-factor data and their agreement with the atomic model. Acta Crystallogr. D Biol. Crystallogr. 55:191-205.
56. Watson AA, Mattick JS, Alm RA. 1996. Functional expression of heterologous type 4 fimbriae in Pseudomonas aeruginosa. Gene 175:143-150.
57. Winther-Larsen HC, et al. 2007. Pseudomonas aeruginosa type IV pilus expression in Neisseria gonorrhoeae: effects of pilin subunit composition on function and organelle dynamics. J. Bacteriol. 189:6676-6685.
58. Xu XF, et al. 2004. NMR structure of a type IVb pilin from Salmonella typhi and its assembly into pilus. J. Biol. Chem. 279:31599-31605.