Assembly of CS1 pili: The role of specific residues of the major pilin, CooA

Journal of Bacteriology

Volumn 188, Issue 1, 2006, Pages 231-239

  Starks, Angela M ^a   Froehlich, Barbara J ^a   Jones, Tamara N ^a   Scott, June R ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ESCHERICHIA COLI ENTEROTOXIN; STRUCTURAL PROTEIN; VIRULENCE FACTOR; COOA PROTEIN, E COLI; ESCHERICHIA COLI PROTEIN; FIMBRIA PROTEIN;

AMINO ACID SUBSTITUTION; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL VIRULENCE; BACTERIUM PILUS; ENZYME SPECIFICITY; GENE MUTATION; GENETIC CONSERVATION; HYDROPHOBICITY; MULTIGENE FAMILY; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; RESIDUE ANALYSIS; STRUCTURE ANALYSIS; AMINO ACID SEQUENCE; CHEMISTRY; ESCHERICHIA COLI K 12; FIMBRIA; GENETICS; HEMAGGLUTINATION; METABOLISM; MOLECULAR GENETICS; MUTATION; SITE DIRECTED MUTAGENESIS; STRUCTURE ACTIVITY RELATION;

BACTERIA (MICROORGANISMS); BOVINAE; ESCHERICHIA COLI;

AMINO ACID SEQUENCE; ESCHERICHIA COLI K12; ESCHERICHIA COLI PROTEINS; FIMBRIAE PROTEINS; FIMBRIAE, BACTERIAL; HEMAGGLUTINATION; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; MUTATION; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 33644903531     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.188.1.231-239.2006     Document Type: Article

References (57)

1. Amann, E., B. Ochs, and K. J. Abel. 1988. Tightly regulated tac promoter vectors useful for the expression of unfused and fused proteins in Escherichia coli. Gene 69:301-315.
2. Attridge, S. R., G. Wallerstrom, F. Qadri, and A. M. Svennerholm. 2004. Detection of antibodies to toxin-coregulated pili in sera from cholera patients. Infect. Immun. 72:1824-1827.
3. Baneyx, F., and G. Georgiou. 1991. Construction and characterization of Escherichia coli strains deficient in multiple secreted proteases: protease III degrades high-molecular-weight substrates in vivo. J. Bacteriol. 173:2696-2703.
4. Barry, E. M., Z. Altboum, G. Losonsky, and M. M. Levine. 2003. Immune responses elicited against multiple enterotoxigenic Escherichia coli fimbriae and mutant LT expressed in attenuated Shigella vaccine strains. Vaccine 21:333-340.
5. Black, R. E. 1993. Epidemiology of diarrhoeal disease: implications for control by vaccines. Vaccine 11:100-106.
6. Black, R. E. 1990. Epidemiology of travelers' diarrhea and relative importance of various pathogens. Rev. Infect. Dis. 12(Suppl. 1):S73-S79.
7. Black, R. E., K. H. Brown, S. Becker, A. R. Alim, and I. Huq. 1982. Longitudinal studies of infectious diseases and physical growth of children in rural Bangladesh. II. Incidence of diarrhea and association with known pathogens. Am. J. Epidemiol. 115:315-324.
8. Casadaban, M. J. 1976. Transposition and fusion of the lac genes to selected promoters in Escherichia coli using bacteriophage lambda and Mu. J. Mol. Biol. 104:541-555.
9. Dodson, K. W., F. Jacob-Dubuisson, R. T. Striker, and S. J. Hultgren. 1993. Outer-membrane PapC molecular usher discriminately recognizes periplasmic chaperone-pilus subunit complexes. Proc. Natl. Acad. Sci. USA 90:3670-3674.
10. Edwards, R. A., and J. L. Puente. 1998. Fimbrial expression in enteric bacteria: a critical step in intestinal pathogenesis. Trends Microbiol. 6:282-287.
11. Folkesson, A., A. Advani, S. Sukupolvi, J. D. Pfeifer, S. Normark, and S. Lofdahl. 1999. Multiple insertions of fimbrial operons correlate with the evolution of Salmonella serovars responsible for human disease. Mol. Microbiol. 33:612-622.
12. Froehlich, B, J., A. Karakashian, L. R. Melsen, J. C. Wakefield, and J. R. Scott. 1994. CooC and CooD are required for assembly of CS1 pili. Mol. Microbiol. 12:387-401.
13. Gaastra, W., and A. M. Svennerholm. 1996. Colonization factors of human enterotoxigenic Escherichia coli (ETEC). Trends Microbiol. 4:444-452.
14. Giron, J. A., M. M. Levine, and J. B. Kaper. 1994. Longus: a long pilus ultrastructure produced by human enterotoxigenic Escherichia coli. Mol. Microbiol. 12:71-82.
15. Hall, R. H., D. R. Maneval, Jr., J. H. Collins, J. L. Theibert, and M. M. Levine. 1989. Purification and analysis of colonization factor antigen I, coli surface antigen 1, and coli surface antigen 3 fimbriae from enterotoxigenic Escherichia coli. J. Bacteriol. 171:6372-6374.
16. Hammar, M., Z, Bian, and S. Normark. 1996. Nucleator-dependent intercellular assembly of adhesive curli organelles in Escherichia coli. Proc. Natl. Acad. Sci. USA 93:6562-6566.
17. Horton, R. M., H. D. Hunt, S. N. Ho, J. K. Pullen, and L. R. Pease. 1989. Engineering hybrid genes without the use of restriction enzymes: gene splicing by overlap extension. Gene 77:61-68.
18. Hultgren, S. J., C. H. Jones, and S. N. Normark, 1996. Bacterial adhesions and their assembly, p. 2730-2756. In F. C. Neidhardt, R. Curtiss III, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, M. Schaechter, and H. E. Umbarger (ed.), Escherichia coli and Salmonella: cellular and molecular biology. ASM Press, Washington, D.C.
19. Hultgren, S. J., S. Normark, and S. N. Abraham. 1991. Chaperone-assisted assembly and molecular architecture of adhesive pili. Annu. Rev. Microbiol. 45:383-415.
20. Hung, D. L., and S. J. Hultgren. 1998. Pilus biogenesis via the chaperone/usher pathway: an integration of structure and function. J. Struct. Biol. 124:201-220.
21. Kaper, J. B., J. P. Nataro, and H. L. Mobley. 2004. Pathogenic Escherichia coli. Nat. Rev. Microbiol. 2:123-140.
22. Kuehn, M. J., J. Heuser, S. Normark, and S. J. Hultgren. 1992. P pili in uropathogenic E. coli are composite fibers with distinct fibrillar adhesive tips. Nature 356:252-255.
23. Kuehn, M. J., D. J. Ogg, J. Kihlberg, L. N. Slonim, K. Flemmer, T. Bergfors, and S. J. Hultgren. 1993. Structural basis of pilus subunit recognition by the PapD chaperone. Science 262:1234-1241.
24. Levine, M., J. G. Morris, G. Losonsky, E. Boedeker, and B. Rowe. 1986. Fimbriae (pili) adhesins as vaccines, p. 14-145. In D. L. Lark (ed.), Protein-carbohydrate interactions in biological systems. Academic Press, Inc., London, United Kingdom.
25. Levine, M. M., and R. Edelman. 1990. Future vaccines against enteric pathogens. Infect. Dis. Clin. N. Am. 4:105-121.
26. Moon, H. W., and T. O. Bunn. 1993. Vaccines for preventing enterotoxigenic Escherichia coli infections in farm animals. Vaccine 11:213-300.
27. Nataro, J. P., and J. B. Kaper. 1998. Diarrheagenic Escherichia coli. Clin. Microbiol. Rev. 11:142-201.
28. Perez-Casal, J., J. S. Swartley, and J. R. Scott. 1990. Gene encoding the major subunit of CS1 pili of human enterotoxigenic Escherichia coli. Infect. Immun. 58:3594-3600.
29. Roberts, J. A., M. B. Kaack, G. Baskin, M. R. Chapman, D. A, Hunstad, J. S. Pinkner, and S. J. Hultgren. 2004. Antibody responses and protection from pyelonephritis following vaccination with purified Escherichia coli PapDG protein. J. Urol. 171:1682-1685.
30. Sajjan, U. S., L. Sun, R. Goldstein, and J. F. Forstner. 1995. Cable (cbl) type II pili of cystic fibrosis-associated Burkholderia (Pseudomonas) cepacia: nucleotide sequence of the cblA major subunit pilin gene and novel morphology of the assembled appendage fibers. J. Bacteriol. 177:1030-1038.
31. Sakellaris, H., D. P. Balding, and J. R. Scott. 1996. Assembly proteins of CS1 pili of enterotoxigenic Escherichia coli. Mol. Microbiol. 21:529-541.
32. Sakellaris, H., G. P. Munson, and J. R. Scott. 1999. A conserved residue in the tip proteins of CS1 and CFA/I pili of enterotoxigenic Escherichia coli that is essential for adherence. Proc. Natl. Acad. Sci. USA 96:12828-12832.
33. Sakellaris, H., V. R. Penumalli, and J. R. Scott. 1999. The level of expression of the minor pilin subunit, CooD, determines the number of CS1 pili assembled on the cell surface of Escherichia coli. J. Bacteriol. 181:1694-1697.
34. Sakellaris, H., and J. R. Scott. 1998. New tools in an old trade: CS1 pilus morphogenesis. Mol. Microbiol. 30:681-687.
35. Sanchez, J., and J. Holmgren. 2005. Virulence factors, pathogenesis and vaccine protection in cholera and ETEC diarrhea. Curr. Opin. Immunol. 17:1-11.
36. Sauer, F. G., K. Futterer, J. S. Pinkner, K. W. Dodson, S. J. Hultgren, and G. Waksman. 1999. Structural basis of chaperone function and pilus biogenesis. Science 285:1058-1061.
37. Sauer, F. G., S. D. Knight, G. J. Waksman, and S. J. Hultgren. 2000. PapD-like chaperones and pilus biogenesis. Semin. Cell Dev. Biol. 11:27-34.
38. Sauer, F. G., M. A. Mulvey, J. D. Schilling, J. J. Martinez, and S. J. Hultgren. 2000. Bacterial pili: molecular mechanisms of pathogenesis. Curr. Opin. Microbiol. 3:65-72.
39. Schmidt, T. G., J. Koepke, R. Frank, and A. Skerra. 1996. Molecular interaction between the Strep-tag affinity peptide and its cognate target, streptavidin. J. Mol. Biol. 255:753-766.
40. Schnetz, K., S. L. Sutrina, M. H, Saier, Jr., and B. Rak. 1990. Identification of catalytic residues in the beta-glucoside permease of Escherichia coli by site-specific mutagenesis and demonstration of interdomain cross-reactivity between the beta-glucoside and glucose systems. J. Biol. Chem. 265:13464-13471.
41. Scott, J. R., J. C. Wakefield, P. W. Russell, P. E. Orndorff, and B. J. Froehlich. 1992. CooB is required for assembly but not transport of CS1 pilin. Mol. Microbiol. 6:293-300.
42. Sears, C. L., and J. B. Kaper. 1996. Enteric bacterial toxins: mechanisms of action and linkage to intestinal secretion. Microbiol. Rev. 60:167-215.
43. Silber, K. R., and R. T. Sauer. 1994. Deletion of the prc (tsp) gene provides evidence for additional tail-specific proteolytic activity in Escherichia coli K-12. Mol. Gen. Genet. 242:237-240.
44. Skerra, A., and T. G. Schmidt. 2000. Use of the Strep-Tag and streptavidin for detection and purification of recombinant proteins. Methods Enzymol. 326:271-304.
45. Soto, G. E., K. W. Dodson, D. Ogg, C. Liu, J. Heuser, S. Knight, J. Kihlberg, C. H. Jones, and S. J. Hultgren. 1998. Periplasmic chaperone recognition motif of subunits mediates quaternary interactions in the pilus. EMBO J. 17:6155-6167.
46. Soto, G. E., and S. J. Hultgren. 1999. Bacterial adhesins: common themes and variations in architecture and assembly. J. Bacteriol. 181:1059-1071.
47. Stone, K. D., H. Z. Zhang, L. K. Carlson, and M. S. Donnenberg. 1996. A cluster of fourteen genes from enteropathogenic Escherichia coli is sufficient for the biogenesis of a type IV pilus. Mol. Microbiol. 20:325-337.
48. Strom, M. S., and S. Lory. 1993. Structure-function and biogenesis of the type IV pili. Annu. Rev. Microbiol. 47:565-596.
49. - complementation and chloramphenicol- or kanamycin-resistance selection. Gene 61:63-74.
50. Thanassi, D. G., E. T. Saulino, and S. J. Hultgren. 1998. The chaperone/usher pathway: a major terminal branch of the general secretory pathway. Curr. Opin. Microbiol. 1:223-231.
51. Thanassi, D. G., E. T. Saulino, M. J. Lombardo, R. Roth, J. Heuser, and S. J. Hultgren. 1998. The PapC usher forms an oligomeric channel: implications for pilus biogenesis across the outer membrane. Proc. Natl. Acad. Sci. USA 95:3146-3151.
52. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
53. Voegele, K., H. Sakellaris, and J. R. Scott. 1997. CooB plays a chaperone-like role for the proteins involved in formation of CS1 pili of enterotoxigenic Escherichia coli. Proc. Natl. Acad. Sci. USA 94:13257-13261.
54. Wall, D., and D. Kaiser. 1999. Type IV pili and cell motility. Mol. Microbiol. 32:1-10.
55. Waller, P. R., and R. T. Sauer. 1996. Characterization of degQ and degS, Escherichia coli genes encoding homologs of the DegP protease. J. Bacteriol. 178:1146-1153.
56. Wolf, M. K. 1997. Occurrence, distribution, and associations of O and H serogroups, colonization factor antigens, and toxins of enterotoxigenic Escherichia coli. Clin. Microbiol. Rev. 10:569-584.
57. Yanisch-Perron, C., J. Vieira, and J. Messing. 1985. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33:103-119.