The Escherichia coli efflux pump TolC promotes aggregation of enteroaggregative E. coli 042

Infection and Immunity

Volumn 76, Issue 3, 2008, Pages 1247-1256

  Imuta, Naoko ^a   Nishi, Junichiro ^a   Tokuda, Koichi ^a   Fujiyama, Rika ^a   Manago, Kunihiro ^a   Iwashita, Mayumi ^a   Sarantuya, Jav ^a,b   Kawano, Yoshifumi ^a  

^a KAGOSHIMA UNIVERSITY   (Japan)

^b MONGOLIAN NATIONAL UNIVERSITY OF MEDICAL SCIENCES   (Mongolia)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CARRIER PROTEIN; DISPERSIN; PROTEIN AATA; TOLC PROTEIN; UNCLASSIFIED DRUG; AAP PROTEIN, E COLI; ESCHERICHIA COLI PROTEIN; MUTANT PROTEIN; OUTER MEMBRANE PROTEIN; TOLC PROTEIN, E COLI;

ARTICLE; BACTERIAL OUTER MEMBRANE; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; BIOFILM; CELL CULTURE; COCULTURE; CULTURE MEDIUM; ENTEROAGGREGATIVE ESCHERICHIA COLI; ENTEROAGGREGATIVE ESCHERICHIA COLI 042; ESCHERICHIA COLI; HEP 2 CELL; MICROTITER PLATE ASSAY; NONHUMAN; NUCLEOTIDE SEQUENCE; PLANKTON; PLASMID; PRIORITY JOURNAL; PROTEIN SECRETION; PROTEIN TRANSPORT; BACTERIAL COUNT; CELL LINE; GENE DELETION; GENE EXPRESSION REGULATION; GENETIC COMPLEMENTATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; METABOLISM; PHYSIOLOGY;

BACTERIAL ADHESION; BACTERIAL OUTER MEMBRANE PROTEINS; BIOFILMS; CELL LINE; COLONY COUNT, MICROBIAL; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENETIC COMPLEMENTATION TEST; HUMANS; MEMBRANE TRANSPORT PROTEINS; MUTAGENESIS, INSERTIONAL; MUTANT PROTEINS; SEQUENCE DELETION;

EID: 40749115637     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.00758-07     Document Type: Article

References (45)

1. Buckley, A. M., M. A. Webber, S. Cooles, L. P. Randall, R. M. La Ragione, M. J. Woodward, and L. J. Piddock. 2006. The AcrAB-TolC efflux system of Salmonella enterica serovar Typhimurium plays a role in pathogenesis. Cell. Microbiol. 8:847-856.
2. Chart, H., J. Spencer, H. R. Smith, and B. Rowe. 1997. Magnesium ions are required for HEp-2 cell adhesion by enteroaggregative strains of Escherichia coli O126:H27 and O44:H18. FEMS Microbiol. Lett. 148:49-52.
3. Cohen, M. B., J. P. Nataro, D. I. Bernstein, J. Hawkins, N. Roberts, and M. A. Staat. 2005. Prevalence of diarrheagenic Escherichia coli in acute childhood enteritis: a prospective controlled study. J. Pediatr. 146:54-61.
4. Czeczulin, J. R., S. Balepur, S. Hicks, A. Phillips, R. Hall, M. H. Kothary, F. Navarro-Garcia, and J. P. Nataro. 1997. Aggregative adherence fimbria II, a second fimbrial antigen mediating aggregative adherence in enteroaggregative Escherichia coli. Infect. Immun. 65:4135-4145.
5. Dudley, E. G., N. R. Thomson, J. Parkhill, N. P. Morin, and J. P. Nataro. 2006. Proteomic and microarray characterization of the AggR regulon identifies a pheU pathogenicity island in enteroaggregative Escherichia coli. Mol. Microbiol. 61:1267-1282.
6. Elias, W. P., Jr., J. R. Czeczulin, I. R. Henderson, L. R. Trabulsi, and J. P. Nataro. 1999. Organization of biogenesis genes for aggregative adherence fimbria II defines a virulence gene cluster in enteroaggregative Escherichia coli. J. Bacteriol. 181:1779-1785.
7. Eslava, C., F. Navarro-Garcia, J. R. Czeczulin, I. R. Henderson, A. Cravioto, and J. P. Nataro. 1998. Pet, an autotransporter enterotoxin from enteroaggregative Escherichia coli. Infect. Immun. 66:3155-3163.
8. Hanahan, D. 1983. Studies on transformation of Escherichia coli with Plasmids. J. Mol. Biol. 166:557-580.
9. Harrington, S. M., E. G. Dudley, and J. P. Nataro. 2006. Pathogenesis of enteroaggregative Escherichia coli infection. FEMS Microbiol. Lett. 254: 12-18.
10. Hasman, H., T. Chakraborty, and P. Klemm. 1999. Antigen-43-mediated autoaggregation of Escherichia coli is blocked by fimbriation. J. Bacteriol. 181:4834-4841.
11. Henderson, I. R., S. Hicks, F. Navarro-Garcia, W. P. Elias, A. D. Philips, and J. P. Nataro. 1999. Involvement of the enteroaggregative Escherichia coli plasmid-encoded toxin in causing human intestinal damage. Infect. Immun. 67:5338-5344.
12. Huang, D. B., J. P. Nataro, H. L. DuPont, P. P. Kamat, A. D. Mhatre, P. C. Okhuysen, and T. Chiang. 2006. Enteroaggregative Escherichia coli is a cause of acute diarrheal illness: a meta-analysis. Clin. Infect. Dis. 43:556-563.
13. Iwashita, M., J. Nishi, N. Wakimoto, R. Fujiyama, K. Yamamoto, K. Tokuda, K. Manage, and Y. Kawano. 2006. Role of the carboxy-terminal region of the outer membrane protein AatA in the export of dispersin from enteroaggregative Escherichia coli. FEMS Microbiol. Lett. 256:266-272.
14. Kendall, M. M., and V. Sperandio. 2007. Quorum sensing by enteric pathogens. Curr. Opin. Gastroenterol. 23:10-15.
15. Koronakis, V. 2003. TolC - the bacterial exit duct for proteins and drugs. FEBS Lett. 555:66-71.
16. Koronakis, V., J. Eswaran, and C. Hughes. 2004. Structure and function of TolC: the bacterial exit duct for proteins and drugs. Annu. Rev. Biochem. 73:467-489.
17. Mattos-Guaraldi, A. L., L. C. Formiga, and A. F. Andrade. 1999. Cell surface hydrophobicity of sucrose fermenting and nonfermenting Corynebacterium diphtheriae strains evaluated by different methods. Curr. Microbiol. 38:37-42.
18. Mobley, H. L., K. G. Jarvis, J. P. Elwood, D. I. Whittle, C. V. Lockatell, R. G. Russell, D. E. Johnson, M. S. Donnenberg, and J. W. Warren. 1993. Isogenic P-fimbrial deletion mutants of pyelonephritogenic Escherichia coli: the role of alpha Gal(1-4) beta Gal binding in virulence of a wild-type strain. Mol. Microbiol. 10:143-155.
19. Nataro, J. P., M. M. Baldini, J. B. Kaper, R. E. Black, N. Bravo, and M. M. Levine. 1985. Detection of an adherence factor of enteropathogenic Escherichia coli with a DNA probe. J. Infect. Dis. 152:560-565.
20. Nataro, J. P., Y. Deng, S. Cookson, A. Cravioto, S. J. Savarino, L. D. Guers, M. M. Levine, and C. O. Tacket. 1995. Heterogeneity of enteroaggregative Escherichia coli virulence demonstrated in volunteers. J. Infect. Dis. 171:465-468.
21. Nataro, J. P., and A. Jansen. 2005. Aggregation and dispersal on mucosal surfaces, p. 253-263. In J. P. Nataro, P. S. Cohen, H. L. T. Mobley, and J. N. Weiser (ed.), Colonization of mucosal surfaces. ASM Press, Washington, DC.
22. Nataro, J. P., and J. B. Kaper. 1998. Diarrheagenic Escherichia coli. Clin. Microbiol. Rev. 11:142-201.
23. Nataro, J. P., J. B. Kaper, R. Robins-Browne, V. Prado, P. Vial, and M. M. Levine. 1987. Patterns of adherence of diarrheagenic Escherichia coli to HEp-2 cells. Pediatr. Infect. Dis. J. 6:829-831.
24. Nataro, J. P., V. Mai, J. Johnson, W. C. Blackwelder, R. Heimer, S. Tirrell, S. C. Edberg, C. R. Braden, J. G. Morris, Jr., and J. M. Hirshon. 2006. Diarrheagenic Escherichia coli infection in Baltimore, Maryland, and New Haven, Connecticut. Clin. Infect. Dis. 43:402-407.
25. Nishi, J., J. Sheikh, K. Mizuguchi, B. Luisi, V. Burland, A. Boutin, D. J. Rose, F. R. Blattner, and J. P. Nataro. 2003. The export of coat protein from enteroaggregative Escherichia coli by a specific ATP-binding cassette transporter system. J. Biol. Chem. 278:45680-45689.
26. Ochiai, K., T. Kurita-Ochiai, Y. Kamino, and T. Ikeda. 1993. Effect of co-aggregation on the pathogenicity of oral bacteria. J. Med. Microbiol. 39:183-190.
27. Okeke, I. N., and J. P. Nataro. 2001. Enteroaggregative Escherichia coli. Lancet Infect. Dis. 1:304-313.
28. Penfold, R. J., and J. M. Pemberton. 1992. An improved suicide vector for construction of chromosomal insertion mutations in bacteria. Gene 118:145-146.
29. Piddock, L. J. 2006. Clinically relevant chromosomally encoded multidrug resistance efflux pumps in bacteria. Clin. Microbiol. Rev. 19:382-402.
30. Piddock, L. J. 2006. Multidrug-resistance efflux pumps - not just for resistance. Nat. Rev. Microbiol. 4:629-636.
31. Sambrook, J., and D. Russell. 2001. Molecular cloning: a laboratory manual, 3rd ed., vol. 1. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
32. Sarantuya, J., J. Nishi, N. Wakimoto, S. Erdene, J. P. Nataro, J. Sheikh, M. Iwashita, K. Manago, K. Tokuda, M. Yoshinaga, K. Miyata, and Y. Kawano. 2004. Typical enteroaggregative Escherichia coli is the most prevalent pathotype among E. coli strains causing diarrhea in Mongolian children. J. Clin. Microbiol. 42:133-139.
33. Sharff, A., C. Fanutti, J. Shi, C. Calladine, and B. Luisi. 2001. The role of the TolC family in protein transport and multidrug efflux. From stereochemical certainty to mechanistic hypothesis. Eur. J. Biochem. 268:5011-5026.
34. Sheikh, J., J. R. Czeczulin, S. Harrington, S. Hicks, I. R. Henderson, C. Le Bouguenec, P. Gounon, A. Phillips, and J. P. Nataro. 2002. A novel dispersin protein in enteroaggregative Escherichia coli. J. Clin. Investig. 110:1329-1337.
35. Sheikh, J., E. G. Dudley, B. Sui, B. Tamboura, A. Suleman, and J. P. Nataro. 2006. EilA, a HilA-like regulator in enteroaggregative Escherichia coli. Mol. Microbiol. 61:338-350.
36. Sheikh, J., S. Hicks, M. Dall'Agnol, A. D. Phillips, and J. P. Nataro. 2001. Roles for Fis and YafK in biofilm formation by enteroaggregative Escherichia coli. Mol. Microbiol. 41:983-997.
37. Shi, J., T. L. Blundell, and K. Mizuguchi. 2001. FUGUE: sequence-structure homology recognition using environment-specific substitution tables and structure-dependent gap penalties. J. Mol. Biol. 310:243-257.
38. Tzipori, S., J. Montanaro, R. M. Robins-Browne, P. Vial, R. Gibson, and M. M. Levine. 1992. Studies with enteroaggregative Escherichia coli in the gnotobiotic piglet gastroenteritis model. Infect. Immun. 60:5302-5306.
39. Wai, S. N., A. Takade, and K. Amako. 1996. The hydrophobic surface protein layer of enteroaggregative Escherichia coli strains. FEMS Microbiol. Lett. 135:17-22.
40. Wakimoto, N., J. Nishi, J. Sheikh, J. P. Nataro, J. Sarantuya, M. Iwashita, K. Manage, K. Tokuda, M. Yoshinaga, and Y. Kawano. 2004. Quantitative biofilm assay using a microtiter plate to screen for enteroaggregative Escherichia coli. Am. J. Trop. Med. Hyg. 71:687-690.
41. Walters, M., and V. Sperandio. 2006. Quorum sensing in Escherichia coli and Salmonella. Int. J. Med. Microbiol. 296:125-131.
42. Yamanaka, H., N. Morisada, M. Miyano, H. Tsuge, S. Shinoda, E. Takahashi, and K. Okamoto. 2004. Amino-acid residues involved in the expression of the activity of Escherichia coli TolC. Microbiol. Immunol. 48:713-722.
43. Yamanaka, H., T. Nomura, Y. Fujii, and K. Okamoto. 1998. Need for TolC, an Escherichia coli outer membrane protein, in the secretion of heat-stable enterotoxin I across the outer membrane. Microb. Pathog. 25:111-120.
44. Yamanaka, H., T. Nomura, N. Morisada, S. Shinoda, and K. Okamoto. 2002. Site-directed mutagenesis studies of the amino acid residue at position 412 of Escherichia coli TolC which is required for the activity. Microb. Pathog. 33:81-89.
45. Yang, S., C. R. Lopez, and E. L. Zechiedrich. 2006. Quorum sensing and multidrug transporters in Escherichia coli. Proc. Natl. Acad. Sci. USA 103: 2386-2391.