Proteolytic processing is not essential for multiple functions of the Escherichia coli autotransporter adhesin involved in diffuse adherence (AIDA-I)

Journal of Bacteriology

Volumn 188, Issue 24, 2006, Pages 8504-8512

  Charbonneau, Marie Ève ^a   Berthiaume, Frédéric ^a   Mourez, Michael ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; AMPICILLIN; BACTERIAL PROTEIN; OUTER MEMBRANE PROTEIN;

ARTICLE; BACTERIAL GROWTH; BACTERIAL INFECTION; BACTERIUM ADHERENCE; BIOFILM; CIRCULAR DICHROISM; EPITHELIUM CELL; ESCHERICHIA COLI; HUMAN; HUMAN CELL; IMMUNOBLOTTING; NONHUMAN; PLASMID; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; ULTRAVIOLET SPECTROSCOPY;

ADHESINS, ESCHERICHIA COLI; BACTERIAL ADHESION; BIOFILMS; CELL LINE; CELL MEMBRANE; ESCHERICHIA COLI; HUMANS; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN PROCESSING, POST-TRANSLATIONAL;

ESCHERICHIA COLI;

EID: 33845452751     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00864-06     Document Type: Article

References (53)

1. Benz, I., and M. A. Schmidt. 1992. AIDA-I, the adhesin involved in diffuse adherence of the diarrhoeagenic Escherichia coli strain 2787 (O126:H27), is synthesized via a precursor molecule. Mol. Microbiol. 6:1539-1546.
2. Benz, I., and M. A. Schmidt. 1989. Cloning and expression of an adhesin (AIDA-I) involved in diffuse adherence of enteropathogenic Escherichia coli. Infect. Immun. 57:1506-1511.
3. Benz, I., and M. A. Schmidt. 2001. Glycosylation with heptose residues mediated by the aah gene product is essential for adherence of the AIDA-I adhesin. Mol. Microbiol. 40:1403-1413.
4. Benz, I., and M. A. Schmidt. 1992. Isolation and serologic characterization of AIDA-I, the adhesin mediating the diffuse adherence phenotype of the diarrhea-associated Escherichia coli strain 2787 (O126:H27). Infect. Immun. 60:13-18.
5. Bilge, S. S., C. R. Clausen, W. Lau, and S. L. Moseley. 1989. Molecular characterization of a fimbrial adhesin, F1845, mediating diffuse adherence of diarrhea-associated Escherichia coli to HEp-2 cells. J. Bacteriol. 171:4281-4289.
6. Brandon, L. D., N. Goehring, A. Janakiraman, A. W. Van, T. Wu, J. Beckwith, and M. B. Goldberg. 2003. IcsA, a polarly localized autotransporter with an atypical signal peptide, uses the Sec apparatus for secretion, although the Sec apparatus is circumferentially distributed. Mol. Microbiol. 50:45-60.
7. Caffrey, P., and P. Owen. 1989. Purification and N-terminal sequence of the alpha subunit of antigen 43, a unique piotein complex associated with the outer membrane of Escherichia coli. J. Bacteriol. 171:3634-3640.
8. d'Hauteville, H., R. D. Lagelouse, F. Nato, and P. J. Sansonetti. 1996. Lack of cleavage of IcsA in Shigella flexneri causes aberrant movement and allows demonstration of a cross-reactive eukaryotic protein. Infect. Immun. 64:511-517.
9. Dutta, P. R., R. Cappello, F. Navarro-Garcia, and J. P. Nataro. 2002. Functional comparison of serine protease autotransporters of Enterobacteriaceae. Infect. Immun. 70:7105-7113.
10. Egile, C., H. d'Hauteville, C. Parsot, and P. J. Sansonetti. 1997. SopA, the outer membrane protease responsible for polar localization of IcsA in Shigella flexneri. Mol. Microbiol. 23:1063-1073.
11. Elsinghorst, E. A., and D. J. Kopecko. 1992. Molecular cloning of epithelial cell invasion determinants from enterotoxigenic Escherichia coli. Infect. Immun. 60:2409-2417.
12. Elsinghorst, E. A., and J. A. Weitz. 1994. Epithelial cell invasion and adherence directed by the enterotoxigenic Escherichia coli tib locus is associated with a 104-kilodalton outer membrane protein. Infect. Immun. 62:3463-3471.
13. Emsley, P., I. G. Charles, N. F. Fairweather, and N. W. Isaacs. 1996. Structure of Bordetella pertussis virulence factor P.69 pertactin. Nature 381:90-92.
14. Fink, D. L., L. D. Cope, E. J. Hansen, and J. W. Gerne III. 2001. The Hemophilus influenzae Hap autotransporter is a chymotrypsin clan serine protease and undergoes autoproteolysis via an intermolecular mechanism. J. Biol. Chem. 276:39492-39500.
15. Fink, D. L., and J. W. St. Geme III. 2003. Chromosomal expression of the Haemophilus influenzae Hap autotransporter allows fine-tuned regulation of adhesive potential via inhibition of intermolecular autoproteolysis. J. Bacteriol. 185:1608-1615.
16. Fukuda, I., T. Suzuki, H. Munakata, N. Hayashi, E. Katayama, M. Yoshikawa, and C. Sasakawa. 1995. Cleavage of Shigella surface protein VirG occurs at a specific site, but the secretion is not essential for intracellular spreading. J. Bacteriol. 177:1719-1726.
17. Girard, V., and M. Mourez. 2006. Adhesion mediated by autotransporters of Gram-negative bacteria: structural and functional features. Res. Microbiol. 157:407-416.
18. Heller, K. B. 1978. Apparent molecular weights of a heat-modifiable protein from the outer membrane of Escherichia coli in gels with different acrylamide concentrations. J. Bacteriol. 134:1181-1183.
19. Henderson, I. R., J. Czeczulin, C. Eslava, F. Noriega, and J. P. Nataro. 1999. Characterization of Pic, a secreted protease of Shigella flexneri and entero-aggregative Escherichia coli. Infect. Immun. 67:5587-5596.
20. Henderson, I. R., and J. P. Nataro. 2001. Virulence functions of autotransporter proteins. Infect. Immun. 69:1231-1243.
21. Henderson, I. R., F. Navarro-Garcia, M. Desvaux, R. C. Fernandez, and D. Ala'Aldeen. 2004. Type V protein secretion pathway: the autotransporter story. Microbiol. Mol. Biol. Rev. 68:692-744.
22. Henderson, I. R., and P. Owen. 1999. The major phase-variable outer membrane protein of Escherichia coli structurally resembles the immunoglobulin Al protease class of exported protein and is regulated by a novel mechanism involving Dam and OxyR. J. Bacteriol. 181:2132-2141.
23. Hendrixson, D. R., M. L. de la Morena, C. Stathopoulos, and J. W. St. Geme III. 1997. Structural determinants of processing and secretion of the Haemophilus influenzae hap protein. Mol. Microbiol. 26:505-518.
24. Hendrixson, D. R., and J. W. St. Geme III. 1998. The Haemophilus influenzae Hap serine protease promotes adherence and microcolony formation, potentiated by a soluble host protein. Mol. Cell 2:841-850.
25. Jouve, M., M.-I. Garcia, P. Courcoux, A. Labigne, P. Gounon, and C. Le Bouguenec. 1997. Adhesion to and invasion of HeLa cells by pathogenic Escherichia coli carrying the afa-3 gene cluster are mediated by the AfaE and AfaD proteins, respectively. Infect. Immun. 65:4082-4089.
26. Junker, M., C. C. Schuster, A. V. McDonnell, K. A. Sorg, M. C. Finn, B. Berger, and P. L. Clark. 2006. Pertactin beta-helix folding mechanism suggests common themes for the secretion and folding of autotransporter proteins. Proc. Natl. Acad. Sci. USA 103:4918-4923.
27. Kelly, S. M., T. J. Jess, and N. C. Price. 2005. How to study proteins by circular dichroism. Biochim. Biophys. Acta 1751:119-139.
28. Klemm, P., R. M. Vejborg, and O. Sherlock. 2006. Self-associating autotransporters, SAATs: functional and structural similarities. Int. J. Med. Microbiol. 296:187-195.
29. Laarmann, S., and M. A. Schmidt. 2003. The Escherichia coli AIDA auto-transporter adhesin recognizes an integral membrane glycoprotein as receptor. Microbiology 149:1871-1882.
30. Lindenthal, C., and E. A. Elsinghorst. 1999. Identification of a glycoprotein produced by enterotoxigenic Escherichia coli. Infect. Immun. 67:4084-4091.
31. Macao, B., D. G. Johansson, G. C. Hansson, and T. Hard. 2006. Autoproteolysis coupled to protein folding in the SEA domain of the membrane-bound MUC1 mucin. Nat. Struct. Mol. Biol. 13:71-76.
32. Malnil, J. G., E. Jacquemin, P. Pohl, A. Kaeckenbeeck, and I. Benz. 2002. DNA sequences coding for the F18 fimbriae and AIDA adhesin are localised on the same plasmid in Escherichia coli isolates from piglets. Vet. Microbiol. 86:303-311.
33. Mogensen, J. E., J. H. Kleinschmidt, M. A. Schmidt, and D. E. Otzen. 2005. Misfolding of a bacterial autotransporter. Protein Sci. 14:2814-2827.
34. Mogensen, J. E., D. Tapadar, M. A. Schmidt, and D. E. Otzen. 2005. Barriers to folding of the transmembrane domain of the Escherichia coli autotransporter adhesin involved in diffuse adherence. Biochemistry 44:4533-4545.
35. Moormann, C., I. Benz, and M. A. Schmidt. 2002. Functional substitution of the TibC protein of enterotoxigenic Escherichia coli strains for the autotransporter adhesin heptosyltransferase of the AIDA system. Infect. Immun. 70:2264-2270.
36. Muller, D., I. Benz, D. Tapadar, C. Buddenborg, L. Greune, and M. A. Schmidt. 2005. Arrangement of the translocator of the autotransporter adhesin involved in diffuse adherence on the bacterial surface. Infect. Immun. 73:3851-3859.
37. Navarro-Garcia, F., A. Canizalez-Roman, J. Luna, C. Sears, and J. P. Nataro, 2001. Plasmid-encoded toxin of enteroaggregative Escherichia coli is internalized by epithelial cells. Infect. Immun. 69:1053-1060.
38. Ngeleka, M. 2002. Isolation of a new Escherichia coli pathotype associated with diarrhea in piglets. Can. Vet. J. 43:623-624.
39. Niewerth, U., A. Frey, T. Voss, C. Le Bouguénec, G. Baljer, S. Franke, and M. A. Schmidt. 2001. The AIDA autotransporter system is associated with F18 and Stx2e in Escherichia coli isolates from pigs diagnosed with edema disease and postweaning diarrhea. Clin. Diagn. Lab. Immunol. 8:143-149.
40. Oomen, C. J., P. Van Ulsen, P. Van Gelder, M. Feijen, J. Tommassen, and P. Gros. 2004. Structure of the translocator domain of a bacterial autotransporter. EMBO J. 23:1257-1266.
41. O'Toole, G. A., L. A. Pratt, P. I. Watnick, D. K. Newman, V. B. Weaver, and R. Kolter. 1999. Genetic approaches to study of biofilms. Methods Enzymol. 310:91-109.
42. Otto, B. R., R. Sijbrandi, J. Luirink, B. Oudega, J. G. Heddle, K. Mizutani, S. Y. Park, and J. R. Tame. 2005. Crystal structure of hemoglobin protease, a heme binding autotransporter protein from pathogenic Escherichia coli. J. Biol. Chem. 280:17339-17345.
43. Owen, P., P. Caffrey, and L. G. Josefsson. 1987. Identification and partial characterization of a novel bipartite protein antigen associated with the outer membrane of Escherichia coli. J. Bacteriol. 169:3770-3777.
44. Owen, P., M. Meehan, H. de Loughry-Doherty, and I. Henderson. 1996. Phase-variable outer membrane proteins in Escherichia coli. FEMS Immunol. Med. Microbiol. 16:63-76.
45. Pace, C. N., F. Vajdos, L. Fee, G. Grimsley, and T. Gray. 1995. How to measure and predict the molar absorption coefficient of a protein. Protein Sci. 4:2411-2423.
46. Peterson, J. H., R. L. Szabady, and H. D. Bernstein. 2006. An unusual signal peptide extension inhibits the binding of bacterial presecretory proteins to the signal recognition particle, trigger factor, and the SecYEG complex. J. Biol. Chem. 281:9038-9048.
47. Pizarro-Cerda, J., and P. Cossart. 2006. Bacterial adhesion and entry into host cells. Cell 124:715-727.
48. Rutherford, N., M. E. Charbonneau, F. Berthiaume, J. M. Betton, and M. Mourez. 2006. The periplasmic folding of a cysteineless autotransporter passenger domain interferes with its outer membrane translocation. J. Bacteriol. 188:4111-4116.
49. Sherlock, O., U. Dobrindt, J. B. Jensen, R. M. Vejborg, and P. Klemm. 2006. Glycosylation of the self-recognizing Escherichia coli Ag43 autotransporter protein. J. Bacteriol. 188:1798-1807.
50. Sherlock, O., M. A. Schembri, A. Reisner, and P. Klemm. 2004. Novel roles for the AIDA adhesin from diarrheagenic Escherichia coli: cell aggregation and biofilm formation. J. Bacteriol. 186:8058-8065.
51. Sherlock, O., R. M. Vejborg, and P. Klemm. 2005. The TibA adhesin/invasin from enterotoxigenic Escherichia coli is self recognizing and induces bacterial aggregation and biofilm formation. Infect. Immun. 73:1954-1963.
52. St. Geme, J. W., III, M. L. de la Morena, and S. Falkow. 1994. A Haemophilus influenzae IgA protease-like protein promotes intimate interaction with human epithelial cells. Mol. Microbiol. 14:217-233.
53. Suhr, M., I. Benz, and M. A. Schmidt. 1996. Processing of the AIDA-I precursor: removal of AIDAc and evidence for the outer membrane anchoring as a beta-barrel structure. Mol. Microbiol. 22:31-42.