Role of adhesin release for mucosal colonization by a bacterial pathogen

Journal of Experimental Medicine

Volumn 197, Issue 6, 2003, Pages 735-742

  Coutte, Loïc ^a   Alonso, Sylvie ^a,b   Reveneau, Nathalie ^a   Willery, Eve ^a   Quatannens, Brigitte ^a   Locht, Camille ^a   Jacob Dubuisson, Françoise ^a  

^a INSTITUT PASTEUR DE LILLE   (France)

^b Animal Health Diagnostic Center   (United States)

Author keywords

Adhesin; Bordetella pertussis; Colonization; Filamentous hemagglutinin; Maturation protease

Indexed keywords

ADHESIN; HEMAGGLUTININ; PROTEINASE; PROTEINASE SPHB1; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ARTICLE; BACTERIAL COLONIZATION; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; BINDING SITE; BORDETELLA PERTUSSIS; CELL ADHESION; CELL MATURATION; DISEASE MODEL; ENZYME SPECIFICITY; EXTRACELLULAR SPACE; HOST CELL; MUCOSA; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN PURIFICATION; PROTEIN SECRETION; RESPIRATORY SYSTEM; STRAIN IDENTIFICATION; SURFACE PROPERTY; WILD TYPE;

ADHESINS, BACTERIAL; ADMINISTRATION, INTRANASAL; ANIMALS; BACTERIAL ADHESION; BACTERIAL PROTEINS; BORDETELLA INFECTIONS; BORDETELLA PERTUSSIS; CELL LINE; FEMALE; HEMAGGLUTININS; HUMANS; LUNG; MICE; MICE, INBRED BALB C; PERTUSSIS TOXIN; SERINE ENDOPEPTIDASES; TUMOR CELLS, CULTURED; VIRULENCE FACTORS, BORDETELLA;

EID: 0037451176     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.20021153     Document Type: Article

References (46)

1. Beachey, E.H. 1981. Bacterial adherence: adhesin-receptor interactions mediating the attachement of bacteria to mucosal surfaces. J. Infect. Dis. 143:325-345.
2. Isberg, R.R., and G. Tran Van Nhieu. 1994. Binding and internalization of microorganisms by integrin receptors. Trends Microbiol. 2:10-14.
3. Rostand, K.S., and J.D. Esko. 1997. Microbial adherence to and invasion through proteoglycans. Infect. Immun. 65:1-8.
4. Wadström, T., and A. Ljungh. 1999. Glycosaminoglycanbinding microbial proteins in tissue adhesion and invasion: key events in microbial pathogenicity. J. Med. Microbiol. 48:223-233.
5. Menozzi, F.D., K. Pethe, P. Bifani, F. Soncin, M.J. Brennan, and C. Locht. 2002. Enhanced bacterial virulence through exploitation of host glycosaminoglycans. Mol. Microbiol. 43:1379-1386.
6. Arico, B., S. Nuti, V. Scarlato, and R. Rappuoli. 1993. Adhesion of Bordetella pertussis to eukaryotic cells requires a time-dependent export and maturation of filamentous hemagglutinin. Proc. Natl. Acad. Sci. USA. 90:9204-9208.
7. Fink, D.L., L.D. Cope, E.J. Hansen, and J.W. St Geme. 2001. The Haemophilus influenzae Hap autotransporter is a chymotryspin clan protease and undergoes autoproteolysis via an intermolecular mechanism. J. Biol. Chem. 276:39492-39500.
8. Finn, T.M., and L.A. Stevens. 1995. Tracheal colonization factor: a Bordetella pertussis secreted virulence determinant. Mol. Microbiol. 16:625-634.
9. Stathopoulos, C., D.L. Provence, and R. Curtiss. 1999. Characterization of the avian pathogenic Escherichia coli hemagglutinin Tsh, a member of the immunoglobulin A protease-type family of autotransporters. Infect. Immun. 67:772-781.
10. Ward, C.K., S.R. Lumbley, J.L. Latimer, L.D. Cope, and E.J. Hansen. 1998. Haemophilus ducreyi secretes a filamentous hemagglutinin-like protein. J. Bacteriol. 180:6013-6022.
11. St. Geme, J.W., III, and S. Grass. 1998. Secretion of the Haemophilus influenzae HMW1 and HMW2 adhesins involves a periplasmic intermediate and requires the HMWB and HMWC proteins. Mol. Microbiol. 27:617-630.
12. Hewlett, E.L. 1997. Pertussis: current concepts of pathogenesis and prevention. Pediatr. Infect. Dis. J. 16:S78-84.
13. Locht, C. 1999. Molecular aspects of Bordetella pertussis pathogenesis. Int. Microbiol. 2:137-144.
14. Domenighini, M., D. Relman, C. Capiau, S. Falkow, A. Prugnola, V. Scarlato, and R. Rappuoli. 1990. Genetic characterization of Bordetella pertussis filamentous hemagglutinin: a protein processed from an unusually large precursor. Mol. Microbiol. 4:787-800.
15. Locht, C., P. Bertin, F.D. Menozzi, and G. Renauld. 1993. The filamentous haemagglutinin, a multifaceted adhesin produced by virulent Bordetella spp. Mol. Microbiol. 9:653-660.
16. Renauld-Mongénie, G., J. Cornette, N. Mielcarek, F.D. Menozzi, and C. Locht. 1996. Distinct roles of the N-terminal and the C-terminal precursor domains in the biogenesis of the Bordetella pertussis filamentous hemagglutinin. J. Bacteriol. 178:1053-1060.
17. Tuomanen, E., H. Towbin, G. Rosenfelder, D. Braun, G. Larson, G.C. Hansson, and R. Hill. 1988. Receptor analogs and monoclonal antibodies that inhibit adherence of Bordetella pertussis to human ciliated respiratory epithelial cells. J. Exp. Med. 168:267-277.
18. Prasad, S.M., Y. Yin, E. Rodzinski, E.I. Tuomamen, and H.R. Masure. 1993. Identification of a carbohydrate recognition domain in filamentous hemagglutinin from Bordetella pertussis. Infect. Immun. 61:2780-2785.
19. Hannah, J.H., F.D. Menozzi, G. Renauld, C. Locht, and M.J. Brennan. 1994. Sulfated glycoconjugate receptors for the Bordetella pertussis adhesin filamentous hemagglutinin (FHA) and mapping of the heparin-binding domain on FHA. Infect. Immun. 62:5010-5019.
20. 2, CD11b/CD18) binds filamentous hemagglutinin of Bordetella pertussis. Cell. 61:1375-1382.
21. Ishibashi, Y., S. Claus, and D.A. Relman. 1994. Bordetella pertussis filamentous hemagglutinin interacts with a leukocyte signal transduction complex and stimulates bacterial adherence to monocyte CR3 (CD11b/CD18). J. Exp. Med. 180:1225-1233.
22. Menozzi, F.D., P.E. Boucher, G. Riveau, C. Gantiez, and C. Locht. 1994. Surface-associated filamentous hemagglutinin induces autoagglutination of Bordetella pertussis. Infect. Immun. 62:4261-4269.
23. Coutte, L., R. Antoine, H. Drobecq, C. Locht, and F. JacobDubuisson. 2001. Subtilisin-like autotransporter serves as maturation protease in a bacterial secretion pathway. EMBO J. 20:5040-5048.
24. Siezen, R.J., and J.A.M. Leunissen. 1997. Subtilases: the superfamily of subtilisin-like serine proteases. Protein Sci. 6:501-523.
25. Antoine, R., S. Alonzo, D. Raze, L. Coutte, S, Lesjean, E. Willery, C. Locht, and F. Jacob-Dubuisson. 2000. New virulence-activated and virulence-repressed genes identified by systematic gene inactivation and generation of transcriptional fusions in Bordetella pertussis. J. Bacteriol. 182:5902-5905.
26. Locht, C., R. Antoine, and F. Jacob-Dubuisson. 2001. Bordetella pertussis, molecular pathogenesis under multiple aspects. Curr. Opin. Microbiol. 4:82-89.
27. Alonso, S., K. Pethe, N. Mielcarek, D. Raze, and C. Locht. 2001. Role of ADP-ribosyltransferase activity of pertussis toxin in toxin-adhesin redundancy with filamentous hemagglutinin during Bordetella pertussis infection. Infect. Immun. 69:6038-6043.
28. Menozzi, F.D., R. Mutombo, G. Renauld, C. Gantiez, J.H. Hannah, E. Leininger, M.J. Brennan, and C. Locht. 1994. Heparin-inhibitable lectin activity of the filamentous hemagglutinin adhesin of Bordetella pertussis. Infect. Immun. 62:769-778.
29. Antoine, R., and C. Locht. 1990. Roles of the disulfide bond and the carboxy-terminal region of the S1 subunit in the assembly and biosynthesis of pertussis toxin. Infect. Immun. 58:1518-1526.
30. Stibitz, S. 1994. Use of conditionally counterselectable suicide vectors for allelic exchange. Methods Enzymol. 235:458-465.
31. Quandt, J., and M.F. Hynes. 1993. Versatile suicide vectors which allow direct selection for gene replacement in Gramnegative bacteria. Gene. 127:15-21.
32. Locht, C., M.-C. Geoffroy, and G. Renauld. 1992. Common accessory genes for the Bordetella pertussis filamentous hemagglutinin and fimbriae share sequence similarities with the papC and papD gene families. EMBO J. 11:3175-3183.
33. Menozzi, F.D., C. Gantiez, and C. Locht. 1991. Interaction of the Bordetella pertussis filamentous hemagglutinin with heparin. FEMS Microbiol. Lett. 78:59-64.
34. Leininger, E., S. Bowen, G. Renauld-Mongenie, J.H. Rouse, F.D. Menozzi, C. Locht, I. Heron, and M.J. Brennan. 1997. Immunodominant domains present on the Bordetella pertussis vaccine component filamentous hemagglutinin. J. Infect. Dis. 175:1423-1431.
35. Dei-Cas, E., M. Brun-Pascaud, V. Bille-Hansen, A. Allaert, and E.M. Aliouat. 1998. Animal models of pneumocystis. FEMS Immunol. Med. Microbiol. 22:163-168.
36. Travis, J., J. Potempa, and H. Maeda. 1995. Are bacterial proteinases pathogenic factors? Trends Microbiol. 3:405-407.
37. Khelef, N., C.-M. Bachelet, B.B. Vargaftig, and N. Guiso. 1994. Characterization of murine lung inflammation after infection with parental Bordetella pertussis and mutant deficient in adhesins or toxins. Infect. Immun. 62:2893-2900.
38. Mooi, F.R., W.H. Jansen, H. Brunings, H. Gielen, J.G.J. van der Heide, H.C. Walvoort, and P.A.M. Guinee. 1992. Construction and analysis of Bordetella pertussis mutants defective in the production of fimbriae. Microb. Pathog. 12:127-135.
39. Cotter, P.A., and V.J. DiRita. 2000. Bacterial virulence gene regulation: an evolutionary perspective. Annu. Rev. Microbiol. 54:519-565.
40. Rappuoli, R. 1994. Pathogenicity mechanisms of Bordetella. Curr. Top. Microbiol. Immunol. 192:319-336.
41. Kinnear, S.M., R.R. Marques, and N.H. Carbonetti. 2001. Differential regulation of Bvg-activated virulence factors plays a role in Bordetella pertussis pathogenicity. Infect. Immun. 69:1983-1993.
42. Bieber, D., S. Ramer, C.-Y. Wu, W.J. Murray, T. Tobe, R. Fernandez, and G.K. Schoolnik. 1998. Type IV pili, transient bacterial aggregates, and virulence of enteropathogenic Escherichia coli. Science. 280:2114-2118.
43. Pujol, C., E. Eugene, M. Marceau, and X. Nassif. 1999. The meningococcal PilT protein is required for induction of intimate attachement to epithelial cells following pilus-mediated adhesion. Proc. Natl. Acad. Sci. USA. 96:4017-4022.
44. Hoepelman, A.I.M., and E.I. Tuomanen. 1992. Consequences of microbial attachment: directing host cell functions with adhesins. Infect. Immun. 60:1729-1733.
45. Abramson, T., H. Kedem, and D.A. Relman. 2001. Proinflammatory and proapoptotic activites associated with Bordetella pertussis filamentous hemagglutinin. Infect. Immun. 69:2650-2658.
46. Mc Guirk, P., and K.H.G. Mills. 2000. Direct anti-inflammatory virulence factor: IL-10-dependent suppresion of IL-12 production by filamentous hemagglutinin from Bordetella pertussis. Eur. J. Immunol. 30:415-422.