1887

Chapter 10 : Genes for the Filamentous Hemagglutinin and Fimbriae of : Colocation, Coregulation, and Cooperation?

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Zoom in
Zoomout

Genes for the Filamentous Hemagglutinin and Fimbriae of : Colocation, Coregulation, and Cooperation?, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555818340/9781555810825_Chap10-1.gif /docserver/preview/fulltext/10.1128/9781555818340/9781555810825_Chap10-2.gif

Abstract:

There is now evidence to show that filamentous hemagglutinin (FHA) and fimbriae act synergistically, a phenomenon which is reflected in the organization and regulation of their genes. fimbriae have larger diameters (5 nm) and are much longer (up to several hundred nanometers long) than FHA. Three major fimbrial subunit genes, fim2, fim3, and fimX, have been identified in and are scattered around the chromosome. The fim2 and fim3 genes code for the serotype 2 and 3 fimbriae, respectively, while fimX is probably not expressed in most strains because of a deletion in its promoter region. Information about the function of FHA and fimbriae has also been obtained by studying mutants in animal models. Interestingly, the mutant strain was not affected in its ability to colonize the nasopharynx or lungs. The fact that both fimbrial and FHA mutants are affected in their ability to persist in the trachea suggests that fimbriae and FHA may cooperate not only in adherence to and invasion of macrophages but also in colonization of the trachea. There is evidence that other virulence factors also cooperate with FHA. Like fimbriae, pertussis toxin may facilitate the uptake of into macrophages by upregulating the CR3 receptor. Also, it has been proposed that pertactin and FHA interact with each other and that binding to some eukaryotic receptors requires this interaction.

Citation: Mooi F. 1994. Genes for the Filamentous Hemagglutinin and Fimbriae of : Colocation, Coregulation, and Cooperation?, p 145-155. In Miller V, Kaper J, Portnoy D, Isberg R (ed), Molecular Genetics of Bacterial Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/9781555818340.ch10

Key Concept Ranking

Adenylate Cyclase Toxin
0.49252772
0.49252772
Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Figures

Image of Figure 1
Figure 1

Organization and function of , , and genes. Genes are represented by boxes, and arrowed lines indicate transcriptional units. The and genes code for a two-component sensory transduction system which translates environmental signals into transcriptional control of the and genes. BvgA is a positive regulator which binds to the promoter regions of the and genes. The gene codes for a large precursor molecule, which is transported across the inner (IM) and outer membrane (OM), after which it remains attached to the cell surface by means of its C-terminal region. This region is cleaved, and the resulting molecule (FHA) may be released from the cell or remain loosely associated with it. The gene codes for a protein which is required to transport FhaB across the outer membrane. The gene probably represents the ancestral major fimbrial subunit gene. It contains a large deletion and is therefore inactive. The gene codes for a periplasmic chaperon, which associates with fimbrial subunits to prevent nonproductive polymerization. The gene codes for the anchorage protein, which is involved in the transport, assembly, and anchorage of fimbrial subunits. The gene codes for the minor fimbrial subunit, which has been tentatively placed at the tip of the fimbrial structure. The , , and genes code for the major fimbrial subunits and probably arose by duplication of . The gene is not expressed because of an inactive promoter.

Citation: Mooi F. 1994. Genes for the Filamentous Hemagglutinin and Fimbriae of : Colocation, Coregulation, and Cooperation?, p 145-155. In Miller V, Kaper J, Portnoy D, Isberg R (ed), Molecular Genetics of Bacterial Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/9781555818340.ch10
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 2
Figure 2

Nucleotide sequence similarities in the promoter region of -activated genes. The sequence shown to bind to BvgA is overlined. Dots indicate sequence identities with the promoter region. Dashes refer to gaps introduced to increase the number of matches. The numbers refer to the distance to the initiation codons. The sequences of the following genes were obtained from previous reports: ( ), fim3 ( ), ( ), and ( ).

Citation: Mooi F. 1994. Genes for the Filamentous Hemagglutinin and Fimbriae of : Colocation, Coregulation, and Cooperation?, p 145-155. In Miller V, Kaper J, Portnoy D, Isberg R (ed), Molecular Genetics of Bacterial Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/9781555818340.ch10
Permissions and Reprints Request Permissions
Download as Powerpoint

References

/content/book/10.1128/9781555818340.chap10
1. Arai, H.,, and Y. Sato. 1976. Separation and characterization of two distinct hemagglutinins contained in purified leukocytosis-promoting factor from Bordelella pertussis. Biochem. Biophys. Acta 444: 765 782.
2. Arico, B.,, S. Nuti,, V. Scarlato,, and R. Rappuoli. 1993. Adhesion of Bordelella pertussis to eukaryotic cells required a time-dependent export and maturation of filamentous hemagglutinin. Proc. Natl. Acad. Sci. USA 90: 9204 9208.
3. Bertin, P.,, P. Boucher,, M. C. Geoffroy,, R. J. L. Willems,, C. Geuijen,, F. R. Mooi,, and C. Locht. 1993. Regulation of the genes involved in the biogenesis of FHA and fimbriae. Biologicals 21: 31 32.
4. Brennan, M. J.,, J. H. Hannah,, and E. Leininger. 1991. Adhesion of Bordetella pertussis to sulfatides and to the GalNAc beta4Gal sequence found in glycosphingolipids. J. Biol. Chem. 266: 18827 18831.
5. Delisse-Gathoye, A.,, C. Locht,, F. Jacob,, M. Raaschou-Nielsen,, I. Heron,, J. Ruelle,, M. DeWolde,, and T. Cabezon. 1990. Cloning partial sequence, expression, and antigenic analysis of the filamentous hemagglutinin gene of Bordetella pertussis. Infect. Immun. 58: 2895 2905.
6. Domenighini, M.,, D. Relman,, C. Capiau,, S. Falkow,, A. Prugnoloa,, V. Scarlato,, and R. Rappuoli. 1990. Genetic characterization of Bordetella pertussis filamentous haemagglutinin: a protein processed from an unusually large precursor. Mol. Microbiol. 4: 787 800.
7. Hazenbos, W. L. W.,, C. Geuijen,, B. M. vandenBerg,, F. R. Mooi,, and R. van Furth. Submitted for publication.
8. Hazenbos, W. L. W.,, B. M. van den Berg,, and R. van Furth. 1993. Very late antigen-5 and complement receptor type 3 cooperatively mediate the interaction between Bordetella pertussis and human monocytes. J. Immunol. 151: 6274 6282.
9. Hultgren, S. J.,, S. Abraham,, M. Caparon,, P. Falk,, J. W. St. Geme III, and S. Normark. 1993. Pilus and nonpilus bacterial adhesins: assembly and function in cell recognition. Cell 73: 887 901.
10. Irons, L. I.,, L. A. E. Ash worth,, and A. Robinson. 1985. Release and purification of fimbriae from Bordetella pertussis. Proc. 4th Int. Symp. Pertussis, Geneva, 1984. Dev. Biol. Stand. 61: 153 163.
11. Kimura, A.,, K. T. Mountzouros,, D. D. Relman,, S. Falkow,, and J. L. Cowell. 1990. Bordetella pertussis filamentous hemagglutinin: evaluation as a protective antigen and colonization factor in a mouse respiratory infection model. Infect. Immun. 58: 7 16.
12. Livey, I.,, C. J. Duggleby,, and A. Robinson. 1987. Cloning and nucleotide sequence of the serotype 2 fimbrial subunit gene of Bordetella pertussis. Mol. Microbiol. 1: 203 209.
13. Locht, C.,, P. Bertin,, F. D. Menozzi,, and G. Renauld. 1993. The filamentous hemagglutinin, a multifaceted adhesin produced by virulent Bordetella spp. Mol. Microbiol. 9: 653 660.
14. 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. EMBOJ. 11: 3175 3183.
15. Mawhinney, T. P.,, E. Adelstein,, D. A. Morris,, A. M. Mawhinney,, and G. J. Barbero. 1987. Structure determination of five sulfated oligosaccharides derived from tracheobronchial mucus glycoproteins. J. Biol. Chem. 262: 2994 3001.
16. Menozzi, F. D.,, C. Gantiez,, and C. Locht. 1991. Interaction of the Bordetella pertussis filamentous hemagglutinin with heparin. FEMS Microbiol. Lett. 78: 59 64.
17. 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.
18. Miller, J. F.,, C. R. Roy,, and S. Falkow. 1989. Analysis of Bordetella pertussis virulence gene regulation by the use of transcriptional fusions in Escherichia coli. J. Bacteriol. 171: 6345 6348.
19. Mooi, F. R., Bordetella pertussis fimbriae. In P. Klemm (ed.), Fimbriae, Aspects of Adhesion, Genetics, Biogenesis and Vaccines, in press. CRC Press, Inc., Boca Raton, Fla..
20. Mooi, F. R.,, W. H. Jansen,, H. Brunings,, H. Gielen,, H. 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.
21. Mooi, F. R.,, A. terAvest,, and H. G. J. van der Heide. 1990. Structure of the Bordetella pertussis gene coding for the serotype 3 fimbrial subunit. FEMS Microbiol. Lett. 66: 327 332.
22. Mooi, F. R.,, and H. G. J. vanderHeide. Unpublished data.
23. Murphy, P. M. 1993. Molecular mimicry and the generation of host defense protein diversity. Cell 72: 823 826.
24. Pedroni, P.,, B. Riboli,, F. de Ferra,, G. Grandi,, S. Toma,, B. Arico,, and R. Rappuoli. 1988. Cloning of a novel pilin-like gene from Bordetella pertussis: homology to the/im2 gene. Mol. Microbiol. 2: 539 543.
25. Pool, K.,, E. Schiebel,, and V. Braun. 1988. Molecular characterization of the hemolysin determinant of Serratia marcescens. J. Bacteriol. 170: 3177 3188.
26. Prasad, S. M.,, Y. Yin,, E. Rodzinski,, E. T. Tuomanen,, and R. Masure. 1993. Identification of a carbohydrate recognition domain in filamentous hemagglutinin from Bordetella pertussis. I nfect. Immun. 61: 2780 2785.
27. Relman, D.,, E. Tuomanen,, S. Falkow,, D. T. Golenbock,, K. Saukkonen,, and S. D. Wright. 1990. Recognition of a bacterial adhesin by an integrin: macrophage CR (ct MB2, CDllb/CD18) binds filamentous hemagglutinin of B. pertussis. Cell 61: 1375 1382.
28. Relman, D. A.,, M. Dominighini,, E. Tuomanen,, R. Rappuoli,, and S. Falkow. 1989. Filamentous hemagglutinin of Bordetella pertussis: nucleotide sequence and crucial role in adherence. Proc. Natl. Acad. Sci. USA 86: 2637 2641.
29. Robertson, B. D.,, and T. F. Meyer. 1992. Genetic variation in pathogenic bacteria. Trends Genet. 8: 422 427.
30. Roy, C. R.,, and S. Falkow. 1991. Identification of Bordetella pertussis regulatory sequences required for transcriptional activation of the fhaB gene and autoregulation of the bvgAS operon. J. Bacteriol. 173: 2385 2392.
31. Sandros, J.,, and E. Tuomanen. 1993. Attachment factors of Bordetella pertussis: mimicry of eukaryotic cell recognition molecules. Trends Microbiol. 1: 192 196.
32. Saukkonen, K.,, W. N. Burnette,, V. L. Mar,, H. R. Masure,, and E. I. Tuomanen. 1992. Pertussis toxin has eukaryotic-like carbohydrate recognition domains. Proc. Natl. Acad. Sci. USA 89: 118 122.
33. Saukkonen, K.,, C. Cabellos,, M. Burroughs,, S. Prasad,, and E. Tuomanen. 1991. Integrin-mediated localization of Bordetella pertussis within macrophages—role in pulmonary colonization. J. Exp. Med. 173: 1143 1149.
34. Scarlato, V.,, B. Arico,, A. Prugnola,, and R. Rappuoli. 1991. Sequential activation and environmental regulation of virulence genes in Bordetella pertussis. EMBOJ. 10: 3971 3975.
35. St. Geme, J. W.,, S. Falkow,, and S. J. Barenkamp. 1993. High molecular weight proteins of non-typable Haemophilus influenzae mediate attachment to human epithelial cells. Proc. Natl. Acad. Sci. USA 90: 2875 2879.
36. Stibitz, S.,, and T. T. Garletts. 1992. Derivation of a physical map of the chromosome of Bordetella pertussis Tohama I. J. Bacteriol. 174: 7770 7777.
37. Streisinger, G.,, and J. E. Owen. 1984. Mechanisms of spontaneous and induced frameshift mutations in bacteriophage T4. Genetics 109: 633 659.
38. Top, J.,, P. Bertin,, P. Boucher,, F. R. Mooi,, and C. Locht. Unpublished data.
39. Tuomanen, E. I.,, S. M. Prasad,, J. S. George,, A. I. M. Hoepelman,, P. Ibsen,, I. Heron,, and R. M. Starzyk. 1993. Reversible opening of the blood-brain barrier by anti-bacterial antibodies. Proc. Natl. Acad. Sci. USA 90: 7824 7828.
40. Uphoff, T. S.,, and R. A. Welch. 1990. Nucleotide sequencing of Proteus mirabilis calcium-independent hemolysin genes (hpmA and hpmB) reveals sequence similarity with the Serratia marcescens hemolysin genes (shlA and shlB) . J. Bacteriol. 172: 1206 1216.
41. Van Strijp, J. A. G.,, D. G. Rusell,, E. Tuomanen,, E. J. Brown,, and S. D. Wright. 1993. Ligand specificity of purified complement receptor three (CD11b/CD18, α mβ2, Mac-1): indirect effects of an arg-gly-asp (RGD) sequence. J. Immunol. 151: 3324 3336.
42. Van't Wout, J.,, W. N. Burnette,, V. L., Mar,, E. Rozdzinski,, S. D. Wright,, and E. I. Tuomanen. 1992. Role of carbohydrate recognition domains of pertussis toxin in adherence of Bordetella pertussis to human macrophages. Infect. Immun. 60: 3303 3308.
43. Westerlund, B.,, and T. K. Korhonen. 1993. Bacterial proteins binding to the mammalian extracellular matrix. Mol. Microbiol. 9: 687 694.
44. Willems, R. J. L. 1993. Genetic and molecular studies on Bordetella pertussis fimbriae. Thesis. Rijks Universiteit, Utrecht, The Netherlands.
45. Willems, R. J. L.,, C. Geuijen,, H. G. J. van der Heide,, M. Matheson,, A. Robinson,, L. Versluis,, R. Ebberink,, J. Theelen,, and F. R. Mooi. 1993. Isolation of a putative fimbrial adhesin from Bordetella pertussis and the identification of its gene. Mol. Microbiol. 9: 623 634.
46. Willems, R. J. L.,, P. Paul,, H. G. J van der Heide,, A. ter Avest,, and F. R. Mooi. 1990. Fimbrial phase variation in Bordetella pertussis: a novel mechanism for transcriptional regulation. EMBO J. 9: 2803 2809.
47. Willems, R. J. L.,, C. Geuijen,, G. Renauld,, P. Bertin,, H. G. J. van der Heide,, W. M. R. van de Akker,, C. Locht,, and F. R. Mooi. Mutational analysis of the Bordetella pertussis flmlfha gene cluster: identification of a gene with sequence similarities to haemolysin accessory genes involved in export of FHA. Mol. Microbiol. 11: 337 347.
48. Willems, R. J. L.,, H. G. J. van der Heide,, and F. R. Mooi. 1992. Characterization of a Bordetella pertussis fimbrial gene cluster which is located directly downstream of the filamentous hemagglutinin gene. Mol. Microbiol. 6: 2661 2671.
49. Wright, S. D.,, and S. Silverstein. 1993. Receptors for C3b and C3bi promote phagocytosis but not release of toxic oxygen from human phagocytes. J. Exp. Med. 158: 2016 2023.
50. Yanagishita, M.,, and V. C. Hascall. 1992. Cell surface heparan sulfate proteoglycans. J. Biol. Chem. 267: 9451 9454.
51. Zhang, J. M.,, J. L. Cowell,, A. C. Steven,, P. H. Carter,, C. C. McGrath,, and C. R. Manclark. 1985. Purification and characterization of fimbriae isolated from Bordetella pertussis. Infect. Immun. 48: 422 427.

Tables

Generic image for table
Table 1

Binding features of the FHA molecule

See text for references.

Numbers refer to the positions of the amino acid residues in FhaB.

Citation: Mooi F. 1994. Genes for the Filamentous Hemagglutinin and Fimbriae of : Colocation, Coregulation, and Cooperation?, p 145-155. In Miller V, Kaper J, Portnoy D, Isberg R (ed), Molecular Genetics of Bacterial Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/9781555818340.ch10

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error