1887

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

Author: Frits R. Mooi1
VIEW AFFILIATIONS HIDE AFFILIATIONS
Affiliations: 1: National Institute of Public Health and Environmental Protection, P.O. Box 1, 3720 BA Bilthoven, The Netherlands
Content Type: Monograph
Publication Year: 1994

Category: Microbial Genetics and Molecular Biology; Bacterial Pathogenesis

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

Preview this chapter:
Preview Magnify
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
Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Figures

Genes for the Filamentous Hemagglutinin and Fimbriae of Bordetella pertussis: Colocation, Coregulation, and Cooperation?
[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555818340.chap10-1,webId=/content/author/10.1128/9781555818340.chap10-1,properties={foaf_givenname=Frits R., foaf_name=Frits R. Mooi, foaf_surname=Mooi, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555818340.chap10-aff1]]}]]
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
/content/10.1128/9781555818340.chap10.fig10-1
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.

10.1128/9781555818340/fig10-1_thmb.gif
10.1128/9781555818340/fig10-1.gif
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
/content/10.1128/9781555818340.chap10.fig10-2
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 ( ).

10.1128/9781555818340/fig10-2_thmb.gif
10.1128/9781555818340/fig10-2.gif
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

Genes for the Filamentous Hemagglutinin and Fimbriae of Bordetella pertussis: Colocation, Coregulation, and Cooperation?
[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555818340.chap10-1,webId=/content/author/10.1128/9781555818340.chap10-1,properties={foaf_givenname=Frits R., foaf_name=Frits R. Mooi, foaf_surname=Mooi, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555818340.chap10-aff1]]}]]
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
/content/10.1128/9781555818340.chap10.tab10-1
Table 1

Binding features of the FHA molecule

See text for references.

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

10.1128/9781555818340/tab10-1_thmb.gif
10.1128/9781555818340/tab10-1.gif
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

Back to top
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