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Infect Immun. Nov 1994; 62(11): 5010–5019.
PMCID: PMC303220

Sulfated glycoconjugate receptors for the Bordetella pertussis adhesin filamentous hemagglutinin (FHA) and mapping of the heparin-binding domain on FHA.

Abstract

Filamentous hemagglutinin (FHA) is a major adhesin present on the surface of the gram-negative respiratory pathogen Bordetella pertussis. A number of binding mechanisms have been described for the interaction of FHA with eukaryotic cells. We have focused on its function as a sulfated polysaccharide-binding protein and on identifying potential receptors for FHA on the epithelial cell surface. Using a thin-layer overlay technique, we found that FHA binds specifically to sulfated glycolipids but not to gangliosides or other neutral glycolipids. These results suggest that epithelial cell surface sulfated glycolipids function as receptors for FHA. Further studies demonstrated that a Chinese hamster ovary (CHO) cell strain deficient in glycosaminoglycan expression exhibits greatly diminished attachment to FHA. By FHA-Affi-Gel chromatography, a putative receptor for FHA that has characteristics consistent with a heparan sulfate proteoglycan was isolated from epithelial cell extracts. In addition, by using recombinant FHA fusion proteins, a specific glycosaminoglycan-binding domain located near the N terminus of the FHA molecule was identified. Our results indicate that the B. pertussis adhesin FHA may utilize sulfated glycolipids and proteoglycans commonly found on the surface of human cells and tissues to initiate infection.

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  • Aricò B, Nuti S, Scarlato V, Rappuoli R. Adhesion of Bordetella pertussis to eukaryotic cells requires a time-dependent export and maturation of filamentous hemagglutinin. Proc Natl Acad Sci U S A. 1993 Oct 1;90(19):9204–9208. [PMC free article] [PubMed]
  • Ascencio F, Fransson LA, Wadström T. Affinity of the gastric pathogen Helicobacter pylori for the N-sulphated glycosaminoglycan heparan sulphate. J Med Microbiol. 1993 Apr;38(4):240–244. [PubMed]
  • Bergey EJ, Stinson MW. Heparin-inhibitable basement membrane-binding protein of Streptococcus pyogenes. Infect Immun. 1988 Jul;56(7):1715–1721. [PMC free article] [PubMed]
  • Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. [PubMed]
  • Brennan MJ, Hannah JH, Leininger E. Adhesion of Bordetella pertussis to sulfatides and to the GalNAc beta 4Gal sequence found in glycosphingolipids. J Biol Chem. 1991 Oct 5;266(28):18827–18831. [PubMed]
  • Brennan MJ, Li ZM, Cowell JL, Bisher ME, Steven AC, Novotny P, Manclark CR. Identification of a 69-kilodalton nonfimbrial protein as an agglutinogen of Bordetella pertussis. Infect Immun. 1988 Dec;56(12):3189–3195. [PMC free article] [PubMed]
  • Choi SH, Stinson MW. Purification of a Streptococcus mutans protein that binds to heart tissue and glycosaminoglycans. Infect Immun. 1989 Dec;57(12):3834–3840. [PMC free article] [PubMed]
  • Delisse-Gathoye AM, Locht C, Jacob F, Raaschou-Nielsen M, Heron I, Ruelle JL, de Wilde M, Cabezon T. Cloning, partial sequence, expression, and antigenic analysis of the filamentous hemagglutinin gene of Bordetella pertussis. Infect Immun. 1990 Sep;58(9):2895–2905. [PMC free article] [PubMed]
  • Domenighini M, Relman D, Capiau C, Falkow S, Prugnola A, Scarlato V, Rappuoli R. Genetic characterization of Bordetella pertussis filamentous haemagglutinin: a protein processed from an unusually large precursor. Mol Microbiol. 1990 May;4(5):787–800. [PubMed]
  • Esko JD. Genetic analysis of proteoglycan structure, function and metabolism. Curr Opin Cell Biol. 1991 Oct;3(5):805–816. [PubMed]
  • Esko JD, Stewart TE, Taylor WH. Animal cell mutants defective in glycosaminoglycan biosynthesis. Proc Natl Acad Sci U S A. 1985 May;82(10):3197–3201. [PMC free article] [PubMed]
  • Esko JD, Weinke JL, Taylor WH, Ekborg G, Rodén L, Anantharamaiah G, Gawish A. Inhibition of chondroitin and heparan sulfate biosynthesis in Chinese hamster ovary cell mutants defective in galactosyltransferase I. J Biol Chem. 1987 Sep 5;262(25):12189–12195. [PubMed]
  • Ewanowich CA, Melton AR, Weiss AA, Sherburne RK, Peppler MS. Invasion of HeLa 229 cells by virulent Bordetella pertussis. Infect Immun. 1989 Sep;57(9):2698–2704. [PMC free article] [PubMed]
  • Finlay BB, Falkow S. Common themes in microbial pathogenicity. Microbiol Rev. 1989 Jun;53(2):210–230. [PMC free article] [PubMed]
  • di Guan C, Li P, Riggs PD, Inouye H. Vectors that facilitate the expression and purification of foreign peptides in Escherichia coli by fusion to maltose-binding protein. Gene. 1988 Jul 15;67(1):21–30. [PubMed]
  • Hök M, Kjellén L, Johansson S. Cell-surface glycosaminoglycans. Annu Rev Biochem. 1984;53:847–869. [PubMed]
  • Kaesberg PR, Ershler WB, Esko JD, Mosher DF. Chinese hamster ovary cell adhesion to human platelet thrombospondin is dependent on cell surface heparan sulfate proteoglycan. J Clin Invest. 1989 Mar;83(3):994–1001. [PMC free article] [PubMed]
  • Kimura A, Mountzouros KT, Relman DA, Falkow S, Cowell JL. Bordetella pertussis filamentous hemagglutinin: evaluation as a protective antigen and colonization factor in a mouse respiratory infection model. Infect Immun. 1990 Jan;58(1):7–16. [PMC free article] [PubMed]
  • Kjellén L, Lindahl U. Proteoglycans: structures and interactions. Annu Rev Biochem. 1991;60:443–475. [PubMed]
  • Krivan HC, Olson LD, Barile MF, Ginsburg V, Roberts DD. Adhesion of Mycoplasma pneumoniae to sulfated glycolipids and inhibition by dextran sulfate. J Biol Chem. 1989 Jun 5;264(16):9283–9288. [PubMed]
  • Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. [PubMed]
  • Leininger E, Ewanowich CA, Bhargava A, Peppler MS, Kenimer JG, Brennan MJ. Comparative roles of the Arg-Gly-Asp sequence present in the Bordetella pertussis adhesins pertactin and filamentous hemagglutinin. Infect Immun. 1992 Jun;60(6):2380–2385. [PMC free article] [PubMed]
  • Leininger E, Probst PG, Brennan MJ, Kenimer JG. Inhibition of Bordetella pertussis filamentous hemagglutinin-mediated cell adherence with monoclonal antibodies. FEMS Microbiol Lett. 1993 Jan 1;106(1):31–38. [PubMed]
  • Leininger E, Roberts M, Kenimer JG, Charles IG, Fairweather N, Novotny P, Brennan MJ. Pertactin, an Arg-Gly-Asp-containing Bordetella pertussis surface protein that promotes adherence of mammalian cells. Proc Natl Acad Sci U S A. 1991 Jan 15;88(2):345–349. [PMC free article] [PubMed]
  • Liang OD, Ascencio F, Fransson LA, Wadström T. Binding of heparan sulfate to Staphylococcus aureus. Infect Immun. 1992 Mar;60(3):899–906. [PMC free article] [PubMed]
  • Locht C, Bertin P, Menozzi FD, Renauld G. The filamentous haemagglutinin, a multifaceted adhesion produced by virulent Bordetella spp. Mol Microbiol. 1993 Aug;9(4):653–660. [PubMed]
  • Locht C, Geoffroy MC, Renauld G. Common accessory genes for the Bordetella pertussis filamentous hemagglutinin and fimbriae share sequence similarities with the papC and papD gene families. EMBO J. 1992 Sep;11(9):3175–3183. [PMC free article] [PubMed]
  • Lycke E, Johansson M, Svennerholm B, Lindahl U. Binding of herpes simplex virus to cellular heparan sulphate, an initial step in the adsorption process. J Gen Virol. 1991 May;72(Pt 5):1131–1137. [PubMed]
  • Makhov AM, Hannah JH, Brennan MJ, Trus BL, Kocsis E, Conway JF, Wingfield PT, Simon MN, Steven AC. Filamentous hemagglutinin of Bordetella pertussis. A bacterial adhesin formed as a 50-nm monomeric rigid rod based on a 19-residue repeat motif rich in beta strands and turns. J Mol Biol. 1994 Aug 5;241(1):110–124. [PubMed]
  • Mawhinney TP, Adelstein E, Morris DA, Mawhinney AM, Barbero GJ. Structure determination of five sulfated oligosaccharides derived from tracheobronchial mucus glycoproteins. J Biol Chem. 1987 Mar 5;262(7):2994–3001. [PubMed]
  • McGavin MJ, Raucci G, Gurusiddappa S, Hök M. Fibronectin binding determinants of the Staphylococcus aureus fibronectin receptor. J Biol Chem. 1991 May 5;266(13):8343–8347. [PubMed]
  • Menozzi FD, Gantiez C, Locht C. Interaction of the Bordetella pertussis filamentous hemagglutinin with heparin. FEMS Microbiol Lett. 1991 Feb;62(1):59–64. [PubMed]
  • Menozzi FD, Mutombo R, Renauld G, Gantiez C, Hannah JH, Leininger E, Brennan MJ, Locht C. Heparin-inhibitable lectin activity of the filamentous hemagglutinin adhesin of Bordetella pertussis. Infect Immun. 1994 Mar;62(3):769–778. [PMC free article] [PubMed]
  • Ortega-Barria E, Pereira ME. A novel T. cruzi heparin-binding protein promotes fibroblast adhesion and penetration of engineered bacteria and trypanosomes into mammalian cells. Cell. 1991 Oct 18;67(2):411–421. [PubMed]
  • Prasad SM, Yin Y, Rodzinski E, Tuomanen EI, Masure HR. Identification of a carbohydrate recognition domain in filamentous hemagglutinin from Bordetella pertussis. Infect Immun. 1993 Jul;61(7):2780–2785. [PMC free article] [PubMed]
  • Relman D, Tuomanen E, Falkow S, Golenbock DT, Saukkonen K, Wright SD. Recognition of a bacterial adhesion by an integrin: macrophage CR3 (alpha M beta 2, CD11b/CD18) binds filamentous hemagglutinin of Bordetella pertussis. Cell. 1990 Jun 29;61(7):1375–1382. [PubMed]
  • Relman DA, Domenighini M, Tuomanen E, Rappuoli R, Falkow S. Filamentous hemagglutinin of Bordetella pertussis: nucleotide sequence and crucial role in adherence. Proc Natl Acad Sci U S A. 1989 Apr;86(8):2637–2641. [PMC free article] [PubMed]
  • Roberts DD, Ginsburg V. Sulfated glycolipids and cell adhesion. Arch Biochem Biophys. 1988 Dec;267(2):405–415. [PubMed]
  • Rosenberg LC, Choi HU, Tang LH, Johnson TL, Pal S, Webber C, Reiner A, Poole AR. Isolation of dermatan sulfate proteoglycans from mature bovine articular cartilages. J Biol Chem. 1985 May 25;260(10):6304–6313. [PubMed]
  • Sharon N. Bacterial lectins, cell-cell recognition and infectious disease. FEBS Lett. 1987 Jun 15;217(2):145–157. [PubMed]
  • Sobel M, Soler DF, Kermode JC, Harris RB. Localization and characterization of a heparin binding domain peptide of human von Willebrand factor. J Biol Chem. 1992 May 5;267(13):8857–8862. [PubMed]
  • SVENNERHOLM L. THE GANGLIOSIDES. J Lipid Res. 1964 Apr;5:145–155. [PubMed]
  • Towbin H, Staehelin T, Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350–4354. [PMC free article] [PubMed]
  • Tuomanen E, Towbin H, Rosenfelder G, Braun D, Larson G, Hansson GC, Hill R. Receptor analogs and monoclonal antibodies that inhibit adherence of Bordetella pertussis to human ciliated respiratory epithelial cells. J Exp Med. 1988 Jul 1;168(1):267–277. [PMC free article] [PubMed]
  • Tuomanen E, Weiss A. Characterization of two adhesins of Bordetella pertussis for human ciliated respiratory-epithelial cells. J Infect Dis. 1985 Jul;152(1):118–125. [PubMed]
  • Urisu A, Cowell JL, Manclark CR. Filamentous hemagglutinin has a major role in mediating adherence of Bordetella pertussis to human WiDr cells. Infect Immun. 1986 Jun;52(3):695–701. [PMC free article] [PubMed]
  • Willems RJ, Geuijen C, van der Heide HG, Renauld G, Bertin P, van den Akker WM, Locht C, Mooi FR. Mutational analysis of the Bordetella pertussis fim/fha gene cluster: identification of a gene with sequence similarities to haemolysin accessory genes involved in export of FHA. Mol Microbiol. 1994 Jan;11(2):337–347. [PubMed]
  • WuDunn D, Spear PG. Initial interaction of herpes simplex virus with cells is binding to heparan sulfate. J Virol. 1989 Jan;63(1):52–58. [PMC free article] [PubMed]
  • Yamagata T, Saito H, Habuchi O, Suzuki S. Purification and properties of bacterial chondroitinases and chondrosulfatases. J Biol Chem. 1968 Apr 10;243(7):1523–1535. [PubMed]
  • Yanagishita M, Hascall VC. Cell surface heparan sulfate proteoglycans. J Biol Chem. 1992 May 15;267(14):9451–9454. [PubMed]
  • Zhang JP, Stephens RS. Mechanism of C. trachomatis attachment to eukaryotic host cells. Cell. 1992 May 29;69(5):861–869. [PubMed]

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