Erythrocyte and porcine intestinal glycosphingolipids recognized by F4 fimbriae of enterotoxigenic escherichia coli

PLoS ONE

Volumn 6, Issue 9, 2011, Pages

  Coddens, Annelies ^a   Valis, Erik ^b   Benktander, John ^b   Ångström, Jonas ^b   Breimer, Michael E ^c   Cox, Eric ^a   Teneberg, Susann ^b  

^a GHENT UNIVERSITY   (Belgium)

^b UNIVERSITY OF GOTHENBURG   (Sweden)

^c SAHLGRENSKA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

GALACTOSYLCERAMIDE; GANGLIOTRIOSYLCERAMIDE; GLOBOTRIAOSYLCERAMIDE; GLYCOSPHINGOLIPID; HYDROXY FATTY ACID; ISOGLOBOTRIAOSYLCERAMIDE; LACTOSYLCERAMIDE; PARAGLOBOSIDE; PHYTOSPHINGOSINE; SULFATIDE; UNCLASSIFIED DRUG; G(A1) GANGLIOSIDE; GANGLIO N TRIAOSYLCERAMIDE; GANGLIO-N-TRIAOSYLCERAMIDE; GANGLIOSIDE; GLOBOSIDE;

ANIMAL CELL; ARTICLE; CELL ADHESION; CHICKEN; CONTROLLED STUDY; ENTEROTOXIGENIC ESCHERICHIA COLI; ERYTHROCYTE; FIMBRIA; GUINEA PIG; HEMAGGLUTINATION; HUMAN; HUMAN CELL; MASS SPECTROMETRY; NONHUMAN; PROTON NUCLEAR MAGNETIC RESONANCE; RABBIT; SMALL INTESTINE MUCOSA; ANIMAL; BACTERIUM ADHERENCE; BINDING COMPETITION; BINDING SITE; CARBOHYDRATE ANALYSIS; CHEMISTRY; GENETICS; IMMUNOLOGY; INTESTINE; INTESTINE MUCOSA; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; MUTATION; POLYACRYLAMIDE GEL ELECTROPHORESIS; SWINE; THIN LAYER CHROMATOGRAPHY;

ESCHERICHIA COLI; SUIDAE; SUS;

ANIMALS; BACTERIAL ADHESION; BINDING SITES; BINDING, COMPETITIVE; CARBOHYDRATE SEQUENCE; CHICKENS; CHROMATOGRAPHY, THIN LAYER; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ENTEROTOXIGENIC ESCHERICHIA COLI; ERYTHROCYTES; FIMBRIAE, BACTERIAL; GANGLIOSIDES; GLOBOSIDES; GLYCOSPHINGOLIPIDS; HEMAGGLUTINATION; INTESTINAL MUCOSA; INTESTINES; MOLECULAR SEQUENCE DATA; MUTATION; SWINE;

EID: 80052824664     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0023309     Document Type: Article

References (54)

1. Fairbrother JM, Nadeau E, Gyles CL, (2005) Escherichia coli in postweaning diarrhea in pigs: an update on bacterial types, pathogenesis, and prevention strategies. Anim Health Res Re 6: 17-39.
2. Van den Broeck W, Cox E, Oudega B, Goddeeris BM, (2000) The F4 fimbrial antigen of Escherichia coli and its receptors. Vet Microbiol 71: 223-244.
3. Mol O, Oudega B, (1996) Molecular and structural aspects of fimbriae biosynthesis and assembly in Escherichia coli. FEMS Microbiol Rev 19: 25-52.
4. Oudega B, de Graaf M, de Boer L, Bakker D, Vader CE, et al. (1989) Detection and identification of FaeC as a minor component of K88 fibrillae of Escherichia coli. Mol Microbiol 3: 645-652.
5. Valent QA, Zaal J, de Graaf FK, Oudega B, (1995) Subcellular localization and topology of the K88 usher FaeD in Escherichia coli. Mol Microbiol 16: 1243-1257.
6. Bakker D, Vader CE, Roosendaal B, Mooi FR, Oudega B, et al. (1991) Structure and function of periplasmic chaperone-like proteins involved in the biosynthesis of K88 and K99 fimbriae in enterotoxigenic Escherichia coli. Mol Microbiol 5: 875-886.
7. Bakker D, Willemsen PT, Willems RH, Huisman TT, Mooi FR, et al. (1992) Identification of minor fimbrial subunits involved in biosynthesis of K88 fimbriae. J Bacteriol 174: 6350-6358.
8. Bakker D, Willemsen PT, Simons LH, van Zijderveld FG, de Graaf FK, (1992) Characterization of the antigenic and adhesive properties of FaeG, the major subunit of K88 fimbriae. Mol Microbiol 6: 247-255.
9. Guinée PA, Jansen WH, (1979) Behavior of Escherichia coli K antigens K88ab, K88ac, and K88ad in immunoelectrophoresis, double diffusion, and hemagglutination. Infect Immun 23: 700-705.
10. Gaastra W, Klemm P, De Graaf FK, (1983) The nucleotide sequence of the K88ad protein subunit of porcine enterotoxigenic Escherichia coli. FEMS Microbiol Lett 18: 177-183.
11. Payne D, O'Reilly M, Williamson D, (1993) The K88 fimbrial adhesin of enterotoxigenic Escherichia coli binds to ß1-linked galactosyl residues in glycosphingolipids. Infect Immun 61: 3673-3677.
12. Grange PA, Mouricourt MA, Levery SB, Francis DH, Erickson AK, (2002) Evaluation of receptor binding specificity of Escherichia coli K88 (F4) fimbrial adhesin variants using porcine serum transferrin and glycosphingolipids as model receptors. Infect Immun 70: 2336-2343.
13. Grange PA, Erickson AK, Levery SB, Francis DH, (1999) Identification of an intestinal neutral glycosphingolipid as a phenotype-specific receptor for the K88ad fimbrial adhesin of Escherichia coli. Infect Immun 67: 165-172.
14. Seyama Y, Yamakawa T, (1974) Chemical structure of glycolipids of guinea pig red blood cell membrane. J Biochem 75: 837-842.
15. Shiraishi T, Uda Y, (1985) Characterization of neutral sphingolipids from chicken erythrocytes. J Lipid Res 26: 860-866.
16. Karlsson H, Halim A, Teneberg S, (2010) Differentiation of glycosphingolipid-derived glycan structural isomers by liquid chromatography-mass spectrometry. Glycobiology 20: 1103-1116.
17. Dabrowski J, Hanfland P, Egge H, (1980) Structural analysis of glycosphingolipids by high-resolution 1H nuclear magnetic resonance spectroscopy. Biochemistry 19: 5652-5658.
18. Koerner TAW Jr, Prestegard JH, Demou PC, Yu RK, (1983) High-resolution proton NMR studies of gangliosides. 1. Use of homonuclear two-dimensional spin-echo J-correlated spectroscopy for determination of residue composition and anomeric configurations. Biochemistry 22: 2676-2687.
19. Teneberg S, Ångström J, Ljungh Å, (2004) Carbohydrate recognition by enterohemorrhagic Escherichia coli. Characterization of a novel glycosphingolipid from cat small intestine. Glycobiology 14: 187-196.
20. Holgersson J, Jovall P-Å, Breimer ME, (1991) Glycosphingolipids of human large intestine: detailed structural characterization with special reference to blood group compounds and bacterial receptor structures. J Biochem 110: 120-131.
21. Thorn JJ, Levery SB, Salyan MEK, Stroud MR, Cedergren B, et al. (1992) Structural characterization of x2 glycosphingolipid, its extended form, and its sialosyl derivatives: Accumulation associated with the rare blood group p phenotype. Biochemistry 31: 6509-6517.
22. Dabrowski J, Egge H, Hanfland P, (1980) High resolution nuclear magnetic resonance spectroscopy of glycosphingolipids. I: 360 MHz 1H and 90.5 MHz 13C NMR analysis of galactosylceramides. Chem Phys Lipids 26: 187-196.
23. Poppe L, Dabrowski J, von der Lieth C-W, Koike K, Ogawa T, (1990) Three-dimensional structure of the oligosaccharide terminus of globotriaosylceramide and isoglobotriaosylceramide in solution. A rotating-frame NOE study using hydroxyl groups as long-range sensors in conformational analysis by 1H-NMR spectroscopy. Eur J Biochem 189: 313-325.
24. Karlsson KA, Leffler H, Samuelsson BE, (1974) Characterization of the forssman glycolipid hapten of horse kidney by mass spectrometry. J Biol Chem 249: 4819-4823.
25. Falk P, Holgersson J, Jovall PA, Karlsson KA, Strömberg N, et al. (1986) An antigen present in rat adenocarcinoma and normal colon non-epithelial stroma is a novel Forssman-like glycolipid based on isoglobotetraosylceramide. Biochim Biophys Acta 12: 296-299.
26. Blomberg L, Krivan HC, Cohen PS, Conway PL, (1993) Piglet ileal mucus contains protein and glycolipid (galactosylceramide) receptors specific for Escherichia coli K88 fimbriae. Infect Immun 61: 2526-2531.
27. Verdonck F, Cox E, Schepers E, Imberechts H, Joensuu J, et al. (2004) Conserved regions in the sequence of the F4 (K88) fimbrial adhesin FaeG suggest a donor strand mechanism in F4 assembly. Vet Microbiol 102: 215-225.
28. De Greve H, Wyns L, Bouckaert J, (2007) Combining sites of bacterial fimbriae. Curr Op Struct Biol 17: 507-512.
29. Verdonck F, Cox E, Van der Stede Y, Goddeeris BM, (2004) Oral immunization of piglets with recombinant F4 fimbrial adhesin FaeG monomers induces a mucosal and systemic F4-specific immune response. Vaccine 22: 4291-4299.
30. Zhang W, Fang Y, Francis DH, (2009) Characterization of the binding specificity of K88ac and K88ad fimbriae of enterotoxigenic Escherichia coli by constructing K88ac/K88ad chimeric FaeG major subunits. Infect Immun 77: 699-706.
31. Bock K, Breimer ME, Brignole A, Hansson GC, Karlsson K-A, et al. (1985) Specificity of binding of a strain of uropathogenic Escherichia coli to Gal alpha 1- 4Gal-containing glycosphingolipids. J Biol Chem 260: 8545-8551.
32. Lingwood CA, Law H, Richardsson S, Petric M, Brunton JL, et al. (1987) Glycolipid binding of purified and recombinant Escherichia coli produced verotoxin in vitro. J Biol Chem 262: 8834-8839.
33. Waddell T, Head S, Petric M, Cohen A, Lingwood CA, (1988) Globotriosylceramide is specifically recognized by the Escherichia coli verocytotoxin 2. Biochem Biophys Res Commun 152: 674-679.
34. DeGrandis S, Law H, Brunton J, Gyles C, Lingwood CA, (1989) Globotetraosylceramide is recognized by the pig edema disease toxin. J Biol Chem 264: 12520-12525.
35. Samuel JE, Perera LP, Ward S, O'Brien AD, Ginsburg V, et al. (1990) Comparison of the glycolipid receptor specificities of Shiga-like toxin type II and Shiga-like toxin type II variants. Infect Immun 58: 611-618.
36. Bäckhed F, Ahlsén B, Roche N, Ångström J, von Euler A, et al. (2002) Identification of target tissue glycosphingolipid receptors for uropathogenic, F1C-fimbriated Escherichia coli, and its role in mucosal inflammation. J Biol Chem 277: 18198-18205.
37. Jansson L, Tobias J, Jarefjäll C, Lebens M, Svennerholm A-M, et al. (2009) The major subunit (CfaB) of colonization factor antigen I from enterotoxigenic Escherichia coli is a glycosphingolipid binding protein. PLoS ONE 4: e4487.
38. Krivan HC, Olson LD, Barile MF, Ginsburg V, Roberts DD, (1989) Adhesion of Mycoplasma pneumoniae to sulfated glycolipids and inhibition by dextran sulfate. J Biol Chem 264: 9283-9288.
39. Brennan MJ, Hannah JH, Leininger E, (1991) Adhesion of Bordetella pertussis to sulfatides and to the GalNAcß3Gal sequence found in glycosphingolipids. J Biol Chem 266: 18827-18831.
40. Khan AS, Johnston NC, Goldfine H, Schifferli DM, (1996) Porcine 987P glycolipid receptors on the intestinal brush borders and their cognate bacterial ligands. Infect Immun 64: 3688-3693.
41. Saitoh T, Natomi H, Zhao W, Okuzumi K, Sugano K, et al. (1991) Identification of glycolipid receptors for Helicobacter pylori by TLC-immunostaining. FEBS Lett 282: 385-387.
42. Kamisago S, Iwamori M, Tai T, Mitamura K, Yazaki Y, et al. (1996) Role of sulphatides in adhesion of Helicobacter pylori to gastric cancer cells. Infect Immun 64: 624-628.
43. Rousset E, Harel J, Dubreuil JD, (1998) Sulfatide from the pig jejunum brush border epithelial cell surface is involved in binding of Escherichia coli enterotoxin b. Infect Immun 66: 5650-5658.
44. Karlsson K-A, (1989) Animal glycosphingolipids as membrane attachment sites for bacteria. Annu Rev Biochem 58: 309-350.
45. Jin LZ, Zhao X, (2000) Intestinal receptors for adhesive fimbriae of enterotoxigenic Escherichia coli (ETEC) K88 in swine-a review. Appl Microbiol Biotechnol 54: 311-318.
46. Verdonck F, Cox E, Schepers E, Imberechts H, Joensuu J, et al. (2004) Conserved regions in the sequence of the F4 (K88) fimbrial adhesin FaeG suggest a donor strand mechanism in F4 assembly. Vet Microbiol 102: 215-225.
47. Blattner FR, Plunkett G 3rd, Bloch CA, Perna NT, Burland V, et al. (1997) The complete genome sequence of Escherichia coli K-12. Science 277: 1453-1462.
48. Van den Broeck W, Cox E, Goddeeris BM, (1999) Receptor-specific binding of purified F4 to isolated villi. Vet Microbiol 68: 255-263.
49. Karlsson K-A, (1987) Preparation of total non-acid glycolipids for overlay analysis of receptors for bacteria and viruses and for other studies. Meth Enzymol 138: 212-220.
50. Samuelsson BE, Pimlott W, Karlsson K-A, (1990) Mass spectrometry of mixtures of intact glycosphingolipids. Methods Enzymol 193: 623-646.
51. Waldi D, (1962) Sprühreagentien für die dünnschicht-chromatographie. In: Stahl E, editors. Dünnschicht-Chromatographie Berlin Springer-Verlag pp. 496-515.
52. Karlsson K-A, Lanne B, Pimlott W, Teneberg S, (1991) The resolution into molecular species by desorption of glycolipids from thin-layer chromatograms, using combined thin-layer chromatography and fast-atom-bombardment mass spectrometry. Carb Res 221: 49-64.
53. Ito M, Yamagata T, (1989) Purification and characterization of glycosphingolipid-specific endoglycosidases (endoglycoceramidases) from a mutant strain of Rhodococcus sp. Evidence for three molecular species of endoglycoceramidase with different specificities. J Biol Chem 264: 9510-9519.
54. Marion D, Wüthrich K, (1983) Application of phase sensitive two-dimensional correlated spectroscopy (COSY) for measurements of 1H-1H spin-spin coupling constants in proteins. Biochem Biophys Res Commun 113: 967-974.