Relapsing fever Borrelia binds to neolacto glycans and mediates rosetting of human erythrocytes

Proceedings of the National Academy of Sciences of the United States of America

Volumn 106, Issue 46, 2009, Pages 19280-19285

  Guo, Betty P ^a   Teneberg, Susann ^b   Münch, Robert ^a   Terunuma, Daiyo ^c   Hatano, Ken ^c   Matsuoka, Koji ^c   Ångström, Jonas ^b   Borén, Thomas ^a   Bergström, Sven ^a  

^a UMEÅ UNIVERSITY   (Sweden)

^b UNIVERSITY OF GOTHENBURG   (Sweden)

^c SAITAMA UNIVERSITY   (Japan)

Author keywords

Adhesion; Carbohydrate; Glycosphingolipids; Lacto N neotetraose; Red blood cells

Indexed keywords

GLYCAN DERIVATIVE; GLYCOCONJUGATE; GLYCOSPHINGOLIPID; OLIGOSACCHARIDE; PARAGLOBOSIDE; EPITOPE; GLOBOSIDE; POLYSACCHARIDE;

ARTICLE; BINDING AFFINITY; BLEEDING; BORRELIA; BORRELIA CROCIDURAE; BORRELIA DUTTONII; BORRELIA INFECTION; CAPILLARY FLOW; CELL ADHESION; CENTRAL NERVOUS SYSTEM INFECTION; CONTROLLED STUDY; DISEASE SEVERITY; ENCEPHALITIS; ERYTHROCYTE; ERYTHROCYTE MEMBRANE; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN CARBOHYDRATE INTERACTION; ROSETTE FORMATION; IMMUNOLOGY; METHODOLOGY; MICROBIOLOGY;

BORRELIA; BORRELIA CROCIDURAE; BORRELIA DUTTONII;

BORRELIA; EPITOPES; ERYTHROCYTES; GLOBOSIDES; HUMANS; POLYSACCHARIDES; RELAPSING FEVER; ROSETTE FORMATION;

EID: 73349124828     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0905470106     Document Type: Article

References (28)

1. Burman N, Shamaei-Tousi A, Bergstrom S (1998) The spirochete Borrelia crocidurae causes erythrocyte rosetting during relapsing fever. Infect Immun 66:815-819.
2. Mooser H (1958) Erythrocyte adhesion and hemoglomeration by relapsing fever spirochetes. Z Tropenmed Parasitol 9:93-111.
3. Shamaei-Tousi A, Collin O, Bergh A, Bergstrom S (2001) Testicular damage by micro-circulatory disruption and colonization of an immune-privileged site during Borrelia crocidurae infection. J Exp Med 193:995-1004.
4. Shamaei-Tousi A, Martin P, Bergh A, Burman N, Brannstrom T, Bergstrom S (1999) Erythrocyte-aggregating relapsing fever spirochete Borrelia crocidurae induces formation of microemboli. J Infect Dis 180:1929-1938.
5. Esko JD (1999) Microbial Carbohydrate Binding Proteins (Cold Spring Harbor Laboratory Press, Cold Spring Harbor).
6. Ofek I, Doyle RJ (1994) Bacterial Lectins as Adhesins (Chapman & Hall, New York).
7. Albiger B, Johansson L, Jonsson AB (2003) Lipopolysaccharide-deficient Neisseria meningitidis shows altered pilus-associated characteristics. Infect Immun 71:155-162.
8. Falk P, Boren T, Haslam D, Caparon M (1994) Bacterial adhesion and colonization assays. Methods Cell Biol 45:165-192.
9. Karlsson KA (1987) Preparation of total nonacid glycolipids for overlay analysis of receptors for bacteria and viruses and for other studies. Methods Enzymol 138:212-220.
10. Teneberg S, Leonardsson I, Karlsson H, Jovall PA, Angstrom J, et al. (2002) Lactotetraosylceramide, a novel glycosphingolipid receptor for Helicobacter pylori, present in human gastric epithelium. J Biol Chem 277:19709-19719.
11. Waldi D (1982) Spray Reagents for Thin-Layer Chromatography [Translated from German] (Springer-Verlag, Berlin).
12. Teneberg S, Lonnroth I, Torres Lopez JF, Galili U, Halvarsson MO, et al. (1996) Molecular mimicry in the recognition of glycosphingolipids by Gal alpha 3 Gal beta 4 GlcNac beta-binding Clostridium difficile toxin A, human natural anti alpha-galactosyl IgG and the monoclonal antibody Gal-13: Characterization of a binding-active human glycosphingolipid, non-identical with the animal receptor. Glycobiology 6:599-609.
13. Yamada A, Hatano K, Koyama T, Matsuoka K, Esumi Y, Terunuma D (2006) Syntheses of a series of lacto-N-neotetraose clusters using a carbosilane dendrimer scaffold. Carbohydr Res 341:467-473.
14. Macher BA, Klock JC (1980) Isolation and chemical characterization of neutral glycosphingolipids of human neutrophils. J Biol Chem 255:2092-2096.
15. Siddiqui B, Hakomori S (1973) A ceramide tetrasaccharide of human erythrocyte membrane reacting with anti-type XIV pneumococcal polysaccharide antiserum. Biochim Biophys Acta 330:147-155.
16. Chai W, Piskarev V, Lawson AM (2001) Negative-ion electrospray mass spectrometry of neutral underivatized oligosaccharides. Anal Chem 73:651-657.
17. Levery SB, Nudelman E, Kannagi R, Symington FW, Andersen NH, et al. (1988) 1H-n.m.r. analysis of type-2 chain lacto-gangliosides. Carbohydr Res 178:121-144.
18. Montreuil J (1984) Spatial conformation of glycans and glycoproteins. Biol Cell 51:115-131.
19. Ishikawa Y, Gasa S, Minami R, Makita A (1987) Characterization of neutral glycosphingolipids from fetal human brain: Evidence for stage-specific expression of the globo, ganglio, and neolacto series in the central nervous system. J Biochem 101:1369-1375.
20. Ritter G, Krause W, Geyer R, Stirm S, Wiegandt H (1987) Glycosphingolipid composition of human semen. Arch Biochem Biophys 257:370-378.
21. Bjork S, Breimer ME, Hansson GC, Karlsson KA, Leffler H (1987) Structure of blood group glycosphingolipids of human small intestine. A relation between the expression of fucolipids of epithelial cells and the ABO, Le and Se phenotype of the donor. J Biol Chem 262:6758-6765.
22. Aoki C, Hidari KI, Itonori S, Yamada A, Takahashi N, et al. (2006) Identification and characterization of carbohydrate molecules in mammalian cells recognized by dengue virus type 2. J Biochem 139:607-614.
23. Andersson B, Dahmen J, Frejd T, Leffler H, Magnusson G, et al. (1983) Identification of an active disaccharide unit of a glycoconjugate receptor for penumococci attaching to human pharyngeal epithelial cells. J Exp Med 158:559-570.
24. Hugosson S, Angstrom J, Olsson BM, Bergstrom J, Fredlund H, et al. (1998) Glycosphingolipid binding specificities of Neisseria meningitidis and Haemophilus influenzae: Detection, isolation, and characterization of a binding-active glycosphingolipid from human oropharyngeal epithelium. J Biochem 124:1138-1152.
25. Miller-Podraza H, Lanne B, Angstrom J, Teneberg S, Milh MA, et al. (2005) Novel binding epitope for Helicobacter pylori found in neolacto carbohydrate chains: Structure and cross-binding properties. J Biol Chem 280:19695-19703.
26. Teneberg S, Hirst TR, Angstrom J, Karlsson KA (1994) Comparison of the glycolipid-binding specificities of cholera toxin and porcine Escherichia coli heat-labile enterotoxin: Identification of a receptor-active non-ganglioside glycolipid for the heat-labile toxin in infant rabbit small intestine. Glycoconj J 11:533-540.
27. Teneberg S, Berntsson A, Angstrom J (2000) Common architecture of the primary galactose binding sites of Erythrina corallodendron lectin and heat-labile enterotoxin from Escherichia coli in relation to the binding of branched neolactohexaosylceramide. J Biochem 128:481-491.
28. Chester MA (1998) IUPAC-IUB Joint Commission on Biochemical Nomenclature (JCBN). Nomenclature of glycolipids - recommendations 1997. Eur J Biochem 257:293-298.