Shiga-like toxin binds with high avidity to multivalent O-linked blood group P1 determinants on mucin-type fusion proteins

Glycobiology

Volumn 24, Issue 1, 2014, Pages 26-38

  Maria Cherian, Reeja ^a   Gaunitz, Stefan ^b   Nilsson, Anki ^c   Liu, Jining ^a   Karlsson, Niclas G ^a   Holgersson, Jan ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^c Recopharma AB ^*  (Sweden)

Author keywords

blood group P1; mass spectrometry; mucin; Shiga like toxin; SPR

Indexed keywords

ALBUMIN; ALPHA 1,4 GALACTOSYLTRANSFERASE; BETA 1,6 N ACETYLGLUCOSAMINYLTRANSFERASE; GLYCAN; GLYCOSYLTRANSFERASE; HYBRID PROTEIN; IMMUNOGLOBULIN G2B; IMMUNOGLOBULIN M ANTIBODY; MUCIN; N ACETYLGLUCOSAMINYLTRANSFERASE; NEOGLYCOPROTEIN; P SELECTIN GLYCOPROTEIN LIGAND 1; UNCLASSIFIED DRUG; VEROTOXIN 1; VEROTOXIN 2;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; CHO CELL; CONTROLLED STUDY; DRUG PROTEIN BINDING; GENETIC TRANSFECTION; IMMUNOCYTOCHEMISTRY; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CARBOHYDRATE INTERACTION; TOXIN ANALYSIS; TOXIN STRUCTURE; WESTERN BLOTTING;

BLOOD GROUP P1; MASS SPECTROMETRY; MUCIN; SHIGA-LIKE TOXIN; SPR;

ANIMALS; CHO CELLS; COLUMBIDAE; CRICETINAE; CRICETULUS; GLOBOSIDES; HUMANS; IMMUNOGLOBULIN G; MEMBRANE GLYCOPROTEINS; MICE; N-ACETYLGLUCOSAMINYLTRANSFERASES; POLYSACCHARIDES; PROTEIN BINDING; RECOMBINANT FUSION PROTEINS; SHIGA TOXIN 1; SHIGA TOXIN 2; SHIGA-TOXIGENIC ESCHERICHIA COLI;

EID: 84890419928     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cwt086     Document Type: Article

References (59)

1. Bergan J, Dyve Lingelem AB, Simm R, Skotland T, Sandvig K. 2012. Shiga toxins. Toxicon. 60:1085-1107.
2. Bock K, Breimer ME, Brignole A, Hansson GC, Karlsson KA, Larson G, Leffler H, Samuelsson BE, Stromberg N, Eden CS. 1985. Specificity of binding of a strain of uropathogenic Escherichia coli to Gal alpha 1- 4Gal-containing glycosphingolipids. J Biol Chem. 260:8545-8551.
3. Ceroni A, Dell A, Haslam SM. 2007. The GlycanBuilder: A fast, intuitive and flexible software tool for building and displaying glycan structures. Source Code Biol Med. 2:3
4. Ceroni A, Maass K, Geyer H, Geyer R, Dell A, Haslam SM. 2008. GlycoWorkbench: A tool for the computer-assisted annotation of mass spectra of glycans. J Proteome Res. 7:1650-1659.
5. Chatterjee S, Khullar M, Shi WY. 1995. Digalactosylceramide is the receptor for staphylococcal enterotoxin-B in human kidney proximal tubular cells. Glycobiology. 5:327-333.
6. 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.
7. Dohi H, Nishida Y, Mizuno M, Shinkai M, Kobayashi T, Takeda T, Uzawa H, Kobayashi K. 1999. Synthesis of an artificial glycoconjugate polymer carrying Pk-antigenic trisaccharide and its potent neutralization activity against Shiga-like toxin. Bioorg Med Chem. 7:2053-2062.
8. Dundas S, Todd WTA, Stewart AI, Murdoch PS, Chaudhuri AKR, Hutchinson SJ. 2001. The central Scotland Escherichia coli O157:H7 outbreak: Risk factors for the hemolytic uremic syndrome and death among hospitalized patients. Clin Infect Dis. 33:923-931.
9. Endo Y, Tsurugi K, Yutsudo T, Takeda Y, Ogasawara T, Igarashi K. 1988. Site of action of a Vero toxin (VT2) from Escherichia coli O157:H7 and of Shiga toxin on eukaryotic ribosomes. Eur J Biochem. 171:45-50.
10. Flagler MJ, Mahajan SS, Kulkarni AA, Iyer SS, Weiss AA. 2010. Comparison of binding platforms yields insights into receptor binding differences between shiga toxins 1 and 2. Biochemistry. 49:1649-1657.
11. François-Gerard C, Brocteur J. 1980. Application à la sérologie transfusionnelle du caractère antigénique P1 du blanc d'oeuf de pigeon. Rev Fr Transfus Immunohematol. 23:95-102.
12. Francois-Gerard C, Gerday C, Beeley JG. 1979. Turtle-dove ovomucoid, a glycoprotein proteinase inhibitor with P1-blood-group antigen activity. Biochem J. 177:679-685.
13. Fraser ME, Chernaia MM, Kozlov YV, James MN. 1994. Crystal structure of the holotoxin from Shigella dysenteriae at 2.5 A resolution.Nat Struct Biol. 1:59-64.
14. Gallegos KM, Conrady DG, Karve SS, Gunasekera TS, Herr AB, Weiss AA. 2012. Shiga toxin binding to glycolipids and glycans. PLoS One. 7:e30368.
15. Gilboa-Garber N, Sudakevitz D, Sheffi M, Sela R, Levene C. 1994. PA-I and PA-II lectin interactions with the ABO(H) and P blood group glycosphingolipid antigens may contribute to the broad spectrum adherence of Pseudomonas aeruginosa to human tissues in secondary infections. Glycoconj J. 11:414-417.
16. Gustafsson A, Hultberg A, Sjöström R, Kacskovics I, Breimer ME, Borén T, Hammarström L, Holgersson J. 2006. Carbohydrate-dependent inhibition of Helicobacter pylori colonization using porcine milk. Glycobiology. 16:1-10.
17. Gustafsson A, Sjoblom M, Strindelius L, Johansson T, Fleckenstein T, Chatzissavidou N, Lindberg L, Angstrom J, Rova U, Holgersson J. 2011. Pichia pastoris-produced mucin-type fusion proteins with multivalent O-glycan substitution as targeting molecules for mannose-specific receptors of the immune system. Glycobiology. 21:1071-1086.
18. Hayes CA, Karlsson NG, Struwe WB, Lisacek F, Rudd PM, Packer NH, Campbell MP. 2011. UniCarb-DB: A database resource for glycomic discovery. Bioinformatics. 27:1343-1344.
19. Iwamura K, Furukawa K, Uchikawa M, Sojka BN, Kojima Y, Wiels J, Shiku H, Urano T, Furukawa K. 2003. The blood group P1 synthase gene is identical to the Gb3/CD77 synthase gene. A clue to the solution of the P1/P2/p puzzle. J Biol Chem. 278:44429-44438.
20. Johannes L, Romer W. 2010. Shiga toxins-from cell biology to biomedical applications. Nat Rev Microbiol. 8:105-116.
21. Johnson JR, Berggren T. 1994. Pigeon and dove eggwhite protect mice against renal infection due to P fimbriated Escherichia coli. Am J Med Sci. 307:335-339.
22. Johnson JR, Ross AE. 1993. P1-antigen-containing avian egg whites as inhibitors of P adhesins among wild-type Escherichia coli strains from patients with urosepsis. Infect Immun. 61:4902-4905.
23. Johnson JR, Swanson JL, Neill MA. 1992. Avian P1 antigens inhibit agglutination mediated by P fimbriae of uropathogenic Escherichia coli. Infect Immun. 60:578-583.
24. Kale RR, McGannon CM, Fuller-Schaefer C, Hatch DM, Flagler MJ, Gamage SD, Weiss AA, Iyer SS. 2008. Differentiation between structurally homologous Shiga 1 and Shiga 2 toxins by using synthetic glycoconjugates. Angew Chem Int Ed. 47:1265-1268.
25. Karlsson NG, Schulz BL, Packer NH. 2004. Structural determination of neutral O-linked oligosaccharide alditols by negative ion LC-electrospray-MSn. J Am Soc Mass Spectrom. 15:659-672.
26. Karmali MA, Steele BT, Petric M, Lim C. 1983. Sporadic cases of haemolytic-uraemic syndrome associated with faecal cytotoxin and cytotoxin-producing Escherichia coli in stools. Lancet. 1:619-620.
27. Kenny DT, Skoog EC, Lindén SK, Struwe WB, Rudd PM, Karlsson NG. 2012. Presence of terminal N-acetylgalactosamineß1-4N-acetylglucosamine residues on O-linked oligosaccharides from gastric MUC5AC: Involvement in Helicobacter pylori colonization? Glycobiology. 22:1077-1085.
28. Kitov PI, Mulvey GL, Griener TP, Lipinski T, Solomon D, Paszkiewicz E, Jacobson JM, Sadowska JM, Suzuki M, Yamamura K, et al. 2008. In vivo supramolecular templating enhances the activity of multivalent ligands: A potential therapeutic against the Escherichia coli O157 AB5 toxins. P Natl Acad Sci USA. 105:16837-16842.
29. Kitov PI, Sadowska JM, Mulvey G, Armstrong GD, Ling H, Pannu NS, Read RJ, Bundle DR. 2000. Shiga-like toxins are neutralized by tailored multivalent carbohydrate ligands. Nature. 403:669-672.
30. Li X, Wu P, Cheng S, Lv X. 2012. Synthesis and assessment of globotriosechitosan conjugate, a novel inhibitor of shiga toxins produced by Escherichia coli. J Med Chem. 55:2702-2710.
31. Lindberg AA, Brown JE, Stromberg N, Westling-Ryd M, Schultz JE, Karlsson KA. 1987. Identification of the carbohydrate receptor for Shiga toxin produced by Shigella dysenteriae type 1. J Biol Chem. 262:1779-1785.
32. Lindberg L, Liu J, Gaunitz S, Nilsson A, Johansson T, Karlsson NG, Holgersson J. 2013. Mucin-type fusion proteins with blood group A or B determinants on defined O-glycan core chains produced in glycoengineered Chinese hamster ovary cells and their use as immunoaffinity matrices. Glycobiology. 23:720-735.
33. Ling H, Boodhoo A, Hazes B, Cummings MD, Armstrong GD, Brunton JL, Read RJ. 1998. Structure of the shiga-like toxin I B-pentamer complexed with an analogue of its receptor Gb3. Biochemistry. 37:1777-1788.
34. Lingwood CA. 1993. Verotoxins and their glycolipid receptors. Adv Lipid Res. 25:189-211.
35. Lingwood CA, Binnington B, Manis A, Branch DR. 2010. Globotriaosyl ceramide receptor function - Where membrane structure and pathology intersect. FEBS Lett. 584:1879-1886.
36. Lingwood D, Binnington B, Rog T, Vattulainen I, Grzybek M, Coskun U, Lingwood CA, Simons K. 2011. Cholesterol modulates glycolipid conformation and receptor activity. Nat Chem Biol. 7:260-262.
37. Liu J, Gustafsson A, Breimer ME, Kussak A, Holgersson J. 2005. Anti-pig antibody adsorption efficacy of a-Gal carrying recombinant P-selectin glycoprotein ligand-1/immunoglobulin chimeras increases with core 2 ß1, 6-N-acetylglucosaminyltransferase expression. Glycobiology. 15:571-583.
38. Liu J, Qian Y, Holgersson J. 1997. Removal of xenoreactive human anti-pig antibodies by absorption on recombinant mucin-containing glycoproteins carrying the Gal alpha1,3Gal epitope. Transplantation. 63:1673-1682.
39. Liu J, Weintraub A, Holgersson J. 2003. Multivalent Galalpha1, 3Galsubstitution makes recombinant mucin-immunoglobulins efficient absorbers of anti-pig antibodies. Xenotransplantation. 10:149-163.
40. Löfling JC, Hauzenberger E, Holgersson J. 2002. Absorption of anti-blood group A antibodies on P-selectin glycoprotein ligand-1/immunoglobulin chimeras carrying blood group A determinants: Core saccharide chain specificity of the Se and H gene encoded a1,2 fucosyltransferases in different host cells. Glycobiology. 12:173-182.
41. MacConnachie AA, Todd WT. 2004. Potential therapeutic agents for the prevention and treatment of haemolytic uraemic syndrome in shiga toxin producing Escherichia coli infection. Curr Opin Infect Dis. 17:479-482.
42. Mahfoud R, Manis A, Binnington B, Ackerley C, Lingwood CA. 2010. A major fraction of glycosphingolipids in model and cellular cholesterolcontaining membranes is undetectable by their binding proteins. J Biol Chem. 285:36049-36059.
43. Miyake M, Utsuno E, Noda M. 2000. Binding of avian ovomucoid to Shiga-like toxin type 1 and its utilization for receptor analog affinity chromatography. Anal Biochem. 281:202-208.
44. Schmidt H, Scheef J, Morabito S, Caprioli A, Wieler LH, Karch H. 2000. A new Shiga toxin 2 variant (Stx2f) from Escherichia coli isolated from pigeons. Appl Environ Microbiol. 66:1205-1208.
45. Schulz BL, Packer NH, Karlsson NG. 2002. Small-scale analysis of O-linked oligosaccharides from glycoproteins and mucins separated by gel electrophoresis. Anal Chem. 74:6088-6097.
46. Seed B. 1987. An LFA-3 cDNA encodes a phospholipid-linked membrane protein homologous to its receptor CD2. Nature. 329:840-842.
47. Shimizu H, Field RA, Homans SW, Donohue-Rolfe A. 1998. Solution structure of the complex between the B-subunit homopentamer of verotoxin VT-1 from Escherichia coli and the trisaccharide moiety of globotriaosylceramide. Biochemistry. 37:11078-11082.
48. Stein PE, Boodhoo A, Tyrrell GJ, Brunton JL, Read RJ. 1992. Crystal structure of the cell-binding B oligomer of verotoxin-1 from E. coli. Nature. 355:748-750.
49. Suzuki N, Khoo K, Chen C, Chen H, Lee YC. 2003. N-glycan structures of pigeon IgG. J Biol Chem. 278:46293-46306.
50. Suzuki N, Khoo K, Chen H, Johnson JR, Lee YC. 2001. Isolation and characterization of major glycoproteins of pigeon egg white. J Biol Chem. 276:23221-23229.
51. Suzuki N, Yamamoto K. 2010. Molecular cloning of pigeon UDPgalactose: ß-d-galactoside a1,4-galactosyltransferase and UDP-galactose:ß- d-galactoside ß1,4-galactosyltransferase, two novel enzymes catalyzing the formation of Gala1-4Galß1-4Galß1-4GlcNAc sequence. J Biol Chem. 285:5178-5187.
52. Takahashi N, Khoo K, Suzuki N, Johnson JR, Lee YC. 2001. N-glycan structures from the major glycoproteins of pigeon egg white. J Biol Chem. 276:23230-23239.
53. Takeda T, Yoshino K, Adachi E, Sato Y, Yamagata K. 1999. In vitro assessment of a chemically synthesized Shiga toxin receptor analog attached to chromosorb P (Synsorb Pk) as a specific absorbing agent of Shiga toxin 1 and 2. Microbiol Immunol. 43:331-337.
54. Tesh VL, O'Brien AD. 1991. The pathogenic mechanisms of Shiga toxin and the Shiga-like toxins. Mol Microbiol. 5:1817-1822.
55. Thuresson B, Westman JS, Olsson ML. 2011. Identification of a novel A4GALT exon reveals the genetic basis of the P1/P2 histo-blood groups. Blood. 117:678-687.
56. Tikkanen K, Haataja S, Finne J. 1996. The galactosyl-(alpha 1-4)- galactose-binding adhesin of Streptococcus suis: Occurrence in strains of different hemagglutination activities and induction of opsonic antibodies. Infect Immun. 64:3659-3665.
57. Tikkanen K, Haataja S, Francois-Gerard C, Finne J. 1995. Purification of a galactosyl-alpha 1-4-galactose-binding adhesin from the gram-positive meningitis-associated bacterium Streptococcus suis. J Biol Chem. 270: 28874-28878.
58. Tomoda H, Arai M, Koyama N, Matsui H, O mura S, Obata R, Lee YC. 2002. Purification of Shiga-like toxin 1 by pigeon egg white glycoproteins immobilized on Sepharose gels. Anal Biochem. 311:50-56.
59. Varki A, Cummings RD, Esko JD, Freeze HH, Stanley P, Marth JD, Bertozzi CR, Hart GW, Etzler ME. 2009. Symbol nomenclature for glycan representation. Proteomics. 9:5398-5399.