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Research Paper

Helicobacter suis binding to carbohydrates on human and porcine gastric mucins and glycolipids occurs via two modes

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Pages 898-918 | Received 13 Nov 2017, Accepted 01 Apr 2018, Published online: 15 May 2018

References

  • Barbosa AJ, Silva JC, Nogueira AM, Paulino Junior E, Miranda CR. Higher incidence of Gastrospirillum sp. in swine with gastric ulcer of the pars oesophagea. Veterinary pathology 1995; 32:134–9.
  • De Groote D, Ducatelle R, van Doorn LJ, Tilmant K, Verschuuren A, Haesebrouck F. Detection of “Candidatus Helicobacter suis” in gastric samples of pigs by PCR: comparison with other invasive diagnostic techniques. Journal of clinical microbiology 2000; 38:1131–5.
  • De Witte C, Devriendt B, Flahou B, Bosschem I, Ducatelle R, Smet A, Haesebrouck F. Helicobacter suis induces changes in gastric inflammation and acid secretion markers in pigs of different ages. Veterinary research 2017; 48:34.
  • De Bruyne E, Flahou B, Chiers K, Meyns T, Kumar S, Vermoote M, Pasmans F, Millet S, Dewulf J, Haesebrouck F, et al. An experimental Helicobacter suis infection causes gastritis and reduced daily weight gain in pigs. Veterinary microbiology 2012; 160:449–54.
  • Van den Bulck K, Decostere A, Baele M, Driessen A, Debongnie JC, Burette A, Stolte M, Ducatelle R, Haesebrouck F. Identification of non-Helicobacter pylori spiral organisms in gastric samples from humans, dogs, and cats. Journal of clinical microbiology 2005; 43:2256–60.
  • Debongnie JC, Donnay M, Mairesse J. Gastrospirillum hominis (“Helicobacter heilmanii”): a cause of gastritis, sometimes transient, better diagnosed by touch cytology? The American journal of gastroenterology 1995; 90:411–6.
  • Debongnie JC, Donnay M, Mairesse J, Lamy V, Dekoninck X, Ramdani B. Gastric ulcers and Helicobacter heilmannii. European journal of gastroenterology & hepatology 1998; 10:251–4.
  • Morgner A, Bayerdorffer E, Meining A, Stolte M, Kroher G. Helicobacter heilmannii and gastric cancer. Lancet 1995; 346:511–2.
  • Bansil R, Turner BS. Mucin structure, aggregation, physiological functions and biomedical applications. Current Opinion in Colloid & Interface Science 2006; 11:164–70.
  • Ho SB, Shekels LL, Toribara NW, Kim YS, Lyftogt C, Cherwitz DL, Niehans GA. Mucin gene expression in normal, preneoplastic, and neoplastic human gastric epithelium. Cancer Res 1995; 55:2681–90.
  • Hollingsworth MA, Swanson BJ. Mucins in cancer: Protection and control of the cell surface. Nat Rev Cancer 2004; 4:45–60.
  • De Bolos C, Garrido M, Real FX. MUC6 apomucin shows a distinct normal tissue distribution that correlates with Lewis antigen expression in the human stomach. Gastroenterology 1995; 109:723–34.
  • Nordman H, Davies JR, Carlstedt I. Mucus glycoproteins from pig gastric mucosa: different mucins are produced by the surface epithelium and the glands. Biochem J 1998; 331:687–94.
  • Varki A. Essentials of glycobiology. Cold Spring Harbor, N.Y.: Cold Spring Harbor Laboratory Press, 2009.
  • Robbe C, Capon C, Coddeville B, Michalski JC. Structural diversity and specific distribution of O-glycans in normal human mucins along the intestinal tract. Biochem J 2004; 384:307–16.
  • Linden SK, Sutton P, Karlsson NG, Korolik V, McGuckin MA. Mucins in the mucosal barrier to infection. Mucosal Immunol 2008; 1:183–97.
  • Jin C, Kenny DT, Skoog EC, Padra M, Adamczyk B, Vitizeva V, Thorell A, Venkatakrishnan V, Linden SK, Karlsson NG. Structural diversity of human gastric mucin glycans. Molecular & cellular proteomics: MCP 2017; 16:743–758.
  • Perez-Perez GI, Rothenbacher D, Brenner H. Epidemiology of Helicobacter pylori infection. Helicobacter 2004; 9 Suppl 1:1–6.
  • Linden SK, Wickstrom C, Lindell G, Gilshenan K, Carlstedt I. Four modes of adhesion are used during Helicobacter pylori binding to human mucins in the oral and gastric niches. Helicobacter 2008; 13:81–93.
  • Borén T, Falk P, Roth KA, Larson G, Normark S. Attachment of Helicobacter pylori to human gastric epithelium mediated by blood group antigens. Science 1993; 262:1892–5.
  • Mahdavi J, Sonden B, Hurtig M, Olfat FO, Forsberg L, Roche N, Angstrom J, Larsson T, Teneberg S, Karlsson KA, et al. Helicobacter pylori SabA adhesin in persistent infection and chronic inflammation. Science 2002; 297:573–8.
  • Roche N, Angstrom J, Hurtig M, Larsson T, Boren T, Teneberg S. Helicobacter pylori and complex gangliosides. Infection and immunity 2004; 72:1519–29.
  • Senkovich OA, Yin J, Ekshyyan V, Conant C, Traylor J, Adegboyega P, McGee DJ, Rhoads RE, Slepenkov S, Testerman TL. Helicobacter pylori AlpA and AlpB bind host laminin and influence gastric inflammation in gerbils. Infection and immunity 2011; 79:3106–16.
  • Linden S, Nordman H, Hedenbro J, Hurtig M, Boren T, Carlstedt I. Strain- and blood group-dependent binding of Helicobacter pylori to human gastric MUC5AC glycoforms. Gastroenterology 2002; 123:1923–30.
  • Vermoote M, Vandekerckhove TT, Flahou B, Pasmans F, Smet A, De Groote D, Van Criekinge W, Ducatelle R, Haesebrouck F. Genome sequence of Helicobacter suis supports its role in gastric pathology. Veterinary research 2011; 42:51.
  • Snelling WJ, Moran AP, Ryan KA, Scully P, McGourty K, Cooney JC, Annuk H, O'Toole PW. HorB (HP0127) is a gastric epithelial cell adhesin. Helicobacter 2007; 12:200–9.
  • O'Toole PW, Janzon L, Doig P, Huang J, Kostrzynska M, Trust TJ. The putative neuraminyllactose-binding hemagglutinin HpaA of Helicobacter pylori CCUG 17874 is a lipoprotein. Journal of bacteriology 1995; 177:6049–57.
  • Quintana-Hayashi MP, Mahu M, De Pauw N, Boyen F, Pasmans F, Martel A, Premaratne P, Fernandez HR, Teymournejad O, Vande Maele L, et al. The levels of Brachyspira hyodysenteriae binding to porcine colonic mucins differ between individuals, and binding is increased to mucins from infected pigs with de novo MUC5AC synthesis. Infection and immunity 2015; 83:1610–9.
  • Linden S, Semino-Mora C, Liu H, Rick J, Dubois A. Role of mucin Lewis status in resistance to Helicobacter pylori infection in pediatric patients. Helicobacter 2010; 15:251–8.
  • Danon SJ, Lee A. Other Gastric Helicobacters and Spiral Organisms. In: Mobley HLT, Mendz GL, Hazell SL, eds. Helicobacter pylori: Physiology and Genetics. Washington (DC), 2001. Chapter 44.
  • Hellemans A, Chiers K, Decostere A, De Bock M, Haesebrouck F, Ducatelle R. Experimental infection of pigs with ‘Candidatus Helicobacter suis’. Veterinary research communications 2007; 31:385–95.
  • Buisine MP, Devisme L, Maunoury V, Deschodt E, Gosselin B, Copin MC, Aubert JP, Porchet N. Developmental mucin gene expression in the gastroduodenal tract and accessory digestive glands. I. Stomach. A relationship to gastric carcinoma. The journal of histochemistry and cytochemistry: official journal of the Histochemistry Society 2000; 48:1657–66.
  • Skoog EC, Sjoling A, Navabi N, Holgersson J, Lundin SB, Linden SK. Human gastric mucins differently regulate Helicobacter pylori proliferation, gene expression and interactions with host cells. PloS one 2012; 7:e36378.
  • Linden S, Mahdavi J, Hedenbro J, Boren T, Carlstedt I. Effects of pH on Helicobacter pylori binding to human gastric mucins: identification of binding to non-MUC5AC mucins. Biochem J 2004; 384:263–70.
  • Karlsson H, Halim A, Teneberg S. Differentiation of glycosphingolipid-derived glycan structural isomers by liquid chromatography/mass spectrometry. Glycobiology 2010; 20:1103–16.
  • Chai W, Piskarev V, Lawson AM. Negative-ion electrospray mass spectrometry of neutral underivatized oligosaccharides. Analytical chemistry 2001; 73:651–7.
  • Baele M, Decostere A, Vandamme P, Ceelen L, Hellemans A, Mast J, Chiers K, Ducatelle R, Haesebrouck F. Isolation and characterization of Helicobacter suis sp. nov. from pig stomachs. International journal of systematic and evolutionary microbiology 2008; 58:1350–8.
  • Celli JP, Turner BS, Afdhal NH, Keates S, Ghiran I, Kelly CP, Ewoldt RH, McKinley GH, So P, Erramilli S, et al. Helicobacter pylori moves through mucus by reducing mucin viscoelasticity. Proceedings of the National Academy of Sciences of the United States of America 2009; 106:14321–6.
  • Nordman H, Davies JR, Herrmann A, Karlsson NG, Hansson GC, Carlstedt I. Mucus glycoproteins from pig gastric mucosa: identification ofdifferent mucin populations from the surface epithelium. Biochem J 1997; 326 (Pt 3):903–10.
  • Aspholm-Hurtig M, Dailide G, Lahmann M, Kalia A, Ilver D, Roche N, Vikstrom S, Sjostrom R, Linden S, Backstrom A, et al. Functional adaptation of BabA, the H. pylori ABO blood group antigen binding adhesin. Science 2004; 305:519–22.
  • Turck D, Feste AS, Lifschitz CH. Age and Diet Affect the Composition of Porcine Colonic Mucins. Pediatr Res 1993; 33:564–7.
  • Benktander J, Angstrom J, Breimer ME, Teneberg S. Redefinition of the carbohydrate binding specificity of Helicobacter pylori BabA adhesin. The Journal of biological chemistry 2012; 287:31712–24.
  • Linden S, Mahdavi J, Semino-Mora C, Olsen C, Carlstedt I, Boren T, Dubois A. Role of ABO secretor status in mucosal innate immunity and H. pylori infection. PLoS Pathog 2008; 4:e2.
  • Bugaytsova JA, Bjornham O, Chernov YA, Gideonsson P, Henriksson S, Mendez M, Sjostrom R, Mahdavi J, Shevtsova A, Ilver D, et al. Helicobacter pylori Adapts to Chronic Infection and Gastric Disease via pH-Responsive BabA-Mediated Adherence. Cell host & microbe 2017; 21:376–89.
  • Linden SK, Sheng YH, Every AL, Miles KM, Skoog EC, Florin TH, Sutton P, McGuckin MA. MUC1 limits Helicobacter pylori infection both by steric hindrance and by acting as a releasable decoy. PLoS Pathog 2009; 5:e1000617.
  • Teneberg S, Leonardsson I, Karlsson H, Jovall PA, Angstrom J, Danielsson D, Naslund I, Ljungh A, Wadstrom T, Karlsson KA. Lactotetraosylceramide, a novel glycosphingolipid receptor for Helicobacter pylori, present in human gastric epithelium. The Journal of biological chemistry 2002; 277:19709–19.
  • Svennerholm L, Bostrom K, Fredman P, Mansson JE, Rosengren B, Rynmark BM. Human brain gangliosides: developmental changes from early fetal stage to advanced age. Biochimica et biophysica acta 1989; 1005:109–17.
  • Prieto PA, Smith DF. A new ganglioside in human meconium detected by antiserum against the human milk sialyloligosaccharide, LS-tetrasaccharide b. Archives of biochemistry and biophysics 1985; 241:281–9.
  • Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997; 25:3389–402.
  • Lang T, Hansson GC, Samuelsson T. Gel-forming mucins appeared early in metazoan evolution. Proceedings of the National Academy of Sciences of the United States of America 2007; 104:16209–14.
  • Karlsson NG, Wilson NL, Wirth HJ, Dawes P, Joshi H, Packer NH. Negative ion graphitised carbon nano-liquid chromatography/mass spectrometry increases sensitivity for glycoprotein oligosaccharide analysis. Rapid communications in mass spectrometry: RCM 2004; 18:2282–92.