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Glycosyltransferases and Gastric Cancer

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Glycosignals in Cancer: Mechanisms of Malignant Phenotypes

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Abstract

The present chapter describes the pattern of glycosylation and the functional role of glycans in gastric tissues. The mechanisms of biosynthesis of gastric cell oligosaccharide chains and the glycosyltransferases involved in these processes are discussed in normal and pathological settings.

Particular focus is given to the glycosyltransferases controlling the biosynthesis of the fucosylated and sialylated histo-blood group antigens that act as receptors for the outer membrane adhesins of the gastric pathogenic bacteria Helicobacter pylori.

This chapter also addresses the glycosylation alterations and the underlying molecular mechanisms occurring during the gastric carcinogenic pathways, including the expression of simple mucin-type carbohydrate antigens, such as sialyl-Tn.

Moreover, the frequent glycosylation modifications observed in gastric carcinoma, the glycosyltransferases regulating important cancer cell adhesion molecules and signaling pathways, and the glycan-mediated modulation of cell biological functions are also discussed.

The decoding of the functional role of glycans in gastric cells may constitute the basis for defining biomarkers with potential to improve diagnosis and prognosis, contributing for stratification of patients and the development of better therapies.

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References

  • Amado M, Carneiro F, Seixas M, Clausen H, Sobrinho-Simoes M (1998) Dimeric sialyl-Le(x) expression in gastric carcinoma correlates with venous invasion and poor outcome. Gastroenterology 114(3):462–470

    Article  CAS  PubMed  Google Scholar 

  • Aspholm-Hurtig M, Dailide G, Lahmann M, Kalia A, Ilver D, Roche N, Vikstrom S, Sjostrom R, Linden S, Backstrom A, Lundberg C, Arnqvist A, Mahdavi J, Nilsson UJ, Velapatino B, Gilman RH, Gerhard M, Alarcon T, Lopez-Brea M, Nakazawa T, Fox JG, Correa P, Dominguez-Bello MG, Perez-Perez GI, Blaser MJ, Normark S, Carlstedt I, Oscarson S, Teneberg S, Berg DE, Boren T (2004) Functional adaptation of BabA, the H. pylori ABO blood group antigen binding adhesin. Science 305(5683):519–522. doi:10.1126/science.1098801

    Article  CAS  PubMed  Google Scholar 

  • Azevedo M, Eriksson S, Mendes N, Serpa J, Figueiredo C, Resende LP, Ruvoën-Clouet N, Haas R, Borén T, Pendu JL, David L (2008) Infection by Helicobacter pylori expressing the BabA adhesin is influenced by the secretor phenotype. J Pathol 215(3):308–316

    Article  CAS  PubMed  Google Scholar 

  • Bellis SL (2004) Variant glycosylation: an underappreciated regulatory mechanism for β1 integrins. Biochim Biophys Acta Biomembr 1663(1–2):52–60. doi:10.1016/j.bbamem.2004.03.012

    Article  CAS  Google Scholar 

  • Bennett EP, Hassan H, Mandel U, Mirgorodskaya E, Roepstorff P, Burchell J, Taylor-Papadimitriou J, Hollingsworth MA, Merkx G, van Kessel AG, Eiberg H, Steffensen R, Clausen H (1998) Cloning of a human UDP-N-acetyl-alpha-D-Galactosamine:polypeptide N-acetylgalactosaminyltransferase that complements other GalNAc-transferases in complete O-glycosylation of the MUC1 tandem repeat. J Biol Chem 273(46):30472–30481

    Article  CAS  PubMed  Google Scholar 

  • Bennett EP, Mandel U, Clausen H, Gerken TA, Fritz TA, Tabak LA (2012) Control of mucin-type O-glycosylation: a classification of the polypeptide GalNAc-transferase gene family. Glycobiology 22(6):736–756. doi:10.1093/glycob/cwr182

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bierhuizen MF, Maemura K, Fukuda M (1994) Expression of a differentiation antigen and poly-N-acetyllactosaminyl O-glycans directed by a cloned core 2 beta-1,6-N-acetylglucosaminyltransferase. J Biol Chem 269(6):4473–4479

    CAS  PubMed  Google Scholar 

  • Bones J, Byrne JC, O’Donoghue N, McManus C, Scaife C, Boissin H, Nastase A, Rudd PM (2011) Glycomic and glycoproteomic analysis of serum from patients with stomach cancer reveals potential markers arising from host defense response mechanisms. J Proteome Res 10(3):1246–1265. doi:10.1021/pr101036b

    Article  CAS  PubMed  Google Scholar 

  • Boren T, Falk P, Roth KA, Larson G, Normark S (1993) Attachment of Helicobacter pylori to human gastric epithelium mediated by blood group antigens. Science 262(5141):1892–1895. doi:10.1126/science.8018146

    Article  CAS  PubMed  Google Scholar 

  • Brockhausen I (1999) Pathways of O-glycan biosynthesis in cancer cells. Biochim Biophys Acta Gen Subj 1473(1):67–95. doi:10.1016/S0304-4165(99)00170-1

    Article  CAS  Google Scholar 

  • Campos D, Freitas D, Gomes J, Magalhães A, Steentoft C, Gomes C, Vester-Christensen MB, Ferreira JA, Afonso LP, Santos LL, Pinto de Sousa J, Mandel U, Clausen H, Vakhrushev SY, Reis CA (2015) Probing the O-glycoproteome of gastric cancer cell lines for biomarker discovery. Mol Cell Proteomics 14(6):1616–1629. doi:10.1074/mcp.M114.046862

    Article  CAS  PubMed  Google Scholar 

  • Carvalho AS, Harduin-Lepers A, Magalhães A, Machado E, Mendes N, Costa LT, Matthiesen R, Almeida R, Costa J, Reis CA (2010) Differential expression of α-2,3-sialyltransferases and α-1,3/4-fucosyltransferases regulates the levels of sialyl Lewis a and sialyl Lewis x in gastrointestinal carcinoma cells. Int J Biochem Cell Biol 42(1):80–89. doi:10.1016/j.biocel.2009.09.010

    Article  CAS  PubMed  Google Scholar 

  • Clausen H, Bennett EP (1996) A family of UDP-GalNAc: polypeptide N-acetylgalactosaminyl-transferases control the initiation of mucin-type O-linked glycosylation. Glycobiology 6(6):635–646

    Article  CAS  PubMed  Google Scholar 

  • Corso G, Carvalho J, Marrelli D, Vindigni C, Carvalho B, Seruca R, Roviello F, Oliveira C (2013) Somatic mutations and deletions of the E-Cadherin gene predict poor survival of patients with gastric cancer. J Clin Oncol 31(7):868–875. doi:10.1200/jco.2012.44.4612

    Article  CAS  PubMed  Google Scholar 

  • Ferreira B, Marcos NT, David L, Nakayama J, Reis CA (2006) Terminal alpha1,4-linked N-acetylglucosamine in Helicobacter pylori-associated intestinal metaplasia of the human stomach and gastric carcinoma cell lines. J Histochem Cytochem 54(5):585–591. doi:10.1369/jhc.5A6836.2006

    Article  CAS  PubMed  Google Scholar 

  • Gao Y, Liu Z, Feng J, Sun Q, Zhang B, Zheng W, Ma W (2013) Expression pattern of polypeptide N-acetylgalactosaminyltransferase-10 in gastric carcinoma. Oncol lett 5(1):113–116. doi:10.3892/ol.2012.980

    PubMed Central  PubMed  Google Scholar 

  • Gomes J, Marcos NT, Berois N, Osinaga E, Magalhaes A, Pinto-de-Sousa J, Almeida R, Gartner F, Reis CA (2009) Expression of UDP-N-acetyl-D-galactosamine: polypeptide N-acetylgalactosaminyltransferase-6 in gastric mucosa, intestinal metaplasia, and gastric carcinoma. J Histochem Cytochem 57(1):79–86. doi:10.1369/jhc.2008.952283

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gomes C, Almeida A, Ferreira JA, Silva L, Santos-Sousa H, Pinto-de-Sousa J, Santos LL, Amado F, Schwientek T, Levery SB, Mandel U, Clausen H, David L, Reis CA, Osório H (2013a) Glycoproteomic analysis of serum from patients with gastric precancerous lesions. J Proteome Res 12(3):1454–1466. doi:10.1021/pr301112x

    Article  CAS  PubMed  Google Scholar 

  • Gomes C, Osorio H, Pinto MT, Campos D, Oliveira MJ, Reis CA (2013b) Expression of ST3GAL4 leads to SLe(x) expression and induces c-Met activation and an invasive phenotype in gastric carcinoma cells. PLoS ONE 8(6):e66737. doi:10.1371/journal.pone.0066737

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gu J, Taniguchi N (2004) Regulation of integrin functions by N-glycans. Glycoconj J 21(1–2):9–15. doi:10.1023/b:glyc.0000043741.47559.30

    Article  CAS  PubMed  Google Scholar 

  • Guilford P, Hopkins J, Harraway J, McLeod M, McLeod N, Harawira P, Taite H, Scoular R, Miller A, Reeve AE (1998) E-cadherin germ line mutations in familial gastric cancer. Nature 392(6674):402–405

    Article  CAS  PubMed  Google Scholar 

  • Guzman-Murillo MA, Ruiz-Bustos E, Ho BOW, Ascencio F (2001) Involvement of the heparan sulphate-binding proteins of Helicobacter pylori in its adherence to HeLa S3 and Kato III cell lines. J Med Microbiol 50(4):320–329

    Article  CAS  PubMed  Google Scholar 

  • Harduin-Lepers A (2010) Comprehensive analysis of sialyltransferases in vertebrate genomes. Glycobiol Insights 2010(2):29–61. doi:10.4137/gbi.s3123, 1870-GBI-Comprehensive-Analysis-of-Sialyltransferases-in-Vertebrate-Genomes.pdf

    Article  Google Scholar 

  • Harduin-Lepers A, Mollicone R, Delannoy P, Oriol R (2005) The animal sialyltransferases and sialyltransferase-related genes: a phylogenetic approach. Glycobiology 15(8):805–817. doi:10.1093/glycob/cwi063

    Article  CAS  PubMed  Google Scholar 

  • Harduin-Lepers A, Krzewinski-Recchi MA, Colomb F, Foulquier F, Groux-Degroote S, Delannoy P (2012) Sialyltransferases functions in cancers. Front Biosci (Elite Ed) 4:499–515

    Article  Google Scholar 

  • Hassan H, Reis CA, Bennett EP, Mirgorodskaya E, Roepstorff P, Hollingsworth MA, Burchell J, Taylor-Papadimitriou J, Clausen H (2000) The lectin domain of UDP-N-acetyl-D-galactosamine: polypeptide N-acetylgalactosaminyltransferase-T4 directs its glycopeptide specificities. J Biol Chem 275(49):38197–38205. doi:10.1074/jbc.M005783200

    Article  CAS  PubMed  Google Scholar 

  • Holgersson J, Löfling J (2006) Glycosyltransferases involved in type 1 chain and Lewis antigen biosynthesis exhibit glycan and core chain specificity. Glycobiology 16(7):584–593. doi:10.1093/glycob/cwj090

    Article  CAS  PubMed  Google Scholar 

  • Hua D, Shen L, Xu L, Jiang Z, Zhou Y, Yue A, Zou S, Cheng Z, Wu S (2012) Polypeptide N-acetylgalactosaminyltransferase 2 regulates cellular metastasis-associated behavior in gastric cancer. Int J Mol Med 30(6):1267–1274. doi:10.3892/ijmm.2012.1130

    PubMed Central  CAS  PubMed  Google Scholar 

  • Huesca M, Borgia S, Hoffman P, Lingwood CA (1996) Acidic pH changes receptor binding specificity of Helicobacter pylori: a binary adhesion model in which surface heat shock (stress) proteins mediate sulfatide recognition in gastric colonization. Infect Immun 64(7):2643–2648

    PubMed Central  CAS  PubMed  Google Scholar 

  • Ikehara Y, Nishihara S, Yasutomi H, Kitamura T, Matsuo K, Shimizu N, Inada K-i, Kodera Y, Yamamura Y, Narimatsu H, Hamajima N, Tatematsu M (2001) Polymorphisms of two fucosyltransferase genes (lewis and secretor genes) involving type I lewis antigens are associated with the presence of anti-Helicobacter pylori IgG antibody. Cancer Epidemiol Biomarkers Prev 10(9):971–977

    CAS  PubMed  Google Scholar 

  • Ilver D, Arnqvist A, Ogren J, Frick I-M, Kersulyte D, Incecik ET, Berg DE, Covacci A, Engstrand L, Boren T (1998) Helicobacter pylori adhesin binding fucosylated histo-blood group antigens revealed by retagging. Science 279(5349):373–377. doi:10.1126/science.279.5349.373

    Article  CAS  PubMed  Google Scholar 

  • Ju T, Lanneau GS, Gautam T, Wang Y, Xia B, Stowell SR, Willard MT, Wang W, Xia JY, Zuna RE, Laszik Z, Benbrook DM, Hanigan MH, Cummings RD (2008) Human tumor antigens Tn and sialyl Tn arise from mutations in Cosmc. Cancer Res 68(6):1636–1646. doi:10.1158/0008-5472.can-07-2345

    Article  CAS  PubMed  Google Scholar 

  • Kawakubo M, Ito Y, Okimura Y, Kobayashi M, Sakura K, Kasama S, Fukuda MN, Fukuda M, Katsuyama T, Nakayama J (2004) Natural antibiotic function of a human gastric mucin against Helicobacter pylori infection. Science 305(5686):1003–1006. doi:10.1126/science.1099250

    Article  CAS  PubMed  Google Scholar 

  • Kelly RJ, Rouquier S, Giorgi D, Lennon GG, Lowe JB (1995) Sequence and expression of a candidate for the human secretor blood group α(1,2)Fucosyltransferase Gene (FUT2). J Biol Chem 270(9):4640–4649. doi:10.1074/jbc.270.9.4640

    Article  CAS  PubMed  Google Scholar 

  • Lee HS, Choe G, Kim WH, Kim HH, Song J, Park KU (2006) Expression of Lewis antigens and their precursors in gastric mucosa: relationship with Helicobacter pylori infection and gastric carcinogenesis. J Pathol 209(1):88–94. doi:10.1002/path.1949

    Article  CAS  PubMed  Google Scholar 

  • Linden S, Nordman H, Hedenbro J, Hurtig M, Thoma B, Carlstedt I (2002) Strain-and blood group dependent binding of Helicobacter pylori to human gastric MUC5AC glycoforms. Gastroenterology 123(6):1923–1930

    Article  CAS  PubMed  Google Scholar 

  • Lindén S, Mahdavi J, Semino-Mora C, Olsen C, Carlstedt I, Borén T, Dubois A (2008) Role of ABO secretor status in mucosal innate immunity and H. pylori infection. PLoS Pathog 4(1):e2

    Article  PubMed Central  PubMed  Google Scholar 

  • Liu Y, Koda Y, Soejima M, Pang H, Schlaphoff T, du Toit ED, Kimura H (1998) Extensive polymorphism of the FUT2 gene in an African (Xhosa) population of South Africa. Hum Genet 103(2):204–210. doi:10.1007/s004390050808

    Article  CAS  PubMed  Google Scholar 

  • Lopez-Ferrer A, de Bolos C, Barranco C, Garrido M, Isern J, Carlstedt I, Reis CA, Torrado J, Real FX (2000) Role of fucosyltransferases in the association between apomucin and Lewis antigen expression in normal and malignant gastric epithelium. Gut 47(3):349–356

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Magalhaes A, Gomes J, Ismail MN, Haslam SM, Mendes N, Osorio H, David L, Le Pendu J, Haas R, Dell A, Boren T, Reis CA (2009a) Fut2-null mice display an altered glycosylation profile and impaired BabA-mediated Helicobacter pylori adhesion to gastric mucosa. Glycobiology 19(12):1525–1536. doi:10.1093/glycob/cwp131

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Magalhaes A, Marcos NT, Carvalho AS, David L, Figueiredo C, Bastos J, David G, Reis CA (2009b) Helicobacter pylori cag pathogenicity island-positive strains induce syndecan-4 expression in gastric epithelial cells. FEMS Immunol Med Microbiol 56(3):223–232

    Article  CAS  PubMed  Google Scholar 

  • Magalhães A, Marcos-Pinto R, Nairn AV, Dela Rosa M, Ferreira RM, Junqueira-Neto S, Freitas D, Gomes J, Oliveira P, Santos MR, Marcos NT, Xiaogang W, Figueiredo C, Oliveira C, Dinis-Ribeiro M, Carneiro F, Moremen KW, David L, Reis CA (2015) Helicobacter pylori chronic infection and mucosal inflammation switches the human gastric glycosylation pathways. Biochim Biophys Acta 1852(9):1928–1939. doi:10.1016/j.bbadis.2015.07.001

    Article  PubMed Central  PubMed  Google Scholar 

  • Mahdavi J, Sonden B, Hurtig M, Olfat FO, Forsberg L, Roche N, Angstrom J, Larsson T, Teneberg S, Karlsson K-A, Altraja S, Wadstrom T, Kersulyte D, Berg DE, Dubois A, Petersson C, Magnusson K-E, Norberg T, Lindh F, Lundskog BB, Arnqvist A, Hammarstrom L, Boren T (2002) Helicobacter pylori SabA adhesin in persistent infection and chronic inflammation. Science 297(5581):573–578. doi:10.1126/science.1069076

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Marcos NT, Cruz A, Silva F, Almeida R, David L, Mandel U, Clausen H, Von Mensdorff-Pouilly S, Reis CA (2003) Polypeptide GalNAc-transferases, ST6GalNAc-transferase I, and ST3Gal-transferase I expression in gastric carcinoma cell lines. J Histochem Cytochem 51(6):761–771

    Article  CAS  PubMed  Google Scholar 

  • Marcos NT, Pinho S, Grandela C, Cruz A, Samyn-Petit B, Harduin-Lepers A, Almeida R, Silva F, Morais V, Costa J, Kihlberg J, Clausen H, Reis CA (2004) Role of the human ST6GalNAc-I and ST6GalNAc-II in the synthesis of the cancer-associated sialyl-Tn antigen. Cancer Res 64(19):7050–7057. doi:10.1158/0008-5472.can-04-1921

    Article  CAS  PubMed  Google Scholar 

  • Marcos NT, Magalhães A, Ferreira B, Oliveira M, Carvalho A, Mendes N, Gilmartin T, Head S, Figueiredo C, David L, Santos-Silva F, Reis C (2008) Helicobacter pylori induces beta3GnT5 in human gastric cell lines, modulating expression of the SabA ligand sialyl-Lewis x. J Clin Invest 118(6):12

    Google Scholar 

  • Marcos NT, Bennett EP, Gomes J, Magalhaes A, Gomes C, David L, Dar I, Jeanneau C, DeFrees S, Krustrup D, Vogel LK, Kure EH, Burchell J, Taylor-Papadimitriou J, Clausen H, Mandel U, Reis CA (2011) ST6GalNAc-I controls expression of sialyl-Tn antigen in gastrointestinal tissues. Front Biosci (Elite Ed) 3:1443–1455

    Google Scholar 

  • Miyoshi E, Moriwaki K, Nakagawa T (2008) Biological function of fucosylation in cancer biology. J Biochem 143(6):725–729. doi:10.1093/jb/mvn011

    Article  CAS  PubMed  Google Scholar 

  • Mollicone R, Bara J, Le Pendu J, Oriol R (1985) Immunohistologic pattern of type 1 (Lea, Leb) and type 2 (X, Y, H) blood group-related antigens in the human pyloric and duodenal mucosae. Lab Investig 53(2):9

    Google Scholar 

  • Nakamori S, Nishihara S, Ikehara Y, Nagano H, Dono K, Sakon M, Narimatsu H, Monden M (1999) Molecular mechanism involved in increased expression of sialyl Lewis antigens in ductal carcinoma of the pancreas. J Exp Clin Cancer Res 18(3):425–432

    CAS  PubMed  Google Scholar 

  • Namavar F, Sparrius M, Veerman ECI, Appelmelk BJ, Vandenbroucke-Grauls CMJE (1998) Neutrophil-activating protein mediates adhesion of Helicobacter pylori to sulfated carbohydrates on high-molecular-weight salivary mucin. Infect Immun 66(2):444–447

    PubMed Central  CAS  PubMed  Google Scholar 

  • Nordman H, Davies JR, Lindell G, de Bolós C, Real F, Carlstedt I (2002) Gastric MUC5AC and MUC6 are large oligomeric mucins that differ in size, glycosylation and tissue distribution. Biochem J 364(1):191–200

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ohno T, Vallström A, Rugge M, Ota H, Graham DY, Arnqvist A, Yamaoka Y (2011) Effects of blood group antigen–binding adhesin expression during Helicobacter pylori infection of mongolian gerbils. J Infect Dis 203(5):726–735. doi:10.1093/infdis/jiq090

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ota H, Nakayama J, Momose M, Hayama M, Akamatsu T, Katsuyama T, Graham DY, Genta RM (1998) Helicobacter pylori infection produces reversible glycosylation changes to gastric mucins. Virchows Arch 433(5):419–426

    Article  CAS  PubMed  Google Scholar 

  • Pang SS, Nguyen ST, Perry AJ, Day CJ, Panjikar S, Tiralongo J, Whisstock JC, Kwok T (2013) The three-dimensional structure of the extracellular adhesion domain of the sialic acid-binding adhesin SabA from Helicobacter pylori. J Biol Chem. doi:10.1074/jbc.M113.513135

    Google Scholar 

  • Paredes J, Figueiredo J, Albergaria A, Oliveira P, Carvalho J, Ribeiro AS, Caldeira J, Costa AM, Simões-Correia J, Oliveira MJ, Pinheiro H, Pinho SS, Mateus R, Reis CA, Leite M, Fernandes MS, Schmitt F, Carneiro F, Figueiredo C, Oliveira C, Seruca R (2012) Epithelial E-and P-cadherins: role and clinical significance in cancer. Biochim Biophys Acta Rev on Cancer 1826(2):297–311. doi:10.1016/j.bbcan.2012.05.002

    Article  CAS  Google Scholar 

  • Pedersen JW, Bennett EP, Schjoldager KT, Meldal M, Holmer AP, Blixt O, Clo E, Levery SB, Clausen H, Wandall HH (2011) Lectin domains of polypeptide GalNAc transferases exhibit glycopeptide binding specificity. J Biol Chem 286(37):32684–32696. doi:10.1074/jbc.M111.273722

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pinho SS, Reis CA (2015) Glycosylation in cancer: mechanisms and clinical implications. Nat Rev Cancer 15(9):540–555. doi:10.1038/nrc3982

    Article  CAS  PubMed  Google Scholar 

  • Pinho SS, Figueiredo J, Cabral J, Carvalho S, Dourado J, Magalhães A, Gärtner F, Mendonça AM, Isaji T, Gu J, Carneiro F, Seruca R, Taniguchi N, Reis CA (2013) E-cadherin and adherens-junctions stability in gastric carcinoma: functional implications of glycosyltransferases involving N-glycan branching biosynthesis, N-acetylglucosaminyltransferases III and V. Biochim Biophys Acta Gen Subj 1830(3):2690–2700. doi:10.1016/j.bbagen.2012.10.021

    Article  CAS  Google Scholar 

  • Pinto R, Carvalho AS, Conze T, Magalhaes A, Picco G, Burchell JM, Taylor-Papadimitriou J, Reis CA, Almeida R, Mandel U, Clausen H, Soderberg O, David L (2012) Identification of new cancer biomarkers based on aberrant mucin glycoforms by in situ proximity ligation. J Cell Mol Med 16(7):1474–1484. doi:10.1111/j.1582-4934.2011.01436.x

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Reis CA, David L, Nielsen PA, Clausen H, Mirgorodskaya K, Roepstorff P, Sobrinho-Simões M (1997) Immunohistochemical study of MUC5AC expression in human gastric carcinomas using a novel monoclonal antibody. Int J Cancer 74(1):112–121

    Article  CAS  PubMed  Google Scholar 

  • Reis CA, David L, Seixas M, Burchell J, Sobrinho-Simoes M (1998) Expression of fully and under-glycosylated forms of MUC1 mucin in gastric carcinoma. Int J Cancer 79(4):402–410

    Article  CAS  PubMed  Google Scholar 

  • Reis CA, David L, Correa P, Carneiro F, Cd B, Garcia E, Mandel U, Clausen H, Sobrinho-Simoes M (1999) Intestinal metaplasia of human stomach displays distinct patterns of mucin (MUC1, MUC2, MUC5AC, and MUC6) expression. Cancer Res 59(5):1003–1007

    CAS  PubMed  Google Scholar 

  • Reis CA, David L, Carvalho F, Mandel U, de Bolos C, Mirgorodskaya E, Clausen H, Sobrinho-Simoes M (2000) Immunohistochemical study of the expression of MUC6 mucin and co-expression of other secreted mucins (MUC5AC and MUC2) in human gastric carcinomas. J Histochem Cytochem 48(3):377–388

    Article  CAS  PubMed  Google Scholar 

  • Rossez Y, Maes E, Lefebvre Darroman T, Gosset P, Ecobichon C, Joncquel Chevalier Curt M, Boneca IG, Michalski JC, Robbe-Masselot C (2012) Almost all human gastric mucin O-glycans harbor blood group A, B or H antigens and are potential binding sites for Helicobacter pylori. Glycobiology 22(9):1193–1206. doi:10.1093/glycob/cws072

    Article  CAS  PubMed  Google Scholar 

  • Rossez Y, Gosset P, Boneca IG, Magalhães A, Ecobichon C, Reis CA, Cieniewski-Bernard C, Joncquel Chevalier Curt M, Léonard R, Maes E, Sperandio B, Slomianny C, Sansonetti PJ, Michalski JC, Robbe-Masselot C (2014) The lacdiNAc-specific adhesin LabA mediates adhesion of Helicobacter pylori to human gastric mucosa. J Infect Dis 210(8):1286–1295. doi:10.1093/infdis/jiu239

    Article  CAS  PubMed  Google Scholar 

  • Ruiz-Bustos E, Ochoa JL, Wadstrom T, Ascencio F (2001) Isolation and characterisation of putative adhesins from Helicobacter pylori with affinity for heparan sulphate proteoglycan. J Med Microbiol 50(3):215–222

    Article  CAS  PubMed  Google Scholar 

  • Salama NR, Hartung ML, Muller A (2013) Life in the human stomach: persistence strategies of the bacterial pathogen Helicobacter pylori. Nat Rev Microbiol 11(6):385–399. doi:10.1038/nrmicro3016

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sasaki K, Watanabe E, Kawashima K, Sekine S, Dohi T, Oshima M, Hanai N, Nishi T, Hasegawa M (1993) Expression cloning of a novel Gal beta (1-3/1-4) GlcNAc alpha 2,3-sialyltransferase using lectin resistance selection. J Biol Chem 268(30):22782–22787

    CAS  PubMed  Google Scholar 

  • Schwientek T, Nomoto M, Levery SB, Merkx G, van Kessel AG, Bennett EP, Hollingsworth MA, Clausen H (1999) Control of O-Glycan branch formation: molecular cloning of human cDNA encoding a novel β1,6-N-acetylglucosaminyltransferase forming core 2 and core 4. J Biol Chem 274(8):4504–4512. doi:10.1074/jbc.274.8.4504

    Article  CAS  PubMed  Google Scholar 

  • Soejima M, Nakajima T, Fujihara J, Takeshita H, Koda Y (2008) Genetic variation of FUT2 in Ovambos, Turks, and Mongolians. Transfusion 48(7):1423–1431. doi:10.1111/j.1537-2995.2008.01710.x

    Article  CAS  PubMed  Google Scholar 

  • Teixeira A, David L, Reis CA, Costa J, Sobrinho-Simões M (2002) Expression of mucins (MUC1, MUC2, MUC5AC, and MUC6) and type 1 Lewis antigens in cases with and without Helicobacter pylori colonization in metaplastic glands of the human stomach. J Pathol 197(1):37–43

    Article  PubMed  Google Scholar 

  • Ten Hagen KG, Fritz TA, Tabak LA (2003) All in the family: the UDP-GalNAc:polypeptide N-acetylgalactosaminyltransferases. Glycobiology 13(1):1R–16R. doi:10.1093/glycob/cwg007

    Article  PubMed  Google Scholar 

  • Van de Bovenkamp JH, Mahdavi J, Korteland-Van Male AM, Buller HA, Einerhand AW, Boren T, Dekker J (2003) The MUC5AC glycoprotein is the primary receptor for Helicobacter pylori in the human stomach. Helicobacter 8(5):521–532

    Article  PubMed  Google Scholar 

  • Van den Brink GR, Tytgat KMAJ, Van der Hulst RWM, Van der Loos CM, Einerhand AWC, Buller HA, Dekker J (2000) H. pylori colocalises with MUC5AC in the human stomach. Gut 46(5):601–607. doi:10.1136/gut.46.5.601

    Article  PubMed Central  PubMed  Google Scholar 

  • Wandall HH, Hassan H, Mirgorodskaya E, Kristensen AK, Roepstorff P, Bennett EP, Nielsen PA, Hollingsworth MA, Burchell J, Taylor-Papadimitriou J, Clausen H (1997) Substrate specificities of three members of the human UDP-N-acetyl-alpha-D-galactosamine:polypeptide N-acetylgalactosaminyltransferase family, GalNAc-T1, −T2, and -T3. J Biol Chem 272(38):23503–23514

    Article  CAS  PubMed  Google Scholar 

  • Wandall HH, Irazoqui F, Tarp MA, Bennett EP, Mandel U, Takeuchi H, Kato K, Irimura T, Suryanarayanan G, Hollingsworth MA, Clausen H (2007) The lectin domains of polypeptide GalNAc-transferases exhibit carbohydrate-binding specificity for GalNAc: lectin binding to GalNAc-glycopeptide substrates is required for high density GalNAc-O-glycosylation. Glycobiology 17(4):374–387. doi:10.1093/glycob/cwl082

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Ju T, Ding X, Xia B, Wang W, Xia L, He M, Cummings RD (2010) Cosmc is an essential chaperone for correct protein O-glycosylation. Proc Natl Acad Sci USA 107(20):9228–9233. doi:10.1073/pnas.0914004107

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wroblewski LE, Peek RM, Wilson KT (2010) Helicobacter pylori and gastric cancer: factors that modulate disease risk. Clin Microbiol Rev 23(4):713–739. doi:10.1128/cmr.00011-10

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Institute for Research and Innovation in Health (i3S) & Institute of Molecular Pathology and Immunology of the University of Porto (IPATIMUP), Porto, Portugal

    Celso A. Reis & Ana Magalhães

  2. Medical Faculty of the University of Porto (FMUP), Porto, Portugal

    Celso A. Reis

  3. Institute of Biomedical Sciences of Abel Salazar (ICBAS), University of Porto, Porto, Portugal

    Celso A. Reis

Authors
  1. Celso A. Reis
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  2. Ana Magalhães
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Correspondence to Celso A. Reis .

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Editors and Affiliations

  1. Biomedical Sciences, Chubu University, Kasugai, Japan

    Koichi Furukawa

  2. Glycobiology Unit, Sanford-Burnham Med Res Inst, La Jolla, California, USA

    Minoru Fukuda

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Reis, C.A., Magalhães, A. (2016). Glycosyltransferases and Gastric Cancer. In: Furukawa, K., Fukuda, M. (eds) Glycosignals in Cancer: Mechanisms of Malignant Phenotypes . Springer, Tokyo. https://doi.org/10.1007/978-4-431-55939-9_2

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