A comparison of Helicobacter pylori and non-Helicobacter pylori Helicobacter spp. Binding to Canine Gastric Mucosa with Defined Gastric Glycophenotype

Helicobacter

Volumn 19, Issue 4, 2014, Pages 249-259

  Amorim, Irina ^a   Freitas, Daniela P ^a   Magalhães, Ana ^a   Faria, Fátima ^a   Lopes, Célia ^a   Faustino, Augusto M ^a   Smet, Annemieke ^b   Haesebrouck, Freddy ^b   Reis, Celso A ^a,c   Gärtner, Fátima ^a  

^a UNIVERSITY OF PORTO   (Portugal)

^b GHENT UNIVERSITY   (Belgium)

^c Institute of Histology and Embryology   (Portugal)

Author keywords

Bacterial adhesion; Canine gastric mucosa; Helicobacter pylori; Histo blood group antigens; Non Helicobacter pylori helicobacters

Indexed keywords

BLOOD GROUP A ANTIGEN; BLOOD GROUP ANTIGEN; FLUORESCEIN ISOTHIOCYANATE; HISTOCOMPATIBILITY ANTIGEN; POLYSACCHARIDE;

ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; BACTERIAL STRAIN; BACTERIUM ADHERENCE; BLOOD GROUP LEWIS SYSTEM; CONTROLLED STUDY; DOG; GLYCOSYLATION; HELICOBACTER; HELICOBACTER HEILMANNII; HELICOBACTER PYLORI; IN VITRO STUDY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; STOMACH MUCOSA; ANIMAL; CHEMISTRY; MICROBIOLOGY; PHYSIOLOGY;

ANIMALS; BACTERIAL ADHESION; DOGS; GASTRIC MUCOSA; GLYCOSYLATION; HELICOBACTER; HISTOCOMPATIBILITY ANTIGENS; POLYSACCHARIDES;

EID: 84904629577     PISSN: 10834389     EISSN: 15235378     Source Type: Journal    
DOI: 10.1111/hel.12125     Document Type: Article

References (57)

1. Geyer C, Colbatzky F, Lechner J, Hermanns W. Occurrence of spiral-shaped bacteria in gastric biopsies of dogs and cats. Vet Rec 1993;133:18-9.
2. Hermanns W, Kregel K, Breuer W, Lechner J. Helicobacter-like organisms: Histopathological examination of gastric biopsies from dogs and cats. J Comp Pathol 1995;112:307-18.
3. Lecoindre P, Chevallier M, Peyrol S, Boude M, De Montclos H. Contribution à l'étude des hélicobactéries de l'éstomac du chien et de leur role pathogène. Revue Médicine Véterinaire 1995;146:671-80.
4. Hwang CY, Han HR, Youn HY. Prevalence and clinical characterization of gastric Helicobacter species infection in dogs and cats in Korea. J Vet Sci 2002;3:123-33.
5. Polanco R, Salazar V, Reyes N, García-Amado MA, Michelangeli F, Contreras M. High prevalence of DNA from non-H. pylori helicobacters in the gastric mucosa of Venezuelan pet dogs and its histological alterations. Rev Inst Med Trop Sao Paulo 2011;53:207-12.
6. Henry GA, Long PH, Burns JL, Charbonneau DL. Gastric spirillosis in beagles. Am J Vet Res 1987;48:831-6.
7. Eaton KA, Dewhirst FE, Paster BJ, Tzellas N, Coleman BE, Paola J, Sherding R. Prevalence and varieties of Helicobacter species in dogs from random sources and pet dogs: animal and public health implications. J Clin Microbiol 1996;34:3165-70.
8. Simpson KW, Strauss-Ayali D, McDonough PL, Chang YF, Valentine BA. Gastric function in dogs with naturally acquired gastric Helicobacter species infection. J Vet Intern Med 1999;13:507-15.
9. Van den Bulck K, Decostere A, Baele M, Vandamme P, Mast J, Ducatelle R, Haesebrouck F. Helicobacter cynogastricus sp. nov., isolated from the canine gastric mucosa. Int J Syst Evol Microbiol 2006;6:1559-64.
10. Baele M, Pasmans F, Flahou B, Chiers K, Ducatelle R, Haesebrouck F. Non-Helicobacter pylori helicobacters detected in the stomach of humans comprise several naturally occurring Helicobacter species in animals. FEMS Immunol Med Microbiol 2009;55:306-13.
11. Haesebrouck F, Pasmans F, Flahou B, Chiers K, Baele M, Meyns T, Decostere A, Ducatelle R. Gastric helicobacters in domestic animals and nonhuman primates and their significance for human health. Clin Microbiol Rev 2009;22:202-23.
12. Haesebrouck F, Pasmans F, Flahou B, Smet A, Vandamme P, Ducatelle R. Non-Helicobacter pylori Helicobacter species in the human gastric mucosa: a proposal to introduce the terms H. heilmannii sensu lato and sensu stricto. Helicobacter 2011;16:339-40.
13. kman E, Fredriksson M, Trowald-Wigh G. Helicobacter spp. in the saliva, stomach, duodenum and faeces of colony dogs. Vet J 2013;195:127-9.
14. Taulescu M, Catoi C, Gal A, Bolfa P, Rus VI, Budugan M, Tabaran F, Nagy A. Diagnosis of spontaneous gastric infection with Helicobacter species in dogs using PCR method. Lucrari stiintifice USAMV Iasi Med Vet 2009;52:304-10.
15. Chung TH, Kim HD, Lee YS, Hwang CY. Determination of the prevalence of helicobacter heilmannii-like organisms type 2 (HHLO-2) infection in humans and dogs using non-invasive genus/species-specific PCR in Korea. J Vet Med Sci 2013;76:73-9.
16. Ilver D, Arnqvist A, Ogren J, Frick IM, Kersulyte D, Incecik ET, Berg DE, Covacci A, Engstrand L, Borén T. Helicobacter pylori adhesin binding fucosylated histo-blood group antigens revealed by retagging. Science 1998;16:373-7.
17. Mahdavi J, Sondén B, Hurtig M, et al. Helicobacter pylori SabA adhesin in persistent infection and chronic inflammation. Science 2002;297:573-8.
18. Magalhães A, Reis CA. Helicobacter pylori adhesion to gastric epithelial cells is mediated by glycan receptors. Braz J Med Biol Res 2010;43:611-8.
19. Reis CA, Osorio H, Silva L, Gomes C, David L. Alterations in glycosylation as biomarkers for cancer detection. J Clin Pathol 2010;6:322-9.
20. Magalhães A, Ismail MN, Reis AC. Sweet receptors mediate the adhesion of the gastric pathogen Helicobacter pylori: glycoproteomic strategies. Expert Rev Proteomics 2010;7:307-10.
21. Azevedo M, Eriksson S, Mendes N, et al. Infection by Helicobacter pylori expressing the BabA adhesin is influenced by the secretor phenotype. J Pathol 2008;215:308-16.
22. Magalhães A, Gomes J, Ismail MN, et al. Fut2-null mice display an altered glycosylation profile and impaired BabA-mediated Helicobacter pylori adhesion to gastric mucosa. Glycobiology 2009;19:1532-6.
23. Mollicone R, Bara J, Le Pendu J, Oriol R. 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 Invest 1985;53:219-27.
24. Ikehara Y, Nishihara S, Yasutomi H, et al. 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 2001;10:971-7.
25. Lee HS, Choe G, Kim WH, Kim HH, Song J, Park KU. Expression of Lewis antigens and their precursors in gastric mucosa: relationship with Helicobacter pylori infection and gastric carcinogenesis. J Pathol 2006;209:88-94.
26. Ota H, Nakayama J, Momose M, Hayama M, Akamatsu T, Katsuyama T, Graham DY, Genta RM. Helicobacter pylori infection produces reversible glycosylation changes to gastric mucins. Virchows Arch 1998;433:419-26.
27. Marcos NT, Magalhães A, Ferreira B, et al. Helicobacter pylori induces beta3GnT5 in human gastric cell lines, modulating expression of the SabA ligand sialyl-Lewis x. J Clin Invest 2008;118:2325-36.
28. Zweibaum A, Oudea P, Halpern B, Veyre C. Presence in colic glandular cells of various mammalian species of an antigen cross-reacting with human blood group A substance. Nature 1966;8:159-61.
29. Zweibaum A, Oriol R, Feingold N, Dussaulx E, Rousset M, Chevalier G. Studies on canine secretory alloantigens (CSA). Tissue Antigens 1974;4:115-29.
30. Oriol R, Strecker G, Rousset M, Chevalier G, Dalix AM, Dussaulx E, Zweibaum A. Determination of the structure of the immunodominant groups of the canine secretory alloantigens (CSA) by radioimmunoassay. Transplant Proc 1975;7:523-8.
31. Prachasilpchail W, Nuanualsuwan S, Chatsuwan T, Techangamsuwan S, Wangnaitham S, Sailasuta A. Diagnosis of Helicobacter spp. infection in canine stomach. J Vet Sci 2007;8:139-45.
32. Falk P, Roth KA, Bor'en T, Westblom TU, Gordon JI, Normark S. An in vitro adherence assay reveals that Helicobacter pylori exhibits cell lineagespecific tropism in the human gastric epithelium. Proc Natl Acad Sci USA 1993;90:2035-9.
33. Aspholm M, Olfat FO, Nord'en J, et al. SabA is the H. pylori hemagglutinin and is polymorphic in binding to sialylated glycans. PLoS Pathog 2006;2:e110.
34. Smet A, Flahou B, D'Herde K, Vandamme P, Cleenwerck I, Ducatelle R, Pasmans F, Haesebrouck F. Helicobacter heilmannii sp. nov., isolated from feline gastric mucosa. Int J Syst Evol Microbiol 2012;62(Pt 2):299-306.
35. López-Ferrer A, De Bolós C, Barranco C, Garrido M, Isern J, Carlstedt I, Reis CA, Torrado J, Real FX. Role of fucosyltransferases in the association between apomucin and Lewis antigen expression in normal and malignant gastric epithelium. Gut 2000;47:349-56.
36. Teixeira A, David L, Reis CA, Costa J, Sobrinho-Simões M. 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 2002;197:37-43.
37. De Bolòs 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.
38. Moran AP. Relevance of fucosylation and Lewis antigen expression in the bacterial gastroduodenal pathogen Helicobacter pylori. Carbohydr Res 2008;343:1952-65.
39. Smith EL, McKibbin JM, Karlsson KA, Pascher I, Samuelsson BE. Characterization by mass spectrometry of blood group A active glycolipids from human and dog small intestines. Biochemistry 1975;14:2120-4.
40. Kuhlmann WD, Peschke P, Wurster K. Lectin-peroxidase conjugates in histopathology of gastrointestinal mucosa. Virchows Arch A Pathol Anat Histopathol 1983;398:319-28.
41. Oriol R, Mollicone R, Cailleau A, Balanzino L, Breton C. Divergent evolution of fucosyltransferase genes from vertebrates, invertebrates, and bacteria. Glycobiology 1999;9:323-34.
42. Dupuy F, Petit JM, Mollicone R, Oriol R, Julien R, Maftah A. A single amino acid in the hypervariable stem domain of vertebrate alpha1, 3/1, 4-fucosyltransferases determines the type 1/type 2 transfer. Characterization of acceptor substrate specificity of the lewis enzyme by site-directed mutagenesis. J Biol Chem 1999;274:12257-62.
43. Tegtmeyer N, Rivas Traverso F, Rohde M, Oyarzabal OA, Lehn N, Schneider-Brachert W, Ferrero RL, Fox JG, Berg DE, Backert S. Electron microscopic, genetic and protein expression analyses of Helicobacter acinonychis strains from a Bengal tiger. PLoS One 2013;8:e71220.
44. O'Toole PW, Snelling WJ, Canchaya C, et al. Comparative genomics and proteomics of Helicobacter mustelae, an ulcerogenic and carcinogenic gastric pathogen. BMC Genomics 2010;11:164.
45. Schott T, Kondadi PK, Hänninen ML, Rossi M. Comparative genomics of Helicobacter pylori and the human-derived Helicobacter bizzozeronii CIII-1 strain reveal the molecular basis of the zoonotic nature of non-pylori gastric Helicobacter infections in humans. BMC Genomics 2011;12:534.
46. 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. Vet Res 2011;42:51.
47. Smet A, Van Nieuwerburgh F, Ledesma J, Flahou B, Deforce D, Ducatelle R, Haesebrouck F. Genome sequence of Helicobacter heilmannii sensu stricto ASB1 isolated from the gastric mucosa of a kitten with severe gastritis. Genome Announc 2013;1:1-2.
48. Joosten M, Blaecher C, Flahou B, Ducatelle R, Haesebrouck F, Smet A. Diversity in bacterium-host interactions within the species Helicobacter heilmannii sensu stricto. Vet Res 2013;44:65.
49. Yamasaki K, Suematsu H, Takahashi T. Comparison of gastric lesions in dogs and cats with and without gastric spiral organisms. J Am Vet Med Assoc 1998;212:529-33.
50. Anacleto TP, Lopes LR, Andreollo NA, Bernis Filho WO, Resck MC, Macedo A. Studies of distribution and recurrence of Helicobacter spp. gastric mucosa of dogs after triple therapy. Acta Cir Bras 2011;26:82-7.
51. Cattoli G, van Vugt R, Zanoni RG, Sanguinetti V, Chiocchetti R, Gualtieri M, Vandenbroucke-Grauls CM, Gaastra W, Kusters JG. Occurrence and characterization of gastric Helicobacter spp. in naturally infected dogs. Vet Microbiol 1999;70:239-50.
52. Buczolits S, Hirt R, Rosengarten R, Busse HJ. PCR-based genetic evidence for occurrence of Helicobacter pylori and novel Helicobacter species in the canine gastric mucosa. Vet Microbiol 2003;95:259-70.
53. Recordati C, Gualdi V, Craven M, Sala L, Luini M, Lanzoni A, Rishniw M, Simpson KW, Scanziani E. Spatial distribution of Helicobacter spp. in the gastrointestinal tract of dogs. Helicobacter 2009;14:180-91.
54. Gombač M, Švara T, Černe M, Pogačnik M. Histological changes in stomachs of apparently healthy dogs infected with Helicobacter. Acta Vet (Beogr) 2010;60:173-82.
55. Young WW Jr, Portoukalian J, Hakomori S. Two monoclonal anticarbohydrate antibodies directed to glycosphingolipids with a laco-N-glyosil type II chain. J Biol Chem 1981;256:10967-72.
56. Fukushi Y, Hakomori S, Nudelman E, Cochran N. Novel fucolipids accumulating in human adenocarcinoma. II. Selective isolation of hybridoma antibodies that differentially recognize mono-, di-, and trifucosylated type 2 chain. J Biol Chem 1984;259:4681-5.
57. Abe K, McKibbin JM, Hakamori S. The monoclonal antibody directed to difucosylated type 2 chain (Fuc alpha 1 leads to 2Gal beta 1 leads to 4[Fuc alpha 1 leads to 3]GlcNAc; Y Determinant). J Biol Chem 1983;258:11793-7.