Hostname: page-component-cd9895bd7-jn8rn Total loading time: 0 Render date: 2024-12-27T10:03:12.688Z Has data issue: false hasContentIssue false
  • English
  • Français

Adherence of Helicobacter pylori to Opisthorchis viverrini gut epithelium and the tegument mediated via L-fucose binding adhesin

Published online by Cambridge University Press:  29 April 2022

Prissadee Thanaphongdecha ,
Yaovalux Chamgramol ,
Chawalit Pairojkul ,
Raksawan Deenonpoe ,
Sutas Suttiprapa Open the ORCID record for Sutas Suttiprapa [Opens in a new window] ,
Paul J. Brindley  and
Banchob Sripa Open the ORCID record for Banchob Sripa [Opens in a new window]
Prissadee Thanaphongdecha
Affiliation:
Tropical Disease Research Center, Faculty of Medicine, Khon Kaen University, Khon Kaen 40002, Thailand Department of Pathology, Faculty of Medicine, Khon Kaen University, Khon Kaen 40002, Thailand
Yaovalux Chamgramol
Affiliation:
Department of Pathology, Faculty of Medicine, Khon Kaen University, Khon Kaen 40002, Thailand
Chawalit Pairojkul
Affiliation:
Department of Pathology, Faculty of Medicine, Khon Kaen University, Khon Kaen 40002, Thailand
Raksawan Deenonpoe
Affiliation:
Department of Pathology, Faculty of Medicine, Khon Kaen University, Khon Kaen 40002, Thailand
Sutas Suttiprapa
Affiliation:
Tropical Disease Research Center, Faculty of Medicine, Khon Kaen University, Khon Kaen 40002, Thailand
Paul J. Brindley
Affiliation:
Department of Microbiology, Immunology and Tropical Medicine, and Research Center for Neglected Tropical Diseases of Poverty, School of Medicine & Health Sciences, The George Washington University, Washington DC 20037, USA
Banchob Sripa*
Affiliation:
Tropical Disease Research Center, Faculty of Medicine, Khon Kaen University, Khon Kaen 40002, Thailand Department of Pathology, Faculty of Medicine, Khon Kaen University, Khon Kaen 40002, Thailand
*
Author for correspondence: Banchob Sripa, E-mail: banchob@kku.ac.th
Get access Rights & Permissions [Opens in a new window]

Abstract

Recent reports implicate both the liver fluke Opisthorchis viverrini as a reservoir of Helicobacter pylori within the human gastrointestinal tract and H. pylori in the pathogenesis of opisthorchiasis-associated cholangiocarcinoma. We postulated that adherence of bacterial ligands to host receptors initiates colonization of the live fluke by H. pylori and here we aimed to assess the molecular interaction between O. viverrini and H. pylori by investigating host receptors for H. pylori in the fluke. Several known receptors of H. pylori including Lewis B, sialyl-Lewis X, Toll-like receptor 4 and L-fucose were detected immunohistochemically and histochemically by focusing analysis on the gut epithelium and tegument of the adult stage of the fluke. The frequency of detection of Lewis B, sialyl-Lewis X, TLR4 and L-fucose in 100 individual worms was 3, 3, 19 and 70%, respectively. Detection of H. pylori by a diagnostic ureA gene-based PCR assay revealed the presence of H. pylori in individual O. viverrini worms in 41 of 49 (79%) worms examined. In addition, numbers of bacteria decreased in a dose- and time-dependent fashion following exposure to fucosidase. These findings suggested that L-fucose represents a tractable receptor for H. pylori that can mediate bacterial colonization of the gut of O. viverrini.

Keywords

Glycan receptorsHelicobacter pylorihost–pathogen interactionsL-fucoseOpisthorchis viverrini
Type
Research Article
Information
Parasitology , Volume 149 , Special Issue 10: Foodborne Trematodes – time to rise from neglected status , September 2022 , pp. 1374 - 1379
Check for updates
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

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 and Boren, T (2004) Functional adaptation of BabA, the H. pylori ABO blood group antigen binding adhesin. Science 305, 519–522.CrossRefGoogle Scholar
Backert, S, Neddermann, M, Maubach, G and Naumann, M (2016) Pathogenesis of Helicobacter pylori infection. Helicobacter 21(Suppl 1), 19–25.CrossRefGoogle ScholarPubMed
Boonyanugomol, W, Chomvarin, C, Sripa, B, Bhudhisawasdi, V, Khuntikeo, N, Hahnvajanawong, C and Chamsuwan, A (2012) Helicobacter pylori in Thai patients with cholangiocarcinoma and its association with biliary inflammation and proliferation. HPB 14, 177–184.CrossRefGoogle ScholarPubMed
Boonyanugomol, W, Chomvarin, C, Hahnvajanawong, C, Sripa, B, Kaparakis-Liaskos, M and Ferrero, RL (2013) Helicobacter pylori cag pathogenicity island (cagPAI) involved in bacterial internalization and IL-8 induced responses via NOD1- and MyD88-dependent mechanisms in human biliary epithelial cells. PLoS ONE 8, e77358.CrossRefGoogle ScholarPubMed
Chmiela, M and Kupcinskas, J (2019) Review: pathogenesis of Helicobacter pylori infection. Helicobacter 24(Suppl 1), e12638.CrossRefGoogle ScholarPubMed
Dangtakot, R, Pinlaor, S, Itthitaetrakool, U, Chaidee, A, Chomvarin, C, Sangka, A, Wilailuckana, C and Pinlaor, P (2017) Coinfection with Helicobacter pylori and Opisthorchis viverrini enhances the severity of hepatobiliary abnormalities in hamsters. Infection and Immunity 85, e00009-17.CrossRefGoogle ScholarPubMed
Dangtakot, R, Intuyod, K, Chamgramol, Y, Pairojkul, C, Pinlaor, S, Jantawong, C, Pongking, T, Haonon, O, Ma, N and Pinlaor, P (2021) CagA(+) Helicobacter pylori infection and N-nitrosodimethylamine administration induce cholangiocarcinoma development in hamsters. Helicobacter 26, e12817.CrossRefGoogle ScholarPubMed
Deenonpoe, R, Chomvarin, C, Pairojkul, C, Chamgramol, Y, Loukas, A, Brindley, PJ and Sripa, B (2015) The carcinogenic liver fluke Opisthorchis viverrini is a reservoir for species of Helicobacter. Asian Pacific Journal of Cancer Prevention: APJCP 16, 1751–1758.CrossRefGoogle ScholarPubMed
Deenonpoe, R, Mairiang, E, Mairiang, P, Pairojkul, C, Chamgramol, Y, Rinaldi, G, Loukas, A, Brindley, PJ and Sripa, B (2017) Elevated prevalence of Helicobacter species and virulence factors in opisthorchiasis and associated hepatobiliary disease. Scientific Reports 7, 42744.CrossRefGoogle ScholarPubMed
Dheilly, NM, Bolnick, D, Bordenstein, S, Brindley, PJ, Figueres, C, Holmes, EC, Martinez Martinez, J, Phillips, AJ, Poulin, R and Rosario, K (2017) Parasite microbiome project: systematic investigation of microbiome dynamics within and across parasite-host interactions. mSystems 2, e00050-17.CrossRefGoogle ScholarPubMed
Fagoonee, S and Pellicano, R (2019) Helicobacter pylori: molecular basis for colonization and survival in gastric environment and resistance to antibiotics. A short review. Infectious Diseases 51, 399–408.CrossRefGoogle ScholarPubMed
Falk, P, Roth, KA, Boren, T, Westblom, TU, Gordon, JI and Normark, S (1993) An in vitro adherence assay reveals that Helicobacter pylori exhibits cell lineage-specific tropism in the human gastric epithelium. Proceedings of the National Academy of Sciences of the USA 90, 2035–2039.CrossRefGoogle Scholar
Hatakeyama, M (2014) Helicobacter pylori CagA and gastric cancer: a paradigm for hit-and-run carcinogenesis. Cell Host & Microbe 15, 306–316.CrossRefGoogle ScholarPubMed
Ilver, D, Arnqvist, A, Ogren, J, Frick, IM, Kersulyte, D, Incecik, ET, Berg, DE, Covacci, A, Engstrand, L and Boren, T (1998) Helicobacter pylori adhesin binding fucosylated histo-blood group antigens revealed by retagging. Science 279, 373–377.CrossRefGoogle ScholarPubMed
Kao, CY, Sheu, BS and Wu, JJ (2016) Helicobacter pylori infection: an overview of bacterial virulence factors and pathogenesis. Biomedical Journal 39, 14–23.CrossRefGoogle ScholarPubMed
Mahdavi, J, Sonden, B, Hurtig, M, Olfat, FO, Forsberg, L, Roche, N, Angstrom, J, Larsson, T, Teneberg, S, Karlsson, KA, Altraja, S, Wadstrom, T, Kersulyte, D, Berg, DE, Dubois, A, Petersson, C, Magnusson, KE, Norberg, T, Lindh, F, Lundskog, BB, Arnqvist, A, Hammarstrom, L and Boren, T (2002) Helicobacter pylori SabA adhesin in persistent infection and chronic inflammation. Science 297, 573–578.CrossRefGoogle ScholarPubMed
Matos, R, Amorim, I, Magalhaes, A, Haesebrouck, F, Gartner, F and Reis, CA (2021) Adhesion of Helicobacter species to the human gastric mucosa: a deep look into glycans role. Frontiers in Molecular Biosciences 8, 656439.CrossRefGoogle Scholar
Pachathundikandi, SK, Tegtmeyer, N and Backert, S (2013) Signal transduction of Helicobacter pylori during interaction with host cell protein receptors of epithelial and immune cells. Gut Microbes 4, 454–474.CrossRefGoogle ScholarPubMed
Plieskatt, JL, Deenonpoe, R, Mulvenna, JP, Krause, L, Sripa, B, Bethony, JM and Brindley, PJ (2013) Infection with the carcinogenic liver fluke Opisthorchis viverrini modifies intestinal and biliary microbiome. FASEB Journal 27, 4572–4584.CrossRefGoogle ScholarPubMed
Sripa, B, Deenonpoe, R and Brindley, PJ (2017) Co-infections with liver fluke and Helicobacter species: a paradigm change in pathogenesis of opisthorchiasis and cholangiocarcinoma? Parasitology International 66, 383–389.CrossRefGoogle ScholarPubMed
Suyapoh, W, Tirnitz-Parker, JEE, Tangkawattana, S, Suttiprapa, S and Sripa, B (2021) Biliary migration, colonization, and pathogenesis of O. viverrini co-infected with CagA+Helicobacter pylori. Pathogens 10, 1089.CrossRefGoogle Scholar
Talabnin, K, Aoki, K, Saichua, P, Wongkham, S, Kaewkes, S, Boons, GJ, Sripa, B and Tiemeyer, M (2013) Stage-specific expression and antigenicity of glycoprotein glycans isolated from the human liver fluke, Opisthorchis viverrini. International Journal for Parasitology 43, 37–50.CrossRefGoogle ScholarPubMed