Host-pathogen interaction between Helicobacter pylori and biliary cells mediated by sialic acid receptor

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Prissadee Thanaphongdecha
Yaovalux Chamgramol
Chawalit Pairojkul
Raksawan Deenonpoe
Sutas Suttiprapa
Banchob Sripa

Abstract

Commensalism involving H. pylori and O. viverrini may have evolved and may facilitate conveyance of the bacillus into human bile duct. The adherence between bacterial ligands and host receptor is an initial step in colonization of H. pylori in bile duct epithelium leading to disease pathogenesis. We investigated tissue adhesion of FITC-labelled H. pylori on normal, pre-cancerous and cancerous bile duct epithelium from 42 cholangiocarcinoma (CCA) cases. The results revealed that all cases exhibited different degrees of the bacterial adhesion. Quantitatively, normal and pre-cancerous bile duct epithelium showed significantly higher number of H. pylori adhesion per area than those of CCA tissue (p-value < 0.001). The mechanism by which H. pylori binds to the bile duct epithelium was then explored. A H. pylori adhesin, specifically sialic acid-binding adhesin (SabA) which recognizes sialyl-Lewis X glycan receptor was studied in human normal cholangiocytes (H69 cell line). The results revealed that the number of FITC-labelled H. pylori adhesion was significantly decreased after blocking with wheat germ agglutinin (WGA) which binds to sialic acid (p-value < 0.05) but not with
Ulex eropaeus agglutinin I (UEA I) which is specific for alpha-L-fucose. Pretreatment of H69 cells with antibody to sialyl-Lewis X resulted in significantly decreased adhesion of H. pylori-in a dose dependent manner, particularly at a dilution of 1:200 (p-value < 0.005) and 1:1000 (p-value < 0.05). The results clearly show that H. pylori can colonize on the bile duct epithelium and sialyl-Lewis X may be a receptor for the adhesion. 

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1.
Thanaphongdecha P, Chamgramol Y, Pairojkul C, Deenonpoe R, Suttiprapa S, Sripa B. Host-pathogen interaction between Helicobacter pylori and biliary cells mediated by sialic acid receptor. Arch AHS [Internet]. 2022 Apr. 22 [cited 2024 Dec. 19];34(1):21-8. Available from: https://he01.tci-thaijo.org/index.php/ams/article/view/252721
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References

Sripa B, Kaewkes S, Sithithaworn P, Mairiang E, Laha T, Smout M, et al. Liver fluke induces cholangiocarcinoma. PLoS Med 2007; 4(7): e201.

Khuntikeo N, Titapun A, Loilome W, Yongvanit P, Thinkhamrop B, Chamadol N, et al. Current perspectives on opisthorchiasis control and cholangiocarcinoma detection in Southeast Asia. Front Med (Lausanne) 2018; 5: 117.

Deenonpoe R, Chomvarin C, Pairojkul C, Chamgramol Y, Loukas A, Brindley PJ, et al. The carcinogenic liver fluke Opisthorchis viverrini is a reservoir for species of Helicobacter. Asian Pac J Cancer Prev 2015; 16(5): 1751-8.

Deenonpoe R, Mairiang E, Mairiang P, Pairojkul C, Chamgramol Y, Rinaldi G, et al. Elevated prevalence of Helicobacter species and virulence factors in opisthorchiasis and associated hepatobiliary disease. Sci Rep 2017; 7: 42744.

Sripa B, Deenonpoe R, Brindley PJ. Co-infections with liver fluke and Helicobacter species: A paradigm change in pathogenesis of opisthorchiasis and cholangiocarcinoma? Parasitol Int 2017; 66(4): 383-9.

Boonyanugomol W, Chomvarin C, Song JY, Kim KM, Kim JM, Cho MJ, et al. Effects of Helicobacter pylori gamma-glutamyltranspeptidase on apoptosis and inflammation in human biliary cells. Dig Dis Sci 2012; 57(10): 2615-24.

Boonyanugomol W, Chomvarin C, Sripa B, Bhudhisawasdi V, Khuntikeo N, Hahnvajanawong C, et al. Helicobacter pylori in Thai patients with cholangiocarcinoma and its association with biliary inflammation and proliferation. HPB (Oxford) 2012; 14(3): 177-84.

Plieskatt JL, Deenonpoe R, Mulvenna JP, Krause L, Sripa B, Bethony JM, et al. Infection with the carcinogenic liver fluke Opisthorchis viverrini modifies intestinal and biliary microbiome. FASEB J 2013; 27(11): 4572-84.

Boonyanugomol W, Chomvarin C, Hahnvajanawong C, Sripa B, Kaparakis-Liaskos M, Ferrero RL. 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 2013; 8(10): e77358.

Hatakeyama M. Helicobacter pylori CagA and gastric cancer: a paradigm for hit-and-run carcinogenesis. Cell Host Microbe 2014; 15(3): 306-16.

Kalali B, Mejias-Luque R, Javaheri A, Gerhard M. H. pylori virulence factors: influence on immune system and pathology. Mediators Inflamm 2014; 2014: 426309.

Kao CY, Sheu BS, Wu JJ. Helicobacter pylori infection: An overview of bacterial virulence factors and pathogenesis. Biomed J 2016; 39(1): 14-23.

Matos R, Amorim I, Magalhaes A, Haesebrouck F, Gartner F, Reis CA. Adhesion of Helicobacter species to the human gastric mucosa: A deep look into glycans role. Front Mol Biosci 2021; 8: 656439.

Ilver D, Arnqvist A, Ogren J, Frick IM, Kersulyte D, Incecik ET, et al. Helicobacter pylori adhesin binding fucosylated histo-blood group antigens revealed by retagging. Science 1998; 279(5349): 373-7.

Aspholm-Hurtig M, Dailide G, Lahmann M, Kalia A, Ilver D, Roche N, et al. Functional adaptation of BabA, the H. pylori ABO blood group antigen binding adhesin. Science 2004; 305(5683): 519-22.

Fagoonee S, Pellicano R. Helicobacter pylori: molecular basis for colonization and survival in gastric environment and resistance to antibiotics. A short review. Infect Dis (Lond) 2019; 51(6): 399-408.

Sasaki M, Nakanuma Y, Shimizu K, Izumi R. Pathological and immunohistochemical findings in a case of mucinous cholangiocarcinoma. Pathol Int 1995; 45(10): 781-6.

Rhodes JM, Hubscher S, Black R, Elias E, Savage A. Lectin histochemistry of the liver in biliary disease, following transplantation and in cholangiocarcinoma. J Hepatol 1988; 6(3): 277-82.

Indramanee S, Silsirivanit A, Pairojkul C, Wongkham C, Wongkham S. Aberrant glycosylation in cholangiocarcinoma demonstrated by lectin-histochemistry. Asian Pac J Cancer Prev 2012; 13: 119-24.

Saito K, Nakanuma Y. Lectin binding of intrahepatic bile ducts and peribiliary glands in normal livers and hepatolithiasis. Tohoku J Exp Med 1990; 160(1): 81-92.

Falk P KA, Boren T, Westblom T. ULF , Gordon JI, Normark S. An in vitro adherence assay reveals that Helicobacter pylor exhibits cell lineage-specific tropism in the human gastric epithelium. Microbiology 1993; 90: 2035-9.

Suyapoh W, Tirnitz-Parker JEE, Tangkawattana S, Suttiprapa S, Sripa B. Biliary migration, colonization, and pathogenesis of O. viverrini co-infected with CagA+ Helicobacter pylori. Pathogens 2021; 10(9).

Chmiela M, Kupcinskas J. Review: Pathogenesis of Helicobacter pylori infection. Helicobacter 2019; 24(1): e12638.

Mahdavi J, Sonden B, Hurtig M, Olfat FO, Forsberg L, Roche N, et al. Helicobacter pylori SabA adhesin in persistent infection and chronic inflammation. Science 2002; 297(5581): 573-8.

Hynes SO, Hirmo S, Wadstrom T, Moran AP. Differentiation of Helicobacter pylori isolates based on lectin binding of cell extracts in an agglutination assay. J Clin Microbiol 1999; 37(6): 1994-8.

Phillips SG, Lui SL, Phillips DM. Binding of epithelial cells to lectin-coated surfaces. In Vitro 1982; 18(8): 727-38.

Sandoval-Bernal G, Barbosa-Sabanero G, Shibayama M, Perez-Torres A, Tsutsumi V, Sabanero M. Cell wall glycoproteins participate in the adhesion of Sporothrix schenckii to epithelial cells. Mycopathologia 2011; 171(4): 251-9.

Gallagher JE, George G, Brody AR. Sialic acid mediates the initial binding of positively charged inorganic particles to alveolar macrophage membranes. Am Rev Respir Dis 1987; 135(6): 1345-52.

Keilberg D, Ottemann KM. How Helicobacter pylori senses, targets and interacts with the gastric epithelium. Environ Microbiol 2016; 18(3): 791-806.

Wroblewski LE, Peek RM, Jr., Wilson KT. Helicobacter pylori and gastric cancer: factors that modulate disease risk. Clin Microbiol Rev 2010; 23(4): 713-39.

Thanaphongdecha P, Karinshak SE, Ittiprasert W, Mann VH, Chamgramol Y, Pairojkul C, et al. Infection with Helicobacter pylori induces epithelial to mesenchymal transition in human cholangiocytes. Pathogens 2020; 9(11).