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Copyright ©The Author(s) 2015. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Gastroenterol. Oct 28, 2015; 21(40): 11411-11427
Published online Oct 28, 2015. doi: 10.3748/wjg.v21.i40.11411
Tight junction disruption: Helicobacter pylori and dysregulation of the gastric mucosal barrier
Tyler J Caron, Kathleen E Scott, James G Fox, Susan J Hagen
Tyler J Caron, Kathleen E Scott, Susan J Hagen, Department of Surgery, Beth Israel Deaconess Medical Center and Harvard Medical School, Boston, MA 02215, United States
Tyler J Caron, Kathleen E Scott, James G Fox, Division of Comparative Medicine, Massachusetts Institute of Technology, Cambridge, MA 02139, United States
Author contributions: Caron TJ and Scott KE contributed equally to this work; all authors wrote or reviewed the article.
Supported by Department of Surgery funds, BIDMC and NIH No. P30 DK034854 (SJH), No. R01 CA093405, No. P30 ES002109, No. R01 OD011141, and No. P01 CA028842 (JGF); NIH No. T32 OD0109978 (JGF, to Dr. Caron and Dr. Scott).
Conflict-of-interest statement: The authors have no conflicts of interest.
Open-Access: This article is an open-access article which was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/
Correspondence to: Susan J Hagen, PhD, Department of Surgery, Beth Israel Deaconess Medical Center, E/RW-871, 330 Brookline Avenue, Boston, MA 01125, United States. shagen@bidmc.harvard.edu
Telephone: +1-617-6675308 Fax: +1-617-9755562
Received: May 11, 2015
Peer-review started: May 14, 2015
First decision: June 2, 2015
Revised: June 26, 2015
Accepted: September 30, 2015
Article in press: September 30, 2015
Published online: October 28, 2015
Processing time: 164 Days and 23.2 Hours
Abstract

Long-term chronic infection with Helicobacter pylori (H. pylori) is a risk factor for gastric cancer development. In the multi-step process that leads to gastric cancer, tight junction dysfunction is thought to occur and serve as a risk factor by permitting the permeation of luminal contents across an otherwise tight mucosa. Mechanisms that regulate tight junction function and structure in the normal stomach, or dysfunction in the infected stomach, however, are largely unknown. Although conventional tight junction components are expressed in gastric epithelial cells, claudins regulate paracellular permeability and are likely the target of inflammation or H. pylori itself. There are 27 different claudin molecules, each with unique properties that render the mucosa an intact barrier that is permselective in a way that is consistent with cell physiology. Understanding the architecture of tight junctions in the normal stomach and then changes that occur during infection is important but challenging, because most of the reports that catalog claudin expression in gastric cancer pathogenesis are contradictory. Furthermore, the role of H. pylori virulence factors, such as cytotoxin-associated gene A and vacoulating cytotoxin, in regulating tight junction dysfunction during infection is inconsistent in different gastric cell lines and in vivo, likely because non-gastric epithelial cell cultures were initially used to unravel the details of their effects on the stomach. Hampering further study, as well, is the relative lack of cultured cell models that have tight junction claudins that are consistent with native tissues. This summary will review the current state of knowledge about gastric tight junctions, normally and in H. pylori infection, and make predictions about the consequences of claudin reorganization during H. pylori infection.

Keywords: Helicobacter pylori; Tight junction; Claudins; Paracellular permeability; Stomach; Cytotoxin-associated gene A; Vacuolating cytotoxin; Lipopolysaccharide; Urease; Ammonia

Core tip: Tight junction dysfunction is a risk factor for cancer development during Helicobacter pylori (H. pylori) infection. The recent identification of numerous barrier-forming claudins has greatly improved our understanding of properties that regulate selective permeation across the tight junction in general, but little is known about the role of claudins in the stomach, or in H. pylori infection. In this article, we review the current state of knowledge on stomach tight junction composition and organization, discuss the details of claudin expression in various species and in cultured gastric cells, and discuss the implications of tight junction dysregulation in gastric cancer pathogenesis.