Helicobacter suis affects the health and function of porcine gastric parietal cells

Veterinary Research, Oct 2016

The stomach of pigs at slaughter age is often colonized by Helicobacter (H.) suis, which is also the most prevalent gastric non-H. pylori Helicobacter (NHPH) species in humans. It is associated with chronic gastritis, gastric ulceration and other gastric pathological changes in both hosts. Parietal cells are highly specialized, terminally differentiated epithelial cells responsible for gastric acid secretion and regulation. Dysfunction of these cells is closely associated with gastric pathology and disease. Here we describe a method for isolation and culture of viable and responsive parietal cells from slaughterhouse pigs. In addition, we investigated the interactions between H. suis and gastric parietal cells both in H. suis-infected six-month-old slaughter pigs, as well as in our in vitro parietal cell model. A close interaction of H. suis and parietal cells was observed in the fundic region of stomachs from H. suis positive pigs. The bacterium was shown to be able to directly interfere with cultured porcine parietal cells, causing a significant impairment of cell viability. Transcriptional levels of Atp4a, essential for gastric acid secretion, showed a trend towards an up-regulation in H. suis positive pigs compared to H. suis-negative pigs. In addition, sonic hedgehog, an important factor involved in gastric epithelial differentiation, gastric mucosal repair, and stomach homeostasis, was also significantly up-regulated in H. suis positive pigs. In conclusion, this study describes a successful approach for the isolation and culture of porcine gastric parietal cells. The results indicate that H. suis affects the viability and function of this cell type.

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Helicobacter suis affects the health and function of porcine gastric parietal cells

Zhang et al. Vet Res Helicobacter suis affects the health and function of porcine gastric parietal cells Guangzhi Zhang 1 2 5 Richard Ducatelle 1 5 Belgacem Mihi 3 4 Annemieke Smet 1 5 Bram Flahou 0 1 5 Freddy Haesebrouck 0 1 5 0 Bram Flahou and Freddy Haesebrouck shared senior authorship 1 Department of Pathology , Bacteriology and Avian Diseases , Faculty of Veterinary Medicine, Ghent University , Merelbeke , Belgium 2 Present Address: Department of Molecular and Cell Biology, University of California , Berkeley , USA 3 Present Address: Department of Immunol- ogy, Graduate School of Medicine, Chiba University , Chiba , Japan 4 Department of Virol- ogy, Parasitology and Immunology, Faculty of Veterinary Medicine, Ghent University , Merelbeke , Belgium 5 Department of Pathology , Bacteriology and Avian Diseases , Faculty of Veteri- nary Medicine, Ghent University , Merelbeke , Belgium The stomach of pigs at slaughter age is often colonized by Helicobacter (H.) suis, which is also the most prevalent gastric non-H. pylori Helicobacter (NHPH) species in humans. It is associated with chronic gastritis, gastric ulceration and other gastric pathological changes in both hosts. Parietal cells are highly specialized, terminally differentiated epithelial cells responsible for gastric acid secretion and regulation. Dysfunction of these cells is closely associated with gastric pathology and disease. Here we describe a method for isolation and culture of viable and responsive parietal cells from slaughterhouse pigs. In addition, we investigated the interactions between H. suis and gastric parietal cells both in H. suis-infected six-month-old slaughter pigs, as well as in our in vitro parietal cell model. A close interaction of H. suis and parietal cells was observed in the fundic region of stomachs from H. suis positive pigs. The bacterium was shown to be able to directly interfere with cultured porcine parietal cells, causing a significant impairment of cell viability. Transcriptional levels of Atp4a, essential for gastric acid secretion, showed a trend towards an up-regulation in H. suis positive pigs compared to H. suis-negative pigs. In addition, sonic hedgehog, an important factor involved in gastric epithelial differentiation, gastric mucosal repair, and stomach homeostasis, was also significantly up-regulated in H. suis positive pigs. In conclusion, this study describes a successful approach for the isolation and culture of porcine gastric parietal cells. The results indicate that H. suis affects the viability and function of this cell type. - Introduction Helicobacter (H.) suis is a Gram-negative bacterium with a typical spiral-shaped morphology, which frequently colonizes the stomach of pigs as well as a minority of humans [1–3]. Indeed, gastric non-H. pylori helicobacters (NHPH) are found in 0.2–6% of gastric biopsies, depending on the study [4], and H. suis is considered to be the most prevalent NHPH in humans [3–5]. In humans, infection with H. suis has been described to cause gastritis, gastric ulceration, as well as gastric mucosa-associated lymphoid tissue (MALT) lymphoma and sporadically gastric adenocarcinoma [6–8]. In naturally infected or experimentally infected pigs, H. suis infection has been shown to cause gastritis, reduced daily weight gain and other gastric pathological changes [9, 10]. The gastric mucosa is composed of various cell types. Parietal (oxyntic) cells are abundant in the fundic gland region. They are responsible for the secretion of gastric acid and play a vital role in the maintenance of the normal structure and function of the gastric mucosa [11]. In some species, including humans, pigs, rabbits and cats, parietal cells can also secrete intrinsic factor which plays an important role in the absorption of vitamins and other nutrients by the small intestine [12]. Hydrogen potassium ATPase (H+/K+ ATPase) is the proton pump composed of a catalytic subunit (α-subunit) and an accessory subunit (β-subunit) in parietal cells, and it mediates secretion of acid into the gastric lumen [11]. Various studies have shown that atrophic gastritis induced by H. pylori infection is characterized by the dysfunction or loss of parietal cells [13, 14]. While H. pylori is mainly observed in the mucus layer or close to mucus-producing cells, H. © 2016 The Author(s). This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/ publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. suis is often observed near or even inside the canaliculi of pariet (...truncated)


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Guangzhi Zhang, Richard Ducatelle, Belgacem Mihi, Annemieke Smet, Bram Flahou, Freddy Haesebrouck. Helicobacter suis affects the health and function of porcine gastric parietal cells, Veterinary Research, 2016, pp. 101, 47, DOI: 10.1186/s13567-016-0386-1