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A Novel Human Gastric Primary Cell Culture System for Modelling Gut Online First, published on December 24, 2014 as 10.1136/gutjnl-2014-307949 Helicobacter pylori ORIGINAL ARTICLE Gut: first published as 10.1136/gutjnl-2014-307949 on 24 December 2014. Downloaded from A novel human gastric primary cell culture system for modelling Helicobacter pylori infection in vitro Philipp Schlaermann,1 Benjamin Toelle,1 Hilmar Berger,1 Sven C Schmidt,2 Matthias Glanemann,2 Jürgen Ordemann,3 Sina Bartfeld,1,4 Hans J Mollenkopf,1 Thomas F Meyer1 ▸ Additional material is ABSTRACT published online only. To view Background and aims Helicobacter pylori is the Significance of this study please visit the journal online (http://dx.doi.org/10.1136/ causative agent of gastric diseases and the main risk factor gutjnl-2014-307949). in the development of gastric adenocarcinoma. In vitro studies with this bacterial pathogen largely rely on the use 1Department of Molecular What is already known on this subject? Biology, Max Planck Institute of transformed cell lines as infection model. However, this ▸ Helicobacter pylori infects over half of the for Infection Biology, Berlin, approach is intrinsically artificial and especially world’s population and can cause Germany inappropriate when it comes to investigating the fl 2 in ammation, peptic ulcers and ultimately lead Clinics for General, Visceral mechanisms of cancerogenesis. Moreover, common cell to gastric cancer. and Transplant Surgery, Charité ▸ H. pylori University Medicine, Berlin, lines are often defective in crucial signalling pathways Illuminating the molecular basis of - Germany relevant to infection and cancer. A long-lived primary cell induced carcinogenesis has been hampered by 3Center of Bariatric and system would be preferable in order to better approximate the absence of suitable in vitro infection Metabolic Surgery, Charité the human in vivo situation. models, because available cell lines are derived University Medicine, Berlin, Methods Gastric glands were isolated from healthy Germany from neoplastic tissue, which has already 4Hubrecht Institute/KNAW and human stomach tissue and grown in Matrigel containing undergone transformation. University Medical Centre media supplemented with various growth factors, ▸ So far, it has not been possible to culture Utrecht, Utrecht, developmental regulators and apoptosis inhibitors to normal human gastric primary epithelial cells The Netherlands generate long-lasting normal epithelial cell cultures. long enough to permit experimental Correspondence to Results Culture conditions were developed which investigations into many of the processes that Professor Dr Thomas F Meyer, support the formation and quasi-indefinite growth of three underlie gastric pathology. Department of Molecular dimensional (3D) spheroids derived from various sites of Biology, Max Planck Institute the human stomach. Spheroids could be differentiated to What are the new findings? for Infection Biology, ▸ We have established a quasi-immortal tissue gastric organoids after withdrawal of Wnt3A and R- http://gut.bmj.com/ Charitéplatz 1, Berlin 10117, culture model derived from normal, primary Germany; spondin1 from the medium. The 3D cultures exhibit typical [email protected] morphological features of human stomach tissue. Transfer human gastric glands, which can be expanded of sheared spheroids into 2D culture led to the formation in vitro in the form of three dimensional gastric Received 30 June 2014 of dense planar cultures of polarised epithelial cells serving spheroids. Revised 21 November 2014 ▸ Spheroids can be differentiated to organoids Accepted 24 November 2014 as a suitable in vitro model of H. pylori infection. Conclusions A robust and quasi-immortal 3D organoid which recapitulate many facets of the normal model has been established, which is considered gastric architecture and physiology, and can on September 23, 2021 by guest. Protected copyright. instrumental for future research aimed to understand the also be transferred to planar cultures. ▸ underlying mechanisms of infection, mucosal immunity and The primary gastric cells can be infected with H. pylori cancer of the human stomach. to allow analysis of infection-induced changes and can also be genetically manipulated to investigate mechanisms of gastric pathology. INTRODUCTION How might it impact on clinical practice in Bacterial infections are gaining increasing attention as the foreseeable future? 12 ▸ Since even small biopsy specimens are the initiating cause of human cancers. The para- fi digm of a cancer-inducing bacterium is Helicobacter suf cient to create large numbers of cells, our approach serves basic investigation and could pylori. This Gram-negative bacterium is prevalent in fi around 50% of the world’s population3 and is the soon nd personalised medicine application for only one classified as a type I carcinogen by the diagnostics of disease stages and WHO.4 It causes persistent infection of the human pharmacological screening and ultimately for gastric mucosa which often results in acute and tissue regeneration purposes. chronic gastritis.5 While the majority of infections To cite: Schlaermann P, are asymptomatic, duodenal and gastric ulcers association between chronic H. pylori infections and Toelle B, Berger H, et al. – Gut Published Online First: develop in 5% 10% of infected individuals. In a the development of gastric adenocarcinoma, as well [please include Day Month small subset of patients, gastritis progresses over years as its connection to the occurrence of mucosa- Year] doi:10.1136/gutjnl- and decades via atrophic, metaplastic and dysplastic associated lymphatic tissue lymphoma is supported 2014-307949 pathologies to gastric adenocarcinoma.6 This by vast epidemiological evidence.78 Schlaermann P, et al. Gut 2014;0:1–12. doi:10.1136/gutjnl-2014-307949 1 Copyright Article author (or their employer) 2014. Produced by BMJ Publishing Group Ltd (& BSG) under licence. Helicobacter pylori A major risk factor for the development of gastric adenocarcin- National Center for Biotechnology Information and can be oma is chronic inflammation caused by the persistent infection accessed with the GEO accession number GSE58473. For more Gut: first published as 10.1136/gutjnl-2014-307949 on 24 December 2014. Downloaded from with H. pylori. One major virulence factor, the CagA protein, information, see online supplementary methods. which is translocated into host cells via the pathogen’s type IV secretion system (T4SS), has been directly implicated in the Human tissue material process of malignant transformation.910Yet, the detailed Gastric tissue samples were derived from the Clinics for mechanisms that trigger gastric cancer initiation are poorly General, Visceral and Transplant Surgery, and the Center of understood. One major drawback is the lack of suitable animal Bariatric and Metabolic Surgery, Charité University Medicine, models, capable of recapitulating crucial aspects of the human Berlin, Germany. Pseudonymised samples were obtained from infection. For example, infected mice normally do not progress individuals undergoing gastrectomy or sleeve resection. Only further than to the metaplastic stage.11 In contrast, infected anatomically normal gastric tissue samples were used for experi- gerbils reportedly develop tumours after a few weeks of infec- ments and prepared within 3 h after removal. tion12 and, besides lagging behind as an amenable genetic model, might not resemble the human situation. Consequently, current Gastric gland isolation research largely depends on the use of transformed human epi- Tissue samples were washed with cold Hank’s buffered saline solu- thelial cell lines as in vitro models of these infections, which were tion (HBSS) and fat and connective tissue were removed. Samples almost exclusively derived from gastric adenocarcinoma. Since were cut into pieces of approximately 5 mm, washed 8–10 times such tumour cell lines already represent the end-point of with cold HBSS until the supernatant was clear and incubated Correa’s cascade, and as such are the end-product of the process with chelating solution (distilled water with 5.6 mM Na2HPO4, in question, they are badly suited for illuminating the early 8.0 mM KH2PO4, 96.2 mM NaCl, 1.6 mM KCl, 43.4 mM effects of H. pylori on the host. Therefore, a primary cell system sucrose, 54.9 mM D-sorbitol, 0.5 mM DL-dithiothreitol, 2 mM is urgently needed in order to assess the early effects of an H. EDTA) for 30 min at 37°C on a shaking platform. Supernatant pylori infection on healthy epithelial cells. was then removed, tissue fragments placed in a petri dish and During recent years, rapid advances have been made with gently squeezed with a glass slide to isolate the gastric glands. respect to in vitro cultivation of three dimensional (3D) epithelial Isolated glands were resuspended in medium containing 10% primary cell cultures, recapitulating organ physiology and struc- heat-inactivated fetal calf serum (FCS; Biochrom), collected in a ture. Several strategies have been pursued to enable long-term out- tube and allowed to settle for 1 min by gravity before the super- growth of murine intestinal crypts to 3D crypt-villus-like natant containing most of the isolated glands was transferred to a structures: one protocol relies on stromal elements rather than new tube. After five more washes, glands were counted under a extrinsically added growth factors and an air-liquid interface to microscope and centrifuged (250×g, 5 min) followed by three support the growth of 3D epithelial structures13 whereas another washes
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