Helicobacter pylori targets cancer-associated apical-junctional constituents in gastroids and gastric epithelial cells
Open accessAbstract
Objective: Helicobacter pylori strains that express the oncoprotein CagA augment risk for gastric cancer. However, the precise mechanisms through which cag + strains heighten cancer risk have not been fully delineated and model systems that recapitulate the gastric niche are critical for understanding pathogenesis. Gastroids are three-dimensional organ-like structures that provide unique opportunities to study host-H. pylori interactions in a preclinical model. We used gastroids to inform and direct in vitro studies to define mechanisms through which H. pylori modulates expression of the cancer-associated tight junction protein claudin-7. Design: Gastroids were infected by luminal microinjection, and MKN28 gastric epithelial cells were cocultured with H. pylori wild-type cag+ strains or isogenic mutants. β-catenin, claudin-7 and snail localisation was determined by immunocytochemistry. Proliferation was assessed using 5-ethynyl-2′-deoxyuridine, and levels of claudin-7 and snail were determined by western blot and flow cytometry. Results: Gastroids developed into a self-organising differentiation axis and H. pylori induced mislocalisation of claudin-7 and increased proliferation in a CagA- and β-catenin-dependent manner. In MKN28 cells, H pylori-induced suppression of claudin-7 was regulated by β-catenin and snail. Similarly, snail expression was increased and claudin-7 levels were decreased among H. pylori-infected individuals. Conclusions: H. pylori increase proliferation in a strain-specific manner in a novel gastroid system. H. pylori also alter expression and localisation of claudin-7 in gastroids and human epithelial cells, which is mediated by β-catenin and snail activation. These data provide new insights into molecular interactions with carcinogenic potential that occur between H. pylori and epithelial cells within the gastric niche.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Organoids infected with HRV or rotavirus enterotoxin showed lumenal swelling, a characteristic of rotavirus-induced diarrhea.
“Organoids infected with HRV or rotavirus enterotoxin showed lumenal swelling, a characteristic of rotavirus-induced diarrhea181.”
From Organoids (2022) · cites this paper as [181]
The Results section describes gastroids infected with H. pylori and changes in occludin and β-catenin; the Discussion likewise concerns H. pylori infection. Searches for HRV, rotavirus enterotoxin, lumenal swelling, and rotavirus-induced diarrhea found no passage addressing the claimed observation. No page numbers were provided in our copy. (LLM, conf=0.76)
Experimental — accuracy not yet measuredIn human intestinal organoids, differentiated intestinal cells are more susceptible to human rotavirus infection than undifferentiated ones.
“In human intestinal organoids, differentiated intestinal cells are more susceptible to human rotavirus (HRV) infection than undifferentiated ones.”
From Organoids (2022) · cites this paper as [181]
The Results section describes mouse gastric organoids infected with H. pylori, not human intestinal organoids infected with rotavirus. The Discussion discusses differentiation in gastroids but does not compare infection susceptibility in differentiated and undifferentiated intestinal cells. Searches for rotavirus and that susceptibility comparison found no relevant passage in our copy; page numbers were not provided. (LLM, conf=0.78)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Global burden of cancers attributable to infections in 2008: a review and synthetic analysis
de Martel, C., Ferlay, J., Franceschi, S., Vignat, J., Bray, F., Forman, D., & Plummer, M. (2012) · The Lancet Oncology · doi:10.1016/s1470-2045(12)70137-7 · Cited by 2,540 · see citing works
Censini, S., Lange, C., Xiang, Z., Crabtree, J. E., GHIARA, P., Borodovsky, M. Y., Rappuoli, R., & Covacci, A. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.25.14648 · Cited by 1,872 · see citing works
Helicobacter pylori and gastrointestinal tract adenocarcinomas
Peek, R. M., & Blaser, M. J. (2002) · Nature reviews. Cancer · doi:10.1038/nrc703 · Cited by 1,807 · see citing works
Self-citationLgr5+ve Stem Cells Drive Self-Renewal in the Stomach and Build Long-Lived Gastric Units In Vitro
Barker, N., Huch, M., Kujala, P., van de Wetering, M., Snippert, H. J., van Es, J. H., Sato, T., Stange, D. E., Begthel, H., van den Born, M., et al. (2010) · Cell Stem Cell · doi:10.1016/j.stem.2009.11.013 · Cited by 1,547 · see citing works
Schistosomes, liver flukes and Helicobacter pylori.
(1994) · PubMed Central · Cited by 1,529 · see citing works
Helicobacter pylori and Gastric Cancer: Factors That Modulate Disease Risk
Wroblewski, L. E., Peek, R. M., & Wilson, K. T. (2010) · Clinical Microbiology Reviews · doi:10.1128/cmr.00011-10 · Cited by 1,455 · see citing works
Self-citationHelicobacter pylori: gastric cancer and beyond
Polk, D. B., & Peek, R. M. (2010) · Nature Reviews Cancer · doi:10.1038/nrc2857 · Cited by 1,158 · see citing works
Self-citationDisruption of the Epithelial Apical-Junctional Complex by Helicobacter pylori CagA
Amieva, M. R., Vogelmann, R., Covacci, A., Tompkins, L. S., Nelson, W. J., & Falkow, S. (2003) · Science · doi:10.1126/science.1081919 · Cited by 739 · see citing works
Ikenouchi, J., Matsuda, M., Furuse, M., & Tsukita, S. (2003) · Journal of Cell Science · doi:10.1242/jcs.00389 · Cited by 678 · see citing works
Xiang, Z., Censini, S., Bayeli, P. F., Telford, J. L., Figura, N., Rappuoli, R., & Covacci, A. (1995) · Infection and Immunity · doi:10.1128/iai.63.1.94-98.1995 · Cited by 585 · see citing works
Helicobacter pylori CagA targets PAR1/MARK kinase to disrupt epithelial cell polarity
Saadat, I., Higashi, H., Obuse, C., Umeda, M., Murata‐Kamiya, N., Saito, Y., Lu, H., Ohnishi, N., Azuma, T., Suzuki, A., et al. (2007) · Nature · doi:10.1038/nature05765 · Cited by 501 · see citing works
Activation of β-catenin by carcinogenic Helicobacter pylori
Franco, A. T., Israel, D. A., Washington, M. K., Krishna, U. S., Fox, J. G., Rogers, A. B., Neish, A. S., Collier-Hyams, L. S., Perez-Perez, G. I., Hatakeyama, M., et al. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0504927102 · Cited by 479 · see citing works
Self-citationMurata-Kamiya, N., Kurashima, Y., Teishikata, Y., Yamahashi, Y., Saito, Y., Higashi, H., Aburatani, H., Akiyama, T., Peek, R. M., Azuma, T., et al. (2007) · Oncogene · doi:10.1038/sj.onc.1210251 · Cited by 468 · see citing works
Self-citationSrc Is the Kinase of the Helicobacter pylori CagA Protein in Vitro and in Vivo
Selbach, M., Moese, S., Hauck, C. R., Meyer, T. F., & Backert, S. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.c100754200 · Cited by 414 · see citing works
Inverse Associations of Helicobacter pylori With Asthma and Allergy
Chen, Y. (2007) · Archives of Internal Medicine · doi:10.1001/archinte.167.8.821 · Cited by 374 · see citing works
beta-Catenin mutation is a frequent cause of Wnt pathway activation in gastric cancer.
Clements, W. M., Wang, J., Sarnaik, A. A., Kim, O. J., MacDonald, J., Fenoglio‐Preiser, C. M., Groden, J. L., & Lowy, A. M. (2002) · PubMed · Cited by 357 · see citing works
Iron regulation of Shiga-like toxin expression in Escherichia coli is mediated by the fur locus
Calderwood, S. B., & Mekalanos, J. J. (1987) · Journal of Bacteriology · doi:10.1128/jb.169.10.4759-4764.1987 · Cited by 334 · see citing works
Mueller, D., Tegtmeyer, N., Brandt, S., Yamaoka, Y., Poire, E. D., Sgouras, D. N., Weßler, S., Torres, J., Smolka, A. J., & Backert, S. (2012) · Journal of Clinical Investigation · doi:10.1172/jci61143 · Cited by 240 · see citing works
Backert, S., Moese, S., Selbach, M., Brinkmann, V., & Meyer, T. F. (2001) · Molecular Microbiology · doi:10.1046/j.1365-2958.2001.02649.x · Cited by 232 · see citing works
Role of Innate Immunity inHelicobacter pylori-Induced Gastric Malignancy
Peek, R. M., Fiske, C., & Wilson, K. T. (2010) · Physiological Reviews · doi:10.1152/physrev.00039.2009 · Cited by 231 · see citing works
Self-citationInflammation and Disruption of the Mucosal Architecture in Claudin-7–Deficient Mice
Ding, L., Lü, Z., Foreman, O., Tatum, R., Lu, Q., Renegar, R. H., Cao, J. P., & Chen, Y. (2011) · Gastroenterology · doi:10.1053/j.gastro.2011.10.025 · Cited by 219 · see citing works
Tammer, I., Brandt, S., Hartig, R., König, W., & Backert, S. (2007) · Gastroenterology · doi:10.1053/j.gastro.2007.01.050 · Cited by 219 · see citing works
Helicobacter pylori strain-specific genotypes and modulation of the gastric epithelial cell cycle.
Peek, R. M., Blaser, M. J., Mays, D. J., Forsyth, M. H., Cover, T. L., Song, S. Y., Krishna, U. S., & Pietenpol, J. A. (1999) · PubMed · Cited by 210 · see citing works
Self-citationHigh Dietary Salt Intake Exacerbates Helicobacter pylori-Induced Gastric Carcinogenesis
Gaddy, J. A., Radin, J. N., Loh, J. T., Zhang, F., Washington, M. K., Peek, R. M., Algood, H. M. S., & Cover, T. L. (2013) · Infection and Immunity · doi:10.1128/iai.01271-12 · Cited by 209 · see citing works
Self-citationSpermine oxidase mediates the gastric cancer risk associated with Helicobacter pylori CagA
Chaturvedi, R., Asim, M., Romero–Gallo, J., Barry, D. P., Hoge, S., de Sablet, T., Delgado, A. G., Wroblewski, L. E., Piazuelo, M. B., Yan, F., et al. (2011) · Gastroenterology · doi:10.1053/j.gastro.2011.07.045 · Cited by 208 · see citing works
Self-citationWroblewski, L. E., Shen, L., Ogden, S., Romero–Gallo, J., Lapierre, L. A., Israel, D. A., Turner, J. R., & Peek, R. M. (2009) · Gastroenterology · doi:10.1053/j.gastro.2008.10.011 · Cited by 193 · see citing works
Self-citationIron deficiency accelerates Helicobacter pylori–induced carcinogenesis in rodents and humans
Noto, J. M., Gaddy, J. A., Lee, J. Y., Piazuelo, M. B., Friedman, D. B., Colvin, D. C., Romero-Gallo, J., Suarez, G., Loh, J., Slaughter, J. C., et al. (2013) · Journal of Clinical Investigation · doi:10.1172/jci64373 · Cited by 178 · see citing works
Self-citationHelicobacter pylori perturbs iron trafficking in the epithelium to grow on the cell surface
Tan, S., Noto, J. M., Romero-Gallo, J., Peek, R. M., & Amieva, M. R. (2011) · PLoS Pathogens · doi:10.1371/journal.ppat.1002050 · Cited by 175 · see citing works
Self-citationWenzhen, Y., Li, Y., Kehu, Y., Ma, B., Quanlin, G., Donghai, W., & Lijuan, Y. (2010) · Scandinavian Journal of Gastroenterology · doi:10.3109/00365521003663670 · Cited by 155 · see citing works
Tolwinski, N. S., & Wieschaus, E. (2004) · Trends in Genetics · doi:10.1016/j.tig.2004.02.003 · Cited by 151 · see citing works
Lei, Z., Maeda, T., Tamura, A., Nakamura, T., Yamazaki, Y., Shiratori, H., Yashiro, K., Tsukita, S., & Hamada, H. (2012) · Developmental Biology · doi:10.1016/j.ydbio.2012.07.005 · Cited by 151 · see citing works
Effect of iron on yields of exotoxin A in cultures of Pseudomonas aeruginosa PA-103
Bjorn, M. J., Iglewski, B. H., Ives, S. K., SADOFF, J. C., & Vasil, M. L. (1978) · Infection and Immunity · doi:10.1128/iai.19.3.785-791.1978 · Cited by 145 · see citing works
Ebert, M. P. A. (2002) · Carcinogenesis · doi:10.1093/carcin/23.1.87 · Cited by 144 · see citing works
Harrison, L. E., Zhang, Z., Karpeh, M. S., Sun, M., & Kurtz, R. C. (1997) · Cancer · doi:10.1002/(sici)1097-0142(19970915)80:6 · Cited by 143 · see citing works
Wroblewski, L. E., Noble, P. J. M., Pagliocca, A., Pritchard, D. M., Hart, C. A., Campbell, F., Dodson, A. R., Dockray, G. J., & Varró, A. (2003) · Journal of Cell Science · doi:10.1242/jcs.00518 · Cited by 142 · see citing works
Self-citationThe claudin family of proteins in human malignancy: a clinical perspective
Chen, Y., Ding, L., Lü, Z., & Lu, Q. (2013) · Cancer Management and Research · doi:10.2147/cmar.s38294 · Cited by 140 · see citing works
Harrison, L. E., Zhang, Z., Karpeh, M. S., Sun, M., & Kurtz, R. C. (1997) · PubMed · Cited by 133 · see citing works
Yin, Y., Grabowska, A. M., Clarke, P. A., Whelband, E., Robinson, K., Argent, R. H., Tobias, A., Kumari, R., Atherton, J. C., & Watson, S. A. (2010) · Gut · doi:10.1136/gut.2009.199794 · Cited by 123 · see citing works
Nagy, T. A., Frey, M. R., Yan, F., Israel, D. A., Polk, D. B., & Peek, R. M. (2009) · The Journal of Infectious Diseases · doi:10.1086/596660 · Cited by 120 · see citing works
Self-citationDiet, microbial virulence, and Helicobacter pylori -induced gastric cancer
Cover, T. L., & Peek, R. M. (2013) · Gut Microbes · doi:10.4161/gmic.26262 · Cited by 109 · see citing works
Self-citationTai, S.-P. S., Krafft, A. E., Nootheti, P., & Holmes, R. K. (1990) · Microbial Pathogenesis · doi:10.1016/0882-4010(90)90015-i · Cited by 84 · see citing works
Carrozzino, F., Soulié, P., Huber, D., Mensi, N., Orci, L., Cano, A., Féraille, E., & Montesano, R. (2005) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00175.2005 · Cited by 81 · see citing works
Nagy, T. A., Wroblewski, L. E., Wang, D., Piazuelo, M. B., Delgado, A., Romero–Gallo, J., Noto, J. M., Israel, D. A., Ogden, S. R., Correa, P., et al. (2011) · Gastroenterology · doi:10.1053/j.gastro.2011.05.004 · Cited by 73 · see citing works
Self-citationPhenotypic differences between esophageal and gastric intestinal metaplasia
Piazuelo, M. B., Haque, S., Delgado, A., Du, J. X., Rodriguez, F. H., & Correa, P. (2003) · Modern Pathology · doi:10.1038/modpathol.3800016 · Cited by 69 · see citing works
Self-citationGene expression profiling in a mouse model of Helicobacter‐induced gastric cancer
Takaishi, S., & Wang, T. C. (2007) · Cancer Science · doi:10.1111/j.1349-7006.2007.00392.x · Cited by 61 · see citing works
Noto, J. M., Khizanishvili, T., Chaturvedi, R., Piazuelo, M. B., Romero–Gallo, J., Delgado, A. G., Khurana, S. S., Sierra, J. C., Krishna, U. S., Suárez, G., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0054344 · Cited by 52 · see citing works
Self-citationAssociation of serum ferritin levels with the risk of stomach cancer.
Nomura, A. M. Y., Chyou, P., & Stemmermann, G. N. (1993) · PubMed · Cited by 46 · see citing works
Snail is an independent prognostic predictor for progression and patient survival of gastric cancer
He, H., Chen, W., Wang, X., Wang, C., Liu, F., Shen, Z., Xu, J., Gu, J., & Sun, Y. (2012) · Cancer Science · doi:10.1111/j.1349-7006.2012.02295.x · Cited by 44 · see citing works
The neurotoxin of Shigella shigae. III. The effect of iron on production of the toxin.
Heyningen, W. E. V., & Gladstone, G. P. (1953) · PubMed · Cited by 39 · see citing works
Beta-Catenin Expression in Intramucosal Neoplastic Lesions of the Stomach
Tsukashita, S., Kushima, R., Bamba, M., Nakamura, E., Mukaisho, K., Sugihara, H., & Hattori, T. (2003) · Oncology · doi:10.1159/000069310 · Cited by 29 · see citing works
Yoshizawa, K., Nozaki, S., KATO, A., Hirai, M., Yanase, M., YOSHIMOTO, T., Kimura, I., SUGIURA, S., Okamune, A., Kitahara, H., et al. (2012) · Oncology Reports · doi:10.3892/or.2012.2161 · Cited by 26 · see citing works
Expression of beta-catenin and E-cadherin in the adenoma-carcinoma sequence of the stomach.
Kim, H. S., Hong, E. K., Park, S. Y., Kim, W. H., & Lee, H. S. (2003) · PubMed · Cited by 24 · see citing works
Frequent translocalization of β-catenin in gastric cancers and its relevance to tumor progression
Cheng, X., Sun, Y., Chen, X.-Y., Zhang, K., Kong, Q., Liu, J., & Li, H. (2004) · Oncology Reports · doi:10.3892/or.11.6.1201 · Cited by 23 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Organoids as an in vitro model of human development and disease
Fatehullah, A., Tan, S. H., & Barker, N. (2016) · Nature Cell Biology · doi:10.1038/ncb3312 · Cited by 1,508 · see citing works
Zhao, Z., Chen, X., Dowbaj, A. M., Sljukic, A., Bratlie, K., Lin, L., Fong, E. L. S., Balachander, G. M., Chen, Z., Soragni, A., et al. (2022) · Nature Reviews Methods Primers · doi:10.1038/s43586-022-00174-y · Cited by 1,001 · see citing works
Pathobiology of Helicobacter pylori–Induced Gastric Cancer
Amieva, M. R., & Peek, R. M. (2015) · Gastroenterology · doi:10.1053/j.gastro.2015.09.004 · Cited by 907 · see citing works
Self-citationHuman organoids in basic research and clinical applications
Tang, X.-Y., Wu, S., Wang, D., Chu, C., Hong, Y., Tao, M., Hu, H., Xu, M., Guo, X. L., & Liu, Y. (2022) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-022-01024-9 · Cited by 509 · see citing works
Schlaermann, P., Toelle, B., Berger, H., Schmidt, S. C., Glanemann, M., Ordemann, J., Bartfeld, S., Mollenkopf, H., & Meyer, T. F. (2014) · Gut · doi:10.1136/gutjnl-2014-307949 · Cited by 256 · see citing works
Williamson, I., Arnold, J. W., Samsa, L. A., Gaynor, L. T., DiSalvo, M., Cocchiaro, J. L., Carroll, I. M., Azcárate-Peril, M. A., Rawls, J. F., Allbritton, N. L., et al. (2018) · Cellular and Molecular Gastroenterology and Hepatology · doi:10.1016/j.jcmgh.2018.05.004 · Cited by 248 · see citing works
Organoid Models of Human Gastrointestinal Development and Disease
Dedhia, P. H., Bertaux‐Skeirik, N., Zavros, Y. L., & Spence, J. R. (2016) · Gastroenterology · doi:10.1053/j.gastro.2015.12.042 · Cited by 246 · see citing works
Self-citationSigal, M. J., Rothenberg, M. E., Logan, C. Y., Lee, J. Y., Honaker, R. W., Cooper, R. L., Passarelli, B., Camorlinga, M., Bouley, D. M., Cabrera-Álvarez, G., et al. (2015) · Gastroenterology · doi:10.1053/j.gastro.2015.02.049 · Cited by 244 · see citing works
Pathogenesis of Helicobacter pylori infection
Backert, S., Neddermann, M., Maubach, G., & Naumann, M. (2016) · Helicobacter · doi:10.1111/hel.12335 · Cited by 229 · see citing works
High fat diet, gut microbiome and gastrointestinal cancer
Tong, Y., Gao, H., Qi, Q., Liu, X., Li, J., Gao, J., Li, P., Wang, Y., Du, L., & Wang, C. (2021) · Theranostics · doi:10.7150/thno.56157 · Cited by 205 · see citing works
Organoid models of gastrointestinal cancers in basic and translational research
Lau, H. C.-H., Kranenburg, O., Xiao, H., & Yu, J. (2020) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-019-0255-2 · Cited by 195 · see citing works
Collateral damage: Insights into bacterial mechanisms that predispose host cells to cancer
Gagnaire, A., Nadel, B., Raoult, D., Neefjes, J., & Gorvel, J.-P. (2017) · Nature Reviews Microbiology · doi:10.1038/nrmicro.2016.171 · Cited by 189 · see citing works
Applications of organoids for cancer biology and precision medicine
Lo, Y.-H., Karlsson, K., & Kuo, C. J. (2020) · Nature Cancer · doi:10.1038/s43018-020-0102-y · Cited by 182 · see citing works
Huang, Z., Zhang, Z., Zhou, C., Liu, L., & Huang, C. (2022) · MedComm · doi:10.1002/mco2.144 · Cited by 170 · see citing works
CD44 Plays a Functional Role in Helicobacter pylori-induced Epithelial Cell Proliferation
Bertaux‐Skeirik, N., Feng, R., Schumacher, M. A., Li, J., Mahé, M. M., Engevik, A. C., Javier, J. E., Peek, R. M., Ottemann, K. M., Orian‐Rousseau, V., et al. (2015) · PLoS Pathogens · doi:10.1371/journal.ppat.1004663 · Cited by 161 · see citing works
Self-citationHelicobacter pylori Employs a Unique Basolateral Type IV Secretion Mechanism for CagA Delivery
Tegtmeyer, N., Wessler, S., Necchi, V., Rohde, M., Harrer, A., Rau, T. T., Asche, C. I., Boehm, M., Loessner, H., Figueiredo, C., et al. (2017) · Cell Host & Microbe · doi:10.1016/j.chom.2017.09.005 · Cited by 156 · see citing works
Gut organoids: mini-tissues in culture to study intestinal physiology and disease
Almeqdadi, M., Mana, M., Roper, J., & Yilmaz, Ö. H. (2019) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00300.2017 · Cited by 151 · see citing works
Organoids in gastrointestinal diseases: From experimental models to clinical translation
Günther, C., Winner, B., Neurath, M. F., & Stappenbeck, T. S. (2022) · Gut · doi:10.1136/gutjnl-2021-326560 · Cited by 145 · see citing works
Wnt/β-Catenin Signaling as a Molecular Target by Pathogenic Bacteria
Silva-García, O., Valdez-Alarcón, J. J., & Baizabal-Aguirre, V. M. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.02135 · Cited by 142 · see citing works
Crossing the Intestinal Barrier via Listeria Adhesion Protein and Internalin A
Drolia, R., & Bhunia, A. K. (2019) · Trends in Microbiology · doi:10.1016/j.tim.2018.12.007 · Cited by 144 · see citing works
Gastrointestinal tract modeling using organoids engineered with cellular and microbiota niches
Min, S., Kim, S., & Cho, S. (2020) · Experimental & Molecular Medicine · doi:10.1038/s12276-020-0386-0 · Cited by 145 · see citing works
Claudins and Gastric Cancer: An Overview
HASHIMOTO, I., & Oshima, T. (2022) · Cancers · doi:10.3390/cancers14020290 · Cited by 144 · see citing works
Kidney Organoids: A Translational Journey
Morizane, R., & Bonventre, J. V. (2017) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2017.01.001 · Cited by 134 · see citing works
The Gut-Brain Axis in Inflammatory Bowel Disease—Current and Future Perspectives
Günther, C., Rothhammer, V., Karow, M., Neurath, M., & Winner, B. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22168870 · Cited by 123 · see citing works
Wnt/β-catenin, an oncogenic pathway targeted byH. pyloriin gastric carcinogenesis
Song, X., Xin, N., Wang, W., & Zhao, C. (2015) · Oncotarget · doi:10.18632/oncotarget.5758 · Cited by 121 · see citing works
Host‐microbe interaction in the gastrointestinal tract
Parker, A., Lawson, M. A., Vaux, L., & Pin, C. (2017) · Environmental Microbiology · doi:10.1111/1462-2920.13926 · Cited by 123 · see citing works
Seidlitz, T., Koo, B., & Stange, D. E. (2020) · Cell Death and Differentiation · doi:10.1038/s41418-020-00662-2 · Cited by 108 · see citing works
Organoids: a novel modality in disease modeling
Heydari, Z., Moeinvaziri, F., Agarwal, T., Pooyan, P., Shpichka, A. I., Maiti, T. K., Timashev, P. S., Baharvand, H., & Vosough, M. (2021) · Bio-Design and Manufacturing · doi:10.1007/s42242-021-00150-7 · Cited by 100 · see citing works
Tight junction disruption: Helicobacter pylori and dysregulation of the gastric mucosal barrier
Caron, T. J. (2015) · World Journal of Gastroenterology · doi:10.3748/wjg.v21.i40.11411 · Cited by 97 · see citing works
Backert, S., & Tegtmeyer, N. (2017) · Toxins · doi:10.3390/toxins9040115 · Cited by 95 · see citing works
Li, N., Lü, N., & Xie, C. (2019) · FEBS Journal · doi:10.1111/febs.15017 · Cited by 96 · see citing works
Generating human antral and fundic gastric organoids from pluripotent stem cells
Broda, T. R., McCracken, K., & Wells, J. M. (2018) · Nature Protocols · doi:10.1038/s41596-018-0080-z · Cited by 81 · see citing works
Dixon, B. R. E. A., Radin, J. N., Piazuelo, M. B., Contreras, D. C., & Algood, H. M. S. (2016) · PLoS ONE · doi:10.1371/journal.pone.0148514 · Cited by 89 · see citing works
Self-citationGastrointestinal Organoids: Understanding the Molecular Basis of the Host–Microbe Interface
Hill, D. R., & Spence, J. R. (2016) · Cellular and Molecular Gastroenterology and Hepatology · doi:10.1016/j.jcmgh.2016.11.007 · Cited by 87 · see citing works
Helicobacter pylori, Cancer, and the Gastric Microbiota
Wroblewski, L. E., & Peek, R. M. (2016) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-41388-4_19 · Cited by 86 · see citing works
Self-citationClaudins and cancer: Fall of the soldiers entrusted to protect the gate and keep the barrier intact
Singh, A. B., & Dhawan, P. (2015) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2015.05.001 · Cited by 82 · see citing works
Peng, Y., Zhang, X., Ma, Q., Yan, R., Qin, Y., Zhao, Y., Cheng, Y., Yang, M., Wang, Q., Feng, X., et al. (2016) · Cancer Letters · doi:10.1016/j.canlet.2016.10.035 · Cited by 81 · see citing works
Organoid Models for Infectious Disease
Blutt, S. E., & Estes, M. K. (2021) · Annual Review of Medicine · doi:10.1146/annurev-med-042320-023055 · Cited by 78 · see citing works
Gastric Stem Cells: Physiological and Pathological Perspectives
Xiao, S., & Zhou, L. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.571536 · Cited by 78 · see citing works
Role of Helicobacter pylori infection in pathogenesis of gastric carcinoma
Zhang, R. (2016) · World Journal of Gastrointestinal Pathophysiology · doi:10.4291/wjgp.v7.i1.97 · Cited by 72 · see citing works
Downregulation of miR‐491‐5p promotes gastric cancer metastasis by regulating SNAIL and FGFR 4
Yu, T., Wang, L., Li, W., Zuo, Q., Li, M., Zou, Q., & Xiao, B. (2018) · Cancer Science · doi:10.1111/cas.13583 · Cited by 69 · see citing works
Suárez, G., Romero–Gallo, J., Piazuelo, M. B., Sierra, J. C., Delgado, A. G., Washington, M. K., Shah, S. C., Wilson, K. T., & Peek, R. M. (2019) · Cancer Research · doi:10.1158/0008-5472.can-18-2651 · Cited by 67 · see citing works
Self-citationGonzález, M. F., Díaz, P., Sandoval, A., Herrera, D., & Quest, A. F. G. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22094823 · Cited by 67 · see citing works
Drug Discovery via Human-Derived Stem Cell Organoids
Liu, F., Huang, J., Ning, B., Liu, Z., Chen, S., & Zhao, W. (2016) · Frontiers in Pharmacology · doi:10.3389/fphar.2016.00334 · Cited by 66 · see citing works
Li, Y., Gong, Y., Ning, X., Ding, P., Liu, L., He, S., Gong, K., Zhang, C., Li, X., & Zhou, L. (2018) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-018-0924-y · Cited by 65 · see citing works
Heterogeneity and dynamics of active Kras-induced dysplastic lineages from mouse corpus stomach
Min, J., Vega, P. N., Engevik, A. C., Williams, J. A., Yang, Q., Patterson, L. M., Simmons, A. J., Bliton, R. J., Betts, J. W., Lau, K. S., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-13479-6 · Cited by 60 · see citing works
Cellular self-assembly and biomaterials-based organoid models of development and diseases
Shah, S. B., & Singh, A. K. (2017) · Acta Biomaterialia · doi:10.1016/j.actbio.2017.01.075 · Cited by 57 · see citing works
Yang, Z., Xie, C., Xu, W., Liu, G., Cao, X., Li, W., Jiang, C., Zhu, Y., Luo, S., Luo, Z., et al. (2015) · Oncotarget · doi:10.18632/oncotarget.5577 · Cited by 57 · see citing works
Classification of Helicobacter pylori Virulence Factors: Is CagA a Toxin or Not?
Knorr, J., Ricci, V., Hatakeyama, M., & Backert, S. (2019) · Trends in Microbiology · doi:10.1016/j.tim.2019.04.010 · Cited by 56 · see citing works
Gastric Organoids: An Emerging Model System to Study Helicobacter pylori Pathogenesis
Pompaiah, M., & Bartfeld, S. (2017) · Current topics in microbiology and immunology · doi:10.1007/978-3-319-50520-6_7 · Cited by 55 · see citing works
Modeling human disease using organotypic cultures
Schweiger, P. J., & Jensen, K. B. (2016) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2016.07.003 · Cited by 51 · see citing works
Helicobacter pylori Uses the TlpB Receptor To Sense Sites of Gastric Injury
Hanyu, H., Engevik, K. A., Matthis, A. L., Ottemann, K. M., Montrose, M. H., & Aihara, E. (2019) · Infection and Immunity · doi:10.1128/iai.00202-19 · Cited by 49 · see citing works
Self-citationTiffon, C., Giraud, J., Molina‐Castro, S., Peru, S., Seeneevassen, L., Sifré, E., Staedel, C., Bessède, E., Dubus, P. R., Mégraud, F., et al. (2020) · Cells · doi:10.3390/cells9061462 · Cited by 47 · see citing works
Targeting the Mucosal Barrier: How Pathogens Modulate the Cellular Polarity NetworkPreprint
Ruch, T. R., & Engel, J. N. (2017) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a027953 · Cited by 47 · see citing works
Gastric Organoids: Progress and Remaining Challenges
Pang, M.-J., Burclaff, J., Jin, R. U., Adkins-Threats, M., Osaki, L. H., Han, Y., Mills, J. C., Miao, Z., & Wang, Z.-N. (2021) · Cellular and Molecular Gastroenterology and Hepatology · doi:10.1016/j.jcmgh.2021.09.005 · Cited by 43 · see citing works
Backert, S., Schmidt, T. P., Harrer, A., & Weßler, S. (2017) · Current topics in microbiology and immunology · doi:10.1007/978-3-319-50520-6_9 · Cited by 41 · see citing works
Genome engineering of stem cell organoids for disease modeling
Sun, Y., & Ding, Q. (2017) · Protein & Cell · doi:10.1007/s13238-016-0368-0 · Cited by 39 · see citing works
Wroblewski, L. E., Choi, E.-Y. K., Petersen, C. P., Delgado, A. G., Piazuelo, M. B., Romero–Gallo, J., Lantz, T., Zavros, Y. L., Coffey, R. J., Goldenring, J. R., et al. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1903798116 · Cited by 35 · see citing works
Self-citationPeng, Y., Lei, X., Yang, Q., Zhang, G., He, S., Wang, M., Ling, R., Zheng, B., He, J., Chen, X., et al. (2024) · Experimental & Molecular Medicine · doi:10.1038/s12276-024-01167-5 · Cited by 34 · see citing works
Modulation of Intestinal Paracellular Transport by Bacterial Pathogens
Roxas, J. L., & Viswanathan, V. K. (2018) · Comprehensive physiology · doi:10.1002/cphy.c170034 · Cited by 34 · see citing works
Three-Dimensional Culture Systems in Gastric Cancer Research
Alzeeb, G., Metges, J., Corcos, L., & Jossic-Corcos, C. L. (2020) · Cancers · doi:10.3390/cancers12102800 · Cited by 33 · see citing works
Marques, M. S., Melo, J., Cavadas, B., Mendes, N. M., Pereira, L., Carneiro, F., Figueiredo, C., & Leite, M. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.02712 · Cited by 32 · see citing works
Molecular mechanisms of gastric cancer initiation and progression by Helicobacter pylori
Servetas, S. L., Bridge, D. R., & Merrell, D. S. (2016) · Current Opinion in Infectious Diseases · doi:10.1097/qco.0000000000000248 · Cited by 32 · see citing works
Lu, Y., Jing, J., Sun, L. L., Gong, Y., Chen, M., Wang, Z., Sun, M., & Yuan, Y. (2017) · PLoS ONE · doi:10.1371/journal.pone.0174476 · Cited by 30 · see citing works
Bridge, D. R., Blum, F. C., Jang, S., Kim, J., Cha, J., & Merrell, D. S. (2017) · Scientific Reports · doi:10.1038/s41598-017-11382-y · Cited by 30 · see citing works
3D Human Organoids: The Next “Viral” Model for the Molecular Basis of Infectious Diseases
Chia, S. P. S., Kong, S. L. Y., Pang, J. K. S., & Soh, B.-S. (2022) · Biomedicines · doi:10.3390/biomedicines10071541 · Cited by 28 · see citing works
In vitro models to evaluate ingestible devices: Present status and current trends
O’Farrell, C., Stamatopoulos, K., Simmons, M. J. H., & Batchelor, H. K. (2021) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2021.113924 · Cited by 28 · see citing works
Loss of TFF1 promotesHelicobacter pylori-induced β-catenin activation and gastric tumorigenesis
Soutto, M., Romero–Gallo, J., Krishna, U. S., Piazuelo, M. B., Washington, M. K., Belkhiri, A., Peek, R. M., & El-Rifai, W. M. (2015) · Oncotarget · doi:10.18632/oncotarget.3772 · Cited by 28 · see citing works
Self-citationFarzi, N., Behzad, C., Hasani, Z., Alebouyeh, M., Zojaji, H., & Zali, M. R. (2018) · Folia Microbiologica · doi:10.1007/s12223-018-0637-9 · Cited by 27 · see citing works
Ray, A. K., Luis, P. B., Mishra, S. K., Barry, D. P., Asim, M., Pandey, A., Chaturvedi, M., Gupta, J., Gupta, S., Mahant, S., et al. (2021) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2021.765842 · Cited by 27 · see citing works
Self-citationGastric microbiota: an emerging player in gastric cancer
Zhou, S., Li, C., Liu, L., Yuan, Q., Miao, J., Wang, H., Ding, C., & Guan, W. (2023) · Frontiers in Microbiology · doi:10.3389/fmicb.2023.1130001 · Cited by 28 · see citing works
The role of the gut microbiome in gastrointestinal cancers
Mishra, Y., Ranjan, A., Mishra, V. K., Chattaraj, A., Aljabali, A. A. A., El‐Tanani, M., Hromić‐Jahjefendić, A., Uversky, V. N., & Tambuwala, M. M. (2023) · Cellular Signalling · doi:10.1016/j.cellsig.2023.111013 · Cited by 25 · see citing works
Helicobacter pylori pathogen inhibits cellular responses to oncogenic stress and apoptosis
Palrasu, M., Zaika, E. I., Paulrasu, K., Gokulan, R. C., Suárez, G., Que, J., El-Rifai, W. M., Peek, R. M., Garcia-Buitrago, M. T., & Zaika, A. I. (2022) · PLoS Pathogens · doi:10.1371/journal.ppat.1010628 · Cited by 25 · see citing works
Self-citationPeng, Y., Zhang, X., Lin, H., Deng, S., Qin, Y., He, J., Hu, F., Zhu, X., Feng, X., Wang, J., et al. (2021) · Aging · doi:10.18632/aging.202895 · Cited by 24 · see citing works
Jeong, H., Park, J., Kang, J. H., del Río, J. S., Kong, S., & Park, T. (2023) · Advanced Science · doi:10.1002/advs.202300164 · Cited by 23 · see citing works
Uotani, T., Murakami, K., Uchida, T., Tanaka, S., Nagashima, H., Zeng, X., Akada, J. K., Estes, M. K., Graham, D. Y., & Yamaoka, Y. (2019) · Helicobacter · doi:10.1111/hel.12583 · Cited by 24 · see citing works
H. pylori infection confers resistance to apoptosis via Brd4-dependent BIRC3 eRNA synthesis
Chen, Y., Sheppard, D., Dong, X., Hu, X., Chen, M., Chen, R., Chakrabarti, J. L., Zavros, Y. L., Peek, R. M., & Chen, L. (2020) · Cell Death and Disease · doi:10.1038/s41419-020-02894-z · Cited by 24 · see citing works
Self-citationMarques, M. S., Costa, A. C., Osório, H., Pinto, M. L., Relvas, S., Dinis-Ribeiro, M., Carneiro, F., Leite, M., & Figueiredo, C. (2021) · Gut Microbes · doi:10.1080/19490976.2021.1921928 · Cited by 23 · see citing works
Xu, M., Ma, J., Du, J., Yin, J., Liu, L., Cui, F., & Lu, Q. (2020) · Gastroenterology Research and Practice · doi:10.1155/2020/9797841 · Cited by 23 · see citing works
Abdi, E., Latifi‐Navid, S., Sarvestani, F. A., & Esmailnejad, M. H. (2021) · Expert Opinion on Therapeutic Targets · doi:10.1080/14728222.2021.1971195 · Cited by 21 · see citing works
Under the Radar: Strategies Used by Helicobacter pylori to Evade Host Responses
Prashar, A., Capurro, M., & Jones, N. L. (2021) · Annual Review of Physiology · doi:10.1146/annurev-physiol-061121-035930 · Cited by 21 · see citing works
Organoids as a Model to Study Infectious Disease
Engevik, K. A., Matthis, A. L., Montrose, M. H., & Aihara, E. (2017) · Methods in molecular biology · doi:10.1007/978-1-4939-7604-1_8 · Cited by 21 · see citing works
Self-citationMizutani, T., Araki, H., Saigo, C., Takada, J., Kubota, M., Ibuka, T., Suzui, N., Miyazaki, T., & Shimizu, M. (2020) · Digestive Diseases · doi:10.1159/000506120 · Cited by 21 · see citing works
Zhang, J., Wang, L., Song, Q., Xiao, M., Gao, J., Cao, X., & Zheng, W. (2022) · International Journal of Biological Sciences · doi:10.7150/ijbs.70406 · Cited by 20 · see citing works
Chen, Z., Soutto, M., Rahman, B., Fazili, M. W., Peng, D., Piazuelo, M. B., Chen, H., Washington, M. K., Shyr, Y., & El-Rifai, W. M. (2017) · Genes Chromosomes and Cancer · doi:10.1002/gcc.22456 · Cited by 19 · see citing works
Self-citationThe expression of IGF-1R in Helicobacter pylori-infected intestinal metaplasia and gastric cancer
Nakajima, N., Kozu, K., Kobayashi, S., Nishiyama, R., Okubo, R., Akai, Y., Moriyama, M., & Kinukawa, N. (2016) · Journal of Clinical Biochemistry and Nutrition · doi:10.3164/jcbn.16-11 · Cited by 18 · see citing works
Park, J. M., Han, Y. M., & Hahm, K. B. (2021) · Frontiers in Pharmacology · doi:10.3389/fphar.2021.675443 · Cited by 16 · see citing works
Mutated Rnf43 Aggravates Helicobacter Pylori-Induced Gastric Pathology
Neumeyer, V., Vieth, M. W., Gerhard, M., & Mejías‐Luque, R. (2019) · Cancers · doi:10.3390/cancers11030372 · Cited by 16 · see citing works
Regenerative medicine for the upper gastrointestinal tract
Kanetaka, K., & Eguchi, S. (2020) · Regenerative Therapy · doi:10.1016/j.reth.2020.07.002 · Cited by 15 · see citing works
Establishing Human Lung Organoids and Proximal Differentiation to Generate Mature Airway Organoids
Li, C., Chiu, M. C., Yu, Y., Liu, X., Xiao, D., Huang, J., Wan, Z., & Zhou, J. (2022) · Journal of Visualized Experiments · doi:10.3791/63684 · Cited by 19 · see citing works
Breakthroughs in microbiology made possible with organoids
Ramírez‐Flores, C. J., & Knoll, L. J. (2021) · PLoS Pathogens · doi:10.1371/journal.ppat.1010080 · Cited by 14 · see citing works
The diverse actions of cytoskeletal vimentin in bacterial infection and host defense
Miao, C., Zhao, S., Etienne‐Manneville, S., & Jiu, Y. (2023) · Journal of Cell Science · doi:10.1242/jcs.260509 · Cited by 14 · see citing works
Naumann, M., Ferino, L., Sharafutdinov, I., & Backert, S. (2023) · Current topics in microbiology and immunology · doi:10.1007/978-3-031-47331-9_8 · Cited by 14 · see citing works
Kang, D. W., Noh, Y. N., Hwang, W. C., Choi, K., & Min, D. S. (2016) · Biochemical Pharmacology · doi:10.1016/j.bcp.2016.06.003 · Cited by 14 · see citing works
3D Organoids: An Untapped Platform for Studying Host–Microbiome Interactions in Esophageal Cancers
Flashner, S. P., Yan, K. S., & Nakagawa, H. (2021) · Microorganisms · doi:10.3390/microorganisms9112182 · Cited by 13 · see citing works
Modelling adult stem cells and their niche in health and disease with epithelial organoids
Szabó, L., Seubert, A. C., & Kretzschmar, K. (2022) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2022.09.006 · Cited by 14 · see citing works
Chiu, M. C., Li, C., Yu, Y., Liu, X., Huang, J., Wan, Z., Yuen, K.-Y., & Zhou, J. (2023) · BIO-PROTOCOL · doi:10.21769/bioprotoc.4657 · Cited by 12 · see citing works
Next-Generation Human Liver Models for Antimalarial Drug Assays
Kulkeaw, K. (2021) · Antibiotics · doi:10.3390/antibiotics10060642 · Cited by 11 · see citing works
Vallejo-Flores, G., Torres, J., Sandoval‐Montes, C., Arévalo-Romero, H., Meza, I., Camorlinga‐Ponce, M., Torres‐Morales, J., Chávez-Rueda, A. K., Legorreta-Haquet, M. V., & Fuentes‐Pananá, E. M. (2015) · BioMed Research International · doi:10.1155/2015/761501 · Cited by 11 · see citing works
Zhao, H., Collet, C., Peng, D., Sinha, U. K., & Lin, D. (2022) · Computational and Structural Biotechnology Journal · doi:10.1016/j.csbj.2022.09.026 · Cited by 10 · see citing works
- Authors
- Wroblewski, L. E., Piazuelo, M. B., Chaturvedi, R., Schumacher, M., Aihara, E., Feng, R., Noto, J. M., Delgado, A., Israel, D. A., Zavros, Y., Montrose, M. H., Shroyer, N., Correa, P., Wilson, K. T., & Peek, R. M.
- Affiliations
- Vanderbilt University (US)
- University of Cincinnati (US)
- Cincinnati Children's Hospital Medical Center (US)
- Corresponding author
- Peek, Richard M
- ORCID
- Venue
- Gut
- Publisher
- BMJ
- Published
- 2014-08-14
- Volume
- 64
- Issue
- 5
- Pages
- 720-730
- ISSN
- 0017-5749 (ISSN-L)
- 1468-3288
- PMC
- PMC4329117
- OpenAlex
- W2164422245
- Cited by
- 143
- References
- 53
- Citations by year
- 2026: 6 · 2025: 3 · 2024: 4 · 2023: 13 · 2022: 16 · 2021: 19 · 2020: 14 · 2019: 12 · 2018: 10 · 2017: 16 · 2016: 18 · 2015: 11 · 2014: 1
- FWCI
- 15.22
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Gut (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- U.S. Department of Veterans Affairs (I01 BX001453)
- National Institutes of Health (1k01at007324-01, CA 116087, CA-77955, DK 058404)
- National Cancer Institute (CA028842, CA116087), R29CA077955, P01CA028842, CA-77955, R01CA190612, CA 153539, F32CA153539, R01CA077955, P01CA116087)
- National Institute of Diabetes and Digestive and Kidney Diseases (DK058404, R01DK058587, R01DK054940, R01DK083402, R01DK053620, DK-58587, DK053620, R01DK073902, P30DK058404, P30DK078392)
- National Center for Complementary and Integrative Health (K01-AT-007324, R01AT004821, AT 007324)
- Topics
- Health Sciences › Medicine › Surgery › Helicobacter pylori-related gastroenterology studies
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Gastric Cancer Management and Outcomes
- Keywords
- Helicobacter pylori, claudin-7, gastric epithelial cells, MKN28 cells, β-catenin, snails, tight junctions, apical junctions, epithelial cell proliferation, gastric cancer risk, host-pathogen interaction
- MeSH terms
- Snail Family Transcription Factors, Animals, Cells, Cultured, Epithelial Cells, Gastric Mucosa, Humans, Mice, Inbred C57BL, Transcription Factors, Helicobacter pylori, Helicobacter Infections, Coculture Techniques, Cell Proliferation, beta Catenin, Claudins
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
