Tight Junctions, Intestinal Permeability, and Autoimmunity
Celiac Disease and Type 1 Diabetes Paradigms
Funding: Work presented in this review was supported in parts by grants from the National Institutes of Health Grants DK‐48373 and DK‐078699 to AF and by the innovative pilot grant, Dutch Diabetes Foundation, grant number 2006.11.019 to JV.
Abstract
Autoimmune diseases are characterized by tissue damage and loss of function due to an immune response that is directed against specific organs. This review is focused on celiac disease (CD), an autoimmune enteropathy, and type 1 diabetes (T1D), a hyperglycosaemia caused by a destructive autoimmune process targeting the insulin‐producing pancreatic islet cells. Even if environmental factors and genetic susceptibility are clearly involved in the pathogenesis of autoimmunity, for most autoimmune disorders there is no or little knowledge about the causing agent or genetic makeup underlying the disease. In this respect, CD represents a unique autoimmune disorder because a close genetic association with HLA‐DQ2 or HLA‐DQ8 haplotypes and, more importantly, the environmental trigger (the gliadin fraction of gluten‐containing grains wheat, barley, and rye) are known. Conversely, the trigger for autoimmune destruction of pancreatic ß cells in T1D is unclear. Interestingly, recent data suggest that gliadin is also involved in the pathogenesis of T1D. There is growing evidence that increased intestinal permeability plays a pathogenic role in various autoimmune diseases including CD and T1D. Therefore, we hypothesize that besides genetic and environmental factors, loss of intestinal barrier function is necessary to develop autoimmunity. In this review, each of these components will be briefly reviewed.
Number of times cited: 101
- Lisa Rizzetto, Francesca Fava, Kieran M. Tuohy and Carlo Selmi, Connecting the immune system, systemic chronic inflammation and the gut microbiome: The role of sex, Journal of Autoimmunity, 10.1016/j.jaut.2018.05.008, (2018).
- M. C. Buscarinu, S. Romano, R. Mechelli, R. Pizzolato Umeton, M. Ferraldeschi, A. Fornasiero, R. Reniè, B. Cerasoli, E. Morena, C. Romano, N. D. Loizzo, R. Umeton, M. Salvetti and G. Ristori, Intestinal Permeability in Relapsing-Remitting Multiple Sclerosis, Neurotherapeutics, 10.1007/s13311-017-0582-3, 15, 1, (68-74), (2017).
- Annika Borde and Annika Åstrand, Alopecia areata and the gut—the link opens up for novel therapeutic interventions, Expert Opinion on Therapeutic Targets, 10.1080/14728222.2018.1481504, 22, 6, (503-511), (2018).
- Benjamin Lebwohl, David S Sanders and Peter H R Green, Coeliac disease, The Lancet, 10.1016/S0140-6736(17)31796-8, 391, 10115, (70-81), (2018).
- Bradley Leech, Janet Schloss and Amie Steel, Health services research as a framework for expanding a whole systems research agenda in complementary and integrative medicine: The example of intestinal permeability, European Journal of Integrative Medicine, 10.1016/j.eujim.2017.11.003, 17, (22-25), (2018).
- Anja Schuetz, Veselina Radusheva, Susanne M. Krug and Udo Heinemann, Crystal structure of the tricellulin C‐terminal coiled‐coil domain reveals a unique mode of dimerization, Annals of the New York Academy of Sciences, 1405, 1, (147-159), (2017).
- Joana Clímaco Henggeler, Manuel Veríssimo and Fernando Ramos, Non-coeliac gluten sensitivity: A review of the literature, Trends in Food Science & Technology, 10.1016/j.tifs.2017.05.018, 66, (84-92), (2017).
- B.S. Rashmi and D. Gayathri, Molecular characterization of gluten hydrolysing Bacillus sp. and their efficacy and biotherapeutic potential as probiotics using Caco‐2 cell line, Journal of Applied Microbiology, 123, 3, (759-772), (2017).
- Antonella Orlando, Michele Linsalata, Benedetta D'Attoma and Francesco Russo, Changes in paracellular permeability induced by Pepsin-Trypsin digested Gliadin (PTG): Role of polyamines in the Lactobacillus rhamnosus GG protective action, Journal of Functional Foods, 36, (52), (2017).
- Dagmar Ehling, Anticipating Diabetes, Obesity and Polycystic Ovarian Syndrome and Applying Integrative Techniques Using Functional and Oriental Medicine, Anticipation and Medicine, 10.1007/978-3-319-45142-8_18, (293-307), (2016).
- Gabriel Skogberg, Sonya Jackson and Annika Åstrand, Mechanisms of tolerance and potential therapeutic interventions in Alopecia Areata, Pharmacology & Therapeutics, 10.1016/j.pharmthera.2017.05.008, 179, (102-110), (2017).
- Tamara Vorobjova, Helerin Raikkerus, Lumme Kadaja, Ija Talja, Oivi Uibo, Kaire Heilman and Raivo Uibo, Circulating Zonulin Correlates with Density of Enteroviruses and Tolerogenic Dendritic Cells in the Small Bowel Mucosa of Celiac Disease Patients, Digestive Diseases and Sciences, 10.1007/s10620-016-4403-z, 62, 2, (358-371), (2016).
- Wangfeng Cai, Ying Ran, Yanni Li, Bangmao Wang and Lu Zhou, Intestinal microbiome and permeability in patients with autoimmune hepatitis, Best Practice & Research Clinical Gastroenterology, 10.1016/j.bpg.2017.09.013, 31, 6, (669-673), (2017).
- Tamara Vorobjova, Krista Ress, Katrin Luts, Oivi Uibo and Raivo Uibo, The impact of langerin (CD207)+ dendritic cells and FOXP3+ Treg cells in the small bowel mucosa of children with celiac disease and atopic dermatitis in comparison to children with functional gastrointestinal disorders, APMIS, 124, 8, (689-696), (2016).
- Susanne W. Bruun, Knud Josefsen, Julia T. Tanassi, Aleš Marek, Martin H. F. Pedersen, Ulrik Sidenius, Martin Haupt-Jorgensen, Julie C. Antvorskov, Jesper Larsen, Niels H. Heegaard and Karsten Buschard, Large Gliadin Peptides Detected in the Pancreas of NOD and Healthy Mice following Oral Administration, Journal of Diabetes Research, 10.1155/2016/2424306, 2016, (1-11), (2016).
- Fiona McCartney, John P. Gleeson and David J. Brayden, Safety concerns over the use of intestinal permeation enhancers: A mini-review, Tissue Barriers, 10.1080/21688370.2016.1176822, 4, 2, (e1176822), (2016).
- Jayashree Dolpady, Chiara Sorini, Caterina Di Pietro, Ilaria Cosorich, Roberto Ferrarese, Diego Saita, Massimo Clementi, Filippo Canducci and Marika Falcone, Oral Probiotic VSL#3 Prevents Autoimmune Diabetes by Modulating Microbiota and Promoting Indoleamine 2,3-Dioxygenase-Enriched Tolerogenic Intestinal Environment, Journal of Diabetes Research, 10.1155/2016/7569431, 2016, (1-12), (2016).
- Albert J Czaja, Factoring the intestinal microbiome into the pathogenesis of autoimmune hepatitis, World Journal of Gastroenterology, 10.3748/wjg.v22.i42.9257, 22, 42, (9257), (2016).
- Ayumi Abe, Kenichi Takano, Takashi Kojima, Kazuaki Nomura, Takuya Kakuki, Yakuto Kaneko, Motohisa Yamamoto, Hiroki Takahashi and Tetsuo Himi, Interferon-gamma increased epithelial barrier function via upregulating claudin-7 expression in human submandibular gland duct epithelium, Journal of Molecular Histology, 10.1007/s10735-016-9667-2, 47, 3, (353-363), (2016).
- Xiaoping Yang, Duobing Zou, Songtao Tang, Tingting Fan, Huan Su, Ruolei Hu, Qing Zhou, Shuyu Gui, Li Zuo and Yuan Wang, Ameliorative effect of melatonin against increased intestinal permeability in diabetic rats: possible involvement of MLCK-dependent MLC phosphorylation, Molecular and Cellular Biochemistry, 416, 1-2, (23), (2016).
- María G. Herrera, Tania V. Veuthey and Verónica I. Dodero, Self-organization of gliadin in aqueous media under physiological digestive pHs, Colloids and Surfaces B: Biointerfaces, 141, (565), (2016).
- Anton Emmanuel, Darryl Landis, Mark Peucker and A Pali S Hungin, Faecal biomarker patterns in patients with symptoms of irritable bowel syndrome, Frontline Gastroenterology, 10.1136/flgastro-2015-100651, 7, 4, (275-282), (2016).
- Shahryar Khaleghi, Josephine M. Ju, Abhinav Lamba and Joseph A. Murray, The potential utility of tight junction regulation in celiac disease: focus on larazotide acetate, Therapeutic Advances in Gastroenterology, 9, 1, (37), (2016).
- Hanna Karakuła-Juchnowicz, Patrycja Szachta, Aneta Opolska, Justyna Morylowska-Topolska, Mirosława Gałęcka, Dariusz Juchnowicz, Paweł Krukow and Zofia Lasik, The role of IgG hypersensitivity in the pathogenesis and therapy of depressive disorders, Nutritional Neuroscience, (1), (2016).
- Heitor S. P. de Souza and Claudio Fiocchi, Immunopathogenesis of IBD: current state of the art, Nature Reviews Gastroenterology & Hepatology, 13, 1, (13), (2016).
- James T. Rosenbaum, Phoebe Lin and Mark Asquith, Does the Microbiome Cause B27-related Acute Anterior Uveitis?, Ocular Immunology and Inflammation, 24, 4, (440), (2016).
- Bárbara S. Rocha, Carla Nunes and João Laranjinha, Tuning constitutive and pathological inflammation in the gut via the interaction of dietary nitrate and polyphenols with host microbiome, The International Journal of Biochemistry & Cell Biology, 10.1016/j.biocel.2016.10.021, 81, (393-402), (2016).
- Asha Mishra, Shyam Prakash, Vishnubhatla Sreenivas, Taposh K. Das, Vineet Ahuja, Siddhartha D. Gupta and Govind K. Makharia, Structural and Functional Changes in the Tight Junctions of Asymptomatic and Serology-negative First-degree Relatives of Patients With Celiac Disease, Journal of Clinical Gastroenterology, 50, 7, (551), (2016). 2016 IEEE-EMBS International Conference on Biomedical and Health Informatics (BHI), (2016).D. Boschetto, H. Mirzaei, R. W. L. Leong and E. GrisanSuperpixel-based automatic segmentation of villi in confocal endomicroscopy16810.1109/BHI.2016.7455861
- Mingtao Chang, Yang Li, Dong Liu, Lianyang Zhang, Hongguang Zhang, Hao Tang and Huayu Zhang, Melatonin prevents secondary intra-abdominal hypertension in rats possibly through inhibition of the p38 MAPK pathway, Free Radical Biology and Medicine, 97, (192), (2016).
- Susanna Hamari, Tiina Kirveskoski, Virpi Glumoff, Petri Kulmala, Olli Simell, Mikael Knip, Jorma Ilonen and Riitta Veijola, CD4+ T‐cell proliferation responses to wheat polypeptide stimulation in children at different stages of type 1 diabetes autoimmunity, Pediatric Diabetes, 16, 3, (177-188), (2015).
- Chen‐Yu Hsieh, Toshifumi Osaka, Eri Moriyama, Yasuhiro Date, Jun Kikuchi and Satoshi Tsuneda, Strengthening of the intestinal epithelial tight junction by Bifidobacterium bifidum, Physiological Reports, 3, 3, (2015).
- I. Nasr, J. Messing, I.H. Nasr and P.J. Ciclitira, Detection and control of gluten as a food allergen, Handbook of Food Allergen Detection and Control, 10.1533/9781782420217.3.367, (367-377), (2015).
- Tamara Vorobjova, Increased density of tolerogenic dendritic cells in the small bowel mucosa of celiac patients, World Journal of Gastroenterology, 21, 2, (439), (2015).
- K. L. Fogg and S. C. Zyblewski, Nutrition and Growth in Neonates Undergoing Cardiac Surgery, NeoReviews, 10.1542/neo.16-3-e144, 16, 3, (e144-e151), (2015).
- Min Yu, Songwei Yang, Yuan Qiu, Guoqing Chen, Wensheng Wang, Chao Xu, Wenqiang Cai, Lihua Sun, Weidong Xiao and Hua Yang, Par-3 modulates intestinal epithelial barrier function through regulating intracellular trafficking of occludin and myosin light chain phosphorylation, Journal of Gastroenterology, 50, 11, (1103), (2015).
- Mairi H McLean, Dario Dieguez, Lindsey M Miller and Howard A Young, Does the microbiota play a role in the pathogenesis of autoimmune diseases?, Gut, 10.1136/gutjnl-2014-308514, 64, 2, (332-341), (2014).
- Xi Xing, Ronglin Jiang, Lingcong Wang, Shu Lei, Yihui Zhi, Yanchun Wu, Meifei Zhu, Liquan Huang, Guolian Xia and Zheqi Chen, Shenfu injection alleviates intestine epithelial damage in septic rats, The American Journal of Emergency Medicine, 33, 11, (1665), (2015).
- M.E. Mejía-León, K.M. Ruiz-Dyck and A.M. Calderón de la Barca, HLA-DQ genetic risk gradient for type 1 diabetes and celiac disease in north-western Mexico, Revista de Gastroenterología de México (English Edition), 80, 2, (135), (2015).
- Nicole J. Kellow and Melinda T. Coughlan, Effect of diet-derived advanced glycation end products on inflammation, Nutrition Reviews, 73, 11, (737), (2015).
- Cheryl de Vallière, Solange Vidal, Ieuan Clay, Giorgia Jurisic, Irina Tcymbarevich, Silvia Lang, Marie-Gabrielle Ludwig, Michal Okoniewski, Jyrki J. Eloranta, Gerd A. Kullak-Ublick, Carsten A. Wagner, Gerhard Rogler and Klaus Seuwen, The pH-sensing receptor OGR1 improves barrier function of epithelial cells and inhibits migration in an acidic environment, American Journal of Physiology-Gastrointestinal and Liver Physiology, 309, 6, (G475), (2015).
- J Luettig, R Rosenthal, C Barmeyer and JD Schulzke, Claudin-2 as a mediator of leaky gut barrier during intestinal inflammation, Tissue Barriers, 3, 1-2, (e977176), (2015).
- Guillermo Vela, Peter Stark, Michael Socha, Ann Katrin Sauer, Simone Hagmeyer and Andreas M. Grabrucker, Zinc in Gut-Brain Interaction in Autism and Neurological Disorders, Neural Plasticity, 2015, (1), (2015).
- Eric M. Brown, Marta Wlodarska, Benjamin P. Willing, Pascale Vonaesch, Jun Han, Lisa A. Reynolds, Marie-Claire Arrieta, Marco Uhrig, Roland Scholz, Oswaldo Partida, Christoph H. Borchers, Philippe J. Sansonetti and B. Brett Finlay, Diet and specific microbial exposure trigger features of environmental enteropathy in a novel murine model, Nature Communications, 6, 1, (2015).
- M.E. Mejía-León, K.M. Ruiz-Dyck and A.M. Calderón de la Barca, Gradiente de riesgo genético HLA-DQ para diabetes tipo 1 y enfermedad celíaca en el noroeste de México, Revista de Gastroenterología de México, 80, 2, (135), (2015).
- M. O. Ogese, K. Saide, L. Faulkner, P. Whitaker, D. Peckham, A. Alfirevic, D. M. Baker, A. Sette, M. Pirmohamed, B. K. Park and D. J. Naisbitt, HLA‐DQ allele‐restricted activation of nitroso sulfamethoxazole‐specific CD4‐positive T lymphocytes from patients with cystic fibrosis, Clinical & Experimental Allergy, 45, 8, (1305-1316), (2015).
- Drew Sinatra, Naturopathic Medicine and the Prevention and Treatment of Cardiovascular Disease, Nutritional and Integrative Strategies in Cardiovascular Medicine, 10.1201/b18282-9, (179-204), (2015).
- Elke Gülden, F. Susan Wong and Li Wen, The gut microbiota and Type 1 Diabetes, Clinical Immunology, 159, 2, (143), (2015).
- Maria Papastamataki, Ioannis Papassotiriou, Anastasia Bartzeliotou, Andriani Vazeou, Eleftheria Roma, George P. Chrousos and Christina Kanaka‐Gantenbein, Incretins, amylin and other gut‐brain axis hormones in children with coeliac disease , European Journal of Clinical Investigation, 44, 1, (74-82), (2013).
- Saskia van Hemert, Anne C. Breedveld, Jörgen M. P. Rovers, Jan P. W. Vermeiden, Ben J. M. Witteman, Marcel G. Smits and Nicole M. de Roos, Migraine Associated with Gastrointestinal Disorders: Review of the Literature and Clinical Implications, Frontiers in Neurology, 5, (2014).
- Isabelle M. E. Lacroix and Eunice C. Y. Li-Chan, Investigation of the Putative Associations Between Dairy Consumption and Incidence of Type 1 and Type 2 Diabetes, Critical Reviews in Food Science and Nutrition, 54, 4, (411), (2014).
- Dion Smyth, Theresa Smyth and Anne Phillips, Diabetes and coeliac disease: implementing a gluten-free diet, Practice Nursing, 25, 6, (292), (2014).
- Mehrnaz Nouri, Anders Bredberg, Björn Weström, Shahram Lavasani and Jason R. Lees, Intestinal Barrier Dysfunction Develops at the Onset of Experimental Autoimmune Encephalomyelitis, and Can Be Induced by Adoptive Transfer of Auto-Reactive T Cells, PLoS ONE, 9, 9, (e106335), (2014).
- Isabel Polanco Allué and Eva Martinez-Ojinaga Nodal, Sensibilidad al gluten no celíaca: realidad o ficción, Anales de Pediatría Continuada, 12, 6, (289), (2014).
- Pasquale Mansueto, Aurelio Seidita, Alberto D’Alcamo and Antonio Carroccio, Non-Celiac Gluten Sensitivity: Literature Review, Journal of the American College of Nutrition, 33, 1, (39), (2014).
- P. Chen, F. Takeuchi, J.-Y. Lee, H. Li, J.-Y. Wu, J. Liang, J. Long, Y. Tabara, M. O. Goodarzi, M. A. Pereira, Y. J. Kim, M. J. Go, D. O. Stram, E. Vithana, C.-C. Khor, J. Liu, J. Liao, X. Ye, Y. Wang, L. Lu, T. L. Young, J. Lee, A. C. Thai, C.-Y. Cheng, R. M. van Dam, Y. Friedlander, C.-K. Heng, W.-P. Koh, C.-H. Chen, L.-C. Chang, W.-H. Pan, Q. Qi, M. Isono, W. Zheng, Q. Cai, Y. Gao, K. Yamamoto, K. Ohnaka, R. Takayanagi, Y. Kita, H. Ueshima, C. A. Hsiung, J. Cui, W. H.- H. Sheu, J. I. Rotter, Y.-D. I. Chen, C. Hsu, Y. Okada, M. Kubo, A. Takahashi, T. Tanaka, F. J. A. van Rooij, S. K. Ganesh, J. Huang, T. Huang, J. Yuan, J.-Y. Hwang, M. D. Gross, T. L. Assimes, T. Miki, X.-O. Shu, L. Qi, Y.-T. Chen, X. Lin, T. Aung, T.-Y. Wong, Y.-Y. Teo, B.-J. Kim, N. Kato and E.-S. Tai, Multiple Nonglycemic Genomic Loci Are Newly Associated With Blood Level of Glycated Hemoglobin in East Asians, Diabetes, 10.2337/db13-1815, 63, 7, (2551-2562), (2014).
- M. Maes, M. Kubera, J.‐C. Leunis, M. Berk, M. Geffard and E. Bosmans, In depression, bacterial translocation may drive inflammatory responses, oxidative and nitrosative stress (O&NS), and autoimmune responses directed against O&NS‐damaged neoepitopes, Acta Psychiatrica Scandinavica, 127, 5, (344-354), (2012).
- Amani Mankaï, Yosra Thabet, Wiem Manoubi, Achouak Achour, Wahiba Sakly and Ibtissem Ghedira, Anti-Saccharomyces cerevisiaeAntibodies Are Elevated in Graves’ Disease But Not in Hashimoto’s Thyroiditis, Endocrine Research, 38, 2, (98), (2013).
- Mona Landin-Olsson, Magnus Hillman and Charlotte Erlanson-Albertsson, Is type 1 diabetes a food-induced disease?, Medical Hypotheses, 10.1016/j.mehy.2013.03.046, 81, 2, (338-342), (2013).
- Sjoerd F. Bakker, Maarten E. Tushuizen, Wilhelmina H. Stokvis-Brantsma, Henk J. Aanstoot, Per Winterdijk, Petra A. van Setten, Boudewina M. von Blomberg, Chris J. Mulder and Suat Simsek, Frequent delay of coeliac disease diagnosis in symptomatic patients with type 1 diabetes mellitus: Clinical and genetic characteristics, European Journal of Internal Medicine, 10.1016/j.ejim.2013.01.016, 24, 5, (456-460), (2013).
- Eugenia Lauret and Luis Rodrigo, Celiac Disease and Autoimmune-Associated Conditions, BioMed Research International, 2013, (1), (2013).
- Martha R. Herbert and Cindy Sage, Autism and EMF? Plausibility of a pathophysiological link – Part I, Pathophysiology, 10.1016/j.pathophys.2013.08.001, 20, 3, (191-209), (2013).
- R. Jaffe, Functional Assessment of Gastrointestinal Health, Bioactive Food as Dietary Interventions for Liver and Gastrointestinal Disease, 10.1016/B978-0-12-397154-8.00002-6, (23-35), (2013).
- Martha R. Herbert and Julie A. Buckley, Autism and Dietary Therapy, Journal of Child Neurology, 10.1177/0883073813488668, 28, 8, (975-982), (2013).
- Rian M. Nijmeijer, Hjalmar C. van Santvoort, Alexandra Zhernakova, Steffen Teller, Jonas A. Scheiber, Carolien G. de Kovel, Marc G. H. Besselink, Jeroen T. J. Visser, Femke Lutgendorff, Thomas L. Bollen, Marja A. Boermeester, Ger T. Rijkers, Frank U. Weiss, Julia Mayerle, Markus M. Lerch, Hein G. Gooszen, Louis M. A. Akkermans, Cisca Wijmenga and Klaus Brusgaard, Association Analysis of Genetic Variants in the Myosin IXB Gene in Acute Pancreatitis, PLoS ONE, 8, 12, (e85870), (2013).
- Giuseppe Iacomino, Olga Fierro, Sabato D’Auria, Gianluca Picariello, Pasquale Ferranti, Claudia Liguori, Francesco Addeo and Gianfranco Mamone, Structural Analysis and Caco-2 Cell Permeability of the Celiac-Toxic A-Gliadin Peptide 31–55, Journal of Agricultural and Food Chemistry, 10.1021/jf3045523, 61, 5, (1088-1096), (2013).
- J. T. J. Visser, N. A. Bos, L. F. Harthoorn, F. Stellaard, S. Beijer‐Liefers, J. Rozing and E. A. F. Tol, Potential mechanisms explaining why hydrolyzed casein‐based diets outclass single amino acid‐based diets in the prevention of autoimmune diabetes in diabetes‐prone BB rats, Diabetes/Metabolism Research and Reviews, 28, 6, (505-513), (2012).
- Diane Mathis and Christophe Benoist, The influence of the microbiota on type‐1 diabetes: on the threshold of a leap forward in our understanding, Immunological Reviews, 245, 1, (239-249), (2011).
- M. Camilleri, K. Madsen, R. Spiller, B. G. Van Meerveld and G. N. Verne, Intestinal barrier function in health and gastrointestinal disease, Neurogastroenterology & Motility, 24, 6, (503-512), (2012).
- Andrea Gerard Gonzalez and Saleh Adi, Type 1 Diabetes Mellitus, Nutritional and Therapeutic Interventions for Diabetes and Metabolic Syndrome, 10.1016/B978-0-12-385083-6.00001-2, (3-13), (2012).
- Thomas Y. Ma, James M. Anderson and Jerrold R. Turner, Tight Junctions and the Intestinal Barrier, Physiology of the Gastrointestinal Tract, 10.1016/B978-0-12-382026-6.00038-5, (1043-1088), (2012).
- Bu-Yeo Kim, Sung-Gon Yu, Jong-Yeol Kim and Kwang Hoon Song, Pathways Involved inSasangConstitution from Genome-Wide Analysis in a Korean Population, The Journal of Alternative and Complementary Medicine, 18, 11, (1070), (2012).
- Stella Korsgren, Ylva Molin, Kaija Salmela, Torbjörn Lundgren, Åsa Melhus and Olle Korsgren, On the Etiology of Type 1 Diabetes, The American Journal of Pathology, 181, 5, (1735), (2012).
- Alessio Fasano, Leaky Gut and Autoimmune Diseases, Clinical Reviews in Allergy & Immunology, 10.1007/s12016-011-8291-x, 42, 1, (71-78), (2011).
- Matthew Metzgar, Externalities from grain consumption: a survey, International Journal of Food Sciences and Nutrition, 63, 4, (453), (2012).
- N. Bizzaro, R. Tozzoli, D. Villalta, M. Fabris and E. Tonutti, Cutting-Edge Issues in Celiac Disease and in Gluten Intolerance, Clinical Reviews in Allergy & Immunology, 42, 3, (279), (2012).
- G. De Palma, J. Kamanova, J. Cinova, M. Olivares, H. Drasarova, L. Tuckova and Y. Sanz, Modulation of phenotypic and functional maturation of dendritic cells by intestinal bacteria and gliadin: relevance for celiac disease, Journal of Leukocyte Biology, 92, 5, (1043-1054), (2012).
- Umberto Volta, Francesco Tovoli and Giacomo Caio, Clinical and immunological features of celiac disease in patients with Type 1 diabetes mellitus, Expert Review of Gastroenterology & Hepatology, 10.1586/egh.11.38, 5, 4, (479-487), (2014).
- Jana Cinova, Giada De Palma, Renata Stepankova, Olga Kofronova, Miloslav Kverka, Yolanda Sanz, Ludmila Tuckova and François Leulier, Role of Intestinal Bacteria in Gliadin-Induced Changes in Intestinal Mucosa: Study in Germ-Free Rats, PLoS ONE, 6, 1, (e16169), (2011).
- Craig E Taplin, Majid Mojibian, Melissa Simpson, Iman Taki, Edwin Liu, Edward J Hoffenberg, Jill M Norris, Fraser W Scott and Marian Rewers, Antibodies to the Wheat Storage Globulin Glo-3A in Children Before and at Diagnosis of Celiac Disease, Journal of Pediatric Gastroenterology and Nutrition, 10.1097/MPG.0b013e3181f18c7b, 52, 1, (21-25), (2011).
- Tamara Vorobjova, Oivi Uibo, Ivi Ojakivi, Kaupo Teesalu, Marina Panarina, Kaire Heilman and Raivo Uibo, Lower Expression of Tight Junction Protein 1 Gene and Increased FOXP3 Expression in the Small Bowel Mucosa in Coeliac Disease and Associated Type 1 Diabetes Mellitus, International Archives of Allergy and Immunology, 10.1159/000324456, 156, 4, (451-461), (2011).
- M. A. Kriegel, E. Sefik, J. A. Hill, H.-J. Wu, C. Benoist and D. Mathis, Naturally transmitted segmented filamentous bacteria segregate with diabetes protection in nonobese diabetic mice, Proceedings of the National Academy of Sciences, 10.1073/pnas.1108924108, 108, 28, (11548-11553), (2011).
- Raivo Uibo, Marina Panarina, Kaupo Teesalu, Ija Talja, Epp Sepp, Meeme Utt, Marika Mikelsaar, Kaire Heilman, Oivi Uibo and Tamara Vorobjova, Celiac disease in patients with type 1 diabetes: a condition with distinct changes in intestinal immunity?, Cellular and Molecular Immunology, 10.1038/cmi.2010.66, 8, 2, (150-156), (2011).
- Siv Ahrne and Marie-Louise Johansson Hagslatt, Effect of Lactobacilli on Paracellular Permeability in the Gut, Nutrients, 3, 12, (104), (2011).
- Josceli Maria Tenório, Anderson Diniz Hummel, Frederico Molina Cohrs, Vera Lucia Sdepanian, Ivan Torres Pisa and Heimar de Fátima Marin, Artificial intelligence techniques applied to the development of a decision–support system for diagnosing celiac disease, International Journal of Medical Informatics, 80, 11, (793), (2011).
- Stelios F Assimakopoulos, Enterocytes’ tight junctions: From molecules to diseases, World Journal of Gastrointestinal Pathophysiology, 2, 6, (123), (2011).
- Raivo Uibo, Zhigang Tian and M Eric Gershwin, Celiac disease: a model disease for gene–environment interaction, Cellular and Molecular Immunology, 10.1038/cmi.2010.62, 8, 2, (93-95), (2011).
- Ragna Lind, Gülen Arslan Lied, Kristine Lillestøl, Jørgen Valeur and Arnold Berstad, Do psychological factors predict symptom severity in patients with subjective food hypersensitivity?, Scandinavian Journal of Gastroenterology, 45, 7-8, (835), (2010).
- Laura de Magistris, Valeria Familiari, Antonio Pascotto, Anna Sapone, Alessandro Frolli, Patrizia Iardino, Maria Carteni, Mario De Rosa, Ruggiero Francavilla, Gabriele Riegler, Roberto Militerni and Carmela Bravaccio, Alterations of the Intestinal Barrier in Patients With Autism Spectrum Disorders and in Their First-degree Relatives, Journal of Pediatric Gastroenterology and Nutrition, 51, 4, (418), (2010).
- Wahiba Sakly, Amani Mankaï, Nabil Sakly, Yosra Thabet, Achouak Achour, Leila Ghedira-Besbes, Moncef Jeddi and Ibtissem Ghedira, Anti-Saccharomyces cerevisiae Antibodies are Frequent in Type 1 Diabetes, Endocrine Pathology, 21, 2, (108), (2010).
- J. T. J. Visser, K. Lammers, A. Hoogendijk, M. W. Boer, S. Brugman, S. Beijer-Liefers, A. Zandvoort, H. Harmsen, G. Welling, F. Stellaard, N. A. Bos, A. Fasano and J. Rozing, Restoration of impaired intestinal barrier function by the hydrolysed casein diet contributes to the prevention of type 1 diabetes in the diabetes-prone BioBreeding rat, Diabetologia, 53, 12, (2621), (2010).
- Dorottya Nagy Szakál, Hajnalka Győrffy, András Arató, Áron Cseh, Kriszta Molnár, Mária Papp, Antal Dezsőfi and Gábor Veres, Mucosal expression of claudins 2, 3 and 4 in proximal and distal part of duodenum in children with coeliac disease, Virchows Archiv, 456, 3, (245), (2010).
- Patricia Ewert, Sergio Aguilera, Cecilia Alliende, Yoon‐Jeoung Kwon, Amelina Albornoz, Claudio Molina, Ulises Urzúa, Andrew F. G. Quest, Nancy Olea, Paola Pérez, Isabel Castro, María‐José Barrera, Rafael Romo, Marcela Hermoso, Cecilia Leyton and María‐Julieta González, Disruption of tight junction structure in salivary glands from Sjögren's syndrome patients is linked to proinflammatory cytokine exposure, Arthritis & Rheumatism, 62, 5, (1280-1289), (2010).
- Jörg‐Dieter Schulzke and Michael Fromm, Tight Junctions, Annals of the New York Academy of Sciences, 1165, 1, (1-6), (2009).
- Brigitte Sonier, Christopher Patrick, Prabha Ajjikuttira and Fraser W. Scott, Intestinal Immune Regulation as a Potential Diet-Modifiable Feature of Gut Inflammation and Autoimmunity, International Reviews of Immunology, 10.3109/08830180903208329, 28, 6, (414-445), (2009).
- Atiqah Azhari, Farouq Azizan and Gianluca Esposito, A systematic review of gut‐immune‐brain mechanisms in Autism Spectrum Disorder, Developmental Psychobiology, , (2018).
- Stefania De Santis, Elisabetta Cavalcanti, Mauro Mastronardi, Emilio Jirillo and Marcello Chieppa, Nutritional Keys for Intestinal Barrier Modulation, Frontiers in Immunology, 10.3389/fimmu.2015.00612, 6, (2015).
- Amy Masson, Bente Talseth-Palmer, Tiffany-Jane Evans, Desma Grice, Konsta Duesing, Garry Hannan and Rodney Scott, Copy Number Variation in Hereditary Non-Polyposis Colorectal Cancer, Genes, 10.3390/genes4040536, 4, 4, (536-555), (2013).
- Nitya Jain and W. Allan Walker, Diet and host–microbial crosstalk in postnatal intestinal immune homeostasis, Nature Reviews Gastroenterology & Hepatology, 10.1038/nrgastro.2014.153, 12, 1, (14-25), (2014)., (2014).
- Tingting Jiang, Xuejin Gao, Chao Wu, Feng Tian, Qiucheng Lei, Jingcheng Bi, Bingxian Xie, Hong Wang, Shuai Chen and Xinying Wang, Apple-Derived Pectin Modulates Gut Microbiota, Improves Gut Barrier Function, and Attenuates Metabolic Endotoxemia in Rats with Diet-Induced Obesity, Nutrients, 10.3390/nu8030126, 8, 3, (126), (2016).
- Ann-Kathrin Uhde, Vanessa Herder, Muhammad Akram Khan, Malgorzata Ciurkiewicz, Dirk Schaudien, René Teich, Stefan Floess, Wolfgang Baumgärtner, Jochen Huehn and Andreas Beineke, Viral Infection of the Central Nervous System Exacerbates Interleukin-10 Receptor Deficiency-Mediated Colitis in SJL Mice, PLOS ONE, 10.1371/journal.pone.0161883, 11, 9, (e0161883), (2016).




