References
- Pizarro TT, Pastorelli L, Bamias G, Garg RR, Reuter BK, Mercado JR, et al. SAMP1/YitFc mouse strain: a spontaneous model of Crohn’s disease-like ileitis. Inflamm Bowel Dis. 2011;17:1–16. doi:https://doi.org/10.1002/ibd.21638.
- Silva MA. Intestinal dendritic cells and epithelial barrier dysfunction in crohnʼs disease. Inflamm Bowel Dis. 2009;15(3):436–453. doi:https://doi.org/10.1002/ibd.20660.
- Thompson AI, Lees CW. Genetics of ulcerative colitis. Inflamm Bowel Dis. 2011;17(3):831–848. doi:https://doi.org/10.1002/ibd.21375.
- Strober W, Fuss IJ, Blumberg RS. The Immunology of mucosal m odels of Inflammation. Annu Rev Immunol. 2002;20(1):495–549. doi:https://doi.org/10.1146/annurev.immunol.20.100301.064816.
- Meddings J. Barrier dysfunction and Crohn’s Disease. Ann N Y Acad Sci. 2006;915:333–338.
- Consortium UIG, Barrett JC, Lee JC, Lees CW, Prescott NJ, Anderson CA, et al. Genome-wide association study of ulcerative colitis identifies three new susceptibility loci, including the HNF4A region. Nat Genet. 2009;41:1330–1334.
- Lee WY, Chin AC, Voss S, Parkos CA. In vitro neutrophil transepithelial migration. Methods in Molecular Biology (Clifton, N.J.). 2006;341:205–215. doi:https://doi.org/10.1385/1-59745-113-4:205.
- Edens HA, Levi BP, Jaye DL, Walsh S, Reaves TA, Turner JR, Nusrat A, Parkos CA. Neutrophil transepithelial migration: evidence for sequential, contact-dependent signaling events and enhanced paracellular permeability independent of transjunctional migration. J Immunol. 2002;169(1):476–486. doi:https://doi.org/10.4049/jimmunol.169.1.476.
- Nusrat A, Parkos CA, Liang TW, Carnes DK, Madara JL. Neutrophil migration across model intestinal epithelia: monolayer disruption and subsequent events in epithelial repair. Gastroenterology. 1997;113(5):1489–1500. doi:https://doi.org/10.1053/gast.1997.v113.pm9352851.
- Chieppa M, Rescigno M, Huang AY, Germain RN. Dynamic imaging of dendritic cell extension into the small bowel lumen in response to epithelial cell TLR engagement. J Exp Med. 2006;203(13):2841–2852. doi:https://doi.org/10.1084/jem.20061884.
- Del Rio M-L, Bernhardt G, Rodriguez-Barbosa J-I, Förster R. Development and functional specialization of CD103+ dendritic cells. Immunol Rev. 2010;234(1):268–281. doi:https://doi.org/10.1111/j.0105-2896.2009.00874.x.
- Rescigno M. Intestinal dendritic cells. Adv Immunol. 2010;107:109–138.
- Rescigno M, Urbano M, Valzasina B, Francolini M, Rotta G, Bonasio R, et al. Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat Immunol. 2001;2:361–367. doi:https://doi.org/10.1038/86373.
- Cepek KL, Shaw SK, Parker CM, Russell GJ, Morrow JS, Rimm DL, et al. Adhesion between epithelial cells and T lymphocytes mediated by E-cadherin and the alpha E beta 7 integrin. Nature. 1994;372:190–193. doi:https://doi.org/10.1038/372190a0.
- Lamb CA, O’Byrne S, Keir ME, Butcher EC. Gut-selective integrin-targeted therapies for inflammatory bowel disease. J Crohns Colitis. 2018;12(suppl_2):S653–S68. doi:https://doi.org/10.1093/ecco-jcc/jjy060.
- Hollander D, Vadheim CM, Brettholz E, Petersen GM, Delahunty T, Rotter JI. Increased intestinal permeability in patients with Crohn’s disease and their relatives A possible etiologic factor. Ann Intern Med. 1986;105:883–885.
- Fries W, Renda MC, Lo Presti MA, Raso A, Orlando A, Oliva L, Giofre MR, Maggio A, Mattaliano A, Macaluso A, et al. Intestinal permeability and genetic determinants in patients, first-degree relatives, and controls in a high-incidence area of Crohn’s disease in Southern Italy. Am J Gastroenterol. 2005;100(12):2730–2736.
- Hilsden RJ, Meddings JB, Sutherland LR. Intestinal permeability changes in response to acetylsalicylic acid in relatives of patients with Crohn’s disease. Gastroenterology. 1996;110(5):1395–1403. doi:https://doi.org/10.1053/gast.1996.v110.pm8613043.
- Madsen KL, Malfair D, Gray D, Doyle JS, Jewell LD, Fedorak RN. Interleukin-10 gene-deficient mice develop a primary intestinal permeability defect in response to enteric microflora. Inflamm Bowel Dis. 1999;5:262–270.
- Olson TS, Reuter BK, Scott KG, Morris MA, Wang X-M, Hancock LN, Burcin TL, Cohn SM, Ernst PB, Cominelli F, et al. The primary defect in experimental ileitis originates from a nonhematopoietic source. J Exp Med. 2006;203(3):541–552. doi:https://doi.org/10.1084/jem.20050407.
- Komatsu Y, Shimizu Y, Yamano M, Kikuchi M, Nakamura K, Ayabe T, Aizawa T. Disease progression-associated alterations in fecal metabolites in SAMP1/YitFc mice, a Crohn’s disease model. Metabolomics. 2020;16(4):48. doi:https://doi.org/10.1007/s11306-020-01671-5.
- Kozaiwa K, Sugawara K, Smith MF Jr., Carl V, Yamschikov V, Belyea B, Mcewen SB, Moskaluk CA, Pizarro TT, Cominelli F, et al. Identification of a quantitative trait locus for ileitis in a spontaneous mouse model of Crohn’s disease: SAMP1/YitFc. Gastroenterology. 2003;125(2):477–490. doi:https://doi.org/10.1016/S0016-5085(03)00876-X.
- Matsumoto S, Okabe Y, Setoyama H, Takayama K, Ohtsuka J, Funahashi H, Imaoka A, Okada Y, Umesaki Y. Inflammatory bowel disease-like enteritis and caecitis in a senescence accelerated mouse P1/Yit strain. Gut. 1998;43(1):71–78. doi:https://doi.org/10.1136/gut.43.1.71.
- Utech M, Bruwer M, Nusrat A. Tight junctions and cell-cell interactions. Methods Mol Biol. 2006;341:185–195.
- Ma TY, Iwamoto GK, Hoa NT, Akotia V, Pedram A, Boivin MA, Said HM. TNF-α-induced increase in intestinal epithelial tight junction permeability requires NF-κB activation. Am J Physiol Gastrointest Liver Physiol. 2004;286:G367–76.
- Bruewer M, Luegering A, Kucharzik T, Parkos CA, Madara JL, Hopkins AM, Nusrat A. Proinflammatory cytokines disrupt epithelial barrier function by apoptosis-independent mechanisms. J Immunol. 2003;171(11):6164–6172. doi:https://doi.org/10.4049/jimmunol.171.11.6164.
- Nusrat A, Turner JR, Madara JL. IV. Regulation of tight junctions by extracellular stimuli: nutrients, cytokines, and immune cells. Am J Physiol Gastrointest Liver Physiol. 2000;279(5):G851–7. doi:https://doi.org/10.1152/ajpgi.2000.279.5.G851.
- Ostanin DV, Bao J, Koboziev I, Gray L, Robinson-Jackson SA, Kosloski-Davidson M, Price VH, Grisham MB. T cell transfer model of chronic colitis: concepts, considerations, and tricks of the trade. Am J Physiol Gastrointest Liver Physiol. 2009;296(2):G135–46. doi:https://doi.org/10.1152/ajpgi.90462.2008.
- Steinbach EC, Gipson GR, Sheikh SZ. Induction of murine intestinal inflammation by adoptive transfer of effector CD4+CD45RBhigh T cells into immunodeficient Mice. J Vis Exp. 2015;98. doi:https://doi.org/10.3791/52533.
- Kanai T, Kawamura T, Dohi T, Makita S, Nemoto Y, Totsuka T, Watanabe M. TH1/TH2-mediated colitis induced by adoptive transfer of CD4+CD45RBhigh T lymphocytes into nude mice. Inflamm Bowel Dis. 2006;12(2):89–99. doi:https://doi.org/10.1097/01.MIB.0000197237.21387.mL.
- Graham WV, He W, Marchiando AM, Zha J, Singh G, Li H-S, Biswas A, Ong MLDM, Jiang Z-H, Choi W, et al. Intracellular MLCK1 diversion reverses barrier loss to restore mucosal homeostasis. Nat Med. 2019;25(4):690–700. doi:https://doi.org/10.1038/s41591-019-0393-7.
- Arrieta MC, Madsen K, Doyle J, Meddings J. Reducing small intestinal permeability attenuates colitis in the IL10 gene-deficient mouse. Gut. 2009;58(1):41–48. doi:https://doi.org/10.1136/gut.2008.150888.
- Khare V, Krnjic A, Frick A, Gmainer C, Asboth M, Jimenez K, Lang M, Baumgartner M, Evstatiev R, Gasche C. Mesalamine and azathioprine modulate junctional complexes and restore epithelial barrier function in intestinal inflammation. Sci Rep. 2019;9(1):2842. doi:https://doi.org/10.1038/s41598-019-39401-0.
- Ungaro R, Mehandru S, Allen PB, Peyrin-Biroulet L, Colombel J-F. Ulcerative colitis. Lancet. 2017;389(10080):1756–1770. doi:https://doi.org/10.1016/S0140-6736(16)32126-2.
- Sydora BC, Macfarlane SM, Walker JW, Dmytrash AL, Churchill TA, Doyle J, Fedorak RN. Epithelial barrier disruption allows nondisease-causing bacteria to initiate and sustain IBD in the IL-10 gene-deficient mouse. Inflamm Bowel Dis. 2007;13(8):947–954. doi:https://doi.org/10.1002/ibd.20155.
- Andrews C, McLean MH, Durum SK. Cytokine Tuning of Intestinal Epithelial Function. Front Immunol. 2018;9:1270. doi:https://doi.org/10.3389/fimmu.2018.01270.
- Chen P, Bakke D, Kolodziej L, Lodolce J, Weber CR, Boone DL, Toback FG. Antrum mucosal protein-18 peptide targets tight junctions to protect and heal barrier structure and function in models of inflammatory bowel disease. Inflamm Bowel Dis. 2015;21(10):2393–2402. doi:https://doi.org/10.1097/MIB.0000000000000499.
- Clough JN, Omer OS, Tasker S, Lord GM, Irving PM. Regulatory T-cell therapy in Crohn’s disease: challenges and advances. Gut. 2020;69(5):942–952. doi:https://doi.org/10.1136/gutjnl-2019-319850.
- Yamada A, Arakaki R, Saito M, Tsunematsu T, Kudo Y, Ishimaru N. Role of regulatory T cell in the pathogenesis of inflammatory bowel disease. World J Gastroenterol. 2016;22(7):2195–2205. doi:https://doi.org/10.3748/wjg.v22.i7.2195.
- Berg DJ, Davidson N, Kuhn R, Muller W, Menon S, Holland G, Thompson-Snipes L, Leach MW, Rennick D. Enterocolitis and colon cancer in interleukin-10-deficient mice are associated with aberrant cytokine production and CD4(+) TH1-like responses. J Clin Invest. 1996;98(4):1010–1020. doi:https://doi.org/10.1172/JCI118861.
- Suenaert P, Maerten P, Van Assche G, Van Driessche W, Geboes K, Bulteel V, Simaels J, Augustijns P, Ceuppens JL, Rutgeerts P, et al. Effects of T cell-induced colonic inflammation on epithelial barrier function†. Inflamm Bowel Dis. 2010;16(8):1322–1331. doi:https://doi.org/10.1002/ibd.21211.
- Jayawardena D, Tyagi S, Nazmi A, Olivares-Villagomez D, Dudeja PK. ion transport basis of diarrhea in a mouse model of adoptive T cell transfer colitis. Dig Dis Sci. 2020;65(6):1700–1709. doi:https://doi.org/10.1007/s10620-019-05945-4.
- Gumbiner B, Simons K. A functional assay for proteins involved in establishing an epithelial occluding barrier: identification of a uvomorulin-like polypeptide. J Cell Biol. 1986;102(2):457–468. doi:https://doi.org/10.1083/jcb.102.2.457.
- Gumbiner B, Stevenson B, Grimaldi A. The role of the cell adhesion molecule uvomorulin in the formation and maintenance of the epithelial junctional complex. J Cell Biol. 1988;107(4):1575–1587. doi:https://doi.org/10.1083/jcb.107.4.1575.
- Nusrat A, Turner JR, Madara JL. Molecular physiology and pathophysiology of tight junctions. IV Regulation of Tight Junctions by Extracellular Stimuli: Nutrients, Cytokines, and Immune Cells. Am J Physiol Gastrointest Liver Physiol. 2000;279:G851–7.
- Barrett JC, Lee JC, Lees CW, Prescott NJ, Anderson CA, Phillips A, et al. Genome-wide association study of ulcerative colitis identifies three new susceptibility loci, including the HNF4A region. Nat Genet. 2009;41:1330–1334.
- Muise AM, Walters TD, Glowacka WK, Griffiths AM, Ngan B-Y, Lan H, Xu W, Silverberg MS, Rotin D. Polymorphisms in E-cadherin (CDH1) result in a mis-localised cytoplasmic protein that is associated with Crohn’s disease. Gut. 2009;58(8):1121–1127. doi:https://doi.org/10.1136/gut.2008.175117.
- Hermiston ML, Gordon JI. Inflammatory bowel disease and adenomas in mice expressing a dominant negative N-cadherin. Science. 1995;270(5239):1203–1207. doi:https://doi.org/10.1126/science.270.5239.1203.
- Smalley-Freed WG, Efimov A, Burnett PE, Short SP, Davis MA, Gumucio DL, Washington MK, Coffey RJ, Reynolds AB. p120-catenin is essential for maintenance of barrier function and intestinal homeostasis in mice. J Clin Invest. 2010;120(6):1824–1835. doi:https://doi.org/10.1172/JCI41414.
- Smalley-Freed WG, Efimov A, Short SP, Jia P, Zhao Z, Washington MK, Robine S, Coffey RJ, Reynolds AB, et al. Adenoma formation following limited ablation of p120-catenin in the mouse intestine. PLoS One. 2011;6(5):e19880. doi:https://doi.org/10.1371/journal.pone.0019880.
- Petrova YI, Spano MM, Gumbiner BM. Conformational epitopes at cadherin calcium-binding sites and p120-catenin phosphorylation regulate cell adhesion. Mol Biol Cell. 2012;23:2092–2108.
- Shashikanth N, Petrova YI, Park S, Chekan J, Maiden S, Spano M, Ha T, Gumbiner BM, Leckband DE. Allosteric Regulation of E-Cadherin Adhesion. J Biol Chem. 2015;290(35):21749–21761. doi:https://doi.org/10.1074/jbc.M115.657098.
- Na T-Y, Schecterson L, Mendonsa AM, Gumbiner BM. The functional activity of E-cadherin controls tumor cell metastasis at multiple steps. Proc Natl Acad Sci U S A. 2020;117(11):5931–5937. doi:https://doi.org/10.1073/pnas.1918167117.
- Kucharzik T, Walsh SV, Chen J, Parkos CA, Nusrat A. Neutrophil transmigration in inflammatory bowel disease is associated with differential expression of epithelial intercellular junction proteins. Am J Pathol. 2001;159(6):2001–2009. doi:https://doi.org/10.1016/S0002-9440(10)63051-9.
- Demetter P, Baeten D, De Keyser F, De Vos M, Van Damme N, Verbruggen G, et al. Subclinical gut inflammation in spondyloarthropathy patients is associated with upregulation of the E-cadherin/catenin complex. Ann Rheum Dis. 2000;59(3):211–216. doi:https://doi.org/10.1136/ard.59.3.211.
- Gassler N, Rohr C, Schneider A, Kartenbeck J, Bach A, Obermuller N, Otto HF, Autschbach F. Inflammatory bowel disease is associated with changes of enterocytic junctions. American Journal of Physiology-Gastrointestinal and Liver Physiology. 2001;281(1):G216–28. doi:https://doi.org/10.1152/ajpgi.2001.281.1.G216.
- Rezaee F, DeSando SA, Ivanov AI, Chapman TJ, Knowlden SA, Beck LA, Georas SN. Sustained protein kinase D activation mediates respiratory syncytial virus-induced airway barrier disruption. J Virol. 2013;87(20):11088–11095. doi:https://doi.org/10.1128/JVI.01573-13.
- Petrova YI, Schecterson L, Gumbiner BM. Roles for E-cadherin cell surface regulation in cancer. Mol Biol Cell. 2016;27(21):3233–3244. doi:https://doi.org/10.1091/mbc.E16-01-0058.
- Bialkowska AB, Ghaleb AM, Nandan MO, Yang VW. Improved swiss-rolling technique for intestinal tissue preparation for immunohistochemical and immunofluorescent analyses. J Vis Exp. 2016;113. doi:https://doi.org/10.3791/54161.
- Mendonsa AM, Bandyopadhyay C, Gumbiner BM. p120-catenin phosphorylation status alters E-cadherin mediated cell adhesion and ability of tumor cells to metastasize. PLoS One. 2020;15(6):e0235337. doi:https://doi.org/10.1371/journal.pone.0235337.
- Rezaee F, Meednu N, Emo JA, Saatian B, Chapman TJ, Naydenov NG, De Benedetto A, Beck LA, Ivanov AI, Georas SN, et al. Polyinosinic:polycytidylic acid induces protein kinase D–dependent disassembly of apical junctions and barrier dysfunction in airway epithelial cells. J Allergy Clin Immunol. 2011;128(6):1216–24 e11. doi:https://doi.org/10.1016/j.jaci.2011.08.035.
- Saatian B, Rezaee F, Desando S, Emo J, Chapman T, Knowlden S, Georas SN. Interleukin-4 and interleukin-13 cause barrier dysfunction in human airway epithelial cells. Tissue Barriers. 2013;1(2):e24333. doi:https://doi.org/10.4161/tisb.24333.
- Scheinin T, Butler DM, Salway F, Scallon B, Feldmann M. Validation of the interleukin-10 knockout mouse model of colitis: antitumour necrosis factor-antibodies suppress the progression of colitis. Clin Exp Immunol. 2003;133(1):38–43. doi:https://doi.org/10.1046/j.1365-2249.2003.02193.x.
- Kennedy RJ, Hoper M, Deodhar K, Erwin PJ, Kirk SJ, Gardiner KR. Interleukin 10-deficient colitis: new similarities to human inflammatory bowel disease. Br J Surg. 2002;87(10):1346–1351. doi:https://doi.org/10.1046/j.1365-2168.2000.01615.x.
- Keubler LM, Buettner M, Hager C, Bleich A. A multihit model: colitis lessons from the interleukin-10-deficient mouse. Inflamm Bowel Dis. 2015;21(8):1967–1975. doi:https://doi.org/10.1097/MIB.0000000000000468.
- Thorsvik S, Damas JK, Granlund AV, Flo TH, Bergh K, Ostvik AE, Sandvik AK. Fecal neutrophil gelatinase-associated lipocalin as a biomarker for inflammatory bowel disease. J Gastroenterol Hepatol. 2017;32(1):128–135. doi:https://doi.org/10.1111/jgh.13598.
- Wells JM, Brummer RJ, Derrien M, MacDonald TT, Troost F, Cani PD, Theodorou V, Dekker J, Méheust A, de Vos WM, et al. Homeostasis of the gut barrier and potential biomarkers. Am J Physiol Gastrointest Liver Physiol. 2017;312(3):G171–G93. doi:https://doi.org/10.1152/ajpgi.00048.2015.
- Helke K, Angel P, Lu P, Garrett-Mayer E, Ogretmen B, Drake R, Voelkel-Johnson C. Ceramide synthase 6 deficiency enhances inflammation in the DSS model of Colitis. Sci Rep. 2018;8(1):1627. doi:https://doi.org/10.1038/s41598-018-20102-z.
- Castro-Mejia J, Jakesevic M, Krych Ł, Nielsen DS, Hansen LH, Sondergaard BC, Kvist PH, Hansen AK, Holm TL. Treatment with a monoclonal anti-IL-12p40 antibody induces substantial gut microbiota changes in an experimental colitis model. Gastroenterol Res Pract. 2016;2016:4953120. doi:https://doi.org/10.1155/2016/4953120.
- Uhlig HH, McKenzie BS, Hue S, Thompson C, Joyce-Shaikh B, Stepankova R, Robinson N, Buonocore S, Tlaskalova-Hogenova H, Cua DJ, et al. Differential activity of IL-12 and IL-23 in mucosal and systemic innate immune pathology. Immunity. 2006;25(2):309–318. doi:https://doi.org/10.1016/j.immuni.2006.05.017.
- Roy U, Galvez EJC, Iljazovic A, Lesker TR, Blazejewski AJ, Pils MC, Heise U, Huber S, Flavell RA, Strowig T, et al. Distinct microbial communities trigger colitis development upon intestinal barrier damage via innate or adaptive immune cells. Cell Rep. 2017;21(4):994–1008. doi:https://doi.org/10.1016/j.celrep.2017.09.097.
- Balda MS, Whitney JA, Flores C, Gonzalez S, Cereijido M, Matter K. Functional dissociation of paracellular permeability and transepithelial electrical resistance and disruption of the apical-basolateral intramembrane diffusion barrier by expression of a mutant tight junction membrane protein. J Cell Biol. 1996;134(4):1031–1049. doi:https://doi.org/10.1083/jcb.134.4.1031.
- Bruewer M, Samarin S, Nusrat A. Inflammatory bowel disease and the apical junctional complex. Ann N Y Acad Sci. 2006;1072(1):242–252. doi:https://doi.org/10.1196/annals.1326.017.
- Ivanov AI, Nusrat A, Parkos CA. The epithelium in inflammatory bowel disease: potential role of endocytosis of junctional proteins in barrier disruption. Novartis Found Symp. 2004;263:115–118. discussion 24-32, 211-8.
- Ivanov AI, Parkos CA, Nusrat A. Cytoskeletal regulation of epithelial barrier function during inflammation. Am J Pathol. 2010;177(2):512–524. doi:https://doi.org/10.2353/ajpath.2010.100168.
- Ma TY, Iwamoto GK, Hoa NT, Akotia V, Pedram A, Boivin MA, Said HM. TNF-α-induced increase in intestinal epithelial tight junction permeability requires NF-κB activation. Am J Physiol Gastrointest Liver Physiol. 2004;286:G367–76.
- Meddings J. Barrier dysfunction and Crohn’s disease. Ann N Y Acad Sci. 2006;915:333.