Cldn-7 deficiency promotes experimental colitis and associated carcinogenesis by regulating intestinal epithelial integrity

References

• Ng SC, Shi HY, Hamidi N, Underwood FE, Tang W, Benchimol EI, Panaccione R, Ghosh S, Wu JCY, Chan FKL, et al. Worldwide incidence and prevalence of inflammatory bowel disease in the 21st century: a systematic review of population-based studies. Lancet. 2018;390(10114):2769–16. doi:10.1016/S0140-6736(17)32448-0.
   PubMed Web of Science ®Google Scholar
• Kaplan GG, Ng SC. Understanding and preventing the global increase of inflammatory bowel disease. Gastroenterology. 2017;152(2):313–321.e312. doi:10.1053/j.gastro.2016.10.020.
   PubMed Web of Science ®Google Scholar
• Kobayashi T, Siegmund B, Le Berre C, Wei SC, Ferrante M, Shen B, Bernstein CN, Danese S, Peyrin-Biroulet L, Hibi T. Ulcerative colitis. Nat Rev Dis Primers. 2020;6:74.
   PubMed Web of Science ®Google Scholar
• Choi CR, Bakir IA, Hart AL, Graham TA. Clonal evolution of colorectal cancer in IBD. Nat Rev Gastroenterol Hepatol. 2017;14:218–229.
   PubMed Web of Science ®Google Scholar
• Lasry A, Zinger A, Ben-Neriah Y. Inflammatory networks underlying colorectal cancer. Nat Immunol. 2016;17:230–240.
   PubMed Web of Science ®Google Scholar
• Grivennikov SI. Inflammation and colorectal cancer: colitis-associated neoplasia. Semin Immunopathol. 2013;35:229–244.
   PubMed Web of Science ®Google Scholar
• Parikh K, Antanaviciute A, Fawkner-Corbett D, Jagielowicz M, Aulicino A, Lagerholm C, Davis S, Kinchen J, Chen HH, Alham NK, et al. Colonic epithelial cell diversity in health and inflammatory bowel disease. Nature. 2019;567:49–55.
   PubMed Web of Science ®Google Scholar
• Yu LC. Microbiota dysbiosis and barrier dysfunction in inflammatory bowel disease and colorectal cancers: exploring a common ground hypothesis. J Biomed Sci. 2018;25:79.
   PubMed Web of Science ®Google Scholar
• Zihni C, Mills C, Matter K, Balda MS. Tight junctions: from simple barriers to multifunctional molecular gates. Nat Rev Mol Cell Biol. 2016;17:564–580.
   PubMed Web of Science ®Google Scholar
• Zhu L, Han J, Li L, Wang Y, Li Y, Zhang S. Claudin family participates in the pathogenesis of inflammatory bowel diseases and colitis-associated colorectal cancer. Front Immunol. 2019;10:1441. doi:10.3389/fimmu.2019.01441.
   PubMed Web of Science ®Google Scholar
• Gowrikumar S, Ahmad R, Uppada SB, Washington MK, Shi C, Singh AB, Dhawan P. Upregulated claudin-1 expression promotes colitis-associated cancer by promoting β-catenin phosphorylation and activation in Notch/p-AKT-dependent manner. Oncogene. 2019;38(26):5321–5337. doi:10.1038/s41388-019-0795-5.
   PubMed Web of Science ®Google Scholar
• Raju P, Shashikanth N, Tsai PY, Pongkorpsakol P, Chanez-Paredes S, Steinhagen PR, Kuo WT, Singh G, Tsukita S, Turner JR. Inactivation of paracellular cation-selective claudin-2 channels attenuates immune-mediated experimental colitis in mice. J Clin Invest. 2020;130(10):5197–5208. doi:10.1172/JCI138697.
   PubMed Web of Science ®Google Scholar
• Ding L, Lu Z, Foreman O, Tatum R, Lu Q, Renegar R, Cao J, Chen Y; Ding L, Lu Z, Foreman O, Tatum R, Lu Q, Renegar R, Cao J, Chen YH. Inflammation and disruption of the mucosal architecture in claudin-7–deficient mice. Gastroenterology. 2012;142(2):305–315. doi:10.1053/j.gastro.2011.10.025.
   PubMed Web of Science ®Google Scholar
• Tanaka H, Takechi M, Kiyonari H, Shioi G, Tamura A, Tsukita S. Intestinal deletion of Claudin-7 enhances paracellular organic solute flux and initiates colonic inflammation in mice. Gut. 2015;64(10):1529–1538. doi:10.1136/gutjnl-2014-308419.
   PubMed Web of Science ®Google Scholar
• Nakayama M, Ishizuka N, Hempstock W, Ikari A, Hayashi H. Na(+)-coupled nutrient cotransport induced luminal negative potential and claudin-15 play an important role in paracellular Na(+) recycling in mouse small intestine. Int J Mol Sci. 2020;21(2):376. doi:10.3390/ijms21020376.
   PubMed Web of Science ®Google Scholar
• Luissint AC, Williams HC, Kim W, Flemming S, Azcutia V, Hilgarth RS, Leary MNO, Denning TL, Nusrat A, Parkos CA. Macrophage-dependent neutrophil recruitment is impaired under conditions of increased intestinal permeability in JAM-A-deficient mice. Mucosal Immunol. 2019;12(3):668–678. doi:10.1038/s41385-019-0143-7.
   PubMed Web of Science ®Google Scholar
• Mir H, Meena AS, Chaudhry KK, Shukla PK, Gangwar R, Manda B, Padala MK, Shen L, Turner JR, Dietrich P, et al. Occludin deficiency promotes ethanol-induced disruption of colonic epithelial junctions, gut barrier dysfunction and liver damage in mice. Biochim Biophys Acta. 2016;1860(4):765–774. doi:10.1016/j.bbagen.2015.12.013.
   PubMed Web of Science ®Google Scholar
• Amasheh S, Fromm M, Günzel D. Claudins of intestine and nephron - a correlation of molecular tight junction structure and barrier function. Acta Physiol (Oxf). 2011;201(1):133–140. doi:10.1111/j.1748-1716.2010.02148.x.
   PubMed Web of Science ®Google Scholar
• Singh AB, Uppada SB, Dhawan P. Claudin proteins, outside-in signaling, and carcinogenesis. Pflugers Arch. 2017;469(1):69–75. doi:10.1007/s00424-016-1919-1.
   PubMed Web of Science ®Google Scholar
• Garcia-Hernandez V, Quiros M, Nusrat A. Intestinal epithelial claudins: expression and regulation in homeostasis and inflammation. Ann N Y Acad Sci. 2017;1397(1):66–79. doi:10.1111/nyas.13360.
   PubMed Web of Science ®Google Scholar
• Wang K, Li T, Xu C, Ding Y, Li W, Ding L. Claudin-7 downregulation induces metastasis and invasion in colorectal cancer via the promotion of epithelial-mesenchymal transition. Biochem Biophys Res Commun. 2017;390(3):797–804. doi:10.1016/j.bbrc.2018.10.049.
   Web of Science ®Google Scholar
• Kuhn S, Koch M, Nübel T, Ladwein M, Antolovic D, Klingbeil P, Hildebrand D, Moldenhauer G, Langbein L, Franke WW, et al. A complex of EpCAM, claudin-7, CD44 variant isoforms, and tetraspanins promotes colorectal cancer progression. Mol Cancer Res. 2020;130(6):553–567. doi:10.1158/1541-7786.MCR-06-0384.
   Web of Science ®Google Scholar
• Darido C, Buchert M, Pannequin J, Bastide P, Zalzali H, Mantamadiotis T, Bourgaux J-F, Garambois V, Jay P, Blache P, et al. Defective claudin-7 regulation by Tcf-4 and Sox-9 disrupts the polarity and increases the tumorigenicity of colorectal cancer cells. Cancer Res. 2012;142(11):4258–4268. doi:10.1158/0008-5472.CAN-07-5805.
   Web of Science ®Google Scholar
• Kim ER. Colorectal cancer in inflammatory bowel disease: the risk, pathogenesis, prevention and diagnosis. World J Gastroenterol. 2014;20(29):9872–9881. doi:10.3748/wjg.v20.i29.9872.
   PubMed Web of Science ®Google Scholar
• Zeisel MB, Dhawan P, Baumert TF. Tight junction proteins in gastrointestinal and liver disease. Gut. 2019;68(3):547–561. doi:10.1136/gutjnl-2018-316906.
   PubMed Web of Science ®Google Scholar
• Zuo L, Kuo W-T, Turner JR. Tight junctions as targets and effectors of mucosal immune homeostasis. Cell Mol Gastroenterol Hepatol. 2020;10(2):327–340. doi:10.1016/j.jcmgh.2020.04.001.
   PubMed Web of Science ®Google Scholar
• Beaugerie L, Svrcek M, Seksik P, Bouvier AM, Simon T, Allez M, Brixi H, Gornet JM, Altwegg R, Beau P, et al. Risk of colorectal high-grade dysplasia and cancer in a prospective observational cohort of patients with inflammatory bowel disease. Gastroenterology. 2013;145(1):166–175.e168. doi:10.1053/j.gastro.2013.03.044.
   PubMed Web of Science ®Google Scholar
• Xu C, Wang K, Ding Y-H, Li W-J, Ding L. Claudin-7 gene knockout causes destruction of intestinal structure and animal death in mice. World J Gastroenterol. 2019;25(5):584–599. doi:10.3748/wjg.v25.i5.584.
   PubMed Web of Science ®Google Scholar
• Xu C, Wang XN, Li WJ, Wang K, Ding L. Expression and clinical significance of claudin-7 in patients with colorectal cancer. Technol Cancer Res Treat. 2008;68:1–10. doi:10.1177/1533033818817774.
   Google Scholar
• Quan JC, Peng J, Guan X, Liu Z, Jiang Z, Chen HP, Zhuang M, Wang S, Sun P, Wang HY, et al. Evaluation of clinical significance of claudin 7 and construction of prognostic grading system for stage II colorectal cancer. World J Clin Cases. 2020;8:2190–2200.
   PubMed Web of Science ®Google Scholar
• Wen X, Zhao H, Wang L, Wang L, Du G, Guan W, Liu J, Cao X, Jiang X, Tian J, et al. Nobiletin attenuates DSS-induced intestinal barrier damage through the HNF4α-Claudin-7 signaling pathway. J Agric Food Chem. 2020;68:4641–4649.
   PubMed Web of Science ®Google Scholar
• Kiesler P, Fuss IJ, Strober W. Experimental models of inflammatory bowel diseases. Cell Mol Gastroenterol Hepatol. 2015;1:154–170.
   PubMed Web of Science ®Google Scholar
• Xing T, Benderman LJ, Sabu S, Parker J, Yang J, Lu Q, Ding L, Chen YH. Tight junction protein claudin-7 is essential for intestinal epithelial stem cell self-renewal and differentiation. Cell Mol Gastroenterol Hepatol 2020;9:641–659.
   PubMed Web of Science ®Google Scholar
• Bhat AA, Uppada S, Achkar IW, Hashem S, Yadav SK, Shanmugakonar M, Al-Naemi HA, Haris M, Uddin S. Tight junction proteins and signaling pathways in cancer and inflammation: a functional crosstalk. Front Physiol. 2018;9:1942.
   PubMed Web of Science ®Google Scholar
• De Robertis M, Massi E, Poeta ML, Carotti S, Morini S, Cecchetelli L, Signori E, Fazio VM. The AOM/DSS murine model for the study of colon carcinogenesis: from pathways to diagnosis and therapy studies. J Carcinog. 2011;10:9.
   PubMedGoogle Scholar
• Vermeulen L, Emf DS, Van Der Heijden M, Cameron K, De Jong JH, Borovski T, Tuynman JB, Todaro M, Merz C, Rodermond H, et al. Wnt activity defines colon cancer stem cells and is regulated by the microenvironment. Nat Cell Biol. 2010;12:468–476.
   PubMed Web of Science ®Google Scholar
• Reya T, Clevers H. Wnt signalling in stem cells and cancer. Nature. 2005;434:843–850.
   PubMed Web of Science ®Google Scholar
• Pouyet L, Roisin-Bouffay C, Clément A, Millet V, Garcia S, Chasson L, Issaly N, Rostan A, Hofman P, Naquet P, et al. Epithelial vanin-1 controls inflammation-driven carcinogenesis in the colitis-associated colon cancer model. Inflamm Bowel Dis. 2010;16:96–104.
   PubMed Web of Science ®Google Scholar
• Luo C, Zhang H. The role of proinflammatory pathways in the pathogenesis of colitis-associated colorectal cancer. Mediators Inflamm. 2017;2017:5126048.
   PubMed Web of Science ®Google Scholar
• Neal MD, Richardson WM, Sodhi CP, Russo A, Hackam DJ. Intestinal stem cells and their roles during mucosal injury and repair. J Surg Res. 2011;167:1–8.
   PubMed Web of Science ®Google Scholar
• Mennillo E, Yang X, Paszek M, Auwerx J, Benner C, Chen S. NCoR1 protects mice from dextran sodium sulfate-induced colitis by guarding colonic crypt cells from luminal insult. Cell Mol Gastroenterol Hepatol. 2020;10:133–147.
   PubMed Web of Science ®Google Scholar
• Zhang J, Hou S, Gu J, Tian T, Yuan Q, Jia J, Qin Z, Chen Z. S100A4 promotes colon inflammation and colitis-associated colon tumorigenesis. Oncoimmunology. 2018;7:e1461301.
   PubMed Web of Science ®Google Scholar
• Naydenov NG, Feygin A, Wang D, Kuemmerle JF, Harris G, Conti MA, Adelstein RS, Ivanov AI. Nonmuscle Myosin IIA regulates intestinal epithelial barrier in vivo and plays a protective role during experimental colitis. Sci Rep. 2016;6:24161.
   PubMed Web of Science ®Google Scholar
• He C, Yu T, Shi Y, Ma C, Yang W, Fang L, Sun M, Wu W, Xiao F, Guo F, et al. 301A promotes intestinal inflammation and colitis-associated cancer development by inhibiting BTG1. Gastroenterology. 2017;152:1434–1448.e1415.
   PubMed Web of Science ®Google Scholar
• Chang YY, Yu LC, Yu IS, Jhuang YL, Huang WJ, Yang CY, Jeng YM. Deletion of cadherin-17 enhances intestinal permeability and susceptibility to intestinal tumour formation. J Pathol. 2018;246:289–299.
   PubMed Web of Science ®Google Scholar
• Kim Y, Kessler SP, Obery DR, Homer CR, McDonald C. de la Motte CA. Hyaluronan 35kDa treatment protects mice from Citrobacter rodentium infection and induces epithelial tight junction protein ZO-1 in vivo. Matrix Biol. 2017;62:28–39.
   PubMed Web of Science ®Google Scholar
• Bian Y, Dong Y, Sun J, Sun M, Hou Q, Lai Y, Zhang B. Protective effect of kaempferol on LPS-induced inflammation and barrier dysfunction in a coculture model of intestinal epithelial cells and intestinal microvascular endothelial cells. J Agric Food Chem. 2020;68:160–167.
   PubMed Web of Science ®Google Scholar