2,165
Views
57
CrossRef citations to date
0
Altmetric
Review

Non-canonical functions of claudin proteins: Beyond the regulation of cell-cell adhesions

Article: e1327839 | Received 17 Feb 2017, Accepted 03 May 2017, Published online: 26 May 2017

References

  • Van Itallie CM, Anderson JM. Architecture of tight junctions and principles of molecular composition. Semin Cell Dev Biol 2014; 36:157-65; PMID:25171873; https://doi.org/10.1016/j.semcdb.2014.08.011
  • Anderson JM, Van Itallie CM. Physiology and function of the tight junction. Cold Spring Harb Perspect Biol 2009; 1:a002584; PMID:20066090; https://doi.org/10.1101/cshperspect.a002584
  • Suzuki H, Tani K, Tamura A, Tsukita S, Fujiyoshi Y. Model for the architecture of claudin-based paracellular ion channels through tight junctions. J Mol Biol 2015; 427:291-7; PMID:25451028; https://doi.org/10.1016/j.jmb.2014.10.020
  • Tsukita S, Furuse M, Itoh M. Multifunctional strands in tight junctions. Nat Rev Mol Cell Biol 2001; 2:285-93; PMID:11283726; https://doi.org/10.1038/35067088
  • Farquhar MG, Palade GE. Junctional complexes in various epithelia. J Cell Biol 1963; 17:375-412; PMID:13944428
  • Chalcroft JP, Bullivant S. An interpretation of liver cell membrane and junction structure based on observation of freeze-fracture replicas of both sides of the fracture. J Cell Biol 1970; 47:49-60; PMID:4935338
  • Claude P, Goodenough DA. Fracture faces of zonulae occludentes from “tight” and “leaky” epithelia. J Cell Biol 1973; 58:390-400; PMID:4199658
  • Madara JL. Intestinal absorptive cell tight junctions are linked to the cytoskeleton. Am J Physiol 1987; 253:C854-61; PMID:3605327
  • Van Itallie CM, Anderson JM. Claudin interactions in and out of the tight junction. Tissue Barriers 2013; 1:e25247; PMID:24665401; https://doi.org/10.4161/tisb.25247
  • Mineta K, Yamamoto Y, Yamazaki Y, Tanaka H, Tada Y, Saito K, Tamura A, Igarashi M, Endo T, Takeuchi K, et al. Predicted expansion of the claudin multigene family. FEBS Lett 2011; 585:606-612; PMID:21276448; https://doi.org/10.1016/j.febslet.2011.01.028
  • Lu Z, Ding L, Lu Q, Chen YH. Claudins in intestines: Distribution and functional significance in health and disease. Tissue Barriers 2013; 1:e24978; PMID:24478939; https://doi.org10.4161/tisb.24978
  • Luettig J, Rosenthal R, Barmeyer C, Schulzke JD. Claudin-2 as a mediator of leaky gut barrier during intestinal inflammation. Tissue Barriers 2015; 3:e977176; PMID:25838982; https://doi.org/10.4161/21688370.2014.977176
  • Hou J. The kidney tight junction (review). Int J Mol Med 2017; 34:1451-7; PMID:25319473; https://doi.org/10.3892/ijmm.2014.1955
  • Yu ASL. Claudins and the kidney. J Am Soc Nephrol 2015; 26:11-9; PMID:24948743; https://doi.org/10.1681/ASN.2014030284
  • Frank JA. Claudins and alveolar epithelial barrier function in the lung. Ann N Y Acad Sci 2012; 1257:175-83; PMID:22671604; https://doi.org/10.1111/j.1749-6632.2012.06533.x
  • Mruk DD, Cheng CY. The mammalian blood-testis barrier: its biology and regulation. Endocr Rev 2015; 36:564-91; PMID:26357922; https://doi.org//10.1210/er.2014-1101
  • Brandner JM, Zorn-Kruppa M, Yoshida T, Moll I, Beck LA, De Benedetto A. Epidermal tight junctions in health and disease. Tissue Barriers 2015; 3:e974448; PMID:25838981; https://doi.org/10.4161/21688370.2014.974451
  • Stamatovic SM, Johnson AM, Keep RF, Andjelkovic AV. Junctional proteins of the blood-brain barrier: New insights into function and dysfunction. Tissue Barriers 2016; 4:e1154641; PMID:27141427; https://doi.org/10.1080/21688370.2016.1154641
  • Lisewski U, Shi Y, Wrackmeyer U, Fischer R, Chen C, Schirdewan A, Jüttner R, Rathjen F, Poller W, Radke MH, et al. The tight junction protein CAR regulates cardiac conduction and cell-cell communication. J Exp Med 2008; 205:2369-79; PMID:18794341; https://doi.org/10.1084/jem.20080897
  • Itoh M, Nagafuchi A, Yonemura S, Kitani-Yasuda T, Tsukita S, Tsukita S. The 220-kD protein colocalizing with cadherins in non-epithelial cells is identical to ZO-1, a tight junction-associated protein in epithelial cells: cDNA cloning and immunoelectron microscopy. J Cell Biol 1993; 121:491-502; PMID:8486731
  • Denninger AR, Breglio A, Maheras KJ, DeLuc G, Cristiglio V, Deme B, Gow A, Kirschner DA. Claudin-11 tight junctions in myelin are a barrier to diffusion and lack strong adhesive properties. Biophys J 2015; 109:1387-97; PMID:26445439; https://doi.org/10.1016/j.bpj.2015.08.012
  • Devaux J, Fykkolodziej B, Gow A. Claudin proteins and neuronal function. Curr Top Membr 2010; 65:229-53; PMID:25013353; https://doi.org/10.1016/S1063-5823(10)65010-7
  • Rahner C, Mitic LL, Anderson JM. Heterogeneity in expression and subcellular localization of claudins 2, 3, 4, and 5 in the rat liver, pancreas and gut. Gastroenterology 2001; 120:411-23; PMID:11159882
  • Fujita H, Chiba H, Yokozaki H, Sakai N, Sugimoto K, Wada T, Kojima T, Yamashita T, Sawada N. Differential expression and subcellular localization of claudin-7, -8, 12-, -13, and -15 along the mouse intestine. J Histochem Cytochem 2006; 54:933-44; PMID:16651389; https://doi.org/10.1369/jhc.6A6944.2006
  • Tamagawa H, Takahashi I, Furuse M, Yoshitake-Kitano Y, Tsukita S, Ito T, Matsuda H, Kiyono H. Characteristics of claudin expression in follicle-associated epithelium of Peyer's patches: preferential localization of claudin-4 at the apex oof the dome region. Lab Invest 2003; 83:1045-53; PMID:12861044
  • Weber CR, Nalle SC, Tretiakova M, Rubin DT, Turner JR. Claudin-1 and claudin-2 expression is elevated in inflammatory bowel disease and may contribute to early neoplastic transformation. Lab Invest 2008; 88:1110-20; PMID:18711353; https://doi.org/10.1038/labinvest.2008.78
  • Gregory M, Dufresne J, Hermo L, Cyr DG. Claudin-1 is not restricted to tight junctions in the rat epididymis. Endocrinology 2001; 142:854-63; PMID:11159859; https://doi.org/10.1210/endo.142.2.7975
  • Shen L, Weber CR, Turner JR. The tight junction protein complex undergoes rapid and continuous molecular remodeling at steady state. J Cell Biol 2008; 181:683-95; PMID:18474622; https://doi.org/10.1083/jcb.200711165
  • Chalmers AD, Whitley P. Continuous endocytic recycling of tight junction proteins: how and why? Essays Biochem 2012; 53:41-54; PMID:22928507; https://doi.org/10.1042/bse0530041
  • Ivanov AI, Nusrat A, Parkos CA. Endocytosis of the apical junctional complex: mechanisms and possible roles in regulation of epithelial barriers. BioEssays 2005; 27:356-65; PMID:15770686; https://doi.org/10.1002/bies.20203
  • Ivanov AI, Nusrat A, Parkos CA. Endocytosis of epithelial apical junctional proteins by a clathrin-mediated pathway into a unique storage compartment. Mol Biol Cell 2004; 15:176-88; PMID:14528017; https://doi.org/10.1091/mbc.E03-05-0319
  • Lu R, Stewart L, Wilson JM. The scaffolding protein GOPC regulates tight junction structure. Cell Tissue Res 2015; 360:321-32; PMID:25616555; https://doi.org/10.1007/s00441-014-2088-1
  • Lu R, Johnson DL, Stewart L, Waite K, Elliot D, Wilson JM. Rab14 regulation of claudin-2 trafficking modulates epithelial permeability and lumen morphogenesis. Mol Biol Cell 2014; 25:1744-54; PMID:24694596; https://doi.org/10.1091/mbc.E13-12-0724
  • Apodaca G, Gallo LI, Bryant DM. Role of membrane traffic in the generation of epithelial cell asymmetry. Nat Cell Biol 2012; 14:1235-43; PMID:23196841; https://doi.org/10.1038/ncb2635
  • Hayashi D, Tamura A, Tanaka H, Yamazaki Y, Watanabe S, Suzuki K, Suzuki K, Sentani K, Yasui W, Rakugi W, et al. Deficiency of claudin-18 causes paracellular H+ leakage, up-regulation of interleukin-1-beta, and atrophic gastritis in mice. Gastroenterology 2012; 142:292-304; PMID:22079592; https://doi.org/10.1053/j.gastro.2011.10.040
  • Iino R, Koyama I, Kusumi A. Single molecule imaging of green fluorescent proteins in living cells: E-cadherin forms oligomers on the free cell surface. Biophys J 2001; 80:2667-77; PMID:11371443; https://doi.org/10.1016/S0006-3495(01)76236-4
  • Hansen MDH, Ehrlich JS, Nelson WJ. Molecular mechanism for orienting membrane and actin dynamics to nascent cell-cell contacts in epithelial cells. J Biol Chem 2002; 277:45371-6; [PMID:12244058; https://doi.org/10.1074/jbc.M207747200
  • Perez TD, Tamada M, Sheetz MP, Nelson WJ. Immediate-early signaling induced by E-cadherin engagement and adhesion. J Biol Chem 2008; 283:5014-22; PMID:18089563; https://doi.org/10.1074/jbc.M705209200
  • Wu C-J, Mannan P, Lu M, Udey MC. Epithelial cell adhesion molecule (EpCAM) regulates claudin dynamics and tight junctions. J Biol Chem 2013; 288:12253-68; PMID:23486470; https://doi.org/10.1074/jbc.M113.457499
  • Van Itallie CM, Tietgens AJ, LoGrande K, Aponte A, Gucek M, Anderson JM. Phosphorylation of claudin-2 on serine 208 promotes membrane retention and reduces trafficking to lysosomes. J Cell Sci 2012; 125:4902-12; PMID:22825868; https://doi.org/10.1242/jcs.111237
  • Iwamoto DV, Calderwood DA. Regulation of integrin-mediated adhesions. Curr Opin Cell Biol 2015; 36:41-7; PMID:26189062; https://doi.org/10.1016/j.ceb.2015.06.009
  • Ding L, Lu Z, Foreman O, Tatum R, Lu Q, Renegar R, Cao J, Chen Y-H. Inflammation and disruption of the mucosal architecture in claudin-7-deficient mice. Gastroenterology 2012; 142:305-15; PMID:22044670; https://doi.org/10.1053/j.gastro.2011.10.025
  • Ding L, Wang L, Sui L, Zhao H, Xu X, Li T, Wang X, Li W, Zhao P, Kong L. Claudin-7 indirectly regulaters the integrin/FAK signaling pathway in human colon cancer tissue. J Hum Genet 2016; 61:711-20; PMID:27121327; https://doi.org/10.1038/jhg.2016.35
  • Lu Z, Kim DH, Fan J, Lu Q, Verbanac K, Ding L, Renegar R, Chen Y-H. A non-tight junction function of claudin-7-interaction with integrin signaling in suppressing lung cancer cell proliferation and detachment. Mol Cancer 2015; 14:120; PMID:26081244; https://doi.org/10.1186/s12943-015-0387-0
  • Elias BC, Mathew S, Srichai MB, Palamuttam R, Bulus N, Mernaugh G, Singh AB, Sanders CR, Harris RC, Pozzi A, et al. The integrin β1 subunit regulates paracellular permeability of kidney proximal tubule cells. J Biol Chem 2014; 289:8532-44; PMID:24509849; https://doi.org/10.1074/jbc.M113.526509
  • Ladwein M, Pape U-F, Schmidt D-S, Schnölzer M, Fiedler S, Langbein L, Franke WW, Moldenhauer G, Zöller M. The cell-cell adhesion molecule EpCAM interacts directly with the tight junction protein claudin-7. Expt Cell Res 2005; 309:345-57; PMID:16054130; https://doi.org/10.1016/j.yexcr.2005.06.013
  • Nübel T, Preobraschenski J, Tuncay H, Weiss T, Kuhn S, Ladwein M, Langbein L, Zöller M. Claudin-7 regulates EpCAM-mediated functions in tumor progression. Mol Cancer Res 2009; 7:285-99; PMID:19276185; https://doi.org/10.1158/1541-7786.MCR-08-0200
  • Heiler S, Mu W, Zöller M, Thuma F. The importance of claudin-7 palmitoylation on membrane subdomain localization and metastasis-promoting activities. Cell 2015; 13:29; PMID:26054340; https://doi.org/10.1186/s12964-015-0105-y
  • Kozan PA, McGeough MD, Pena CA, Mueller JL, Barrett KE, Marchelletta RR, Sivagnanam M. Mutation of EpCAM leads to intestinal barrier and ion transport dysfunction. J Mol Med 2015; 93:535-45; PMID:25482158; https://doi.org/10.1007/s00109-014-1239-x
  • Tabaries S, Dong Z, Annis MG, Omeroglu A, Pepin F, Ouellet V, Russo C, Hassanain M, Metrakos P, Diaz Z, et al. Claudin-2 is selectively enriched in and promotes the formation of breast cancer liver metastases through engagement of integrin complexes. Oncogene 2011; 30:1318-28; PMID:21076473; https://doi.org/10.1038/onc.2010.518
  • Zheng J, Xie Y, Campbell R, Song J, Samira M, Razi M, Chiu R, Berenson J, Yang OO, Chen ISY, et al. Involvement of claudin-7 in HIV infection of CD4(-) cells. Retrovirology 2005; 2:79; PMID:16368003
  • Gruzu S, Silveanu C, Fetyko A, Butiurca V, Kovacs Z, Jung I. Systematic review of the old and new concepts in the epithelial-mesenchymal transition of colorectal cancer. World J Gastroenterol 2016; 22:6764-75; PMID:27570416; https://doi.org/10.3748/wjg.v22.i30.6764
  • Agarwal R, D'Souza T, Morin PJ. Claudin-3 and claudin-4 expression in ovarian epithelial cells enhances invasion and is associated with increased matrix metalloproteinase-2 activity. Cancer Res 2005; 65:7378-85; PMID:16103090; https://doi.org/10.1158/0008-5472.CAN-05-1036
  • Yoon CH, Kim MJ, Park MJ, Park IC, Hwang SG, An S, Choi YH, Yoon G, Lee SJ. Claudin-1 acts through c-Abl-protein kinase cδ (PKCδ) signaling and has a causal role in the acquisition of invasive capacity in human liver cells. J Biol Chem 2010; 285:226-33; PMID:19897486; https://doi.org/10.1074/jbc.M109.054189
  • Pope JL, Bhat AA, Sharma A, Ahmad R, Krishnan M, Washington MK, Beauchamp RD, Singh AB, Dhawan P. Claudin-1 regulates intestinal epithelial homeostasis through the modulation of Notch signaling. Gut 2014; 63:622-34; PMID:24997475; https://doi.org/10.1186/1476-4598-13-167
  • Leotlela PD, Wade MS, Duray PH, Rhode MJ, Brown HF, Rosenthal DT, Dissanayake SK, Earley R, Indig FE, Nickoloff BJ, et al. Claudin-1 overexpression in melanoma is regulated by PKC and contributes to melanoma cell motility. Oncogene 2007; 26:3846-56; PMID:17160014; https://doi.org/10.1038/sj.onc.1210155
  • Miyamori H, Takino T, Kobayashi Y, Tokai H, Itoh Y, Seiki M, Sato H. Claudin promotes activation of pro-matrix metalloproteinase-2 mediated by membrane-type matrix metalloproteinases. J Biol Chem 2001; 276:28204-11; PMID:11382769; https://doi.org/10.1074/jbc.M103083200
  • Ikari A, Sato T, Watanabe R, Yamazaki Y, Sugatani J. Increase in claudin-2 expression by an EGFR/MEK/ERK/c-Fos pathway in lung adenocarcinoma A549 cells. Biochim Biophys Acta 2012; 1823:1118; PMID:22546605; https://doi.org/10.1016/j.bbamcr.2012.04.005
  • Torres-Martinez AC, Gallardo-Vera JF, Lara-Holguin AN, Montano LF, Rendon-Huerta EP. Claudin-6 enhances cell invasiveness through claudin-1 in AGS human adenocarcinoma gastric cancer cells. Exp Cell Res 2017; 350:226-35; PMID:27914788; https://doi.org/10.1016/j.yexcr.2016.11.025
  • Liu Y, Jin X, Li Y, Ruan Y, Lu Y, Yang M, Lin D, Song P, Guo Y, Zhao S, et al. DNA methylation of claudin-6 promotes breast cancer cell migration and invasion by recruiting MeCP2 and deacetylating H3Ac and H4Ac. J Exp Clin Cancer Res 2016; 35:120; PMID:27461117; https://doi.org/10.1186/s13046-016-0396-x
  • Gottardi CJ, Arpin M, Fanning AS, Louvard D. The junction-associated protein, zonula occludens-1, localizes to the nucleus before the maturation and during the remodeling of cell-cell contacts. Proc Natl Acad Sci USA 1996; 93:10779-84; PMID:8855257
  • Islas S, Vega J, Ponce L, González-Garcia M. Nuclear localization of the tight junction protein ZO-2 in epithelial cells. Exp Cell Res 2002; 274:138-48; PMID:11855865; https://doi.org/10.1006/excr.2001.5457
  • Sourisseau T, Georgiadis A, Tsapara A, Ali RR, Pestell R, Matter K, Balda MS. Regulation of PCNA and cyclin D1 expression and epithelial morphogenesis by the ZO-1-regulated transcription factor ZONAB/DbpA. Mol Cell Biol 2006; 26:2387-98; PMID:16508013; https://doi.org/10.1128/MCB.26.6.2387-2398.2006
  • Spadaro D, Tapia R, Pulimeno P, Citi S. The control of gene expression and cell proliferation by the epithelial apical junctional complex. Essays Biochem 2012; 53:83-93; PMID:22928510; https://doi.org/10.1042/bse0530083
  • Dhawan P, Singh AB, Deane NG, No YR, Shiou S-R, Schmidt C, Neff J, Washington MK, Beauchamp RD. Claudin-1 regulates cellular transformation and metastatic behavior in colon cancer. J Clin Invest 2005; 115:1765-76; https://doi.org/10.1172/JCI24543
  • Lee J-W, Hsiao W-T, Chen H-Y, Hsu L-P, Chen P-R, Lin M-D, Chiu S-J, Shih W-L, Hsu Y-C. Upregulated claudin-1 expression confers resistance to cell death of nasopharyngeal carcinoma cells. Int J Cancer 2010; 126:1353-66; PMID:19739116; https://doi.org/10.1002/ijc.24857
  • French AD, Fiori JL, Camilli TC, Leotlela PD, O'Connell MP, Frank BP, Subaran S, Indig FE, Traub DD, Weeraratna AT. PKC and PKA phosphorylation affect the subcellular localization of claudin-1 in melanoma cells. Int J Med Sci 2009; 6:93-101; PMID:19305641
  • Fujita H, Chalubinski M, Rhyner C, Indermitte P, Ing D, Meyer N, Ferstl R, Treis A, Gomez E, Akkaya A, et al. Claudin-1 expression in airway smooth muscle cells exacerbates airway remodeling in asthmatic subjects. J Allergy Clin Immunol 2011; 127:1612-21; PMID:21624620; https://doi.org/10.1016/j.jaci.2011.03.039
  • Zwanziger D, Badziong J, Ting S, Mooeller LC, Schmid KW, Siebolts U, Wickenhauser C, Dralle H, Fuehrer D. The impact of CLAUDIN-1 on follicular thyroid carcinoma aggrressiveness. Endocr Relat Cancer 2015; 22:819-30; PMID:26219679; https://doi.org/10.1530/ERC-14-0502
  • Ikari A, Watanabe R, Sato T, Taga S, Simobaba S, Yamaguchi M, Yamazaki Y, Endo S, Matsunaga T, Sugatani J. Nuclear distribution of claudin-2 increases cell proliferation in human lung adenocarcinoma cells. Biochim Biophys Acta 2014; 1843:2079-88; PMID:24907662; https://doi.org/10.1016/j.bbamcr.2014.05.017
  • Todd MC, Petty HM, King JM, Piana Marshall BN, Sheller RA, Cuevas ME. Overexpression and delocalization of claudin-3 protein in MCF-7 and MDA-MB-415 breast cancer cell lines. Oncol Lett 2015; 10:156-62; PMID:26170992; https://doi.org/10.3892/ol.2015.3160
  • Cuevas ME, Gaska JM, Gist AC, King JM, Sheller RA, Todd MC. Estrogen-dependent expression and subcellular localization of the tight junction protein claudin-4 in HEC-1A endometrial cancer cells. Int J Oncol 2015; 47:650-6; PMID:26043767; https://doi.org/10.3892/ijo.2015.3030
  • Huerta M, Munoz R, Tapia R, Soto-Reyes E, Ramirez L, Recillas-Targa F, González-Garcia M, Lopez-Bayghen E. Cyclin D1 is transcriptionally down-regulated by ZO-2 via an E box and the transcription factor c-myc. Mol Biol Cell 2017; 18:4826-36; PMID:17881732; https://doi.org/10.1091/mbc.E07-02-0109
  • González-Garcia M, Islas S, Contreras RG, Garcia-Villegas MR, Betanzos A, Vega J, Diaz-Quinonez A, Martin-Orozco N, Ortiz-Navarrete V, Creijido M, et al. Molecular characterization of the tight junction protein ZO-1 in MDCK cells. Exp Cell Res 1999; 248:97-109; PMID:10094817
  • Acharya P, Beckel J, Ruiz WG, Wang E, Rojas R, Birder L, Apodaca G. Distribution of the tight junction proteins ZO-1, occludin, claudin-4, -8, and -12 in bladder epithelium. Am J Physiol Renal Physiol 2004; 287:F305-18; PMID:15068973; https://doi.org/10.1152/ajprenal.00341.2003
  • Fujita H, Sugimoto K, Inatomi S, Maeda T, Osani M, Uchiyama Y, Yamamoto H, Wada T, Kojima T, Yokozaki H, et al. Tight junction proteins claudin-2 and -12 are critical for vitamin D-dependent Ca2+ absorption between enterocytes. Mol Biol Cell 2008; 19:1912-21; PMID:18287530; https://doi.org/10.1091/mbc.E07-09-0973
  • Wang W, Tan X, Zhou L, Gao F, Dai X. Involvement of the expression and redistribution of claudin-23 in pancreatic cancer cell dissociation. Mol Med Rep 2010; 3:845-50; PMID:21472324; https://doi.org/10.3892/mmr.2010.334
  • Bhansali M, Zhou J, Shemshedini L. TM4SF3 and AR: A nuclear complex that stabilizes both proteins. Mol Endocrinol 2016; 30:13-25; PMID:26649804; https://doi.org/10.1210/me.2015-1075
  • Rappa G, Green TM, Lorico A. The nuclear pool of tetraspanin CD9 contributes to mitotic processes in human breast carcinoma. Mol Cancer Res 2014; 12:1840-50; PMID:25103498; https://doi.org/10.1158/1541-7786.MCR-14-0242
  • Rappa G, Santos MF, Green TM, Karbanova J, Hassler J, Bai Y, Barsky SH, Corbeil D, Lorico A. Nuclear transport of cancer extracellular vesicle-derived biomaterials through nuclear envelope invagination-associated late endosomes. Oncotarget 2017; 8:14443-61; PMID:28129640; https://doi.org/10.18632/oncotarget.14804
  • Ferber EC, Kajita M, Wadlow A, Tobiansky L, Niessen C, Ariga H, Daniel J, Fujita Y. A role for the cleaved cytoplasmic domain of E-cadherin in the nucleus. J Biol Chem 2008; 283:12691-700
  • Du W, Liu S, Fan G, Zhao X, Sun Y, Wang T, Zhao R, Wang G, Zhao C, Zhu Y, et al. From cell membrane to the nucleus: an emerging role of E-cadherin in gene transcriptional regulation. J Cell Mol Med 2017; 18:1712-9
  • Cukierman L, Meertens L, Bertaux C, Kajumo F, Dragic T. Residues in a highly conserved claudin-1 motif are required for hepatitis C virus entry and mediate the formation of cell-cell contacts. J Virol 2009; 83:5477-84; PMID:19297469; https://doi.org/10.1128/JVI.02262-08
  • Furuse M, Hata M, Furuse K, Yoshida Y, Haratake A, Sugitani Y, Noda T, Kubo A, Tsukita S. Claudin-based tight junctions are critical for the mammalian epidermal barrier: a lesson from claudin-1-deficient mice. J Cell Biol 2002; 156:1099-111; PMID:11889141; https://doi.org/10.1083/jcb.200110122
  • Meng J, Holdcraft RW, Shima JE, Griswold MD, Braun RE. Androgens regulate the permeability of the blood-testis barrier. Proc Natl Acad Sci USA 2005; 102:16696-700; PMID:16275920; https://doi.org/10.1073/pnas.0506084102
  • Resnick MB, Gavilanez M, Newton E, Konkin T, Bhattacharya B, Britt DE, Sabo E, Moss SE. Claudin expression in gastric adenocarcinomas: a tissue microarray study with prognostic correlation. Hum Pathol 2005; 36:886-92; PMID:16112005; https://doi.org/10.1016/j.humpath.2005.05.019
  • Chang TL, Ito K, Ko TK, Liu Q, Salto-Tellez M, Yeoh KG, Fukamachi H, Ito Y. Claudin-1 has tumor suppressive activity and is a direct target of RUNX3 in gastric epithelial cells. Gastroenterology 2010; 138:255-65; PMID:19706291; https://doi.org/10.1053/j.gastro.2009.08.044
  • Psáder R, Jakab C, Mathe S, Balka G, Papa K, Sterczer A. Expression of claudins in the normal canine gastric mucosa. Acta Vet Hung 2014; 62:13-21; PMID:24334088; https://doi.org/10.1556/AVet.2013.053
  • Sanada Y, Oue N, Mitani Y, Yoshida K, Nakayama H, Yasui W. Down-regulation of the claudin-18 gene, identified through serial analysis of gene expression data analysis, in gastric cancer with an intestinal phenotype. J Pathol 2006; 208:633-42; PMID:16435283; https://doi.org/10.1002/path.1922
  • Matsuda Y, Semba S, Ueda J, Fuku T, Hasuo T, Chiba H, Sawada N, Kuroda Y, Yokozaki H. Gastric and intestinal claudin expression at the invasive front of gastric carcinoma. Cancer Sci 2007; 98:1014-9; PMID:17459057; https://doi.org/10.1111/j.1349-7006.2007.00490.x
  • Darido C, Buchert M, Pannequin J, Bastide P, Zalzali H, Mantamadiotis T, Burgaux J-F, Garambois V, Jay P, Blache P, et al. Defective claudin-7 regulation by Tcf-4 and SOX9 disrupts the polarity and increases the tumorgenicity of colorectal cancer cells. Cancer Res 2008; 68:4258-68; PMID:18519685; https://doi.org/10.1158/0008-5472.CAN-07-5805
  • Li WY, Huey CL, Yu ASL. Expression of claudin-7 and -8 along the mouse nephron. Am J Physiol Lung Cell Mol Physiol 2004; 286:F1063-71; PMID:14722018; https://doi.org/10.1152/ajprenal.00384.2003
  • Alexandre MD, Lu Q, Chen Y-H. Overexpresssion of claudin-7 decreases the paracellular Cl- conductance and increases the paracellular Na+ conductance in LLC-PK1 cells. J Cell Sci 2005; 118:2683-93; PMID:15928046; https://doi.org/10.1242/jcs.02406
  • Gonzalez-Mariscal L, Namorado MDC, Martin D, Sierra G, Reyes JL. The tight junction proteins claudin-7 and -8 display a different subcellular localization at Henle's loops and collecting ducts of rabbit kidney. Nephrol Dial Transplant 2006; 21:2391-8; PMID:16766545; https://doi.org/10.1093/ndt/gfl255
  • Coyne CB, Gambling TM, Boucher RC, Carson JL, Johnson LG. Role of claudin interactions in airway tight junctional permeability. Am J Physiol Lung Cell Mol Physiol 2003; 285:L1166-78; PMID:12909588; https://doi.org/10.1152/ajplung.00182.2003
  • Marzesco A-M, Dunia I, Pandjaitan R, Recouvreur M, Dauzonne D, Benedetti EL, Louvard D, Zahraoui A. The small GTPase Rab13 regulates assembly of functional tight junctions in epithelial cells. Mol Biol Cell 2002; 13:1819-31; PMID:12058051; https://doi.org/ 02-02-0029

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.