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Review

Epithelial adhesion molecules and the regulation of intestinal homeostasis during neutrophil transepithelial migration

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Article: e969100 | Received 19 Sep 2014, Accepted 14 Aug 2014, Published online: 25 Feb 2015

References

  • Fasano A, Shea-Donohue T. Mechanisms of disease: the role of intestinal barrier function in the pathogenesis of gastrointestinal autoimmune diseases. Nat Clin Pract Gastroenterol Hepatol 2005; 2:416-22; PMID:16265432; http://dx.doi.org/10.1038/ncpgasthep0259
  • Costa F, Mumolo MG, Ceccarelli L, Bellini M, Romano MR, Sterpi C, Ricchiuti A, Marchi S, Bottai M. Calprotectin is a stronger predictive marker of relapse in ulcerative colitis than in Crohn's disease. Gut 2005; 54:364-8; PMID:15710984; http://dx.doi.org/10.1136/gut.2004.043406
  • Xavier RJ, Podolsky DK. Unravelling the pathogenesis of inflammatory bowel disease. Nature 2007; 448:427-34; PMID:17653185; http://dx.doi.org/10.1038/nature06005
  • Langhorst J, Elsenbruch S, Mueller T, Rueffer A, Spahn G, Michalsen A, Dobos GJ. Comparison of 4 neutrophil-derived proteins in feces as indicators of disease activity in ulcerative colitis. Inflam Bowel Dis 2005; 11:1085-91; http://dx.doi.org/10.1097/01.MIB.0000187980.08686.18
  • Nusrat A, Parkos CA, Liang TW, Carnes DK, Madara JL. Neutrophil migration across model intestinal epithelia: monolayer disruption and subsequent events in epithelial repair. Gastroenterol 1997; 113:1489-500; http://dx.doi.org/10.1053/gast.1997.v113.pm9352851
  • Maloy KJ, Powrie F. Intestinal homeostasis and its breakdown in inflammatory bowel disease. Nature 2011; 474:298-306; PMID:21677746; http://dx.doi.org/10.1038/nature10208
  • Schmitz H, Barmeyer C, Fromm M, Runkel N, Foss HD, Bentzel CJ, Riecken EO, Schulzke JD. Altered tight junction structure contributes to the impaired epithelial barrier function in ulcerative colitis. Gastroenterol 1999; 116:301-9; http://dx.doi.org/10.1016/S0016-5085(99)70126-5
  • Ma TY. Intestinal epithelial barrier dysfunction in Crohn's disease. Proc Soc Exp Biol Med Soc Exp Biol Med 1997; 214:318-27; http://dx.doi.org/10.3181/00379727-214-44099
  • Sumagin R, Sarelius IH. InterCellular adhesion molecule-1 enrichment near triCellular endothelial junctions is preferentially associated with leukocyte transmigration and signals for reorganization of these junctions to accommodate leukocyte passage. J Immunol 2010; 184:5242-52; PMID:20363969; http://dx.doi.org/10.4049/jimmunol.0903319
  • Ley K, Bullard DC, Arbones ML, Bosse R, Vestweber D, Tedder TF, Beaudet AL. Sequential contribution of L- and P-selectin to leukocyte rolling in vivo. J Exp Med 1995; 181:669-75; PMID:7530761; http://dx.doi.org/10.1084/jem.181.2.669
  • Sumagin R, Sarelius IH. A role for ICAM-1 in maintenance of leukocyte-endothelial Cell rolling interactions in inflamed arterioles. Am J Physiol Heart Circulat Physiol 2007; 293:H2786-98; http://dx.doi.org/10.1152/ajpheart.00720.2007
  • Yang L, Kowalski JR, Yacono P, Bajmoczi M, Shaw SK, Froio RM, Golan DE, Thomas SM, Luscinskas FW. Endothelial Cell cortactin coordinates interCellular adhesion molecule-1 clustering and actin cytoskeleton remodeling during polymorphonuclear leukocyte adhesion and transmigration. J Immunol 2006; 177:6440-9; PMID:17056576; http://dx.doi.org/10.4049/jimmunol.177.9.6440
  • Phillipson M, Heit B, Colarusso P, Liu L, Ballantyne CM, Kubes P. Intraluminal crawling of neutrophils to emigration sites: a Molly distinct process from adhesion in the recruitment cascade. J Exp Med 2006; 203:2569-75; PMID:17116736; http://dx.doi.org/10.1084/jem.20060925
  • Sumagin R, Prizant H, Lomakina E, Waugh RE, Sarelius IH. LFA-1 and Mac-1 define characteristically different intralumenal crawling and emigration patterns for monocytes and neutrophils in situ. J Immunol 2010; 185:7057-66; PMID:21037096; http://dx.doi.org/10.4049/jimmunol.1001638
  • Nourshargh S, Hordijk PL, Sixt M. Breaching multiple barriers: leukocyte motility through venular walls and the interstitium. Nat Rev Mol Cell Biol 2010; 11:366-78; PMID:20414258; http://dx.doi.org/10.1038/nrm2889
  • Ley K, Laudanna C, Cybulsky MI, Nourshargh S. Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat Rev Immunol 2007; 7:678-89; PMID:17717539; http://dx.doi.org/10.1038/nri2156
  • Voisin MB, Woodfin A, Nourshargh S. Monocytes and neutrophils exhibit both distinct and common mechanisms in penetrating the vascular basement membrane in vivo. Arterioscl Thromb Vas 2009; 29:1193-9; http://dx.doi.org/10.1161/ATVBAHA.109.187450
  • Wang S, Cao C, Chen Z, Bankaitis V, Tzima E, Sheibani N, Burridge K. Pericytes regulate vascular basement membrane remodeling and govern neutrophil extravasation during inflammation. PloS one 2012; 7:e45499; PMID:23029055; http://dx.doi.org/10.1371/journal.pone.0045499
  • Lerchenberger M, Uhl B, Stark K, Zuchtriegel G, Eckart A, Miller M, Puhr-Westerheide D, Praetner M, Rehberg M, Khandoga AG, et al. Matrix metalloproteinases modulate ameboid-like migration of neutrophils through inflamed interstitial tissue. Blood 2013; 122:770-80; PMID:23757732; http://dx.doi.org/10.1182/blood-2012-12-472944
  • Garrod D, Chidgey M. Desmosome structure, composition and function. Biochim Biophys Acta 2008; 1778:572-87; PMID:17854763; http://dx.doi.org/10.1016/j.bbamem.2007.07.014
  • Matter K, Balda MS. Signalling to and from tight junctions. Nat Rev Mol Cell Biol 2003; 4:225-36; PMID:12612641; http://dx.doi.org/10.1038/nrm1055
  • Nusrat A, Turner JR, Madara JL. Mol physiology and pathophysiology of tight junctions. IV. Regulation of tight junctions by extraCellular stimuli: nutrients, cytokines, and immune Cells. Am J Physiol Gastr L 2000; 279:G851-7;
  • Parkos CA, Delp C, Arnaout MA, Madara JL. Neutrophil migration across a cultured intestinal epithelium. Dependence on a CD11b/CD18-mediated event and enhanced efficiency in physiological direction. J Clin Invest 1991; 88:1605-12; PMID:1682344; http://dx.doi.org/10.1172/JCI115473
  • Agace WW, Patarroyo M, Svensson M, Carlemalm E, Svanborg C. Escherichia coli induces transuroepithelial neutrophil migration by an interCellular adhesion molecule-1-dependent mechanism. Infect Immun 1995; 63:4054-62; PMID:7558319
  • Wright SD, Weitz JI, Huang AJ, Levin SM, Silverstein SC, Loike JD. Complement receptor type three (CD11b/CD18) of human polymorphonuclear leukocytes recognizes fibrinogen. Proc Natl Acad Sci U S A 1988; 85:7734-8; PMID:2971974; http://dx.doi.org/10.1073/pnas.85.20.7734
  • Ueda T, Rieu P, Brayer J, Arnaout MA. Identification of the complement iC3b binding site in the beta 2 integrin CR3 (CD11b/CD18). Proc Natl Acad Sci U S A 1994; 91:10680-4.;
  • Cai TQ, Wright SD. Human leukocyte elastase is an endogenous ligand for the integrin CR3 (CD11b/CD18, Mac-1, alpha M beta 2) and modulates polymorphonuclear leukocyte adhesion. J Exp Med 1996; 184:1213-23; PMID:8879192; http://dx.doi.org/10.1084/jem.184.4.1213
  • Xia Y, Vetvicka V, Yan J, Hanikyrova M, Mayadas T, Ross GD. The beta-glucan-binding lectin site of mouse CR3 (CD11b/CD18) and its function in generating a primed state of the receptor that mediates cytotoxic activation in response to iC3b-opsonized target Cells. J Immunol 1999; 162:2281-90; PMID:9973505
  • Diamond MS, Alon R, Parkos CA, Quinn MT, Springer TA. Heparin is an adhesive ligand for the leukocyte integrin Mac-1 (CD11b/CD1). J Cell Biol 1995; 130:1473-82; PMID:7559767; http://dx.doi.org/10.1083/jcb.130.6.1473
  • Xia Y, Ross GD. Generation of recombinant fragments of CD11b expressing the functional beta-glucan-binding lectin site of CR3 (CD11b/CD18). J Immunol 1999; 162:7285-93; PMID:10358177
  • Diamond MS, Staunton DE, de Fougerolles AR, Stacker SA, Garcia-Aguilar J, Hibbs ML, Springer TA. ICAM-1 (CD54): a counter-receptor for Mac-1 (CD11b/CD18). J Cell Biol 1990; 111:3129-39; PMID:1980124; http://dx.doi.org/10.1083/jcb.111.6.3129
  • Ross GD, Cain JA, Lachmann PJ. Membrane complement receptor type three (CR3) has lectin-like properties analogous to bovine conglutinin as functions as a receptor for zymosan and rabbit erythrocytes as well as a receptor for iC3b. J Immunol 1985; 134:3307-15; PMID:2984286;
  • Zen K, Liu Y, Cairo D, Parkos CA. CD11b/CD18-dependent interactions of neutrophils with intestinal epithelium are mediated by fucosylated proteoglycans. J Immunol 2002; 169:5270-8; PMID:12391246; http://dx.doi.org/10.4049/jimmunol.169.9.5270
  • Colgan SP, Parkos CA, McGuirk D, Brady HR, Papayianni AA, Frendl G, Madara JL. Receptors involved in carbohydrate binding modulate intestinal epithelial-neutrophil interactions. J Biol Chem 1995; 270:10531-9; PMID:7537733; http://dx.doi.org/10.1074/jbc.270.18.10531
  • 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; 169:476-86; PMID:12077279; http://dx.doi.org/10.4049/jimmunol.169.1.476
  • Chin AC, Lee WY, Nusrat A, Vergnolle N, Parkos CA. Neutrophil-mediated activation of epithelial protease-activated receptors-1 and -2 regulates barrier function and transepithelial migration. J Immunol 2008; 181:5702-10; PMID:18832729; http://dx.doi.org/10.4049/jimmunol.181.8.5702
  • Bornslaeger EA, Corcoran CM, Stappenbeck TS, Green KJ. Breaking the connection: displacement of the desmosomal plaque protein desmoplakin from Cell-Cell interfaces disrupts anchorage of intermediate filament bundles and alters interCellular junction assembly. J Cell Biol 1996; 134:985-1001; PMID:8769422; http://dx.doi.org/10.1083/jcb.134.4.985
  • Lie PP, Cheng CY, Mruk DD. Crosstalk between desmoglein-2/desmocollin-2/Src kinase and coxsackie and adenovirus receptor/ZO-1 protein complexes, regulates blood-testis barrier dynamics. Int J Biochem Cell Biol 2010; 42:975-86; PMID:20188849; http://dx.doi.org/10.1016/j.biocel.2010.02.010
  • 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. Am J phys Gastrointest L 2001; 281:G216-28
  • Schlegel N, Meir M, Heupel WM, Holthofer B, Leube RE, Waschke J. Desmoglein 2-mediated adhesion is required for intestinal epithelial barrier integrity. Am J phys Gastrointest L 2010; 298:G774-83; http://dx.doi.org/10.1152/ajpgi.00239.2009
  • Lorch JH, Klessner J, Park JK, Getsios S, Wu YL, Stack MS, Green KJ. Epidermal growth factor receptor inhibition promotes desmosome assembly and strengthens interCellular adhesion in squamous Cell carcinoma Cells. J Biol Chem 2004; 279:37191-200; PMID:15205458; http://dx.doi.org/10.1074/jbc.M405123200
  • Kolegraff K, Nava P, Laur O, Parkos CA, Nusrat A. Characterization of full-length and proteolytic cleavage fragments of desmoglein-2 in native human colon and colonic epithelial Cell lines. Cell Adhes Migr 2011; 5:306-14; http://dx.doi.org/10.4161/cam.5.4.16911
  • Wang H, Li ZY, Liu Y, Persson J, Beyer I, Moller T, Koyuncu D, Drescher MR, Strauss R, Zhang XB, et al. Desmoglein 2 is a receptor for adenovirus serotypes 3, 7, 11 and 14. Nature Med 2011; 17:96-104; PMID:21151137; http://dx.doi.org/10.1038/nm.2270
  • Kamekura R, Kolegraff KN, Nava P, Hilgarth RS, Feng M, Parkos CA, Nusrat A. Loss of the desmosomal cadherin desmoglein-2 suppresses colon cancer Cell proliferation through EGFR signaling. Oncogene 2013; PMID:24166502;
  • Nava P, Laukoetter MG, Hopkins AM, Laur O, Gerner-Smidt K, Green KJ, Parkos CA, Nusrat A. Desmoglein-2: a novel regulator of apoptosis in the intestinal epithelium. Mol Biol Cell 2007; 18:4565-78; PMID:17804817; http://dx.doi.org/10.1091/mbc.E07-05-0426
  • Kolegraff K, Nava P, Helms MN, Parkos CA, Nusrat A. Loss of desmocollin-2 confers a tumorigenic phenotype to colonic epithelial Cells through activation of Akt/beta-catenin signaling. Mol Biol Cell 2011; 22:1121-34; PMID:21325624; http://dx.doi.org/10.1091/mbc.E10-10-0845
  • Green KJ, Gaudry CA. Are desmosomes more than tethers for intermediate filaments? Nat Rev Mol Cell Biol 2000; 1:208-16; PMID:11252896; http://dx.doi.org/10.1038/35043032
  • Delva E, Tucker DK, Kowalczyk AP. The desmosome. Cold Spring Harbor perspectives in Biol 2009; 1:a002543; http://dx.doi.org/10.1101/cshperspect.a002543
  • Ireton RC, Davis MA, van Hengel J, Mariner DJ, Barnes K, Thoreson MA, Anastasiadis PZ, Matrisian L, Bundy LM, Sealy L, et al. A novel role for p120 catenin in E-cadherin function. J Cell Biol 2002; 159:465-76; PMID:12427869; http://dx.doi.org/10.1083/jcb.200205115
  • 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; 120:1824-35; PMID:20484816; http://dx.doi.org/10.1172/JCI41414
  • Kovacs EM, Goodwin M, Ali RG, Paterson AD, Yap AS. Cadherin-directed actin assembly: E-cadherin physically associates with the Arp2/3 complex to direct actin assembly in nascent adhesive contacts. Curr Biol: CB 2002; 12:379-82; http://dx.doi.org/10.1016/S0960-9822(02)00661-9
  • Behrens J. Cadherins and catenins: role in signal transduction and tumor progression. Cancer Metast Rev 1999; 18:15-30; http://dx.doi.org/10.1023/A:1006200102166
  • Troxell ML, Gopalakrishnan S, McCormack J, Poteat BA, Pennington J, Garringer SM, Schneeberger EE, Nelson WJ, Marrs JA. Inhibiting cadherin function by dominant mutant E-cadherin expression increases the extent of tight junction assembly. J Cell science 2000; 113(Pt 6):985-96; PMID:10683147;
  • Guo X, Rao JN, Liu L, Zou TT, Turner DJ, Bass BL, Wang JY. Regulation of adherens junctions and epithelial paraCellular permeability: a novel function for polyamines. Am J Physiol Cell Physiol 2003; 285:C1174-87; PMID:12853285; http://dx.doi.org/10.1152/ajpcell.00015.2003
  • Ginzberg HH, Cherapanov V, Dong Q, Cantin A, McCulloch CA, Shannon PT, Downey GP. Neutrophil-mediated epithelial injury during transmigration: role of elastase. Am J Phys Gastrointest L 2001; 281:G705-17
  • Evans SM, Blyth DI, Wong T, Sanjar S, West MR. Decreased distribution of lung epithelial junction proteins after intratracheal antigen or lipopolysaccharide challenge: correlation with neutrophil influx and levels of BALF sE-cadherin. Am J Respir Cell Mol Biol 2002; 27:446-54; PMID:12356578; http://dx.doi.org/10.1165/rcmb.4776
  • Fujita T, Kishimoto A, Shiba H, Hayashida K, Kajiya M, Uchida Y, Matsuda S, Takeda K, Ouhara K, Kawaguchi H, et al. Irsogladine maleate regulates neutrophil migration and E-cadherin expression in gingival epithelium stimulated by Aggregatibacter actinomycetemcomitans. Biochem Pharmacol 2010; 79:1496-505; PMID:20096665; http://dx.doi.org/10.1016/j.bcp.2010.01.017
  • Grotendorst GR, Smale G, Pencev D. Production of transforming growth factor beta by human peripheral blood monocytes and neutrophils. J Cell Physiol 1989; 140:396-402; PMID:2745570; http://dx.doi.org/10.1002/jcp.1041400226
  • Wright CD, Mulsch A, Busse R, Osswald H. Generation of nitric oxide by human neutrophils. Biochem Biophys Res Commun 1989; 160:813-9; PMID:2541713; http://dx.doi.org/10.1016/0006-291X(89)92506-0
  • Ardi VC, Kupriyanova TA, Deryugina EI, Quigley JP. Human neutrophils uniquely release TIMP-free MMP-9 to provide a potent catalytic stimulator of angiogenesis. Proc Natl Acad Sci U S A 2007; 104:20262-7; PMID:18077379; http://dx.doi.org/10.1073/pnas.0706438104
  • Vogelmann R, Nguyen-Tat MD, Giehl K, Adler G, Wedlich D, Menke A. TGFbeta-induced downregulation of E-cadherin-based Cell-Cell adhesion depends on PI3-kinase and PTEN. J Cell Sci 2005; 118:4901-12; PMID:16219695; http://dx.doi.org/10.1242/jcs.02594
  • Mei JM, Borchert GL, Donald SP, Phang JM. Matrix metalloproteinase(s) mediate(s) NO-induced dissociation of beta-catenin from membrane bound E-cadherin and formation of nuclear beta-catenin/LEF-1 complex. Carcinogenesis 2002; 23:2119-22; PMID:12507936; http://dx.doi.org/10.1093/carcin/23.12.2119
  • Zheng G, Lyons JG, Tan TK, Wang Y, Hsu TT, Min D, Succar L, Rangan GK, Hu M, Henderson BR, et al. Disruption of E-cadherin by matrix metalloproteinase directly mediates epithelial-mesenchymal transition downstream of transforming growth factor-beta1 in renal tubular epithelial Cells. Am J Pathol 2009; 175:580-91; PMID:19590041; http://dx.doi.org/10.2353/ajpath.2009.080983
  • Zemans RL, Briones N, Campbell M, McClendon J, Young SK, Suzuki T, Yang IV, De Langhe S, Reynolds SD, Mason RJ, et al. Neutrophil transmigration triggers repair of the lung epithelium via beta-catenin signaling. Proc Natl Acad Sci U S A 2011; 108:15990-5; PMID:21880956; http://dx.doi.org/10.1073/pnas.1110144108
  • Pecina-Slaus N. Tumor suppressor gene E-cadherin and its role in normal and malignant cells. Cancer Cell Int 2003; 3:17; PMID:14613514; http://dx.doi.org/10.1186/1475-2867-3-17
  • Semb H, Christofori G. The tumor-suppressor function of E-cadherin. Am J Hum Genet 1998; 63:1588-93; PMID:9837810; http://dx.doi.org/10.1086/302173
  • Bae GY, Choi SJ, Lee JS, Jo J, Lee J, Kim J, Cha HJ. Loss of E-cadherin activates EGFR-MEK/ERK signaling, which promotes invasion via the ZEB1/MMP2 axis in non-small Cell lung cancer. Oncotarget 2013; 4:2512-22; PMID:24318272;
  • Gaida MM, Steffen TG, Gunther F, Tschaharganeh DF, Felix K, Bergmann F, Schirmacher P, Hansch GM. Polymorphonuclear neutrophils promote dyshesion of tumor Cells and elastase-mediated degradation of E-cadherin in pancreatic tumors. Eur J Immunol 2012; 42:3369-80; PMID:23001948; http://dx.doi.org/10.1002/eji.201242628
  • Mengaud J, Ohayon H, Gounon P, Mege RM, Cossart P. E-cadherin is the receptor for internalin, a surface protein required for entry of L. monocytogenes into epithelial Cells. Cell 1996; 84:923-32; PMID:8601315; http://dx.doi.org/10.1016/S0092-8674(00)81070-3
  • Le Floc'h A, Jalil A, Vergnon I, Le Maux Chansac B, Lazar V, Bismuth G, Chouaib S, Mami-Chouaib F. Alpha E beta 7 integrin interaction with E-cadherin promotes antitumor CTL activity by triggering lytic granule polarization and exocytosis. J Exp Med 2007; 204:559-70; PMID:17325197; http://dx.doi.org/10.1084/jem.20061524
  • Martin-Padura I, Lostaglio S, Schneemann M, Williams L, Romano M, FrusCella P, Panzeri C, Stoppacciaro A, Ruco L, Villa A, et al. Junctional adhesion molecule, a novel member of the immunoglobulin superfamily that distributes at interCellular junctions and modulates monocyte transmigration. J Cell Biol 1998; 142:117-27; PMID:9660867; http://dx.doi.org/10.1083/jcb.142.1.117
  • Woodfin A, Voisin MB, Imhof BA, Dejana E, Engelhardt B, Nourshargh S. Endothelial Cell activation leads to neutrophil transmigration as supported by the sequential roles of ICAM-2, JAM-A, and PECAM-1. Blood 2009; 113:6246-57; PMID:19211506; http://dx.doi.org/10.1182/blood-2008-11-188375
  • Liu Y, Nusrat A, Schnell FJ, Reaves TA, Walsh S, Pochet M, Parkos CA. Human junction adhesion molecule regulates tight junction resealing in epithelia. J Cell Sci 2000; 113(Pt 13):2363-74; PMID:10852816
  • Weber DA, Sumagin R, McCall IC, Leoni G, Neumann PA, Andargachew R, Brazil JC, Medina-Contreras O, Denning TL, Nusrat A, et al. Neutrophil-derived JAML inhibits repair of intestinal epithelial injury during acute inflammation. Mucosal Immunol 2014; PMID:24621992
  • Ikenouchi J, Furuse M, Furuse K, Sasaki H, Tsukita S, Tsukita S. TriCellulin constitutes a novel barrier at triCellular contacts of epithelial Cells. J Cell Biol 2005; 171:939-45; PMID:16365161; http://dx.doi.org/10.1083/jcb.200510043
  • Huber D, Balda MS, Matter K. Occludin modulates transepithelial migration of neutrophils. J Biol Chem 2000; 275:5773-8; PMID:10681565; http://dx.doi.org/10.1074/jbc.275.8.5773
  • Gunzel D, Yu AS. Claudins and the modulation of tight junction permeability. Physiol Rev 2013; 93:525-69; PMID:23589827; http://dx.doi.org/10.1152/physrev.00019.2012
  • Anderson JM, Van Itallie CM. Physiology and function of the tight junction. Cold Spring Harbor Perspect Biol 2009; 1:a002584; http://dx.doi.org/10.1101/cshperspect.a002584
  • McCarthy KM, Skare IB, Stankewich MC, Furuse M, Tsukita S, Rogers RA, Lynch RD, Schneeberger EE. Occludin is a functional component of the tight junction. J Cell Sci 1996; 109(Pt 9):2287-98; PMID:8886979
  • Murata M, Kojima T, Yamamoto T, Go M, Takano K, Osanai M, Chiba H, Sawada N. Down-regulation of survival signaling through MAPK and Akt in occludin-deficient mouse hepatocytes in vitro. Exp Cell Res 2005; 310:140-51; PMID:16112666; http://dx.doi.org/10.1016/j.yexcr.2005.07.017
  • Flynn AN, Buret AG. Caspases-3, -8, and -9 are required for induction of epithelial Cell apoptosis by enteropathogenic E. coli but are dispensable for increased paraCellular permeability. Microb Pathogenesis 2008; 44:311-9; http://dx.doi.org/10.1016/j.micpath.2007.10.007
  • Beeman NE, Baumgartner HK, Webb PG, Schaack JB, Neville MC. Disruption of occludin function in polarized epithelial Cells activates the extrinsic pathway of apoptosis leading to cell extrusion without loss of transepithelial resistance. BMC Cell Biol 2009; 10:85; PMID:20003227; http://dx.doi.org/10.1186/1471-2121-10-85
  • Du D, Xu F, Yu L, Zhang C, Lu X, Yuan H, Huang Q, Zhang F, Bao H, Jia L, et al. The tight junction protein, occludin, regulates the directional migration of epithelial cells. Dev Cell 2010; 18:52-63; PMID:20152177; http://dx.doi.org/10.1016/j.devcel.2009.12.008
  • Monteiro AC, Sumagin R, Rankin CR, Leoni G, Mina MJ, Reiter DM, Stehle T, Dermody TS, Schaefer SA, Hall RA, et al. JAM-A associates with ZO-2, afadin, and PDZ-GEF1 to activate Rap2c and regulate epithelial barrier function. Mol Biol Cell 2013; 24:2849-60; PMID:23885123; http://dx.doi.org/10.1091/mbc.E13-06-0298
  • Ebnet K. JAM-A and aPKC: A close pair during cell-cell contact maturation and tight junction formation in epithelial cells. Tissue Barriers 2013; 1:e22993
  • Laukoetter MG, Nava P, Lee WY, Severson EA, Capaldo CT, Babbin BA, Williams IR, Koval M, Peatman E, Campbell JA, et al. JAM-A regulates permeability and inflammation in the intestine in vivo. J Exp Med 2007; 204:3067-76; PMID:18039951; http://dx.doi.org/10.1084/jem.20071416
  • Nava P, Capaldo CT, Koch S, Kolegraff K, Rankin CR, Farkas AE, Feasel ME, Li L, Addis C, Parkos CA, et al. JAM-A regulates epithelial proliferation through Akt/beta-catenin signalling. EMBO Reports 2011; 12:314-20; PMID:21372850; http://dx.doi.org/10.1038/embor.2011.16
  • McSherry EA, Brennan K, Hudson L, Hill AD, Hopkins AM. Breast cancer Cell migration is regulated through junctional adhesion molecule-A-mediated activation of Rap1 GTPase. Breast Cancer Res: BCR 2011; 13:R31
  • Yamamoto M, Ramirez SH, Sato S, Kiyota T, Cerny RL, Kaibuchi K, Persidsky Y, Ikezu T. Phosphorylation of claudin-5 and occludin by rho kinase in brain endothelial Cells. Am J Pathol 2008; 172:521-33; PMID:18187566; http://dx.doi.org/10.2353/ajpath.2008.070076
  • 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; 159:2001-9; PMID:11733350; http://dx.doi.org/10.1016/S0002-9440(10)63051-9
  • Severson EA, Lee WY, Capaldo CT, Nusrat A, Parkos CA. Junctional adhesion molecule A interacts with Afadin and PDZ-GEF2 to activate Rap1A, regulate beta1 integrin levels, and enhance Cell migration. Mol Biol of the Cell 2009; 20:1916-25; http://dx.doi.org/10.1091/mbc.E08-10-1014
  • Monteiro AC, Luissint AC, Sumagin R, Lai C, Vielmuth F, Wolf MF, Laur O, Reiss K, Spindler V, Stehle T, et al. Trans-dimerization of JAM-A regulates Rap2 and is mediated by a domain that is distinct from the cis-dimerization interface. Mol Biol Cell 2014; 25:1574-85; PMID:24672055; http://dx.doi.org/10.1091/mbc.E14-01-0018
  • Raschperger E, Thyberg J, Pettersson S, Philipson L, Fuxe J, Pettersson RF. The coxsackie- and adenovirus receptor (CAR) is an in vivo marker for epithelial tight junctions, with a potential role in regulating permeability and tissue homeostasis. Exp Cell Res 2006; 312:1566-80; PMID:16542650; http://dx.doi.org/10.1016/j.yexcr.2006.01.025
  • Morton PE, Hicks A, Nastos T, Santis G, Parsons M. CAR regulates epithelial Cell junction stability through control of E-cadherin trafficking. Sci Rep 2013; 3:2889; PMID:24096322; http://dx.doi.org/10.1038/srep02889
  • Cohen CJ, Shieh JT, Pickles RJ, Okegawa T, Hsieh JT, Bergelson JM. The coxsackievirus and adenovirus receptor is a transmembrane component of the tight junction. Proc Natl Acad Sci U S A 2001; 98:15191-6; PMID:11734628; http://dx.doi.org/10.1073/pnas.261452898
  • Witherden DA, Verdino P, Rieder SE, Garijo O, Mills RE, Teyton L, Fischer WH, Wilson IA, Havran WL. The junctional adhesion molecule JAML is a costimulatory receptor for epithelial gammadelta T cell activation. Science 2010; 329:1205-10; PMID:20813954; http://dx.doi.org/10.1126/science.1192698
  • Lindberg FP, Gresham HD, Schwarz E, Brown EJ. Mol cloning of integrin-associated protein: an immunoglobulin family member with multiple membrane-spanning domains implicated in alpha v beta 3-dependent ligand binding. J Cell Biol 1993; 123:485-96; PMID:7691831; http://dx.doi.org/10.1083/jcb.123.2.485
  • Parkos CA, Colgan SP, Liang TW, Nusrat A, Bacarra AE, Carnes DK, Madara JL. CD47 mediates post-adhesive events required for neutrophil migration across polarized intestinal epithelia. J Cell Biol 1996; 132:437-50; PMID:8636220; http://dx.doi.org/10.1083/jcb.132.3.437
  • Jiang P, Lagenaur CF, Narayanan V. Integrin-associated protein is a ligand for the P84 neural adhesion molecule. J Biol Chem 1999; 274:559-62; PMID:9872987; http://dx.doi.org/10.1074/jbc.274.2.559
  • Seiffert M, Cant C, Chen Z, Rappold I, Brugger W, Kanz L, Brown EJ, Ullrich A, Buhring HJ. Human signal-regulatory protein is expressed on normal, but not on subsets of leukemic myeloid Cells and mediates Cellular adhesion involving its counterreceptor CD47. Blood 1999; 94:3633-43; PMID:10572074;
  • Freyberg MA, Kaiser D, Graf R, Vischer P, Friedl P. Integrin-associated protein and thrombospondin-1 as endothelial mechanosensitive death mediators. Biochem Biophys Res Commun 2000; 271:584-8; PMID:10814505; http://dx.doi.org/10.1006/bbrc.2000.2678
  • Graf R, Freyberg M, Kaiser D, Friedl P. Mechanosensitive induction of apoptosis in fibroblasts is regulated by thrombospondin-1 and integrin associated protein (CD47). Apoptosis: Int J Prog Cell Death 2002; 7:493-8; http://dx.doi.org/10.1023/A:1020634924760
  • Trzpis M, McLaughlin PM, de Leij LM, Harmsen MC. Epithelial Cell adhesion molecule: more than a carcinoma marker and adhesion molecule. Am J Pathol 2007; 171:386-95; PMID:17600130; http://dx.doi.org/10.2353/ajpath.2007.070152
  • Munz M, Baeuerle PA, Gires O. The emerging role of EpCAM in cancer and stem Cell signaling. Cancer Res 2009; 69:5627-9; PMID:19584271; http://dx.doi.org/10.1158/0008-5472.CAN-09-0654
  • Munz M, Kieu C, Mack B, Schmitt B, Zeidler R, Gires O. The carcinoma-associated antigen EpCAM upregulates c-myc and induces Cell proliferation. Oncogene 2004; 23:5748-58; PMID:15195135; http://dx.doi.org/10.1038/sj.onc.1207610
  • Maetzel D, Denzel S, Mack B, Canis M, Went P, Benk M, Kieu C, Papior P, Baeuerle PA, Munz M, et al. Nuclear signalling by tumour-associated antigen EpCAM. Nat Cell Biol 2009; 11:162-71; PMID:19136966; http://dx.doi.org/10.1038/ncb1824
  • Grommes J, Soehnlein O. Contribution of neutrophils to acute lung injury. Mol Med 2011; 17:293-307; PMID:21046059; http://dx.doi.org/10.2119/molmed.2010.00138
  • Downey DG, Bell SC, Elborn JS. Neutrophils in cystic fibrosis. Thorax 2009; 64:81-8; PMID:19103874; http://dx.doi.org/10.1136/thx.2007.082388
  • Biffl WL, Moore EE, Moore FA, Barnett CC, Jr., Carl VS, Peterson VN. Interleukin-6 delays neutrophil apoptosis. Arch Surg 1996; 131:24-9; discussion 9-30; PMID:8546573; http://dx.doi.org/10.1001/archsurg.1996.01430130026005
  • Taneja R, Parodo J, Jia SH, Kapus A, Rotstein OD, Marshall JC. Delayed neutrophil apoptosis in sepsis is associated with maintenance of mitochondrial transmembrane potential and reduced caspase-9 activity. Crit Care Med 2004; 32:1460-9; PMID:15241089; http://dx.doi.org/10.1097/01.CCM.0000129975.26905.77
  • Le'Negrate G, Rostagno P, Auberger P, Rossi B, Hofman P. Downregulation of caspases and Fas ligand expression, and increased lifespan of neutrophils after transmigration across intestinal epithelium. Cell Death Differ 2003; 10:153-62; PMID:12700643; http://dx.doi.org/10.1038/sj.cdd.4401110
  • Kaiserlian D, Rigal D, Abello J, Revillard JP. Expression, function and regulation of the intercellular adhesion molecule-1 (ICAM-1) on human intestinal epithelial cell lines. Eur J Immunol 1991; 21:2415-21; PMID:1680698; http://dx.doi.org/10.1002/eji.1830211018
  • Louis NA, Hamilton KE, Kong T, Colgan SP. HIF-dependent induction of apical CD55 coordinates epithelial clearance of neutrophils. FASEB J: Off Pub Fed Am Soc Exp Biol 2005; 19:950-9; http://dx.doi.org/10.1096/fj.04-3251com
  • Leir SH, Holgate ST, Lackie PM. Inflammatory cytokines can enhance CD44-mediated airway epithelial Cell adhesion independently of CD44 expression. Am J Physiol Lung Cell Mol Physiol 2003; 285:L1305-11; PMID:12909589;
  • Yang L, Froio RM, Sciuto TE, Dvorak AM, Alon R, Luscinskas FW. ICAM-1 regulates neutrophil adhesion and transCellular migration of TNF-alpha-activated vascular endothelium under flow. Blood 2005; 106:584-92; PMID:15811956; http://dx.doi.org/10.1182/blood-2004-12-4942
  • Lawson C, Wolf S. ICAM-1 signaling in endothelial Cells. Pharmacol Rep: PR 2009; 61:22-32; http://dx.doi.org/10.1016/S1734-1140(09)70004-0
  • Sumagin R, Lomakina E, Sarelius IH. Leukocyte-endothelial Cell interactions are linked to vascular permeability via ICAM-1-mediated signaling. Am J Physiol Heart Circ Physiol 2008; 295:H969-H77; PMID:18641276; http://dx.doi.org/10.1152/ajpheart.00400.2008
  • Parkos CA, Colgan SP, Diamond MS, Nusrat A, Liang TW, Springer TA, Madara JL. Expression and polarization of interCellular adhesion molecule-1 on human intestinal epithelia: consequences for CD11b/CD18-mediated interactions with neutrophils. Mol Med 1996; 2:489-505; PMID:8827719
  • Paolieri F, Battifora M, Riccio AM, Pesce G, Canonica GW, Bagnasco M. InterCellular adhesion molecule-1 on cultured human epithelial Cell lines: influence of proinflammatory cytokines. Allergy 1997; 52:521-31; PMID:9201363; http://dx.doi.org/10.1111/j.1398-9995.1997.tb02595.x
  • Lhotta K, Neumayer HP, Joannidis M, Geissler D, Konig P. Renal expression of interCellular adhesion molecule-1 in different forms of glomerulonephritis. Clin Sci 1991; 81:477-81; PMID:1682080;
  • Look DC, Rapp SR, Keller BT, Holtzman MJ. Selective induction of interCellular adhesion molecule-1 by interferon-gamma in human airway epithelial Cells. Am J Physiol 1992; 263:L79-87; PMID:1353306;
  • Burns AR, Takei F, Doerschuk CM. Quantitation of ICAM-1 expression in mouse lung during pneumonia. J Immunol 1994; 153:3189-98; PMID:7916369;
  • Sumagin R, Robin AZ, Nusrat A, Parkos CA. Transmigrated neutrophils in the intestinal lumen engage ICAM-1 to regulate the epithelial barrier and neutrophil recruitment. Mucosal Immunol 2014; 7:905-15; PMID:24345805; http://dx.doi.org/10.1038/mi.2013.106
  • Gay AN, Mushin OP, Lazar DA, Naik-Mathuria BJ, Yu L, Gobin A, Smith CW, Olutoye OO. Wound healing characteristics of ICAM-1 null mice devoid of all isoforms of ICAM-1. J Surg Res 2011; 171:e1-7; PMID:21872884; http://dx.doi.org/10.1016/j.jss.2011.06.053
  • Byeseda SE, Burns AR, Dieffenbaugher S, Rumbaut RE, Smith CW, Li Z. ICAM-1 is necessary for epithelial recruitment of gammadelta T cells and efficient corneal wound healing. Am J Pathol 2009; 175:571-9; PMID:19608878; http://dx.doi.org/10.2353/ajpath.2009.090112
  • Kevil CG, Orr AW, Langston W, Mickett K, Murphy-Ullrich J, Patel RP, Kucik DF, Bullard DC. InterCellular adhesion molecule-1 (ICAM-1) regulates endothelial Cell motility through a nitric oxide-dependent pathway. J Biol Chem 2004; 279:19230-8; PMID:14985356; http://dx.doi.org/10.1074/jbc.M312025200
  • Lublin DM, Atkinson JP. Decay-accelerating factor: biochemistry, Mol Biol, and function. Ann Rev Immunol 1989; 7:35-58; http://dx.doi.org/10.1146/annurev.iy.07.040189.000343
  • Tieng V, Le Bouguenec C, du Merle L, Bertheau P, Desreumaux P, Janin A, Charron D, Toubert A. Binding of Escherichia coli adhesin AfaE to CD55 triggers cell-surface expression of the MHC class I-related molecule MICA. Proc Natl Acad Sci U S A 2002; 99:2977-82; PMID:11830641; http://dx.doi.org/10.1073/pnas.032668099
  • Lawrence DW, Bruyninckx WJ, Louis NA, Lublin DM, Stahl GL, Parkos CA, Colgan SP. Antiadhesive role of apical decay-accelerating factor (CD55) in human neutrophil transmigration across mucosal epithelia. J Exp Med 2003; 198:999-1010; PMID:14530374; http://dx.doi.org/10.1084/jem.20030380
  • Heine H, El-Samalouti VT, Notzel C, Pfeiffer A, Lentschat A, Kusumoto S, Schmitz G, Hamann L, Ulmer AJ. CD55/decay accelerating factor is part of the lipopolysaccharide-induced receptor complex. European J Immunol 2003; 33:1399-408; http://dx.doi.org/10.1002/eji.200323381
  • Leemans JC, te Velde AA, Florquin S, Bennink RJ, de Bruin K, van Lier RA, van der Poll T, Hamann J. The epidermal growth factor-seven transmembrane (EGF-TM7) receptor CD97 is required for neutrophil migration and host defense. J Immunol 2004; 172:1125-31; PMID:14707087; http://dx.doi.org/10.4049/jimmunol.172.2.1125
  • Brazil JC, Lee WY, Kolegraff KN, Nusrat A, Parkos CA, Louis NA. Neutrophil migration across intestinal epithelium: evidence for a role of CD44 in regulating detachment of migrating cells from the luminal surface. J Immunol 2010; 185:7026-36; PMID:20974992; http://dx.doi.org/10.4049/jimmunol.1001293
  • Ponta H, Sherman L, Herrlich PA. CD44: from adhesion molecules to signalling regulators. Nat Rev Mol Cell Biol 2003; 4:33-45; PMID:12511867; http://dx.doi.org/10.1038/nrm1004
  • Lesley J, Hascall VC, Tammi M, Hyman R. Hyaluronan binding by cell surface CD44. J Biol Chem 2000; 275:26967-75; PMID:10871609;
  • Borland G, Ross JA, Guy K. Forms and functions of CD44. Immunol 1998; 93:139-48; http://dx.doi.org/10.1046/j.1365-2567.1998.00431.x
  • Bourguignon LY, Zhu H, Shao L, Zhu D, Chen YW. Rho-kinase (ROK) promotes CD44v(3,8-10)-ankyrin interaction and tumor cell migration in metastatic breast cancer cells. Cell Motil Cytoskel 1999; 43:269-87; http://dx.doi.org/10.1002/(SICI)1097-0169(1999)43:4%3c269::AID-CM1%3e3.0.CO;2-5
  • Tsukita S, Oishi K, Sato N, Sagara J, Kawai A, Tsukita S. ERM family members as Mol linkers between the cell surface glycoprotein CD44 and actin-based cytoskeletons. J Cell Biol 1994; 126:391-401; PMID:7518464; http://dx.doi.org/10.1083/jcb.126.2.391
  • Yu Q, Stamenkovic I. Localization of matrix metalloproteinase 9 to the cell surface provides a mechanism for CD44-mediated tumor invasion. Genes Dev 1999; 13:35-48; PMID:9887098; http://dx.doi.org/10.1101/gad.13.1.35
  • Yu Q, Toole BP, Stamenkovic I. Induction of apoptosis of metastatic mammary carcinoma cells in vivo by disruption of tumor cell surface CD44 function. J Exp Med 1997; 186:1985-96; PMID:9396767; http://dx.doi.org/10.1084/jem.186.12.1985
  • Brazil JC, Liu R, Sumagin R, Kolegraff KN, Nusrat A, Cummings RD, Parkos CA, Louis NA. alpha3/4 Fucosyltransferase 3-dependent synthesis of Sialyl Lewis A on CD44 variant containing exon 6 mediates polymorphonuclear leukocyte detachment from intestinal epithelium during transepithelial migration. J Immunol 2013; 191:4804-17; PMID:24068663; http://dx.doi.org/10.4049/jimmunol.1301307
  • Yu Q, Stamenkovic I. Cell surface-localized matrix metalloproteinase-9 proteolytically activates TGF-beta and promotes tumor invasion and angiogenesis. Genes Dev 2000; 14:163-76; PMID:10652271;
  • Lammich S, Okochi M, Takeda M, Kaether C, Capell A, Zimmer AK, Edbauer D, Walter J, Steiner H, Haass C. Presenilin-dependent intramembrane proteolysis of CD44 leads to the liberation of its intracellular domain and the secretion of an Abeta-like peptide. J Biol Chem 2002; 277:44754-9; PMID:12223485; http://dx.doi.org/10.1074/jbc.M206872200
  • Okamoto I, Kawano Y, Murakami D, Sasayama T, Araki N, Miki T, Wong AJ, Saya H. Proteolytic release of CD44 intracellular domain and its role in the CD44 signaling pathway. J Cell Biol 2001; 155:755-62; PMID:11714729; http://dx.doi.org/10.1083/jcb.200108159
  • Brennan D, Peltonen S, Dowling A, Medhat W, Green KJ, Wahl JK, 3rd, Del Galdo F, Mahoney MG. A role for caveolin-1 in desmoglein binding and desmosome dynamics. Oncogene 2012; 31:1636-48; PMID:21841821; http://dx.doi.org/10.1038/onc.2011.346
  • Kobayashi N, Ikesue A, Majumdar S, Siahaan TJ. Inhibition of e-cadherin-mediated homotypic adhesion of Caco-2 cells: a novel evaluation assay for peptide activities in modulating cell-cell adhesion. J Pharmacol Exp Ther 2006; 317:309-16; PMID:16371447; http://dx.doi.org/10.1124/jpet.105.097535
  • Lee MG, Sharrow SO, Farr AG, Singer A, Udey MC. Expression of the homotypic adhesion molecule E-cadherin by immature murine thymocytes and thymic epithelial cells. J Immunol 1994; 152:5653-9; PMID:8207198;
  • Cording J, Berg J, Kading N, Bellmann C, Tscheik C, Westphal JK, Milatz S, Gunzel D, Wolburg H, Piontek J, et al. In tight junctions, claudins regulate the interactions between occludin, tricellulin and marvelD3, which, inversely, modulate claudin oligomerization. J Cell Sci 2013; 126:554-64; PMID:23203797; http://dx.doi.org/10.1242/jcs.114306
  • Ikenouchi J, Sasaki H, Tsukita S, Furuse M, Tsukita S. Loss of occludin affects tricellular localization of tricellulin. Mol Biol Cell 2008; 19:4687-93; PMID:18768749; http://dx.doi.org/10.1091/mbc.E08-05-0530
  • Babinska A, Kedees MH, Athar H, Sobocki T, Sobocka MB, Ahmed T, Ehrlich YH, Hussain MM, Kornecki E. Two regions of the human platelet F11-receptor (F11R) are critical for platelet aggregation, potentiation and adhesion. Thromb Haemostasis 2002; 87:712-21;
  • Bazzoni G, Martinez-Estrada OM, Mueller F, Nelboeck P, Schmid G, Bartfai T, Dejana E, Brockhaus M. Homophilic interaction of junctional adhesion molecule. J Biol Chem 2000; 275:30970-6; PMID:10913139; http://dx.doi.org/10.1074/jbc.M003946200
  • Kostrewa D, Brockhaus M, D'Arcy A, Dale GE, Nelboeck P, Schmid G, Mueller F, Bazzoni G, Dejana E, Bartfai T, et al. X-ray structure of junctional adhesion molecule: structural basis for homophilic adhesion via a novel dimerization motif. EMBO J 2001; 20:4391-8; PMID:11500366; http://dx.doi.org/10.1093/emboj/20.16.4391
  • Hirabayashi S, Tajima M, Yao I, Nishimura W, Mori H, Hata Y. JAM4, a junctional cell adhesion molecule interacting with a tight junction protein, MAGI-1. Mol Cell Biol 2003; 23:4267-82; PMID:12773569; http://dx.doi.org/10.1128/MCB.23.12.4267-4282.2003
  • Ding ZM, Babensee JE, Simon SI, Lu H, Perrard JL, Bullard DC, Dai XY, Bromley SK, Dustin ML, Entman ML, et al. Relative contribution of LFA-1 and Mac-1 to neutrophil adhesion and migration. J Immunol 1999; 163:5029-38; PMID:10528208

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