Tight junction dynamics: The role of junctional adhesion molecules (JAMs)

Cell and Tissue Research

Volumn 355, Issue 3, 2014, Pages 701-715

  Garrido Urbani, S ^a   Bradfield, P F ^a   Imhof, B A ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

Author keywords

Inflammation; JAM; Leukocyte migration; Polarity; Tight junction

Indexed keywords

JUNCTIONAL ADHESION MOLECULE;

ANIMAL; CELL MOTION; HUMAN; LEUKOCYTE; PHYSIOLOGY; TIGHT JUNCTION;

ANIMALS; CELL MOVEMENT; HUMANS; JUNCTIONAL ADHESION MOLECULES; LEUKOCYTES; TIGHT JUNCTIONS;

EID: 84899432057     PISSN: 0302766X     EISSN: 14320878     Source Type: Journal    
DOI: 10.1007/s00441-014-1820-1     Document Type: Review

References (131)

1. Angelow S, Ahlstrom R, Yu AS (2008) Biology of claudins. Am J Physiol Ren Physiol 295:F867-F876
2. Arrate MP, Rodriguez JM, Tran TM, Brock TA, Cunningham SA (2001) Cloning of human junctional adhesion molecule 3 (JAM3) and its identification as the JAM2 counter-receptor. J Biol Chem 276:45826-45832
3. Arthur FE, Shivers RR, Bowman PD (1987) Astrocyte-mediated induction of tight junctions in brain capillary endothelium: an efficient in vitro model. Brain Res 433:155-159
4. Asakura T, Nakanishi H, Sakisaka T, Takahashi K, Mandai K, Nishimura M, Sasaki T, Takai Y (1999) Similar and differential behaviour between the nectin-afadin-ponsin and cadherin-catenin systems during the formation and disruption of the polarized junctional alignment in epithelial cells. Genes Cells 4:573-581
5. Aurrand-Lions MA, Duncan L, Pasquier LD, Imhof BA (2000) Cloning of JAM-2 and JAM-3: an emerging junctional adhesion molecular family? Curr Top Microbiol Immunol 251:91-98
6. Aurrand-Lions M, Duncan L, Ballestrem C, Imhof BA (2001a) JAM-2, a novel immunoglobulin superfamily molecule, expressed by endothelial and lymphatic cells. J Biol Chem 276:2733-2741
7. Aurrand-Lions M, Johnson-Leger C, Wong C, Pasquier LD, Imhof BA (2001b) Heterogeneity of endothelial junctions is reflected by differential expression and specific subcellular localization of the three JAM family members. Blood 98:3699-3707
8. Barton ES, Forrest JC, Connolly JL, Chappell JD, Liu Y, Schnell FJ, Nusrat A, Parkos CA, Dermody TS (2001) Junction adhesion molecule is a receptor for reovirus. Cell 104:441-451
9. Bazzoni G, Dejana E (2004) Endothelial cell-to-cell junctions: molecular organization and role in vascular homeostasis. Physiol Rev 84:869-901
10. Bazzoni G, Martinez-Estrada OM, Mueller F, Nelboeck P, Schmid G, Bartfai T, Dejana E, Brockhaus M (2000) Homophilic interaction of junctional adhesion molecule. J Biol Chem 275:30970-30976
11. Bergelson JM, Cunningham JA, Droguett G, Kurt-Jones EA, Krithivas A, Hong JS, Horwitz MS, Crowell RL, Finberg RW (1997) Isolation of a common receptor for Coxsackie B viruses and adenoviruses 2 and 5. Science 275:1320-1323
12. Bradfield PF, Nourshargh S, Aurrand-Lions M, Imhof BA (2007a) JAM family and related proteins in leukocyte migration (Vestweber series). Arterioscler Thromb Vasc Biol 27:2104-2112
13. Bradfield PF, Scheiermann C, Nourshargh S, Ody C, Luscinskas FW, Rainger GE, Nash GB, Miljkovic-Licina M, Aurrand-Lions M, Imhof BA (2007b) JAM-C regulates unidirectional monocyte transendothelial migration in inflammation. Blood 110:2545-2555
14. Brightman MW, Reese TS (1969) Junctions between intimately apposed cell membranes in the vertebrate brain. J Cell Biol 40:648-677
15. Butcher EC, Picker LJ (1996) Lymphocyte homing and homeostasis. Science 272:60-66
16. Cera MR, Del Prete A, Vecchi A, Corada M, Martin-Padura I, Motoike T, Tonetti P, Bazzoni G, Vermi W, Gentili F, Bernasconi S, Sato TN, Mantovani A, Dejana E (2004) Increased DC trafficking to lymph nodes and contact hypersensitivity in junctional adhesion molecule-A-deficient mice. J Clin Invest 114:729-738
17. Chretien I, Marcuz A, Courtet M, Katevuo K, Vainio O, Heath JK, White SJ, Pasquier LD (1998) CTX, a Xenopus thymocyte receptor, defines a molecular family conserved throughout vertebrates. Eur J Immunol 28:4094-4104
18. Christen S, Coppieters K, Rose K, Holdener M, Bayer M, Pfeilschifter JM, Hintermann E, von Herrath MG, Aurrand-Lions M, Imhof BA, Christen U (2013) Blockade but not overexpression of the junctional adhesion molecule C influences virus-induced type 1 diabetes in mice. PLoS ONE 8:e54675
19. Claude P (1978) Morphological factors influencing transepithelial permeability: a model for the resistance of the zonula occludens. J Membr Biol 39:219-232
20. Claude P, Goodenough DA (1973) Fracture faces of zonulae occludentes from "tight" and "leaky" epithelia. J Cell Biol 58:390-400
21. Cohen CJ, Shieh JT, Pickles RJ, Okegawa T, Hsieh JT, Bergelson JM (2001) The coxsackievirus and adenovirus receptor is a transmembrane component of the tight junction. Proc Natl Acad Sci U S A 98:15191-15196
22. Coyne CB, Voelker T, Pichla SL, Bergelson JM (2004) The coxsackievirus and adenovirus receptor interacts with the multi-PDZ domain protein-1 (MUPP-1) within the tight junction. J Biol Chem 279:48079-48084
23. Cunningham SA, Arrate MP, Rodriguez JM, Bjercke RJ, Vanderslice P, Morris AP, Brock TA (2000) A novel protein with homology to the junctional adhesion molecule. Characterization of leukocyte interactions. J Biol Chem 275:34750-34756
24. Cunningham SA, Rodriguez JM, Arrate MP, Tran TM, Brock TA (2002) JAM2 interacts with alpha4beta1. Facilitation by JAM3. J Biol Chem 277:27589-27592
25. Del Maschio A, De Luigi A, Martin-Padura I, Brockhaus M, Bartfai T, Fruscella P, Adorini L, Martino G, Furlan R, De Simoni MG, Dejana E (1999) Leukocyte recruitment in the cerebrospinal fluid of mice with experimental meningitis is inhibited by an antibody to junctional adhesion molecule (JAM). J Exp Med 190:1351-1356
26. Du Pasquier L, Courtet M, Chretien I (1999) Duplication and MHC linkage of the CTX family of genes in Xenopus and in mammals. Eur J Immunol 29:1729-1739
27. Ebnet K, Schulz CU, Meyer Zu Brickwedde MK, Pendl GG, Vestweber D (2000) Junctional adhesion molecule interacts with the PDZ domain-containing proteins AF-6 and ZO-1. J Biol Chem 275:27979-27988
28. Ebnet K, Suzuki A, Horikoshi Y, Hirose T, Meyer Zu Brickwedde MK, Ohno S, Vestweber D (2001) The cell polarity protein ASIP/PAR-3 directly associates with junctional adhesion molecule (JAM). EMBO J 20:3738-3748
29. Ebnet K, Aurrand-Lions M, Kuhn A, Kiefer F, Butz S, Zander K, Meyer zu Brickwedde MK, Suzuki A, Imhof BA, Vestweber D (2003) The junctional adhesion molecule (JAM) family members JAM-2 and JAM-3 associate with the cell polarity protein PAR-3: a possible role for JAMs in endothelial cell polarity. J Cell Sci 116:3879-3891
30. Engelhardt B, Ransohoff RM (2012) Capture, crawl, cross: the T cell code to breach the blood-brain barriers. Trends Immunol 33:579-589
31. Excoffon KJ, Hruska-Hageman A, Klotz M, Traver GL, Zabner J (2004) A role for the PDZ-binding domain of the coxsackie B virus and adenovirus receptor (CAR) in cell adhesion and growth. J Cell Sci 117:4401-4409
32. Fanning AS, Jameson BJ, Jesaitis LA, Anderson JM (1998) The tight junction protein ZO-1 establishes a link between the transmembrane protein occludin and the actin cytoskeleton. J Biol Chem 273:29745-29753
33. Farquhar MG, Palade GE (1963) Junctional complexes in various epithelia. J Cell Biol 17:375-412
34. Fechner H, Haack A, Wang H, Wang X, Eizema K, Pauschinger M, Schoemaker R, Veghel R, Houtsmuller A, Schultheiss HP, Lamers J, Poller W (1999) Expression of coxsackie adenovirus receptor and alphav-integrin does not correlate with adenovector targeting in vivo indicating anatomical vector barriers. Gene Ther 6:1520-1535
35. Fukuhara A, Irie K, Yamada A, Katata T, Honda T, Shimizu K, Nakanishi H, Takai Y (2002) Role of nectin in organization of tight junctions in epithelial cells. Genes Cells 7:1059-1072
36. Furuse M, Tsukita S (2006) Claudins in occluding junctions of humans and flies. Trends Cell Biol 16:181-188
37. Furuse M, Sasaki H, Fujimoto K, Tsukita S (1998) A single gene product, claudin-1 or -2, reconstitutes tight junction strands and recruits occludin in fibroblasts. J Cell Biol 143:391-401
38. Gao L, Macara IG, Joberty G (2002) Multiple splice variants of Par3 and of a novel related gene, Par3L, produce proteins with different binding properties. Gene 294:99-107
39. Garrido-Urbani S, Bradfield PF, Lee BP, Imhof BA (2008) Vascular and epithelial junctions: a barrier for leucocyte migration. Biochem Soc Trans 36:203-211
40. Gliki G, Ebnet K, Aurrand-Lions M, Imhof BA, Adams RH (2004) Spermatid differentiation requires the assembly of a cell polarity complex downstream of junctional adhesion molecule-C. Nature 431:320-324
41. Guillemot L, Paschoud S, Pulimeno P, Foglia A, Citi S (2008) The cytoplasmic plaque of tight junctions: a scaffolding and signalling center. Biochim Biophys Acta 1778:601-613
42. Guo YL, Bai R, Chen CX, Liu DQ, Liu Y, Zhang CY, Zen K (2009) Role of junctional adhesion molecule-like protein in mediating monocyte transendothelial migration. Arterioscler Thromb Vasc Biol 29:75-83
43. Hamazaki Y, Itoh M, Sasaki H, Furuse M, Tsukita S (2002) Multi-PDZ domain protein 1 (MUPP1) is concentrated at tight junctions through its possible interaction with claudin-1 and junctional adhesion molecule. J Biol Chem 277:455-461
44. Hirabayashi S, Tajima M, Yao I, Nishimura W, Mori H, Hata Y (2003) JAM4, a junctional cell adhesion molecule interacting with a tight junction protein, MAGI-1. Mol Cell Biol 23:4267-4282
45. Hirata K, Ishida T, Penta K, Rezaee M, Yang E, Wohlgemuth J, Quertermous T (2001) Cloning of an immunoglobulin family adhesion molecule selectively expressed by endothelial cells. J Biol Chem 276:16223-16231
46. Iden S, Misselwitz S, Peddibhotla SS, Tuncay H, Rehder D, Gerke V, Robenek H, Suzuki A, Ebnet K (2012) aPKC phosphorylates JAM-A at Ser285 to promote cell contact maturation and tight junction formation. J Cell Biol 196:623-639
47. Inoue M, Ishida T, Yasuda T, Toh R, Hara T, Cangara HM, Rikitake Y, Taira K, Sun L, Kundu RK, Quertermous T, Hirata K (2010) Endothelial cell-selective adhesion molecule modulates atherosclerosis through plaque angiogenesis and monocyte-endothelial interaction. Microvasc Res 80:179-187
48. Itoh M, Sasaki H, Furuse M, Ozaki H, Kita T, Tsukita S (2001) Junctional adhesion molecule (JAM) binds to PAR-3: a possible mechanism for the recruitment of PAR-3 to tight junctions. J Cell Biol 154:491-497
49. Johnson-Leger C, Imhof BA (2003) Forging the endothelium during inflammation: pushing at a half-open door? Cell Tissue Res 314:93-105
50. Johnson-Leger CA, Aurrand-Lions M, Beltraminelli N, Fasel N, Imhof BA (2002) Junctional adhesion molecule-2 (JAM-2) promotes lymphocyte transendothelial migration. Blood 100:2479-2486
51. Kansaku A, Hirabayashi S, Mori H, Fujiwara N, Kawata A, Ikeda M, Rokukawa C, Kurihara H, Hata Y (2006) Ligand-of-Numb protein X is an endocytic scaffold for junctional adhesion molecule 4. Oncogene 25:5071-5084
52. Keiper T, Al-Fakhri N, Chavakis E, Athanasopoulos AN, Isermann B, Herzog S, Saffrich R, Hersemeyer K, Bohle RM, Haendeler J, Preissner KT, Santoso S, Chavakis T (2005) The role of junctional adhesion molecule-C (JAM-C) in oxidized LDL-mediated leukocyte recruitment. FASEB J 19:2078-2080
53. Khounlotham M, Kim W, Peatman E, Nava P, Medina-Contreras O, Addis C, Koch S, Fournier B, Nusrat A, Denning TL, Parkos CA (2012) Compromised intestinal epithelial barrier induces adaptive immune compensation that protects from colitis. Immunity 37:563-573
54. Koenen RR, Pruessmeyer J, Soehnlein O, Fraemohs L, Zernecke A, Schwarz N, Reiss K, Sarabi A, Lindbom L, Hackeng TM, Weber C, Ludwig A (2009) Regulated release and functional modulation of junctional adhesion molecule A by disintegrin metalloproteinases. Blood 113:4799-4809
55. Kostrewa D, Brockhaus M, D'Arcy A, Dale GE, Nelboeck P, Schmid G, Mueller F, Bazzoni G, Dejana E, Bartfai T, Winkler FK, Hennig M (2001) X-ray structure of junctional adhesion molecule: structural basis for homophilic adhesion via a novel dimerization motif. EMBO J 20:4391-4398
56. Lakshmi SP, Reddy AT, Naik MU, Naik UP, Reddy RC (2012) Effects of JAM-A deficiency or blocking antibodies on neutrophil migration and lung injury in a murine model of ALI. Am J Physiol Lung Cell Mol Physiol 303:L758-L766
57. Lamagna C, Meda P, Mandicourt G, Brown J, Gilbert RJ, Jones EY, Kiefer F, Ruga P, Imhof BA, Aurrand-Lions M (2005) Dual interaction of JAM-C with JAM-B and alpha(M)beta2 integrin: function in junctional complexes and leukocyte adhesion. Mol Biol Cell 16:4992-5003
58. Laukoetter MG, Nava P, Lee WY, Severson EA, Capaldo CT, Babbin BA, Williams IR, Koval M, Peatman E, Campbell JA, Dermody TS, Nusrat A, Parkos CA (2007) JAM-A regulates permeability and inflammation in the intestine in vivo. J Exp Med 204:3067-3076
59. Lechner F, Sahrbacher U, Suter T, Frei K, Brockhaus M, Koedel U, Fontana A (2000) Antibodies to the junctional adhesion molecule cause disruption of endothelial cells and do not prevent leukocyte influx into the meninges after viral or bacterial infection. J Infect Dis 182:978-982
60. Li X, Stankovic M, Lee BP, Aurrand-Lions M, Hahn CN, Lu Y, Imhof BA, Vadas MA, Gamble JR (2009) JAM-C induces endothelial cell permeability through its association and regulation of {beta}3 integrins. Arterioscler Thromb Vasc Biol 29:1200-1206
61. Liang TW, DeMarco RA, Mrsny RJ, Gurney A, Gray A, Hooley J, Aaron HL, Huang A, Klassen T, Tumas DB, Fong S (2000) Characterization of huJAM: evidence for involvement in cell-cell contact and tight junction regulation. Am J Physiol Cell Physiol 279:C1733-C1743
62. Liang TW, Chiu HH, Gurney A, Sidle A, Tumas DB, Schow P, Foster J, Klassen T, Dennis K, DeMarco RA, Pham T, Frantz G, Fong S (2002) Vascular endothelial-junctional adhesion molecule (VE-JAM)/JAM 2 interacts with T, NK, and dendritic cells through JAM 3. J Immunol 168:1618-1626
63. Liu Y, Nusrat A, Schnell FJ, Reaves TA, Walsh S, Pochet M, Parkos CA (2000) Human junction adhesion molecule regulates tight junction resealing in epithelia. J Cell Sci 113(Pt 13):2363-2374
64. Ludwig RJ, Zollner TM, Santoso S, Hardt K, Gille J, Baatz H, Johann PS, Pfeffer J, Radeke HH, Schon MP, Kaufmann R, Boehncke WH, Podda M (2005) Junctional adhesion molecules (JAM)-B and -C contribute to leukocyte extravasation to the skin and mediate cutaneous inflammation. J Investig Dermatol 125:969-976
65. Ludwig RJ, Hardt K, Hatting M, Bistrian R, Diehl S, Radeke HH, Podda M, Schon MP, Kaufmann R, Henschler R, Pfeilschifter JM, Santoso S, Boehncke WH (2009) Junctional adhesion molecule (JAM)-B supports lymphocyte rolling and adhesion through interaction with alpha4beta1 integrin. Immunology 128:196-205
66. Luissint AC, Lutz PG, Calderwood DA, Couraud PO, Bourdoulous S (2008) JAM-L-mediated leukocyte adhesion to endothelial cells is regulated in cis by alpha4beta1 integrin activation. J Cell Biol 183:1159-1173
67. Mamdouh Z, Mikhailov A, Muller WA (2009) Transcellular migration of leukocytes is mediated by the endothelial lateral border recycling compartment. J Exp Med 206:2795-2808
68. Mandell KJ, Parkos CA (2005) The JAM family of proteins. Adv Drug Deliv Rev 57:857-867
69. Mandell KJ, Babbin BA, Nusrat A, Parkos CA (2005) Junctional adhesion molecule 1 regulates epithelial cell morphology through effects on beta1 integrins and Rap1 activity. J Biol Chem 280:11665-11674
70. Mandell KJ, Holley GP, Parkos CA, Edelhauser HF (2006) Antibody blockade of junctional adhesion molecule-A in rabbit corneal endothelial tight junctions produces corneal swelling. Investig Ophthalmol Vis Sci 47:2408-2416
71. Mandicourt G, Iden S, Ebnet K, Aurrand-Lions M, Imhof BA (2007) JAM-C regulates tight junctions and integrin-mediated cell adhesion and migration. J Biol Chem 282:1830-1837
72. Mapoles JE, Krah DL, Crowell RL (1985) Purification of a HeLa cell receptor protein for group B coxsackieviruses. J Virol 55:560-566
73. Martinez-Estrada OM, Villa A, Breviario F, Orsenigo F, Dejana E, Bazzoni G (2001) Association of junctional adhesion molecule with calcium/calmodulin- dependent serine protein kinase (CASK/LIN-2) in human epithelial caco-2 cells. J Biol Chem 276:9291-9296
74. Martin-Padura I, Lostaglio S, Schneemann M, Williams L, Romano M, Fruscella P, Panzeri C, Stoppacciaro A, Ruco L, Villa A, Simmons D, Dejana E (1998) Junctional adhesion molecule, a novel member of the immunoglobulin superfamily that distributes at intercellular junctions and modulates monocyte transmigration. J Cell Biol 142:117-127
75. Mirza M, Hreinsson J, Strand ML, Hovatta O, Soder O, Philipson L, Pettersson RF, Sollerbrant K (2006) Coxsackievirus and adenovirus receptor (CAR) is expressed in male germ cells and forms a complex with the differentiation factor JAM-C in mouse testis. Exp Cell Res 312:817-830
76. Mitic LL, Anderson JM (1998) Molecular architecture of tight junctions. Annu Rev Physiol 60:121-142
77. Mochida GH, Ganesh VS, Felie JM, Gleason D, Hill RS, Clapham KR, Rakiec D, Tan WH, Akawi N, Al-Saffar M, Partlow JN, Tinschert S, Barkovich AJ, Ali B, Al-Gazali L, Walsh CA (2010) A homozygous mutation in the tight-junction protein JAM3 causes hemorrhagic destruction of the brain, subependymal calcification, and congenital cataracts. Am J Hum Genet 87:882-889
78. Monteiro AC, Sumagin R, Rankin CR, Leoni G, Mina MJ, Reiter DM, Stehle T, Dermody TS, Schaefer SA, Hall RA, Nusrat A, Parkos CA (2013) JAM-A associates with ZO-2, afadin, and PDZ-GEF1 to activate Rap2c and regulate epithelial barrier function. Mol Biol Cell 24:2849-2860
79. Moog-Lutz C, Cave-Riant F, Guibal FC, Breau MA, Di Gioia Y, Couraud PO, Cayre YE, Bourdoulous S, Lutz PG (2003) JAML, a novel protein with characteristics of a junctional adhesion molecule, is induced during differentiation of myeloid leukemia cells. Blood 102:3371-3378
80. Muller WA (2003) Leukocyte-endothelial-cell interactions in leukocyte transmigration and the inflammatory response. Trends Immunol 24:327-334
81. Muller WA (2011) Mechanisms of leukocyte transendothelial migration. Annu Rev Pathol 6:323-344
82. Murakami M, Francavilla C, Torselli I, Corada M, Maddaluno L, Sica A, Matteoli G, Iliev ID, Mantovani A, Rescigno M, Cavallaro U, Dejana E (2010) Inactivation of junctional adhesion molecule-A enhances antitumoral immune response by promoting dendritic cell and T lymphocyte infiltration. Cancer Res 70:1759-1765
83. Nagai-Tamai Y, Mizuno K, Hirose T, Suzuki A, Ohno S (2002) Regulated protein-protein interaction between aPKC and PAR-3 plays an essential role in the polarization of epithelial cells. Genes Cells 7:1161-1171
84. Nagamatsu G, Ohmura M, Mizukami T, Hamaguchi I, Hirabayashi S, Yoshida S, Hata Y, Suda T, Ohbo K (2006) A CTX family cell adhesion molecule, JAM4, is expressed in stem cell and progenitor cell populations of both male germ cell and hematopoietic cell lineages. Mol Cell Biol 26:8498-8506
85. Nagy Z, Peters H, Huttner I (1984) Fracture faces of cell junctions in cerebral endothelium during normal and hyperosmotic conditions. Lab Investig 50:313-322
86. Naik MU, Mousa SA, Parkos CA, Naik UP (2003) Signaling through JAM-1 and alphavbeta3 is required for the angiogenic action of bFGF: dissociation of the JAM-1 and alphavbeta3 complex. Blood 102:2108-2114
87. Nasdala I, Wolburg-Buchholz K, Wolburg H, Kuhn A, Ebnet K, Brachtendorf G, Samulowitz U, Kuster B, Engelhardt B, Vestweber D, Butz S (2002) A transmembrane tight junction protein selectively expressed on endothelial cells and platelets. J Biol Chem 277:16294-16303
88. Noutsias M, Fechner H, de Jonge H, Wang X, Dekkers D, Houtsmuller AB, Pauschinger M, Bergelson J, Warraich R, Yacoub M, Hetzer R, Lamers J, Schultheiss HP, Poller W (2001) Human coxsackie-adenovirus receptor is colocalized with integrins alpha(v)beta(3) and alpha(v)beta(5) on the cardiomyocyte sarcolemma and upregulated in dilated cardiomyopathy: implications for cardiotropic viral infections. Circulation 104:275-280
89. Orlova VV, Economopoulou M, Lupu F, Santoso S, Chavakis T (2006) Junctional adhesion molecule-C regulates vascular endothelial permeability by modulating VE-cadherin-mediated cell-cell contacts. J Exp Med 203:2703-2714
90. Ostermann G, Weber KS, Zernecke A, Schroder A, Weber C (2002) JAM-1 is a ligand of the beta(2) integrin LFA-1 involved in transendothelial migration of leukocytes. Nat Immunol 3:151-158
91. Ozaki H, Ishii K, Horiuchi H, Arai H, Kawamoto T, Okawa K, Iwamatsu A, Kita T (1999) Cutting edge: combined treatment of TNF-alpha and IFN-gamma causes redistribution of junctional adhesion molecule in human endothelial cells. J Immunol 163:553-557
92. Padden M, Leech S, Craig B, Kirk J, Brankin B, McQuaid S (2007) Differences in expression of junctional adhesion molecule-A and beta-catenin in multiple sclerosis brain tissue: increasing evidence for the role of tight junction pathology. Acta Neuropathol 113:177-186
93. Palmeri D, van Zante A, Huang CC, Hemmerich S, Rosen SD (2000) Vascular endothelial junction-associated molecule, a novel member of the immunoglobulin superfamily, is localized to intercellular boundaries of endothelial cells. J Biol Chem 275:19139-19145
94. Prota AE, Campbell JA, Schelling P, Forrest JC, Watson MJ, Peters TR, Aurrand-Lions M, Imhof BA, Dermody TS, Stehle T (2003) Crystal structure of human junctional adhesion molecule 1: implications for reovirus binding. Proc Natl Acad Sci USA 100:5366-5371
95. Rabquer BJ, Pakozdi A, Michel JE, Gujar BS, Haines GK 3rd, Imhof BA, Koch AE (2008) Junctional adhesion molecule C mediates leukocyte adhesion to rheumatoid arthritis synovium. Arthritis Rheum 58:3020-3029
96. Rabquer BJ, Amin MA, Teegala N, Shaheen MK, Tsou PS, Ruth JH, Lesch CA, Imhof BA, Koch AE (2010) Junctional adhesion molecule-C is a soluble mediator of angiogenesis. J Immunol 185:1777-1785
97. Reese TS, Karnovsky MJ (1967) Fine structural localization of a blood-brain barrier to exogenous peroxidase. J Cell Biol 34:207-217
98. Rubin LL, Hall DE, Porter S, Barbu K, Cannon C, Horner HC, Janatpour M, Liaw CW, Manning K, Morales J et al (1991) A cell culture model of the blood-brain barrier. J Cell Biol 115:1725-1735
99. Saitou M, Furuse M, Sasaki H, Schulzke JD, Fromm M, Takano H, Noda T, Tsukita S (2000) Complex phenotype of mice lacking occludin, a component of tight junction strands. Mol Biol Cell 11:4131-4142
100. Salifu MO, Kolff Q, Murty P, Haria DM, Zimpa M, Shakeel M, Lee H, Kornecki E, Babinska A (2007) Relationship between the soluble F11 receptor and markers of inflammation in hemodialysis patients. J Investig Med 55:115-119
101. Santoso S, Sachs UJ, Kroll H, Linder M, Ruf A, Preissner KT, Chavakis T (2002) The junctional adhesion molecule 3 (JAM-3) on human platelets is a counterreceptor for the leukocyte integrin Mac-1. J Exp Med 196:679-691
102. Scheiermann C, Colom B, Meda P, Patel NS, Voisin MB, Marrelli A, Woodfin A, Pitzalis C, Thiemermann C, Aurrand-Lions M, Imhof BA, Nourshargh S (2009) Junctional adhesion molecule-C mediates leukocyte infiltration in response to ischemia reperfusion injury. Arterioscler Thromb Vasc Biol 29:1509-1515
103. Schmitt MM, Megens RT, Zernecke A, Bidzhekov K, van den Akker NM, Rademakers T, van Zandvoort MA, Hackeng TM, Koenen RR, Weber C (2013) Endothelial JAM-A guides monocytes into flow-dependent predilection sites of atherosclerosis. Circulation 24(4):217-222
104. Shaw SK, Perkins BN, Lim YC, Liu Y, Nusrat A, Schnell FJ, Parkos CA, Luscinskas FW (2001) Reduced expression of junctional adhesion molecule and platelet/endothelial cell adhesion molecule-1 (CD31) at human vascular endothelial junctions by cytokines tumor necrosis factor-alpha plus interferon-gamma Does not reduce leukocyte transmigration under flow. Am J Pathol 159:2281-2291
105. Shaw SK, Ma S, Kim MB, Rao RM, Hartman CU, Froio RM, Yang L, Jones T, Liu Y, Nusrat A, Parkos CA, Luscinskas FW (2004) Coordinated redistribution of leukocyte LFA-1 and endothelial cell ICAM-1 accompany neutrophil transmigration. J Exp Med 200:1571-1580
106. Sircar M, Bradfield PF, Aurrand-Lions M, Fish RJ, Alcaide P, Yang L, Newton G, Lamont D, Sehrawat S, Mayadas T, Liang TW, Parkos CA, Imhof BA, Luscinskas FW (2007) Neutrophil transmigration under shear flow conditions in vitro is junctional adhesion molecule-C independent. J Immunol 178:5879-5887
107. Sobocka MB, Sobocki T, Banerjee P, Weiss C, Rushbrook JI, Norin AJ, Hartwig J, Salifu MO, Markell MS, Babinska A, Ehrlich YH, Kornecki E (2000) Cloning of the human platelet F11 receptor: a cell adhesion molecule member of the immunoglobulin superfamily involved in platelet aggregation. Blood 95:2600-2609
108. Sollerbrant K, Raschperger E, Mirza M, Engstrom U, Philipson L, Ljungdahl PO, Pettersson RF (2003) The Coxsackievirus and adenovirus receptor (CAR) forms a complex with the PDZ domain-containing protein ligand-of-numb protein-X (LNX). J Biol Chem 278:7439-7444
109. Stalker TJ, Wu J, Morgans A, Traxler EA, Wang L, Chatterjee MS, Lee D, Quertermous T, Hall RA, Hammer DA, Diamond SL, Brass LF (2009) Endothelial cell specific adhesion molecule (ESAM) localizes to platelet-platelet contacts and regulates thrombus formation in vivo. J Thromb Haemost 7:1886-1896
110. Suzuki A, Ohno S (2006) The PAR-aPKC system: lessons in polarity. J Cell Sci 119:979-987
111. Suzuki A, Yamanaka T, Hirose T, Manabe N, Mizuno K, Shimizu M, Akimoto K, Izumi Y, Ohnishi T, Ohno S (2001) Atypical protein kinase C is involved in the evolutionarily conserved par protein complex and plays a critical role in establishing epithelia-specific junctional structures. J Cell Biol 152:1183-1196
112. Suzuki A, Ishiyama C, Hashiba K, Shimizu M, Ebnet K, Ohno S (2002) aPKC kinase activity is required for the asymmetric differentiation of the premature junctional complex during epithelial cell polarization. J Cell Sci 115:3565-3573
113. Tao-Cheng JH, Nagy Z, Brightman MW (1987) Tight junctions of brain endothelium in vitro are enhanced by astroglia. J Neurosci 7:3293-3299
114. Tomko RP, Johansson CB, Totrov M, Abagyan R, Frisen J, Philipson L (2000) Expression of the adenovirus receptor and its interaction with the fiber knob. Exp Cell Res 255:47-55
115. Tsukita S, Furuse M, Itoh M (2001) Multifunctional strands in tight junctions. Nat Rev Mol Cell Biol 2:285-293
116. Van Itallie CM, Anderson JM (2006) Claudins and epithelial paracellular transport. Annu Rev Physiol 68:403-429
117. Vorbrodt AW, Dobrogowska DH (2004) Molecular anatomy of interendothelial junctions in human blood-brain barrier microvessels. Folia Histochem Cytobiol 42:67-75
118. Wegmann F, Ebnet K, Pasquier LD, Vestweber D, Butz S (2004) Endothelial adhesion molecule ESAM binds directly to the multidomain adaptor MAGI-1 and recruits it to cell contacts. Exp Cell Res 300:121-133
119. Wegmann F, Petri B, Khandoga AG, Moser C, Khandoga A, Volkery S, Li H, Nasdala I, Brandau O, Fassler R, Butz S, Krombach F, Vestweber D (2006) ESAM supports neutrophil extravasation, activation of Rho, and VEGF-induced vascular permeability. J Exp Med 203:1671-1677
120. Williams AF, Barclay AN (1988) The immunoglobulin superfamily-domains for cell surface recognition. Annu Rev Immunol 6:381-405
121. Williams DW, Calderon TM, Lopez L, Carvallo-Torres L, Gaskill PJ, Eugenin EA, Morgello S, Berman JW (2013) Mechanisms of HIV Entry into the CNS: increased sensitivity of HIV infected CD14(+)CD16(+) monocytes to CCL2 and key roles of CCR2, JAM-A, and ALCAM in diapedesis. PLoS ONE 8:e69270
122. Wolburg H, Lippoldt A (2002) Tight junctions of the blood-brain barrier: development, composition and regulation. Vasc Pharmacol 38:323-337
123. Wolburg H, Neuhaus J, Kniesel U, Krauss B, Schmid EM, Ocalan M, Farrell C, Risau W (1994) Modulation of tight junction structure in blood-brain barrier endothelial cells. Effects of tissue culture, second messengers and cocultured astrocytes. J Cell Sci 107(Pt 5):1347-1357
124. Wong AD, Ye M, Levy AF, Rothstein JD, Bergles DE, Searson PC (2013) The blood-brain barrier: an engineering perspective. Front Neuroenerg 6:7
125. Woodfin A, Reichel CA, Khandoga A, Corada M, Voisin MB, Scheiermann C, Haskard DO, Dejana E, Krombach F, Nourshargh S (2007) JAM-A mediates neutrophil transmigration in a stimulus-specific manner in vivo: evidence for sequential roles for JAM-A and PECAM-1 in neutrophil transmigration. Blood 110:1848-1856
126. Woodfin A, Voisin MB, Imhof BA, Dejana E, Engelhardt B, Nourshargh S (2009) Endothelial cell activation leads to neutrophil transmigration as supported by the sequential roles of ICAM-2, JAM-A, and PECAM-1. Blood 113:6246-6257
127. Woodfin A, Voisin MB, Beyrau M, Colom B, Caille D, Diapouli FM, Nash GB, Chavakis T, Albelda SM, Rainger GE, Meda P, Imhof BA, Nourshargh S (2011) The junctional adhesion molecule JAM-C regulates polarized transendothelial migration of neutrophils in vivo. Nat Immunol 12:761-769
128. Wyss L, Schafer J, Liebner S, Mittelbronn M, Deutsch U, Enzmann G, Adams RH, Aurrand-Lions M, Plate KH, Imhof BA, Engelhardt B (2012) Junctional adhesion molecule (JAM)-C deficient C57BL/6 mice develop a severe hydrocephalus. PLoS ONE 7:e45619
129. Yamanaka T, Horikoshi Y, Suzuki A, Sugiyama Y, Kitamura K, Maniwa R, Nagai Y, Yamashita A, Hirose T, Ishikawa H, Ohno S (2001) PAR-6 regulates aPKC activity in a novel way and mediates cell-cell contact-induced formation of the epithelial junctional complex. Genes Cells 6:721-731
130. Yeung D, Manias JL, Stewart DJ, Nag S (2008) Decreased junctional adhesion molecule-A expression during blood-brain barrier breakdown. Acta Neuropathol 115:635-642
131. Zen K, Liu Y, McCall IC, Wu T, Lee W, Babbin BA, Nusrat A, Parkos CA (2005) Neutrophil migration across tight junctions is mediated by adhesive interactions between epithelial coxsackie and adenovirus receptor and a junctional adhesion molecule-like protein on neutrophils. Mol Biol Cell 16:2694-2703