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Published in: Acta Neuropathologica 6/2008

01-06-2008 | Original Paper

Decreased junctional adhesion molecule-A expression during blood–brain barrier breakdown

Authors: Dennis Yeung, Janet L. Manias, Duncan J. Stewart, Sukriti Nag

Published in: Acta Neuropathologica | Issue 6/2008

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Abstract

Tight junctions between brain endothelial cells are one of the specialized structural components of the blood–brain barrier (BBB) to proteins. Research in the last decade has demonstrated that the integral membrane proteins of cerebral endothelial tight junctions are claudin, occludin, and junctional adhesion molecule (JAM). Altered expression of these tight junction proteins could cause BBB breakdown following brain injury leading to edema. In this study, expression of JAM-A, was analyzed by immunostaining and immunoblotting in the rat cortical cold injury model, a well-characterized in vivo model of BBB breakdown. Temporal and spatial expression of JAM-A was examined at 12 hours, days 2, 4, and 6 post-lesion in cold-injured and control rats. Control rats showed punctate JAM-A immunoreactivity at intervals along the circumference of the endothelial layer at tight junctions where JAM-A colocalized with occludin. A significant decrease in JAM-A expression was noted at the lesion site by immunoblotting at 12 h only. At this time period, lesion vessels showed loss of endothelial JAM-A immunostaining while day 2 onwards, there was recovery of endothelial JAM-A immunoreactivity. Dual labelling for JAM-A and fibronectin showed that only lesion vessels with BBB breakdown to fibronectin at 12 h also showed lack of endothelial JAM-A immunoreactivity supporting the evidence that JAM-A contributes to tight junction integrity.
Literature
1.
go back to reference Aurrand-Lions M, Johnson-Leger C, Wong C, Du PL, Imhof BA (2001) Heterogeneity of endothelial junctions is reflected by differential expression and specific subcellular localization of the three JAM family members. Blood 98:3699–3707PubMedCrossRef Aurrand-Lions M, Johnson-Leger C, Wong C, Du PL, Imhof BA (2001) Heterogeneity of endothelial junctions is reflected by differential expression and specific subcellular localization of the three JAM family members. Blood 98:3699–3707PubMedCrossRef
2.
go back to reference Ballabh P, Hu F, Kumarasiri M, Braun A, Nedergaard M (2005) Development of tight junction molecules in blood vessels of germinal matrix, cerebral cortex, and white matter. Pediatr Res 58:791–798PubMedCrossRef Ballabh P, Hu F, Kumarasiri M, Braun A, Nedergaard M (2005) Development of tight junction molecules in blood vessels of germinal matrix, cerebral cortex, and white matter. Pediatr Res 58:791–798PubMedCrossRef
3.
go back to reference 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 104:441–451PubMedCrossRef 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 104:441–451PubMedCrossRef
4.
go back to reference Bauer H-C, Traweger A, Bauer H (2004) Proteins of the tight junction in the blood–brain barrier. In: Sharma HS, Westman J (eds) Blood–spinal cord and brain barriers in health and disease. Elsevier, San Diego, pp 1–10CrossRef Bauer H-C, Traweger A, Bauer H (2004) Proteins of the tight junction in the blood–brain barrier. In: Sharma HS, Westman J (eds) Blood–spinal cord and brain barriers in health and disease. Elsevier, San Diego, pp 1–10CrossRef
5.
6.
go back to reference Bazzoni G, MartinezEstrada OM, Orsenigo F, Cordenonsi M, Citi S, Dejana E (2000) Interaction of junctional adhesion molecule with the tight junction components ZO-1, cingulin, and occludin. J Biol Chem 275:20520–20526PubMedCrossRef Bazzoni G, MartinezEstrada OM, Orsenigo F, Cordenonsi M, Citi S, Dejana E (2000) Interaction of junctional adhesion molecule with the tight junction components ZO-1, cingulin, and occludin. J Biol Chem 275:20520–20526PubMedCrossRef
7.
go back to reference Citi S, Sabanay H, Jakes R, Geiger B, Kendrick-Jones J (1988) Cingulin, a new peripheral component of tight junctions. Nature 333:272–276PubMedCrossRef Citi S, Sabanay H, Jakes R, Geiger B, Kendrick-Jones J (1988) Cingulin, a new peripheral component of tight junctions. Nature 333:272–276PubMedCrossRef
8.
go back to reference Dallasta LM, Pisarov LA, Esplen JE, Werley JV, Moses AV, Nelson JA, Achim CL (1999) Blood–brain barrier tight junction disruption in human immunodeficiency virus-1 encephalitis. Am J Pathol 155:1915–1927PubMed Dallasta LM, Pisarov LA, Esplen JE, Werley JV, Moses AV, Nelson JA, Achim CL (1999) Blood–brain barrier tight junction disruption in human immunodeficiency virus-1 encephalitis. Am J Pathol 155:1915–1927PubMed
9.
go back to reference 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 190:1351–1356PubMedCrossRef 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 190:1351–1356PubMedCrossRef
10.
go back to reference 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 275:27979–27988PubMed 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 275:27979–27988PubMed
11.
go back to reference 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 116:3879–3891PubMedCrossRef 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 116:3879–3891PubMedCrossRef
12.
go back to reference 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 273:29745–29753PubMedCrossRef 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 273:29745–29753PubMedCrossRef
13.
go back to reference Forrest JC, Campbell JA, Schelling P, Stehle T, Dermody TS (2003) Structure–function analysis of reovirus binding to junctional adhesion molecule 1. Implications for the mechanism of reovirus attachment. J Biol Chem 278:48434–48444PubMedCrossRef Forrest JC, Campbell JA, Schelling P, Stehle T, Dermody TS (2003) Structure–function analysis of reovirus binding to junctional adhesion molecule 1. Implications for the mechanism of reovirus attachment. J Biol Chem 278:48434–48444PubMedCrossRef
14.
go back to reference Furuse M, Fujita K, Hiiragi T, Fujimoto K, Tsukita S (1998) Claudin-1 and -2: novel integral membrane proteins localizing at tight junctions with no sequence similarity to occludin. J Cell Biol 141:1539–1550PubMedCrossRef Furuse M, Fujita K, Hiiragi T, Fujimoto K, Tsukita S (1998) Claudin-1 and -2: novel integral membrane proteins localizing at tight junctions with no sequence similarity to occludin. J Cell Biol 141:1539–1550PubMedCrossRef
15.
go back to reference Furuse M, Hirase T, Itoh M, Nagafuchi A, Yonemura S, Tsukita S, Tsukita S (1993) Occludin: a novel integral membrane protein localizing at tight junctions. J Cell Biol 123:1777–1788PubMedCrossRef Furuse M, Hirase T, Itoh M, Nagafuchi A, Yonemura S, Tsukita S, Tsukita S (1993) Occludin: a novel integral membrane protein localizing at tight junctions. J Cell Biol 123:1777–1788PubMedCrossRef
16.
go back to reference Gumbiner B, Lowenkopf T, Apatira D (1991) Identification of a 160-kDa polypeptide that binds to the tight junction protein ZO-1. Proc Natl Acad Sci USA 88:3460–3464PubMedCrossRef Gumbiner B, Lowenkopf T, Apatira D (1991) Identification of a 160-kDa polypeptide that binds to the tight junction protein ZO-1. Proc Natl Acad Sci USA 88:3460–3464PubMedCrossRef
17.
go back to reference 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 277:455–461PubMedCrossRef 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 277:455–461PubMedCrossRef
18.
go back to reference Haskins J, Gu L, Wittchen ES, Hibbard J, Stevenson BR (1998) ZO-3, a novel member of the MAGUK protein family found at the tight junction, interacts with ZO-1 and occludin. J Cell Biol 141:199–208PubMedCrossRef Haskins J, Gu L, Wittchen ES, Hibbard J, Stevenson BR (1998) ZO-3, a novel member of the MAGUK protein family found at the tight junction, interacts with ZO-1 and occludin. J Cell Biol 141:199–208PubMedCrossRef
19.
go back to reference Itoh M, Nagafuchi A, Moroi S, Tsukita S (1997) Involvement of ZO-1 in cadherin-based cell adhesion through its direct binding to alpha catenin and actin filaments. J Cell Biol 138:181–192PubMedCrossRef Itoh M, Nagafuchi A, Moroi S, Tsukita S (1997) Involvement of ZO-1 in cadherin-based cell adhesion through its direct binding to alpha catenin and actin filaments. J Cell Biol 138:181–192PubMedCrossRef
20.
go back to reference 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 154:491–497PubMedCrossRef 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 154:491–497PubMedCrossRef
21.
go back to reference Knerlich F, Schilling L, Gorlach C, Wahl M, Ehrenreich H, Siren AL (1999) Temporal profile of expression and cellular localization of inducible nitric oxide synthase, interleukin-1 beta and interleukin converting enzyme after cryogenic lesion of the rat parietal cortex. Mol Brain Res 68:73–87PubMedCrossRef Knerlich F, Schilling L, Gorlach C, Wahl M, Ehrenreich H, Siren AL (1999) Temporal profile of expression and cellular localization of inducible nitric oxide synthase, interleukin-1 beta and interleukin converting enzyme after cryogenic lesion of the rat parietal cortex. Mol Brain Res 68:73–87PubMedCrossRef
22.
go back to reference Kornecki E, Walkowiak B, Naik UP, Ehrlich YH (1990) Activation of human platelets by a stimulatory monoclonal antibody. J Biol Chem 265:10042–10048PubMed Kornecki E, Walkowiak B, Naik UP, Ehrlich YH (1990) Activation of human platelets by a stimulatory monoclonal antibody. J Biol Chem 265:10042–10048PubMed
23.
go back to reference 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 113:2363–2374PubMed 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 113:2363–2374PubMed
24.
go back to reference Lossinsky AS, Shivers RR (2004) Structural pathways for macromolecular and cellular transport across the blood–brain barrier during inflammatory conditions. Review. Histol Histopathol 19:535–564PubMed Lossinsky AS, Shivers RR (2004) Structural pathways for macromolecular and cellular transport across the blood–brain barrier during inflammatory conditions. Review. Histol Histopathol 19:535–564PubMed
25.
go back to reference Malergue F, Galland F, Martin F, Mansuelle P, Aurrand-Lions M, Naquet P (1998) A novel immunoglobulin superfamily junctional molecule expressed by antigen presenting cells, endothelial cells and platelets. Mol Immunol 35:1111–1119PubMedCrossRef Malergue F, Galland F, Martin F, Mansuelle P, Aurrand-Lions M, Naquet P (1998) A novel immunoglobulin superfamily junctional molecule expressed by antigen presenting cells, endothelial cells and platelets. Mol Immunol 35:1111–1119PubMedCrossRef
26.
go back to reference 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 142:117–127PubMedCrossRef 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 142:117–127PubMedCrossRef
27.
go back to reference 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 276:9291–9296PubMedCrossRef 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 276:9291–9296PubMedCrossRef
28.
go back to reference Morita K, Furuse M, Fujimoto K, Tsukita S (1999) Claudin multigene family encoding four-transmembrane domain protein components of tight junction strands. Proc Natl Acad Sci USA 96:511–516PubMedCrossRef Morita K, Furuse M, Fujimoto K, Tsukita S (1999) Claudin multigene family encoding four-transmembrane domain protein components of tight junction strands. Proc Natl Acad Sci USA 96:511–516PubMedCrossRef
29.
go back to reference Nag S (1996) Cold-injury of the cerebral cortex: immunolocalization of cellular proteins and blood–brain barrier permeability studies. J Neuropathol Exp Neurol 55:880–888PubMed Nag S (1996) Cold-injury of the cerebral cortex: immunolocalization of cellular proteins and blood–brain barrier permeability studies. J Neuropathol Exp Neurol 55:880–888PubMed
30.
go back to reference Nag S (2003) Immunohistochemical detection of endothelial proteins. Methods Mol Med 89:489–501PubMed Nag S (2003) Immunohistochemical detection of endothelial proteins. Methods Mol Med 89:489–501PubMed
31.
go back to reference Nag S (2003) Pathophysiology of blood–brain barrier breakdown. Methods Mol Med 89:97–119PubMed Nag S (2003) Pathophysiology of blood–brain barrier breakdown. Methods Mol Med 89:97–119PubMed
32.
go back to reference Nag S, Eskandarian MR, Davis J, Eubanks JH (2002) Differential expression of vascular endothelial growth factor-A (VEGF-A) and VEGF-B after brain injury. J Neuropathol Exp Neurol 61:778–788PubMed Nag S, Eskandarian MR, Davis J, Eubanks JH (2002) Differential expression of vascular endothelial growth factor-A (VEGF-A) and VEGF-B after brain injury. J Neuropathol Exp Neurol 61:778–788PubMed
33.
go back to reference Nag S, Picard P, Stewart DJ (2001) Expression of nitric oxide synthases and nitrotyrosine during blood–brain barrier breakdown and repair after cold injury. Lab Invest 81:41–49PubMed Nag S, Picard P, Stewart DJ (2001) Expression of nitric oxide synthases and nitrotyrosine during blood–brain barrier breakdown and repair after cold injury. Lab Invest 81:41–49PubMed
34.
go back to reference Nag S, Venugopalan R, Stewart DJ (2007) Increased caveolin-1 expression precedes decreased expression of occludin and claudin-5 during blood–brain barrier breakdown. Acta Neuropathol 114:459–469PubMedCrossRef Nag S, Venugopalan R, Stewart DJ (2007) Increased caveolin-1 expression precedes decreased expression of occludin and claudin-5 during blood–brain barrier breakdown. Acta Neuropathol 114:459–469PubMedCrossRef
35.
go back to reference 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 102:2108–2114PubMedCrossRef 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 102:2108–2114PubMedCrossRef
36.
go back to reference Naik UP, Naik MU, Eckfeld K, Martin-DeLeon P, Spychala J (2001) Characterization and chromosomal localization of JAM-1, a platelet receptor for a stimulatory monoclonal antibody. J Cell Sci 114:539–547PubMed Naik UP, Naik MU, Eckfeld K, Martin-DeLeon P, Spychala J (2001) Characterization and chromosomal localization of JAM-1, a platelet receptor for a stimulatory monoclonal antibody. J Cell Sci 114:539–547PubMed
37.
go back to reference Nourhaghighi N, Teichert-Kuliszewska K, Davis J, Stewart DJ, Nag S (2003) Altered expression of angiopoietins during blood–brain barrier breakdown and angiogenesis. Lab Invest 83:1211–1222PubMedCrossRef Nourhaghighi N, Teichert-Kuliszewska K, Davis J, Stewart DJ, Nag S (2003) Altered expression of angiopoietins during blood–brain barrier breakdown and angiogenesis. Lab Invest 83:1211–1222PubMedCrossRef
38.
go back to reference 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 3:151–158PubMedCrossRef 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 3:151–158PubMedCrossRef
39.
go back to reference Ozaki H, Ishii K, Arai H, Horiuchi H, Kawamoto T, Suzuki H, Kita T (2000) Junctional adhesion molecule (JAM) is phosphorylated by protein kinase C upon platelet activation. Biochem Biophys Res Commun 276:873–878PubMedCrossRef Ozaki H, Ishii K, Arai H, Horiuchi H, Kawamoto T, Suzuki H, Kita T (2000) Junctional adhesion molecule (JAM) is phosphorylated by protein kinase C upon platelet activation. Biochem Biophys Res Commun 276:873–878PubMedCrossRef
40.
go back to reference 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 163:553–557PubMed 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 163:553–557PubMed
41.
go back to reference 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 113:177–186PubMedCrossRef 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 113:177–186PubMedCrossRef
42.
go back to reference Plumb J, McQuaid S, Mirakhur M, Kirk J (2002) Abnormal endothelial tight junctions in active lesions and normal-appearing white matter in multiple sclerosis. Brain Pathol 12:154–169PubMedCrossRef Plumb J, McQuaid S, Mirakhur M, Kirk J (2002) Abnormal endothelial tight junctions in active lesions and normal-appearing white matter in multiple sclerosis. Brain Pathol 12:154–169PubMedCrossRef
43.
go back to reference 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 159:2281–2291PubMed 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 159:2281–2291PubMed
44.
go back to reference Stevenson BR, Siliciano JD, Mooseker MS, Goodenough DA (1986) Identification of ZO-1: a high molecular weight polypeptide associated with the tight junction (zonula occludens) in a variety of epithelia. J Cell Biol 103:755–766PubMedCrossRef Stevenson BR, Siliciano JD, Mooseker MS, Goodenough DA (1986) Identification of ZO-1: a high molecular weight polypeptide associated with the tight junction (zonula occludens) in a variety of epithelia. J Cell Biol 103:755–766PubMedCrossRef
45.
go back to reference Williams LA, Martin-Padura I, Dejana E, Hogg N, Simmons DL (1999) Identification and characterisation of human Junctional Adhesion Molecule (JAM). Mol Immunol 36(17):1175–1188PubMedCrossRef Williams LA, Martin-Padura I, Dejana E, Hogg N, Simmons DL (1999) Identification and characterisation of human Junctional Adhesion Molecule (JAM). Mol Immunol 36(17):1175–1188PubMedCrossRef
46.
go back to reference Wolburg H, Wolburg-Buchholz K, Kraus J, Rascher-Eggstein G, Liebner S, Hamm S, Duffner F, Grote EH, Risau W, Engelhardt B (2003) Localization of claudin-3 in tight junctions of the blood–brain barrier is selectively lost during experimental autoimmune encephalomyelitis and human glioblastoma multiforme. Acta Neuropathol 105(6):586–592PubMed Wolburg H, Wolburg-Buchholz K, Kraus J, Rascher-Eggstein G, Liebner S, Hamm S, Duffner F, Grote EH, Risau W, Engelhardt B (2003) Localization of claudin-3 in tight junctions of the blood–brain barrier is selectively lost during experimental autoimmune encephalomyelitis and human glioblastoma multiforme. Acta Neuropathol 105(6):586–592PubMed
47.
go back to reference Yamamoto T, Harada N, Kano K, Taya S, Canaani E, Matsuura Y, Mizoguchi A, Ide C, Kaibuchi K (1997) The Ras target AF-6 interacts with ZO-1 and serves as a peripheral component of tight junctions in epithelial cells. J Cell Biol 139(3):785–795PubMedCrossRef Yamamoto T, Harada N, Kano K, Taya S, Canaani E, Matsuura Y, Mizoguchi A, Ide C, Kaibuchi K (1997) The Ras target AF-6 interacts with ZO-1 and serves as a peripheral component of tight junctions in epithelial cells. J Cell Biol 139(3):785–795PubMedCrossRef
48.
go back to reference Zhong Y, Saitoh T, Minase T, Sawada N, Enomoto K, Mori M (1993) Monoclonal antibody 7H6 reacts with a novel tight junction-associated protein distinct from ZO-1, cingulin and ZO-2. J Cell Biol 120(2):477–483PubMedCrossRef Zhong Y, Saitoh T, Minase T, Sawada N, Enomoto K, Mori M (1993) Monoclonal antibody 7H6 reacts with a novel tight junction-associated protein distinct from ZO-1, cingulin and ZO-2. J Cell Biol 120(2):477–483PubMedCrossRef
Metadata
Title
Decreased junctional adhesion molecule-A expression during blood–brain barrier breakdown
Authors
Dennis Yeung
Janet L. Manias
Duncan J. Stewart
Sukriti Nag
Publication date
01-06-2008
Publisher
Springer-Verlag
Published in
Acta Neuropathologica / Issue 6/2008
Print ISSN: 0001-6322
Electronic ISSN: 1432-0533
DOI
https://doi.org/10.1007/s00401-008-0364-4

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