Junctional Adhesion Molecule, a Novel Member of the Immunoglobulin Superfamily That Distributes at Intercellular Junctions and Modulates Monocyte Transmigration

doi:10.1083/jcb.142.1.117

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© The Rockefeller University Press, 0021-9525/1998//117 $5.00
The Journal of Cell Biology, Volume 142, Number 1, , 1998 117-127

Articles

Junctional Adhesion Molecule, a Novel Member of the Immunoglobulin Superfamily That Distributes at Intercellular Junctions and Modulates Monocyte Transmigration

Inés Martìn-Padura^*, Susan Lostaglio^*, Markus Schneemann, Lisa Williams, Maria Romano^*, Paolo Fruscella^*, Carla Panzeri, Antonella Stoppacciaro^||, Luigi Ruco^||, Antonello Villa, David Simmons, and Elisabetta Dejana^*

^* Istituto di Ricerche Farmacologiche Mario Negri, 20157 Milano, Italy; Institute of Molecular Medicine, University of Oxford, John Radcliffe Hospital, Headington, Oxford, OX3 9DU, United Kingdom; Dipartimento di Farmacologia, Universita degli Studi di Milano, and DIBIT, Milano, Italy 20129; and ^|| Universita' degli Studi La Sapienza, Dipartimento di Medicina Sperimentale e Patologia, 00161 Roma, Italy

Tight junctions are the most apical components of endothelialand epithelial intercellular cleft. In the endothelium thesestructures play an important role in the control of paracellularpermeability to circulating cells and solutes. The only knownintegral membrane protein localized at sites of membrane–membraneinteraction of tight junctions is occludin, which is linkedinside the cells to a complex network of cytoskeletal and signalingproteins. We report here the identification of a novel protein(junctional adhesion molecule [JAM]) that is selectively concentratedat intercellular junctions of endothelial and epithelial cellsof different origins. Confocal and immunoelectron microscopyshows that JAM codistributes with tight junction componentsat the apical region of the intercellular cleft. A cDNA cloneencoding JAM defines a novel immunoglobulin gene superfamilymember that consists of two V-type Ig domains. An mAb directedto JAM (BV11) was found to inhibit spontaneous and chemokine-inducedmonocyte transmigration through an endothelial cell monolayerin vitro. Systemic treatment of mice with BV11 mAb blockedmonocyte infiltration upon chemokine administration in subcutaneousair pouches. Thus, JAM is a new component of endothelial andepithelial junctions that play a role in regulating monocytetransmigration.

Key Words: endothelium • epithelium • monocyte • tight junctions • inflammation

Abbreviations used in this paper: AJ, adherens junctions; EC, endothelial cells; IgSF, immunoglobulin superfamily; JAM, junctional adhesion molecule; LPS, lipopolysaccaride; MCP, monocyte chemotactic protein; PECAM, platelet endothelial cell adhesion molecule; TJ, tight junctions; VE, vascular endothelial; ZO, zonula occludens.

Address all correspondence to Inés Martìn-Padura,Istituto di Ricerche Farmacologiche Mario Negri, Via Eritrea62, 20157 Milano, Italy. Tel.: 39-2-39014477; Fax: 39-2-3546277;E-mail: ines{at}irfmn.mnegri.it

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Khandoga, A., Kessler, J. S., Meissner, H., Hanschen, M., Corada, M., Motoike, T., Enders, G., Dejana, E., Krombach, F. (2005). Junctional adhesion molecule-A deficiency increases hepatic ischemia-reperfusion injury despite reduction of neutrophil transendothelial migration. Blood 106: 725-733 [Abstract] [Full Text]
Campbell, J. A., Schelling, P., Wetzel, J. D., Johnson, E. M., Forrest, J. C., Wilson, G. A. R., Aurrand-Lions, M., Imhof, B. A., Stehle, T., Dermody, T. S. (2005). Junctional Adhesion Molecule A Serves as a Receptor for Prototype and Field-Isolate Strains of Mammalian Reovirus. J. Virol. 79: 7967-7978 [Abstract] [Full Text]
Hawkins, B. T., Davis, T. P. (2005). The Blood-Brain Barrier/Neurovascular Unit in Health and Disease. Pharmacol. Rev. 57: 173-185 [Abstract] [Full Text]
Martinez-Estrada, O. M., Manzi, L., Tonetti, P., Dejana, E., Bazzoni, G. (2005). Opposite effects of tumor necrosis factor and soluble fibronectin on junctional adhesion molecule-A in endothelial cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 288: L1081-L1088 [Abstract] [Full Text]
Zen, K., Liu, Y., McCall, I. C., Wu, T., Lee, W., Babbin, B. A., Nusrat, A., Parkos, C. A. (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 [Abstract] [Full Text]
Aurrand-Lions, M., Lamagna, C., Dangerfield, J. P., Wang, S., Herrera, P., Nourshargh, S., Imhof, B. A. (2005). Junctional Adhesion Molecule-C Regulates the Early Influx of Leukocytes into Tissues during Inflammation. J. Immunol. 174: 6406-6415 [Abstract] [Full Text]
Miyamoto, T., Morita, K., Takemoto, D., Takeuchi, K., Kitano, Y., Miyakawa, T., Nakayama, K., Okamura, Y., Sasaki, H., Miyachi, Y., Furuse, M., Tsukita, S. (2005). Tight junctions in Schwann cells of peripheral myelinated axons: a lesson from claudin-19-deficient mice. JCB 169: 527-538 [Abstract] [Full Text]
Ostermann, G., Fraemohs, L., Baltus, T., Schober, A., Lietz, M., Zernecke, A., Liehn, E. A., Weber, C. (2005). Involvement of JAM-A in Mononuclear Cell Recruitment on Inflamed or Atherosclerotic Endothelium: Inhibition by Soluble JAM-A. Arterioscler. Thromb. Vasc. Bio. 25: 729-735 [Abstract] [Full Text]
Mandell, K. J., Babbin, B. A., Nusrat, A., Parkos, C. A. (2005). Junctional Adhesion Molecule 1 Regulates Epithelial Cell Morphology through Effects on {beta}1 Integrins and Rap1 Activity. J. Biol. Chem. 280: 11665-11674 [Abstract] [Full Text]
Watts, G. M., Beurskens, F. J. M., Martin-Padura, I., Ballantyne, C. M., Klickstein, L. B., Brenner, M. B., Lee, D. M. (2005). Manifestations of Inflammatory Arthritis Are Critically Dependent on LFA-1. J. Immunol. 174: 3668-3675 [Abstract] [Full Text]
Yun, P. L. W., Decarlo, A. A., Chapple, C. C., Hunter, N. (2005). Functional Implication of the Hydrolysis of Platelet Endothelial Cell Adhesion Molecule 1 (CD31) by Gingipains of Porphyromonas gingivalis for the Pathology of Periodontal Disease. Infect. Immun. 73: 1386-1398 [Abstract] [Full Text]