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© The Rockefeller University Press, 0021-9525/1999//1351 $5.00
The Journal of Cell Biology, Volume 147, Number 6, , 1999 1351-1363

Direct Binding of Three Tight Junction-Associated Maguks, Zo-1, Zo-2, and Zo-3, with the Cooh Termini of Claudins

^a Department of Cell Biology, Faculty of Medicine, Kyoto University, Sakyo-ku, Kyoto 606-8501, Japan
^b Department of Dermatology, Faculty of Medicine, Kyoto University, Sakyo-ku, Kyoto 606-8501, Japan
Department of Cell Biology, Faculty of Medicine, Kyoto University, Sakyo-ku, Kyoto 606-8501, Japan.81-75-753-466081-75-753-4372

htsukita{at}mfour.med.kyoto-u.ac.jp

ZO-1, ZO-2, and ZO-3, which contain three PDZ domains (PDZ1 to -3), are concentrated at tight junctions (TJs) in epithelial cells. TJ strands are mainly composed of two distinct types of four-transmembrane proteins, occludin, and claudins, between which occludin was reported to directly bind to ZO-1/ZO-2/ZO-3. However, in occludin-deficient intestinal epithelial cells, ZO-1/ZO-2/ZO-3 were still recruited to TJs. We then examined the possible interactions between ZO-1/ZO-2/ZO-3 and claudins. ZO-1, ZO-2, and ZO-3 bound to the COOH-terminal YV sequence of claudin-1 to -8 through their PDZ1 domains in vitro. Then, claudin-1 or -2 was transfected into L fibroblasts, which express ZO-1 but not ZO-2 or ZO-3. Claudin-1 and -2 were concentrated at cell–cell borders in an elaborate network pattern, to which endogenous ZO-1 was recruited. When ZO-2 or ZO-3 were further transfected, both were recruited to the claudin-based networks together with endogenous ZO-1. Detailed analyses showed that ZO-2 and ZO-3 are recruited to the claudin-based networks through PDZ2 (ZO-2 or ZO-3)/PDZ2 (endogenous ZO-1) and PDZ1 (ZO-2 or ZO-3)/COOH-terminal YV (claudins) interactions. In good agreement, PDZ1 and PDZ2 domains of ZO-1/ZO-2/ZO-3 were also recruited to claudin-based TJs, when introduced into cultured epithelial cells. The possible molecular architecture of TJ plaque structures is discussed.

Key Words: claudin • tight junction • ZO-1 • ZO-2 • ZO-3

© 1999 The Rockefeller University Press

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• Colegio, O. R., Itallie, C. V., Rahner, C., Anderson, J. M. (2003). Claudin extracellular domains determine paracellular charge selectivity and resistance but not tight junction fibril architecture. Am. J. Physiol. Cell Physiol. 284: C1346-C1354 [Abstract] [Full Text]  
• Yu, A. S. L., Enck, A. H., Lencer, W. I., Schneeberger, E. E. (2003). Claudin-8 Expression in Madin-Darby Canine Kidney Cells Augments the Paracellular Barrier to Cation Permeation. J. Biol. Chem. 278: 17350-17359 [Abstract] [Full Text]  
• Burns, A. R., Smith, C. W., Walker, D. C. (2003). Unique Structural Features That Influence Neutrophil Emigration Into the Lung. Physiol. Rev. 83: 309-336 [Abstract] [Full Text]  
• Sasaki, H., Matsui, C., Furuse, K., Mimori-Kiyosue, Y., Furuse, M., Tsukita, S. (2003). Dynamic behavior of paired claudin strands within apposing plasma membranes. Proc. Natl. Acad. Sci. USA 100: 3971-3976 [Abstract] [Full Text]  
• Lui, W.-Y., Mruk, D., Lee, W. M, Cheng, C. Y. (2003). Sertoli Cell Tight Junction Dynamics: Their Regulation During Spermatogenesis. Biol. Reprod. 68: 1087-1097 [Abstract] [Full Text]  
• Basuroy, S., Sheth, P., Kuppuswamy, D., Balasubramanian, S., Ray, R. M., Rao, R. K. (2003). Expression of Kinase-inactive c-Src Delays Oxidative Stress-induced Disassembly and Accelerates Calcium-mediated Reassembly of Tight Junctions in the Caco-2 Cell Monolayer. J. Biol. Chem. 278: 11916-11924 [Abstract] [Full Text]  
• Olsen, O., Bredt, D. S. (2003). Functional Analysis of the Nucleotide Binding Domain of Membrane-associated Guanylate Kinases. J. Biol. Chem. 278: 6873-6878 [Abstract] [Full Text]  
• Brown, R. C., Mark, K. S., Egleton, R. D., Huber, J. D., Burroughs, A. R., Davis, T. P. (2003). Protection against hypoxia-induced increase in blood-brain barrier permeability: role of tight junction proteins and NF{kappa}B. J. Cell Sci. 116: 693-700 [Abstract] [Full Text]  
• Takekuni, K., Ikeda, W., Fujito, T., Morimoto, K., Takeuchi, M., Monden, M., Takai, Y. (2003). Direct Binding of Cell Polarity Protein PAR-3 to Cell-Cell Adhesion Molecule Nectin at Neuroepithelial Cells of Developing Mouse. J. Biol. Chem. 278: 5497-5500 [Abstract] [Full Text]  
• Asada, M., Irie, K., Morimoto, K., Yamada, A., Ikeda, W., Takeuchi, M., Takai, Y. (2003). ADIP, a Novel Afadin- and alpha -Actinin-Binding Protein Localized at Cell-Cell Adherens Junctions. J. Biol. Chem. 278: 4103-4111 [Abstract] [Full Text]  
• Nielsen, P. A., Beahm, D. L., Giepmans, B. N. G., Baruch, A., Hall, J. E., Kumar, N. M. (2002). Molecular Cloning, Functional Expression, and Tissue Distribution of a Novel Human Gap Junction-forming Protein, Connexin-31.9. INTERACTION WITH ZONA OCCLUDENS PROTEIN-1. J. Biol. Chem. 277: 38272-38283 [Abstract] [Full Text]  
• Cheng, C. Y., Mruk, D. D. (2002). Cell Junction Dynamics in the Testis: Sertoli-Germ Cell Interactions and Male Contraceptive Development. Physiol. Rev. 82: 825-874 [Abstract] [Full Text]  
• 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 [Abstract] [Full Text]  
• Nunbhakdi-Craig, V., Machleidt, T., Ogris, E., Bellotto, D., White, C. L. III, Sontag, E. (2002). Protein phosphatase 2A associates with and regulates atypical PKC and the epithelial tight junction complex. JCB 158: 967-978 [Abstract] [Full Text]  

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