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MBC in Press, published online ahead of print March 8, 2006
Mol. Biol. Cell 10.1091/mbc.E05-09-0826

A more recent version of this article appeared on May 1, 2006
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Submitted on September 2, 2005
Revised on February 21, 2006
Accepted on February 27, 2006

JRAB/MICAL-L2 Is a Junctional Rab13-binding Protein Mediating the Endocytic Recycling of Occludin

Tomoya Terai,*{dagger} Noriyuki Nishimura,* Ikuno Kanda,* Natsuo Yasui,{dagger} and Takuya Sasaki*

Departments of *Biochemistry and {dagger}Orthopedics, Institute of Health Biosciences, University of Tokushima Graduate School, Tokushima 770-8503, Japan

Monitoring Editor: Asma Nusrat

The dynamic turnover of tight junctions (TJs) is essential for epithelial-mesenchymal transitions and/or mesenchymal-epithelial transitions during epithelial morphogenesis. We previously demonstrated that Rab13 specifically mediates the endocytic recycling of occludin. Here we identified MICAL-L2 (molecule interacting with CasL-like 2) as a novel Rab13-binding protein. Immunoprecipitation and immunofluorescence microscopy showed that MICAL-L2 specifically bound to the GTP-bound form of Rab13 via its C-terminus, which contained a coiled-coil domain, and localized at TJs in epithelial MTD-1A cells. Recycling assay demonstrated that a MICAL-L2 mutant lacking the Rab13-binding domain (MICAL-L2-N) specifically inhibited the endocytic recycling of occludin, but not transferrin receptor. Ca2+-switch assay further revealed that MICAL-L2-N as well as Rab13 Q67L inhibited the recruitment of occludin to the plasma membrane, the development of transepithelial electrical resistance, and the formation of a paracellular diffusion barrier. MICAL-L2 was displaced from TJs upon actin depolymerization and was distributed along radiating actin cables and stress fibers in Ca2+-depleted MTD-1A and fibroblastic NIH3T3 cells, respectively. These results suggest that MICAL-L2 mediates the endocytic recycling of occludin and the formation of functional TJs by linking Rab13 to actin cytoskeleton. We rename MICAL-L2 as JRAB (junctional Rab13-binding protein).

Address correspondence to: Takuya Sasaki (sasaki{at}basic.med.tokushima-u.ac.jp)




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