J. Cell Biol., Volume 140, Number 3, February 9, 1998 647-657

Rho-Kinase Phosphorylates COOH-terminal Threonines of Ezrin/Radixin/Moesin (ERM) Proteins and Regulates Their Head-to-Tail Association

Takeshi Matsui,^* Masato Maeda,^* Yoshinori Doi,^* Shigenobu Yonemura,^* Mutsuki Amano,^§ Kozo Kaibuchi,^§ Sachiko Tsukita,^* and Shoichiro Tsukita^*

^* Department of Cell Biology,  First Department of Surgery, Faculty of Medicine, Kyoto University, Sakyo-ku, Kyoto 606, Japan; ^§ Division of Signal Transduction, Nara Institute of Science and Technology, Nara 630-01, Japan; and  College of Medical Technology, Kyoto University, Sakyo-ku, Kyoto 606, Japan

The ezrin/radixin/moesin (ERM) proteins are involved in actin filament/plasma membrane interaction that is regulated by Rho. We examined whether ERM proteins are directly phosphorylated by Rho- associated kinase (Rho-kinase), a direct target of Rho. Recombinant full-length and COOH-terminal half radixin were incubated with constitutively active catalytic domain of Rho-kinase, and ~30 and ~100% of these molecules, respectively, were phosphorylated mainly at the COOH-terminal threonine (T564). Next, to detect Rho-kinase-dependent phosphorylation of ERM proteins in vivo, we raised a mAb that recognized the T564-phosphorylated radixin as well as ezrin and moesin phosphorylated at the corresponding threonine residue (T567 and T558, respectively). Immunoblotting of serum-starved Swiss 3T3 cells with this mAb revealed that after LPA stimulation ERM proteins were rapidly phosphorylated at T567 (ezrin), T564 (radixin), and T558 (moesin) in a Rho-dependent manner and then dephosphorylated within 2 min. Furthermore, the T564 phosphorylation of recombinant COOH-terminal half radixin did not affect its ability to bind to actin filaments in vitro but significantly suppressed its direct interaction with the NH₂-terminal half of radixin. These observations indicate that the Rho-kinase-dependent phosphorylation interferes with the intramolecular and/ or intermolecular head-to-tail association of ERM proteins, which is an important mechanism of regulation of their activity as actin filament/plasma membrane cross-linkers.

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• Coscoy, S., Waharte, F., Gautreau, A., Martin, M., Louvard, D., Mangeat, P., Arpin, M., Amblard, F. (2002). Molecular analysis of microscopic ezrin dynamics by two-photon FRAP. Proc. Natl. Acad. Sci. USA 99: 12813-12818 [Abstract] [Full Text]  
• Chen, B.-H., Tzen, J. T. C., Bresnick, A. R., Chen, H.-C. (2002). Roles of Rho-associated Kinase and Myosin Light Chain Kinase in Morphological and Migratory Defects of Focal Adhesion Kinase-null Cells. J. Biol. Chem. 277: 33857-33863 [Abstract] [Full Text]  
• Barreiro, O., Yanez-Mo, M., Serrador, J. M., Montoya, M. C., Vicente-Manzanares, M., Tejedor, R., Furthmayr, H., Sanchez-Madrid, F. (2002). Dynamic interaction of VCAM-1 and ICAM-1 with moesin and ezrin in a novel endothelial docking structure for adherent leukocytes. J. Cell Biol. 157: 1233-1245 [Abstract] [Full Text]  
• Yonemura, S., Matsui, T., Tsukita, S., Tsukita, S. (2002). Rho-dependent and -independent activation mechanisms of ezrin/radixin/moesin proteins: an essential role for polyphosphoinositides in vivo. J. Cell Sci. 115: 2569-2580 [Abstract] [Full Text]  
• Blindt, R., Zeiffer, U., Krott, N., Filzmaier, K., Voss, M., Hanrath, P., vom Dahl, J., Bosserhoff, A.-K. (2002). Upregulation of the cytoskeletal-associated protein Moesin in the neointima of coronary arteries after balloon angioplasty: a new marker of smooth muscle cell migration?. Cardiovasc Res 54: 630-639 [Abstract] [Full Text]  
• Burgstaller, G., Kranewitter, W. J., Gimona, M. (2002). The molecular basis for the autoregulation of calponin by isoform-specific C-terminal tail sequences. J. Cell Sci. 115: 2021-2029 [Abstract] [Full Text]  
• Khan, N. A., Wang, Y., Kim, K. J., Chung, J. W., Wass, C. A., Kim, K. S. (2002). Cytotoxic Necrotizing Factor-1 Contributes to Escherichia coli K1 Invasion of the Central Nervous System. J. Biol. Chem. 277: 15607-15612 [Abstract] [Full Text]  
• Jeon, S., Kim, S., Park, J.-B., Suh, P.-G., Kim, Y. S., Bae, C.-D., Park, J. (2002). RhoA and Rho Kinase-dependent Phosphorylation of Moesin at Thr-558 in Hippocampal Neuronal Cells by Glutamate. J. Biol. Chem. 277: 16576-16584 [Abstract] [Full Text]  

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