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© The Rockefeller University Press, 0021-9525/1998//1625 $5.00
The Journal of Cell Biology, Volume 141, Number 7, , 1998 1625-1636

Molecular Dissection of the Rho-associated Protein Kinase (p160ROCK)-regulated Neurite Remodeling in Neuroblastoma N1E-115 Cells

Masaya Hirose^*, Toshimasa Ishizaki^*, Naoki Watanabe^*, Masayoshi Uehata, Onno Kranenburg, Wouter H. Moolenaar, Fumio Matsumura^||, Midori Maekawa^*, Haruhiko Bito^*, and Shuh Narumiya^*

^* Department of Pharmacology, Kyoto University Faculty of Medicine, Sakyo, Kyoto 606-8315, Japan; Discovery Research, Yoshitomi Pharmaceutical Industries, Iruma, Saitama 358-0026, Japan; Division of Cellular Biochemistry, The Netherlands Cancer Institute, 1066 CX, Amsterdam, The Netherlands; and ^|| Department of Molecular Biology and Biochemistry, Rutgers University, Piscataway, New Jersey 08855-1059

A critical role for the small GTPase Rho and one of its targets, p160ROCK (a Rho-associated coiled coil-forming protein kinase), in neurite remodeling was examined in neuroblastoma N1E-115 cells. Using wild-type and a dominant-negative form of p160ROCK and a p160ROCK-specific inhibitor, Y-27632, we show here that p160ROCK activation is necessary and sufficient for the agonist-induced neurite retraction and cell rounding. The neurite retraction was accompanied by elevated phosphorylation of myosin light chain and the disassembly of the intermediate filaments and microtubules. Y-27632 blocked both neurite retraction and the elevation of myosin light chain phosphorylation in a similar concentration-dependent manner. On the other hand, suppression of p160ROCK activity by expression of a dominant-negative form of p160ROCK induced neurites in the presence of serum by inducing the reassembly of the intermediate filaments and microtubules. The neurite outgrowth by the p160ROCK inhibition was blocked by coexpression of dominant-negative forms of Cdc42 and Rac, indicating that p160ROCK constitutively and negatively regulates neurite formation at least in part by inhibiting activation of Cdc42 and Rac. The assembly of microtubules and intermediate filaments to form extended processes by inhibitors of the Rho–ROCK pathway was also observed in Swiss 3T3 cells. These results indicate that Rho/ROCK-dependent tonic inhibition of cell process extension is exerted via activation of the actomysin-based contractility, in conjunction with a suppression of assembly of intermediate filaments and microtubules in many cell types including, but not exclusive to, neuronal cells.

Abbreviations used in this paper: GFAP, glial fibrillary acidic protein; LPA, lysophosphatidic acid; MLC, myosin light chain; p160ROCK, p160 Rho-associated coiled coil-forming protein kinase.

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• Gohla, A., Schultz, G., Offermanns, S. (2000). Role for G12/G13 in Agonist-Induced Vascular Smooth Muscle Cell Contraction. Circ. Res. 87: 221-227 [Abstract] [Full Text]  
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• Nakayama, A. Y., Harms, M. B., Luo, L. (2000). Small GTPases Rac and Rho in the Maintenance of Dendritic Spines and Branches in Hippocampal Pyramidal Neurons. J. Neurosci. 20: 5329-5338 [Abstract] [Full Text]  
• Wong, W. T., Faulkner-Jones, B. E., Sanes, J. R., Wong, R. O. L. (2000). Rapid Dendritic Remodeling in the Developing Retina: Dependence on Neurotransmission and Reciprocal Regulation by Rac and Rho. J. Neurosci. 20: 5024-5036 [Abstract] [Full Text]  
• Ishizaki, T., Uehata, M., Tamechika, I., Keel, J., Nonomura, K., Maekawa, M., Narumiya, S. (2000). Pharmacological Properties of Y-27632, a Specific Inhibitor of Rho-Associated Kinases. Mol. Pharmacol. 57: 976-983 [Abstract] [Full Text]  
• Wahl, S., Barth, H., Ciossek, T., Aktories, K., Mueller, B. K. (2000). Ephrin-A5 Induces Collapse of Growth Cones by Activating Rho and Rho Kinase. JCB 149: 263-270 [Abstract] [Full Text]  
• Ohashi, K., Nagata, K., Maekawa, M., Ishizaki, T., Narumiya, S., Mizuno, K. (2000). Rho-associated Kinase ROCK Activates LIM-kinase 1 by Phosphorylation at Threonine 508 within the Activation Loop. J. Biol. Chem. 275: 3577-3582 [Abstract] [Full Text]  
• Nath, D, Slocombe, P., Webster, A, Stephens, P., Docherty, A., Murphy, G (2000). Meltrin gamma(ADAM-9) mediates cellular adhesion through alpha(6)beta(1 )integrin, leading to a marked induction of fibroblast cell motility. J. Cell Sci. 113: 2319-2328 [Abstract]  
• Sarner, S., Kozma, R., Ahmed, S., Lim, L. (2000). Phosphatidylinositol 3-Kinase, Cdc42, and Rac1 Act Downstream of Ras in Integrin-Dependent Neurite Outgrowth in N1E-115 Neuroblastoma Cells. Mol. Cell. Biol. 20: 158-172 [Abstract] [Full Text]  
• Olsson, P.-A., Korhonen, L., Mercer, E. A., Lindholm, D. (1999). MIR Is a Novel ERM-like Protein That Interacts with Myosin Regulatory Light Chain and Inhibits Neurite Outgrowth. J. Biol. Chem. 274: 36288-36292 [Abstract] [Full Text]  
• Inada, H., Togashi, H., Nakamura, Y., Kaibuchi, K., Nagata, K.-i., Inagaki, M. (1999). Balance between Activities of Rho Kinase and Type 1 Protein Phosphatase Modulates Turnover of Phosphorylation and Dynamics of Desmin/Vimentin Filaments. J. Biol. Chem. 274: 34932-34939 [Abstract] [Full Text]  
• Kawano, Y., Fukata, Y., Oshiro, N., Amano, M., Nakamura, T., Ito, M., Matsumura, F., Inagaki, M., Kaibuchi, K. (1999). Phosphorylation of Myosin-Binding Subunit (Mbs) of Myosin Phosphatase by Rho-Kinase in Vivo. JCB 147: 1023-1038 [Abstract] [Full Text]  
• Amano, M., Chihara, K., Nakamura, N., Kaneko, T., Matsuura, Y., Kaibuchi, K. (1999). The COOH Terminus of Rho-kinase Negatively Regulates Rho-kinase Activity. J. Biol. Chem. 274: 32418-32424 [Abstract] [Full Text]  
• Paul, B. Z. S., Daniel, J. L., Kunapuli, S. P. (1999). Platelet Shape Change Is Mediated by both Calcium-dependent and -independent Signaling Pathways. ROLE OF p160 Rho-ASSOCIATED COILED-COIL-CONTAINING PROTEIN KINASE IN PLATELET SHAPE CHANGE. J. Biol. Chem. 274: 28293-28300 [Abstract] [Full Text]  

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