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Science 2 February 1996:
Vol. 271. no. 5249, pp. 645 - 648
DOI: 10.1126/science.271.5249.645
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Reports

Protein Kinase N (PKN) and PKN-Related Protein Rhophilin as Targets of Small GTPase Rho

Go Watanabe,  Yuji Saito,  Pascal Madaule,  Toshimasa Ishizaki,  Kazuko Fujisawa,  Narito Morii,  Hideyuki Mukai,  Yoshitaka Ono,  Akira Kakizuka,  Shuh Narumiya (1)

The Rho guanosine 5'-triphosphatase (GTPase) cycles between the active guanosine triphosphate (GTP)-bound form and the inactive guanosine diphosphate-bound form and regulates cell adhesion and cytokinesis, but how it exerts these actions is unknown. The yeast two-hybrid system was used to clone a complementary DNA for a protein (designated Rhophilin) that specifically bound to GTP-Rho. The Rho-binding domain of this protein has 40 percent identity with a putative regulatory domain of a protein kinase, PKN. PKN itself bound to GTP-Rho and was activated by this binding both in vitro and in vivo. This study indicates that a serine-threonine protein kinase is a Rho effector and presents an amino acid sequence motif for binding to GTP-Rho that may be shared by a family of Rho target proteins.


G. Watanabe, Y. Saito, P. Madaule, T. Ishizaki, K. Fujisawa, N. Morii, A. Kakizuka, S. Narumiya, Department of Pharmacology, Kyoto University Faculty of Medicine, Kyoto 606, Japan.
H. Mukai and Y. Ono, Department of Biology, Faculty of Science, Kobe University, Kobe 657, Japan.
(1) To whom correspondence should be addressed.


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Y. Takai, T. Sasaki, and T. Matozaki (2001)
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T. Ishizaki, M. Uehata, I. Tamechika, J. Keel, K. Nonomura, M. Maekawa, and S. Narumiya (2000)
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J. Biol. Chem. 275, 11064-11070
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Stimulation of Phosphatidylinositol-4-phosphate 5-Kinase by Rho-Kinase.
P. A. O. Weernink, P. Schulte, Y. Guo, J. Wetzel, M. Amano, K. Kaibuchi, S. Haverland, M. Vo{beta}, M. Schmidt, G. W. Mayr, et al. (2000)
J. Biol. Chem. 275, 10168-10174
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R. T. Terry-Lorenzo, M. Inoue, J. H. Connor, T. A. J. Haystead, B. N. Armbruster, R. P. Gupta, C. J. Oliver, and S. Shenolikar (2000)
J. Biol. Chem. 275, 2439-2446
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Induction of a 55-kDa PKN Cleavage Product by Ischemia/Reperfusion Model in the Rat Retina.
K. Sumioka, Y. Shirai, N. Sakai, T. Hashimoto, C. Tanaka, M. Yamamoto, M. Takahashi, Y. Ono, and N. Saito (2000)
Invest. Ophthalmol. Vis. Sci. 41, 29-35
   Abstract »    Full Text »
Ropporin, a sperm-specific binding protein of rhophilin, that is localized in the fibrous sheath of sperm flagella.
A Fujita, K Nakamura, T Kato, N Watanabe, T Ishizaki, K Kimura, A Mizoguchi, and S Narumiya (2000)
J. Cell Sci. 113, 103-112
   Abstract »    PDF »
Balance between Activities of Rho Kinase and Type 1 Protein Phosphatase Modulates Turnover of Phosphorylation and Dynamics of Desmin/Vimentin Filaments.
H. Inada, H. Togashi, Y. Nakamura, K. Kaibuchi, K.-i. Nagata, and M. Inagaki (1999)
J. Biol. Chem. 274, 34932-34939
   Abstract »    Full Text »    PDF »
Mitogen-Activated Signaling in Airway Smooth Muscle . A Central Role for Ras.
M. B. Hershenson and M. K. Abe (1999)
Am. J. Respir. Cell Mol. Biol. 21, 651-654
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Phosphorylation of Myosin-Binding Subunit (Mbs) of Myosin Phosphatase by Rho-Kinase in Vivo.
Y. Kawano, Y. Fukata, N. Oshiro, M. Amano, T. Nakamura, M. Ito, F. Matsumura, M. Inagaki, and K. Kaibuchi (1999)
J. Cell Biol. 147, 1023-1038
   Abstract »    Full Text »    PDF »
The COOH Terminus of Rho-kinase Negatively Regulates Rho-kinase Activity.
M. Amano, K. Chihara, N. Nakamura, T. Kaneko, Y. Matsuura, and K. Kaibuchi (1999)
J. Biol. Chem. 274, 32418-32424
   Abstract »    Full Text »    PDF »
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.
B. Z. S. Paul, J. L. Daniel, and S. P. Kunapuli (1999)
J. Biol. Chem. 274, 28293-28300
   Abstract »    Full Text »    PDF »
The Neuronal Architecture of Xenopus Retinal Ganglion Cells Is Sculpted by Rho-Family GTPases In Vivo.
M. L. Ruchhoeft, S.-i. Ohnuma, L. McNeill, C. E. Holt, and W. A. Harris (1999)
J. Neurosci. 19, 8454-8463
   Abstract »    Full Text »    PDF »
Characterization of a Novel Giant Scaffolding Protein, CG-NAP, That Anchors Multiple Signaling Enzymes to Centrosome and the Golgi Apparatus.
M. Takahashi, H. Shibata, M. Shimakawa, M. Miyamoto, H. Mukai, and Y. Ono (1999)
J. Biol. Chem. 274, 17267-17274
   Abstract »    Full Text »    PDF »
Rho and Rho Kinase Mediate Thrombin-Stimulated Vascular Smooth Muscle Cell DNA Synthesis and Migration.
T. M. Seasholtz, M. Majumdar, D. D. Kaplan, and J. H. Brown (1999)
Circ. Res. 84, 1186-1193
   Abstract »    Full Text »    PDF »
Agonist-Induced Regulation of Myosin Phosphatase Activity in Human Platelets Through Activation of Rho-Kinase.
Y. Suzuki, M. Yamamoto, H. Wada, M. Ito, T. Nakano, Y. Sasaki, S. Narumiya, H. Shiku, and M. Nishikawa (1999)
Blood 93, 3408-3417
   Abstract »    Full Text »    PDF »
Rho3 of Saccharomyces cerevisiae, Which Regulates the Actin Cytoskeleton and Exocytosis, Is a GTPase Which Interacts with Myo2 and Exo70.
N. G. G. Robinson, L. Guo, J. Imai, A. Toh-e, Y. Matsui, and F. Tamanoi (1999)
Mol. Cell. Biol. 19, 3580-3587
   Abstract »    Full Text »    PDF »
The Drosophila Pkn protein kinase is a Rho/Rac effector target required for dorsal closure during embryogenesis.
Y. Lu and J. Settleman (1999)
Genes & Dev. 13, 1168-1180
   Abstract »    Full Text »
Phosphorylation of Adducin by Rho-Kinase Plays a Crucial Role in Cell Motility.
Y. Fukata, N. Oshiro, N. Kinoshita, Y. Kawano, Y. Matsuoka, V. Bennett, Y. Matsuura, and K. Kaibuchi (1999)
J. Cell Biol. 145, 347-361
   Abstract »    Full Text »    PDF »
Fission Yeast {alpha}-Glucan Synthase Mok1 Requires the Actin Cytoskeleton to Localize the Sites of Growth and Plays an Essential Role in Cell Morphogenesis Downstream of Protein Kinase C Function.
S. Katayama, D. Hirata, M. Arellano, P. Perez, and T. Toda (1999)
J. Cell Biol. 144, 1173-1186
   Abstract »    Full Text »    PDF »
Interaction of the Small G Protein RhoA with the C Terminus of Human Phospholipase D1.
M. Yamazaki, Y. Zhang, H. Watanabe, T. Yokozeki, S. Ohno, K. Kaibuchi, H. Shibata, H. Mukai, Y. Ono, M. A. Frohman, et al. (1999)
J. Biol. Chem. 274, 6035-6038
   Abstract »    Full Text »    PDF »
Identification and Cloning of Xp95, a Putative Signal Transduction Protein in Xenopus Oocytes.
S. Che, H. M. El-Hodiri, C.-F. Wu, M. Nelman-Gonzalez, M. M. Weil, L. D. Etkin, R. B. Clark, and J. Kuang (1999)
J. Biol. Chem. 274, 5522-5531
   Abstract »    Full Text »    PDF »
Rho-associated Kinase of Chicken Gizzard Smooth Muscle.
J. Feng, M. Ito, Y. Kureishi, K. Ichikawa, M. Amano, N. Isaka, K. Okawa, A. Iwamatsu, K. Kaibuchi, D. J. Hartshorne, et al. (1999)
J. Biol. Chem. 274, 3744-3752
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Novel Roles of Specific Isoforms of Protein Kinase C in Activation of the c-fos Serum Response Element.
J.-W. Soh, E. H. Lee, R. Prywes, and I. B. Weinstein (1999)
Mol. Cell. Biol. 19, 1313-1324
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Cytoskeletal changes induced by GRAF, the GTPase regulator associated with focal adhesion kinase, are mediated by Rho.
J. Taylor, M. Macklem, and J. Parsons (1999)
J. Cell Sci. 112, 231-242
   Abstract »    PDF »
Phosphorylation of Moesin by Rho-associated Kinase (Rho-kinase) Plays a Crucial Role in the Formation of Microvilli-like Structures.
N. Oshiro, Y. Fukata, and K. Kaibuchi (1998)
J. Biol. Chem. 273, 34663-34666
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Roles of Rho-associated Kinase in Cytokinesis; Mutations in Rho-associated Kinase Phosphorylation Sites Impair Cytokinetic Segregation of Glial Filaments.
Y. Yasui, M. Amano, K.-i. Nagata, N. Inagaki, H. Nakamura, H. Saya, K. Kaibuchi, and M. Inagaki (1998)
J. Cell Biol. 143, 1249-1258
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Pasteurella multocida Toxin Increases Endothelial Permeability via Rho Kinase and Myosin Light Chain Phosphatase.
M. Essler, K. Hermann, M. Amano, K. Kaibuchi, J. Heesemann, P. C. Weber, and M. Aepfelbacher (1998)
J. Immunol. 161, 5640-5646
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Proteolytic activation of PKN by caspase-3 or related protease during apoptosis.
M. Takahashi, H. Mukai, M. Toshimori, M. Miyamoto, and Y. Ono (1998)
PNAS 95, 11566-11571
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A Protein Kinase, PKN, Accumulates in Alzheimer Neurofibrillary Tangles and Associated Endoplasmic Reticulum-Derived Vesicles and Phosphorylates Tau Protein.
T. Kawamata, T. Taniguchi, H. Mukai, M. Kitagawa, T. Hashimoto, K. Maeda, Y. Ono, and C. Tanaka (1998)
J. Neurosci. 18, 7402-7410
   Abstract »    Full Text »    PDF »
Thrombin Inactivates Myosin Light Chain Phosphatase via Rho and Its Target Rho Kinase in Human Endothelial Cells.
M. Essler, M. Amano, H.-J. Kruse, K. Kaibuchi, P. C. Weber, and M. Aepfelbacher (1998)
J. Biol. Chem. 273, 21867-21874
   Abstract »    Full Text »    PDF »
Different Regions of Rho Determine Rho-selective Binding of Different Classes of Rho Target Molecules.
K. Fujisawa, P. Madaule, T. Ishizaki, G. Watanabe, H. Bito, Y. Saito, A. Hall, and S. Narumiya (1998)
J. Biol. Chem. 273, 18943-18949
   Abstract »    Full Text »    PDF »
Guanine Nucleotide Exchange Factors Regulate Specificity of Downstream Signaling from Rac and Cdc42.
K. Zhou, Y. Wang, J. L. Gorski, N. Nomura, J. Collard, and G. M. Bokoch (1998)
J. Biol. Chem. 273, 16782-16786
   Abstract »    Full Text »    PDF »
Identification of a Potential Effector Pathway for the Trimeric Go Protein Associated with Secretory Granules. Go STIMULATES A GRANULE-BOUND PHOSPHATIDYLINOSITOL 4-KINASE BY ACTIVATING RhoA IN CHROMAFFIN CELLS.
S. Gasman, S. Chasserot-Golaz, P. Hubert, D. Aunis, and M.-F. Bader (1998)
J. Biol. Chem. 273, 16913-16920
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Physiological Features of Visceral Smooth Muscle Cells, With Special Reference to Receptors and Ion Channels.
H. KURIYAMA, K. KITAMURA, T. ITOH, and R. INOUE (1998)
Physiol Rev 78, 811-920
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Signal Transduction and Signal Modulation by Cell Adhesion Receptors: The Role of Integrins, Cadherins, Immunoglobulin-Cell Adhesion Molecules, and Selectins.
A. E. Aplin, A. Howe, S. K. Alahari, and R. L. Juliano (1998)
Pharmacol. Rev. 50, 197-264
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Phosphatidic Acid-induced Elevation of Intracellular Ca2+ Is Mediated by RhoA and H2O2 in Rat-2 Fibroblasts.
Z.-W. Lee, S.-M. Kweon, B.-C. Kim, S.-H. Leem, I. Shin, J.-H. Kim, and K.-S. Ha (1998)
J. Biol. Chem. 273, 12710-12715
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Determination of Interaction Sites on the Small G Protein RhoA for Phospholipase D.
C. D. Bae, D. S. Min, I. N. Fleming, and J. H. Exton (1998)
J. Biol. Chem. 273, 11596-11604
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Phosphorylation of Vimentin by Rho-associated Kinase at a Unique Amino-terminal Site That Is Specifically Phosphorylated during Cytokinesis.
H. Goto, H. Kosako, K. Tanabe, M. Yanagida, M. Sakurai, M. Amano, K. Kaibuchi, and M. Inagaki (1998)
J. Biol. Chem. 273, 11728-11736
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Activation of Rho-Dependent Cell Spreading and Focal Adhesion Biogenesis by the v-Crk Adaptor Protein.
Z. F. Altun-Gultekin, S. Chandriani, C. Bougeret, T. Ishizaki, S. Narumiya, P. de Graaf, P. Van Bergen en Henegouwen, H. Hanafusa, J. A. Wagner, and R. B. Birge (1998)
Mol. Cell. Biol. 18, 3044-3058
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Association of the Myosin-binding Subunit of Myosin Phosphatase and Moesin: Dual Regulation of Moesin Phosphorylation by Rho-associated Kinase and Myosin Phosphatase.
Y. Fukata, K. Kimura, N. Oshiro, H. Saya, Y. Matsuura, and K. Kaibuchi (1998)
J. Cell Biol. 141, 409-418
   Abstract »    Full Text »    PDF »
Crystal Structure of Human RhoA in a Dominantly Active Form Complexed with a GTP Analogue.
K. Ihara, S. Muraguchi, M. Kato, T. Shimizu, M. Shirakawa, S. Kuroda, K. Kaibuchi, and T. Hakoshima (1998)
J. Biol. Chem. 273, 9656-9666
   Abstract »    Full Text »    PDF »
Analysis of RhoA-binding Proteins Reveals an Interaction Domain Conserved in Heterotrimeric G Protein beta  Subunits and the Yeast Response Regulator Protein Skn7.
A. S. Alberts, N. Bouquin, L. H. Johnston, and R. Treisman (1998)
J. Biol. Chem. 273, 8616-8622
   Abstract »    Full Text »    PDF »
Rho Guanosine Triphosphatase Mediates the Selective Stabilization of Microtubules Induced by Lysophosphatidic Acid.
T. A. Cook, T. Nagasaki, and G. G. Gundersen (1998)
J. Cell Biol. 141, 175-185
   Abstract »    Full Text »    PDF »
A Conserved Negative Regulatory Region in alpha PAK: Inhibition of PAK Kinases Reveals Their Morphological Roles Downstream of Cdc42 and Rac1.
Z.-S. Zhao, E. Manser, X.-Q. Chen, C. Chong, T. Leung, and L. Lim (1998)
Mol. Cell. Biol. 18, 2153-2163
   Abstract »    Full Text »
Comparative Effects of GTPgamma S and Insulin on the Activation of Rho, Phosphatidylinositol 3-Kinase, and Protein Kinase N in Rat Adipocytes. RELATIONSHIP TO GLUCOSE TRANSPORT.
M. Standaert, G. Bandyopadhyay, L. Galloway, Y. Ono, H. Mukai, and R. Farese (1998)
J. Biol. Chem. 273, 7470-7477
   Abstract »    Full Text »    PDF »
The Low Molecular Weight GTPase Rho Regulates Myofibril Formation and Organization in Neonatal Rat Ventricular Myocytes. INVOLVEMENT OF Rho KINASE.
M. Hoshijima, V. P. Sah, Y. Wang, K. R. Chien, and J. H. Brown (1998)
J. Biol. Chem. 273, 7725-7730
   Abstract »    Full Text »    PDF »
Regulation of the Association of Adducin with Actin Filaments by Rho-associated Kinase (Rho-kinase) and Myosin Phosphatase.
K. Kimura, Y. Fukata, Y. Matsuoka, V. Bennett, Y. Matsuura, K. Okawa, A. Iwamatsu, and K. Kaibuchi (1998)
J. Biol. Chem. 273, 5542-5548
   Abstract »    Full Text »    PDF »
Evidence for distinct mechanisms of transition state stabilization of GTPases by fluoride.
S. Vincent, M. Brouns, M. J. Hart, and J. Settleman (1998)
PNAS 95, 2210-2215
   Abstract »    Full Text »    PDF »
The Rho Family G Proteins Play a Critical Role in Muscle Differentiation.
H. Takano, I. Komuro, T. Oka, I. Shiojima, Y. Hiroi, T. Mizuno, and Y. Yazaki (1998)
Mol. Cell. Biol. 18, 1580-1589
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PRK1 Is Targeted to Endosomes by the Small GTPase, RhoB.
H. Mellor, P. Flynn, C. D. Nobes, A. Hall, and P. J. Parker (1998)
J. Biol. Chem. 273, 4811-4814
   Abstract »    Full Text »    PDF »
Small GTP-binding Protein Rho Stimulates the Actomyosin System, Leading to Invasion of Tumor Cells.
K. Yoshioka, F. Matsumura, H. Akedo, and K. Itoh (1998)
J. Biol. Chem. 273, 5146-5154
   Abstract »    Full Text »    PDF »
Rho-Kinase Phosphorylates COOH-terminal Threonines of Ezrin/Radixin/Moesin (ERM) Proteins and Regulates Their Head-to-Tail Association.
T. Matsui, M. Maeda, Y. Doi, S. Yonemura, M. Amano, K. Kaibuchi, S. Tsukita, and S. Tsukita (1998)
J. Cell Biol. 140, 647-657
   Abstract »    Full Text »    PDF »
RhoA-Dependent Phosphorylation and Relocalization of ERM Proteins into Apical Membrane/Actin Protrusions in Fibroblasts.
R. J. Shaw, M. Henry, F. Solomon, and T. Jacks (1998)
Mol. Biol. Cell 9, 403-419
   Abstract »    Full Text »
p160 RhoA-binding Kinase ROKalpha Induces Neurite Retraction.
H. Katoh, J. Aoki, A. Ichikawa, and M. Negishi (1998)
J. Biol. Chem. 273, 2489-2492
   Abstract »    Full Text »    PDF »
Multiple Interactions of PRK1 with RhoA. FUNCTIONAL ASSIGNMENT OF THE HR1 REPEAT MOTIF.
P. Flynn, H. Mellor, R. Palmer, G. Panayotou, and P. J. Parker (1998)
J. Biol. Chem. 273, 2698-2705
   Abstract »    Full Text »    PDF »
Rho GTPases and the Actin Cytoskeleton.
A. Hall (1998)
Science 279, 509-514
   Abstract »    Full Text »
DRhoGEF2 encodes a member of the Dbl family of oncogenes and controls cell shape changes during gastrulation in Drosophila.
U. Häcker and N. Perrimon (1998)
Genes & Dev. 12, 274-284
   Abstract »    Full Text »
GTPgammaS-induced actin polymerisation in vitro: ATP- and phosphoinositide-independent signalling via Rho-family proteins and a plasma membrane-associated guanine nucleotide exchange factor.
V. Katanaev and M. Wymann (1998)
J. Cell Sci. 111, 1583-1594
   Abstract »    PDF »


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