CRMP-2 Is Involved in Kinesin-1-Dependent Transport of the Sra-1/WAVE1 Complex and Axon Formation

REFERENCES

• Arimura, N., N. Inagaki, K. Chihara, C. Menager, N. Nakamura, M. Amano, A. Iwamatsu, Y. Goshima, and K. Kaibuchi. 2000. Phosphorylation of collapsin response mediator protein-2 by Rho-kinase. Evidence for two separate signaling pathways for growth cone collapse. J. Biol. Chem. 275:23973–23980.
   PubMed Web of Science ®Google Scholar
• Baas, P. W. 1997. Microtubules and axonal growth. Curr. Opin. Cell Biol. 9:29–36.
   PubMed Web of Science ®Google Scholar
• Blatch, G. L., and M. Lassle. 1999. The tetratricopeptide repeat: a structural motif mediating protein-protein interactions. Bioessays 21:932–939.
   PubMed Web of Science ®Google Scholar
• Bradke, F., and C. G. Dotti. 2000. Establishment of neuronal polarity: lessons from cultured hippocampal neurons. Curr. Opin. Neurobiol. 10:574–581.
   PubMed Web of Science ®Google Scholar
• Bradke, F., and C. G. Dotti. 1999. The role of local actin instability in axon formation. Science 283:1931–1934.
   PubMedGoogle Scholar
• Brady, S. T. 1985. A novel brain ATPase with properties expected for the fast axonal transport motor. Nature 317:73–75.
   PubMed Web of Science ®Google Scholar
• Brendza, K. M., D. J. Rose, S. P. Gilbert, and W. M. Saxton. 1999. Lethal kinesin mutations reveal amino acids important for ATPase activation and structural coupling. J. Biol. Chem. 274:31506–31514.
   PubMedGoogle Scholar
• Brown, M., T. Jacobs, B. Eickholt, G. Ferrari, M. Teo, C. Monfries, R. Z. Qi, T. Leung, L. Lim, and C. Hall. 2004. α2-Chimaerin, cyclin-dependent kinase 5/p35, and its target collapsin response mediator protein-2 are essential components in semaphorin 3A-induced growth-cone collapse. J. Neurosci. 24:8994–9004.
   PubMedGoogle Scholar
• Byk, T., S. Ozon, and A. Sobel. 1998. The Ulip family phosphoproteins-common and specific properties. Eur. J. Biochem. 254:14–24.
   PubMedGoogle Scholar
• Chalfie, M., E. Dean, E. Reilly, K. Buck, and J. N. Thomson. 1986. Mutations affecting microtubule structure in Caenorhabditis elegans. J. Cell Sci. Suppl. 5:257–271.
   PubMedGoogle Scholar
• Craig, A. M., and G. Banker. 1994. Neuronal polarity. Annu. Rev. Neurosci. 17:267–310.
   PubMed Web of Science ®Google Scholar
• Deo, R. C., E. F. Schmidt, A. Elhabazi, H. Togashi, S. K. Burley, and S. M. Strittmatter. 2004. Structural bases for CRMP function in plexin-dependent semaphorin3A signaling. EMBO J. 23:9–22.
   PubMed Web of Science ®Google Scholar
• Desai, C., G. Garriga, S. L. McIntire, and H. R. Horvitz. 1988. A genetic pathway for the development of the Caenorhabditis elegans HSN motor neurons. Nature 336:638–646.
   PubMed Web of Science ®Google Scholar
• Eden, S., R. Rohatgi, A. V. Podtelejnikov, M. Mann, and M. W. Kirschner. 2002. Mechanism of regulation of WAVE1-induced actin nucleation by Rac1 and Nck. Nature 418:790–793.
   PubMed Web of Science ®Google Scholar
• Ferreira, A., J. Niclas, R. D. Vale, G. Banker, and K. S. Kosik. 1992. Suppression of kinesin expression in cultured hippocampal neurons using antisense oligonucleotides. J. Cell Biol. 117:595–606.
   PubMedGoogle Scholar
• Fukata, Y., T. J. Itoh, T. Kimura, C. Menager, T. Nishimura, T. Shiromizu, H. Watanabe, N. Inagaki, A. Iwamatsu, H. Hotani, and K. Kaibuchi. 2002. CRMP-2 binds to tubulin heterodimers to promote microtubule assembly. Nat. Cell Biol. 4:583–591.
   PubMed Web of Science ®Google Scholar
• Gaetano, C., T. Matsuo, and C. J. Thiele. 1997. Identification and characterization of a retinoic acid-regulated human homologue of the unc-33-like phosphoprotein gene (hUlip) from neuroblastoma cells. J. Biol. Chem. 272:12195–12201.
   PubMedGoogle Scholar
• Goshima, Y., F. Nakamura, P. Strittmatter, and S. M. Strittmatter. 1995. Collapsin-induced growth cone collapse mediated by an intracellular protein related to UNC-33. Nature 376:509–514.
   PubMed Web of Science ®Google Scholar
• Govek, E. E., S. E. Newey, and L. Van Aelst. 2005. The role of the Rho GTPases in neuronal development. Genes Dev. 19:1–49.
   PubMed Web of Science ®Google Scholar
• Gu, Y., N. Hamajima, and Y. Ihara. 2000. Neurofibrillary tangle-associated collapsin response mediator protein-2 (CRMP-2) is highly phosphorylated on Thr-509, Ser-518, and Ser-522. Biochemistry 39:4267–4275.
   PubMed Web of Science ®Google Scholar
• Hedgecock, E. M., J. G. Culotti, J. N. Thomson, and L. A. Perkins. 1985. Axonal guidance mutants of Caenorhabditis elegans identified by filling sensory neurons with fluorescein dyes. Dev. Biol. 111:158–170.
   PubMedGoogle Scholar
• Hirokawa, N., and R. Takemura. 2004. Kinesin superfamily proteins and their various functions and dynamics. Exp. Cell Res. 301:50–59.
   PubMedGoogle Scholar
• Inagaki, N., K. Chihara, N. Arimura, C. Menager, Y. Kawano, N. Matsuo, T. Nishimura, M. Amano, and K. Kaibuchi. 2001. CRMP-2 induces axons in cultured hippocampal neurons. Nat. Neurosci. 4:781–782.
   PubMed Web of Science ®Google Scholar
• Inatome, R., T. Tsujimura, T. Hitomi, N. Mitsui, P. Hermann, S. Kuroda, H. Yamamura, and S. Yanagi. 2000. Identification of CRAM, a novel unc-33 gene family protein that associates with CRMP3 and protein-tyrosine kinase(s) in the developing rat brain. J. Biol. Chem. 275:27291–27302.
   PubMedGoogle Scholar
• Innocenti, M., A. Zucconi, A. Disanza, E. Frittoli, L. B. Areces, A. Steffen, T. E. Stradal, P. P. Di Fiore, M. F. Carlier, and G. Scita. 2004. Abi1 is essential for the formation and activation of a WAVE2 signalling complex. Nat. Cell Biol. 6:319–327.
   PubMed Web of Science ®Google Scholar
• Johnson, C. S., D. Buster, and J. M. Scholey. 1990. Light chains of sea urchin kinesin identified by immunoadsorption. Cell Motil. Cytoskeleton 16:204–213.
   PubMedGoogle Scholar
• Kamal, A., and L. S. Goldstein. 2002. Principles of cargo attachment to cytoplasmic motor proteins. Curr. Opin. Cell Biol. 14:63–68.
   PubMedGoogle Scholar
• Kamal, A., G. B. Stokin, Z. Yang, C. H. Xia, and L. S. Goldstein. 2000. Axonal transport of amyloid precursor protein is mediated by direct binding to the kinesin light chain subunit of kinesin-I. Neuron 28:449–459.
   PubMed Web of Science ®Google Scholar
• Kawano, Y., Y. Fukata, N. Oshiro, M. Amano, T. Nakamura, M. Ito, F. Matsumura, M. Inagaki, and K. Kaibuchi. 1999. Phosphorylation of myosin-binding subunit (MBS) of myosin phosphatase by Rho-kinase in vivo. J. Cell Biol. 147:1023–1038.
   PubMed Web of Science ®Google Scholar
• Kimura, T., N. Arimura, Y. Fukata, H. Watanabe, A. Iwamatsu, and K. Kaibuchi. 2005. Tubulin and CRMP-2 complex is transported via Kinesin-1. J. Neurochem. 93:1371–1382.
   PubMedGoogle Scholar
• Kobayashi, K., S. Kuroda, M. Fukata, T. Nakamura, T. Nagase, N. Nomura, Y. Matsuura, N. Yoshida-Kubomura, A. Iwamatsu, and K. Kaibuchi. 1998. p140Sra-1 (specifically Rac1-associated protein) is a novel specific target for Rac1 small GTPase. J. Biol. Chem. 273:291–295.
   PubMed Web of Science ®Google Scholar
• Lawrence, C. J., R. K. Dawe, K. R. Christie, D. W. Cleveland, S. C. Dawson, S. A. Endow, L. S. Goldstein, H. V. Goodson, N. Hirokawa, J. Howard, R. L. Malmberg, J. R. McIntosh, H. Miki, T. J. Mitchison, Y. Okada, A. S. Reddy, W. M. Saxton, M. Schliwa, J. M. Scholey, R. D. Vale, C. E. Walczak, and L. Wordeman. 2004. A standardized kinesin nomenclature. J. Cell Biol. 167:19–22.
   PubMed Web of Science ®Google Scholar
• Lee, S., J. H. Kim, C. S. Lee, Y. Kim, K. Heo, Y. Ihara, Y. Goshima, P. G. Suh, and S. H. Ryu. 2002. Collapsin response mediator protein-2 inhibits neuronal phospholipase D(2) activity by direct interaction. J. Biol. Chem. 277:6542–6549.
   PubMedGoogle Scholar
• Li, W. 1992. Characterization of the Caenorhabditis elegans axonal guidance and outgrowth gene unc-33 and a viariant Tc4 transposon. Ph.D. dissertation at University of Minnesota.
   Google Scholar
• Luo, L., Y. J. Liao, L. Y. Jan, and Y. N. Jan. 1994. Distinct morphogenetic functions of similar small GTPases: Drosophila Drac1 is involved in axonal outgrowth and myoblast fusion. Genes Dev. 8:1787–1802.
   PubMed Web of Science ®Google Scholar
• Matsuura, Y., R. D. Possee, H. A. Overton, and D. H. Bishop. 1987. Baculovirus expression vectors: the requirements for high level expression of proteins, including glycoproteins. J Gen. Virol. 68(Part 5):1233–1250.
   PubMedGoogle Scholar
• McIntire, S. L., G. Garriga, J. White, D. Jacobson, and H. R. Horvitz. 1992. Genes necessary for directed axonal elongation or fasciculation in C. elegans. Neuron 8:307–322.
   PubMedGoogle Scholar
• Miki, H., S. Suetsugu, and T. Takenawa. 1998. WAVE, a novel WASP-family protein involved in actin reorganization induced by Rac. EMBO J. 17:6932–6941.
   PubMed Web of Science ®Google Scholar
• Minturn, J. E., H. J. Fryer, D. H. Geschwind, and S. Hockfield. 1995. TOAD-64, a gene expressed early in neuronal differentiation in the rat, is related to unc-33, a C. elegans gene involved in axon outgrowth. J. Neurosci. 15:6757–6766.
   PubMedGoogle Scholar
• Nakata, T., and N. Hirokawa. 2003. Microtubules provide directional cues for polarized axonal transport through interaction with kinesin motor head. J. Cell Biol. 162:1045–1055.
   PubMed Web of Science ®Google Scholar
• Nishimura, T., Y. Fukata, K. Kato, T. Yamaguchi, Y. Matsuura, H. Kamiguchi, and K. Kaibuchi. 2003. CRMP-2 regulates polarized Numb-mediated endocytosis for axon growth. Nat. Cell Biol. 5:819–826.
   PubMed Web of Science ®Google Scholar
• Nishimura, T., K. Kato, T. Yamaguchi, Y. Fukata, S. Ohno, and K. Kaibuchi. 2004. Role of the PAR-3-KIF3 complex in the establishment of neuronal polarity. Nat. Cell Biol. 6:328–334.
   PubMedGoogle Scholar
• Nishimura, T., T. Yamaguchi, K. Kato, M. Yoshizawa, Y. Nabeshima, S. Ohno, M. Hoshino, and K. Kaibuchi. 2005. PAR-6-PAR-3 mediates Cdc42 signaling to Rac activation through STEF/Tiam1, RacGEFs. Nat. Cell Biol. 7:270–277.
   PubMed Web of Science ®Google Scholar
• Noda, Y., Y. Okada, N. Saito, M. Setou, Y. Xu, Z. Zhang, and N. Hirokawa. 2001. KIFC3, a microtubule minus end-directed motor for the apical transport of annexin XIIIb-associated triton-insoluble membranes. J. Cell Biol. 155:77–88.
   PubMedGoogle Scholar
• Schenck, A., B. Bardoni, C. Langmann, N. Harden, J. L. Mandel, and A. Giangrande. 2003. CYFIP/Sra-1 controls neuronal connectivity in Drosophila and links the Rac1 GTPase pathway to the fragile X protein. Neuron 38:887–898.
   PubMed Web of Science ®Google Scholar
• Schenck, A., B. Bardoni, A. Moro, C. Bagni, and J. L. Mandel. 2001. A highly conserved protein family interacting with the fragile X mental retardation protein (FMRP) and displaying selective interactions with FMRP-related proteins FXR1P and FXR2P. Proc. Natl. Acad. Sci. USA 98:8844–8849.
   PubMed Web of Science ®Google Scholar
• Shi, S. H., L. Y. Jan, and Y. N. Jan. 2003. Hippocampal neuronal polarity specified by spatially localized mPar3/mPar6 and PI 3-kinase activity. Cell 112:63–75.
   PubMed Web of Science ®Google Scholar
• Soderling, S. H., K. L. Binns, G. A. Wayman, S. M. Davee, S. H. Ong, T. Pawson, and J. D. Scott. 2002. The WRP component of the WAVE-1 complex attenuates Rac-mediated signalling. Nat. Cell Biol. 4:970–975.
   PubMed Web of Science ®Google Scholar
• Steffen, A., K. Rottner, J. Ehinger, M. Innocenti, G. Scita, J. Wehland, and T. E. Stradal. 2004. Sra-1 and Nap1 link Rac to actin assembly driving lamellipodia formation. EMBO J. 23:749–759.
   PubMed Web of Science ®Google Scholar
• Stradal, T. E., K. Rottner, A. Disanza, S. Confalonieri, M. Innocenti, and G. Scita. 2004. Regulation of actin dynamics by WASP and WAVE family proteins. Trends Cell Biol. 14:303–311.
   PubMed Web of Science ®Google Scholar
• Strasser, G. A., N. A. Rahim, K. E. VanderWaal, F. B. Gertler, and L. M. Lanier. 2004. Arp2/Arp3 is a negative regulator of growth cone translocation. Neuron 43:81–94.
   PubMedGoogle Scholar
• Suetsugu, S., H. Miki, and T. Takenawa. 1999. Identification of two human WAVE/SCAR homologues as general actin regulatory molecules which associate with the Arp2/3 complex. Biochem. Biophys. Res. Commun. 260:296–302.
   PubMed Web of Science ®Google Scholar
• Takenawa, T., and H. Miki. 2001. WASP and WAVE family proteins: key molecules for rapid rearrangement of cortical actin filaments and cell movement. J. Cell Sci. 114:1801–1809.
   PubMedGoogle Scholar
• Terada, S., M. Kinjo, and N. Hirokawa. 2000. Oligomeric tubulin in large transporting complex is transported via kinesin in squid giant axons. Cell 103:141–155.
   PubMed Web of Science ®Google Scholar
• Tsuboi, D., T. Hikita, H. Qadota, M. Amano, and K. Kaibuchi. J. Neurochem., in press.
   Google Scholar
• Vale, R. D. 2003. The molecular motor toolbox for intracellular transport. Cell 112:467–480.
   PubMed Web of Science ®Google Scholar
• Vale, R. D., T. S. Reese, and M. P. Sheetz. 1985. Identification of a novel force-generating protein, kinesin, involved in microtubule-based motility. Cell 42:39–50.
   PubMed Web of Science ®Google Scholar
• Verhey, K. J., D. Meyer, R. Deehan, J. Blenis, B. J. Schnapp, T. A. Rapoport, and B. Margolis. 2001. Cargo of kinesin identified as JIP scaffolding proteins and associated signaling molecules. J. Cell Biol. 152:959–970.
   PubMed Web of Science ®Google Scholar
• Wang, L. H., and S. M. Strittmatter. 1997. Brain CRMP forms heterotetramers similar to liver dihydropyrimidinase. J. Neurochem. 69:2261–2269.
   PubMed Web of Science ®Google Scholar
• Westphal, R. S., S. H. Soderling, N. M. Alto, L. K. Langeberg, and J. D. Scott. 2000. Scar/WAVE-1, a Wiskott-Aldrich syndrome protein, assembles an actin-associated multi-kinase scaffold. EMBO J. 19:4589–4600.
   PubMedGoogle Scholar
• Yoshimura, T., Y. Kawano, N. Arimura, S. Kawabata, A. Kikuchi, and K. Kaibuchi. 2005. GSK-3β regulates phosphorylation of CRMP-2 and neuronal polarity. Cell 120:137–149.
   PubMed Web of Science ®Google Scholar
• Zallen, J. A., Y. Cohen, A. M. Hudson, L. Cooley, E. Wieschaus, and E. D. Schejter. 2002. SCAR is a primary regulator of Arp2/Arp3-dependent morphological events in Drosophila. J. Cell Biol. 156:689–701.
   PubMedGoogle Scholar