Molecules and Cells

Korean Society for Molecular and Cellular Biology (한국분자세포생물학회)
권호 표지

Interaction of Nonreceptor Tyrosine-Kinase Fer and p120 Catenin Is Involved in Neuronal Polarization

  • Received : 2005.05.26
  • Accepted : 2005.07.27
  • Published : 2005.10.31
⟨ Previous Next ⟩

Abstract

The neuronal cytoskeleton is essential for establishment of neuronal polarity, but mechanisms controlling generation of polarity in the cytoskeleton are poorly understood. The nonreceptor tyrosine kinase, Fer, has been shown to bind to microtubules and to interact with several actin-regulatory proteins. Furthermore, Fer binds p120 catenin and has been shown to regulate cadherin function by modulating cadherin-${\beta}$-catenin interaction. Here we show involvement of Fer in neuronal polarization and neurite development. Fer is concentrated in growth cones together with cadherin, ${\beta}$-catenin, and cortactin in stage 2 hippocampal neurons. Inhibition of Fer-p120 catenin interaction with a cell-permeable inhibitory peptide (FerP) increases neurite branching. In addition, the peptide significantly delays conversion of one of several dendrites into an axon in early stage hippocampal neurons. FerP-treated growth cones also exhibit modified localization of the microtubule and actin cytoskeleton. Together, this indicates that the Fer-p120 interaction is required for normal neuronal polarization and neurite development.

Keywords

Acknowledgement

Supported by : Korean Research Foundation

References

  1. Anastasiadis, P. Z. and Reynolds, P. B. (2000) The p120 catenin family: complex roles in adhesion, signaling and cancer. J. Cell Sci. 113, 1319-1334
  2. Arimura, N., Menager, C., Fukata, Y., and Kaibuchi, K. (2004) Role of CRMP-2 in neuronal polarity. J. Neurobiol. 58, 34-47 https://doi.org/10.1002/neu.10269
  3. Arregui, C., Pathre, P., Lilien, J., and Balsamo, J. (2000) The nonreceptor tyrosine kinase fer mediates cross-talk between N-cadherin and beta1-integrins. J. Cell Biol. 149, 1263-1274 https://doi.org/10.1083/jcb.149.6.1263
  4. Baas, P. W. (1999) Microtubules and neuronal polarity: lessons from mitosis. Neuron 22, 23-31 https://doi.org/10.1016/S0896-6273(00)80675-3
  5. Bamji, S. X., Shimazu, K., Kimes, N., Huelsken, J., Birchmeier, W., et al. (2003) Role of beta-catenin in synaptic vesicle localization and presynaptic assembly. Neuron 40, 719-731 https://doi.org/10.1016/S0896-6273(03)00718-9
  6. Bradke, F. and Dotti, C. G. (1999) The role of local actin instability in axon formation. Science 283, 1931-1934 https://doi.org/10.1126/science.283.5409.1931
  7. Chen, X., Kojima, S., Borisy, G. G., and Green, K. J. (2003) p120 catenin associates with kinesin and facilitates the transport of cadherin-catenin complexes to intercellular junctions. J. Cell Biol. 163, 547-557 https://doi.org/10.1083/jcb.200305137
  8. Condic, M. L. and Letourneau, P. C. (1997) Ligand-induced changes in integrin expression regulate neuronal adhesion and neurite outgrowth. Nature 389, 852-856 https://doi.org/10.1038/39878
  9. Craig, A. W., Zirngibl, R., and Greer, P. (1999) Disruption of coiled-coil domains in Fer protein-tyrosine kinase abolishes trimerization but not kinase activation. J. Biol. Chem. 274, 19934-19942 https://doi.org/10.1074/jbc.274.28.19934
  10. Craig, A. W., Zirngibl, R., Williams, K., Cole, L. A., and Greer, P. A. (2001) Mice devoid of fer protein-tyrosine kinase activity are viable and fertile but display reduced cortactin phosphorylation. Mol. Cell Biol. 21, 603-613 https://doi.org/10.1128/MCB.21.2.603-613.2001
  11. Daly, R. J. (2004) Cortactin signalling and dynamic actin networks. Biochem. J. 382, 13-25 https://doi.org/10.1042/BJ20040737
  12. Dent, E. W. and Kalil, K. (2001) Axon branching requires interactions between dynamic microtubules and actin filaments. J. Neurosci. 15, 9757-9769
  13. Derossi, D., Joliot, A. H., Chassaing, G., and Prochiantz, A. (1994) The third helix of the Antennapedia homeodomain translocates through biological membranes. J. Biol. Chem. 269, 10444-10450
  14. Dotti, C. G., Sullivan, C. A., and Banker, G. A. (1988) The establishment of polarity by hippocampal neurons in culture. J. Neurosci. 8, 1454-1468
  15. Etienne-Manneville, S. and Hall, A. (2003) Cdc42 regulates GSK-3beta and adenomatous polyposis coli to control cell polarity. Nature 421, 753-756 https://doi.org/10.1038/nature01423
  16. Fan, L., Di Ciano-Oliveira, C., Weed, S. A., Craig, A. W., Greer, P. A., et al. (2004) Actin depolymerization-induced tyrosine phosphorylation of cortactin: the role of Fer kinase. Biochem. J. 380, 581-591 https://doi.org/10.1042/BJ20040178
  17. Franz, C. M. and Ridley, A. J. (2003) p120 catenin associates with microtubules: inverse relationship between microtubule binding and Rho GTPase regulation. J. Biol. Chem. 279, 6588-6594 https://doi.org/10.1074/jbc.M312812200
  18. Fukata, Y., Kimura, T., and Kaibuchi, K. (2002) Axon specification in hippocampal neurons. Neurosci. Res. 43, 305-315 https://doi.org/10.1016/S0168-0102(02)00062-7
  19. Greer, P. (2002) Closing in on the biological functions of Fps/Fes and Fer. Nat. Rev. Mol. Cell. Biol. 3, 278-289 https://doi.org/10.1038/nrm783
  20. Hong, J.-H., Noh, K., Yoo, Y., Choi, S., Park, S., et al. (2003) Iron promotes the survival and neurite extension of serumstarved PC12 cells in the presence of NGF by enhancing cell attachment. Mol. Cells 15, 10-19
  21. Horton, A. C. and Ehlers, M. D. (2003) Neuronal polarity and trafficking. Neuron 40, 277-295 https://doi.org/10.1016/S0896-6273(03)00629-9
  22. Jalink, K., van Corven, E. J., Hengeveld, T., Morii, N., Narumiya, S., et al. (1994) Inhibition of lysophosphatidate- and thrombin-induced neurite retraction and neuronal cell rounding by ADP ribosylation of the small GTP-binding protein Rho. J. Cell Biol. 126, 801-810 https://doi.org/10.1083/jcb.126.3.801
  23. Kempf, M., Clement, A., Faissner, A., Lee, G., and Brandt, R. (1996) Tau Binds to the distal axon early in development of polarity in a microtubule- and microfilament-dependent manner. J. Neurosci. 16, 5583-5592
  24. Kim, L. and Wong, T. W. (1998) Growth factor-dependent phosphorylation of the actin-binding protein cortactin is mediated by the cytoplasmic tyrosine kinase FER. J. Biol. Chem. 273, 23542-23548 https://doi.org/10.1074/jbc.273.36.23542
  25. Kogata, N., Masuda, M., Kamioka, Y., Yamagishi, A., Endo, A., et al. (2003) Identification of Fer tyrosine kinase localized on microtubules as a platelet endothelial cell adhesion molecule- 1 phosphorylating kinase in vascular endothelial cells. Mol. Biol. Cell 14, 3553-3564 https://doi.org/10.1091/mbc.E03-02-0080
  26. Kozma, R., Sarner, S., Ahmed, S., and Lim, L. (1997) Rho family GTPases and neuronal growth cone remodelling: relationship between increased complexity induced by Cdc42Hs, Rac1, and acetylcholine and collapse induced by RhoA and lysophosphatidic acid. Mol. Cell. Biol. 17, 1201-1211
  27. Kunda, P., Paglini, G., Quiroga, S., Kosik, K., and Caceres, A. (2001) Evidence for the involvement of Tiam1 in axon formation. J. Neurosci. 21, 2361-2372
  28. Leu, S. T., Jacques, S. A., Wingerd, K. L., Hikita, S. T., Tolhurst, E. C., et al. (2004) Integrin alpha4beta1 function is required for cell survival in developing retina. Dev. Biol. 276, 416-430 https://doi.org/10.1016/j.ydbio.2004.09.003
  29. Li, H., Leung, T. C., Hoffman, S., Balsamo, J., and Lilien, J. (2000) Coordinate regulation of cadherin and integrin function by the chondroitin sulfate proteoglycan neurocan. J. Cell Biol. 149, 1275-1288 https://doi.org/10.1083/jcb.149.6.1275
  30. Luo, L. (2002) Actin cytoskeleton regulation in neuronal morphogenesis and structural plasticity. Annu. Rev. Cell. Dev. Biol. 18, 601-635 https://doi.org/10.1146/annurev.cellbio.18.031802.150501
  31. Martinez, M. C., Ochiishi, T., Majewski, M., and Kosik, K. S. (2003) Dual regulation of neuronal morphogenesis by a delta-catenin-cortactin complex and Rho. J. Cell Biol. 162, 99-111 https://doi.org/10.1083/jcb.200211025
  32. Ng, J. and Luo, L. (2004) Rho GTPases regulate axon growth through convergent and divergent signaling pathways. Neuron 44, 779-793 https://doi.org/10.1016/j.neuron.2004.11.014
  33. Nishimura, T., Yamaguchi, T., Kato, K., Yoshizawa, M., Nabeshima, Y., et al. (2005) PAR-6-PAR-3 mediates Cdc42- induced Rac activation through the Rac GEFs STEF/Tiam1. Nat. Cell Biol. 7, 270-277 https://doi.org/10.1038/ncb1227
  34. Noren, N. K., Liu, B. P., Burridge, K., and Kreft, B. (2000) p120 catenin regulates the actin cytoskeleton via Rho family GTPases. J. Cell Biol. 150, 567-580 https://doi.org/10.1083/jcb.150.3.567
  35. Peifer, M. and Yap, A. S. (2003) Traffic control: p120-catenin acts as a gatekeeper to control the fate of classical cadherins in mammalian cells. J. Cell Biol. 163, 437-440 https://doi.org/10.1083/jcb.200310090
  36. Roczniak-Ferguson, A. and Reynolds, A. B. (2003) Regulation of p120-catenin nucleocytoplasmic shuttling activity. J. Cell Sci. 116, 4201-4212 https://doi.org/10.1242/jcs.00724
  37. Sabo, S. L. and McAllister, A. K. (2003) Mobility and cycling of synaptic protein-containing vesicles in axonal growth cone filopodia. Nat. Neurosci. 6, 1264-1269 https://doi.org/10.1038/nn1149
  38. Tomaselli, K. J., Doherty, P., Emmett, C. J., Damsky, C. H., Walsh, F. S., et al. (1993) Expression of beta 1 integrins in sensory neurons of the dorsal root ganglion and their functions in neurite outgrowth on two laminin isoforms. J. Neurosci. 13, 4880-4888
  39. Xu, G., Craig, A. W., Greer, P., Miller, M., Anastasiadis, P. Z., et al. (2004) Continuous association of cadherin with betacatenin requires the non-receptor tyrosine-kinase Fer. J. Cell Sci. 117, 3207-3219 https://doi.org/10.1242/jcs.01174
  40. Yoshimura, T., Kawano, Y., Arimura, N., Kawabata, S., Kikuchi, A., et al. (2005) GSK-3beta regulates phosphorylation of CRMP-2 and neuronal polarity. Cell 120, 137-149 https://doi.org/10.1016/j.cell.2004.11.012
  41. Zhou, F. Q., Waterman-Storer, C. M., and Cohan, C. S. (2002) Focal loss of actin bundles causes microtubule redistribution and growth cone turning. J. Cell Biol. 27, 839-849