The interaction between L1-type proteins and ankyrins - a master switch for L1-type CAM functions

• Autorzy: Hortsch M , Nagaraj K. , Godenschwege T.A.
• Języki publikacji: EN

Abstrakty

EN

L1-type cell adhesion molecules (CAMs) are important mediators of neural differentiation, including axonal outgrowth and pathfinding and also of synapse formation and maintenance. In addition, their interactions with cytoskeletal components are highly conserved and regulated. How these different aspects of CAM functionality relate to each other is not well understood. Based on results from our and other laboratories we propose that ankyrin-binding to L1-type CAMs provides a master switch. The interaction with ankyrins directs L1-type adhesive proteins into different functional contexts, either ankyrin-independent functions, such as neurite outgrowth and axonal pathfinding or into ankyrin-dependent functions, such as L1’s role at axon initial segments (AIS), paranodal regions, synapses and in dendrites.

Słowa kluczowe

EN

interaction; L1-type protein; ankyrin; cell adhesion; membrane skeleton; tyrosine phosphorylation; neuromuscular junction; synapse; synaptogenesis; Drosophila; cell adhesion molecule; growth factor receptor

• Wydawca: -
• Czasopismo: Cellular and Molecular Biology Letters
• Rocznik: 2009
• Tom: 14
• Numer: 1
• Opis fizyczny: p.57-69,fig.,ref.

Twórcy

autor

Hortsch M

• University of Michigan, Ann Arbor, MI 48109, USA

autor

Nagaraj K.

autor

Godenschwege T.A.

Bibliografia

• 1. Hortsch, M. Structural and functional evolution of the L1-family: Are four adhesion molecules better than one? Mol. Cell. Neurosci. 15 (2000) 1-10.
• 2. Hortsch, M. and Margolis, B. Septate and paranodal junctions: Kissing cousins. Trends Cell. Biol. 13 (2003) 557-561.
• 3. Panicker, A.K., Buhusi, M., Thelen, K. and Maness, P.F. Cellular signalling mechanisms of neural cell adhesion molecules. Front. Biosci. 8 (2003) D900-911.
• 4. Godenschwege, T.A., Kristiansen, L.V., Uthaman, S.B., Hortsch, M. and Murphey, R.K. A conserved role for Drosophila Neuroglian and human L1- CAM in central-synapse formation. Curr. Biol. 16 (2006) 12-23.
• 5. Ango, F., di Cristo, G., Higashiyama, H., Bennett, V., Wu, P. and Huang, Z.J. Ankyrin-based subcellular gradient of neurofascin, an immunoglobulin family protein, directs GABAergic innervation at purkinje axon initial segment. Cell 119 (2004) 257-272.
• 6. Triana-Baltzer, G.B., Liu, Z. and Berg, D.K. Pre- and postsynaptic actions of L1-CAM in nicotinic pathways. Mol. Cell. Neurosci. 33 (2006) 214-226.
• 7. Hortsch, M. The L1 family of neural cell adhesion molecules: Old proteins performing new tricks. Neuron 17 (1996) 587-593.
• 8. Davis, J.Q., McLaughlin, T. and Bennett, V. Ankyrin-binding proteins related to nervous system cell adhesion molecules: candidates to provide transmembrane and intercellular connections in adult brain. J. Cell. Biol. 121 (1993) 121-133.
• 9. Davis, J.Q. and Bennett, V. Ankyrin binding activity shared by the neurofascin/L1/NrCAM family of nervous system cell adhesion molecules. J. Biol. Chem. 269 (1994) 27163-27166.
• 10. Dubreuil, R.R., MacVicar, G., Dissanayake, S., Liu, C., Homer, D. and Hortsch, M. Neuroglian-mediated cell adhesion induces assembly of the membrane skeleton at cell contact sites. J. Cell. Biol. 133 (1996) 647-655.
• 11. Malhotra, J.D., Tsiotra, P., Karagogeos, D. and Hortsch, M. Cis-activation of L1-mediated ankyrin recruitment by TAG-1 homophilic cell adhesion. J. Biol. Chem. 273 (1998) 33354-33359.
• 12. Hortsch, M., Homer, D., Malhotra, J.D., Chang, S., Frankel, J., Jefford, G. and Dubreuil, R.R. Structural requirements for "outside-in" and "inside-out" signaling by Drosophila neuroglian, a member of the L1 family of cell adhesion molecules. J. Cell. Biol. 142 (1998) 251-261.
• 13. Garver, T.D., Ren, Q., Tuvia, S. and Bennett, V. Tyrosine phosphorylation at a site highly conserved in the L1 family of cell adhesion molecules abolishes ankyrin binding and increases lateral mobility of neurofascin. J. Cell. Biol. 137 (1997) 703-714.
• 14. Bouley, M., Tian, M.-Z., Paisley, K., Shen, Y.-C., Malhotra, J.D. and Hortsch, M. The L1-type cell adhesion molecule neuroglian influences the stability of neural ankyrin in the Drosophila embryo but not its axonal localization. J. Neurosci. 20 (2000) 4515-4523.
• 15. Tuvia, S., Garver, T.D. and Bennett, V. The phosphorylation state of the FIGQY tyrosine of neurofascin determines ankyrin-binding activity and patterns of cell segregation. Proc. Natl. Acad. Sci. USA 94 (1997) 12957- 12962.
• 16. Kizhatil, K., Wu, Y.X., Sen, A. and Bennett, V. A new activity of doublecortin in recognition of the phospho-FIGQY tyrosine in the cytoplasmic domain of neurofascin. J. Neurosci. 22 (2002) 7948-7958.
• 17. Jenkins, S.M., Kizhatil, K., Kramarcy, N.R., Sen, A., Sealock, R. and Bennett, V. FIGQY phosphorylation defines discrete populations of L1 cell adhesion molecules at sites of cell-cell contact and in migrating neurons. J. Cell Sci. 114 (2001) 3823-3835.
• 18. Whittard, J.D., Sakurai, T., Cassella, M.R., Gazdoiu, M. and Felsenfeld, D.P. MAP kinase pathway-dependent phosphorylation of the L1-CAM ankyrin-binding site regulates neuronal growth. Mol. Biol. Cell (2006).
• 19. Gil, O.D., Sakurai, T., Bradley, A.E., Fink, M.Y., Cassella, M.R., Kuo, J.A. and Felsenfeld, D.P. Ankyrin binding mediates L1CAM interactions with static components of the cytoskeleton and inhibits retrograde movement of L1CAM on the cell surface. J. Cell. Biol. 162 (2003) 719-730.
• 20. Chen, L., Ong, B. and Bennett, V. LAD-1, the Caenorhabditis elegans L1CAM homologue, participates in embryonic and gonadal morphogenesis and is a substrate for fibroblast growth factor receptor pathway-dependent phosphotyrosine-based signaling. J. Cell. Biol. 154 (2001) 841-856.
• 21. Bennett, V. and Baines, A.J. Spectrin and ankyrin-based pathways: metazoan inventions for integrating cells into tissues. Physiol. Rev. 81 (2001) 1353-1392.
• 22. Mohler, P.J., Gramolini, A.O. and Bennett, V. Ankyrins. J. Cell Sci. 115 (2002) 1565-1566.
• 23. Otsuka, A.J., Franco, R., Yang, B., Shim, K.H., Tang, L.Z., Zhang, Y.Y., Boontrakulpoontawee, P., Jeyaprakash, A., Hedgecock, E., Wheaton, V.I. and Sobery, A. An ankyrin-related gene (unc-44) is necessary for proper axonal guidance in Caenorhabditis elegans. J. Cell. Biol. 129 (1995) 1081- 1092.
• 24. Dubreuil, R.R. and Yu, J.-Q. Ankyrin and beta-spectrin accumulate independently of alpha-spectrin in Drosophila. Proc. Natl. Acad. Sci. USA 91 (1994) 10285-10289.
• 25. Koch, I., Schwarz, H., Beuchle, D., Goellner, B., Langegger, M. and Aberle, H. Drosophila ankyrin 2 is required for synaptic stability. Neuron 58 (2008) 210-222.
• 26. Hortsch, M., Paisley, K.L., Tian, M.Z., Qian, M., Bouley, M. and Chandler, R. The axonal localization of large Drosophila ankyrin2 protein isoforms is essential for neuronal functionality. Mol. Cell. Neurosci. 20 (2002) 43-55.
• 27. Pielage, J., Cheng, L., Fetter, R.D., Carlton, P.M., Sedat, J.W. and Davis, G.W. A presynaptic giant ankyrin stabilizes the NMJ through regulation of presynaptic microtubules and transsynaptic cell adhesion. Neuron 58 (2008) 195-209.
• 28. Otsuka, A.J., Boontrakulpoontawee, P., Rebeiz, N., Domanus, M., Otsuka, D., Velamparampil, N., Chan, S., Vande Wyngaerde, M., Campagna, S. and Cox, A. Novel UNC-44 AO13 ankyrin is required for axonal guidance in C. elegans, contains six highly repetitive STEP blocks separated by seven potential transmembrane domains, and is localized to neuronal processes and the periphery of neural cell bodies. J. Neurobiol. 50 (2002) 333-349.
• 29. Kordeli, E., Davis, J., Trapp, B. and Bennett, V. An isoform of ankyrin is localized at nodes of Ranvier in myelinated axons of central and peripheral nerves. J. Cell. Biol. 110 (1990) 1341-1352.
• 30. Islam, R., Kristansen, L.V., Romani, S., Garcia-Alonso, L. and Hortsch, M. Activation of EGF receptor kinase by L1-mediated homophilic cell interactions. Mol. Biol. Cell 15 (2004) 1509-1518.
• 31. Garcia-Alonso, L., Romani, S. and Jimenez, F. The EGF and FGF receptors mediate neuroglian function to control growth cone decisions during sensory axon guidance in Drosophila. Neuron 28 (2000) 741-752.
• 32. Kristiansen, L.V., Velasquez, E., Romani, S., Baars, S., Berezin, V., Bock, E., Hortsch, M. and Garcia-Alonso, L. Genetic analysis of an overlapping functional requirement for L1- and NCAM-type proteins during sensory axon guidance in Drosophila. Mol. Cell. Neurosci. 28 (2005) 141-152.
• 33. Nishimura, K., Yoshihara, F., Tojima, T., Ooashi, N., Yoon, W., Mikoshiba, K., Bennett, V. and Kamiguchi, H. L1-dependent neuritogenesis involves ankyrinB that mediates L1-CAM coupling with retrograde actin flow. J. Cell. Biol. 163 (2003) 1077-1088.
• 34. Davey, F., Hill, M., Falk, J., Sans, N. and Gunn-Moore, F.J. Synapse associated protein 102 is a novel binding partner to the cytoplasmic terminus of neurone-glial related cell adhesion molecule. J. Neurochem. 94 (2005) 1243-1253.
• 35. Dirks, P., Thomas, U. and Montag, D. The cytoplasmic domain of NrCAM binds to PDZ domains of synapse-associated proteins SAP90/PSD95 and SAP97. Eur. J. Neurosci. 24 (2006) 25-31.
• 36. Bieber, A.J., Snow, P.M., Hortsch, M., Patel, N.H., Jacobs, J.R., Traquina, Z.R., Schilling, J. and Goodman, C.S. Drosophila neuroglian: a member of the immunoglobulin superfamily with extensive homology to the vertebrate neural adhesion molecule L1. Cell 59 (1989) 447-460.
• 37. Pielage, J., Fetter, R.D. and Davis, G.W. A postsynaptic spectrin scaffold defines active zone size, spacing, and efficacy at the Drosophila neuromuscular junction. J. Cell. Biol. 175 (2006) 491-503.
• 38. Yamamoto, M., Ueda, R., Takahashi, K., Saigo, K. and Uemura, T. Control of axonal sprouting and dendrite branching by the nrg-ank complex at the neuron-glia interface. Curr. Biol. 16 (2006) 1678-1683.
• 39. Bennett, V. and Lambert, S. Physiological roles of axonal ankyrins in survival of premyelinated axons and localization of voltage-gated sodium channels. J. Neurocytol. 28 (1999) 303-318.
• 40. Lambert, S., Davis, J.Q. and Bennett, V. Morphogenesis of the node of Ranvier: co-clusters of ankyrin and ankyrin-binding integral proteins define early developmental intermediates. J. Neurosci. 17 (1997) 7025-7036.
• 41. Davis, J.Q., Lambert, S. and Bennett, V. Molecular composition of the node of Ranvier: Identification of ankyrin-binding cell adhesion molecules neurofascin (mucin+/third FNIII domain-) and NrCAM at nodal axon segments. J. Cell. Biol. 135 (1996) 1355-1367.
• 42. Winckler, B., Forscher, P. and Mellman, I. A diffusion barrier maintains distribution of membrane proteins in polarized neurons. Nature 397 (1999) 698-701.
• 43. Boiko, T., Vakulenko, M., Ewers, H., Yap, C.C., Norden, C. and Winckler, B. Ankyrin-dependent and -independent mechanisms orchestrate axonal compartmentalization of L1 family members neurofascin and L1/neuron-glia cell adhesion molecule. J. Neurosci. 27 (2007) 590-603.
• 44. Dickson, T.C., Mintz, C.D., Benson, D.L. and Salton, S.R. Functional binding interaction identified between the axonal CAM L1 and members of the ERM family. J. Cell. Biol. 157 (2002) 1105-1112.
• 45. Shimada, T., Toriyama, M., Uemura, K., Kamiguchi, H., Sugiura, T., Watanabe, N. and Inagaki, N. Shootin1 interacts with actin retrograde flow and L1-CAM to promote axon outgrowth. J. Cell. Biol. 181 (2008) 817-829.
• 46. Kamiguchi, H., Long, K.E., Pendergast, M., Schaefer, A.W., Rapoport, I., Kirchhausen, T. and Lemmon, V. The neural cell adhesion molecule L1 interacts with the AP-2 adaptor and is endocytosed via the clathrin-mediated pathway. J. Neurosci. 18 (1998) 5311-5321.