The EphA4 receptor regulates dendritic spine remodeling by affecting β1-integrin signaling pathways

Journal of Cell Biology

Volumn 178, Issue 7, 2007, Pages 1295-1307

  Bourgin, Caroline ^a   Murai, Keith K ^b   Richter, Melanie ^a   Pasquale, Elena B ^a,c  

^a BURNHAM INSTITUTE   (United States)

^b MONTREAL GENERAL HOSPITAL   (Canada)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA1 INTEGRIN; CELLULAR APOPTOSIS SUSCEPTIBILITY PROTEIN; CRK ASSOCIATED SUBSTRATE PROTEIN; EPHRIN A3; EPHRIN RECEPTOR A4; FOCAL ADHESION KINASE; FOCAL ADHESION KINASE 2; PROTEIN KINASE FYN;

ANIMAL TISSUE; ARTICLE; DENDRITIC SPINE; HIPPOCAMPUS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ANIMALS; ANTIGENS, CD29; CELL ADHESION; CRK-ASSOCIATED SUBSTRATE PROTEIN; DENDRITIC SPINES; ENZYME ACTIVATION; EPHRIN-A3; HIPPOCAMPUS; HUMANS; MICE; NERVE TISSUE PROTEINS; PHOSPHOPROTEINS; PHOSPHORYLATION; PHOSPHOTYROSINE; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS C-CRK; PROTO-ONCOGENE PROTEINS C-FYN; RATS; RECEPTOR, EPHA4; SIGNAL TRANSDUCTION; SRC HOMOLOGY DOMAINS; SUBSTRATE SPECIFICITY;

EID: 34748829242     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200610139     Document Type: Article

References (77)

1. Arnaout, M.A., B. Mahalingam, and J.P. Xiong. 2005. Integrin structure, allostery, and bidirectional signaling. Annu. Rev. Cell Dev. Biol. 21:381-410.
2. Bazzoni, G., D.T. Shih, C.A. Buck, and M.E. Hemler. 1995. Monoclonal antibody 9EG7 defines a novel beta 1 integrin epitope induced by soluble ligand and manganese, but inhibited by calcium. J. Biol. Chem. 270:25570-25577.
3. Bernard-Trifilo, J.A., E.A. Kramar, R. Torp, C.Y. Lin, E.A. Pineda, G. Lynch, and C.M. Gall. 2005. Integrin signaling cascades are operational in adult hippocampal synapses and modulate NMDA receptor physiology. J. Neurochem. 93:834-849.
4. Boda, B., S. Alberi, I. Nikonenko, R. Node-Langlois, P. Jourdain, M. Moosmayer, L. Parisi-Jourdain, and D. Muller. 2004. The mental retardation protein PAK3 contributes to synapse formation and plasticity in hippocampus. J. Neurosci. 24:10816-10825.
5. Bonhoeffer, T., and R. Yuste. 2002. Spine motility. Phenomenology, mechanisms, and function. Neuron. 35:1019-1027.
6. Bouton, A.H., R.B. Riggins, and P.J. Bruce-Staskal. 2001. Functions of the adapter protein Cas: signal convergence and the determination of cellular responses. Oncogene. 20:6448-6458.
7. Bromann, P.A., H. Korkaya, and S.A. Courtneidge. 2004. The interplay between Src family kinases and receptor tyrosine kinases. Oncogene. 23:7957-7968.
8. Chan, C.S., E.J. Weeber, L. Zong, E. Fuchs, J.D. Sweatt, and R.L. Davis. 2006. Beta 1-integrins are required for hippocampal AMPA receptor-dependent synaptic transmission, synaptic plasticity, and working memory. J. Neurosci. 26:223-232.
9. Chen, K., P.G. Ochalski, T.S. Tran, N. Sahir, M. Schubert, A. Pramatarova, and B.W. Howell. 2004. Interaction between Dab1 and CrkII is promoted by Reelin signaling. J. Cell Sci. 117:4527-4536.
10. Chodniewicz, D., and R.L. Klemke. 2004. Regulation of integrin-mediated cellular responses through assembly of a CAS/Crk scaffold. Biochim. Biophys. Acta. 1692:63-76.
11. Chun, D., C.M. Gall, X. Bi, and G. Lynch. 2001. Evidence that integrins contribute to multiple stages in the consolidation of long term potentiation in rat hippocampus. Neuroscience. 105:815-829.
12. Clegg, D.O., K.L. Wingerd, S.T. Hikita, and E.C. Tolhurst. 2003. Integrins in the development, function and dysfunction of the nervous system. Front. Biosci. 8:d723-d750.
13. Cowan, C.W., Y.R. Shao, M. Sahin, S.M. Shamah, M.Z. Lin, P.L. Greer, S. Gao, E.C. Griffith, J.S. Brugge, and M.E. Greenberg. 2005. Vav family GEFs link activated Ephs to endocytosis and axon guidance. Neuron. 46:205-217.
14. Ellis, C., F. Kasmi, P. Ganju, E. Walls, G. Panayotou, and A.D. Reith. 1996. A juxtamembrane autophosphorylation site in the Eph family receptor tyrosine kinase, Sek, mediates high affinity interaction with p59fyn. Oncogene. 12:1727-1736.
15. Ethell, I.M., and E.B. Pasquale. 2005. Molecular mechanisms of dendritic spine development and remodeling. Prog. Neurobiol. 75:161-205.
16. Ethell, I.M., F. Irie, M.S. Kalo, J.R. Couchman, E.B. Pasquale, and Y. Yamaguchi. 2001. EphB/syndecan-2 signaling in dendritic spine morphogenesis. Neuron. 31:1001-1013.
17. Feller, S.M. 2001. Crk family adaptors-signalling complex formation and biological roles. Oncogene. 20:6348-6371.
18. Fiala, J.C., J. Spacek, and K.M. Harris. 2002. Dendritic spine pathology: cause or consequence of neurological disorders? Brain Res. Brain Res. Rev. 39:29-54.
19. Fonseca, P.M., N.Y. Shin, J. Brabek, L. Ryzhova, J. Wu, and S.K. Hanks. 2004. Regulation and localization of CAS substrate domain tyrosine phosphorylation. Cell. Signal. 16:621-629.
20. Fu, W.Y., Y. Chen, M. Sahin, X.S. Zhao, L. Shi, J.B. Bikoff, K.O. Lai, W.H. Yung, A.K. Fu, M.E. Greenberg, and N.Y. Ip. 2007. Cdk5 regulates EphA4-mediated dendritic spine retraction through an ephexin1-dependent mechanism. Nat. Neurosci. 10:67-76.
21. Girault, J.A., A. Costa, P. Derkinderen, J.M. Studler, and M. Toutant. 1999. FAK and PYK2/CAKbeta in the nervous system: a link between neuronal activity, plasticity and survival? Trends Neurosci. 22:257-263.
22. Govek, E.E., S.E. Newey, C.J. Akerman, J.R. Cross, L. Van Der Veken, and L. Van Aelst. 2004. The X-linked mental retardation protein oligophrenin-1 is required for dendritic spine morphogenesis. Nat. Neurosci. 7:364-372.
23. Grant, S.G., T.J. O'Dell, K.A. Karl, P.L. Stein, P. Soriano, and E.R. Kandel. 1992. Impaired long-term potentiation, spatial learning, and hippocampal development in fyn mutant mice. Science. 258:1903-1910.
24. Grunwald, I.C., M. Korte, G. Adelmann, A. Plueck, K. Kullander, R.H. Adams, M. Frotscher, T. Bonhoeffer, and R. Klein. 2004. Hippocampal plasticity requires postsynaptic ephrinBs. Nat. Neurosci. 7:33-40.
25. Hama, H., C. Hara, K. Yamaguchi, and A. Miyawaki. 2004. PKC signaling mediates global enhancement of excitatory synaptogenesis in neurons triggered by local contact with astrocytes. Neuron. 41:405-415.
26. Henkemeyer, M., O.S. Itkis, M. Ngo, P.W. Hickmott, and I.M. Ethell. 2003. Multiple EphB receptor tyrosine kinases shape dendritic spines in the hippocampus. J. Cell Biol. 163:1313-1326.
27. Hering, H., and M. Sheng. 2001. Dendritic spines: structure, dynamics and regulation. Nat. Rev. Neurosci. 2:880-888.
28. Huang, J., R. Sakai, and T. Furuichi. 2006. The docking protein Cas links tyrosine phosphorylation signaling to elongation of cerebellar granule cell axons. Mol. Biol. Cell. 17:3187-3196.
29. Huang, Z., K. Shimazu, N.H. Woo, K. Zang, U. Muller, B. Lu, and L.F. Reichardt. 2006. Distinct roles of the beta 1-class integrins at the developing and the mature hippocampal excitatory synapse. J. Neurosci. 26:11208-11219.
30. Husi, H., M.A. Ward, J.S. Choudhary, W.P. Blackstock, and S.G. Grant. 2000. Proteomic analysis of NMDA receptor-adhesion protein signaling complexes. Nat. Neurosci. 3:661-669.
31. Ivins, J.K., P.D. Yurchenco, and A.D. Lander. 2000. Regulation of neurite outgrowth by integrin activation. J. Neurosci. 20:6551-6560.
32. Kennedy, M.B., H.C. Beale, H.J. Carlisle, and L.R. Washburn. 2005. Integration of biochemical signalling in spines. Nat. Rev. Neurosci. 6:423-434.
33. Knoll, B., and U. Drescher. 2004. Src family kinases are involved in EphA receptor-mediated retinal axon guidance. J. Neurosci. 24:6248-6257.
34. Kojima, N., J. Wang, I.M. Mansuy, S.G. Grant, M. Mayford, and E.R. Kandel. 1997. Rescuing impairment of long-term potentiation in fyn-deficient mice by introducing Fyn transgene. Proc. Natl. Acad. Sci. USA. 94:4761-4765.
35. Korkotian, E., D. Holcman, and M. Segal. 2004. Dynamic regulation of spinedendrite coupling in cultured hippocampal neurons. Eur. J. Neurosci. 20:2649-2663.
36. Kramar, E.A., B. Lin, C.S. Rex, C.M. Gall, and G. Lynch. 2006. Integrin-driven actin polymerization consolidates long-term potentiation. Proc. Natl. Acad. Sci. USA. 103:5579-5584.
37. Kullander, K., and R. Klein. 2002. Mechanisms and functions of Eph and ephrin signalling. Nat. Rev. Mol. Cell Biol. 3:475-486.
38. Lauri, S.E., T. Taira, and H. Rauvala. 2000. High-frequency synaptic stimulation induces association of fyn and c-src to distinct phosphorylated components. Neuroreport. 11:997-1000.
39. Li, Y., P. Maher, and D. Schubert. 1997. A role for 12-lipoxygenase in nerve cell death caused by glutathione depletion. Neuron. 19:453-463.
40. Lin, B., A.C. Arai, G. Lynch, and C.M. Gall. 2003. Integrins regulate NMDA receptor-mediated synaptic currents. J. Neurophysiol. 89:2874-2878.
41. Liu, W.S., C. Pesold, M.A. Rodriguez, G. Carboni, J. Auta, P. Lacor, J. Larson, B.G. Condie, A. Guidotti, and E. Costa. 2001. Down-regulation of dendritic spine and glutamic acid decarboxylase 67 expressions in the reelin haploinsufficient heterozygous reeler mouse. Proc. Natl. Acad. Sci. USA. 98:3477-3482.
42. Maruoka, H., D. Konno, K. Hori, and K. Sobue. 2005. Collaboration of PSD-Zip70 with its binding partner, SPAR, in dendritic spine maturity. J. Neurosci. 25:1421-1430.
43. Mataga, N., Y. Mizuguchi, and T.K. Hensch. 2004. Experience-dependent pruning of dendritic spines in visual cortex by tissue plasminogen activator. Neuron. 44:1031-1041.
44. Matus, A. 2000. Actin-based plasticity in dendritic spines. Science. 290:754-758.
45. Miao, H., E. Burnett, M. Kinch, E. Simon, and B. Wang. 2000. Activation of EphA2 kinase suppresses integrin function and causes focal-adhesion-kinase dephosphorylation. Nat. Cell Biol. 2:62-69.
46. Moeller, M.L., Y. Shi, L.F. Reichardt, and I.M. Ethell. 2006. EphB receptors regulate dendritic spine morphogenesis through the recruitment/phosphorylation of focal adhesion kinase and RhoA activation. J. Biol. Chem. 281:1587-1598.
47. Morita, A., N. Yamashita, Y. Sasaki, Y. Uchida, O. Nakajima, F. Nakamura, T. Yagi, M. Taniguchi, H. Usui, R. Katoh-Semba, et al. 2006. Regulation of dendritic branching and spine maturation by semaphorin3A-Fyn signaling. J. Neurosci. 26:2971-2980.
48. Murai, K.K., L.N. Nguyen, F. Irie, Y. Yamaguchi, and E.B. Pasquale. 2003. Control of hippocampal dendritic spine morphology through ephrin-A3/EphA4 signaling. Nat. Neurosci. 6:153-160.
49. Nakamoto, T., R. Sakai, K. Ozawa, Y. Yazaki, and H. Hirai. 1996. Direct binding of C-terminal region of p130Cas to SH2 and SH3 domains of Src kinase. J. Biol. Chem. 271:8959-8965.
50. Nimchinsky, E.A., B.L. Sabatini, and K. Svoboda. 2002. Structure and function of dendritic spines. Annu. Rev. Physiol. 64:313-353.
51. Noguchi, J., M. Matsuzaki, G.C. Ellis-Davies, and H. Kasai. 2005. Spine-neck geometry determines NMDA receptor-dependent Ca2+ signaling in dendrites. Neuron. 46:609-622.
52. O'Neill, G.M., S.J. Fashena, and E.A. Golemis. 2000. Integrin signalling: a new Cas(t) of characters enters the stage. Trends Cell Biol. 10:111-119.
53. Oray, S., A. Majewska, and M. Sur. 2004. Dendritic spine dynamics are regulated by monocular deprivation and extracellular matrix degradation. Neuron. 44:1021-1030.
54. Pasquale, E.B. 2005. Eph receptor signalling casts a wide net on cell behaviour. Nat. Rev. Mol. Cell Biol. 6:462-475.
55. Penzes, P., A. Beeser, J. Chernoff, M.R. Schiller, B.A. Eipper, R.E. Mains, and R.L. Huganir. 2003. Rapid induction of dendritic spine morphogenesis by trans-synaptic EphrinB-EphB receptor activation of the Rho-GEF Kalirin. Neuron. 37:263-274.
56. Pinkstaff, J.K., J. Detterich, G. Lynch, and C. Gall. 1999. Integrin subunit gene expression is regionally differentiated in adult brain. J. Neurosci. 19:1541-1556.
57. Playford, M.P., and M.D. Schaller. 2004. The interplay between Src and integrins in normal and tumor biology. Oncogene. 23:7928-7946.
58. Poliakov, A., M. Cotrina, and D.G. Wilkinson. 2004. Diverse roles of eph receptors and ephrins in the regulation of cell migration and tissue assembly. Dev. Cell. 7:465-480.
59. Prevost, N., D.S. Woulfe, H. Jiang, T.J. Stalker, P. Marchese, Z.M. Ruggeri, and L.F. Brass. 2005. Eph kinases and ephrins support thrombus growth and stability by regulating integrin outside-in signaling in platelets. Proc. Natl. Acad. Sci. USA. 102:9820-9825.
60. Rogers, C., and S. Lemaire. 1991. Role of the sigma receptor in the inhibition of [3H]-noradrenaline uptake in brain synaptosomes and adrenal chromaffin cells. Br. J. Pharmacol. 103:1917-1922.
61. Ruest, P.J., N.Y. Shin, T.R. Polte, X. Zhang, and S.K. Hanks. 2001. Mechanisms of CAS substrate domain tyrosine phosphorylation by FAK and Src. Mol. Cell. Biol. 21:7641-7652.
62. Ruoslahti, E. 1996. RGD and other recognition sequences for integrins. Annu. Rev. Cell Dev. Biol. 12:697-715.
63. Sahin, M., P.L. Greer, M.Z. Lin, H. Poucher, J. Eberhart, S. Schmidt, T.M. Wright, S.M. Shamah, S. O'Connell, C.W. Cowan, et al. 2005. Ephdependent tyrosine phosphorylation of ephexin1 modulates growth cone collapse. Neuron. 46:191-204.
64. Salter, M.W., and L.V. Kalia. 2004. Src kinases: a hub for NMDA receptor regulation. Nat. Rev. Neurosci. 5:317-328.
65. Schubert, D., S. Heinemann, W. Carlisle, H. Tarikas, B. Kimes, J. Patrick, J.H. Steinbach, W. Culp, and B.L. Brandt. 1974. Clonal cell lines from the rat central nervous system. Nature. 249:224-227.
66. Schuster, T., M. Krug, M. Stalder, N. Hackel, R. Gerardy-Schahn, and M. Schachner. 2001. Immunoelectron microscopic localization of the neural recognition molecules L1, NCAM, and its isoform NCAM180, the NCAM-associated polysialic acid, beta1 integrin and the extracellular matrix molecule tenascin-R in synapses of the adult rat hippocampus. J. Neurobiol. 49:142-158.
67. Segal, M. 2005. Dendritic spines and long-term plasticity. Nat. Rev. Neurosci. 6:277-284.
68. Shamah, S.M., M.Z. Lin, J.L. Goldberg, S. Estrach, M. Sahin, L. Hu, M. Bazalakova, R.L. Neve, G. Corfas, A. Debant, and M.E. Greenberg. 2001. EphA receptors regulate growth cone dynamics through the novel guanine nucleotide exchange factor ephexin. Cell. 105:233-244.
69. Shi, Y., and I.M. Ethell. 2006. Integrins control dendritic spine plasticity in hippocampal neurons through NMDA receptor and Ca2+/ calmodulindependent protein kinase II-mediated actin reorganization. J. Neurosci. 26:1813-1822.
70. Shimaoka, M., and T.A. Springer. 2003. Therapeutic antagonists and conformational regulation of integrin function. Nat. Rev. Drug Discov. 2:703-716.
71. Stoppini, L., P.A. Buchs, and D. Muller. 1991. A simple method for organotypic cultures of nervous tissue. J. Neurosci. Methods. 37:173-182.
72. Webb, D.J., H. Zhang, D. Majumdar, and A.F. Horwitz. 2007. alpha5 integrin signaling regulates the formation of spines and synapses in hippocampal neurons. J. Biol. Chem. 282:6929-6935.
73. Yamaguchi, Y., and E.B. Pasquale. 2004. Eph receptors in the adult brain. Curr. Opin. Neurobiol. 14:288-296.
74. Yuste, R., and T. Bonhoeffer. 2001. Morphological changes in dendritic spines associated with long-term synaptic plasticity. Annu. Rev. Neurosci. 24:1071-1089.
75. Zafra, F., B. Hengerer, J. Leibrock, H. Thoenen, and D. Lindholm. 1990. Activity dependent regulation of BDNF and NGF mRNAs in the rat hippocampus is mediated by non-NMDA glutamate receptors. EMBO J. 9:3545-3550.
76. Zisch, A.H., M.S. Kalo, L.D. Chong, and E.B. Pasquale. 1998. Complex formation between EphB2 and Src requires phosphorylation of tyrosine 611 in the EphB2 juxtamembrane region. Oncogene. 16:2657-2670.
77. Zisch, A.H., C. Pazzagli, A.L. Freeman, M. Schneller, M. Hadman, J.W. Smith, E. Ruoslahti, and E.B. Pasquale. 2000. Replacing two conserved tyrosines of the EphB2 receptor with glutamic acid prevents binding of SH2 domains without abrogating kinase activity and biological responses. Oncogene. 19:177-187.