Transcriptional Regulation of the Tbr1-CASK-CINAP Protein Complex in Response to Neuronal Activity

  • Yi-Ping Hsueh


In neurons, postsynaptic density (PSD) refers to an electron dense structure underneath the plasma membrane at the postsynaptic site, containing various protein molecules essential for responding to the presynaptic signals, including ion channels, scaffold proteins, signaling molecules, and cytoskeletons. The scaffold proteins provide the linkage among ion channels, signaling molecules and the cytoskeleton. Accumulating data indicate that the membrane associated guanylate kinase (MAGUK) proteins are important postsynaptic scaffold proteins involved in synaptic targeting, clustering and signaling of ion channels (Sheng and Sala 2001; Kim and Sheng 2004; Montgomery, Zamorano and Garner 2004). Calcium/calmodulin-dependent serine protein kinase (CASK) belongs to MAGUK protein family. Although CASK contains a CaMK-like domain, it doesn’t possess kinase activity. Instead, like other MAGUK proteins, CASK functions as multidomain scaffolding protein. Recent studies showed that CASK not only performs its function at the postsynaptic site but also enters the nuclei of neurons and regulates gene expression via the interaction with transcriptional factor T-brain-1 (Tbr-1) and nucleosome assembly protein CINAP (CASK-interacting nucleosome assembly protein). The Tbr-1-CASK-CINAP complex modulates expression of NMDA receptor subunit 2b (NR2b). More interestingly, CINAP protein levels in neurons are controlled by synaptic activity. The studies with the Tbr-1-CASK-CINAP complex provide a novel feedback mechanism that explains how synaptic activity regulates gene expression. In this chapter, the molecular characteristics of CASK, Tbr-1, and CINAP proteins will be described first, followed by a discussion of the regulation of NR2b expression by the CINAP-CASK-Tbr-1 protein complex.


Postsynaptic Site Guanylate Kinase Synaptic Target NR2b Expression Nucleosome Assembly Protein 
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  1. Adams, C.R. and Kamakaka, R.T. (1999) Chromatin assembly: biochemical identities and genetic redundancy. Curr. Opin. Genet. Dev. 9, 185–190.PubMedCrossRefGoogle Scholar
  2. Agarwal, K.C., Miech, R.P. and Parks, R.E., Jr. (1978) Guanylate kinases from human erythrocytes, hog brain, and rat liver. Methods Enzymol. 51, 483–490.PubMedCrossRefGoogle Scholar
  3. Akazawa, C., Shigemoto, R., Bessho, Y., Nakanishi, S. and Mizuno, N. (1994) Differential expression of five N-methyl-D-aspartate receptor subunit mRNAs in the cerebellum of developing and adult rats. J. Comp. Neurol. 347, 150–160.PubMedCrossRefGoogle Scholar
  4. Behar, T.N., Scott, C.A., Greene, C.L., Wen, X., Smith, S.V., Maric, D., Liu, Q.Y., Colton, C.A. and Barker, J.L. (1999) Glutamate acting at NMDA receptors stimulates embryonic cortical neuronal migration. J. Neurosci. 19, 4449–4461.PubMedGoogle Scholar
  5. Biederer, T. and Sudhof, T.C. (2001) CASK and protein 4.1 support F-actin nucleation on neurexins. J. Biol. Chem. 276, 47869–47876.PubMedGoogle Scholar
  6. Biederer, T., Sara, Y., Mozhayeva, M., Atasoy, D., Liu, X., Kavalali, E.T. and Sudhof, T.C. (2002) SynCAM, a synaptic adhesion molecule that drives synapse assembly. Science 297, 1525–1531.PubMedCrossRefGoogle Scholar
  7. Borg, J.P., Straight, S.W., Kaech, S.M., de Taddeo-Borg, M., Kroon, D.E., Karnak, D., Turner, R.S., Kim, S.K. and Margolis, B. (1998) Identification of an evolutionarily conserved heterotrimeric protein complex involved in protein targeting. J. Biol. Chem. 273, 31633–31636.PubMedCrossRefGoogle Scholar
  8. Bretscher, A., Edwards, K. and Fehon, R.G. (2002) ERM proteins and merlin: integrators at the cell cortex. Nat. Rev. Mol. Cell Biol. 3, 586–599.PubMedCrossRefGoogle Scholar
  9. Bulfone, A., Smiga, S.M., Shimamura, K., Peterson, A., Puelles, L. and Rubenstein, J.L. (1995) T-brain-1: a homolog of Brachyury whose expression defines molecularly distinct domains within the cerebral cortex. Neuron 15, 63–78.PubMedCrossRefGoogle Scholar
  10. Bulfone, A., Wang, F., Hevner, R., Anderson, S., Cutforth, T., Chen, S., Meneses, J., Pedersen, R., Axel, R. and Rubenstein J.L. (1998) An olfactory sensory map develops in the absence of normal projection neurons or GABAergic interneurons. Neuron 21, 1273–1282.PubMedCrossRefGoogle Scholar
  11. Butz, S., Okamoto, M.and Sudhof, T.C. (1998) A tripartite protein complex with the potential to couple synaptic vesicle exocytosis to cell adhesion in brain. Cell 94, 773–782.PubMedCrossRefGoogle Scholar
  12. Chai, Z., Sarcevic, B., Mawson, A. and Toh, B.H. (2001) SET-related cell division autoantigen-1 (CDA1) arrests cell growth. J. Biol. Chem. 276, 33665–33674.PubMedCrossRefGoogle Scholar
  13. Cho, K.O., Hunt, C.A. and Kennedy, M.B. (1992) The rat brain postsynaptic density fraction contains a homolog of the Drosophila discs-large tumor suppressor protein. Neuron 9, 929–942.PubMedCrossRefGoogle Scholar
  14. Cohen, A.R., Woods, D.F., Marfatia, S.M., Walther, Z., Chishti, A.H., Anderson, J.M. and Wood, D.F. (1998) Human CASK/LIN-2 binds syndecan-2 and protein 4.1 and localizes to the basolateral membrane of epithelial cells. J. Cell Biol. 142, 129–138.PubMedCrossRefGoogle Scholar
  15. Dickson, K.S. and Kind, P.C. (2003) NMDA receptors: neural map designers and refiners? Curr. Biol. 13, R920–922.PubMedCrossRefGoogle Scholar
  16. Doerks, T., Bork, P., Kamberov, E., Makarova, O., Muecke, S. and Margolis, B. (2000) L27, a novel heterodimerization domain in receptor targeting proteins Lin-2 and Lin-7. Trends Biochem. Sci. 25, 317–318.PubMedCrossRefGoogle Scholar
  17. Ehlers, M.D. (2003) Activity level controls postsynaptic composition and signaling via the ubiquitin-proteasome system. Nat. Neurosci. 6, 231–242.PubMedCrossRefGoogle Scholar
  18. Eichmuller, S., Usener, D., Dummer, R., Stein, A., Thiel, D. and Schadendorf, D. (2001) Serological detection of cutaneous T-cell lymphoma-associated antigens. Proc. Natl. Acad. Sci. USA 98, 629–634 Epub 2001 Jan 2009.PubMedCrossRefGoogle Scholar
  19. Englund, C., Fink, A., Lau, C., Pham, D., Daza, R.A., Bulfone, A., Kowalczyk, T. and Hevner, R.F. (2005) Pax6, Tbr2, and Tbr1 are expressed sequentially by radial glia, intermediate progenitor cells, and postmitotic neurons in developing neocortex. J. Neurosci. 25, 247–251.PubMedCrossRefGoogle Scholar
  20. Ethell, I.M. and Yamaguchi, Y. (1999) Cell surface heparan sulfate proteoglycan syndecan-2 induces the maturation of dendritic spines in rat hippocampal neurons. J. Cell Biol. 144, 575–586.PubMedCrossRefGoogle Scholar
  21. Fallon, L., Moreau, F., Croft, B.G., Labib, N., Gu, W.J. and Fon, E.A. (2002) Parkin and CASK/LIN-2 associate via a PDZ-mediated interaction and are co-localized in lipid rafts and postsynaptic densities in brain. J. Biol. Chem. 277, 486–491.PubMedCrossRefGoogle Scholar
  22. Fink, A.J., Englund, C., Daza, R.A., Pham, D., Lau, C., Nivison, M., Kowalczyk, T. and Hevner, R.F. (2006) Development of the deep cerebellar nuclei: transcription factors and cell migration from the rhombic lip. J. Neurosci. 26, 3066–3076.PubMedCrossRefGoogle Scholar
  23. Follesa, P. and Ticku, M.K. (1996) Chronic ethanol-mediated up-regulation of the N-methyl-D-aspartate receptor polypeptide subunits in mouse cortical neurons in culture. J. Biol. Chem. 271, 13297–13299.PubMedCrossRefGoogle Scholar
  24. Gruss, C. and Sogo, J.M. (1992) Chromatin replication. Bioessays 14, 1–8.PubMedCrossRefGoogle Scholar
  25. Hata, Y., Butz, S. and Sudhof, T.C. (1996) CASK: a novel dlg/PSD95 homolog with an N-terminal calmodulin-dependent protein kinase domain identified by interaction with neurexins. J. Neurosci. 16, 2488–2494.PubMedGoogle Scholar
  26. Herkert, M., Rottger, S. and Becker, C.M. (1998) The NMDA receptor subunit NR2B of neonatal rat brain: complex formation and enrichment in axonal growth cones. Eur. J. Neurosci. 10, 1553–1562.PubMedCrossRefGoogle Scholar
  27. Hevner, R.F., Shi, L., Justice, N., Hsueh, Y., Sheng, M., Smiga, S., Bulfone, A., Goffinet, A.M., Campagnoni, A.T. and Rubenstein J.L. (2001) Tbr1 regulates differentiation of the preplate and layer 6. Neuron 29, 353–366.PubMedCrossRefGoogle Scholar
  28. Hoover, K.B. and Bryant, P.J. (2000) The genetics of the protein 4.1 family: organizers of the membrane and cytoskeleton. Curr. Opin. Cell Biol. 12, 229–234.PubMedCrossRefGoogle Scholar
  29. Hsueh, Y.P. and Sheng, M. (1999) Regulated expression and subcellular localization of syndecan heparan sulfate proteoglycans and the syndecan-binding protein CASK/LIN-2 during rat brain development. J. Neurosci. 19, 7415–7425.PubMedGoogle Scholar
  30. Hsueh, Y.P., Wang, T.F., Yang, F.C. and Sheng, M. (2000) Nuclear translocation and transcription regulation by the membrane-associated guanylate kinase CASK/LIN-2. Nature 404, 298–302.PubMedCrossRefGoogle Scholar
  31. Hsueh, Y.P., Roberts, A.M., Volta, M., Sheng, M. and Roberts, R.G. (2001) Bipartite interaction between neurofibromatosis type I protein (neurofibromin) and syndecan transmembrane heparan sulfate proteoglycans. J. Neurosci. 21, 3764–3770.PubMedGoogle Scholar
  32. Hsueh, Y.P., Yang, F.C., Kharazia, V., Naisbitt, S., Cohen, A.R., Weinberg, R.J. and Sheng, M. (1998) Direct interaction of CASK/LIN-2 and syndecan heparan sulfate proteoglycan and their overlapping distribution in neuronal synapses. J. Cell Biol. 142, 139–151.PubMedCrossRefGoogle Scholar
  33. Hung, A.Y. and Sheng, M. (2002) PDZ domains: structural modules for protein complex assembly. J. Biol. Chem. 277, 5699–5702.PubMedCrossRefGoogle Scholar
  34. Irie, M., Hata, Y., Takeuchi, M., Ichtchenko, K., Toyoda, A., Hirao, K., Takai, Y., Rosahl, T.W. and Sudhof, T.C. (1997) Binding of neuroligins to PSD-95. Science 277, 1511–1515.PubMedCrossRefGoogle Scholar
  35. Jo, K., Derin, R., Li, M. and Bredt, D.S. (1999) Characterization of MALS/Velis-1, -2, and -3: a family of mammalian LIN-7 homologs enriched at brain synapses in association with the postsynaptic density-95/NMDA receptor postsynaptic complex. J. Neurosci. 19, 4189–4199.PubMedGoogle Scholar
  36. Kaech, S.M., Whitfield, C.W. and Kim, S.K. (1998) The LIN-2/LIN-7/LIN-10 complex mediates basolateral membrane localization of the C. elegans EGF receptor LET-23 in vulval epithelial cells. Cell 94, 761–771.PubMedCrossRefGoogle Scholar
  37. Kim, E. and Sheng, M. (2004) PDZ domain proteins of synapses. Nat. Rev. Neurosci. 5, 771–781.PubMedCrossRefGoogle Scholar
  38. Kim, E., Niethammer, M., Rothschild, A., Jan, Y.N. and Sheng, M. (1995) Clustering of Shaker-type K+ channels by interaction with a family of membrane-associated guanylate kinases. Nature 378, 85–88.PubMedCrossRefGoogle Scholar
  39. Kornau, H.C., Schenker, L.T., Kennedy, M.B. and Seeburg, P.H. (1995) Domain interaction between NMDA receptor subunits and the postsynaptic density protein PSD-95. Science 269, 1737–1740.PubMedCrossRefGoogle Scholar
  40. Laverty, H.G. and Wilson, J.B. (1998) Murine CASK is disrupted in a sex-linked cleft palate mouse mutant. Genomics 53, 29–41.PubMedCrossRefGoogle Scholar
  41. Lee, S., Fan, S., Makarova, O., Straight, S. and Margolis, B. (2002) A novel and conserved protein-protein interaction domain of mammalian Lin-2/CASK binds and recruits SAP97 to the lateral surface of epithelia. Mol. Cell Biol. 22, 1778–1791.PubMedCrossRefGoogle Scholar
  42. Leonoudakis, D., Conti, L.R., Radeke, C.M., McGuire, L.M. and Vandenberg, C.A. (2004) A multiprotein trafficking complex composed of SAP97, CASK, Veli, and Mint1 is associated with inward rectifier Kir2 potassium channels. J. Biol. Chem. 279, 19051–19063 Epub 12004 Feb 19011.PubMedCrossRefGoogle Scholar
  43. Leonoudakis, D., Conti, L.R., Anderson, S., Radeke, C.M., McGuire, L.M., Adams, M.E., Froehner, S.C., Yates, J.R., 3rd and Vandenberg, C.A. (2004) Protein trafficking and anchoring complexes revealed by proteomic analysis of inward rectifier potassium channel (Kir2.x)-associated proteins. J. Biol. Chem. 279, 22331–22346 Epub 22004 Mar 22315.PubMedCrossRefGoogle Scholar
  44. Levinson, J.N., Chery, N., Huang, K., Wong, T.P., Gerrow, K., Kang, R., Prange, O., Wang, Y.T. and El-Husseini, A. (2005) Neuroligins mediate excitatory and inhibitory synapse formation: involvement of PSD-95 and neurexin-1beta in neuroligin-induced synaptic specificity. J. Biol. Chem. 280, 17312–17319.PubMedCrossRefGoogle Scholar
  45. Lin, C.W., Huang, T.N., Wang, G.S., Kuo, T.Y., Yen, T.Y. and Hsueh, Y.P. (2006) Neural activity- and development-dependent expression and distribution of CASK interacting nucleosome assembly protein in mouse brain. J. Comp. Neurol. 494, 606–619.PubMedCrossRefGoogle Scholar
  46. Liu, L., Wong, T.P., Pozza, M.F., Lingenhoehl, K., Wang, Y., Sheng, M., Auberson, Y.P. and Wang, Y.T. (2004) Role of NMDA receptor subtypes in governing the direction of hippocampal synaptic plasticity. Science 304, 1021–1024.PubMedCrossRefGoogle Scholar
  47. Loftis, J.M. and Janowsky, A. (2003) The N-methyl-D-aspartate receptor subunit NR2B: localization, functional properties, regulation, and clinical implications. Pharmacol. Ther. 97, 55–85.PubMedCrossRefGoogle Scholar
  48. Marfatia, S.M., Morais-Cabral, J.H., Kim, A.C., Byron, O. and Chishti, A.H. (1997) The PDZ domain of human erythrocyte p55 mediates its binding to the cytoplasmic carboxyl terminus of glycophorin C. Analysis of the binding interface by in vitro mutagenesis. J. Biol. Chem. 272, 24191–24197.PubMedCrossRefGoogle Scholar
  49. Mattson, M.P., Dou, P. and Kater, S.B. (1988) Outgrowth-regulating actions of glutamate in isolated hippocampal pyramidal neurons. J. Neurosci. 8, 2087–2100.PubMedGoogle Scholar
  50. Maximov, A. and Bezprozvanny, I. (2002) Synaptic targeting of N-type calcium channels in hippocampal neurons. J. Neurosci. 22, 6939–6952.PubMedGoogle Scholar
  51. Maximov, A., Sudhof, T.C. and Bezprozvanny, I. (1999) Association of neuronal calcium channels with modular adaptor proteins. J. Biol. Chem. 274, 24453–24456.PubMedCrossRefGoogle Scholar
  52. Missler, M., Fernandez-Chacon, R. and Sudhof, T.C. (1998) The making of neurexins. J. Neurochem. 71, 1339–1347.PubMedCrossRefGoogle Scholar
  53. Montgomery, J.M., Zamorano, P.L. and Garner, C.C. (2004) MAGUKs in synapse assembly and function: an emerging view. Cell. Mol. Life Sci. 61, 911–929.PubMedCrossRefGoogle Scholar
  54. Monyer, H., Burnashev, N., Laurie, D.J., Sakmann, B. and Seeburg, P.H. (1994) Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 12, 529–540.PubMedCrossRefGoogle Scholar
  55. Naiche, L.A., Harrelson, Z., Kelly, R.G. and Papaioannou, V.E. (2005) T-box genes in vertebrate development. Annu. Rev. Genet. 39, 219–239.PubMedCrossRefGoogle Scholar
  56. Nam, C.I. and Chen, L. (2005) Postsynaptic assembly induced by neurexin-neuroligin interaction and neurotransmitter. Proc. Natl. Acad. Sci. USA 102, 6137–6142.PubMedCrossRefGoogle Scholar
  57. Nix, S.L., Chishti, A.H., Anderson, J.M. and Walther, Z. (2000) hCASK and hDlg associate in epithelia, and their src homology 3 and guanylate kinase domains participate in both intramolecular and intermolecular interactions. J. Biol. Chem. 275, 41192–41200.PubMedCrossRefGoogle Scholar
  58. Ogawa, M., Miyata, T., Nakajima, K., Yagyu, K., Seike, M., Ikenaka, K., Yamamoto, H. and Mikoshiba, K. (1995) The reeler gene-associated antigen on Cajal-Retzius neurons is a crucial molecule for laminar organization of cortical neurons. Neuron 14, 899–912.PubMedCrossRefGoogle Scholar
  59. Ohno, H., Hirabayashi, S., Kansaku, A., Yao, I., Tajima, M., Nishimura, W., Ohnishi, H., Mashima, H., Fujita, T., Omata, M. and Hata, Y. (2003) Carom: a novel membrane-associated guanylate kinase-interacting protein with two SH3 domains. Oncogene 22, 8422–8431.PubMedCrossRefGoogle Scholar
  60. Olsen, O., Moore, K.A., Fukata, M., Kazuta, T., Trinidad, J.C., Kauer, F.W., Streuli, M., Misawa, H., Burlingame, A.L., Nicoll, R.A. and Bredt, D.S. (2005) Neurotransmitter release regulated by a MALS-liprin-alpha presynaptic complex. J. Cell Biol. 170, 1127–1134.PubMedCrossRefGoogle Scholar
  61. Ozbun, L.L., You, L., Kiang, S., Angdisen, J., Martinez, A. and Jakowlew, S.B. (2001) Identification of differentially expressed nucleolar TGF-beta1 target (DENTT) in human lung cancer cells that is a new member of the TSPY/SET/NAP-1 superfamily. Genomics 73, 179–193.PubMedCrossRefGoogle Scholar
  62. Ozbun, L.L., Martinez, A., Angdisen, J., Umphress, S., Kang, Y., Wang, M., You, M. and Jakowlew, S.B. (2003) Differentially expressed nucleolar TGF-beta1 target (DENTT) in mouse development. Dev. Dyn. 226, 491–511.PubMedCrossRefGoogle Scholar
  63. Portera-Cailliau, C., Price, D.L. and Martin, L.J. (1996) N-methyl-D-aspartate receptor proteins NR2A and NR2B are differentially distributed in the developing rat central nervous system as revealed by subunit-specific antibodies. J. Neurochem. 66, 692–700.PubMedCrossRefGoogle Scholar
  64. Porteus, M.H., Brice, A.E., Bulfone, A., Usdin, T.B., Ciaranello, R.D. and Rubenstein, J.L. (1992) Isolation and characterization of a library of cDNA clones that are preferentially expressed in the embryonic telencephalon. Brain Res. Mol. Brain Res. 12, 7–22.PubMedCrossRefGoogle Scholar
  65. Rao, A. and Craig, A.M. (1997) Activity regulates the synaptic localization of the NMDA receptor in hippocampal neurons. Neuron 19, 801–812.PubMedCrossRefGoogle Scholar
  66. Rice, D.S. and Curran, T. (2001) Role of the reelin signaling pathway in central nervous system development. Annu. Rev. Neurosci. 24, 1005–1039.PubMedCrossRefGoogle Scholar
  67. Riefler, G.M. and Firestein, B.L. (2001) Binding of neuronal nitric-oxide synthase (nNOS) to carboxyl-terminal-binding protein (CtBP) changes the localization of CtBP from the nucleus to the cytosol: a novel function for targeting by the PDZ domain of nNOS. J. Biol. Chem. 276, 48262–48268.PubMedGoogle Scholar
  68. Setou, M., Nakagawa, T., Seog, D.H. and Hirokawa, N. (2000) Kinesin superfamily motor protein KIF17 and mLin-10 in NMDA receptor-containing vesicle transport. Science 288, 1796–1802.PubMedCrossRefGoogle Scholar
  69. Sheng, M. and Sala, C. (2001) PDZ domains and the organization of supramolecular complexes. Annu. Rev. Neurosci. 24, 1–29.PubMedCrossRefGoogle Scholar
  70. Song, J.Y., Ichtchenko, K., Sudhof, T.C. and Brose, N. (1999) Neuroligin 1 is a postsynaptic cell-adhesion molecule of excitatory synapses. Proc. Natl. Acad. Sci. USA 96, 1100–1105.PubMedCrossRefGoogle Scholar
  71. Songyang, Z., Fanning, A.S., Fu, C., Xu, J., Marfatia, S.M., Chishti, A.H., Crompton, A., Chan, A.C., Anderson, J.M. and Cantley, L.C. (1997) Recognition of unique carboxyl-terminal motifs by distinct PDZ domains. Science 275, 73–77.PubMedCrossRefGoogle Scholar
  72. Szabo, S.J., Kim, S.T., Costa, G.L., Zhang, X., Fathman, C.G. and Glimcher, L.H. (2000) A novel transcription factor, T-bet, directs Th1 lineage commitment. Cell 100, 655–669.PubMedCrossRefGoogle Scholar
  73. Szabo, S.J., Sullivan, B.M., Stemmann, C., Satoskar, A.R., Sleckman, B.P. and Glimcher, L.H. (2002) Distinct effects of T-bet in TH1 lineage commitment and IFN-gamma production in CD4 and CD8 T cells. Science 295, 338–342.PubMedCrossRefGoogle Scholar
  74. Tabuchi, K., Biederer, T., Butz, S. and Sudhof, T.C. (2002) CASK participates in alternative tripartite complexes in which Mint 1 competes for binding with caskin 1, a novel CASK-binding protein. J. Neurosci. 22, 4264–4273.PubMedGoogle Scholar
  75. Tissir, F. and Goffinet, A.M. (2003) Reelin and brain development. Nat. Rev. Neurosci. 4, 496–505.PubMedCrossRefGoogle Scholar
  76. Wang, G.S., Hong, C.J., Yen, T.Y., Huang, H.Y., Ou, Y., Huang, T.N., Jung, W.G., Kuo, T.Y., Sheng, M., Wang, T.F. and Hsueh, Y.P. (2004a) Transcriptional modification by a CASK-interacting nucleosome assembly protein. Neuron 42, 113–128.CrossRefGoogle Scholar
  77. Wang, T.F., Ding, C.N., Wang, G.S., Luo, S.C., Lin, Y.L., Ruan, Y., Hevner, R., Rubenstein, J.L. and Hsueh, Y.P. (2004b) Identification of Tbr-1/CASK complex target genes in neurons. J. Neurochem. 91, 1483–1492.CrossRefGoogle Scholar
  78. Wenzel, A., Fritschy, J.M., Mohler, H. and Benke, D. (1997) NMDA receptor heterogeneity during postnatal development of the rat brain: differential expression of the NR2A, NR2B, and NR2C subunit proteins. J. Neurochem. 68, 469–478.PubMedCrossRefGoogle Scholar
  79. Willott, E., Balda, M.S., Fanning, A.S., Jameson, B., Van Itallie, C. and Anderson, J.M. (1993) The tight junction protein ZO-1 is homologous to the Drosophila discs-large tumor suppressor protein of septate junctions. Proc. Natl. Acad. Sci. USA 90, 7834–7838.PubMedCrossRefGoogle Scholar
  80. Woods, D.F. and Bryant, P.J. (1991) The discs-large tumor suppressor gene of Drosophila encodes a guanylate kinase homolog localized at septate junctions. Cell 66, 451–464.PubMedCrossRefGoogle Scholar
  81. Yap, C.C., Liang, F., Yamazaki, Y., Muto, Y., Kishida, H., Hayashida, T., Hashikawa, T. and Yano, R. (2003) CIP98, a novel PDZ domain protein, is expressed in the central nervous system and interacts with calmodulin-dependent serine kinase. J. Neurochem. 85, 123–134.PubMedCrossRefGoogle Scholar
  82. Zheng, J.Q., Wan, J.J. and Poo, M.M. (1996) Essential role of filopodia in chemotropic turning of nerve growth cone induced by a glutamate gradient. J. Neurosci. 16, 1140–1149.PubMedGoogle Scholar

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