Activation of EphA Receptors Mediates the Recruitment of the Adaptor Protein Slap, Contributing to the Downregulation of N-Methyl-d-Aspartate Receptors

REFERENCES

• Alifragis P, Molnar Z, Parnavelas JG. 2003. Restricted expression of Slap-1 in the rodent cerebral cortex. Gene Expr. Patterns 3:437–440.
   PubMedGoogle Scholar
• Manes G, Bello P, Roche S. 2000. Slap negatively regulates Src mitogenic function but does not revert Src-induced cell morphology changes. Mol. Cell. Biol. 20:3396–3406.
   PubMedGoogle Scholar
• Sosinowski T, Pandey A, Dixit VM, Weiss A. 2000. Src-like adaptor protein (SLAP) is a negative regulator of T cell receptor signaling. J. Exp. Med. 191:463–474.
   PubMedGoogle Scholar
• Myers MD, Dragone LL, Weiss A. 2005. Src-like adaptor protein down-regulates T cell receptor (TCR)-CD3 expression by targeting TCRzeta for degradation. J. Cell Biol. 170:285–294.
   PubMedGoogle Scholar
• Fu AK, Hung KW, Fu WY, Shen C, Chen Y, Xia J, Lai KO, Ip NY. 2011. APC(Cdh1) mediates EphA4-dependent downregulation of AMPA receptors in homeostatic plasticity. Nat. Neurosci. 14:181–189.
   PubMedGoogle Scholar
• Pandey A, Duan H, Dixit VM. 1995. Characterization of a novel Src-like adapter protein that associates with the Eck receptor tyrosine kinase. J. Biol. Chem. 270:19201–19204.
   PubMed Web of Science ®Google Scholar
• Dalva MB, Takasu MA, Lin MZ, Shamah SM, Hu L, Gale NW, Greenberg ME. 2000. EphB receptors interact with NMDA receptors and regulate excitatory synapse formation. Cell 103:945–956.
   PubMed Web of Science ®Google Scholar
• Irie F, Yamaguchi Y. 2004. EPHB receptor signaling in dendritic spine development. Front. Biosci. 9:1365–1373.
   PubMedGoogle Scholar
• Henkemeyer M, Itkis OS, Ngo M, Hickmott PW, Ethell IM. 2003. Multiple EphB receptor tyrosine kinases shape dendritic spines in the hippocampus. J. Cell Biol. 163:1313–1326.
   PubMed Web of Science ®Google Scholar
• Murai KK, Pasquale EB. 2004. Eph receptors, ephrins, and synaptic function. Neuroscientist 10:304–314.
   PubMed Web of Science ®Google Scholar
• Gerlai R. 2001. Eph receptors and neural plasticity. Nat. Rev. Neurosci. 2:205–209.
   PubMedGoogle Scholar
• Henderson JT, Georgiou J, Jia Z, Robertson J, Elowe S, Roder JC, Pawson T. 2001. The receptor tyrosine kinase EphB2 regulates NMDA-dependent synaptic function. Neuron 32:1041–1056.
   PubMedGoogle Scholar
• Contractor A, Rogers C, Maron C, Henkemeyer M, Swanson GT, Heinemann SF. 2002. Trans-synaptic Eph receptor-ephrin signaling in hippocampal mossy fiber LTP. Science 296:1864–1869.
   PubMedGoogle Scholar
• Grunwald IC, Korte M, Adelmann G, Plueck A, Kullander K, Adams RH, Frotscher M, Bonhoeffer T, Klein R. 2004. Hippocampal plasticity requires postsynaptic ephrinBs. Nat. Neurosci. 7:33–40.
   PubMed Web of Science ®Google Scholar
• Calò L, Cinque C, Patane M, Schillaci D, Battaglia G, Melchiorri D, Nicoletti F, Bruno V. 2006. Interaction between ephrins/Eph receptors and excitatory amino acid receptors: possible relevance in the regulation of synaptic plasticity and in the pathophysiology of neuronal degeneration. J. Neurochem. 98:1–10.
   PubMed Web of Science ®Google Scholar
• Takasu MA, Dalva MB, Zigmond RE, Greenberg ME. 2002. Modulation of NMDA receptor-dependent calcium influx and gene expression through EphB receptors. Science 295:491–495.
   PubMed Web of Science ®Google Scholar
• Knöll B, Drescher U. 2002. Ephrin-As as receptors in topographic projections. Trends Neurosci. 25:145–149.
   PubMed Web of Science ®Google Scholar
• Dickson BJ. 2002. Molecular mechanisms of axon guidance. Science 298:1959–1964.
   PubMed Web of Science ®Google Scholar
• Klein R. 2004. Eph/ephrin signaling in morphogenesis, neural development and plasticity. Curr. Opin. Cell Biol. 16:580–589.
   PubMed Web of Science ®Google Scholar
• Martínez A, Soriano E. 2005. Functions of ephrin/Eph interactions in the development of the nervous system: emphasis on the hippocampal system. Brain Res. Brain Res. Rev. 49:211–226.
   PubMed Web of Science ®Google Scholar
• Pasquale EB. 2005. Eph receptor signalling casts a wide net on cell behaviour. Nat. Rev. Mol. Cell Biol. 6:462–475.
   PubMed Web of Science ®Google Scholar
• Pasquale EB. 1997. The Eph family of receptors. Curr. Opin. Cell Biol. 9:608–615.
   PubMedGoogle Scholar
• Kayser MS, Nolt MJ, Dalva MB. 2008. EphB receptors couple dendritic filopodia motility to synapse formation. Neuron 59:56–69.
   PubMed Web of Science ®Google Scholar
• Akaneya Y, Sohya K, Kitamura A, Kimura F, Washburn C, Zhou R, Ninan I, Tsumoto T, Ziff EB. 2010. Ephrin-A5 and EphA5 interaction induces synaptogenesis during early hippocampal development. PLoS One 5:e12486. doi:10.1371/journal.pone.0012486.
   PubMed Web of Science ®Google Scholar
• Murai KK, Nguyen LN, Irie F, Yamaguchi Y, Pasquale EB. 2003. Control of hippocampal dendritic spine morphology through ephrin-A3/EphA4 signaling. Nat. Neurosci. 6:153–160.
   PubMed Web of Science ®Google Scholar
• Carmona MA, Murai KK, Wang L, Roberts AJ, Pasquale EB. 2009. Glial ephrin-A3 regulates hippocampal dendritic spine morphology and glutamate transport. Proc. Natl. Acad. Sci. U. S. A. 106:12524–12529.
   PubMedGoogle Scholar
• Davy A, Gale NW, Murray EW, Klinghoffer RA, Soriano P, Feuerstein C, Robbins SM. 1999. Compartmentalized signaling by GPI-anchored ephrin-A5 requires the Fyn tyrosine kinase to regulate cellular adhesion. Genes Dev. 13:3125–3135.
   PubMed Web of Science ®Google Scholar
• Meima L, Kljavin IJ, Moran P, Shih A, Winslow JW, Caras IW. 1997. AL-1-induced growth cone collapse of rat cortical neurons is correlated with REK7 expression and rearrangement of the actin cytoskeleton. Eur. J. Neurosci. 9:177–188.
   PubMedGoogle Scholar
• Gao WQ, Shinsky N, Armanini MP, Moran P, Zheng JL, Mendoza-Ramirez JL, Phillips HS, Winslow JW, Caras IW. 1998. Regulation of hippocampal synaptic plasticity by the tyrosine kinase receptor, REK7/EphA5, and its ligand, AL-1/Ephrin-A5. Mol. Cell. Neurosci. 11:247–259.
   PubMed Web of Science ®Google Scholar
• Waxman SJ, Kukanich B, Milligan M, Beard WL, Davis EG. 2012. Pharmacokinetics of concurrently administered intravenous lidocaine and flunixin in healthy horses. J. Vet. Pharmacol. Ther. 35:413–416.
   PubMedGoogle Scholar
• Hajós F. 1975. An improved method for the preparation of synaptosomal fractions in high purity. Brain Res. 93:485–489.
   PubMed Web of Science ®Google Scholar
• Chen Y, Stevens B, Chang J, Milbrandt J, Barres BA, Hell JW. 2008. NS21: re-defined and modified supplement B27 for neuronal cultures. J. Neurosci. Methods 171:239–247.
   PubMed Web of Science ®Google Scholar
• Erreger K, Geballe MT, Kristensen A, Chen PE, Hansen KB, Lee CJ, Yuan H, Le P, Lyuboslavsky PN, Micale N, Jorgensen L, Clausen RP, Wyllie DJ, Snyder JP, Traynelis SF. 2007. Subunit-specific agonist activity at NR2A-, NR2B-, NR2C-, and NR2D-containing N-methyl-D-aspartate glutamate receptors. Mol. Pharmacol. 72:907–920.
   PubMedGoogle Scholar
• Chen PE, Geballe MT, Katz E, Erreger K, Livesey MR, O'Toole KK, Le P, Lee CJ, Snyder JP, Traynelis SF, Wyllie DJ. 2008. Modulation of glycine potency in rat recombinant NMDA receptors containing chimeric NR2A/2D subunits expressed in Xenopus laevis oocytes. J. Physiol. 586:227–245.
   PubMedGoogle Scholar
• Wanisch K, Yanez-Munoz RJ. 2009. Integration-deficient lentiviral vectors: a slow coming of age. Mol. Ther. 17:1316–1332.
   PubMed Web of Science ®Google Scholar
• Yáñez-Muñoz RJ, Balaggan KS, MacNeil A, Howe SJ, Schmidt M, Smith AJ, Buch P, MacLaren RE, Anderson PN, Barker SE, Duran Y, Bartholomae C, von Kalle C, Heckenlively JR, Kinnon C, Ali RR, Thrasher AJ. 2006. Effective gene therapy with nonintegrating lentiviral vectors. Nat. Med. 12:348–353.
   PubMed Web of Science ®Google Scholar
• Bolte S, Cordelieres FP. 2006. A guided tour into subcellular colocalization analysis in light microscopy. J. Microsc. 224:213–232.
   PubMed Web of Science ®Google Scholar
• Wagey R, Hu J, Pelech SL, Raymond LA, Krieger C. 2001. Modulation of NMDA-mediated excitotoxicity by protein kinase C. J. Neurochem. 78:715–726.
   PubMedGoogle Scholar
• Cesca F, Baldelli P, Valtorta F, Benfenati F. 2010. The synapsins: key actors of synapse function and plasticity. Prog. Neurobiol. 91:313–348.
   PubMed Web of Science ®Google Scholar
• Yun ME, Johnson RR, Antic A, Donoghue MJ. 2003. EphA family gene expression in the developing mouse neocortex: regional patterns reveal intrinsic programs and extrinsic influence. J. Comp. Neurol. 456:203–216.
   PubMedGoogle Scholar
• Fu AK, Ip NY. 2007. Cyclin-dependent kinase 5 links extracellular cues to actin cytoskeleton during dendritic spine development. Cell Adh. Migr. 1:110–112.
   PubMed Web of Science ®Google Scholar
• Fu CT, Tran T, Sretavan D. 2010. Axonal/glial upregulation of EphB/ephrin-B signaling in mouse experimental ocular hypertension. Invest. Ophthalmol. Vis. Sci. 51:991–1001.
   PubMed Web of Science ®Google Scholar
• O'Brien RJ, Mammen AL, Blackshaw S, Ehlers MD, Rothstein JD, Huganir RL. 1997. The development of excitatory synapses in cultured spinal neurons. J. Neurosci. 17:7339–7350.
   PubMedGoogle Scholar
• Papa M, Bundman MC, Greenberger V, Segal M. 1995. Morphological analysis of dendritic spine development in primary cultures of hippocampal neurons. J. Neurosci. 15:1–11.
   PubMed Web of Science ®Google Scholar
• Gerlai R, Shinsky N, Shih A, Williams P, Winer J, Armanini M, Cairns B, Winslow J, Gao W, Phillips HS. 1999. Regulation of learning by EphA receptors: a protein targeting study. J. Neurosci. 19:9538–9549.
   PubMedGoogle Scholar
• Davis S, Gale NW, Aldrich TH, Maisonpierre PC, Lhotak V, Pawson T, Goldfarb M, Yancopoulos GD. 1994. Ligands for EPH-related receptor tyrosine kinases that require membrane attachment or clustering for activity. Science 266:816–819.
   PubMed Web of Science ®Google Scholar
• Pasquale EB. 2004. Eph-ephrin promiscuity is now crystal clear. Nat. Neurosci. 7:417–418.
   PubMed Web of Science ®Google Scholar
• Flanagan JG, Vanderhaeghen P. 1998. The ephrins and Eph receptors in neural development. Annu. Rev. Neurosci. 21:309–345.
   PubMed Web of Science ®Google Scholar
• Cowan CW, Shao YR, Sahin M, Shamah SM, Lin MZ, Greer PL, Gao S, Griffith EC, Brugge JS, Greenberg ME. 2005. Vav family GEFs link activated Ephs to endocytosis and axon guidance. Neuron 46:205–217.
   PubMed Web of Science ®Google Scholar
• Chen C, Leonard JP. 1996. Protein tyrosine kinase-mediated potentiation of currents from cloned NMDA receptors. J. Neurochem. 67:194–200.
   PubMed Web of Science ®Google Scholar
• Zheng F, Gingrich MB, Traynelis SF, Conn PJ. 1998. Tyrosine kinase potentiates NMDA receptor currents by reducing tonic zinc inhibition. Nat. Neurosci. 1:185–191.
   PubMed Web of Science ®Google Scholar
• Kim HJ, Zou W, Ito Y, Kim SY, Chappel J, Ross FP, Teitelbaum SL. 2010. Src-like adaptor protein regulates osteoclast generation and survival. J. Cell. Biochem. 110:201–209.
   PubMedGoogle Scholar
• Lau A, Tymianski M. 2010. Glutamate receptors, neurotoxicity and neurodegeneration. Pflugers Arch. 460:525–542.
   PubMed Web of Science ®Google Scholar
• Raymond LA, Tingley WG, Blackstone CD, Roche KW, Huganir RL. 1994. Glutamate receptor modulation by protein phosphorylation. J. Physiol. Paris 88:181–192.
   PubMedGoogle Scholar
• Grant ER, Bacskai BJ, Anegawa NJ, Pleasure DE, Lynch DR. 1998. Opposing contributions of NR1 and NR2 to protein kinase C modulation of NMDA receptors. J. Neurochem. 71:1471–1481.
   PubMedGoogle Scholar
• Raymond LA, Moshaver A, Tingley WG, Huganir RL. 1996. Glutamate receptor ion channel properties predict vulnerability to cytotoxicity in a transfected nonneuronal cell line. Mol. Cell. Neurosci. 7:102–115.
   PubMedGoogle Scholar
• Watt AJ, van Rossum MC, MacLeod KM, Nelson SB, Turrigiano GG. 2000. Activity coregulates quantal AMPA and NMDA currents at neocortical synapses. Neuron 26:659–670.
   PubMedGoogle Scholar
• Kato A, Rouach N, Nicoll RA, Bredt DS. 2005. Activity-dependent NMDA receptor degradation mediated by retrotranslocation and ubiquitination. Proc. Natl. Acad. Sci. U. S. A. 102:5600–5605.
   PubMedGoogle Scholar
• Ehlers MD. 2003. Activity level controls postsynaptic composition and signaling via the ubiquitin-proteasome system. Nat. Neurosci. 6:231–242.
   PubMed Web of Science ®Google Scholar
• Wang Y, Ota S, Kataoka H, Kanamori M, Li Z, Band H, Tanaka M, Sugimura H. 2002. Negative regulation of EphA2 receptor by Cbl. Biochem. Biophys. Res. Commun. 296:214–220.
   PubMedGoogle Scholar
• Walker-Daniels J, Riese DJ, Kinch MS. 2002. c-Cbl-dependent EphA2 protein degradation is induced by ligand binding. Mol. Cancer Res. 1:79–87.
   PubMed Web of Science ®Google Scholar
• Dragone LL, Myers MD, White C, Gadwal S, Sosinowski T, Gu H, Weiss A. 2006. Src-like adaptor protein (SLAP) regulates B cell receptor levels in a c-Cbl-dependent manner. Proc. Natl. Acad. Sci. U. S. A. 103:18202–18207.
   PubMedGoogle Scholar
• Dragone LL, Shaw LA, Myers MD, Weiss A. 2009. SLAP, a regulator of immunoreceptor ubiquitination, signaling, and trafficking. Immunol. Rev. 232:218–228.
   PubMedGoogle Scholar
• Kalo MS, Pasquale EB. 1999. Signal transfer by eph receptors. Cell Tissue Res. 298:1–9.
   Google Scholar
• Wang YT, Salter MW. 1994. Regulation of NMDA receptors by tyrosine kinases and phosphatases. Nature 369:233–235.
   PubMed Web of Science ®Google Scholar
• Mulvey CS, Zhang K, Liu WH, Waxman DJ, Bigio IJ. 2011. Wavelength-dependent backscattering measurements for quantitative monitoring of apoptosis, Part 1: early and late spectral changes are indicative of the presence of apoptosis in cell cultures. J. Biomed. Opt. 16:117001. doi:10.1117/1.3644389.
   PubMedGoogle Scholar
• Arunachalam S, Waxman SR. 2011. Grammatical form and semantic context in verb learning. Lang. Learn. Dev. 7:169–184.
   PubMedGoogle Scholar