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Nerve growth factor (NGF) regulates activity of nuclear factor of activated T-cells (NFAT) in neurons via the phosphatidylinositol 3-kinase (PI3K)-Akt-glycogen synthase kinase 3β (GSK3β) pathway
Journal article   Open access   Peer reviewed

Nerve growth factor (NGF) regulates activity of nuclear factor of activated T-cells (NFAT) in neurons via the phosphatidylinositol 3-kinase (PI3K)-Akt-glycogen synthase kinase 3β (GSK3β) pathway

Man-Su Kim, Leonid P Shutov, Aswini Gnanasekaran, Zhihong Lin, Jacob E Rysted, Jason D Ulrich and Yuriy M Usachev
The Journal of biological chemistry, Vol.289(45), pp.31349-31360
11/07/2014
DOI: 10.1074/jbc.M114.587188
PMCID: PMC4223335
PMID: 25231981
url
https://doi.org/10.1074/jbc.M114.587188View
Published (Version of record) Open Access

Abstract

The Ca(2+)/calcineurin-dependent transcription factor nuclear factor of activated T-cells (NFAT) plays an important role in regulating many neuronal functions, including excitability, axonal growth, synaptogenesis, and neuronal survival. NFAT can be activated by action potential firing or depolarization that leads to Ca(2+)/calcineurin-dependent dephosphorylation of NFAT and its translocation to the nucleus. Recent data suggest that NFAT and NFAT-dependent functions in neurons can also be potently regulated by NGF and other neurotrophins. However, the mechanisms of NFAT regulation by neurotrophins are not well understood. Here, we show that in dorsal root ganglion sensory neurons, NGF markedly facilitates NFAT-mediated gene expression induced by mild depolarization. The effects of NGF were not associated with changes in [Ca(2+)]i and were independent of phospholipase C activity. Instead, the facilitatory effect of NGF depended on activation of the PI3K/Akt pathway downstream of the TrkA receptor and on inhibition of glycogen synthase kinase 3β (GSK3β), a protein kinase known to phosphorylate NFAT and promote its nuclear export. Knockdown or knockout of NFATc3 eliminated this facilitatory effect. Simultaneous monitoring of EGFP-NFATc3 nuclear translocation and [Ca(2+)]i changes in dorsal root ganglion neurons indicated that NGF slowed the rate of NFATc3 nuclear export but did not affect its nuclear import rate. Collectively, our data suggest that NGF facilitates depolarization-induced NFAT activation by stimulating PI3K/Akt signaling, inactivating GSK3β, and thereby slowing NFATc3 export from the nucleus. We propose that NFAT serves as an integrator of neurotrophin action and depolarization-driven calcium signaling to regulate neuronal gene expression.
Animals, Newborn Cell Line Phosphorylation Nerve Growth Factor - metabolism Signal Transduction Calcium - metabolism NFATC Transcription Factors - metabolism Gene Expression Regulation Rats Glycogen Synthase Kinase 3 beta Phosphatidylinositol 3-Kinases - metabolism Glycogen Synthase Kinase 3 - metabolism Rats, Sprague-Dawley Animals Cell Nucleus - metabolism Receptor, trkA - metabolism Mice Mice, Inbred BALB C Neurons - metabolism Active Transport, Cell Nucleus Proto-Oncogene Proteins c-akt - metabolism Genes, Reporter

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