Corrêa, Sônia A. L., Hunter, Christopher J., Palygin, Oleg, Wauters, Sandrine, Martin, Kirsty J., McKenzie, Colin, McKelvey, Kim, Morris, R. G. M. (Richard G. M.), Pankratov, Yuriy, Arthur, J. Simon C. and Frenguelli, Bruno G.. (2012) MSK1 regulates homeostatic and experience-dependent synaptic plasticity. Journal of Neuroscience, Vol.32 (No.38). pp. 13039-13051. ISSN 0270-6474

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Abstract

The ability of neurons to modulate synaptic strength underpins synaptic plasticity, learning and memory, and adaptation to sensory experience. Despite the importance of synaptic adaptation in directing, reinforcing, and revising the behavioral response to environmental influences, the cellular and molecular mechanisms underlying synaptic adaptation are far from clear. Brain-derived neurotrophic factor (BDNF) is a prime initiator of structural and functional synaptic adaptation. However, the signaling cascade activated by BDNF to initiate these adaptive changes has not been elucidated. We have previously shown that BDNF activates mitogen- and stress-activated kinase 1 (MSK1), which regulates gene transcription via the phosphorylation of both CREB and histone H3. Using mice with a kinase-dead knock-in mutation of MSK1, we now show that MSK1 is necessary for the upregulation of synaptic strength in response to environmental enrichment in vivo. Furthermore, neurons from MSK1 kinase-dead mice failed to show scaling of synaptic transmission in response to activity deprivation in vitro, a deficit that could be rescued by reintroduction of wild-type MSK1. We also show that MSK1 forms part of a BDNF-and MAPK-dependent signaling cascade required for homeostatic synaptic scaling, which likely resides in the ability of MSK1 to regulate cell surface GluA1 expression via the induction of Arc/Arg3.1. These results demonstrate that MSK1 is an integral part of a signaling pathway that underlies the adaptive response to synaptic and environmental experience. MSK1 may thus act as a key homeostat in the activity- and experience-dependent regulation of synaptic strength.

Item Type:	Journal Article
Subjects:	Q Science > QP Physiology
Divisions:	Faculty of Science > Life Sciences (2010- )
Library of Congress Subject Headings (LCSH):	Neuroplasticity, Mitogen-activated protein kinases, Neurons -- Physiology
Journal or Publication Title:	Journal of Neuroscience
Publisher:	Society for Neuroscience
ISSN:	0270-6474
Date:	19 September 2012
Volume:	Vol.32
Number:	No.38
Page Range:	pp. 13039-13051
Identification Number:	10.1523/JNEUROSCI.0930-12.2012
Status:	Peer Reviewed
Publication Status:	Published
Access rights to Published version:	Restricted or Subscription Access
Funder:	Medical Research Council (Great Britain) (MRC), Sixth Framework Programme (European Commission) (FP6), Biotechnology and Biological Sciences Research Council (Great Britain) (BBSRC), University of Warwick, GlaxoSmithKline, Wellcome Trust (London, England), Engineering and Physical Sciences Research Council (EPSRC), University of Warwick. Molecular Organisation and Assembly in Cells
References:	Alder J, Thakker-Varia S, Bangasser DA, Kuroiwa M, Plummer MR, Shors TJ, Black IB (2003) Brain-derived neurotrophic factor-induced gene expression reveals novel actions of VGF in hippocampal synaptic plasticity. J Neurosci 23:10800 –10808. Arthur JS (2008) MSK activation and physiological roles. Front Biosci 13:5866 –5879. Arthur JS, Fong AL, Dwyer JM, Davare M, Reese E, Obrietan K, Impey S (2004) Mitogen- and stress-activated protein kinase 1 mediates cAMP response element-binding protein phosphorylation and activation by neurotrophins. J Neurosci 24:4324–4332. Baroncelli L, Braschi C, Spolidoro M, Begenisic T, Sale A, Maffei L (2010) Nurturing brain plasticity: impact of environmental enrichment. Cell Death Differ 17:1092–1103. Be´ïque JC, Na Y, Kuhl D, Worley PF, Huganir RL (2011) Arc-dependent synapse-specific homeostatic plasticity. Proc Natl Acad Sci U S A 108:816–821. Bramham CR, Alme MN, Bittins M, Kuipers SD, Nair RR, Pai B, Panja D, Schubert M, Soule J, Tiron A, Wibrand K (2010) The Arc of synaptic memory. Exp Brain Res 200:125–140. Brami-Cherrier K, Valjent E, Herve´ D, Darragh J, Corvol JC, Pages C, Arthur SJ, Simon AJ, Girault JA, Caboche J (2005) Parsing molecular and behavioral effects of cocaine in mitogen- and stress-activated protein kinase-1-deficient mice. J Neurosci 25:11444 –11454. Butcher GQ, Lee B, Cheng HY, Obrietan K (2005) Light stimulates MSK1 activation in the suprachiasmatic nucleus via a PACAP-ERK/MAP kinase-dependent mechanism. J Neurosci 25:5305–5313. Chandramohan Y, Droste SK, Arthur JS, Reul JM (2008) The forced swimming-induced behavioural immobility response involves histone H3 phospho-acetylation and c-Fos induction in dentate gyrus granule neurons via activation of the N-methyl-D-aspartate/extracellular signalregulated kinase/mitogen- and stress-activated kinase signalling pathway. Eur J Neurosci 27:2701–2713. Chowdhury S, Shepherd JD, Okuno H, Lyford G, Petralia RS, Plath N, Kuhl D, Huganir RL, Worley PF (2006) Arc/Arg3.1 interacts with the endocytic machinery to regulate AMPA receptor trafficking. Neuron 52: 445–459. Chwang WB, Arthur JS, Schumacher A, Sweatt JD (2007) The nuclear kinase mitogen- and stress-activated protein kinase 1 regulates hippocampal chromatin remodeling in memory formation. J Neurosci 27:12732–12742. Citri A, Malenka RC (2008) Synaptic plasticity: multiple forms, functions, and mechanisms. Neuropsychopharmacology 33:18–41. Correˆa SA, Mu¨ller J, Collingridge GL, Marrion NV (2009) Rapid endocytosis provides restricted somatic expression of a K channel in central neurons. J Cell Sci 122:4186–4194. Cowansage KK, LeDoux JE, Monfils MH (2010) Brain-derived neurotrophic factor: a dynamic gatekeeper of neural plasticity. Curr Mol Pharmacol 3:12–29. D’Amato FR, Zanettini C, Sgobio C, Sarli C, Carone V, Moles A, Ammassari- Teule M (2011) Intensification of maternal care by double-mothering boosts cognitive function and hippocampal morphology in the adult offspring. Hippocampus 21:298 –308. Davis GW (2006) Homeostatic control of neural activity: from phenomenology to molecular design. Annu Rev Neurosci 29:307–323. Delaney KR (2010) Loading neurons with dextran-conjugated calcium indicators in intact nervous tissue. Curr Protoc Neurosci 50:2.5.1–2.5.11. Frenguelli BG, Correˆa SA (2012) Regulation and role of MSK in the mammalian brain. In: MSKs (Vermeulen L, Arthur JS, eds). Austin, TX: Landes Bioscience, in press. Gutie`rrez-Mecinas M, Trollope AF, Collins A, Morfett H, Hesketh SA, Kersante´ F, Reul JM (2011) Long-lasting behavioral responses to stress involve a direct interaction of glucocorticoid receptors with ERK1/2-MSK1-Elk-1 signaling. Proc Natl Acad Sci U S A 108:13806–13811. Ho VM, Lee JA, Martin KC (2011) The cell biology of synaptic plasticity. Science 334:623– 628. Holtmaat A, Svoboda K (2009) Experience-dependent structural synaptic plasticity in the mammalian brain. Nat Rev Neurosci 10:647– 658. Hu¨bener M, Bonhoeffer T (2010) Searching for engrams. Neuron 67:363–371. Kerchner GA, Nicoll RA (2008) Silent synapses and the emergence of a postsynaptic mechanism for LTP. Nat Rev Neurosci 9:813– 825. Kessels HW, Malinow R (2009) Synaptic AMPA receptor plasticity and behavior. Neuron 61:340 –350. Markham JA, Greenough WT (2004) Experience-driven brain plasticity: beyond the synapse. Neuron Glia Biol 1:351–363. Martin KJ, Shpiro N, Traynor R, Elliott M, Arthur JS (2011) Comparison of the specificity of Trk inhibitors in recombinant and neuronal assays. Neuropharmacology 61:148 –155. McCoy CE, Campbell DG, Deak M, Bloomberg GB, Arthur JS (2005) MSK1 activity is controlled by multiple phosphorylation sites. Biochem J 387:507–517. McCoy CE, Macdonald A, Morrice NA, Campbell DG, Deak M, Toth R, McIlrath J, Arthur JS (2007) Identification of novel phosphorylation sites in MSK1 by precursor ion scanning MS. Biochem J 402:491–501. McCurry CL, Shepherd JD, Tropea D, Wang KH, Bear MF, Sur M (2010) Loss of Arc renders the visual cortex impervious to the effects of sensory experience or deprivation. Nat Neurosci 13:450–457. Messaoudi E, Kanhema T, Soule´ J, Tiron A, Dagyte G, da Silva B, Bramham CR (2007) Sustained Arc/Arg3.1 synthesis controls long-term potentiation consolidation through regulation of local actin polymerization in the dentate gyrus in vivo. J Neurosci 27:10445–10455. Molna´r E, Baude A, Richmond SA, Patel PB, Somogyi P, McIlhinney RA (1993) Biochemical and immunocytochemical characterization of antipeptide antibodies to a cloned GluR1 glutamate receptor subunit: cellular and subcellular distribution in the rat forebrain. Neuroscience 53: 307–326. Morris RG (2006) Elements of a neurobiological theory of hippocampal function: the role of synaptic plasticity, synaptic tagging and schemas. Eur J Neurosci 23:2829 –2846. Neves G, Cooke SF, Bliss TV (2008) Synaptic plasticity, memory and the hippocampus: a neural network approach to causality. Nat Rev Neurosci 9:65–75. Nithianantharajah J, Hannan AJ (2006) Enriched environments, experiencedependent plasticity and disorders of the nervous system. Nat Rev Neurosci 7:697–709. O’Brien RJ, Kamboj S, Ehlers MD, Rosen KR, Fischbach GD, Huganir RL (1998) Activity-dependent modulation of synaptic AMPA receptor accumulation. Neuron 21:1067–1078. Pankratov YV, Krishtal OA (2003) Distinct quantal features of AMPA and NMDA synaptic currents in hippocampal neurons: implication of glutamate spillover and receptor saturation. Biophys J 85:3375–3387. Pankratov Y, Lalo U, Verkhratsky A, North RA (2007) Quantal release of ATP in mouse cortex. J Gen Physiol 129:257–265. Peebles CL, Yoo J, Thwin MT, Palop JJ, Noebels JL, Finkbeiner S (2010) Arc regulates spine morphology and maintains network stability in vivo. Proc Natl Acad Sci U S A 107:18173–18178. Plath N, Ohana O, Dammermann B, Errington ML, Schmitz D, Gross C, Mao X, Engelsberg A, Mahlke C, Welzl H, Kobalz U, Stawrakakis A, Fernandez E, Waltereit R, Bick-Sander A, Therstappen E, Cooke SF, Blanquet V, Wurst W, Salmen B, et al. (2006) Arc/Arg3.1 is essential for the consolidation of synaptic plasticity and memories. Neuron 52:437– 444. Pozo K, Goda Y (2010) Unraveling mechanisms of homeostatic synaptic plasticity. Neuron 66:337–351. Putignano E, Lonetti G, Cancedda L, Ratto G, Costa M, Maffei L, Pizzorusso T (2007) Developmental downregulation of histone posttranslational modifications regulates visual cortical plasticity. Neuron 53:747–759. Rao VR, Pintchovski SA, Chin J, Peebles CL, Mitra S, Finkbeiner S (2006) AMPA receptors regulate transcription of the plasticity-related immediate-early gene Arc. Nat Neurosci 9:887– 895. Rial Verde EM, Lee-Osbourne J, Worley PF, Malinow R, Cline HT (2006) Increased expression of the immediate-early gene arc/arg3.1 reduces AMPA receptor-mediated synaptic transmission. Neuron 52:461– 474. Richmond SA, Irving AJ, Molna´r E, McIlhinney RA, Michelangeli F, Henley JM, Collingridge GL (1996) Localisation of the glutamate receptor subunit GluR1 on the surface of living and within cultured hippocampal neurones. Neuroscience 75:69–82. Rodriguez A, Ehlenberger DB, Dickstein DL, Hof PR, Wearne SL (2008) Automated three-dimensional detection and shape classification of dendritic spines from fluorescence microscopy images. PLoS One 3:e1997. Rosenzweig MR, Bennett EL (1996) Psychobiology of plasticity: effects of training and experience on brain and behavior. Behav Brain Res 78:57– 65. Roze E, Betuing S, Deyts C, Marcon E, Brami-Cherrier K, Page`s C, Humbert S, Me´rienne K, Caboche J (2008) Mitogen- and stress-activated protein kinase-1 deficiency is involved in expanded-huntingtininduced transcriptional dysregulation and striatal death. FASEB J 22:1083–1093. Rutherford LC, Nelson SB, Turrigiano GG (1998) BDNF has opposite effects on the quantal amplitude of pyramidal neuron and interneuron excitatory synapses. Neuron 21:521–530. Shepherd JD, Bear MF (2011) New views of Arc, a master regulator of synaptic plasticity. Nat Neurosci 14:279 –284. Shepherd JD, Rumbaugh G, Wu J, Chowdhury S, Plath N, Kuhl D, Huganir RL, Worley PF (2006) Arc/Arg3.1 mediates homeostatic synaptic scaling of AMPA receptors. Neuron 52:475– 484. Soloaga A, Thomson S, Wiggin GR, Rampersaud N, Dyson MH, Hazzalin CA, Mahadevan LC, Arthur JS (2003) MSK2 and MSK1 mediate the mitogenand stress-induced phosphorylation of histone H3 and HMG-14. EMBO J 22:2788–2797. TurrigianoGG (2008) The self-tuning neuron: synaptic scaling of excitatory synapses. Cell 135:422– 435. Turrigiano GG, Leslie KR, Desai NS, Rutherford LC, Nelson SB (1998) Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature 391:892– 896. Wearne SL, Rodriguez A, Ehlenberger DB, Rocher AB, Henderson SC, Hof PR (2005) New techniques for imaging, digitization and analysis of threedimensional neural morphology on multiple scales. Neuroscience 136:661–680. Wiggin GR, Soloaga A, Foster JM, Murray-Tait V, Cohen P, Arthur JS (2002) MSK1 and MSK2 are required for the mitogen- and stress-induced phosphorylation of CREB and ATF1 in fibroblasts. Mol Cell Biol 22:2871–2881. Yin Y, Edelman GM, Vanderklish PW (2002) The brain-derived neurotrophic factor enhances synthesis of Arc in synaptoneurosomes. Proc Natl Acad Sci U S A 99:2368 –2373. Ying SW, Futter M, Rosenblum K, Webber MJ, Hunt SP, Bliss TV, Bramham CR (2002) Brain-derived neurotrophic factor induces longterm potentiation in intact adult hippocampus: requirement for ERK activation coupled to CREB and upregulation of Arc synthesis. J Neurosci 22:1532–1540.
URI:	http://wrap.warwick.ac.uk/id/eprint/50278

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