Developmental regulation of hippocampal long-term depression by cofilin-mediated actin reorganization

ABSTRACT Long lasting synaptic plasticity involves both functional and morphological changes, but how these processes are molecularly linked to achieve coordinated plasticity remains poorly understood. Cofilin is a common target of multiple signaling pathways at the synapse and is required for both functional and spine plasticity, but how it is regulated is unclear. In this study, we investigate whether the involvement of cofilin in plasticity is developmentally regulated by examining the role of cofilin in hippocampal long‐term depression (LTD) in both young (2 weeks) and mature (2 months) mice. We show that both total protein level of cofilin and its activation undergo significant changes as the brain matures, so that although the amount of cofilin decreases significantly in mature mice, its regulation by protein phosphorylation becomes increasingly important. Consistent with these biochemical data, we show that cofilin‐mediated actin reorganization is essential for LTD in mature, but not in young mice. In contrast to cofilin, the GluA2 interactions with NSF and PICK1 appear to be required in both young and mature mice, indicating that AMPAR internalization is a common key mechanism for LTD expression regardless of the developmental stages. These results establish the temporal specificity of cofilin in LTD regulation and suggest that cofilin‐mediated actin reorganization may serve as a key mechanism underlying developmental regulation of synaptic and spine plasticity. This article is part of the Special Issue entitled ‘Ionotropic glutamate receptors’. HIGHLIGHTSThe protein level and activity of cofilin are developmentally regulated.Hippocampal LTD requires cofilin in mature but not in young mice.Hippocampal LTD requires GluA2 interactions with NSF and PICK1 in both young and mature mice.

[1]  E. Nishida,et al.  Cofilin phosphorylation by LIM-kinase 1 and its role in Rac-mediated actin reorganization , 1998, Nature.

[2]  R. Nicoll,et al.  AMPA Receptor Trafficking at Excitatory Synapses , 2003, Neuron.

[3]  J. Mellor,et al.  PICK1 inhibition of the Arp2/3 complex controls dendritic spine size and synaptic plasticity , 2011, The EMBO journal.

[4]  Y. Goda,et al.  Actin in action: the interplay between the actin cytoskeleton and synaptic efficacy , 2008, Nature Reviews Neuroscience.

[5]  G. Collingridge,et al.  NSF Binding to GluR2 Regulates Synaptic Transmission , 1998, Neuron.

[6]  Jurgen Müller,et al.  The MK2/3 cascade regulates AMPAR trafficking and cognitive flexibility , 2014, Nature Communications.

[7]  G. Collingridge,et al.  The Small GTPase Arf1 Modulates Arp2/3-Mediated Actin Polymerization via PICK1 to Regulate Synaptic Plasticity , 2013, Neuron.

[8]  G. Collingridge,et al.  Surface Expression of AMPA Receptors in Hippocampal Neurons Is Regulated by an NSF-Dependent Mechanism , 1999, Neuron.

[9]  Z. Bashir,et al.  Induction of LTD in the adult hippocampus by the synaptic activation of AMPA/kainate and metabotropic glutamate receptors , 1999, Neuropharmacology.

[10]  Zhengping Jia,et al.  Regulation of hippocampal long-term potentiation by p21-activated protein kinase 1 (PAK1) , 2009, Neuropharmacology.

[11]  Liqun Luo,et al.  Actin cytoskeleton regulation in neuronal morphogenesis and structural plasticity. , 2002, Annual review of cell and developmental biology.

[12]  P. Caroni,et al.  Regulation of actin dynamics through phosphorylation of cofilin by LIM-kinase , 1998, Nature.

[13]  Zhengping Jia,et al.  Molecular mechanisms coordinating functional and morphological plasticity at the synapse: role of GluA2/N-cadherin interaction-mediated actin signaling in mGluR-dependent LTD. , 2013, Cellular signalling.

[14]  Zhengping Jia,et al.  Regulation of Spine Morphology and Synaptic Function by LIMK and the Actin Cytoskeleton , 2003, Reviews in the neurosciences.

[15]  J. Bamburg Proteins of the ADF/cofilin family: essential regulators of actin dynamics. , 1999, Annual review of cell and developmental biology.

[16]  Chris J. McBain,et al.  The Role of the GluR2 Subunit in AMPA Receptor Function and Synaptic Plasticity , 2007, Neuron.

[17]  R. Malenka,et al.  AMPA receptor trafficking and synaptic plasticity. , 2002, Annual review of neuroscience.

[18]  Jinsong Meng,et al.  Regulation of ADF/cofilin phosphorylation and synaptic function by LIM-kinase , 2004, Neuropharmacology.

[19]  Andreas Lüthi,et al.  Hippocampal LTD Expression Involves a Pool of AMPARs Regulated by the NSF–GluR2 Interaction , 1999, Neuron.

[20]  Jinsong Meng,et al.  Abnormal Long-Lasting Synaptic Plasticity and Cognition in Mice Lacking the Mental Retardation Gene Pak3 , 2005, The Journal of Neuroscience.

[21]  Zhengping Jia,et al.  A critical role of Rho-kinase ROCK2 in the regulation of spine and synaptic function , 2009, Neuropharmacology.

[22]  Y. Goshima,et al.  Phosphorylation of cofilin by LIM-kinase is necessary for semaphorin 3A-induced growth cone collapse , 2001, Nature Neuroscience.

[23]  Z. Bashir,et al.  Different forms of LTD in the CA1 region of the hippocampus: role of age and stimulus protocol , 2000, The European journal of neuroscience.

[24]  J. Bamburg,et al.  ADF/cofilin: a functional node in cell biology. , 2010, Trends in cell biology.

[25]  R. Huganir,et al.  Clustering of AMPA Receptors by the Synaptic PDZ Domain–Containing Protein PICK1 , 1999, Neuron.

[26]  J. Macdonald,et al.  Abnormal Spine Morphology and Enhanced LTP in LIMK-1 Knockout Mice , 2002, Neuron.

[27]  G. Collingridge,et al.  Receptor trafficking and synaptic plasticity , 2004, Nature Reviews Neuroscience.

[28]  T. Bliss,et al.  A synaptic model of memory: long-term potentiation in the hippocampus , 1993, Nature.

[29]  R. Huganir,et al.  Glutamate Receptor Subunit 2 Serine 880 Phosphorylation Modulates Synaptic Transmission and Mediates Plasticity in CA1 Pyramidal Cells , 2003, The Journal of Neuroscience.

[30]  Mark von Zastrow,et al.  Role of AMPA Receptor Cycling in Synaptic Transmission and Plasticity , 1999, Neuron.

[31]  Yu Tian Wang,et al.  Clathrin Adaptor AP2 and NSF Interact with Overlapping Sites of GluR2 and Play Distinct Roles in AMPA Receptor Trafficking and Hippocampal LTD , 2002, Neuron.

[32]  Mriganka Sur,et al.  Structural and Molecular Remodeling of Dendritic Spine Substructures during Long-Term Potentiation , 2014, Neuron.

[33]  G. Collingridge,et al.  Long-term depression in the CNS , 2010, Nature Reviews Neuroscience.

[34]  M. Giustetto,et al.  Learning, AMPA receptor mobility and synaptic plasticity depend on n‐cofilin‐mediated actin dynamics , 2010, The EMBO journal.

[35]  Young Ho Suh,et al.  An Essential Role for PICK1 in NMDA Receptor-Dependent Bidirectional Synaptic Plasticity , 2008, Neuron.

[36]  G. Collingridge,et al.  Metabotropic Glutamate Receptor-Mediated LTD Involves Two Interacting Ca2+ Sensors, NCS-1 and PICK1 , 2008, Neuron.

[37]  R. Huganir,et al.  Interaction of the AMPA receptor subunit GluR2/3 with PDZ domains regulates hippocampal long-term depression , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[38]  O. Snead,et al.  LIMK1 Regulates Long-Term Memory and Synaptic Plasticity via the Transcriptional Factor CREB , 2015, Molecular and Cellular Biology.

[39]  L. Van Aelst,et al.  The role of the Rho GTPases in neuronal development. , 2005, Genes & development.

[40]  G. Collingridge,et al.  PDZ Proteins Interacting with C-Terminal GluR2/3 Are Involved in a PKC-Dependent Regulation of AMPA Receptors at Hippocampal Synapses , 2000, Neuron.

[41]  Bernardo L Sabatini,et al.  Anatomical and physiological plasticity of dendritic spines. , 2007, Annual review of neuroscience.

[42]  O. Bernard Lim kinases, regulators of actin dynamics. , 2007, The international journal of biochemistry & cell biology.

[43]  M. Bear,et al.  LTP and LTD An Embarrassment of Riches , 2004, Neuron.

[44]  J. Bourne,et al.  Balancing structure and function at hippocampal dendritic spines. , 2008, Annual review of neuroscience.

[45]  Mu-ming Poo,et al.  Shrinkage of Dendritic Spines Associated with Long-Term Depression of Hippocampal Synapses , 2004, Neuron.

[46]  Christian Lüscher,et al.  Group 1 mGluR-Dependent Synaptic Long-Term Depression: Mechanisms and Implications for Circuitry and Disease , 2010, Neuron.

[47]  Ryohei Yasuda,et al.  Biochemical Computation for Spine Structural Plasticity , 2015, Neuron.

[48]  M. Rust ADF/cofilin: a crucial regulator of synapse physiology and behavior , 2015, Cellular and Molecular Life Sciences.

[49]  R. Huganir,et al.  The cell biology of synaptic plasticity: AMPA receptor trafficking. , 2007, Annual review of cell and developmental biology.

[50]  R. Huganir,et al.  Interaction of the N-Ethylmaleimide–Sensitive Factor with AMPA Receptors , 1998, Neuron.

[51]  D. Pak,et al.  Neuroligin 1 regulates spines and synaptic plasticity via LIMK1/cofilin-mediated actin reorganization , 2016, The Journal of cell biology.

[52]  Zhengping Jia,et al.  p21-Activated Kinases 1 and 3 Control Brain Size through Coordinating Neuronal Complexity and Synaptic Properties , 2010, Molecular and Cellular Biology.

[53]  G. Collingridge,et al.  A characterisation of long‐term depression induced by metabotropic glutamate receptor activation in the rat hippocampus in vitro , 2001, The Journal of physiology.

[54]  Yu Zhang,et al.  Synaptic Transmission and Plasticity in the Absence of AMPA Glutamate Receptor GluR2 and GluR3 , 2003, Neuron.

[55]  Joseph E LeDoux,et al.  Structural plasticity and memory , 2004, Nature Reviews Neuroscience.

[56]  J. Rizo,et al.  Calcium Binding to PICK1 Is Essential for the Intracellular Retention of AMPA Receptors Underlying Long-Term Depression , 2010, The Journal of Neuroscience.

[57]  Emma L. Jenkins,et al.  Inhibition of Arp2/3-mediated actin polymerization by PICK1 regulates neuronal morphology and AMPA receptor endocytosis , 2008, Nature Cell Biology.

[58]  H. C. Hartzell,et al.  ADF/Cofilin-Mediated Actin Dynamics Regulate AMPA Receptor Trafficking during Synaptic Plasticity , 2010, Nature Neuroscience.

[59]  M. Passafaro,et al.  GluA2 (GluR2) Regulates Metabotropic Glutamate Receptor-Dependent Long-Term Depression through N-Cadherin-Dependent and Cofilin-Mediated Actin Reorganization , 2011, The Journal of Neuroscience.

[60]  R. Malenka,et al.  Differential roles for NSF and GRIP/ABP in AMPA receptor cycling , 2002, Proceedings of the National Academy of Sciences of the United States of America.