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Articles, Cellular/Molecular

Actin Tyrosine-53-Phosphorylation in Neuronal Maturation and Synaptic Plasticity

Enni Bertling, Jonas Englund, Rimante Minkeviciene, Mikko Koskinen, Mikael Segerstråle, Eero Castrén, Tomi Taira and Pirta Hotulainen
Journal of Neuroscience 11 May 2016, 36 (19) 5299-5313; https://doi.org/10.1523/JNEUROSCI.2649-15.2016
Enni Bertling
1Neuroscience Center and
4Minerva Institute for Medical Research, 00290 Helsinki, Finland, and
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Jonas Englund
1Neuroscience Center and
2Department of Biosciences, Physiology and Neuroscience, and
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Rimante Minkeviciene
1Neuroscience Center and
4Minerva Institute for Medical Research, 00290 Helsinki, Finland, and
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  • ORCID record for Rimante Minkeviciene
Mikko Koskinen
1Neuroscience Center and
5Department of Neuroscience, Karolinska Institutet, SE-171 77 Stockholm, Sweden
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Mikael Segerstråle
2Department of Biosciences, Physiology and Neuroscience, and
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Eero Castrén
1Neuroscience Center and
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Tomi Taira
3Department of Veterinary Biosciences, University of Helsinki, 00014 Helsinki, Finland,
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Pirta Hotulainen
1Neuroscience Center and
4Minerva Institute for Medical Research, 00290 Helsinki, Finland, and
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Abstract

Rapid reorganization and stabilization of the actin cytoskeleton in dendritic spines enables cellular processes underlying learning, such as long-term potentiation (LTP). Dendritic spines are enriched in exceptionally short and dynamic actin filaments, but the studies so far have not revealed the molecular mechanisms underlying the high actin dynamics in dendritic spines. Here, we show that actin in dendritic spines is dynamically phosphorylated at tyrosine-53 (Y53) in rat hippocampal and cortical neurons. Our findings show that actin phosphorylation increases the turnover rate of actin filaments and promotes the short-term dynamics of dendritic spines. During neuronal maturation, actin phosphorylation peaks at the first weeks of morphogenesis, when dendritic spines form, and the amount of Y53-phosphorylated actin decreases when spines mature and stabilize. Induction of LTP transiently increases the amount of phosphorylated actin and LTP induction is deficient in neurons expressing mutant actin that mimics phosphorylation. Actin phosphorylation provides a molecular mechanism to maintain the high actin dynamics in dendritic spines during neuronal development and to induce fast reorganization of the actin cytoskeleton in synaptic plasticity. In turn, dephosphorylation of actin is required for the stabilization of actin filaments that is necessary for proper dendritic spine maturation and LTP maintenance.

SIGNIFICANCE STATEMENT Dendritic spines are small protrusions from neuronal dendrites where the postsynaptic components of most excitatory synapses reside. Precise control of dendritic spine morphology and density is critical for normal brain function. Accordingly, aberrant spine morphology is linked to many neurological diseases. The actin cytoskeleton is a structural element underlying the proper morphology of dendritic spines. Therefore, defects in the regulation of the actin cytoskeleton in neurons have been implicated in neurological diseases. Here, we revealed a novel mechanism for regulating neuronal actin cytoskeleton that explains the specific organization and dynamics of actin in spines. The better we understand the regulation of the dendritic spine morphology, the better we understand what goes wrong in neurological diseases.

  • actin cytoskeleton
  • dendritic spines
  • LTP
  • phosphorylation
  • spinogenesis
  • synaptic plasticity
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The Journal of Neuroscience: 36 (19)
Journal of Neuroscience
Vol. 36, Issue 19
11 May 2016
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Actin Tyrosine-53-Phosphorylation in Neuronal Maturation and Synaptic Plasticity
Enni Bertling, Jonas Englund, Rimante Minkeviciene, Mikko Koskinen, Mikael Segerstråle, Eero Castrén, Tomi Taira, Pirta Hotulainen
Journal of Neuroscience 11 May 2016, 36 (19) 5299-5313; DOI: 10.1523/JNEUROSCI.2649-15.2016

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Actin Tyrosine-53-Phosphorylation in Neuronal Maturation and Synaptic Plasticity
Enni Bertling, Jonas Englund, Rimante Minkeviciene, Mikko Koskinen, Mikael Segerstråle, Eero Castrén, Tomi Taira, Pirta Hotulainen
Journal of Neuroscience 11 May 2016, 36 (19) 5299-5313; DOI: 10.1523/JNEUROSCI.2649-15.2016
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Keywords

  • actin cytoskeleton
  • dendritic spines
  • LTP
  • phosphorylation
  • spinogenesis
  • synaptic plasticity

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