Complexity of dendritic SER increases at enlarging synapses during LTP

Abstract

Smooth endoplasmic reticulum (SER) forms a membranous network that extends throughout neurons. SER regulates intracellular calcium and the posttranslational modification and trafficking of membrane and proteins. As the structure of dendritic SER shifts from a tubular to a more complex, branched form, the movement of membrane cargo slows and delivery to nearby spines increases. Here we discovered changes in the structural complexity of SER that have important functional implications during long-term potentiation (LTP) in adult rat hippocampus. By 2 hours after the induction of LTP with theta-burst stimulation, synapse enlargement was greatest on spines that contained SER. More spines had an elaborate spine apparatus than a simple tubule of SER. The SER in dendritic shafts became more complex beneath spines with both polyribosomes and SER, and less complex along aspiny dendritic regions. The findings suggest that local changes in dendritic SER support enhanced growth of specific synapses during LTP.

Intracellular Ca2+Release and Synaptic Plasticity: A Tale of Many Stores

“…The ER permeates the dendritic arbor and a fraction of dendritic spines (10%-50% depending on region) in mammalian neurons (Chirillo and others 2015; Holbro and others 2009; Jedlicka and Deller 2017; Ng and others 2014; Spacek and Harris 1997). It is typically found in spines with large spine heads where it can take the form of a stacked structure known as the spine apparatus, for which the actin-binding protein synaptopodin is essential (Chirillo and others 2015; Cooney and others 2002; Deller and others 2003; Spacek and Harris 1997).…”

“…The ER permeates the dendritic arbor and a fraction of dendritic spines (10%-50% depending on region) in mammalian neurons (Chirillo and others 2015; Holbro and others 2009; Jedlicka and Deller 2017; Ng and others 2014; Spacek and Harris 1997). It is typically found in spines with large spine heads where it can take the form of a stacked structure known as the spine apparatus, for which the actin-binding protein synaptopodin is essential (Chirillo and others 2015; Cooney and others 2002; Deller and others 2003; Spacek and Harris 1997). The ER is dynamic and its localization is dependent on synaptic activity, with spine ER content being increased by NMDAR and L-type voltage-gated Ca 2+ channel (L-VGCC) activity (Chirillo and others 2015; Dittmer and others 2017; Kucharz and others 2009; Ng and others 2014; Yamazaki and others 2001), and decreased by group I metabotropic glutamate receptor activity (mGluR1 and mGlur5) (Ng and Toresson 2011).…”

Intracellular calcium stores mediate metaplasticity at hippocampal dendritic spines

“…; Chirillo et al . ). Further, recent imaging studies on cultured hippocampal neurons from mice reveal a dynamic picture of the ER distribution in spines (Toresson & Grant, ); ER can undergo rapid growth in individual spine heads on a time scale of minutes, which was shown to be regulated by NMDAR activation (Ng et al .…”

Intracellular calcium stores mediate a synapse-specific form of metaplasticity at hippocampal dendritic spines

“…Here, we consider a synapse-specific form of metaplasticity that may be introduced by Ca 2+ stores associated with the ER in these large dendritic spines. Our investigation is motivated by the observation that larger spines that have ER are associated with stronger synapses and have most likely been potentiated [31][32][33][34] . Further, recent imaging studies on cultured hippocampal neurons from mice reveal a dynamic picture of the ER distribution in spines 35 ; ER can undergo rapid growth in individual spine heads on a timescale of minutes, which was shown to be regulated by NMDAR activation 36 , and accompanies spine enlargement 37,38 .…”