Abstract
Presynaptic neuronal activity requires the localization of thousands of proteins that are typically synthesized in the soma and transported to nerve terminals. Local translation for some dendritic proteins occurs, but local translation in mammalian presynaptic nerve terminals is difficult to demonstrate. Here, we show an essential ribosomal component, 5.8S rRNA, at a glutamatergic nerve terminal in the mammalian brain. We also show active translation in nerve terminals, in situ, in brain slices demonstrating ongoing presynaptic protein synthesis in the mammalian brain. Shortly after inhibiting translation, the presynaptic terminal exhibits increased spontaneous release, an increased paired pulse ratio, an increased vesicle replenishment rate during stimulation trains, and a reduced initial probability of release. The rise and decay rates of postsynaptic responses were not affected. We conclude that ongoing protein synthesis can limit excessive vesicle release which reduces the vesicle replenishment rate, thus conserving the energy required for maintaining synaptic transmission.
Highlights
Synaptic transmission requires the synthesis, localization, interaction and ongoing replenishment of thousands of pre- and postsynaptic proteins (Witzmann et al, 2005; Gonzalez-Lozano et al, 2016; Loh et al, 2016)
We have shown that 5.8S ribosomal RNA (rRNA), a major component of ribosomes, is present in the presynaptic terminal at the calyx of Held synapse
This provides further evidence that presynaptic ribosomal components are present in established mammalian central nervous system (CNS) nerve terminals (Younts et al, 2016) in addition to developing neurites and axons (Taylor et al, 2013; Batista et al, 2017)
Summary
Synaptic transmission requires the synthesis, localization, interaction and ongoing replenishment of thousands of pre- and postsynaptic proteins (Witzmann et al, 2005; Gonzalez-Lozano et al, 2016; Loh et al, 2016). The highly structured and polarized morphology of neurons, with axons and dendrites that can project long distances, creates a unique challenge to maintain sufficient levels of numerous necessary proteins at distant locations (Alvarez et al, 2000; Maday et al, 2014; Tasdemir-Yilmaz and Segal, 2016) These remote regions need to rapidly modify the magnitude and duration of their responses, which can require changes in pre- and postsynaptic protein expression levels. RNA based mechanisms have been discovered that respond to extrinsic signals that affect postsynaptic local translation in dendrites, providing a mechanism to modify or maintain activity at specific regions (LiuYesucevitz et al, 2011; Yoon et al, 2016) This is possible due to the targeting of coding and noncoding RNA (Vo et al, 2010) with RNA binding proteins, and the presence of ribosomes that are located in, or moved to, specific neuronal regions or compartments (Ostroff et al, 2002). The role of local translation in resting and sustained levels of synaptic transmission is a major issue of interest
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