Role of the Endoplasmic Reticulum in Synaptic Transmission

Overview

Journal Curr Opin Neurobiol

Specialties Biology
Neurology

Date 2022 Apr 8

PMID 35395547

Authors

Natali L Chanaday

Ege T Kavalali

Affiliations

Soon will be listed here.

Abstract

Neurons possess a complex morphology spanning long distances and a large number of subcellular specializations such as presynaptic terminals and dendritic spines. This structural complexity is essential for maintenance of synaptic junctions and associated electrical as well as biochemical signaling events. Given the structural and functional complexity of neurons, neuronal endoplasmic reticulum is emerging as a key regulator of neuronal function, in particular synaptic signaling. Neuronal endoplasmic reticulum mediates calcium signaling, calcium and lipid homeostasis, vesicular trafficking, and proteostasis events that underlie autonomous functions of numerous subcellular compartments. However, based on its geometric complexity spanning the whole neuron, endoplasmic reticulum also integrates the activity of these autonomous compartments across the neuron and coordinates their interactions with the soma. In this article, we review recent work regarding neuronal endoplasmic reticulum function and its relationship to neurotransmission and plasticity.

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References

Terasaki M, Slater N, Fein A, Schmidek A, Reese T . Continuous network of endoplasmic reticulum in cerebellar Purkinje neurons. Proc Natl Acad Sci U S A. 1994; 91(16):7510-4. PMC: 44431. DOI: 10.1073/pnas.91.16.7510. View

Deller T, Korte M, Chabanis S, Drakew A, Schwegler H, Stefani G . Synaptopodin-deficient mice lack a spine apparatus and show deficits in synaptic plasticity. Proc Natl Acad Sci U S A. 2003; 100(18):10494-9. PMC: 193589. DOI: 10.1073/pnas.1832384100. View

Reese A, Kavalali E . Spontaneous neurotransmission signals through store-driven Ca(2+) transients to maintain synaptic homeostasis. Elife. 2015; 4. PMC: 4534843. DOI: 10.7554/eLife.09262. View

Krivoi I, Petrov A . Cholesterol and the Safety Factor for Neuromuscular Transmission. Int J Mol Sci. 2019; 20(5). PMC: 6429197. DOI: 10.3390/ijms20051046. View

Patel J, Witkovsky P, Avshalumov M, Rice M . Mobilization of calcium from intracellular stores facilitates somatodendritic dopamine release. J Neurosci. 2009; 29(20):6568-79. PMC: 2892889. DOI: 10.1523/JNEUROSCI.0181-09.2009. View

Kirmiz M, Palacio S, Thapa P, King A, Sack J, Trimmer J . Remodeling neuronal ER-PM junctions is a conserved nonconducting function of Kv2 plasma membrane ion channels. Mol Biol Cell. 2018; 29(20):2410-2432. PMC: 6233057. DOI: 10.1091/mbc.E18-05-0337. View

Wild A, Sinnen B, Dittmer P, Kennedy M, Sather W, DellAcqua M . Synapse-to-Nucleus Communication through NFAT Is Mediated by L-type Ca Channel Ca Spike Propagation to the Soma. Cell Rep. 2019; 26(13):3537-3550.e4. PMC: 6521872. DOI: 10.1016/j.celrep.2019.03.005. View

Pchitskaya E, Kraskovskaya N, Chernyuk D, Popugaeva E, Zhang H, Vlasova O . Stim2-Eb3 Association and Morphology of Dendritic Spines in Hippocampal Neurons. Sci Rep. 2017; 7(1):17625. PMC: 5732248. DOI: 10.1038/s41598-017-17762-8. View

Maneshi M, Toth A, Ishii T, Hori K, Tsujikawa S, Shum A . Orai1 Channels Are Essential for Amplification of Glutamate-Evoked Ca Signals in Dendritic Spines to Regulate Working and Associative Memory. Cell Rep. 2020; 33(9):108464. PMC: 7832685. DOI: 10.1016/j.celrep.2020.108464. View

10.

Pivovarova N, Leapman R, Buchanan R, Reese T, Andrews S . Activity-dependent calcium sequestration in dendrites of hippocampal neurons in brain slices. J Neurosci. 1997; 17(22):8729-38. PMC: 6573076. View

11.

Szikra T, Cusato K, Thoreson W, Barabas P, Bartoletti T, Krizaj D . Depletion of calcium stores regulates calcium influx and signal transmission in rod photoreceptors. J Physiol. 2008; 586(20):4859-75. PMC: 2614069. DOI: 10.1113/jphysiol.2008.160051. View

12.

Rahbek-Clemmensen T, Lycas M, Erlendsson S, Eriksen J, Apuschkin M, Vilhardt F . Super-resolution microscopy reveals functional organization of dopamine transporters into cholesterol and neuronal activity-dependent nanodomains. Nat Commun. 2017; 8(1):740. PMC: 5622129. DOI: 10.1038/s41467-017-00790-3. View

13.

Dason J, Smith A, Marin L, Charlton M . Cholesterol and F-actin are required for clustering of recycling synaptic vesicle proteins in the presynaptic plasma membrane. J Physiol. 2013; 592(4):621-33. PMC: 3934705. DOI: 10.1113/jphysiol.2013.265447. View

14.

Spacek J, Harris K . Three-dimensional organization of smooth endoplasmic reticulum in hippocampal CA1 dendrites and dendritic spines of the immature and mature rat. J Neurosci. 1997; 17(1):190-203. PMC: 6793680. View

15.

Castellano-Munoz M, Schnee M, Ricci A . Calcium-induced calcium release supports recruitment of synaptic vesicles in auditory hair cells. J Neurophysiol. 2015; 115(1):226-39. PMC: 4760492. DOI: 10.1152/jn.00559.2015. View

16.

Lindhout F, Cao Y, Kevenaar J, Bodzeta A, Stucchi R, Boumpoutsari M . VAP-SCRN1 interaction regulates dynamic endoplasmic reticulum remodeling and presynaptic function. EMBO J. 2019; 38(20):e101345. PMC: 6792018. DOI: 10.15252/embj.2018101345. View

17.

Stavoe A, Holzbaur E . Autophagy in Neurons. Annu Rev Cell Dev Biol. 2019; 35:477-500. PMC: 6996145. DOI: 10.1146/annurev-cellbio-100818-125242. View

18.

Wei D, Mei Y, Xia J, Hu H . Orai1 and Orai3 Mediate Store-Operated Calcium Entry Contributing to Neuronal Excitability in Dorsal Root Ganglion Neurons. Front Cell Neurosci. 2018; 11:400. PMC: 5742109. DOI: 10.3389/fncel.2017.00400. View

19.

Timofeeva Y, Volynski K . Calmodulin as a major calcium buffer shaping vesicular release and short-term synaptic plasticity: facilitation through buffer dislocation. Front Cell Neurosci. 2015; 9:239. PMC: 4486835. DOI: 10.3389/fncel.2015.00239. View

20.

Horvath P, Chanaday N, Alten B, Kavalali E, Monteggia L . A subthreshold synaptic mechanism regulating BDNF expression and resting synaptic strength. Cell Rep. 2021; 36(5):109467. PMC: 8371576. DOI: 10.1016/j.celrep.2021.109467. View