A central role of the endoplasmic reticulum in the cell emerges from its functional contact sites with multiple organell
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Cellular and Molecular Life Sciences
REVIEW
A central role of the endoplasmic reticulum in the cell emerges from its functional contact sites with multiple organelles Celso Almeida1 · Margarida D. Amaral1 Received: 3 February 2020 / Revised: 30 March 2020 / Accepted: 6 April 2020 © Springer Nature Switzerland AG 2020
Abstract Early eukaryotic cells emerged from the compartmentalization of metabolic processes into specific organelles through the development of an endomembrane system (ES), a precursor of the endoplasmic reticulum (ER), which was essential for their survival. Recently, substantial evidence emerged on how organelles communicate among themselves and with the plasma membrane (PM) through contact sites (CSs). From these studies, the ER—the largest single structure in eukaryotic cells—emerges as a central player communicating with all organelles to coordinate cell functions and respond to external stimuli to maintain cellular homeostasis. Herein we review the functional insights into the ER–CSs with other organelles in a physiological perspective. We hypothesize that, in addition to the primitive role by the ES in the appearance of protoeukaryotes, its successor—the ER—emerges as the key coordinator of inter-organelle/PM communication. The ER thus appears to be the ‘maestro’ driving eukaryotic cell evolution by incorporating new functions/organelles, while remaining the real coordinator overarching cellular functions and orchestrating them with the external milieu. Keywords Organellar functions · Organelle interactions · Organelle disorders · Endosymbiosis · Mitochondria · Lysosomes Abbreviations AD Alzheimer’s disease ALS Amyotrophic lateral sclerosis AM Arbuscular mycorrhizae CHL Chloroplast EE(s) Early endosome(s) ER Endoplasmic reticulum ERAD ER-associated (protein) degradation ERGIC ER-Golgi intermediate compartment ERMES ER-mitochondrial tethering complex FTD Fronto-temporal dementia MAM Mitochondria-associated ER membranes ES Endomembrane system GFP Green fluorescent protein Celso Almeida and Margarida D. Amaral have contributed equally to this article. * Celso Almeida [email protected] * Margarida D. Amaral [email protected] 1
Faculty of Sciences, BioISI, Biosystems and Integrative Sciences Institute, University of Lisboa, Campo Grande, C8 bdg, 1749‑016 Lisbon, Portugal
IM Isolation membrane LD(s) Lipid droplet(s) LE(s) Late endosome(s) LTP(s) Lipid-transfer protein(s) MCS(s) Membrane contact site(s) MITO Mitochondria MT (s) Microtubule(s) PD Parkinson’s disease PH Pleckstrin homology (domain) PLAM(s) Plastid-associated membranes PLD Plasmodesmata PM Plasma membrane PMCS(s) Plasma membrane contact site(s) PMP(s) Peroxisomal membrane proteins(s) PPA Pre-penetration apparatus PV(s) Parasitophorous vacuole(s) PBs Processing bodies RER Rough ER SER Smooth ER SE(s) Steryl ester(s) SOCE Store-operated Ca2+ entry STIM Stromal interaction molecule TEM Transmission electron microscopy TG Triacylglycerol TPC(s) Two-pore channel(s)
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