Johnson, Lance A.

Poitelon, Yannick

Tremblay, Marie-Ève

English

PubMed

University of Kentucky

University of Kentucky UKnowledge Physiology Faculty Publications Physiology 11-5-2021 Editorial: The Metabolism of the Neuron-Glia Unit Yannick Poitelon Albany Medical College Lance A. Johnson University of Kentucky, Johnson.Lance@uky.edu Marie-Ève Tremblay University of Victoria, Canada Follow this and additional works at: https://uknowledge.uky.edu/physiology_facpub  Part of the Neurosciences Commons, and the Physiology Commons Right click to open a feedback form in a new tab to let us know how this document benefits you. Repository Citation Poitelon, Yannick; Johnson, Lance A.; and Tremblay, Marie-Ève, "Editorial: The Metabolism of the Neuron-Glia Unit" (2021). Physiology Faculty Publications. 180. https://uknowledge.uky.edu/physiology_facpub/180 This Editorial is brought to you for free and open access by the Physiology at UKnowledge. It has been accepted for inclusion in Physiology Faculty Publications by an authorized administrator of UKnowledge. For more information, please contact UKnowledge@lsv.uky.edu. Editorial: The Metabolism of the Neuron-Glia Unit Digital Object Identifier (DOI) https://doi.org/10.3389/fncel.2021.791389 Notes/Citation Information Published in Frontiers in Cellular Neuroscience, v. 15, article 791389. © 2021 Poitelon, Johnson and Tremblay This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. This editorial is available at UKnowledge: https://uknowledge.uky.edu/physiology_facpub/180 EDITORIALpublished: 05 November 2021doi: 10.3389/fncel.2021.791389Frontiers in Cellular Neuroscience | www.frontiersin.org 1 November 2021 | Volume 15 | Article 791389Edited and reviewed by:Dirk M. Hermann,University ofDuisburg-Essen, Germany*Correspondence:Yannick Poitelonpoitely@amc.eduSpecialty section:This article was submitted toCellular Neuropathology,a section of the journalFrontiers in Cellular NeuroscienceReceived: 08 October 2021Accepted: 19 October 2021Published: 05 November 2021Citation:Poitelon Y, Johnson LA and TremblayM-È (2021) Editorial: The Metabolismof the Neuron-Glia Unit.Front. Cell. Neurosci. 15:791389.doi: 10.3389/fncel.2021.791389Editorial: The Metabolism of theNeuron-Glia UnitYannick Poitelon 1*, Lance A. Johnson 2 and Marie-Ève Tremblay 31Department of Neuroscience and Experimental Therapeutics, Albany Medical College, Albany, NY, United States,2Department of Physiology and Sanders Brown Center on Aging, University of Kentucky, Lexington, KY, United States,3Division of Medical Sciences, University of Victoria, Victoria, BC, CanadaKeywords: metabolism, astrocyte, oligodendrocyte, microglia, Schwann cell, neuron, diseaseEditorial on the Research TopicThe Metabolism of the Neuron-Glia UnitInitially thought to simply hold the nervous system together, glial cells are now known to regulatea variety of critical functions in the nervous system. These functions include providing trophicsupport to neurons, ensuring fast impulse conduction, modulating synaptic formation, maturation,action, plasticity, and maintaining parenchymal homeostasis by actively regulating metabolites andclearing cell debris. Whilst the concept of metabolic coupling between neurons and glia has beenentertained for years, especially for astrocytes, more recent work has resulted in major advancesin our understanding of the molecular and cellular aspects of this coupling, notably investigatingnovel glial cell types, utilizing cutting edge technical tools, and developing unique animal models.The collection of articles in this Research Topic adds further insight to this growing knowledge baseand provides new information worth considering in future research. Here, we present an overviewabout the included review articles as well as novel method and original research.Throughout the nervous system tissues, neurons are closely associated with glial cells, includingastrocytes, oligodendrocytes, microglia, and Schwann cells. Their dynamic interactions areimportant for nervous system development and function throughout adult life, as neurons relyon glial cells to fulfill their energetic demands. There is also emerging evidence that metabolicalterations in glial cells can modify their function and result in neuronal dysfunction, while everyneurological disease involves some glial component, whether it be a primary or secondary cause forthe disease.In their review Afridi et al., examine recent developments that implicate the regulation ofmicroglial and astrocytic phenotypic changes and their consequences on neuron–glia interactionsin neurological disorders that include multiple sclerosis, Parkinson’s disease, Alzheimer’s disease,amyotrophic lateral sclerosis, and cerebral ischemia. They also discuss the challenges andpossibilities of targeting glial metabolism as a strategy to treat neurological disorders. Shippy et al.discuss a similar theme in their review while focusing on Alzheimer’s disease and the involvementof neuron-glia metabolic coupling in the context of neurodegeneration. The authors particularlydiscuss how microglial metabolism affects immune responses in dementia and how modulation ofimmunometabolism may be a valuable strategy for the development of advanced therapeutics totreat human diseases.In their contribution, Niiyama et al. examine sex-dependent changes in spine structure ofgranule neurons of the dentate gyrus in male and female mice with hyperthyroidism, a conditionwhich affects metabolism. The authors report that both sex-independent increases in spine densityand sex-dependent alterations of spine morphology. These results may help to understand thefunctions of thyroid hormones in the central nervous system, and highlight the importance of fullyPoitelon et al. Editorial: The Metabolism of the Neuron-Glia Unitunderstanding sex-dependent effects to better treat or preventneurological symptoms related to thyroid dysfunction.Jha et al. discuss the importance of monocarboxylatetransporters (MCTs) by summarizing the emerging roles oflactate, pyruvate and ketone bodies transporters in glia-neuronmetabolic interactions of the central and peripheral nervoussystems. Though the metabolic support of neurons through theshuttling of lactate by glial cells was proposed many years ago, itis in part thanks to conditional knockout models targeting MCTsthat the lactate shuttle hypothesis is now well-acknowledged.The authors provide a comprehensive analysis of the expressionpatterns and functions of MCTs and highlight their roles inmodulating glia-neuron bidirectional metabolic crosstalk.Boucanova et al. more deeply examine the role of Schwanncells, the principal glia in the peripheral nervous system of highervertebrates, in the metabolic support of axons. Schwann cells aremainly known for wrapping and myelinating axons. However,the trophic support of axons by Schwann cell is beginning tobe considered, as these glial cells have been shown to exchangeboth neurotransmitters and glycolysis by-products with axons.In this minireview, the authors present the role of Schwann cellas metabolic supporters of axonal health and make the case thatcharacterization of the Schwann cell-axon metabolic relationshipis necessary to better understand peripheral neuropathies.Lana et al. describe how perturbation in the regulation of brainenergy metabolism–not only in neurons, but also in astrocytesandmicroglia–may be one of the pathophysiological mechanismsof neurodegeneration, especially in hypoxia/ischemia. In thisreview, the authors analyze published data to demonstratethat glial responses to the same hypoxic insult are not equal,as the quantitative and morpho-functional alterations of theneuron–astrocyte–microglia response varied significantly in thehippocampus between the CA1 (more vulnerable to ischemia)and CA3 (less vulnerable to ischemia) regions.Finally, Lerchundi et al. developed a new strategy toselectively permeabilize neurons and astrocytes in organotypicbrain slice cultures to enable a free exchange of ATP acrossthe plasma membrane. They show that their new procedureenables the quantitative measurement of changes in intracellularATP, through ATeam, a FRET-based nanosensor. This novelmethodology is of high interest for our Research Topic, as it isapplicable to animals expressing ATeam in the brain and maybe employed for the calibration of other genetically encodedbiosensors sensitive to lactate, pyruvate, or glucose.We thank all authors for their valuable contributions, andhope that the readers of this Research Topic will enjoy asmuch as we did the expert opinions and excellent originalresearch presented.AUTHOR CONTRIBUTIONSYP wrote the first draft of the editorial. All the authors havecontributed to this editorial, by editing and writing commentsfor the different articles.FUNDINGYP was supported by the National Institutes of Health(NS110627). LJ was supported by the National Institutes ofHealth (R01AG060056 and R01AG062550). M-ÈT was a Tier IICanada Research Chair in Neurobiology of Aging and Cognition.Conflict of Interest: The authors declare that the research was conducted in theabsence of any commercial or financial relationships that could be construed as apotential conflict of interest.Publisher’s Note: All claims expressed in this article are solely those of the authorsand do not necessarily represent those of their affiliated organizations, or those ofthe publisher, the editors and the reviewers. Any product that may be evaluated inthis article, or claim that may be made by its manufacturer, is not guaranteed orendorsed by the publisher.Copyright © 2021 Poitelon, Johnson and Tremblay. This is an open-access articledistributed under the terms of the Creative Commons Attribution License (CC BY).The use, distribution or reproduction in other forums is permitted, provided theoriginal author(s) and the copyright owner(s) are credited and that the originalpublication in this journal is cited, in accordance with accepted academic practice.No use, distribution or reproduction is permitted which does not comply with theseterms.Frontiers in Cellular Neuroscience | www.frontiersin.org 2 November 2021 | Volume 15 | Article 791389

Editorial: The Metabolism of the Neuron-Glia Unit

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Editorial: The Metabolism of the Neuron-Glia Unit

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