Energy metabolism in astrocytes: High rate of oxidative metabolism and spatiotemporal dependence on glycolysis/glycogenolysis

Hertz, Leif; Peng, Liang; Dienel, Gerald A

doi:10.1038/sj.jcbfm.9600343

Cited by 587Neuroscience and Neuropharmacology ResearchMitochondrial Function and PathologyAdvanced MRI Techniques and Applications

Energy metabolism in astrocytes: High rate of oxidative metabolism and spatiotemporal dependence on glycolysis/glycogenolysis

Hertz, Leif, Peng, Liang, Dienel, Gerald A·2007·Journal of Cerebral Blood Flow & Metabolism

DOI 10.1038/sj.jcbfm.9600343

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Abstract

Astrocytic energy demand is stimulated by K(+) and glutamate uptake, signaling processes, responses to neurotransmitters, Ca(2+) fluxes, and filopodial motility. Astrocytes derive energy from glycolytic and oxidative pathways, but respiration, with its high-energy yield, provides most adenosine 5' triphosphate (ATP). The proportion of cortical oxidative metabolism attributed to astrocytes ( approximately 30%) in in vivo nuclear magnetic resonance (NMR) spectroscopic and autoradiographic studies corresponds to their volume fraction, indicating similar oxidation rates in astrocytes and neurons. Astrocyte-selective expression of pyruvate carboxylase (PC) enables synthesis of glutamate from glucose, accounting for two-thirds of astrocytic glucose degradation via combined pyruvate carboxylation and dehydrogenation. Together, glutamate synthesis and oxidation, including neurotransmitter turnover, generate almost as much energy as direct glucose oxidation. Glycolysis and glycogenolysis are essential for astrocytic responses to increasing energy demand because astrocytic filopodial and lamellipodial extensions, which account for 80% of their surface area, are too narrow to accommodate mitochondria; these processes depend on glycolysis, glycogenolysis, and probably diffusion of ATP and phosphocreatine formed via mitochondrial metabolism to satisfy their energy demands. High glycogen turnover in astrocytic processes may stimulate glucose demand and lactate production because less ATP is generated when glucose is metabolized via glycogen, thereby contributing to the decreased oxygen to glucose utilization ratio during brain activation. Generated lactate can spread from activated astrocytes via low-affinity monocarboxylate transporters and gap junctions, but its subsequent fate is unknown. Astrocytic metabolic compartmentation arises from their complex ultrastructure; astrocytes have high oxidative rates plus dependence on glycolysis and glycogenolysis, and their energetics is underestimated if based solely on glutamate cycling.

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Glutamate functions as an excitatory neurotransmitter and a glutamate-glutamine cycle exists between astrocytes and neurons, allowing for the movement of anaplerotic carbon units and the sequestration of ammonia, which is neurotoxic.
“Glutamate functions as an excitatory neurotransmitter and a glutamate–glutamine cycle exists between astrocytes and neurons, allowing for the movement of anaplerotic carbon units and the sequestration of ammonia, which is neurotoxic [132].”
From Mitochondrial Oxidative and Nitrosative Stress and Alzheimer Disease (2020) · cites this paper as [132]
There is ample evidence of glutamate oxidation by astrocytes.
“and there is ample evidence of glutamate oxidation by astrocytes (Hertz et al., 2007; Dienel, 2017).”
From Fueling thought: Management of glycolysis and oxidative phosphorylation in neuronal metabolism (2018) · cites this paper as Hertz et al., 2007

THE [ 14 C]DEOXYGLUCOSE METHOD FOR THE MEASUREMENT OF LOCAL CEREBRAL GLUCOSE UTILIZATION: THEORY, PROCEDURE, AND NORMAL VALUES IN THE CONSCIOUS AND ANESTHETIZED ALBINO RAT 1
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The entry of [1-13C]glucose into biochemical pathways reveals a complex compartmentation and metabolite trafficking between glia and neurons: a study by 13C-NMR spectroscopy
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Astrocytes contribute to regulation of extracellular calcium and potassium in the rat cerebral cortex during spreading depression
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Compartmentation of Lactate Originating from Glycogen and Glucose in Cultured Astrocytes
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Significant Amounts of Glycogen are Synthesized from 3‐Carbon Compounds in Astroglial Primary Cultures from Mice with Participation of the Mitochondrial Phosphoenolpyruvate Carboxykinase Isoenzyme
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Activation-Induced Resetting of Cerebral Metabolism and Flow Is Abolished by β-Adrenergic Blockade With Propranolol
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The central noradrenergic system in the rat: Metabolic mapping with α-adrenergic blocking agents
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Transport and metabolism of acetate in rat brain cortex in vitro
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Cerebral pyruvate carboxylase flux is unaltered during bicuculline‐seizures
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Noradrenaline induced stimulation of oxidative metabolism in astrocytes but not in neurons in primary cultures
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Pharmacological characteristics of potassium-induced, glycogenolysis in astrocytes
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Whole‐brain glutamate metabolism evaluated by steady‐state kinetics using a double‐isotope procedure: effects of gabapentin
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Separate Neuronal and Glial Na + ,K + -ATPase Isoforms Regulate Glucose Utilization in Response to Membrane Depolarization and Elevated Extracellular Potassium
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Potassium homeostasis in the brain at the organ and cell level
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The astrocytic syncytium
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Functional role of the potassium‐induced stimulation of oxygen uptake in brain slices studied with cesium as a probe
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Decoding calcium wave signaling
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The Mystery and Magic of Glia: A Perspective on Their Roles in Health and Disease
Barres, B. A. (2008) · Neuron · doi:10.1016/j.neuron.2008.10.013 · Cited by 1,352 · see citing works
A Cellular Perspective on Brain Energy Metabolism and Functional Imaging
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Myelination and the trophic support of long axons
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The Glia-Neuron Lactate Shuttle and Elevated ROS Promote Lipid Synthesis in Neurons and Lipid Droplet Accumulation in Glia via APOE/D
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Blood lactate is an important energy source for the human brain.
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Transient Opening of the Mitochondrial Permeability Transition Pore Induces Microdomain Calcium Transients in Astrocyte Processes
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Exercise Benefits Brain Function: The Monoamine Connection
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Fueling thought: Management of glycolysis and oxidative phosphorylation in neuronal metabolism
Yellen, G. (2018) · Journal of Cell Biology · doi:10.1083/jcb.201803152 · Cited by 371 · see citing works
“, 2013), and there is ample evidence of glutamate oxidation by astrocytes (Hertz et al., 2007; Dienel, 2017).”
Background
Lactate kinetics in human tissues at rest and during exercise
van Hall, G. (2010) · Acta Physiologica · doi:10.1111/j.1748-1716.2010.02122.x · Cited by 346 · see citing works
13 C MRS studies of neuroenergetics and neurotransmitter cycling in humans
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Cerebral Blood Flow Response to Functional Activation
Paulson, O. B., Hasselbalch, S. G., Rostrup, E., Knudsen, G. M., & Pelligrino, D. (2010) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2009.188 · Cited by 264 · see citing works
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Inflammation-Induced Alteration of Astrocyte Mitochondrial Dynamics Requires Autophagy for Mitochondrial Network Maintenance
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Predominant enhancement of glucose uptake in astrocytes versus neurons during activation of the somatosensory cortex
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The effect of fluoxetine on astrocyte autophagy flux and injured mitochondria clearance in a mouse model of depression
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The ketogenic diet and brain metabolism of amino acids: Relationship to the anticonvulsant effect
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Direct evidence for activity-dependent glucose phosphorylation in neurons with implications for the astrocyte-to-neuron lactate shuttle
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Lack of appropriate stoichiometry: Strong evidence against an energetically important astrocyte-neuron lactate shuttle in brain
Dienel, G. A. (2017) · Journal of Neuroscience Research · doi:10.1002/jnr.24015 · Cited by 168 · see citing works
Astrocytes are poised for lactate trafficking and release from activated brain and for supply of glucose to neurons
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Authors: Hertz, L., Peng, L., & Dienel, G. A.
Affiliations: China Medical University (CN)
University of Arkansas for Medical Sciences (US)
Corresponding author: Hertz, Leif
ORCID: Hertz, Leif
Peng, Liang
Dienel, Gerald A
Venue: Journal of Cerebral Blood Flow & Metabolism
Publisher: SAGE Publications
Published: 2007-02
Volume: 27
Issue: 2
Pages: 219-249
ISSN: 0271-678X (ISSN-L)
1559-7016
DOI: 10.1038/sj.jcbfm.9600343
OpenAlex: W2094633691
Cited by: 587
References: 158
Citations by year: 2026: 10 · 2025: 18 · 2024: 15 · 2023: 30 · 2022: 23 · 2021: 27 · 2020: 26 · 2019: 25 · 2018: 21 · 2017: 35 · 2016: 28 · 2015: 35 · 2014: 40 · 2013: 45 · 2012: 45
FWCI: 2.92
Type: journal article
Language: en
Open access: closed
Licence: journals.sagepub.com/page/policies/text-and-data-mining-license (tdm)
Locations: Journal of Cerebral Blood Flow & Metabolism (publishedVersion)
PubMed (publishedVersion)
Funders: National Institute of Neurological Disorders and Stroke (NS 36728, R01NS036728)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced MRI Techniques and Applications
Keywords: astrocytes, oxidative metabolism, glycolysis, glycogenolysis, pyruvate carboxylase, glutamate synthesis, lactate, astrocyte-neuron metabolic coupling, astrocyte ultrastructure, monocarboxylate transporters, gap junctions, ATP diffusion, phosphocreatine, brain energy demand
MeSH terms: Animals, Astrocytes, Brain Chemistry, Citric Acid Cycle, Energy Metabolism, Glucose, Glutamine, Glycolysis, Humans, Oxidation-Reduction, Neurotransmitter Agents, Glutamic Acid, Glycogenolysis

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Energy metabolism in astrocytes: High rate of oxidative metabolism and spatiotemporal dependence on glycolysis/glycogenolysis

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