Astrocytic contributions to bioenergetics of cerebral ischemia

Dienel, Gerald A.; Hertz, Leif

doi:10.1002/glia.20157

Cited by 150Neurological Disorders and TreatmentsNeuroscience and Neuropharmacology ResearchAcute Ischemic Stroke Management

Astrocytic contributions to bioenergetics of cerebral ischemia

Dienel, Gerald A., Hertz, Leif·2005·Glia

DOI 10.1002/glia.20157

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Abstract

Astrocytes are multifunctional cells that interact with neurons and other astrocytes in signaling and metabolic functions, and their resistance to pathophysiological conditions can help restrict loss of tissue after an ischemic event provided adequate nutrients are supplied to support their requirements. Astrocytes have substantial oxidative capacity and mechanisms to upregulate glycolytic capability when respiration is impaired. An astrocytic enzyme that synthesizes a powerful activator of glycolysis is not present in neurons, endowing astrocytes with the ability to sustain ATP production under restrictive conditions. The monocarboxylic acid transporter (MCT) isoforms predominating in astrocytes are optimized to facilitate very large increases in lactate flux as lactate concentration increases within (1-3 mM) and above (>3 mM) the normal range. In sharp contrast, the major neuronal MCT serves as a barrier to increased transmembrane transport as lactate rises above 1 mM, restricting both entry and efflux. Lactate can serve as fuel during recovery from ischemia but direct evidence that lactate is oxidized by neurons (vs. astrocytes) to maintain synaptic function is lacking. Astrocytes have critical roles in regulation of ionic homeostasis and control of extracellular glutamate levels, and spreading depression associated with ischemia places high demands on energy supplies in astrocytes and contributes to metabolic exhaustion and demise. Disruption of Ca2+ homeostasis, generation of oxygen free radicals and nitric oxide, and mitochondrial depolarization contribute to astrocyte death during and after a metabolic insult. Novel pharmaceutical agents targeted to astrocytes and hyperoxic therapy that restores penumbral oxygen level during energy failure might improve postischemic outcome.

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Neuroprotective Role of Astrocytic Gap Junctions in Ischemic Stroke
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Brain Glucose Metabolism: Integration of Energetics with Function.
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Role of glial cells in cerebral ischemia
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The Transcriptional Activator Hypoxia Inducible Factor 2 (HIF-2/EPAS-1) Regulates the Oxygen-Dependent Expression of Erythropoietin in Cortical Astrocytes
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“Perhaps, the deviation between these values and what we observe may be related to astrocytes or other mechanisms that expand the diffusion limit by providing alternative metabolic substrates such as lactate [25].”
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Lack of appropriate stoichiometry: Strong evidence against an energetically important astrocyte-neuron lactate shuttle in brain
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Effects of Metformin in Experimental Stroke
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Overexpression of Mitochondrial Hsp70/Hsp75 in Rat Brain Protects Mitochondria, Reduces Oxidative Stress, and Protects from Focal Ischemia
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Targeting Astrocytes for Stroke Therapy
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Oxygen Tension Regulates Survival and Fate of Mouse Central Nervous System Precursors at Multiple Levels
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Glial conversion of SVZ-derived committed neuronal precursors after ectopic grafting into the adult brain
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A glycogen phosphorylase inhibitor selectively enhances local rates of glucose utilization in brain during sensory stimulation of conscious rats: implications for glycogen turnover
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Overexpression of Mitochondrial Hsp70/Hsp75 Protects Astrocytes against Ischemic Injury in vitro
Voloboueva, L. A., Duan, M., Ouyang, Y., Emery, J. F., Stoy, C., & Giffard, R. G. (2007) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/sj.jcbfm.9600600 · Cited by 123 · see citing works
Gene expression profiling reveals the profound upregulation of hypoxia-responsive genes in primary human astrocytes
Mense, S. M., Sengupta, A., Zhou, M., Lan, C., Bentsman, G., Volsky, D. J., & Li, Z. (2006) · Physiological Genomics · doi:10.1152/physiolgenomics.00315.2005 · Cited by 120 · see citing works
Inhibition of mitochondrial function in astrocytes: implications for neuroprotection
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Baicalin combats glutamate excitotoxicity via protecting glutamine synthetase from ROS-induced 20S proteasomal degradation
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Astroglial Pentose Phosphate Pathway Rates in Response to High-Glucose Environments
Takahashi, S., Izawa, Y., & Suzuki, N. (2012) · ASN NEURO · doi:10.1042/an20120002 · Cited by 93 · see citing works
Leptin Attenuates Cerebral Ischemia Injury through the Promotion of Energy Metabolism via the PI 3 K/Akt Pathway
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Persistent astroglial swelling accompanies rapid reversible dendritic injury during stroke-induced spreading depolarizations
Risher, W. C., Croom, D., & Kirov, S. A. (2012) · Glia · doi:10.1002/glia.22390 · Cited by 88 · see citing works
Lactate Shuttling and Lactate use as Fuel after Traumatic Brain Injury: Metabolic Considerations
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Critical Role of Flavin and Glutathione in Complex I–Mediated Bioenergetic Failure in Brain Ischemia/Reperfusion Injury
Kahl, A., Степанова, А., Konràd, C., Anderson, C. J., Manfredi, G., Zhou, P., Iadecola, C., & Galkin, A. S. (2018) · Stroke · doi:10.1161/strokeaha.117.019687 · Cited by 86 · see citing works
Energy metabolism in brain cells: effects of elevated ammonia concentrations
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Lactate Supply from Astrocytes to Neurons and its Role in Ischemic Stroke-induced Neurodegeneration
Yamagata, K. (2021) · Neuroscience · doi:10.1016/j.neuroscience.2021.11.035 · Cited by 80 · see citing works
Evolution of neuronal and astroglial disruption in the peri-contusional cortex of mice revealed by in vivo two-photon imaging
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Astrocytes are More Resistant to Focal Cerebral Ischemia Than Neurons and Die by a Delayed Necrosis
Gürer, G., Özdemir, Y., Erdemlı, E., Can, A., & Dalkara, T. (2008) · Brain Pathology · doi:10.1111/j.1750-3639.2008.00226.x · Cited by 80 · see citing works
Cerebral glycolysis: a century of persistent misunderstanding and misconception
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Pathophysiology of perinatal asphyxia: can we predict and improve individual outcomes?
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Carbenoxolone inhibits volume-regulated anion conductance in cultured rat cortical astroglia
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AMP-activated protein kinase mediates activity-dependent regulation of peroxisome proliferator-activated receptor γ coactivator-1α and nuclear respiratory factor 1 expression in rat visual cortical neurons
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Dysfunctional TCA-Cycle Metabolism in Glutamate Dehydrogenase Deficient Astrocytes
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Aerobic production and utilization of lactate satisfy increased energy demands upon neuronal activation in hippocampal slices and provide neuroprotection against oxidative stress
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Sustained astrocytic clusterin expression improves remodeling after brain ischemia
Imhof, A., Charnay, Y., Vallet, P. G., Aronow, B., Kovari, E., French, L. E., Bouras, C., & Giannakopoulos, P. (2006) · Neurobiology of Disease · doi:10.1016/j.nbd.2005.11.009 · Cited by 73 · see citing works
Purinergic Receptor Stimulation Reduces Cytotoxic Edema and Brain Infarcts in Mouse Induced by Photothrombosis by Energizing Glial Mitochondria
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Mitochondrial function in Müller cells - Does it matter?
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Glutamate Transport and Preterm Brain Injury
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Astrocyte‐neuron lactate shuttle sensitizes nociceptive transmission in the spinal cord
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Integration of P2Y receptor-activated signal transduction pathways in G protein-dependent signalling networks
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Selective overexpression of excitatory amino acid transporter 2 (EAAT2) in astrocytes enhances neuroprotection from moderate but not severe hypoxia–ischemia
Weller, M. L., Stone, I. M., Goss, A., Rau, T., Rova, C. R. L., & Poulsen, D. J. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.05.059 · Cited by 62 · see citing works
Effects of heat shock protein 72 (Hsp72) on evolution of astrocyte activation following stroke in the mouse
Barreto, G. E., White, R., Xu, L., Palm, C. J., & Giffard, R. G. (2012) · Experimental Neurology · doi:10.1016/j.expneurol.2012.08.015 · Cited by 59 · see citing works
Stroke Neuroprotection: Targeting Mitochondria
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Astrocyte‐specific insulin‐like growth factor‐1 gene transfer in aging female rats improves stroke outcomes
Okoreeh, A. K., Bake, S., & Sohrabji, F. (2017) · Glia · doi:10.1002/glia.23142 · Cited by 55 · see citing works
Why does the brain (not) have glycogen?
DiNuzzo, M., Maraviglia, B., & Giove, F. (2011) · BioEssays · doi:10.1002/bies.201000151 · Cited by 53 · see citing works
Astrocyte glutathione maintains endothelial barrier stability
Huang, S.-F., Othman, A., Koshkin, A., Fischer, S., Fischer, D., Zamboni, N., Ono, K., Sawa, T., & Ogunshola, O. O. (2020) · Redox Biology · doi:10.1016/j.redox.2020.101576 · Cited by 52 · see citing works
Transcriptome Analysis of Gene Expression Provides New Insights into the Effect of Mild Therapeutic Hypothermia on Primary Human Cortical Astrocytes Cultured under Hypoxia
Salman, M. M., Kitchen, P., Woodroofe, M. N., Bill, R. M., Conner, A. C., Heath, P. R., & Conner, M. T. (2017) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2017.00386 · Cited by 50 · see citing works
1,5-Dicaffeoylquinic acid-mediated glutathione synthesis through activation of Nrf2 protects against OGD/reperfusion-induced oxidative stress in astrocytes
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Brain 3-Mercaptopyruvate Sulfurtransferase (3MST): Cellular Localization and Downregulation after Acute Stroke
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Oxygen and Glucose Deprivation-Induced Changes in Astrocyte Membrane Potential and Their Underlying Mechanisms in Acute Rat Hippocampal Slices
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In Situ Mitochondrial Ca2+ Buffering Differences of Intact Neurons and Astrocytes from Cortex and Striatum
Oliveira, J. M. A., & Gonçalves, J. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m807459200 · Cited by 45 · see citing works
Mitochondrial bioenergetics and dynamics in Huntington’s disease: tripartite synapses and selective striatal degeneration
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Potentiation of excitotoxicity in HIV-1-associated Dementia and the significance of glutaminase
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Neuron–Glial Interactions: Implications for Plasticity, Behavior, and Cognition
Rangel‐Gomez, M., Alberini, C. M., Deneen, B., Drummond, G. T., Manninen, T., Sur, M., & Vicentic, A. (2024) · Journal of Neuroscience · doi:10.1523/jneurosci.1231-24.2024 · Cited by 46 · see citing works
Imaging Brain Activation
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Self-citation
Expression of the human isoform of glutamate dehydrogenase, hGDH2, augments TCA cycle capacity and oxidative metabolism of glutamate during glucose deprivation in astrocytes
Nissen, J. D., Lykke, K., Bryk, J., Stridh, M. H., Zaganas, I. V., Skytt, D. M., Schousboe, A., Bak, L. K., Enard, W., Pääbo, S., et al. (2016) · Glia · doi:10.1002/glia.23105 · Cited by 41 · see citing works
Cell Type‐Specific Mechanisms in the Pathogenesis of Ischemic Stroke: The Role of Apoptosis Signal‐Regulating Kinase 1
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Salvianolic acid A protects human SH-SY5Y neuroblastoma cells against H2O2-induced injury by increasing stress tolerance ability
Zhang, H., Gao, M., Zhang, L., Zhao, Y., Shi, L., Chen, B.-N., Wang, Y., Wang, S., & Du, G. (2012) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2012.04.021 · Cited by 41 · see citing works
Changes in Lipid-Sensitive Two-Pore Domain Potassium Channel TREK-1 Expression and Its Involvement in Astrogliosis Following Cerebral Ischemia in Rats
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Sevoflurane Protects Rat Mixed Cerebrocortical Neuronal–Glial Cell Cultures against Transient Oxygen–Glucose Deprivation
Canas, P. T., Velly, L. J., Labrande, C. N., Guillet, B. A., Sautou, V., Masmejean, F., Nieoullon, A. L., Gouin, F. M., Bruder, N. J., & Pisano, P. S. (2006) · Anesthesiology · doi:10.1097/00000542-200611000-00021 · Cited by 39 · see citing works
Sustained hydrogen peroxide stress decreases lactate production by cultured astrocytes
Liddell, J. R., Zwingmann, C., Schmidt, M., Thiessen, A., Leibfritz, D., Robinson, S. R., & Dringen, R. (2009) · Journal of Neuroscience Research · doi:10.1002/jnr.22093 · Cited by 38 · see citing works
Nitric Oxide Synthase Isoforms Undertake Unique Roles During Excitotoxicity
Parathath, S. R., Gravanis, I., & Tsirka, S. E. (2007) · Stroke · doi:10.1161/strokeaha.106.478826 · Cited by 38 · see citing works
Stat3 mediates LIF‐induced protection of astrocytes against toxic ROS by upregulating the UPC2 mRNA pool
Lapp, D. W., Zhang, S. S.-M., & Barnstable, C. J. (2013) · Glia · doi:10.1002/glia.22594 · Cited by 38 · see citing works
13C NMR spectroscopy applications to brain energy metabolism
Rodrigues, T. B., Valette, J., & Bouzier‐Sore, A. (2013) · Frontiers in Neuroenergetics · doi:10.3389/fnene.2013.00009 · Cited by 36 · see citing works
Measurement of Lactate Content and Amide Proton Transfer Values in the Basal Ganglia of a Neonatal Piglet Hypoxic-Ischemic Brain Injury Model Using MRI
Yang, Z., & Wang, X. (2017) · American Journal of Neuroradiology · doi:10.3174/ajnr.a5066 · Cited by 36 · see citing works
l ‐Lactate mediates neuroprotection against ischaemia by increasing TREK 1 channel expression in rat hippocampal astrocytesin vitro
Banerjee, A., Ghatak, S., & Sikdar, S. K. (2016) · Journal of Neurochemistry · doi:10.1111/jnc.13638 · Cited by 35 · see citing works
Phosphorylation of GFAP is Associated with Injury in the Neonatal Pig Hypoxic-Ischemic Brain
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Authors: Dienel, G. A., & Hertz, L.
Affiliations: University of Arkansas for Medical Sciences (US)
China Medical University (CN)
Corresponding author: Dienel, Gerald A.
ORCID: Dienel, Gerald A.
Hertz, Leif
Venue: Glia
Publisher: Wiley
Published: 2005-04-21
Volume: 50
Issue: 4
Pages: 362-388
ISSN: 0894-1491 (ISSN-L)
1098-1136
DOI: 10.1002/glia.20157
OpenAlex: W1964844927
Cited by: 150
References: 331
Citations by year: 2026: 2 · 2025: 6 · 2024: 2 · 2023: 1 · 2022: 3 · 2021: 2 · 2020: 6 · 2019: 3 · 2018: 7 · 2017: 8 · 2016: 4 · 2015: 6 · 2014: 7 · 2013: 10 · 2012: 10
FWCI: 1.21
Type: journal article
Language: en
Open access: closed
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: Glia (publishedVersion)
PubMed (publishedVersion)
Funders: National Institute of Neurological Disorders and Stroke (NS 36728, R01NS036728, NS38230)
Topics: Life Sciences › Neuroscience › Neurology › Neurological Disorders and Treatments
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Health Sciences › Medicine › Epidemiology › Acute Ischemic Stroke Management
Keywords: astrocytes, cerebral ischemia, glycolysis, lactate transport, monocarboxylate transporters, lactate oxidation, cortical spreading depression, ion homeostasis, extracellular glutamate, calcium homeostasis, mitochondrial depolarization, reactive oxygen species, nitric oxide, penumbra, neuroprotection
MeSH terms: Animals, Astrocytes, Cell Survival, Brain Ischemia, Energy Metabolism, Humans

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