Cited by 2,927Neuroscience and Neuropharmacology ResearchAmino Acid Enzymes and MetabolismNeuroinflammation and Neurodegeneration Mechanisms

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Glutamate uptake into astrocytes stimulates aerobic glycolysis: a mechanism coupling neuronal activity to glucose utilization.

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Pellerin, L, Magistretti, P J·1994·Proceedings of the National Academy of Sciences

DOI 10.1073/pnas.91.22.10625PMC PMC45074

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Abstract

Glutamate, released at a majority of excitatory synapses in the central nervous system, depolarizes neurons by acting at specific receptors. Its action is terminated by removal from the synaptic cleft mostly via Na(+)-dependent uptake systems located on both neurons and astrocytes. Here we report that glutamate, in addition to its receptor-mediated actions on neuronal excitability, stimulates glycolysis--i.e., glucose utilization and lactate production--in astrocytes. This metabolic action is mediated by activation of a Na(+)-dependent uptake system and not by interaction with receptors. The mechanism involves the Na+/K(+)-ATPase, which is activated by an increase in the intracellular concentration of Na+ cotransported with glutamate by the electrogenic uptake system. Thus, when glutamate is released from active synapses and taken up by astrocytes, the newly identified signaling pathway described here would provide a simple and direct mechanism to tightly couple neuronal activity to glucose utilization. In addition, glutamate-stimulated glycolysis is consistent with data obtained from functional brain imaging studies indicating local nonoxidative glucose utilization during physiological activation.

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“It has been suggested that glutamate uptake in astrocytes stimulates lactate synthesis, which is subsequently shuttled to neurons to support oxidative metabolism (Pellerin & Magistretti, 1994).”
Background
A metabolic switch in brain: glucose and lactate metabolism modulation by ascorbic acid
Castro, M. A., Beltrán, F. A., Brauchi, S. E., & Concha, I. I. (2009) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2009.06151.x · Cited by 147
Loss-or gain-of-function mutations in ACOX1 cause axonal loss via different mechanisms
Chung, H.-L., Wangler, M. F., Marcogliese, P. C., Jo, J., Ravenscroft, T. A., Zuo, Z., Duraine, L., Sadeghzadeh, S., Li-Kroeger, D., Schmidt, R. E., et al. (2020) · Neuron · doi:10.1016/j.neuron.2020.02.021 · Cited by 154
Modulation of astrocytic metabolic phenotype by proinflammatory cytokines
Gavillet, M., Allaman, I., & Magistretti, P. J. (2008) · Glia · doi:10.1002/glia.20671 · Cited by 147
NBCe1 Mediates the Acute Stimulation of Astrocytic Glycolysis by Extracellular K +
Ruminot, I., Gutiérrez, R., Peña-Münzenmayer, G., Añazco, C. C., Sotelo-Hitschfeld, T., Lerchundi, R., Niemeyer, M. I., Shull, G. E., & Barros, L. F. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.2310-11.2011 · Cited by 148
“Multiple roles have been ascribed to lactate in the brain, including preferential fueling of neurons (Pellerin and Magistretti, 1994; Suzuki et al., 2011), intercellular signaling (Lam et al., 2005; Shimizu et al., 2007; Gordon et al., 2008), and macromolecular synthesis (Rinholm et al., 2011), but…”
Background
Glucose and lactate supply to the synapse
Barros, L. F., & Deitmer, J. W. (2009) · Brain Research Reviews · doi:10.1016/j.brainresrev.2009.10.002 · Cited by 155
“The alternative model is termed the “astrocyte-to-neuron-lactate shuttle hypothesis” (ANLSH; Pellerin and Magistretti, 1994), which states that astrocytes take most of the glucose and export it in the form of lactate, which is then takenupandoxidizedbyneurons (Fig.”
Method
Astrocytes as Guardians of Neuronal Excitability: Mechanisms Underlying Epileptogenesis
Verhoog, Q. P., Holtman, L., Aronica, E., & van Vliet, E. A. (2020) · Frontiers in Neurology · doi:10.3389/fneur.2020.591690 · Cited by 149
Reactive Oxygen Species: Beyond Their Reactive Behavior
Tauffenberger, A., & Magistretti, P. J. (2021) · Neurochemical Research · doi:10.1007/s11064-020-03208-7 · Cited by 157
The redox switch/redox coupling hypothesis
Cerdán, S., Rodrigues, T. B., Sierra, A., Benito, M., Fonseca, L. L., Fonseca, C. P., & García-Martín, M. L. (2006) · Neurochemistry International · doi:10.1016/j.neuint.2005.12.036 · Cited by 146
“1 summarizes the main aspects of the astrocyte to neuron lactate shuttle (ANLS) hypothesis (Pellerin and Magistretti, 1994; Tsacopoulos and Magistretti, 1996; Tsacopoulos et al., 1998; Magistretti, 2000; Magistretti and Pellerin, 2000; Tsacopoulos, 2002; Pellerin, 2003).”
Background
Differential distribution of the enzymes glutamate dehydrogenase and aspartate aminotransferase in cortical synaptic mitochondria contributes to metabolic compartmentation in cortical synaptic terminals
McKenna, M. C., Stevenson, J., Huang, X., & Hopkins, I. B. (2000) · Neurochemistry International · doi:10.1016/s0197-0186(00)00042-5 · Cited by 147
Digitoxin as an anticancer agent with selectivity for cancer cells: possible mechanisms involved
López-Lázaro, M. (2007) · Expert Opinion on Therapeutic Targets · doi:10.1517/14728222.11.8.1043 · Cited by 145
“, ouabain) can inhibit aerobic glycolysis [119-123] .”
Background
Neuronal Activity and Glutamate Uptake Decrease Mitochondrial Mobility in Astrocytes and Position Mitochondria Near Glutamate Transporters
Jackson, J. G., O’Donnell, J. C., Takano, H., Coulter, D. A., & Robinson, M. B. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.3510-13.2014 · Cited by 152
“Glutamate transport results in a significant increase in intracellular [Na ] (Rose and Ransom, 1996) and stimulates Na /K -ATPase activity (Pellerin and Magistretti, 1994).”
BackgroundInfluential
Astroglial glutamate transporters coordinate excitatory signaling and brain energetics
Robinson, M. B., & Jackson, J. G. (2016) · Neurochemistry International · doi:10.1016/j.neuint.2016.03.014 · Cited by 150
Decreased Brain pH as a Shared Endophenotype of Psychiatric Disorders
Hagihara, H., Catts, V. S., Katayama, Y., Shoji, H., Takagi, T., Huang, F. L., Nakao, A., Mori, Y., Huang, K., Ishii, S., et al. (2017) · Neuropsychopharmacology · doi:10.1038/npp.2017.167 · Cited by 147
“Glycolysis is also stimulated by the uptake of glutamate in astrocytes following neuronal excitation (Pellerin and Magistretti, 1994).”
Background
Magnetic resonance spectroscopy of neurotransmitters in human brain
Novotny, E. J., Fulbright, R. K., Pearl, P. L., Gibson, K. M., & Rothman, D. L. (2003) · Annals of Neurology · doi:10.1002/ana.10697 · Cited by 145
The central role of aquaporins in the pathophysiology of ischemic stroke
Vella, J. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00108 · Cited by 146
“In contrast to AQP4, Frontiers in Cellular Neuroscience | www.frontiersin.org 12 April 2015 | Volume 9 | Article 108 AQP9 is not polarized on astrocyte end-feet and its pattern of expression is thought to support a role in the ‘lactate shuttle’ model as proposed by Pellerin and Magistretti (1994).”
Background
Glial Contribution to Excitatory and Inhibitory Synapse Loss in Neurodegeneration
Henstridge, C. M., Tzioras, M., & Paolicelli, R. C. (2019) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2019.00063 · Cited by 155
Alzheimer's disease: the amyloid hypothesis and the Inverse Warburg effect
Demetrius, L., Magistretti, P. J., & Pellerin, L. (2015) · Frontiers in Physiology · doi:10.3389/fphys.2014.00522 · Cited by 151
“…model as it pertains to the origin of age-related neurodegenerative diseases, rests on three critical factors, namely: (a) The analytic integration of mitochondrial energetics in neurons with the cytosolic energetics in astrocytes—the ANLS shuttle hypothesis (Pellerin and Magistretti, 1994).”
InfluentialSelf-citation
Distribution and possible roles of aquaporin 9 in the brain
Badaut, J., & Regli, L. (2004) · Neuroscience · doi:10.1016/j.neuroscience.2004.06.035 · Cited by 142
Lactate administration attenuates cognitive deficits following traumatic brain injury
Rice, A. C., Zsoldos, R., Chen, T., Wilson, M. S., Alessandri, B., Hamm, R. J., & Bullock, M. R. (2002) · Brain Research · doi:10.1016/s0006-8993(01)03299-1 · Cited by 139
Sodium homeostasis in the tumour microenvironment
Leslie, T. K., James, A. D., Zaccagna, F., Grist, J. T., Deen, S. S., Kennerley, A. J., Riemer, F., Kaggie, J. D., Gallagher, F. A., Gilbert, F. J., et al. (2019) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2019.07.001 · Cited by 141
Old Things New View: Ascorbic Acid Protects the Brain in Neurodegenerative Disorders
Covarrubias‐Pinto, A., Acuña, A. I., Beltrán, F. A., Torres-Díaz, L., & Castro, M. A. (2015) · International Journal of Molecular Sciences · doi:10.3390/ijms161226095 · Cited by 140
“The uptake of glutamate is able to stimulate glucose uptake, glycolysis and lactate release in astrocytes [155,156].”
Background
Lactylation, an emerging hallmark of metabolic reprogramming: Current progress and open challenges
Liu, X., Zhang, Y., Li, W., & Zhou, X. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.972020 · Cited by 146
“A classic example is the astrocyte-neuron lactate shuttle hypothesis, holding that neurons can metabolize lactate produced by astrocytes and consecutively released glutamate, in turn, for astrocytes uptake (Pellerin and Magistretti, 1994).”
Background
Interaction between Astrocytes and Neurons Studied using a Mathematical Model of Compartmentalized Energy Metabolism
Aubert, A., & Costalat, R. (2005) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/sj.jcbfm.9600144 · Cited by 142
“In the last decade, Pellerin and Magistretti (1994) proposed an integrated view of the relationship between brain activity and astrocytic and neuronal metabolism, stating that: (i) during neural activity, glutamate, after being released by presynaptic glutamatergic neurons, is taken up by…”
BackgroundMethodInfluential
Glutamate mediates acute glucose transport inhibition in hippocampal neurons
Porras, O. H., Loaiza, A., & Barros, L. F. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.1882-04.2004 · Cited by 139
“Pellerin and Magistretti proposed that neuronal firing may be supported pref - erentially by lactate ( Pellerin and Magistretti , 1994 ; Magistretti et al .”
Influential
Synapses: The Brain’s Energy-Demanding Sites
Faria‐Pereira, A., & Morais, V. A. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23073627 · Cited by 152
“In 1994, a possible mechanism to explain how synaptic energetic demands are fulfilled upon synaptic activity, known as the astrocyte-neuron lactate shuttle (ANLS) hypothesis, was described [50].”
Background
Blockade of lactate transport exacerbates delayed neuronal damage in a rat model of cerebral ischemia
Schurr, A., Payne, R. S., Miller, J. J., Tseng, M. T., & Rigor, B. M. (2001) · Brain Research · doi:10.1016/s0006-8993(01)02082-0 · Cited by 139
Reactive astrocytes give neurons less support: implications for Alzheimer's disease
Steele, M. L., & Robinson, S. R. (2010) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2010.09.018 · Cited by 145
A quantitative analysis of l ‐glutamate‐regulated Na+ dynamics in mouse cortical astrocytes: implications for cellular bioenergetics
Chatton, J., Marquet, P. P., & Magistretti, P. J. (2000) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2000.00269.x · Cited by 138
Glia fuel neurons with locally synthesized ketone bodies to sustain memory under starvation
Silva, B., Mantha, O. L., Schor, J., Pascual, A., Plaçais, P.-Y., Pavlowsky, A., & Préat, T. (2022) · Nature Metabolism · doi:10.1038/s42255-022-00528-6 · Cited by 145
“During starvation, FAs are mobilized from the internal stores of cortex glia via the action of the lipase Bmm (3).”
Background
Role of the Glyoxalase System in Astrocyte-Mediated Neuroprotection
Bélanger, M., Yang, J.-Y., Petit, J.-M., Laroche, T., Magistretti, P. J., & Allaman, I. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.1249-11.2011 · Cited by 140
“Numerous reports have shown that astrocytes display high metabolic plasticity in terms of glucose utilization, which is not the case for neurons (Pellerin and Magistretti, 1994; Almeida et al., 2001; Prapong et al., 2002; Porras et al., 2004; Gavillet et al., 2008; Allaman et al., 2010; Bélanger…”
Background
Neuronal damage and cognitive impairment associated with hypoglycemia: An integrated view
Languren, G., Montiel, T., Julio-Amilpas, A., & Massieu, L. (2013) · Neurochemistry International · doi:10.1016/j.neuint.2013.06.018 · Cited by 141
“On the other hand, several studies have suggested that lactate produced in glial cells is released and transported to neurons where it can be used as a metabolic substrate during high-energy demand (Belánger et al., 2011; Pellerin and Magistretti, 1994; Pellerin, 2010).”
Lactate, not pyruvate, is neuronal aerobic glycolysis end product: An in vitro electrophysiological study
Schurr, A., & Payne, R. S. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2007.05.002 · Cited by 138
Energy Dynamics in the Brain: Contributions of Astrocytes to Metabolism and pH Homeostasis
Deitmer, J. W., Theparambil, S. M., Ruminot, I., Noor, S. I., & Becker, H. M. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.01301 · Cited by 137
How Astrocytes Feed Hungry Neurons
Pellerin, L. (2005) · Molecular Neurobiology · doi:10.1385/mn:32:1:059 · Cited by 149
“Glutamate (the major excitatory neurotransmitter in the CNS) was shown to enhance glucose utilization in cultured astrocytes, as measured by the uptake of the glucose analog 2-deoxyglucose (16).”
BackgroundSelf-citation
Astrocytes in stress accumulate lipid droplets
Smolič, T., Tavčar, P., Horvat, A., Černe, U., Halužan Vasle, A., Tratnjek, L., Kreft, M. E., Scholz, N., Matis, M., Petan, T., et al. (2021) · Glia · doi:10.1002/glia.23978 · Cited by 127
“…during times of stress), when the metabolic demands of neural cells are increased, despite normal oxygen levels, astrocytes metabolize glycogen to glucose and further into lactate in the process of aerobic glycolysis (Bélanger et al., 2011; Dienel & Cruz, 2016; Pellerin & Magistretti, 1994).”
Background
Astrocyte metabolism and signaling pathways in the CNS
Zhang, Y.-M., Qi, Y., Gao, Y.-N., Chen, W.-G., Zhou, T., Zang, Y., & Li, J. X. (2023) · Frontiers in Neuroscience · doi:10.3389/fnins.2023.1217451 · Cited by 152
“The lactate produced is then released extracellularly and taken up by surrounding neurons to fuel oxidative metabolism during activity (Pellerin and Magistretti, 1994).”
Background
Comparison of Lactate and Glucose Metabolism in Cultured Neocortical Neurons and Astrocytes Using 13C-NMR Spectroscopy
Waagepetersen, H. S., Bakken, I. J., Larsson, O. M., Sonnewald, U., & Schousboe, A. (1998) · Developmental Neuroscience · doi:10.1159/000017326 · Cited by 135
Functional Studies in Cultured Astrocytes
Hertz, L., Peng, L., & Lai, J. C. K. (1998) · Methods · doi:10.1006/meth.1998.0686 · Cited by 136
Pyruvate Administered After Severe Hypoglycemia Reduces Neuronal Death and Cognitive Impairment
Suh, S. W., Aoyama, K., Matsumori, Y., Liu, J., & Swanson, R. A. (2005) · Diabetes · doi:10.2337/diabetes.54.5.1452 · Cited by 135
Functional connectivity and network analysis of midbrain and brainstem nuclei
Bär, K.-J., de la Cruz, F., Schumann, A., Koehler, S., Sauer, H., Critchley, H., & Wagner, G. (2016) · NeuroImage · doi:10.1016/j.neuroimage.2016.03.071 · Cited by 134
“Furthermore, there is accumulating information about the function of the neurovascular unit regarding the association between changes in blood flow and metabolism, the synaptic activity of glutamate and its recycling through astrocytes (Pellerin and Magistretti, 1994; Raichle, 2015).”
Background
Effects of cerebral perfusion pressure and increased fraction of inspired oxygen on brain tissue oxygen, lactate and glucose in patients with severe head injury
Reinert, M., Barth, A., Rothen, H.-U., Schaller, B. J., Takala, J. A., & Seiler, R. W. (2003) · Acta Neurochirurgica · doi:10.1007/s00701-003-0027-0 · Cited by 134
Cerebral Energy Metabolism in Hepatic Encephalopathy and Hyperammonemia
Rao, K. V. R., & Norenberg, M. D. (2001) · Metabolic Brain Disease · doi:10.1023/a:1011666612822 · Cited by 134
“Glutamate plays a pivotal role in the CNS as a major excitatory neurotransmitter and is involved in several critical reactions associated with cerebral energy metabolism, as well as with metabolic trafficking between neurons and astrocytes (Benjamin and Quastel, 1972; Pellerin and Magistretti, 1994; Schousboe et al.,…”
Background
Macrophages treated with particulate matter PM 2.5 induce selective neurotoxicity through glutaminase‐mediated glutamate generation
Liu, F., Huang, Y., Zhang, F., Chen, Q., Wu, B., Rui, W., Zheng, J., & Ding, W. (2015) · Journal of Neurochemistry · doi:10.1111/jnc.13135 · Cited by 138
Unraveling the complex metabolic nature of astrocytes
Bouzier-Sore, A.-K., & Pellerin, L. (2013) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2013.00179 · Cited by 134
“Moreover, using the same approach, the same group was able to demonstrate that the glycolytic action of potassium in astrocytes requires the implication of the Na+/HCO−3 cotransporter NBCe1, while the Na+/K+ ATPase only plays a permissive role in this case (Ruminot et al., 2011).”
MethodSelf-citation
Glycolytic Metabolism, Brain Resilience, and Alzheimer’s Disease
Zhang, X., Alshakhshir, N., & Zhao, L. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.662242 · Cited by 134
Robust glycogen shunt activity in astrocytes: Effects of glutamatergic and adrenergic agents
Walls, A. B., Heimbürger, C. M., Bouman, S. D., Schousboe, A., & Waagepetersen, H. S. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.09.058 · Cited by 133
Individual variability in the shape and amplitude of the BOLD‐HRF correlates with endogenous GABAergic inhibition
Muthukumaraswamy, S. D., Evans, J., Edden, R. A. E., Wise, R. G., & Singh, K. D. (2011) · Human Brain Mapping · doi:10.1002/hbm.21223 · Cited by 136
“Relatively decreased principal cell activity would then reduce the metabolic costs associated with glutamate cycling [Magistretti et al., 1999; Pellerin and Magistretti, 1994] and therefore cause an overall decreased BOLD response.”
Background
The effects of trifluoperazine on brain edema, aquaporin-4 expression and metabolic markers during the acute phase of stroke using photothrombotic mouse model
Sylvain, N. J., Salman, M. M., Pushie, M. J., Hou, H., Meher, V. R., Herlo, R., Peeling, L. M., & Kelly, M. (2021) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2021.183573 · Cited by 132
13C MR Spectroscopy Study of Lactate as Substrate for Rat Brain
Qu, H., Haberg, A. K., Haraldseth, O., Unsgård, G., & Sonnewald, U. (2000) · Developmental Neuroscience · doi:10.1159/000017472 · Cited by 132
“In cultured astrocytes, lactate release was shown to be increased by glutamate uptake [Pellerin and Magistretti, 1994], and in freely moving rats, administration of glutamate caused a transient increase in dialysate lactate concentration [Demestre et al.”
Background
ATP-Sensitive Potassium Channel-Mediated Lactate Effect on Orexin Neurons: Implications for Brain Energetics during Arousal
Parsons, M. P., & Hirasawa, M. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.5741-09.2010 · Cited by 138
“As glutamate stimulates lactate production in astrocytes (Pellerin and Magistretti, 1994), our result indicates that excitatory inputs from other brain areas would have a dual excitatory effect on orexin neurons.”
BackgroundResultInfluential

Authors: Pellerin, L., & Magistretti, P. J.
Affiliations: University of Lausanne (CH)
ORCID: Pellerin, L
Magistretti, P J
Venue: Proceedings of the National Academy of Sciences
Publisher: National Academy of Sciences
Published: 1994-10-25
Volume: 91
Issue: 22
Pages: 10625-10629
ISSN: 0027-8424 (ISSN-L)
1091-6490
DOI: 10.1073/pnas.91.22.10625
PMC: PMC45074
OpenAlex: W2092635505
Cited by: 2,927
References: 41
Citations by year: 2026: 143 · 2025: 146 · 2024: 138 · 2023: 137 · 2022: 147 · 2021: 168 · 2020: 122 · 2019: 133 · 2018: 109 · 2017: 113 · 2016: 107 · 2015: 116 · 2014: 126 · 2013: 91 · 2012: 88
FWCI: 10.61
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Proceedings of the National Academy of Sciences (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Infoscience (Ecole Polytechnique Fédérale de Lausanne) (submittedVersion)
Infoscience (Ecole Polytechnique Fédérale de Lausanne) (submittedVersion, cc-by-nc-nd)
IRIS (submittedVersion)
SERVAL (Université de Lausanne) (submittedVersion)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Amino Acid Enzymes and Metabolism
Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Keywords: glutamate uptake, astrocytes, aerobic glycolysis, Na+/K+-ATPase, neuronal activity, glucose utilization, lactic acid production, nonoxidative glucose metabolism, astrocyte-neuron interaction
MeSH terms: Sodium-Potassium-Exchanging ATPase, Aerobiosis, Animals, Animals, Newborn, Astrocytes, Biological Transport, Brain, Cells, Cultured, Cerebral Cortex, Deoxyglucose, Glycolysis, Lactates, Models, Neurological, Neurons, Radionuclide Imaging, Tritium, Excitatory Amino Acid Antagonists, Glutamic Acid, Mice

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Glutamate uptake into astrocytes stimulates aerobic glycolysis: a mechanism coupling neuronal activity to glucose utilization.

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