Bidirectional astrocytic GLUT1 activation by elevated extracellular K

3-O-methylglucose fluorescence microscopy genetically encoded FRET sensor glucose transport

Journal

Glia
ISSN: 1098-1136
Titre abrégé: Glia
Pays: United States
ID NLM: 8806785

Informations de publication

Date de publication:
04 2021
Historique:
received: 24 07 2020
revised: 23 11 2020
accepted: 25 11 2020
pubmed: 6 12 2020
medline: 8 2 2022
entrez: 5 12 2020
Statut: ppublish

Résumé

The acute rise in interstitial K

Identifiants

pubmed: 33277953
doi: 10.1002/glia.23944
doi:

Substances chimiques

Glucose Transporter Type 1 0
Lactic Acid 33X04XA5AT
Glucose IY9XDZ35W2

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1012-1021

Informations de copyright

© 2020 Wiley Periodicals LLC.

Références

Attwell, D., & Laughlin, S. B. (2001). An energy budget for signaling in the grey matter of the brain. Journal of Cerebral Blood Flow and Metabolism, 21, 1133-1145.
Baeza-Lehnert, F., Saab, A. S., Gutierrez, R., Larenas, V., Diaz, E., Horn, M., … Barros, L. F. (2019). Non-canonical control of neuronal energy status by the Na(+) pump. Cell Metabolism, 29, 668-680.
Bak, L. K., & Walls, A. B. (2018). Lack of evidence supporting an astrocyte-to-neuron lactate shuttle coupling neuronal activity to glucose utilisation in the brain. The Journal of Physiology, 596, 351-353.
Barros, L. F. (1999). Measurement of sugar transport in single living cells. Pflügers Archiv, 437, 763-770.
Barros, L. F., Barnes, K., Ingram, J. C., Castro, J., Porras, O. H., & Baldwin, S. A. (2001). Hyperosmotic shock induces both activation and translocation of glucose transporters in mammalian cells. Pflügers Archiv, 442, 614-621.
Barros, L. F., Bittner, C. X., Loaiza, A., & Porras, O. H. (2007). A quantitative overview of glucose dynamics in the gliovascular unit. Glia, 55, 1222-1237.
Barros, L. F., Porras, O. H., & Bittner, C. X. (2005). Why glucose transport in the brain matters for PET. Trends in Neurosciences, 28, 117-119.
Barros, L. F., Ruminot, I., San Martín, A., Lerchundi, R., Fernández-Moncada, I., & Baeza-Lehnert, F. (2020). Aerobic glycolysis in the brain: Warburg and Crabtree contra Pasteur. Neurochemical Research. https://doi.org/10.1007/s11064-020-02964-w. [Online ahead of print].
Barros, L. F., San, M. A., Ruminot, I., Sandoval, P. Y., Fernandez-Moncada, I., Baeza-Lehnert, F., … Alegria, K. (2017). Near-critical GLUT1 and neurodegeneration. Journal of Neuroscience Research, 95, 2267-2274.
Barros, L. F., San Martin, A., Sotelo-Hitschfeld, T., Lerchundi, R., Fernández-Moncada, I., Ruminot, I., … Espinoza, D. (2013). Small is fast: Astrocytic glucose and lactate metabolism at cellular resolution. Frontiers in Cellular Neuroscience, 7, 27. https://doi.org/10.3389/fncel.2013.00027.
Barros, L. F., & Weber, B. (2018). CrossTalk proposal: An important astrocyte-to-neuron lactate shuttle couples neuronal activity to glucose utilisation in the brain. The Journal of Physiology, 596, 347-350.
Bittner, C. X., Loaiza, A., Ruminot, I., Larenas, V., Sotelo-Hitschfeld, T., Gutiérrez, R., … Barros, L. F. (2010). High resolution measurement of the glycolytic rate. Frontiers in Neuroenergetics, 2, 1-11. https://doi.org/10.3389/fnene.2010.00026
Bittner, C. X., Valdebenito, R., Ruminot, I., Loaiza, A., Larenas, V., Sotelo-Hitschfeld, T., … Barros, L. F. (2011). Fast and reversible stimulation of astrocytic glycolysis by K+ and a delayed and persistent effect of glutamate. The Journal of Neuroscience, 31, 4709-4713.
Carruthers, A. (1990). Facilitated diffusion of glucose. Physiological Reviews, 70, 1135-1176.
Chuquet, J., Quilichini, P., Nimchinsky, E. A., & Buzsaki, G. (2010). Predominant enhancement of glucose uptake in astrocytes versus neurons during activation of the somatosensory cortex. The Journal of Neuroscience, 30, 15298-15303.
Deng, D., Xu, C., Sun, P., Wu, J., Yan, C., Hu, M., & Yan, N. (2014). Crystal structure of the human glucose transporter GLUT1. Nature, 510, 121-125.
Diaz-Garcia, C. M., Mongeon, R., Lahmann, C., Koveal, D., Zucker, H., & Yellen, G. (2017). Neuronal stimulation triggers neuronal glycolysis and not lactate uptake. Cell Metabolism, 26, 361-374.
Dienel, G. A. (2019). Brain glucose metabolism: Integration of energetics with function. Physiological Reviews, 99, 949-1045.
Ding, F., O'Donnell, J., Xu, Q., Kang, N., Goldman, N., & Nedergaard, M. (2016). Changes in the composition of brain interstitial ions control the sleep-wake cycle. Science, 352, 550-555.
Fehr, M., Lalonde, S., Lager, I., Wolff, M. W., & Frommer, W. B. (2003). In vivo imaging of the dynamics of glucose uptake in the cytosol of COS-7 cells by fluorescent nanosensors. The Journal of Biological Chemistry, 278, 19127-19133.
Fernandez-Moncada, I., Ruminot, I., Robles-Maldonado, D., Alegria, K., Deitmer, J. W., & Barros, L. F. (2018). Neuronal control of astrocytic respiration through a variant of the Crabtree effect. Proceedings of the National Academy of Sciences of the United States of America, 115, 1623-1628.
Ferreira, J. M., Burnett, A. L., & Rameau, G. A. (2011). Activity-dependent regulation of surface glucose transporter-3. The Journal of Neuroscience, 31, 1991-1999.
Frohlich, F., Bazhenov, M., Iragui-Madoz, V., & Sejnowski, T. J. (2008). Potassium dynamics in the epileptic cortex: New insights on an old topic. The Neuroscientist, 14, 422-433.
Giaume, C. B., Naus, C. C., Saez, J. C., & Leybaert, L. (2021). Glial connexins and pannexins in the healthy and diseased brain. Physiological Reviews, 101(1), 93-145.
Hasel, P., Dando, O., Jiwaji, Z., Baxter, P., Todd, A. C., Heron, S., … Hardingham, G. E. (2017). Neurons and neuronal activity control gene expression in astrocytes to regulate their development and metabolism. Nature Communications, 8, 15132.
Hou, B. H., Takanaga, H., Grossmann, G., Chen, L. Q., Qu, X. Q., Jones, A. M., … Frommer, W. B. (2011). Optical sensors for monitoring dynamic changes of intracellular metabolite levels in mammalian cells. Nature Protocols, 6, 1818-1833.
Kacem, K., Lacombe, P., Seylaz, J., & Bonvento, G. (1998). Structural organization of the perivascular astrocyte endfeet and their relationship with the endothelial glucose transporter: A confocal microscopy study. Glia, 23, 1-10.
Kohler, S., Winkler, U., Sicker, M., & Hirrlinger, J. (2018). NBCe1 mediates the regulation of the NADH/NAD(+) redox state in cortical astrocytes by neuronal signals. Glia, 66, 2233-2245.
Leybaert, L. (2005). Neurobarrier coupling in the brain: A partner of neurovascular and neurometabolic coupling? Journal of Cerebral Blood Flow and Metabolism, 25, 2-16.
Loaiza, A., Porras, O. H., & Barros, L. F. (2003). Glutamate triggers rapid glucose transport stimulation in astrocytes as evidenced by real-time confocal microscopy. The Journal of Neuroscience, 23, 7337-7342.
Lowry, J. P., O'Neill, R. D., Boutelle, M. G., & Fillenz, M. (1998). Continuous monitoring of extracellular glucose concentrations in the striatum of freely moving rats with an implanted glucose biosensor. Journal of Neurochemistry, 70, 391-396.
Machler, P., Wyss, M. T., Elsayed, M., Stobart, J., Gutierrez, R., von Faber-Castell, A., … Weber, B. (2016). In vivo evidence for a lactate gradient from astrocytes to neurons. Cell Metabolism, 23, 94-102.
Magistretti, P. J., & Allaman, I. (2018). Lactate in the brain: From metabolic end-product to signalling molecule. Nature Reviews. Neuroscience, 19, 235-249.
Malaisse-Lagae, F., Giroix, M. H., Sener, A., & Malaisse, W. J. (1986). Phosphorylation of 3-O-methyl-D-glucose by yeast and beef hexokinase. FEBS Letters, 198, 292-294.
Mamczur, P., Borsuk, B., Paszko, J., Sas, Z., Mozrzymas, J., Wisniewski, J. R., … Rakus, D. (2015). Astrocyte-neuron crosstalk regulates the expression and subcellular localization of carbohydrate metabolism enzymes. Glia, 63, 328-340.
Mathiisen, T. M., Lehre, K. P., Danbolt, N. C., & Ottersen, O. P. (2010). The perivascular astroglial sheath provides a complete covering of the brain microvessels: An electron microscopic 3D reconstruction. Glia, 58, 1094-1103.
Miyawaki, A., Griesbeck, O., Heim, R., & Tsien, R. Y. (1999). Dynamic and quantitative Ca2+ measurements using improved cameleons. Proceedings of the National Academy of Sciences of the United States of America, 96, 2135-2140.
Pellerin, L., & Magistretti, P. J. (1994). Glutamate uptake into astrocytes stimulates aerobic glycolysis: A mechanism coupling neuronal activity to glucose utilization. Proceedings of the National Academy of Sciences of the United States of America, 91, 10625-10629.
Porras, O. H., Ruminot, I., Loaiza, A., & Barros, L. F. (2008). Na(+)-Ca(2+) cosignaling in the stimulation of the glucose transporter GLUT1 in cultured astrocytes. Glia, 56, 59-68.
Raichle, M. E., & Mintun, M. A. (2006). Brain work and brain imaging. Annual Review of Neuroscience, 29, 449-476.
Rasmussen, R., Nicholas, E., Petersen, N. C., Dietz, A. G., Xu, Q., Sun, Q., & Nedergaard, M. (2019). Cortex-wide changes in extracellular potassium ions parallel brain state transitions in awake behaving mice. Cell Reports, 28, 1182-1194.
Reivich, M., Kuhl, D., Wolf, A., Greenberg, J., Phelps, M., Ido, T., … Sokoloff, L. (1979). The [18F]fluorodeoxyglucose method for the measurement of local cerebral glucose utilization in man. Circulation Research, 44, 127-137.
Rose, C. R., & Ransom, B. R. (1996). Intracellular sodium homeostasis in rat hippocampal astrocytes. The Journal of Physiology, 491, 291-305.
Ruminot, I., Gutiérrez, R., Peña-Munzenmeyer, G., Añazco, C., Sotelo-Hitschfeld, T., Lerchundi, R., … Barros, L. F. (2011). NBCe1 mediates the acute stimulation of astrocytic glycolysis by extracellular K+. The Journal of Neuroscience, 31, 14264-14271.
Ruminot, I., Schmalzle, J., Leyton, B., Barros, L. F., & Deitmer, J. W. (2017). Tight coupling of astrocyte energy metabolism to synaptic activity revealed by genetically encoded FRET nanosensors in hippocampal tissue. Journal of Cerebral Blood Flow and Metabolism, 39, 513-523.
Rusakov, D. A., & Kullmann, D. M. (1998). Extrasynaptic glutamate diffusion in the hippocampus: Ultrastructural constraints, uptake, and receptor activation. The Journal of Neuroscience, 18, 3158-3170.
Saab, A. S., Tzvetavona, I. D., Trevisiol, A., Baltan, S., Dibaj, P., Kusch, K., … Nave, K. A. (2016). Oligodendroglial NMDA receptors regulate glucose import and axonal energy metabolism. Neuron, 91, 119-132.
San Martín, A., Sotelo-Hitschfeld, T., Lerchundi, R., Fenandez-Moncada, I., Ceballo, S., Valdebenito, R., … Barros, L. F. (2014). Single-cell imaging tools for brain energy metabolism: A review. Neurophotonics, 1, 011004.
Simpson, I. A., Carruthers, A., & Vannucci, S. J. (2007). Supply and demand in cerebral energy metabolism: The role of nutrient transporters. Journal of Cerebral Blood Flow and Metabolism, 27, 1766-1791.
Sokoloff, L., Reivich, M., Kennedy, C., Des Rosiers, M. H., Patlak, C. S., Pettigrew, K. D., … Shinohara, M. (1977). The [14C]deoxyglucose method for the measurement of local cerebral glucose utilization: Theory, procedure, and normal values in the conscious and anesthetized albino rat. Journal of Neurochemistry, 28, 897-916.
Sotelo-Hitschfeld, T., Niemeyer, M. I., Machler, P., Ruminot, I., Lerchundi, R., Wyss, M. T., … Barros, L. F. (2015). Channel-mediated lactate release by k+-stimulated astrocytes. The Journal of Neuroscience, 35, 4168-4178.
Sykova, E. (1983). Extracellular K+ accumulation in the central nervous system. Progress in Biophysics and Molecular Biology, 42, 135-189.
Theparambil, S. M., Weber, T., Schmalzle, J., Ruminot, I., & Deitmer, J. W. (2016). Proton fall or bicarbonate rise: Glycolytic rate in mouse astrocytes is paved by intracellular alkalinization. The Journal of Biological Chemistry, 291, 19108-19117.
Vannucci, S. J., Maher, F., & Simpson, I. A. (1997). Glucose transporter proteins in brain: Delivery of glucose to neurons and glia. Glia, 21, 2-21.
Widdas, W. F. (1952). Inability of diffusion to account for placental glucose transfer in the sheep and consideration of the kinetics of a possible carrier transfer. The Journal of Physiology, 118, 23-39.
Zhang, Y., Chen, K., Sloan, S. A., Bennett, M. L., Scholze, A. R., O'Keeffe, S., … Wu, J. Q. (2014). An RNA-sequencing transcriptome and splicing database of glia, neurons, and vascular cells of the cerebral cortex. The Journal of Neuroscience, 34, 11929-11947.
Zuend, M., Saab, A. S., Wyss, M. T., Ferrari, K. D., Hösli, L., Looser, Z. J., … Weber, B. (2020). Arousal-induced cortical activity triggers lactate release from astrocytes. Nature Metabolism, 2, 179-191.

Auteurs

Ignacio Fernández-Moncada (I)

Centro de Estudios Científicos, Valdivia, Chile.
INSERM U1215 NeuroCentre Magendie, Bordeaux, France.

Daniel Robles-Maldonado (D)

Centro de Estudios Científicos, Valdivia, Chile.
Universidad Austral de Chile, Valdivia, Chile.

Pablo Castro (P)

Centro de Estudios Científicos, Valdivia, Chile.

Karin Alegría (K)

Centro de Estudios Científicos, Valdivia, Chile.

Robert Epp (R)

Institute of Fluid Dynamics, ETH Zurich, Zurich, Switzerland.

Iván Ruminot (I)

Centro de Estudios Científicos, Valdivia, Chile.

Luis Felipe Barros (LF)

Centro de Estudios Científicos, Valdivia, Chile.

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