Glucose metabolism links astroglial mitochondria to cannabinoid effects.

Animals Astrocytes / cytology Cannabinoid Receptor Agonists / pharmacology Cells, Cultured Dronabinol / pharmacology Electron Transport Complex I / chemistry Energy Metabolism / drug effects Glucose / metabolism Glycolysis / drug effects Humans Hypoxia-Inducible Factor 1 / metabolism Lactic Acid / metabolism Male Mice Mitochondria / drug effects Mitochondrial Membranes / metabolism Oxidation-Reduction Phosphorylation Reactive Oxygen Species / metabolism Receptor, Cannabinoid, CB1 / agonists Social Behavior

Journal

Nature

ISSN: 1476-4687

Titre abrégé: Nature

Pays: England

ID NLM: 0410462

Informations de publication

Date de publication:
07 2020

Historique:

received: 09 03 2018

accepted: 29 05 2020

pubmed: 10 7 2020

medline: 21 10 2020

entrez: 10 7 2020

Statut: ppublish

Résumé

Astrocytes take up glucose from the bloodstream to provide energy to the brain, thereby allowing neuronal activity and behavioural responses

Identifiants

DOI: 10.1038/s41586-020-2470-y PMID: 32641832

pubmed: 32641832

doi: 10.1038/s41586-020-2470-y

pii: 10.1038/s41586-020-2470-y

doi:

Substances chimiques

Cannabinoid Receptor Agonists 0

Hypoxia-Inducible Factor 1 0

Reactive Oxygen Species 0

Receptor, Cannabinoid, CB1 0

Lactic Acid 33X04XA5AT

Dronabinol 7J8897W37S

Electron Transport Complex I EC 7.1.1.2

NDUFS4 protein, human EC 7.1.1.2

Glucose IY9XDZ35W2

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

Pagination

603-608

Subventions

Organisme : NIH HHS

ID : 1R21DA037678-01

Pays : United States

Organisme : European Research Council

Pays : International

Commentaires et corrections

Type : CommentIn

Références

Magistretti, P. J. & Allaman, I. Lactate in the brain: from metabolic end-product to signalling molecule. Nat. Rev. Neurosci. 19, 235–249 (2018).

pubmed: 29515192

Barros, L. F. & Weber, B. CrossTalk proposal: an important astrocyte-to-neuron lactate shuttle couples neuronal activity to glucose utilisation in the brain. J. Physiol. 596, 347–350 (2018).

pubmed: 29292516 pmcid: 5792514

Bolaños, J. P. Bioenergetics and redox adaptations of astrocytes to neuronal activity. J. Neurochem. 139, 115–125 (2016).

pubmed: 26968531 pmcid: 5018236

Suzuki, A. et al. Astrocyte-neuron lactate transport is required for long-term memory formation. Cell 144, 810–823 (2011).

pubmed: 21376239 pmcid: 3073831

Allen, N. J. & Barres, B. A. Glia — more than just brain glue. Nature 457, 675–677 (2009).

pubmed: 19194443

Hansson, E. & Rönnbäck, L. Astrocytes in neurotransmission. a review. Cell. Mol. Biol. 36, 487–496 (1990).

pubmed: 1963574

Araque, A. et al. Gliotransmitters travel in time and space. Neuron 81, 728–739 (2014).

pubmed: 24559669 pmcid: 4107238

Almeida, A., Almeida, J., Bolaños, J. P. & Moncada, S. Different responses of astrocytes and neurons to nitric oxide: the role of glycolytically generated ATP in astrocyte protection. Proc. Natl Acad. Sci. USA 98, 15294–15299 (2001).

pubmed: 11742096

Lopez-Fabuel, I. et al. Complex I assembly into supercomplexes determines differential mitochondrial ROS production in neurons and astrocytes. Proc. Natl Acad. Sci. USA 113, 13063–13068 (2016).

pubmed: 27799543

Semenza, G. L., Roth, P. H., Fang, H. M. & Wang, G. L. Transcriptional regulation of genes encoding glycolytic enzymes by hypoxia-inducible factor 1. J. Biol. Chem. 269, 23757–23763 (1994).

pubmed: 8089148

Busquets-Garcia, A., Bains, J. & Marsicano, G. CB

pubmed: 28862250

Araque, A., Castillo, P. E., Manzoni, O. J. & Tonini, R. Synaptic functions of endocannabinoid signaling in health and disease. Neuropharmacology 124, 13–24 (2017).

pubmed: 28625718 pmcid: 5662005

Robin, L. M. et al. Astroglial CB

pubmed: 29779943

Bénard, G. et al. Mitochondrial CB

pubmed: 22388959

Hebert-Chatelain, E. et al. A cannabinoid link between mitochondria and memory. Nature 539, 555–559 (2016).

pubmed: 27828947

Mendizabal-Zubiaga, J. et al. Cannabinoid CB

pubmed: 27826249 pmcid: 5078489

Aquila, S. et al. Human sperm anatomy: ultrastructural localization of the cannabinoid1 receptor and a potential role of anandamide in sperm survival and acrosome reaction. Anat. Rec. 293, 298–309 (2010).

Koch, M. et al. Hypothalamic POMC neurons promote cannabinoid-induced feeding. Nature 519, 45–50 (2015).

pubmed: 25707796 pmcid: 4496586

Gutiérrez-Rodríguez, A. et al. Localization of the cannabinoid type-1 receptor in subcellular astrocyte compartments of mutant mouse hippocampus. Glia 66, 1417–1431 (2018).

pubmed: 29480581

Hebert-Chatelain, E. et al. Cannabinoid control of brain bioenergetics: exploring the subcellular localization of the CB

pubmed: 24944910 pmcid: 4060213

Han, J. et al. Acute cannabinoids impair working memory through astroglial CB

pubmed: 22385967

Guaras, A. M. & Enríquez, J. A. Building a beautiful beast: mammalian respiratory complex I. Cell Metab. 25, 4–5 (2017).

pubmed: 28076765

Mimaki, M., Wang, X., McKenzie, M., Thorburn, D. R. & Ryan, M. T. Understanding mitochondrial complex I assembly in health and disease. Biochim. Biophys. Acta 1817, 851–862 (2012).

pubmed: 21924235

De Rasmo, D., Panelli, D., Sardanelli, A. M. & Papa, S. cAMP-dependent protein kinase regulates the mitochondrial import of the nuclear encoded NDUFS4 subunit of complex I. Cell Signal. 20, 989–997 (2008).

pubmed: 18291624

Hammond, S. L., Leek, A. N., Richman, E. H. & Tjalkens, R. B. Cellular selectivity of AAV serotypes for gene delivery in neurons and astrocytes by neonatal intracerebroventricular injection. PLoS ONE 12, e0188830 (2017).

pubmed: 29244806 pmcid: 5731760

Vicente-Gutierrez, C. et al. Astrocytic mitochondrial ROS modulate brain metabolism and mouse behavior. Nat. Metab. 1, 201–211 (2019).

Chandel, N. S. et al. Mitochondrial reactive oxygen species trigger hypoxia-induced transcription. Proc. Natl Acad. Sci. USA 95, 11715–11720 (1998).

pubmed: 9751731

Patten, D. A. et al. Hypoxia-inducible factor-1 activation in nonhypoxic conditions: the essential role of mitochondrial-derived reactive oxygen species. Mol. Biol. Cell 21, 3247–3257 (2010).

pubmed: 20660157 pmcid: 2938389

Shadel, G. S. & Horvath, T. L. Mitochondrial ROS signaling in organismal homeostasis. Cell 163, 560–569 (2015).

pubmed: 26496603 pmcid: 4634671

Semenza, G. L. Hypoxia-inducible factors: coupling glucose metabolism and redox regulation with induction of the breast cancer stem cell phenotype. EMBO J. 36, 252–259 (2017).

pubmed: 28007895

Semenza, G. L. Dynamic regulation of stem cell specification and maintenance by hypoxia-inducible factors. Mol. Aspects Med. 47–48, 15–23 (2016).

pubmed: 26549347

Almeida, A., Moncada, S. & Bolaños, J. P. Nitric oxide switches on glycolysis through the AMP protein kinase and 6-phosphofructo-2-kinase pathway. Nat. Cell Biol. 6, 45–51 (2004).

pubmed: 14688792

Herrero-Mendez, A. et al. The bioenergetic and antioxidant status of neurons is controlled by continuous degradation of a key glycolytic enzyme by APC/C-Cdh1. Nat. Cell Biol. 11, 747–752 (2009).

pubmed: 19448625

Jimenez-Blasco, D., Santofimia-Castaño, P., Gonzalez, A., Almeida, A. & Bolaños, J. P. Astrocyte NMDA receptors’ activity sustains neuronal survival through a Cdk5–Nrf2 pathway. Cell Death Differ. 22, 1877–1889 (2015).

pubmed: 25909891 pmcid: 4648333

Morland, C. et al. The lactate receptor, G-protein-coupled receptor 81/hydroxycarboxylic acid receptor 1: expression and action in brain. J. Neurosci. Res. 93, 1045–1055 (2015).

pubmed: 25881750

Liu, C. et al. 3,5-Dihydroxybenzoic acid, a specific agonist for hydroxycarboxylic acid 1, inhibits lipolysis in adipocytes. J. Pharmacol. Exp. Ther. 341, 794–801 (2012).

pubmed: 22434674

Pierre, K., Magistretti, P. J. & Pellerin, L. MCT2 is a major neuronal monocarboxylate transporter in the adult mouse brain. J. Cereb. Blood Flow Metab. 22, 586–595 (2002).

pubmed: 11973431

Mazuel, L. et al. A neuronal MCT2 knockdown in the rat somatosensory cortex reduces both the NMR lactate signal and the BOLD response during whisker stimulation. PLoS One 12, e0174990 (2017).

pubmed: 28388627 pmcid: 5384673

Hollis, F. et al. Mitochondrial function in the brain links anxiety with social subordination. Proc. Natl Acad. Sci. USA 112, 15486–15491 (2015).

pubmed: 26621716

Picard, M., McEwen, B. S., Epel, E. S. & Sandi, C. An energetic view of stress: focus on mitochondria. Front. Neuroendocrinol. 49, 72–85 (2018).

pubmed: 29339091 pmcid: 5964020

Melser, S. et al. Functional analysis of mitochondrial CB1 cannabinoid receptors (mtCB1) in the brain. Methods Enzymol. 593, 143–174 (2017).

pubmed: 28750801

Jollé, C., Déglon, N., Pythoud, C., Bouzier-Sore, A. K. & Pellerin, L. Development of AAV2/DJ-based viral vectors to selectively downregulate the expression of neuronal or astrocytic target proteins in the rat central nervous system. Front Mol. Neurosci. 12, 201 (2019).

pubmed: 31481874 pmcid: 6710342

Marsicano, G. et al. The endogenous cannabinoid system controls extinction of aversive memories. Nature 418, 530–534 (2002).

pubmed: 12152079

Puente, N., Bonilla-Del Río, I., Achicallende, S., Nahirney, P. C. & Grandes, P. High-resolution immunoelectron microscopy techniques for revealing distinct subcellular type 1 cannabinoid receptor domains in brain. Bio-protocol 9, e3145 (2019).

De Rasmo, D. et al. Activation of the cAMP cascade in human fibroblast cultures rescues the activity of oxidatively damaged complex I. Free Radic. Biol. Med. 52, 757–764 (2012).

pubmed: 22198267

Acin-Perez, R., Fernandez-Silva, P., Peleato, M. L., Perez-Martos, A. & Enriquez, J. A. Respiratory active mitochondrial supercomplexes. Mol. Cell 32, 529–539 (2008).

pubmed: 19026783

Belousov, V. V. et al. Genetically encoded fluorescent indicator for intracellular hydrogen peroxide. Nat. Methods 3, 281–286 (2006).

pubmed: 16554833

Darley-Usmar, V. M., Rickwood, D. & Wilson, M. T. (eds) Mitochondria: A Practical Approach (IRL, 1987).

King, T. E. in Methods in Enzymology Vol. 10 (eds Estabrook, R. W. & Pullman, M. E.) 216–225 (Academic, 1967).

Wharton, D. C. & Tzagoloff, A. in Methods in Enzymology Vol. 10 (eds Estabrook, R. W. & Pullman, M. E.) 245–250 (Academic, 1967).

Shepherd, D. & Garland, P. B. The kinetic properties of citrate synthase from rat liver mitochondria. Biochem. J. 114, 597–610 (1969).

pubmed: 5820645 pmcid: 1184933

Busquets-Garcia, A. et al. Pregnenolone blocks cannabinoid-induced acute psychotic-like states in mice. Mol. Psychiatry 22, 1594–1603 (2017).

pubmed: 28220044 pmcid: 5447368

Soria-Gómez, E. et al. Habenular CB

pubmed: 26412490

Paxinos, G. & Franklin, K. B. J. The Mouse Brain in Stereotaxic Coordinates (Academic, 2001).

Martin, P. M. & O’Callaghan, J. P. A direct comparison of GFAP immunocytochemistry and GFAP concentration in various regions of ethanol-fixed rat and mouse brain. J. Neurosci. Methods 58, 181–192 (1995).

pubmed: 7475226

Huang, H. et al. Chronic and acute intranasal oxytocin produce divergent social effects in mice. Neuropsychopharmacol. 39, 1102–1114 (2014).