Endocannabinoid signaling in oligodendroglia.
cannabinoid
differentiation
oligodendrocyte
signaling
Journal
Glia
ISSN: 1098-1136
Titre abrégé: Glia
Pays: United States
ID NLM: 8806785
Informations de publication
Date de publication:
01 2023
01 2023
Historique:
revised:
10
03
2022
received:
10
12
2021
accepted:
28
03
2022
pubmed:
13
4
2022
medline:
23
11
2022
entrez:
12
4
2022
Statut:
ppublish
Résumé
In the central nervous system, oligodendrocytes synthesize the myelin, a specialized membrane to wrap axons in a discontinuous way allowing a rapid saltatory nerve impulse conduction. Oligodendrocytes express a number of growth factors and neurotransmitters receptors that allow them to sense the environment and interact with neurons and other glial cells. Depending on the cell cycle stage, oligodendrocytes may respond to these signals by regulating their survival, proliferation, migration, and differentiation. Among these signals are the endocannabinoids, lipidic molecules synthesized from phospholipids in the plasma membrane in response to cell activation. Here, we discuss the evidence showing that oligodendrocytes express a full endocannabinoid signaling machinery involved in physiological oligodendrocyte functions that can be therapeutically exploited to promote remyelination in central nervous system pathologies.
Substances chimiques
Endocannabinoids
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
91-102Informations de copyright
© 2022 Wiley Periodicals LLC.
Références
Aguado, T., Huerga-Gómez, A., Sánchez-de la Torre, A., Resel, E., Chara, J. C., Matute, C., Mato, S., Galve-Roperh, I., Guzman, M., & Palazuelos, J. (2021). Δ 9 -tetrahydrocannabinol promotes functional remyelination in the mouse brain. British Journal of Pharmacology, 178, 4176-4192.
Alpár, A., Tortoriello, G., Calvigioni, D., Niphakis, M. J., Milenkovic, I., Bakker, J., Cameron, G. A., Hanics, J., Morris, C. V., Fuzik, J., Kovacs, G. G., Cravatt, B. F., Parnavelas, J. G., Andrews, W. D., Hurd, Y. L., Keimpema, E., & Harkany, T. (2014). Endocannabinoids modulate cortical development by configuring Slit2/Robo1 signalling. Nature Communications, 5, 4421.
Arevalo-Martin, A., Garcia-Ovejero, D., & Molina-Holgado, E. (2010). The endocannabinoid 2-arachidonoylglycerol reduces lesion expansion and white matter damage after spinal cord injury. Neurobiology of Disease, 38, 304-312.
Arevalo-Martin, A., Garcia-Ovejero, D., Rubio-Araiz, A., Gomez, O., Molina-Holgado, F., & Molina-Holgado, E. (2007). Cannabinoids modulate Olig2 and polysialylated neural cell adhesion molecule expression in the subventricular zone of post-natal rats through cannabinoid receptor 1 and cannabinoid receptor 2. The European Journal of Neuroscience, 26, 1548-1559.
Arevalo-Martin, A., Garcia-Ovejero, D., Sierra-Palomares, Y., Paniagua-Torija, B., Gonzalez-Gil, I., Ortega-Gutierrez, S., & Molina-Holgado, E. (2012). Early endogenous activation of CB1 and CB2 receptors after spinal cord injury is a protective response involved in spontaneous recovery. PLoS One, 7, e49057.
Arevalo-Martin, A., Molina-Holgado, E., & Garcia-Ovejero, D. (2016). Cannabinoids to treat spinal cord injury. Prog Neuro-Psychopharmacology Biol Psychiatry, 64, 190-199.
Arévalo-Martı́n, Á., Vela, J. M., Molina-Holgado, E., Borrell, J., & Guaza, C. (2003). Therapeutic action of cannabinoids in a murine model of multiple sclerosis. The Journal of Neuroscience, 23, 2511-2516.
Bénard, G., Massa, F., Puente, N., Lourenço, J., Bellocchio, L., Soria-Gómez, E., Matias, I., Delamarre, A., Metna-Laurent, M., Cannich, A., Hebert-Chatelain, E., Mulle, C., Ortega-Gutiérrez, S., Martín-Fontecha, M., Klugmann, M., Guggenhuber, S., Lutz, B., Gertsch, J., Chaouloff, F., … Marsicano, G. (2012). Mitochondrial CB1 receptors regulate neuronal energy metabolism. Nature Neuroscience, 15, 558-564.
Benito, C., Romero, J. P., Tolon, R. M., Clemente, D., Docagne, F., Hillard, C. J., Guaza, C., & Romero, J. (2007). Cannabinoid CB1 and CB2 receptors and fatty acid amide hydrolase are specific markers of plaque cell subtypes in human multiple sclerosis. The Journal of Neuroscience, 27, 2396-2402.
Bernal-Chico, A., Canedo, M., Manterola, A., Victoria Sánchez-Gómez, M., Pérez-Samartín, A., Rodríguez-Puertas, R., Matute, C., & Mato, S. (2015). Blockade of monoacylglycerol lipase inhibits oligodendrocyte excitotoxicity and prevents demyelination in vivo. Glia, 63, 163-176.
Berrendero, F., Garcia-Gil, L., Hernandez, M. L., Romero, J., Cebeira, M., de Miguel, R., Ramos, J. A., & Fernandez-Ruiz, J. J. (1998). Localization of mRNA expression and activation of signal transduction mechanisms for cannabinoid receptor in rat brain during fetal development. Development, 125, 3179-3188.
Berrendero, F., Sepe, N., Ramos, J. A., Di Marzo, V., & Fernández-Ruiz, J. J. (1999). Analysis of cannabinoid receptor binding and mRNA expression and endogenous cannabinoid contents in the developing rat brain during late gestation and early postnatal period. Synapse, 33, 181-191.
Bisogno, T., Howell, F., Williams, G., Minassi, A., Cascio, M. G., Ligresti, A., Matias, I., Schiano-Moriello, A., Paul, P., Williams, E.-J., Gangadharan, U., Hobbs, C., Di Marzo, V., & Doherty, P. (2003). Cloning of the first sn1-DAG lipases points to the spatial and temporal regulation of endocannabinoid signaling in the brain. The Journal of Cell Biology, 163, 463-468.
Blankman, J. L., Simon, G. M., & Cravatt, B. F. (2007). A comprehensive profile of brain enzymes that hydrolyze the endocannabinoid 2-Arachidonoylglycerol. Chemistry & Biology, 14, 1347-1356.
Bouaboula, M., Poinot-Chazel, C., Bourrié, B., Canat, X., Calandra, B., Rinaldi-Carmona, M., Le Fur, G., & Casellas, P. (1995). Activation of mitogen-activated protein kinases by stimulation of the central cannabinoid receptor CB1. The Biochemical Journal, 312, 637-641.
Brailoiu, G. C., Oprea, T. I., Zhao, P., Abood, M. E., & Brailoiu, E. (2011). Intracellular cannabinoid type 1 (CB1) receptors are activated by anandamide. The Journal of Biological Chemistry, 286, 29166-29174.
Cahoy, J. D., Emery, B., Kaushal, A., Foo, L. C., Zamanian, J. L., Christopherson, K. S., Xing, Y., Lubischer, J. L., Krieg, P. A., Krupenko, S. A., Thompson, W. J., & Barres, B. A. (2008). A transcriptome database for astrocytes, neurons, and oligodendrocytes: A new resource for understanding brain development and function. The Journal of Neuroscience, 28, 264-278.
Ceprián, M., Jiménez-Sánchez, L., Vargas, C., Barata, L., Hind, W., & Martínez-Orgado, J. (2017). Cannabidiol reduces brain damage and improves functional recovery in a neonatal rat model of arterial ischemic stroke. Neuropharmacology, 116, 151-159.
Ceprián, M., Vargas, C., García-Toscano, L., Penna, F., Jiménez-Sánchez, L., Achicallende, S., Elezgarai, I., Grandes, P., Hind, W., Pazos, M. R., & Martínez-Orgado, J. (2019). Cannabidiol administration prevents hypoxia-ischemia-induced Hypomyelination in newborn rats. Frontiers in Pharmacology, 10, 1131.
Cravatt, B. F., Giang, D. K., Mayfield, S. P., Boger, D. L., Lerner, R. A., & Gilula, N. B. (1996). Molecular characterization of an enzyme that degrades neuromodulatory fatty-acid amides. Nature, 384, 83-87.
Dalton, G., Bass, C., Van Horn, C., & Howlett, A. (2009). Signal transduction via cannabinoid receptors. CNS Neurol Disord - Drug Targets, 8, 422-431.
del Río-Hortega, P. (1921). Estudios sobre la neuroglía. La glía de escasas radiaciones (oligodendroglía). Boletín de la Real Sociedad Española de Historia Natural, 21, 63-92.
Derkinderen, P., Ledent, C., Parmentier, M., & Girault, J.-A. (2001a). Cannabinoids activate p38 mitogen-activated protein kinases through CB1 receptors in hippocampus. Journal of Neurochemistry, 77, 957-960.
Derkinderen, P., Toutant, M., Kadaré, G., Girault, J.-A., Ledent, C., & Parmentier, M. (2001b). Dual role of Fyn in the regulation of FAK+6,7 by cannabinoids in hippocampus. The Journal of Biological Chemistry, 276, 38289-38296.
Derkinderen, P., Valjent, E., Toutant, M., Corvol, J.-C., Enslen, H., Ledent, C., Trzaskos, J., Caboche, J., & Girault, J.-A. (2003). Regulation of extracellular signal-regulated kinase by cannabinoids in hippocampus. The Journal of Neuroscience, 23, 2371-2382.
Devane, W. A., & Axelrod, J. (1994). Enzymatic synthesis of anandamide, an endogenous ligand for the cannabinoid receptor, by brain membranes. Proceedings of the National Academy of Sciences, 91, 6698-6701.
Devane, W. A., Dysarz, F. A., 3rd, Johnson, M. R., Melvin, L. S., & Howlett, A. C. (1988). Determination and characterization of a cannabinoid receptor in rat brain. Molecular Pharmacology, 34, 605-613.
Devane, W. A., Hanuš, L., Breuer, A., Pertwee, R. G., Stevenson, L. A., Griffin, G., Gibson, D., Mandelbaum, A., Etinger, A., & Mechoulam, R. (1992). Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science, 258, 1946-1949.
Díaz-Alonso, J., Aguado, T., de Salas-Quiroga, A., Ortega, Z., Guzmán, M., & Galve-Roperh, I. (2015). CB1 cannabinoid receptor-dependent activation of mTORC1/Pax6 signaling drives Tbr2 expression and basal progenitor expansion in the developing mouse cortex. Cerebral Cortex, 25, 2395-2408.
Diaz-Alonso, J., Aguado, T., Wu, C.-S., Palazuelos, J., Hofmann, C., Garcez, P., Guillemot, F., Lu, H.-C., Lutz, B., Guzman, M., Galve-Roperh, I. (2012). The CB1 cannabinoid receptor drives corticospinal motor neuron differentiation through the Ctip2/Satb2 transcriptional regulation axis. The Journal of Neuroscience, 32, 16651-16665.
Dinh, T. P., Carpenter, D., Leslie, F. M., Freund, T. F., Katona, I., Sensi, S. L., Kathuria, S., & Piomelli, D. (2002). Brain monoglyceride lipase participating in endocannabinoid inactivation. Proceedings of the National Academy of Sciences, 99, 10819-10824.
Esteban, P. F., Garcia-Ovejero, D., Paniagua-Torija, B., Moreno-Luna, R., Arredondo, L. F., Zimmer, A., Martín, Á. A., & Molina-Holgado, E. (2020). Revisiting CB1 cannabinoid receptor detection and the exploration of its interacting partners. Journal of Neuroscience Methods, 337, 108680.
Feliú, A., Bonilla del Río, I., Carrillo-Salinas, F. J., Hernández-Torres, G., Mestre, L., Puente, N., Ortega-Gutiérrez, S., López-Rodríguez, M. L., Grandes, P., Mecha, M., & Guaza, C. (2017). 2-Arachidonoylglycerol reduces proteoglycans and enhances Remyelination in a progressive model of demyelination. The Journal of Neuroscience, 37, 8385-8398.
Feliu, A., Mestre, L., Carrillo-Salinas, F. J., Yong, V. W., Mecha, M., Guaza, C. (2020). 2-arachidonoylglycerol reduces chondroitin sulphate proteoglycan production by astrocytes and enhances oligodendrocyte differentiation under inhibitory conditions. Glia, 68, 1255-1273.
Fernández-López, D., Pazos, M. R., Tolón, R. M., Moro, M. A., Romero, J., Lizasoain, I., & Martínez-Orgado, J. (2007). The cannabinoid agonist Win55212 reduces brain damage in an in vivo model of hypoxic-ischemic encephalopathy in newborn rats. Pediatric Research, 62, 255-260.
Fernández-Ruiz, J. (2019). The biomedical challenge of neurodegenerative disorders: An opportunity for cannabinoid-based therapies to improve on the poor current therapeutic outcomes. British Journal of Pharmacology, 176, 1370-1383.
Floriddia, E. M., Lourenço, T., Zhang, S., van Bruggen, D., Hilscher, M. M., Kukanja, P., Gonçalves dos Santos, J. P., Altınkök, M., Yokota, C., Llorens-Bobadilla, E., Mulinyawe, S. B., Grãos, M., Sun, L. O., Frisén, J., Nilsson, M., & Castelo-Branco, G. (2020). Distinct oligodendrocyte populations have spatial preference and different responses to spinal cord injury. Nature Communications, 11, 5860.
Frühbeis, C., Kuo-Elsner, W. P., Müller, C., Barth, K., Peris, L., Tenzer, S., Möbius, W., Werner, H. B., Nave, K.-A., Fröhlich, D., & Krämer-Albers, E.-M. (2020). Oligodendrocytes support axonal transport and maintenance via exosome secretion. PLoS Biology, 18, e3000621.
Fünfschilling, U., Supplie, L. M., Mahad, D., Boretius, S., Saab, A. S., Edgar, J., Brinkmann, B. G., Kassmann, C. M., Tzvetanova, I. D., Möbius, W., Diaz, F., Meijer, D., Suter, U., Hamprecht, B., Sereda, M. W., Moraes, C. T., Frahm, J., Goebbels, S., & Nave, K.-A. (2012). Glycolytic oligodendrocytes maintain myelin and long-term axonal integrity. Nature, 485, 517-521.
Furgiuele, A., Cosentino, M., Ferrari, M., & Marino, F. (2021). Immunomodulatory potential of Cannabidiol in multiple sclerosis: A systematic review. Journal of Neuroimmune Pharmacology, 16, 251-269.
Galve-Roperh, I., Chiurchiù, V., Díaz-Alonso, J., Bari, M., Guzmán, M., & Maccarrone, M. (2013). Cannabinoid receptor signaling in progenitor/stem cell proliferation and differentiation. Progress in Lipid Research, 52, 633-650.
Galve-Roperh, I., Rueda, D., Gómez del Pulgar, T., Velasco, G., & Guzmán, M. (2002). Mechanism of extracellular signal-regulated kinase activation by the CB1 cannabinoid receptor. Molecular Pharmacology, 62, 1385-1392.
Garcia-Ovejero, D., Arevalo-Martin, A., Petrosino, S., Docagne, F., Hagen, C., Bisogno, T., Watanabe, M., Guaza, C., Di Marzo, V., & Molina-Holgado, E. (2009). The endocannabinoid system is modulated in response to spinal cord injury in rats. Neurobiology of Disease, 33, 57-71.
Gómez del Pulgar, T., de Ceballos, M. L., Guzmán, M., & Velasco, G. (2002). Cannabinoids protect astrocytes from ceramide-induced apoptosis through the phosphatidylinositol 3-kinase/protein kinase B pathway. The Journal of Biological Chemistry, 277, 36527-36533.
Gómez Del Pulgar, T., Velasco, G., & Guzmán, M. (2000). The CB1 cannabinoid receptor is coupled to the activation of protein kinase B/Akt. The Biochemical Journal, 347, 369.
Gomez, O., Arevalo-Martin, A., Garcia-Ovejero, D., Ortega-Gutierrez, S., Cisneros, J. A., Almazan, G., Sanchez-Rodriguez, M. A., Molina-Holgado, F., & Molina-Holgado, E. (2010). The constitutive production of the endocannabinoid 2-arachidonoylglycerol participates in oligodendrocyte differentiation. Glia, 58, 1913-1927.
Gomez, O., Sanchez-Rodriguez, A., Le, M., Sanchez-Caro, C., Molina-Holgado, F., & Molina-Holgado, E. (2011). Cannabinoid receptor agonists modulate oligodendrocyte differentiation by activating PI3K/Akt and the mammalian target of rapamycin (mTOR) pathways. British Journal of Pharmacology, 163, 1520-1532.
Gomez, O., Sanchez-Rodriguez, M. A., Ortega-Gutierrez, S., Vazquez-Villa, H., Guaza, C., Molina-Holgado, F., & Molina-Holgado, E. (2015). A basal tone of 2-Arachidonoylglycerol contributes to early oligodendrocyte progenitor proliferation by activating phosphatidylinositol 3-kinase (PI3K)/AKT and the mammalian target of rapamycin (MTOR) pathways. Journal of Neuroimmune Pharmacology, 10, 309-317.
Gutiérrez-Rodríguez, A., Bonilla-Del Río, I., Puente, N., Gómez-Urquijo, S. M., Fontaine, C. J., Egaña-Huguet, J., Elezgarai, I., Ruehle, S., Lutz, B., Robin, L. M., Soria-Gómez, E., Bellocchio, L., Padwal, J. D., van der Stelt, M., Mendizabal-Zubiaga, J., Reguero, L., Ramos, A., Gerrikagoitia, I., Marsicano, G., & Grandes, P. (2018). Localization of the cannabinoid type-1 receptor in subcellular astrocyte compartments of mutant mouse hippocampus. Glia, 66, 1417-1431.
Haspula, D., & Clark, M. A. (2020). Cannabinoid receptors: An update on cell signaling, pathophysiological roles and therapeutic opportunities in neurological, cardiovascular, and inflammatory diseases. International Journal of Molecular Sciences, 21, 7693.
Hebert-Chatelain, E., Desprez, T., Serrat, R., Bellocchio, L., Soria-Gomez, E., Busquets-Garcia, A., Pagano Zottola, A. C., Delamarre, A., Cannich, A., Vincent, P., Varilh, M., Robin, L. M., Terral, G., García-Fernández, M. D., Colavita, M., Mazier, W., Drago, F., Puente, N., Reguero, L., … Marsicano, G. (2016). A cannabinoid link between mitochondria and memory. Nature, 539, 555-559.
Hegyi, Z., Oláh, T., Kőszeghy, Á., Piscitelli, F., Holló, K., Pál, B., Csernoch, L., Di Marzo, V., & Antal, M. (2018). CB1 receptor activation induces intracellular Ca2+ mobilization and 2-arachidonoylglycerol release in rodent spinal cord astrocytes. Scientific Reports, 8, 10562.
Herkenham, M., Lynn, A. B., Johnson, M. R., Melvin, L. S., de Costa, B. R., & Rice, K. C. (1991). Characterization and localization of cannabinoid receptors in rat brain: A quantitative in vitro autoradiographic study. The Journal of Neuroscience, 11, 563-583.
Herkenham, M., Lynn, A. B., Little, M. D., Johnson, M. R., Melvin, L. S., de Costa, B. R., & Rice, K. C. (1990). Cannabinoid receptor localization in brain. Proceedings of the National Academy of Sciences, 87, 1932-1936.
Huerga-Gómez, A., Aguado, T., Sánchez-de la Torre, A., Bernal-Chico, A., Matute, C., Mato, S., Guzmán, M., Galve-Roperh, I., & Palazuelos, J. (2021). Δ 9 -tetrahydrocannabinol promotes oligodendrocyte development and CNS myelination in vivo. Glia, 69, 532-545.
Ilyasov, A. A., Milligan, C. E., Pharr, E. P., & Howlett, A. C. 2018. The endocannabinoid system and oligodendrocytes in health and disease. Frontiers in Neuroscience, 12, 733.
Ishii, A., Fyffe-Maricich, S. L., Furusho, M., Miller, R. H., & Bansal, R. (2012). ERK1/ERK2 MAPK signaling is required to increase myelin thickness independent of oligodendrocyte differentiation and initiation of myelination. The Journal of Neuroscience, 32, 8855-8864.
Jackson, S. J., Pryce, G., Diemel, L. T., Cuzner, M. L., & Baker, D. (2005). Cannabinoid-receptor 1 null mice are susceptible to neurofilament damage and caspase 3 activation. Neuroscience, 134, 261-268.
Jimenez-Blasco, D., Busquets-Garcia, A., Hebert-Chatelain, E., Serrat, R., Vicente-Gutierrez, C., Ioannidou, C., Gómez-Sotres, P., Lopez-Fabuel, I., Resch-Beusher, M., Resel, E., Arnouil, D., Saraswat, D., Varilh, M., Cannich, A., Julio-Kalajzic, F., Bonilla-Del Río, I., Almeida, A., Puente, N., Achicallende, S., … Marsicano, G. (2020). Glucose metabolism links astroglial mitochondria to cannabinoid effects. Nature, 583, 603-608.
Kano, M., Ohno-Shosaku, T., Hashimotodani, Y., Uchigashima, M., & Watanabe, M. (2009). Endocannabinoid-mediated control of synaptic transmission. Physiological Reviews, 89, 309-380.
Katona, I., & Freund, T. F. (2012). Multiple functions of endocannabinoid signaling in the brain. Annual Review of Neuroscience, 35, 529-558.
Katona, I., Sperlágh, B., Sík, A., Käfalvi, A., Vizi, E. S., Mackie, K., & Freund, T. F. (1999). Presynaptically located CB1 cannabinoid receptors regulate GABA release from axon terminals of specific hippocampal interneurons. The Journal of Neuroscience, 19, 4544-4558.
Kessaris, N., Fogarty, M., Iannarelli, P., Grist, M., Wegner, M., & Richardson, W. D. (2006). Competing waves of oligodendrocytes in the forebrain and postnatal elimination of an embryonic lineage. Nature Neuroscience, 9, 173-179.
Kessaris, N., Pringle, N., & Richardson, W. D. (2008). Specification of CNS glia from neural stem cells in the embryonic neuroepithelium. Philos Trans R Soc B Biol Sci, 363, 71-85.
Kreitzer, A. C., & Regehr, W. G. (2001). Retrograde inhibition of presynaptic calcium influx by endogenous cannabinoids at excitatory synapses onto Purkinje cells. Neuron, 29, 717-727.
Lee, Y., Morrison, B. M., Li, Y., Lengacher, S., Farah, M. H., Hoffman, P. N., Liu, Y., Tsingalia, A., Jin, L., Zhang, P.-W., Pellerin, L., Magistretti, P. J., & Rothstein, J. D. (2012). Oligodendroglia metabolically support axons and contribute to neurodegeneration. Nature, 487, 443-448.
Maccarrone, M., Guzmán, M., Mackie, K., Doherty, P., & Harkany, T. (2014). Programming of neural cells by (endo)cannabinoids: From physiological rules to emerging therapies. Nature Reviews. Neuroscience, 15, 786-801.
Mailleux, P., & Vanderhaeghen, J.-J. (1992). Distribution of neuronal cannabinoid receptor in the adult rat brain: A comparative receptor binding radioautography and in situ hybridization histochemistry. Neuroscience, 48, 655-668.
Manterola, A., Bernal-Chico, A., Cipriani, R., Canedo-Antelo, M., Moreno-García, Á., Martín-Fontecha, M., Pérez-Cerdá, F., Sánchez-Gómez, M. V., Ortega-Gutiérrez, S., Brown, J. M., Hsu, K. L., Cravatt, B., Matute, C., & Mato, S. (2018). Deregulation of the endocannabinoid system and therapeutic potential of ABHD6 blockade in the cuprizone model of demyelination. Biochemical Pharmacology, 157, 189-201.
Marinelli, C., Bertalot, T., Zusso, M., Skaper, S. D., & Giusti, P. (2016). Systematic review of pharmacological properties of the oligodendrocyte lineage. Frontiers in Cellular Neuroscience, 10, 27.
Marques, S., Zeisel, A., Codeluppi, S., Van Bruggen, D., Falcão, A. M., Xiao, L., Li, H., Häring, M., Hochgerner, H., Romanov, R. A., Gyllborg, D., Muñoz-Manchado, A. B., La Manno, G., Lönnerberg, P., Floriddia, E. M., Rezayee, F., Ernfors, P., Arenas, E., Hjerling-Leffler, J., … Castelo-Branco, G. (2016). Oligodendrocyte heterogeneity in the mouse juvenile and adult central nervous system. Science, 352(80), 1326-1329.
Martínez-Orgado, J. (2003). Neuroprotection by the cannabinoid agonist WIN-55212 in an in vivo newborn rat model of acute severe asphyxia. Molecular Brain Research, 114, 132-139.
Mato, S., Alberdi, E., Ledent, C., Watanabe, M., & Matute, C. (2009). CB1 cannabinoid receptor-dependent and -independent inhibition of depolarization-induced calcium influx in oligodendrocytes. Glia, 57, 295-306.
Mato, S., Victoria Sánchez-Gómez, M., & Matute, C. (2010). Cannabidiol induces intracellular calcium elevation and cytotoxicity in oligodendrocytes. Glia, 58, 739-747.
Matsuda, L. A., Lolait, S. J., Brownstein, M. J., Young, A. C., & Bonner, T. I. (1990). Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature, 346, 561-564.
Mecha, M., Torrao, A. S., Mestre, L., Carrillo-Salinas, F. J., Mechoulam, R., & Guaza, C. (2012). Cannabidiol protects oligodendrocyte progenitor cells from inflammation-induced apoptosis by attenuating endoplasmic reticulum stress. Cell Death & Disease 3, e331.
Mechoulam, R., Ben-Shabat, S., Hanus, L., Ligumsky, M., Kaminski, N. E., Schatz, A. R., Gopher, A., Almog, S., Martin, B. R., Compton, D. R., Pertwee, R. G., Griffin, G., Bayewitch, M., Barg, J., & Vogel, Z. (1995). Identification of an endogenous 2-monoglyceride, present in canine gut, that binds to cannabinoid receptors. Biochemical Pharmacology, 50, 83-90.
Mechoulam, R., Parker, L. A., & Gallily, R. (2002). Cannabidiol: An overview of some pharmacological aspects. Journal of Clinical Pharmacology, 42, 11S-19S.
Meyer, N., & Rinholm, J. E. (2021). Mitochondria in Myelinating oligodendrocytes: Slow and out of breath? Metabolites, 11, 359.
Moldrich, G., & Wenger, T. (2000). Localization of the CB1 cannabinoid receptor in the rat brain. An immunohistochemical study☆. Peptides, 21, 1735-1742.
Molina-Holgado, E., Paniagua-Torija, B., Arevalo-Martin, A., Moreno-Luna, R., Esteban, P. F., Le, M. Q. U., Del Cerro, M., & del Garcia-Ovejero, D. (2021). Cannabinoid receptor 1 associates to different molecular complexes during GABAergic neuron maturation. Journal of Neurochemistry, 158, 640-656.
Molina-Holgado, E., Vela, J. M., Arevalo-Martin, A., Almazan, G., Molina-Holgado, F., Borrell, J., & Guaza, C. (2002). Cannabinoids promote oligodendrocyte progenitor survival: Involvement of cannabinoid receptors and phosphatidylinositol-3 kinase/Akt signaling. The Journal of Neuroscience, 22, 9742-9753.
Moreno-Luna, R., Esteban, P. F., Paniagua-Torija, B., Arevalo-Martin, A., Garcia-Ovejero, D., & Molina-Holgado, E. (2021). Heterogeneity of the endocannabinoid system between cerebral cortex and spinal cord oligodendrocytes. Molecular Neurobiology, 58, 689-702.
Mulder, J., Aguado, T., Keimpema, E., Barabas, K., Ballester Rosado, C. J., Nguyen, L., Monory, K., Marsicano, G., Di Marzo, V., Hurd, Y. L., Guillemot, F., Mackie, K., Lutz, B., Guzman, M., Lu, H. C., Galve-Roperh, I., & Harkany, T. (2008). Endocannabinoid signaling controls pyramidal cell specification and long-range axon patterning. Proceedings of the National Academy of Sciences of the United States of America, 105, 8760-8765.
Munro, S., Thomas, K. L., & Abu-Shaar, M. (1993). Molecular characterization of a peripheral receptor for cannabinoids. Nature, 365, 61-65.
Navarrete, M., & Araque, A. (2008). Endocannabinoids mediate neuron-astrocyte communication. Neuron, 57, 883-893.
Nave, K.-A. (2010). Myelination and the trophic support of long axons. Nature Reviews. Neuroscience, 11, 275-283.
Ohno-Shosaku, T., Maejima, T., & Kano, M. (2001). Endogenous cannabinoids mediate retrograde signals from depolarized postsynaptic neurons to presynaptic terminals. Neuron, 29, 729-738.
Ong, W. Y., & Mackie, K. (1999). A light and electron microscopic study of the CB1 cannabinoid receptor in the primate spinal cord. Journal of Neurocytology, 28, 39-45.
Ozaita, A., Puighermanal, E., & Maldonado, R. (2007). Regulation of PI3K/Akt/GSK-3 pathway by cannabinoids in the brain. Journal of Neurochemistry, 102, 1105-1114.
Pacher, P., Kogan, N. M., & Mechoulam, R. (2020). Beyond THC and endocannabinoids. Annual Review of Pharmacology and Toxicology, 60, 637-659.
Pacher, P., & Kunos, G. (2013). Modulating the endocannabinoid system in human health and disease - successes and failures. The FEBS Journal, 280, 1918-1943.
Palazuelos, J., Ortega, Z., Díaz-Alonso, J., Guzmán, M., & Galve-Roperh, I. (2012). CB2 cannabinoid receptors promote neural progenitor cell proliferation via mTORC1 signaling. The Journal of Biological Chemistry, 287, 1198-1209.
Panikashvili, D., Simeonidou, C., Ben-Shabat, S., Hanuš, L., Breuer, A., Mechoulam, R., & Shohami, E. (2001). An endogenous cannabinoid (2-AG) is neuroprotective after brain injury. Nature, 413, 527-531.
Pérez-Cerdá, F., Sánchez-Gómez, M. V., & Matute, C. (2015). Pío del Río Hortega and the discovery of the oligodendrocytes. Frontiers in Neuroanatomy, 9, 92.
Pettit, D. A. D., Harrison, M. P., Olson, J. M., Spencer, R. F., & Cabral, G. A. (1998). Immunohistochemical localization of the neural cannabinoid receptor in rat brain. Journal of Neuroscience Research, 51, 391-402.
Piomelli, D. (2003). The molecular logic of endocannabinoid signalling. Nature Reviews. Neuroscience, 4, 873-884.
Pringle, N. P., & Richardson, W. D. (1993). A singularity of PDGF alpha-receptor expression in the dorsoventral axis of the neural tube may define the origin of the oligodendrocyte lineage. Development, 117, 525-533.
Puighermanal, E., Marsicano, G., Busquets-Garcia, A., Lutz, B., Maldonado, R., & Ozaita, A. (2009). Cannabinoid modulation of hippocampal long-term memory is mediated by mTOR signaling. Nature Neuroscience, 12, 1152-1158.
Romero, J., Garcia-Palomero, E., Berrendero, F., Garcia-Gil, L., Hernandez, M. L., Ramos, J. A., & Fernandez-Ruiz, J. J. (1997). Atypical location of cannabinoid receptors in white matter areas during rat brain development. Synapse, 26, 317-323.
Rubino, T., Forlani, G., Viganò, D., Zippel, R., & Parolaro, D. (2004). Modulation of extracellular signal-regulated kinases cascade by chronic delta 9-tetrahydrocannabinol treatment. Molecular and Cellular Neurosciences, 25, 355-362.
Rueda, D., Navarro, B., Martı́nez-Serrano, A., Guzmán, M., & Galve-Roperh, I. (2002). The endocannabinoid anandamide inhibits neuronal progenitor cell differentiation through attenuation of the Rap1/B-Raf/ERK pathway. The Journal of Biological Chemistry, 277, 46645-46650.
Sagredo, O., Palazuelos, J., Gutierrez-Rodriguez, A., Satta, V., Galve-Roperh, I., & Martínez-Orgado, J. (2018). Cannabinoid signalling in the immature brain: Encephalopathies and neurodevelopmental disorders. Biochemical Pharmacology, 157, 85-96.
Sanchez-Rodriguez, M. A., Gomez, O., Esteban, P. F., Garcia-Ovejero, D., & Molina-Holgado, E. (2018). The endocannabinoid 2-arachidonoylglycerol regulates oligodendrocyte progenitor cell migration. Biochemical Pharmacology, 157, 180-188.
Scarante, F. F., Ribeiro, M. A., Almeida-Santos, A. F., Guimarães, F. S., & Campos, A. C. (2021). Glial cells and their contribution to the mechanisms of action of Cannabidiol in neuropsychiatric disorders. Frontiers in Pharmacology, 11, 618065.
Seeker, L. A., & Williams, A. (2022). Oligodendroglia heterogeneity in the human central nervous system. Acta Neuropathologica, 143, 143-157.
Serrat, R., Covelo, A., Kouskoff, V., Delcasso, S., Ruiz-Calvo, A., Chenouard, N., Stella, C., Blancard, C., Salin, B., Julio-Kalajzić, F., Cannich, A., Massa, F., Varilh, M., Deforges, S., Robin, L. M., De Stefani, D., Busquets-Garcia, A., Gambino, F., Beyeler, A., … Marsicano, G. (2021). Astroglial ER-mitochondria calcium transfer mediates endocannabinoid-dependent synaptic integration. Cell Reports, 37, 110133.
Sherman, D. L., & Brophy, P. J. (2005). Mechanisms of axon ensheathment and myelin growth. Nature Reviews. Neuroscience, 6, 683-690.
Sim, F. J., Lang, J. K., Waldau, B., Roy, N. S., Schwartz, T. E., Pilcher, W. H., Chandross, K. J., Natesan, S., Merrill, J. E., & Goldmanm, S. A. (2006). Complementary patterns of gene expression by human oligodendrocyte progenitors and their environment predict determinants of progenitor maintenance and differentiation. Annals of Neurology, 59, 763-779.
Sock, E., & Wegner, M. (2021). Using the lineage determinants Olig2 and Sox10 to explore transcriptional regulation of oligodendrocyte development. Developmental Neurobiology, 81, 892-901.
Solbrig, M. V., Fan, Y., Hermanowicz, N., Morgese, M. G., & Giuffrida, A. (2010). A synthetic cannabinoid agonist promotes oligodendrogliogenesis during viral encephalitis in rats. Experimental Neurology, 226, 231-241.
Spitzer, S. O., Sitnikov, S., Kamen, Y., Evans, K. A., Kronenberg-Versteeg, D., Dietmann, S., de Faria, O., Agathou, S., & Káradóttir, R. T. (2019). Oligodendrocyte progenitor cells become regionally diverse and heterogeneous with age. Neuron, 101, 459-471.
Sun, J., Fang, Y., Ren, H., Chen, T., Guo, J., Yan, J., Song, S., Zhang, L., & Liao, H. (2013). WIN55,212-2 protects oligodendrocyte precursor cells in stroke penumbra following permanent focal cerebral ischemia in rats. Acta Pharmacologica Sinica, 34, 119-128.
Thomas, A., Baillie, G. L., Phillips, A. M., Razdan, R. K., Ross, R. A., & Pertwee, R. G. (2007). Cannabidiol displays unexpectedly high potency as an antagonist of CB1 and CB2 receptor agonists in vitro. British Journal of Pharmacology, 150, 613-623.
Tomas-Roig, J., Agbemenyah, H. Y., Celarain, N., Quintana, E., Ramió-Torrentà, L., & Havemann-Reinecke, U. (2020). Dose-dependent effect of cannabinoid WIN-55,212-2 on myelin repair following a demyelinating insult. Scientific Reports, 10, 590.
Trazzi, S., Steger, M., Mitrugno, V. M., Bartesaghi, R., & Ciani, E. (2010). CB1 cannabinoid receptors increase neuronal precursor proliferation through AKT/glycogen synthase kinase-3β/β-catenin signaling. The Journal of Biological Chemistry, 285, 10098-10109.
Tsou, K., Brown, S., Sanudo-Pena, M. C., Mackie, K., & Walker, J. M. (1998). Immunohistochemical distribution of cannabinoid CB1 receptors in the rat central nervous system. Neuroscience, 83, 393-411.
Tyler, W. A., Gangoli, N., Gokina, P., Kim, H. A., Covey, M., Levison, S. W., & Wood, T. L. (2009). Activation of the mammalian target of rapamycin (mTOR) is essential for oligodendrocyte differentiation. The Journal of Neuroscience, 29, 6367-6378.
van Tilborg, E., de Theije, C. G. M., van Hal, M., Wagenaar, N., de Vries, L. S., Benders, M. J., Rowitch, D. H., & Nijboer, C. H. (2018). Origin and dynamics of oligodendrocytes in the developing brain: Implications for perinatal white matter injury. Glia, 66, 221-238.
Watanabe, M., Sakurai, Y., Ichinose, T., Aikawa, Y., Kotani, M., & Itoh, K. (2006). Monoclonal antibody rip specifically recognizes 2′,3′-cyclic nucleotide 3′-phosphodiesterase in oligodendrocytes. Journal of Neuroscience Research, 84, 525-533.
Wilson, R. I., & Nicoll, R. A. (2001). Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses. Nature, 410, 588-592.
Younes-Rapozo, V., Felgueiras, L. O. R., Viana, N. L., Fierro, I. M., Barja-Fidalgo, C., Manhães, A. C., & Barradas, P. C. (2009). A role for the MAPK/ERK pathway in oligodendroglial differentiation in vitro: Stage specific effects on cell branching. International Journal of Developmental Neuroscience, 27, 757-768.
Zhang, Y., Chen, K., Sloan, S. A., Bennett, M. L., Scholze, A. R., O'Keeffe, S., Phatnani, H. P., Guarnieri, P., Caneda, C., Ruderisch, N., Deng, S., Liddelow, S. A., Zhang, C., Daneman, R., Maniatis, T., Barres, B. A., & 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.