Role for astroglial α1-adrenoreceptors in gliotransmission and control of synaptic plasticity in the neocortex

Frontiers in Cellular Neuroscience

Volumn 9, Issue June, 2015, Pages 1-11

  Pankratov, Yuriy ^a   Lalo, Ulyana ^a  

^a UNIVERSITY OF WARWICK   (United Kingdom)

Author keywords

Astrocyte neuron interactions; ATP release; D serine; Desensitization; Exocytosis; Metaplasticy; Norepinephrine; P2X receptor

Indexed keywords

ALPHA 1 ADRENERGIC RECEPTOR; ENHANCED GREEN FLUORESCENT PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CALCIUM SIGNALING; CONTROLLED STUDY; DOWN REGULATION; ELECTROPHYSIOLOGY; EXCITATORY POSTSYNAPTIC POTENTIAL; EXOCYTOSIS; LONG TERM POTENTIATION; MOUSE; NEOCORTEX; NERVE CELL PLASTICITY; NEUROTRANSMISSION; NONHUMAN; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SYNAPTIC POTENTIAL; SYNAPTIC TRANSMISSION;

EID: 84935876289     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2015.00230     Document Type: Article

References (45)

1. Akinaga, J., Lima, V., Kiguti, L. R., Hebeler-Barbosa, F., Alcántara-Hernández, R., García-Sáinz, J. A., et al. (2013). Differential phosphorylation, desensitization and internalization of alpha1A-adrenoceptors activated by norepinephrine and oxymetazoline. Mol. Pharmacol. 83, 870-881. doi:10.1124/mol.112.082313
2. Allsopp, R. C., Lalo, U., and Evans, R. J. (2010). Lipid raft association and cholesterol sensitivity of P2X1-4 receptors for ATP: chimeras and point mutants identify intracellular amino-terminal residues involved in lipid regulation of P2X1 receptors. J. Biol. Chem. 285, 32770-32777. doi:10.1074/jbc.m110.148940
3. Araque, A., Carmignoto, G., Haydon, P. G., Oliet, S. H., Robitaille, R., and Volterra, A. (2014). Gliotransmitters travel in time and space. Neuron 81, 728-739. doi:10.1016/j.neuron.2014.02.007
4. Attwell, D., Buchan, A. M., Charpak, S., Lauritzen, M., Macvicar, B. A., and Newman, E. A. (2010). Glial and neuronal control of brain blood flow. Nature 468, 232-243. doi:10.1038/nature09613
5. Butt, A. M. (2011). ATP: a ubiquitous gliotransmitter integrating neuron-glial networks. Semin. Cell Dev. Biol. 22, 205-213. doi:10.1016/j.semcdb.2011.02.023
6. Butt, A. M., Fern, R. F., and Matute, C. (2014). Neurotransmitter signaling in white matter. Glia 62, 1762-1779. doi:10.1002/glia.22674
7. Ding, F., O’Donnell, J., Thrane, A. S., Zeppenfeld, D., Kang, H., Xie, L., et al. (2013). alpha1-Adrenergic receptors mediate coordinated Ca2+ signaling of cortical astrocytes in awake, behaving mice. Cell Calcium 54, 387-394. doi:10.1016/j.ceca.2013.09.001
8. Duguid, I. C., Pankratov, Y., Moss, G. W., and Smart, T. G. (2007). Somatodendritic release of glutamate regulates synaptic inhibition in cerebellar Purkinje cells via autocrine mGluR1 activation. J. Neurosci. 27, 12464-12474. doi:10.1523/jneurosci.0178-07.2007
9. Frenguelli, B. G., Wigmore, G., Llaudet, E., and Dale, N. (2007). Temporal and mechanistic dissociation of ATP and adenosine release during ischaemia in the mammalian hippocampus. J. Neurochem. 101, 1400-1413. doi:10.1111/j.1471-4159.2006.04425.x
10. Fujita, T., Chen, M. J., Li, B., Smith, N. A., Peng, W., Sun, W., et al. (2014). Neuronal transgene expression in dominant-negative SNARE mice. J. Neurosci. 34, 16594-16604. doi:10.1523/jneurosci.2585-14.2014
11. Giaume, C., Koulakoff, A., Roux, L., Holcman, D., and Rouach, N. (2010). Astroglial networks: a step further in neuroglial and gliovascular interactions. Nat. Rev. Neurosci. 11, 87-99. doi:10.1038/nrn2757
12. Gordon, G. R., Iremonger, K. J., Kantevari, S., Ellis-Davies, G. C., MacVicar, B. A., and Bains, J. S. (2009). Astrocyte-mediated distributed plasticity at hypothalamic glutamate synapses. Neuron 64, 391-403. doi:10.1016/j.neuron.2009.10.021
13. Gourine, A. V., Kasymov, V., Marina, N., Tang, F., Figueiredo, M. F., Lane, S., et al. (2010). Astrocytes control breathing through pH-dependent release of ATP. Science 329, 571-575. doi:10.1126/science.1190721
14. Gyoneva, S., and Traynelis, S. F. (2013). Norepinephrine modulates the motility of resting and activated microglia via different adrenergic receptors. J. Biol. Chem. 288, 15291-15302. doi:10.1074/jbc.m113.458901
15. Halassa, M. M., Fellin, T., and Haydon, P. G. (2007). The tripartite synapse: roles for gliotransmission in health and disease. Trends Mol. Med. 13, 54-63. doi:10.1016/j.molmed.2006.12.005
16. Halassa, M. M., Florian, C., Fellin, T., Munoz, J. R., Lee, S. Y., Abel, T., et al. (2009). Astrocytic modulation of sleep homeostasis and cognitive consequences of sleep loss. Neuron 61, 213-219. doi:10.1016/j.neuron.2008.11.024
17. Halassa, M. M., and Haydon, P. G. (2010). Integrated brain circuits: astrocytic networks modulate neuronal activity and behavior. Annu. Rev. Physiol. 72, 335-355. doi:10.1146/annurev-physiol-021909-135843
18. Hamilton, N. B., and Attwell, D. (2010). Do astrocytes really exocytose neurotransmitters? Nat. Rev. Neurosci. 11, 227-238. doi:10.1038/nrn2803
19. Henneberger, C., Papouin, T., Oliet, S. H., and Rusakov, D. A. (2010). Long-term potentiation depends on release of D-serine from astrocytes. Nature 463, 232-236. doi:10.1038/nature08673
20. Hulme, S. R., Jones, O. D., and Abraham, W. C. (2013a). Emerging roles of metaplasticity in behaviour and disease. Trends Neurosci. 36, 353-362. doi:10.1016/j.tins.2013.03.007
21. Hulme, S. R., Jones, O. D., Raymond, C. R., Sah, P., and Abraham, W. C. (2013b). Mechanisms of heterosynaptic metaplasticity. Philos. Trans. R. Soc. Lond. B Biol. Sci. 369:20130148. doi:10.1098/rstb.2013.0148
22. Jiang, T., Yu, J. T., Tan, M. S., Zhu, X. C., and Tan, L. (2013). beta-Arrestins as potential therapeutic targets for Alzheimer’s disease. Mol. Neurobiol. 48, 812-818. doi:10.1007/s12035-013-8469-8
23. Khakh, B. S., and McCarthy, K. D. (2015). Astrocyte calcium signaling: from observations to functions and the challenges therein. Cold Spring Harb. Perspect. Biol. 7:a020404. doi:10.1101/cshperspect.a020404
24. Lalo, U., Palygin, O., North, R. A., Verkhratsky, A., and Pankratov, Y. (2011a). Age-dependent remodelling of ionotropic signalling in cortical astroglia. Aging Cell 10, 392-402. doi:10.1111/j.1474-9726.2011.00682.x
25. Lalo, U., Palygin, O., Rasooli-Nejad, S., Andrew, J., Haydon, P. G., and Pankratov, Y. (2014a). Exocytosis of ATP from astrocytes modulates phasic and tonic inhibition in the neocortex. PLoS Biol. 12:e1001747. doi:10.1371/journal.pbio.1001857
26. Lalo, U., Rasooli-Nejad, S., and Pankratov, Y. (2014b). Exocytosis of gliotransmitters from cortical astrocytes: implications for synaptic plasticity and aging. Biochem. Soc. Trans. 42, 1275-1281. doi:10.1042/bst20140163
27. Lalo, U., Roberts, J. A., and Evans, R. J. (2011b). Identification of human P2X1 receptor-interacting proteins reveals a role of the cytoskeleton in receptor regulation. J. Biol. Chem. 286, 30591-30599. doi:10.1074/jbc.m111.253153
28. Martineau, M., Shi, T., Puyal, J., Knolhoff, A. M., Dulong, J., Gasnier, B., et al. (2013). Storage and uptake of D-serine into astrocytic synaptic-like vesicles specify gliotransmission. J. Neurosci. 33, 3413-3423. doi:10.1523/jneurosci.3497-12.2013
29. Min, R., and Nevian, T. (2012). Astrocyte signaling controls spike timing-dependent depression at neocortical synapses. Nat. Neurosci. 15, 746-753.doi:10.1038/nn.3075
30. Mohan, M. L., Vasudevan, N. T., Gupta, M. K., Martelli, E. E., and Naga Prasad, S. V. (2013). G-protein coupled receptor resensitization-appreciating the balancing act of receptor function. Curr. Mol. Pharmacol. 5, 350-361. doi:10.2174/1874467211205030004
31. Montero, T. D., and Orellana, J. A. (2015). Hemichannels: new pathways for gliotransmitter release. Neuroscience 286, 45-59. doi:10.1016/j.neuroscience.2014.11.048
32. Morris, D. P., Lei, B., Wu, Y. X., Michelotti, G. A., and Schwinn, D. A. (2008). The alpha1a-adrenergic receptor occupies membrane rafts with its G protein effectors but internalizes via clathrin-coated pits. J. Biol. Chem. 283, 2973-2985. doi:10.1074/jbc.m705795200
33. Nithianantharajah, J., and Hannan, A. J. (2006). Enriched environments, experience-dependent plasticity and disorders of the nervous system. Nat. Rev. Neurosci. 7, 697-709. doi:10.1038/nrn1970
34. Palygin, O., Lalo, U., and Pankratov, Y. (2011). Distinct pharmacological and functional properties of NMDA receptors in mouse cortical astrocytes. Br. J. Pharmacol. 163, 1755-1766. doi:10.1111/j.1476-5381.2011.01374.x
35. Panatier, A., Vallée, J., Haber, M., Murai, K. K., Lacaille, J. C., and Robitaille, R. (2011). Astrocytes are endogenous regulators of basal transmission at central synapses. Cell 146, 785-798. doi:10.1016/j.cell.2011.07.022
36. Pankratov, Y., Lalo, U., Verkhratsky, A., and North, R. A. (2007). Quantal release of ATP in mouse cortex. J. Gen. Physiol. 129, 257-265. doi:10.1085/jgp.200609693
37. Pascual, O., Casper, K. B., Kubera, C., Zhang, J., Revilla-Sanchez, R., Sul, J. Y., et al. (2005). Astrocytic purinergic signaling coordinates synaptic networks. Science 310, 113-116. doi:10.1126/science.1116916
38. Paukert, M., Agarwal, A., Cha, J., Doze, V. A., Kang, J. U., and Bergles, D. E. (2014). Norepinephrine controls astroglial responsiveness to local circuit activity. Neuron 82, 1263-1270. doi:10.1016/j.neuron.2014.04.038
39. Pearson, T., and Frenguelli, B. G. (2004). Adrenoreceptor subtype-specific acceleration of the hypoxic depression of excitatory synaptic transmission in area CA1 of the rat hippocampus. Eur. J. Neurosci. 20, 1555-1565. doi: 10.1111/j.1460-9568.2004.03602.x
40. Pougnet, J. T., Toulme, E., Martinez, A., Choquet, D., Hosy, E., and Boué-Grabot, E. (2014). ATP P2X receptors downregulate AMPA receptor trafficking and postsynaptic efficacy in hippocampal neurons. Neuron 83, 417-430. doi:10.1016/j.neuron.2014.06.005
41. Rasooli-Nejad, S., Palygin, O., Lalo, U., and Pankratov, Y. (2014). Cannabinoid receptors contribute to astroglia lCa2+-signalling and control of synaptic plasticity in the neocortex. Philos. Trans. R. Soc. Lond. B Biol. Sci. 369:20140077. doi:10.1098/rstb.2014.0077
42. Schipke, C. G., Haas, B., and Kettenmann, H. (2008). Astrocytes discriminate and selectively respond to the activity of a subpopulation of neurons within the barrel cortex. Cereb. Cortex 18, 2450-2459. doi:10.1093/cercor/bhn009
43. Woo, D. H., Han, K. S., Shim, J. W., Yoon, B. E., Kim, E., Bae, J. Y., et al. (2012). TREK-1 and Best1 channels mediate fast and slow glutamate release in astrocytes upon GPCR activation. Cell 151, 25-40. doi:10.1016/j.cell.2012.09.005
44. Yoshiki, H., Uwada, J., Umada, H., Kobayashi, T., Takahashi, T., Yamakawa, T., et al. (2013). Agonist pharmacology at recombinant alpha1A-and alpha1L-adrenoceptors and in lower urinary tract alpha1-adrenoceptors. Br. J. Pharmacol. 170, 1242-1252. doi:10.1111/bph.12403
45. Zucchi, R., and Ronca-Testoni, S. (1997). The sarcoplasmic reticulum Ca2+ channel/ryanodine receptor: modulation by endogenous effectors, drugs and disease states. Pharmacol. Rev. 49, 1-51.