Hostname: page-component-586b7cd67f-dlnhk Total loading time: 0 Render date: 2024-11-24T11:15:52.243Z Has data issue: false hasContentIssue false
  • English
  • Français

Glial cell regulation of neurotransmission and behavior in Drosophila

Published online by Cambridge University Press:  27 October 2008

F. Rob Jackson  and
Philip G. Haydon
F. Rob Jackson*
Affiliation:
Department of Neuroscience, Tufts Center for Neuroscience Research, Tufts University School of Medicine, Boston MA, USA
Philip G. Haydon
Affiliation:
Department of Neuroscience, Tufts Center for Neuroscience Research, Tufts University School of Medicine, Boston MA, USA
*
Correspondence should be addressed to: F. Rob Jackson, Department of Neuroscience, Tufts Center for Neuroscience Research, Tufts University School of Medicine, 136 Harrison Avenue, Boston MA, USA phone: +1 617 636 6752 fax: +1 617 636 3459 email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Mounting evidence demonstrates that glial cells might have important roles in regulating the physiology and behavior of adult animals. We summarize some of this evidence here, with an emphasis on the roles of glia of the differentiated nervous system in controlling neuronal excitability, behavior and plasticity. In the review we highlight studies in Drosophila and discuss results from the analysis of mammalian astrocytes that demonstrate roles for glia in the adult nervous system.

Keywords

GliaDrosophilabehavior
Type
Research Article
Information
Neuron Glia Biology , Volume 4 , Issue 1 , February 2008 , pp. 11 - 17
Copyright
Copyright © Cambridge University Press 2008

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Angulo, M.C., Kozlov, A.S., Charpak, S. and Audinat, E. (2004) Glutamate released from glial cells synchronizes neuronal activity in the hippocampus. Journal of Neuroscience 24, 6920–6927.CrossRefGoogle ScholarPubMed
Araque, A., Carmignoto, G. and Haydon, P.G. (2001) Dynamic signaling between astrocytes and neurons. Annual Review of Physiology 63, 795–813.CrossRefGoogle ScholarPubMed
Augustin, H., Grosjean, Y., Chen, K., Sheng, Q. and Featherstone, D.E. (2007) Nonvesicular release of glutamate by glial xCT transporters suppresses glutamate receptor clustering in vivo. Journal of Neuroscience 27, 111–123.CrossRefGoogle ScholarPubMed
Bainton, R.J., Tsai, L.T., Schwabe, T., DeSalvo, M., Gaul, U. and Heberlein, U. (2005) moody encodes two GPCRs that regulate cocaine behaviors and blood-brain barrier permeability in Drosophila. Cell 123, 145–156.CrossRefGoogle ScholarPubMed
Bauer, K. (2005) Carnosine and homocarnosine, the forgotten, enigmatic peptides of the brain. Neurochemistry Research 30, 1339–1345.CrossRefGoogle ScholarPubMed
Bauerly, K.A., Storms, D.H., Harris, C.B., Hajizadeh, S., Sun, M.Y., Cheung, C.P. et al. (2006) Pyrroloquinoline quinone nutritional status alters lysine metabolism and modulates mitochondrial DNA content in the mouse and rat. Biochimica et Biophysica Acta-General Subjects 1760, 1741–1748.CrossRefGoogle ScholarPubMed
Beckervordersandforth, R.M., Altenhein, B. and Technau, G. (2006) Identification and characterization of Drosophila genes involved in glial specification and differentiation. Journal of Neurogenetics 20, 80.Google Scholar
Beckervordersandforth, R.M., Rickert, C., Altenhein, B. and Technau, G. (2008) Identification and characterization of Drosophila genes involved in glial specification and differentiation. Mechanisms of Development 125, 542–557.CrossRefGoogle Scholar
Biffo, S., Grillo, M. and Margolis, F.L. (1990) Cellular localization of carnosine-like and anserine-like immunoreactivities in rodent and avian central nervous system. Neuroscience 35, 637–651.CrossRefGoogle ScholarPubMed
Bonfanti, L., Peretto, P., DeMarchis, S. and Fasolo, A. (1999) Carnosine-related dipeptides in the mammalian brain. Progress in Neurobiology 59, 333–353.CrossRefGoogle ScholarPubMed
Bridges, C. and Morgan, T.H. (1923) The third-chromosome group of mutant characters of Drosophila melanogaster. Carnegie Institute of Washington Publication 327, 1–251.Google Scholar
Cafferty, P. and Auld, V.J. (2007) No pun intended: future directions in invertebrate glial cell migration studies. Neuron Glia Biology 3, 45–54.CrossRefGoogle ScholarPubMed
Comas, D., Petit, F. and Preat, T. (2004) Drosophila long-term memory formation involves regulation of cathepsin activity. Nature 430, 460–463.CrossRefGoogle ScholarPubMed
D'Ascenzo, M., Fellin, T., Terunuma, M., Revilla-Sanchez, R., Meaney, D.F., Auberson, Y.P. et al. (2007) mGluR5 stimulates gliotransmission in the nucleus accumbens. Proceedings of the National Academy of Sciences of the U.S.A. 104, 1995–2000.CrossRefGoogle ScholarPubMed
Ding, S., Fellin, T., Zhu, Y., Lee, S.Y., Auberson, Y.P., Meaney, D.F. et al. (2007) Enhanced astrocytic Ca2+ signals contribute to neuronal excitotoxicity after status epilepticus. Journal of Neuroscience 27, 10674–10684.CrossRefGoogle ScholarPubMed
Ewer, J., Frisch, B., Hamblen-Coyle, M.J., Rosbash, M. and Hall, J.C. (1992) Expression of the period clock gene within different cell types in the brain of Drosophila adults and mosaic analysis of these cells influence on circadian behavioral rhythms. Journal of Neuroscience 12, 3321–3349.CrossRefGoogle ScholarPubMed
Fellin, T., Pascual, O., Gobbo, S., Pozzan, T., Haydon, P.G. and Carmignoto, G. (2004) Neuronal synchrony mediated by astrocytic glutamate through activation of extrasynaptic NMDA receptors. Neuron 43, 729–743.CrossRefGoogle ScholarPubMed
Fields, R.D. (2006) Advances in understanding neuron-glia interactions. Neuron Glia Biology 2, 23–26.CrossRefGoogle ScholarPubMed
Freeman, M.R. and Doherty, J. (2006) Glial cell biology in Drosophila and vertebrates. Trends in Neurosciences 29, 82–90.CrossRefGoogle ScholarPubMed
Grosjean, Y., Grillet, M., Augustin, H., Ferveur, J.F. and Featherstone, D.E. (2008) A glial amino-acid transporter controls synapse strength and courtship in Drosophila. Nature Neuroscience 11, 54–61.CrossRefGoogle ScholarPubMed
Halassa, M.M., Fellin, T., Munoz, J.R., Haydon, P.G. and Frank, M.G. (2007b) Astrocytes regulate sleep homeostasis. Society for Neuroscience Abstracts 37.Google Scholar
Halassa, M.M., Fellin, T. and Haydon, P.G. (2007a) The tripartite synapse: roles for gliotransmission in health and disease. Trends in Molecular Medicine 13, 54–63.CrossRefGoogle ScholarPubMed
Hartenstein, V., Nassif, C. and Lekven, A. (1998) Embryonic development of the Drosophila brain. II. Pattern of glial cells. Journal of Comparative Neurology 402, 32–47.3.0.CO;2-V>CrossRefGoogle ScholarPubMed
Haydon, P.G. (2001) GLIA: listening and talking to the synapse. Nature Reviews Neuroscience 2, 185–193.CrossRefGoogle Scholar
Haydon, P.G., Blendy, J., Moss, S.J. and Jackson, F.R. (2008) Astrocytic control of synaptic transmission and plasticity: a target for drugs of abuse? Neuropharmacology in press.Google ScholarPubMed
Hendricks, J.C., Finn, S.M., Panckeri, K.A., Chavkin, J., Williams, J.A., Sehgal, A. et al. (2000) Rest in Drosophila is a sleep-like state. Neuron 25, 129–138.CrossRefGoogle ScholarPubMed
Hoffmann, A.M., Bakardjiev, A. and Bauer, K. (1996) Carnosine-synthesis in cultures of rat glial cells is restricted to oligodendrocytes and carnosine uptake to astrocytes. Neuroscience Letters 215, 29–32.CrossRefGoogle ScholarPubMed
Hotta, Y. and Benzer, S. (1969) Abnormal electroretinograms in visual mutants of Drosophila. Nature 222, 354–356.CrossRefGoogle ScholarPubMed
Hovemann, B.T., Ryseck, R.P., Walldorf, U., Stortkuhl, K.F., Dietzel, I.D. and Dessen, E. (1998) The Drosophila ebony gene is closely related to microbial peptide synthetases and shows specific cuticle and nervous system expression. Gene 221, 1–9.CrossRefGoogle ScholarPubMed
Ito, K., Urban, J. and Technau, G.M. (1995) Distribution, classification, and development of Drosophila glial cells in the late embryonic and early larval ventral nerve cord. Roux's Archives of Developmental Biology 204, 284–307.CrossRefGoogle ScholarPubMed
Jan, L.Y. and Jan, Y.N. (1976) L-glutamate as an excitatory transmitter at the Drosophila larval neuromuscular junction. Journal of Physiology 262, 215–236.CrossRefGoogle ScholarPubMed
Jones, B.W. (2005) Transcriptional control of glial cell development in Drosophila. Developmental Biology 278, 265–273.CrossRefGoogle ScholarPubMed
Jourdain, P., Bergersen, L.H., Bhaukaurally, K., Bezzi, P., Santello, M., Domercq, M. et al. (2007) Glutamate exocytosis from astrocytes controls synaptic strength. Nature Neuroscience 10, 331–339.CrossRefGoogle ScholarPubMed
Kyriacou, C.P., Burnet, B. and Connolly, K. (1978) The behavioral basis of overdominance in competitive mating success at the ebony locus of Drosophila melanogaster. Animal Behavior 26, 1195–1206.CrossRefGoogle Scholar
Lee, C.J., Mannaioni, G., Yuan, H., Woo, D.H., Gingrich, M.B. and Traynelis, S.F. (2007) Astrocytic control of synaptic NMDA receptors. Journal of Physiology 581, 1057–1081.CrossRefGoogle ScholarPubMed
Liang, S.L., Carlson, G.C. and Coulter, D.A. (2006) Dynamic regulation of synaptic GABA release by the glutamate-glutamine cycle in hippocampal area CA1. Journal of Neuroscience 26, 8537–8548.CrossRefGoogle ScholarPubMed
MacDonald, J.M., Beach, M.G., Porpiglia, E., Sheehan, A.E., Watts, R.J. and Freeman, M.R. (2006) The Drosophila cell corpse engulfment receptor draper mediates glial clearance of severed axons. Neuron 50, 869–881.CrossRefGoogle ScholarPubMed
Newby, L.M. and Jackson, F.R. (1991) Drosophila ebony mutants have altered circadian activity rhythms but normal eclosion rhythms. Journal of Neurogenetics 7, 85–101.CrossRefGoogle ScholarPubMed
Newman, E.A. (2003a) Glial cell inhibition of neurons by release of ATP. Journal of Neuroscience 23, 1659–1666.CrossRefGoogle ScholarPubMed
Newman, E.A. (2003b) New roles for astrocytes: Regulation of synaptic transmission. Trends in Neurosciences 26, 536–542.CrossRefGoogle ScholarPubMed
Pak, W.L., Grossfield, J. and White, N.V. (1969) Nonphototactic mutants in a study of vision of Drosophila. Nature 222, 351–354.CrossRefGoogle Scholar
Panatier, A., Theodosis, D.T., Mothet, J.P., Touquet, B., Pollegioni, L., Poulain, D.A. et al. (2006) Glia-derived D-serine controls NMDA receptor activity and synaptic memory. Cell 125, 775–784.CrossRefGoogle ScholarPubMed
Parker, R.J. and Auld, V.J. (2006) Roles of glia in the Drosophila nervous system. Seminars in Cell and Developmental Biology 17, 66–77.CrossRefGoogle ScholarPubMed
Parpura, V., Basarsky, T.A., Liu, F., Jeftinija, K., Jeftinija, S. and Haydon, P.G. (1994) Glutamate-mediated astrocyte-neuron signalling. Nature 369, 744–747.CrossRefGoogle ScholarPubMed
Parri, H.R., Gould, T.M. and Crunelli, V. (2001) Spontaneous astrocytic Ca2+ oscillations in situ drive NMDAR-mediated neuronal excitation. Nature Neuroscience 4, 803–812.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Perea, G. and Araque, A. (2007) Astrocytes potentiate transmitter release at single hippocampal synapses. Science 317, 1083–1086.CrossRefGoogle ScholarPubMed
Richardt, A., Kemme, T., Wagner, S., Schwarzer, D., Marahiel, M.A. and Hovemann, B.T. (2003) Ebony, a novel nonribosomal peptide synthetase for beta-alanine conjugation with biogenic amines in Drosophila. Journal of Biological Chemistry 278, 41160–41166.CrossRefGoogle ScholarPubMed
Richardt, A., Rybak, A., Strortkuhl, K.F., Meinertzhagen, L.A. and Hovemann, B. (2002) Ebony protein in the Drosophila nervous system: Optic neuropile expression in glial cells. Journal of Comparative Neurology 452, 93–102.CrossRefGoogle ScholarPubMed
Rival, T., Soustelle, L., Cattaert, D., Strambi, C., Iche, M. and Birman, S. (2006) Physiological requirement for the glutamate transporter dEAAT1 at the adult Drosophila neuromuscular junction. Journal of Neurobiology 66, 1061–1074.CrossRefGoogle ScholarPubMed
Robitaille, R. (1998) Modulation of synaptic efficacy and synaptic depression by glial cells at the frog neuromuscular junction. Neuron 21, 847–855.CrossRefGoogle ScholarPubMed
Rodriguez, J.J., Davies, H.A., Errington, M.L., Verkhratsky, A., Bliss, T.V. and Stewart, M.G. (2008) ARG3.1/ARC expression in hippocampal dentate gyrus astrocytes: ultrastructural evidence and co-localization with glial fibrillary acidic protein. Journal of Cellular and Molecular Medicine 12, 671–678.CrossRefGoogle ScholarPubMed
Sanchez, D., Lopez-Arias, B., Torroja, L., Canal, I., Wang, X., Bastiani, M.J. et al. (2006) Loss of glial lazarillo, a homolog of apolipoprotein D, reduces lifespan and stress resistance in Drosophila. Current Biology 16, 680–686.CrossRefGoogle ScholarPubMed
Shaw, P.J., Cirelli, C., Greenspan, R.J. and Tononi, G. (2000) Correlates of sleep and waking in Drosophila melanogaster. Science 287, 1834–1837.CrossRefGoogle ScholarPubMed
Silies, M., Edenfeld, G., Engelen, D., Stork, T. and Klambt, C. (2007) Development of the peripheral glial cells in Drosophila. Neuron Glia Biology 3, 35–43.CrossRefGoogle ScholarPubMed
Stuart, A.E., Borycz, J. and Meinertzhagen, I.A. (2007) The dynamics of signaling at the histaminergic photoreceptor synapse of arthropods. Progress in Neurobiology 82, 202–227.CrossRefGoogle ScholarPubMed
Suh, J. and Jackson, F.R. (2007) Drosophila ebony activity is required in glia for the circadian regulation of locomotor activity. Neuron 55, 435–447.CrossRefGoogle ScholarPubMed
Tanaka, K., Watase, K., Manabe, T., Yamada, K., Watanabe, M., Takahashi, K. et al. (1997) Epilepsy and exacerbation of brain injury in mice lacking the glutamate transporter GLT-1. Science 276, 1699–1702.CrossRefGoogle ScholarPubMed
Tsuneyoshi, Y., Tomonaga, S., Asechi, M., Morishita, K., Denbow, M. and Furuse, M. (2007) Central administration of dipeptides, beta-alanyl-BCAAs, induces hyperactivity in chicks. BMC Neuroscience 8, 37.CrossRefGoogle ScholarPubMed
Volterra, A. and Meldolesi, J. (2005) Astrocytes, from brain glue to communication elements: the revolution continues. Nature Reviews Neuroscience 6, 626–640.CrossRefGoogle ScholarPubMed
Wagner, S., Heseding, C., Szlachta, K., True, J.R., Prinz, H. and Hovemann, B.T. (2007) Drosophila photoreceptors express cysteine peptidase tan. Journal of Comparative Neurology 500, 601–611.CrossRefGoogle ScholarPubMed
Walker, D.W., Muffat, J., Rundel, C. and Benzer, S. (2006) Overexpression of a Drosophila homolog of apolipoprotein D leads to increased stress resistance and extended lifespan. Current Biology 16, 674–679.CrossRefGoogle ScholarPubMed
Wang, L., Jil, C., Xu, Y., Xu, J., Dai, J., Wu, Q. et al. (2005) Cloning and characterization of a novel human homolog of mouse U26, a putative PQQ-dependent AAS dehydrogenase. Molecular Biology Reports 32, 47–53.CrossRefGoogle ScholarPubMed
Wolf, F.W. and Heberlein, U. (2003) Invertebrate models of drug abuse. Journal of Neurobiology 54, 161–178.CrossRefGoogle ScholarPubMed
Yang, Y., Ge, W., Chen, Y., Zhang, Z., Shen, W., Wu, C. et al. (2003) Contribution of astrocytes to hippocampal long-term potentiation through release of D-serine. Proceedings of the National Academy of Sciences of the U.S.A. 100, 15194–15199.CrossRefGoogle ScholarPubMed
Yuan, L.L. and Ganetzky, B. (1999) A glial-neuronal signaling pathway revealed by mutations in a neurexin-related protein. Science 283, 1343–1345.CrossRefGoogle Scholar
Zeigenfuss, J., Logan, M., Avery, M., Biswas, R., Stanley, E.R. and Freeman, M.R. (2007) The role of Draper/CED-1 signaling in glial phagocytosis of neuronal cell corpses and degenerating axons. Neuron Glia Biology 2, S10–S11.Google Scholar