Activity-dependent regulation of astrocyte GAT levels during synaptogenesis

Nature Neuroscience

Volumn 17, Issue 10, 2014, Pages 1340-1350

  Muthukumar, Allie K ^a   Stork, Tobias ^a   Freeman, Marc R ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID CARRIER; 4 AMINOBUTYRIC ACID RECEPTOR; EXCITATORY AMINO ACID TRANSPORTER; GABA TRANSPORTER 3; DROSOPHILA PROTEIN; GAL4 PROTEIN, DROSOPHILA; GAT; PEPTIDE; PHOTOPROTEIN; TRANSCRIPTION FACTOR;

4 AMINOBUTYRIC ACID RELEASE; ACTION POTENTIAL; ARTICLE; ASTROCYTE; CELL BODY; CELL COUNT; CELL GROWTH; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; GLIA CELL; IMMUNOREACTIVITY; IN VIVO STUDY; INTERNEURON; MOTOR ACTIVITY; NEUROPIL; NEUROTRANSMISSION; NEUROTRANSMITTER RELEASE; NONHUMAN; POSTSYNAPTIC DENSITY; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; REGULATORY MECHANISM; RNA INTERFERENCE; SUBESOPHAGEAL GANGLION; SYNAPSE; SYNAPSE VESICLE; SYNAPTOGENESIS; ANALYSIS OF VARIANCE; ANIMAL; CONFOCAL MICROSCOPY; DROSOPHILA; GENETICS; METABOLISM; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; PARALYSIS; PHYSIOLOGY; STIMULATION; TEMPERATURE; TRANSGENIC ANIMAL; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE;

ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, GENETICALLY MODIFIED; ASTROCYTES; DROSOPHILA; DROSOPHILA PROTEINS; GABAERGIC NEURONS; LUMINESCENT PROTEINS; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, TRANSMISSION; NEUROGENESIS; NEURONS; PARALYSIS; PEPTIDES; PHYSICAL STIMULATION; SYNAPSES; TEMPERATURE; TRANSCRIPTION FACTORS;

EID: 84921755691     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.3791     Document Type: Article

References (63)

1. Ullian, E.M.E., Sapperstein, S.K.S., Christopherson, K.S.K. & Barres, B.A.B. Control of synapse number by glia. Science 291, 657-661 (2001).
2. Schafer, D.P. et al. Microglia sculpt postnatal neural circuits in an activity and complement-dependent manner. Neuron 74, 691-705 (2012).
3. Allen, N.J. et al. Astrocyte glypicans 4 and 6 promote formation of excitatory synapses via GluA1 AMPA receptors. Nature 486, 410-414 (2012).
4. Eroglu, C. et al. Gabapentin receptor α2ä-1 is a neuronal thrombospondin receptor responsible for excitatory CNS synaptogenesis. Cell 139, 380-392 (2009).
5. Christopherson, K.S. et al. Thrombospondins are astrocyte-secreted proteins that promote CNS synaptogenesis. Cell 120, 421-433 (2005).
6. Tasdemir-Yilmaz, O.E. & Freeman, M.R. Astrocytes engage unique molecular programs to engulf pruned neuronal debris from distinct subsets of neurons. Genes Dev. 28, 20-33 (2014).
7. Su, Z.-Z. et al. Insights into glutamate transport regulation in human astrocytes: cloning of the promoter for excitatory amino acid transporter 2 (EAAT2). Proc. Natl. Acad. Sci. USA 100, 1955-1960 (2003).
8. Lehre, K.P.K., Levy, L.M.L., Ottersen, O.P.O., Storm-Mathisen, J.J. & Danbolt, N.C.N. Differential expression of two glial glutamate transporters in the rat brain: quantitative and immunocytochemical observations. J. Neurosci. 15, 1835-1853 (1995).
9. Isaacson, J.S., Solís, J.M. & Nicoll, R.A. Local and diffuse synaptic actions of GABA in the hippocampus. Neuron 10, 165-175 (1993).
10. Rossi, D.J. & Hamann, M. Spillover-mediated transmission at inhibitory synapses promoted by high affinity alpha6 subunit GABAA receptors and glomerular geometry. Neuron 20, 783-795 (1998).
11. Briggs, S.W. & Galanopoulou, A.S. Altered GABA signaling in early life epilepsies. Neural Plast. 2011, 527605 (2011).
12. Dudek, F.E. & Staley, K.J. How does the balance of excitation and inhibition shift during epileptogenesis? Epilepsy Curr. 7, 86-88 (2007).
13. Cope, D.W. et al. Enhanced tonic GABAA inhibition in typical absence epilepsy. Nat. Med. 15, 1392-1398 (2009).
14. Jacob, T.C., Moss, S.J. & Jurd, R. GABAA receptor trafficking and its role in the dynamic modulation of neuronal inhibition. Nat. Rev. Neurosci. 9, 331-343 (2008).
15. Schousboe, A. Role of astrocytes in the maintenance and modulation of glutamatergic and GABAergic neurotransmission. Neurochem. Res. 28, 347-352 (2003).
16. Sarup, A., Larsson, O.M. & Schousboe, A. GABA transporters and GABA-transaminase as drug targets. Curr. Drug Targets CNS Neurol. Disord. 2, 269-277 (2003).
17. Shigetomi, E., Tong, X., Kwan, K.Y., Corey, D.P. & Khakh, B.S. TRPA1 channels regulate astrocyte resting calcium and inhibitory synapse efficacy through GAT-3. Nat. Neurosci. 15, 70-80 (2012).
18. Kersanté, F. et al. A functional role for both GABA transporter-1 and GABA transporter-3 in the modulation of extracellular GABA and GABAergic tonic conductances in the rat hippocampus. J. Physiol. (Lond.) 591 (Pt. 10), 2429-2941 (2013).
19. Vitellaro-Zuccarello, L. & Calvaresi, N. Expression of GABA transporters, GAT-1 and GAT-3, in the cerebral cortex and thalamus of the rat during postnatal development. Cell Tissue Res. 313, 245-257 (2003).
20. Freeman, M.R. Specification and morphogenesis of astrocytes. Science 330, 774-778 (2010).
21. Enell, L., Hamasaka, Y., Kolodziejczyk, A. & Nässel, D.R. γ-Aminobutyric acid (GABA) signaling components in Drosophila: immunocytochemical localization of GABAB receptors in relation to the GABAA receptor subunit RDL and a vesicular GABA transporter. J. Comp. Neurol. 505, 18-31 (2007).
22. Köppers, B., Sánchez-Soriano, N., Letzkus, J.J., Technau, G.M. & Prokop, A. In developing Drosophila neurones the production of gamma-amino butyric acid is tightly regulated downstream of glutamate decarboxylase translation and can be influenced by calcium. J. Neurochem. 84, 939-951 (2003).
23. Neckameyer, W.S. & Cooper, R.L. GABA transporters in Drosophila melanogaster: molecular cloning, behavior, and physiology. Invert. Neurosci. 3, 279-294 (1998).
24. Stork, T., Sheehan, A., Tasdemir-Yilmaz, O.E. & Freeman, M.R. Neuron-glia interactions through the Heartless FGF receptor signaling pathway mediate morphogenesis of Drosophila astrocytes. Neuron 83, 388-403 (2014).
25. Jefferis, G.S.X.E. et al. Developmental origin of wiring specificity in the olfactory system of Drosophila. Development 131, 117-130 (2004).
26. Marin, E.C., Watts, R.J., Tanaka, N.K., Ito, K. & Luo, L. Developmentally programmed remodeling of the Drosophila olfactory circuit. Development 132, 725-737 (2005).
27. Zhu, S., Chiang, A.-S. & Lee, T. Development of the Drosophila mushroom bodies: elaboration, remodeling and spatial organization of dendrites in the calyx. Development 130, 2603-2610 (2003).
28. Hughes, E.G., Elmariah, S.B. & Balice-Gordon, R.J. Astrocyte secreted proteins selectively increase hippocampal GABAergic axon length, branching, and synaptogenesis. Mol. Cell. Neurosci. 43, 136-145 (2010).
29. Madsen, K.K., White, H.S. & Schousboe, A. Neuronal and non-neuronal GABA transporters as targets for antiepileptic drugs. Pharmacol. Ther. 125, 394-401 (2010).
30. Benediktsson, A.M. et al. Neuronal activity regulates glutamate transporter dynamics in developing astrocytes. Glia 60, 175-188 (2012).
31. Tanaka, K. et al. Epilepsy and exacerbation of brain injury in mice lacking the glutamate transporter GLT-1. Science 276, 1699-1702 (1997).
32. Devaraju, P., Sun, M.-Y., Myers, T.L., Lauderdale, K. & Fiacco, T.A. Astrocytic group I mGluR dependent potentiation of astrocytic glutamate and potassium uptake. J. Neurophysiol. 109, 2404-2414 (2013).
33. Yang, Y. et al. Presynaptic regulation of astroglial excitatory neurotransmitter transporter GLT1. Neuron 61, 880-894 (2009).
34. Charles, K.J., Calver, A.R., Jourdain, S. & Pangalos, M.N. Distribution of a GABAB-like receptor protein in the rat central nervous system. Brain Res. 989, 135-146 (2003).
35. Uwechue, N.M., Marx, M.-C., Chevy, Q. & Billups, B. Activation of glutamate transport evokes rapid glutamine release from perisynaptic astrocytes. J. Physiol. (Lond.) 590, 2317-2331 (2012).
36. Porter, J.T. & McCarthy, K.D. Astrocytic neurotransmitter receptors in situ and in vivo. Prog. Neurobiol. 51, 439-455 (1997).
37. Hamilton, N.B. & Attwell, D. Do astrocytes really exocytose neurotransmitters? Nat. Rev. Neurosci. 11, 227-238 (2010).
38. Padgett, C.L. & Slesinger, P.A. GABAB receptor coupling to G-proteins and ion channels. Adv. Pharmacol. 58, 123-147 (2010).
39. Mezler, M., Möller, T. & Raming, K. Cloning and functional expression of GABAB receptors from Drosophila. Eur. J. Neurosci. 13, 477-486 (2001).
40. Bettler, B., Kaupmann, K., Mosbacher, J. & Gassmann, M. Molecular structure and physiological functions of GABAB receptors. Physiol. Rev. 84, 835-867 (2004).
41. Kaupmann, K. et al. GABAB-receptor subtypes assemble into functional heteromeric complexes. Nature 396, 683-687 (1998).
42. Dahdal, D., Reeves, D.C., Ruben, M., Akabas, M.H. & Blau, J. Drosophila pacemaker neurons require g protein signaling and GABAergic inputs to generate twenty-four hour behavioral rhythms. Neuron 68, 964-977 (2010).
43. Parker, L., Howlett, I.C., Rusan, Z.M. & Tanouye, M.A. Seizure and epilepsy: studies of seizure disorders in Drosophila. Int. Rev. Neurobiol. 99, 1-21 (2011).
44. Pavlidis, P. & Tanouye, M.A. Seizures and failures in the giant fiber pathway of Drosophila bang-sensitive paralytic mutants. J. Neurosci. 15, 5810-5819 (1995).
45. Pavlidis, P., Ramaswami, M. & Tanouye, M.A. The Drosophila easily shocked gene: a mutation in a phospholipid synthetic pathway causes seizure, neuronal failure, and paralysis. Cell 79, 23-33 (1994).
46. Reynolds, E.R. et al. Treatment with the antiepileptic drugs phenytoin and gabapentin ameliorates seizure and paralysis of Drosophila bang-sensitive mutants. J. Neurobiol. 58, 503-513 (2004).
47. Kuebler, D. & Tanouye, M. Anticonvulsant valproate reduces seizure-susceptibility in mutant Drosophila. Brain Res. 958, 36-42 (2002).
48. Sills, G.J. & Brodie, M.J. Update on the mechanisms of action of antiepileptic drugs. Epileptic Disord. 3, 165-172 (2001).
49. Kucukdereli, H. et al. Control of excitatory CNS synaptogenesis by astrocyte-secreted proteins Hevin and SPARC. Proc. Natl. Acad. Sci. USA 108, E440-E449 (2011).
50. Oka, M., Wada, M., Wu, Q., Yamamoto, A. & Fujita, T. Functional expression of metabotropic GABAB receptors in primary cultures of astrocytes from rat cerebral cortex. Biochem. Biophys. Res. Commun. 341, 874-881 (2006).
51. Doherty, J., Logan, M.A., Taşdemir, O.E. & Freeman, M.R. Ensheathing glia function as phagocytes in the adult Drosophila brain. J. Neurosci. 29, 4768-4781 (2009).
52. Ng, M. et al. Transmission of olfactory information between three populations of neurons in the antennal lobe of the fly. Neuron 36, 463-474 (2002).
53. Luo, L., Liao, Y.J., Jan, L.Y. & Jan, Y.N. Distinct morphogenetic functions of similar small GTPases: Drosophila Drac1 is involved in axonal outgrowth and myoblast fusion. Genes Dev. 8, 1787-1802 (1994).
54. Potter, C.J., Tasic, B., Russler, E.V., Liang, L. & Luo, L. The Q system: a repressible binary system for transgene expression, lineage tracing, and mosaic analysis. Cell 141, 536-548 (2010).
55. Lee, T., Lee, A. & Luo, L. Development of the Drosophila mushroom bodies: sequential generation of three distinct types of neurons from a neuroblast. Development 126, 4065-4076 (1999).
56. Zhang, Y.Q., Rodesch, C.K. & Broadie, K. Living synaptic vesicle marker: synaptotagmin-GFP. Genesis 34, 142-145 (2002).
57. Grether, M.E., Abrams, J.M., Agapite, J., White, K. & Steller, H. The head involution defective gene of Drosophila melanogaster functions in programmed cell death. Genes Dev. 9, 1694-1708 (1995).
58. Kitamoto, T. Conditional modification of behavior in Drosophila by targeted expression of a temperature-sensitive shibire allele in defined neurons. J. Neurobiol. 47, 81-92 (2001).
59. Sweeney, S.T., Broadie, K., Keane, J., Niemann, H. & OKane, C.J. Targeted expression of tetanus toxin light chain in Drosophila specifically eliminates synaptic transmission and causes behavioral defects. Neuron 14, 341-351 (1995).
60. Baines, R.A., Uhler, J.P., Thompson, A., Sweeney, S.T. & Bate, M. Altered electrical properties in Drosophila neurons developing without synaptic transmission. J. Neurosci. 21, 1523-1531 (2001).
61. Hamada, F.N. et al. An internal thermal sensor controlling temperature preference in Drosophila. Nature 454, 217-220 (2008).
62. Ferris, J., Ge, H., Liu, L. & Roman, G. Go signaling is required for Drosophila associative learning. Nat. Neurosci. 9, 1036-1040 (2006).
63. McGuire, S.E., Le, P.T., Osborn, A.J., Matsumoto, K. & Davis, R.L. Spatiotemporal rescue of memory dysfunction in Drosophila. Science 302, 1765-1768 (2003).