Astrocytes potentiate GABAergic transmission in the thalamic reticular nucleus via endozepine signaling

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 50, 2013, Pages 20278-20283

  Christian, Catherine A ^a   Huguenard, John R ^a  

^a STANFORD UNIVERSITY   (United States)

Author keywords

Electrophysiology; Epilepsy; Glia; Thalamus; Uncaging

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID CARRIER; DIAZEPAM BINDING INHIBITOR; FLUMAZENIL; FLUOROCITRIC ACID;

ANIMAL CELL; ARTICLE; ASTROCYTE; BINDING SITE; CELLULAR DISTRIBUTION; CHROMOSOME DELETION; CONTROLLED STUDY; GABAERGIC TRANSMISSION; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MODULATION; MOUSE; NERVE CELL; NONHUMAN; PHOTOSTIMULATION; POINT MUTATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SYNAPTIC INHIBITION; THALAMUS RETICULAR NUCLEUS;

EID: 84890285161     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1318031110     Document Type: Article

References (66)

1. Gavish M, Snyder SH (1980) Benzodiazepine recognition sites on GABA receptors. Nature 287(5783):651-652.
2. Braestrup C, Squires RF (1977) Specific benzodiazepine receptors in rat brain characterized by high-affinity (3H)diazepam binding. Proc Natl Acad Sci USA 74(9):3805-3809.
3. Möhler H, Okada T (1977) Benzodiazepine receptor: Demonstration in the central nervous system. Science 198(4319):849-851.
4. Iversen L (1977) Anti-anxiety receptors in the brain? Nature 266:678.
5. Guidotti A, et al. (1983) Isolation, characterization, and purification to homogeneity of an endogenous polypeptide with agonistic action on benzodiazepine receptors. Proc Natl Acad Sci USA 80(11):3531-3535.
6. Alho H, et al. (1985) Diazepam-binding inhibitor: A neuropeptide located in selected neuronal populations of rat brain. Science 229(4709):179-182.
7. Bormann J (1991) Electrophysiological characterization of diazepam binding inhibitor (DBI) on GABAA receptors. Neuropharmacology 30(12B):1387-1389.
8. Alho H, Bovolin P, Jenkins D, Guidotti A, Costa E (1989) Cellular and subcellular localization of an octadecaneuropeptide derived from diazepam binding inhibitor: Immunohistochemical studies in the rat brain. J Chem Neuroanat 2(6):301-318.
9. Vidnyánszky Z, Görcs TJ, Hámori J (1994) Diazepam binding inhibitor fragment 33-50 (octadecaneuropeptide) immunoreactivity in the cerebellar cortex is restricted to glial cells. Glia 10(2):132-141.
10. Malagon M, et al. (1993) Ontogeny of diazepam-binding inhibitor-related peptides (endozepines) in the rat brain. Neuroscience 57(3):777-786.
11. Tonon MC, Désy L, Nicolas P, Vaudry H, Pelletier G (1990) Immunocytochemical localization of the endogenous benzodiazepine ligand octadecaneuropeptide (ODN) in the rat brain. Neuropeptides 15(1):17-24.
12. Alho H, Harjuntausta T, Schultz R, Pelto-Huikko M, Bovolin P (1991) Immunohistochemistry of diazepam binding inhibitor (DBI) in the central nervous system and peripheral organs: Its possible role as an endogenous regulator of different types of benzodiazepine receptors. Neuropharmacology 30(12B):1381-1386.
13. Loomis WF, Behrens MM, Williams ME, Anjard C (2010) Pregnenolone sulfate and cortisol induce secretion of acyl-CoA-binding protein and its conversion into endozepines from astrocytes. J Biol Chem 285(28):21359-21365.
14. Patte C, et al. (1999) GABA inhibits endozepine release from cultured rat astrocytes. Glia 25(4):404-411.
15. Masmoudi O, et al. (2005) Somatostatin down-regulates the expression and release of endozepines from cultured rat astrocytes via distinct receptor subtypes. J Neurochem 94(3):561-571.
16. Tokay T, et al. (2008) Beta-amyloid peptide stimulates endozepine release in cultured rat astrocytes through activation of N-formyl peptide receptors. Glia 56(13):1380-1389.
17. Masmoudi O, et al. (2003) Pituitary adenylate cyclase-activating polypeptide (PACAP) stimulates endozepine release from cultured rat astrocytes via a PKA-dependent mechanism. FASEB J 17(1):17-27.
18. Masmoudi-Kouki O, et al. (2006) PACAP stimulates biosynthesis and release of endozepines from rat astrocytes. Ann N Y Acad Sci 1070:411-416.
19. Papadopoulos V, Berkovich A, Krueger KE, Costa E, Guidotti A (1991) Diazepam binding inhibitor and its processing products stimulate mitochondrial steroid biosynthesis via an interaction with mitochondrial benzodiazepine receptors. Endocrinology 129(3):1481-1488.
20. Gandolfo P, et al. (2000) The triakontatetraneuropeptide (TTN) stimulates thymidine incorporation in rat astrocytes through peripheral-type benzodiazepine receptors. J Neurochem 75(2):701-707.
21. Christian CA, et al. (2013) Endogenous positive allosteric modulation of GABA(A) receptors by diazepam binding inhibitor. Neuron 78(6):1063-1074.
22. Jones EG (1975) Some aspects of the organization of the thalamic reticular complex. J Comp Neurol 162(3):285-308.
23. Houser CR, Vaughn JE, Barber RP, Roberts E (1980) GABA neurons are the major cell type of the nucleus reticularis thalami. Brain Res 200(2):341-354.
24. Huntsman MM, Porcello DM, Homanics GE, DeLorey TM, Huguenard JR (1999) Reciprocal inhibitory connections and network synchrony in the mammalian thalamus. Science 283(5401):541-543.
25. Schofield CM, Kleiman-Weiner M, Rudolph U, Huguenard JR (2009) A gain in GABAA receptor synaptic strength in thalamus reduces oscillatory activity and absence seizures. Proc Natl Acad Sci USA 106(18):7630-7635.
26. Löw K, et al. (2000) Molecular and neuronal substrate for the selective attenuation of anxiety. Science 290(5489):131-134.
27. Ohgami RS, et al. (2005) Identification of a ferrireductase required for efficient transferrin-dependent iron uptake in erythroid cells. Nat Genet 37(11):1264-1269.
28. Paulsen RE, Contestabile A, Villani L, Fonnum F (1987) An in vivo model for studying function of brain tissue temporarily devoid of glial cell metabolism: The use of fluorocitrate. J Neurochem 48(5):1377-1385.
29. Hassel B, Paulsen RE, Johnsen A, Fonnum F (1992) Selective inhibition of glial cell metabolism in vivo by fluorocitrate. Brain Res 576(1):120-124.
30. Nakanishi H, Kawachi A, Okada M, Fujiwara M, Yamamoto K (1996) Protective effect of MK-801 on the anoxia-aglycemia induced damage in the fluorocitrate-treated hippocampal slice of the rat. Brain Res 732(1-2):232-236.
31. Costa E, Guidotti A (1991) Diazepam binding inhibitor (DBI): A peptide with multiple biological actions. Life Sci 49(5):325-344.
32. Nimmerjahn A, Kirchhoff F, Kerr JN, Helmchen F (2004) Sulforhodamine 101 as a specific marker of astroglia in the neocortex in vivo. Nat Methods 1(1):31-37.
33. Kafitz KW, Meier SD, Stephan J, Rose CR (2008) Developmental profile and properties of sulforhodamine 101-labeled glial cells in acute brain slices of rat hippocampus. J Neurosci Methods 169(1):84-92.
34. Keros S, Hablitz JJ (2005) Subtype-specific GABA transporter antagonists synergistically modulate phasic and tonic GABAA conductances in rat neocortex. J Neurophysiol 94(3):2073-2085.
35. Beenhakker MP, Huguenard JR (2010) Astrocytes as gatekeepers of GABAB receptor function. J Neurosci 30(45):15262-15276.
36. Jensen K, Chiu CS, Sokolova I, Lester HA, Mody I (2003) GABA transporter-1 (GAT1)-deficient mice: Differential tonic activation of GABAA versus GABAB receptors in the hippocampus. J Neurophysiol 90(4):2690-2701.
37. De Biasi S, Vitellaro-Zuccarello L, Brecha NC (1998) Immunoreactivity for the GABA transporter-1 and GABA transporter-3 is restricted to astrocytes in the rat thalamus: A light and electron-microscopic immunolocalization. Neuroscience 83(3):815-828.
38. Vitellaro-Zuccarello L, Calvaresi N, De Biasi S (2003) 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(3):245-257.
39. Christian CA, Huguenard JR (2013) Sniffer patch laser uncaging response (SPLURgE): An assay of regional differences in allosteric receptor modulation and neurotransmitter clearance. J Neurophysiol 110(7):1722-1731.
40. Barres BA (2008) The mystery and magic of glia: A perspective on their roles in health and disease. Neuron 60(3):430-440.
41. Ward AA, Jr. (1947) Convulsive activity induced by fluoroacetate. J Neurophysiol 10(2):105-111.
42. Chenoweth MB, St John EF (1947) Studies on the pharmacology of fluoroacetate: Effects on the central nervous systems of dogs and rabbits. J Pharmacol Exp Ther 90(1):76-82.
43. Goldberg ND, Passonneau JV, Lowry OH (1966) Effects of changes in brain metabolism on the levels of citric acid cycle intermediates. J Biol Chem 241(17):3997-4003.
44. Hornfeldt CS, Larson AA (1990) Seizures induced by fluoroacetic acid and fluorocitric acid may involve chelation of divalent cations in the spinal cord. Eur J Pharmacol 179(3):307-313.
45. Bryant AS, Li B, Beenhakker MP, Huguenard JR (2009) Maintenance of thalamic epileptiform activity depends on the astrocytic glutamate-glutamine cycle. J Neurophysiol 102(5):2880-2888.
46. Huguenard JR, McCormick DA (2007) Thalamic synchrony and dynamic regulation of global forebrain oscillations. Trends Neurosci 30(7):350-356.
47. Thompson SM, Gähwiler BH (1992) Effects of the GABA uptake inhibitor tiagabine on inhibitory synaptic potentials in rat hippocampal slice cultures. J Neurophysiol 67(6):1698-1701.
48. Isaacson JS, Solís JM, Nicoll RA (1993) Local and diffuse synaptic actions of GABA in the hippocampus. Neuron 10(2):165-175.
49. Scanziani M (2000) GABA spillover activates postsynaptic GABA(B) receptors to control rhythmic hippocampal activity. Neuron 25(3):673-681.
50. Nusser Z, Mody I (2002) Selective modulation of tonic and phasic inhibitions in dentate gyrus granule cells. J Neurophysiol 87(5):2624-2628.
51. Engel D, et al. (1998) Laminar difference in GABA uptake and GAT-1 expression in rat CA1. J Physiol 512(Pt 3):643-649.
52. Kang J, Jiang L, Goldman SA, Nedergaard M (1998) Astrocyte-mediated potentiation of inhibitory synaptic transmission. Nat Neurosci 1(8):683-692.
53. Ortinski PI, et al. (2010) Selective induction of astrocytic gliosis generates deficits in neuronal inhibition. Nat Neurosci 13(5):584-591.
54. Liu QY, Schaffner AE, Chang YH, Maric D, Barker JL (2000) Persistent activation of GABA(A) receptor/Cl(-) channels by astrocyte-derived GABA in cultured embryonic rat hippocampal neurons. J Neurophysiol 84(3):1392-1403.
55. Kozlov AS, Angulo MC, Audinat E, Charpak S (2006) Target cell-specific modulation of neuronal activity by astrocytes. Proc Natl Acad Sci USA 103(26):10058-10063.
56. Lee S, et al. (2010) Channel-mediated tonic GABA release from glia. Science 330(6005):790-796.
57. Benedetti B, Matyash V, Kettenmann H (2011) Astrocytes control GABAergic inhibition of neurons in the mouse barrel cortex. J Physiol 589(Pt 5):1159-1172.
58. Abrahamsen H, Stenmark H (2010) Protein secretion: Unconventional exit by exophagy. Curr Biol 20(9):R415-R418.
59. Duran JM, Anjard C, Stefan C, Loomis WF, Malhotra V (2010) Unconventional secretion of Acb1 is mediated by autophagosomes. J Cell Biol 188(4):527-536.
60. Manjithaya R, Anjard C, Loomis WF, Subramani S (2010) Unconventional secretion of Pichia pastoris Acb1 is dependent on GRASP protein, peroxisomal functions, and autophagosome formation. J Cell Biol 188(4):537-546.
61. Hamilton NB, Attwell D (2010) Do astrocytes really exocytose neurotransmitters? Nat Rev Neurosci 11(4):227-238.
62. Araque A, Li N, Doyle RT, Haydon PG (2000) SNARE protein-dependent glutamate release from astrocytes. J Neurosci 20(2):666-673.
63. Perea G, Araque A (2007) Astrocytes potentiate transmitter release at single hippocampal synapses. Science 317(5841):1083-1086.
64. Schubert V, Bouvier D, Volterra A (2011) SNARE protein expression in synaptic terminals and astrocytes in the adult hippocampus: A comparative analysis. Glia 59(10):1472-1488.
65. Ohgami RS, et al. (2005) nm1054: A spontaneous, recessive, hypochromic, microcytic anemia mutation in the mouse. Blood 106(10):3625-3631.
66. Huguenard JR, Prince DA (1994) Clonazepam suppresses GABAB-mediated inhibition in thalamic relay neurons through effects in nucleus reticularis. J Neurophysiol 71(6):2576-2581.