Neurosteroids promote phosphorylation and membrane insertion of extrasynaptic GABAA receptors

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

Volumn 111, Issue 19, 2014, Pages 7132-7137

  Abramian, Armen M ^a   Comenencia Ortiz, Eydith ^a   Modgil, Amit ^a   Vien, Thuy N ^a   Nakamura, Yasuko ^a   Moore, Yvonne E ^a,b   Maguire, Jamie L ^a   Terunuma, Miho ^a   Davies, Paul A ^a   Moss, Stephen J ^a,b  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Current rundown; PKC; Receptor insertion; Tonic current

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR ALPHA4; ALANINE; ALPHA BUNGAROTOXIN; BOTULINUM TOXIN A; NEUROSTEROID; POTASSIUM CHLORIDE COTRANSPORTER; PROTEIN KINASE C; RECOMBINANT RECEPTOR; RED FLUORESCENT PROTEIN; SERINE;

ANIMAL EXPERIMENT; ARTICLE; BRAIN REGION; CELL MEMBRANE; CELL SURFACE; CONTROLLED STUDY; DENTATE GYRUS; ENDOCYTOSIS; FLUORESCENCE MICROSCOPY; FOREBRAIN; HIPPOCAMPAL NEURONAL CULTURE; HIPPOCAMPUS; IMMUNOREACTIVITY; MEMBRANE INSERTION; MEMBRANE TRANSPORT; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; WHOLE CELL PATCH CLAMP;

CURRENT RUNDOWN; PKC; RECEPTOR INSERTION; TONIC CURRENT;

ANIMALS; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; COS CELLS; HEK293 CELLS; HIPPOCAMPUS; HUMANS; NEURONS; NEUROTRANSMITTER AGENTS; PATCH-CLAMP TECHNIQUES; PHOSPHORYLATION; PROTEIN KINASE C; RECEPTORS, CELL SURFACE; RECEPTORS, GABA-A; SENSORY GATING; SYNAPSES;

EID: 84900502560     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1403285111     Document Type: Article

References (43)

1. Belelli D, Lambert JJ (2005) Neurosteroids: Endogenous regulators of the GABA(A) receptor. Nat Rev Neurosci 6(7):565-575.
2. Paul SM, Purdy RH (1992) Neuroactive steroids. FASEB J 6(6):2311-2322.
3. Purdy RH, Morrow AL, Moore PH, Jr., Paul SM (1991) Stress-induced elevations of gamma-aminobutyric acid type A receptor-active steroids in the rat brain. Proc Natl Acad Sci USA 88(10):4553-4557.
4. Crawley JN, Glowa JR, Majewska MD, Paul SM (1986) Anxiolytic activity of an endogenous adrenal steroid. Brain Res 398(2):382-385.
5. Belelli D, Herd MB (2003) The contraceptive agent Provera enhances GABA(A) receptor-mediated inhibitory neurotransmission in the rat hippocampus: Evidence for endogenous neurosteroids? J Neurosci 23(31):10013-10020.
6. Stell BM, Brickley SG, Tang CY, Farrant M, Mody I (2003) Neuroactive steroids reduce neuronal excitability by selectively enhancing tonic inhibition mediated by delta subunit-containing GABAA receptors. Proc Natl Acad Sci USA 100(24):14439-14444.
7. Belelli D, Casula A, Ling A, Lambert JJ (2002) The influence of subunit composition on the interaction of neurosteroids with GABA(A) receptors. Neuropharmacology 43(4): 651-661.
8. Majewska MD, Harrison NL, Schwartz RD, Barker JL, Paul SM (1986) Steroid hormone metabolites are barbiturate-like modulators of the GABA receptor. Science 232(4753): 1004-1007.
9. Rudolph U, Möhler H (2004) Analysis of GABAA receptor function and dissection of the pharmacology of benzodiazepines and general anesthetics through mouse genetics. Annu Rev Pharmacol Toxicol 44:475-498.
10. Rudolph U, Möhler H (2006) GABA-based therapeutic approaches: GABAA receptor subtype functions. Curr Opin Pharmacol 6(1):18-23.
11. Brickley SG, Mody I (2012) Extrasynaptic GABA(A) receptors: Their function in the CNS and implications for disease. Neuron 73(1):23-34.
12. Luscher B, Fuchs T, Kilpatrick CL (2011) GABAA receptor trafficking-mediated plasticity of inhibitory synapses. Neuron 70(3):385-409.
13. Jacob TC, Moss SJ, Jurd R (2008) GABA(A) receptor trafficking and its role in the dynamic modulation of neuronal inhibition. Nat Rev Neurosci 9(5):331-343.
14. Olsen RW, Chang CS, Li G, Hanchar HJ, Wallner M (2004) Fishing for allosteric sites on GABA(A) receptors. Biochem Pharmacol 68(8):1675-1684.
15. Hosie AM, Clarke L, da Silva H, Smart TG (2009) Conserved site for neurosteroid modulation of GABA A receptors. Neuropharmacology 56(1):149-154.
16. Hosie AM, Wilkins ME, da Silva HM, Smart TG (2006) Endogenous neurosteroids regulate GABAA receptors through two discrete transmembrane sites. Nature 444(7118): 486-489.
17. Hosie AM, Wilkins ME, Smart TG (2007) Neurosteroid binding sites on GABA(A) receptors. Pharmacol Ther 116(1):7-19.
18. Brussaard AB, Wossink J, Lodder JC, Kits KS (2000) Progesterone- metabolite prevents protein kinase C-dependent modulation of gamma-aminobutyric acid type A receptors in oxytocin neurons. Proc Natl Acad Sci USA 97(7):3625-3630.
19. Maguire JL, Stell BM, Rafizadeh M, Mody I (2005) Ovarian cycle-linked changes in GABA(A) receptors mediating tonic inhibition alter seizure susceptibility and anxiety. Nat Neurosci 8(6):797-804.
20. Maguire J, Mody I (2007) Neurosteroid synthesis-mediated regulation of GABA(A) receptors: Relevance to the ovarian cycle and stress. J Neurosci 27(9):2155-2162.
21. Farrant M, Nusser Z (2005) Variations on an inhibitory theme: Phasic and tonic activation of GABA(A) receptors. Nat Rev Neurosci 6(3):215-229.
22. Yee BK, et al. (2004) GABA receptors containing the alpha5 subunit mediate the trace effect in aversive and appetitive conditioning and extinction of conditioned fear. Eur J Neurosci 20(7):1928-1936.
23. Chandra D, et al. (2006) GABAA receptor alpha 4 subunits mediate extrasynaptic inhibition in thalamus and dentate gyrus and the action of gaboxadol. Proc Natl Acad Sci USA 103(41):15230-15235.
24. Abramian AM, et al. (2010) Protein kinase C phosphorylation regulates membrane insertion of GABAA receptor subtypes that mediate tonic inhibition. J Biol Chem 285(53):41795-41805.
25. Parker PJ, Murray-Rust J (2004) PKC at a glance. J Cell Sci 117(Pt 2):131-132.
26. Mihalek RM, et al. (1999) Attenuated sensitivity to neuroactive steroids in gamma-aminobutyrate type A receptor delta subunit knockout mice. Proc Natl Acad Sci USA 96(22):12905-12910.
27. Glykys J, Mann EO, Mody I (2008) Which GABA(A) receptor subunits are necessary for tonic inhibition in the hippocampus? J Neurosci 28(6):1421-1426.
28. Lee HH, Deeb TZ, Walker JA, Davies PA, Moss SJ (2011) NMDA receptor activity downregulates KCC2 resulting in depolarizing GABAA receptor-mediated currents. Nat Neurosci 14(6):736-743.
29. Trache A, Meininger GA (2008) Total internal reflection fluorescence (TIRF) microscopy. Curr Protoc Microbiol Chapter 2:1, 22.
30. Jacob TC, et al. (2012) Benzodiazepine treatment induces subtype-specific changes in GABA(A) receptor trafficking and decreases synaptic inhibition. Proc Natl Acad Sci USA 109(45):18595-18600.
31. Lambert JJ, Peters JA, Sturgess NC, Hales TG (1990) Steroid modulation of the GABAA receptor complex: Electrophysiological studies. Ciba Found Symp 153:56-71, discussion 71-82.
32. Jia F, et al. (2005) An extrasynaptic GABAA receptor mediates tonic inhibition in thalamic VB neurons. J Neurophysiol 94(6):4491-4501.
33. Gulinello M, Gong QH, Li X, Smith SS (2001) Short-term exposure to a neuroactive steroid increases alpha4 GABA(A) receptor subunit levels in association with increased anxiety in the female rat. Brain Res 910(1-2):55-66.
34. Hsu FC, Waldeck R, Faber DS, Smith SS (2003) Neurosteroid effects on GABAergic synaptic plasticity in hippocampus. J Neurophysiol 89(4):1929-1940.
35. Lambert JJ, Cooper MA, Simmons RD, Weir CJ, Belelli D (2009) Neurosteroids: Endogenous allosteric modulators of GABA(A) receptors. Psychoneuroendocrinology 34(Suppl 1):S48-S58.
36. Harney SC, Frenguelli BG, Lambert JJ (2003) Phosphorylation influences neurosteroid modulation of synaptic GABAA receptors in rat CA1 and dentate gyrus neurones. Neuropharmacology 45(6):873-883.
37. Brandon NJ, et al. (1999) Subunit-specific association of protein kinase C and the receptor for activated C kinase with GABA type A receptors. J Neurosci 19(21): 9228-9234.
38. Brandon NJ, Jovanovic JN, Smart TG, Moss SJ (2002) Receptor for activated C kinase-1 facilitates protein kinase C-dependent phosphorylation and functional modulation of GABA(A) receptors with the activation of G-protein-coupled receptors. J Neurosci 22(15):6353-6361.
39. Hodge CW, et al. (2002) Decreased anxiety-like behavior, reduced stress hormones, and neurosteroid supersensitivity in mice lacking protein kinase Cepsilon. J Clin Invest 110(7):1003-1010.
40. Qi ZH, et al. (2007) Protein kinase C epsilon regulates gamma-aminobutyrate type A receptor sensitivity to ethanol and benzodiazepines through phosphorylation of gamma2 subunits. J Biol Chem 282(45):33052-33063.
41. Chou WH, et al. (2010) GABAA receptor trafficking is regulated by protein kinase C(epsilon) and the N-ethylmaleimide-sensitive factor. J Neurosci 30(42):13955-13965.
42. Pirker S, Schwarzer C, Wieselthaler A, Sieghart W, Sperk G (2000) GABA(A) receptors: Immunocytochemical distribution of 13 subunits in the adult rat brain. Neuroscience 101(4):815-850.
43. Saliba RS, Kretschmannova K, Moss SJ (2012) Activity-dependent phosphorylation of GABAA receptors regulates receptor insertion and tonic current. EMBO J 31(13): 2937-2951.