Neurosteroidogenesis is required for the physiological response to stress: Role of neurosteroid-sensitive GABA A receptors

Journal of Neuroscience

Volumn 31, Issue 50, 2011, Pages 18198-18210

  Sarkar, Jhimly ^a   Wakefield, Seth ^b   MacKenzie, Georgina ^a   Moss, Stephen J ^a   Maguire, Jamie ^a  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b TUFTS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID A RECEPTOR DELTA; CORTICOSTERONE; CORTICOTROPIN RELEASING FACTOR; FINASTERIDE; NEUROSTEROID; TETRAHYDRODEOXYCORTICOSTERONE; UNCLASSIFIED DRUG;

ACUTE STRESS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEPHOSPHORYLATION; ELECTROPHYSIOLOGY; EXCITATION; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; IMMUNOHISTOCHEMISTRY; MALE; MAZE TEST; MOUSE; NEUROSTEROIDEGENESIS; NONHUMAN; OPEN FIELD TEST; PARAVENTRICULAR THALAMIC NUCLEUS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STEROIDOGENESIS; STRESS; WESTERN BLOTTING;

5-ALPHA REDUCTASE INHIBITORS; ANIMALS; BEHAVIOR, ANIMAL; CORTICOTROPIN-RELEASING HORMONE; DESOXYCORTICOSTERONE; FINASTERIDE; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; HYPOTHALAMUS; MALE; MICE; MICE, TRANSGENIC; NEURONS; NEUROTRANSMITTER AGENTS; PITUITARY-ADRENAL SYSTEM; RECEPTORS, GABA-A; STRESS, PHYSIOLOGICAL;

EID: 83455179222     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2560-11.2011     Document Type: Article

References (64)

1. Banke TG, McBain CJ (2006) GABAergic input onto CA3 hippocampal interneurons remains shunting throughout development. J Neurosci 26:11720-11725.
2. Barnard EA, Skolnick P, Olsen RW, Mohler H, Sieghart W, Biggio G, Braestrup C, Bateson AN, Langer SZ (1998) International Union of Pharmacology. XV. Subtypes of gamma-aminobutyric acidA receptors: classification on the basis of subunit structure and receptor function. Pharmacol Rev 50:291-313.
3. Belelli D, Casula A, Ling A, Lambert JJ (2002) The influence of subunit composition on the interaction of neurosteroids with GABA(A) receptors. Neuropharmacology 43:651-661.
4. Ben-Ari Y (2002) Excitatory actions of gaba during development: the nature of the nurture. Nat Rev Neurosci 3:728-739.
5. Boehm SL 2nd, Homanics GE, Blednov YA, Harris RA (2006) delta-Subunit GABAA receptor knockout mice are less sensitive to the actions of 4,5,6,7- tetrahydroisoxazolo-[5,4-c]pyridin-3-ol. Eur J Pharmacol 541:158-162.
6. Bolte S, Cordelières FP (2006) A guided tour into subcellular colocalization analysis in light microscopy. J Microsc 224:213-232.
7. Brown N, Kerby J, Bonnert TP, Whiting PJ, Wafford KA (2002) Pharmacological characterization of a novel cell line expressing human alpha(4)beta(3)delta GABA(A) receptors. Br J Pharmacol 136:965-974.
8. Browne SH, Kang J, Akk G, Chiang LW, Schulman H, Huguenard JR, Prince DA (2001) Kinetic and pharmacological properties of GABA(A) receptors in single thalamic neurons and GABA(A) subunit expression. J Neurophysiol 86:2312-2322.
9. Buijs RM, Kalsbeek A (2001) Hypothalamic integration of central and peripheral clocks. Nat Rev Neurosci 2:521-526.
10. Chrousos GP (2009) Stress and disorders of the stress system. Nat Rev Endocrinol 5:374-381.
11. Cohen I, Navarro V, Clemenceau S, Baulac M, Miles R (2002) On the origin of interictal activity in human temporal lobe epilepsy in vitro. Science 298:1418-1421.
12. Coull JA, Boudreau D, Bachand K, Prescott SA, Nault F, Sík A, De Koninck P, De Koninck Y (2003) Trans-synaptic shift in anion gradient in spinal lamina I neurons as a mechanism of neuropathic pain. Nature 424:938-942.
13. Crawley JN, Glowa JR, Majewska MD, Paul SM (1986) Anxiolytic activity of an endogenous adrenal steroid. Brain Res 398:382-385.
14. Decavel C, Van den Pol AN (1990) GABA: a dominant neurotransmitter in the hypothalamus. J Comp Neurol 302:1019-1037.
15. Dzhala VI, Talos DM, Sdrulla DA, Brumback AC, Mathews GC, Benke TA, Delpire E, Jensen FE, Staley KJ (2005) NKCC1 transporter facilitates seizures in the developing brain. Nat Med 11:1205-1213.
16. Farrant M, Kaila K (2007) The cellular, molecular and ionic basis of GABA(A) receptor signalling. Prog Brain Res 160:59-87.
17. Farrant M, Nusser Z (2005) Variations on an inhibitory theme: Phasic and tonic activation of GABA(A) receptors. Nat Rev Neurosci 6:215-229.
18. Guo AL, Petraglia F, Criscuolo M, Ficarra G, Nappi RE, Palumbo MA, Trentini GP, Purdy RH, Genazzani AR (1995) Evidence for a role of neurosteroids in modulation of diurnal changes and acute stress-induced corticosterone secretion in rats. Gynecol Endocrinol 9:1-7.
19. Herman JP, Figueiredo H, Mueller NK, Ulrich-Lai Y, Ostrander MM, Choi DC, Cullinan WE (2003) Central mechanisms of stress integration: hierarchical circuitry controlling hypothalamo-pituitary-adrenocortical responsiveness. Front Neuroendocrinol 24:151-180.
20. Herman JP, Mueller NK, FigueiredoH (2004) Role of GABA and glutamate circuitry in hypothalamo-pituitary-adrenocortical stress integration. Ann N Y Acad Sci 1018:35-45.
21. Hevers W, Lüddens H (1998) The diversity of GABA(A) receptors-Pharmacological and electrophysiological properties of GABA(A) channel subtypes. Mol Neurobiol 18:35-86.
22. Hewitt SA, Wamsteeker JI, Kurz EU, Bains JS (2009) Altered chloride homeostasis removes synaptic inhibitory constraint of the stress axis. Nat Neurosci 12:438-443.
23. Hoyda TD, Samson WK, Ferguson AV (2009) Adiponectin depolarizes parvocellular paraventricular nucleus neurons controlling neuroendocrine and autonomic function. Endocrinology 150:832-840.
24. Huberfeld G, Wittner L, Clemenceau S, Baulac M, Kaila K, Miles R, Rivera C (2007) Perturbed chloride homeostasis and GABAergic signaling in human temporal lobe epilepsy. J Neurosci 27:9866-9873.
25. Hübner CA, Stein V, Hermans-Borgmeyer I, Meyer T, Ballanyi K, Jentsch TJ (2001) Disruption of KCC2 reveals an essential role of K-Cl cotransport already in early synaptic inhibition. Neuron 30:515-524.
26. Jin X, Huguenard JR, Prince DA (2005) Impaired Cl- extrusion in layer V pyramidal neurons of chronically injured epileptogenic neocortex. J Neurophysiol 93:2117-2126.
27. Kahle KT, Staley KJ, Nahed BV, Gamba G, Hebert SC, Lifton RP, Mount DB (2008) Roles of the cation-chloride cotransporters in neurological disease. Nat Clin Pract Neurol 4:490-503.
28. Kuzmiski JB, Marty V, Baimoukhametova DV, Bains JS (2010) Stressinduced priming of glutamate synapses unmasks associative short-term plasticity. Nat Neurosci 13:1257-1264.
29. Larsen PJ, Seier V, Fink-Jensen A, Holst JJ, Warberg J, Vrang N (2003) Cocaine-and amphetamine-regulated transcript is present in hypothalamic neuroendocrine neurones and is released to the hypothalamicpituitary portal circuit. J Neuroendocrinol 15:219-226.
30. Lee HH, Walker JA, Williams JR, Goodier RJ, Payne JA, Moss SJ (2007) Direct protein kinase C-dependent phosphorylation regulates the cell surface stability and activity of the potassium chloride cotransporter KCC2. J Biol Chem 282:29777-29784.
31. Lee HH, Jurd R, Moss SJ (2010) Tyrosine phosphorylation regulates the membrane trafficking of the potassium chloride co-transporter KCC2. Mol Cell Neurosci 45:173-179.
32. Lee HH, Deeb TZ, Walker JA, Davies PA, Moss SJ (2011) NMDA receptor activity downregulates KCC2 resulting in depolarizing GABA(A) receptor-mediated currents. Nat Neurosci 14:736-743.
33. Luther JA, Daftary SS, Boudaba C, Gould GC, Halmos KC, Tasker JG (2002) Neurosecretory and non-neurosecretory parvocellular neurones of the hypothalamic paraventricular nucleus express distinct electrophysiological properties. J Neuroendocrinol 14:929-932.
34. Maguire J, Mody I (2007) Neurosteroid synthesis-mediated regulation of GABA(A) receptors: relevance to the ovarian cycle and stress. J Neurosci 27:2155-2162.
35. 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 8:797-804.
36. Maguire J, Ferando I, Simonsen C, Mody I (2009) Excitability changes related to GABAA receptor plasticity during pregnancy. J Neurosci 29:9592-9601.
37. Mihalek RM, Banerjee PK, Korpi ER, Quinlan JJ, Firestone LL, Mi ZP, Lagenaur C, Tretter V, Sieghart W, Anagnostaras SG, Sage JR, Fanselow MS, Guidotti A, Spigelman I, Li Z, DeLorey TM, Olsen RW, Homanics GE (1999) Attenuated sensitivity to neuroactive steroids in gammaaminobutyrate type A receptor delta subunit knockout mice. Proc Natl Acad Sci U S A 96:12905-12910.
38. Mody I, Pearce RA (2004) Diversity of inhibitory neurotransmission through GABAA receptors. Trends Neurosci 27:569-575.
39. Mortensen M, Ebert B, Wafford K, Smart TG (2010) Distinct activities of GABA agonists at synaptic-and extrasynaptic-type GABAA receptors. J Physiol 588:1251-1268.
40. Muñoz A, Méndez P, DeFelipe J, Alvarez-Leefmans FJ (2007) Cationchloride cotransporters and GABA-ergic innervation in the human epileptic hippocampus. Epilepsia 48:663-673.
41. Nabekura J, Ueno T, Okabe A, Furuta A, Iwaki T, Shimizu-Okabe C, Fukuda A, Akaike N (2002) Reduction of KCC2 expression and GABAA receptor-mediated excitation after in vivo axonal injury. J Neurosci 22:4412-4417.
42. Papp E, Rivera C, Kaila K, Freund TF (2008) Relationship between neuronal vulnerability and potassium-chloride cotransporter 2 immunoreactivity in hippocampus following transient forebrain ischemia. Neuroscience 154:677-689.
43. Park JB, Skalska S, Son S, Stern JE (2007) Dual GABAA receptor-mediated inhibition in rat presympathetic paraventricular nucleus neurons. J Physiol 582:539-551.
44. Payne JA, Rivera C, Voipio J, Kaila K (2003) Cation-chloride co-transporters in neuronal communication, development and trauma. Trends Neurosci 26:199-206.
45. 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 101:815-850.
46. Prescott SA, Sejnowski TJ, De Koninck Y (2006) Reduction of anion reversal potential subverts the inhibitory control of firing rate in spinal lamina I neurons: towards a biophysical basis for neuropathic pain. Mol Pain 2:32.
47. 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 U S A 88:4553-4557.
48. Reddy DS (2003) Is there a physiological role for the neurosteroid THDOC in stress-sensitive conditions? Trends Pharmacol Sci 24:103-106.
49. Reddy DS, Kulkarni SK (1997) Differential anxiolytic effects of neurosteroids in the mirrored chamber behavior test in mice. Brain Res 752:61-71.
50. Rivera C, Voipio J, Payne JA, Ruusuvuori E, Lahtinen H, Lamsa K, Pirvola U, Saarma M, Kaila K (1999) The K+/Cl- co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature 397:251-255.
51. Rivera C, Voipio J, Thomas-Crusells J, Li H, Emri Z, Sipilä S, Payne JA, Minichiello L, Saarma M, Kaila K (2004) Mechanism of activitydependent downregulation of the neuron-specific K-Cl cotransporter KCC2. J Neurosci 24:4683-4691.
52. Rivera C, Voipio J, Kaila K (2005) Two developmental switches in GABAergic signalling: the K+-Cl- cotransporter KCC2 and carbonic anhydrase CAVII. J Physiol 562:27-36.
53. Rodgers RJ, Johnson NJ (1998) Behaviorally selective effects of neuroactive steroids on plus-maze anxiety in mice. Pharmacol Biochem Behav 59:221-232.
54. Smith SS, Ruderman Y, Frye C, Homanics G, Yuan M (2006) Steroid withdrawal in the mouse results in anxiogenic effects of 3alpha,5beta-THP: a possible model of premenstrual dysphoric disorder. Psychopharmacology (Berl) 186:323-333.
55. Spigelman I, Li Z, Liang J, Cagetti E, Samzadeh S, Mihalek RM, Homanics GE, Olsen RW (2003) Reduced inhibition and sensitivity to neurosteroids in hippocampus of mice lacking the GABA(A) receptor delta subunit. J Neurophysiol 90:903-910.
56. Staley KJ, Mody I (1992) Shunting of excitatory input to dentate gyrus granule cells by a depolarizing GABAA receptor-mediated postsynaptic conductance. J Neurophysiol 68:197-212.
57. 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 GABA(A) receptors. Proc Natl Acad Sci U S A 100:14439-14444.
58. Ulrich-Lai YM, Herman JP (2009) Neural regulation of endocrine and autonomic stress responses. Nat Rev Neurosci 10:397-409.
59. Verkuyl JM, Hemby SE, Joëls M (2004) Chronic stress attenuates GABAergic inhibition and alters gene expression of parvocellular neurons in rat hypothalamus. Eur J Neurosci 20:1665-1673.
60. Verkuyl JM, Karst H, Joëls M (2005) GABAergic transmission in the rat paraventricular nucleus of the hypothalamus is suppressed by corticosterone and stress. Eur J Neurosci 21:113-121.
61. Wake H, Watanabe M, Moorhouse AJ, Kanematsu T, Horibe S, Matsukawa N, Asai K, Ojika K, Hirata M, Nabekura J (2007) Early changes in KCC2 phosphorylation in response to neuronal stress result in functional downregulation. J Neurosci 27:1642-1650.
62. Wamsteeker JI, Bains JS (2010) A synaptocentric view of the neuroendocrine response to stress. Eur J Neurosci 32:2011-2021.
63. Whiting PJ, Bonnert TP, McKernan RM, Farrar S, Le Bourdelles B, Heavens RP, Smith DW, Hewson L, Rigby MR, Sirinathsinghji DJ, Thompson SA, Wafford KA (1999) Molecular and functional diversity of the expanding GABA-A receptor gene family. Ann N Y Acad Sci 868:645-653.
64. Wohlfarth KM, Bianchi MT, Macdonald RL (2002) Enhanced neurosteroid potentiation of ternary GABA(A) receptors containing the delta subunit. J Neurosci 22:1541-1549.