The effect of the neuroactive steroid 5β-pregnane-3β, 20(R)-diol on the time course of GABA evoked currents is different to that of pregnenolone sulphate

European Journal of Pharmacology

Volumn 605, Issue 1-3, 2009, Pages 78-86

  Strömberg, Jessica ^a   Lundgren, Per ^a   Taube, Magdalena ^b   Bäckström, Torbjörn ^a   Wang, Mingde ^a   Haage, David ^a,c  

^a Umea Neurosteroid Research Center   (Sweden)

^b UNIVERSITY OF GOTHENBURG   (Sweden)

^c UMEÅ UNIVERSITY   (Sweden)

Author keywords

(Rat); Desensitization; Patch clamp; sIPSCs; Tau decay

Indexed keywords

3ALPHA HYDROXY 5ALPHA PREGNAN 20 ONE; 4 AMINOBUTYRIC ACID; 5BETA PREGNAN 3BETA,20 DIOL; PREGNANEDIOL; PREGNENOLONE SULFATE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DESENSITIZATION; INHIBITORY POSTSYNAPTIC POTENTIAL; MALE; MEDIAL PREOPTIC AREA; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; RAT;

ANIMALS; ELECTROPHYSIOLOGY; GAMMA-AMINOBUTYRIC ACID; INHIBITORY POSTSYNAPTIC POTENTIALS; MALE; NEURONS; PATCH-CLAMP TECHNIQUES; PREGNANEDIOL; PREGNENOLONE; PREOPTIC AREA; RATS; RATS, SPRAGUE-DAWLEY; TIME FACTORS;

EID: 60649091074     PISSN: 00142999     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ejphar.2008.12.038     Document Type: Article

References (54)

1. Andreen L., Sundstrom-Poromaa I., Bixo M., Andersson A., Nyberg S., and Backstrom T. Relationship between allopregnanolone and negative mood in postmenopausal women taking sequential hormone replacement therapy with vaginal progesterone. Psychoneuroendocrinology 30 (2005) 212-224
2. Backstrom T., Andreen L., Birzniece V., Bjorn I., Johansson I.M., Nordenstam-Haghjo M., Nyberg S., Sundstrom-Poromaa I., Wahlstrom G., Wang M., and Zhu D. The role of hormones and hormonal treatments in premenstrual syndrome. CNS Drugs 17 (2003) 325-342
3. Bitran D., and Smith S.S. Termination of pseudopregnancy in the rat produces an anxiogenic-like response that is associated with an increase in benzodiazepine receptor binding density and a decrease in GABA-stimulated chloride influx in the hippocampus. Brain Res. Bull. 64 (2005) 511-518
4. Bitran D., and Solano S.M. Termination of pseudopregnancy in the rat alters the response to progesterone, chlordiazepoxide, and MK-801 in the elevated plus-maze. Psychopharmacology 180 (2005) 447-454
5. Brot M., Akwa Y., Purdy P., Koob G.F., and Britton K. The anxiolytic-like effects of the neurosteroid allopregnanolone: interactions with GABA(A) receptors. Eur. J. Pharmacol. 325 (1997) 1-7
6. Coolen L.M., Peters H.J.P.W., and Veening J.G. Fos immunoreactivity in the rat brain following consummatory elements of sexual behavior: a sex comparison. Brain Res. 738 (1996) 67-82
7. Eisenman L.N., He Y., Fields C., Zorumski C.F., and Mennerick S. Activation-dependent properties of pregnenolone sulfate inhibition of GABAA receptor-mediated current. J. Physiol. 550 3 (2003) 679-691
8. Finn D.A., and Gee K.W. The influence of estrus cycle on neurosteroid potency at the gamma-aminobutyric acidA receptor complex. J. Pharmacol. Exp. Ther. 265 (1993) 1374-1379
9. Fish E.W., Faccidomo S., DeBold J.F., and Miczek K.A. Alcohol, allopregnanolone and aggression in mice. Psychopharmacology (Berl) 153 (2001) 473-483
10. Garrett K.M., and Gan J. Enhancement of gamma-aminobutyric acidA receptor activity by alpha-chloralose. J. Pharmacol. Exp. Ther. 285 (1998) 680-686
11. Gulinello M., Gong Q.H., Li X., and Smith S.S. 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 (2001) 55-66
12. Haage D., and Johansson S. Neurosteroid modulation of synaptic and GABA-evoked currents in neurons from the rat medial preoptic nucleus. J. Neurophysiol. 82 (1999) 143-151
13. Haage D., Karlsson U., and Johansson S. Heterogeneous presynaptic Ca2+ channel types triggering GABA release onto medial preoptic neurons from rat. J. Physiol. 507 Pt 1 (1998) 77-91
14. Haage D., Druzin M., and Johansson S. Allopregnanolone modulates spontaneous GABA release via presynaptic Cl- permeability in rat preoptic nerve terminals. Brain Res. 958 (2002) 405-413
15. Haage D., Backstrom T., and Johansson S. Interaction between allopregnanolone and pregnenolone sulfate in modulating GABA-mediated synaptic currents in neurons from the rat medial preoptic nucleus. Brain Res. 1033 (2005) 58-67
16. Herd M.B., Belelli D., and Lambert J.J. Neurosteroid modulation of synaptic and extrasynaptic GABAA receptors. Pharmacol. Ther. (2007)
17. Horn R., and Marty A. Muscarinic activation of ionic currents measured by a new whole-cell recording method. J. Gen. Physiol. 92 (1988) 145-159
18. Johansson S., Sundgren A.K., and Klimenko V. Graded action potentials generated by neurons in rat hypothalamic slices. Brain Res. 700 (1995) 240-244
19. Johansson I.M., Birzniece V., Lindblad C., Olsson T., and Backstrom T. Allopregnanolone inhibits learning in the Morris water maze. Brain Res. 934 (2002) 125-131
20. Jones M.V., and Westbrook G.L. Desensitized states prolong GABAA channel responses to brief agonist pulses. Neuron 15 (1995) 181-191
21. Jones M.V., Sahara Y., Dzubay J.A., and Westbrook G.L. Defining affinity with the GABAA receptor. J. Neurosci. 18 (1998) 8590-8604
22. Jussofie A. Brain region-specific effects of neuroactive steroids on the affinity and density of the GABA-binding site. Biol. Chem. Hoppe Seyler 374 (1993) 265-270
23. Karlsson U., Sundgren A.K., Nasstrom J., and Johansson S. Glutamate-evoked currents in acutely dissociated neurons from the rat medial preoptic nucleus. Brain Res. 759 (1997) 270-276
24. Kokate T.G., Juhng K.N., Kirkby D., Llamas J., Yamaguchi S.-I., and Rogawski M.A. Convulsant actions of the neurosteroid pregnenolone sulfate in mice. Brain Res. 831 (1999) 119-124
25. Korpi E., and Sinkkonen S. GABAA receptor subtypes as targets for neuropsychiatric drug development. Pharmacol. Ther. 109 (2006) 12-32
26. Lagrange A.H., Botzolakis E.J., and MacDonald R.L. Enhanced macroscopic desensitization shapes the response of a4 subtype-containing GABAA receptors to synaptic and extrasynaptic GABA. J. Physiol. 578 (2007) 655-676
27. Lambert J.J., Belelli D., Peden D.R., Vardy A.W., and Peters J.A. Neurosteroid modulation of GABAA receptors. Prog. Neurobiol. 71 (2003) 67-80
28. Lundgren P., Stromberg J., Backstrom T., and Wang M. Allopregnanolone-stimulated GABA-mediated chloride ion flux is inhibited by 3beta-hydroxy-5alpha-pregnan-20-one (isoallopregnanolone). Brain Res. 982 (2003) 45-53
29. Maitra R., and Reynolds J.N. Modulation of GABA(A) receptor function by neuroactive steroids: evidence for heterogeneity of steroid sensitivity of recombinant GABA(A) receptor isoforms. Can. J. Physiol. Pharmacol. 76 (1998) 909-920
30. Majewska M.D., Harrison N.L., Schwartz R.D., Barker J.L., and Paul S.M. Steroid hormone metabolites are barbiturate-like modulators of the GABA receptor. Science 232 (1986) 1004-1007
31. Mennerick S., He Y., Jiang X., Manion B.D., Wang M., Shute A., Benz A., Evers A.S., Covey D.F., and Zorumski C.F. Selective antagonism of 5alpha-reduced neurosteroid effects at GABA(A) receptors. Mol. Pharmacol. 65 (2004) 1191-1197
32. Mody I., and Pearce R.A. Diversity of inhibitory neurotransmission through GABA(A) receptors. Trends Neurosci. 27 (2004) 569-575
33. Naylor D.E., Liu H., and Wasterlain C.G. Trafficking of GABAA receptors, loss of inhibition, and a mechanism for pharmacoresistance in status epilepticus. J. Neurosci. 25 (2005) 7724-7733
34. Neher E. Correction for liquid junction potentials in patch clamp experiments. Methods Enzymol. 207 (1992) 123-131
35. Norberg L., Wahlstrom G., and Backstrom T. The anaesthetic potency of 3 alpha-hydroxy-5 alpha-pregnan-20-one and 3 alpha-hydroxy-5 beta-pregnan-20-one determined with an intravenous EEG-threshold method in male rats. Pharmacol. Toxicol. 61 (1987) 42-47
36. Rae J., Cooper K., Gates P., and Watsky M. Low access resistance perforated patch recordings using amphotericin B. J. Neurosci. Methods 37 (1991) 15-26
37. Rupprecht R., and Holsboer F. Neuroactive steroids: mechanisms of action and neuropsychopharmacological perspectives. Trends Neurosci. 22 (1999) 410-416
38. Sapp D.W., Witte U., Turner D.M., Longoni B., Kokka N., and Olsen R.W. Regional variation in steroid anesthetic modulation of [35S]TBPS binding to gamma-aminobutyric acidA receptors in rat brain. J. Pharmacol. Exp. Ther. 262 (1992) 801-808
39. Shen W., Mennerick S., Covey D.F., and Zorumski C.F. Pregnenolone sulfate modulates inhibitory synaptic transmission by enhancing GABA(A) receptor desensitization. J. Neurosci. 20 (2000) 3571-3579
40. Smith S.S., Gong Q.H., Li X., Moran M.H., Bitran D., Frye C.A., and Hsu F.C. Withdrawal from 3alpha-OH-5alpha-pregnan-20-One using a pseudopregnancy model alters the kinetics of hippocampal GABAA-gated current and increases the GABAA receptor alpha4 subunit in association with increased anxiety. J. Neurosci. 18 (1998) 5275-5284
41. Stromberg J., Haage D., Taube M., Backstrom T., and Lundgren P. Neurosteroid modulation of allopregnanolone and GABA effect on the GABA-A receptor. Neuroscience 143 (2006) 73-81
42. Swann J.M. Gonadal steroids regulate behavioral response to pheromones by actions on a subdivision of the medial preoptic nucleus. Brain Res. 750 (1997) 189-194
43. Turkmen S., Lundgren P., Birzniece V., Zingmark E., Backstrom T., and Johansson I.M. 3beta-20beta-dihydroxy-5alpha-pregnane (UC1011) antagonism of the GABA potentiation and the learning impairment induced in rats by allopregnanolone. Eur. J. Neurosci. 20 (2004) 1604-1612
44. Wang M., Seippel L., Purdy R.H., and Backstrom T. Relationship between symptom severity and steroid variation in women with premenstrual syndrome: study on serum pregnenolone, pregnenolone sulfate, 5 alpha-pregnane-3,20-dione and 3 alpha-hydroxy-5 alpha-pregnan-20-one. J. Clin. Endocrinol. Metab. 81 (1996) 1076-1082
45. Wang M.D., Backstrom T., and Landgren S. The inhibitory effects of allopregnanolone and pregnanolone on the population spike, evoked in the rat hippocampal CA1 stratum pyramidale in vitro, can be blocked selectively by epiallopregnanolone. Acta Physiol. Scand. 169 (2000) 333-341
46. Wang M., He Y., Eisenman L.N., Fields C., Zeng C.M., Mathews J., Benz A., Fu T., Zorumski E., Steinbach J.H., Covey D.F., Zorumski C.F., and Mennerick S. 3beta-hydroxypregnane steroids are pregnenolone sulfate-like GABA(A) receptor antagonists. J. Neurosci. 22 (2002) 3366-3375
47. Wang M.D., Rahman M., Zhu D., Johansson I.M., and Backstrom T. 3Beta-hydroxysteroids and pregnenolone sulfate inhibit recombinant rat GABA(A) receptor through different channel property. Eur. J. Pharmacol. 557 (2007) 124-131
48. Wieland S., Lan N.C., Mirasedeghi S., and Gee K.W. Anxiolytic activity of the progesterone metabolite 5 alpha-pregnan-3 alpha-o1-20-one. Brain Res. 565 (1991) 263-268
49. Wilson M.A., and Biscardi R. Influence of gender and brain region on neurosteroid modulation of GABA responses in rats. Life Sci. 60 (1997) 1679-1691
50. Vincens M., Dartois E., Popelier M., Marquette C., Moyse E., Fillion G., and Haour F. Autoradiographic study of neurosteroid binding sites labelled with [35S]-TBPS in brain of different species. Brain Res. Bull. 32 (1993) 251-256
51. Vorobjev V. Vibrodissociation of sliced mammalian nervous. J. Neurosci. Methods 38 (1991) 145-150
52. Yu R., Follesa P., and Ticku M.K. Down-regulation of the GABA receptor subunits mRNA levels in mammalian cultured cortical neurons following chronic neurosteroid treatment. Brain Res. Mol. Brain Res. 41 (1996) 163-168
53. Zhu W.J., Wang J.F., Krueger K.E., and Vicini S. δ subunit inhibits neurosteroid modulation of GABAA receptors. J. Neurosci. 16 (1996) 6648-6656
54. Zhu W.J., and Vicini S. Neurosteroid prolongs GABAA channel deactivation by altering kinetics of desensitized states. J. Neurosci. 17 (1997) 4022-4031