Partial Agonism of Taurine at Gamma-Containing Native and Recombinant GABAA Receptors

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  Kletke, Olaf ^a,b   Gisselmann, Guenter ^a   May, Andrea ^b   Hatt, Hanns ^a   A Sergeeva, Olga ^b  

^a RUHR UNIVERSITY BOCHUM   (Germany)

^b HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

3 AMINO 2 (3 CARBOXYPROPYL) 6 (4 METHOXYPHENYL)PYRIDAZINIUM BROMIDE; 4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID A RECEPTOR ALPHA1; 4 AMINOBUTYRIC ACID A RECEPTOR ALPHA2; 4 AMINOBUTYRIC ACID A RECEPTOR BETA1; 4 AMINOBUTYRIC ACID A RECEPTOR BETA3; 4 AMINOBUTYRIC ACID A RECEPTOR GAMMA1; 4 AMINOBUTYRIC ACID A RECEPTOR GAMMA2; TAURINE; TRACAZOLATE; ZOLPIDEM; 4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR STIMULATING AGENT; PROTEIN SUBUNIT; PYRIDINE DERIVATIVE; RECOMBINANT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BETA CHAIN; BRAIN ELECTROPHYSIOLOGY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG BINDING SITE; DRUG DETERMINATION; DRUG EFFICACY; DRUG POTENCY; DRUG POTENTIATION; DRUG RECEPTOR BINDING; DRUG STRUCTURE; GABAERGIC TRANSMISSION; HUMAN; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; RAT; SITE DIRECTED MUTAGENESIS; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; GENETICS; HYPOTHALAMUS; METABOLISM; MOLECULAR GENETICS; MUTATION; NERVE CELL; PROTEIN SUBUNIT; SEQUENCE ALIGNMENT; XENOPUS;

MAMMALIA;

AMINO ACID SEQUENCE; ANIMALS; GABA-A RECEPTOR AGONISTS; GAMMA-AMINOBUTYRIC ACID; HYPOTHALAMUS; MALE; MICE; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; MUTATION; NEURONS; PROTEIN SUBUNITS; PYRIDINES; RECEPTORS, GABA-A; RECOMBINANT PROTEINS; SEQUENCE ALIGNMENT; TAURINE; XENOPUS;

EID: 84876955433     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0061733     Document Type: Article

References (49)

1. Chepkova AN, Doreulee N, Yanovsky Y, Mukhopadhyay D, Haas HL, et al. (2002) Long-lasting enhancement of corticostriatal neurotransmission by taurine. Eur J Neurosci 16: 1523-1530.
2. Chepkova AN, Sergeeva OA, Haas HL, (2006) Taurine rescues hippocampal long-term potentiation from ammonia-induced impairment. Neurobiol Dis 23: 512-521.
3. Huxtable RJ, (1992) Physiological actions of taurine. Physiol Rev 72: 101-163.
4. Sergeeva OA, Chepkova AN, Doreulee N, Eriksson KS, Poelchen W, et al. (2003) Taurine-induced long-lasting enhancement of synaptic transmission in mice: role of transporters. J Physiol 550: 911-919.
5. Gundersen V, Chaudhry FA, Bjaalie JG, Fonnum F, Ottersen OP, et al. (1998) Synaptic vesicular localization and exocytosis of L-aspartate in excitatory nerve terminals: a quantitative immunogold analysis in rat hippocampus. J Neurosci 18(16): 6059-6070.
6. Kontro P, Marnela KM, Oja SS, (1980) Free amino acids in the synaptosome and synaptic vesicle fractions of different bovine brain areas. Brain Res 184: 129-141.
7. Molchanova S, Oja SS, Saransaari P, (2004) Characteristics of basal taurine release in the rat striatum measured by microdialysis. Amino Acids 27: 261-268.
8. Albrecht J, Schousboe A, (2005) Taurine interaction with neurotransmitter receptors in the CNS: an update. Neurochem Res 30: 1615-1621.
9. Lerma J, Herranz AS, Herreras O, Abraira V, Martin del RR, (1986) In vivo determination of extracellular concentration of amino acids in the rat hippocampus. A method based on brain dialysis and computerized analysis. Brain Res 384: 145-155.
10. Liu QR, Lopez-Corcuera B, Nelson H, Mandiyan S, Nelson N, (1992) Cloning and expression of a cDNA encoding the transporter of taurine and beta-alanine in mouse brain. Proc Natl Acad Sci U S A 89: 12145-12149.
11. Jia F, Yue M, Chandra D, Keramidas A, Goldstein PA, et al. (2008) Taurine is a potent activator of extrasynaptic GABA(A) receptors in the thalamus. J Neurosci 28: 106-115.
12. Sergeeva OA, Fleischer W, Chepkova AN, Warskulat U, Haussinger D, et al. (2007) GABAA-receptor modification in taurine transporter knockout mice causes striatal disinhibition. J Physiol 585: 539-548.
13. Schmieden V, Kuhse J, Betz H, (1992) Agonist pharmacology of neonatal and adult glycine receptor alpha subunits: identification of amino acid residues involved in taurine activation. EMBO J 11: 2025-2032.
14. Sergeeva OA, Haas HL, (2001) Expression and function of glycine receptors in striatal cholinergic interneurons from rat and mouse. Neuroscience 104: 1043-1055.
15. Dominguez-Perrot C, Feltz P, Poulter MO, (1996) Recombinant GABAA receptor desensitization: the role of the gamma 2 subunit and its physiological significance. J Physiol 497: 145-159.
16. Hadley SH, Amin J, (2007) Rat alpha6beta2delta GABAA receptors exhibit two distinct and separable agonist affinities. J Physiol 581: 1001-1018.
17. Olsen RW, Sieghart W, (2009) GABA A receptors: subtypes provide diversity of function and pharmacology. Neuropharmacology 56: 141-148.
18. Baumann SW, Baur R, Sigel E, (2002) Forced subunit assembly in alpha1beta2gamma2 GABAA receptors. Insight into the absolute arrangement. J Biol Chem 277: 46020-46025.
19. Farrant M, Nusser Z, (2005) Variations on an inhibitory theme: phasic and tonic activation of GABA(A) receptors. Nat Rev Neurosci 6: 215-229.
20. Sigel E, Buhr A, (1997) The benzodiazepine binding site of GABAA receptors. Trends Pharmacol Sci 18: 425-429.
21. Downing SS, Lee YT, Farb DH, Gibbs TT, (2005) Benzodiazepine modulation of partial agonist efficacy and spontaneously active GABA(A) receptors supports an allosteric model of modulation. Br J Pharmacol 145: 894-906.
22. Ju YH, Guzzo A, Chiu MW, Taylor P, Moran MF, et al. (2009) Distinct properties of murine alpha 5 gamma-aminobutyric acid type a receptors revealed by biochemical fractionation and mass spectroscopy. J Neurosci Res 87: 1737-1747.
23. McKernan RM, Whiting PJ, (1996) Which GABAA-receptor subtypes really occur in the brain? Trends Neurosci 19: 139-143.
24. Nutt D, (2006) GABAA receptors: subtypes, regional distribution, and function. J Clin Sleep Med 2: S7-11.
25. Sergeeva OA, Eriksson KS, Sharonova IN, Vorobjev VS, Haas HL, (2002) GABA(A) receptor heterogeneity in histaminergic neurons. Eur J Neurosci 16: 1472-1482.
26. Sergeeva OA, Andreeva N, Garret M, Scherer A, Haas HL, (2005) Pharmacological properties of GABAA receptors in rat hypothalamic neurons expressing the epsilon-subunit. J Neurosci 25: 88-95.
27. Sergeeva OA, Kletke O, Kragler A, Poppek A, Fleischer W, et al. (2010) Fragrant dioxane derivatives identify beta1-subunit-containing GABAA receptors. J Biol Chem 285: 23985-23993.
28. Yanovsky Y, Schubring S, Fleischer W, Gisselmann G, Zhu XR, et al. (2011) GABA(A) receptors involved in sleep and anaesthesia: beta1- versus beta3-containing assemblies. Pflugers Arch. 463: 187-199.
29. Cope DW, Halbsguth C, Karayannis T, Wulff P, Ferraguti F, et al. (2005) Loss of zolpidem efficacy in the hippocampus of mice with the GABAA receptor gamma2 F77I point mutation. Eur J Neurosci 21: 3002-3016.
30. Schubring SR, Fleischer W, Lin JS, Haas HL, Sergeeva OA, (2012) The bile steroid chenodeoxycholate is a potent antagonist at NMDA and GABA(A) receptors. Neurosci Lett 506: 322-326.
31. Ho SN, Hunt HD, Horton RM, Pullen JK, Pease LR, (1989) Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77: 51-59.
32. Saras A, Gisselmann G, Vogt-Eisele AK, Erlkamp KS, Kletke O, et al. (2008) Histamine action on vertebrate GABAA receptors: direct channel gating and potentiation of GABA responses. J Biol Chem 283: 10470-10475.
33. Draguhn A, Verdorn TA, Ewert M, Seeburg PH, Sakmann B, (1990) Functional and molecular distinction between recombinant rat GABAA receptor subtypes by Zn2+. Neuron 5: 781-788.
34. Nagaya N, Macdonald RL, (2001) Two gamma2L subunit domains confer low Zn2+ sensitivity to ternary GABA(A) receptors. J Physiol 532: 17-30.
35. Thompson SA, Wingrove PB, Connelly L, Whiting PJ, Wafford KA, (2002) Tracazolate reveals a novel type of allosteric interaction with recombinant gamma-aminobutyric acid(A) receptors. Mol Pharmacol 61: 861-869.
36. Bollan K, King D, Robertson LA, Brown K, Taylor PM, et al. (2003) GABA(A) receptor composition is determined by distinct assembly signals within alpha and beta subunits. J Biol Chem 278: 4747-4755.
37. Kreienkamp HJ, Maeda RK, Sine SM, Taylor P, (1995) Intersubunit contacts governing assembly of the mammalian nicotinic acetylcholine receptor. Neuron 14: 635-644.
38. Taylor PM, Connolly CN, Kittler JT, Gorrie GH, Hosie A, et al. (2000) Identification of residues within GABA(A) receptor alpha subunits that mediate specific assembly with receptor beta subunits. J Neurosci 20: 1297-1306.
39. Wingrove PB, Thompson SA, Wafford KA, Whiting PJ, (1997) Key amino acids in the gamma subunit of the gamma-aminobutyric acidA receptor that determine ligand binding and modulation at the benzodiazepine site. Mol Pharmacol 52: 874-881.
40. Wagner DA, Czajkowski C, Jones MV, (2004) An arginine involved in GABA binding and unbinding but not gating of the GABA(A) receptor. J Neurosci 24: 2733-2741.
41. Gunther U, Benson J, Benke D, Fritschy JM, Reyes G, et al. (1995) Benzodiazepine-insensitive mice generated by targeted disruption of the gamma 2 subunit gene of gamma-aminobutyric acid type A receptors. Proc Natl Acad Sci U S A 92: 7749-7753.
42. Walters RJ, Hadley SH, Morris KD, Amin J, (2000) Benzodiazepines act on GABAA receptors via two distinct and separable mechanisms. Nat Neurosci 3: 1274-1281.
43. Baur R, Kaur KH, Sigel E, (2010) Diversity of structure and function of alpha1alpha6beta3delta GABAA receptors: comparison with alpha1beta3delta and alpha6beta3delta receptors. J Biol Chem 285(23): 17398-17405.
44. Kaur KH, Baur R, Sigel E, (2009) Unanticipated structural and functional properties of delta-subunit-containing GABAA receptors. J Biol Chem 20 284(12): 7889-7896.
45. Bracamontes JR, Steinbach JH, (2008) Multiple modes for conferring surface expression of homomeric beta1 GABAA receptors. J Biol Chem 19 283: 26128-26136.
46. Lape R, Colquhoun D, Sivilotti LG, (2008) On the nature of partial agonism in the nicotinic receptor superfamily. Nature 454: 722-727.
47. Mukhtasimova N, Lee WY, Wang HL, Sine SM, (2009) Detection and trapping of intermediate states priming nicotinic receptor channel opening. Nature 459: 451-454.
48. Ribeiro RA, Bonfleur ML, Amaral AG, Vanzela EC, Rocco SA, et al. (2009) Taurine supplementation enhances nutrient-induced insulin secretion in pancreatic mice islets. Diabetes Metab Res Rev 25: 370-379.
49. Bailey SJ, Ravier MA, Rutter GA, (2007) Glucose-dependent regulation of gamma-aminobutyric acid (GABA A) receptor expression in mouse pancreatic islet alpha-cells. Diabetes 56: 320-327.