Putative TRP channel antagonists, SKF 96365, flufenamic acid and 2-APB, are non-competitive antagonists at recombinant human α1β2γ2 GABAA receptors

Neurochemistry International

Volumn 60, Issue 6, 2012, Pages 543-554

  Rae, M G ^a   Hilton, J ^b   Sharkey, J ^c  

^a UNIVERSITY COLLEGE CORK   (Ireland)

^b James Black Centre   (United Kingdom)

^c UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

1 2 2 GABAA; 2 APB; Flufenamate; Patch clamp; SKF 96365; TRP

Indexed keywords

1 [2 (4 METHOXYPHENYL) 2 [3 (4 METHOXYPHENYL)PROPOXY]ETHYL] 1H IMIDAZOLE; 2 AMINOETHOXYDIPHENYLBORANE; 4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID A RECEPTOR ALPHA1; 4 AMINOBUTYRIC ACID A RECEPTOR ALPHA1BETA2GAMMA2; 4 AMINOBUTYRIC ACID A RECEPTOR BETA2; 4 AMINOBUTYRIC ACID A RECEPTOR GAMMA2; FLUFENAMIC ACID; TRANSIENT RECEPTOR POTENTIAL CHANNEL; UNCLASSIFIED DRUG;

ARTICLE; CELL STRAIN HEK293; CHLORIDE CURRENT; CONTROLLED STUDY; GABAERGIC SYSTEM; HUMAN; HUMAN CELL; IC 50; KINETICS; PATCH CLAMP; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR DOWN REGULATION;

ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; BINDING, COMPETITIVE; BORON COMPOUNDS; FLUFENAMIC ACID; GABA-A RECEPTOR ANTAGONISTS; HEK293 CELLS; HUMANS; IMIDAZOLES; RECEPTORS, GABA-A; RECOMBINANT PROTEINS; TRPC CATION CHANNELS;

EID: 84860445828     PISSN: 01970186     EISSN: 18729754     Source Type: Journal    
DOI: 10.1016/j.neuint.2012.02.014     Document Type: Article

References (76)

1. S.P.H. Alexander, A. Mathie, and J. Peters Guide to receptors and channels (GRAC) Br. J. Pharmacol. 158 2009 S1 S254 (fourth ed.)
2. D.J. Beech, K. Muraki, and R. Flemming Non-selective cationic channels of smooth muscle and the mammalian homologues of Drosophila TRP J. Physiol. 559 2004 685 706
3. C.P. Bengtson, A. Tozzi, G. Bernardi, and N.B. Mercuri Transient receptor potential-like channels mediate metabotropic glutamate receptor EPSCs in rat dopamine neurones J. Physiol. 555 2004 323 330
4. 2+ pumps by 2-aminoethoxydiphenyl borate (2-APB) Eur. J. Biochem. 269 2002 3678 3687
5. 2+ release FASEB J. 16 2002 1145 1150
6. N. Brown, J. Kerby, T.P. Bonnert, P.J. Whiting, and K.A. Wafford Pharmacological characterization of a novel cell line expressing human alpha(4)beta(3)delta GABA(A) receptors Br. J. Pharmacol. 136 2002 965 974
7. Q. Chen, J.W. Olney, P.D. Lukasiewicz, T. Almli, and C. Romano Fenamates protect neurons against ischemic and excitotoxic injury in chick embryo retina Neurosci. Lett. 242 1998 163 166
8. W. Cheng, C. Sun, and J. Zheng Heteromerization of TRP channel subunits: extending functional diversity Protein Cell 1 2011 802 810
9. D.W. Cope, P. Wulff, A. Oberto, M.I. Aller, M. Capogna, F. Ferraguti, C. Halbsguth, H. Hoeger, H.E. Jolin, A. Jones, A.N. McKenzie, W. Ogris, A. Poeltl, S.T. Sinkkonen, O.Y. Vekovischeva, E.R. Korpi, W. Sieghart, E. Sigel, P. Somogyi, and W. Wisden Abolition of zolpidem sensitivity in mice with a point mutation in the GABAA receptor gamma2 subunit Neuropharmacology 47 2004 17 34
10. J.L. Cousin, and R. Motais Inhibition of anion transport in the red blood cell by anionic amphiphilic compounds. II. Chemical properties of the flufenamate-binding site on the band 3 protein Biochim. Biophys. Acta 687 1982 156 164
11. L. Coyne, J. Su, D. Patten, and R.F. Halliwell Characterization of the interaction between fenamates and hippocampal neuron GABA(A) receptors Neurochem. Int. 51 2007 440 446
12. P.A. Davies, E.B. Hoffmann, H.J. Carlisle, R.F. Tyndale, and T.G. Hales The influence of an endogenous [beta]3 subunit on recombinant GABAA receptor assembly and pharmacology in WSS-1 cells and transiently transfected HEK293 cells Neuropharmacology 39 2000 611 620
13. R. Davies, S. Hayat, C.B. Wigley, and J. Robbins The calcium influx pathway in rat olfactory ensheathing cells shows TRPC channel pharmacology Brain Res. 1023 2004 154 156
14. B.N. Desai, and D.E. Clapham TRP channels and mice deficient in TRP channels Pflugers Arch. 451 2005 11 18
15. C. D'Hulst, J.R. Atack, and R.F. Kooy The complexity of the GABAA receptor shapes unique pharmacological profiles Drug Discovery Today 14 2009 866 875
16. J. Ding, Y. Xiao, D. Lu, Y.R. DU, X.Y. Cui, and J. Chen Effects of SKF-96365, a TRPC inhibitor, on melittin-induced inward current and intracellular Ca(2+) rise in primary sensory cells Neurosci. Bull. 27 2011 135 142
17. Y. El Hiani, A. Ahidouch, V. Lehen'kyi, F. Hague, F. Gouilleux, R. Mentaverri, S. Kamel, K. Lassoued, G. Brûlé, and H. Ouadid-Ahidouch Extracellular signal-regulated kinases 1 and 2 and TRPC1 channels are required for calcium-sensing receptor-stimulated MCF-7 breast cancer cell proliferation Cell. Physiol. Biochem. 23 2009 335 346
18. M. Fernandez, C. Lao-Peregrín, and E.D. Martín Flufenamic acid suppresses epileptiform activity in hippocampus by reducing excitatory synaptic transmission and neuronal excitability Epilepsia 51 2010 384 390
19. D. Franzius, M. Hoth, and R. Penner Non-specific effects of calcium entry antagonists in mast cells Pflugers Arch. 428 1994 433 438
20. 2+ release in Aplysia bag cell neurons J. Neurophysiol. 100 2008 38 49
21. H. Gogelein, and B. Pfannmuller The nonselective cation channel in the basolateral membrane of rat exocrine pancreas. Inhibition by 3′,5-dichlorodiphenylamine-2-carboxylic acid (DCDPC) and activation by stilbene disulfonates Pflugers Arch. 413 1989 287 298
22. E.B. Gonzales, C.L. Bell-Horner, M.I. Dibas, R.-Q. Huang, and G.H. Dillon Stoichiometric analysis of the TM2 6′ phenylalanine mutation on desensitization in [alpha]1[beta]2 and [alpha]1[beta]2[gamma]2 GABAA receptors Neurosci. Lett. 431 2008 184 189
23. A. Guilbert, M. Gautier, I. Dhennin-Duthille, N. Haren, H. Sevestre, and H. Ouadid-Ahidouch Evidence that TRPM7 is required for breast cancer cell proliferation Am. J. Physiol. Cell Physiol. 297 2009 C493 C502
24. R.F. Halliwell, P. Thomas, D. Patten, C.H. James, A. Martinez-Torres, R. Miledi, and T.G. Smart Subunit-selective modulation of GABAA receptors by the non-steroidal anti-inflammatory agent, mefenamic acid Eur. J. Neurosci. 11 1999 2897 2905
25. W. Hevers, and H. Luddens The diversity of GABAA receptors. Pharmacological and electrophysiological properties of GABAA channel subtypes Mol. Neurobiol. 18 1998 35 86
26. A. Hinman, H.H. Chuang, D.M. Bautista, and D. Julius TRP channel activation by reversible covalent modification Proc. Natl. Acad. Sci. USA 103 2006 19564 19568
27. S.J. Hong, W.W. Lin, and C.C. Chang Inhibition of the sodium channel by SK&F 96365, an inhibitor of the receptor-operated calcium channel, in mouse diaphragm J. Biomed. Sci. 1 1994 172 178
28. H.Z. Hu, Q. Gu, C. Wang, C.K. Colton, J. Tang, M. Kinoshita-Kawada, L.Y. Lee, J.D. Wood, and M.X. Zhu 2-Aminoethoxydiphenyl borate is a common activator of TRPV1, TRPV2, and TRPV3 J. Biol. Chem. 279 2004 35741 35748
29. H. Hu, J. Tian, Y. Zhu, C. Wang, R. Xiao, J.M. Herz, J.D. Wood, and M.X. Zhu Activation of TRPA1 channels by fenamate nonsteroidal anti-inflammatory drugs Pflugers Arch. 459 2010 579 592
30. C. Ikonomidou-Turski, E.A. Cavalheiro, L. Turski, Z.A. Bortolotto, Z. Kleinrok, L.S. Calderazzo-Filho, and W.A. Turski Differential effects of non-steroidal anti-inflammatory drugs on seizures produced by pilocarpine in rats Brain Res. 462 1988 275 285
31. 2+-permeable cation channel Circ. Res. 88 2001 325 332
32. F. Jia, L. Pignataro, C.M. Schofield, M. Yue, N.L. Harrison, and P.A. Goldstein An extrasynaptic GABAA receptor mediates tonic inhibition in thalamic VB neurons J. Neurophysiol. 94 2005 4491 4501
33. M.V. Jones, and G.L. Westbrook Desensitized states prolong GABAA channel responses to brief agonist pulses Neuron 15 1995 181 191
34. M.V. Jones, and G.L. Westbrook The impact of receptor desensitization on fast synaptic transmission TINS 19 1996 96 101
35. S. Jung, R. Strotmann, G. Schultz, and T.D. Plant TRPC6 is a candidate channel involved in receptor-stimulated cation currents in A7r5 smooth muscle cells Am. J. Physiol. Cell Physiol. 282 2002 C347 C359
36. P.S. Khansari, and R.F. Halliwell Evidence for neuroprotection by the fenamate NSAID, mefenamic acid Neurochem. Int. 55 2009 683 688
37. S.J. Kim, Y.S. Kim, J.P. Yuan, R.S. Petralia, P.F. Worley, and D.J. Linden Activation of the TRPC1 cation channel by metabotropic glutamate receptor mGluR1 Nature 426 2003 285 291
38. K. Kiselyov, X. Xu, G. Mozhayeva, T. Kuo, I. Pessah, G. Mignery, X. Zhu, L. Birnbaumer, and S. Muallem Functional interaction between InsP3 receptors and store-operated Htrp3 channels Nature 396 1998 478 482
39. E.R. Korpi, M.J. Mattila, W. Wisden, and H. Luddens GABA(A)-receptor subtypes: clinical efficacy and selectivity of benzodiazepine site ligands Ann. Rev. Med. 29 1997 275 282
40. E.R. Korpi, G. Grunder, and H. Luddens Drug interactions at GABA(A) receptors Prog. Neurobiol. 67 2002 113 159
41. J. Lerma, and R. Martin del Rio Chloride transport blockers prevent N-methyl-d-aspartate receptor-channel complex activation Mol. Pharmacol. 41 1992 217 222
42. J. Lipski, T.I. Park, D. Li, S.C. Lee, A.J. Trevarton, K.K. Chung, P.S. Freestone, and J.Z. Bai Involvement of TRP-like channels in the acute ischemic response of hippocampal CA1 neurons in brain slices Brain Res. 1077 2006 187 199
43. D. Liu, A. Scholze, Z. Zhu, R. Kreutz, M. Wehland-von-Trebra, W. Zidek, and M. Tepel Increased transient receptor potential channel TRPC3 expression in spontaneously hypertensive rats Am. J. Hypertens. 18 2005 1503 1507
44. 2+ channels Science 287 2000 1647 1651
45. 2+ entry channels J. Biol. Chem. 276 2001 18888 18896
46. 2+ release J. Biochem. 122 1997 498 505
47. R.M. McKernan, and P.J. Whiting Which GABAA-receptor subtypes really occur in the brain? TINS 19 1996 139 143
48. J.E. Merritt, W.P. Armstrong, C.D. Benham, T.J. Hallam, R. Jacob, A. Jaxa-Chamiec, B.K. Leigh, S.A. McCarthy, K.E. Moores, and T.J. Rink SK&F 96365, a novel inhibitor of receptor-mediated calcium entry Biochem. J. 271 1990 515 522
49. 2+ stores in permeabilized A7r5 cells Cell Calcium 29 2001 111 116
50. B. Nilius, G. Owsianik, T. Voets, and J.A. Peters Transient receptor potential cation channels in disease Physiol. Rev. 87 2007 165 217
51. R.W. Olsen, and W. Sieghart International Union of Pharmacology. LXX. Subtypes of GABAA-aminobutyric acid A receptors: classification on the basis of subunit composition, pharmacology, and function. Update Pharmacol. Rev. 60 2008 243 260
52. A.B. Parekh, A. Fleig, and R. Penner The store-operated calcium current I(CRAC): nonlinear activation by InsP3 and dissociation from calcium release Cell 89 1997 973 980
53. A. Patapoutian, S. Tate, and C.J. Woolf Transient receptor potential channels: targeting pain at the source Nat. Rev. Drug Discovery 8 2009 55 68
54. D.R. Peden, C.M. Petitjean, M.B. Herd, M.S. Durakoglugil, T.W. Rosahl, K. Wafford, G.E. Homanics, D. Belelli, J.-M. Fritschy, and J.J. Lambert Developmental maturation of synaptic and extrasynaptic GABAA receptors in mouse thalamic ventrobasal neurones J. Physiol. 586 2008 965 987
55. A.J. Picton, and J.L. Fisher Effect of the [alpha] subunit subtype on the macroscopic kinetic properties of recombinant GABAA receptors Brain Res. 1165 2007 40 49
56. S.S. Pong, and L. Levine Prostaglandin synthetase systems of rabbit tissues and their inhibition by nonsteroidal anti-inflammatory drugs J. Pharmacol. Exp. Ther. 196 1976 226 230
57. 2+ release by flufenamic acid and other blockers of the non-selective cation channel FEBS Lett. 296 1992 245 248
58. 3 receptors Cell Calcium 536 2001 3 19
59. J. Qiu, Y. Fang, O.K. Ronnekleiv, and M.J. Kelly Leptin excites proopiomelanocortin neurons via activation of TRPC channels J. Neurosci. 30 2010 1560 1565
60. I.S. Ramsey, M. Delling, and D.E. Clapham An introduction to TRP channels Annu. Rev. Physiol. 68 2006 619 647
61. A. Riccio, A.D. Medhurst, C. Mattei, R.E. Kelsell, A.R. Calver, A.D. Randall, C.D. Benham, and M.N. Pangalos MRNA distribution analysis of human TRPC family in CNS and peripheral tissues Mol. Brain Res. 109 2002 95 104
62. Y. Schiller Activation of a calcium-activated cation current during epileptiform discharges and its possible role in sustaining seizure-like events in neocortical slices J. Neurophysiol. 92 2004 862 872
63. G. Schwarz, G. Droogmans, and B. Nilius Multiple effects of SK&F 96365 on ionic currents and intracellular calcium in human endothelial cells Cell Calcium 15 1994 45 54
64. A. Singh, M.E. Hildebrand, E. Garcia, and T.P. Snutch The transient receptor potential channel antagonist SKF96365 is a potent blocker of low-voltage-activated T-type calcium channels Br. J. Pharmacol. 160 2010 1464 1475
65. S.T. Sinkkonen, S. Mansikkamaki, T. Moykkynen, H. Luddens, M. Uusi-Oukari, and E.R. Korpi Receptor subtype-dependent positive and negative modulation of GABA(A) receptor function by niflumic acid, a nonsteroidal anti-inflammatory drug Mol. Pharmacol. 64 2003 753 763
66. S.C. Smolinske, A.H. Hall, S.A. Vandenberg, D.G. Spoerke, and P.V. McBride Toxic effects of nonsteroidal anti-inflammatory drugs in overdose. An overview of recent evidence on clinical effects and dose-response relationships Drug Safety 5 1990 252 274
67. K. Togashi, H. Inada, and M. Tominaga Inhibition of the transient receptor potential cation channel TRPM2 by 2-aminoethoxydiphenyl borate (2-APB) Br. J. Pharmacol. 1531 2008 324 330
68. S. Ueno, C. Zorumski, J. Bracamontes, and J.H. Steinbach Endogenous subunits can cause ambiguities in the pharmacology of exogenous gamma-aminobutyric acid A receptors expressed in human embryonic kidney 293 cells Mol. Pharmacol. 50 1996 931 938
69. 2+-activated cation channels TRPM4 and TRPM5 from mice Cell Calcium 37 2005 267 278
70. T. Voets, J. Prenen, A. Fleig, R. Vennekens, H. Watanabe, J.G. Hoenderop, R.J. Bindels, G. Droogmans, R. Penner, and B. Nilius CaT1 and the calcium release-activated calcium channel manifest distinct pore properties J. Biol. Chem. 276 2001 47767 47770
71. M.C. Wallenstein Attenuation of epileptogenesis by nonsteroidal anti-inflammatory drugs in the rat Neuropharmacology 30 1991 657 663
72. - channels in Xenopus oocytes Mol. Pharmacol. 37 1990 720 724
73. C.V. Winder, J. Wax, B. Serrano, E.M. Jones, and P.M. Mc Anti-inflammatory and antipyretic properties of N-(alpha, alpha, alpha-trifluoro-m-tolyl) anthranilic acid (CI-440; flufenamic acid) Arthritis Rheum. 6 1963 36 47
74. A receptors expressed in Xenopus oocytes J. Pharm. Exp. Ther. 268 1994 806 817
75. S.Z. Xu, F. Zeng, G. Boulay, C. Grimm, C. Harteneck, and D.J. Beech Block of TRPC5 channels by 2-aminoethoxydiphenyl borate: a differential, extracellular and voltage-dependent effect Br. J. Pharmacol. 145 2005 405 414
76. W.J. Zhu, and S. Vicini Neurosteroid prolongs GABAA channel deactivation by altering kinetics of desensitized states J. Neurosci. 17 1997 4022 4031