High-throughput screening of neuronal Cl- channels: Why and how?

Current Neuropharmacology

Volumn 3, Issue 3, 2005, Pages 207-216

  Lynch, J W ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Anion channel; Drug discovery; Ligand gated; Neronal inhibition; Neuropharmacology; Voltage gated

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; ANION CHANNEL; CALCIUM CHANNEL; CALCIUM ION; CHLORIDE CHANNEL; RECEPTOR SUBTYPE; RECEPTOR SUBUNIT; VOLTAGE GATED CALCIUM CHANNEL; YELLOW FLUORESCENT PROTEIN;

ASSAY; CELL LINE; CELLULAR DISTRIBUTION; GENETIC TRANSFECTION; HIGH THROUGHPUT SCREENING; HUMAN; METHODOLOGY; NERVOUS SYSTEM; NONHUMAN; PROTEIN FUNCTION; REVIEW;

EID: 22944434191     PISSN: 1570159X     EISSN: None     Source Type: Journal    
DOI: 10.2174/1570159054368286     Document Type: Review

References (101)

1. Adkins, C.E., Pillai, G.V., Kerby, J., Bonnert, T.P., Haldon, C., McKernan, R.M., Gonzalez, J.E., Oades, K., Whiting, P.J., Simpson, P.B. (2001) α4β3δ GABA(A) receptors characterized by fluorescence resonance energy transfer-derived measurements of membrane potential. J. Biol. Chem., 276, 38934-38939.
2. Agnel, M., Vermat, T., Culouscou, J.M. (1999) Identification of three novel members of the calcium-dependent chloride channel (CaCC) family predominantly expressed in the digestive tract and trachea. FEBS Lett., 455, 295-301.
3. Ahmadi, S., Lippross, S., Neuhuber, W.L., Zeilhofer, H.U. (2002) PGE(2) selectively blocks inhibitory glycinergic neurotransmission onto rat superficial dorsal horn neurons. Nat. Neurosci., 5, 34-40.
4. Akaike, N., Sadoshima, J. (1989) Caffeine affects four different ionic currents in the bull-frog sympathetic neurone. J. Physiol., 412, 221-244.
5. Amara, S.G., Fontana, A.C. (2002) Excitatory amino acid transporters: keeping up with glutamate. Neurochem. Int., 41, 313-318.
6. Arriza, J.L., Eliasof, S., Kavanaugh, M.P., Amara, S.G. (1997) Excitatory amino acid transporter 5, a retinal glutamate transporter coupled to a chloride conductance. Proc. Natl. Acad. Sci. USA, 94, 4155-4160.
7. Arriza, J.L., Fairman, W.A., Wadiche, J.I., Murdoch, G.H., Kavanaugh, M.P., Amara, S.G. (1994) Functional comparisons of three glutamate transporter subtypes cloned from human motor cortex. J. Neurosci., 14, 5559-5569.
8. Bader, C.R., Bertrand, D., Schwartz, E.A. (1982) Voltage-activated and calcium-activated currents studied in solitary rod inner segments from the salamander retina. J. Physiol., 331, 253-284.
9. Bakall, B., Marmorstein, L.Y., Hoppe, G., Peachey, N.S., Wadelius, C., Marmorstein, A.D. (2003) Expression and localization of bestrophin during normal mouse development. Invest. Ophthalmol. Vis. Sci., 44, 3622-3628.
10. Changeux, J.P., Edelstein, S.J. (1998) Allosteric receptors after 30 years. Neuron, 21, 959-980.
11. Chaudhry, F.A., Lehre, K.P., van Lookeren Campagne, M., Ottersen, O.P., Danbolt, N.C., Storm-Mathisen, J. (1995) Glutamate transporters in glial plasma membranes: highly differentiated localizations revealed by quantitative ultrastructural immunocytochemistry. Neuron, 15, 711-720.
12. Chesler, M. (2003) Regulation and modulation of pH in the brain. Physiol. Rev., 83, 1183-1221.
13. Clark, S., Jordt, S.E., Jentsch, T.J., Mathie, A. (1998) Characterization of the hyperpolarization-activated chloride current in dissociated rat sympathetic neurons. J. Physiol., 506 (Pt 3), 665-678.
14. Cully, D.F., Vassilatis, D.K., Liu, K.K., Paress, P.S., Van der Ploeg, L.H., Schaeffer, J.M., Arena, J.P. (1994) Cloning of an avermectin-sensitive glutamate-gated chloride channel from Caenorhabditis elegans. Nature, 371, 707-711.
15. Danbolt, N.C. (2001) Glutamate uptake. Prog. Neurobiol., 65, 1-105.
16. Decher, N., Lang, H.J., Nilius, B., Bruggemann, A., Busch, A.E., Steinmeyer, K. (2001) DCPIB is a novel selective blocker of I(Cl,swell) and prevents swelling-induced shortening of guinea-pig atrial action potential duration. Br. J. Pharmacol., 134, 1467-1479.
17. Dehnes, Y., Chaudhry, F.A., Ullensvang, K., Lehre, K.P., Storm-Mathisen, J., Danbolt, N.C. (1998) The glutamate transporter EAAT4 in rat cerebellar Purkinje cells: a glutamate-gated chloride channel concentrated near the synapse in parts of the dendritic membrane facing astroglia. J. Neurosci., 18, 3606-3619.
18. Eliasof, S., Jahr, C.E. (1996) Retinal glial cell glutamate transporter is coupled to an anionic conductance. Proc. Natl. Acad. Sci. USA, 93, 4153-4158.
19. + secretion. Nature, 414, 558-561.
20. Fairman, W.A., Vandenberg, R.J., Arriza, J.L., Kavanaugh, M.P., Amara, S.G. (1995) An excitatory amino-acid transporter with properties of a ligand-gated chloride channel. Nature, 375, 599-603.
21. Friedrich, T., Breiderhoff, T., Jentsch, T.J. (1999) Mutational analysis demonstrates that ClC-4 and ClC-5 directly mediate plasma membrane currents. J. Biol. Chem., 274, 896-902.
22. - channels-homing in on an elusive channel species. Prog. Neurobiol., 60, 247-289.
23. Frings, S., Seifert, R., Godde, M., Kaupp, U.B. (1995) Profoundly different calcium permeation and blockage determine the specific function of distinct cyclic nucleotide-gated channels. Neuron, 15, 169-179.
24. Frizzell, R.A. (1999) Ten years with CFTR. Physiol. Rev., 79, S1-2.
25. Galietta, L.J., Haggie, P.M., Verkman, A.S. (2001) Green fluorescent protein-based halide indicators with improved chloride and iodide affinities. FEBS Lett., 499, 220-224.
26. Galietta, L.J., Moran, O. (2004) Identification of CFTR activators and inhibitors: chance or design? Curr. Opin. Pharmacol., 4, 497-503.
27. Galietta, L.V., Jayaraman, S., Verkman, A.S. (2001) Cell-based assay for high-throughput quantitative screening of CFTR chloride transport agonists. Am. J. Physiol. Cell Physiol., 281, C1734-1742.
28. Gisselmann, G., Pusch, H., Hovemann, B.T., Hatt, H. (2002) Two cDNAs coding for histamine-gated ion channels in D. melanogaster. Nat. Neurosci., 5, 11-12.
29. Gonzalez, J.E., Tsien, R.Y. (1997) Improved indicators of cell membrane potential that use fluorescence resonance energy transfer. Chem. Biol., 4, 269-277.
30. Grudzinska, J., Schemm, R., Haeger, S., Nicke, A., Schmalzing, G., Betz, H., Laube, B. (2005) The beta subunit determines the ligand binding properties of synaptic glycine receptors. Neuron, 45, 727-739.
31. Harvey, R.J., Depner, U.B., Wassle, H., Ahmadi, S., Heindl, C., Reinold, H., Smart, T.G., Harvey, K., Schutz, B., Abo-Salem, O.M., Zimmer, A., Poisbeau, P., Welzl, H., Wolfer, D.P., Betz, H., Zeilhofer, H.U., Muller, U. (2004) GlyR alpha3: an essential target for spinal PGE2-mediated inflammatory pain sensitization. Science, 304, 884-887.
32. Haug, K., Warnstedt, M., Alekov, A.K., Sander, T., Ramirez, A., Poser, B., Maljevic, S., Hebeisen, S., Kubisch, C., Rebstock, J., Horvath, S., Hallmann, K., Dullinger, J.S., Rau, B., Haverkamp, F., Beyenburg, S., Schulz, H., Janz, D., Giese, B., Muller-Newen, G., Propping, P., Elger, C.E., Fahlke, C., Lerche, H., Heils, A. (2003) Mutations in CLCN2 encoding a voltage-gated chloride channel are associated with idiopathic generalized epilepsies. Nat. Genet., 33, 527-532.
33. Ikejima, K., Qu, W., Stachlewitz, R.F., Thurman, R.G. (1997) Kupffer cells contain a glycine-gated chloride channel. Am. J. Physiol., 272, G1581-1586.
34. Iversen, L. (2004) GABA pharmacology- what prospects for the future? Biochem. Pharmacol., 68, 1537-1540.
35. Jensen, A.A., Brauner-Osborne, H. (2004) Pharmacological characterization of human excitatory amino acid transporters EAAT1, EAAT2 and EAAT3 in a fluorescence-based membrane potential assay. Biochem. Pharmacol., 67, 2115-2127.
36. Jensen, A.A., Kristiansen, U. (2004) Functional characterisation of the human alpha1 glycine receptor in a fluorescence-based membrane potential assay. Biochem. Pharmacol., 67, 1789-1799.
37. - channels gleaned from human genetic disease and mouse models. Annu. Rev. Physiol., 67, 779-807.
38. Jentsch, T.J., Stein, V., Weinreich, F., Zdebik, A.A. (2002) Molecular structure and physiological function of chloride channels. Physiol. Rev., 82, 503-568.
39. Jentsch, T.J., Steinmeyer, K., Schwarz, G. (1990) Primary structure of Torpedo marmorata chloride channel isolated by expression cloning in Xenopus oocytes. Nature, 348, 510-514.
40. Johnston, G.A., Chebib, M., Hanrahan, J.R., Mewett, K.N. (2003) GABA(C) receptors as drug targets. Curr. Drug Targets CNS Neurol. Disord., 2, 260-268.
41. Jurkat-Rott, K., Lehmann-Horn, F. (2004) The patch clamp technique in ion channel research. Curr. Pharm. Biotechnol., 5, 387-395.
42. Kaneko, H., Putzier, I., Frings, S., Kaupp, U.B., Gensch, T. (2004) Chloride accumulation in mammalian olfactory sensory neurons. J. Neurosci., 24, 7931-7938.
43. - ion flux measurements. Synapse, 13, 74-93.
44. Kleene, S.J. (1993) Origin of the chloride current in olfactory transduction. Neuron, 11, 123-132.
45. Kleene, S.J., Gesteland, R.C. (1991) Calcium-activated chloride conductance in frog olfactory cilia. J. Neurosci., 11, 3624-3629.
46. Kornak, U., Kasper, D., Bosl, M.R., Kaiser, E., Schweizer, M., Schulz, A., Friedrich, W., Delling, G., Jentsch, T.J. (2001) Loss of the ClC-7 chloride channel leads to osteopetrosis in mice and man. Cell, 104, 205-215.
47. Kruger, W., Gilbert, D., Hawthorne, R., Hryciw, D.H., Frings, S., Poronnik, P., Lynch, J.W. (2005) A yellow fluorescent protein-based assay for high-throughput screening of glycine and GABAA receptor chloride channels. Neurosci. Lett., 380, 340-345.
48. Kurahashi, T., Yau, K.W. (1993) Co-existence of cationic and chloride components in odorant-induced current of vertebrate olfactory receptor cells. Nature, 363, 71-74.
49. Leung, J.W., Xue, H. (2003) GABAergic functions and depression: from classical therapies to herbal medicine. Curr. Drug Targets CNS Neurol. Disord., 2, 363-374.
50. Lorenz, C., Pusch, M., Jentsch, T.J. (1996) Heteromultimeric CLC chloride channels with novel properties. Proc. Natl. Acad. Sci. USA, 93, 13362-13366.
51. Lowe, G., Gold, G.H. (1993) Nonlinear amplification by calcium-dependent chloride channels in olfactory receptor cells. Nature, 366, 283-286.
52. Lynch, J.W. (2004) Molecular structure and function of the glycine receptor chloride channel. Physiol. Rev., 84, 1051-1095.
53. Marquardt, A., Stohr, H., Passmore, L.A., Kramer, F., Rivera, A., Weber, B.H. (1998) Mutations in a novel gene, VMD2, encoding a protein of unknown properties cause juvenile-onset vitelliform macular dystrophy (Best's disease). Hum. Mol. Genet., 7, 1517-1525.
54. Mayer, M.L. (1985) A calcium-activated chloride current generates the after-depolarization of rat sensory neurones in culture. J. Physiol., 364, 217-239.
55. Meizel, S. (1997) Amino acid neurotransmitter receptor/chloride channels of mammalian sperm and the acrosome reaction. Biol. Reprod, 56, 569-574.
56. Milligan, C.J., Buckley, N.J., Garret, M., Deuchars, J., Deuchars, S.A. (2004) Evidence for inhibition mediated by coassembly of GABAA and GABAC receptor subunits in native central neurons. J. Neurosci., 24, 7241-7250.
57. Mongan, N.P., Baylis, H.A., Adcock, C., Smith, G.R., Sansom, M.S., Sattelle, D.B. (1998) An extensive and diverse gene family of nicotinic acetylcholine receptor alpha subunits in Caenorhabditis elegans. Recept. Channels, 6, 213-228.
58. Niemeyer, M.I., Yusef, Y.R., Cornejo, I., Flores, C.A., Sepulveda, F.V., Cid, L.P. (2004) Functional evaluation of human ClC-2 chloride channel mutations associated with idiopathic generalized epilepsies. Physiol. Genomics, 19, 74-83.
59. Nilius, B., Droogmans, G. (2003) Amazing chloride channels: an overview. Acta Physiol. Scand., 177, 119-147.
60. Nobile, M., Pusch, M., Rapisarda, C., Ferroni, S. (2000) Single-channel analysis of a ClC-2-like chloride conductance in cultured rat cortical astrocytes. FEBS Lett., 479, 10-14.
61. - conductance in cultured mouse spinal neurones. Nature, 311, 567-570.
62. Owens, D.F., Kriegstein, A.R. (2002) Is there more to GABA than synaptic inhibition? Nat. Rev. Neurosci., 3, 715-727.
63. Pan, Z.H., Zhang, D., Zhang, X., Lipton, S.A. (2000) Evidence for coassembly of mutant GABAC rho1 with GABAA gamma2S, glycine alpha1 and glycine alpha2 receptor subunits in vitro. Eur. J. Neurosci., 12, 3137-3145.
64. Petrukhin, K., Koisti, M.J., Bakall, B., Li, W., Xie, G., Marknell, T., Sandgren, O., Forsman, K., Holmgren, G., Andreasson, S., Vujic, M., Bergen, A.A., McGarty-Dugan, V., Figueroa, D., Austin, C.P., Metzker, M.L., Caskey, C.T., Wadelius, C. (1998) Identification of the gene responsible for Best macular dystrophy. Nat. Genet., 19, 241-247.
65. Pritchett, D.B., Sontheimer, H., Shivers, B.D., Ymer, S., Kettenmann, H., Schofield, P.R., Seeburg, P.H. (1989) Importance of a novel GABAA receptor subunit for benzodiazepine pharmacology. Nature, 338, 582-585.
66. Pusch, M. (2004) Ca(2+)-activated chloride channels go molecular. J. Gen. Physiol., 123, 323-325.
67. Qu, Z., Fischmeister, R., Hartzell, C. (2004) Mouse bestrophin-2 is a bona fide Cl(-) channel: identification of a residue important in anion binding and conduction. J. Gen. Physiol., 123, 327-340.
68. Qu, Z., Wei, R.W., Mann, W., Hartzell, H.C. (2003) Two bestrophins cloned from Xenopus laevis oocytes express Ca(2+)-activated Cl(-) currents. J. Biol. Chem., 278, 49563-49572.
69. Ranganathan, R., Cannon, S.C., Horvitz, H.R. (2000) MOD-1 is a serotonin-gated chloride channel that modulates locomotory behaviour in C. elegans. Nature, 408, 470-475.
70. Raymond, V., Sattelle, D.B. (2002) Novel animal-health drug targets from ligand-gated chloride channels. Nat. Rev. Drug Discov., 1, 427-436.
71. Rudolph, U., Crestani, F., Mohler, H. (2001) GABA(A) receptor subtypes: dissecting their pharmacological functions. Trends Pharmacol. Sci., 22, 188-194.
72. Rudolph, U., Mohler, 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.
73. Sardini, A., Amey, J.S., Weylandt, K.H., Nobles, M., Valverde, M.A., Higgins, C.F. (2003) Cell volume regulation and swelling-activated chloride channels. Biochim. Biophys. Acta, 1618, 153-162.
74. Sheppard, D.N., Gray, M.A., Gong, X., Sohma, Y., Kogan, I., Benos, D.J., Scott-Ward, T.S., Chen, J.H., Li, H., Cai, Z., Gupta, J., Li, C., Ramjeesingh, M., Berdiev, B.K., Ismailov, II, Bear, C.E., Hwang, T.C., Linsdell, P., Hug, M.J. (2004) The patch-clamp and planar lipid bilayer techniques: powerful and versatile tools to investigate the CFTR Cl- channel. J. Cyst. Fibros., 3 Suppl. 2, 101-108.
75. Sieghart, W., Fuchs, K., Tretter, V., Ebert, V., Jechlinger, M., Hoger, H., Adamiker, D. (1999) Structure and subunit composition of GABA(A) receptors. Neurochem. Int., 34, 379-385.
76. Sieghart, W., Sperk, G. (2002) Subunit composition, distribution and function of GABA(A) receptor subtypes. Curr. Top. Med. Chem., 2, 795-816.
77. Simpson, P.B., Woollacott, A.J., Pillai, G.V., Maubach, K.A., Hadingham, K.L., Martin, K., Choudhury, H.I., Seabrook, G.R. (2000) Pharmacology of recombinant human GABA(A) receptor subtypes measured using a novel pH-based high-throughput functional efficacy assay. J. Neurosci. Methods, 99, 91-100.
78. Smith, R.L., Clayton, G.H., Wilcox, C.L., Escudero, K.W., Staley, K.J. (1995) Differential expression of an inwardly rectifying chloride conductance in rat brain neurons: a potential mechanism for cell-specific modulation of postsynaptic inhibition. J. Neurosci., 15, 4057-4067.
79. Steinmeyer, K., Ortland, C., Jentsch, T.J. (1991) Primary structure and functional expression of a developmentally regulated skeletal muscle chloride channel. Nature, 354, 301-304.
80. Steinmeyer, K., Schwappach, B., Bens, M., Vandewalle, A., Jentsch, T.J. (1995) Cloning and functional expression of rat CLC-5, a chloride channel related to kidney disease. J. Biol. Chem., 270, 31172-31177.
81. Stobrawa, S.M., Breiderhoff, T., Takamori, S., Engel, D., Schweizer, M., Zdebik, A.A., Bosl, M.R., Ruether, K., Jahn, H., Draguhn, A., Jahn, R., Jentsch, T.J. (2001) Disruption of ClC-3, a chloride channel expressed on synaptic vesicles, leads to a loss of the hippocampus. Neuron, 29, 185-196.
82. Suginta, W., Karoulias, N., Aitken, A., Ashley, R.H. (2001) Chloride intracellular channel protein CLIC4 (p64H1) binds directly to brain dynamin I in a complex containing actin, tubulin and 14-3-3 isoforms. Biochem. J., 359, 55-64.
83. Sun, H., Tsunenari, T., Yau, K.W., Nathans, J. (2002) The vitelliform macular dystrophy protein defines a new family of chloride channels. Proc. Natl. Acad. Sci. USA, 99, 4008-4013.
84. Tang, W., Wildey, M.J. (2004) Development of a colorimetric method for functional chloride channel assay. J. Biomol. Screen, 9, 607-613.
85. Terlau, H., Olivera, B.M. (2004) Conus venoms: a rich source of novel ion channel-targeted peptides. Physiol. Rev., 84, 41-68.
86. Venglarik, C.J., Bridges, R.J., Frizzell, R.A. (1990) A simple assay for agonist-regulated Cl and K conductances in salt-secreting epithelia cells. Am. J. Physiol., 259, C358-364.
87. Verkman, A.S. (2004) Drug discovery and epithelial physiology. Curr. Opin. Nephrol. Hypertens., 13, 563-568.
88. Wachter, R.M., Remington, S.J. (1999) Sensitivity of the yellow variant of green fluorescent protein to halides and nitrate. Curr. Biol., 9, R628-629.
89. Wafford, K.A., Macaulay, A.J., Fradley, R., O'Meara, G.F., Reynolds, D.S., Rosahl, T.W. (2004) Differentiating the role of gamma-aminobutyric acid type A (GABAA) receptor subtypes. Biochem. Soc. Trans., 32, 553-556.
90. Wang, X., Li, M. (2003) Automated electrophysiology: high throughput of art. Assay Drug Dev. Technol., 1, 695-708.
91. Weinreich, F., Jentsch, T.J. (2001) Pores formed by single subunits in mixed dimers of different CLC chloride channels. J. Biol. Chem., 276, 2347-2353.
92. Whiting, P.J. (2003) The GABAA receptor gene family: new opportunities for drug development. Curr. Opin. Drug Discov. Devel., 6, 648-657.
93. Whiting, P.J., Bonnert, T.P., McKernan, R.M., Farrar, S., Le Bourdelles, B., Heavens, R.P., Smith, D.W., Hewson, L., Rigby, M.R., Sirinathsinghji, D.J., Thompson, S.A., Wafford, K.A. (1999) Molecular and functional diversity of the expanding GABA-A receptor gene family. Ann. N.Y. Acad. Sci., 868, 645-653.
94. Willumsen, N.J., Bech, M., Olesen, S.P., Jensen, B.S., Korsgaard, M.P., Christophersen, P. (2003) High throughput electrophysiology: new perspectives for ion channel drug discovery. Recept. Channels, 9, 3-12.
95. Wolff, C., Fuks, B., Chatelain, P. (2003) Comparative study of membrane potential-sensitive fluorescent probes and their use in ion channel screening assays. J. Biomol. Screen, 8, 533-543.
96. Yamada, K., Watanabe, M., Shibata, T., Tanaka, K., Wada, K., Inoue, Y. (1996) EAAT4 is a post-synaptic glutamate transporter at Purkinje cell synapses. Neuroreport, 7, 2013-2017.
97. Yang, H., Shelat, A.A., Guy, R.K., Gopinath, V.S., Ma, T., Du, K., Lukacs, G.L., Taddei, A., Folli, C., Pedemonte, N., Galietta, L.J., Verkman, A.S. (2003) Nanomolar affinity small molecule correctors of defective Delta F508-CFTR chloride channel gating. J. Biol. Chem., 278, 35079-35085.
98. Young, A.B., Snyder, S.H. (1973) Strychnine binding associated with glycine receptors of the central nervous system. Proc. Natl. Acad. Sci. USA, 70, 2832-2836.
99. Zerangue, N., Kavanaugh, M.P. (1996) Flux coupling in a neuronal glutamate transporter. Nature, 383, 634-637.
100. Zhang, D., Pan, Z.H., Awobuluyi, M., Lipton, S.A. (2001) Structure and function of GABA(C) receptors: a comparison of native versus recombinant receptors. Trends Pharmacol. Sci., 22, 121-132.
101. Zheng, W., Spencer, R.H., Kiss, L. (2004) High throughput assay technologies for ion channel drug discovery. Assay Drug Dev. Technol., 2, 543-552.