Functional characterization of ivermectin binding sites in α1β2γ2L gaba(A) receptors

Frontiers in Molecular Neuroscience

Volumn 8, Issue September, 2015, Pages

  Estrada Mondragon, Argel ^a   Lynch, Joseph W ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Avermectin; Cys loop receptor; GABA; Ion channel; Ligand gated; Macrocyclic lactone; Pharmacology

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID A RECEPTOR ALPHA1; 4 AMINOBUTYRIC ACID A RECEPTOR BETA2; 4 AMINOBUTYRIC ACID A RECEPTOR GAMMA2; IVERMECTIN;

ARTICLE; CAENORHABDITIS ELEGANS; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG BINDING SITE; DRUG RECEPTOR BINDING; ELECTROPHYSIOLOGY; HUMAN; HUMAN CELL; MOLECULAR BIOLOGY; MOLECULAR DOCKING; MOLECULAR MODEL; PROTEIN INTERACTION; PROTEIN SUBUNIT; SEQUENCE ALIGNMENT; SITE DIRECTED MUTAGENESIS;

EID: 84942798917     PISSN: 16625099     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnmol.2015.00055     Document Type: Article

References (30)

1. Adelsberger, H., Lepier, A., and Dudel, J. (2000). Activation of rat recombinant alpha(1)beta(2)gamma(2S) GABA(A) receptor by the insecticide ivermectin. Eur. J. Pharmacol. 394, 163-170. doi: 10.1016/S0014-2999(00)00164-3
2. Akk, G., Covey, D. F., Evers, A. S., Steinbach, J. H., Zorumski, C. F., and Mennerick, S. (2007). Mechanisms of neurosteroid interactions with GABA(A) receptors. Pharmacol. Ther. 116,35-57.doi: 10.1016/j.pharmthera.2007.03.004
3. Althoff, T., Hibbs, R. E., Banerjee, S., and Gouaux, E. (2014). X-ray structures of GluCl in apo states reveal a gating mechanism of Cys-loop receptors. Nature 512, 333-337. doi: 10.1038/nature13669
4. Baumann, S. W., Baur, R., and Sigel, E. (2001). Subunit arrangement of gamma-aminobutyric acid type a receptors. J. Biol. Chem. 276, 36275-36280. doi: 10.1074/jbc.M105240200
5. Campbell, W. C. (2012). History of avermectin and ivermectin, with notes on the history of other macrocyclic lactone antiparasitic agents. Curr. Pharm. Biotechnol. 13, 853-865. doi: 10.2174/138920112800399095
6. Chiara, D. C., Jayakar, S. S., Zhou, X., Zhang, X., Savechenkov, P. Y., Bruzik, K. S., et al. (2013). Specificity of intersubunit general anesthetic-binding sites in the transmembrane domain of the human alpha1beta3gamma2 gamma-aminobutyric acid type A (GABAA) receptor. J. Biol. Chem. 288, 19343-19357. doi: 10.1074/jbc.M113.479725
7. Collins, T., and Millar, N. S. (2010). Nicotinic acetylcholine receptor transmembrane mutations convert ivermectin from a positive to a negative allosteric modulator. Mol. Pharmacol. 78, 198-204. doi: 10.1124/mol.110.064295
8. Crump, A., and Omura, S. (2011). Ivermectin, ‘wonder drug' from Japan: the human use perspective. Proc. Jpn. Acad. Ser. B Phys. Biol. Sci. 87, 13-28. doi: 10.2183/pjab.87.13
9. Gallagher, M. J., Song, L., Arain, F., and Macdonald, R. L. (2004). The juvenile myoclonic epilepsy GABA(A) receptor alpha1 subunit mutation A322D produces asymmetrical, subunit position-dependent reduction ofheterozygous receptor currents and alpha1 subunit protein expression. J. Neurosci. 24, 5570-5578. doi: 10.1523/JNEUR0SCI.1301-04.2004
10. Henin, J., Salari, R., Murlidaran, S., and Brannigan, G. (2014). A predicted binding site for cholesterol on the GABAA receptor. Biophys. J. 106, 1938-1949. doi: 10.1016/j.bpj.2014.03.024
11. Hibbs, R. E., and Gouaux, E. (2011). Principles of activation and permeation in an anion-selective Cys-loop receptor. Nature 474, 54-60. doi: 10.1038/nature10139
12. Khakh, B. S., Proctor, W. R., Dunwiddie, T. V., Labarca, C., and Lester, H. A. (1999). Allosteric control of gating and kinetics at P2X(4) receptor channels. J. Neurosci. 19, 7289-7299.
13. Krause, R. M., Buisson, B., Bertrand, S., Corringer, P. J., Galzi, J. L., Changeux, J. P.,et al. (1998). Ivermectin: a positive allosteric effector of the alpha7 neuronal nicotinic acetylcholine receptor. Mol. Pharmacol. 53, 283-294
14. Krusek, J., and Zemkova, H. (1994). Effect of ivermectin on gamma-aminobutyric acid-induced chloride currents in mouse hippocampal embryonic neurones. Eur. J. Pharmacol. 259, 121-128. doi: 10.1016/0014-2999(94)90500-2
15. Li, G. D., Chiara, D. C., Cohen, J. B., and Olsen, R. W. (2009). Neurosteroids allosterically modulate binding of the anesthetic etomidate to gamma-aminobutyric acid type a receptors. J. Biol. Chem. 284, 11771-11775. doi: 10.1074/jbc.C900016200
16. Lynagh, T., and Lynch, J. W. (2010). A glycine residue essential for high ivermectin sensitivity in Cys-loop ion channel receptors. Int. J. Parasitol. 40, 1477-1481. doi: 10.1016/j.ijpara.2010.07.010
17. Lynagh, T., and Lynch, J. W. (2012a). Ivermectin binding sites in human and invertebrate Cys-loop receptors. Trends Pharmacol. Sci. 33, 432-441. doi: 10.1016/j.tips.2012.05.002
18. Lynagh, T., and Lynch, J. W. (2012b). Molecular mechanisms of Cys-loop ion channel receptor modulation by ivermectin. Front. Mol. Neurosci. 5:60. doi: 10.3389/fnmol.2012.00060
19. Lynagh, T., Webb, T. I., Dixon, C. L., Cromer, B. A., and Lynch, J. W. (2011). Molecular determinants of ivermectin sensitivity at the glycine receptor chloride channel. J. Biol. Chem. 286, 43913-43924. doi: 10.1074/jbc.M111.262634
20. Mascia, M. P., Trudell, J. R., and Harris, R. A. (2000). Specific binding sites for alcohols and anesthetics on ligand-gated ion channels. Proc. Natl. Acad. Sci. U.S.A. 97, 9305-9310. doi: 10.1073/pnas.160128797
21. Nakao, T., Banba, S., and Hirase, K. (2015). Comparison between the modes of action of novel meta-diamide and macrocyclic lactone insecticides on the RDL GABA receptor. Pestic. Biochem. Physiol. 120, 101-108. doi: 10.1016/j.pestbp.2014.09.011
22. Olsen, R. W., and Sieghart, W. (2009). GABA A receptors: subtypes provide diversity offunction and pharmacology. Neuropharmacology 56, 141-148. doi: 10.1016/j.neuropharm.2008.07.045
23. Sali, A., and Blundell, T. L. (1993). Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 234, 779-815. doi: 10.1006/jmbi.1993.1626
24. Sauguet, L., Shahsavar, A., and Delarue, M. (2015). Crystallographic studies of pharmacological sites in pentameric ligand-gated ion channels. Biochim. Biophys. Acta 1850, 511-523. doi: 10.1016/j.bbagen.2014.05.007
25. Schrodinger, L. L. C. (2010). ThePyMOLMolecular GraphicsSystem, Version 1.3r1.
26. Shan, Q., Haddrill, J. L., and Lynch, J. W. (2001). Ivermectin, an unconventional agonist of the glycine receptor chloride channel. J. Biol. Chem. 276, 12556-12564. doi: 10.1074/jbc.M011264200
27. Sieghart, W., and Sperk, G. (2002). Subunit composition, distribution and function of GABA(A) receptor subtypes. Curr. Top. Med. Chem. 2, 795-816. doi: 10.2174/1568026023393507
28. Sigel, E., and Baur, R. (1987). Effect of avermectin B1a on chick neuronal gamma-aminobutyrate receptor channels expressed in Xenopus oocytes. Mol. Pharmacol. 32, 749-752.
29. Wolstenholme, A. J., and Rogers, A. T. (2005). Glutamate-gated chloride channels and the mode of action of the avermectin/milbemycin anthelmintics. Parasitology 131(Suppl.),S85-S95. doi: 10.1017/s0031182005008218
30. Yoluk, O., Bromstrup, T., Bertaccini, E. J., Trudell, J. R., and Lindahl, E. (2013). Stabilization ofthe GluCl ligand-gated ion channel in the presence and absence ofivermectin. Biophys.J. 105, 640-647. doi: 10.1016/j.bpj.2013.06.037