Mechanism of action of the insecticides, lindane and fipronil, on glycine receptor chloride channels

British Journal of Pharmacology

Volumn 165, Issue 8, 2012, Pages 2707-2720

  Islam, Robiul ^a   Lynch, Joseph W ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Binding site; Chloride channel; Cys loop receptor; Inhibitory neurotransmission; Molecular structure function; Toxicity

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; ALPHA1 GLYCINE RECEPTOR; ALPHA1BETA GLYCINE RECEPTOR; ALPHA2 GLYCINE RECEPTOR; ALPHA3 GLYCINE RECEPTOR; CHLORIDE CHANNEL; FIPRONIL; GLYCINE RECEPTOR; HYDROGEN; INSECTICIDE; LINDANE; THREONINE; UNCLASSIFIED DRUG;

ARTICLE; BETA CHAIN; CELL STRAIN HEK293; CONTROLLED STUDY; DRUG BINDING SITE; DRUG PROTEIN BINDING; DRUG RECEPTOR BINDING; DRUG TARGETING; HUMAN; HUMAN CELL; HYDROGEN BOND; HYDROPHOBICITY; IC 50; INSECTICIDAL ACTIVITY; MOLECULAR DOCKING; NEUROTOXICITY; PRIORITY JOURNAL; PROTEIN EXPRESSION;

CHLORIDE CHANNELS; DNA, COMPLEMENTARY; HEK293 CELLS; HUMANS; INSECTICIDES; LINDANE; MUTATION; PYRAZOLES; RECEPTORS, GLYCINE; RECOMBINANT PROTEINS;

EID: 84859023471     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/j.1476-5381.2011.01722.x     Document Type: Article

References (40)

1. Alexander SPH, Mathie A, Peters JA (2011). Guide to Receptors and Channels (GRAC), 5th Edition. Br J Pharmacol 164 (Suppl. 1): S1-S324.
2. Aspinwall LS, Bermudez I, King LA, Wafford KA (1997). The interactions of hexachlorocyclohexane isomers with human gamma-aminobutyric acid(A) receptors expressed in Xenopus oocytes. J Pharmacol Exp Ther 282: 1557-1564. (Pubitemid 27408341)
3. Becker CM, Hoch W, Betz H (1988). Glycine receptor heterogeneity in rat spinal cord during postnatal development. EMBO J 7: 3717-3726.
4. Chen L, Durkin KA, Casida JE (2006). Structural model for gamma-aminobutyric acid receptor noncompetitive antagonist binding: widely diverse structures fit the same site. Proc Natl Acad Sci U S A 103: 5185-5190.
5. Chen X, Cromer B, Webb TI, Yang Z, Hantke J, Harvey RJ et al. (2009). Dihydropyridine inhibition of the glycine receptor: subunit selectivity and a molecular determinant of inhibition. Neuropharmacology 56: 318-327.
6. Cheng J, Ju XL, Chen XY, Liu GY (2009). Homology modeling of human alpha 1 beta 2 gamma 2 and house fly beta 3 GABA receptor channels and Surflex-docking of fipronil. J Mol Model 15: 1145-1153.
7. Ci S, Ren T, Su Z (2007). Modeling the interaction of fipronil-related non-competitive antagonists with the GABA beta3-receptor. J Mol Model 13: 457-464. (Pubitemid 46477018)
8. Cole LM, Roush RT, Casida JE (1995). Drosophila GABA-gated chloride channel: modified [3H]EBOB binding site associated with Ala->Ser or Gly mutants of Rdl subunit. Life Sci 56: 757-765.
9. Collins T, Millar NS (2010). Nicotinic acetylcholine receptor transmembrane mutations convert ivermectin from a positive to a negative allosteric modulator. Mol Pharmacol 78: 198-204.
10. Gilbert DF, Islam R, Lynagh T, Lynch JW, Webb TI (2009). High throughput techniques for discovering new glycine receptor modulators and their binding sites. Front Mol Neurosci 2: 17.
11. Hainzl D, Cole LM, Casida JE (1998). Mechanisms for selective toxicity of fipronil insecticide and its sulfone metabolite and desulfinyl photoproduct. Chem Res Toxicol 11: 1529-1535. (Pubitemid 29013629)
12. Hall RC (1999). Long-term psychological and neurological complications of lindane poisoning. Psychosomatics 40: 513-517.
13. Handford CA, Lynch JW, Baker E, Webb GC, Ford JH, Sutherland GR et al. (1996). The human glycine receptor beta subunit: primary structure, functional characterisation and chromosomal localisation of the human and murine genes. Brain Res Mol Brain Res 35: 211-219. (Pubitemid 26036749)
14. Hawthorne R, Cromer BA, Ng HL, Parker MW, Lynch JW (2006). Molecular determinants of ginkgolide binding in the glycine receptor pore. J Neurochem 98: 395-407. (Pubitemid 44133145)
15. Hibbs RE, Gouaux E (2011). Principles of activation and permeation in an anion-selective Cys-loop receptor. Nature 474: 54-60.
16. Hirata K, Ishida C, Eguchi Y, Sakai K, Ozoe F, Ozoe Y et al. (2008). Role of a serine residue (S278) in the pore-facing region of the housefly L-glutamate-gated chloride channel in determining sensitivity to noncompetitive antagonists. Insect Mol Biol 17: 341-350.
17. Hosie AM, Baylis HA, Buckingham SD, Sattelle DB (1995). Actions of the insecticide fipronil, on dieldrin-sensitive and- resistant GABA receptors of Drosophila melanogaster. Br J Pharmacol 115: 909-912.
18. Hosie AM, Wilkins ME, da Silva HM, Smart TG (2006). Endogenous neurosteroids regulate GABAA receptors through two discrete transmembrane sites. Nature 444: 486-489. (Pubitemid 44809065)
19. Ikeda T, Zhao X, Nagata K, Kono Y, Shono T, Yeh JZ et al. (2001). Fipronil modulation of gamma-aminobutyric acid(A) receptors in rat dorsal root ganglion neurons. J Pharmacol Exp Ther 296: 914-921. (Pubitemid 32187365)
20. Law RJ, Lightstone FC (2008). Gaba receptor insecticide non-competitive antagonists may bind at allosteric modulator sites. Int J Neurosci 118: 705-734.
21. Le Goff G, Hamon A, Berge JB, Amichot M (2005). Resistance to fipronil in Drosophila simulans: influence of two point mutations in the RDL GABA receptor subunit. J Neurochem 92: 1295-1305. (Pubitemid 40389200)
22. Li GD, Chiara DC, Sawyer GW, Husain SS, Olsen RW, Cohen JB (2006). Identification of a GABAA receptor anesthetic binding site at subunit interfaces by photolabeling with an etomidate analog. J Neurosci 26: 11599-11605. (Pubitemid 44772131)
23. Li P, Akk G (2008). The insecticide fipronil and its metabolite fipronil sulphone inhibit the rat alpha1beta2gamma2L GABA(A) receptor. Br J Pharmacol 155: 783-794.
24. Lobo IA, Harris RA (2005). Sites of alcohol and volatile anesthetic action on glycine receptors. Int Rev Neurobiol 65: 53-87. (Pubitemid 43588580)
25. Lobo IA, Harris RA, Trudell JR (2008). Cross-linking of sites involved with alcohol action between transmembrane segments 1 and 3 of the glycine receptor following activation. J Neurochem 104: 1649-1662. (Pubitemid 351316761)
26. Lynagh T, Lynch JW (2010). A glycine residue essential for high ivermectin sensitivity in Cys-loop ion channel receptors. Int J Parasitol 40: 1477-1481.
27. Maskell PD, Wafford KA, Bermudez I (2001). Effects of gamma-HCH and delta-HCH on human recombinant GABA(A) receptors: dependence on GABA(A) receptor subunit combination. Br J Pharmacol 132: 205-212. (Pubitemid 32128450)
28. Miller PS, Smart TG (2010). Binding, activation and modulation of Cys-loop receptors. Trends Pharmacol Sci 31: 161-174.
29. Mohamed F, Senarathna L, Percy A, Abeyewardene M, Eaglesham G, Cheng R et al. (2004). Acute human self-poisoning with the N-phenylpyrazole insecticide fipronil-a GABAA-gated chloride channel blocker. J Toxicol Clin Toxicol 42: 955-963. (Pubitemid 40024261)
30. Narahashi T (2002). Nerve membrane ion channels as the target site of insecticides. Mini Rev Med Chem 2: 419-432.
31. Nury H, Van Renterghem C, Weng Y, Tran A, Baaden M, Dufresne V et al. (2011). X-ray structures of general anaesthetics bound to a pentameric ligand-gated ion channel. Nature 469: 428-431.
32. Pribilla I, Takagi T, Langosch D, Bormann J, Betz H (1992). The atypical M2 segment of the beta subunit confers picrotoxinin resistance to inhibitory glycine receptor channels. EMBO J 11: 4305-4311.
33. Rundstrom N, Schmieden V, Betz H, Bormann J, Langosch D (1994). Cyanotriphenylborate: subtype-specific blocker of glycine receptor chloride channels. Proc Natl Acad Sci U S A 91: 8950-8954.
34. Sedelnikova A, Erkkila BE, Harris H, Zakharkin SO, Weiss DS (2006). Stoichiometry of a pore mutation that abolishes picrotoxin-mediated antagonism of the GABAA receptor. J Physiol 577: 569-577. (Pubitemid 44804013)
35. Shan Q, Haddrill JL, Lynch JW (2001). A single beta subunit M2 domain residue controls the picrotoxin sensitivity of alphabeta heteromeric glycine receptor chloride channels. J Neurochem 76: 1109-1120. (Pubitemid 32167385)
36. Stehr CM, Linbo TL, Incardona JP, Scholz NL (2006). The developmental neurotoxicity of fipronil: notochord degeneration and locomotor defects in zebrafish embryos and larvae. Toxicol Sci 92: 270-278. (Pubitemid 43985809)
37. Sunol C, Tusell JM, Gelpi E, Rodriguez-Farre E (1989). GABAergic modulation of lindane (gamma-hexachlorocyclohexane)-induced seizures. Toxicol Appl Pharmacol 100: 1-8. (Pubitemid 19209320)
38. Vale C, Fonfria E, Bujons J, Messeguer A, Rodriguez-Farre E, Sunol C (2003). The organochlorine pesticides gamma-hexachlorocyclohexane (lindane), alpha-endosulfan and dieldrin differentially interact with GABA(A) and glycine-gated chloride channels in primary cultures of cerebellar granule cells. Neuroscience 117: 397-403. (Pubitemid 36259754)
39. Yamakura T, Mihic SJ, Harris RA (1999). Amino acid volume and hydropathy of a transmembrane site determine glycine and anesthetic sensitivity of glycine receptors. J Biol Chem 274: 23006-23012.
40. Yang Z, Cromer BA, Harvey RJ, Parker MW, Lynch JW (2007). A proposed structural basis for picrotoxinin and picrotin binding in the glycine receptor pore. J Neurochem 103: 580-589. (Pubitemid 47498044)