Pyrethroids pp 49-72 | Cite as

Advances in the Mode of Action of Pyrethroids

Chapter
Part of the Topics in Current Chemistry book series (TOPCURRCHEM, volume 314)

Abstract

The ability to clone, express, and electrophysiologically measure currents carried by voltage-gated ion channels has allowed a detailed assessment of the action of pyrethroids on various target proteins.

Recently, the heterologous expression of various rat brain voltage-gated sodium channel isoforms in Xenopus laevis oocytes has determined a wide range of sensitivities to the pyrethroids, with some channels virtually insensitive and others highly sensitive. Furthermore, some isoforms show selective sensitivity to certain pyrethroids and this selectivity can be altered in a state-dependent manner. Additionally, some rat brain isoforms are apparently more sensitive to pyrethroids than the corresponding human isoform. These finding may have significant relevance in judging the merit and value of assessing the risk of pyrethroid exposures to humans using toxicological studies done in rat.

Other target sites for certain pyrethroids include the voltage-gated calcium and chloride channels. Of particular interest is the increased effect of Type II pyrethroids on certain phosphoforms of the N-type Cav2.2 calcium channel following post-translational modification and its relationship to enhanced neurotransmitter release seen in vivo.

Lastly, parallel neurobehavioral and mechanistic studies on three target sites suggest that a fundamental difference exists between the action of Types I and II pyrethroids, both on a functional and molecular level. These differences should be considered in any future risk evaluation of the pyrethroids.

Keywords

CS-syndrome Neurotransmitter release Pyrethroids T-syndrome Voltage-gated calcium channels Voltage-gated sodium channels 

References

  1. 1.
    Soderlund DM, Clark JM, Sheets LP, Mullin LS, Piccirillo VJ, Sargent D, Stevens JT, Weiner ML (2002) Mechanisms of pyrethroid neurotoxicity: implications for cumulative risk assessment. Toxicology 171:3–59CrossRefGoogle Scholar
  2. 2.
    Aldridge WN, Clothier B, Froshaw P, Johnson MK, Parker VH, Price RJ, Skilleter DN, Verscholyle RD, Stevens C (1978) The effect of DDT and the pyrethroids cismethrin and decamethrin on the acetylcholine and cyclic nucleotide content of rat brain. Biochem Pharmacol 27:1703–1706CrossRefGoogle Scholar
  3. 3.
    Catterall WA (1998) Structure and function of neuronal Ca2+ channels and their role in neurotransmitter release. Cell Calcium 24:307–323CrossRefGoogle Scholar
  4. 4.
    Turner TJ, Adams ME, Dunlap K (1993) Multiple Ca2+ channel types coexist to regulate synaptosomal neurotransmitter release. Proc Natl Acad Sci USA 90:9518–9522CrossRefGoogle Scholar
  5. 5.
    Koenig JH, Yamaoka K, Ikeda K (1998) Omega images at the active zone may be endocytotic rather than exocytotic: implications for the vesicle hypothesis of transmitter release. Proc Natl Acad Sci USA 95:12677–12682CrossRefGoogle Scholar
  6. 6.
    Catterall WA (1999) Interactions of presynaptic Ca2+ channels and snare proteins in neurotransmitter release. Ann N Y Acad Sci 868:144–159CrossRefGoogle Scholar
  7. 7.
    Harlow ML, Ress D, Stoschek A, Marshall RM, McMahan UJ (2001) The architecture of active zone material at the frog’s neuromuscular junction. Nature 409:479–484CrossRefGoogle Scholar
  8. 8.
    Shafer TJ, Meyer DA (2004) Effects of pyrethroids on voltage-sensitive calcium channels: a critical evaluation of strengths, weaknesses, data needs, and relationship to assessment of cumulative neurotoxicity. Toxicol Appl Pharmacol 196:303–318CrossRefGoogle Scholar
  9. 9.
    Narahashi T, Zhao X, Ikeda T, Salgado VL, Yeh JZ (2010) Glutamate-activated chloride channels: unique fipronil targets present in insects but not in mammals. Pestic Biochem Physiol 97:149–152CrossRefGoogle Scholar
  10. 10.
    Soderlund DM (2010) Toxicology and mode of action of pyrethroid insecticides. In: Krieger R (ed) Hayes’ handbook of pesticide toxicology. Academic Press, New York, pp 1665–1686Google Scholar
  11. 11.
    Casida JE (2010) Michael Elliott’s billion dollar crystals and other discoveries in insecticide chemistry. Pest Manag Sci 66:1163–1170CrossRefGoogle Scholar
  12. 12.
    Elliott M (1995) Pyrethrum flowers: production, chemistry, toxicology, and uses. In: Casida JE, Quistad GB (eds) Chemicals in insect control. Oxford University Press, New YorkGoogle Scholar
  13. 13.
    Elliott M, Janes NF, Pulman DA (1974) The pyrethrins and related compounds. Part XVIII. Insecticidal 2,2-dimethylcyclopropanecarboxylates with new unsaturated substituents. J Chem Soc Perkin 1 2470–2474Google Scholar
  14. 14.
    Elliott M, Farnham AW, Janes NF, Soderlund DM (1978) Insecticidal activity of the pyrethrins and related compounds. Part XXI. Relative potencies of isomeric cyano-substituted 3-phenoxybenzyl esters. Pestic Sci 9:112–116CrossRefGoogle Scholar
  15. 15.
    Verschoyle RD, Barnes JM (1972) Toxicity of natural and synthetic pyrethrins to rats. Pestic Biochem Physiol 2:308–311CrossRefGoogle Scholar
  16. 16.
    Barnes JM, Verscholyle RD (1974) Toxicity of new pyrethroid insecticide. Nature 248:711CrossRefGoogle Scholar
  17. 17.
    Verscholyle RD, Aldridge WN (1980) Structure-activity relationships of some pyrethroids in rats. Arch Toxicol 45:325–329CrossRefGoogle Scholar
  18. 18.
    Lawrence LJ, Casida JE (1982) Pyrethroid toxicology: mouse intracerebral structure toxicity relationships. Pestic Biochem Physiol 18:9–14CrossRefGoogle Scholar
  19. 19.
    Weiner ML, Nemec M, Sheets L, Sargent D, Breckenridge C (2009) Comparative functional observational battery study of twelve commercial pyrethroid insecticides in male rats following acute oral exposure. Neurotoxicology 30(Suppl 1):S1–S16CrossRefGoogle Scholar
  20. 20.
    Narahashi T (1992) Nerve membrane Na+ channels as targets of insecticides. Trends Pharmacol Sci 13:236–241CrossRefGoogle Scholar
  21. 21.
    Bloomquist JR (1993) Toxicology, mode of action and target site-mediated resistance to insecticides acting on chloride channels. Comp Biochem Physiol C 106:301–314Google Scholar
  22. 22.
    Narahashi T (1996) Neuronal ion channels as the target sites of insecticides. Pharmacol Toxicol 79:1–14CrossRefGoogle Scholar
  23. 23.
    Bloomquist JR (1996) Ion channels as targets for insecticides. Annu Rev Entomol 41:163–190CrossRefGoogle Scholar
  24. 24.
    Clark JM (1995) Effects and mechanisms of action of pyrethrins and pyrethroid insecticides. In: Chang LW, Dyer RS (eds) Handbook of neurotoxicity. Marcel Dekker, New York, NY, pp 511–546Google Scholar
  25. 25.
    Soderlund DM (1995) Mode of action of pyrethrins and pyrethroids. In: Casida JE, Quistad GB (eds) Pyrethrum flowers: production, chemistry, toxicology and uses. Oxford University Press, New York, NY, pp 217–233Google Scholar
  26. 26.
    Lund AE, Narahashi T (1983) Kinetics of sodium channel modification as the basis for the variation in the nerve membrane effects of pyrethroids and DDT analogs. Pestic Biochem Physiol 20:203–216CrossRefGoogle Scholar
  27. 27.
    Catterall WA, Goldin AL, Waxman SG (2005) International Union of Pharmacology. XLVIII. Nomenclature and structure-function relationships of voltage-gated sodium channels. Pharmacol Rev 57:397–409CrossRefGoogle Scholar
  28. 28.
    Goldin AL (2001) Resurgence of sodium channel research. Annu Rev Physiol 63:871–894CrossRefGoogle Scholar
  29. 29.
    Meadows LS, Isom LL (2005) Sodium channels as macromolecular complexes: implications for inherited arrhythmia syndromes. Cardiovasc Res 67:448–458CrossRefGoogle Scholar
  30. 30.
    Ginsburg KS, Narahashi T (1993) Differential sensitivity of tetrodotoxin-sensitive and tetrodotoxin-resistant sodium channels to the insecticide allethrin in rat dorsal root ganglion neurons. Brain Res 627:239–248CrossRefGoogle Scholar
  31. 31.
    Song JH, Narahashi T (1996) Differential effects of the pyrethroid tetramethrin on tetrodotoxin-sensitive and tetrodotoxin-resistant single sodium channels. Brain Res 712:258–264CrossRefGoogle Scholar
  32. 32.
    Tabarean IV, Narahashi T (1998) Potent modulation of tetrodotoxin-sensitive and tetrodotoxin-resistant sodium channels by the type II pyrethroid deltamethrin. J Pharmacol Exp Ther 284:958–965Google Scholar
  33. 33.
    Smith TJ, Soderlund DM (1998) Action of the pyrethroid insecticide cypermethrin on rat brain IIa sodium channels expressed in Xenopus oocytes. Neurotoxicology 19:823–832Google Scholar
  34. 34.
    Choi JS, Soderlund DM (2006) Structure-activity relationships for the action of 11 pyrethroid insecticides on rat NaV1.8 sodium channels expressed in Xenopus oocytes. Toxicol Appl Pharmacol 211:233–244CrossRefGoogle Scholar
  35. 35.
    Meacham CA, Brodfuehrer PD, Watkins JA, Shafer TJ (2008) Developmentally-regulated sodium channel subunits are differentially sensitive to alpha-cyano containing pyrethroids. Toxicol Appl Pharmacol 231:273–281CrossRefGoogle Scholar
  36. 36.
    Tan J, Soderlund DM (2009) Human and rat Nav1.3 voltage-gated sodium channels differ in inactivation properties and sensitivity to the pyrethroid insecticide tefluthrin. Neurotoxicology 30:81–89CrossRefGoogle Scholar
  37. 37.
    Tan J, Soderlund DM (2011) Independent and joint modulation of rat Nav1.6 voltage-gated sodium channels by coexpression with the auxiliary beta1 and beta2 subunits. Biochem Biophys Res Commun 407:788–792CrossRefGoogle Scholar
  38. 38.
    Tan J, Soderlund DM (2010) Divergent actions of the pyrethroid insecticides S-bioallethrin, tefluthrin, and deltamethrin on rat Nav1.6 sodium channels. Toxicol Appl Pharmacol 247:229–237CrossRefGoogle Scholar
  39. 39.
    Peng F, Mellor IR, Williamson MS, Davies TG, Field LM, Usherwood PN (2009) Single channel study of deltamethrin interactions with wild-type and mutated rat Nav1.2 sodium channels expressed in Xenopus oocytes. Neurotoxicology 30:358–367CrossRefGoogle Scholar
  40. 40.
    He B, Soderlund DM (2010) Human embryonic kidney (HEK293) cells express endogenous voltage-gated sodium currents and Nav1.7 sodium channels. Neurosci Lett 469:268–272CrossRefGoogle Scholar
  41. 41.
    Soderlund DM (2011). Molecular mechanisms of pyrethroid insecticide neurotoxicity: recent advances. Arch Toxicol. in pressGoogle Scholar
  42. 42.
    Bloomquist JR, Soderlund DM (1988) Pyrethroid insecticides and DDT modify alkaloid-dependent sodium channel activation and its enhancement by sea anemone toxin. Mol Pharmacol 33:543–550Google Scholar
  43. 43.
    Ghiasuddin SM, Soderlund DM (1985) Voltage-dependent chloride channels: from invertebrates to man. Pestic Biochem Physiol 24:200–206CrossRefGoogle Scholar
  44. 44.
    Brown GB, Gaupp JE, Olsen RW (1988) Pyrethroid insecticides: stereospecific allosteric interaction with the batrachotoxinin-α benzoate binding site of mammalian voltage-sensitive sodium channels. Mol Pharmacol 34:54–59Google Scholar
  45. 45.
    Lombet A, Mourre C, Lazdunski M (1988) Interaction of insecticides of the pyrethroid family with specific binding sites on the voltage-dependent sodium channel from mammalian brain. Brain Res 459:44–53CrossRefGoogle Scholar
  46. 46.
    Trainer VL, Moreau E, Guedin D, Baden DG, Catterall WA (1993) Neurotoxin binding and allosteric modulation at receptor sites 2 and 5 on purified and reconstituted rat brain sodium channels. J Biol Chem 268:17114–17119Google Scholar
  47. 47.
    Trainer VL, McPhee JC, Boutelet-Bochan H, Baker C, Scheuer T, Babin D, Demoute JP, Guedin D, Catterall WA (1997) High affinity binding of pyrethroids to the alpha subunit of brain sodium channels. Mol Pharmacol 51:651–657Google Scholar
  48. 48.
    Soderlund DM (1995) Sodium channels. In: Gilbert L (ed) Comprehensive molecular insect science, vol 5. Pergamon, Oxford, UK, pp 1–24Google Scholar
  49. 49.
    Lee SH, Soderlund DM (2001) The V410M mutation associated with pyrethroid resistance in Heliothis virescens reduces the pyrethroid sensitivity of house fly sodium channels expressed in Xenopus oocytes. Insect Biochem Mol Biol 31:19–29CrossRefGoogle Scholar
  50. 50.
    Tan J, Soderlund DM (2005) Identification of amino acids residues in the insect sodium channel critical for pyrethroids binding. Mol Pharmacol 67:513–522CrossRefGoogle Scholar
  51. 51.
    Vais H, Atkinson S, Pluteanu F, Goodson SJ, Devonshire AL, Williamson MS, Usherwood PNR (2003) Mutations of the para sodium channel of Drosophila melanogaster identify putative binding sites for pyrethroids. Mol Pharmacol 67:513–522Google Scholar
  52. 52.
    Shrivastava IH, Durell SR, Guy HR (2004) A model of voltage gating developed using the Kvap channel crystal structure. Biophys J 87:2255–2270CrossRefGoogle Scholar
  53. 53.
    Zhao Y, Yarov-Yarovoy V, Scheuer T, Catterall WA (2004) A gating hinge in Na+ channels; a molecular switch for electrical signaling. Neuron 41:859–865CrossRefGoogle Scholar
  54. 54.
    O’Reilly AO, Khambay BP, Williamson MS, Field LM, Wallace BA, Davies TG (2006) Modelling insecticide-binding sites in the voltage-gated sodium channel. Biochem J 396:255–263CrossRefGoogle Scholar
  55. 55.
    Vais H, Williamson MS, Goodson SJ, Devonshire AL, Warmke JW, Usherwood PN, Cohen CJ (2000) Activation of drosophila sodium channels promotes modification by deltamethrin. Reductions in affinity caused by knock-down resistance mutations. J Gen Physiol 115:305–318CrossRefGoogle Scholar
  56. 56.
    Symington SB, Clark JM (2005) Action of deltamethrin on N-type (Cav2.2) voltage-sensitive calcium channels in rat brain. Pestic Biochem Physiol 82:1–15CrossRefGoogle Scholar
  57. 57.
    Neal AP, Yuan Y, Atchison WD (2010) Allethrin differentially modulates voltage-gated calcium channel subtypes in rat PC12 cells. Toxicol Sci 116:604–613CrossRefGoogle Scholar
  58. 58.
    Neal AP, Fox SM, Wiwatratana D, Yuan Y, Atchison WD (2011) Effects of allethrin on N- and L-type neuronal voltage gated calcium channels in differentiated PC12 cells. 50th Annual Society of Toxicology Meeting, Washington DCGoogle Scholar
  59. 59.
    Hildebrand ME, McRory JE, Snutch TP, Stea A (2004) Mammalian voltage-gated calcium channels are potently blocked by the pyrethroid insecticide allethrin. J Pharmacol Exp Ther 308:805–813CrossRefGoogle Scholar
  60. 60.
    Narahashi T, Tsunoo A, Yoshii M (1987) Characterization of two types of calcium channels in mouse neuroblastoma cells. J Physiol (Lond) 383:231–249Google Scholar
  61. 61.
    Xiao H, Zhang XC, Zhang L, Dai XQ, Gong W, Cheng J, Gao R, Wang X (2006) Fenvalerate modifies T-type Ca2+ channels in mouse spermatogenic cells. Reprod Toxicol 21:48–53CrossRefGoogle Scholar
  62. 62.
    Mutanguha EM, Valentine ZH, Symington SB (2010) Pyrethroid inhibition of a human T-type voltage-sensitive calcium channel is structural specific and concentration -dependent. 49th Annual Society of Toxicology, Salt Lake City, UTGoogle Scholar
  63. 63.
    Clark JM, Symington SB (2008) Neurotoxic implications of the agonistic action of Cs-syndrome pyrethroids on the N-type Cav2.2 calcium channel. Pest Manag Sci 64:628–638CrossRefGoogle Scholar
  64. 64.
    Alves AM, Symington SB, Lee SH, Clark JM (2010) PKC-dependent phosphorylations modify the action of deltamethrin on rat brain N-type (Cav2.2) voltage-sensitive calcium channel. Pestic Biochem Physiol 97:101–108CrossRefGoogle Scholar
  65. 65.
    De Waard M, Liu H, Walker D, Scott VE, Gurnett CA, Campbell KP (1997) Direct binding of G-protein betagamma complex to voltage-dependent calcium channels. Nature 385:446–450CrossRefGoogle Scholar
  66. 66.
    Zamponi GW, Bourinet E, Nelson D, Nargeot J, Snutch TP (1997) Crosstalk between G proteins and protein kinase C mediated by the calcium channel alpha1 subunit. Nature 385:442–446CrossRefGoogle Scholar
  67. 67.
    Symington SB, Frisbie RK, Kim HJ, Clark JM (2007) Mutation of threonine 422 to glutamic acid mimics the phosphorylation state and alters the action of deltamethrin on Cav2.2. Pestic Biochem Physiol 88:312–320CrossRefGoogle Scholar
  68. 68.
    Nicholson RA, Wilson RC, Potter C, Black MH (1987) Pyrethroid- and DDT-evoked release of GABA from the nervous system in vitro. In: Miyamoto J, Kearney PC (eds) Pesticide chemistry: human welfare and the environment, vol 3. Pergamon, Oxford, UK, pp 75–78Google Scholar
  69. 69.
    Eells JT, Dubocovich ML (1988) Pyrethroid insecticides evoke neurotransmitter release from rabbit striatal slices. J Pharmacol Exp Ther 246:514–521Google Scholar
  70. 70.
    Doherty JD, Nishimura K, Kurihara N, Fujita T (1987) Promotion of norepinephrine release and inhibition of calcium uptake by pyrethroids in rat brain synaptosomes. Pestic Biochem Physiol 29:187–196CrossRefGoogle Scholar
  71. 71.
    Meder W, Fink K, Zentner J, Gothert M (1999) Calcium channels involved in K+- and veratridine-induced increase of cytosolic calcium concentration in human cerebral cortical synaptosomes. J Pharmacol Exp Ther 290:1126–1131Google Scholar
  72. 72.
    Fink K, Meder WP, Clusmann H, Gothert M (2002) Ca2+ entry via P/Q-Type Ca2+ channels and the Na+/Ca2+ exchanger in rat and human neocortical synaptosomes. Naunyn Schmiedebergs Arch Pharmacol 366:458–463CrossRefGoogle Scholar
  73. 73.
    Clark JM, Brooks MW (1989) Role of ion channels and intraterminal calcium homeostasis in the action of deltamethrin at presynaptic nerve terminals. Biochem Pharmacol 38:2233–2245CrossRefGoogle Scholar
  74. 74.
    Symington SB, Frisbie RK, Lu KD, Clark JM (2007) Action of cismethrin and deltamethrin on functional attributes of isolated presynaptic nerve terminals from rat brain. Pestic Biochem Physiol 82:172–181CrossRefGoogle Scholar
  75. 75.
    Clark JM, Symington SB (2007) Pyrethroid action on calcium channels: neurotoxicological implications. Invert Neurosci 7:3–16CrossRefGoogle Scholar
  76. 76.
    Symington SB, Frisbie RK, Clark JM (2008) Characterization of 11 commercial pyrethroids on the functional attributes of rat brain synaptosomes. Pestic Biochem Physiol 92:61–69CrossRefGoogle Scholar
  77. 77.
    Grosse G, Thiele T, Heuckendorf E, Schopp E, Merder S, Pickert G, Ahnert-Hilger G (2002) Deltamethrin differentially affects neuronal subtypes in hippocampal primary culture. Neuroscience 112:233–241CrossRefGoogle Scholar
  78. 78.
    Meyer DA, Carter JM, Johnstone AF, Shafer TJ (2008) Pyrethroid modulation of spontaneous neuronal excitability and neurotransmission in hippocampal neurons in culture. Neurotoxicology 29:213–225CrossRefGoogle Scholar
  79. 79.
    Johnstone AF, Gross GW, Weiss DG, Schroeder OH, Gramowski A, Shafer TJ (2010) Microelectrode arrays: a physiologically based neurotoxicity testing platform for the 21st century. Neurotoxicology 31:331–350CrossRefGoogle Scholar
  80. 80.
    Shafer TJ, Rijal SO, Gross GW (2008) Complete inhibition of spontaneous activity in neuronal networks in vitro by deltamethrin and permethrin. Neurotoxicology 29:203–212CrossRefGoogle Scholar
  81. 81.
    Cao Z, Shafer TJ, Murray TF (2010) Mechanisms of pyrethroid insecticide-induced stimulation of calcium influx in neocortical neurons. J Pharmacol Exp Ther 336:197–205CrossRefGoogle Scholar
  82. 82.
    Dunlop J, Bowlby M, Peri R, Vasilyev D, Arias R (2008) High-throughput electrophysiology: an emerging paradigm for ion-channel screening and physiology. Nat Rev Drug Discov 7:358–368CrossRefGoogle Scholar
  83. 83.
    Gelband CH, Greco PG, Martens JR (1996) Voltage-dependent chloride channels: invertebrates to man. J Exp Zool 275:277–282CrossRefGoogle Scholar
  84. 84.
    Jentsch TJ (1996) Chloride channels: a molecular perspective. Curr Opin Neurobiol 6:303–310CrossRefGoogle Scholar
  85. 85.
    Jentsch TJ, Friedrich T, Schriever A, Yamada H (1999) The Clc chloride channel family. Pflugers Arch 437:783–795CrossRefGoogle Scholar
  86. 86.
    Forshaw PJ, Lister T, Rav DE (1987) The effects of two types of pyrethroid on rat skeletal muscle. Eur J Pharmacol 134:89–96CrossRefGoogle Scholar
  87. 87.
    Forshaw PJ, Ray DE (1990) A novel action of deltamethrin on membrane resistance in mammalian skeletal muscle and non-myelinated nerve fibres. Neuropharmacology 29:71–81CrossRefGoogle Scholar
  88. 88.
    Abalis IM, Eldefrawi AT, Eldefrawi ME (1986) Actions of avermectin B1a on the gamma-aminobutyric acid receptor and chloride channels in rat brain. J Biochem Toxicol 1:69–82CrossRefGoogle Scholar
  89. 89.
    Abalis IM, Eldefrawi ME, Eldefrawi AT (1986) Effects of insecticides on GABA-induced chloride influx into rat brain microsacs. J Toxicol Environ Health 18:13–23CrossRefGoogle Scholar
  90. 90.
    Forshaw PJ, Lister T, Ray DE (1993) Inhibition of a neuronal voltage-dependent chloride channel by the type II pyrethroid, deltamethrin. Neuropharmacology 32:105–111CrossRefGoogle Scholar
  91. 91.
    Ray DE, Sutharsan S, Forshaw PJ (1997) Actions of pyrethroid insecticides on voltage-gated chloride channels in neuroblastoma cells. Neurotoxicology 18:755–760Google Scholar
  92. 92.
    Burr SA, Ray DE (2004) Structure-activity and interaction effects of 14 different pyrethroids on voltage-gated chloride ion channels. Toxicol Sci 77:341–346CrossRefGoogle Scholar
  93. 93.
    Symington SB, Hodgdon HE, Frisbie RK, Clark JM (2011) Binary mixtures of pyrethroids produce differential effects on Ca2+ influx and glutamate release at isolated presynaptic nerve terminals from rat brain. Pestic Biochem Physiol 99:131–139CrossRefGoogle Scholar
  94. 94.
    Hossain MM, Suzuki T, Sato I, Takewaki T, Suzuki K, Kobayashi H (2004) The modulatory effect of pyrethroids on acetylcholine release in the hippocampus of freely moving rats. Neurotoxicology 25:825–833CrossRefGoogle Scholar
  95. 95.
    Hossain MM, Suzuki T, Sato I, Takewaki T, Suzuki K, Kobayashi H (2005) Neuromechanical effects of pyrethroids, allethrin, cyhalothrin and deltamethrin on the cholinergic processes in rat brain. Life Sci 77:795–807CrossRefGoogle Scholar
  96. 96.
    Hossain MM, Suzuki T, Sato N, Sato I, Takewaki T, Suzuki K, Tachikawa E, Kobayashi H (2006) Differential effects of pyrethroid insecticides on extracellular dopamine in the striatum of freely moving rats. Toxicol Appl Pharmacol 217:25–34CrossRefGoogle Scholar
  97. 97.
    Hossain MM, Suzuki T, Unno T, Komori S, Kobayashi H (2008) Differential presynaptic actions of pyrethroid insecticides on glutamatergic and GABAergic neurons in the hippocampus. Toxicology 243:155–163CrossRefGoogle Scholar
  98. 98.
    Wolansky MJ, Harrill JA (2008) Neurobehavioral toxicology of pyrethroid insecticides in adult animals: a critical review. Neurotoxicol Teratol 30:55–78CrossRefGoogle Scholar
  99. 99.
    Breckenridge CB, Holden L, Sturgess N, Weiner M, Sheets L, Sargent D, Soderlund DM, Choi JS, Symington S, Clark JM, Burr S, Ray D (2009) Evidence for a separate mechanism of toxicity for the Type I and the Type II pyrethroid insecticides. Neurotoxicology 30(Suppl 1):S17–S31CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2011

Authors and Affiliations

  1. 1.University of MassachusettsAmherstUSA
  2. 2.Salve Regina UniversityNewportUSA

Personalised recommendations