Molecular biology of insect sodium channels and pyrethroid resistance

Insect Biochemistry and Molecular Biology

Volumn 50, Issue 1, 2014, Pages 1-17

  Dong, Ke ^a   Du, Yuzhe ^a   Rinkevich, Frank ^a   Nomura, Yoshiko ^a   Xu, Peng ^a   Wang, Lingxin ^a   Silver, Kristopher ^b   Zhorov, Boris S ^c,d  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b KANSAS STATE UNIVERSITY   (United States)

^c MCMASTER UNIVERSITY   (Canada)

^d SECHENOV INSTITUTE OF EVOLUTIONARY PHYSIOLOGY AND BIOCHEMISTRY   (Russian Federation)

Author keywords

Alternative splicing; Knockdown resistance; Pyrethroid receptor sites; Pyrethroids; RNA editing; Sodium channel

Indexed keywords

INSECTICIDE; PYRETHROID; SODIUM CHANNEL;

ALTERNATIVE RNA SPLICING; ANIMAL; DRUG EFFECTS; GENETICS; INSECT; INSECTICIDE RESISTANCE; METABOLISM; PHYSIOLOGY; RNA EDITING;

ALTERNATIVE SPLICING; ANIMALS; INSECTICIDE RESISTANCE; INSECTICIDES; INSECTS; PYRETHRINS; RNA EDITING; SODIUM CHANNELS;

EID: 84899680293     PISSN: 09651748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ibmb.2014.03.012     Document Type: Short Survey

References (159)

1. Bass B.L. RNA Editing 2001, Oxford University Press.
2. Bende N.S., Kang E., Herzig V., Bosmans F., Nicholson G.M., Mobli M., King G.F. The insecticidal neurotoxin Aps III is an atypical knottin peptide that potently blocks insect voltage-gated sodium channels. Biochem Pharmacol. 2013, 85:1542-1554.
3. + channels. Toxicon 2007, 49:550-560.
4. Bourdin C.M., Moignot B., Wang L., Murillo L., Juchaux M., Quinchard S., Lapied B., Guerineau N.C., Dong K., Legros C. Intron retention in mRNA encoding ancillary subunit of insect voltage-gated sodium channel modulates channel expression, gating regulation and drug sensitivity. PLoS One 2013, 8:e67290.
5. Brackenbury W.J., Isom L.L. Na channel β subunits: overachievers of the ion channel family. Front. Pharmacol. 2011, 2:53.
6. Burton M.J., Mellor I.R., Duce I.R., Davies T.G., Field L.M., Williamson M.S. Differential resistance of insect sodium channels with kdr mutations to deltamethrin, permethrin and DDT. Insect Biochem Mol. Biol. 2011, 41:723-732.
7. Catterall W.A. From ionic currents to molecular mechanisms: the structure and function of voltage-gated sodium channels. Neuron 2000, 26:13-25.
8. Catterall W.A. Voltage-gated sodium channels at 60: structure, function and pathophysiology. J.Physiol. 2012, 590:2577-2589.
9. Catterall W.A. Sodium channels, inherited epilepsy, and antiepileptic drugs. Annu Rev. Pharmacol. Toxicol. 2014, 54:317-338.
10. Catterall W.A., Cestele S., Yarov-Yarovoy V., Yu F.H., Konoki K., Scheuer T. Voltage-gated ion channels and gating modifier toxins. Toxicon 2007, 49:124-141.
11. Cestele S., Catterall W.A. Molecular mechanisms of neurotoxin action on voltage-gated sodium channels. Biochimie 2000, 82:883-892.
12. Chang C., Shen W.K., Wang T.T., Lin Y.H., Hsu E.L., Dai S.M. Anovel amino acid substitution in a voltage-gated sodium channel is associated with knockdown resistance to permethrin in Aedes aegypti. Insect Biochem Mol. Biol. 2009, 39:272-278.
13. Choi J.S., Soderlund D.M. Structure-activity relationships for the action of 11 pyrethroid insecticides on rat Na v. 1.8 sodium channels expressed in Xenopus oocytes. Toxicol. Appl. Pharmacol. 2006, 211:233-244.
14. Crill W.E. Persistent sodium current in mammalian central neurons. Annu Rev. Physiol. 1996, 58:349-362.
15. Cui Y.J., Yu L.L., Xu H.J., Dong K., Zhang C.X. Molecular characterization of DSC1 orthologs in invertebrate species. Insect Biochem Mol. Biol. 2012, 42:353-359.
16. Davies T.G., Field L.M., Usherwood P.N., Williamson M.S. Acomparative study of voltage-gated sodium channels in the Insecta: implications for pyrethroid resistance in Anopheline and other Neopteran species. Insect Mol. Biol. 2007, 16:361-375.
17. Derst C., Walther C., Veh R.W., Wicher D., Heinemann S.H. Four novel sequences in Drosophila melanogaster homologous to the auxiliary Para sodium channel subunit TipE. Biochem Biophys. Res. Commun. 2006, 339:939-948.
18. Dong K. Asingle amino acid change in the para sodium channel protein is associated with knockdown-resistance (kdr) to pyrethroid insecticides in German cockroach. Insect Biochem Mol. Biol. 1997, 27:93-100.
19. Dong K. Insect sodium channels and insecticide resistance. Invert. Neurosci. 2007, 7:17-30.
20. Dong K., Scott J.G. Linkage of kdr-type resistance and the para-homologous sodium channel gene in German cockroaches (Blattella germanica). Insect Biochem Mol. Biol. 1994, 24:647-654.
21. Doyle D.A., Morais Cabral J., Pfuetzner R.A., Kuo A., Gulbis J.M., Cohen S.L., Chait B.T., MacKinnon R. The structure of the potassium channel: molecular basis of K+ conduction and selectivity. Science 1998, 280:69-77.
22. Du Y., Garden D.P., Wang L., Zhorov B.S., Dong K. Identification of new batrachotoxin-sensing residues in segment IIIS6 of the sodium channel. J.Biol. Chem. 2011, 286:13151-13160.
23. Du Y., Lee J.E., Nomura Y., Zhang T., Zhorov B.S., Dong K. Identification of a cluster of residues in transmembrane segment 6 of domain III of the cockroach sodium channel essential for the action of pyrethroid insecticides. Biochem. J. 2009, 419:377-385.
24. Du Y., Liu Z., Nomura Y., Khambay B., Dong K. An alanine in segment 3 of domain III (IIIS3) of the cockroach sodium channel contributes to the low pyrethroid sensitivity of an alternative splice variant. Insect Biochem Mol. Biol. 2006, 36:161-168.
25. Du Y., Nomura Y., Liu Z., Huang Z.Y., Dong K. Functional expression of an arachnid sodium channel reveals residues responsible for tetrodotoxin resistance in invertebrate sodium channels. J.Biol. Chem. 2009, 284:33869-33875.
26. Du Y., Nomura Y., Luo N., Liu Z., Lee J.E., Khambay B., Dong K. Molecular determinants on the insect sodium channel for the specific action of type II pyrethroid insecticides. Toxicol. Appl. Pharmacol. 2009, 234:266-272.
27. Du Y., Nomura Y., Satar G., Hu Z., Nauen R., He S.Y., Zhorov B.S., Dong K. Molecular evidence for dual pyrethroid-receptor sites on a mosquito sodium channel. Proc. Nat. Acad. Sci. 2013, 110:11785-11790.
28. Du Y., Song W., Groome J.R., Nomura Y., Luo N., Dong K. Anegative charge in transmembrane segment 1 of domain II of the cockroach sodium channel is critical for channel gating and action of pyrethroid insecticides. Toxicol. Appl. Pharmacol. 2010, 247:53-59.
29. + channel predict a clockwise arrangement of the domains. J.Gen. Physiol. 2000, 116:679-690.
30. Feng G., Deak P.t., Chopra M., Hall L.M. Cloning and functional analysis of tipE, a novel membrane protein that enhances drosophila para sodium channel function. Cell 1995, 82:1001-1011.
31. Frank H.Y., Catterall W.A. Overview of the voltage-gated sodium channel family. Genome Bio 2003, 4:207.
32. Garber G., Smith L.A., Reenan R.A., Rogina B. Effect of sodium channel abundance on Drosophila development, reproductive capacity and aging. Fly. (Austin) 2012, 6:57-67.
33. Ginsburg K.S., Narahashi T. Differential sensitivity of tetrodotoxin-sensitive and tetrodotoxin-resistant sodium channels to the insecticide allethrin in rat dorsal root ganglion neurons. Brain Res. 1993, 627:239-248.
34. + channels. J.Exp. Biol. 2002, 205:575-584.
35. Goldin A.L., Barchi R.L., Caldwell J.H., Hofmann F., Howe J.R., Hunter J.C., Kallen R.G., Mandel G., Meisler M.H., Netter Y.B. Nomenclature of voltage-gated sodium channels. Neuron 2000, 28:365.
36. Gordon D. Anew approach to insect-pest control-combination of neurotoxins interacting with voltage sensitive sodium channels to increase selectivity and specificity. Invert. Neurosci. 1997, 3:103-116.
37. Gordon D., Karbat I., Ilan N., Cohen L., Kahn R., Gilles N., Dong K., Stuhmer W., Tytgat J., Gurevitz M. The differential preference of scorpion alpha-toxins for insect or mammalian sodium channels: implications for improved insect control. Toxicon 2007, 49:452-472.
38. Gur M., Kahn R., Karbat I., Regev N., Wang J., Catterall W.A., Gordon D., Gurevitz M. Elucidation of the molecular basis of selective recognition uncovers the interaction site for the core domain of scorpion alpha-toxins on sodium channels. J.Biol. Chem. 2011, 286:35209-35217.
39. Gurevitz M. Mapping of scorpion toxin receptor sites at voltage-gated sodium channels. Toxicon 2012, 60:502-511.
40. Gurevitz M., Karbat I., Cohen L., Ilan N., Kahn R., Turkov M., Stankiewicz M., Stuhmer W., Dong K., Gordon D. The insecticidal potential of scorpion beta-toxins. Toxicon 2007, 49:473-489.
41. + channel transcript. Evolutionary conservation and developmental regulation. Genetics 2000, 155:1149-1160.
42. Hu Z., Du Y., Nomura Y., Dong K. Asodium channel mutation identified in Aedes aegypti selectively reduces cockroach sodium channel sensitivity to type I, but not type II pyrethroids. Insect Biochem. Molec. Biol. 2011, 41:9-13.
43. Ingles P.J., Adams P.M., Knipple D.C., Soderlund D.M. Characterization of voltage-sensitive sodium channel gene coding sequences from insecticide-susceptible and knockdown-resistant house fly strains. Insect Biochem Mol. Biol. 1996, 26:319-326.
44. Jepson J.E., Reenan R.A. Adenosine-to-inosine genetic recoding is required in the adult stage nervous system for coordinated behavior in Drosophila. J.Biol. Chem. 2009, 284:31391-31400.
45. Jepson J.E., Savva Y.A., Jay K.A., Reenan R.A. Visualizing adenosine-to-inosine RNA editing in the Drosophila nervous system. Nat. Methods 2011, 9:189-194.
46. Jin Y., Tian N., Cao J., Liang J., Yang Z., Lv J. RNA editing and alternative splicing of the insect nAChR subunit alpha6 transcript: evolutionary conservation, divergence and regulation. BMC Evol. Biol. 2007, 7:98.
47. Jones A.K., Buckingham S.D., Papadaki M., Yokota M., Sattelle B.M., Matsuda K., Sattelle D.B. Splice-variant- and stage-specific RNA editing of the Drosophila GABA receptor modulates agonist potency. J.Neurosci. 2009, 29:4287-4292.
48. Jones C.M., Liyanapathirana M., Agossa F.R., Weetman D., Ranson H., Donnelly M.J., Wilding C.S. Footprints of positive selection associated with a mutation (N1575Y) in the voltage-gated sodium channel of Anopheles gambiae. Proc. Natl. Acad. Sci. 2012, 109:6614-6619.
49. Kiss T. Persistent Na-channels: origin and function. A review. Acta Biol. Hung 2008, 59(Suppl):1-12.
50. Klint J.K., Senff S., Rupasinghe D.B., Er S.Y., Herzig V., Nicholson G.M., King G.F. Spider-venom peptides that target voltage-gated sodium channels: pharmacological tools and potential therapeutic leads. Toxicon 2012, 60:478-491.
51. Kulkarni N.H., Yamamoto A.H., Robinson K.O., Mackay T.F.C., Anholt R.R.H. The DSC1 channel, encoded by the smi60E locus, contributes to odor-guided behavior in Drosophila melanogaster. Genetics 2002, 161:1507-1516.
52. Lee S.H., Ingles P.J., Knipple D.C., Soderlund D.M. Developmental regulation of alternative exon usage in the house fly Vssc1 sodium channel gene. Invert. Neurosci. 2002, 4:125-133.
53. Lee S.H., Smith T.J., Ingles P.J., Soderlund D.M. Cloning and functional characterization of a putative sodium channel auxiliary subunit gene from the house fly (Musca domestica). Insect Biochem Mol. Biol. 2000, 30:479-487.
54. Lee S.H., Smith T.J., Knipple D.C., Soderlund D.M. Mutations in the house fly Vssc1 sodium channel gene associated with super-kdr resistance abolish the pyrethroid sensitivity of Vssc1/tipE sodium channels expressed in Xenopus oocytes. Insect Biochem Mol. Biol. 1999, 29:185-194.
55. Lee S.H., Soderlund D.M. 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. 2001, 31:19-29.
56. Li T., Zhang L., Reid W.R., Xu Q., Dong K., Liu N. Multiple mutations and mutation combinations in the sodium channel of permethrin resistant mosquitoes, Culex quinquefasciatus. Sci. Rep. 2012, 2:781.
57. Lilly B., Galewsky S., Firulli A.B., Schulz R.A., Olson E.N. D-MEF2: a MADS box transcription factor expressed in differentiating mesoderm and muscle cell lineages during Drosophila embryogenesis. Proc. Natl. Acad. Sci. U S A 1994, 91:5662-5666.
58. Lin W.H., Gunay C., Marley R., Prinz A.A., Baines R.A. Activity-dependent alternative splicing increases persistent sodium current and promotes seizure. J.Neurosci. 2012, 32:7267-7277.
59. v regulates activation, inactivation, and persistent current. J.Neurophysiol. 2009, 102:1994-2006.
60. Lindsay H.A., Baines R., ffrench-Constant R., Lilley K., Jacobs H.T., O'Dell K.M. The dominant cold-sensitive out-cold mutants of Drosophila melanogaster have novel missense mutations in the voltage-gated sodium channel gene paralytic. Genetics 2008, 180:873-884.
61. Lipkind G.M., Fozzard H.A. KcsA crystal structure as framework for a molecular model of the Na(+) channel pore. Biochemistry 2000, 39:8161-8170.
62. Lipkind G.M., Fozzard H.A. Molecular modeling of local anesthetic drug binding by voltage-gated sodium channels. Mol. Pharmacol. 2005, 68:1611-1622.
63. Liu Z., Chung I., Dong K. Alternative splicing of the BSC1 gene generates tissue-specific isoforms in the German cockroach. Insect Biochem Mol. Biol. 2001, 31:703-713.
64. Liu Z., Song W., Dong K. Persistent tetrodotoxin-sensitive sodium current resulting from U-to-C RNA editing of an insect sodium channel. Proc. Natl. Acad. Sci. U S A 2004, 101:11862-11867.
65. Liu Z., Tan J., Valles S.M., Dong K. Synergistic interaction between two cockroach sodium channel mutations and a tobacco budworm sodium channel mutation in reducing channel sensitivity to a pyrethroid insecticide. Insect Biochem Mol. Biol. 2002, 32:397-404.
66. Liu Z., Valles S.M., Dong K. Novel point mutations in the German cockroach para sodium channel gene are associated with knockdown resistance (kdr) to pyrethroid insecticides. Insect Biochem Mol. Biol. 2000, 30:991-997.
67. + channel. Science 2005, 309:897-903.
68. Loughney K., Kreber R., Ganetzky B. Molecular analysis of the para locus, a sodium channel gene in Drosophila. Cell 1989, 58:1143-1154.
69. Lund A.E., Narahashi T. Dose-dependent interaction of the pyrethroid isomers with sodium channels of squid axon membranes. Neurotoxicology 1982, 3:11-24.
70. Maldonado C., Alicea D., Gonzalez M., Bykhovskaia M., Marie B. Adar is essential for optimal presynaptic function. Mol. Cell. Neurosci. 2013, 52:173-180.
71. Marley R., Baines R.A. Increased persistent Na+ current contributes to seizure in the slamdance bang-sensitive Drosophila mutant. J.Neurophysiol. 2011, 106:18-29.
72. Milani R. Mendelian behavior of resistance to the knock-down action of DDT and correlation between knock-down and mortality in Musca domestica L. Rend. Ist. Sup Sanit. 1956, 19:1107-1143.
73. Miyazaki M., Ohyama K., Dunlap D.Y., Matsumura F. Cloning and sequencing of the para-type sodium channel gene from susceptible and kdr-resistant German cockroaches (Blattella germanica) and house fly (Musca domestica). Mol. Gen. Genet. 1996, 252:61-68.
74. Moignot B.n.d., Lemaire C., Quinchard S., Lapied B., Legros C. The discovery of a novel sodium channel in the cockroach Periplaneta americana: evidence for an early duplication of the para-like gene. Insect Biochem Molec Biol. 2009, 39:814-823.
75. Moran Y., Gordon D., Gurevitz M. Sea anemone toxins affecting voltage-gated sodium channels-molecular and evolutionary features. Toxicon 2009, 54:1089-1101.
76. + channels. Biochem. J. 2007, 406:41-48.
77. Narahashi T. Neuronal ion channels as the target sites of insecticides. Pharmacol. Toxicol. 1996, 78:1-14.
78. Narahashi T. Neuroreceptors and ion channels as the basis for drug action: past, present, and future. J.Pharmacol. Exp. Ther. 2000, 294:1-26.
79. Narahashi T. Nerve membrane ion channels as the target site of insecticides. Mini Rev. Medic Chem. 2002, 2:419-432.
80. Nishikura K. Functions and regulation of RNA editing by ADAR deaminases. Annu Rev. Biochem 2010, 79:321-349.
81. Numann R., Catterall W.A., Scheuer T. Functional modulation of brain sodium channels by protein kinase C phosphorylation. science 1991, 254:115-118.
82. O'Dowd D.K. Voltage-gated currents and firing properties of embryonic Drosophila neurons grown in a chemically defined medium. J.Neurobiol. 1995, 27:113-126.
83. O'Reilly A.O., Khambay B.P., Williamson M.S., Field L.M., Wallace B.A., Davies T.G. Modelling insecticide-binding sites in the voltage-gated sodium channel. Biochem J. 2006, 396:255-263.
84. O'Reilly A.O., Williamson M.S., Gonzalez-Cabrera J., Turberg A., Field L.M., Wallace B.A., Davies T.G. Predictive 3D modelling of the interactions of pyrethroids with the voltage-gated sodium channels of ticks and mites. Pest Manag. Sci. 2014, 70:369-377.
85. Okamoto H., Sakai K., Goto S., Takasu-Ishikawa E., Hotta Y. Isolation of Drosophila genomic clones homologous to the eel sodium channel gene. Proc. Jpn. Acad. B 1987, 63:284-288.
86. Oliveira E.E., Du Y., Nomura Y., Dong K. Aresidue in the transmembrane segment 6 of domain I in insect and mammalian sodium channels regulate differential sensitivities to pyrethroid insecticides. Neurotoxicology 2013, 38C:42-50.
87. Olson R.O., Liu Z.Q., Nomura Y., Song W.Z., Dong K. Molecular and functional characterization of voltage-gated sodium channel variants from Drosophila melanogaster. Insect Biochem Mol. Biol. 2008, 38:604-610.
88. Palladino M.J., Keegan L.P., O'Connell M.A., Reenan R.A. A-to-I pre-mRNA editing in Drosophila is primarily involved in adult nervous system function and integrity. Cell 2000, 102:437-449.
89. Park J.W., Parisky K., Celotto A.M., Reenan R.A., Graveley B.R. Identification of alternative splicing regulators by RNA interference in Drosophila. Proc. Natl. Acad. Sci. U S A 2004, 101:15974-15979.
90. Park Y., Taylor M.F., Feyereisen R. Voltage-gated sodium channel genes hscp and hDSC1 of Heliothis virescens F. genomic organization. Insect Mol. Biol. 1999, 8:161-170.
91. Parker L., Howlett I.C., Rusan Z.M., Tanouye M.A. Seizure and epilepsy: studies of seizure disorders in Drosophila. Int. Rev. Neurobiol. 2011, 99:1-21.
92. Pauron D., Barhanin J., Amichot M., Pralavorio M., Berge J.B., Lazdunski M. Pyrethroid receptor in the insect sodium channel: alteration of its properties in pyrethroid-resistant flies. Biochemistry 1989, 28:1673-1677.
93. Payandeh J., Scheuer T., Zheng N., Catterall W.A. The crystal structure of a voltage-gated sodium channel. Nature 2011, 475:353-358.
94. V1.2 sodium channels expressed in Xenopus oocytes. Neurotoxicology 2009, 30:358-367.
95. Plummer N.W., McBurney M.W., Meisler M.H. Alternative splicing of the sodium channel SCN8A predicts a truncated two-domain protein in fetal brain and non-neuronal cells. J.Biol. Chem. 1997, 272:24008-24015.
96. Ramaswami M., Tanouye M.A. Two sodium-channel genes in Drosophila: implications for channel diversity. Proc. Nat. Acad. Sci. 1989, 86:2079-2082.
97. + channel transcript in a region of RNA editing. Neuron 2000, 25:139-149.
98. Rieder L.E., Staber C.J., Hoopengardner B., Reenan R.A. Tertiary structural elements determine the extent and specificity of messenger RNA editing. Nat. Commun. 2013, 4:2232.
99. Rinkevich F.D., Du Y., Dong K. Diversity and convergence of sodium channel mutations involved in resistance to pyrethroids. Pestic. Biochem Physiol. 2013, 106:93-100.
100. Rossignol D.P. Reduction in number of nerve membrane sodium channels in pyrethroid resistant house flies. Pestic. Biochem Physiol. 1988, 32:146-152.
101. Salkoff L., Butler A., Wei A., Scavarda N., Giffen K., Ifune C., Goodman R., Mandel G. Genomic organization and deduced amino acid sequence of a putative sodium channel gene in Drosophila. Science 1987, 237:744-749.
102. Seeburg P.H. RNA helicase participates in the editing game. Neuron 2000, 25:261-263.
103. Shao Y.M., Dong K., Tang Z.H., Zhang C.X. Molecular characterization of a sodium channel gene from the Silkworm Bombyx mori. Insect Biochem Mol. Biol. 2009, 39:145-151.
104. Silver K.S., Nomura Y., Salgado V.L., Dong K. Role of the sixth transmembrane segment of domain IV of the cockroach sodium channel in the action of sodium channel blocker insecticides. Neurotoxicology 2009, 30:613-621.
105. Silver K.S., Song W., Nomura Y., Salgado V.L., Dong K. Mechanism of action of sodium channel blocker insecticides (SCBIs) on insect sodium channels. Pestic. Biochem Physiol. 2010, 97:87-92.
106. Skinner W.S., Dennis P.A., Li J.P., Quistad G.B. Identification of insecticidal peptides from venom of the trap-door spider, Aptostichus schlingeri (Ctenizidae). Toxicon 1992, 30:1043-1050.
107. Smith R.D., Goldin A.L. Phosphorylation of brain sodium channels in the I-II linker modulates channel function in Xenopus oocytes. J.Neurosci. 1996, 16:1965-1974.
108. Smith R.D., Goldin A.L. Phosphorylation at a single site in the rat brain sodium channel is necessary and sufficient for current reduction by protein kinase A. J.Neurosci. 1997, 17:6086-6093.
109. Smith R.D., Goldin A.L. Potentiation of rat brain sodium channel currents by PKA in Xenopus oocytes involves the I-II linker. Am. J. Physiol. Cell. Physiol. 2000, 278:C638-C645.
110. Smith T.J., Lee S.H., Ingles P.J., Knipple D.C., Soderlund D.M. The L1014F point mutation in the house fly Vssc1 sodium channel confers knockdown resistance to pyrethroids. Insect Biochem Mol. Biol. 1997, 27:807-812.
111. Smith T.J., Soderlund D.M. Action of the pyrethroid insecticide cypermethrin on rat brain IIa sodium channels expressed in xenopus oocytes. Neurotoxicology 1998, 19:823-832.
112. Soderlund D.M. Sodium channels. Comprehensive Molecular Insect Science 2005, 1-24. Elsevier, Amsterdam. L.I. Gilbert, K. Iatrou, S.S. Gill (Eds.).
113. Soderlund D.M. Molecular mechanisms of pyrethroid insecticide neurotoxicity: recent advances. Arch. Toxicol. 2012, 86:165-181.
114. Soderlund D.M., Bloomquist J.R. Molecular mechanisms of insecticide resistance. Pesticide Resistance in Arthropods 1990, 58. Chapman and Hall, New York and London. R.T. Roush, B.E. Tabashnik (Eds.).
115. Song J.H., Narahashi T. Differential effects of the pyrethroid tetramethrin on tetrodotoxin-sensitive and tetrodotoxin-resistant single sodium channels. Brain Res. 1996, 712:258-264.
116. Song W., Du Y., Liu Z., Luo N., Turkov M., Gordon D., Gurevitz M., Goldin A.L., Dong K. Substitutions in the domain III voltage-sensing module enhance the sensitivity of an insect sodium channel to a scorpion beta-toxin. J.Biol. Chem. 2011, 286:15781-15788.
117. Song W., Liu Z., Dong K. Molecular basis of differential sensitivity of insect sodium channels to DCJW, a bioactive metabolite of the oxadiazine insecticide indoxacarb. Neurotoxicology 2006, 27:237-244.
118. Song W., Liu Z., Tan J., Nomura Y., Dong K. RNA editing generates tissue-specific sodium channels with distinct gating properties. J.Biol. Chem. 2004, 279:32554-32561.
119. Sonoda S., Igaki C., Ashfaq M., Tsumuki H. Pyrethroid-resistant diamondback moth expresses alternatively spliced sodium channel transcripts with and without T929I mutation. Insect Biochem Mol. Biol. 2006, 36:904-910.
120. Sonoda S., Tsukahara Y., Ashfaq M., Tsumuki H. Genomic organization of the para-sodium channel alpha-subunit genes from the pyrethroid-resistant and -susceptible strains of the diamondback moth. Arch. Insect Biochem Physiol. 2008, 69:1-12.
121. Stafstrom C.E. Persistent sodium current and its role in epilepsy. Epilepsy Curr. 2007, 7:15-22.
122. Strugatsky D., Zilberberg N., Stankiewicz M., Ilan N., Turkov M., Cohen L., Pelhate M., Gilles N., Gordon D., Gurevitz M. Genetic polymorphism and expression of a highly potent scorpion depressant toxin enable refinement of the effects on insect Na channels and illuminate the key role of Asn-58. Biochemistry 2005, 44:9179-9187.
123. Sun L., Gilligan J., Staber C., Schutte R.J., Nguyen V., O'Dowd D.K., Reenan R. Aknock-in model of human epilepsy in Drosophila reveals a novel cellular mechanism associated with heat-induced seizure. J.Neurosci. 2012, 32:14145-14155.
124. Tan J., Liu Z., Nomura Y., Goldin A.L., Dong K. Alternative splicing of an insect sodium channel gene generates pharmacologically distinct sodium channels. J.Neurosci. 2002, 22:5300-5309.
125. Tan J., Liu Z., Tsai T.D., Valles S.M., Goldin A.L., Dong K. Novel sodium channel gene mutations in Blattella germanica reduce the sensitivity of expressed channels to deltamethrin. Insect Biochem Mol. Biol. 2002, 32:445-454.
126. Tan J., Liu Z., Wang R., Huang Z.Y., Chen A.C., Gurevitz M., Dong K. Identification of amino acid residues in the insect sodium channel critical for pyrethroid binding. Mol. Pharmacol. 2005, 67:513-522.
127. v1.3 voltage-gated sodium channels differ in inactivation properties and sensitivity to the pyrethroid insecticide tefluthrin. Neurotoxicology 2009, 30:81-89.
128. v1.6 sodium channels. Toxicol. Appl. Pharmacol. 2010, 247:229-237.
129. v1.7 voltage-gated sodium channels expressed in Xenopus oocytes. Pestic. Biochem Physiol. 2011, 101:21-26.
130. Tatebayashi H., Narahashi T. Differential mechanism of action of the pyrethroid tetramethrin on tetrodotoxin-sensitive and tetrodotoxin-resistant sodium channels. J.Pharmacol. Exp. Ther. 1994, 270:595-603.
131. + currents that fail to inactivate. Trends Neurosci. 1993, 16:455-460.
132. Thackeray J.R., Ganetzky B. Developmentally regulated alternative splicing generates a complex array of Drosophila para sodium channel isoforms. J.Neurosci. 1994, 14:2569-2578.
133. Thackeray J.R., Ganetzky B. Conserved alternative splicing patterns and splicing signals in the Drosophila sodium channel gene para. Genetics 1995, 141:203-214.
134. Tikhonov D.B., Zhorov B.S. Modeling P-loops domain of sodium channel: homology with potassium channels and interaction with ligands. Biophys. J. 2005, 88:184-197.
135. Tikhonov D.B., Zhorov B.S. Sodium channel activators: model of binding inside the pore and a possible mechanism of action. FEBS Lett. 2005, 579:4207-4212.
136. Tikhonov D.B., Zhorov B.S. Sodium channels: ionic model of slow inactivation and state-dependent drug binding. Biophys. J. 2007, 93:1557-1570.
137. Usherwood P.N., Davies T.G., Mellor I.R., O'Reilly A.O., Peng F., Vais H., Khambay B.P., Field L.M., Williamson M.S. Mutations in DIIS5 and the DIIS4-S5 linker of Drosophila melanogaster sodium channel define binding domains for pyrethroids and DDT. FEBS Lett. 2007, 581:5485-5492.
138. Usherwood P.N.R., Vais H., Khambay B.P.S., Davies T.G.E., Williamson M.S. Sensitivity of the Drosophila para sodium channel to DDT is not lowered by the super-kdr mutation M918T on the IIS4-S5 linker that profoundly reduces sensitivity to permethrin and deltamethrin. FEBS Lett. 2005, 579:6317-6325.
139. Vais H., Atkinson S., Eldursi N., Devonshire A.L., Williamson M.S., Usherwood P.N. Asingle amino acid change makes a rat neuronal sodium channel highly sensitive to pyrethroid insecticides. FEBS Lett. 2000, 470:135-138.
140. Vais H., Atkinson S., Pluteanu F., Goodson S.J., Devonshire A.L., Williamson M.S., Usherwood P.N. Mutations of the para sodium channel of Drosophila melanogaster identify putative binding sites for pyrethroids. Mol. Pharmacol. 2003, 64:914-922.
141. Vais H., Williamson M.S., Devonshire A.L., Usherwood P.N. The molecular interactions of pyrethroid insecticides with insect and mammalian sodium channels. Pest Manag. Sci. 2001, 57:877-888.
142. Vais H., Williamson M.S., Hick C.A., Eldursi N., Devonshire A.L., Usherwood P.N. Functional analysis of a rat sodium channel carrying a mutation for insect knock-down resistance (kdr) to pyrethroids. FEBS Lett. 1997, 413:327-332.
143. von Stein R.T., Soderlund D.M. Role of the local anesthetic receptor in the state-dependent inhibition of voltage-gated sodium channels by the insecticide metaflumizone. Mol. Pharmacol. 2012, 81:366-374.
144. Wang L., Nomura Y., Du Y., Dong K. Differential effects of TipE and a TipE-homologous protein on modulation of gating properties of sodium channels from Drosophila melanogaster. PLoS One 2013, 8:e67551.
145. Wang R., Huang Z.Y., Dong K. Molecular characterization of an arachnid sodium channel gene from the varroa mite (Varroa destructor). Insect Biochem Mol. Biol. 2003, 33:733-739.
146. + channels is critical for pyrethroid action. Mol. Pharmacol. 2001, 60:620-628.
147. Wang S.Y., Wang G.K. Voltage-gated sodium channels as primary targets of diverse lipid-soluble neurotoxins. Cell. Signal. 2003, 15:151-159.
148. Wang X.J., Reynolds E.R., Deak P., Hall L.M. The seizure locus encodes the Drosophila homolog of the HERG potassium channel. J.Neurosci. 1997, 17:882-890.
149. Warmke J.W., Reenan R.A.G., Wang P.Y., Qian S., Arena J.P., Wang J.X., Wunderler D., Liu K., Kaczorowski G.J., VanderPloeg L.H.T., Ganetzky B., Cohen C.J. Functional expression of Drosophila para sodium channels - modulation by the membrane protein TipE and toxin pharmacology. J.Gen. Physiol. 1997, 110:119-133.
150. West J.W., Numann R., Murphy B.J., Scheuer T., Catterall W.A. Aphosphorylation site in the Na+ channel required for modulation by protein kinase C. Science 1991, 254:866-868.
151. Williamson M.S., Martinez-Torres D., Hick C.A., Devonshire A.L. Identification of mutations in the housefly para-type sodium channel gene associated with knockdown resistance (kdr) to pyrethroid insecticides. Mol. Gen. Genet. 1996, 252:51-60.
152. Wing K.D., Andaloro J.T., McCann S.F., Salgado V.L. Indoxacarb and the Sodium Channel Blocker Insecticides: Chemistry, Physiology and Biology in Insects 2005, Elsevier, New York.
153. Xu Q., Zhang L., Li T., Zhang L., He L., Dong K., Liu N. Evolutionary adaptation of the amino acid and codon usage of the mosquito sodium channel following insecticide selection in the field mosquitoes. PloS one 2012, 7:e47609.
154. Yoon K.S., Kwon D.H., Strycharz J.P., Hollingsworth C.S., Lee S.H., Clark J.M. Biochemical and molecular analysis of deltamethrin resistance in the common bed bug (Hemiptera: Cimicidae). J.Med. Entomol. 2008, 45:1092-1101.
155. Zhang T., Liu Z., Song W., Du Y., Dong K. Molecular characterization and functional expression of the DSC1 channel. Insect Biochem Mol. Biol. 2011, 41:451-458.
156. Zhao Y., Park Y., Adams M.E. Functional and evolutionary consequences of pyrethroid resistance mutations in S6 transmembrane segments of a voltage-gated sodium channel. Biochem Biophys. Res. Commun. 2000, 278:516-521.
157. Zhorov B.S., Tikhonov D.B. Potassium, sodium, calcium and glutamate-gated channels: pore architecture and ligand action. J.Neurochem 2004, 88:782-799.
158. Zhou W., Chung I., Liu Z., Goldin A.L., Dong K. Avoltage-gated calcium-selective channel encoded by a sodium channel-like gene. Neuron 2004, 42:101-112.
159. Zlotkin E. The insect voltage-gated sodium channel as target of insecticides. Annu Rev. Entomol. 1999, 44:429-455.