Drosophila seizure disorders: genetic suppression of seizure susceptibility
Arunesh Saras, Laura E. Simon, Harlan J. Brawer, Richard E. Price, Mark A. Tanouye
Drosophila seizure disorders: genetic suppression of seizure susceptibility
Various Drosophila models of human disease have recently received increased interest. The main goal is to uncover the fundamental biological basis for human pathology taking advantage of the power of Drosophila genetics. This review examines a set of Drosophila seizure-sensitive mutations that model human seizure disorders, especially epilepsy. Also described is a novel set of mutations that act as seizure-suppressors that ameliorate epilepsy phenotypes in double mutant combinations.
Drosophila / epilepsy / seizure disorders / sodium channel / seizure-suppressor genes
[1a] |
Barreto E, Cressman J R (2011). Ion concentration dynamics as a mechanism for neuronal bursting. J Biol Phys, 37(3): 361–373
|
[1] |
Bassuk A G, Wallace R H, Buhr A, Buller A R, Afawi Z, Shimojo M, Miyata S, Chen S, Gonzalez-Alegre P, Griesbach H L, Wu S, Nashelsky M, Vladar E K, Antic D, Ferguson P J, Cirak S, Voit T, Scott M P, Axelrod J D, Gurnett C, Daoud A S, Kivity S, Neufeld M Y, Mazarib A, Straussberg R, Walid S, Korczyn A D, Slusarski D C, Berkovic S F, El-Shanti H I (2008). A homozygous mutation in human PRICKLE1 causes an autosomal-recessive progressive myoclonus epilepsy-ataxia syndrome. Am J Hum Genet, 83(5): 572–581
CrossRef
Google scholar
|
[2] |
Ben-Ari Y (2002). Excitatory actions of GABA during development: the nature of the nurture. Nature, 3: 728–739
|
[3] |
Ben-Ari Y, Gaiarsa J L, Tyzio R, Khazipov R (2007). GABA: a pioneer transmitter that excites immature neurons and generates primitive oscillations. Physiol Rev, 87(4): 1215–1284
CrossRef
Google scholar
|
[4] |
Benzer S (1971). From the gene to behavior. JAMA, 218(7): 1015–1022
CrossRef
Google scholar
|
[5] |
Boettger T, Rust M B, Maier H, Seidenbecher T, Schweizer M, Keating D J, Faulhaber J, Ehmke H, Pfeffer C, Scheel O,
CrossRef
Google scholar
|
[6] |
Bullock T H, Horridge G A (1965). “Structure and Function in the Nervous System of Invertebrates”, 2 vol. San Francisco and London: W H Freeman A Comp Ltd, XXVIII, 1722pp
|
[7] |
Carlson S D, Juang J L, Hilgers S L, Garment M B (2000). Blood barriers of the insect. Annu Rev Entomol, 45(1): 151–174
CrossRef
Google scholar
|
[8] |
Catterall W A (2014). Sodium channels, inherited epilepsy, and antiepileptic drugs. Annu Rev Pharmacol Toxicol, 54(1): 317–338
CrossRef
Google scholar
|
[9] |
Catterall W A, Goldin A L, Waxman S G (2003). International Union of Pharmacology, XXXIX Compendium of voltage-gated ion channels: sodium channels. Pharmacol Rev, 55(4): 575–578
CrossRef
Google scholar
|
[10] |
Champoux J J (2001). DNA topoisomerases: Structure, function and mechanism. Annu Rev Biochem, 70(1): 369–413
CrossRef
Google scholar
|
[11] |
Chung H, Sztal T, Pasricha S, Sridhar M, Batterham P, Daborn P J (2009). Characterization of Drosophila melanogaster cytochrome P450 genes. Proc Natl Acad Sci USA, 106(14): 5731–5736
CrossRef
Google scholar
|
[12] |
Chvatal A, Sykova E (2000). Glial influence on neuronal signaling. Prog Brain Res, 125: 199–216
CrossRef
Google scholar
|
[13] |
Cressman J RJr, Ullah G, Ziburkus J, Schiff S J, Barreto E (2009). The influence of sodium and potassium dynamics on excitability, seizures, and the stability of persistent states: I. single neuron dynamics. J Comput Neurosci, 26(2): 159–170
CrossRef
Google scholar
|
[14] |
D'Ambrosio R (2004). The role of glial membrane ion channels in seizures and epileptogenesis. Pharmacol Ther, 103(2): 95–108
CrossRef
Google scholar
|
[15] |
Devinsky O, Vezzani A, Najjar S, De Lanerolle N C, Rogawski M A (2013). Glia and epilepsy: excitability and inflammation. Trends Neurosci, 36(3): 174–184
CrossRef
Google scholar
|
[16] |
DiMauro S, Hirano M, Kaufmann P, Tanji K, Sano M, Shungu D C, Bonilla E, DeVivo D C,
|
[17] |
Dong K (2007). Insect sodium channels and insecticide resistance. Invert Neurosci, 7(1): 17–30
CrossRef
Google scholar
|
[18] |
Engel J E, Wu C F (1994). Altered mechanoreceptor response in Drosophila bang-sensitive mutants. J Comp Physiol A Neuroethol Sens Neural Behav Physiol, 175(3): 267–278
CrossRef
Google scholar
|
[19] |
Fahmy O G, Fahmy M J (1960). Cytogenetic analysis of the action of carcinogens and tumor inhibitors in Drosophila melanogaster. Genetics, 45: 419–438
|
[20] |
Feng G, Deak P, Chopra M, Hall L M (1995). Cloning and functional analysis of TipE, a novel membrane protein that enhances Drosophila para sodium channel function. Cell, 82(6): 1001–1011
CrossRef
Google scholar
|
[21] |
Fergestad T, Bostwick B, Ganetzky B (2006). Metabolic disruption in Drosophila bang-sensitive seizure mutants. Genetics, 173(3): 1357–1364
CrossRef
Google scholar
|
[22] |
Fertziger A P, Ranck J BJr (1970). Potassium accumulation in interstitial space during epileptiform seizures. Exp Neurol, 26(3): 571–585
CrossRef
Google scholar
|
[23] |
Florence G, Dahlem M A, Almeida A C G, Bassani J W M, Kurths J (2009). The role of extracellular potassium dynamics in the different stages of ictal bursting and spreading depression: a computational study. J Theor Biol, 258(2): 219–228
CrossRef
Google scholar
|
[24] |
Freeman A A, Syed S, Sanyal S (2013). Modeling the genetic basis for human sleep disorders in Drosophila. Commun Integr Biol, 6(1): e22733
CrossRef
Google scholar
|
[25] |
Ganetzky B (1984). Genetic studies of membrane excitability in Drosophila: lethal interaction between two temperature-sensitive paralytic mutations. Genetics, 108: 897–911
|
[26] |
Ganetzky B, Wu C F (1982a). Indirect suppression involving behavioral mutants with altered nerve excitability in Drosophila melanogaster. Genetics, 100: 597–614
|
[27] |
Ganetzky B, Wu C F (1982b). Drosophila mutants with opposing effects on nerve excitability: genetic and spatial interactions in repetitive firing. J Neurophysiol, 47: 501–514
|
[28] |
Glasscock E, Singhania A, Tanouye M A (2005). The mei-p26 gene encodes an RBCC-NHL protein that regulates seizure susceptibility in Drosophila. Genetics, 170: 1677–1689
CrossRef
Google scholar
|
[29] |
Glasscock E, Tanouye M A (2005). Drosophila couch potato mutants exhibit complex neurological abnormalities including epilepsy phenotypes. Genetics, 169(4): 2137–2149
CrossRef
Google scholar
|
[30] |
Goldin A L (2001). Resurgence of sodium channel research. Annu Rev Physiol, 63(1): 871–894
CrossRef
Google scholar
|
[31] |
Greenhill S D, Jones R S G (2010). Diverse antiepileptic drugs increase the ratio of background synaptic inhibition to excitation and decrease neuronal excitability in neurons of the rat entorhinal cortex in vitro. Neurosci, 167(2): 456–474
CrossRef
Google scholar
|
[32] |
Griesemer D A, Kellner C H, Beale M D, Smith G M (1997). Electroconvulsive therapy for treatment of intractable seizures: initial findings in two children. Neurology, 49(5): 1389–1392
CrossRef
Google scholar
|
[33] |
Grigliatti T A, Hall L, Rosenbluth R, Suzuki D T (1973). Temperature-sensitive mutations in Drosophila melanogaster. Mol Gen Genet, 120(2): 107–114
CrossRef
Google scholar
|
[34] |
Guo M (2012). Drosophila as a model to study mitochondrial dysfunction in Parkinson’s disease. Cold Spring Harb Perspect Med, 2(11): a009944
CrossRef
Google scholar
|
[35] |
Hariharan I K, Haber D A (2003). Yeast, flies, worms, and fish in the study of human disease. N Engl J Med, 348(24): 2457–2463
CrossRef
Google scholar
|
[36] |
Hebert S C, Mount D B, Gamba G (2004). Molecular physiology of cation-coupled Cl– cotransport: the SLC12 family. Pflugers Arch, 447(5): 580–593
CrossRef
Google scholar
|
[37] |
Hekmat-Scafe D S, Lundy M Y, Ranga R, Tanouye M A (2006). Mutations in the K+/Cl– cotransporter gene kazachoc (kcc) increase seizure susceptibility in Drosophila. J Neurosci, 26(35): 8943–8954
CrossRef
Google scholar
|
[38] |
Hekmat-Scafe D S, Mercado A, Fajilan A A, Lee A W, Hsu R, Mount D B, Tanouye M A (2010). Seizure sensitivity is ameliorated by targeted expression of K+-Cl– cotransporter function in the mushroom body of the Drosophila brain. Genetics, 184(1): 171–183
CrossRef
Google scholar
|
[39] |
Hirth F (2010). Drosophila melanogaster in the study of human neurodegeneration. CNS Neurol Disord Drug Targets, 9(4): 504–523
CrossRef
Google scholar
|
[40] |
Howlett I C, Tanouye M A (2013). Seizure-sensitivity in Drosophila is ameliorated by dorsal vessel injection of the antiepileptic drug valproate. J Neurogenet, 27(4): 143–150
CrossRef
Google scholar
|
[41] |
Hubner C A, Stein V, Hermans-Borgmeyer I, Meyer T, Ballanyi K, Jentsch T J (2001). Disruption of KCC2 reveals an essential role of K-Cl cotransport already in early synaptic inhibition. Neuron, 30(2): 515–524
CrossRef
Google scholar
|
[42] |
Imbrici P, Jaffe S L, Eunson L H, Davies N P, Herd C, Robertson R, Kullmann D M, Hanna M G (2004). Dysfunction of the brain calcium channel CaV2.1 in absence epilepsy and episodic ataxia. Brain, 127(12): 2682–2692
CrossRef
Google scholar
|
[43] |
Jacobs J, Dubeau F, Olivier A, Andermann F (2008). Pathways of seizure propagation from the temporal to the occipital lobe. Epileptic Disord, 10: 266–270
|
[44a] |
Kager H, Wadman W J, Somjen G G (2000). Simulated seizures and spreading depression in a neuron model incorporating interstitial space and ion concentrations. J Neurophysiol, 84(1): 195–512
|
[44] |
Kandel E R, Spencer W A (1961). The pyramidal cell during hippocampal seizure. Epilepsia, 2(1): 63–69
CrossRef
Google scholar
|
[45] |
Kawasaki F, Felling R, Ordway R W (2000). A temperature-sensitive paralytic mutant defines a primary synaptic calcium channel in Drosophila. J Neurosci, 20: 4885–4889
|
[46] |
Kitamoto T (2001). Conditional modification of behavior in Drosophila by targeted expression of a temperature-sensitive shibire allele in defined neurons. J Neurobiol, 47(2): 81–92
CrossRef
Google scholar
|
[47] |
Koenig J H, Ikeda K (1989). Disappearance and reformation of synaptic vesicle membrane upon transmitter release observed under reversible blockage of membrane retrieval. J Neurosci, 9: 3844–3860
|
[48] |
Kroll J R, Wong K G, Siddiqui F M, Tanouye M A (2015). Disruption of endocytosis with the dynamin mutant shibirets1 suppresses seizures in Drosophila. Genetics, 201(3): 1087–1102
CrossRef
Google scholar
|
[49] |
Kuebler D, Tanouye M A (2000). Modifications of seizure susceptibility in Drosophila. J Neurophysiol, 83: 998–1009
|
[50] |
Kuebler D, Tanouye M A (2002). The anticonvulsant sodium valproate reduces seizure-susceptibility in mutant Drosophila. Brain Res, 958(1): 36–42
CrossRef
Google scholar
|
[51] |
Kuebler D, Zhang H, Ren X, Tanouye M A (2001). Genetic suppression of seizure susceptibility in Drosophila. J Neurophysiol, 86: 1211–1225
|
[52] |
Kuromi H, Honda A, Kidokoro Y (2004). Ca2<?A3B2 h=-0.3h?>+ influx through distinct routes controls exocytosis and endocytosis at Drosophila presynaptic terminals. Neuron, 41(1): 101–111
CrossRef
Google scholar
|
[53] |
Kwan P, Brodie M J (2000). Early identification of refractory epilepsy. N Engl J Med, 342(5): 314–319
CrossRef
Google scholar
|
[54] |
Landmark C J (2008). Targets for antiepileptic drugs in the synapse. Med Sci Monit, 13: RA1–RA7
|
[55] |
Lee J, Wu C F (2002). Electroconvulsive seizure behavior in Drosophila: analysis of the physiological repertoire underlying a stereotyped action pattern in bang sensitive mutants. J Neurosci, 22: 11065–11079
|
[56] |
Lee J, Wu C F (2006). Genetic modifications of seizure susceptibility and expression by altered excitability in Drosophila Na(+) and K(+) channel mutants. J Neurophysiol, 96(5): 2465–2478
CrossRef
Google scholar
|
[57] |
Lilly M, Carlson J (1990). smellblind: a gene required for Drosophila olfaction. Genetics, 124: 293–302
|
[58] |
Lin W H, Baines R A (2014). Regulation of membrane excitability: a convergence on voltage-gated sodium conductance. Molec Neurobiol, 10.1007/s12035-014-8674-0 /fulltext.html
|
[59] |
Lin W H, Wright D E, Muraro N I, Baines R A (2009). Alternative splicing in the voltage-gated sodium channel DmNav regulates activation, inactivation, and persistent current. J Neurophysiol, 102(3): 1994–2006
CrossRef
Google scholar
|
[60] |
Loscher W (2002). Basic pharmacology of valproate: a review after 35 years of clinical use for the treatment of epilepsy. CNS Drugs, 16: 669–694
CrossRef
Google scholar
|
[61] |
Lossin C (2009). A catalog of SCN1A variants. Brain Dev, 31(2): 114–130
CrossRef
Google scholar
|
[62] |
Loughney K, Kreber R, Ganetzky B (1989). Molecular analysis of the para locus, a sodium channel gene in Drosophila. Cell, 58(6): 1143–1154
CrossRef
Google scholar
|
[63] |
Lunde M E, Lee E K, Rasmussen K G (2006). Electroconvulsive therapy in patients with epilepsy. Epilepsy Behav, 9(2): 355–359
CrossRef
Google scholar
|
[64] |
Mayer F, Mayer N, Chinn L, Pinsonneault R L, Kroetz D, Bainton R J (2009). Evolutionary conservation of vertebrate blood-brain barrier chemoprotective mechanisms in Drosophila. J Neurosci, 29(11): 3538–3550
CrossRef
Google scholar
|
[65] |
McIntyre D C, Gilby K L (2008). Mapping seizure pathways in the temporal lobe. Epilepsia, 49(s3Suppl 3): 23–30
CrossRef
Google scholar
|
[66] |
McNamara J O (1994). Cellular and molecular basis of epilepsy. J Neurosci, 14: 3413–3425
|
[67] |
Mount D B, Delpire E, Gamba G, Hall A E, Poch E, Hoover R S, Herbert S C (1998). The electroneutral cation-chloride cotransporters. J Exp Biol, 201: 2091–2102
|
[68] |
Mulley J C, Scheffer I E, Petrou S, Dibbens L M, Berkovic S F, Harkin L A (2005). SCN1A mutations and epilepsy. Hum Mutat, 25(6): 535–542
CrossRef
Google scholar
|
[69] |
Noebels J L (1996). Targeting epilepsy genes. Neuron, 16(2): 241–244
CrossRef
Google scholar
|
[70] |
O’Dowd D K, Gee J R, Smith M A (1995). Sodium current density correlates with expression of specific alternatively spliced sodium channel mRNAs in single neurons. J Neurosci, 15: 4005–4012
|
[71] |
Oh C Y, Bainbridge J (2012). Lowering the seizure threshold associated with antidepressants, stimulants, antipsychotics, and others. Mental Health Clinician: November 2012-Epilepsy and seizure disorders and their treatment, Vol. 2, No. 5, pp. 127–128
|
[72] |
Olson R O, Liu Z, Nomura Y, Song W, Dong K (2008). Molecular and functional characterization of voltage-gated sodium channel variants from Drosophila melanogaster. Insect Biochem Mol Biol, 38(5): 604–610
CrossRef
Google scholar
|
[73] |
Paemka L, Mahajan V B, Ehaideb S N, Skeie J M, Tan M C, Wu S, Cox A J, Sowers L P, Gecz J, Jolly L, Ferguson P J, Darbro B, Schneider A, Scheffer I E, Carvill G L, Mefford H C, El-Shanti H, Wood S A, Manak J R, Bassuk A G (2015). Seizures are regulated by ubiquitin-specific peptidase 9 X-linked (USP9X), a de-ubiquitinase. PLoS Genet, 11(3): e1005022
CrossRef
Google scholar
|
[74] |
Parker L, Padilla M, Du Y, Dong K, Tanouye M A (2011). Drosophila as a model for epilepsy: bss is a gain-of-function mutation in the Para sodium channel gene that leads to seizures. Genetics, 187(2): 523–534
CrossRef
Google scholar
|
[75] |
Pavlidis P, Ramaswami M, Tanouye M A (1994). The Drosophila easily shocked gene: a mutation in a phospholipid synthetic pathway causes seizure, neuronal failure, and paralysis. Cell, 79(1): 23–33
CrossRef
Google scholar
|
[76] |
Pavlidis P, Tanouye M A (1995). Seizures and failures in the giant fiber pathway of Drosophila bang-sensitive paralytic mutants. J Neurosci, 15: 5810–5819
|
[77] |
Pfeiffer B D, Truman J W, Rubin G M (2012). Using translational enhancers to increase transgene expression in Drosophila. Proc Natl Acad Sci USA, 109(17): 6626–6631
CrossRef
Google scholar
|
[78] |
Phelan P, Nakagawa M, Wilkin M B, Moffat K G, O’Kane C J, Davies J A, Bacon J P (1996). Mutations in shaking-B prevent electrical synapse formation in the Drosophila giant fiber system. J Neurosci, 16: 1101–1113
|
[79] |
Phelan P, Starich T A (2001). Innexins get into the gap. BioEssays, 23(5): 388–396
CrossRef
Google scholar
|
[80] |
Phelan P, Stebbings L A, Baines R A, Bacon J P, Davies J A, Ford C (1998). Drosophila shaking-B protein forms gap junctions in paired Xenopus oocytes. Nature, 391(6663): 181–184
CrossRef
Google scholar
|
[81] |
Pisani F, Oteri G, Costa C, Di Raimando G, Di Perri R (2002). Effects of psychotropic drugs on seizure threshold. Drug Saf, 25(2): 91–110
CrossRef
Google scholar
|
[82] |
Pittendrigh B, Reenan R, ffrench-Constant R H, Ganetzky B (1997). Point mutations in the Drosophila sodium channel gene para associated with resistance to DDT and pyrethroid insecticides. Mol Gen Genet, 356(6): 602–610
CrossRef
Google scholar
|
[83] |
Ramaswami M, Tanouye M A (1989). Two sodium channel genes in Drosophila: implications for channel diversity. Proc Natl Acad Sci USA, 86(6): 2079–2082
CrossRef
Google scholar
|
[84] |
Read R (2011). Drosophila melanogaster as a model system for human brain cancers. Glia, 59(9): 1364–1376
CrossRef
Google scholar
|
[85] |
Regenold W T, Weintraub D, Taller A (1998). Electroconvulsive therapy for epilepsy and major depression. Am J Geriatr Psychiatry, 6(2): 180–183(Top of Form)
CrossRef
Google scholar
|
[86] |
Rein K, Zöckler M, Mader M T, Grübel C, Heisenberg M (2002). The Drosophila standard brain. Curr Biol, 12(3): 227–231
CrossRef
Google scholar
|
[87] |
Reiter L T, Bier E (2001). Using Drosophila melanogaster to uncover human disease gene function and potential drug target proteins. Expert Opin Ther Targets, 6: 387–399
|
[88] |
Reynolds E R, Stauffer E A, Feeney L, Rojahn E, Jacobs B, McKeever C (2003). Treatment with the antiepileptic drugs phenytoin and gabapentin ameliorates seizure and paralysis of Drosophila bang-sensitive mutants. J Neurobiol, 58(4): 503–513
CrossRef
Google scholar
|
[89] |
Rieckhof G E, Yoshihara M, Guan Z, Littleton J T (2003). Presynaptic N-type calcium channels regulate synaptic growth. J Biol Chem, 278(42): 41099–41108
CrossRef
Google scholar
|
[90] |
Royden C S, Pirrotta V, Jan L Y (1987). The tko locus, site of a behavioral mutation in D. melanogaster, codes for a protein homologous to prokaryotic ribosomal protein S12. Cell, 51(2): 165–173
CrossRef
Google scholar
|
[91] |
Rusan Z M, Kingsford O A, Tanouye M A (2014). Modeling glial contributions to seizures and epileptogenesis: cation-chloride cotransporters in Drosophila melanogaster. PLoS ONE, 9(6): e101117
CrossRef
Google scholar
|
[92] |
Sackeim H A, Decina P, Prohovnik I, Malitz S S R, Resor S R (1987). Anticonvulsant and antidepressant properties of electroconvulsive therapy: a proposed mechanism of action. Biol Psychiatry, 18: 1301–1310
|
[93] |
Salkoff L, Kelly L (1978). Temperature-induced seizure and frequency-dependent neuromuscular block in a ts mutant of Drosophila. Nature, 273(5658): 156–158
CrossRef
Google scholar
|
[94] |
Saras A, Tanouye M A (2016). Mutations of the calcium channel gene cacophony suppress seizures in Drosophila. PLoS Genet, 12(1): e1005784
CrossRef
Google scholar
|
[95] |
Schutte R J, Schutte S S, Algara J, Barragan E V, Gilligan J, Staber C, Savva Y A, Smith M A, Reenan R, O’Dowd D K (2014). Knock-in model of Dravet syndrome reveals a constitutive and conditional reduction in sodium current. J Neurophysiol, 112(4): 903–912
CrossRef
Google scholar
|
[96] |
Schwarz N, Hahn A, Bast T, Müller S, Löffler H, Maljevic S, Gaily E, Prehl I, Biskup S, Joensuu T, Lehesjoki A E, Neubauer B A, Lerche H, Hedrich U B (2016). Mutations in the sodium channel gene SCN2A cause neonatal epilepsy with late-onset episodic ataxia. J Neurol, 263(2): 334–343
CrossRef
Google scholar
|
[97] |
Sehgal A, Mignot E (2011). Genetics of sleep and sleep disorders. Cell, 146(2): 194–207
CrossRef
Google scholar
|
[98] |
Seifert G, Carmignoto G, Steinhäuser C (2010). Astrocyte dysfunction in epilepsy. Brain Res Brain Res Rev, 63(1-2): 212–221
CrossRef
Google scholar
|
[99] |
Shneker B F, Fountain N B (2003). Epilepsy. Dis Mon, 49(7): 426–478
CrossRef
Google scholar
|
[100] |
Siddiqi O, Benzer S (1976). Neurophysiological defects in temperature-sensitive paralytic mutants of Drosophila melanogaster. Proc Natl Acad Sci USA, 73(9): 3253–3257
CrossRef
Google scholar
|
[101] |
Smith L A, Wang X, Peixoto A A, Neumann E K, Hall L M, Hall J C (1996). A Drosophila calcium channel alpha1 subunit gene maps to a genetic locus associated with behavioral and visual defects. J Neurosci, 16: 7868–7879
|
[102] |
Somjen G G (2004). “Ions in the Brain : Normal Function, Seizures, and Stroke: Normal Function, Seizures, and Stroke”. Oxford University Press, USA. At<https://books.google.com/books?id=WjSoQVt-taYC&pgis=1>
|
[103] |
Song J, Hu J, Tanouye M A (2007). Seizure suppression by top1 mutations in Drosophila. J Neurosci, 27(11): 2927–2937
CrossRef
Google scholar
|
[104] |
Song J, Parker L, Hormozi L, Tanouye M A (2008). DNA topoisomerase I inhibitors ameliorate seizure-like behaviors and paralysis in a Drosophila model of epilepsy. Neuroscience, 156(3): 722–728
CrossRef
Google scholar
|
[105] |
Song J, Tanouye M A (2006). Seizure suppression by shakB2, a gap junction mutation in Drosophila. J Neurophysiol, 95(2): 627–635
CrossRef
Google scholar
|
[106] |
Song J, Tanouye M A (2007). Role for para sodium channel gene 3′ UTR in the modification of Drosophila seizure susceptibility. Dev Neurobiol, 67(14): 1944–1956
CrossRef
Google scholar
|
[107] |
Stefan H, Lopes da Silva F H (2013). Epileptic neuronal networks: methods of identification and clinical relevance. Front Neurol, 4: 8
CrossRef
Google scholar
|
[108] |
Steinhoff B, Hirsch E, Mutani R, Nakken K (2003). The ideal characteristics of antiepileptic therapy: an overview of old and new AEDs. Acta Neurol Scand, 107(2): 87–95
CrossRef
Google scholar
|
[109] |
Stilwell G E, Saraswati S, Littleton J T, Chouinard S W (2006). Development of a Drosophila seizure model for in vivo high-throughput drug screening. Eur J Neurosci, 24(8): 2211–2222
CrossRef
Google scholar
|
[110] |
Stödberg T, McTague A, Ruiz A J, Hirata H, Zhen J, Long P, Farabella I, Meyer E, Kawahara A, Vassallo G, Stivaros S M, Bjursell M K, Stranneheim H, Tigerschiöld S, Persson B, Bangash I, Das K, Hughes D, Lesko N, Lundeberg J, Scott R C, Poduri A, Scheffer I E, Smith H, Gissen P, Schorge S, Reith M E, Topf M, Kullmann D M, Harvey R J, Wedell A, Kurian M A (2015). Mutations in SLC12A5 in epilepsy of infancy with migrating focal seizures. Nat Commun, 6: 8038
CrossRef
Google scholar
|
[111] |
Stork T, Engelen D, Krudewig A, Silies M, Bainton R J, Klambt C (2008). Organization and function of the blood-brain barrier in Drosophila. J Neurosci, 28(3): 587–597
CrossRef
Google scholar
|
[112] |
Sun L, Gilligan J, Staber C, Schutte R J, Nguyen V, O’Dowd D K, Reenan R (2012). A knock-in model of human epilepsy in Drosophila reveals a novel cellular mechanism associated with heat-induced seizure. J Neurosci, 32(41): 14145–14155
CrossRef
Google scholar
|
[113] |
Suzuki D, Grigliatti T, Williamson R (1971). Temperature-sensitive mutations in Drosophila melanogaster, VII. A mutation (parats) causing reversible adult paralysis. Proc Natl Acad Sci USA, 68(5): 890–893
CrossRef
Google scholar
|
[114] |
Tan J S, Lin F, Tanouye M A (2004). Potassium bromide, an anticonvulsant, is effective at alleviating seizures in the Drosophila bang-sensitive mutant bang senseless. Brain Res, 1020(1-2): 45–52
CrossRef
Google scholar
|
[115] |
Tanouye M A, Ferrus A, Fujita S C (1981). Abnormal action potentials associated with the Shaker complex locus of Drosophila. Proc Natl Acad Sci USA, 78(10): 6548–6552
CrossRef
Google scholar
|
[116] |
Tao H, Manak J R, Sowers L, Mei X, Kiyonari H, Abe T, Dahdaleh N S, Yang T, Wu S, Chen S, Fox M H, Gurnett C, Montine T, Bird T, Shaffer L G, Rosenfeld J A, McConnell J, Madan-Khetarpal S, Berry-Kravis E, Griesbach H, Saneto R P, Scott M P, Antic D, Reed J, Boland R, Ehaideb S N, El-Shanti H, Mahajan V B, Ferguson P J, Axelrod J D, Lehesjoki A E, Fritzsch B, Slusarski D C, Wemmie J, Ueno N, Bassuk A G (2011). Mutations in Prickle orthologs cause seizures in flies, mice, and humans. Am J Hum Genet, 88(2): 138–149
CrossRef
Google scholar
|
[117] |
Thackeray J R, Ganetzky B (1994). Developmentally regulated alternative splicing generates a complex array of Drosophila para sodium channel isoforms. J Neurosci, 14: 2569–2578
|
[118] |
Thackeray J R, Ganetzky B (1995). Conserved alternative splicing patterns and splicing signals in the Drosophila sodium channel gene para. Genetics, 141: 203–214
|
[119] |
Tornberg J, Voikar V, Savilahti H, Rauvala H, Airaksinen M S (2005). Behavioural phenotypes of hypomorphic KCC2-deficient mice. Eur J Neurosci, 21(5): 1327–1337
CrossRef
Google scholar
|
[120] |
Ueda A, Grabbe C, Lee J, Lee J, Palmer R H, Wu C F (2008). Mutation of Drosophila focal adhesion kinase induces bang-sensitive behavior and disrupts glial function, axonal conduction and synaptic transmission. Eur J Neurosci, 27(11): 2860–2870
CrossRef
Google scholar
|
[121] |
van der Bliek A M, Meyerowitz E M (1991). Dynamin-like protein encoded by the Drosophila shibire gene associated with vesicular traffic. Nature, 351(6325): 411–414
CrossRef
Google scholar
|
[122] |
Warmke J W, Reenan R A G, Wang P, Qian S, Arena J P, Wang J, Wunderler D, Liu K, Kaczorowski G J, Ploeg L H T V, Ganetzky B, Cohen C J (1997). Functional expression of Drosophila para sodium channels: modulation by the membrane protein tipE and toxin pharmacology. J Gen Physiol, 110(2): 119–133
CrossRef
Google scholar
|
[123] |
Watanabe T K, Yamazaki T (1976). Evidence for coadaptation: negative correlation between lethal genes and polymorphic inversions in Drosophila melanogaster. Genetics, 82: 697–702
|
[124] |
White H S, Smith M D, Wilcox K S (2007). Mechanisms of action of antiepileptic drugs. Int Rev Neurobiol, 81: 85–110
CrossRef
Google scholar
|
[125] |
Willoughby L, Chang H, Lumb C, Robin C, Batterham P, Daborn P J (2006). A comparison of Drosophila melanogaster detoxification gene induction responses for six insecticides, caffeine and Phenobarbital. Insect Biochem Mol Biol, 36(12): 934–942
CrossRef
Google scholar
|
[126] |
Woo N S, Lu J, England R, McClellan R, Dufour S, Mount D B, Deutch A Y, Lovinger D M, Delpire E (2002). Hyperexcitability and epilepsy associated with disruption of the mouse neuronal-specific K-Cl cotransporter gene. Hippocampus, 12(2): 258–268
CrossRef
Google scholar
|
[127] |
Wu C F, Ganetzky B (1980). Genetic alteration of nerve membrane excitability in temperature-sensitive paralytic mutants of Drosophila melanogaster. Nature, 286(5775): 814–816
CrossRef
Google scholar
|
[128] |
Zhang H, Tan J, Reynolds E, Kuebler D, Faulhaber S, Tanouye M A (2002). The Drosophila slamdance gene: a mutation in an aminopeptidase can cause seizure, paralysis and neuronal failure. Genetics, 162: 1283–1299
|
[129] |
Zhang Y Q, Roote J, Brogna S, Davis A W, Barbash D A, Nash D, Ashburner M (1999). Stress sensitive B encodes an adenine nucleotide translocase in Drosophila melanogaster. Genetics, 153: 891–903
|
[130] |
Zuckermann E C, Glaser G H (1970). Activation of experimental epileptogenic foci. Action of increased K+ in extracellular spaces of the brain. Arch Neurol, 23(4): 358–364
CrossRef
Google scholar
|
/
〈 | 〉 |