Portal de Periódicos da CAPES

Shaw potassium channel genes inDrosophila

2005; Wiley; Volume: 63; Issue: 3 Linguagem: Inglês

10.1002/neu.20126

1097-4695

James J. L. Hodge, James C. Choi, Cahir J. O’Kane, Leslie C. Griffith,

Animal Behavior and Reproduction

Journal of NeurobiologyVolume 63, Issue 3 p. 235-254 Research Articles Shaw potassium channel genes in Drosophila James J. L. Hodge, James J. L. Hodge Department of Genetics, University of Cambridge, Downing Site, Cambridge CB2 3EH, United Kingdom Department of Biology and Volen Center for Complex Systems, Brandeis University MS008, 415 South Street, Waltham, Massachusetts 02454-9110Search for more papers by this authorJames C. Choi, James C. Choi Department of Biology and Volen Center for Complex Systems, Brandeis University MS008, 415 South Street, Waltham, Massachusetts 02454-9110Search for more papers by this authorCahir J. O'Kane, Corresponding Author Cahir J. O'Kane [email protected] Department of Genetics, University of Cambridge, Downing Site, Cambridge CB2 3EH, United KingdomDepartment of Genetics, University of Cambridge, Downing Site, Cambridge CB2 3EH, United KingdomSearch for more papers by this authorLeslie C. Griffith, Leslie C. Griffith Department of Biology and Volen Center for Complex Systems, Brandeis University MS008, 415 South Street, Waltham, Massachusetts 02454-9110Search for more papers by this author James J. L. Hodge, James J. L. Hodge Department of Genetics, University of Cambridge, Downing Site, Cambridge CB2 3EH, United Kingdom Department of Biology and Volen Center for Complex Systems, Brandeis University MS008, 415 South Street, Waltham, Massachusetts 02454-9110Search for more papers by this authorJames C. Choi, James C. Choi Department of Biology and Volen Center for Complex Systems, Brandeis University MS008, 415 South Street, Waltham, Massachusetts 02454-9110Search for more papers by this authorCahir J. O'Kane, Corresponding Author Cahir J. O'Kane [email protected] Department of Genetics, University of Cambridge, Downing Site, Cambridge CB2 3EH, United KingdomDepartment of Genetics, University of Cambridge, Downing Site, Cambridge CB2 3EH, United KingdomSearch for more papers by this authorLeslie C. Griffith, Leslie C. Griffith Department of Biology and Volen Center for Complex Systems, Brandeis University MS008, 415 South Street, Waltham, Massachusetts 02454-9110Search for more papers by this author First published: 04 March 2005 https://doi.org/10.1002/neu.20126Citations: 35AboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onEmailFacebookTwitterLinkedInRedditWechat Abstract Drosophila Shaw encodes a voltage-insensitive, slowly activating, noninactivating K+ current. The functional and developmental roles of this channel are unknown. In this study, we use a dominant transgenic strategy to investigate Shaw function and describe a second member of the Shaw family, Shawl. In situ hybridization showed that the two Shaw family genes, Shaw and Shawl, have largely nonoverlapping expression patterns in embryos. Shaw is expressed mainly in excitable cells of the CNS and PNS of late embryos. Shawl is expressed in many nonexcitable cell types: ubiquitously in embryos until the germband extends, then transiently in the developing CNS and PNS, becoming restricted to progressively smaller subsets of the CNS. Ectopic full-length and truncated Shaw localize differently within neurons, and produce uneclosed small pupae and adults with unfurled wings and softened cuticle. This phenotype was mapped to the crustacean cardioactive peptide (CCAP)-neuropeptide circuit. Widespread expression of Shaw in the nervous system results in a reduction in body mass, ether-induced shaking, and lethality. Expression of full-length Shaw had more extreme phenotypic consequences and caused earlier lethality than expression of truncated Shaw in a given GAL4 pattern. Whole cell recordings from ventral ganglion motor neurons expressing the truncated Shaw protein suggest that a major role of Shaw channels in these cells is to contribute to the resting potential. © 2005 Wiley Periodicals, Inc. J Neurobiol, 2005 REFERENCES Adams MD, Celniker SE, Holt RA, et al. 2000. The genome sequence of Drosophila melanogaster. Science 287: 2185–2195. 10.1126/science.287.5461.2185 CASPubMedWeb of Science®Google Scholar Altschul SF, Gish W, Miller W, Myers EW, Lipman D. 1990. Basic local alignment search tool. J Mol Biol 215: 403–410. 10.1016/S0022-2836(05)80360-2 CASPubMedWeb of Science®Google Scholar Ashburner MA. 1989. Drosophila: a laboratory manual. Cold Spring Harbor Press, New York, p 399–402. Google Scholar Baines RA, Bate M. 1998. Electrophysiological developmental of central neurons in the Drosophila embryos. J Neurosci 18: 4673–4683. CASPubMedWeb of Science®Google Scholar Baines RA, Uhler JP, Thompson A, Sweeney ST, Bate M. 2001. Altered electrical properties in Drosophila neurons developing without synaptic transmission. J Neurosci 21: 1523–1531. 10.1523/JNEUROSCI.21-05-01523.2001 CASPubMedWeb of Science®Google Scholar Boynton S, Tully T. 1992. latheo, a new gene involved in associative learning and memory in Drosophila melanogaster from P-element mutagenesis. Genetics 131: 655–672. CASPubMedWeb of Science®Google Scholar Brand AH, Perrimon N. 1993. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401–415. CASPubMedWeb of Science®Google Scholar Broughton SJ, Kitamoto T, Greenspan RJ. 2004. Excitatory and inhibitory switches for courtship in the brain of Drosophila melanogaster. Curr Biol 14: 538–547. 10.1016/j.cub.2004.03.037 CASPubMedWeb of Science®Google Scholar Butler A, Wei A, Baker K, Salkoff L. 1989. A family of putative potassium channel genes in Drosophila. Science 243: 943–947. 10.1126/science.2493160 CASPubMedWeb of Science®Google Scholar Campos-Ortega JA, Hartenstein V. 1997. The embryonic development of Drosophila melanogaster. Springer-Verlag, Heidelberg, p 231–268. 10.1007/978-3-662-22489-2 Google Scholar Cavener DR. 1987. Comparison of the consensus sequence flanking translational start sites in Drosophila and vertebrates. Nucleic Acid Res 15: 1353–1361. 10.1093/nar/15.4.1353 CASPubMedWeb of Science®Google Scholar Choi JC, Park D, Griffith LC. 2004. Electrophysiological and morphological characterization of identified motor neurons in the Drosophila central nervous system. J Neurophysiol 91: 2353–2365. 10.1152/jn.01115.2003 PubMedWeb of Science®Google Scholar Covarrubias M, Wei A, Salkoff L. 1991. Shaker, Shal, Shab and Shaw express independent K+ current systems. Neuron 7: 763–773. 10.1016/0896-6273(91)90279-9 CASPubMedWeb of Science®Google Scholar Covarrubias M, Rubin E. 1993. Ethanol selectively blocks a non-inactivating K+ current expressed in Xenopus oocytes. Proc Natl Acad Sci USA 15: 1353–1361. Google Scholar Covarrubias M, Vyas TB, Escobar L, Wei A. 1995. Alcohols inhibit a cloned potassium channel at a discrete saturable site. J Biol Chem 270: 19408–19416. 10.1074/jbc.270.33.19408 CASPubMedWeb of Science®Google Scholar Deutsch C. 2002. Potassium channel ontogeny. Annu Rev Physiol 64: 19–46. 10.1146/annurev.physiol.64.081501.155934 CASPubMedWeb of Science®Google Scholar Deutsch C. 2003. The birth of a channel. Neuron 40: 265–276. 10.1016/S0896-6273(03)00506-3 CASPubMedWeb of Science®Google Scholar Elkes DA, Cardozo DL, Madison J, Kaplan JM. 1997. Egl-36 Shaw channels regulate C. elegans egg-laying muscle activity. Neuron 19: 165–174. 10.1016/S0896-6273(00)80356-6 CASPubMedWeb of Science®Google Scholar French LB, Lanning CC, Matly M, Harris-Warrick RM. 2004. Cellular localization of Shab and Shaw potassium channels in the lobster stomatogastric ganglion. Neuroscience 123: 919–930. 10.1016/j.neuroscience.2003.08.036 CASPubMedWeb of Science®Google Scholar Ghanshani S, Pak M, McPherson JD, et al. 1992. Genomic organization, nucleotide sequence, and cellular distribution of a Shaw-related potassium channel gene, Kv3.3, and mapping of Kv3.3 and Kv3.4 to chromosomes 19 and 1. Genomics 12: 190–196. 10.1016/0888-7543(92)90365-Y CASPubMedWeb of Science®Google Scholar Gisselmann G, Sewing S, Madsen BW, et al. 1989. The interference of truncated with normal potassium channel subunits leads to abnormal behaviour in transgenic Drosophila. EMBO J 8: 2358–2364. Google Scholar Gorczyca M, Augart C, Budnik V. 1993. Insulin-like receptor and insulin-like peptide are localized at neuromuscular junctions in Drosophila. J Neurosci 13: 3692–3704. 10.1523/JNEUROSCI.13-09-03692.1993 CASPubMedWeb of Science®Google Scholar Harris T, Shahidullah M, Ellingson JS, Covarrubias M. 2000. General anesthetic action at an internal protein site involving the S4-S5 cytoplasmic loop of a neuronal K+ channel. J Biol Chem 275: 4928–4936. 10.1074/jbc.275.7.4928 CASPubMedWeb of Science®Google Scholar Haugland FN, Wu C-F. 1990. A voltage-clamp analysis of gene-dosage effects of the Shaker locus on larval muscle potassium currents Drosophila. J Neurosci 10: 1357–1371. 10.1523/JNEUROSCI.10-04-01357.1990 CASPubMedWeb of Science®Google Scholar Hegde P, Gu G-G, Chen D, Free SJ, Singh S. 1999. Mutational analysis of the Shab-encoded delayed rectifier K+ channels in Drosophila. J Biol Chem 274: 22109–22113. 10.1074/jbc.274.31.22109 CASPubMedWeb of Science®Google Scholar Ho CS, Grange RW, Joho RH. 1997. Pleiotropic effects of a disrupted K+ channel gene: reduced body weight, impaired motor skill and muscle contraction, but no seizures. Proc Natl Acad Sci USA 94: 1533–1538. 10.1073/pnas.94.4.1533 CASPubMedWeb of Science®Google Scholar Hoang B, Chiba A. 2001. Single-cell analysis of Drosophila larval neuromuscular synapses. Dev Biol 229: 55–70. 10.1006/dbio.2000.9983 CASPubMedWeb of Science®Google Scholar Hopp TP, Prickett KS, Price VL, et al. 1988. A short polypeptide marker sequence useful for recombinant protein identification and purification. Biotechnology 6: 1204–1210. 10.1038/nbt1088-1204 CASWeb of Science®Google Scholar Hung AY, Sheng M. 2002. PDZ domains: structural modules for protein complex assembly. J Biol Chem 277: 5699–5702. 10.1093/emboj/17.8.2285 CASPubMedWeb of Science®Google Scholar Ikeda K, Kaplan WD. 1970a. Patterned neural activity of a mutant Drosophila melanogaster. Proc Natl Acad Sci USA 66: 765–772. 10.1073/pnas.66.3.765 CASPubMedWeb of Science®Google Scholar Ikeda K, Kaplan WD. 1970b. Unilaterally patterned neural activity of gynandromorphs, mosaic for a neurological mutant Drosophila melanogaster. Proc Natl Acad Sci USA 67: 1480–1487. 10.1073/pnas.67.3.1480 CASPubMedWeb of Science®Google Scholar Jelga T, Salkoff L. 1995. A multigene family of novel K+ channels from Paramecium tetraurelia. Recept Channels 3: 51–60. PubMedWeb of Science®Google Scholar Johnstone DB, Wei A, Butler A, Salkoff L, Thomas JH. 1997. Behavioral defects in C. elegans egl-36 mutants result from potassium channels shifted in voltage-dependence of activation. Neuron 19: 151–164. 10.1016/S0896-6273(00)80355-4 CASPubMedWeb of Science®Google Scholar Kaplan WD, Trout WE. 1969. The behavior of four neurological mutants of Drosophila. Genetics 61: 399–409. 10.1093/genetics/61.2.399 CASPubMedWeb of Science®Google Scholar Kupershmidt S, Yang T, Chanthaphaychith S, Wang Z, Towbin JA, Roden DM. 2002. Defective Human Ether-à-go-go-related gene trafficking linked to an endoplasmic reticulum retention signal in the C-terminus. J Biol Chem 277: 27442–27448. 10.1074/jbc.M112375200 CASPubMedWeb of Science®Google Scholar Li M, Jan Y-N, Jan LY. 1992. Specification of subunit assembly by the hydrophilic amino-terminal domain of the Shaker potassium channel. Science 257: 1225–1230. 10.1126/science.1519059 CASPubMedWeb of Science®Google Scholar Lin DM, Goodman CS. 1994. Ectopic and increased expression of Fasciclin II alters motorneuron growth cone guidance. Neuron 13: 507–523. 10.1016/0896-6273(94)90022-1 CASPubMedWeb of Science®Google Scholar Littleton JT, Ganetzky B. 2000. Ion channels and synaptic organization: analysis of the Drosophila genome. Neuron 26: 35–43. 10.1016/S0896-6273(00)81135-6 CASPubMedWeb of Science®Google Scholar Lu CS, Hodge JJL, Mehren J, Sun X-X, Griffith LC. 2003. Regulation of the Ca2+/CaM-responsive pool of CaMKII by scaffold-dependent autophosphorylation. Neuron 40: 1185–1197. 10.1016/S0896-6273(03)00786-4 CASPubMedWeb of Science®Google Scholar Luneau CJ, Williams JB, Marshall J, et al. 1991. Alternative splicing contributes to K+ channel diversity in the mammalian central nervous system. Proc Natl Acad Sci USA 88: 3932–3936. 10.1073/pnas.88.9.3932 CASPubMedWeb of Science®Google Scholar McCormack T, Vega-Saenz de Miera EC. 1990. Molecular cloning of a member of a third class of K+ channel genes in mammals. Proc Natl Acad Sci USA 87: 5227–5231. 10.1073/pnas.87.13.5227 CASPubMedWeb of Science®Google Scholar McCormack K, Tanouye MA, Iverson LE, et al. 1991. A role for the hydrophobic residues in the voltage-dependent gating of Shaker K+ channels. Proc Natl Acad Sci USA 88: 2931–2935. 10.1073/pnas.88.7.2931 CASPubMedWeb of Science®Google Scholar Mottes JR, Iverson LE. 1995. Tissue-specific alternative splicing of hybrid/lacZ genes correlates with kinetic differences in Shaker K+ currents in vivo. Neuron 14: 613–623. 10.1016/0896-6273(95)90318-6 CASPubMedWeb of Science®Google Scholar Mount SM, Burks C, Hertz G, Storm GD, White O, Fields C. 1992. Splicing signals in Drosophila: intron size, information content and consensus sequences. Nucleic Acids Res 20: 4255–4262. 10.1093/nar/20.16.4255 CASPubMedWeb of Science®Google Scholar Nitabach MN, Blau J, Holmes TC. 2002. Electrical silencing of Drosophila pacemaker neurons stops the free-running circadian clock. Cell 109: 485–495. 10.1016/S0092-8674(02)00737-7 CASPubMedWeb of Science®Google Scholar Ottschytsch N, Raes A, Van Hoorick D, Snyders DJ. 2002. Obligatory heterotetramerization of three previously uncharacterized Kv channel α-subunits identified in the human genome. Proc Natl Acad Sci USA 99: 7986–7991. 10.1073/pnas.122617999 CASPubMedWeb of Science®Google Scholar Packard M, Koo ES, Gorczyca M, Sharpe J, Cumberledge S, Budnik V. 2002. The Drosophila Wnt, wingless, provides an essential signal for pre- and postsynaptic differentiation. Cell 111: 319–330. 10.1016/S0092-8674(02)01047-4 CASPubMedWeb of Science®Google Scholar Papazian DM, Shao XM, Seoh S-A, Mock AF, Huang Y, Wainstock DH. 1995. Electrostatic interactions of S4 voltage sensor in Shaker K+ channel. Neuron 14: 1293–1301. 10.1016/0896-6273(95)90276-7 CASPubMedWeb of Science®Google Scholar Park D, Coleman MJ, Hodge JJL, Budnik V, Griffith LC. 2002. Regulation of neuronal excitability in Drosophila by constitutively active CaMKII. J Neurobiol 52: 24–42. 10.1002/neu.10066 CASPubMedWeb of Science®Google Scholar Park JH, Schroeber AJ, Helfrich-Forster C, Jackson FR, Ewer J. 2003. Targeted ablation of CCAP neuropeptide-containing neurons of Drosophila causes specific defects in execution and circadian timing of ecdysis behavior. Development 130: 2645–2656. 10.1242/dev.00503 CASPubMedWeb of Science®Google Scholar Rettig J, Wunder F, Stocker M, et al. 1992. Characterization of a Shaw related potassium channel family in rat brain. EMBO J 11: 2473–2486. 10.1002/j.1460-2075.1992.tb05312.x CASPubMedWeb of Science®Google Scholar Salamov AA, Solovyev VV. 2000. Ab initio gene finding in Drosophila genomic DNA. Genome Res 10: 516–522. 10.1101/gr.10.4.516 CASPubMedWeb of Science®Google Scholar Salkoff L, Baker K, Butler A, Covarrubias M, Pak MD, Wei A. 1992. An essential “set” of K+ channels conserved in flies, mice and humans. Trends Neurosci 15: 161–166. 10.1016/0166-2236(92)90165-5 CASPubMedWeb of Science®Google Scholar Schwarz TL, Tempel BL, Papazian DM, Jan Y-N, Jan LY. 1988. Multiple potassium-channel components are produced by alternative splicing at the Shaker locus in Drosophila. Nature 331: 137–142. 10.1038/331137a0 CASPubMedWeb of Science®Google Scholar Shahidullah M, Harris T, Germann GW, Covarrubias M. 2003. Molecular features of an alcohol binding site in a neuronal K+ channel. Biochemistry 43: 11243–11252. 10.1021/bi034738f CASWeb of Science®Google Scholar Sheng M, Liao YJ, Jan Y-N, Jan LY. 1993. Presynaptic A-current based on heteromultimeric K+ channels detected in vivo. Nature 365: 72–75. 10.1038/365072a0 CASPubMedWeb of Science®Google Scholar Shih TM, Goldin AM. 1997. Topology of the Shaker potassium channel probed with hydrophilic epitope insertions. J Cell Biol 136: 1037–1045. 10.1083/jcb.136.5.1037 CASPubMedWeb of Science®Google Scholar Smith-Maxwell CJ, Ledwell JL, Aldrich RW. 1998. Role of the S4 in cooperativity of voltage-dependent potassium channel activation. J Gen Physiol 111: 399–402. 10.1085/jgp.111.3.399 CASPubMedWeb of Science®Google Scholar Spradling AC. 1986. P-element mediated transformation in Drosophila—a practical approach. Oxford: IRL Press, p 60–73. Google Scholar Sun X-X, Hodge JJL, Zhou Y, Nguyen M, Griffith LC. 2004. The eag potassium channel binds and locally activates calcium/calmodulin-dependent protein kinase II. J Biol Chem 279: 10206–10214. 10.1074/jbc.M310728200 CASPubMedWeb of Science®Google Scholar Tautz D, Hulskamp M, Sommer RJ. 1992. Whole mount in situ hybridisation in Drosophila. In: DG Wilkinson, editor. In situ hybridisation—the practical approach series. Oxford: IRL Press, p 61–74. Google Scholar Tejedor FJ, Bokhari A, Rogero O, et al. 1997. Essential role of dlg in synaptic clustering of Shaker K+ channels in vivo. J Neurosci 17: 152–159. 10.1523/JNEUROSCI.17-01-00152.1997 CASPubMedWeb of Science®Google Scholar Torroja L, Chu H, Kotovsky I, White K. 1999. Neuronal overexpression of APPL, the Drosophila homologue of the amyloid precursor protein (APP), disrupts axonal transport. Curr Biol 9: 489–492. 10.1016/S0960-9822(99)80215-2 CASPubMedWeb of Science®Google Scholar Tsunoda S, Salkoff L. 1995a. Genetic analysis of Drosophila neurons: Shab, Shal and Shaw encode most embryonic potassium currents. J Neurosci 15: 1741–1754. CASPubMedWeb of Science®Google Scholar Tsunoda S, Salkoff L. 1995b. The major delayed rectifier in both Drosophila neurons and muscle is encoded by Shab. J Neurosci 15: 5209–5221. CASPubMedWeb of Science®Google Scholar Tu L, Santarelli V, Deutsch C. 1995. Truncated K+ channel DNA sequences specifically suppress lymphocyte K+ channel gene expression. Biophys J 68: 147–156. 10.1016/S0006-3495(95)80169-4 CASPubMedWeb of Science®Google Scholar Wei A, Covarrubias M, Butler A, Baker K, Pak M, Salkoff L. 1990. K+ current diversity is produced by an extended gene family conserved in Drosophila and mouse. Science 248: 599–603. 10.1126/science.2333511 CASPubMedWeb of Science®Google Scholar Wei A, Jegla T, Salkoff L. 1996. Eight potassium channel families revealed by the C. elegans genome project. Neuropharmacol 35: 805–829. 10.1016/0028-3908(96)00126-8 CASPubMedWeb of Science®Google Scholar Weiser M, Vega-Saenz de Miera E, Kentros C, et al. 1994. Differential expression of Shaw-related K + channels in the rat central nervous system. J Neurosci 14: 949–972. 10.1523/JNEUROSCI.14-03-00949.1994 CASPubMedWeb of Science®Google Scholar White BH, Osterwalder TP, Yoon KS, Joiner WJ, Whim MD, Kaczmarek LK, Keshishian H. 2001. Targeted attenuation of electrical activity in Drosophila using a genetically modified K+ channel. Neuron 31: 699–711. 10.1016/S0896-6273(01)00415-9 CASPubMedWeb of Science®Google Scholar Xu J, Yu W, Jan Y-N, Jan LY, Li M. 1995. Assembly of voltage-gated potassium channels. Conserved hydrophilic motifs determine subfamily-specific interactions between α-subunits. J Biol Chem 270: 24761–24768. 10.1074/jbc.270.42.24761 CASPubMedWeb of Science®Google Scholar Zagotta WN, Brainard MS, Aldrich RW. 1988. Single-channel analysis of four distinct classes of potassium channels in Drosophila muscle. J Neurosci 8: 4765–4779. CASPubMedWeb of Science®Google Scholar Zito K, Fetter RD, Goodman CS, Isacoff EY. 1997. Synaptic clustering of Fasciclin II and Shaker: essential targeting sequences and role of Dlg. Neuron 19: 1007–1016. 10.1016/S0896-6273(00)80393-1 CASPubMedWeb of Science®Google Scholar Citing Literature Volume63, Issue3June 2005Pages 235-254 ReferencesRelatedInformation