Ion channels to inactivate neurons in Drosophila

Frontiers in Molecular Neuroscience

Volumn 2, Issue AUG, 2009, Pages

  Hodge, James J L ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

Behaviour; Drosophila; Electrical inactivation; Intrinsic excitability; Ion channels; Membrane potential; Neural circuits; Receptors

Indexed keywords

EID: 77953931841     PISSN: 16625099     EISSN: None     Source Type: Journal    
DOI: 10.3389/neuro.02.013.2009     Document Type: Review

References (108)

1. Agosto, J., Choi, J. C., Parisky, K. M., Stilwell, G., Rosbash, M., and Griffith, L. C. (2008). Modulation of GABAA receptor desensitization uncouples sleep onset and maintenance in Drosophila. Nat. Neurosci. 11, 354-359.
2. Ashcroft, F. M. (2006). From molecule to malady. Nature 440, 440-447.
3. Baines, R. A., Uhler, J. P., Thompson, A., Sweeney, S. T., and Bate M. (2001). Altered electrical properties in Drosophila neurons developing without synaptic transmission. J. Neurosci. 21, 1523-1531.
4. Baker, B. S., Taylor, B. J., and Hall, J. C. (2001). Are complex behaviors specified by dedicated regulatory genes? Reasoning from Drosophila. Cell 105, 13-24.
5. Beck, H., and Yaari, Y. (2008). Plasticity of intrinsic neuronal properties in CNS disorders. Nat. Rev. Neurosci. 9, 357-369.
6. Brand, A. H., and Perrimon, N. (1993). Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401-415.
7. Brickley, S. G., Revilla V., Cull-Candy, S. G., Wisden, W., and Farrant, M. (2001). Adaptive regulation of neuronal excitability by voltage-independent potassium conductance. Nature 409, 88-92.
8. Broughton, S. J., Kitamoto, T., and Greenspan, R. J. (2004). Excitatory and inhibitory switches four courtship in the brain of Drosophila melanogaster. Curr. Biol. 24, 538-547.
9. Brown, T. M., and Piggins, H. D., (2007). Electrophysiology of the suprachiasmatic clock. Prog. Neurobiol. 82, 229-255.
10. Burrone, J., O'Byrne, M., and Murphey, V. T. (2002). Multiple forms of synaptic plasticity triggered by selective suppression of activity in individual neurons. Nature 420, 414-418.
11. Cannon, S. C. (2006). Pathomechanisms in channelopathies of skeletal muscle and brain. Annu. Rev. Neurosci. 29, 387-425.
12. Cao, G., and Nitabach, M. N. (2008). Circadian control of membrane excitability in Drosophila melanogaster lateral ventral clock neurons. J. Neurosci. 28, 6493-6501.
13. Cardnell, R. J. G., Nogare, D. E. D., Ganetzky, B., and Stern, M. (2006). In vivo analysis of a gain-offunction mutation in the Drosophila eag-encoded K--channel. Genetics 172, 2351-2358.
14. Cirelli, C., Bushey, D., Hill, S., Huber, R., Kreber, R., Ganetzky, B., and Tononi, G. (2005). Reduced sleep in Drosophila Shaker mutants. Nature 434, 1087-1092.
15. Clyne, J. D., and Miesenböck, G. (2008). Sex-specific control and tuning of the pattern generator for courtship song in Drosophila. Cell 133, 354-363.
16. Davis, G. W. (2006). Homeostatic control of neural activity: from phenomenology to molecular design. Annu. Rev. Neurosci. 29, 307-323.
17. Dietzl, G., Chen, D., Schnorrer, F., Su, K. C., Barinova, Y., Fellner, M., Gasser, B., Kinsey, K., Oppel, S., Scheiblauer, S., Couto, A., Marra, V., Keleman, K., and Dickson, B. J. (2007). A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448, 151-156.
18. Donlea, G. M., Ramanan, R., and Shaw, P. J. (2009). Use-dependent plasticity in clock neurons regulates sleep need in Drosophila. Science 324, 105-108.
19. Duch, C., Vonhoff, F., and Ryglewski, S. (2008). Dendrite elongation and dendritic branching are affected are affected separately by different forms of intrinsic motorneuron excitability. J. Neurophysiol. 100, 2525-2536.
20. Fortin, D. L., Banghart, M. R., Dunn, T. W., Borges, K., Wagenaar, D. A., Gaudry, Q., Karakossian, M. H., Otis, T. S., Kristan, W. B., Trauner, D., and Kramer, R. H., (2008). Photochemical control of endogenous ion channels and cellular excitability. Nat. Methods 5, 331-338.
21. Gasque, G., Labarca, P., Delgado, R., and Darszon, A. (2006). Bridging behaviour and physiology: ion-channel perspective on mushroom bodydependent olfactory learning and memory in Drosophila. J. Cell. Physiol. 209, 1046-1053.
22. Giese, K. P., Peters, M., and Vernon, J. (2001). Modulation of excitability as a learning and memory mechanism: a molecular genetic perspective. Physiol. Behav. 73, 803-810.
23. Gilestro, G. F., Tononi, G., and Cirelli, C. (2009). Widespread changes in synaptic markers as a function of sleep and wakefulness in Drosophila. Science 324, 109-112.
24. Gisselmann, G., Sewing, S., Madsen, B. W., Mallart, A., Angaut-Petit, D., Müller-Holtkamp, F., Ferrus, A., and Pongs, O. (1989). The interference of truncated with normal potassium channel subunits leads to abnormal behaviour in transgenic Drosophila melanogaster. EMBO J. 8, 2359-2364.
25. Gordon, M. D., and Scott, K. (2009). Motor control in a Drosophila taste circuit. Neuron 61, 373-384.
26. Gosgnach, S., Lanuza, G. M., Butt, S. J., Saueressig, H., Zhang, Y., Velasquez, T., Riethmacher, D., Callaway, E. M., Kiehn, O., and Goulding, M. (2008). V1 spinal neurons regulate the speed of vertebrate locomotor outputs. Nature 440, 215-219.
27. Griffith, L. C., Wang, J., Zhong, Y., Wu, C.-F., and Greenspan, R. J. (1994). Calcium/calmodulin dependent kinase II and potassium channel subunit eag similarly affect plasticity in Drosophila. Proc. Natl. Acad. Sci. U.S.A. 91, 10044-10048.
28. Guan, Z., Saraswati, S., Adolfsen, B., and Littleton, J. T., (2005). Genomewide transcriptional changes associated with enhanced activity in the Drosophila nervous system. Neuron 48, 91-107.
29. Haghighi, A. P., McCabe, B. D., Fetter, R. D., Palmer, J. E., Hom, S., and Goodman, C. S. (2003). Retrograde control of synaptic transmission by postsynaptic CaMKII at the Drosophila Neuromuscular Junction. Neuron 39, 255-267.
30. Hall, J. C. (2005). Systems approaches to biological rhythms in Drosophila. Meth. Enzymol. 393, 61-185.
31. Haugland, F. N., and Wu, C.-F. (1990). A voltage-clamp analysis of genedosage effects of the Shaker locus on larval muscle potassium currents in Drosophila. J. Neurosci. 10, 1357-1371.
32. Herlitze, S., and Landmesser, L. T. (2007). New optical tools for controlling neuronal activity. Curr. Opin. Neurobiol. 17, 87-94.
33. Hodge, J. J. L., Choi, J. C., O'Kane, C. J., and Griffith, L. C. (2005). Shaw potassium channel genes in Drosophila. J. Neurobiol. 63, 235-254.
34. Hodge, J. J. L., Mullasseril, P., and Griffith, L. C. (2006). Activitydependent gating of CaMKII autonomous activity by Drosophila CASK. Neuron 51, 327-337.
35. Hodge, J. J. L., and Stanewsky, R. (2008). Function of the Shaw potassium channel within the Drosophila circadian clock. PLoS ONE 3, e2274. doi: 10.1371/journal.pone.0002274.
36. Holmes, T. C., Sheeba, V., Mizrak, D., Rubovszky, B., and Dahdal, D. (2007). Circuit-breaking and behavioural analysis by molecular genetic manipulation of neural activity in Drosophila. In Invertebrate Neurobiology, G. North and R. J. Greenspan, eds (CSHL Press, New York), pp. 19-52.
37. Hsueh, Y.-P. (2006). The role of the MAGUK protein CASK in neural development and synaptic function. Curr. Med. Chem. 13, 1915-1927.
38. Itri, J. N., Michel, S., Vansteensel, M. J., Meijer, J. H., and Colwell, C. S. (2005). Fast delayed rectifier potassium channel is required for circadian neural activity. Nat. Neurosci. 8, 650-656.
39. Johns, D. C., Marx, R., Mains, R. E., O'Rouke B., and Marbán, E. (1999). Inducible genetic suppression of neuronal excitability. J. Neurosci. 19, 1691-1697.
40. Joiner, W. J., Crocker, A., White, B. H., and Sehgal, A. (2006). Sleep in Drosophila is regulated by adult mushroom bodies. Nature 441, 757-760.
41. Kaczmarek, L. K. (2006). Non-conducting functions of voltage-gated ion channels. Nat. Rev. Neurosci. 7, 761-771.
42. Kim, S. K., and Rulifson, E. J. (2004). Conserved mechanism of glucose sensing and regulation by Drosophila corpora cardiaca cells. Nature 431, 316-320.
43. Kuhlman, S. J., and McMahon, D. G. (2004). Rhythmic regulation of membrane potential and potassium current persists in SCN neurons in the absence of environmental input. Eur. J. Neurosci. 20, 1113-1117.
44. Lear, B. C., Lin, J.-M., Keath, J. R., McGill, J. J., Raman, I. M., and Allada, R. (2005). The ion channel narrow abdomen is critical for neural output of the Drosophila circadian pacemaker. Neuron 48, 965-976.
45. Lima, S. Q., and Miesenböck, G. (2005). Remote control of behavior through genetically targeted photostimulation of neurons. Cell 121, 141-152.
46. Littleton, J. T., and Ganetzky, B. (2000). Ion channels and synaptic organization: analysis of the Drosophila genome. Neuron 26, 35-43.
47. Liu, X., Krause, W. C., and Davis, R. L. (2007). GABAA receptor RDL inhibits Drosophila olfactory associative learning. Neuron 56, 1090-1102.
48. 2+ CaMresponsive pool of CaMKII by scaffold-dependent autophosphorylation. Neuron 40, 1185-1197.
49. Luan, H., Lemon, W. C., Peabody, N. C., Pohl, J. B., Zelensky, P. K., Wang, D., Nitabach, M. N., Holmes, T. C., and White, B. H. (2006). Functional dissection of a neuronal network required for cuticle tanning and wing expansion. J. Neurosci. 26, 573-584.
50. MacClean, J. N., Zhang, Y., Johnson, B. R., and Harris-Warrick, R. M. (2003). Activity-independent homeostasis in rhythmically active neurons. Neuron 37, 109-120.
51. Mackay, T. F. C., and Anholt, R. H. (2006). Of flies and man: Drosophila as a model for Human complex traits. Annu. Rev. Genomics Hum. Genet. 7, 339-367.
52. Marder, E. (2002). Non-mammalian models for studying neural development and function. Nature 417, 318-321.
53. Marder, E., and Prinz, A. A. (2002). Modeling stability in neuron and network function: the role of activity in homeostasis. Bioessays 24, 1145-1154.
54. Markstein, M., Pitsouli, C., Villalta, C., Celniker, S. E., and Perrimon, N. (2008). Exploiting position effects and the gypsy retrovirus insulator to engineer precisely expressed transgenes. Nature Genet. 40, 476-484.
55. McGuire, S. E., Roman, G., and Davis, R. L. (2004). Gene expression systems in Drosophila: a synthesis of time and space. Trends Genet. 20, 384-391.
56. Morice, E., Andreae, L. C., Cooke, S. F., Vanes, L., Fisher, E. M. C., Tybulewicz, V. L. J., and Bliss, T. V. P. (2008). Preservation of long-term memory and synaptic plasticity despite short-term impairments in the Tc1 mouse model of Down Syndrome. Learn. Mem. 15, 492-500.
57. Mosca, T. J., Carrillo, R. A., White, B. H., and Keshishian, H. (2005). Dissection of synaptic excitability phenotypes by using dominant negative Shaker K channel subunit. Proc. Natl. Acad. Sci. U.S.A. 102, 3477-3482.
58. Nadeau, H., McKinney, S., Anderson, D. J., and Lester, H. A. (2000). ROMK1 (Kir1.1) causes apoptosis and chronic silencing of hippocampal neurons. J. Neurophysiol. 84, 1062-1075.
59. Nelson, A. B., Gittis, A. H., and du Lac, S. (2005). Decreases in CaMKII activity trigger persistent potentiation of intrinsic excitability in spontaneously firing vestibular neurons. Neuron 46, 623-631.
60. Nelson, S. B., and Turrigiano, G. G. (2008). Strength through diversity. Neuron 60, 477-482.
61. Nitabach, M. N., Blau, J., and Holmes, T. C. (2002). Electrical silencing of Drosophila pacemaker neurons stops the free-running circadian clock. Cell 109, 485-495.
62. Nitabach, M. N., Sheeba, V., Vera, D. A., Blau, J., and Holmes, T. C. (2005). Membrane electrical silencing is necessary for the free-running larval Drosophila circadian clock. J. Neurobiol. 62, 1-13.
63. Nitabach, M. N., Wu, Y., Sheeba, V., Lemon, W. C., Strumbos, J., Zelensky, P. K., Benjamin, B. H., and Holmes, T. C. (2006). Electrical hyperexcitation of lateral ventral pacemaker neurons desynchronizes downstream circadian oscillators in the fly circadian circuit and induces multiple behavioural periods. J. Neurosci. 26, 479-489.
64. Osterwalder, T., Yoon, K. S., White, B. H., and Keshishian, H. (2001). A conditional tissue-specific transgene expression system using inducible Gal4. Proc. Natl. Acad. Sci. U.S.A. 98, 12596-12601.
65. Paradis, S., Sweeney, S. T., and Davis, G. W. (2001). Homeostatic control of presynaptic release is triggered by postsynaptic membrane depolarization. Neuron 30, 737-749.
66. Parisky, K. M., Agosto, J., Pulver, S. R., Shang, Y., Kuklin, E., Hodge, J. J., Kang, K., Liu, X., Garrity, P. A., Hodge Channels to inactivate Drosophila neurons Rosbash, M., and Griffith, L. C. (2008). PDF cells are a GABA-responsive wake-promoting component of the Drosophila sleep circuit. Neuron 60, 672-682.
67. Park, D., Coleman, M. J., Hodge, J. J. L., Budnik, V., and Griffith, L. C. (2001). Regulation of neuronal excitability in Drosophila by constitutively active CaMKII. J. Neurobiol. 52, 24-42.
68. Park, D., and Griffith, L. C. (2005). Electrophysiological and anatomical characterization of PDF-positive clock neurons in the intact adult Drosophila brain. J. Neurophysiol. 95, 3955-3960.
69. Peabody, N. C., Diao, F., Luan, H., Wang, H., Dewey, E. M., Honegger, H. W., and White, B. H. (2008). Bursicon functions within the Drosophila CNS to modulate wing expansion, behaviour, hormone, secretion, and cell death. J. Neurosci. 28, 14379-14391.
70. Peabody, N. C., Pohl, J. B., Diao, F., Vreede, A. P., Sandstrom, D. J., Wang, H., Zelensky, P. K., and White, B. H. (2009). Characterization of the decision network for wing expansion in Drosophila using targeted expression of the TRPM8 channel. J. Neurosci. 29, 3343-3353.
71. Prinz, A. A., Abbott, L. F., and Marder, E. (2004). The dynamic clamp comes of age. Trends Neurosci. 27, 218-224.
72. Pulver, S., Pashkovski, S. L., Hornstein, N. J., Garrity, P. A., and Griffith, L. C. (2009). Temporal dynamics of neuronal activation by Channelrhodopsin-2 and TRPA1 determine behavioural output in Drosophila larvae. J. Neurophysiol. 101, 3075-3088.
73. Reenan, R., Kreber, R., and Ganetzky, B. (1995). Mutations of the para sodium channel gene in Drosophila conferring a range of phenotypes. Dros. Res. Conf. 36, 345A.
74. Rohrbough, J., O'Dowd, D. K., Baines, R. A., and Broadie, K. (2003). Cellular bases of behavioural plasticity: establishing and modifying synaptic circuits in the Drosophila genetic system. J. Neurobiol. 54, 254-271.
75. Rosenweig, M., Brennan, K. M., Tayler, T. D., Phelps, P. O. Patapoutian, A., and Garrity, P. A. (2005). The Drosophila ortholog of vertebrate TRPA1 regulates thermotaxis. Genes Dev. 19, 419-424.
76. Roy, B., Singh, A. J., Shetty, C., Chaudhary, V., North, A., Landgraf, M., VijayRaghavan, K., and Rodrigues, V. (2007). Metamorphosis of an identified serotonergic neuron in the Drosophila olfactory system. Neural. Dev. 2, 20.
77. + channels conserved in flies, mice and humans. Trends Neurosci. 15, 161-166.
78. Saper, C. B., Scammell, T. E., and Lu, J. (2005). Hypothalamic regulation of sleep and circadian rhythms. Nature 437, 1257-1263.
79. Schmid, A., Hallermann, S., Kittel, R. J., Khorramshahi, O., Frölich, A. M. J., Quentin, C., Rasse, T. M., Mertel, S., Heckmann, M., and Sigrist, S. J. (2008). Activity-dependent site-specific changes of glutamate receptor composition in vivo. Nat. Neurosci. 11, 659-666.
80. Schroll, C., Riemensperger, T., Bucher, D., Ehmer, J., Völler, T., Erbguth, K., Gerber B., Hendel, T., Nagel, G., Buchner, E., and Fiala, A. (2006). Light-induced activation of distinct modulatory neurons triggers appetitive or aversive learning in Drosophila learning. Curr. Biol. 16, 1741-1747.
81. Shang, Y., Griffith, L. C., and Rosbash, M. (2008). Light-arousal and circadian photoreception circuits intersect at the large PDF cells of the Drosophila brain. Proc. Natl. Acad. Sci. U.S.A. 105, 19587-19594.
82. Sheeba, V., Gu, H., Sharma, V. K., O'Dowd, D. K., and Holmes, T. C. (2008a). Circadian-and lightdependent regulation of resting membrane potential firing of Drosophila circadian pacemaker neurons. J. Neurophysiol. 99, 976-988.
83. Sheeba, V., Sharma, V. K., Gu, H., Chou, Y.-T., O'Dowd, D. K., and Holmes, T. C. (2008b). Pigment dispersing factor-dependent and independent circadian locomotor behavioural rhythms. J. Neurosci. 28, 217-227.
84. Sjulson, L., and Miesenböck, G. (2008). Photocontrol of neural activity: biophysical mechanisms and performance in vivo. Chem. Rev. 108, 1588-1602.
85. Smith, L. A., Peixoto, A. A., Kramer, E. M., Villella, A., and Hall, J. C. (1998). Courtship and visual defects of cacophony mutants reveal functional complexity of calcium-channel c1 subunit in Drosophila. Genetics 149, 1407-1426.
86. Song, J., and Tanouye, M. A. (2008). From bench to drug: human seizure modelling using Drosophila. Prog. Neurobiol. 84, 182-191.
87. Sun, X.-X., Hodge, J. J. L., Zhou, Y., Nguyen, M., and Griffith, L. C. (2004). The eag potassium channel binds and locally activates calcium/ calmodulindependent protein kinase. J. Biol. Chem. 279, 10206-10214.
88. Suzuki, N., and Wu, C.-F. (1984). Altered sensitivity to sodium channel-specific neurotoxins in cultured neurons from temperature-sensitive paralytic mutants of Drosophila. J. Neurogenet. 1, 225-238.
89. Tsunoda, S., and Salkoff, L. (1995). Genetic analysis of Drosophila neurons: Shab, Shal, and Shaw encode most embryonic potassium currents. J. Neurosci. 15, 1741-1754.
90. Turrigiano, G. G. (2008). The self-tuning neuron: synaptic scaling of excitatory synapses. Cell 135, 422-435.
91. Vähäsöyrinki, M., Niven, J. E., Hardie, R. C., Weckström, M., and Juusola, M. (2006). Robustness of neural coding in Drosophila photoreceptors in the absence of the slow delayed rectifier Krrchannels. J. Neurosci. 26, 2652-2660.
92. van Swinderen, B., and Greenspan, R. J. (2005). Flexibility in a gene network affecting a simple behaviour in Drosophila. Genetics 169, 2151-2163.
93. White, B. H., Osterwalder, T. P., Yoon, K. S., Joiner, W. J., Whim, M. D., Kaczmarek, L. K., and Keshishian, H. (2001a). Targeted attenuation of electrical activity in Drosophila using a genetically modified Kaachannel. Neuron 31, 699-711.
94. White, B. H., Osterwalder, T. P., and Keshishian, H. (2001b). Molecular genetic approaches to the targeted suppression of neuronal activity. Curr. Biol. 31, 699-711.
95. Wicher, D., Walther, C., and Wicher, C. (2001). Non-synaptic ion channels in insects-basic properties of currents and their modulation in neurons and skeletal muscles. Prog. Neurobiol. 64, 431-525.
96. 2+ currents in identified motorneurons in situ. J. Neurophysiol. 100, 868-878.
97. Wu, C. L., Xia, S., Fu, T.-F., Wang, H., Chen, Y.-H., Leong, D., Chaing, A.-S., and Tully, T. (2007). Specific requirement of NMDA receptors for longterm memory consolidation in Drosophila ellipsoid bodies. Nat. Neurosci. 10, 1578-1586.
98. Wu, Y., Cao, G., and Nitabach, M. N. (2008a). Electrical silencing of PDF neurons advances the phase of non-PDF clock neurons in Drosophila. J. Biol. Rhythms 23, 117-128.
99. Wu, Y., Cao, G., Pavlicek, B., Luo, X., and Nitabach, M. N. (2008b). Phase coupling of a circadian neuropeptide with rest/activity rhythms detected using a membrane-tethered spider toxin. PLoS Biol. 6, e273. doi: 10.1371/journal. pbio.0060273.
100. Wulff, P., Goetz, T., Leppä, E., Linden, A.-M., Renzi, M., Swinny, J. D., Vekovischeva, O. Y., Sieghart, W., Somogyi, P., Korpi, E. R., Farrant, M., and Wisden, W. (2007). From synapse to behaviour: rapid modulation of defined neuronal types with engineered GABAA receptors. Nat. Neurosci. 10, 923-929.
101. Wulff, P., and Wisden, W. (2005). Dissecting neural circuitry by combining genetics and pharmacology. Trends Neurosci. 28, 44-50.
102. Yang, C.-H., Rumpf, S., Xiang, Y., Gordon, M. D., Song, W., Jan, L.-Y., and Jan, Y.-N. (2009). Control of the postmating behavioural switch in Drosophila females by internal sensory neurons. Neuron 61, 519-526.
103. Yao, W.-D., and Wu, C.-F. (2001). Distinct roles of CaMKII and PKA in regulation of firing patterns and Koocurrents in Drosophila neurons. J. Neurophysiol. 85, 1384-1394.
104. Yu, C. R., Power, J., Barnea, G., O'Donnell, S., Brown, H. E. V., Osborne, J., Axel, R., and Gogos, J. A., (2004). Spontaneous neural activity is required for the establishment and maintenance of the olfactory sensory map. Neuron 42, 553-566.
105. Zemelman, B. V., Lee, G. A., Ng, M., and Miesenböck, G. (2002). Selective photostimulation of genetically charged neurons. Neuron 33, 15-22.
106. Zhang, F., Aravanis, A. M., Adamantidis, A., de Lecea, L. D., and Deisseroth, K. (2007). Circuit-breakers: optical technologies for probing neural signals and systems. Nat. Rev. Neurosci. 8, 577-581.
107. Zhang, Y., Narayan, S., Geiman, E., Lanuza, G. M., Velasquez, T., Shanks, B., Akay, T., Dyck, J., Pearson, K., Gosgnach, S., Fan, C. M., and Goulding, M. (2008). V3 spinal neurons establish a robust and balanced locomotor rhythm during walking. Neuron 60, 84-96.
108. Zimmermann, G., Wang, L.-P., Vaughan, A. G., Manoli, D. S., Zhang, F., Deisseroth, K., Baker, B. S., and Scott, M. P. (2009). Manipulation of an innate escape response in Drosophila: photoexcitation of acj6 neurons induces the escape response. PLoS ONE 4, e5100. doi: 10.1371/journal. pone.0005100.