The expanding reach of the GAL4/UAS system into the behavioral neurobiology of Drosophila

BMB Reports

Volumn 42, Issue 11, 2009, Pages 705-712

  Jones, Walton D ^a  

^a Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

Author keywords

Behavior; Drosophila; GAL4 UAS; Neurobiology; Techniques

Indexed keywords

DROSOPHILA PROTEIN;

ANIMAL; DROSOPHILA; NERVOUS SYSTEM FUNCTION; PHYSIOLOGY; REVIEW;

ANIMALS; DROSOPHILA; DROSOPHILA PROTEINS; NERVOUS SYSTEM PHYSIOLOGICAL PHENOMENA;

EID: 73449119315     PISSN: 19766696     EISSN: 1976670X     Source Type: Journal    
DOI: 10.5483/BMBRep.2009.42.11.705     Document Type: Short Survey

References (69)

1. Benzer, S. (1967) Behavioral mutants of Drosophila isolated by countercurrent distribution. Proc. Natl. Acad. Sci. U.S.A. 58, 1112-1119.
2. Heisenberg, M. (1997) Genetic approaches to neuroethology. BioEssays 19, 1065-1073.
3. Pflugfelder, G. O. (1998) Genetic lesions in Drosophila behavioural mutants. Behav. Brain Res. 95, 3-15.
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. Olsen, S. R. and Wilson, R. I. (2008) Cracking neural circuits in a tiny brain: new approaches for understanding the neural circuitry of Drosophila. Trends Neurosci. 31, 512-520.
6. Luo, L., Callaway, E. M. and Svoboda, K. (2008) Genetic dissection of neural circuits. Neuron 57, 634-660.
7. 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.
8. Brand, A. H. and Dormand, E. L. (1995) The GAL4 system as a tool for unravelling the mysteries of the Drosophila nervous system. Curr. Opin. Neurobiol. 5, 572-578.
9. Ito, K., Urban, J. and Technau, G. M. (1995) Distribution, classification, and development of Drosophila glial cells in the late embryonic and early larval ventral nerve cord. Roux's Arch. Dev. Biol. 204, 284-307.
10. Yang, M. Y., Armstrong, J. D., Vilinsky, I., Strausfeld, N. J. and Kaiser, K. (1995) Subdivision of the Drosophila mushroom bodies by enhancer-trap expression patterns. Neuron 15, 45-54.
11. Pfeiffer, B. D., Jenett, A., Hammonds, A. S., Ngo, T. T., Misra, S., Murphy, C., Scully, A., Carlson, J. W., Wan, K. H., Laverty, T. R., Mungall, C., Svirskas, R., Kadonaga, J. T., Doe, C. Q., Eisen, M. B., Celniker, S. E. and Rubin, G. M. (2008) Tools for neuroanatomy and neurogenetics in Drosophila. Proc. Natl. Acad. Sci. U.S.A. 105, 9715-9720.
12. Lee, T. and Luo, L. (1999) Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22, 451-461.
13. Brand, A. (1995) GFP in Drosophila. Trends Genet 11, 324-325.
14. Williams, D. W., Tyrer, M. and Shepherd, D. (2000) Tau and tau reporters disrupt central projections of sensory neurons in Drosophila. J. Comp. Neurol. 428, 630-640.
15. Ito, K., Suzuki, K., Estes, P., Ramaswami, M., Yamamoto, D. and Strausfeld, N. J. (1998) The organization of extrinsic neurons and their implications in the functional roles of the mushroom bodies in Drosophila melanogaster Meigen. Learn Mem. 5, 52-77.
16. Fishilevich, E. and Vosshall, L. B. (2005) Genetic and functional subdivision of the Drosophila antennal lobe. Curr. Biol. 15, 1548-1553.
17. Couto, A., Alenius, M. and Dickson, B. J. (2005) Molecular, anatomical, and functional organization of the Drosophila olfactory system. Curr. Biol. 15, 1535-1547.
18. White, J., Southgate, E., Thomson, J. N. and Brenner, S. (1986) The structure of the nervous system of the nematode Caenorhabditis elegans. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 314, 1-340.
19. Macosko, E. Z., Pokala, N., Feinberg, E. H., Chalasani, S. H., Butcher, R. A., Clardy, J. and Bargmann, C. I. (2009) A hub-and-spoke circuit drives pheromone attraction and social behaviour in C. elegans. Nature 458, 1171-1175.
20. Briggman, K. L. and Denk, W. (2006) Towards neural circuit reconstruction with volume electron microscopy techniques. Curr. Opin. Neurobiol. 16, 562-570.
21. Livet, J., Weissman, T. A., Kang, H., Draft, R. W., Lu, J., Bennis, R. A., Sanes, J. R. and Lichtman, J. W. (2007) Transgenic strategies for combinatorial expression of fluorescent proteins in the nervous system. Nature 450, 56-62.
22. Lichtman, J. W., Livet, J. and Sanes, J. R. (2008) A technicolour approach to the connectome. Nat. Rev. Neurosci. 9, 417-422.
23. Stepanyants, A. and Chklovskii, D. B. (2005) Neurogeometry and potential synaptic connectivity. Trends Neurosci. 28, 387-394.
24. Ramaekers, A., Magnenat, E., Marin, E. C., Gendre, N., Jefferis, G. S., Luo, L. and Stocker, R. F. (2005) Glomerular maps without cellular redundancy at successive levels of the Drosophila larval olfactory circuit. Curr. Biol. 15, 982-992.
25. Patterson, G. H. and Lippincott-Schwartz, J. (2002) A photoactivatable GFP for selective photolabeling of proteins and cells. Science 297, 1873-1877.
26. Datta, S. R., Vasconcelos, M. L., Ruta, V., Luo, S., Wong, A., Demir, E., Flores, J., Balonze, K., Dickson, B. J. and Axel, R. (2008) The Drosophila pheromone cVA activates a sexually dimorphic neural circuit. Nature 452, 473-477.
27. Callaway, E. M. (2008) Transneuronal circuit tracing with neurotropic viruses. Curr. Opin. Neurobiol. 18, 617-623.
28. Yoshihara, Y., Mizuno, T., Nakahira, M., Kawasaki, M., Watanabe, Y., Kagamiyama, H., Jishage, K., Ueda, O., Suzuki, H., Tabuchi, K., Sawamoto, K., Okano, H., Noda, T. and Mori, K. (1999) A genetic approach to visualization of multisynaptic neural pathways using plant lectin transgene. Neuron 22, 33-41.
29. Tabuchi, K., Sawamoto, K., Suzuki, E., Ozaki, K., Sone, M., Hama, C., Tanifuji-Morimoto, T., Yuasa, Y., Yoshihara, Y., Nose, A. and Okano, H. (2000) GAL4/UAS-WGA system as a powerful tool for tracing Drosophila transsynaptic neural pathways. J. Neurosci. Res. 59, 94-99.
30. Tanaka, N. K., Awasaki, T., Shimada, T. and Ito, K. (2004) Integration of chemosensory pathways in the Drosophila second-order olfactory centers. Curr. Biol. 14, 449-457.
31. Gordon, M. D. and Scott, K. (2009) Motor control in a Drosophila taste circuit. Neuron 61, 373-384.
32. Feinberg, E. H., Vanhoven, M. K., Bendesky, A., Wang, G., Fetter, R. D., Shen, K. and Bargmann, C. I. (2008) GFP Reconstitution Across Synaptic Partners (GRASP) defines cell contacts and synapses in living nervous systems. Neuron 57, 353-363.
33. Lai, S. L. and Lee, T. (2006) Genetic mosaic with dual binary transcriptional systems in Drosophila. Nat. Neurosci. 9, 703-709.
34. Gouwens, N. W. and Wilson, R. I. (2009) Signal propagation in Drosophila central neurons. J. Neurosci. 29, 6239-6249.
35. Wilson, R. I., Turner, G. C. and Laurent, G. (2004) Transformation of olfactory representations in the Drosophila antennal lobe. Science 303, 366-370.
36. Wang, J. W., Wong, A. M., Flores, J., Vosshall, L. B. and Axel, R. (2003) Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain. Cell 112, 271-282.
37. Nakai, J., Ohkura, M. and Imoto, K. (2001) A high signalto-noise Ca(2+) probe composed of a single green fluorescent protein. Nat. Biotechnol. 19, 137-141.
38. Reiff, D. F., Ihring, A., Guerrero, G., Isacoff, E., Joesch, M., Nakai, J. and Borst, A. (2005) In vivo performance of genetically encoded indicators of neural activity in flies. J. Neurosci. 25, 4766-4778.
39. Jayaraman, V. and Laurent, G. (2007) Evaluating a genetically encoded optical sensor of neural activity using electrophysiology in intact adult fruit flies. Front Neural. Circuits. 1, 3.
40. Miesenböck, G., De Angelis, D. A. and Rothman, J. E. (1998) Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 394, 192-195.
41. Ng, M., Roorda, R. D., Lima, S. Q., Zemelman, B. V., Morcillo, P. and Miesenböck, G. (2002) Transmission of olfactory information between three populations of neurons in the antennal lobe of the fly. Neuron 36, 463-474.
42. Shang, Y., Claridge-Chang, A., Sjulson, L., Pypaert, M. and Miesenböck, G. (2007) Excitatory local circuits and their implications for olfactory processing in the fly antennal lobe. Cell 128, 601-612.
43. Ignell, R., Root, C. M., Birse, R. T., Wang, J. W., Nässel, D. R. and Winther, A. M. (2009) Presynaptic peptidergic modulation of olfactory receptor neurons in Drosophila. PNAS 106, 13070-13075.
44. Zemelman, B. V. and Miesenböck, G. (2001) Genetic schemes and schemata in neurophysiology. Curr. Opin. Neurobiol. 11, 409-414.
45. Kuner, T. and Augustine, G. J. (2000) A genetically encoded ratiometric indicator for chloride: capturing chloride transients in cultured hippocampal neurons. Neuron 27, 447-459.
46. Berglund, K., Schleich, W., Krieger, P., Loo, L. S., Wang, D., Cant, N. B., Feng, G., Augustine, G. J. and Kuner, T. (2006) Imaging synaptic inhibition in transgenic mice expressing the chloride indicator, Clomeleon. Brain Cell Biology 35, 207-228.
47. Siegel, M. S. and Isacoff, E. Y. (1997) A genetically en coded optical probe of membrane voltage. Neuron 19, 735-741.
48. Ataka, K. and Pieribone, V. A. (2002) A genetically targetable fluorescent probe of channel gating with rapid kinetics. Biophys. J. 82, 509-516.
49. Chanda, B., Blunck, R., Faria, L. C., Schweizer, F. E., Mody, I. and Bezanilla, F. (2005) A hybrid approach to measuring electrical activity in genetically specified neurons. Nat. Neurosci. 8, 1619-1626.
50. Sjulson, L. and Miesenböck, G. (2007) Optical recording of action potentials and other discrete physiological events: a perspective from signal detection theory. Physiology (Bethesda, Md) 22, 47-55.
51. Sjulson, L. and Miesenböck, G. (2008) Rational optimization and imaging in vivo of a genetically encoded optical voltage reporter. J. Neurosci. 28, 5582-5593.
52. McNabb, S. L., Baker, J. D., Agapite, J., Steller, H., Riddiford, L. M. and Truman, J. W. (1997) Disruption of a behavioral sequence by targeted death of peptidergic neurons in Drosophila. Neuron 19, 813-823.
53. Kunes, S. and Steller, H. (1991) Ablation of Drosophila photoreceptor cells by conditional expression of a toxin gene. Genes Dev. 5, 970-983.
54. Bellen, H. J., D'Evelyn, D., Harvey, M. and Elledge, S. J. (1992) Isolation of temperature-sensitive diphtheria toxins in yeast and their effects on Drosophila cells. Development 114, 787-796.
55. Johns, D. C., Marx, R., Mains, R. E., O'Rourke, B. and Marbán, E. (1999) Inducible genetic suppression of neuronal excitability. J. Neurosci. 19, 1691-1697.
56. 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.
57. Sweeney, S. T., Broadie, K., Keane, J., Niemann, H. and O'Kane, C. J. (1995) Targeted expression of tetanus toxin light chain in Drosophila specifically eliminates synaptic transmission and causes behavioral defects. Neuron 14, 341-351.
58. Kamikouchi, A., Inagaki, H. K., Effertz, T., Hendrich, O., Fiala, A., Göpfert, M. C. and Ito, K. (2009) The neural basis of Drosophila gravity-sensing and hearing. Nature 458, 165-171.
59. Kitamoto, T. (2001) Conditional modification of behavior in Drosophila by targeted expression of a temperaturesensitive shibire allele in defined neurons. J. Neurobiol. 47, 81-92.
60. Suh, G. S., Wong, A. M., Hergarden, A. C., Wang, J. W., Simon, A. F., Benzer, S., Axel, R. and Anderson, D. J. (2004) A single population of olfactory sensory neurons mediates an innate avoidance behaviour in Drosophila. Nature 431, 854-859.
61. Nitabach, M. N., Wu, Y., Sheeba, V., Lemon, W. C., Strumbos, J., Zelensky, P. K., White, 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 behavioral periods. J. Neurosci. 26, 479-489.
62. Al-Anzi, B., Sapin, V., Waters, C., Zinn, K., Wyman, R. J. and Benzer, S. (2009) Obesity-blocking neurons in Drosophila. Neuron 63, 329-341.
63. Marella, S., Fischler, W., Kong, P., Asgarian, S., Rueckert, E. and Scott, K. (2006) Imaging taste responses in the fly brain reveals a functional map of taste category and behavior. Neuron 49, 285-295.
64. Lima, S. Q. and Miesenböck, G. (2005) Remote control of behavior through genetically targeted photostimulation of neurons. Cell 121, 141-152.
65. 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.
66. Zhang, W., Ge, W. and Wang, Z. (2007) A toolbox for light control of Drosophila behaviors through Channelrhodopsin 2-mediated photoactivation of targeted neurons. Eur. J. Neurosci. 26, 2405-2416.
67. 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 larvae. Curr. Biol. 16, 1741-1747.
68. Suh, G. S., Ben-Tabou de Leon, S., Tanimoto, H., Fiala, A., Benzer, S. and Anderson, D. J. (2007) Light activation of an innate olfactory avoidance response in Drosophila. Curr. Biol. 17, 905-908.
69. Hwang, R. Y., Zhong, L., Xu, Y., Johnson, T., Zhang, F., Deisseroth, K. and Tracey, W. D. (2007) Nociceptive neurons protect Drosophila larvae from parasitoid wasps. Curr. Biol. 17, 2105-2116.