Functional characterization of dopamine transporter in vivo using Drosophila melanogaster behavioral assays

Frontiers in Behavioral Neuroscience

Volumn 8, Issue SEP, 2014, Pages

  Ueno, Taro ^a,b   Kume, Kazuhiko ^a,c  

^a KUMAMOTO UNIVERSITY   (Japan)

^b TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

^c NAGOYA CITY UNIVERSITY   (Japan)

Author keywords

Dopamine; Dopamine transporter; Drosophila melanogaster; Memory; Sleep; Volume transmission

Indexed keywords

EID: 84906911961     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2014.00303     Document Type: Article

References (45)

1. Andretic, R., Kim, Y. C., Jones, F. S., Han, K. A., and Greenspan, R. J. (2008). Drosophila D1 dopamine receptor mediates caffeine-induced arousal. Proc. Natl. Acad. Sci. U S A 105, 20392-20397. doi: 10. 1073/pnas. 0806776105.
2. Aso, Y., Grubel, K., Busch, S., Friedrich, A. B., Siwanowicz, I., and Tanimoto, H. (2009). The mushroom body of adult Drosophila characterized by GAL4 drivers. J. Neurogenet. 23, 156-172. doi: 10. 1080/01677060802471718.
3. Aso, Y., Siwanowicz, I., Bracker, L., Ito, K., Kitamoto, T., and Tanimoto, H. (2010). Specific dopaminergic neurons for the formation of labile aversive memory. Curr. Biol. 20, 1445-1451. doi: 10. 1016/j. cub. 2010. 06. 048.
4. Benoit-Marand, M., Jaber, M., and Gonon, F. (2000). Release and elimination of dopamine in vivo in mice lacking the dopamine transporter: functional consequences. Eur. J. Neurosci. 12, 2985-2992. doi: 10. 1046/j. 1460-9568. 2000. 00155. x.
5. Bradberry, C. W., Barrett-Larimore, R. L., Jatlow, P., and Rubino, S. R. (2000). Impact of self-administered cocaine and cocaine cues on extracellular dopamine in mesolimbic and sensorimotor striatum in rhesus monkeys. J. Neurosci. 20, 3874-3883.
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. Claridge-Chang, A., Roorda, R. D., Vrontou, E., Sjulson, L., Li, H., Hirsh, J., et al. (2009). Writing memories with light-addressable reinforcement circuitry. Cell 139, 405-415. doi: 10. 1016/j. cell. 2009. 08. 034.
8. Cragg, S. J., and Rice, M. E. (2004). DAncing past the DAT at a DA synapse. Trends Neurosci. 27, 270-277. doi: 10. 1016/j. tins. 2004. 03. 011.
9. Danbolt, N. C. (2001). Glutamate uptake. Prog. Neurobiol. 65, 1-105. doi: 10. 1016/S0301-0082(00)00067-8.
10. de Belle, J. S., and Heisenberg, M. (1994). Associative odor learning in Drosophila abolished by chemical ablation of mushroom bodies. Science 263, 692-695. doi: 10. 1126/science. 8303280.
11. Dietzl, G., Chen, D., Schnorrer, F., Su, K. C., Barinova, Y., Fellner, M., et al. (2007). A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448, 151-156. doi: 10. 1038/nature05954.
12. Donlea, J. M., Thimgan, M. S., Suzuki, Y., Gottschalk, L., and Shaw, P. J. (2011). Inducing sleep by remote control facilitates memory consolidation in Drosophila. Science 332, 1571-1576. doi: 10. 1126/science. 1202249.
13. Farrant, M., and Nusser, Z. (2005). Variations on an inhibitory theme: phasic and tonic activation of GABA(A) receptors. Nat. Rev. Neurosci. 6, 215-229. doi: 10. 1038/nrn1625.
14. Floresco, S. B., West, A. R., Ash, B., Moore, H., and Grace, A. A. (2003). Afferent modulation of dopamine neuron firing differentially regulates tonic and phasic dopamine transmission. Nat. Neurosci. 6, 968-973. doi: 10. 1038/nn1103.
15. Hendricks, J. C., Finn, S. M., Panckeri, K. A., Chavkin, J., Williams, J. A., Sehgal, A., et al. (2000). Rest in Drosophila is a sleep-like state. Neuron 25, 129-138. doi: 10. 1016/s0896-6273(00)80877-6.
16. 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. doi: 10. 1038/nature04811.
17. Kim, Y. C., Lee, H. G., and Han, K. A. (2007). D1 dopamine receptor dDA1 is required in the mushroom body neurons for aversive and appetitive learning in Drosophila. J. Neurosci. 27, 7640-7647. doi: 10. 1523/jneurosci. 1167-07. 2007.
18. Knapek, S., Sigrist, S., and Tanimoto, H. (2011). Bruchpilot, a synaptic active zone protein for anesthesia-resistant memory. J. Neurosci. 31, 3453-3458. doi: 10. 1523/JNEUROSCI. 2585-10. 2011.
19. Kong, E. C., Woo, K., Li, H., Lebestky, T., Mayer, N., Sniffen, M. R., et al. (2010). A pair of dopamine neurons target the D1-like dopamine receptor DopR in the central complex to promote ethanol-stimulated locomotion in Drosophila. PLoS One 5: e9954. doi: 10. 1371/journal. pone. 0009954.
20. Kume, K., Kume, S., Park, S. K., Hirsh, J., and Jackson, F. R. (2005). Dopamine is a regulator of arousal in the fruit fly. J. Neurosci. 25, 7377-7384. doi: 10. 1523/jneurosci. 2048-05. 2005.
21. Liu, Q., Liu, S., Kodama, L., Driscoll, M. R., and Wu, M. N. (2012b). Two dopaminergic neurons signal to the dorsal fan-shaped body to promote wakefulness in Drosophila. Curr. Biol. 22, 2114-2123. doi: 10. 1016/j. cub. 2012. 09. 008.
22. Liu, C., Placais, P. Y., Yamagata, N., Pfeiffer, B. D., Aso, Y., Friedrich, A. B., et al. (2012a). A subset of dopamine neurons signals reward for odour memory in Drosophila. Nature 488, 512-516. doi: 10. 1038/nature11304.
23. Makos, M. A., Kim, Y. C., Han, K. A., Heien, M. L., and Ewing, A. G. (2009). In vivo electrochemical measurements of exogenously applied dopamine in Drosophila melanogaster. Anal. Chem. 81, 1848-1854. doi: 10. 1021/ac802297b.
24. McGuire, S. E., Le, P. T., Osborn, A. J., Matsumoto, K., and Davis, R. L. (2003). Spatiotemporal rescue of memory dysfunction in Drosophila. Science 302, 1765-1768. doi: 10. 1126/science. 1089035.
25. Nakai, Y., Horiuchi, J., Tsuda, M., Takeo, S., Akahori, S., Matsuo, T., et al. (2011). Calcineurin and its regulator sra/DSCR1 are essential for sleep in Drosophila. J. Neurosci. 31, 12759-12766. doi: 10. 1523/JNEUROSCI. 1337-11. 2011.
26. 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. doi: 10. 1073/pnas. 221303298.
27. Park, S. K., George, R., Cai, Y., Chang, H. Y., Krantz, D. E., Friggi-Grelin, F., et al. (2006). Cell-type-specific limitation on in vivo serotonin storage following ectopic expression of the Drosophila serotonin transporter, dSERT. J. Neurobiol. 66, 452-462. doi: 10. 1002/neu. 20222.
28. Pech, U., Pooryasin, A., Birman, S., and Fiala, A. (2013). Localization of the contacts between Kenyon cells and aminergic neurons in the Drosophila melanogaster brain using SplitGFP reconstitution. J. Comp. Neurol. 521, 3992-4026. doi: 10. 1002/cne. 23388.
29. Pitman, J. L., McGill, J. J., Keegan, K. P., and Allada, R. (2006). A dynamic role for the mushroom bodies in promoting sleep in Drosophila. Nature 441, 753-756. doi: 10. 1038/nature04739.
30. Poirier, L., Shane, A., Zheng, J., and Seroude, L. (2008). Characterization of the Drosophila gene-switch system in aging studies: a cautionary tale. Aging Cell 7, 758-770. doi: 10. 1111/j. 1474-9726. 2008. 00421. x.
31. Porzgen, P., Park, S. K., Hirsh, J., Sonders, M. S., and Amara, S. G. (2001). The antidepressant-sensitive dopamine transporter in Drosophila melanogaster: a primordial carrier for catecholamines. Mol. Pharmacol. 59, 83-95. doi: 10. 1124/mol. 59. 1. 83.
32. Seal, R. P., and Amara, S. G. (1999). Excitatory amino acid transporters: a family in flux. Annu. Rev. Pharmacol. Toxicol. 39, 431-456. doi: 10. 1146/annurev. pharmtox. 39. 1. 431.
33. Shang, Y., Haynes, P., Pirez, N., Harrington, K. I., Guo, F., Pollack, J., et al. (2011). Imaging analysis of clock neurons reveals light buffers the wake-promoting effect of dopamine. Nat. Neurosci. 14, 889-895. doi: 10. 1038/nn. 2860.
34. Shao, L., Shuai, Y., Wang, J., Feng, S., Lu, B., Li, Z., et al. (2011). Schizophrenia susceptibility gene dysbindin regulates glutamatergic and dopaminergic functions via distinctive mechanisms in Drosophila. Proc. Natl. Acad. Sci. U S A 108, 18831-18836. doi: 10. 1073/pnas. 1114569108.
35. Shaw, P. J., Cirelli, C., Greenspan, R. J., and Tononi, G. (2000). Correlates of sleep and waking in Drosophila melanogaster. Science 287, 1834-1837. doi: 10. 1126/science. 287. 5459. 1834.
36. Suh, J., and Jackson, F. R. (2007). Drosophila ebony activity is required in glia for the circadian regulation of locomotor activity. Neuron 55, 435-447. doi: 10. 1016/j. neuron. 2007. 06. 038.
37. Syková, E. (2004). Extrasynaptic volume transmission and diffusion parameters of the extracellular space. Neuroscience 129, 861-876. doi: 10. 1016/j. neuroscience. 2004. 06. 077.
38. Tomita, J., Mitsuyoshi, M., Ueno, T., Aso, Y., Tanimoto, H., Nakai, Y., et al. (2011). Pan-neuronal knockdown of calcineurin reduces sleep in the fruit fly, Drosophila melanogaster. J. Neurosci. 31, 13137-13146. doi: 10. 1523/JNEUROSCI. 5860-10. 2011.
39. Tully, T., and Quinn, W. G. (1985). Classical conditioning and retention in normal and mutant Drosophila melanogaster. J. Comp. Physiol. A 157, 263-277. doi: 10. 1007/bf01350033.
40. Ueno, T., Masuda, N., Kume, S., and Kume, K. (2012a). Dopamine modulates the rest period length without perturbation of its power law distribution in Drosophila melanogaster. PLoS One 7: e32007. doi: 10. 1371/journal. pone. 0032007.
41. Ueno, T., Tomita, J., Kume, S., and Kume, K. (2012b). Dopamine modulates metabolic rate and temperature sensitivity in Drosophila melanogaster. PLoS One 7: e31513. doi: 10. 1371/journal. pone. 0031513.
42. Ueno, T., Tomita, J., Tanimoto, H., Endo, K., Ito, K., Kume, S., et al. (2012c). Identification of a dopamine pathway that regulates sleep and arousal in Drosophila. Nat. Neurosci. 15, 1516-1523. doi: 10. 1038/nn. 3238.
43. Wisor, J. P., Nishino, S., Sora, I., Uhl, G. H., Mignot, E., and Edgar, D. M. (2001). Dopaminergic role in stimulant-induced wakefulness. J. Neurosci. 21, 1787-1794.
44. Yamazaki, M., Tomita, J., Takahama, K., Ueno, T., Mitsuyoshi, M., Sakamoto, E., et al. (2012). High calorie diet augments age-associated sleep impairment in Drosophila. Biochem. Biophys. Res. Commun. 417, 812-816. doi: 10. 1016/j. bbrc. 2011. 12. 041.
45. Zhang, S., Yin, Y., Lu, H., and Guo, A. (2008). Increased dopaminergic signaling impairs aversive olfactory memory retention in Drosophila. Biochem. Biophys. Res. Commun. 370, 82-86. doi: 10. 1016/j. bbrc. 2008. 03. 015.