Visualizing neuromodulation in vivo: TANGO-mapping of dopamine signaling reveals appetite control of sugar sensing

Cell

Volumn 148, Issue 3, 2012, Pages 583-595

  Inagaki, Hidehiko K ^a   Ben Tabou De Leon, Shlomo ^a   Wong, Allan M ^a   Jagadish, Smitha ^c   Ishimoto, Hiroshi ^b   Barnea, Gilad ^d   Kitamoto, Toshihiro ^b   Axel, Richard ^a,c   Anderson, David J ^a  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^b UNIVERSITY OF IOWA   (United States)

^c College of Physicians and Surgeons ^*  (United States)

^d BROWN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOPAMINE; SUCROSE;

ANIMAL EXPERIMENT; APPETITE; ARTICLE; CALCIUM TRANSPORT; CONTROLLED STUDY; DOPAMINE RELEASE; DROSOPHILA; FEMALE; GENE EXPRESSION; GUSTATORY SYSTEM; IN VITRO STUDY; IN VIVO STUDY; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; SENSORY NERVE CELL; SIGNAL TRANSDUCTION; STARVATION;

EID: 84863393497     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2011.12.022     Document Type: Article

References (82)

1. R.J. Bainton, L.T. Tsai, C.M. Singh, M.S. Moore, W.S. Neckameyer, and U. Heberlein Dopamine modulates acute responses to cocaine, nicotine and ethanol in Drosophila Curr. Biol. 10 2000 187 194 (Pubitemid 30146783)
2. G. Barnea, W. Strapps, G. Herrada, Y. Berman, J. Ong, B. Kloss, R. Axel, and K.J. Lee The genetic design of signaling cascades to record receptor activation Proc. Natl. Acad. Sci. USA 105 2008 64 69
3. H. Benveniste, and P.C. Hüttemeier Microdialysis - theory and application Prog. Neurobiol. 35 1990 195 215 (Pubitemid 20270228)
4. K.C. Berridge Modulation of taste affect by hunger, caloric satiety, and sensory-specific satiety in the rat Appetite 16 1991 103 120
5. A. Bhattacharya, G.G. Gu, and S. Singh Modulation of dihydropyridine- sensitive calcium channels in Drosophila by a cAMP-mediated pathway J. Neurobiol. 39 1999 491 500 (Pubitemid 29260770)
6. G. Bicker, and R. Menzel Chemical codes for the control of behaviour in arthropods Nature 337 1989 33 39 (Pubitemid 19022549)
7. J.T. Birmingham, and D.L. Tauck Neuromodulation in invertebrate sensory systems: from biophysics to behavior J. Exp. Biol. 206 2003 3541 3546 (Pubitemid 37343058)
8. G.L. Brookhart, R.S. Edgecomb, and L.L. Murdock Amphetamine and reserpine deplete brain biogenic amines and alter blow fly feeding behavior J. Neurochem. 48 1987 1307 1315 (Pubitemid 18001358)
9. M.E. Chiappe, J.D. Seelig, M.B. Reiser, and V. Jayaraman Walking modulates speed sensitivity in Drosophila motion vision Curr. Biol. 20 2010 1470 1475
10. A. Crocker, M. Shahidullah, I.B. Levitan, and A. Sehgal Identification of a neural circuit that underlies the effects of octopamine on sleep:wake behavior Neuron 65 2010 670 681
11. A. Dahanukar, Y.T. Lei, J.Y. Kwon, and J.R. Carlson Two Gr genes underlie sugar reception in Drosophila Neuron 56 2007 503 516 (Pubitemid 350026272)
12. V.G. Dethier The Hungry Fly: A Physiological Study of the Behavior Associated with Feeding 1976 Harvard University Press Cambridge, MA
13. R. Dubner The effect of behavioral state on the sensory processing of nociceptive and non-nociceptive information Prog. Brain Res. 77 1988 213 228
14. F. Friggi-Grelin, H. Coulom, M. Meller, D. Gomez, J. Hirsh, and S. Birman Targeted gene expression in Drosophila dopaminergic cells using regulatory sequences from tyrosine hydroxylase J. Neurobiol. 54 2003 618 627 (Pubitemid 36232667)
15. R. Gillette, R.C. Huang, N. Hatcher, and L.L. Moroz Cost-benefit analysis potential in feeding behavior of a predatory snail by integration of hunger, taste, and pain Proc. Natl. Acad. Sci. USA 97 2000 3585 3590 (Pubitemid 30183346)
16. M.D. Gordon, and K. Scott Motor control in a Drosophila taste circuit Neuron 61 2009 373 384
17. F. Gotzes, S. Balfanz, and A. Baumann Primary structure and functional characterization of a Drosophila dopamine receptor with high homology to human D1/5 receptors Receptors Channels 2 1994 131 141 (Pubitemid 24262700)
18. F.N. Hamada, M. Rosenzweig, K. Kang, S.R. Pulver, A. Ghezzi, T.J. Jegla, and P.A. Garrity An internal thermal sensor controlling temperature preference in Drosophila Nature 454 2008 217 220 (Pubitemid 351969888)
19. K.A. Han, N.S. Millar, M.S. Grotewiel, and R.L. Davis DAMB, a novel dopamine receptor expressed specifically in Drosophila mushroom bodies Neuron 16 1996 1127 1135 (Pubitemid 26227234)
20. R.M. Harris-Warrick, and E. Marder Modulation of neural networks for behavior Annu. Rev. Neurosci. 14 1991 39 57
21. M.G. Hearn, Y. Ren, E.W. McBride, I. Reveillaud, M. Beinborn, and A.S. Kopin A Drosophila dopamine 2-like receptor: Molecular characterization and identification of multiple alternatively spliced variants Proc. Natl. Acad. Sci. USA 99 2002 14554 14559 (Pubitemid 35257709)
22. L.M. Hurley, D.M. Devilbiss, and B.D. Waterhouse A matter of focus: monoaminergic modulation of stimulus coding in mammalian sensory networks Curr. Opin. Neurobiol. 14 2004 488 495 (Pubitemid 39089088)
23. E.C. Kong, K. Woo, H. Li, T. Lebestky, N. Mayer, M.R. Sniffen, U. Heberlein, R.J. Bainton, J. Hirsh, and F.W. Wolf 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 2010 e9954
24. M.J. Krashes, S. DasGupta, A. Vreede, B. White, J.D. Armstrong, and S. Waddell A neural circuit mechanism integrating motivational state with memory expression in Drosophila Cell 139 2009 416 427
25. T. Lebestky, J.S. Chang, H. Dankert, L. Zelnik, Y.C. Kim, K.A. Han, F.W. Wolf, P. Perona, and D.J. Anderson Two different forms of arousal in Drosophila are oppositely regulated by the dopamine D1 receptor ortholog DopR via distinct neural circuits Neuron 64 2009 522 536
26. G. Lee, and J.H. Park Hemolymph sugar homeostasis and starvation-induced hyperactivity affected by genetic manipulations of the adipokinetic hormone-encoding gene in Drosophila melanogaster Genetics 167 2004 311 323 (Pubitemid 38736390)
27. T.F. Long, R.S. Edgecomb, and L.L. Murdock Effects of substituted phenylethylamines on blowfly feeding behavior Comp. Biochem. Physiol. C. Comp. Pharmacol. Toxicol. 83 1986 201 209 (Pubitemid 16148124)
28. G. Maimon, A.D. Straw, and M.H. Dickinson Active flight increases the gain of visual motion processing in Drosophila Nat. Neurosci. 13 2010 393 399
29. Z. Mao, and R.L. Davis Eight different types of dopaminergic neurons innervate the Drosophila mushroom body neuropil: anatomical and physiological heterogeneity Front Neural Circuits 3 2009 5
30. E. Marder, and D. Bucher Understanding circuit dynamics using the stomatogastric nervous system of lobsters and crabs Annu. Rev. Physiol. 69 2007 291 316 (Pubitemid 46457645)
31. S. Marella, W. Fischler, P. Kong, S. Asgarian, E. Rueckert, and K. Scott Imaging taste responses in the fly brain reveals a functional map of taste category and behavior Neuron 49 2006 285 295 (Pubitemid 43089644)
32. N. Meunier, Y.H. Belgacem, and J.R. Martin Regulation of feeding behaviour and locomotor activity by takeout in Drosophila J. Exp. Biol. 210 2007 1424 1434 (Pubitemid 46761999)
33. M.R. Miller, K.J. Robinson, M.D. Cleary, and C.Q. Doe TU-tagging: cell type-specific RNA isolation from intact complex tissues Nat. Methods 6 2009 439 441
34. M. Monastirioti Biogenic amine systems in the fruit fly Drosophila melanogaster Microsc. Res. Tech. 45 1999 106 121 (Pubitemid 29227672)
35. C. Montell A taste of the Drosophila gustatory receptors Curr. Opin. Neurobiol. 19 2009 345 353
36. H.R. Moskowitz, V. Kumraiah, K.N. Sharma, H.L. Jacobs, and S.D. Sharma Effects of hunger, satiety and glucose load upon taste intensity and taste hedonics Physiol. Behav. 16 1976 471 475
37. C.F. Moss, and V.G. Dethier Central nervous system regulation of finicky feeding by the blowfly Behav. Neurosci. 97 1983 541 548 (Pubitemid 13016215)
38. D.R. Nässel, and A.M. Winther Drosophila neuropeptides in regulation of physiology and behavior Prog. Neurobiol. 92 2010 42 104
39. C.M. Niell, and M.P. Stryker Modulation of visual responses by behavioral state in mouse visual cortex Neuron 65 2010 472 479
40. M.P. Nusbaum, and M.P. Beenhakker A small-systems approach to motor pattern generation Nature 417 2002 343 350 (Pubitemid 34534722)
41. T. Osterwalder, K.S. Yoon, B.H. White, and H. Keshishian A conditional tissue-specific transgene expression system using inducible GAL4 Proc. Natl. Acad. Sci. USA 98 2001 12596 12601 (Pubitemid 33019991)
42. R.E. Page Jr.; J. Erber, and M.K. Fondrk The effect of genotype on response thresholds to sucrose and foraging behavior of honey bees (Apis mellifera L.) J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 182 1998 489 500 (Pubitemid 28190207)
43. A. Pauli, F. Althoff, R.A. Oliveira, S. Heidmann, O. Schuldiner, C.F. Lehner, B.J. Dickson, and K. Nasmyth Cell-type-specific TEV protease cleavage reveals cohesin functions in Drosophila neurons Dev. Cell 14 2008 239 251 (Pubitemid 351189182)
44. D.W. Pfaff, B.L. Kieffer, and L.W. Swanson Mechanisms for the regulation of state changes in the central nervous system: an introduction Ann. N Y Acad. Sci. 1129 2008 1 7 (Pubitemid 351990299)
45. P.E. Phillips, D.L. Robinson, G.D. Stuber, R.M. Carelli, and R.M. Wightman Real-time measurements of phasic changes in extracellular dopamine concentration in freely moving rats by fast-scan cyclic voltammetry Methods Mol. Med. 79 2003 443 464
46. T. Riemensperger, G. Isabel, H. Coulom, K. Neuser, L. Seugnet, K. Kume, M. Iché-Torres, M. Cassar, R. Strauss, and T. Preat Behavioral consequences of dopamine deficiency in the Drosophila central nervous system Proc. Natl. Acad. Sci. USA 108 2011 834 839
47. C.M. Root, K.I. Ko, A. Jafari, and J.W. Wang Presynaptic facilitation by neuropeptide signaling mediates odor-driven food search Cell 145 2011 133 144
48. R. Scheiner, S. Plückhahn, B. Oney, W. Blenau, and J. Erber Behavioural pharmacology of octopamine, tyramine and dopamine in honey bees Behav. Brain Res. 136 2002 545 553 (Pubitemid 35333270)
49. R. Scheiner, M.B. Sokolowski, and J. Erber Activity of cGMP-dependent protein kinase (PKG) affects sucrose responsiveness and habituation in Drosophila melanogaster Learn. Mem. 11 2004 303 311 (Pubitemid 38697896)
50. K. Scott, R. Brady Jr.; A. Cravchik, P. Morozov, A. Rzhetsky, C. Zuker, and R. Axel A chemosensory gene family encoding candidate gustatory and olfactory receptors in Drosophila Cell 104 2001 661 673 (Pubitemid 32241017)
51. S.D. Shea, and D. Margoliash Behavioral state-dependent reconfiguration of song-related network activity and cholinergic systems J. Chem. Neuroanat. 39 2010 132 140
52. T. Shiraiwa, and J.R. Carlson Proboscis extension response (PER) assay in Drosophila J. Vis. Exp. 3 2007 193
53. D.P. Srivastava, E.J. Yu, K. Kennedy, H. Chatwin, V. Reale, M. Hamon, T. Smith, and P.D. Evans Rapid, nongenomic responses to ecdysteroids and catecholamines mediated by a novel Drosophila G-protein-coupled receptor J. Neurosci. 25 2005 6145 6155 (Pubitemid 40923481)
54. K.S. Sugamori, L.L. Demchyshyn, F. McConkey, M.A. Forte, and H.B. Niznik A primordial dopamine D1-like adenylyl cyclase-linked receptor from Drosophila melanogaster displaying poor affinity for benzazepines FEBS Lett. 362 1995 131 138
55. A.L. Szymczak, and D.A. Vignali Development of 2A peptide-based strategies in the design of multicistronic vectors Expert Opin. Biol. Ther. 5 2005 627 638 (Pubitemid 40780547)
56. S.T. Thibault, M.A. Singer, W.Y. Miyazaki, B. Milash, N.A. Dompe, C.M. Singh, R. Buchholz, M. Demsky, R. Fawcett, and H.L. Francis-Lang A complementary transposon tool kit for Drosophila melanogaster using P and piggyBac Nat. Genet. 36 2004 283 287 (Pubitemid 38282754)
57. N. Thorne, C. Chromey, S. Bray, and H. Amrein Taste perception and coding in Drosophila Curr. Biol. 14 2004 1065 1079 (Pubitemid 38791568)
58. L. Tian, S.A. Hires, T. Mao, D. Huber, M.E. Chiappe, S.H. Chalasani, L. Petreanu, J. Akerboom, S.A. McKinney, and E.R. Schreiter Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators Nat. Methods 6 2009 875 881
59. Y. Tsuno, and K. Mori Behavioral state-dependent changes in the information processing mode in the olfactory system Commun. Integr. Biol. 2 2009 362 364
60. Z. Wang, A. Singhvi, P. Kong, and K. Scott Taste representations in the Drosophila brain Cell 117 2004 981 991 (Pubitemid 38798862)
61. L.A. Weiss, A. Dahanukar, J.Y. Kwon, D. Banerjee, and J.R. Carlson The molecular and cellular basis of bitter taste in Drosophila Neuron 69 2011 258 272
62. Q. Wu, Z. Zhao, and P. Shen Regulation of aversion to noxious food by Drosophila neuropeptide Y- and insulin-like systems Nat. Neurosci. 8 2005 1350 1355 (Pubitemid 41630423)
63. F. Zhang, L.P. Wang, E.S. Boyden, and K. Deisseroth Channelrhodopsin-2 and optical control of excitable cells Nat. Methods 3 2006 785 792 (Pubitemid 44445824)
64. W. Zhang, W. Ge, and Z. Wang A toolbox for light control of Drosophila behaviors through Channelrhodopsin 2-mediated photoactivation of targeted neurons Eur. J. Neurosci. 26 2007 2405 2416 (Pubitemid 350050436)
65. Berndt, A.; Yizhar, O.; Gunaydin, L.A.; Hegemann, P.; and Deisseroth, K. (2009). Bi-stable neural state switches. Nat. Neurosci. 12, 229-234.
66. Dietzl, G.; Chen, D.; Schnorrer, F.; Su, K.C.; Barinova, Y.; Fellner, M.; Gasser, B.; Kinsey, K.; Oppel, S.; Scheiblauer, S.; et al. (2007). A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448, 151-156. (Pubitemid 47067374)
67. Donnelly, M.L.; Hughes, L.E.; Luke, G.; Mendoza, H.; ten Dam, E.; Gani, D.; and Ryan, M.D. (2001). The 'cleavage' activities of foot-and-mouth disease virus 2A site-directed mutants and naturally occurring '2A-like' sequences. J. Gen. Virol. 82, 1027-1041. (Pubitemid 32454603)
68. Friggi-Grelin, F.; Coulom, H.; Meller, M.; Gomez, D.; Hirsh, J.; and Birman, S. (2003). Targeted gene expression in Drosophila dopaminergic cells using regulatory sequences from tyrosine hydroxylase. J. Neurobiol. 54, 618-627. (Pubitemid 36232667)
69. Groth, A.C.; Fish, M.; Nusse, R.; and Calos, M.P. (2004). Construction of transgenic Drosophila by using the site-specific integrase from phage phiC31. Genetics 166, 1775-1782. (Pubitemid 38621059)
70. Hodgson, E.S.; Lettvin, J.Y.; and Roeder, K.D. (1955). Physiology of a primary chemoreceptor unit. Science 122, 417-418.
71. Lai, S.L.; and Lee, T. (2006). Genetic mosaic with dual binary transcriptional systems in Drosophila. Nat. Neurosci. 9, 703-709. (Pubitemid 44012270)
72. Li, M.Z.; and Elledge, S.J. (2007). Harnessing homologous recombination in vitro to generate recombinant DNA via SLIC. Nat. Methods 4, 251-256. (Pubitemid 46358876)
73. Lim, J.S. (1990). Two-Dimensional Signal and Image Processing (Englewood Cliffs, NJ: Prentice Hall).
74. Mank, M.; Santos, A.F.; Direnberger, S.; Mrsic-Flogel, T.D.; Hofer, S.B.; Stein, V.; Hendel, T.; Reiff, D.F.; Levelt, C.; Borst, A.; et al. (2008). A genetically encoded calcium indicator for chronic in vivo two-photon imaging. Nat. Methods 5, 805-811.
75. 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. Nat. Genet. 40, 476-483. (Pubitemid 351450875)
76. Ni, J.Q.; Markstein, M.; Binari, R.; Pfeiffer, B.; Liu, L.P.; Villalta, C.; Booker, M.; Perkins, L.; and Perrimon, N. (2008). Vector and parameters for targeted transgenic RNA interference in Drosophila melanogaster. Nat. Methods 5, 49-51.
77. 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.; et al. (2008). Tools for neuroanatomy and neurogenetics in Drosophila. Proc. Natl. Acad. Sci. USA 105, 9715-9720. (Pubitemid 352031366)
78. Pfeiffer, B.D.; Ngo, T.T.; Hibbard, K.L.; Murphy, C.; Jenett, A.; Truman, J.W.; and Rubin, G.M. (2010). Refinement of tools for targeted gene expression in Drosophila. Genetics 186, 735-755.
79. Shafer, O.T.; Kim, D.J.; Dunbar-Yaffe, R.; Nikolaev, V.O.; Lohse, M.J.; and Taghert, P.H. (2008). Widespread receptivity to neuropeptide PDF throughout the neuronal circadian clock network of Drosophila revealed by real-time cyclic AMP imaging. Neuron 58, 223-237. (Pubitemid 351539003)
80. Verkhusha, V.V.; Otsuna, H.; Awasaki, T.; Oda, H.; Tsukita, S.; and Ito, K. (2001). An enhanced mutant of red fluorescent protein DsRed for double labeling and developmental timer of neural fiber bundle formation. J. Biol. Chem. 276, 29621-29624.
81. Wan, Y.; Otsuna, H.; Chien, C.B.; and Hansen, C. (2009). An interactive visualization tool for multi-channel confocal microscopy data in neurobiology research. IEEE Trans. Vis. Comput. Graph. 15, 1489-1496.
82. Wilson, R.I.; Turner, G.C.; and Laurent, G. (2004). Transformation of olfactory representations in the Drosophila antennal lobe. Science 303, 366-370. (Pubitemid 38095775)