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Overexpression of the Drosophila vesicular monoamine transporter increases motor activity and courtship but decreases the behavioral response to cocaine

Molecular Psychiatry volume 11, pages 99–113 (2006)Cite this article

Abstract

Aminergic signaling pathways have been implicated in a variety of neuropsychiatric illnesses, but the mechanisms by which these pathways influence complex behavior remain obscure. Vesicular monoamine transporters (VMATs) have been shown to regulate the amount of monoamine neurotransmitter that is stored and released from synaptic vesicles in mammalian systems, and an increase in their expression has been observed in bipolar patients. The model organism Drosophila melanogaster provides a powerful, but underutilized genetic system for studying how dopamine (DA) and serotonin (5HT) may influence behavior. We show that a Drosophila isoform of VMAT (DVMAT-A) is expressed in both dopaminergic and serotonergic neurons in the adult Drosophila brain. Overexpression of DVMAT-A in these cells potentiates stereotypic grooming behaviors and locomotion and can be reversed by reserpine, which blocks DVMAT activity, and haloperidol, a DA receptor antagonist. We also observe a prolongation of courtship behavior, a decrease in successful mating and a decrease in fertility, suggesting a role for aminergic circuits in the modulation of sexual behaviors. Finally, we find that DMVAT-A overexpression decreases the fly's sensitivity to cocaine, suggesting that the synaptic machinery responsible for this behavior may be downregulated. DVMAT transgenes may be targeted to additional neuronal pathways using standard Drosophila techniques, and our results provide a novel paradigm to study the mechanisms by which monoamines regulate complex behaviors relevant to neuropsychiatric illness.

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References

  1. Corey JL, Quick MW, Davidson N, Lester HA, Guastella J . A cocaine-sensitive Drosophila serotonin transporter: cloning, expression, and electrophysiological characterization. Proc Natl Acad Sci USA 1994; 91: 1188–1192.

    PubMed  CAS  Google Scholar 

  2. Blenau W, Baumann A . Molecular and pharmacological properties of insect biogenic amine receptors: lessons from Drosophila melanogaster and Apis mellifera. Arch Insect Biochem Physiol 2001; 48: 13–38.

    PubMed  CAS  Google Scholar 

  3. Porzgen P, Park SK, Hirsh J, Sonders MS, Amara SG . The antidepressant-sensitive dopamine transporter in Drosophila: a primordial carrier for catecholamines. Mol Pharmacol 2001; 59: 83–95.

    PubMed  CAS  Google Scholar 

  4. Yellman C, Tao H, He B, Hirsh J . Conserved and sexually dimorphic behavioral responses to biogenic amines in decapitated Drosophila. Proc Natl Acad Sci USA 1997; 94: 4131–4136.

    PubMed  CAS  Google Scholar 

  5. Valles AM, White K . Serotonin-containing neurons in Drosophila melanogaster: development and distribution. J Comp Neurol 1988; 268: 400–413.

    Google Scholar 

  6. McClung C, Hirsh J . Stereotypic behavioral responses to free-base cocaine and the development of behavioral sensitization in Drosophila. Curr Biol 1998; 8: 109–112.

    PubMed  CAS  Google Scholar 

  7. McClung C, Hirsh J . The trace amine tyramine is essential for sensitization to cocaine in Drosophila. Curr Biol 1999; 9: 853–860.

    PubMed  CAS  Google Scholar 

  8. Li H, Chaney S, Forte M, Hirsch J . Ectopic G-protein expression in dopamine and serotonin neurons blocks cocaine sensitization in Drosophila melanogaster. Curr Biol 2000; 10: 211–214.

    PubMed  CAS  Google Scholar 

  9. Bainton RJ, Tsai LTY, Singh CM, Moore MS, Neckameyer WS, Heberlein U . Dopamine modulates acute responses to cocaine, nicotine and ethanol in Drosophila. Curr Biol 2000; 10: 187–194.

    PubMed  CAS  Google Scholar 

  10. Lee G, Hall JC . Abnormalities of male-specific FRU protein and serotonin expression in the CNS of fruitless mutants in Drosophila. J Neurosci 2001; 21: 513–526.

    PubMed  CAS  Google Scholar 

  11. Neckameyer WS . Dopamine modulates female sexual receptivity in Drosophila melanogaster. J Neurogenet 1998; 12: 101–114.

    PubMed  CAS  Google Scholar 

  12. Neckameyer WS . Dopamine and mushroom bodies in Drosophila: experience-dependent and -independent aspects of sexual behavior. Learn Mem 1998; 5: 157–165.

    PubMed  PubMed Central  CAS  Google Scholar 

  13. Hernandez L, Lee F, Hoebel BG . Microdialysis in the nucleus accumbens during feeding on drugs of abuse: amphetamine, cocaine and phencyclidine. Ann N.Y. Acad Sci 1988; 537: 508–511.

    Google Scholar 

  14. Carboni E, Imperato A, Perezzani L, Chiara GD . Amphetamine, cocaine, phencyclidine and nomifensine increase extracellular dopamine concentrations preferentially in the rat nucleus accumbens of freely moving rats. Neuroscience 1989; 28: 653–661.

    PubMed  CAS  Google Scholar 

  15. Imperato A, Mele A, Scrocco MG, Puglici-Allegra S . Chronic cocaine alters limbic extracellular dopamine. Neurochemical basis for addiction. Eur J Pharmacol 1992; 212: 299–300.

    PubMed  CAS  Google Scholar 

  16. Amara SG, Kuhar MJ . Neurotransmitter transporters: recent progress. Ann Rev Neurosci 1993; 16: 73–93.

    PubMed  CAS  Google Scholar 

  17. Krantz DE, Chaudhry FA, Edwards RH . Neurotransmitter transporters. In: Bellen HJ (ed.), Neurotransmitter Release. Oxford: Oxford University Press, 1999, pp 145–207.

    Google Scholar 

  18. Liu Y, Peter D, Roghani A, Schuldiner S, Prive GG, Eisenberg D et al. A cDNA that supresses MPP+ toxicity encodes a vesicular amine transporter. Cell 1992; 70: 539–551.

    PubMed  CAS  Google Scholar 

  19. Peter D, Liu Y, Sternini C, de Giorgio R, Brecha N, Edwards RH . Differential expression of two vesicular monoamine transporters. J Neurosci 1995; 15: 6179–6188.

    PubMed  CAS  Google Scholar 

  20. Fon EA, Pothos EN, Sun B-C, Kileen N, Sulzer D, Edwards RH . Vesicular transport regulates monoamine storage and release but is not essential for amphetamine action. Neuron 1997; 19: 1271–1283.

    PubMed  CAS  Google Scholar 

  21. Takahashi N, Miner LL, Sora I, Ujike H, Revay RS, Kostic V et al. VMAT2 knockout mice: heterozygotes display reduced amphetamine-conditioned reward, enhanced amphetamine locomotion, and enhanced MPTP toxicity. Proc Natl Acad Sci USA 1997; 94: 9938–9943.

    PubMed  CAS  Google Scholar 

  22. Wang Y-M, Gainetdinov RR, Fumagalli F, Xu F, Jones SR, Block CB et al. Knockout of the vesicular monoamine transporter 2 gene results in neonatal death and supersensitivity to cocaine and amphetamine. Neuron 1997; 19: 1285–1296.

    PubMed  CAS  Google Scholar 

  23. Mooslehner KA, Chan PM, Xu W, Liu L, Smadja C, Humby T et al. Mice with very low expression of the vesicular monoamine transporter 2 gene survive into adulthood: potential mouse model for parkinsonism. Mol Cell Biol 2001; 21: 5321–5331.

    PubMed  PubMed Central  CAS  Google Scholar 

  24. Pothos EN, Larsen KE, Krantz DE, Liu Y, Haycock JW, Setlik W et al. Synaptic vesicle transporter expression regulates vesicle phenotype and quantal size. J Neurosci 2000; 20: 7297–7306.

    PubMed  CAS  Google Scholar 

  25. Colliver TL, Pyott SJ, Achalabun M, Ewing AG . VMAT-Mediated changes in quantal size and vesicular volume. J Neurosci 2000; 20: 5276–5282.

    PubMed  CAS  Google Scholar 

  26. Zubieta JK, Taylor SF, Huguelet P, Koeppe RA, Kilbourn MR, Frey KA . Vesicular monoamine transporter concentrations in bipolar disorder type I, schizophrenia, and healthy subjects. Biol Psychiatry 2001; 49: 110–116.

    PubMed  CAS  Google Scholar 

  27. Zubieta JK, Huguelet P, Ohl LE, Koeppe RA, Kilbourn MR, Carr JM et al. High vesicular monoamine transporter binding in asymptomatic bipolar I disorder: sex differences and cognitive correlates. Am J Psychiatry 2000; 157: 1619–1628.

    PubMed  CAS  Google Scholar 

  28. Freis ED . Mental depression in hypertensive patients treated for long periods with high doses of reserpine. N Engl J Med 1954; 251: 1006–1008.

    PubMed  CAS  Google Scholar 

  29. Brand AH, Perrimon N . Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 1993; 118: 401–415.

    PubMed  CAS  Google Scholar 

  30. Greer CL, Grygoruk A, Patton DE, Ley B, Romero-Calderon R, Chang H-Y et al. A splice variant of the Drosophila vesicular monoamine transporter contains a conserved trafficking domain and functions in the storage of dopamine, serotonin and octopamine. J Neurobiol 2005; 64: 239–258.

    PubMed  CAS  Google Scholar 

  31. Greenspan R . Fly Pushing: The Theory and Practice of Drosophila Genetics. Plainview, NY: Cold Spring Harbor Laboratory Press, 1997.

    Google Scholar 

  32. Rubin GM, Spradling AC . Genetic transformation of Drosophila with transposable element vectors. Science 1982; 218: 348–353.

    PubMed  CAS  Google Scholar 

  33. Hay BA, Wolff T, Rubin GM . Expression of baculovirus P35 prevents cell death in Drosophila. Development 1994; 120: 2121–2129.

    PubMed  CAS  Google Scholar 

  34. Krantz DE, Waites C, Oorschot V, Liu Y, Wilson RI, Tan PK et al. A phosphorylation site regulates sorting of the vesicular acetylcholine transporter to dense core vesicles. J Cell Biol 2000; 149: 379–395.

    PubMed  PubMed Central  CAS  Google Scholar 

  35. Zipursky SL, Venkatesh TR, Teplow DB, Benzer S . Neuronal development in the Drosophila retina: monoclonal antibodies as molecular probes. Cell 1984; 36: 15–26.

    PubMed  CAS  Google Scholar 

  36. Chang HY, Ready DF . Rescue of photoreceptor degeneration in rhodopsin-null Drosophila mutants by activated Rac1. Science 2000; 290: 1978–1980.

    PubMed  CAS  Google Scholar 

  37. van de Goor J, Ramaswami M, Kelly R . Redistribution of synaptic vesicles and their proteins in temperature-sensitive shibire(ts1) mutant Drosophila. Proc Natl Acad Sci USA 1995; 92: 5739–5743.

    PubMed  CAS  Google Scholar 

  38. Daniels RW, Collins CA, Gelfand MV, Dant J, Brooks ES, Krantz DE et al. Increased expression of the Drosophila vesicular glutamate transporter leads to excess glutamate release and a compensatory decrease in quantal content. J Neurosci 2004; 24: 10466–10474.

    PubMed  CAS  Google Scholar 

  39. Monastirioti M . Biogenic amine systems in the fruit fly Drosophila melanogaster. Microscop Res Tech 1999; 45: 106–121.

    CAS  Google Scholar 

  40. Feany MB, Bender WW . A Drosophila model of Parkinson's disease. Nature 2000; 404: 394–398.

    PubMed  CAS  Google Scholar 

  41. Auluck PK, Chan HY, Trojanowski JQ, Lee VM, Bonini NM . Chaperone suppression of alpha-synuclein toxicity in a Drosophila model for Parkinson's disease. Science 2002; 295: 865–868.

    PubMed  CAS  Google Scholar 

  42. Morgan BA, Johnson WA, Hirsh J . Regulated splicing produces different forms of dopa decarboxylase in the central nervous system and hypoderm of Drosophila melanogaster. EMBO J 1986; 5: 3335–3342.

    PubMed  PubMed Central  CAS  Google Scholar 

  43. Konrad KD, Marsh JL . Developmental expression and spatial distribution of dopa decarboxylase in Drosophila. Dev Biol 1987; 122: 172–185.

    PubMed  CAS  Google Scholar 

  44. Budnik V, White K . Catecholamine containing neurons in Drosophila melanogaster: distribution and development. J Comp Neurol 1988; 268: 400–413.

    PubMed  CAS  Google Scholar 

  45. Lundell MJ, Hirsh J . Temporal and spatial development of serotonin and dopamine neurons in the Drosophila CNS. Dev Biol 1994; 165: 385–396.

    PubMed  CAS  Google Scholar 

  46. Birman S, Morgan B, Anzivino M, Hirsh J . A novel and major isoform of tyrosine hydroxylase in Drosophila is generated by alternative RNA processing. J Biol Chem 1994; 269: 26559–26567.

    PubMed  CAS  Google Scholar 

  47. Hevers W, Hardie RC . Serotonin modulates the voltage dependence of delayed rectifier and Shaker potassium channels in Drosophila photoreceptors. Neuron 1995; 14: 845–856.

    PubMed  CAS  Google Scholar 

  48. Strauss R, Heisenberg M . A higher control center of locomotor behavior in the Drosophila brain. J Neurosci 1993; 13: 1852–1861.

    PubMed  CAS  Google Scholar 

  49. Melzig J, Burg M, Gruhn M, Pak WL, Buchner E . Selective histamine uptake rescues photo- and mechanoreceptor function of histidine decarboxylase-deficicient Drosophila mutant. J Neurosci 1998; 18: 7160–7166.

    PubMed  CAS  Google Scholar 

  50. Liu Y, Edwards RH . The role of vesicular transport proteins in synaptic transmission and neural degeneration. Annu Rev Neurosci 1997b; 20: 125–156.

    PubMed  CAS  Google Scholar 

  51. Pendleton RG, Rasheed A, Hillman R . Effects of adrenergic agents on locomotor behavior and reproductive development in Drosophila. Drug Development Research 2000; 50: 142–146.

    CAS  Google Scholar 

  52. Pendleton RG, Robinson N, Roychowdhury R, Rasheed A, Hillman R . Reproduction and development in Drosophila are dependent upon catecholamines. Life Sci 1996; 59: 2083–2091.

    PubMed  CAS  Google Scholar 

  53. Pendleton RG, Parvez F, Sayed M, Hillman R . Effects of pharmacological agents upon a transgenic model of Parkinson's disease in Drosophila melanogaster. J Pharmacol Exp Ther 2002; 300: 91–96.

    PubMed  CAS  Google Scholar 

  54. Wright TR . The genetics of biogenic amine metabolism, sclerotization, and melanization in Drosophila melanogaster. Adv Genet 1987; 24: 127–222.

    PubMed  CAS  Google Scholar 

  55. Krantz DE, Peter D, Liu Y, Edwards RH . Phosphorylation of a vesicular monoamine transporter by casein kinase II. J Biol Chem 1997; 272: 6752–6759.

    PubMed  CAS  Google Scholar 

  56. Waites CL, Mehta A, Tan PK, Thomas G, Edwards RH, Krantz DE . An acidic motif retains vesicular monoamine transporter 2 on large dense core vesicles. J Cell Biol 2001; 152: 1159–1168.

    PubMed  PubMed Central  CAS  Google Scholar 

  57. Clift-O'Grady L, Linstedt AD, Lowe AW, Grote E, Kelly RB . Biogenesis of synaptic vesicle-like structures in a pheochromocytoma cell line PC12. J Cell Biol 1990; 110: 1693–1703.

    PubMed  CAS  Google Scholar 

  58. Monastirioti M, Linn CEJ, White K . Characterization of Drosophila tyramine beta-hydroxylase gene and isolation of mutant flies lacking octopamine. J Neurosci 1996; 16: 3900–3911.

    PubMed  CAS  Google Scholar 

  59. Torres G, Horowitz JM . Activating properties of cocaine and cocaethylene in a behavioral preparation of Drosophila melanogaster. Synapse 1998; 29: 148–161.

    PubMed  CAS  Google Scholar 

  60. Kalivas PW, Sorg BA, Hooks MS . The pharmacology and neural circuitry of sensitization to psychostimulants. Behav Pharmacol 1993; 4: 315–334.

    PubMed  CAS  Google Scholar 

  61. Ackerman JM, White FJ . A10 somatodendritic dopamine autoreceptor sensitivity following withdrawal from repeated cocaine treatment. Neurosci Lett 1990; 117: 181–187.

    PubMed  CAS  Google Scholar 

  62. Grace AA, Bunney BS . Electrophysiological properties of midbrain dopamine neurons. In: Bloom FE, Kupfer DJ (eds.), Psychopharmacology: The Fourth Generation of Progress. New York: Raven Press, 1995, pp 163–178.

    Google Scholar 

  63. Schmitz Y, Lee CJ, Schmauss C, Gonon F, Sulzer D . Amphetamine distorts stimulation-dependent dopamine overflow: effects on D2 autoreceptors, transporters, and synaptic vesicle stores. J Neurosci 2001; 21: 5916–5924.

    PubMed  CAS  Google Scholar 

  64. Chiodo LA, Freeman AS, Bunney BS . Dopamine autoreceptor signal transduction and regulation. In: Bloom FE, Kupfer DJ (eds.), Psychopharmacology: The Fourth Generation of Progress. New York: Rave Press, 1995.

    Google Scholar 

  65. Neckameyer WS . Multiple roles for dopamine in Drosophila development. Dev Biol 1996; 176: 209–219.

    PubMed  CAS  Google Scholar 

  66. Song H-J, Ming G-L, Fon E, Bellocchio E, Edwards RH, Poo M-M . Expression of a putative vesicular acetylcholine transporter facilitates quantal transmitter packaging. Neuron 1997; 18: 815–826.

    PubMed  CAS  Google Scholar 

  67. Wojcik SM, Rhee JS, Herzog E, Sigler A, Jahn R, Takamori S et al. An essential role for vesicular glutamate transporter 1 (VGLUT1) in postnatal development and control of quantal size. Proc Natl Acad Sci USA 2004; 101: 7158–7163.

    PubMed  CAS  Google Scholar 

  68. Watson F, Kiernan RS, Deavall DG, Varro A, Dimaline R . Transcriptional activation of the rat vesicular transporter 2 promoter in gastric epithelial cells: regulation by gastrin. J Biol Chem 2000; 276: 7661–7671.

    PubMed  Google Scholar 

  69. Brown JM, Hanson GR, Fleckenstein AE . Regulation of the vesicular monoamine transporter-2: a novel mechanism for cocaine and other psychostimulants. J Pharmacol Exp Ther 2001; 296: 762–767.

    PubMed  CAS  Google Scholar 

  70. Holtje M, Winter S, Walther D, Pahner I, Hortnagl H, Ottersen OP et al. The vesicular monoamine content regulates VMAT2 activity through Galphaq in mouse platelets. Evidence for autoregulation of vesicular transmitter uptake. J Biol Chem 2003; 278: 15850–15858.

    PubMed  Google Scholar 

  71. Pendleton RG, Rasheed A, Sardina T, Tully T, Hillman R . Effects of tyrosine hydroxylase mutants on locomotor activity in Drosophila: a study in functional genomics. Behav Genet 2002; 32: 89–94.

    PubMed  Google Scholar 

  72. Fumagalli F, Gainetdinov RR, Wang YM, Valenzano KJ, Miller GW, Caron MG . Increased methamphetamine neurotoxicity in heterozygous vesicular monoamine transporter 2 knock-out mice. J Neurosci 1999; 19: 2424–2431.

    PubMed  CAS  Google Scholar 

  73. Duerr JS, Frisby DL, Gaskin J, Duke A, Asermely K, Huddleston D et al. The cat-1 gene of Caenorhabditis elegans encodes a vesicular monoamine transporter required for specific monoamine-dependent behaviors. J Neurosci 1999; 19: 72–84.

    PubMed  CAS  Google Scholar 

  74. Holtje M, von Jagow B, Pahner I, Lautenschlager M, Hortnagl H, Nurnberg B et al. The neuronal monoamine transporter VMAT2 is regulated by the trimeric GTPase Go(2). J Neurosci 2000; 20: 2131–2141.

    PubMed  CAS  Google Scholar 

  75. Lotharius J, Barg S, Wiekop P, Lundberg C, Raymon HK, Brundin P . Effect of mutant alpha-synuclein on dopamine homeostasis in a new human mesencephalic cell line. J Biol Chem 2002; 277: 38884–38894.

    PubMed  CAS  Google Scholar 

  76. Meyer P, Bohnen NI, Minoshima S, Koeppe RA, Wernette K, Kilbourn MR et al. Striatal presynaptic monoaminergic vesicles are not increased in Tourette's syndrome. Neurology 1999; 53: 371–374.

    PubMed  CAS  Google Scholar 

  77. Toren P, Rehavi M, Luski A, Roz N, Laor N, Lask M et al. Decreased platelet vesicular monoamine transporter density in children and adolescents with attention deficit/hyperactivity disorder. Eur Neuropsychopharmacol 2005; 15: 159–162.

    PubMed  CAS  Google Scholar 

  78. Andretic R, Chaney S, Hirsh J . Requirement of circadian genes for cocaine sensitization in Drosophila. Science 1999; 285: 1066–1068.

    PubMed  CAS  Google Scholar 

  79. Gainetdinov RR, Premont RT, Bohn LM, Lefkowitz RJ, Caron MG . Desensitization of G protein-coupled receptors and neuronal functions. Annu Rev Neurosci 2004; 27: 107–144.

    PubMed  CAS  Google Scholar 

  80. Kahlig KM, Galli A . Regulation of dopamine transporter function and plasma membrane expression by dopamine, amphetamine, and cocaine. Eur J Pharmacol 2003; 479: 153–158.

    PubMed  CAS  Google Scholar 

  81. Cole SH, Carney GE, McClung CA, Willard SS, Taylor BJ, Hirsh J . Two functional but noncomplementing Drosophila tyrosine decarboxylase genes: distinct roles for neural tyramine and octopamine in female fertility. J Biol Chem 2005; 280: 14948–14955.

    PubMed  CAS  Google Scholar 

  82. Friggi-Grelin F, Coulom H, Meller M, Gomez D, Hirsh J, Birman S . Targeted gene expression in Drosophila dopaminergic cells using regulatory sequences from tyrosine hydroxylase. J Neurobiol 2003; 54: 618–627.

    PubMed  CAS  Google Scholar 

  83. Lee T, Luo L . Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 1999; 22: 451–461.

    PubMed  CAS  Google Scholar 

  84. Broughton SJ, Kitamoto T, Greenspan RJ . Excitatory and inhibitory switches for courtship in the brain of Drosophila melanogaster. Curr Biol 2004; 14: 538–547.

    PubMed  CAS  Google Scholar 

  85. Mehren JE, Ejima A, Griffith LC . Unconventional sex: fresh approaches to courtship learning. Curr Opin Neurobiol 2004; 14: 745–750.

    PubMed  CAS  Google Scholar 

  86. Mehren JE, Griffith LC . Calcium-independent calcium/calmodulin-dependent protein kinase II in the adult Drosophila CNS enhances the training of pheromonal cues. J Neurosci 2004; 24: 10584–10593.

    PubMed  CAS  Google Scholar 

  87. Kalivas PW, Stewart J . Dopamine transmission in the initiation and expression of drug- and stress-induced sensitization of motor activity. Brain Res Rev 1991; 16: 223–244.

    PubMed  CAS  Google Scholar 

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Acknowledgements

This work was supported by grants from the NIMH (MH01709), NIDDKD (DK60857), NIEHS (ES012078) and the Edward Mallinckrodt, Jr and EJLB Foundations (DEK), NIDA (DA00481, to RJB), and a predoctoral fellowship from the ARCS (AG).

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  1. Department of Psychiatry and Biobehavioral Sciences, Gonda (Goldschmied) Center for Genetic and Neuroscience Research, and Hatos Center for Neuropharmacology, The David Geffen School of Medicine at UCLA, Los Angeles, CA, USA

    H-Y Chang, A Grygoruk, E S Brooks & D E Krantz

  2. Department of Psychiatry and Biobehavioral Sciences, Neuropsychiatric Institute, Hatos Center for Neuropharmacology, The David Geffen School of Medicine at UCLA, Los Angeles, CA, USA

    L C Ackerson & N T Maidment

  3. Department of Anesthesia, University of California at San Francisco, San Francisco, CA, USA

    R J Bainton

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  1. H-Y Chang
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Chang, HY., Grygoruk, A., Brooks, E. et al. Overexpression of the Drosophila vesicular monoamine transporter increases motor activity and courtship but decreases the behavioral response to cocaine. Mol Psychiatry 11, 99–113 (2006). https://doi.org/10.1038/sj.mp.4001742

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