Vigorous motor activity in Caenorhabditis elegans requires efficient clearance of dopamine mediated by synaptic localization of the dopamine transporter DAT-1

Journal of Neuroscience

Volumn 27, Issue 51, 2007, Pages 14216-14227

  McDonald, Paul W ^a   Hardie, Shannon L ^a   Jessen, Tammy N ^a   Carvelli, Lucia ^a   Matthies, Dawn Signor ^a   Blakely, Randy D ^a,b  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MRBIII   (United States)

Author keywords

C. elegans; Cat 1; Dat 1; Dopamine; Localization; PDZ binding domain; Receptor; Synapse; Transporter; Unc 104

Indexed keywords

COCAINE; DOPAMINE 3 RECEPTOR; DOPAMINE TRANSPORTER; DOPAMINE TRANSPORTER DAT 1; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; UNCLASSIFIED DRUG; VESICULAR MONOAMINE TRANSPORTER; CAENORHABDITIS ELEGANS PROTEIN; DOPAMINE; SLC6A3 PROTEIN, HUMAN;

ARTICLE; BINDING SITE; CAENORHABDITIS ELEGANS; CARBOXY TERMINAL SEQUENCE; DOPAMINERGIC TRANSMISSION; GENE DELETION; GENE DISRUPTION; IN VIVO STUDY; MOTOR ACTIVITY; NEMATODE; NERVE CELL CULTURE; NONHUMAN; PARALYSIS; PHENOTYPE; PHYSICAL ACTIVITY; POINT MUTATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SYNAPSE; VALIDITY; WILD TYPE; ANIMAL; CELL LINE; CHEMISTRY; COMPARATIVE STUDY; HUMAN; MALE; METABOLIC CLEARANCE RATE; METABOLISM; PHYSIOLOGY; TRANSGENIC ANIMAL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL LINE; DOPAMINE; DOPAMINE PLASMA MEMBRANE TRANSPORT PROTEINS; HUMANS; MALE; METABOLIC CLEARANCE RATE; MOTOR ACTIVITY; SYNAPSES;

EID: 38449119973     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2992-07.2007     Document Type: Article

References (68)

1. Ahmari SE, Buchanan J, Smith SJ (2000) Assembly of presynaptic active zones from cytoplasmic transport packets. Nat Neurosci 3:445-451.
2. Altun ZF, Hall DH (2005) Handbook of C. elegans anatomy. In: Worm-Atlas. E-book available at http://www.wormatlas.org/handbook/contents.htm.
3. Bannon MJ, Poosch MS, Xia Y, Goebel DJ, Cassin B, Kapatos G (1992) Dopamine transporter mRNA content in human substantia nigra decreases precipitously with age. Proc Natl Acad Sci USA 89:7095-7099.
4. Barstead RJ, Kleiman L, Waterston RH (1991) Cloning, sequencing, and mapping of an alpha-actinin gene from the nematode Caenorhabditis elegans. Cell Motil Cytoskeleton 20:69-78.
5. Benoit-Marand M, Jaber M, Gonon F (2000) Release and elimination of dopamine in vivo in mice lacking the dopamine transporter: functional consequences. Eur J Neurosci 12:2985-2992.
6. Bjerggaard C, Fog JU, Hastrup H, Madsen K, Loland CJ, Javitch JA, Gether U (2004) Surface targeting of the dopamine transporter involves discrete epitopes in the distal C terminus but does not require canonical PDZ domain interactions. J Neurosci 24:7024-7036.
7. Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77:71-94.
8. Campbell RE, Tour O, Palmer AE, Steinbach PA, Baird GS, Zacharias DA, Tsien RY (2002) A monomeric red fluorescent protein. Proc Natl Acad Sci USA 99:7877-7882.
9. Carlsson ML, Carlsson A, Nilsson M (2004) Schizophrenia: from dopamine to glutamate and back. Curr Med Chem 11:267-277.
10. Carneiro AM, Ingram SL, Beaulieu JM, Sweeney A, Amara SG, Thomas SM, Caron MG, Torres GE (2002) The multiple LIM domain-containing adaptor protein Hic-5 synaptically colocalizes and interacts with the dopamine transporter. J Neurosci 22:7045-7054.
11. Carvelli L, McDonald PW, Blakely RD, Defelice LJ (2004) Dopamine transporters depolarize neurons by a channel mechanism. Proc Natl Acad Sci USA 101:16046-16051.
12. Chase DL, Pepper JS, Koelle MR (2004) Mechanism of extrasynaptic dopamine signaling in Caenorhabditis elegans. Nat Neurosci 7:1096-1103.
13. Ciliax BJ, Drash GW, Staley JK, Haber S, Mobley CJ, Miller GW, Mufson EJ, Mash DC, Levey AI (1999) Immunocytochemical localization of the dopamine transporter in human brain. J Comp Neurol 409:38-56.
14. Clark SG, Chiu C (2003) C. elegans ZAG-1, a Zn-finger-homeodomain protein, regulates axonal development and neuronal differentiation. Development 130:3781-3794.
15. Crossman AR, Clarke CE, Boyce S, Robertson RG, Sambrook MA (1987) MPTP-induced parkinsonism in the monkey: neurochemical pathology, complications of treatment and pathophysiological mechanisms. Can J Neurol Sci 14:428-435.
16. Dani JA, Zhou FM (2004) Selective dopamine filter of glutamate striatal afferents. Neuron 42:522-524.
17. Duerr JS, Frisby DL, Gaskin J, Duke A, Asermely K, Huddleston D, Eiden LE, Rand JB (1999) The cat-1 gene of Caenorhabditis elegans encodes a vesicular monoamine transporter required for specific monoamine-dependent behaviors. J Neurosci 19:72-84.
18. Erickson JD, Eiden LE, Hoffman BJ (1992) Expression cloning of a reserpine-sensitive vesicular monoamine transporter. Proc Natl Acad Sci USA 89:10993-10997.
19. Farhan H, Korkhov VM, Paulitschke V, Dorostkar MM, Scholze P, Kudlacek O, Freissmuth M, Sitte HH (2004) Two discontinuous segments in the carboxyl terminus are required for membrane targeting of the rat gamma-aminobutyric acid transporter-1 (GAT1). J Biol Chem 279:28553-28563.
20. Ferguson SM, Savchenko V, Apparsundaram S, Zwick M, Wright J, Heilman CJ, Yi H, Levey AI, Blakely RD (2003) Vesicular localization and activity-dependent trafficking of presynaptic choline transporters. J Neurosci 23:9697-9709.
21. Finney M, Ruvkun G (1990) The unc-86 gene product couples cell lineage and cell identity in C. elegans. Cell 63:895-905.
22. Fiorino DF, Coury A, Fibiger HC, Phillips AG (1993) Electrical stimulation of reward sites in the ventral tegmental area increases dopamine transmission in the nucleus accumbens of the rat. Behav Brain Res 55:131-141.
23. Foster JD, Cervinski MA, Gorentla BK, Vaughan RA (2006) Regulation of the dopamine transporter by phosphorylation. Handb Exp Pharmacol 197-214.
24. Gainetdinov RR, Jones SR, Fumagalli F, Wightman RM, Caron MG (1998) Re-evaluation of the role of the dopamine transporter in dopamine system homeostasis. Brain Res Brain Res Rev 26:148-153.
25. Gainetdinov RR, Sotnikova TD, Caron MG (2002) Monoamine transporter pharmacology and mutant mice. Trends Pharmacol Sci 23:367-373.
26. Giros B, Jaber M, Jones SR, Wightman RM, Caron MG (1996) Hyperlocomotion and indifference to cocaine and amphetamine in mice lacking the dopamine transporter. Nature 379:606-612.
27. Hall DH, Hedgecock EM (1991) Kinesin-related gene unc-104 is required for axonal transport of synaptic vesicles in C. elegans. Cell 65:837- 847.
28. Hayashi Y, Shi SH, Esteban JA, Piccini A, Poncer JC, Malinow R (2000) Driving AMPA receptors into synapses by LTP and CaMKII: requirement for GluR1 and PDZ domain interaction. Science 287:2262-2267.
29. Hernandez L, Hoebel BG (1988) Food reward and cocaine increase extracellular dopamine in the nucleus accumbens as measured by microdialysis. Life Sci 42:1705-1712.
30. Hironaka N, Ikeda K, Sora I, Uhl GR, Niki H (2004) Food-reinforced operant behavior in dopamine transporter knockout mice: enhanced resistance to extinction. Ann NY Acad Sci 1025:140-145.
31. Hoffman BJ, Hansson SR, Mezey E, Palkovits M (1998) Localization and dynamic regulation of biogenic amine transporters in the mammalian central nervous system. Front Neuroendocrinol 19:187-231.
32. Holton KL, Loder MK, Melikian HE (2005) Nonclassical, distinct endocytic signals dictate constitutive and PKC-regulated neurotransmitter transporter internalization. Nat Neurosci 8:881-888.
33. Jayanthi LD, Apparsundaram S, Malone MD, Ward E, Miller DM, Eppler M, Blakely RD (1998) The Caenorhabditis elegans gene T23G5.5 encodes an antidepressant- and cocaine-sensitive dopamine transporter. Mol Pharmacol 54:601-609.
34. Kim CH, Takamiya K, Petralia RS, Sattler R, Yu S, Zhou W, Kalb R, Wenthold R, Huganir R (2005) Persistent hippocampal CA1 LTP in mice lacking the C-terminal PDZ ligand of GluR1. Nat Neurosci 8:985-987.
35. Kornau HC, Seeburg PH, Kennedy MB (1997) Interaction of ion channels and receptors with PDZ domain proteins. Curr Opin Neurobiol 7:368-373.
36. Lints R, Emmons SW (1999) Patterning of dopaminergic neurotransmitter identity among Caenorhabditis elegans ray sensory neurons by a TGFbeta family signaling pathway and a Hox gene. Development 126:5819-5831.
37. Loder MK, Melikian HE (2003) The dopamine transporter constitutively internalizes and recycles in a protein kinase C-regulated manner in stably transfected PC12 cell lines. J Biol Chem 278:22168-22174.
38. Lorang D, Amara SG, Simerly RB (1993) Cell-type specific expression of catecholamine transporters in the rat brain. J Neurosci 14:4903-4914.
39. Madsen KL, Beuming T, Niv MY, Chang CW, Dev KK, Weinstein H, Gether U (2005) Molecular determinants for the complex binding specificity of the PDZ domain in PICK1. J Biol Chem 280:20539-20548.
40. Matthies DS, Fleming PA, Wilkes DM, Blakely RD (2006) The Caenorhabditis elegans choline transporter CHO-1 sustains acetylcholine synthesis and motor function in an activity-dependent manner. J Neurosci 26:6200-6212.
41. McDonald PW, Jessen T, Field JR, Blakely RD (2006) Dopamine signaling architecture in Caenorhabditis elegans. Cell Mol Neurobiol 26:593-618.
42. Medvedev IO, Gainetdinov RR, Sotnikova TD, Bohn LM, Caron MG, Dykstra LA (2005) Characterization of conditioned place preference to cocaine in congenic dopamine transporter knockout female mice. Psychopharmacology (Berl) 180:408-413.
43. Melikian HE (2004) Neurotransmitter transporter trafficking: endocytosis, recycling, and regulation. Pharmacol Ther 104:17-27.
44. Mello CC, Kramer JM, Stinchcomb D, Ambros V (1991) Efficient gene transfer in C. elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J 10:3959-3970.
45. Miles PR, Mundorf ML, Wightman RM (2002) Release and uptake of catecholamines in the bed nucleus of the stria terminalis measured in the mouse brain slice. Synapse 44:188-197.
46. Miller III DM, Niemeyer CJ (1995) Expression of the unc-4 homeoprotein in Caenorhabditis elegans motor neurons specifies presynaptic input. Development 121:2877-2886.
47. Miranda M, Sorkina T, Grammatopoulos TN, Zawada WM, Sorkin A (2004) Multiple molecular determinants in the carboxyl terminus regulate dopamine transporter export from endoplasmic reticulum. J Biol Chem 279:30760-30770.
48. Nass R, Hall DH, Miller III DM, Blakely RD (2002) Neurotoxin-induced degeneration of dopamine neurons in Caenorhabditis elegans. Proc Natl Acad Sci USA 99:3264-3269.
49. Nass R, Hahn MK, Jessen T, McDonald PW, Carvelli L, Blakely RD (2005) A genetic screen in Caenorhabditis elegans for dopamine neuron insensitivity to 6-hydroxydopamine identifies dopamine transporter mutants impacting transporter biosynthesis and trafficking. J Neurochem 94:774-785.
50. Nirenberg MJ, Chan J, Vaughan RA, Uhl GR, Kuhar MJ, Pickel VM (1997a) Immunogold localization of the dopamine transporter: an ultrastructural study of the rat ventral tegmental area. J Neurosci 17:5255-5262.
51. Nirenberg MJ, Chan J, Pohorille A, Vaughan RA, Uhl GR, Kuhar MJ, Pickel VM (1997b) The dopamine transporter: comparative ultrastructure of dopaminergic axons in limbic and motor compartments of the nucleus accumbens. J Neurosci 17:6899-6907.
52. Nonet ML, Grundahl K, Meyer BJ, Rand JB (1993) Synaptic function is impaired but not eliminated in C. elegans mutants lacking synaptotagmin. Cell 73:1291-1305.
53. Nonet ML, Saifee O, Zhao H, Rand JB, Wei L (1998) Synaptic transmission deficits in Caenorhabditis elegans synaptobrevin mutants. J Neurosci 18:70-80.
54. Powell SB, Lehmann-Masten VD, Paulus MP, Gainetdinov RR, Caron MG, Geyer MA (2004) MDMA"ecstasy" alters hyperactive and perseverative behaviors in dopamine transporter knockout mice. Psychopharmacology (Berl) 173:310-317.
55. Ranganathan R, Sawin ER, Trent C, Horvitz HR (2001) Mutations in the Caenorhabditis elegans serotonin reuptake transporter MOD-5 reveal serotonin-dependent and -independent activities of fluoxetine. J Neurosci 21:5871-5884.
56. Reimherr FW, Wender PH, Ebert MH, Wood DR (1984) Cerebrospinal fluid homovanillic acid and 5-hydroxy-indoleacetic acid in adults with attention deficit disorder, residual type. Psychiatry Res 11:71-78.
57. Rodriguiz RM, Chu R, Caron MG, Wetsel WC (2004) Aberrant responses in social interaction of dopamine transporter knockout mice. Behav Brain Res 148:185-198.
58. Sanyal S, Wintle RF, Kindt KS, Nuttley WM, Arvan R, Fitzmaurice P, Bigras E, Merz DC, Hebert TE, van der Kooy D, Schafer WR, Culotti JG, Van Tol HH (2004) Dopamine modulates the plasticity of mechanosensory responses in Caenorhabditis elegans. EMBO J 23:473-482.
59. Sawin ER, Ranganathan R, Horvitz HR (2000) C. elegans locomotory rate is modulated by the environment through a dopaminergic pathway and by experience through a serotonergic pathway. Neuron 26:619-631.
60. Schafer WR, Kenyon CJ (1995) A calcium-channel homologue required for adaptation to dopamine and serotonin in Caenorhabditis elegans. Nature 375:73-78.
61. Seamans JK, Yang CR (2004) The principal features and mechanisms of dopamine modulation in the prefrontal cortex. Prog Neurobiol 74:1-58.
62. Sulston J, Dew M, Brenner S (1975) Dopaminergic neurons in the nematode Caenorhabditis elegans. J Comp Neurol 163:215-226.
63. Terskikh A, Fradkov A, Ermakova G, Zaraisky AG, Tan P, Kajava AV, Zhao X, Lukyanov S, Matz M, Kim S, Weissman I, Siebert P (2000) "Fluorescent timer": protein that changes color with time. Science 290:1585-1588.
64. Tillerson JL, Caudle WM, Parent JM, Gong C, Schallert T, Miller GW (2006) Olfactory discrimination deficits in mice lacking the dopamine transporter or the D2 dopamine receptor. Behav Brain Res 172:97-105.
65. Torres GE, Yao WD, Mohn RR, Quan H, Kim K, Levey AI, Staudinger J, Caron MG (2001) Functional interaction between monoamine plasma membrane transporters and the synaptic PDZ domain-containing protein PICK1. Neuron 30:121-134.
66. White JG, Southgate E, Thompson JN, 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.
67. Williams BD, Schrank B, Huynh C, Shownkeen R, Waterston RH (1992) A genetic mapping system in Caenorhabditis elegans based on polymorphic sequence-tagged sites. Genetics 131:609-624.
68. Zhai RG, Vardinon-Friedman H, Cases-Langhoff C, Becker B, Gundelfinger ED, Ziv NE, Garner CC (2001) Assembling the presynaptic active zone: a characterization of an active one precursor vesicle. Neuron 29:131-143.