Fast phasic release properties of dopamine studied with a channel biosensor

Journal of Neuroscience

Volumn 34, Issue 35, 2014, Pages 11792-11802

  Kress, Geraldine J ^a   Shu, Hong Jin ^a   Yu, Andrew ^a   Taylor, Amanda ^a   Benz, Ann ^a   Harmon, Steve ^a   Mennerick, Steven ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Dopamine release; Ligand gated ion channel; Nicotinic; Presynaptic; Striatum

Indexed keywords

2, 3, 4, 5 TETRAHYDRO 7, 8 DIHYDROXY 1 PHENYL 1H 3 BENZAZEPINE; 3 AMINO 2 (3 CARBOXYPROPYL) 6 (4 METHOXYPHENYL) PYRIDAZINIUM BROMIDE; 4 AMINOBUTYRIC ACID A RECEPTOR; 6 NITRO 7 SULFAMOYLBENZO [F] QUINOXALINE 2, 3 DIONE; ADRENALIN; CHLORIDE CHANNEL; DOPAMINE 1 RECEPTOR; DOPAMINE 2 RECEPTOR; EMONAPRIDE; ETICLOPRIDE; GLUCONIC ACID; GLUTAMIC ACID; HALOPERIDOL; LIGAND GATED ION CHANNEL; MECAMYLAMINE; MESYLIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NICOTINIC RECEPTOR; NORADRENALIN; PREGNENOLONE SULFATE; QUINPIROLE; RACLOPRIDE; SPIPERONE; SULPIRIDE; UNCLASSIFIED DRUG; VANOXERINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOPHYSICS; BIOSENSOR; CELL CULTURE; CONTROLLED STUDY; CORPUS STRIATUM; CULTURE MEDIUM; DOPAMINE RELEASE; EVOKED RESPONSE; FEMALE; HUMAN; HUMAN CELL; INNERVATION; LENTIVIRUS INFECTION; METABOLIC REGULATION; MOLECULAR BIOLOGY; MONOSYNAPTIC POTENTIAL; NONHUMAN; OOCYTE; POSTSYNAPTIC POTENTIAL; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; RAT; VOLTAGE CLAMP TECHNIQUE; WHOLE CELL PATCH CLAMP; XENOPUS LAEVIS;

DOPAMINE RELEASE; LIGAND-GATED ION CHANNEL; NICOTINIC; PRESYNAPTIC; STRIATUM;

ANIMALS; BIOSENSING TECHNIQUES; CAENORHABDITIS ELEGANS; CELL LINE; CHLORIDE CHANNELS; CORPUS STRIATUM; DOPAMINE; HUMANS; LIGAND-GATED ION CHANNELS; NEURONS; PATCH-CLAMP TECHNIQUES; RATS; XENOPUS;

EID: 84906568747     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2355-14.2014     Document Type: Article

References (42)

1. Adrover M. F, Shin JH, Alvarez VA (2014) Glutamate and dopamine transmission from midbrain dopamine neurons share similar release properties but are differentially affected by cocaine. J Neurosci 34:3183-3192. CrossRef Medline
2. Alcantara A. A, Chen V, Herring BE, Mendenhall JM, Berlanga ML (2003) Localization of dopamine D2 receptors on cholinergic interneurons of the dorsal striatum and nucleus accumbens of the rat. Brain Res 986:22-29. CrossRef Medline
3. Bormann J., Hamill OP, Sakmann B (1987) Mechanism of anion permeation through channels gated by glycine and gamma-aminobutyric acid in mouse cultured spinal neurones. J Physiol 385:243-286. Medline
4. Cachope R., Mateo Y, Mathur BN, Irving J, Wang HL, Morales M, Lovinger DM, Cheer JF (2012) Selective activation of cholinergic interneurons enhances accumbal phasic dopamine release: setting the tone for reward processing. Cell Rep 2:33-41. CrossRef Medline
5. A receptor function in the absence of a conventional binding site. Br J Pharmacol 164:667-680. CrossRef Medline
6. Contant C., Umbriaco D, Garcia S, Watkins KC, Descarries L (1996) Ultrastructural characterization of the acetylcholine innervation in adult rat neostriatum. Neuroscience 71:937-947. CrossRef Medline
7. Cragg S. J (2003) Variable dopamine release probability and short-term plasticity between functional domains of the primate striatum. J Neurosci 23:4378-4385. Medline
8. Daniel J. A, Galbraith S, Iacovitti L, Abdipranoto A, Vissel B (2009) Functional heterogeneity at dopamine release sites. J Neurosci 29:14670-14680. CrossRef Medline
9. Descarries L., Watkins KC, Garcia S, Bosler O, Doucet G (1996) Dual character, asynaptic and synaptic, of the dopamine innervation in adult rat neostriatum: a quantitative autoradiographic and immunocytochemical analysis. J Comp Neurol 375:167-186. CrossRef Medline
10. Ding J. B, Guzman JN, Peterson JD, Goldberg JA, Surmeier DJ (2010) Thalamic gating of corticostriatal signaling by cholinergic interneurons. Neuron 67:294-307. CrossRef Medline
11. Doucet G., Descarries L, Garcia S (1986) Quantification of the dopamine innervation in adult rat neostriatum. Neuroscience 19:427-445. CrossRef Medline
12. Dubinsky J. M (1989) Development of inhibitory synapses among striatal neurons in vitro. J Neurosci 9:3955-3965. Medline
13. A receptor function by neuroactive steroids. In: Neurosteroid effects in the central nervous system (Smith SS, ed), pp 95-117. Boca Raton, FL: CRC.
14. Ford C. P, Phillips PE, Williams JT (2009) The time course of dopamine transmission in the ventral tegmental area. J Neurosci 29:13344-13352. CrossRef Medline
15. Gantz S. C, Bunzow JR, Williams JT (2013) Spontaneous inhibitory synaptic currents mediated by a G protein-coupled receptor. Neuron 78:807-812. CrossRef Medline
16. Garcia-Reitböck P., Anichtchik O, Bellucci A, Iovino M, Ballini C, Fineberg E, Ghetti B., Della Corte L, Spano P, Tofaris GK, Goedert M, Spillantini MG (2010) SNARE protein redistribution and synaptic failure in a transgenic mouse model of Parkinson's disease. Brain 133:2032-2044. CrossRef Medline
17. Goto Y., Otani S, Grace AA (2007) The Yin and Yang of dopamine release: a new perspective. Neuropharmacology 53:583-587. CrossRef Medline
18. Gubernator N. G, Zhang H, Staal RG, Mosharov EV, Pereira DB, Yue M, Balsanek V., Vadola PA, Mukherjee B, Edwards RH, Sulzer D, Sames D (2009) Fluorescent false neurotransmitters visualize dopamine release from individual presynaptic terminals. Science 324:1441-1444. CrossRef Medline
19. Harris K. M, Weinberg RJ (2012) Ultrastructure of synapses in the mammalian brain. Cold Spring Harb Perspect Biol 4:a005587. CrossRef Medline
20. Jones I. W, Bolam JP, Wonnacott S (2001) Presynaptic localisation of the nicotinic acetylcholine receptor beta2 subunit immunoreactivity in rat nigrostriatal dopaminergic neurones. J Comp Neurol 439:235-247. CrossRef Medline
21. Kim K. T, Koh DS, Hille B (2000) Loading of oxidizable transmitters into secretory vesicles permits carbon-fiber amperometry. J Neurosci 20: RC101(1-5). Medline
22. Lehmann J., Langer SZ (1983) The striatal cholinergic interneuron: synaptic target of dopaminergic terminals? Neuroscience 10:1105-1120. CrossRef Medline
23. Li M., Husic N, Lin Y, Christensen H, Malik I, McIver S, LaPash Daniels CM, Harris D. A, Kotzbauer PT, Goldberg MP, Snider BJ (2010) Optimal promoter usage for lentiviral vector-mediated transduction of cultured central nervous system cells. J Neurosci Methods 189:56-64. CrossRef Medline
24. A receptors. J Physiol 588:1251-1268. CrossRef Medline
25. Moulder K. L, Jiang X, Taylor AA, Shin W, Gillis KD, Mennerick S (2007) Vesicle pool heterogeneity at hippocampal glutamate and GABA synapses. J Neurosci 27:9846-9854. CrossRef Medline
26. Nelson A. B, Hammack N, Yang CF, Shah NM, Seal RP, Kreitzer AC (2014) Striatal cholinergic interneurons Drive GABA release from dopamine terminals. Neuron 82:63-70. CrossRef Medline
27. A receptors. J Neurosci 20:7914-7921. Medline
28. Patneau D. K, Mayer ML (1990) Structure-activity relationships for amino acid transmitter candidates acting at N-methyl-D-aspartate and quisqualate receptors. J Neurosci 10:2385-2399. Medline
29. Pisani A., Bonsi P, Centonze D, Calabresi P, Bernardi G (2000) Activation of D2-like dopamine receptors reduces synaptic inputs to striatal cholinergic interneurons. J Neurosci 20:RC69(1-6). Medline
30. Ringstad N., Abe N, Horvitz HR (2009) Ligand-gated chloride channels are receptors for biogenic amines in C. elegans. Science 325:96-100. CrossRef Medline
31. Rodriguez P. C, Pereira DB, Borgkvist A, Wong MY, Barnard C, Sonders MS, Zhang H., Sames D, Sulzer D (2013) Fluorescent dopamine tracer resolves individual dopaminergic synapses and their activity in the brain. Proc Natl Acad Sci U S A 110:870-875. CrossRef Medline
32. Sankaranarayanan S., De Angelis D, Rothman JE, Ryan TA (2000) The use of pHluorins for optical measurements of presynaptic activity. Biophys J 79:2199-2208. CrossRef Medline
33. Scott D. A, Tabarean I, Tang Y, Cartier A, Masliah E, Roy S (2010) A pathologic cascade leading to synaptic dysfunction in α-synuclein-induced neurodegeneration. J Neurosci 30:8083-8095. CrossRef Medline
34. Seeman P., Van Tol HH (1994) Dopamine receptor pharmacology. Trends Pharmacol Sci 15:264-270. CrossRef Medline
35. Staal R. G, Mosharov EV, Sulzer D (2004) Dopamine neurons release transmitter via a flickering fusion pore. Nat Neurosci 7:341-346. CrossRef Medline
36. Threlfell S., Lalic T, Platt NJ, Jennings KA, Deisseroth K, Cragg SJ (2012) Striatal dopamine release is triggered by synchronized activity in cholinergic interneurons. Neuron 75:58-64. CrossRef Medline
37. Tong G., Shepherd D, Jahr CE (1995) Synaptic desensitization of NMDA receptors by calcineurin. Science 267:1510-1512. CrossRef Medline
38. Trussell L. O, Fischbach GD (1989) Glutamate receptor desensitization and its role in synaptic transmission. Neuron 3:209-218. CrossRef Medline
39. Wang L., Zhang X, Xu H, Zhou L, Jiao R, Liu W, Zhu F, Kang X, Liu B, Teng S, Wu Q, Li M, Dou H, Zuo P, Wang C, Wang S, Zhou Z (2014) Temporal components of cholinergic terminal to dopaminergic terminal transmission in dorsal striatum slices of mice. J Physiol. Advance online publication. CrossRef Medline
40. Zhang C., Zhou Z (2002) Ca2-independent but voltage-dependent secretion in mammalian dorsal root ganglion neurons. Nat Neurosci 5:425-430. CrossRef Medline
41. Zorumski C. F, Mennerick S, Que J (1996) Modulation of excitatory synaptic transmission by low concentrations of glutamate in cultured rat hippocampal neurons. J Physiol 494:465-477. Medline
42. Zucker R. S, Regehr WG (2002) Short-term synaptic plasticity. Annu Rev Physiol 64:355-405. CrossRef Medline