Distinct modes of dopamine and GABA release in a dual transmitter neuron

Journal of Neuroscience

Volumn 33, Issue 5, 2013, Pages 1790-1796

  Borisovska, Maria ^a   Bensen, AeSoon L ^a   Chong, Gene ^a   Westbrook, Gary L ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; DOPAMINE; TYROSINE 3 MONOOXYGENASE; VESICULAR INHIBITORY AMINO ACID TRANSPORTER; VESICULAR MONOAMINE TRANSPORTER 2;

AMPEROMETRY; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ELECTRON MICROSCOPY; ELECTROPHYSIOLOGY; FEMALE; FLUORESCENCE ACTIVATED CELL SORTING; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INHIBITORY POSTSYNAPTIC POTENTIAL; MALE; MOUSE; NERVE POTENTIAL; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; SPIKE WAVE; SYNAPSE VESICLE; SYNAPTIC TRANSMISSION;

ANIMALS; CELLS, CULTURED; DOPAMINE; GAMMA-AMINOBUTYRIC ACID; MICE; NEURONS; OLFACTORY BULB; SYNAPTIC TRANSMISSION; SYNAPTIC VESICLES; TYROSINE 3-MONOOXYGENASE; VESICULAR MONOAMINE TRANSPORT PROTEINS;

EID: 84873029794     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4342-12.2013     Document Type: Article

References (50)

1. B heteroreceptors. J Neurophysiol 84:1194-1203. Medline
2. Bergquist F, Ludwig M (2008) Dendritic transmitter release: a comparison of two model systems. J Neuroendocrinol 20:677-686. CrossRef Medline
3. Borisovska M, Zhao Y, Tsytsyura Y, Glyvuk N, Takamori S, Matti U, Rettig J, Sudhof T, Bruns D (2005) v-SNAREs control exocytosis of vesicles from priming to fusion. EMBO J 24:2114-2126. CrossRef Medline
4. Borisovska M, McGinley MJ, Bensen A, Westbrook GL (2011) Loss of olfactory cell adhesion molecule reduces the synchrony of mitral cell activity in olfactory glomeruli. J Physiol 589:1927-1941. CrossRef Medline
5. Bruns D (2004) Detection of transmitter release with carbon fiber electrodes. Methods 33:312-321. CrossRef Medline
6. Bruns D, Jahn R (1995) Real-time measurement of transmitter release from single synaptic vesicles. Nature 377:62-65. CrossRef Medline
7. Burger PM, Mehl E, Cameron PL, Maycox PR, Baumert M, Lottspeich F, De Camilli P, Jahn R (1989) Synaptic vesicles immunoisolated from rat cerebral cortex contain high levels of glutamate. Neuron 3:715-720. CrossRef Medline
8. Chuhma N, Zhang H, Masson J, Zhuang X, Sulzer D, Hen R, Rayport S (2004) Dopamine neurons mediate a fast excitatory signal via their glutamatergic synapses. J Neurosci 24:972-981. CrossRef Medline
9. Coopersmith R, Weihmuller FB, Kirstein CL, Marshall JF, Leon M (1991) Extracellular dopamine increases in the neonatal olfactory bulb during odor preference training. Brain Res 564:149-153. CrossRef Medline
10. Coronas V, Srivastava LK, Liang JJ, Jourdan F, Moyse E (1997) Identification and localization of dopamine receptor subtypes in rat olfactory mucosa and bulb: a combined in situ hybridization and ligand binding radioautographic approach. J Chem Neuroanat 12:243-257. CrossRef Medline
11. Cragg SJ, Nicholson C, Kume-Kick J, Tao L, Rice ME (2001) Dopaminemediated volume transmission in midbrain is regulated by distinct extracellular geometry and uptake. J Neurophysiol 85:1761-1771. Medline
12. Dahlström A, Fuxe K (1964) Localization of monoamines in the lower brain stem. Experientia 20:398-399. CrossRef Medline
13. Doty RL (2012) Olfaction in Parkinson's disease and related disorders. Neurobiol Dis 46:527-552. CrossRef Medline
14. Ennis M, Zhou FM, Ciombor KJ, Aroniadou-Anderjaska V, Hayar A, Borrelli E, Zimmer LA, Margolis F, Shipley MT (2001) Dopamine D2 receptormediated presynaptic inhibition of olfactory nerve terminals. J Neurophysiol 86:2986-2997. Medline
15. Ford CP, Phillips PEM, Williams JT (2009) The time course of dopamine transmission in the ventral tegmental area. J Neurosci 29:13344-13352. CrossRef Medline
16. Gong LW, Hafez I, Alvarez de Toledo G, Lindau M (2003) Secretory vesicles membrane area is regulated in tandem with quantal size in chromaffin cells. J Neurosci 23:7917-7921. Medline
17. Halász N, Hökfelt T, Ljungdahl A, Johansson O, Goldstein M (1977) Dopamine neurons in the olfactory bulb. Adv Biochem Psychopharmacol 16:169-177. Medline
18. Hannah MJ, Weiss U, Huttner WB (1998) Differential extraction of proteins from paraformaldehyde-fixed cells: lessons from synaptophysin and other membrane proteins. Methods 16:170-181. CrossRef Medline
19. Hefft S, Jonas P (2005) Asynchronous GABA release generates long-lasting inhibition at a hippocampal interneuron-principal neuron synapse. Nat Neurosci 8:1319-1328. CrossRef Medline
20. Hnasko TS, Edwards RH (2012) Neurotransmitter corelease: mechanism and physiological role. Annu Rev Physiol 74:225-243. CrossRef Medline
21. Hsia AY, Vincent JD, Lledo PM (1999) Dopamine depresses synaptic inputs into the olfactory bulb. J Neurophysiol 82:1082-1085. Medline
22. Jaffe EH, Marty A, Schulte A, Chow RH (1998) Extrasynaptic vesicular transmitter release from the somata of substantia nigra neurons in rat midbrain slices. J Neurosci 18:3548-3553. Medline
23. Kasowski HJ, Kim H, Greer CA (1999) Compartmental organization of the olfactory bulb glomerulus. J Comp Neurol 407:261-274. CrossRef Medline
24. Kiyokage E, Pan YZ, Shao Z, Kobayashi K, Szabo G, Yanagawa Y, Obata K, Okano H, Toida K, Puche AC, Shipley MT (2010) Molecular identity of periglomerular and short axon cells. J Neurosci 30:1185-1196. CrossRef Medline
25. Leszczyszyn DJ, Jankowski JA, Viveros OH, Diliberto EJ Jr, Near JA, Wightman RM (1990) Nicotinic receptor-mediated catecholamine secretion from individual chromaffin cells: chemical evidence for exocytosis. J Biol Chem 265:14736-14737. Medline
26. Maher BJ, Westbrook GL (2008) Co-transmission of dopamine and GABA in periglomerular cells. J Neurophysiol 99:1559-1564. CrossRef Medline
27. Masurovsky EB, Bunge RP (1968) Fluoroplastic coverslips for long-term nerve tissue culture. Stain Technol 43:161-165. Medline
28. Mittelsteadt T, Seifert G, Alvárez-Barón E, Steinhäuser C, Becker AJ, Schoch S (2009) Differential mRNA expression patterns of the synaptotagmin gene family in the rodent brain. J Comp Neurol 512:514-528. CrossRef Medline
29. Murphy GJ, Darcy DP, Isaacson JS (2005) Intraglomerular inhibition: signaling mechanisms of an olfactory microcircuit. Nat Neurosci 8:354-364. CrossRef Medline
30. Onoa B, Li H, Gagnon-Bartsch JA, Elias LAB, Edwards RH (2010) Vesicular monoamine and glutamate transporters select distinct synaptic vesicle recycling pathways. J Neurosci 30:7917-7927. CrossRef Medline
31. 2+-triggered exocytosis. Curr Opin Cell Biol 22:496-505. CrossRef Medline
32. Parker LK, Shanks JA, Kennard JA, Brain KL (2010) Dynamic monitoring of NET activity in mature murine sympathetic terminals using a fluorescent substrate. Br J Pharmacol 159:797-807. CrossRef Medline
33. Parrish-Aungst S, Shipley MT, Erdelyi F, Szabo G, Puche AC (2007) Quantitative analysis of neuronal diversity in the mouse olfactory bulb. J Comp Neurol 501:825-836. CrossRef Medline
34. Parsons TD, Coorssen JR, Horstmann H, Almers W (1995) Docked granules, the exocytic burst, and the need for ATP hydrolysis in endocrine cells. Neuron 15:1085-1096. CrossRef Medline
35. Peter D, Liu Y, Sternini C, de Giorgio R, Brecha N, Edwards RH (1995) Differential expression of two vesicular monoamine transporters. J Neurosci 15:6179-6188. Medline
36. Pinching AJ, Powell TPS (1971) The neuron types of the glomerular layer of the olfactory bulb. J Cell Sci 9:305-345. Medline
37. Pothos EN, Davila V, Sulzer D (1998) Presynaptic recording of quanta from midbrain dopamine neurons and modulation of the quantal size. J Neurosci 18:4106-4118. Medline
38. Pothos E, Desmond M, Sulzer D (1996) l-3,4-Dihydroxyphenylalanine increases the quantal size of exocytotic dopamine release in vitro. J Neurochem 66:629-636. CrossRef Medline
39. Puopolo M, Hochstetler SE, Gustincich S, Wightman RM, Raviola E (2001) Extrasynaptic release of dopamine in a retinal neuron: activity dependence and transmitter modulation. Neuron 30:211-225. CrossRef Medline
40. Rosenmund C, Stevens CF (1996) Definition of the readily releasable pool of vesicles at hippocampal synapses. Neuron 16:1197-1207. CrossRef Medline
41. Sawamoto K, Nakao N, Kobayashi K, Matsushita N, Takahashi H, Kakishita K, Yamamoto A, Yoshizaki T, Terashima T, Murakami F, Itakura T, Okano H (2001) Visualization, direct isolation, and transplantation of midbrain dopaminergic neurons. Proc Natl Acad Sci U S A 98:6423-6428. CrossRef Medline
42. Smith TC, Jahr CE (2002) Self-inhibition of olfactory bulb neurons. Nat Neurosci 5:760-766. CrossRef Medline
43. Staal RGW, Mosharov EV, Sulzer D (2004) Dopamine neurons release transmitter via a flickering fusion pore. Nature Neuroscience 7:341-346. CrossRef Medline
44. Taylor TN, Caudle WM, Shepherd KR, Noorian A, Jackson CR, Iuvone PM, Weinshenker D, Greene JG, Miller GW (2009) Non-motor symptoms of Parkinson's disease revealed in an animal model with reduced monoamine storage capacity. J Neurosci 29:8103-8113. CrossRef Medline
45. 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. CrossRef Medline
46. Toida K, Kosaka K, Aika Y, Kosaka T (2000) Chemically defined neuron groups and their subpopulations in the glomerular layer of the rat main olfactory bulb-IV. Intraglomerular synapses of tyrosine hydroxylaseimmunoreactive neurons. Neuroscience 101:11-17. CrossRef Medline
47. Tovar KR, Maher BJ, Westbrook GL (2009) Direct actions of carbenoxolone on synaptic transmission and neuronal membrane properties. J Neurophysiol 102:974-978. CrossRef Medline
48. 2 release from internal stores controls exocytosis in pituitary gonadotrophs. Neuron 18:121-132. CrossRef Medline
49. Weihe E, Depboylu C, Schutz B, Schäfer M, Eiden L (2006) Three types of tyrosine hydroxylase-positive CNS neurons distinguished by DOPA decarboxylase and VMAT2 Co-expression. Cell Mol Neurobiol 26:657-676. CrossRef
50. Wightman RM, Jankowski JA, Kennedy RT, Kawagoe KT, Schroeder TJ, Leszczyszyn DJ, Near JA, Diliberto EJ Jr, Viveros OH (1991) Temporally resolved catecholamine spikes correspond to single vesicle release from individual chromaffin cells. Proc Natl Acad Sci U S A 88:10754-10758. CrossRef Medline