Corelease of dopamine and GABA by a retinal dopaminergic neuron

Journal of Neuroscience

Volumn 32, Issue 38, 2012, Pages 13281-13291

  Hirasawa, Hajime ^a,c   Betensky, Rebecca A ^b   Raviola, Elio ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^c RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; DOPAMINE; VESICULAR INHIBITORY AMINO ACID TRANSPORTER; VESICULAR MONOAMINE TRANSPORTER 2;

ANIMAL CELL; ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; ELECTRON MICROSCOPY; ELECTROPHYSIOLOGY; EXOCYTOSIS; FEMALE; IMMUNOCYTOCHEMISTRY; MALE; MOUSE; NONHUMAN; PERIKARYON; PRIORITY JOURNAL; RETINA;

ALKALINE PHOSPHATASE; ANIMALS; DOPAMINE; DOPAMINERGIC NEURONS; ELECTRIC STIMULATION; FEMALE; GAMMA-AMINOBUTYRIC ACID; GPI-LINKED PROTEINS; HUMANS; ISOENZYMES; MALE; MEMBRANE POTENTIALS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROSCOPY, ELECTRON, TRANSMISSION; MICROSCOPY, IMMUNOELECTRON; MONTE CARLO METHOD; PATCH-CLAMP TECHNIQUES; RETINA; TYROSINE 3-MONOOXYGENASE; VESICULAR INHIBITORY AMINO ACID TRANSPORT PROTEINS; VESICULAR MONOAMINE TRANSPORT PROTEINS;

EID: 84866419560     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2213-12.2012     Document Type: Article

References (48)

1. Bianchetta MJ, Betensky RA, Cohen JB (2005) Cell-surface MuSK self-association: a crucial role for the putative signal sequence. Biochemistry 44:16229-16238. CrossRef Medline
2. Boulland JL, Jenstad M, Boekel AJ, Wouterlood FG, Edwards RH, Storm-Mathisen J, Chaudhry FA (2009) Vesicular glutamate and GABA transporters sort to distinct sets of vesicles in a population of presynaptic terminals. Cereb Cortex 19:241-248. CrossRef Medline
3. Braun M, Wendt A, Karanauskaite J, Galvanovskis J, Clark A, MacDonald PE, Rorsman P (2007) Corelease and differential exit via the fusion pore of GABA, serotonin, and ATP from LDCV in rat pancreatic beta cells. J Gen Physiol 129:221-231. CrossRef Medline
4. Bruns D, Riedel D, Klingauf J, Jahn R (2000) Quantal release of serotonin. Neuron 28:205-220. CrossRef Medline
5. Chaudhry FA, Reimer RJ, Bellocchio EE, Danbolt NC, Osen KK, Edwards RH, Storm-Mathisen J (1998) The vesicular GABA transporter, VGAT, localizes to synaptic vesicles in sets of glycinergic as well as GABAergic neurons. J Neurosci 18:9733-9750. Medline
6. Chow RH, von Ruden L, Neher E (1992) Delay in vesicle fusion revealed by electrochemical monitoring of single secretory events in adrenal chromaffin cells. Nature 356:60-63. CrossRef Medline
7. 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
8. Contini M, Raviola E (2003) GABAergic synapses made by a retinal dopaminergic neuron. Proc Natl Acad Sci U S A 100:1358-1363. CrossRef Medline
9. Contini M, Lin B, Kobayashi K, Okano H, Masland RH, Raviola E (2010) Synaptic input of ON-bipolar cells onto the dopaminergic neurons of the mouse retina. J Comp Neurol 518:2035-2050. CrossRef Medline
10. de Waele P, De Groote G, Van De Voorde A, Fiers W, Franssen JD, Herion P, Urbain J (1982) Isolation and identification of monoclonal antibodies directed against human placental alkaline phosphatase. Arch Int Physiol Biochim 90:B21.
11. Edwards RH (2007) The neurotransmitter cycle and quantal size. Neuron 55:835-858. CrossRef Medline
12. Eliasson L, Abdulkader F, Braun M, Galvanovskis J, Hoppa MB, Rorsman P (2008) Novel aspects of the molecular mechanisms controlling insulin secretion. J Physiol 586:3313-3324. CrossRef Medline
13. Farajian R, Pan F, Akopian A, Völgyi B, Bloomfield SA (2011) Masked excitatory crosstalk between the ON and OFF visual pathways in the mammalian retina. J Physiol 589:4473-4489. CrossRef Medline
14. Fattorini G, Verderio C, Melone M, Giovedì S, Benfenati F, Matteoli M, Conti F (2009) VGLUT1 and VGAT are sorted to the same population of synaptic vesicles in subsets of cortical axon terminals. J Neurochem 110:1538-1546. CrossRef Medline
15. Feigenspan A, Gustincich S, Bean BP, Raviola E (1998) Spontaneous activity of solitary dopaminergic cells of the retina. J Neurosci 18:6776-6789. Medline
16. Gustincich S, Feigenspan A, Wu DK, Koopman LJ, Raviola E (1997) Control of dopamine release in the retina: a transgenic approach to neural networks. Neuron 18:723-736. CrossRef Medline
17. Gustincich S, Contini M, Gariboldi M, Puopolo M, Kadota K, Bono H, Le-Mieux J, Walsh P, Carninci P, Hayashizaki Y, Okazaki Y, Raviola E (2004) Gene discovery in genetically labeled singe dopaminergic neurons of the retina. Proc Natl Acad Sci U S A 101:5069-5074. CrossRef Medline
18. Hirasawa H, Puopolo M, Raviola E (2009) Extrasynaptic release of GABA by retinal dopaminergic neurons. J Neurophysiol 102:146-158. CrossRef Medline
19. Hnasko TS, Edwards RH (2012) Neurotransmitter corelease: mechanism and physiological role. Annu Rev Physiol 74:225-243. CrossRef Medline
20. Hochstetler SE, Puopolo M, Gustincich S, Raviola E, Wightman RM (2000) Real-time amperometric measurements of zeptomole quantities of dopamine released from neurons. Anal Chem 72:489-496. CrossRef Medline
21. Hua Z, Leal-Ortiz S, Foss SM, Waites CL, Garner CC, Voglmaier SM, Edwards RH (2011) v-SNARE composition distinguishes synaptic vesicle pools. Neuron 71:474-487. CrossRef Medline
22. Jonas P, Bischofberger J, Sandkuhler J (1998) Corelease of two fast neurotransmitters at a central synapse. Science 281:419-424. CrossRef Medline
23. Joyce MP, Rayport S (2000) Mesoaccumbens dopamine neuron synapses reconstructed in vitro are glutamatergic. Neuroscience 99:445-456. CrossRef Medline
24. Lee S, Kim K, Zhou ZJ (2010) Role of ACh-GABA cotransmission in detecting image motion and motion direction. Neuron 68:1159-1172. CrossRef Medline
25. Liang KY, Zeger SL (1986) Longitudinal data analysis using generalized linear models. Biometrika 73:13-22. CrossRef
26. Li WC, Soffe SR, Roberts A (2004) Glutamate and acetylcholine corelease at developing synapses. Proc Natl Acad Sci U S A 101:15488-15493. CrossRef Medline
27. Maher BJ, Westbrook GL (2008) Co-transmission of dopamine and GABA in periglomerular cells. J Neurophysiol 99:1559-1564. CrossRef Medline
28. Nirenberg MJ, Chan J, Liu Y, Edwards RH, Pickel VM (1996) Ultrastructural localization of the vesicular monoamine transporter-2 in midbrain dopaminergic neurons: potential sites for somatodendritic storage and release of dopamine. J Neurosci 16:4135-4145. Medline
29. Nirenberg MJ, Chan J, Liu Y, Edwards RH, Pickel VM (1997) Vesicular monoamine transporter-2: immunogold localization in striatal axons and terminals. Synapse 26:194-198. CrossRef Medline
30. O'Brien JA, Berger AJ (1999) Cotransmission of GABA and glycine to brain stem motoneurons. J Neurophysiol 82:1638-1641. Medline
31. Onoa B, Li H, Gagnon-Bartsch JA, Elias LA, Edwards RH (2010) Vesicular monoamine and glutamate transporters select distinct synaptic vesicle recycling pathways. J Neurosci 30:7917-7927. CrossRef Medline
32. 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
33. Roska B, Werblin F (2001) Vertical interactions across ten parallel, stacked representations in the mammalian retina. Nature 410:583-587. CrossRef Medline
34. Saheki Y, De Camilli P (2012) Synaptic vesicle endocytosis. Cold Spring Harbor Perspect Biol. Advance online publication. Retrieved August 12, 2012. CrossRef Medline
35. Seal RP, Edwards RH (2006) Functional implications of neurotransmitter co-release: glutamate and GABA share the load. Curr Opin Pharmacol 6:114-119. CrossRef Medline
36. Stuber GD, Hnasko TS, Britt JP, Edwards RH, Bonci A (2010) Dopaminergic terminals in the nucleus accumbens but not the dorsal striatum corelease glutamate. J Neurosci 30:8229-8233. CrossRef Medline
37. Sulzer D, Joyce MP, Lin L, Geldwert D, Haber SN, Hattori T, Rayport S (1998) Dopamine neurons make glutamatergic synapses in vitro. J Neurosci 18:4588-4602. Medline
38. Takamori S, Rhee JS, Rosenmund C, Jahn R (2000) Identification of a vesicular glutamate transporter that defines a glutamatergic phenotype in neurons. Nature 407:189-194. CrossRef Medline
39. Takamori S, Rhee JS, Rosenmund C, Jahn R (2001) Identification of differentiation-associated brain-specific phosphate transporter as a second vesicular glutamate transporter (VGLUT2). J Neurosci 21:RC182. Medline
40. Takamori S, Holt M, Stenius K, Lemke EA, Grønborg M, Riedel D, Urlaub H, Schenck S, Brugger B, Ringler P, Muller SA, Rammner B, Gräter F, Hub JS, De Groot BL, Mieskes G, Moriyama Y, Klingauf J, Grubmuller H, Heuser J, Wieland F, Jahn R (2006) Molecular anatomy of a trafficking organelle. Cell 127:831-846. CrossRef Medline
41. Tan PK, Waites C, Liu Y, Krantz DE, Edwards RH (1998) A leucine-based motif mediates the endocytosis of vesicular monoamine and acetylcholine transporters. J Biol Chem 273:17351-17360. CrossRef Medline
42. Tsen G, Williams B, Allaire P, Zhou YD, Ikonomov O, Kondova I, Jacob MH (2000) Receptors with opposing functions are in postsynaptic microdomains under one presynaptic terminal. Nat Neurosci 3:126-132. CrossRef Medline
43. Voglmaier SM, Kam K, Yang H, Fortin DL, Hua Z, Nicoll RA, Edwards RH (2006) Distinct endocytic pathways control the rate and extent of synaptic vesicle protein recycling. Neuron 51:71-84. CrossRef Medline
44. Whim MD (2006) Near simultaneous release of classical and peptide cotransmitters from chromaffin cells. J Neurosci 26:6637-6642. CrossRef Medline
45. 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
46. Witkovsky P (2004) Dopamine and retinal function. Doc Ophthalmol 108:17-40. CrossRef Medline
47. Wojcik SM, Katsurabayashi S, Guillemin I, Friauf E, Rosenmund C, Brose N, Rhee JS (2006) A shared vesicular carrier allows synaptic corelease of GABA and glycine. Neuron 50:575-587. CrossRef Medline
48. Xin D, Bloomfield SA (1999) Comparison of the responses of AII amacrine cells in the dark-and light-adapted rabbit retina. Vis Neurosci 16:653-665. CrossRef Medline