Role of the vesicular transporter VGLUT3 in retrograde release of glutamate by cerebellar Purkinje cells

Journal of Neurophysiology

Volumn 105, Issue 3, 2011, Pages 1023-1032

  Crépe, Françis ^a   Galante, Micaela ^a   Habbas, Samia ^a   McLean, Heather ^a   Danie, Hervé ^a  

^a CNRS   (France)

Author keywords

Depolarization; Parallel fibers; Postsynaptic currents

Indexed keywords

GLUTAMATE TRANSPORTER; GLUTAMIC ACID; N ETHYLMALEIMIDE; NEUROTRANSMITTER; VESICULAR GLUTAMATE TRANSPORTER 3;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CEREBELLUM; CONCENTRATION (PARAMETERS); EXTRACELLULAR SPACE; FACILITATION; MOUSE; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; PULSE RATE; PURKINJE CELL;

AMINO ACID TRANSPORT SYSTEMS, ACIDIC; ANIMALS; CELLS, CULTURED; GLUTAMIC ACID; MICE; MICE, KNOCKOUT; NEUROTRANSMITTER AGENTS; PURKINJE CELLS; SYNAPTIC TRANSMISSION;

EID: 79955156547     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00736.2010     Document Type: Article

References (48)

1. Atluri P, Regehr WG. Determinants of the time course of facilitation at the Granule cell to Purkinje cell synapse. J Neurosci 16: 5661-5671, 1996.
2. Baker DA, Xi ZX, Shen H, Swanson CJ, Kalivas PW. The origin and neuronal function of in vivo nonsynaptic glutamate. J Neurosci 22: 9134-9141, 2002.
3. Bergles DE, Dzubay JA, Jahr CE. Glutamate transporter currents in Bergmann glial cells follow the time course of extrasynaptic glutamate. Proc Natl Acad Sci USA 94: 14821-14825, 1997.
4. Boulland JL, Qureshi T, Seal RP, Rafiki A, Gundersen V, Bergersen LH, Fremeau RT Jr, Edwards RH, Storm-Mathisen J, Chaudhry FA. Expression of the vesicular glutamate transporters during development indicates the widespread corelease of multiple neurotransmitters. J Comp Neurol 480: 264-280, 2004.
5. Brenowitz SD, Regehr WG. Calcium dependence of retrograde inhibition by endocannabinoids at synapses onto Purkinje cells. J Neurosci 23: 6373-6384, 2003.
6. Cho K, Francis JC, Hirbec H, Dev K, Brown MW, Henley JM, Bashir ZI. Regulation of kainate receptors by protein kinase C and metabotropic glutamate receptors. J Physiol 548: 723-730, 2003.
7. Clark BA, Barbour B. Currents evoked in Bergmann glial cells by parallel fibre stimulation in rat cerebellar slices. J Physiol 502: 335-350, 1997.
8. Clements JD, Bekkers JM. Detection of spontaneous synaptic events with an optimally scaled template. Biophys J 73: 220-229, 1997.
9. Crépel F. Regression of functional synapses in the immature mammalian cerebellum. Trends Neurosci 5: 266-269, 1982.
10. Crépel F. Developmental changes in retrograde messengers involved in depolarization-induced suppression of excitation at parallel fiber-purkinje cell synapses in rodents. J Neurophysiol 97: 824-836, 2007.
11. Crépel F. Role of presynaptic kainate receptors at parallel fiber-Purkinje cell synapses in induction of cerebellar LTD; interplay with climbing fiber input. J Neurophysiol 102: 965-973, 2009.
12. Crépel F, Daniel H. Developmental changes in agonist-induced retrograde signaling at parallel fiber-Purkinje cell synapses: role of calcium-induced calcium release. J Neurophysiol 98: 2550-2565, 2007.
13. Cossart R, Epsztein J, Tyzio R, Becq H, Hirsch J, Ben-Ari Y, Crepel V. Quantal release of glutamate generates pure kainate and mixed AMPA/ kainate EPSCs in hippocampal neurons. Neuron 35: 147-159, 2002.
14. Daniel H, Levenes C, Fagni L, Conquet F, Bockaert J, Crépel F. Inositol- 1,4,5-trisphosphate-mediated rescue of cerebellar long-term depression in subtype 1 metabotropic glutamate receptor mutant mouse. Neuroscience 92: 1-6, 1999.
15. Delaney AJ, Jahr CE. Kainate receptors differentially regulate release at two parallel fiber synapses. Neuron 36: 476-482, 2002.
16. DeVries SH. Bipolar cells use kainate and AMPA receptors to filter visual information into separate channels. Neuron 28: 847-856, 2000.
17. Diana MA, Levenes C, Mackie K, Marty A. Short-term retrograde inhibition of GABAergic synaptic currents in rat Purkinje cells is mediated by endogenous cannabinoids. J Neurosci 22: 200-208, 2002.
18. Duguid IC, Smart TG. Retrograde activation of pre-synaptic NMDA receptors enhances GABA release at cerebellar interneuron-Purkinje cell synapses. Nat Neurosci 7: 525-533, 2004.
19. Duguid IC, Pankratov Y, Moss GW, Smart TG. Somatodendritic release of glutamate regulates synaptic inhibition in cerebellar Purkinje cells via autocrine mGluR1 activation. J Neurosci 27: 12464-12474, 2007.
20. Epsztein J, Represa A, Jorquera I, Ben-Ari Y, Crepel V. Recurrent mossy fibers establish aberrant kainate receptor-operated synapses on granule cells from epileptic rats. J Neurosci 25: 8229-8239, 2005.
21. Glitsch M, Parra P, Llano I. The retrograde inhibition of IPSCs in rat cerebellar purkinje cells is highly sensitive to intracellular Calcium. Eur J Neurosci 12: 987-993, 2000.
22. Gras C, Vinatier J, Amilhon B, Guerci A, Christov C, Ravassard P, Giros B, El Mestikawy S. Developmentally regulated expression of VGLUT3 during early postnatal life. Neuropharmacology 49: 901-911, 2005.
23. Harkany T, Holmgren C, Härtig W, Qureshi T, Chaudhry FA, Storm- Mathisen J, Dobszay MB, Berghuis P, Schulte G, Sousa KM, Fremeau RT Jr, Edwards RH, Mackie K, Ernfors P, Zilberter Y. Endocannabinoid- independent retrograde signaling at inhibitory synapses in layer 2/3 of neocortex: involvement of vesicular glutamate transporter 3. J Neurosci 24: 4978-4988, 2004.
24. Jabaudon A, Shimamoto K, Yasuda-Kamatani Y, Scanziani M, Gähwiler BH, Gerber U. Inhibition of uptake unmasks rapid extracellular turnover of glutamate of nonvesicular origin. Proc Natl Acad Sci USA 96: 8733-8738, 1999.
25. Kano M, Rexhausen U, Dreessen J, Konnerth A. Synaptic excitation produces a long-lasting rebound potentiation of inhibitory synaptic signals in cerebellar Purkinje cells. Nature 356: 601-604, 1992.
26. Kim J, Alger BE. Random response fluctuations lead to spurious paired-pulse facilitation. J Neurosci 21: 9608-9618, 2001.
27. Kim YS, Shin JH, Hall FS, Linden DJ. Dopamine signaling is required for depolarization-induced slow current in cerebellar Purkinje cells. J Neurosci 29: 8530-8538, 2009.
28. Kreitzer AC, Regehr WG. Cerebellar depolarization-induced suppression of inhibition is mediated by endogenous cannabinoids. J Neurosci 21: 1-5, 2001a.
29. Kreitzer AC, Regehr WG. Retrograde inhibition of pre-synaptic calcium influx by endogenous cannabinoids at excitatory synapses onto Purkinje cells. Neuron 29: 717-727, 2001b.
30. Levenes C, Daniel H, Crépel F. Retrograde modulation of transmitter release by post-synaptic subtype 1 metabotropic glutamate receptors in the rat cerebellum. J Physiol 537: 125-140, 2001.
31. Levenes C, Daniel H, Soubrie P, Crépel F. Cannabinoids decrease excitatory synaptic transmission and impair long- term depression in rat cerebellar Purkinje cells. J Physiol 510: 867-879, 1998.
32. Li P, Wilding TJ, Kim SJ, Calejesan AA, Huettner JE, Zhuo M. Kainatereceptor- mediated sensory synaptic transmission in mammalian spinal cord. Nature 397: 161-164, 1999.
33. Llano I, Leresche N, Marty A. Calcium entry increases the sensitivity of cerebellar Purkinje cells to applied GABA and decreases inhibitory synaptic currents. Neuron 6: 565-574, 1991a.
34. Llano I, Marty A, Armstrong C, Konnerth A. Synaptic- and agonistinduced excitatory currents of Purkinje cells in rat cerebellar slices. J Physiol 434: 183-213, 1991b.
35. McNaughton B. Long-term synaptic enhancement and short-term potentiation in rat fascia dentata act through different mechanisms. J Physiol 324: 249-262, 1982.
36. Ohno-Shosaku T, Maejima T, Kano M. Endogenous cannabinoids mediate retrograde signals from depolarized post-synaptic neurons to pre-synaptic terminals. Neuron 29: 729-738, 2001.
37. Petitet F, Marin L, Doble A. Biochemical and pharmacological characterization of cannabinoid binding sites using [3H]SR141716A. Neuroreport 7: 789-792, 1996.
38. Pitler TA, Alger BE. Post-synaptic spike firing reduces synaptic GABAA responses in hippocampal pyramidal cells. J Neurosci 12: 4122-4132, 1992.
39. Pitler TA, Alger BE. Depolarization-induced suppression of GABAergic inhibition in rat hippocampal pyramidal cells: G protein involvement in a pre-synaptic mechanism. Neuron 13: 1447-1455, 1994.
40. Rabacchi S, Bailly Y, Delhaye-Bouchaud N, Mariani J. Involvement of the N-methyl D-aspartate (NMDA) receptor in synapse elimination during cerebellar development. Science 256: 1823-1825, 1992.
41. Safo PK, Regehr WG. Endocannabinoids control the induction of cerebellar LTD. Neuron 48: 647-659, 2005.
42. Schultz P, Cook E, Johnston D. Changes in paired-pulse facilitation suggest pre-synaptic involvement in long-term potentiation. J Neurosci 14: 5325-5337, 1994.
43. Shin JH, Kim YS, Linden DJ. Dendritic glutamate release produces autocrine activation of mGluR1 in cerebellar Purkinje cells. Proc Natl Acad Sci USA 105: 746-750, 2008.
44. Vincent SR, Kimura H. Histochemical mapping of nitric oxide synthase in the rat brain. Neuroscience 46: 755-784, 1992.
45. Wang J, Zucker RS. Photolysis-induced suppression of inhibition in rat hippocampal CA1 pyramidal neurons. J Physiol 533: 757-763, 2001.
46. Wilson RI, Kunos G, Nicoll RA. Pre-synaptic specificity of endocannabinoid signaling in the hippocampus. Neuron 31: 453-462, 2001.
47. Zhou LM, Gu ZQ, Costa AM, Yamada KA, Mansson PE, Giordano T, Skolnick P, Jones KA. (2S,4R)-4-Methylglutamic acid (SYM 2081): a selective, high-affinity ligand for kainate receptors. Pharmacology 280: 422-427, 1997.
48. Zilberter Y. Dendritic release of glutamate suppresses synaptic inhibition of pyramidal neurons in rat neocortex. J Physiol 528:489-496, 2000.