Depression of release by mGluR8 Alters Ca 2+ dependence of release machinery

Cerebral Cortex

Volumn 22, Issue 7, 2012, Pages 1498-1509

  Erdmann, Evelyn ^a,b   Rupprecht, Vanessa ^a   Matthews, Elizabeth ^a   Kukley, Maria ^a,c   Schoch, Susanne ^a   Dietrich, Dirk ^a  

^a UNIVERSITY HOSPITAL BONN   (Germany)

^b UNIVERSITY HOSPITAL FRANKFURT   (Germany)

^c UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

calcium; metabotropic glutamate receptor; presynaptic; release machinery; transmitter release

Indexed keywords

ADENYLATE CYCLASE; CALCIUM ION; GLUTAMIC ACID; GUANINE NUCLEOTIDE BINDING PROTEIN; METABOTROPIC RECEPTOR 8; OMEGA CONOTOXIN GVIA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALCIUM TRANSPORT; ENZYME INHIBITION; HIPPOCAMPUS; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECRETION; QUANTITATIVE ANALYSIS; RAT; SYNAPSE; SYNAPTIC TRANSMISSION;

ANIMALS; CALCIUM; CALCIUM SIGNALING; CELLS, CULTURED; COMPUTER SIMULATION; EXCITATORY POSTSYNAPTIC POTENTIALS; GLUTAMIC ACID; HIPPOCAMPUS; MALE; MODELS, NEUROLOGICAL; NEURAL INHIBITION; RATS; RATS, WISTAR; RECEPTORS, METABOTROPIC GLUTAMATE; SYNAPSES;

EID: 84862862051     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhr217     Document Type: Article

References (63)

1. Akaike N, Lee KS, Brown AM. 1978. The calcium current of Helix neuron. J Gen Physiol. 71:509-531.
2. Anwyl R. 1999. Metabotropic glutamate receptors: electrophysiological properties and role in plasticity. Brain Res Brain Res Rev. 29:83-120.
3. Bedingfield JS, Kemp MC, Jane DE, Tse HW, Roberts PJ, Watkins JC. 1995. Structure-activity relationships for a series of phenylglycine derivatives acting at metabotropic glutamate receptors (mGluRs). Br J Pharmacol. 116:3323-3329.
4. Blackmer T, Larsen EC, Takahashi M, Martin TF, Alford S, Hamm HE. 2001. G protein betagamma subunit-mediated presynaptic inhibition: regulation of exocytotic fusion downstream of Ca2+ entry. Science. 292:293-297.
5. Bollmann JH, Sakmann B, Borst JG. 2000. Calcium sensitivity of glutamate release in a calyx-type terminal. Science. 289:953-957.
6. Bushell TJ, Jane DE, Tse HW, Watkins JC, Davies CH, Garthwaite J, Collingridge GL. 1995. Antagonism of the synaptic depressant actions of L-AP4 in the lateral perforant path by MAP4. Neuropharmacology. 34:239-241.
7. Bushell TJ, Jane DE, Tse HW, Watkins JC, Garthwaite J, Collingridge GL. 1996. Pharmacological antagonism of the actions of group II and III mGluR agonists in the lateral perforant path of rat hippocampal slices. Br J Pharmacol. 117:1457-1462.
8. Byrne JH, Kandel ER. 1996. Presynaptic facilitation revisited: state and time dependence. J Neurosci. 16:425-435.
9. Carbone E, Lux HD. 1987. Kinetics and selectivity of a low-voltageactivated calcium current in chick and rat sensory neurones. J Physiol (Lond). 386:547-570.
10. Clements JD, Bekkers JM. 1997. Detection of spontaneous synaptic events with an optimally scaled template. Biophys J. 73:220-229.
11. Cochilla AJ, Alford S. 1998. Metabotropic glutamate receptor-mediated control of neurotransmitter release. Neuron. 20:1007-1016.
12. Collin T, Marty A, Llano I. 2005. Presynaptic calcium stores and synaptic transmission. Curr Opin Neurobiol. 15:275-281.
13. Conn PJ, Pin JP. 1997. Pharmacology and functions of metabotropic glutamate receptors. Annu Rev Pharmacol Toxicol. 37:205-237.
14. Delaney AJ, Crane JW, Sah P. 2007. Noradrenaline modulates transmission at a central synapse by a presynaptic mechanism. Neuron. 56:880-892.
15. Dietrich D, Beck H, Kral T, Clusmann H, Elger CE, Schramm J. 1997. Metabotropic glutamate receptors modulate synaptic transmission in the perforant path: pharmacology and localization of two distinct receptors. Brain Res. 767:220-227.
16. Dietrich D, Kirschstein T, Kukley M, Pereverzev A, von der BC, Schneider T, Beck H. 2003. Functional specialization of presynaptic Cav2.3 Ca2+ channels. Neuron. 39:483-496.
17. Dietrich D, Kral T, Clusmann H, Friedl M, Schramm J. 2002. Presynaptic group II metabotropic glutamate receptors reduce stimulated and spontaneous transmitter release in human dentate gyrus. Neuropharmacology. 42:297-305.
18. Dittman JS, Regehr WG. 1998. Calcium dependence and recovery kinetics of presynaptic depression at the climbing fiber to Purkinje cell synapse. J Neurosci. 18:6147-6162.
19. El Far O, Betz H. 2002. G-protein-coupled receptors for neurotransmitter amino acids: C-terminal tails, crowded signalosomes. Biochem J. 365:329-336.
20. Forsythe ID, Tsujimoto T, Barnes-Davies M, Cuttle MF, Takahashi T. 1998. Inactivation of presynaptic calcium current contributes to synaptic depression at a fast central synapse. Neuron. 20:797-807.
21. Friedl M, Clusmann H, Kral T, Dietrich D, Schramm J. 1999. Analysing metabotropic glutamate group III receptor mediated modulation of synaptic transmission in the amygdala-kindled dentate gyrus of the rat. Brain Res. 821:117-123.
22. Geiger JR, Jonas P. 2000. Dynamic control of presynaptic Ca(2+) inflow by fast-inactivating K(+) channels in hippocampal mossy fiber boutons. Neuron. 28:927-939.
23. Gereau RW, Conn PJ. 1995. Multiple presynaptic metabotropic glutamate receptors modulate excitatory and inhibitory synaptic transmission in hippocampal area CA1. J Neurosci. 15:6879-6889.
24. Heidelberger R, Heinemann C, Neher E, Matthews G. 1994. Calcium dependence of the rate of exocytosis in a synaptic terminal. Nature. 371:513-515.
25. Hille B. 1992. Ionic channels of excitable membranes. Sunderland (MA): Sinauer.
26. Hosoi N, Sakaba T, Neher E. 2007. Quantitative analysis of calciumdependent vesicle recruitment and its functional role at the calyx of Held synapse. J Neurosci. 27:14286-14298.
27. Jackson MB, Konnerth A, Augustine GJ. 1991. Action potential broadening and frequency-dependent facilitation of calcium signals in pituitary nerve terminals. Proc Natl Acad Sci USA. 88:380-384.
28. Kamiya H, Ozawa S. 1999. Dual mechanism for presynaptic modulation by axonal metabotropic glutamate receptor at the mouse mossy fibre-CA3 synapse. J Physiol (Lond). 518:497-506.
29. Kukley M, Capetillo-Zarate E, Dietrich D. 2007. Vesicular glutamate release from axons in white matter. Nat Neurosci. 10:311-320.
30. Kupchik YM, Barchad-Avitzur O, Wess J, Ben-Chaim Y, Parnas I, Parnas H. 2011. A novel fast mechanism for GPCR-mediated signal transduction-control of neurotransmitter release. J Cell Biol. 192:137-151.
31. Lou X, Scheuss V, Schneggenburger R. 2005. Allosteric modulation of the presynaptic Ca2+ sensor for vesicle fusion. Nature. 435:497-501.
32. Macek TA, Winder DG, Gereau RW, Ladd CO, Conn PJ. 1996. Differential involvement of group II and group III mGluRs as autoreceptors at lateral and medial perforant path synapses. J Neurophysiol. 76:3798-3806.
33. Manzoni O, Michel JM, Bockaert J. 1997. Metabotropic glutamate receptors in the rat nucleus accumbens. Eur J Neurosci. 9:1514-1523.
34. McNaughton BL. 1980. Evidence for two physiologically distinct perforant pathways to the fascia dentata. Brain Res. 199:1-19.
35. Mintz IM, Sabatini BL, Regehr WG. 1995. Calcium control of transmitter release at a cerebellar synapse. Neuron. 15:675-688.
36. Muller A, Kukley M, Uebachs M, Beck H, Dietrich D. 2007. Nanodomains of single Ca2+ channels contribute to action potential repolarization in cortical neurons. J Neurosci. 27:483-495.
37. Naples MA, Hampson DR. 2001. Pharmacological profiles of the metabotropic glutamate receptor ligands [(3)H]L-AP4 and [(3)H]CPPG. Neuropharmacology. 40:170-177.
38. Nicoll RA, Malenka RC. 1995. Contrasting properties of two forms of long-term potentiation in the hippocampus. Nature. 377:115-118.
39. Parnas H, Parnas I. 2007. The chemical synapse goes electric: Ca2+-and voltage-sensitive GPCRs control neurotransmitter release. Trends Neurosci. 30:54-61.
40. Podlogar M, Dietrich D. 2006. Firing pattern of rat hippocampal neurons: a perforated patch clamp study. Brain Res. 1085:95-101.
41. Poncer JC, Shinozaki H, Miles R. 1995. Dual modulation of synaptic inhibition by distinct metabotropic glutamate receptors in the rat hippocampus. J Physiol (Lond). 485:121-134.
42. Qian J, Noebels JL. 2001. Presynaptic Ca2+ channels and neurotransmitter release at the terminal of a mouse cortical neuron. J Neurosci. 21:3721-3728.
43. Rusakov DA, Fine A. 2003. Extracellular Ca2+ depletion contributes to fast activity-dependent modulation of synaptic transmission in the brain. Neuron. 37:287-297.
44. Rusakov DA, Wuerz A, Kullmann DM. 2004. Heterogeneity and specificity of presynaptic Ca2+ current modulation by mGluRs at individual hippocampal synapses. Cereb Cortex. 14:748-758.
45. Sakaba T, Neher E. 2001. Preferential potentiation of fast-releasing synaptic vesicles by cAMP at the calyx of Held. Proc Natl Acad Sci USA. 98:331-336.
46. Sakaba T, Neher E. 2003. Direct modulation of synaptic vesicle priming by GABA(B) receptor activation at a glutamatergic synapse. Nature. 424:775-778.
47. Scanziani M, Gahwiler BH, Thompson SM. 1995. Presynaptic inhibition of excitatory synaptic transmission by muscarinic and metabotropic glutamate receptor activation in the hippocampus: are Ca2+ channels involved? Neuropharmacology. 34:1549-1557.
48. Schmidt-Hieber C, Jonas P, Bischofberger J. 2007. Subthreshold dendritic signal processing and coincidence detection in dentate gyrus granule cells. J Neurosci. 27:8430-8441.
49. Schneggenburger R, Neher E. 2000. Intracellular calcium dependence of transmitter release rates at a fast central synapse. Nature. 406:889-893.
50. Schoppa NE, Westbrook GL. 1997. Modulation of mEPSCs in olfactory bulb mitral cells by metabotropic glutamate receptors. J Neurophysiol. 78:1468-1475.
51. Schulte G, Fredholm BB. 2002. Diverse inhibitors of intracellular signalling act as adenosine receptor antagonists. Cell Signal. 14:109-113.
52. Segel IH. 1976. Biochemical calculations. New York: John Wiley & Sons.
53. Shigemoto R, Kinoshita A, Wada E, Nomura S, Ohishi H, Takada M, Flor PJ, Neki A, Abe T, Nakanishi S, et al. 1997. Differential presynaptic localization of metabotropic glutamate receptor subtypes in the rat hippocampus. J Neurosci. 17:7503-7522.
54. Sinha SR, Wu LG, Saggau P. 1997. Presynaptic calcium dynamics and transmitter release evoked by single action potentials at mammalian central synapses. Biophys J. 72:637-651.
55. Stevens CF, Wesseling JF. 1998. Activity-dependent modulation of the rate at which synaptic vesicles become available to undergo exocytosis. Neuron. 21:415-424.
56. Takahashi T, Forsythe ID, Tsujimoto T, Barnes-Davies M, Onodera K. 1996. Presynaptic calcium current modulation by a metabotropic glutamate receptor. Science. 274:594-597.
57. Tyler EC, Lovinger DM. 1995. Metabotropic glutamate receptor modulation of synaptic transmission in corticostriatal co-cultures: role of calcium influx. Neuropharmacology. 34:939-952.
58. Wang LY, Kaczmarek LK. 1998. High-frequency firing helps replenish the readily releasable pool of synaptic vesicles. Nature. 394:384-388.
59. Weisskopf MG, Castillo PE, Zalutsky RA, Nicoll RA. 1994. Mediation of hippocampal mossy fiber long-term potentiation by cyclic AMP. Science. 265:1878-1882.
60. Wu LG, Saggau P. 1997. Presynaptic inhibition of elicited neurotransmitter release. Trends Neurosci. 20:204-212.
61. Wu S, Wright RA, Rockey PK, Burgett SG, Arnold JS, Rosteck PR, Jr., Johnson BG, Schoepp DD, Belagaje RM. 1998. Group III human metabotropic glutamate receptors 4, 7 and 8: molecular cloning, functional expression, and comparison of pharmacological properties in RGT cells. Brain Res Mol Brain Res. 53:88-97.
62. Zhai J, Tian MT, Wang Y, Yu JL, Koster A, Baez M, Nisenbaum ES. 2002. Modulation of lateral perforant path excitatory responses by metabotropic glutamate 8 (mGlu8) receptors. Neuropharmacology. 43:223-230.
63. Zucker RS, Regehr WG. 2002. Short-term synaptic plasticity. Annu Rev Physiol. 64:355-405.