Synaptically driven endocannabinoid release requires Ca2+- assisted metabotropic glutamate receptor subtype 1 to phospholipase C β4 signaling cascade in the cerebellum

Journal of Neuroscience

Volumn 25, Issue 29, 2005, Pages 6826-6835

  Maejima, Takashi ^a,b   Oka, Saori ^c   Hashimotodani, Yuki ^a   Ohno Shosaku, Takako ^a   Aiba, Atsu ^d   Wu, Dianqing ^e   Waku, Keizo ^c   Sugiura, Takayuki ^c   Kano, Masanobu ^a  

^a KANAZAWA UNIVERSITY   (Japan)

^b NATIONAL INSTITUTE FOR PHYSIOLOGICAL SCIENCES   (Japan)

^c TEIKYO UNIVERSITY   (Japan)

^d KOBE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^e UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

2 arachidonoylglycerol; Calcium; Metabotropic glutamate receptor type 1; Phospholipase C 4; Purkinje cell; Retrograde signaling

Indexed keywords

2 ARACHIDONOYLGLYCEROL; CALCIUM ION; ENDOCANNABINOID; G PROTEIN COUPLED RECEPTOR; METABOTROPIC RECEPTOR 1; PHOSPHOLIPASE C BETA4; RECEPTOR SUBTYPE;

ANIMAL TISSUE; ARTICLE; BRAIN REGION; BRAIN SLICE; CALCIUM CELL LEVEL; CENTRAL NERVOUS SYSTEM; CEREBELLUM; CONTROLLED STUDY; DEPOLARIZATION; EXCITATORY POSTSYNAPTIC POTENTIAL; INHIBITORY POSTSYNAPTIC POTENTIAL; MOUSE; NERVE FIBER; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PURKINJE CELL; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION; SYNAPSE; SYNAPTIC TRANSMISSION;

ANIMALS; ARACHIDONIC ACIDS; CALCIUM; CEREBELLUM; ENDOCANNABINOIDS; GLYCERIDES; HIPPOCAMPUS; ISOENZYMES; MEMBRANE POTENTIALS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEURONAL PLASTICITY; ORGAN CULTURE TECHNIQUES; PATCH-CLAMP TECHNIQUES; PHOSPHOLIPASE C; PURKINJE CELLS; RECEPTORS, METABOTROPIC GLUTAMATE; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 22544438407     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0945-05.2005     Document Type: Article

References (59)

1. Aiba A, Kano M, Chen C, Stanton ME, Fox GD, Herrup K, Zwingman TA, Tonegawa S (1994) Deficient cerebellar long-term depression and impaired motor learning in mGluR1 mutant mice. Cell 79:377-388.
2. Alger BE (2002) Retrograde signaling in the regulation of synaptic transmission: focus on endocannabinoids. Prog Neurobiol 68:247-286.
3. Bisogno T, Howell F, Williams G, Minassi A, Cascio MG, Ligresti A, Matias I, Schiano-Moriello A, Paul P, Williams EJ, Gangadharan U, Hobbs C, Di Marzo V, Doherty P (2003) Cloning of the first sn1-DAG lipases points to the spatial and temporal regulation of endocannabinoid signaling in the brain. J Cell Biol 163:463-468.
4. Brenowitz SD, Regehr WG (2003) Calcium dependence of retrograde inhibition by endocannabinoids at synapses onto Purkinje cells. J Neurosci 23:6373-6384.
5. Brenowitz SD, Regehr WG (2005) Associative short-term synaptic plasticity mediated by endocannabinoids. Neuron 45:419-431.
6. Brown SP, Brenowitz SD, Regehr WG (2003) Brief presynaptic bursts evoke synapse-specific retrograde inhibition mediated by endogenous cannabinoids. Nat Neurosci 6:1048-1057.
7. Chevaleyre V, Castillo PE (2003) Heterosynaptic LTD of hippocampal GABAergic synapses: a novel role of endocannabinoids in regulating excitability. Neuron 38:461-472.
8. Conquet F, Bashir ZI, Davies CH, Daniel H, Ferraguti F, Bordi F, Franz-Bacon K, Reggiani A, Matarese V, Conde F, Collingridge GL, Crepel F (1994) Motor deficit and impairment of synaptic plasticity in mice lacking mGluR1. Nature 372:237-243.
9. Devane WA, Hanus L, Breuer A, Pertwee RG, Stevenson LA, Griffin G, Gibson D, Mandelbaum A, Etinger A, Mechoulam R (1992) Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science 258:1946-1949.
10. Diana MA, Levenes C, Mackie K, Marty A (2002) Short-term retrograde inhibition of GABAergic synaptic currents in rat Purkinje cells is mediated by endogenous cannabinoids. J Neurosci 22:200-208.
11. Di Marzo V, Fontana A, Cadas H, Schinelli S, Cimino G, Schwartz JC, Piomelli D (1994) Formation and inactivation of endogenous cannabinoid anandamide in central neurons. Nature 372:686-691.
12. 3-mediated indirect suppression through endocannabinoid signalling. Eur J Neurosci 19:2682-2692.
13. Galante M, Diana MA (2004) Group I metabotropic glutamate receptors inhibit GABA release at interneuron-Purkinje cell synapses through endocannabinoid production. J Neurosci 24:4865-4874.
14. Gerdeman GL, Lovinger DM (2003) Emerging roles for endocannabinoids in long-term synaptic plasticity. Br J Pharmacol 140:781-789.
15. Gerdeman GL, Ronesi J, Lovinger DM (2002) Postsynaptic endocannabinoid release is critical to long-term depression in the striatum. Nat Neurosci 5:446-451.
16. 2+ indicators with greatly improved fluorescence properties. J Biol Chem 260:3440-3450.
17. Hashimoto K, Kano M (2003) Functional differentiation of multiple climbing fiber inputs during synapse elimination in the developing cerebellum. Neuron 38:785-796.
18. Hashimoto K, Miyata M, Watanabe M, Kano M (2001) Roles of phospholipase C β4 in synapse elimination and plasticity in developing and mature cerebellum. Mol Neurobiol 23:69-82.
19. 2+ dependency for triggering retrograde endocannabinoid signal. Neuron 45:257-268.
20. Howlett AC, Barth F, Bonner TI, Cabral G, Casellas P, Devane WA, Felder CC, Herkenham M, Mackie K, Martin BR, Mechoulam R, Pertwee RG (2002) International union of pharmacology. XXVII. Classification of cannabinoid receptors. Pharmacol Rev 54:161-202.
21. Ichise T, Kano M, Hashimoto K, Yanagihara D, Nakao K, Shigemoto R, Katsuki M, Aiba A (2000) mGluR1 in cerebellar Purkinje cells essential for long-term depression, synapse elimination, and motor coordination. Science 288:1832-1835.
22. Jiang H, Lyubarsky A, Dodd R, Vardi N, Pugh E, Baylor D, Simon MI, Wu D (1996) Phospholipase C β4 is involved in modulating the visual response in mice. Proc Natl Acad Sci USA 93:14598-14601.
23. Kano M, Hashimoto K, Kurihara H, Watanabe M, Inoue Y, Aiba A, Tonegawa S (1997) Persistent multiple climbing fiber innervation of cerebellar Purkinje cells in mice lacking mGluR1. Neuron 18:71-79.
24. Kano M, Hashimoto K, Watanabe M, Kurihara H, Offermanns S, Jiang H, Wu Y, Jun K, Shin HS, Inoue Y, Simon MI, Wu D (1998) Phospholipase C β4 is specifically involved in climbing fiber synapse elimination in the developing cerebellum. Proc Natl Acad Sci USA 95:15724-15729.
25. Kim J, Alger BE (2004) Inhibition of cyclooxygenase-2 potentiates retrograde endocannabinoid effects in hippocampus. Nat Neurosci 7:697-698.
26. Kim J, Isokawa M, Ledent C, Alger BE (2002) Activation of muscarinic acetylcholine receptors enhances the release of endogenous cannabinoids in the hippocampus. J Neurosci 22:10182-10191.
27. Kondo S, Sugiura T, Kodaka T, Kudo N, Waku K, Tokumura A (1998a) Accumulation of various N-acylethanolamines including N-arachidonoylethanolamine (anandamide) in cadmium chloride-administered rat testis. Arch Biochem Biophys 354:303-310.
28. 2+-dependent and -independent mechanisms. FEBS Lett 429:152-156.
29. 2+ oscillations in mouse eggs. J Biol Chem 279:10408-10412.
30. Kreitzer AC, Regehr WG (2001a) Retrograde inhibition of presynaptic calcium influx by endogenous cannabinoids at excitatory synapses onto Purkinje cells. Neuron 29:717-727.
31. Kreitzer AC, Regehr WG (2001b) Cerebellar depolarization-induced suppression of inhibition is mediated by endogenous cannabinoids. J Neurosci 21:RC174(1-5).
32. Llano I, Leresche N, Marty A (1991) Calcium entry increases the sensitivity of cerebellar Purkinje cells to applied GABA and decreases inhibitory synaptic currents. Neuron 6:565-574.
33. Maejima T, Ohno-Shosaku T, Kano M (2001a) Endogenous cannabinoid as a retrograde messenger from depolarized postsynaptic neurons to presynaptic terminals. Neurosci Res 40:205-210.
34. Maejima T, Hashimoto K, Yoshida T, Aiba A, Kano M (2001b) Presynaptic inhibition caused by retrograde signal from metabotropic glutamate to cannabinoid receptors. Neuron 31:463-475.
35. Marsicano G, Wotjak CT, Azad SC, Bisogno T, Rammes G, Cascio MG, Hermann H, Tang J, Hofmann C, Zieglgansberger W, Di Marzo V, Lutz B (2002) The endogenous cannabinoid system controls extinction of aversive memories. Nature 418:530-534.
36. Martin LJ, Blackstone CD, Huganir RL, Price DL (1992) Cellular localization of a metabotropic glutamate receptor in rat brain. Neuron 9:259-270.
37. Mechoulam R, Ben-Shabat S, Hanus L, Ligumsky M, Kaminski NE, Schatz AR, Gopher A, Almog S, Martin BR, Compton DR, Pertwee RG, Griffin G, Bayewitch M, Barg J, Vogel Z (1995) Identification of an endogenous 2-monoglyceride, present in canine gut, that binds to cannabinoid receptors. Biochem Pharmacol 50:83-90.
38. Miyata M, Kim HT, Hashimoto K, Lee TK, Cho SY, Jiang H, Wu Y, Jun K, Wu D, Kano M, Shin HS (2001) Deficient long-term synaptic depression in the rostral cerebellum correlated with impaired motor learning in phospholipase C β4 mutant mice. Eur J Neurosci 13:1945-1954.
39. Neale SA, Garthwaite J, Batchelor AM (2001) mGlu1 receptors mediate a post-tetanic depression at parallel fibre-Purkinje cell synapses in rat cerebellum. Eur J Neurosci 14:1313-1319.
40. Offermanns S, Hashimoto K, Watanabe M, Sun W, Kurihara H, Thompson RF, Inoue Y, Kano M, Simon MI (1997) Impaired motor coordination and persistent multiple climbing fiber innervation of cerebellar Purkinje cells in mice lacking Gαq. Proc Natl Acad Sci USA 94:14089-14094.
41. Ohno-Shosaku T, Maejima T, Kano M (2001) Endogenous cannabinoids mediate retrograde signals from depolarized postsynaptic neurons to presynaptic terminals. Neuron 29:729-738.
42. Ohno-Shosaku T, Shosaku J, Tsubokawa H, Kano M (2002) Cooperative endocannabinoid production by neuronal depolarization and group I metabotropic glutamate receptor activation. Eur J Neurosci 15:953-961.
43. 3 receptors are responsible for the muscarinic enhancement of retrograde endocannabinoid signalling in the hippocampus. Eur J Neurosci 18:109-116.
44. Piomelli D (2003) The molecular logic of endocannabinoid signalling. Nat Rev Neurosci 4:873-884.
45. Rebecchi MJ, Pentyala SN (2000) Structure, function, and control of phosphoinositide-specific phospholipase C. Physiol Rev 80:1291-1335.
46. Rhee SG (2001) Regulation of phosphoinositide-specific phospholipase C. Annu Rev Biochem 70:281-312.
47. Robbe D, Kopf M, Remaury A, Bockaert J, Manzoni OJ (2002) Endogenous cannabinoids mediate long-term synaptic depression in the nucleus accumbens. Proc Natl Acad Sci USA 99:8384-8388.
48. Stella N, Piomelli D (2001) Receptor-dependent formation of endogenous cannabinoids in cortical neurons. Eur J Pharmacol 425:189-196.
49. Stella N, Schweitzer P, Piomelli D (1997) A second endogenous cannabinoid that modulates long-term potentiation. Nature 388:773-778.
50. Sugiura T, Waku K (2000) 2-Arachidonoylglycerol and the cannabinoid receptors. Chem Phys Lipids 108:89-106.
51. Sugiura T, Kondo S, Sukagawa A, Nakane S, Shinoda A, Itoh K, Yamashita A, Waku K (1995) 2-Arachidonoylglycerol: a possible endogenous cannabinoid receptor ligand in brain. Biochem Biophys Res Commun 215:89-97.
52. Sugiura T, Yoshinaga N, Kondo S, Waku K, Ishima Y (2000) Generation of 2-arachidonoylglycerol, an endogenous cannabinoid receptor ligand, in picrotoxinin-administered rat brain. Biochem Biophys Res Commun 271:654-658.
53. Takechi H, Eilers J, Konnerth A (1998) A new class of synaptic response involving calcium release in dendritic spines. Nature 396:757-760.
54. Varma N, Carlson GC, Ledent C, Alger BE (2001) Metabotropic glutamate receptors drive the endocannabinoid system in hippocampus. J Neurosci 21:RC188(1-5).
55. Wang J, Zucker RS (2001) Photolysis-induced suppression of inhibition in rat hippocampal CA1 pyramidal neurons. J Physiol (Lond) 533:757-763.
56. Watanabe M, Nakamura M, Sato K, Kano M, Simon MI, Inoue Y (1998) Patterns of expression for the mRNA corresponding to the four isoforms of phospholipase Cβ in mouse brain. Eur J Neurosci 10:2016-2025.
57. Wilson RI, Nicoll RA (2001) Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses. Nature 410:588-592.
58. Wilson RI, Nicoll RA (2002) Endocannabinoid signaling in the brain. Science 296:678-682.
59. Yoshida T, Hashimoto K, Zimmer A, Maejima T, Araishi K, Kano M (2002) The cannabinoid CB1 receptor mediates retrograde signals for depolarization-induced suppression of inhibition in cerebellar Purkinje cells. J Neurosci 22:1690-1697.