Synapse type-independent degradation of the endocannabinoid 2-arachidonoylglycerol after retrograde synaptic suppression

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 30, 2012, Pages 12195-12200

  Tanimura, Asami ^a   Uchigashima, Motokazu ^b   Yamazaki, Maya ^c   Uesaka, Naofumi ^a   Mikuni, Takayasu ^a   Abe, Manabu ^c   Hashimoto, Kouichi ^a,d,e   Watanabe, Masahiko ^b   Sakimura, Kenji ^c   Kano, Masanobu ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b HOKKAIDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c NIIGATA UNIVERSITY   (Japan)

^d HIROSHIMA UNIVERSITY   (Japan)

^e JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Basket cell; Cannabinoid CB1 receptor; Diacylglycerol lipase; Stellate cell; Synaptic transmission

Indexed keywords

2 ARACHIDONOYLGLYCEROL; ACYLGLYCEROL LIPASE; VIRUS VECTOR;

ANIMAL TISSUE; ARTICLE; ASTROCYTE; BERGMAN GLIAL CELL; CEREBELLUM; CEREBELLUM CORTEX; CLIMBING FIBER; CONTROLLED STUDY; GRANULE CELL; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOGOLD ELECTRON MICROSCOPY; LIPID DEGRADATION; MOUSE; NERVE ENDING; NERVE FIBER C; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PURKINJE CELL; RETROGRADE SYNAPTIC SUPPRESSION; SIGNAL TRANSDUCTION; SYNAPSE;

ANALYSIS OF VARIANCE; ANIMALS; ARACHIDONIC ACIDS; CALCIUM; CLONING, MOLECULAR; DNA PRIMERS; ENDOCANNABINOIDS; EXCITATORY POSTSYNAPTIC POTENTIALS; GLYCERIDES; IMMUNOHISTOCHEMISTRY; MICE; MICE, KNOCKOUT; MONOACYLGLYCEROL LIPASES; NEUROGLIA; POLYMERASE CHAIN REACTION; PROTEOLYSIS; PURKINJE CELLS; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION;

MUS;

EID: 84864353441     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1204404109     Document Type: Article

References (49)

1. 2+-assisted receptor-driven endocannabinoid release: Mechanisms that associate presynaptic and postsynaptic activities. Curr Opin Neurobiol 17:360-365.
2. Heifets BD, Castillo PE (2009) Endocannabinoid signaling and long-term synaptic plasticity. Annu Rev Physiol 71:283-306.
3. Kano M, Ohno-Shosaku T, Hashimotodani Y, Uchigashima M, Watanabe M (2009) Endocannabinoid-mediated control of synaptic transmission. Physiol Rev 89:309-380.
4. Devane WA, et al. (1992) Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science 258:1946-1949. (Pubitemid 23026736)
5. Mechoulam R, et al. (1995) Identification of an endogenous 2-monoglyceride, present in canine gut, that binds to cannabinoid receptors. Biochem Pharmacol 50:83-90.
6. Sugiura T, et al. (1995) 2-Arachidonoylglycerol: A possible endogenous cannabinoid receptor ligand in brain. Biochem Biophys Res Commun 215:89-97.
7. Tanimura A, et al. (2010) The endocannabinoid 2-arachidonoylglycerol produced by diacylglycerol lipase α mediates retrograde suppression of synaptic transmission. Neuron 65:320-327.
8. Gao Y, et al. (2010) Loss of retrograde endocannabinoid signaling and reduced adult neurogenesis in diacylglycerol lipase knock-out mice. J Neurosci 30:2017-2024.
9. Kreitzer AC, Regehr WG (2001) Retrograde inhibition of presynaptic calcium influx by endogenous cannabinoids at excitatory synapses onto Purkinje cells. Neuron 29:717-727. (Pubitemid 32323944)
10. Ohno-Shosaku T, Maejima T, Kano M (2001) Endogenous cannabinoids mediate retrograde signals from depolarized postsynaptic neurons to presynaptic terminals. Neuron 29:729-738. (Pubitemid 32323945)
11. Wilson RI, Nicoll RA (2001) Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses. Nature 410:588-592. (Pubitemid 32267203)
12. Maejima T, Hashimoto K, Yoshida T, Aiba A, Kano M (2001) Presynaptic inhibition caused by retrograde signal from metabotropic glutamate to cannabinoid receptors. Neuron 31:463-475. (Pubitemid 32778564)
13. 2+ dependency for triggering retrograde endocannabinoid signal. Neuron 45:257-268.
14. 2+-assisted metabotropic glutamate receptor subtype 1 to phospholipase Cβ4 signaling cascade in the cerebellum. J Neurosci 25:6826-6835.
15. Lujan R, Nusser Z, Roberts JD, Shigemoto R, Somogyi P (1996) Perisynaptic location of metabotropic glutamate receptors mGluR1 and mGluR5 on dendrites and dendritic spines in the rat hippocampus. Eur J Neurosci 8:1488-1500.
16. Tanaka J, et al. (2000) Gq protein α subunits Gαq and Gα11 are localized at postsynaptic extra-junctional membrane of cerebellar Purkinje cells and hippocampal pyramidal cells. Eur J Neurosci 12:781-792. (Pubitemid 30168755)
17. Nakamura M, et al. (2004) Signaling complex formation of phospholipase Cβ4 with metabotropic glutamate receptor type 1α and 1,4,5-trisphosphate receptor at the perisynapse and endoplasmic reticulum in the mouse brain. Eur J Neurosci 20:2929-2944. (Pubitemid 40007287)
18. Katona I, et al. (2006) Molecular composition of the endocannabinoid system at glutamatergic synapses. J Neurosci 26:5628-5637. (Pubitemid 44315254)
19. Lafourcade M, et al. (2007) Molecular components and functions of the endocannabinoid system in mouse prefrontal cortex. PLoS ONE 2:e709.
20. Uchigashima M, et al. (2007) Subcellular arrangement of molecules for 2-arachidonoyl glycerol-mediated retrograde signaling and its physiological contribution to synaptic modulation in the striatum. J Neurosci 27:3663-3676. (Pubitemid 46557660)
21. Yoshida T, et al. (2006) Localization of diacylglycerol lipase-α around postsynaptic spine suggests close proximity between production site of an endocannabinoid, 2-arachidonoyl-glycerol, and presynaptic cannabinoid CB1 receptor. J Neurosci 26:4740-4751. (Pubitemid 44315313)
22. Yoshida T, et al. (2011) Unique inhibitory synapse with particularly rich endocannabinoid signaling machinery on pyramidal neurons in basal amygdaloid nucleus. Proc Natl Acad Sci USA 108:3059-3064.
23. Katona I, Freund TF (2008) Endocannabinoid signaling as a synaptic circuit breaker in neurological disease. Nat Med 14:923-930.
24. Kawamura Y, et al. (2006) The CB1 cannabinoid receptor is the major cannabinoid receptor at excitatory presynaptic sites in the hippocampus and cerebellum. J Neurosci 26:2991-3001.
25. Blankman JL, Simon GM, Cravatt BF (2007) A comprehensive profile of brain enzymes that hydrolyze the endocannabinoid 2-arachidonoylglycerol. Chem Biol 14:1347-1356. (Pubitemid 350257008)
26. Chanda PK, et al. (2010) Monoacylglycerol lipase activity is a critical modulator of the tone and integrity of the endocannabinoid system. Mol Pharmacol 78:996-1003.
27. Schlosburg JE, et al. (2010) Chronic monoacylglycerol lipase blockade causes functional antagonism of the endocannabinoid system. Nat Neurosci 13:1113-1119.
28. Hashimotodani Y, Ohno-Shosaku T, Kano M (2007) Presynaptic monoacylglycerol lipase activity determines basal endocannabinoid tone and terminates retrograde endocannabinoid signaling in the hippocampus. J Neurosci 27:1211-1219. (Pubitemid 46203330)
29. Pan B, et al. (2009) Blockade of 2-arachidonoylglycerol hydrolysis by selective monoacylglycerol lipase inhibitor 4-nitrophenyl 4-(dibenzo[d][1,3] dioxol-5-yl(hydroxy) methyl)piperidine-1-carboxylate (JZL184) enhances retrograde endocannabinoid signaling. J Pharmacol Exp Ther 331:591-597.
30. Straiker A, et al. (2009) Monoacylglycerol lipase limits the duration of endocannabinoid-mediated depolarization-induced suppression of excitation in autaptic hippocampal neurons. Mol Pharmacol 76:1220-1227.
31. Pan B, et al. (2011) Alterations of endocannabinoid signaling, synaptic plasticity, learning, and memory in monoacylglycerol lipase knock-out mice. J Neurosci 31:13420-13430.
32. Zhong P, et al. (2011) Genetic deletion of monoacylglycerol lipase alters endocannabinoid-mediated retrograde synaptic depression in the cerebellum. J Physiol 589:4847-4855.
33. Dinh TP, et al. (2002) Brain monoglyceride lipase participating in endocannabinoid inactivation. Proc Natl Acad Sci USA 99:10819-10824.
34. Gulyas AI, et al. (2004) Segregation of two endocannabinoid-hydrolyzing enzymes into pre- and postsynaptic compartments in the rat hippocampus, cerebellum and amygdala. Eur J Neurosci 20:441-458. (Pubitemid 38969629)
35. Uchigashima M, et al. (2011) Molecular and morphological configuration for 2-arachidonoylglycerol-mediated retrograde signaling at mossy cell-granule cell synapses in the dentate gyrus. J Neurosci 31:7700-7714.
36. Hashimotodani Y, Ohno-Shosaku T, Maejima T, Fukami K, Kano M (2008) Pharmacological evidence for the involvement of diacylglycerol lipase in depolarization-induced endocanabinoid release. Neuropharmacology 54:58-67. (Pubitemid 350299399)
37. Tanimura A, Kawata S, Hashimoto K, Kano M (2009) Not glutamate but endocannabinoids mediate retrograde suppression of cerebellar parallel fiber to Purkinje cell synaptic transmission in young adult rodents. Neuropharmacology 57:157-163.
38. A receptors. Proc Natl Acad Sci USA 105:13151-13156.
39. Fremeau RT, Jr., et al. (2001) The expression of vesicular glutamate transporters defines two classes of excitatory synapse. Neuron 31:247-260.
40. Yamada K, et al. (2000) Dynamic transformation of Bergmann glial fibers proceeds in correlation with dendritic outgrowth and synapse formation of cerebellar Purkinje cells. J Comp Neurol 418:106-120. (Pubitemid 30090943)
41. v2.1 in cerebellar Purkinje cells regulates competitive excitatory synaptic wiring, cell survival, and cerebellar biochemical compartmentalization. J Neurosci 32:1311-1328.
42. 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. (Pubitemid 34033498)
43. Kreitzer AC, Regehr WG (2001) Cerebellar depolarization-induced suppression of inhibition is mediated by endogenous cannabinoids. J Neurosci 21:RC174.
44. 1 receptor mediates retrograde signals for depolarization-induced suppression of inhibition in cerebellar Purkinje cells. J Neurosci 22:1690-1697.
45. Hashimoto K, Ichikawa R, Kitamura K, Watanabe M, Kano M (2009) Translocation of a "winner" climbing fiber to the Purkinje cell dendrite and subsequent elimination of "losers" from the soma in developing cerebellum. Neuron 63:106-118.
46. Roth A, HäusserM(2001) Compartmental models of rat cerebellar Purkinje cells based on simultaneous somatic and dendritic patch-clamp recordings. J Physiol 535:445-472. (Pubitemid 32825682)
47. Long JZ, et al. (2009) Selective blockade of 2-arachidonoylglycerol hydrolysis produces cannabinoid behavioral effects. Nat Chem Biol 5:37-44.
48. Vincent P, Marty A (1993) Neighboring cerebellar Purkinje cells communicate via retrograde inhibition of common presynaptic interneurons. Neuron 11:885-893. (Pubitemid 23347473)
49. Kreitzer AC, Carter AG, Regehr WG (2002) Inhibition of interneuron firing extends the spread of endocannabinoid signaling in the cerebellum. Neuron 34:787-796. (Pubitemid 34628740)