The Endocannabinoid System Controls Key Epileptogenic Circuits in the Hippocampus

Neuron

Volumn 51, Issue 4, 2006, Pages 455-466

  Monory, Krisztina ^a,b   Massa, Federico ^a,b   Egertová, Michaela ^c   Eder, Matthias ^b   Blaudzun, Heike ^b   Westenbroek, Ruth ^d   Kelsch, Wolfgang ^b   Jacob, Wolfgang ^b   Marsch, Rudolf ^b   Ekker, Marc ^e   Long, Jason ^f   Rubenstein, John L ^f   Goebbels, Sandra ^g   Nave, Klaus Armin ^g   During, Matthew ^h   Klugmann, Matthias ^h   Wölfel, Barbara ^b   Dodt, Hans Ulrich ^b   Zieglgänsberger, Walter ^b   Wotjak, Carsten T ^b   Mackie, Ken ^d   Elphick, Maurice R ^c   Marsicano, Giovanni ^a,b   Lutz, Beat ^a,b   more..

^a JOHANNES GUTENBERG UNIVERSITY   (Germany)

^b MAX PLANCK INSTITUTE OF PSYCHIATRY   (Germany)

^c QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^d UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF OTTAWA   (Canada)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

^h UNIVERSITY OF AUCKLAND   (New Zealand)

Author keywords

HUMDISEASE; MOLNEURO; SYSNEURO

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; CANNABINOID 1 RECEPTOR; ENDOCANNABINOID; KAINIC ACID; VESICULAR GLUTAMATE TRANSPORTER 1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN FUNCTION; EPILEPTOGENESIS; FOREBRAIN; GENE DELETION; HIPPOCAMPUS; MALE; MOUSE; NERVE CELL; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; SEIZURE;

ANALYSIS OF VARIANCE; ANIMALS; BEHAVIOR, ANIMAL; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CALCIUM CHANNEL BLOCKERS; ENDOCANNABINOIDS; EPILEPSY; GAMMA-AMINOBUTYRIC ACID; GENE EXPRESSION; GLUTAMIC ACID; HIPPOCAMPUS; KAINIC ACID; MALE; MEMBRANE POTENTIALS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MORPHOLINES; NAPHTHALENES; NERVE NET; PYRAMIDAL CELLS; RECEPTOR, CANNABINOID, CB1; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; VESICULAR GLUTAMATE TRANSPORT PROTEIN 1;

EID: 33746913292     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2006.07.006     Document Type: Article

References (59)

1. Alger E. Retrograde signaling in the regulation of synaptic transmission: focus on endocannabinoids. Prog. Neurobiol. 68 (2002) 247-286
2. Aparicio L.C., Candeletti S., Binaschi A., Mazzuferi M., Mantovani S., Di B.M., Landuzzi D., Lopetuso G., Romualdi P., and Simonato M. Kainate seizures increase nociceptin/orphanin FQ release in the rat hippocampus and thalamus: a microdialysis study. J. Neurochem. 91 (2004) 30-37
3. Ben-Ari Y., and Cossart R. Kainate, a double agent that generates seizures: two decades of progress. Trends Neurosci. 23 (2000) 580-587
4. Branda C.S., and Dymecki S.M. Talking about a revolution: The impact of site-specific recombinases on genetic analyses in mice. Dev. Cell 6 (2004) 7-28
5. Chevaleyre V., Takahashi K.A., and Castillo P.E. Endocannabinoid-mediated synaptic plasticity in the CNS. Annu. Rev. Neurosci. 29 (2006) 37-76
6. Clark K.R., Liu X., McGrath J.P., and Johnson P.R. Highly purified recombinant adeno-associated virus vectors are biologically active and free of detectable helper and wild-type viruses. Hum. Gene Ther. 10 (1999) 1031-1039
7. De Petrocellis L., Cascio M.G., and Di Marzo V. The endocannabinoid system: a general view and latest additions. Br. J. Pharmacol. 141 (2004) 765-774
8. Di Marzo V., Bifulco M., and De Petrocellis L. The endocannabinoid system and its therapeutic exploitation. Nat. Rev. Drug Discov. 3 (2004) 771-784
9. Domenici M.R., Azad S.C., Marsicano G., Schierloh A., Wotjak C.T., Dodt H.U., Zieglgänsberger W., Lutz B., and Rammes G. Cannabinoid receptor type 1 located on presynaptic terminals of principal neurons in the forebrain controls glutamatergic synaptic transmission. J. Neurosci. 26 (2006) 5794-5799
10. Egertová M., and Elphick M.R. Localisation of cannabinoid receptors in the rat brain using antibodies to the intracellular C-terminal tail of CB1. J. Comp. Neurol. 422 (2000) 159-171
11. Földy C., Neu A., Jones M.V., and Soltész I. Presynaptic, activity-dependent modulation of cannabinoid type 1 receptor-mediated inhibition of GABA release. J. Neurosci. 26 (2006) 1465-1469
12. Fremeau Jr. R.T., Voglmaier S., Seal R.P., and Edwards R.H. VGLUTs define subsets of excitatory neurons and suggest novel roles for glutamate. Trends Neurosci. 27 (2004) 98-103
13. Freund T.F., Katona I., and Piomelli D. Role of endogenous cannabinoids in synaptic signaling. Physiol. Rev. 83 (2003) 1017-1066
14. Gerdeman G.L., and Lovinger D.M. Emerging roles for endocannabinoids in long-term synaptic plasticity. Br. J. Pharmacol. 140 (2003) 781-789
15. Ghanem N., Jarinova O., Amores A., Long Q., Hatch G., Park B.K., Rubenstein J.L., and Ekker M. Regulatory roles of conserved intergenic domains in vertebrate Dlx bigene clusters. Genome Res. 13 (2003) 533-543
16. Gu H., Zou Y.R., and Rajewsky K. Independent control of immunoglobulin switch recombination at individual switch regions evidenced through Cre-loxP-mediated gene targeting. Cell 73 (1993) 1155-1164
17. Hájos N., Ledent C., and Freund T.F. Novel cannabinoid-sensitive receptor mediates inhibition of glutamatergic synaptic transmission in the hippocampus. Neuroscience 106 (2001) 1-4
18. Harkány T., Hartig W., Berghuis P., Dobszay M.B., Zilberter Y., Edwards R.H., Mackie K., and Ernfors P. Complementary distribution of type 1 cannabinoid receptors and vesicular glutamate transporter 3 in basal forebrain suggests input-specific retrograde signalling by cholinergic neurons. Eur. J. Neurosci. 18 (2003) 1979-1992
19. Hoffman A.F., Macgill A.M., Smith D., Oz M., and Lupica C.R. Species and strain differences in the expression of a novel glutamate-modulating cannabinoid receptor in the rodent hippocampus. Eur. J. Neurosci. 22 (2005) 2387-2391
20. Howlett A.C., Barth F., Bonner T.I., Cabral G., Casellas P., Devane W.A., Felder C.C., Herkenham M., Mackie K., Martin B.R., et al. International union of pharmacology. XXVII. Classification of cannabinoid receptors. Pharmacol. Rev. 54 (2002) 161-202
21. Johnston D., and Amaral D.G. Hippocampus. In: Shepherd G.M. (Ed). The synaptic organization of the brain (2004), Oxford University Press, Oxford 455-498
22. Kaneko T., Fujiyama F., and Hioki H. Immunohistochemical localization of candidates for vesicular glutamate transporters in the rat brain. J. Comp. Neurol. 444 (2002) 39-62
23. Katona I., Sperlágh B., Sik A., Köfalvi A., Vizi E.S., Mackie K., and Freund T.F. Presynaptically located CB1 cannabinoid receptors regulate GABA release from axon terminals of specific hippocampal interneurons. J. Neurosci. 19 (1999) 4544-4558
24. Katona I., Urbán G.M., Wallace M., Ledent C., Jung K.M., Piomelli D., Mackie K., and Freund T.F. Molecular composition of the endocannabinoid system at glutamatergic synapses. J. Neurosci. 26 (2006) 5628-5637
25. Kawamura Y., Fukaya M., Maejima T., Yoshida T., Miura E., Watanabe M., Ohno-Shosaku T., and Kano M. The CB1 cannabinoid receptor is the major cannabinoid receptor at excitatory presynaptic sites in the hippocampus and cerebellum. J. Neurosci. 26 (2006) 2991-3001
26. Kleppisch T., Wolfsgruber W., Feil S., Allmann R., Wotjak C.T., Goebbels S., Nave K.A., Hofmann F., and Feil R. Hippocampal cGMP-dependent protein kinase I supports an age- and protein synthesis-dependent component of long-term potentiation but is not essential for spatial reference and contextual memory. J. Neurosci. 23 (2003) 6005-6012
27. Klugmann M., Wymond S.C., Leichtlein C.B., Klaussner B.K., Dunning J., Fong D., Young D., and During M.J. AAV-mediated hippocampal expression of short and long Homer 1 proteins differentially affect cognition and seizure activity in adult rats. Mol. Cell. Neurosci. 28 (2005) 347-360
28. Lee J., Park K., Lee S., Whang K., Kang M., Park C., and Huh Y. Differential changes of calcium binding proteins in the rat striatum after kainic acid-induced seizure. Neurosci. Lett. 333 (2002) 87-90
29. Li X.G., Somogyi P., Ylien A., and Buszáki G. The hippocampal CA3 network: an in vivo intracellular labeling study. J. Comp. Neurol. 339 (1994) 181-208
30. Lobe C.G., Koop K.E., Kreppner W., Lomeli H., Gertsenstein M., and Nagy A. Z/AP, a double reporter for cre-mediated recombination. Dev. Biol. 208 (1999) 281-292
31. Lutz B. On-demand activation of the endocannabinoid system in the control of neuronal excitability and epileptiform seizures. Biochem. Pharmacol. 68 (2004) 1691-1698
32. Mackie K. Cannabinoid receptors as therapeutic targets. Annu. Rev. Pharmacol. Toxicol. 46 (2006) 101-122
33. Marsicano G., and Lutz B. Expression of the cannabinoid receptor CB1 in distinct neuronal subpopulations in the adult mouse forebrain. Eur. J. Neurosci. 11 (1999) 4213-4225
34. Marsicano G., and Lutz B. Neuromodulatory functions of the endocannabinoid system. J. Endocrinol. Invest. 29 (2006) 27-46
35. Marsicano G., Wotjak C.T., Azad S.C., Bisogno T., Rammes G., Cascio M.G., Hermann H., Tang J., Hofmann C., Zieglgänsberger W., et al. The endogenous cannabinoid system controls extinction of aversive memories. Nature 418 (2002) 530-534
36. Marsicano G., Goodenough S., Monory K., Hermann H., Eder M., Cannich A., Azad S.C., Cascio M.G., Gutiérrez S.O., van der Stelt M., et al. CB1 cannabinoid receptors and on-demand defense against excitotoxicity. Science 302 (2003) 84-88
37. Matsuda L.A., Bonner T.I., and Lolait S.J. Localization of cannabinoid receptor mRNA in rat brain. J. Comp. Neurol. 327 (1993) 535-550
38. Möhler H., Fritschy J.M., and Rudolph U. A new benzodiazepine pharmacology. J. Pharmacol. Exp. Ther. 300 (2002) 2-8
39. Morozov A., Kellendonk C., Simpson E., and Tronche F. Using conditional mutagenesis to study the brain. Biol. Psychiatry 54 (2003) 1125-1133
40. Nomura M., Ueta Y., Hannibal J., Serino R., Yamamoto Y., Shibuya I., Matsumoto T., and Yamashita H. Induction of pituitary adenylate cyclase-activating polypeptide mRNA in the medial parvocellular part of the paraventricular nucleus of rats following kainic-acid-induced seizure. Neuroendocrinology 71 (2000) 318-326
41. Novak A., Guo C., Yang W., Nagy A., and Lobe C.G. Z/EG, a double reporter mouse line that expresses enhanced green fluorescent protein upon Cre-mediated excision. Genesis 28 (2000) 147-155
42. Ong W.Y., and Mackie K. A light and electron microscopic study of the CB1 cannabinoid receptor in primate brain. Neuroscience 92 (1999) 1177-1191
43. Panikashvili D., Simeonidou C., Ben Shabat S., Hanus L., Breuer A., Mechoulam R., and Shohami E. An endogenous cannabinoid (2-AG) is neuroprotective after brain injury. Nature 413 (2001) 527-531
44. Paterna J.C., Moccetti T., Mura A., Feldon J., and Bueler H. Influence of promoter and WHV post-transcriptional regulatory element on AAV-mediated transgene expression in the rat brain. Gene Ther. 7 (2000) 1304-1311
45. Paxinos G., and Franklin K.B.J. The Mouse Brain in Stereotaxic Coordinates (2001), Academic Press, San Diego, CA
46. Pettit D.A., Harrison M.P., Olson J.M., Spencer R.F., and Cabral G.A. Immunohistochemical localization of the neural cannabinoid receptor in rat brain. J. Neurosci. Res. 51 (1998) 391-402
47. Piomelli D. The molecular logic of endocannabinoid signalling. Nat. Rev. Neurosci. 4 (2003) 873-884
48. Ratzliff A.H., Santhakumar V., Howard A., and Soltész I. Mossy cells in epilepsy: rigor mortis or vigor mortis?. Trends Neurosci. 25 (2002) 140-144
49. Schauwecker P.E., and Steward O. Genetic determinants of susceptibility to excitotoxic cell death: implications for gene targeting approaches. Proc. Natl. Acad. Sci. USA 94 (1997) 4103-4108
50. Schwab M.H., Bartholomae A., Heimrich B., Feldmeyer D., Druffel-Augustin S., Goebbels S., Naya F.J., Zhao S., Frotscher M., Tsai M.J., and Nave K.A. Neuronal basic helix-loop-helix proteins (NEX and BETA2/Neuro D) regulate terminal granule cell differentiation in the hippocampus. J. Neurosci. 20 (2000) 3714-3724
51. Soriano P. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 21 (1999) 70-71
52. Takahashi K.A., and Castillo P.E. The CB1 cannabinoid receptor mediates glutamatergic synaptic suppression in the hippocampus. Neuroscience 139 (2006) 795-802
53. Tsou K., Brown S., Sanudo-Pena M.C., Mackie K., and Walker J.M. Immunohistochemical distribution of cannabinoid CB1 receptors in the rat central nervous system. Neuroscience 83 (1998) 393-411
54. Tsou K., Mackie K., Sanudo-Pena M.C., and Walker J.M. Cannabinoid CB1 receptors are localized primarily on cholecystokinin-containing gabaergic interneurons in the rat hippocampal formation. Neuroscience 93 (1999) 969-975
55. van der Stelt M., Veldhuis W.B., Maccarrone M., Bar P.R., Nicolay K., Veldink G.A., Di Marzo V., and Vliegenthart J.F. Acute neuronal injury, excitotoxicity, and the endocannabinoid system. Mol. Neurobiol. 26 (2002) 317-346
56. Wager-Miller J., Westenbroek R., and Mackie K. Dimerization of G protein-coupled receptors: CB1 cannabinoid receptors as an example. Chem. Phys. Lipids 121 (2002) 83-89
57. Wilson R.I., Kunos G., and Nicoll R.A. Presynaptic specificity of endocannabinoid signaling in the hippocampus. Neuron 31 (2001) 453-462
58. Wu S.X., Goebbels S., Nakamura K., Nakamura K., Kometani K., Minato N., Kaneko T., Nave K.A., and Tamamaki N. Pyramidal neurons of upper cortical layers generated by NEX-positive progenitor cells in the subventricular zone. Proc. Natl. Acad. Sci. USA 102 (2005) 17172-17177
59. Zerucha T., Stuhmer T., Hatch G., Park B.K., Long Q., Yu G., Gambarotta A., Schultz J.R., Rubenstein J.L., and Ekker M. A highly conserved enhancer in the Dlx5/Dlx6 intergenic region is the site of cross-regulatory interactions between Dlx genes in the embryonic forebrain. J. Neurosci. 20 (2000) 709-721