Forebrain-specific inactivation of Gq/G11 family G proteins results in age-dependent epilepsy and impaired endocannabinoid formation

Molecular and Cellular Biology

Volumn 26, Issue 15, 2006, Pages 5888-5894

  Wettschureck, Nina ^a   Van Der Stelt, Mario ^b,f   Tsubokawa, Hiroshi ^c   Krestel, Heinz ^d,g   Moers, Alexandra ^a   Petrosino, Stefania ^b   Schütz, Günther ^e   Di Marzo, Vincenzo ^b   Offermanns, Stefan ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b CNR   (Italy)

^c TOHOKU UNIVERSITY   (Japan)

^d MAX PLANCK INSTITUTE FOR MEDICAL RESEARCH   (Germany)

^e GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^f NV ORGANON   (Netherlands)

^g UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ENDOCANNABINOID; G PROTEIN COUPLED RECEPTOR; G11 PROTEIN; GQ PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; KAINIC ACID; METABOTROPIC RECEPTOR; RIMONABANT; UNCLASSIFIED DRUG;

ALPHA CHAIN; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL LEVEL; CONTROLLED STUDY; DISEASE EXACERBATION; EPILEPSY; FOREBRAIN; IN VIVO STUDY; MOUSE; MOUSE MUTANT; NERVE CELL EXCITABILITY; NERVOUS SYSTEM FUNCTION; NEUROPROTECTION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATORY MECHANISM; SEIZURE SUSCEPTIBILITY; SYNAPTIC TRANSMISSION;

AGE FACTORS; ANIMALS; ENDOCANNABINOIDS; EPILEPSY; EXCITATORY AMINO ACID AGONISTS; GTP-BINDING PROTEIN ALPHA SUBUNITS, GQ-G11; KAINIC ACID; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEURONS; PATCH-CLAMP TECHNIQUES; PROSENCEPHALON; PROTEIN SUBUNITS;

EID: 33746513147     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00397-06     Document Type: Article

References (70)

1. Aiba, A., M. Kano, C. Chen, M. E. Stanton, G. D. Fox, K. Herrup, T. A. Zwingman, and S. Tonegawa. 1994. Deficient cerebellar long-term depression and impaired motor learning in mGluR1 mutant mice. Cell 79:377-388.
2. Alger, B. E. 2002. Retrograde signaling in the regulation of synaptic transmission: focus on endocannabinoids. Prog. Neurobiol. 68:247-286.
3. Bisogno, T., F. Howell, G. Williams, A. Minassi, M. G. Cascio, A. Ligresti, I. Matias, A. Schiano-Moriello, P. Paul, E. J. Williams, U. Gangadharan, C. Hohbs, V. Di Marzo, and P. Doherty. 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. Bisogno, T., D. Melck, L. De Petrocellis, and V. Di Marzo. 1999. Phosphatidic acid as the biosynthetic precursor of the endocannabinoid 2-arachidonoylglycerol in intact mouse neuroblastoma cells stimulated with ionomycin. J. Neurochem. 72:2113-2119.
5. Bouilleret, V., V. Ridoux, A. Depaulis, C. Marescaux, A. Nehlig, and G. Le Gal Le Salle. 1999. Recurrent seizures and hippocampal sclerosis following intrahippocampal kainate injection in adult mice: electroencephalography, histopathology and synaptic reorganization similar to mesial temporal lobe epilepsy. Neuroscience 89:717-729.
6. Camon, L., P. Vives, N. de Vera, and E. Martinez. 1998. Seizures and neuronal damage induced in the rat by activation of group 1 metabotropic glutamate receptors with their selective agonist 3,5-dihydroxyphenylglycine. J. Neurosci. Res. 51:339-348.
7. Chapman, A. G., K. Nanan, M. Williams, and B. S. Meldrum. 2000. Anticonvulsant activity of two metabotropic glutamate group 1 antagonists selective for the mGlu5 receptor: 2-methyl-6-(phenylethynyl)-pyridine (MPEP), and (E)-6-methyl-2-styryl-pyridine (SIB 1893). Neuropharmacology 39:1567-1574.
8. Chapman, A. G., P. K. Yip, J. S. Yap, L. P. Quinn, E. Tang, J. R. Harris, and B. S. Meldrum. 1999. Anticonvulsant actions of LY 367385 ((+)-2-methyl-4-carhoxyphenylglycine) and AIDA ((RS)-1-aminoindan-1,5- dicarboxylic acid). Eur. J. Pharmacol. 368:17-24.
9. Chevalcyre, V., and P. E. Castillo. 2003. Heterosynaptic LTD of hippocampal GABAergic synapses: a novel role of endocannabinoids in regulating excitability. Neuron 38:461-472.
10. Chuang, S. C., R. Bianchi, D. Kim, H. S. Shin, and R. K. Wong. 2001. Group 1 metabotropic glutamate receptors elicit epileptiform discharges in the hippocampus through PLCbeta1 signaling. J. Neurosci. 21:6387-6394.
11. Conn, P. J., and J. P. Pin. 1997. Pharmacology and functions of metabotropic glutamate receptors. Annu. Rev. Pharmacol. Toxicol. 37:205-237.
12. Delmas, P., M. Crest, and D. A. Brown. 2004. Functional organization of PLC signaling microdomains in neurons. Trends Neurosci. 27:41-47.
13. De Petrocellis, L., M. G. Cascio, and V. Di Marzo. 2004. The endocannabinoid system: a general view and latest additions. Br. J. Pharmacol. 141:765-774.
14. Diana, M. A., C. Levenes, K. Mackie, and A. Marty. 2002. Short-term retrograde inhibition of GABAergic synaptic currents in rat Purkinje cells is mediated by endogenous cannabinoids. J. Neurosci. 22:200-208.
15. Di Marzo, V., A. Fontana, H. Cadas, S. Schinelli, G. Cimino, J. C. Schwartz, and D. Piomelli. 1994. Formation and inactivation of endogenous cannabinoid anandamide in central neurons. Nature 372:686-691.
16. Di Marzo, V., D. Melck, T. Bisogno, and L. De Petrocellis. 1998. Endocannabinoids: endogenous cannabinoid receptor ligands with neuromodulatory action. Trends Neurosci. 21:521-528.
17. Dolphin, A. C. 2003. G protein modulation of voltage-gated calcium channels. Pharmacol. Rev. 55:607-627.
18. Exton, J. H. 1996. Regulation of phosphoinositide phospholipases by hormones, neurotransmitters, and other agonists linked to G proteins. Annu. Rev. Pharmacol. Toxicol. 36:481-509.
19. Freund, T. F., I. Katona, and D. Piomelli. 2003. Role of endogenous cannabinoids in synaptic signaling. Physiol. Rev. 83:1017-1066.
20. Fukudome, Y., T. Ohno-Shosaku, M. Matsui, Y. Omori, M. Fukaya, H. Tsubokawa, M. M. Taketo, M. Watanabe, T. Manabe, and M. Kano. 2004. Two distinct classes of muscarinic action on hippocampal inhibitory synapses: M2-mediated direct suppression and M1/M3-mcdiated indirect suppression through endocannabinoid signalling. Eur. J. Neurosci. 19:2682-2692.
21. Galante, M., and M. A. Diana. 2004. Group 1 metabotropic glutamate receptors inhibit GABA release at interneuron-Purkinje cell synapses through endocannabinoid production. J. Neurosci. 24:4865-4874.
22. Gamper, N., V. Reznikov, Y. Yamada, J. Yang, and M. S. Shapiro. 2004. Phosphatidylinositol 4,5-bisphosphate signals underlie receptor-specific Gq/11-mediated modulation of N-type Ca2+ channels. J. Neurosci. 24:10980-10992. (Erratum, vol. 25, 2005.)
23. Gingrich, M. H., C. E. Junge, P. Lyuboslavsky, and S. F. Traynelis. 2000. Potentiation of NMDA receptor function by the serine protease thrombin. J. Neurosci. 20:4582-4595.
24. Hamilton, S. E., M. D. Loose, M. Qi, A. I. Levey, B. Hille, G. S. McKnight, K. L. Idzerda, and N. M. Nathanson. 1997. Disruption of the m1 receptor gene ablates muscarinic receptor-dependent M current regulation and seizure activity in mice. Proc. Natl. Acad. Sci. USA 94:13311-13316.
25. Hartmann, J., K. Blum, Y. Kovalchuk, H. Adelsherger, K. Kuner, G. M. Durand, M. Miyata, M. Kano, S. Offermanns, and A. Konnerth. 2004. Distinct roles of Galpha (q) and Galpha11 for Purkinje cell signaling and motor behavior. J. Neurosci. 24:5119-5130.
26. Hillman, K. L., C. A. Knudson, P. A. Carr, V. A. Doze, and J. E. Porter. 2005. Adrenergic receptor characterization of CA1 hippocampal neurons using real time single cell RT-PCR. Brain Res. Mol. Brain Res. 139:267-276.
27. Howlett, A. C. 2002. The cannabinoid receptors. Prostaglandins Other Lipid Mediat. 68-69:619-631.
28. Howlett, A. C. 2004. Efficacy in CB1 receptor-mediated signal transduction. Br. J. Pharmacol. 142:1209-1218.
29. Kammermeier, P. J., V. Ruiz-Velasco, and S. R. Ikeda. 2000. A voltage-independent calcium current inhibitory pathway activated by muscarinic agonists in rat sympathetic neurons requires both Galpha q/11 and Gbeta gamma. J. Neurosci. 20:5623-5629.
30. Kiessling, M., and P. Gass. 1993. Immediate early gene expression in experimental epilepsy. Brain Pathol. 3:381-393.
31. Kim, D., K. S. Jun, S. B. Lee, N. G. Kang, D. S. Min, Y. H. Kim, S. H. Ryu, P. G. Sun, and H. S. Shin. 1997. Phospholipase C isozymes selectively couple to specific neurotransmitter receptors. Nature 389:290-293.
32. Kim, J., M. Isokawa, C. Ledent, and B. E. Alger. 2002. Activation of muscarinic acetylcholine receptors enhances the release of endogenous cannabinoids in the hippocampus. J. Neurosci. 22:10182-10191.
33. Kleppisch, T., V. Voigt, R. Allmann, and S. Offermanns. 2001. G(alpha)q-deficient mice lack metabotropic glutamate receptor-dependent long-term depression but show normal long-term potentiation in the hippocampal CA1 region. J. Neurosci. 21:4943-4948.
34. Kreitzer, A. C., and W. G. Regehr. 2001. Retrograde inhibition of presynaptic calcium influx by endogenous cannabinoids at excitatory synapses onto Purkinje cells. Neuron 29:717-727.
35. Krestel, H. E., D. R. Shimshek, V. Jensen, T. Nevian, J. Kim, Y. Geng, T. Bast, A. Depaulis, K. Schonig, K. Schwenk, H. Bujard, O. Hvalby, R. Sprengel, and P. H. Seeburg. 2004. A genetic switch for epilepsy in adult mice. J. Neurosci. 24:10568-10578.
36. Lauckner, J. E., B. Hille, and K. Mackie. 2005. The cannabinoid agonist WIN55,212-2 increases intracellular calcium via CB1 receptor coupling to Gq/11 G proteins. Proc. Natl. Acad. Sci. USA 102:19144-191449.
37. Lu, Y. M., Z. Jia, C. Janus, J. T. Henderson, R. Gerlai, J. M. Wojtowicz, and J. C. Roder. 1997. Mice lacking metabotropic glutamate receptor 5 show impaired learning and reduced CA1 long-term potentiation (LTP) but normal CA3 LTP. J. Neurosci. 17:5196-5205.
38. Maejima, T., K. Hashimoto, T. Yoshida, A. Aiba, and M. Kano. 2001. Presynaptic inhibition caused by retrograde signal from metabotropic glutamate to cannabinoid receptors. Neuron 31:463-475.
39. Mantamadiotis, T., T. Lemberger, S. C. Bleckmann, H. Kern, O. Kretz, A. Martin Villalba, F. Tronche, C. Kellendonk, D. Gau, J. Kapfhammer, C. Otto, W. Schmid, and G. Schutz. 2002. Disruption of CREB function in brain leads to neurodegeneration. Nat. Genet. 31:47-54.
40. Marsicano, G., S. Goodenough, K. Monory, H. Hermann, M. Eder, A. Cannich, S. C. Azad, M. G. Cascio, S. O. Gutierrez, M. van der Stelt, M. L. Lopez-Rodriguez, E. Casanova, G. Schutz, W. Zieglgansherger, V. Di Marzo, C. Behl, and B. Lutz. 2003. CB1 cannabinoid receptors and on-demand defense against excitotoxicity. Science 302:84-88.
41. Martin, L. A., and B. E. Alger. 1999. Muscarinic facilitation of the occurrence of depolarization-induced suppression of inhibition in rat hippocampus. Neuroscience 92:61-71.
42. Matsumoto, M., T. Nakugawa, T. Inoue, E. Nagata, K. Tanaka, H. Takano, O. Minowa, J. Kuno, S. Sakakihara, M. Yamada, H. Yoneshima, A. Miyawaki, Y. Fukuuchi, T. Furuichi, H. Okano, K. Mikoshiba, and T. Noda. 1996. Alaxia and epileptic seizures in mice lacking type 1 inositol 1,4,5-trisphosphate receptor. Nature 379:168-171.
43. Mechoulam, R., M. Spatz, and E. Shohami. 2002. Endocannabinoids and neuroprotection. Sci. STKE 2002:RE5. [Online.]
44. Melis, M., M. Pistis, S. Perra, A. L. Muntoni, G. Pillolla, and G. L. Gessa. 2004. Endocannabinoids mediate presynaptic inhibition of glutamatergic transmission in rat ventral tegmental area dopamine neurons through activation of CB1 receptors. J. Neurosci. 24:53-62.
45. Mirotznik, R. R., X. Zheng, and E. F. Stanley. 2000. G-protein types involved in calcium channel inhibition at a presynaptic nerve terminal. J. Neurosci. 20:7614-7621.
46. Miura, M., M. Watanabe, S. Offermanns, M. I. Simon, and M. Kano. 2002. Group 1 metabotropic glutamate receptor signaling via Galpha q/Galpha 11 secures the induction of long-term potentiation in the hippocampal area CA1. J. Neurosci. 22:8379-8390.
47. Mukhopadhyay, S., J. Y. Shim, A. A. Assi, D. Norford, and A. C. Howlett. 2002. CB(1) cannahinoid receptor-G protein association: a possible mechanism for differential signaling. Chem. Phys. Lipids 121:91-109.
48. Offermanns, S., K. Hashimoto, M. Watanabe, W. Sun, H. Kurihara, R. F. Thompson, Y. Inoue, M. Kano, and M. I. Simon. 1997. Impaired motor coordination and persistent multiple climbing fiber innervation of cerebellar Purkinje cells in mice lacking Galphaq. Proc. Natl. Acad. Sci. USA 94:14089-14094.
49. Offermanns, S., L. P. Zhao, A. Gohla, I. Sarosi, M. I. Simon, and T. M. Wilkie. 1998. Embryonic cardiomyocyte hypoplasia and craniofacial defects in G alpha q/G alpha 11-mutant mice. EMBO J. 17:4304-4312.
50. Ohno-Shosaku, T., T. Maejima, and M. Kano. 2001. Endogenous cannabinoids mediate retrograde signals from depolarized postsynaptic neurons to presynaptic terminals. Neuron 29:729-738.
51. Ohno-Shosaku, T., M. Matsui, Y. Fukudome, J. Shosaku, H. Tsubokawa, M. M. Taketo, T. Manabe, and M. Kano. 2003. Postsynaptic M1 and M3 receptors are responsible for the muscarinic enhancement of retrograde endocannabinoid signalling in the hippocampus. Eur. J. Neurosci. 18:109-116.
52. Ohno-Shosaku, T., J. Shosaku, H. Tsubokawa, and M. Kano. 2002. Cooperative endocannabinoid production by neuronal depolarization and group 1 metabotropic glutamate receptor activation. Eur. J. Neurosci. 15:953-961.
53. Ohno-Shosaku, T., H. Tsubokawa, I. Mizushima, N. Yoneda, A. Zimmer, and M. Kano. 2002. Presynaptic cannabinoid sensitivity is a major determinant of depolarization-induced retrograde suppression at hippocampal synapses. J. Neurosci. 22:3864-3872.
54. Ortar, G., A. Ligresti, L. De Petrocellis, E. Morera, and V. Di Marzo. 2003. Novel selective and metabolically stable inhibitors of anandamide cellular uptake. Biochem. Pharmacol. 65:1473-1481.
55. Pertwee, R. G. 1999. Pharmacology of cannabinoid receptor ligands. Curr. Med. Chem. 6:635-664.
56. Piomelli, D. 2003. The molecular logic of endocannabinoid signalling. Nat. Rev. Neurosci. 4:873-884.
57. Savolainen, K. M., and M. R. Hirvonen. 1992. Second messengers in cholinergic-induced convulsions and neuronal injury. Toxicol. Lett. 64-65(Spec. No.):437-445.
58. Stella, N., P. Schweitzer, and D. Piomelli. 1997. A second endogenous cannabinoid that modulates long-term potentiation. Nature 388:773-778.
59. Sugiura, T., Y. Kobayashi, S. Oka, and K. Waku. 2002. Biosynthesis and degradation of anandamide and 2-arachidonoylglycerol and their possible physiological significance. Prostaglandins Leukot Essent Fatty Acids 66:173-192.
60. Tecott, L. H., L. M. Sun, S. F. Akana, A. M. Strack, D. H. Lowenstein, M. F. Dallman, and D. Julius. 1995. Eating disorder and epilepsy in mice lacking 5-HT2c serotonin receptors. Nature 374:542-546.
61. van der Stelt, M., M. Trevisani, V. Vellani, L. De Petrocellis, A. Schiano Moriello, B. Campi, P. McNaughton, P. Geppetti, and V. Di Marzo. 2005. Anandamide acts as an intracellular messenger amplifying Ca2+ influx via TRPVI channels. EMBO J. 24:3026-3037.
62. van der Stelt, M., W. B. Veldhuis, M. Maccarrone, P. R. Bar, K. Nicolay, G. A. Veldink, V. Di Marzo, and J. F. Vliegenthart. 2002. Acute neuronal injury, excitotoxicity, and the endocannabinoid system. Mol. Neurobiol. 26:317-346.
63. van der Stelt, M., W. B. Veldhuis, G. W. van Haaften, F. Fezza, T. Bisogno, P. R. Bar, G. A. Veldink, J. F. Vliegenthart, V. Di Marzo, and K. Nicolay. 2001. Exogenous anandamide protects rat brain against acute neuronal injury in vivo. J. Neurosci. 21:8765-8771.
64. van Hooft, J. A., R. Giuffrida, M. Blatow, and H. Monyer. 2000. Differential expression of group 1 metabotropic glutamate receptors in functionally distinct hippocampal interneurons. J. Neurosci. 20:3544-3551.
65. Varma, N., G. C. Carlson, C. Ledent, and B. E. Alger. 2001. Metabotropic glutamate receptors drive the endocannabinoid system in hippocampus. J. Neurosci. 21:RC188. [Online.]
66. q/11 family are crucial for the induction of maternal behavior in mice. Mol. Cell. Biol. 24:8048-8054.
67. Wettschureck, N., H. Rutten, A. Zywietz, D. Gehring, T. M. Wilkie, J. Chen, K. R. Chien, and S. Offermanns. 2001. Absence of pressure overload induced myocardial hypertrophy after conditional inactivation of Galphaq/Galpha11 in cardiomyocytes. Nat. Med. 7:1236-1240.
68. Wilson, R. I., and R. A. Nicoll. 2002. Endocannabinoid signaling in the brain. Science 296:678-682.
69. Wilson, R. I., and R. A. Nicoll. 2001. Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses. Nature 410:588-592.
70. Zhang, J., D. Zhang, J. S. McQuade, M. Behbehani, J. Z. Tsien, and M. Xu. 2002. c-fos regulates neuronal excitability and survival. Nat. Genet. 30:416-420.