Unbalance of CB1 receptors expressed in GABAergic and glutamatergic neurons in a transgenic mouse model of Huntington's disease

Neurobiology of Disease

Volumn 45, Issue 3, 2012, Pages 983-991

  Chiodi, Valentina ^a   Uchigashima, Motokazu ^b   Beggiato, Sarah ^c   Ferrante, Antonella ^a   Armida, Monica ^a   Martire, Alberto ^a   Potenza, Rosa Luisa ^a   Ferraro, Luca ^c   Tanganelli, Sergio ^c   Watanabe, Masahiko ^b   Domenici, Maria Rosaria ^a   Popoli, Patrizia ^a  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^b HOKKAIDO UNIVERSITY   (Japan)

^c UNIVERSITY OF FERRARA   (Italy)

Author keywords

Cannabinoid CB1 receptor; Huntington's disease; Immunoelectron microscopy; Neurotransmitter release; R6 2 mice; Synaptic transmission

Indexed keywords

2,3 DIHYDRO 5 METHYL 3 (MORPHOLINOMETHYL) 6 (1 NAPHTHOYL)PYRROLO[1,2,3 DE][1,4]BENZOXAZINE; 4 AMINOBUTYRIC ACID; CANNABINOID 1 RECEPTOR; GLUTAMIC ACID;

4 AMINOBUTYRIC ACID RELEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CELL POPULATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CORPUS STRIATUM; GABAERGIC TRANSMISSION; HUNTINGTON CHOREA; MOUSE; NEUROPATHOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN SECRETION; SYNAPTIC TRANSMISSION; WILD TYPE;

ACTION POTENTIALS; ANALYSIS OF VARIANCE; ANIMALS; BENZOXAZINES; BRAIN; DISEASE MODELS, ANIMAL; DRUG INTERACTIONS; ELECTRIC STIMULATION; EXCITATORY AMINO ACID AGENTS; GAMMA-AMINOBUTYRIC ACID; GLUTAMATES; HUMANS; HUNTINGTON DISEASE; MICE; MICE, TRANSGENIC; MICROSCOPY, IMMUNOELECTRON; MORPHOLINES; MOTOR ACTIVITY; NAPHTHALENES; NERVE TISSUE PROTEINS; NEURONS; NUCLEAR PROTEINS; PATCH-CLAMP TECHNIQUES; PIPERIDINES; POTASSIUM; PYRAZOLES; RECEPTOR, CANNABINOID, CB1; STATISTICS, NONPARAMETRIC; SYNAPTOSOMES; TETRAHYDROCANNABINOL; TRINUCLEOTIDE REPEATS; TRITIUM; VESICULAR GLUTAMATE TRANSPORT PROTEIN 1; VESICULAR INHIBITORY AMINO ACID TRANSPORT PROTEINS;

EID: 84856561254     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2011.12.017     Document Type: Article

References (46)

1. Adermark L., Lovinger D.M. Retrograde endocannabinoid signaling at striatal synapses requires a regulated postsynaptic release step. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:20564-20569.
2. Anderson W.W., Collingridge G.L. The LTP program: a data acquisition program for on-line analysis of long-term potentiation and other synaptic events. J. Neurosci. Methods 2001, 15:71-83.
3. Battista N., Bari M., Tarditi A., Mariotti C., Bachoud-Levi A.C., Zuccato C., Finazzi-Agrò A., Genitrini S., Penschanki M., Di Donato S., Cattaneo E., Maccarone M. Severe deficiency of the fatty acid amide hydrolase (FAAH) activity segregates with the Huntington's disease mutation in peripheral lymphocytes. Neurobiol. Dis. 2007, 27:108-116.
4. Bisogno T., Martire A., Petrosino S., Popoli P., Di Marzo V. Symptom-related changes of endocannabinoid and palmitoylethanolamide levels in brain areas of R6/2 mice, a transgenic model of Huntington's disease. Neurochem. Int. 2008, 52:307-313.
5. Blázquez C., Chiarlone A., Sagredo O., Aguado T., Pazos M.R., Resel E., Palazuelos J., Julien B., Salazar M., Börner C., Benito C., Carrasco C., Diez-Zaera M., Paoletti P., Díaz-Hernández M., Ruiz C., Sendtner M., Lucas J.J., de Yébenes J.G., Marsicano G., Monory K., Lutz B., Romero J., Alberch J., Ginés S., Kraus J., Fernández-Ruiz J., Galve-Roperh I., Guzmán M. Loss of striatal type 1 cannabinoid receptors is a key pathogenic factor in Huntington's disease. Brain 2011, 134:119-136.
6. Bradford M.M. A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principles of protein-dye binding. Anal. Biochem. 1976, 72:248-254.
7. Centonze D., Battista N., Rossi S., Mercuri N.B., Finazzi-Agro A., Bernardi G., Calabrese P., Maccarrone M. A critical interaction between dopamine D2 receptors and endocannabinoids mediates the effects of cocaine on striatal GABAergic transmission. Neuropsychopharmacology 2004, 29:1488-1497.
8. Centonze D., Rossi S., Prosperetti C., Tscherter A., Bernardi G., Maccarrone M., Calabresi P. Abnormal sensitivity to cannabinoid receptor stimulation might contribute to altered gamma-aminobutyric acid transmission in the striatum of R6/2 Huntington's disease mice. Biol. Psychiatry 2005, 57:1583-1589.
9. Cepeda C., Hurst R.S., Calvert C.R., Hernàndez-Echeagaray E., Nguyen O.K., Jocoy E., Christian L.J., Ariano M.A., Levine M.S. Transient and progressive electrophysiological alterations in the corticostriatal pathway in a mouse model of Huntington's disease. J. Neurosci. 2003, 23:961-969.
10. Cepeda C., Starling A.J., Wu N., Nguyen O.K., Uzgil B., Soda T., Andrè V.M., Ariano M.A., Levine M.S. Increased GABAergic function in mouse models of Huntington's disease: reversal by BDNF. J. Neurosci. Res. 2004, 78:855-867.
11. Cepeda C., Wu N., André V.M., Cummings D.M., Levine M.S. The corticostriatal pathway in Huntington's disease. Prog. Neurobiol. 2007, 81:253-271.
12. Cha J.J. Transcriptional dysregulation in Huntington's disease. Trends Neurosci. 2000, 23:387-392.
13. Dowie M.J., Bradshaw H.B., Howard M.L., Nicholson L.F., Faull R.L., Hannan A.J., Glass M. Altered CB1 receptor and endocannabinoid levels precede motor symptom onset in a transgenic mouse model of Huntington's disease. Neuroscience 2009, 163:456-465.
14. Dowie M.J., Howard M.L., Nicholson L.F., Faull R.L., Hannan A.J., Glass M. Behavioural and molecular consequences of chronic cannabinoid treatment in Huntington's disease transgenic mice. Neuroscience 2010, 170:324-336.
15. Fernández-Ruiz J., Gonzáles S. Cannabinoid control of motor function at the basal ganglia. Handb. Exp. Pharmacol. 2005, 168:479-507.
16. 3H]-dopamine efflux from rat striatal synaptosomes. A novel action of cocaine. J. Neural Transm. 2010, 117:593-597.
17. Ferré S., Fuxe K., von Euler G., Johansson B., Fredholm B.B. Adenosine-dopamine interactions in the brain. Neuroscience 1992, 51:501-512.
18. Fukudome Y., Ohno-Shosaku T., Matsui M., Omori Y., Fukaya M., Tsubokawa H., Taketo M.M., Watanabe M., Manabe T., Kano M. Two distinct classes of muscarinic action on hippocampal inhibitory synapses: M2-mediated direct suppression and M1/M3-mediated indirect suppression through endocannabinoid signalling. Eur. J. Neurosci. 2004, 19:2682-2692.
19. Gerdeman G., Lovinger D.M. CB1 cannabinoid receptor inhibits synaptic release of glutamate in rat dorsolateral striatum. J. Neurophysiol. 2001, 85:468-471.
20. Gil J.M., Rego A.C. Mechanisms of neurodegeneration in Huntington's disease. Eur. J. Neurosci. 2008, 27:2803-2820.
21. Glass M., Dragunow M., Faull R.L.M. The pattern of neurodegeneration in Huntington's disease: a comparative study of cannabinoid, dopamine adenosine and GABAA receptor alterations in the human basal ganglia in Huntington's disease. Neuroscience 2000, 97:505-519.
22. Klapstein G.J., Fisher R.S., Zanjani H., Cepeda C., Jokel E.S., Chesselet M.F., Levine M.S. Electrophysiological and morphological changes in striatal spiny neurons in R6/2 Huntington's disease transgenic mice. J. Neurophysiol. 2001, 86:2667-2677.
23. Kofalvi A., Rodrigues R.J., Ledent C., Macie K., Vizi E.S., Cunha R.A., Sperlágh B. Involvement of cannabinoid receptors in the regulation of neurotransmitter release in the rodent striatum: a combined immunochemical and pharmacological analysis. J. Neurosci. 2005, 25:2874-2884.
24. Kreitzer A.C., Malenka R.C. Endocannabinoid-mediated rescue of striatal LTD and motor deficits in Parkinson's disease models. Nature 2007, 445:643-647.
25. Lastres-Becker I., Bizat N., Boyer F., Hantraye P., Brouillet E., Fernández-Ruiz J. Effects of cannabinoids in the rat model of Huntington's disease generated by an intrastriatal injection of malonate. Neuroreport 2003, 14:813-816.
26. Lastres-Becker I., Bizat N., Boyer F., Hantraye P., Fernandez-Ruiz J., Brouillet E. Potential involvement of cannabinoid receptors in 3-nitropropionic acid toxicity in vivo. Neuroreport 2004, 15:2375-2379.
27. Lu Y., Grady S., Marks M.J., Picciotto M., Changeux J.P., Collins A.C. Pharmacological characterization of nicotinic receptor-stimulated GABA release from mouse brain synaptosomes. J. Pharmacol. Exp. Ther. 1998, 287:648-657.
28. Maccarrone M., Battista N., Centonze D. The endocannabinoid pathway in Huntington's disease: a comparison with other neurodegenerative diseases. Prog. Neurobiol. 2007, 81:349-379.
29. Mangiarini L., Sathasivam K., Selle M., Cozens B., Harper A., Hetherington C., Lawton M., Trottier Y., Lehrach H., Davies S.W., Bates G.P. Exon 1 of the HD gene with an expanded CAG repeat is sufficient to cause a progressive neurological phenotype in transgenic mice. Cell 1996, 87:493-506.
30. Marsicano G., Wotjak C.T., Azad S.C., Bisogno T., Rammes G., Cascio M.G., Hermann H., Tang J., Hofmann C., Zieglgänsberger W., Di Marzo V., Lutz B. The endogenous cannabinoid system controls extinction of aversive memories. Nature 2002, 418:530-534.
31. Marsicano G., Goodenough S., Monoroy K., Hermann H., Eder M., Cannich A., Azad S.C., Cascio M.G., Gutiérrez S.O., van der Stelt M., López-Rodriguez M.L., Casanova E., Schütz G., Zieglgänsberger W., Di Marzo V., Behl C., Lutz B. CB1 cannabinoid receptors and on-demand defense against excitotoxicity. Science 2003, 302:84-88.
32. Martire A., Tebano M.T., Chiodi V., Ferreira S.G., Cunha R.A., Köfalvi A., Popoli P. Presynaptic adenosine A(2A) receptors control cannabinoid CB(1) receptor-mediated inhibition of striatal glutamatergic neurotransmission. J. Neurochem. 2011, 116:273-280.
33. McCaw E.A., Hu H., Gomez G.T., Hebb A.L., Kelly M.E., Denovan-Wright E.M. Structure, expression and regulation of the cannabinoid receptor gene (CB1) in Huntington's disease transgenic mice. Eur. J. Biochem. 2004, 271:4909-4920.
34. Mievis S., Blum D., Ledent C. Worsening of Huntington disease phenotype in CB1 receptor knockout mice. Neurobiol. Dis. 2011, 42:524-529.
35. Miyazaki T., Fukaya M., Shimizu H., Watanabe M. Subtype switching of vesicular glutamate transporters at parallel fibre-Purkinje cell synapses in developing mouse cerebellum. Eur. J. Neurosci. 2003, 17:2563-2572.
36. Monory K., Massa F., Egertová M., Eder M., Blaudzun H., Westenbroek R., Kelsch W., Jacob W., Marsch R., Ekker M., Long J., Rubenstein J.L., Goebbels S., Nave K.A., During M., Klugmann M., Wölfe B., Dodt H.U., Zieglgänsberger W., Wotjak C.T., Mackie K., Elphick M.R., Marsicano G., Lutz B. The endocannabinoid system controls key epileptogenic circuits in the hippocampus. Neuron 2006, 51:455-466.
37. Pintor A., Tebano M.T., Martire A., Grieco R., Galluzzo M., Scattoni M.L., Pèzzola A., Cuccurello R., Felici F., Cuomo V., Piomelli D., Calamandrei G., Popoli P. The cannabinoid receptor agonist WIN 55,212-2 attenuates the effects induced by quinolinic acid in the rat striatum. Neuropharmacology 2006, 51:1004-1012.
38. Richfield E.K., Herkenham M. Selective vulnerability in Huntington's disease: preferential loss of cannabinoid receptors in lateral globus pallidus. Ann. Neurol. 1994, 36:577-584.
39. Riess O., Noerremoelle A., Soerensen S.A., Epplen J.T. Improved PCR conditions for the stretch of (CAG)n repeats causing Huntington's disease. Hum. Mol. Genet. 1993, 2:637.
40. Rossi S., Prosperetti C., Picconi B., De Chiara V., Mataluni G., Bernardi G., Calabresi P., Centonze D. Deficits of glutamate transmission in the striatum of toxic and genetic models of Huntington's disease. Neurosci. Lett. 2006, 410:6-10.
41. Schulz P.E., Cook E.P., Johnston D. Changes in paired-pulse facilitation suggest presynaptic involvement in long-term potentiation. J. Neurosci. 1994, 14:5325-5337.
42. Scotter E., Abood M.E., Glass M. The endocannabinoid system as a target for the treatment of neurodegenerative disease. Br. J. Pharmacol. 2010, 160:480-498.
43. Tebano M.T., Domenici M.R., Popoli P. SCH 58261 differentially influences quinolinic acid-induced effects in striatal and in hippocampal slices. Eur. J. Pharmacol. 2002, 450:253-257.
44. The Huntington's Disease Collaborative Research Group A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosome. Cell 1993, 72:971-983.
45. Tsou K., Brown S., Sañudo-Peña M.C., Mackie K., Walker J.M. Immunohistochemical distribution of cannabinoid CB1 receptors in the rat central nervous system. Neuroscience 1998, 83:393-411.
46. Uchigashima M., Narushima M., Fukaya M., Katona I., Kano M., Watanabe M. Subcellular arrangement of molecules for 2-arachidonoyl-glycerol-mediated retrograde signaling and its physiological contribution to synaptic modulation in the striatum. J. Neurosci. 2007, 27:3663-3676.