Does modulation of the endocannabinoid system have potential therapeutic utility in cerebellar ataxia?

Journal of Physiology

Volumn 594, Issue 16, 2016, Pages 4631-4641

  Stephens, G J ^a  

^a UNIVERSITY OF READING   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA TOCOPHEROL; ATAXIN 1; ATAXIN 2; CALCIUM CHANNEL; CALCIUM CHANNEL CAV 2.1; CANNABIDIOL; CANNABIDIVARIN; CANNABINOID; CANNABINOID 1 RECEPTOR; CANNABINOID 1 RECEPTOR ANTAGONIST; G PROTEIN COUPLED RECEPTOR; IDEBENONE; TALTIRELIN; UBIDECARENONE; UNCLASSIFIED DRUG;

4 AMINOBUTYRIC ACID RELEASE; CALCIUM CURRENT; CANNABINOID SIGNALLING; CEREBELLAR ATAXIA; CEREBELLUM; CEREBELLUM CORTEX; DRUG MECHANISM; ENDOCANNABINOID SYSTEM; FRIEDREICH ATAXIA; GENE SILENCING; HUMAN; INHIBITORY INTERNEURON; INHIBITORY POSTSYNAPTIC POTENTIAL; INTERNEURON; LONG TERM DEPRESSION; MOTOR COORDINATION; NERVE DEGENERATION; NERVOUS SYSTEM; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PURKINJE CELL; REVIEW; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION;

EID: 84982238810     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/JP271106     Document Type: Review

References (88)

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. Arjmand S, Vaziri Z, Behzadi M, Abbassian H, Stephens GJ & Shabani M (2015). Cannabinoids and tremor induced by motor-related disorders: friend or foe? Neurotherapeutics 12, 778–787.
3. 1 receptor allosteric modulators display both agonist and signaling pathway specificity. Mol Pharmacol 83, 322–338.
4. Barclay J, Balaguero N, Mione M, Ackerman SL, Letts VA, Brodbeck J, Canti C, Meir A, Page KM, Kusumi K, Perez-Reyes E, Lander ES, Frankel WN, Gardiner RM, Dolphin AC & Rees M (2001). Ducky mouse phenotype of epilepsy and ataxia is associated with mutations in the Cacna2d2 gene and decreased calcium channel current in cerebellar PCs. J Neurosci 21, 6095–6104.
5. 1 receptors. Proc Natl Acad Sci USA 102, 15670–15675.
6. Brodbeck J, Davies A, Courtney JM, Meir A, Balaguero N, Canti C, Moss FJ, Page KM, Pratt WS, Hunt SP, Barclay J, Rees M & Dolphin AC (2002). The ducky mutation in Cacna2d2 results in altered Purkinje cell morphology and is associated with the expression of a truncated α2δ-2 protein with abnormal function. J Biol Chem 277, 7684–7693.
7. Brown SP, Safo PK & Regehr WG (2004). Endocannabinoids inhibit transmission at granule cell to Purkinje cell synapses by modulating three types of presynaptic calcium channels. J Neurosci 24, 5623–5631.
8. Chen C, Kano M, Abeliovich A, Chen L, Bao S, Kim JJ, Hashimoto K, Thompson RF & Tonegawa S (1995). Impaired motor coordination correlates with persistent multiple climbing fiber innervation in PKCγ mutant mice. Cell 83, 1233–1242.
9. Clifford DB (1983). Tetrahydrocannabinol for tremor in multiple sclerosis. Ann Neurol 13, 669–671.
10. Cole RL, Lechner SM, Williams ME, Prodanovich P, Bleicher L, Varney MA & Gu G (2005). Differential distribution of voltage-gated calcium channel alpha-2 delta (α2δ) subunit mRNA-containing cells in the rat central nervous system and the dorsal root ganglia. J Comp Neurol 491, 246–269.
11. Cooper JM, Korlipara LV, Hart PE, Bradley JL & Schapira AH (2008). Coenzyme Q10 and vitamin E deficiency in Friedreich's ataxia: predictor of efficacy of vitamin E and CoQ10 therapy. Eur J Neurol 15, 1371–1379.
12. 1 receptor in mice. Pharmacol Biochem Behav 69, 251–259.
13. Devinsky O, Cilio MR, Cross H, Fernandez-Ruiz J, French J, Hill C, Katz R, Di Marzo V, Jutras-Aswad D, Notcutt WG, Martinez-Orgado J, Robson PJ, Rohrback BG, Thiele E, Whalley B & Friedman D (2014). Cannabidiol: Pharmacology and potential therapeutic role in epilepsy and other neuropsychiatric disorders. Epilepsia 55, 791–802.
14. 1 receptor allosteric modulator ORG27569 in rats. Pharmacol Res Perspect 2, e00069.
15. Dolphin AC (2012). Calcium channel auxiliary α2δ and β subunits: trafficking and one step beyond. Nat Rev Neurosci 13, 542–555.
16. 2J mutation in Cacna2d2 results in reduced spontaneous Purkinje cell activity and altered gene expression. J Neurosci 26, 12576–12586.
17. Feliú A, Moreno-Martet M, Mecha M, Carrillo-Salinas FJ, de Lago E, Fernández-Ruiz J & Guaza C (2015). A Sativex®-like combination of phytocannabinoids as a disease-modifying therapy in a viral model of multiple sclerosis. Br J Pharmacol 172, 3579–3595.
18. Fernández-Ruiz J, Moreno-Martet M, Rodríguez-Cueto C, Palomo-Garo C, Gómez-Cañas M, Valdeolivas S, Guaza C, Romero J, Guzmán M, Mechoulam R & Ramos JA (2011). Prospects for cannabinoid therapies in basal ganglia disorders. Br J Pharmacol 163, 1365–1378.
19. 2+ signals and calcium channels in axons of developing rat cerebellar interneurones. J Physiol 527, 33–48.
20. 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.
21. 1-receptor allosteric modulator Org-27569. Behav Pharmacol 25, 182–185.
22. +-channel activators in Cacna1a(S218L) mutant mice. J Neurosci 32, 15533–15546.
23. 1 cannabinoid receptors heterologously expressed in mammalian neurons. Mol Pharmacol 65, 665–674.
24. 9-tetrahydrocannabinol are neuroprotective antioxidants. Proc Natl Acad Sci USA 95, 8268–8273.
25. Herkenham M, Groen BG, Lynn AB, De Costa BR & Richfield EK (1991). Neuronal localization of cannabinoid receptors and second messengers in mutant mouse cerebellum. Brain Res 552, 301–310.
26. Hill AJ, Mercier MS, Hill TD, Glyn SE, Jones NA, Yamasaki Y, Futamura T, Duncan M, Stott CG, Stephens GJ, Williams CM & Whalley BJ (2012b). Cannabidivarin is anticonvulsant in mouse and rat in vitro and in seizure models. Br J Pharmacol 167, 1629–1642.
27. Hill AJ, Williams CM, Whalley BJ & Stephens GJ (2012a). Phytocannabinoids as novel therapeutic agents in CNS disorders. Pharmacol Ther 133, 79–97.
28. 1 receptor-independent mechanism. Br J Pharmacol 170, 679–692.
29. Hoppa MB, Lana B, Margas W, Dolphin AC & Ryan TA (2012). α2δ expression sets presynaptic calcium channel abundance and release probability. Nature 486, 122–125.
30. 1 receptors with hypophagic effects in rats. Br J Pharmacol 152, 805–814.
31. 1 cannabinoid receptors and their associated proteins. Curr Med Chem 17, 1382–1393.
32. Ito M (1989). Long-term depression. Annu Rev Neurosci 12, 85–102.
33. 1A-subunit. Proc Natl Acad Sci USA 96, 15245–15250.
34. A receptor expression in the epileptic and ataxic mouse mutant, Tottering. Neuroscience 148, 115–125.
35. Kano M, Ohno-Shosaku T, Hashimotodani Y, Uchigashima M & Watanabe M (2009). Endocannabinoid-mediated control of synaptic transmission. Physiol Rev 89, 309–380.
36. 1 is the major cannabinoid receptor at excitatory presynaptic site in the hippocampus and cerebellum. J Neurosci 26, 2991–3001.
37. 1 cannabinoid receptor. Mol Pharmacol 88, 368–379.
38. 1 receptor is essential for cerebellum-dependent discrete motor learning. J Neurosci 26, 8829–8837.
39. Klockgether T (2011). Update on degenerative ataxias. Curr Opin Neurol 24, 339–345.
40. Kluger B, Triolo P, Jones W & Jankovic J (2015). The therapeutic potential of cannabinoids for movement disorders. Mov Disord 30, 313–327.
41. Kreitzer AC, Carter AG & Regehr WG (2002). Inhibition of interneuron firing extends the spread of endocannabinoid signaling in the cerebellum. Neuron 34, 787–796.
42. A subunit of the P/Q-type calcium channel in the rat cerebellum. Eur J Neurosci 19, 2169–2178.
43. Laprairie RB, Bagher AM, Kelly ME & Denovan-Wright EM (2015). Cannabidiol is a negative allosteric modulator of the type 1 cannabinoid receptor. Br J Pharmacol 172, 4790–4805.
44. Laprairie RB, Bagher AM, Kelly ME, Dupré DJ & Denovan-Wright EM (2014). Type 1 cannabinoid receptor ligands display functional selectivity in a cell culture model of striatal medium spiny projection neurons. J Biol Chem 289, 24845–24862.
45. Lichtman AH, Wiley JL, LaVecchia KL, Neviaser ST, Arthur DB, Wilson DM & Martin BR (1998). Effects of SR 141716A after acute or chronic cannabinoid administration in dogs. Eur J Pharmacol 357, 139–148.
46. 2+-channels impairs synaptic GABA and glutamate release in the mouse cerebellar cortex in cultured slices. Eur J Neurosci 30, 2293–2307.
47. Lynch DR, Perlman SL & Meier T (2010). A phase 3, double-blind, placebo-controlled trial of idebenone in Friedreich ataxia. Arch Neurol 67, 941–947.
48. 9-tetrahydrocannabivarin modulates inhibitory neurotransmission in the cerebellum. Br J Pharmacol 154, 204–215.
49. Mackie K & Hille B (1992). Cannabinoids inhibit N-type calcium channels in neuroblastoma-glioma cells. Proc Natl Acad Sci USA 89, 3825–3829.
50. Maejima T, Wollenweber P, Teusner LU, Noebels JL, Herlitze S & Mark MD (2013). Postnatal loss of P/Q-type channels confined to rhombic-lip-derived neurons alters synaptic transmission at the parallel fiber to purkinje cell synapse and replicates genomic Cacna1a mutation phenotype of ataxia and seizures in mice. J Neurosci 33, 5162–5174.
51. Mark MD, Maejima T, Kuckelsberg D, Yoo JW, Hyde RA, Shah V, Gutierrez D, Moreno RL, Kruse W, Noebels JL & Herlitze S (2011). Delayed postnatal loss of P/Q-type calcium channels recapitulates the absence epilepsy, dyskinesia, and ataxia phenotypes of genomic Cacna1A mutations. J Neurosci 31, 4311–4326.
52. 9-tetrahydrocannabivarin negative modulators of the endocannabinoid system? A systematic review. Br J Pharmacol 172, 737–753.
53. Meinck HM, Schönle PW & Conrad B (1989). Effect of cannabinoids on spasticity and ataxia in multiple sclerosis. J Neurol 236, 120–122.
54. Mills RJ, Yap L & Young CA (2007). Treatment for ataxia in multiple sclerosis. Cochrane Database Syst Rev 1, CD005029.
55. Mintz IM, Sabatini BL & Regehr WG (1995). Calcium control of transmitter release at a cerebellar synapse. Neuron 15, 675–688.
56. Mintz IM, Venema VJ, Swiderek KM, Lee TD, Bean BP & Adams ME (1992). P-type calcium channels blocked by the spider toxin omega-Aga-IVA. Nature 355, 827–829.
57. Nathan PJ, O'Neill BV, Napolitano A & Bullmore ET (2011). Neuropsychiatric adverse effects of centrally acting antiobesity drugs. CNS Neurosci Ther 17, 490–505.
58. Ohno-Shosaku T & Kano M (2014). Endocannabinoid-mediated retrograde modulation of synaptic transmission. Curr Opin Neurobiol 29, 1–8.
59. 1 receptor agonists produce cerebellar dysfunction in mice. J Pharmacol Exp Ther 297, 629–637.
60. Pertwee RG, Howlett AC, Abood ME, Alexander SP, Di Marzo V, Elphick MR, Greasley PJ, Hansen HS, Kunos G, Mackie K, Mechoulam R & Ross RA (2010). International Union of Basic and Clinical Pharmacology. LXXIX. Cannabinoid receptors and their ligands: beyond CB₁ and CB₂. Pharmacol Rev 62, 588–631.
61. V2.1 channelopathies. Pflugers Arch 460, 375–393.
62. 1 receptor. Mol Pharmacol 68, 1484–1495.
63. Rajakulendran S, Kaski D & Hanna MG (2012). Neuronal P/Q-type calcium channel dysfunction in inherited disorders of the CNS. Nat Rev Neurol 8, 86–96.
64. 2 receptors in the post-mortem cerebellum of humans affected by spinocerebellar ataxias. Br J Pharmacol 171, 1472–1489.
65. Rodríguez-Cueto C, Benito C, Romero J, Hernández-Gálvez M, Gómez-Ruiz M & Fernández-Ruiz J (2014b). Endocannabinoid-hydrolysing enzymes in the post-mortem cerebellum of humans affected by hereditary autosomal dominant ataxias. Pathobiology 81, 149–159.
66. Regehr WG & Mintz IM (1994). Participation of multiple calcium channel types in transmission at single climbing fiber to Purkinje cell synapses. Neuron 12, 605–613.
67. Safo PK & Regehr WG (2005). Endocannabinoids control the induction of cerebellar LTD. Neuron 48, 647–659.
68. Shibusawa N, Hashimoto K & Yamada M (2008). Thyrotropin-releasing hormone (TRH) in the cerebellum. Cerebellum 7, 84–95.
69. Skosnik PD, Edwards CR, O'Donnell BF, O'Donnell BF, Steffen A, Steinmetz JE & Hetrick WP (2008). Cannabis use disrupts eyeblink conditioning: evidence for cannabinoid modulation of cerebellar-dependent learning. Neuropsychopharmacol 33, 1432–1440.
70. 1 cannabinoid receptor knockout mice. Proc Natl Acad Sci USA 96, 5786–5790.
71. Steinmetz AB & Freeman JH (2010). Central cannabinoid receptors modulate acquisition of eyeblink conditioning. Learn Mem 17, 571–576.
72. Stephens GJ (2009). G-protein-coupled-receptor-mediated presynaptic inhibition in the cerebellum. Trends Pharmacol Sci 30, 421–430.
73. V2.1/α1A (P/Q-type) voltage-dependent calcium channel mediates inhibitory neurotransmission onto mouse cerebellar Purkinje cells. Eur J Neurosci 13, 1902–1912.
74. Szabo B, Than M, Thorn D & Wallmichrath I (2004). Analysis of the effects of cannabinoids on synaptic transmission between basket and Purkinje cells in the cerebellar cortex of the rat. J Pharmacol Exp Ther 310, 915–925.
75. Szabo B, Urbanski MJ, Bisogno T, Di Marzo V, Mendiguren A, Baer WU & Freiman I (2006). Depolarization-induced retrograde synaptic inhibition in the mouse cerebellar cortex is mediated by 2-arachidonoylglycerol. J Physiol 577, 263–280.
76. Takahashi KA & Linden DJ (2000). Cannabinoid receptor modulation of synapses received by cerebellar Purkinje cells. J Neurophysiol 83, 1167–1180.
77. 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. Neuropharmacol 57, 157–163.
78. Tanimura A, Uchigashima M, Yamazaki M, Uesaka N, Mikuni T, Abe M, Hashimoto K, Watanabe M, Sakimura K & Kano M (2012). Synapse type-independent degradation of the endocannabinoid 2-arachidonoylglycerol after retrograde synaptic suppression. Proc Natl Acad Sci USA 109, 12195–12200.
79. V2.1 channels is sufficient to cause cerebellar ataxia in mice. Cerebellum 11, 246–58.
80. 1 receptors in the rat central nervous system. Neuroscience 83, 393–411.
81. Twitchell W, Brown S & Mackie K (1997). Cannabinoids inhibit N- and P/Q-type calcium channels in cultured rat hippocampal neurons J Neurophysiol 78, 43–50.
82. Walter JT, Alviña K, Womack MD, Chevez C & Khodakhah K (2006). Decreases in the precision of Purkinje cell pacemaking cause cerebellar dysfunction and ataxia. Nat Neurosci 9, 389–397.
83. 1 receptor modulation in the cerebellum. Mol Pharmacol 79, 758–767.
84. 1 receptor-mediated signalling. J Physiol 591, 3919–3933.
85. Westenbroek RE, Sakurai T, Elliott EM, Hell JW, Starr TV, Snutch TP & Catterall WA (1995). Immunochemical identification and subcellular distribution of the alpha 1A subunits of brain calcium channels. J Neurosci 15, 6403–6418.
86. 2+ rise are selectively suppressed by cannabinoid receptor activation in cerebellar Purkinje cells. J Neurosci 26, 86–95.
87. 1 receptor. J Neurosci 26, 4740–4751.
88. 2+ channel-mutant mouse, tottering. J Physiol 547, 497–507.