Detection of cannabinoid receptors CB1 and CB2 within basal ganglia output neurons in macaques: changes following experimental parkinsonism

Brain Structure and Function

Volumn 220, Issue 5, 2015, Pages 2721-2738

  Sierra, Salvador ^a,b   Luquin, Natasha ^a,b   Rico, Alberto J ^a,b   Gómez Bautista, Virginia ^a,b   Roda, Elvira ^a,b   Dopeso Reyes, Iria G ^a,b   Vázquez, Alfonso ^c   Martínez Pinilla, Eva ^a   Labandeira García, José L ^b,d   Franco, Rafael ^a,e   Lanciego, José L ^a,b  

^a UNIVERSITY OF NAVARRA   (Spain)

^b CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED SOBRE ENFERMEDADES NEURODEGENERATIVAS CIBERNED   (Spain)

^c Universidad Pública de Navarra   (Spain)

^d UNIVERSITY OF SANTIAGO DE COMPOSTELA   (Spain)

^e UNIVERSITY OF BARCELONA   (Spain)

Author keywords

Cannabinoid receptor heteromer; Cannabis; Dyskinesia; Globus pallidus; GPCRs; MPTP

Indexed keywords

CANNABINOID 1 RECEPTOR; CANNABINOID 2 RECEPTOR; LEVODOPA; CANNABINOID; CNR2 PROTEIN, MOUSE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BASAL GANGLION; CONTROLLED STUDY; EXPERIMENTAL PARKINSONISM; FLUORESCENCE IN SITU HYBRIDIZATION; HUMAN; HUMAN CELL; MACACA FASCICULARIS; MALE; NERVE CELL; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; ANIMAL; MACACA; METABOLISM; PARKINSONISM;

ANIMALS; BASAL GANGLIA; CANNABINOIDS; LEVODOPA; MACACA; MALE; NEURONS; PARKINSONIAN DISORDERS; RECEPTOR, CANNABINOID, CB1; RECEPTOR, CANNABINOID, CB2;

EID: 84940612728     PISSN: 18632653     EISSN: 18632661     Source Type: Journal    
DOI: 10.1007/s00429-014-0823-8     Document Type: Article

References (88)

1. Ashton JC, Friberg D, Darlington CL, Smith PF (2006) Expression of the cannabinoid CB2 receptor in the rat cerebellum: an immunohistochemical study. Neurosci Lett 396:113–116
2. 2 cannabinoid receptors inhibit synaptic transmission when expressed in cultured autaptic neurons. Neuropharmacology 63:514–523
3. Bayewitch M, Avidor-Reiss T, Levy R, Barg J, Mechoulam R, Vogel Z (1995) The peripheral cannabinoid receptor: adenylate cyclase inhibition and G protein coupling. FEBS Lett 375:143–147
4. Beltramo M, Bernardini N, Bertorelli R, Campanella M, Nicolussi E, Fredduzzi S, Reggiani A (2006) CB2 receptor-mediated antihyperalgesia: possible direct involvement of neural mechanisms. Eur J Neurosci 23:1530–1538
5. 2 dopamine receptor heteromers in the caudate nucleus. Neuropharmacol 79:90–100
6. Brown TM, Brotchie JM, Fitzjohn SM (2003) Cannabinoids decrease corticostriatal synaptic transmission via an effect on glutamate uptake. J Neurosci 23:11073–11077
7. Brusco A, Tagliaferro P, Saez T, Onaivi ES (2008a) Postsynaptic localization of CB2 cannabinoid receptors in the rat hippocampus. Synapse 62:944–949
8. Brusco A, Tagliaferro PA, Saez T, Onaivi ES (2008b) Ultrastructural localization of neuronal brain CB2 cannabinoid receptors. Ann NY Acad Sci 1139:450–457
9. 2 form functional heteromers in brain. J Biol Chem 287:20851–20865
10. Chiu CQ, Puente N, Grandes P, Castillo PE (2010) Dopaminergic modulation of endocannabinoid-mediated plasticity at GABAergic synapses in the prefrontal cortex. J Neurosci 30:7236–7248
11. Ciruela F, Casado V, Rodrigues RJ, Luján R, Burgueño J, Canals M, Borycz J, Rebola N, Goldberg SR, Mallol J, Cortés A, Canela EI, López-Giménez JF, Milligan G, Lluis C, Cunha RA, Ferré S, Franco R (2006) Presynaptic control of striatal glutamatergic transmission by adenosine A1-A2A receptor heteromers. J Neurosci 26:2080–2087
12. Constantino CM, Gomes I, Sotckton SD, Lim MP, Devi LA (2012) Opioid receptor heteromers in analgesia. Expert Rev Mol Med 14:e9
13. Conte-Perales L, Rico AJ, Barroso-Chinea P, Gómez-Bautista V, Roda E, Luquin N, Sierra S, Lanciego JL (2011) Pallidothalamic-projecting neurons in Macaca fascicularis co-express GABAergic and glutamatergic markers as seen in control, MPTP-treated and dyskinetic monkeys. Brain Struct Funct 216:371–386
14. Demuth DG, Molleman A (2006) Cannabinoid signalling. Life Sci 78:549–563
15. den Boon FS, Chameau P, Schaafsma-Zhao Q, van Aken W, Bari M, Oddi S, Kruse CG, Maccarrone M, Wadman WJ, Werkman TR (2012) Excitability of prefrontal cortical pyramidal neurons is modulated by activation of intracellular type-2 cannabinoid receptors. Proc Natl Acad Sci 109:3534–3539
16. Egertová M, Elphick MR (2000) Localisation of cannabinoid receptors in the rat brain using antibodies to the intracellular C-terminal tail of CB. J Comp Neurol 422:159–171
17. 1 receptor in the primate neocortex: a regional and laminar analysis. Cereb Cortex 17:175–191
18. 2 receptor: a new target for controlling neural cell survival? Trends Pharmacol Sci 28:39–45
19. 2 receptors in neuroprotective effects of cannabinoids. Mol Cell Endocrinol 286:S91–S96
20. Ferré S, Baler R, Bouvier M, Caron MG, Devi LA, Durroux T, Fuxe K, George SR, Javitch JA, Lohse MJ, Mackie K, Milligan G, Pfleger KD, Volkow ND, Waldhoer M, Wood AS, Franco R (2009) Building a new conceptual framework for receptor heteromers. Nat Chem Biol 5:131–134
21. Ferrer B, Asbrock N, Kathuria S, Piomelli D, Giuffrida A (2003) Effects of levodopa on endocannabinoid levels in rat basal ganglia: implications for the treatment of levodopa-induced dyskinesias. Eur J Neurosci 18:1607–1614
22. Freund TF, Katona I, Piomelli D (2003) Role of endogenous cannabinoids in synaptic signaling. Physiol Rev 83:1017–1066
23. Galiegue S, Mary S, Marchand J, Dussossoy D, Carriere D, Carayon P, Bouaboula M, Shire D, Le Fur G, Casellas P (1995) Expression of central and peripheral cannabinoid receptors in human immune tissues and leukocyte subpopulations. Eur J Biochem 232:54–61
24. Garcia-Arencibia M, Garcia C, Kurz A, Rodriguez-Navarro JA, Gispert-Sachez S, Mena MA, Auburger G, de Yebenes JG, Fernandez-Ruiz J (2009) Cannabinoid CB1 receptors are early downregulated followed by a further upregulation in the basal ganglia of mice with deletion of specific park genes. J Neural Transm Suppl 73:269–275
25. Gerdeman G, Lovinger DM (2001) CB1 cannabinoid receptor inhibits synaptic release of glutamate in rat dorsolateral striatum. J Neurophysiol 85:468–471
26. 1 cannabinoid receptor agonist, HU-210, reduces levodopa-induced rotations in 6-hydroxydopamine-lesioned rats. Pharmacol Toxicol 93:66–70
27. Golech SA, McCarron RM, Chen Y, Bembry J, Lenz F, Mechoulam R, Shohami E, Spatz M (2004) Human brain endothelium: coexpression and function of vanilloid and endocannabinoid receptors. Brain Res Mol Brain Res 132:87–92
28. Gong JP, Onaivi ES, Ishiguro H, Liu QR, Tagliaferro PA, Brusco A, Uhl GR (2006) Cannabinoid CB2 receptors: immunohistochemical localization in rat brain. Brain Res 1071:10–23
29. Gonsiorek W, Lunn C, Fan X, Narula S, Lundell D, Hipkin RW (2000) Endocannabinoid 2-arachidonyl glycerol is a full agonist through human type 2 cannabinoid receptor: antagonism by anandamide. Mol Pharmacol 57:1045–1050
30. 4 receptors modulates melatonin synthesis and release in the pineal gland. PLoS Biol 10:e1001347
31. 2 receptor absence in the rat central nervous system. Eur J Pharmacol 377:117–125
32. Grimsey NL, Goodfellow CE, Scotter EL, Dowie MJ, Glass M, Graham ES (2008) Specific detection of CB1 receptors: cannabinoid CB1 receptor antibodies are not all created equal! J Neurosci Method 171:78–86
33. Hasbi A, Fan T, Alijaniaram M, Nguyen T, Perreault ML, O’Dowd BF, George SR (2009) Calcium signaling cascade links dopamine D1-D2 receptor heteromer to striatal BDNF production and neuronal growth. Proc Natl Acad Sci 106:21377–21382
34. Heng L, Beverley JA, Steiner H, Tseng KY (2011) Differential developmental trajectories for CB1 cannabinoid receptor expression in limbic/associative and sensorimotor cortical areas. Synapse 65:278–286
35. Herkenham M, Lynn AB, de Costa BR, Richfield EK (1991a) Neuronal localization of cannabinoid receptors in the basal ganglia of the rat. Brain Res 547:267–274
36. Herkenham M, Lynn AB, Johnson MR, Melvin LS, de Costa BR, Rice KC (1991b) Characterization and localization of cannabinoid receptors in rat brain: a quantitative in vitro autoradiographic study. J Neurosci 11:563–583
37. Hiller C, Kühhorn J, Gmeiner P (2013) Class A G-protein-coupled receptor (GPCR) dimers and bivalent ligands. J Med Chem 56:6542–6559
38. 1 receptor mRNA in neuronal subpopulations of rat striatum: a double-label in situ hybridization study. Synapse 37:71–80
39. Julian MD, Martin AB, Cuellar B, Rodriguez De Fonseca F, Navarro M, Moratalla R, Garcia-Segura LM (2003) Neuroanatomical relationship between type 1 cannabinoid receptors and dopaminergic systems in the rat basal ganglia. Neuroscience 119:309–318
40. Katona I, Sperlágh B, Sik A, Käfalvi A, Vizi ES, Mackie K, Freund TF (1999) Presynaptically located CB1 cannabinoid receptors regulate GABA release from axon terminals of specific hippocampal interneurons. J Neurosci 19:4544–4558
41. Katona I, Sperlágh B, Maglóczky Z, Sántha E, Köfalvi A, Czirjaák S, Mackie K, Vizi ES, Freund TF (2000) GABAergic interneurons are the targets of cannabinoid actions in the human hippocampus. Neuroscience 100:797–804
42. Kearn CS, Hilliard CJ (1997) Rat microglial cell express the peripheral-type cannabinoid receptor (CB2) which is negatively coupled to adenylyl cyclase. Proceedings of the symposium on the Cannabinoids. International Cannabinoid Research Society, Burlington, p 57
43. Klein TW, Newton C, Larsen K, Lu L, Perkins I, Nong L, Friedman H (2003) The cannabinoid system and immune modulation. J Leukoc Biol 74:486–496
44. Kurlan R, Kim MH, Gash DM (1991) Oral levodopa dose-response study in MPTP-induced hemiparkinsonian monkeys: assessment with a new rating scale for monkey parkinsonism. Mov Disord 6:111–118
45. Lafourcade M, Elezgarai I, Mato S, Bakiri Y, Grandes P, Manzoni OJ (2007) Molecular components and functions of the endocannabinoid system in mouse prefrontal cortex. PLoS One 2:e709
46. Lanciego JL, Vázquez A (2012) The basal ganglia and thalamus of the long-tailed macaque in stereotaxic coordinates. A template atlas based on coronal, sagittal and horizontal brain sections. Brain Struct Funct 217:613–666
47. Lanciego JL, Barroso-Chinea P, Rico AJ, Conte-Perales L, Callen L, Roda E, Gómez-Bautista V, Lopez IP, Lluis C, Labandeira-Garcia JL, Franco R (2011) Expression of the mRNA coding the cannabinoid receptor 2 in the pallidal complex of Macaca fascicularis. J Psychopharmacol 25:97–104
48. 1 receptor binding and activation of GTP-binding proteins in the basal ganglia of patients with Parkinson’s syndrome and of MPTP-treated marmosets. Eur J Neurosci 14:1827–1832
49. Leterrier C, Lainé J, Darmon M, Boudin H, Rossier J, Lenkei Z (2006) Constitutive activation drives compartment-selective endocytosis and axonal targeting of type 1 cannabinoid receptors. J Neurosci 26:3141–3153
50. Liu QR, Pan CH, Hishimoto A, Li CY, Xi ZX, Llorente-Berzal A, Viveros MP, Ishiguro H, Arinami T, Onaivi ES, Uhl GR (2009) Species differences in cannabinoid receptor 2 (CNR2 gene): identification of novel human and rodent CB2 isoforms, differential tissue expression and regulation by cannabinoid receptor ligands. Genes Brain Behav 8:519–530
51. Lovinger DM (2008) Presynaptic modulation by endocannabinoids. Handbook Exp Pharmacol 184:435–477
52. Maccarrone M, Gubellini P, Bari M, Picconi B, Battista N, Centonze D, Bernardi G, Finazzi-Agro A, Calabresi P (2003) Levodopa treatment reverses endocannabinoid system abnormalities in experimental parkinsonism. J Neurochem 85:1018–1025
53. Mailleux P, Vanderhaeghen JJ (1992) Distribution of neuronal cannabinoid receptor in the adult rat brain: a comparative receptor binding radioautography and in situ hybridization histochemistry. Neuroscience 48:655–668
54. Mailleux P, Vanderhaeghen JJ (1993) Dopaminergic regulation of cannabinoid receptor mRNA levels in the rat caudate-putamen: an in situ hybridization study. J Neurochem 61:1705–1712
55. Mailleux P, Vanderhaeghen JJ (1994) Glutamatergic regulation of cannabinoid receptor gene expression in the caudate-putamen. Eur J Pharmacol 266:193–196
56. 2 receptor in microglial cells in response to inflammatory stimuli. J Neurochem 95:437–445
57. Mátyás F, Yanovsky Y, Mackie K, Kelsch W, Misgeld U, Freund TF (2006) Subcellular localization of type 1 cannabinoid receptors in the rat basal ganglia. Neuroscience 137:337–361
58. 1 cannabinoid receptor in the rat brain. An immunohistochemical study. Peptides 21:1735–1742
59. Morgese MG, Cassano T, Cuomo V, Giuffrida A (2007) Anti-dyskinetic effects of cannabinoids in a rat model of Parkinson’s disease: role of CB(1) and TRPV1 receptors. Exp Neurol 208:110–119
60. Morgese MG, Cassano T, Gaetani S, Macheda T, Laconca L, Dipasquale P, Ferraro L, Antonelli T, Cuomo V, Giuffrida A (2009) Neurochemical changes in the striatum of dyskinetic rats after administration of the cannabinoid agonist WIN55,212-2. Neurochem Int 54:56–64
61. Munro S, Thomas KL, Abu-Shaar M (1993) Molecular characterization of a peripheral receptor for cannabinoids. Nature 365:61–65
62. 2 receptors are expressed by perivascular microglial cells in the human brain: an immunohistochemical study. Synapse 53:208–213
63. Onaivi ES, Ishiguro H, Gong JP, Patel S, Perchuk A, Meozzi PA, Myers L, Mora Z, Tagliaferro P, Gardner E, Brusco A, Akinshola BE, Liu QR, Hope B, Iwasaki S, Arinami T, Teasenfitz L, Uhl GR (2006) Discovery of the presence and functional expression of cannabinoid CB2 receptors in brain. Ann NY Acad Sci 1074:514–536
64. Ong WY, Mackie K (1999) A light and electron microscopic study of the CB1 cannabinoid receptor in primate brain. Neuroscience 92:1177–1191
65. Perreault ML, Hasbi A, O’Dowd BF, George SR (2012) The dopamine d1-d2 receptor heteromer in striatal medium spiny neurons: evidence for a third distinct neuronal pathway in Basal Ganglia. Front Neuroanat 5:31
66. Pickel VM, Chan J, Kash TL, Rodríguez JJ, Mackie K (2004) Compartment-specific localization of cannabinoid 1 (CB1) and mu-opioid receptors in rat nucleus accumbens. Neuroscience 127:101–112
67. Puente N, Elezgarai I, Lafourcade M, Reguero L, Marsicano G, Georges F, Manzoni OJ, Grandes P (2010) Localization and function of the cannabinoid CB1 receptor in the anterolateral bed nucleus of the stria terminalis. PLoS One 5:e8869
68. Reguero L, Puente N, Elezgarai I, Mendizabal-Zubiaga J, Canduela MJ, Buceta I, Ramos A, Suárez J, Rodríguez de Fonseca F, Marsicano G, Grandes P (2011) GABAergic and cortical and subcortical glutamatergic axon terminals contain CB1 cannabinoid receptors in the ventromedial nucleus of the hypothalamus. PLoS One 6:e26167
69. Rico AJ, Barroso-Chinea P, Conte-Perales L, Roda E, Gomez-Bautista V, Gendive M, Obeso JA, Lanciego JL (2010) A direct projection from the subthalamic nucleus to the ventral thalamus in monkeys. Neurobiol Dis 39:381–392
70. Rodríguez JJ, Mackie K, Pickel VM (2001) Ultrastructural localization of the CB1 cannabinoid receptor in μ-opioid receptor patches of the rat caudate putamen nucleus. J Neurosci 21:823–833
71. Romero J, Berrendero F, Perez-Rosado A, Manzanares J, Rojo A, Fernandez-Ruiz JJ, de Yebenes JG, Ramos JA (2000) Unilateral 6-hydroxydopamine lesions of nigrostriatal dopaminergic neurons increased CB1 receptor mRNA levels in the caudate-putamen. Life Sci 66:485–494
72. 2 receptor agonists protect the striatum against malonate toxicity: relevance for Huntington’s disease. Glia 57:1154–1167
73. Sañudo-Peña MC, Tsou K, Walker JM (1999) Motor actions of cannabinoids in the basal ganglia output nuclei. Life Sci 65:703–713
74. Segovia G, Mora F, Crossman AR, Brotchie JM (2003) Effects of CB1 cannabinoid receptor modulating compounds on the hyperkinesia induced by high-dose levodopa in the reserpine-treated rat model of Parkinson’s disease. Mov Disord 18:138–149
75. Shen M, Piser TM, Seybold VS, Thayer SA (1996) Cannabinoid receptor agonists inhibit glutamatergic synaptic transmission in rat hippocampal cultures. J Neurosci 16:4322–4334
76. Shoemaker JL, Joseph BK, Ruckle MB, Mayeux PR, Prather PL (2005) The endocannabinoid noladin ether acts as a full agonist at human CB2 cannabinoid receptors. J Pharmacol Exp Ther 314:868–875
77. Skaper SD, Buriani A, Dal Toso R, Petrelli L, Romanello S, Facci L, Leon A (1996) The ALIAmide palmitoylethanolamide and cannabinoids, but not anandamide, are protective in a delayed postglutamate paradigm of excitotoxic death in cerebellar granule neurons. Proc Natl Acad Sci 93:3984–3989
78. Söderberg O, Leuchowius KJ, Gullberg M, Jarvius M, Weibrecht I, Larsson LG, Landegren U (2008) Characterizing proteins and their interactions in cells and tissues using the in situ proximity ligation assay. Methods 45:227–232
79. Sossin WS, DesGroseillers L (2006) Intracellular trafficking of RNA in neurons. Traffic 7:1581–1589
80. Stander S, Schmelz M, Metze D, Luger T, Rukwied R (2005) Distribution of cannabinoid receptor 1 (CB1) and 2 (CB2) on sensory nerve fibers and adnexal structures in human skin. J Dermatol Sci 38:177–188
81. Stella N (2004) Cannabinoid signaling in glial cells. Glia 48:267–277
82. 2A receptor complexes in the striatum. Biotechniques 51:111–118
83. van der Stelt M, Fox SH, Hill M, Crossman AR, Petrosino S, Di Marzo V, Brotchie JM (2005) A role for endocannabinoids in the generation of parkinsonism and levodopa-induced dyskinesia in MPTP-lesioned non-human primate models of Parkinson’s disease. FASEB J 19:1140–1142
84. 2 receptors. Science 310:329–332
85. Wang H, Pickel VM (2002) Dopamine D2 receptors are present in prefrontal cortical afferents and their targets in patches of the rat caudate-putamen nucleus. J Comp Neurol 442:392–404
86. Wilson-Poe AR, Morgan MM, Aicher SA, Hegarty DM (2012) Distribution of CB1 cannabinoid receptors and their relationship with mu-opioid receptors in the rat periaqueductal gray. Neuroscience 213:191–200
87. Wotherspoon G, Fox A, McIntyre P, Colley S, Bevan S, Winter J (2005) Peripheral nerve injury induces cannabinoid receptor 2 protein expression in rat sensory neurons. Neuroscience 135:235–245
88. Zeng BY, Dass B, Owen A, Rose S, Cannizzaro C, Tel BC, Jenner P (1999) Chronic L-DOPA treatment increases striatal cannabinoid CB1 receptor mRNA expression in 6-hydroxydopamine-lesioned rats. Neurosci Lett 276:71–74