Neuronal expression of CB2 cannabinoid receptor mRNAs in the mouse hippocampus

Neuroscience

Volumn 311, Issue , 2015, Pages 253-267

  Li, Y ^a   Kim, J ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

Cannabinoid; CB2 cannabinoid receptor; Confocal microscopy; Immunohistochemistry; In situ hybridization; RNAscope

Indexed keywords

CANNABINOID 2 RECEPTOR; GLUTAMIC ACID; MESSENGER RNA; CNR2 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CB2R GENE; DENTATE GYRUS; FEMALE; GENE EXPRESSION REGULATION; GENE INACTIVATION; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; HIPPOCAMPUS; IN SITU HYBRIDIZATION; MALE; MICROGLIA; MOUSE; NERVE CELL EXCITABILITY; NERVE CELL INHIBITION; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; RNASCOPE; STABLE EXPRESSION; ANIMAL; C57BL MOUSE; CONFOCAL MICROSCOPY; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNOHISTOCHEMISTRY; KNOCKOUT MOUSE; METABOLISM; NERVE CELL; POLYMERASE CHAIN REACTION; PROCEDURES; TISSUE CULTURE TECHNIQUE; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; GLUTAMIC ACID; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROGLIA; MICROSCOPY, CONFOCAL; NEURONS; POLYMERASE CHAIN REACTION; RECEPTOR, CANNABINOID, CB2; RNA, MESSENGER; TISSUE CULTURE TECHNIQUES;

EID: 84948733129     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2015.10.041     Document Type: Article

References (59)

1. 2 receptors and the endocannabinoid system for the treatment of pain. Brain Res Rev 2009, 60:255-266.
2. 2 receptors in the mouse hippocampus. Neurochem Int 2012, 60:145-152.
3. Ashton J.C. The use of knockout mice to test the specificity of antibodies for cannabinoid receptors. Hippocampus 2012, 22:643-644.
4. Ashton J.C., Zheng Y., Darlington C., Baek J.H., Smith P.F. Cannabinoid CB2 receptor immunolabelling in the healthy brain-still a live possibility. Naunyn Schmiedebergs Arch Pharmacol 2014, 387:301.
5. 2: a cannabinoid receptor with an identity crisis. Br J Pharmacol 2010, 160:467-479.
6. 2 receptor. J Neurosci Methods 2013, 216:87-95.
7. 2 receptor expression in the rat brainstem cochlear and vestibular nuclei. Acta Otolaryngol 2008, 128:961-967.
8. Balenga N.A., Martinez-Pinilla E., Kargl J., Schroder R., Peinhaupt M., Platzer W., Balint Z., Zamarbide M., Dopeso-Reyes I.G., Ricobaraza A., Perez-Ortiz J.M., Kostenis E., Waldhoer M., Heinemann A., Franco R. Heteromerization of GPR55 and cannabinoid CB2 receptors modulates signalling. Br J Pharmacol 2014, 171:5387-5406.
9. Becher B., Antel J.P. Comparison of phenotypic and functional properties of immediately ex vivo and cultured human adult microglia. Glia 1996, 18:1-10.
10. Brownjohn P.W., Ashton J.C. Spinal cannabinoid CB2 receptors as a target for neuropathic pain: an investigation using chronic constriction injury. Neuroscience 2012, 203:180-193.
11. Brusco A., Tagliaferro P., Saez T., Onaivi E.S. Postsynaptic localization of CB2 cannabinoid receptors in the rat hippocampus. Synapse 2008, 62:944-949.
12. 2 cannabinoid receptor by rodent macrophages and macrophage-like cells in relation to cell activation. Int Immunopharmacol 2002, 2:69-82.
13. Cecyre B., Thomas S., Ptito M., Casanova C., Bouchard J.F. Evaluation of the specificity of antibodies raised against cannabinoid receptor type 2 in the mouse retina. Naunyn Schmiedebergs Arch Pharmacol 2014, 387:175-184.
14. Chen Y., Dong E., Grayson D.R. Analysis of the GAD1 promoter: trans-acting factors and DNA methylation converge on the 5' untranslated region. Neuropharmacology 2011, 60:1075-1087.
15. Choi K., Le T., McGuire J., Xing G., Zhang L., Li H., Parker C.C., Johnson L.R., Ursano R.J. Expression pattern of the cannabinoid receptor genes in the frontal cortex of mood disorder patients and mice selectively bred for high and low fear. J Psychiatr Res 2012, 46:882-889.
16. den Boon F.S., Chameau P., Schaafsma-Zhao Q., van Aken W., Bari M., Oddi S., Kruse C.G., Maccarrone M., Wadman W.J., Werkman T.R. Excitability of prefrontal cortical pyramidal neurons is modulated by activation of intracellular type-2 cannabinoid receptors. Proc Natl Acad Sci USA 2012, 109:3534-3539.
17. Derbenev A.V., Stuart T.C., Smith B.N. Cannabinoids suppress synaptic input to neurones of the rat dorsal motor nucleus of the vagus nerve. J Physiol 2004, 559:923-938.
18. Devane W.A., Dysarz F.A., Johnson M.R., Melvin L.S., Howlett A.C. Determination and characterization of a cannabinoid receptor in rat brain. Mol Pharmacol 1988, 34:605-613.
19. Fernandez-Ruiz J., Berrendero F., Hernandez M.L., Ramos J.A. The endogenous cannabinoid system and brain development. Trends Neurosci 2000, 23:14-20.
20. A receptors. Br J Pharmacol 2012, 165:951-964.
21. Garcia-Gutierrez M.S., Ortega-Alvaro A., Busquets-Garcia A., Perez-Ortiz J.M., Caltana L., Ricatti M.J., Brusco A., Maldonado R., Manzanares J. Synaptic plasticity alterations associated with memory impairment induced by deletion of CB2 cannabinoid receptors. Neuropharmacology 2013, 73:388-396.
22. Gong J.P., Onaivi E.S., Ishiguro H., Liu Q.R., Tagliaferro P.A., Brusco A., Uhl G.R. Cannabinoid CB2 receptors: immunohistochemical localization in rat brain. Brain Res 2006, 1071:10-23.
23. 2) selective agonists. J Med Chem 2013, 56:8224-8256.
24. 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., Mechoulam R., Pertwee R.G. International Union of Pharmacology. XXVII. Classification of cannabinoid receptors. Pharmacol Rev 2002, 54:161-202.
25. Ishiguro H., Horiuchi Y., Ishikawa M., Koga M., Imai K., Suzuki Y., Morikawa M., Inada T., Watanabe Y., Takahashi M., Someya T., Ujike H., Iwata N., Ozaki N., Onaivi E.S., Kunugi H., Sasaki T., Itokawa M., Arai M., Niizato K., Iritani S., Naka I., Ohashi J., Kakita A., Takahashi H., Nawa H., Arinami T. Brain cannabinoid CB2 receptor in schizophrenia. Biol Psychiatry 2010, 67:974-982.
26. Kim J., Li Y. Chronic activation of CB2 cannabinoid receptors in the hippocampus increases excitatory synaptic transmission. J Physiol 2015, 593:871-886.
27. Lanciego J.L., Barroso-Chinea P., Rico A.J., Conte-Perales L., Callen L., Roda E., Gomez-Bautista V., Lopez I.P., Lluis C., Labandeira-Garcia J.L., Franco R. Expression of the mRNA coding the cannabinoid receptor 2 in the pallidal complex of Macaca fascicularis. J Psychopharmacol 2011, 25:97-104.
28. Liu Q.R., Pan C.H., Hishimoto A., Li C.Y., Xi Z.X., Llorente-Berzal A., Viveros M.P., Ishiguro H., Arinami T., Onaivi E.S., Uhl G.R. 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 2009, 8:519-530.
29. Marchalant Y., Brownjohn P.W., Bonnet A., Kleffmann T., Ashton J.C. Validating antibodies to the cannabinoid CB2 receptor: antibody sensitivity is not evidence of antibody specificity. J Histochem Cytochem 2014, 62:395-404.
30. 2 receptor in microglial cells in response to inflammatory stimuli. J Neurochem 2005, 95:437-445.
31. Matsuda L.A., Lolait S.J., Brownstein M.J., Young A.C., Bonner T.I. Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature 1990, 346:561-564.
32. McIsaac R.S., Silverman S.J., Parsons L., Xu P., Briehof R., McClean M.N., Botstein D. Visualization and analysis of mRNA molecules using fluorescence in situ hybridization in Saccharomyces cerevisiae. J Vis Exp 2013, 76:e50382.
33. Mechoulam R., Ben-Shabat S., Hanus L., Ligumsky M., Kaminski N.E., Schatz A.R., Gopher A., Almog S., Martin B.R., Compton D.R., Pertwee R.G., Griffin G., Bayewitch M., Barg J., Vogel Z. Identification of an endogenous 2-monoglyceride, present in canine gut, that binds to cannabinoid receptors. Biochem Pharmacol 1995, 50:83-90.
34. Minocci D., Massei J., Martino A., Milianti M., Piz L., Di Bello D., Sbrana A., Martinotti E., Rossi A.M., Nieri P. Genetic association between bipolar disorder and 524A>C (Leu133Ile) polymorphism of CNR2 gene, encoding for CB2 cannabinoid receptor. J Affect Disord 2011, 134:427-430.
35. Morgan N.H., Stanford I.M., Woodhall G.L. Functional CB2 type cannabinoid receptors at CNS synapses. Neuropharmacology 2009, 57:356-368.
36. Munro S., Thomas K.L., Abu-Shaar M. Molecular characterization of a peripheral receptor for cannabinoids. Nature 1993, 365:61-65.
37. 2 receptor-mediated regulation of impulsive-like behaviour in DBA/2 mice. Br J Pharmacol 2012, 165:260-273.
38. Onaivi E.S. Neuropsychobiological evidence for the functional presence and expression of cannabinoid CB2 receptors in the brain. Neuropsychobiology 2006, 54:231-246.
39. Onaivi E.S., Ishiguro H., Gong J.P., Patel S., Meozzi P.A., Myers L., Perchuk A., Mora Z., Tagliaferro P.A., Gardner E., Brusco A., Akinshola B.E., Hope B., Lujilde J., Inada T., Iwasaki S., Macharia D., Teasenfitz L., Arinami T., Uhl G.R. Brain neuronal CB2 cannabinoid receptors in drug abuse and depression: from mice to human subjects. PLoS One 2008, 3:e1640.
40. 2 cannabinoid receptor induces schizophrenia-related behaviors in mice. Neuropsychopharmacology 2011, 36:1489-1504.
41. 2) receptor activation. Br J Pharmacol 2003, 140:261-268.
42. Pinal C.S., Tobin A.J. Uniqueness and redundancy in GABA production. Perspect Dev Neurobiol 1998, 5:109-118.
43. 2 receptor agonists on responses of DRG neurons and dorsal horn neurons in neuropathic rats. Eur J Neurosci 2005, 22:371-379.
44. Showalter V.M., Compton D.R., Martin B.R., Abood M.E. Evaluation of binding in a transfected cell line expressing a peripheral cannabinoid receptor (CB2): identification of cannabinoid receptor subtype selective ligands. J Pharmacol Exp Ther 1996, 278:989-999.
45. Sierra S., Luquin N., Rico A.J., Gomez-Bautista V., Roda E., Dopeso-Reyes I.G., Vazquez A., Martinez-Pinilla E., Labandeira-Garcia J.L., Franco R., Lanciego J.L. Detection of cannabinoid receptors CB1 and CB2 within basal ganglia output neurons in macaques: changes following experimental parkinsonism. Brain Struct Funct 2015, 220:2721-2738.
46. Skaper S.D., Buriani A., Dal Toso R., Petrelli L., Romanello S., Facci L., Leon A. 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 USA 1996, 93:3984-3989.
47. Stella N. Cannabinoid signaling in glial cells. Glia 2004, 48:267-277.
48. Sugiura T., Kondo S., Kishimoto S., Miyashita T., Nakane S., Kodaka T., Suhara Y., Takayama H., Waku K. Evidence that 2-arachidonoylglycerol but not N-palmitoylethanolamine or anandamide is the physiological ligand for the cannabinoid CB2 receptor. Comparison of the agonistic activities of various cannabinoid receptor ligands in HL-60 cells. J Biol Chem 2000, 275:605-612.
49. Tong D., He S., Wang L., Jin L., Si P., Cheng X. Association of single-nucleotide polymorphisms in the cannabinoid receptor 2 gene with schizophrenia in the Han Chinese population. J Mol Neurosci 2013, 51:454-460.
50. Valenzano K.J., Tafesse L., Lee G., Harrison J.E., Boulet J.M., Gottshall S.L., Mark L., Pearson M.S., Miller W., Shan S., Rabadi L., Rotshteyn Y., Chaffer S.M., Turchin P.I., Elsemore D.A., Toth M., Koetzner L., Whiteside G.T. Pharmacological and pharmacokinetic characterization of the cannabinoid receptor 2 agonist, GW405833, utilizing rodent models of acute and chronic pain, anxiety, ataxia and catalepsy. Neuropharmacology 2005, 48:658-672.
51. 2 receptors. Science 2005, 310:329-332.
52. Wager-Miller J., Westenbroek R., Mackie K. Dimerization of G protein-coupled receptors: CB1 cannabinoid receptors as an example. Chem Phys Lipids 2002, 121:83-89.
53. Walter L., Franklin A., Witting A., Wade C., Xie Y., Kunos G., Mackie K., Stella N. Nonpsychotropic cannabinoid receptors regulate microglial cell migration. J Neurosci 2003, 23:1398-1405.
54. Wang F., Flanagan J., Su N., Wang L.C., Bui S., Nielson A., Wu X., Vo H.T., Ma X.J., Luo Y. RNAscope: a novel in situ RNA analysis platform for formalin-fixed, paraffin-embedded tissues. J Mol Diagn 2012, 14:22-29.
55. 2 receptors modulate cocaine's actions in mice. Nat Neurosci 2011, 14:1160-1166.
56. Zhang H.Y., Bi G.H., Li X., Li J., Qu H., Zhang S.J., Li C.Y., Onaivi E.S., Gardner E.L., Xi Z.X., Liu Q.R. Species differences in cannabinoid receptor 2 and receptor responses to cocaine self-administration in mice and rats. Neuropsychopharmacology 2015, 40:1037-1051.
57. 2 receptors modulate midbrain dopamine neuronal activity and dopamine-related behavior in mice. Proc Natl Acad Sci USA 2014, 111:E5007-E5015.
58. Zhang J., Hoffert C., Vu H.K., Groblewski T., Ahmad S., O'Donnell D. Induction of CB2 receptor expression in the rat spinal cord of neuropathic but not inflammatory chronic pain models. Eur J Neurosci 2003, 17:2750-2754.
59. Zhang Y., Chen K., Sloan S.A., Bennett M.L., Scholze A.R., O'Keeffe S., Phatnani H.P., Guarnieri P., Caneda C., Ruderisch N., Deng S., Liddelow S.A., Zhang C., Daneman R., Maniatis T., Barres B.A., Wu J.Q. An RNA-sequencing transcriptome and splicing database of glia, neurons, and vascular cells of the cerebral cortex. J Neurosci 2014, 34:11929-11947.