Species differences in cannabinoid receptor 2 and receptor responses to cocaine self-administration in mice and rats

Neuropsychopharmacology

Volumn 40, Issue 4, 2015, Pages 1037-1051

  Zhang, Hai Ying ^a   Bi, Guo Hua ^a   Li, Xia ^a   Li, Jie ^a   Qu, Hong ^b   Zhang, Shi Jian ^b   Li, Chuan Yun ^b   Onaivi, Emmanuel S ^c   Gardner, Eliot L ^a   Xi, Zheng Xiong ^a   Liu, Qing Rong ^a  

^a NATIONAL INSTITUTE ON DRUG ABUSE   (United States)

^b PEKING UNIVERSITY   (China)

^c WILLIAM PATERSON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1 DEOXY 3 (1,1 DIMETHYLBUTYL) DELTA8 TETRAHYDROCANNABINOL; CANNABINOID 2 RECEPTOR; COCAINE; G PROTEIN COUPLED RECEPTOR KINASE; RNA ISOFORM; SUCROSE; 1,1-DIMETHYLBUTYL-1-DEOXY-DELTA(9)-THC; CANNABINOID; CNR2 PROTEIN, MOUSE; DOPAMINE UPTAKE INHIBITOR; SWEETENING AGENT;

AGAR GEL ELECTROPHORESIS; ALTERNATIVE RNA SPLICING; AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ARTICLE; AUTOPHOSPHORYLATION; BRAIN REGION; CONTROLLED STUDY; DRUG MEGADOSE; DRUG SELF ADMINISTRATION; GENE EXPRESSION; GENE STRUCTURE; LOW DRUG DOSE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN STRUCTURE; RAT; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SPLICING; SIGNAL TRANSDUCTION; SPECIES DIFFERENCE; STOP CODON; ANIMAL; ANTAGONISTS AND INHIBITORS; BRAIN; C57BL MOUSE; GENETICS; INSTRUMENTAL CONDITIONING; KNOCKOUT MOUSE; LONG EVANS RAT; METABOLISM; MOLECULAR MODEL; ORAL DRUG ADMINISTRATION; REINFORCEMENT;

ADMINISTRATION, ORAL; ANIMALS; BRAIN; CANNABINOIDS; COCAINE; CONDITIONING, OPERANT; DOPAMINE UPTAKE INHIBITORS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MODELS, MOLECULAR; RATS; RATS, LONG-EVANS; RECEPTOR, CANNABINOID, CB2; REINFORCEMENT SCHEDULE; SELF ADMINISTRATION; SPECIES SPECIFICITY; SUCROSE; SWEETENING AGENTS;

EID: 84925461045     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2014.297     Document Type: Article

References (76)

1. Adamczyk P, Miszkiel J, McCreary AC, Filip M, Papp M, Przegalinski E (2012). The effects of cannabinoid CB1, CB2 and vanilloid TRPV1 receptor antagonists on cocaine addictive behavior in rats. Brain Res 1444: 45-54.
2. Al Mansouri S, Ojha S, Al Maamari E, Al Ameri M, Nurulain SM, Bahi A (2014). The cannabinoid receptor 2 agonist, b-caryophyllene, reduced voluntary alcohol intake and attenuated ethanol-induced place preference and sensitivity in mice. Pharmacol Biochem Behav 124: 260-268.
3. Aracil-Fernández A, Trigo JM, Garcá-Gutiérrez MS, Ortega-A lvaro A, Ternianov A, Navarro D et al (2012). Decreased cocaine motor sensitization and self-administration in mice overexpressing cannabinoid CB2 receptors. Neuropsychopharmacology 37: 1749-1763.
4. Arnold K, Bordoli L, Kopp J, Schwede T (2006). The SWISSMODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22: 195-201.
5. Atwood BK, Mackie K (2010). CB2: a cannabinoid receptor with an identity crisis. Br J Pharmacol 160: 467-479.
6. Bar-Shira O, Chechik G (2013). Predicting protein-protein interactions in the post synaptic density. Mol Cell Neurosci 56: 128-139.
7. Barbosa-Morais NL, Irimia M, Pan Q, Xiong HY, Gueroussov S, Lee LJ et al (2012). The evolutionary landscape of alternative splicing in vertebrate species. Science 338: 1587-1593.
8. Benarroch E (2007). Endocannabinoids in basal ganglia circuits: implications for Parkinson disease. Neurology 69: 306-309.
9. Bingham B, Jones PG, Uveges AJ, Kotnis S, Lu P, Smith VA et al (2007). Species-specific in vitro pharmacological effects of the cannabinoid receptor 2 (CB2) selective ligand AM1241 and its resolved enantiomers. Br J Pharmacol 151: 1061-1070.
10. Blanco-Calvo E, Rivera P, Arrabal S, Vargas A, Pavón FJ, Serrano A et al (2014). Pharmacological blockade of either cannabinoid CB1 or CB2 receptors prevents both cocaine-induced conditioned locomotion and cocaine-induced reduction of cell proliferation in the hippocampus of adult male rat. Front Integr Neurosci 7: 106.
11. Bouaboula M, Dussossoy D, Casellas P (1999). Regulation of peripheral cannabinoid receptor CB2 phosphorylation by the inverse agonist SR 144528. Implications for receptor biological responses. J Biol Chem 274: 20397-20405.
12. Brown SM, Wager-Miller J, Mackie K (2002). Cloning and molecular characterization of the rat CB2 cannabinoid receptor. Biochim Biophys Acta 1576: 255-264.
13. Brusco A, Tagliaferro P, Saez T, Onaivi ES (2008a). Postsynaptic localization of CB2 cannabinoid receptors in the rat hippocampus. Synapse 62: 944-949.
14. Brusco A, Tagliaferro PA, Saez T, Onaivi ES (2008b). Ultrastructural localization of neuronal brain CB2 cannabinoid receptors. Ann NY Acad Sci 1139: 450-457.
15. Buckley NE, McCoy KL, Mezey E, Bonner T, Zimmer A, Felder CC et al (2000). Immunomodulation by cannabinoids is absent in mice deficient for the cannabinoid CB2 receptor. Eur J Pharmacol 396: 141-149.
16. Callén L, Moreno E, Barroso-Chinea P, Moreno-Delgado D, Cortés A, Mallol J et al (2012). Cannabinoid receptors CB1 and CB2 form functional heteromers in brain. J Biol Chem 287: 20851-20865.
17. Costantino HR, Illum L, Brandt G, Johnson PH, Quay SC (2007). Intranasal delivery: physicochemical and therapeutic aspects. Int J Pharm 337: 1-24.
18. Cutando L, Busquets-Garcia A, Puighermanal E, Gomis-Gonzalez M, Delgado-Garcia JM, Gruart A et al (2013). Microglial activation underlies cerebellar deficits produced by repeated cannabis exposure. J Clin Invest 123: 2816-2831.
19. den Boon FS, Chameau P, Schaafsma-Zhao Q, van Aken W, Bari M, Oddi S et al (2012). Excitability of prefrontal cortical pyramidal neurons is modulated by activation of intracellular type-2 cannabinoid receptors. Proc Natl Acad Sci USA 109: 3534-3539.
20. Dinkel H, Michael S, Weatheritt RJ, Davey NE, Van Roey K, Altenberg B et al (2012). ELM-the database of eukaryotic linear motifs. Nucleic Acids Res 40(Database issue): D242-D251.
21. Elphick MR (2007). BfCBR: a cannabinoid receptor ortholog in the cephalochordate Branchiostoma floridae (Amphioxus). Gene 399: 65-71.
22. Elphick MR (2012). The evolution and comparative neurobiology of endocannabinoid signalling. Philos Trans R Soc Lond B Biol Sci 367: 3201-3215.
23. Feng W, Song ZH (2003). Effects of D3.49A, R3.50A, and A6.34E mutations on ligand binding and activation of the cannabinoid-2 (CB2) receptor. Biochem Pharmacol 65: 1077-1085.
24. Filipek S, Teller DC, Palczewski K, Stenkamp R (2003). The crystallographic model of rhodopsin and its use in studies of other G protein-coupled receptors. Annu Rev Biophys Biomol Struct 32: 375-397.
25. Gamaleddin I, Wertheim C, Zhu AZ, Coen KM, Vemuri K, Makryannis A et al (2012a). Cannabinoid receptor stimulation increases motivation for nicotine and nicotine seeking. Addict Biol 17: 47-61.
26. Gamaleddin I, Zvonok A, Makriyannis A, Goldberg SR, Le Foll B (2012b). Effects of a selective cannabinoid CB2 agonist and antagonist on intravenous nicotine self administration and reinstatement of nicotine seeking. PLoS One 7: e29900.
27. Garcia-Gutiérrez MS, Manzanares J (2011). Overexpression of CB2 cannabinoid receptors decreased vulnerability to anxiety and impaired anxiolytic action of alprazolam in mice. J Psychopharmacol 25: 111-120.
28. Gong J-P, Onaivi ES, Ishiguro H, Liu Q-R, Tagliaferro PA, Brusco A et al (2006). Cannabinoid CB2 receptors: immunohistochemical localization in rat brain. Brain Res 1071: 10-23.
29. Griffin G, Tao Q, Abood ME (2000). Cloning and pharmacological characterization of the rat CB(2) cannabinoid receptor. J Pharmacol Exp Ther 292: 886-894.
30. Guex N, Peitsch MC (1997). SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18: 2714-2723.
31. Gutiérrez MS, Ortega-A lvaro A, Busquets-Garcá A, Pérez-Ortiz JM, Caltana L, Ricatti MJ et al (2013). Synaptic plasticity alterations associated with memory impairment induced by deletion of CB2 cannabinoid receptors. Neuropharmacology 73: 388-396.
32. Huffman JW, Liddle J, Yu S, Aung MM, Abood ME, Wiley JL et al (1999). 3-(10,10-Dimethylbutyl)-1-deoxy-delta8-THC and related compounds: synthesis of selective ligands for the CB2 receptor. Bioorg Med Chem 7: 2905-2914.
33. Ignatowska-Jankowska BM, Muldoon PP, Lichtman AH, Damaj MI (2013). The cannabinoid CB receptor is necessary for nicotineconditioned place preference, but not other behavioral effects of nicotine in mice. Psychopharmacology (Berl) 229: 591-601.
34. Illum L, Watts P, Fisher AN, Hinchcliffe M, Norbury H, Jabbal-Gill I et al (2002). Intranasal delivery of morphine. J Pharmacol Exp Ther 301: 391-400.
35. Ishiguro H, Carpio O, Horiuchi Y, Shu A, Higuchi S, Schanz N et al (2010a). A nonsynonymous polymorphism in cannabinoid CB2 receptor gene is associated with eating disorders in humans and food intake is modified in mice by its ligands. Synapse 64: 92-96.
36. Ishiguro H, Horiuchi Y, Ishikawa M, Koga M, Imai K, Suzuki Y et al (2010b). Brain cannabinoid CB2 receptor in schizophrenia. Biol Psychiatry 67: 974-982.
37. Jorda MA, Rayman N, Valk P, De Wee E, Delwel R (2003). Identification, characterization, and function of a novel oncogene: the peripheral cannabinoid receptor Cb2. Ann NY Acad Sci 996: 10-16.
38. Koren E, Lev-Maor G, Ast G (2007). The emergence of alternative 3' and 5' splice site exons from constitutive exons. PLoS Comput Biol 3: e95.
39. Kosten TA, Zhang XY, Haile CN (2007). Strain differences in maintenance of cocaine self-administration and their relationship to novelty activity responses. Behav Neusci 121: 380-388.
40. Lanciego JL, Barroso-Chinea P, Rico AJ, Conte-Perales L, Callen L, Roda E et al (2011). Expression of the mRNA coding the cannabinoid receptor 2 in the pallidal complex of Macaca fascicularis. J Psychopharmacol 25: 97-104.
41. Liu Q-R, Pan CH, Hishimoto A, Li C-Y, Xi Z-X, Llorente-Berzal A et al (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.
42. Liu Q-R, Rubio FJ, Bossert JM, Marchant NJ, Fanous S, Hou X et al (2014). Detection of molecular alterations in methamphetamineactivated Fos-expressing neurons from a single rat dorsal striatum using fluorescence-activated cell sorting (FACS). J Neurochem 128: 173-185.
43. Marriott KS, Huffman JW, Wiley JL, Martin BR (2006). Synthesis and pharmacology of 11-nor-1-methoxy-9-hydroxyhexahydrocannabinols and 11-nor-1-deoxy-9-hydroxyhexahydrocannabinols: new selective ligands for the cannabinoid CB2 receptor. Bioorg Med Chem 14: 2386-2397.
44. Matsuda LA (1997). Molecular aspects of cannabinoid receptors. Crit Rev Neurobiol 11: 143-166.
45. McPartland JM (2004). Phylogenomic and chemotaxonomic analysis of the endocannabinoid system. Brain Res Brain Res Rev 45: 18-29.
46. Mechoulam R, Parker LA (2013). The endocannabinoid system and the brain. Annu Rev Psychol 64: 21-47.
47. Mercier RW, Pei Y, Pandarinathan L, Janero DR, Zhang J, Makriyannis A (2010). hCB2 ligand-interaction landscape: cysteine residues critical to biarylpyrazole antagonist binding motif and receptor modulation. Chem Biol 17: 1132-1142.
48. Merkin J, Russell C, Chen P, Burge CB (2012). Evolutionary dynamics of gene and isoform regulation in Mammalian tissues. Science 338: 1593-1599.
49. Modrek B, Lee CJ (2003). Alternative splicing in the human, mouse and rat genomes is associated with an increased frequency of exon creation and /or loss. Nat Genet 34: 177-180.
50. Morgan NH, Stanford IM, Woodhall GL (2009). Functional CB2 type cannabinoid receptors at CNS synapses. Neuropharmacology 57: 356-368.
51. Mukherjee S, Adams M, Whiteaker K, Daza A, Kage K, Cassar S et al (2004). Species comparison and pharmacological characterization of rat and human CB2 cannabinoid receptors. Eur J Pharmacol 505: 1-9.
52. Navarrete F, Rodrguez-Arias M, Martn-Garcá E, Navarro D, Garcá-Gutiérrez MS, Aguilar MA et al (2013). Role of CB2 cannabinoid receptors in the rewarding, reinforcing, and physical effects of nicotine. Neuropsychopharmacology 38: 2515-2524.
53. Onaivi ES, Ishiguro H, Gong J-P, Patel S, Meozzi PA, Myers L et al (2008). Functional expression of brain neuronal CB2 cannabinoid receptors are involved in the effects of drugs of abuse and in depression. Ann NY Acad Sci 1139: 434-449.
54. Onaivi ES, Ishiguro H, Gu S, Liu Q-R (2012). CNS effects of CB2 cannabinoid receptors: beyond neuro-immuno-cannabinoid activity. J Psychopharmacol 26: 92-103.
55. Pickel VM, Chan J, Kearn CS, Mackie K (2006). Targeting dopamine D2 and cannabinoid-1 CB1 receptors in rat nucleus accumbens. J Comp Neurol 495: 299-313.
56. Reyes BA, Rosario JC, Piana PM, Van Bockstaele EJ (2009). Cannabinoid modulation of cortical adrenergic receptors and transporters. J Neurosci Res 87: 3671-3678.
57. Rivera P, Miguens M, Coria SM, Rubio L, Higuera-Matas A, Bermudez-Silva FJ et al (2013). Cocaine self-administration differentially modulates the expression of endogenous cannabinoid system-related proteins in the hippocampus of Lewis vs. Fischer 344 rats. Int J Neuropsychopharmacol 16: 1277-1293.
58. Rosenbaum DM, Rasmussen SG, Kobilka BK (2009). The structure and function of G-protein-coupled receptors. Nature 459: 356-363.
59. Schwede T, Kopp J, Guex N, Peitsch MC (2003). SWISS-MODEL: an automated protein homology-modeling server. Nucleic Acids Res 31: 3381-3385.
60. Shire D, Carillon C, Kaghad M, Calandra B, Rinaldi-Carmona M, Le Fur G et al (1995). An amino-terminal variant of the central cannabinoid receptor resulting from alternative splicing. J Biol Chem 270: 3726-3731.
61. Song R, Zhang HY, Li X, Bi GH, Gardner EL, Xi ZX (2012). Increased vulnerability to cocaine in mice lacking dopamine D3 receptors. Proc Natl Acad Sci USA 109: 17675-17680.
62. Song ZH, Feng W (2002). Absence of a conserved proline and presence of a conserved tyrosine in the CB2 cannabinoid receptor are crucial for its function. FEBS Lett 531: 290-294.
63. Suárez J, Llorente R, Romero-Zerbo SY, Mateos B, Bermúdez-Silva FJ, de Fonseca FR et al (2009). Early maternal deprivation induces gender-dependent changes on the expression of hippocampal CB1 and CB2 cannabinoid receptors of neonatal rats. Hippocampus 19: 623-632.
64. Tao Q, McAllister SD, Andreassi J, Nowell KW, Cabral GA, Hurst DP et al (1999). Role of a conserved lysine residue in the peripheral cannabinoid receptor CB2: evidence for subtype specificity. Mol Pharmacol 55: 605-613.
65. Tubbs RR, Wang H, Wang Z, Minca EC, Portier BP, Gruver AM et al (2013). Ultrasensitive RNA in situ hybridization for detection of restricted clonal expression of low-abundance immunoglobulin light chain mRNA in B-cell lymphoproliferative disorders. Am J Clin Pathol 140: 736-746.
66. Van Sickle MD, Duncan M, Kingsley PJ, Mouihate A, Urbani P, Mackie K et al (2005). Identification and functional characterization of brainstem cannabinoid CB2 receptors. Science 310: 329-332.
67. Vinckenbosch N, Dupanloup I, Kaessmann H (2006). Evolutionary fate of retroposed gene copies in the human genome. Proc Natl Acad Sci USA 103: 3220-3225.
68. Wang F, Flanagan J, Su N, Wang L-C, Bui S, Nielson A et al (2012). RNAscope: a novel in situ RNA analysis platform for formalinfixed, paraffin-embedded tissues. J Mol Diagn 14: 22-29.
69. Wooding S (2011). Signatures of natural selection in a primate bitter taste receptor. J Mol Evol 73: 257-265.
70. Xi Z-X, Gilbert JG, Pak AC, Ashby CR Jr., Heidbreder CA, Gardner EL (2005). Selective dopamine D3 receptor antagonism by SB-277011A attenuates cocaine reinforcement as assessed by progressive-ratio and variable-cost-variable-payoff fixedratio cocaine self-administration in rats. Eur J Neurosci 21: 3427-3438.
71. Xi Z-X, Peng X-Q, Li X, Song R, Zhang H-Y, Liu Q-R et al (2011). Brain cannabinoid CB receptors modulate cocaine's actions in mice. Nat Neurosci 14: 1160-1166.
72. Yao BB, Mukherjee S, Fan Y, Garrison TR, Daza AV, Grayson GK et al (2006). In vitro pharmacological characterization of AM1241: a protean agonist at the cannabinoid CB2 receptor? Br J Pharmacol 149: 145-154.
73. Zhang J, Webb DM (2003). Evolutionary deterioration of the vomeronasal pheromone transduction pathway in catarrhine primates. Proc Natl Acad Sci USA 100: 8337-8341.
74. Zhang S-J, Liu C-J, Shi M, Kong L, Chen J-Y, Zhou W-Z et al (2013). RhesusBase: a knowledgebase for the monkey research community. Nucleic Acids Res 41(Database issue): D892-D905.
75. Zhang S-J, Liu C-J, Yu P, Zhong X, Chen J-Y, Yang X et al (2014a). Evolutionary interrogation of human biology in well-annotated genomic framework of rhesus macaque.Mol Biol Evol 31: 1309-1324.
76. Zhang Y, Chen K, Sloan SA, Bennett ML, Scholze AR, O'Keeffe S et al (2014b). An RNA-sequencing transcriptome and splicing database of glia, neurons, and vascular cells of the cerebral cortex. J Neurosci 34: 11929-11947.