Cannabinoid, melanocortin and opioid receptor expression on DRD1 and DRD2 subpopulations in rat striatum

Frontiers in Neuroanatomy

Volumn 8, Issue MAR, 2014, Pages

  Oude Ophuis, Ralph J A ^a   Boender, Arjen J ^a   van Rozen, Andrea J ^a   Adan, Roger A H ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

Cannabinoid; Dopaminergic; FISH; GPCR; Melanocortin; Opioid; Striatum

Indexed keywords

CANNABINOID RECEPTOR; DOPAMINE 1 RECEPTOR; DOPAMINE 2 RECEPTOR; MELANOCORTIN 3 RECEPTOR; MELANOCORTIN 4 RECEPTOR; MELANOCORTIN RECEPTOR; NEUROTRANSMITTER; OPIATE RECEPTOR;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CORPUS STRIATUM; DATA ANALYSIS; GENE EXPRESSION; GENE SEQUENCE; HYBRIDIZATION; IN SITU HYBRIDIZATION; MALE; NONHUMAN; NUCLEIC ACID PROBE; NUCLEOTIDE SEQUENCE; RAT; SEQUENCE HOMOLOGY;

EID: 84924358109     PISSN: None     EISSN: 16625129     Source Type: Journal    
DOI: 10.3389/fnana.2014.00014     Document Type: Article

References (69)

1. Aizman, O., Brismar, H., Uhlen, P., Zettergren, E., Levey, A. I., Forssberg, H., et al. (2000). Anatomical and physiological evidence for D1 and D2 dopamine receptor colocalization in neostriatal neurons. Nat. Neurosci. 3, 226-230. doi: 10.1038/72929
2. Albin, R. L., Young, A. B., and Penney, J. B. (1989). The functional anatomy of basal ganglia disorders. Trends Neurosci. 12, 366-375. doi: 10.1016/0166- 2236(89)90074-X
3. Alexander, G. E., Delong, M. R., and Strick, P. L. (1986). Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu. Rev. Neurosci. 9, 357-381. doi: 10.1146/annurev.ne.09.030186.002041.
4. Ambrose, L. M., Gallagher, S. M., Unterwald, E. M., and Van Bockstaele, E. J. (2006). Dopamine-D1 and delta-opioid receptors co-exist in rat striatal neurons. Neurosci. Lett. 399, 191-196. doi: 10.1016/j.neulet.2006.02.027
5. Azdad, K., Gall, D., Woods, A. S., Ledent, C., Ferre, S., and Schiffmann, S. N. (2009). Dopamine D2 and adenosine A2A receptors regulate NMDA-mediated excitation in accumbens neurons through A2A-D2 receptor heteromerization. Neuropsychopharmacology 34, 972-986. doi: 10.1038/npp.2008.144.
6. Balleine, B. W., Delgado, M. R., and Hikosaka, O. (2007). The role of the dorsal striatum in reward and decision-making. J. Neurosci. 27, 8161-8165. doi: 10.1523/JNEUROSCI.1554-07.2007.
7. Bals-Kubik, R., Herz, A., and Shippenberg, T. S. (1989). Evidence that the aver-sive effects of opioid antagonists and kappa-agonists are centrally mediated. Psychopharmacology (Berl). 98, 203-206. doi: 10.1007/BF00444692.
8. Bernard, V., Normand, E., and Bloch, B. (1992). Phenotypical characterization of the rat striatal neurons expressing muscarinic receptor genes. J. Neurosci. 12, 3591-3600.
9. Bertran-Gonzalez, J., Bosch, C., Maroteaux, M., Matamales, M., Herve, D., Valjent, E, et al. (2008). Opposing patterns of signaling activation in dopamine D1 and D2 receptor-expressing striatal neurons in response to cocaine and haloperidol. J. Neurosci. 28, 5671-5685. doi: 10.1523/JNEUROSCI.1039-08. 2008
10. Bertran-Gonzalez, J., Herve, D., Girault, J. A., and Valjent, E. (2010). What is the degree of segregation between striatonigral and striatopallidal projections? Front. Neuroanat. 4:136. doi: 10.3389/fnana.2010.00136.
11. Bolam, J. P., Hanley, J. J., Booth, P. A., and Bevan, M. D. (2000). Synaptic organisation of the basal ganglia. J. Anat. 196(pt 4), 527-542. doi: 10.1046/j.1469-7580.2000.19640527.x
12. Canals, M., Marcellino, D., Fanelli, F., Ciruela, F., De Benedetti, P., Goldberg, S. R., et al. (2003). Adenosine A2A-dopamine D2 receptor-receptor heteromeriza-tion: qualitative and quantitative assessment by fluorescence and bioluminescence energy transfer. J. Biol. Chem. 278, 46741-46749. doi: 10.1074/jbc.M3064 51200
13. Cardinal, R. N., Parkinson, J. A., Hall, J., and Everitt, B. J. (2002). Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex. Neurosci. Biobehav. Rev. 26, 321-352. doi: 10.1016/S0149-7634(02) 00007-6
14. Chang, J. Y., Chen, L., Luo, F., Shi, L. H., and Woodward, D. J. (2002). Neuronal responses in the frontal cortico-basal ganglia system during delayed matching-to-sample task: ensemble recording in freely moving rats. Exp. Brain Res. 142, 67-80. doi: 10.1007/s00221-001-0918-3.
15. Corbett, A. D., Henderson, G., McKnight, A. T., and Paterson, S. J. (2006). 75 years of opioid research: the exciting but vain quest for the Holy Grail. Br. J. Pharmacol. 147(Suppl. 1), S153-S162. doi: 10.1038/sj.bjp.07 06435
16. Cui, G., Jun, S. B., Jin, X., Pham, M. D., Vogel, S. S., Lovinger, D. M., et al. (2013). Concurrent activation of striatal direct and indirect pathways during action initiation. Nature 494, 238-242. doi: 10.1038/nature11846.
17. Cui, H., and Lutter, M. (2013). The expression of MC4Rs in D1R neurons regulates food intake and locomotor sensitization to cocaine. Genes Brain Behav. 12, 658-665. doi: 10.1111/gbb. 12057.
18. Cui, H., Mason, B. L., Lee, C., Nishi, A., Elmquist, J. K., and Lutter, M. (2012). Melanocortin 4 receptor signaling in dopamine 1 receptor neurons is required for procedural memory learning. Physiol. Behav. 106, 201-210. doi: 10.1016/j.physbeh.2012.01.025.
19. Di Chiara, G., and Imperato, A. (1988). Opposite effects of mu and kappa opiate agonists on dopamine release in the nucleus accumbens and in the dorsal caudate of freely moving rats. J. Pharmacol. Exp. Ther. 244, 1067-1080.
20. Durieux, P. F., Schiffmann, S. N., and De Kerchove D'Exaerde, A. (2012). Differential regulation of motor control and response to dopaminergic drugs by D1R and D2R neurons in distinct dorsal striatum subregions. EMBO J. 31, 640-653. doi: 10.1038/emboj.2011.400.
21. Ferre, S., Lluis, C., Justinova, Z., Quiroz, C., Orru, M., Navarro, G., et al. (2010). Adenosine-cannabinoid receptor interactions. Implications for striatal function. Br. J. Pharmacol. 160, 443-453. doi: 10.1111/j.1476-5381.2010.00 723.x
22. Filliol, D., Ghozland, S., Chluba, J., Martin, M., Matthes, H. W., Simonin, F., et al. (2000). Mice deficient for delta- and mu-opioid receptors exhibit opposing alterations of emotional responses. Nat. Genet. 25, 195-200. doi: 10.1038/ 76061
23. Fitzgerald, M. L., Shobin, E., and Pickel, V. M. (2012). Cannabinoid modulation of the dopaminergic circuitry: implications for limbic and striatal output. Prog. Neuropsychopharmacol. Biol. Psychiatry 38, 21-29. doi: 10.1016/j.pnpbp.2011.12.004.
24. Gangarossa, G., Espallergues, J., De Kerchove D'Exaerde, A., El Mestikawy, S., Gerfen, C. R., Herve, D., et al. (2013a). Distribution and compartmen-tal organization of GABAergic medium-sized spiny neurons in the mouse nucleus accumbens. Front. Neural Circuits 7:22. doi: 10.3389/fncir.2013.00022
25. Gangarossa, G., Espallergues, J., Mailly, P., De Bundel, D., De Kerchove D'Exaerde, A., Herve, D., et al. (2013b). Spatial distribution of D1R- and D2R-expressing medium-sized spiny neurons differs along the rostro-caudal axis of the mouse dorsal striatum. Front. Neural Circuits 7:124. doi: 10.3389/fncir.2013.00124
26. Gantz, I., and Fong, T. M. (2003). The melanocortin system. Am. J. Physiol. Endocrinol. Metab. 284, E468-E474. doi: 10.1152/ajpendo.00434.2002.
27. Gerfen, C. R. (1992). The neostriatal mosaic: multiple levels of compartmen-tal organization in the basal ganglia. Annu. Rev. Neurosci. 15, 285-320. doi: 10.1146/annurev.ne.15.030192.001441.
28. Gerfen, C. R., Engber, T. M., Mahan, L. C., Susel, Z., Chase, T. N., Monsma, J., et al. (1990). D1 and D2 dopamine receptor-regulated gene expression of striatonigral and striatopallidal neurons. Science 250, 1429-1432. doi: 10.1126/science.2147780
29. Gerfen, C. R., and Surmeier, D. J. (2011). Modulation of striatal projection systems by dopamine. Annu. Rev. Neurosci. 34, 441-466. doi: 10.1146/annurev-neuro-061010-113641
30. Gerfen, C. R., and Young, W. S. 3rd (1988). Distribution of striatonigral and stri-atopallidal peptidergic neurons in both patch and matrix compartments: an in situ hybridization histochemistry and fluorescent retrograde tracing study. BrainRes. 460, 161-167. doi: 10.1016/0006-8993(88)91217-6.
31. Graybiel, A. M. (2000). The basal ganglia. Curr. Biol. 10, R509-R511. doi: 10.1016/S0960-9822(00)00593-5.
32. Graybiel, A. M., Aosaki, T., Flaherty, A. W., and Kimura, M. (1994). The basal ganglia and adaptive motor control. Science 265, 1826-1831. doi: 10.1126/sci-ence.8091209
33. Haber, S. N. (2003). The primate basal ganglia: parallel and integrative networks. J. Chem. Neuroanat. 26, 317-330. doi: 10.1016/j.jchemneu.2003.10.003.
34. Hasbi, A., Fan, T., Alijaniaram, M., Nguyen, T., Perreault, M. L., O'Dowd, B. F., et al. (2009). Calcium signaling cascade links dopamine D1-D2 receptor heteromer to striatal BDNF production and neuronal growth. Proc. Natl. Acad. Sci. U.S.A. 106, 21377-21382. doi: 10.1073/pnas.0903676106.
35. Hermann, H., Marsicano, G., and Lutz, B. (2002). Coexpression of the cannabinoid receptor type 1 with dopamine and serotonin receptors in distinct neuronal subpopulations of the adult mouse forebrain. Neuroscience 109, 451-460. doi: 10.1016/S0306-4522(01)00509-7.
36. Hsu, R., Taylor, J. R., Newton, S. S., Alvaro, J. D., Haile, C., Han, G., et al. (2005). Blockade ofmelanocortin transmission inhibits cocaine reward. Eur. J. Neurosci. 21, 2233-2242. doi: 10.1111/j.1460-9568.2005.04038.x
37. Ikemoto, S. (2007). Dopamine reward circuitry: two projection systems from the ventral midbrain to the nucleus accumbens-olfactory tubercle complex. Brain Res. Rev. 56, 27-78. doi: 10.1016/j.brainresrev.2007.05.004.
38. Ince, E., Ciliax, B. J., and Levey, A. I. (1997). Differential expression of D1 and D2 dopamine and m4 muscarinic acetylcholine receptor proteins in identified striatonigral neurons. Synapse 27, 357-366. doi: 10.1002/(SICI)1098-2396(199712)27:4<357::AID-SYN9>3.0.C0;2-B
39. Jog, M. S., Kubota, Y., Connolly, C. I., Hillegaart, V., and Graybiel, A. M. (1999). Building neural representations of habits. Science 286, 1745-1749. doi: 10.1126/science.286.5445.1745.
40. Kawaguchi, Y. (1997). Neostriatal cell subtypes and their functional roles. Neurosci. Res. 27, 1-8. doi: 10.1016/S0168-0102(96)01134-0.
41. Kelley, A. E., and Domesick, V. B. (1982). The distribution of the projection from the hippocampal formation to the nucleus accumbens in the rat: an anterograde- and retrograde-horseradish peroxidase study. Neuroscience 7, 2321-2335. doi: 10.1016/0306-4522(82)90198-1.
42. Kelley, A. E., Domesick, V. B., and Nauta, W. J. (1982). The amygdalostriatal projection in the rat-an anatomical study by anterograde and retrograde tracing methods. Neuroscience7, 615-630. doi: 10.1016/0306-4522(82)90067-7.
43. Kincaid, A. E., Zheng, T., and Wilson, C. J. (1998). Connectivity and convergence of single corticostriatal axons. J. Neurosci. 18, 4722-4731.
44. Kreitzer, A. C. (2009). Physiologyand pharmacology of striatal neurons. Annu. Rev. Neurosci. 32, 127-147. doi: 10.1146/annurev.neuro.051508.135422.
45. Larson, E. R., and Ariano, M. A. (1994). Dopamine receptor binding on identified striatonigral neurons. Neurosci. Lett. 172, 101-106. doi: 10.1016/0304-3940(94)90672-6
46. Le Moine, C., and Bloch, B. (1995). D1 and D2 dopamine receptor gene expression in the rat striatum: sensitive cRNA probes demonstrate prominent segregation of D1 and D2 mRNAs in distinct neuronal populations of the dorsal and ventral striatum. J. Comp. Neurol. 355, 418-426. doi: 10.1002/cne.9035 50308
47. Lim, B. K., Huang, K. W., Grueter, B. A., Rothwell, P. E., and Malenka, R. C. (2012). Anhedonia requires MC4R-mediated synaptic adaptations in nucleus accumbens. Nature 487, 183-189. doi: 10.1038/nature11160.
48. Mansour, A., Fox, C. A., Akil, H., and Watson, S. J. (1995). Opioid-receptor mRNA expression in the rat CNS: anatomical and functional implications. Trends Neurosci. 18,22-29. doi: 10.1016/0166-2236(95)93946-U
49. Mansour, A., Fox, C. A., Burke, S., Meng, F., Thompson, R. C., Akil, H., et al. (1994). Mu, delta, and kappa opioid receptor mRNA expression in the rat CNS: an in situ hybridization study. J. Comp. Neurol. 350, 412-438. doi: 10.1002/cne.903500307.
50. Martin, A. B., Fernandez-Espejo, E., Ferrer, B., Gorriti, M. A., Bilbao, A., Navarro, M., et al. (2008). Expression and function of CB1 receptor in the rat striatum: localization and effects on D1 and D2 dopamine receptor-mediated motor behaviors. Neuropsychopharmacology 33, 1667-1679. doi: 10.1038/sj.npp.1301558.
51. Matamales, M., Bertran-Gonzalez, J., Salomon, L., Degos, B., Deniau, J. M., Valjent, E., et al. (2009). Striatal medium-sized spiny neurons: identification by nuclear staining and study of neuronal subpopulations in BAC transgenic mice. PLoS ONE 4:e4770. doi: 10.1371/journal.pone.0004770.
52. McGeorge, A. J., and Faull, R. L. (1989). The organization of the projection from the cerebral cortex to the striatum in the rat. Neuroscience 29, 503-537. doi: 10.1016/0306-4522(89)90128-0.
53. Mink, J. W. (2003). The basal ganglia and involuntary movements: impaired inhibition of competing motor patterns. Arch. Neurol. 60, 1365-1368. doi: 10.1001/archneur.60.10.1365.
54. Mogenson, G. J., Jones, D. L., and Yim, C. Y. (1980). From motivation to action: functional interface between the limbic system and the motor system. Prog. Neurobiol. 14, 69-97. doi: 10.1016/0301-0082(80) 90018-0
55. Monory, K., Blaudzun, H., Massa, F., Kaiser, N., Lemberger, T., Schutz, G., et al. (2007). Genetic dissection of behavioural and autonomic effects of Delta(9)-tetrahydrocannabinol in mice. PLoS Biol. 5:e269. doi: 10.1371/jour-nal.pbio.0050269
56. Mulder, A. H., Wardeh, G., Hogenboom, F., and Frankhuyzen, A. L. (1984). Kappa-and delta-opioid receptor agonists differentially inhibit striatal dopamine and acetylcholine release. Nature 308, 278-280. doi: 10.1038/308278a0.
57. Perreault, M. L., Hasbi, A., Alijaniaram, M., O'Dowd, B. F., and George, S. R. (2012). Reduced striatal dopamine D1-D2 receptor heteromer expression and behavioural subsensitivity in juvenile rats. Neuroscience 225, 130-139. doi: 10.1016/j.neuroscience.2012.08.042.
58. Perrine, S. A., Hoshaw, B. A., and Unterwald, E. M. (2006). Delta opioid receptor ligands modulate anxiety-like behaviors in the rat. Br. J. Pharmacol. 147, 864-872. doi: 10.1038/sj.bjp.0706686.
59. Pfeiffer, A., Brantl, V., Herz, A., and Emrich, H. M. (1986). Psychotomimesis mediated by kappa opiate receptors. Science 233, 774-776. doi: 10.1126/sci-ence.3016896
60. Phillips, A. G., and Carr, G. D. (1987). Cognition and the basal ganglia: a possible substrate for procedural knowledge. Can. J. Neurol. Sci. 14, 381-385.
61. Ragnauth, A., Schuller, A., Morgan, M., Chan, J., Ogawa, S., Pintar, J., et al. (2001). Female preproenkephalin-knockout mice display altered emotional responses. Proc. Natl. Acad. Sci. U.S.A. 98, 1958-1963. doi: 10.1073/pnas.98. 4.1958
62. Roberts, A. J., Gold, L. H., Polis, I., McDonald, J. S., Filliol, D., Kieffer, B. L., et al. (2001). Increased ethanol self-administration in delta-opioid receptor knockout mice. Alcohol. Clin. Exp. Res. 25, 1249-1256. doi: 10.1111/j.1530-0277.2001.tb02344.x
63. Schiffmann, S. N., Jacobs, O., and Vanderhaeghen, J. J. (1991). Striatal restricted adenosine A2 receptor (RDC8) is expressed by enkephalin but not by substance P neurons: an in situ hybridization histochemistry study. J. Neurochem. 57, 1062-1067. doi: 10.1111/j.1471-4159.1991.tb08257.x
64. Shetreat, M. E., Lin, L., Wong, A. C., and Rayport, S. (1996). Visualization of D1 dopamine receptors on living nucleus accumbens neurons and their colocalization with D2 receptors. J. Neurochem. 66, 1475-1482. doi: 10.1046/j.1471-4159.1996.66041475.x
65. Shippenberg, T. S., Chefer, V. I., Zapata, A., and Heidbreder, C. A. (2001). Modulation of the behavioral and neurochemical effects of psychostimulants by kappa-opioid receptor systems. Ann. N. Y. Acad. Sci. 937, 50-73. doi: 10.1111/j.1749-6632.2001.tb03558.x
66. Shippenberg, T. S., and Herz, A. (1987). Place preference conditioning reveals the involvement of D1-dopamine receptors in the motivational properties of mu- and kappa-opioid agonists. Brain Res. 436, 169-172. doi: 10.1016/0006-8993(87)91571-X
67. Smith, Y., Bennett, B. D., Bolam, J. P., Parent, A., and Sadikot, A. F. (1994). Synaptic relationships between dopaminergic afferents and cortical or thalamic input in the sensorimotor territory of the striatum in monkey. J. Comp. Neurol. 344, 1-19. doi: 10.1002/cne.903440102.
68. Torrecilla, M., Marker, C. L., Cintora, S. C., Stoffel, M., Williams, J. T., and Wickman, K. (2002). G-protein-gated potassium channels containing Kir3.2 and Kir3.3 subunits mediate the acute inhibitory effects of opioids on locus ceruleus neurons. J. Neurosci. 22, 4328-4334.
69. Voorn, P., Vanderschuren, L. J., Groenewegen, H. J., Robbins, T. W., and Pennartz, C. M. (2004). Putting a spin on the dorsal-ventral divide of the striatum. Trends Neurosci. 27, 468-474. doi: 10.1016/j.tins.2004.06.006