Cannabinoids increase type 1 cannabinoid receptor expression in a cell culture model of striatal neurons: Implications for Huntington's disease

Neuropharmacology

Volumn 72, Issue , 2013, Pages 47-57

  Laprairie, Robert B ^a   Kelly, Melanie E M ^a   Denovan Wright, Eileen M ^a  

^a DALHOUSIE UNIVERSITY   (Canada)

Author keywords

Akt; Cannabinoids; Gene expression; Huntington's disease; NF kB; Type 1 cannabinoid receptor (CB1)

Indexed keywords

2 (2 CHLORO 4 IODOANILINO) N CYCLOPROPYLMETHOXY 3,4 DIFLUOROBENZAMIDE; 4 AMINOBUTYRIC ACID; ADENOSINE TRIPHOSPHATE; ANANDAMIDE; ARACHIDONYL 2' CHLOROETHYLAMIDE; BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR 2; CANNABINOID; CANNABINOID 1 RECEPTOR; CANNABINOID 1 RECEPTOR AGONIST; CANNABINOID 1 RECEPTOR ANTAGONIST; HUNTINGTIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; JSH 23; MESSENGER RNA; METHANANDAMIDE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PROTEIN KINASE B; UNCLASSIFIED DRUG; WORTMANNIN;

4 AMINOBUTYRIC ACID RELEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN NERVE CELL; CELL CULTURE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG MECHANISM; ENZYME ACTIVITY; HUNTINGTON CHOREA; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN SYNTHESIS; STRIATE CORTEX; TREATMENT OUTCOME;

EID: 84884889597     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2013.04.006     Document Type: Article

References (51)

1. Ahn, K.H., Mahmoud, M.M., Kendall, D.A., 2012. Allosteric modulator ORG27569 induces CB1 cannabinoid receptor high affinity agonist binding state, receptor internalization, and Gi-independent ERK1/2 kinase activation. J. Biol. Chem. 287, 12070-12082.
2. Blázquez, C., Chiarlone, A., Sagredo, O., Aguado, T., Pazos, M.R., Resel, E., Palazuelos, J., Julien, B., Salazar, M., Börner, C., Benito, C., Carrasco, C., Diez-Zaera, M., Paoletti, P., Díaz-Hernández, M., Ruiz, C., Sendtner, M., Lucas, J.J., de Yébenes, J.G., Marsicano, G., Monory, K., Lutz, B., Romero, J., Alberch, J., Ginés, S., Kraus, J., Fernández-Ruiz, J., Galve-Roperh, I., Guzmán, M., 2011. Loss of striatal type 1 cannabinoid receptors is a key pathogenic factor in Huntington's disease. Brain 134, 119-136.
3. Borner, C., Bedini, A., Holt, V., Kraus, J., 2008. Analysis of promoter regions regulating basal and interleukin-4 inducible expression of the human CB1 receptor gene in T lymphocytes. Mol. Pharmacol. 73, 1013-1019. (Pubitemid 351397906)
4. Borner, C., Holt, V., Kraus, J., 2007a. Transcriptional regulation of the cannabinoid receptor type 1 gene in T cells by cannabinoids. J. Leukoc. Biol. 81, 336-343. (Pubitemid 46021284)
5. Borner, C., Holt, V., Kraus, J., 2007b. Activation of human T cells induces upregulation of cannabinoid type 1 transcription. Neuroimmunomodulation 14, 281-286. (Pubitemid 351737854)
6. Brailoiu, G.C., Oprea, T.I., Zhao, P., Abood, M.E., Brailoiu, E., 2011. Intracellular cannabinoid type 1 (CB1) receptors are activated by anandamide. J. Biol. Chem. 19, 29166-29174.
7. Cepeda, C., StarlingAJ, Wu N., Nguyen, O.K., Uzgil, B., Soda, T., André, V.M., Ariano, M.A., Levine, M.S., 2004. Increased GABAergic function in mouse models of Huntington's disease: reversal by BDNF. J. Neurosci. Res. 78, 855-867. (Pubitemid 39657573)
8. Corchero, J., Romero, J., Berrendero, F., Fernandez-Ruiz, J., Ramos, J.A., Fuentes, J.A., Manzanares, J., 1999. Time-dependent differences of repeated administration with Delta9-tetrahydrocannabinol in proenkephalin and cannabinoid receptor gene expression and G-protein activation by mu-opiod and CB1-cannabinoid receptors in the caudate-putamen. Brain Res. Mol. Brain Res. 67, 148-157. (Pubitemid 29170077)
9. Cosenza, M., Gifford, A.M., Gatley, S.J., Pyatt, B., Liu, Q., Makriyannis, A., Volkow, N.D., 2000. Locomotor activity and occupancy of brain cannabinoid CB1 receptors by the antagonist/inverse agonist AM281. Synapse 38, 477-482.
10. Coutts, A.A., Anavi-Goffer, S., Ross, R.A., MacEwan, D.J., Mackie, K., Pertwee, R.G., Irving, A.J., 2001. Agonist-induced internalization and trafficking of cannabinoid CB1 receptors in hippocampal neurons. J. Neurosci. 21, 2425-2433. (Pubitemid 32240539)
11. Cui, L., Jeong, H., Borovecki, F., Parkhurst, C.N., Tanese, N., Krainc, D., 2006. Transcriptional repression of PGC-1alpha by mutant huntingtin leads to mitochondrial dysfunction and neurodegeneration. Cell 127, 59-69. (Pubitemid 44466642)
12. Daigle, T.L., Kearn, C.S., Mackie, K., 2008. Rapid CB1 cannabinoid receptor desensitization defines the time course of ERK1/2 MAP kinase signalling. Neuropharmacology 54, 36-44. (Pubitemid 350299401)
13. Denovan-Wright, E.M., Robertson, H.A., 2000. Cannabinoid receptor messenger RNA levels decrease in a subset of neurons of the lateral striatum, cortex and hippocampus of transgenic Huntington's disease mice. Neuroscience 98, 705-713. (Pubitemid 30417587)
14. Dowie, M.J., Bradshaw, H.B., Howard, M.L., Nicholson, L.F., Faull, R.L., Hannan, A.J.M., Glass, M., 2009. Altered CB1 receptor and endocannabinoid levels precede motor symptom onset in a transgenic mouse model of Huntington's disease. Neuroscience 163, 456-465.
15. Dowie, M.J., Howard, M.L., Nicholson, L.F., Faull, R.L., Hannan, A.J., Glass, M., 2010. Behavioural and molecular consequences of chronic cannabinoid treatment in Huntington's disease transgenic mice. Neuroscience 170, 324-336.
16. Eggan, S.M., Mizoguchi, Y., Stoyak, S.R., Lewis, D.A., 2010. Development of cannabinoid receptor 1 protein and messenger RNA in monkey dorsolateral prefrontal cortex. Cereb. Cortex 20, 1164-1174.
17. Fernandez-Ruiz, J.J., Berrendero, F., Hernandez, M.L., Romero, J., Ramos, J.A., 1999. Role of endocannabinoids in brain development. Life Sci. 65, 725-736. (Pubitemid 29362778)
18. Fernandez-Ruiz, J., Gomez, M., Hernandez, M., de Miguel, R., Ramos, J.A., 2004. Cannabinoids and gene expression during brain development. Neurotox. Res. 6, 389-401.
19. Fitzgerald, M.L., Chan, J., Mackie, K., Lupica, C.R., Pickel, V.M., 2012. Altered dendritic distribution of dopamine D2 receptors and reduction in mitochondrial number in parvalbumin-containing interneurons in medial prefrontal cortex of cannabinoid-1 (CB1) receptor knockout mice. J. Comp. Neurol. 520, 4013-4031.
20. Ghose, J., Sinha, M., Das, E., Jana, N.R., Battacharyya, N.P., 2011. Regulation of miR-146a by RelA/NFkB and p53 in STHdh(Q111)/Hdh(Q111) cells, a cell model of Huntington's disease. PLoS One 6, e23837.
21. Graham, E.S., Ball, N., Scotter, E.L., Narayan, P., Dragunow, M., Glass, M., 2006. Induction of Krox-24 by endogenous cannabinoid type 1 receptors in Neuro2a cells is mediated by the MEK-ERK MAPK pathway and is suppressed by the phosphatidylinositol 3-kinase pathway. J. Biol. Chem. 281, 29085-29095. (Pubitemid 44507052)
22. Gomez, G.T., Hu, H., McCaw, E.A., Denovan-Wright, E.M., 2006. Brain-specific factors in combination with mutant huntingtin induce gene-specific transcriptional dysregulation. Mol. Cell. Neurosci. 31, 661-675.
23. Hill, M.N., Hillard, C.J., McEwen, B.S., 2011. Alterations in corticolimbic dendritic morphology and emotional behaviour in cannabinoid CB1 receptor-deficient mice parallel the effects of chronic stress. Cereb. Cortex 21, 2056-2064.
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., 2002. International Union of Pharmacology. XXVII. Classification of cannabinoid receptors. Pharmacol. Rev. 54, 161-202. (Pubitemid 34575709)
25. Howlett, A.C., Reggio, P.H., Childers, S.R., Hampson, R.E., Ulloa, N.M., Deutsch, D.G., 2011. Endocannabinoid tone versus constitutive activity of cannabinoid receptors. Br. J. Pharmacol. 163, 1329-1343.
26. Kim, J., Alger, B.E., 2010. Reduction in endocannabinoid tone is a homeostatic mechanism for specific inhibitory synapses. Nat. Neurosci. 13, 592-600.
27. Kreitzer, A.C., Regehr, W.G., 2001. Retrograde inhibition of presynaptic calcium influx by endogenous cannabinoids at excitatory synapses onto Purkinje cells. Neuron 29, 717-727. (Pubitemid 32323944)
28. Kunkel, T.A., 1985. Rapid and efficient site-specific mutagenesis without phenotypic selection. PNAS 89, 488-492. (Pubitemid 15128292)
29. Laprairie, R.B., Kelly, M.E.M., Denovan-Wright, E.M., 2012. The dynamic nature of type 1 cannabinoid receptor (CB1) gene transcription. Br. J. Pharmacol. 167, 1583-1595.
30. Luthi-Carter, R., Strand, A., Peters, N.L., Solano, S.M., Hollingsworth, Z.R., Menon, A.S., Frey, A.S., Spektor, B.S., Pennery, E.B., Schilling, G., Ross, C.A., Borchelt, D.R., Tapscott, S.J., Young, A.B., Cha, J.H., Olson, J.M., 2000. Decreased expression of striatal signaling genes in a mouse model of Huntington's disease. Hum. Mol. Genet. 9, 1259-1271. (Pubitemid 30312475)
31. Mallet, C., Daulhac, L., Bonnefont, J., Ledent, C., Etienne, M., Chapuy, E., Libert, F., Eschalier, A., 2008. Endocannabinoid and serotonergic systems are needed for acetaminophen-induced analgesia. Pain 139, 190-200.
32. Marcora, E., Kennedy, M.D., 2010. The Huntington's disease mutation impairs huntingtin's role in the transport of NF-kB from the synapse to the nucleus. Hum. Mol. Genet. 19, 4373-4384.
33. McCaw, E.A., Hu, H., Gomez, G.T., Hebb, A.L., Kelly, M.E., Denovan-Wright, E.M., 2004. Structure, expression, and regulation of the cannabinoid receptor gene (CB1) in Huntington's disease transgenic mice. Eur. J. Biochem. 271, 4909-4920. (Pubitemid 40065594)
34. Mievis, S., Blum, D., Ledent, C., 2011. Worsening of Huntington's disease phenotype in CB1 receptor knockout mice. Neurobiol. Dis. 42, 524-529.
35. Monnet-Tschudi, F., Hazekamp, A., Perret, N., Zurich, M.G., Mangin, P., Giroud, C., Honegger, P., 2008. Delta-9-tetrahydrocannabinol accumulation, metabolism and cell-type specific adverse effects in aggregating brain cell cultures. Toxicol. Appl. Pharmacol. 228, 8-16.
36. Mor, M., Rivara, S., Lodola, A., Piazzi, P.V., Tarzia, G., Duranti, A., Tontini, A., Piersanti, G., Kathuria, S., Piomelli, D., 2004. Cyclohexylcarbamic acid 30-or 40-substituted biphenyl-3-yl esters as fatty acid amide hydrolase inhibitors: synthesis, quantitative structure-activity relationships, and molecular modeling studies. J. Med. Chem. 47, 4998-5008. (Pubitemid 39314898)
37. Mukhopadhyay, B., Liu, J., Osei-Hyiaman, D., Godlewski, G.,Mukhopadhyay, P.,Wang, L., Jeong, W.I., Gao, B., Duester, G., Mackie, K., Kojima, S., Kunos, G., 2010. Transcriptional regulation of cannabinoid receptor-1 expression in the liver by retinoic acid acting via retinoic acid receptor-gamma. J. Biol. Chem. 285, 19002-19011.
38. Nolan, G.P., Ghosh, S., Liou, H.C., Tempst, P., Baltimore, D., 1991. DNA binding and I kappa B inhibition of the cloned p65 subunit of NF-kappa B, a rel-related polypeptide. Cell 64, 961-969. (Pubitemid 121001183)
39. Pertwee, R.G., 2005. Pharmacological actions of cannabinoids. Handb Exp. Pharmacol. 168, 1-51.
40. Polo, M.L., Arnoni, M.V., Riggio, M., Wargon, V., Lanari, C., Novaro, V., 2010. Responsiveness of PI3K and MEK inhibitors in Breast Cancer. Use of a 3D Culture System to Study Pathways Related to Hormone Independence in Mice. PLoS One 5, e10786.
41. Proto, M.C., Gazzerro, P., Di Croce, L., Santoro, A., Malfitano, A.M., Pisanti, S., Laezza, C., Bifulco, M., 2011. Interaction of endocannabinoid system and steroid hormones in the control of colon cancer cell growth. J. Cell. Physiol. 227, 250-258.
42. Reijonen, S., Kukkonen, J.P., Hyrskyluoto, A., Kivinen, J., Kairisalo, M., Takei, N., Lindholm, D., Korhonen, L., 2010. Downregulation of NF-kappaB signaling by mutant huntingtin proteins induces oxidative stress and cell death. Cell. Mol. Life Sci. 67, 1929-1941.
43. Sanchez, M.G., Ruiz-Llorente, L., Sanchez, A.M., Diaz-Laviada, I., 2003. Activation of phosphoinositide 3-kinase/PKB pathway by CB(1) and CB(2) cannabinoid receptors expressed in prostate PC-3 cells. Involvement in Raf-1 stimulation and NGF induction. Cell. Signal. 15, 851-859. (Pubitemid 36776659)
44. Sapp, E., Ge, P., Aizawa, H., Bird, E., Penney, J., Young, A.B., Vonsattel, J.P., DiFiglia, M., 1995. Evidence for a preferential loss of enkephalin immunoreactivity in the external globus pallidus in low grade Huntington's disease using high resolution image analysis. Neuroscience 64, 397-404.
45. Trettel, F., Rigamonti, D., Hilditch-Maguire, P., Wheeler, V.C., Sharp, A.H., Persichetti, F., Cattaneo, E., MacDonald, M.E., 2000. Dominant phenotypes produced by the HD mutation in STHdh(Q111) striatal cells. Hum. Mol. Genet. 9, 2799-2809.
46. Van Laere, K., Casteels, C., Dhollander, I., Goffin, K., Grachev, I., Bormans, G., Vandernberghe, W., 2010. Widespread decrease of type 1 cannabinoid receptor availability in Huntington's disease in vivo. J. Nucl. Med. 51, 1413-1417.
47. Vitalis, T., Laine, J., Simon, A., Roland, A., Leterrier, C., Lenkei, Z., 2008. The type 1 cannabinoid receptor is highly expressed in embryonic cortical projection neurons and negatively regulates neurite growth in vitro. Euro J. Neurosci. 28, 1705-1718.
48. Walker, F.O., 2007. Huntington's disease. Semin. Neurol. 27, 143-150. (Pubitemid 46564475)
49. Wiley, J.L., Breivogel, C.S., Mahadevan, A., Pertwee, R.G., Cascio, M.G., Bolognini, D., Huffman, J.W., Welentiny, D.M., Vann, R.E., Razdan, R.K., Martin, B.R., 2011. Structural and pharmacological analysis of O-2050, a putative neutral cannabinoid CB(1) antagonist. Eur. J. Pharmacol. 651, 96-105.
50. Wilson, R.I., Nicoll, R.A., 2001. Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses. Nature 410, 588-592. (Pubitemid 32267203)
51. Zuccato, C., Marullo, M., Conforti, P., MacDonald, M.E., Tartari, M., Cattaneo, E., 2008. Systematic assessment of BDNF and its receptor levels in human cortices affected by Huntington's disease. Brain Pathol. 18, 225-238. (Pubitemid 351430396)