Cannabinoid modulation of alpha2 adrenergic receptor function in rodent medial prefrontal cortex

European Journal of Neuroscience

Volumn 40, Issue 8, 2014, Pages 3202-3214

  Cathel, Alessandra M ^a   Reyes, Beverly A S ^b   Wang, Qin ^c   Palma, Jonathan ^a   Mackie, Kenneth ^d   Van Bockstaele, Elisabeth J ^b   Kirby, Lynn G ^a  

^a TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^d INDIANA UNIVERSITY   (United States)

Author keywords

Electron microscopy; Electrophysiology; Immunohistochemistry; Mouse; Rat

Indexed keywords

2,3 DIHYDRO 5 METHYL 3 (MORPHOLINOMETHYL) 6 (1 NAPHTHOYL)PYRROLO[1,2,3 DE][1,4]BENZOXAZINE; ALPHA 2 ADRENERGIC RECEPTOR; CANNABINOID 1 RECEPTOR; CLONIDINE; ALPHA 2 ADRENERGIC RECEPTOR STIMULATING AGENT; BENZOXAZINE DERIVATIVE; MORPHOLINE DERIVATIVE; NAPHTHALENE DERIVATIVE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL MEMBRANE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DENDRITE; EVOKED RESPONSE; GENETICALLY ENGINEERED MOUSE STRAIN; IMMUNOCYTOCHEMISTRY; IMMUNOELECTRON MICROSCOPY; IN VITRO STUDY; MALE; MEDIAL PREFRONTAL CORTEX; MOUSE; NERVE CELL EXCITABILITY; NERVE CELL MEMBRANE CONDUCTANCE; NERVE ENDING; NEUROMODULATION; NONHUMAN; PROTEIN PROTEIN INTERACTION; PYRAMIDAL NERVE CELL; RAT; ROUGH ENDOPLASMIC RETICULUM; SPRAGUE DAWLEY RAT; WHOLE CELL PATCH CLAMP; ACTION POTENTIAL; AGONISTS; ANIMAL; DRUG EFFECTS; GENE TARGETING; GENETICS; PHYSIOLOGY; PREFRONTAL CORTEX; ULTRASTRUCTURE;

ACTION POTENTIALS; ADRENERGIC ALPHA-2 RECEPTOR AGONISTS; ANIMALS; BENZOXAZINES; CLONIDINE; GENE KNOCK-IN TECHNIQUES; MALE; MICE; MORPHOLINES; NAPHTHALENES; PREFRONTAL CORTEX; PYRAMIDAL CELLS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, CANNABINOID, CB1; RECEPTORS, ADRENERGIC, ALPHA-2;

EID: 84911448152     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.12690     Document Type: Article

References (75)

1. Alger, B.E., Dhanjal, S.S., Dingledine, R., Garthwaite, J., Henderson, G., King, G.L., Lipton, P., North, A., Schwartzkroin, P.A., Sears, T.A., Segal, M., Whittingham, T.S. & Williams, J. (1984) Appendix: Brain slice methods. In Dingledine, R. (Ed.), Brain Slices. Plenum Press, New York, NY, pp. 381-438.
2. Andrews, G.D. & Lavin, A. (2006) Methylphenidate increases cortical excitability via activation of alpha-2 noradrenergic receptors. Neuropsychopharmacology, 31, 594-601.
3. Aoki, C., Joh, T.H. & Pickel, V.M. (1987) Ultrastructural localization of beta-adrenergic receptor-like immunoreactivity in the cortex and neostriatum of rat brain. Brain Res., 437, 264-282.
4. Aoki, C., Go, C.G., Venkatesan, C. & Kurose, H. (1994) Perikaryal and synaptic localization of alpha 2A-adrenergic receptor-like immunoreactivity. Brain Res., 650, 181-204.
5. Arnsten, A.F. (2011) Catecholamine influences on dorsolateral prefrontal cortical networks. Biol. Psychiat., 69, e89-e99.
6. Arnsten, A.F. & Pliszka, S.R. (2011) Catecholamine influences on prefrontal cortical function: relevance to treatment of attention deficit/hyperactivity disorder and related disorders. Pharmacol. Biochem. Be., 99, 211-216.
7. Arnsten, A.F., Scahill, L. & Findling, R.L. (2007) alpha2-Adrenergic receptor agonists for the treatment of attention-deficit/hyperactivity disorder: emerging concepts from new data. J. Child Adol. Psychop., 17, 393-406.
8. Aston-Jones, G. (1985) Behavioral functions of locus-coeruleus derived from cellular attributes. Physiol. Psychol., 13, 118-126.
9. Berrendero, F., Garcia-Gil, L., Hernandez, M.L., Romero, J., Cebeira, M., de Miguel, R., Ramos, J.A. & Fernandez-Ruiz, J.J. (1998) Localization of mRNA expression and activation of signal transduction mechanisms for cannabinoid receptor in rat brain during fetal development. Development, 125, 3179-3188.
10. Bertler, A. (1961) Occurrence and localization of catechol amines in human brain. Acta Physiol. Scand., 51, 97-107.
11. Bylund, D.B., Blaxall, H.S., Iversen, L.J., Caron, M.G., Lefkowitz, R.J. & Lomasney, J.W. (1992) Pharmacological characteristics of alpha 2-adrenergic receptors: comparison of pharmacologically defined subtypes with subtypes identified by molecular cloning. Mol. Pharmacol., 42, 1-5.
12. Bymaster, F.P., Katner, J.S., Nelson, D.L., Hemrick-Luecke, S.K., Threlkeld, P.G., Heiligenstein, J.H., Morin, S.M., Gehlert, D.R. & Perry, K.W. (2002) Atomoxetine increases extracellular levels of norepinephrine and dopamine in prefrontal cortex of rat: a potential mechanism for efficacy in attention deficit/hyperactivity disorder. Neuropsychopharmacology, 27, 699-711.
13. Carr, D.B., Andrews, G.D., Glen, W.B. & Lavin, A. (2007) alpha2-Noradrenergic receptors activation enhances excitability and synaptic integration in rat prefrontal cortex pyramidal neurons via inhibition of HCN currents. J. Physiol., 584, 437-450.
14. Carvalho, A.F., Mackie, K. & Van Bockstaele, E.J. (2010) Cannabinoid modulation of limbic forebrain noradrenergic circuitry. Eur. J. Neurosci., 31, 286-301.
15. Cerrito, F. & Preziosi, P. (1985) Rat brain alpha 2-pre- and postsynaptic receptors are different or differently modulated? J. Neurosci. Res., 14, 423-431.
16. Chan, J., Aoki, C. & Pickel, V.M. (1990) Optimization of differential immunogold-silver and peroxidase labeling with maintenance of ultrastructure in brain sections before plastic embedding. J. Neurosci. Meth., 33, 113-127.
17. Crean, R.D., Crane, N.A. & Mason, B.J. (2011) An evidence based review of acute and long-term effects of cannabis use on executive cognitive functions. J. Addict. Med., 5, 1-8.
18. Dell'osso, B., Buoli, M., Baldwin, D.S. & Altamura, A.C. (2010) Serotonin norepinephrine reuptake inhibitors (SNRIs) in anxiety disorders: a comprehensive review of their clinical efficacy. Hum. Psychopharm. Clin., 25, 17-29.
19. Dennis, T., L'Heureux, R., Carter, C. & Scatton, B. (1987) Presynaptic alpha-2 adrenoceptors play a major role in the effects of idazoxan on cortical noradrenaline release (as measured by in vivo dialysis) in the rat. J. Pharmacol. Exp. Ther., 241, 642-649.
20. D'Souza, D.C., Ranganathan, M., Braley, G., Gueorguieva, R., Zimolo, Z., Cooper, T., Perry, E. & Krystal, J. (2008) Blunted psychotomimetic and amnestic effects of delta-9-tetrahydrocannabinol in frequent users of cannabis. Neuropsychopharmacology, 33, 2505-2516.
21. Egerton, A., Allison, C., Brett, R.R. & Pratt, J.A. (2006) Cannabinoids and prefrontal cortical function: insights from preclinical studies. Neurosci. Biobehav. R., 30, 680-695.
22. Fitzgerald, M.L., Shobin, E. & Pickel, V.M. (2012) Cannabinoid modulation of the dopaminergic circuitry: implications for limbic and striatal output. Prog. Neuro-psychoph., 38, 21-29.
23. Fitzgerald, M.L., Mackie, K. & Pickel, V.M. (2013) The impact of adolescent social isolation on dopamine D2 and cannabinoid CB1 receptors in the adult rat prefrontal cortex. Neuroscience, 235, 40-50.
24. Flugge, G., Van Kampen, M. & Mijnster, M.J. (2004) Perturbations in brain monoamine systems during stress. Cell Tissue Res., 315, 1-14.
25. Franklin, B.J.K. & Paxinos, G. (2008) The Mouse Brain in Stereotaxic Coordinates. Academic Press, San Diego, CA.
26. Gamo, N.J. & Arnsten, A.F. (2011) Molecular modulation of prefrontal cortex: rational development of treatments for psychiatric disorders. Behav. Neurosci., 125, 282-296.
27. Gibb, A.J. & Edwards, F.A. (1994) Patch clamp recording from cells in sliced tissues. In Standen, N.B. (Ed.), Microelectrode Techniques, the Plymouth Workshop Handbook. Company of Biologists, Cambridge, UK, pp. 255-274.
28. Gray, E.G. (1959) Axo-somatic and axo-dendritic synapses of the cerebral cortex: an electron microscopic study. J. Anat., 93, 420-433.
29. Hamdani, N. & van der Velden, J. (2009) Lack of specificity of antibodies directed against human beta-adrenergic receptors. N.-S. Arch. Pharmacol., 379, 403-407.
30. Hill, M.N. & Gorzalka, B.B. (2009) The endocannabinoid system and the treatment of mood and anxiety disorders. CNS Neurol. Disord.-Dr., 8, 451-458.
31. Hu, L.A., Tang, Y., Miller, W.E., Cong, M., Lau, A.G., Lefkowitz, R.J. & Hall, R.A. (2000) beta 1-adrenergic receptor association with PSD-95. Inhibition of receptor internalization and facilitation of beta 1-adrenergic receptor interaction with N-methyl-D-aspartate receptors. J. Biol. Chem., 275, 38659-38666.
32. Hudson, B.D., Hebert, T.E. & Kelly, M.E. (2010) Physical and functional interaction between CB1 cannabinoid receptors and beta2-adrenoceptors. Brit. J. Pharmacol., 160, 627-642.
33. Jensen, B.C., Swigart, P.M. & Simpson, P.C. (2009) Ten commercial antibodies for alpha-1-adrenergic receptor subtypes are nonspecific. N.-S. Arch. Pharmacol., 379, 409-412.
34. Jewell-Motz, E.A., Donnelly, E.T., Eason, M.G. & Liggett, S.B. (1998) Agonist-mediated downregulation of G alpha i via the alpha 2-adrenergic receptor is targeted by receptor-Gi interaction and is independent of receptor signaling and regulation. Biochemistry, 37, 15720-15725.
35. Jones, S.B., Leone, S.L. & Bylund, D.B. (1990) Desensitization of the alpha-2 adrenergic receptor in HT29 and opossum kidney cell lines. J. Pharmacol. Exp. Ther., 254, 294-300.
36. Katona, I., Urban, G.M., Wallace, M., Ledent, C., Jung, K.M., Piomelli, D., Mackie, K. & Freund, T.F. (2006) Molecular composition of the endocannabinoid system at glutamatergic synapses. J. Neurosci., 26, 5628-5637.
37. Kirby, L.G., Freeman-Daniels, E., Lemos, J.C., Nunan, J.D., Lamy, C., Akanwa, A. & Beck, S.G. (2008) Corticotropin-releasing factor increases GABA synaptic activity and induces inward current in 5-hydroxytryptamine dorsal raphe neurons. J. Neurosci., 28, 12927-12937.
38. Kuzmiski, J.B., Pittman, Q.J. & Bains, J.S. (2009) Metaplasticity of hypothalamic synapses following in vivo challenge. Neuron, 62, 839-849.
39. Lapiz, M.D. & Morilak, D.A. (2006) Noradrenergic modulation of cognitive function in rat medial prefrontal cortex as measured by attentional set shifting capability. Neuroscience, 137, 1039-1049.
40. Leranth, C. & Pickel, V.M. (1989) Electron microscopic preembedding double-labeling methods. In Heimer, L. & Zaborszky, L. (Eds), Neuroanatomical Tracing Methods 2. Plenum Press, New York, pp. 129-172.
41. Li, B.M., Mao, Z.M., Wang, M. & Mei, Z.T. (1999) Alpha-2 adrenergic modulation of prefrontal cortical neuronal activity related to spatial working memory in monkeys. Neuropsychopharmacology, 21, 601-610.
42. Liggett, S.B., Ostrowski, J., Chesnut, L.C., Kurose, H., Raymond, J.R., Caron, M.G. & Lefkowitz, R.J. (1992) Sites in the third intracellular loop of the alpha 2A-adrenergic receptor confer short term agonist-promoted desensitization. Evidence for a receptor kinase-mediated mechanism. J. Biol. Chem., 267, 4740-4746.
43. Lu, R., Li, Y., Zhang, Y., Chen, Y., Shields, A.D., Winder, D.G., Angelotti, T., Jiao, K., Limbird, L.E., Zhou, Y. & Wang, Q. (2009) Epitope-tagged receptor knock-in mice reveal that differential desensitization of alpha2-adrenergic responses is because of ligand-selective internalization. J. Biol. Chem., 284, 13233-13243.
44. Matthews, G.A., Patel, R., Walsh, A., Davies, O., Martinez-Ricos, J. & Brennan, P.A. (2013) Mating increases neuronal tyrosine hydroxylase expression and selectively gates transmission of male chemosensory information in female mice. PLoS One, 8, e69943.
45. McCune, S.K., Voigt, M.M. & Hill, J.M. (1993) Expression of multiple alpha adrenergic receptor subtype messenger RNAs in the adult rat brain. Neuroscience, 57, 143-151.
46. Meana, J.J., Barturen, F. & Garcia-Sevilla, J.A. (1992) Alpha 2-adrenoceptors in the brain of suicide victims: increased receptor density associated with major depression. Biol. Psychiat., 31, 471-490.
47. Miller, E.K. & Cohen, J.D. (2001) An integrative theory of prefrontal cortex function. Annu. Rev. Neurosci., 24, 167-202.
48. Milligan, G., Wise, A., MacEwan, D.J., Grassie, M.A., Kennedy, F.R., Lee, T.W., Adie, E.J., Kim, G.D., McCallum, J.F. & Burt, A. (1995) Mechanisms of agonist-induced G-protein elimination. Biochem. Soc. T., 23, 166-170.
49. Nicholas, A.P., Pieribone, V. & Hokfelt, T. (1993) Distributions of mRNAs for alpha-2 adrenergic receptor subtypes in rat brain: an in situ hybridization study. J. Comp Neurol., 328, 575-594.
50. Oropeza, V.C., Page, M.E. & Van Bockstaele, E.J. (2005) Systemic administration of WIN 55, 212-2 increases norepinephrine release in the rat frontal cortex. Brain Res., 1046, 45-54.
51. Oropeza, V.C., Mackie, K. & Van Bockstaele, E.J. (2007) Cannabinoid receptors are localized to noradrenergic axon terminals in the rat frontal cortex. Brain Res., 1127, 36-44.
52. Page, M.E., Oropeza, V.C., Sparks, S.E., Qian, Y., Menko, A.S. & Van Bockstaele, E.J. (2007) Repeated cannabinoid administration increases indices of noradrenergic activity in rats. Pharmacol. Biochem. Be., 86, 162-168.
53. Page, M.E., Oropeza, V.C. & Van Bockstaele, E.J. (2008) Local administration of a cannabinoid agonist alters norepinephrine efflux in the rat frontal cortex. Neurosci. Lett., 431, 1-5.
54. Pattij, T., Wiskerke, J. & Schoffelmeer, A.N. (2008) Cannabinoid modulation of executive functions. Eur. J. Pharmacol., 585, 458-463.
55. Peters, A. & Palay, S.L. (1996) The morphology of synapses. J. Neurocytol., 25, 687-700.
56. Peters, A., Palay, S.L. & Webster, H.D. (1991) The Fine Structure of the Nervous System. Oxford University Press, New York.
57. Polanski, W., Enzensperger, C., Reichmann, H. & Gille, G. (2010) The exceptional properties of 9-methyl-beta-carboline: stimulation, protection and regeneration of dopaminergic neurons coupled with anti-inflammatory effects. J. Neurochem., 113, 1659-1675.
58. Pradidarcheep, W., Stallen, J., Labruyere, W.T., Dabhoiwala, N.F., Michel, M.C. & Lamers, W.H. (2009) Lack of specificity of commercially available antisera against muscarinergic and adrenergic receptors. N.-S. Arch. Pharmacol., 379, 397-402.
59. Pudovkina, O.L., Kawahara, Y., de Vries, J. & Westerink, B.H. (2001) The release of noradrenaline in the locus coeruleus and prefrontal cortex studied with dual-probe microdialysis. Brain Res., 906, 38-45.
60. Ramos, B.P. & Arnsten, A.F. (2007) Adrenergic pharmacology and cognition: focus on the prefrontal cortex. Pharmacol. Therapeut., 113, 523-536.
61. Ranganathan, M. & D'Souza, D.C. (2006) The acute effects of cannabinoids on memory in humans: a review. Psychopharmacology (Berl.), 188, 425-444.
62. Reyes, B.A., Rosario, J.C., Piana, P.M. & Van Bockstaele, E.J. (2009) Cannabinoid modulation of cortical adrenergic receptors and transporters. J. Neurosci. Res., 87, 3671-3678.
63. Reyes, B.A., Szot, P., Sikkema, C., Cathel, A.M., Kirby, L.G. & Van Bockstaele, E.J. (2012) Stress-induced sensitization of cortical adrenergic receptors following a history of cannabinoid exposure. Exp. Neurol., 236, 327-335.
64. Richter, H., Teixeira, F.M., Ferreira, S.G., Kittel, A., Kofalvi, A. & Sperlagh, B. (2012) Presynaptic alpha(2)-adrenoceptors control the inhibitory action of presynaptic CB(1) cannabinoid receptors on prefrontocortical norepinephrine release in the rat. Neuropharmacology, 63, 784-797.
65. Robbins, T.W. (1984) Cortical noradrenaline, attention and arousal. Psychol. Med., 14, 13-21.
66. Scavone, J.L., Mackie, K. & Van Bockstaele, E.J. (2010) Characterization of cannabinoid-1 receptors in the locus coeruleus: relationship with mu-opioid receptors. Brain Res., 1312, 18-31.
67. Scheinin, M., Lomasney, J.W., Hayden-Hixson, D.M., Schambra, U.B., Caron, M.G., Lefkowitz, R.J. & Fremeau, R.T. Jr. (1994) Distribution of alpha 2-adrenergic receptor subtype gene expression in rat brain. Mol. Brain Res., 21, 133-149.
68. Strader, C.D., Pickel, V.M., Joh, T.H., Strohsacker, M.W., Shorr, R.G., Lefkowitz, R.J. & Caron, M.G. (1983) Antibodies to the beta-adrenergic receptor: attenuation of catecholamine-sensitive adenylate cyclase and demonstration of postsynaptic receptor localization in brain. Proc. Natl. Acad. Sci. USA, 80, 1840-1844.
69. Verrico, C.D., Jentsch, J.D. & Roth, R.H. (2003) Persistent and anatomically selective reduction in prefrontal cortical dopamine metabolism after repeated, intermittent cannabinoid administration to rats. Synapse, 49, 61-66.
70. Wang, R.X. & Limbird, L.E. (1997) Distribution of mRNA encoding three alpha 2-adrenergic receptor subtypes in the developing mouse embryo suggests a role for the alpha 2A subtype in apoptosis. Mol. Pharmacol., 52, 1071-1080.
71. Wang, M., Ramos, B.P., Paspalas, C.D., Shu, Y., Simen, A., Duque, A., Vijayraghavan, S., Brennan, A., Dudley, A., Nou, E., Mazer, J.A., McCormick, D.A. & Arnsten, A.F. (2007) Alpha2A-adrenoceptors strengthen working memory networks by inhibiting cAMP-HCN channel signaling in prefrontal cortex. Cell, 129, 397-410.
72. Westerink, B.H., Kawahara, Y., De Boer, P., Geels, C., De Vries, J.B., Wikstrom, H.V., Van Kalkeren, A., Van Vliet, B., Kruse, C.G. & Long, S.K. (2001) Antipsychotic drugs classified by their effects on the release of dopamine and noradrenaline in the prefrontal cortex and striatum. Eur. J. Pharmacol., 412, 127-138.
73. Winzer-Serhan, U.H. & Leslie, F.M. (1999) Expression of alpha2A adrenoceptors during rat neocortical development. J. Neurobiol., 38, 259-269.
74. Witkin, J.M., Tzavara, E.T. & Nomikos, G.G. (2005) A role for cannabinoid CB1 receptors in mood and anxiety disorders. Behav. Pharmacol., 16, 315-331.
75. Zhang, W., Perry, K.W., Wong, D.T., Potts, B.D., Bao, J., Tollefson, G.D. & Bymaster, F.P. (2000) Synergistic effects of olanzapine and other antipsychotic agents in combination with fluoxetine on norepinephrine and dopamine release in rat prefrontal cortex. Neuropsychopharmacology, 23, 250-262.