Abstract
In recent years, we demonstrated that prolonged (48-h) treatment of rats or mice with selective μ-opioid receptor (μOR) agonists induced a translocation of δ-opioid receptors (δORs) from intracellular compartments to neuronal plasma membranes in the dorsal horn of the spinal cord. It remained to be determined whether this phenomenon also occurred in the brain. To resolve this issue, we analyzed by immunogold histochemistry the subcellular distribution of δORs in the nucleus accumbens, dorsal neostriatum, and frontal cortex in mice treated or not with morphine (48 h). We observed that prolonged treatment with morphine induced a translocation of δORs from intracellular to subplasmalemmal and membrane compartments in dendrites from both the nucleus accumbens and the dorsal neostriatum but not from the frontal cortex. We propose that this μOR-δOR interaction might prolong and modulate the sensitivity of neurons to opiates in specific target regions.
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References
Bausch S. B., Patterson T. A., Appleyard S. M., and Chavkin C. (1995) Immunocytochemical localization of delta opioid receptors in mouse brain. J. Chem. Neuroanat. 8, 175–189.
Bowen W. D., Gentleman S., Herkenham M., and Pert C. B. (1981) Interconverting mu and delta forms of the opiate receptor in rat striatal patches. Proc. Natl. Acad. Sci. U. S. A. 78, 4818–4822.
Cahill C. M., McClellan K. A., Morinville A., Hoffert C., Hubatsch D., O’Donnell D., and Beaudet A. (2001a) Immunohistochemical distribution of delta opioid receptors in the rat central nervous system: evidence for somatodendritic labeling and antigen-specific cellular compartmentalization. J. Comp. Neurol. 440, 65–84.
Cahill C. M., Morinville A., Lee M. C., Vincent J. P., Collier B., and Beaudet A. (2001b) Prolonged morphine treatment targets delta opioid receptors to neuronal plasma membranes and enhances delta-mediated antinociception. J. Neurosci. 21, 7598–7607.
Chefer V. I., Kieffer B. L., and Shippenberg T. S. (2003) Basal and morphine-evoked dopaminergic neurotransmission in the nucleus accumbens of MOR- and DOR-knockout mice. Eur. J. Neurosci. 18, 1915–1922.
Christie M. J. and Hack S. P. (2003) Emergence of delta opioid receptor mediated presynaptic inhibition in periaqueductal grey neurons after chronic morphine. Annual Meeting for the Society for Neuroscience, New Orleans, LA, Poster 890.1.
Ferezou I. F., Hill E., Cauli B., Gibelin N., Rossier J., and Lambolez B. (2003) A cellular mechanism for the involvement of mu opioid receptors in nicotine addiction. Annual meeting for the Society for Neuroscience, New Orleans, LA, Poster 802.12.
Gainetdinov R. R., Premont R. T., Bohn L. M., Lefkowitz R. J., and Caron M. G. (2004) Desensitization of G protein-coupled receptors and neuronal functions. Annu. Rev. Neurosci. 27, 107–144.
George S. R., Fan T., Xie Z., Tse R., Tam V., Varghese G., and O’Dowd B. F. (2000) Oligomerization of mu- and delta-opioid receptors. Generation of novel functional properties. J. Biol. Chem. 275, 26128–26135.
Gomes I., Gupta A., Filipovska J., Szeto H. H., Pintar J. E., and Devi L. A. (2004) A role for heterodimerization of mu and delta opiate receptors in enhancing morphine analgesia. Proc. Natl. Acad. Sci. U. S. A. 101, 5135–5139.
Gomes I., Jordan B. A., Gupta A., Trapaidze N., Nagy V., and Devi L. A. (2000) Heterodimerization of mu and delta opioid receptors: a role in opiate synergy. J. Neurosci. 20, RC110.
Gouarderes C., Jhamandas K., Cridland R., Cros J., Quirion R., and Zajac J. M. (1993) Opioid and substance P receptor adaptations in the rat spinal cord following subchronic intrathecal treatment with morphine and naloxone. Neuroscience 54, 799–807.
Johnson P. I. and Stellar J. R. (1994) Comparison of delta opiate receptor agonist induced reward and motor effects between the ventral pallidum and dorsal striatum. Neuropharmacology 33, 1171–1182.
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.
Mansour A., Fox C. A., Thompson R. C., Akil H., and Watson S. J. (1994) mu-Opioid receptor mRNA expression in the rat CNS: comparison to mu-receptor binding. Brain Res. 643, 245–265.
Morinville A., Cahill C. M., Esdaile M. J., Aibak H., Collier B., Kieffer B. L., and Beaudet A. (2003) Regulation of delta-opioid receptor trafficking via mu-opioid receptor stimulation: evidence from mu-opioid receptor knock-out mice. J. Neurosci. 23, 4888–4898.
Peters A., Palay S. L., and Webster H. (1991) The Fine Structure of the Nervous System, 3rd Ed. Oxford University Press, New York.
Quirion R., Bowen W. D., and Pert C. B. (1981) Mu, delta, and kappa opiate receptors: interconvertible forms of the same receptor. Proceedings of the International Narcotics Research Conference, Kyoto, Japan, pp. 63–65.
Ragnauth A., Moroz M., and Bodnar R. J. (2000) Multiple opioid receptors mediate feeding elicited by mu and delta opioid receptor subtype agonists in the nucleus accumbens shell in rats. Brain Res. 876, 76–87.
Svingos A. L., Clarke C. L., and Pickel V. M. (1998) Cellular sites for activation of delta-opioid receptors in the rat nucleus accumbens shell: relationship with Met5-enkephalin. J. Neurosci. 18, 1923–1933.
Wang H. and Pickel V. M. (2001) Preferential cytoplasmic localization of delta-opioid receptors in rat striatal patches: comparison with plasmalemmal mu-opioid receptors. J. Neurosci. 21, 3242–3250.
Williams J. T., Christie M. J., and Manzoni O. (2001) Cellular and synaptic adaptations mediating opioid dependence. Physiol. Rev. 81, 299–343.
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Lucido, A.L., Morinville, A., Gendron, L. et al. Prolonged morphine treatment selectively increases membrane recruitment of δ-opioid receptors in mouse basal ganglia. J Mol Neurosci 25, 207–214 (2005). https://doi.org/10.1385/JMN:25:3:207
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DOI: https://doi.org/10.1385/JMN:25:3:207