- About this Journal
- Abstracting and Indexing
- Aims and Scope
- Annual Issues
- Article Processing Charges
- Articles in Press
- Author Guidelines
- Bibliographic Information
- Citations to this Journal
- Contact Information
- Editorial Board
- Editorial Workflow
- Free eTOC Alerts
- Publication Ethics
- Reviewers Acknowledgment
- Submit a Manuscript
- Subscription Information
- Table of Contents
BioMed Research International
Volume 2013 (2013), Article ID 501086, 9 pages
Ligand-Specific Regulation of the Endogenous Mu-Opioid Receptor by Chronic Treatment with Mu-Opioid Peptide Agonists
1Institute of Biochemistry, Biological Research Center, Hungarian Academy of Sciences, P.O. Box 521, Szeged 6701, Hungary
2Department of Pathophysiology, Faculty of Medicine, University of Szeged, Szeged, Hungary
Received 30 April 2013; Revised 22 August 2013; Accepted 6 September 2013
Academic Editor: Eiichi Kumamoto
Copyright © 2013 Marianna Murányi et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
- J. E. Zadina, L. Hackler, L. J. Ge, and A. J. Kastin, “A potent and selective endogenous agonist for the μ-opiate receptor,” Nature, vol. 386, no. 6624, pp. 499–502, 1997.
- G. Horvath, M. Szikszay, C. Tömböly, and G. Benedek, “Antinociceptive effects of intrathecal endomorphin-1 and -2 in rats,” Life Sciences, vol. 65, no. 24, pp. 2635–2641, 1999.
- A. Keresztes, M. Szűcs, A. Borics et al., “New endomorphin analogues containing alicyclic beta-amino acids: influence on bioactive conformation and pharmacological profile,” Journal of Medicinal Chemistry, vol. 51, pp. 4270–4279, 2008.
- C. Tömböly, A. Péter, and G. Tóth, “In vitro quantitative study of the degradation of endomorphins,” Peptides, vol. 23, pp. 1573–1580, 2002.
- E. J. Nestler, B. T. Hope, and K. L. Widnell, “Drug addiction: a model for the molecular basis of neural plasticity,” Neuron, vol. 11, no. 6, pp. 995–1006, 1993.
- T. Koch and V. Höllt, “Role of receptor internalization in opioid tolerance and dependence,” Pharmacology and Therapeutics, vol. 117, no. 2, pp. 199–206, 2008.
- J. T. Williams, S. L. Ingram, G. Henderson et al., “Regulation of μ-opioid receptors: desensitization, phosphorylation, internalization, and tolerance,” Pharmacological Reviews, vol. 65, no. 1, pp. 223–254, 2013.
- J. L. Whistler, “Examining the role of mu opioid receptor endocytosis in the beneficial and side-effects of prolonged opioid use: from a symposium on new concepts in mu-opioid pharmacology,” Drug and Alcohol Dependence, vol. 121, no. 3, pp. 189–204, 2012.
- K. Nagi and G. Piñeyro, “Regulation of opioid receptor signalling: implications for the development of analgesic tolerance,” Molecular Brain, vol. 4, article 25, 2011.
- J. R. Arden, V. Segredo, Z. Wang, J. Lameh, and W. Sadee, “Phosphorylation and agonist-specific intracellular trafficking of an epitope-tagged μ-opioid receptor expressed in HEK 293 cells,” Journal of Neurochemistry, vol. 65, no. 4, pp. 1636–1645, 1995.
- N. T. Burford, L. M. Tolbert, and W. Sadee, “Specific G protein activation and μ-opioid receptor internalization caused by morphine, DAMGO and endomorphin I,” European Journal of Pharmacology, vol. 342, no. 1, pp. 123–126, 1998.
- K. Stafford, A. B. Gomes, J. Shen, and B. C. Yoburn, “μ-opioid receptor downregulation contributes to opioid tolerance in vivo,” Pharmacology Biochemistry and Behavior, vol. 69, no. 1-2, pp. 233–237, 2001.
- Y. Qiu, P. Y. Law, and H. H. Loh, “μ-opioid receptor desensitization: role of receptor phosphorylation, internalization, and resensitization,” Journal of Biological Chemistry, vol. 278, no. 38, pp. 36733–36739, 2003.
- C. Sternini, M. Spann, B. Anton et al., “Agonist-selective endocytosis of μ opioid receptor by neurons in vivo,” Proceedings of the National Academy of Sciences of the United States of America, vol. 93, no. 17, pp. 9241–9246, 1996.
- L. Martini and J. L. Whistler, “The role of mu opioid receptor desensitization and endocytosis in morphine tolerance and dependence,” Current Opinion in Neurobiology, vol. 17, no. 5, pp. 556–564, 2007.
- A. Alt, A. Mansour, H. Akil, F. Medzihradsky, J. R. Traynor, and J. H. Woods, “Stimulation of guanosine-5′-O-(3-[35s]thio)triphosphate binding by endogenous opioids acting at a cloned mu receptor,” Journal of Pharmacology and Experimental Therapeutics, vol. 286, no. 1, pp. 282–288, 1998.
- J. L. Whistler and M. von Zastrow, “Morphine-activated opioid receptors elude desensitization by β-arrestin,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 17, pp. 9914–9919, 1998.
- K. McConalogue, E. F. Grady, J. Minnis et al., “Activation and internalization of the μ-opioid receptor by the newly discovered endogenous agonists, endomorphin-1 and endomorphin-2,” Neuroscience, vol. 90, no. 3, pp. 1051–1059, 1999.
- A. Duttaroy and B. C. Yoburn, “The effect of intrinsic efficacy on opioid tolerance,” Anesthesiology, vol. 82, no. 5, pp. 1226–1236, 1995.
- J. McPherson, G. Rivero, M. Baptist et al., “μ-opioid receptors: correlation of agonist efficacy for signalling with ability to activate internalization,” Molecular Pharmacology, vol. 78, no. 4, pp. 756–766, 2010.
- M. Pawar, P. Kumar, S. Sunkaraneni, S. Sirohi, E. A. Walker, and B. C. Yoburn, “Opioid agonist efficacy predicts the magnitude of tolerance and the regulation of μ-opioid receptors and dynamin-2,” European Journal of Pharmacology, vol. 563, no. 1–3, pp. 92–101, 2007.
- H. Xu, J. S. Partilla, X. Wang et al., “A comparison of noninternalizing (Herkinorin) and internalizing (DAMGO) μ-opioid agonists on cellular markers related to opioid tolerance and dependence,” Synapse, vol. 61, no. 3, pp. 166–175, 2007.
- A. K. Finn and J. L. Whistler, “Endocytosis of the mu opioid receptor reduces tolerance and a cellular hallmark of opiate withdrawal,” Neuron, vol. 32, no. 5, pp. 829–839, 2001.
- A. R. Gintzler and S. Chakrabarti, “Opioid tolerance and the emergence of new opioid receptor-coupled signaling,” Molecular Neurobiology, vol. 21, no. 1-2, pp. 21–33, 2000.
- T. Kenakin, “Functional selectivity through protean and biased agonism: who steers the ship?” Molecular Pharmacology, vol. 72, no. 6, pp. 1393–1401, 2007.
- J. D. Urban, W. P. Clarke, M. von Zastrow et al., “Functional selectivity and classical concepts of quantitative pharmacology,” Journal of Pharmacology and Experimental Therapeutics, vol. 320, no. 1, pp. 1–13, 2007.
- Y. Wang, E. J. van Bockstaele, and L. Y. Liu-Chen, “In vivo trafficking of endogenous opioid receptors,” Life Sciences, vol. 83, no. 21-22, pp. 693–699, 2008.
- G. Fábián, B. Bozó, M. Szikszay, G. Horváth, C. J. Coscia, and M. Szücs, “Chronic morphine-induced changes in mu-opioid receptors and G proteins of different subcellular loci in rat brain,” Journal of Pharmacology and Experimental Therapeutics, vol. 302, pp. 774–780, 2002.
- R. Cinar, O. Kékesi, E. Birkás, G. Fábián, H. Schmidhammer, and M. Szücs, “Lack of regulatory changes of mu-opioid receptors by 14-methoxymetopon treatment in rat brain. Further evidence for functional selectivity,” Current Pharmaceutical Design. In press.
- B. L. Roth, M. B. Laskowski, and C. J. Coscia, “Evidence for distinct subcellular sites of opiate receptors: demonstration of opiate receptors in smooth microsomal fractions isolated from rat brain,” Journal of Biological Chemistry, vol. 256, no. 19, pp. 10117–10123, 1981.
- M. Szűcs and C. J. Coscia, “Differential coupling of opioid binding sites to guanosine triphosphate binding regulatory proteins in subcellular fractions of rat brain,” Journal of Neuroscience Research, vol. 31, no. 3, pp. 565–572, 1992.
- G. Szabó, M. Mácsai, E. G. Kicsi et al., “Long-lasting antinociceptive effect of DAMGO chloromethyl ketone in rats,” Peptides, vol. 20, no. 11, pp. 1321–1326, 1999.
- L. J. Pellegrino, A. S. Pellegrino, and A. J. Cushman, Stereotactic Atlas of the Rat Brain, vol. 8, Plenum, New York, NY, USA, 2nd edition, 1979.
- R. Cinar, T. F. Freund, I. Katona, K. Mackie, and M. Szűcs, “Reciprocal inhibition of G-protein signaling is induced by CB1 cannabinoid and GABAB receptor interactions in rat hippocampal membranes,” Neurochemistry International, vol. 52, no. 8, pp. 1402–1409, 2008.
- M. M. Bradford, “A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding,” Analytical Biochemistry, vol. 72, no. 1-2, pp. 248–254, 1976.
- B. Przewłocka, J. Mika, D. Łabuz, G. Toth, and R. Przewłocki, “Spinal analgesic action of endomorphins in acute, inflammatory and neuropathic pain in rats,” European Journal of Pharmacology, vol. 367, no. 2-3, pp. 189–196, 1999.
- P. Sánchez-Blázquez, M. Rodríguez-Díaz, I. DeAntonio, and J. Garzón, “Endomorphin-1 and endomorphin-2 show differences in their activation of mu opioid receptor-regulated G proteins in supraspinal antinociception in mice,” Journal of Pharmacology and Experimental Therapeutics, vol. 291, pp. 12–18, 1999.
- H. Xie, J. H. Woods, J. R. Traynor, and M. C. Ko, “The spinal antinociceptive effects of endomorphins in rats: behavioral and G protein functional studies,” Anesthesia and Analgesia, vol. 106, no. 6, pp. 1873–1881, 2008.
- M. Ohsawa, H. Mizoguchi, M. Narita, M. Chu, H. Nagase, and L. F. Tseng, “Differential mechanisms mediating descending pain controls for antinociception induced by supraspinally administered endomorphin-1 and endomorphin-2 in the mouse,” Journal of Pharmacology and Experimental Therapeutics, vol. 294, no. 3, pp. 1106–1111, 2000.
- G. Rivero, J. Llorente, J. McPherson et al., “Endomorphin-2: a biased agonist at the μ-opioid receptor,” Molecular Pharmacology, vol. 82, no. 2, pp. 178–188, 2012.
- C. S. Breivogel, D. E. Selley, and S. R. Childers, “Acute and chronic effects of opioids on δ and μ receptor activation of G proteins in NG108-15 and SK-N-SH cell membranes,” Journal of Neurochemistry, vol. 68, no. 4, pp. 1462–1472, 1997.
- P. Sánchez-Blázquez, P. Gómez-Serranillos, and J. Garzón, “Agonists determine the pattern of G-protein activation in mu-opioid receptor-mediated supraspinal analgesia,” Brain Research Bulletin, vol. 54, no. 2, pp. 229–235, 2001.
- J. Garzón, M. Castro, and P. Sánchez-Blázquez, “Influence of Gz and Gi2 transducer proteins in the affinity of opioid agonists to mu receptors,” European Journal of Neuroscience, vol. 10, no. 8, pp. 2557–2564, 1998.
- T. J. Martin, S. I. Dworkin, and J. E. Smith, “Effects of intracerebroventricular administration of β-funaltrexamine on [3H]DAMGO binding to rat brain sections,” Journal of Pharmacology and Experimental Therapeutics, vol. 267, no. 1, pp. 506–514, 1993.
- E. Reiter, S. Ahn, A. K. Shukla, and R. J. Lefkowitz, “Molecular mechanism of β-arrestin-biased agonism at seven-transmembrane receptors,” Annual Review of Pharmacology and Toxicology, vol. 52, pp. 179–197, 2012.
- L. M. Bohn, R. J. Lefkowitz, R. R. Gainetdinov, K. Peppel, M. G. Caron, and F. T. Lin, “Enhanced morphine analgesia in mice lacking β-arrestin 2,” Science, vol. 286, no. 5449, pp. 2495–2498, 1999.