Does PKC activation increase the homologous desensitization of μ opioid receptors?

British Journal of Pharmacology

Volumn 172, Issue 2, 2015, Pages 583-592

  Arttamangkul, Seksiri ^a   Birdsong, William ^a   Williams, John T ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

desensitization; fluorescent PKC sensor; hyperpolarization; internalization; muscarine; phorbol esters; PKC; staurosporine; opioid receptor

Indexed keywords

METENKEPHALIN; MORPHINE; MU OPIATE RECEPTOR; MUSCARINE; PHORBOL 13 ACETATE 12 MYRISTATE; PHORBOL DIBUTYRATE; PROTEIN KINASE C; STAUROSPORINE; NARCOTIC ANALGESIC AGENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EC50; ELECTROPHYSIOLOGICAL PROCEDURES; ENZYME ACTIVATION; HEK293 CELL LINE; HUMAN; HUMAN CELL; HYPERPOLARIZATION; INTERNALIZATION; LOCUS CERULEUS; MALE; NONHUMAN; RAT; RECEPTOR DOWN REGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; BRAIN; DRUG EFFECTS; GENETICS; METABOLISM; NERVE CELL; PHYSIOLOGY; PROTEIN TRANSPORT; SPRAGUE DAWLEY RAT; TRANSGENIC MOUSE;

ANALGESICS, OPIOID; ANIMALS; BRAIN; ENKEPHALIN, METHIONINE; HEK293 CELLS; HUMANS; MALE; MICE, TRANSGENIC; MORPHINE; MUSCARINE; NEURONS; PHORBOL 12,13-DIBUTYRATE; PROTEIN KINASE C; PROTEIN TRANSPORT; RATS, SPRAGUE-DAWLEY; RECEPTORS, OPIOID, MU; TETRADECANOYLPHORBOL ACETATE;

EID: 84920152919     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/bph.12712     Document Type: Article

References (47)

1. Alexander SPH, Benson HE, Faccenda E, Pawson AJ, Sharman JL, Spedding M, et al. and CGTP Collaborators (2013a). The Concise Guide to PHARMACOLOGY 2013/14: G protein-coupled receptors. Br J Pharmacol 170: 1459-1581.
2. Alexander SPH, Benson HE, Faccenda E, Pawson AJ, Sharman JL, Spedding M, et al. and CGTP Collaborators (2013b). The Concise Guide to PHARMACOLOGY 2013/14: Ion channels. Br J Pharmacol 170: 1607-1651.
3. Arttamangkul S, Quillinan N, Low MJ, von Zastrow M, Pintar J, Williams JT, (2008). Differential activation and trafficking of μ-opioid receptors in brain slices. Mol Pharmacol 74: 972-979.
4. Arttamangkul S, Lau EK, Lu HW, Williams JT, (2012). Desensitization and trafficking of μ-opioid receptor in locus coeruleus neurons: modulation by kinases. Mol Pharm 81: 348-355.
5. Bailey CP, Kelly E, Henderson G, (2004). Protein kinase C activation enhances morphine-induced rapid desensitization of mu-opioid receptors in mature rat locus coeruleus neurons. Mol Pharmacol 66: 1592-1598.
6. Bailey CP, Smith FL, Kelly E, Dewey WL, Henderson G, (2006). How important is protein kinase C in μ-opioid receptor desensitization and morphine tolerance? Trends Pharmacol Sci 27: 558-565.
7. Bailey CP, Oldfield S, Llorente J, Caunt CJ, Teschemacher AG, Roberts L, et al. (2009). Involvement of PLC alpha and G-protein-coupled receptor kinase 2 in agonist-selective desensitization of mu-opioid receptors in mature brain neurons. Br J Pharmacol 158: 157-164.
8. Birdsong WT, Arttamangkul S, Clark MJ, Cheng K, Rice KC, Traynor JR, et al. (2013). Increased agonist affinity at the μ-opioid receptor induced by prolonged agonist exposure. J Neurosci 33: 4118-4127.
9. Brose N, Rosenmund C, (2002). Move over protein kinase C, you've got company: alternative cellular effectors of diacylglycerol and phorbol esters. J Cell Sci 115: 4399-4411.
10. Castagna M, Takai Y, Kaibuchi K, Sano K, Kikkawa U, Nishizuka Y, (1982). Direct activation of calcium-activated, phospholipid-dependent protein kinase by tumor-promoting phorbol esters. J Biol Chem 257: 7847-7851.
11. Chen YJ, Oldfield S, Butcher AJ, Tobin AB, Saxena K, Gurevich VV, et al. (2012). Identification of phosphorylation sites in the COOH-terminal tail of the μ-opioid receptor. J Neurochem 124: 189-199.
12. Cho H, Kim YA, Yoon JY, Lee D, Kim JH, Lee SH, et al. (2005a). Low mobility of phosphatidylinositol 4,5-bisphosphate underlies receptor specificity of Gq-mediated ion channel regulation in atrial myocytes. Proc Natl Acad Sci USA 102: 15241-15246.
13. Cho H, Lee D, Lee SH, Ho WK, (2005b). Receptor-induced depletion of phosphatidylinositol 4,5-bisphosphate inhibits inwardly rectifying K + channels in a receptor-specific manner. Proc Natl Acad Sci USA 102: 4643-4648.
14. Christie MJ, Williams JT, North RA, (1987). Cellular mechanisms of opioid tolerance: studies in single brain neurons. Mol Pharmacol 32: 633-638.
15. Connor M, Osborne PB, Christie MJ, (2004). Mu-opioid receptor desensitization: is morphine different? Br J Pharmacol 143: 685-696.
16. Cui S, Ho WK, Kim ST, Cho H, (2010). Agonist-induced localization of Gq-coupled receptors and G protein-gated inwardly rectifying K + (GIRK) channels to caveolae determines receptor specificity of phosphatidylinositol 4,5-bisphosphate signaling. J Biol Chem 285: 41732-41739.
17. Doll C, Konietzko J, Poll F, Koch T, Hollt V, Schulz S, (2011). Agonist-selective patterns of μ-opioid receptor phosphorylation revealed by phosphosite-specific antibodies. Br J Pharmacol 164: 298-307.
18. Driedger PE, Blumberg PM, (1980). Specific binding of phorbol ester tumor promoters. Proc Natl Acad Sci USA 77: 567-571.
19. Feng B, Li Z, Wang JB, (2011). Protein kinase C-mediated phosphorylation of the μ-opioid receptor and its effects on receptor signaling. Mol Pharmacol 79: 768-775.
20. Fiorillo CD, Williams JT, (1996). Opioid desensitization: interactions with G-protein-coupled receptors in the locus coeruleus. J Neurosci 16: 1479-1485.
21. Harris GC, Williams JT, (1991). Transient homologous μ-opioid receptor desensitization rat locus coeruleus neurons. J Neurosci 11: 2574-2581.
22. Illing S, Mann A, Schulz S, (2013). Heterologous regulation of agonist-independent μ-opioid receptor phosphorylation by protein kinase C. Br J Pharmacol 171: 1330-1340.
23. Johnson EA, Oldfield S, Braksator E, Gonzalez-Cuello A, Couch D, Hall KJ, et al. (2006). Agonist-selective mechanisms of mu-opioid receptor desensitization in human embryonic kidney 293 cells. Mol Pharmacol 70: 676-685.
24. Kazanietz MG, (2002). Novel 'nonkinase' phorbol ester receptors: the C1 domain connection. Mol Pharmacol 61: 759-767.
25. Kelly E, Bailey CP, Henderson G, (2008). Agonist-selective mechanisms of GPCR desensitization. Br J Pharmacol 153: 5379-5388.
26. Lau EK, Trester-Zedlitz M, Trinidad JC, Kotowski SJ, Krutchinsky AN, Burlingame AL, et al. (2011). Quantitative encoding of the effect of a partial agonist on individual opioid receptors by multisite phosphorylation and threshold detection. Sci Signal 4: ra52.
27. Levitt ES, Williams JT, (2012). Morphine desensitization and cellular tolerance are distinguished in rat locus ceruleus neurons. Mol Pharmacol 82: 983-992.
28. Matsui A, Williams JT, (2010). Activation of μ-opioid receptors and block of Kir3 potassium channels and NMDA receptor conductance by L- and D-methadone in rat locus coeruleus. Br J Pharmacol 161: 1403-1413.
29. Mestek A, Hurley JH, Bye LS, Campbell AD, Chen Y, Tian M, et al. (1995). The human mu opioid receptor: modulation of functional desensitization by calcium/calmodulin-dependent protein kinase and protein kinase C. J Neurosci 15: 2396-2406.
30. Mosior M, Newton AC, (1995). Mechanism of interaction of protein kinase C with phorbol esters. J Biol Chem 270: 25526-25533.
31. Newton A, (2001). Protein kinase C: structure and spatial regulation by phosphorylation, cofactors and macromolecular interactions. Chem Dev 101: 2353-2364.
32. Osborne PB, Williams JT, (1995). Characterization of acute homologous desensitization of μ-opioid receptor-induced currents in locus coeruleus neurons. Br J Pharmacol 115: 925-932.
33. Pologruto TA, Sabatini BL, Svoboda K, (2003). ScanImage: flexible software for operating laser scanning microscopes. Biomed Eng Online 2: 13.
34. Rodriguez-Martin I, Braksator E, Bailey CP, Goodchild S, Marrion NV, Kelly E, et al. (2008). Methadone: does it really have low efficacy at μ-opioid receptors? Neuroreport 19: 589-593.
35. Rüegg UT, Burgess GM, (1989). Staurosporine, K-252 and UCN-01: potent but nonspecific inhibitors or protein kinases. Trends Pharmacol Sci 10: 218-220.
36. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, et al. (2012). Fiji: and open-source platform for biological-image analysis. Nat Methods 9: 676-682.
37. Shirai Y, Kashiwagi K, Yagi K, Sakai N, Saito N, (1998). Distinct effects of fatty acids on translocation of γ- and ε-subspecies of protein kinase C. J Cell Biol 143: 511-521.
38. Tewson P, Westenberg M, Zhao Y, Campbell RE, Quinn AM, Hughes TE, (2012). Simultaneous detection of Ca2+ and diacylglycerol signaling in living cells. PLoS ONE 7: e42791.
39. Tewson PH, Quinn AM, Hughes TE, (2013). A multiplexed fluorescent assay for independent second-messenger systems: decoding GPCR activation in living cells. J Biomol Screen 18: 797-806.
40. Virk MS, Arttamangkul S, Birdsong WT, Williams JT, (2009). Buprenorphine is a weak partial agonist that inhibits opioid receptor desensitization. J Neurosci 29: 7341-7348.
41. Wang Q, Bhattacharyya D, Garfield S, Nacro K, Marquez VE, Blumberg PM, (1999). Differential localization of protein kinase C δ by phorbol esters and related compounds using a fusion protein with green fluorescent protein. J Bio Chem 274: 37233-37239.
42. Wang QJ, Fang TW, Fenick D, Garfield S, Bienfait B, Marquez VE, et al. (2000). The lipophilicity of phorbol esters as a critical factor in determining the pattern of translocation of protein kinase C δ fused to green fluorescent protein. J Biol Chem 275: 12136-12146.
43. Whorton MR, MacKinnon R, (2011). Crystal structure of the mammalian GIRK2K+ channel and gating regulation by G proteins, PIP2, and sodium. Cell 147: 199-208.
44. Whorton MR, MacKinnon R, (2013). X-ray structure of the mammalian GIRK2-βγ G-protein complex. Nature 498: 190-197.
45. Williams JT, North RA, Shefner SA, Nishi S, Egan TM, (1984). Membrane properties of rat locus coeruleus neurons. Neuroscience 13: 137-156.
46. Williams JT, Ingram SL, Henderson G, Chavkin C, von Zastrow M, Schulz S, et al. (2013). Regulation of μ-opioid receptors: desensitization, phosphorylation, internalization, and tolerance. Pharmacol Rev 65: 223-254.
47. Zhang L, Yu Y, Mackin S, Weight FF, Uhl GR, Wang JB, (1996). Differential mu opioid receptor phosphorylation and desensitization induced by agonists and phorbol esters. J Biol Chem 271: 11449-11454.