Morphine induces μ opioid receptor endocytosis in guinea pig enteric neurons following prolonged receptor activation

Gastroenterology

Volumn 140, Issue 2, 2011, Pages 618-626

  Patierno, Simona ^a,b   Anselmi, Laura ^a,b   Jaramillo, Ingrid ^b   Scott, David ^a,b   Garcia, Rachel ^a   Sternini, Catia ^a,b  

^a VA GREATER LOS ANGELES HEALTHCARE SYSTEM   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

G ProteinCoupled Receptors; Opiate Drugs; Opioid Peptides; Tolerant and Na ve Animals

Indexed keywords

BETA ARRESTIN; DYNAMIN; ENKEPHALIN[2 DEXTRO ALANINE 4 METHYLPHENYLALANINE 5 GLYCINE]; MORPHINE; MU OPIATE RECEPTOR; NEUROTRANSMITTER;

ANIMAL EXPERIMENT; ARTICLE; CELL MEMBRANE; CELLULAR DISTRIBUTION; CONTINUOUS INFUSION; CONTROLLED STUDY; ENDOCYTOSIS; GUINEA PIG; ILEUM; IMMUNOREACTIVITY; INTERNALIZATION; INTESTINE; MALE; MOLECULAR INTERACTION; NERVE CELL; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

EID: 79251565243     PISSN: 00165085     EISSN: None     Source Type: Journal    
DOI: 10.1053/j.gastro.2010.11.005     Document Type: Article

References (54)

1. G.W. Pasternak Pharmacological mechanisms of opioid analgesics Clin Neuropharmacol 16 1993 1 18
2. M. Minami, and M. Satoh Molecular biology of the opioid receptors: structures, functions and distributions Neurosci Res 23 1995 121 145
3. C.J. Nelson, G.M. Schneider, and D.T. Lysle Involvement of central mu- but not delta- or kappa-opioid receptors in immunomodulation Brain Behav Immun 14 2000 170 184
4. G.B. Stefano, B. Scharrer, and E.M. Smith Opioid and opiate immunoregulatory processes Crit Rev Immunol 16 1996 109 144
5. C. Sternini Receptors and transmission in the brain-gut axis: potential for novel therapies. III. μ opioid receptors in the enteric nervous system Am J Physiol 281 2001 G8 G15
6. C.J. Evans Agonist selective mu-opioid receptor trafficking in rat central nervous system Mol Psychiatry 5 2000 121
7. B.L. Kieffer Opioids: first lessons from knockout mice Trends Pharmacol Sci 20 1999 19 26
8. D. Bagnol, A. Mansour, and H. Akil Cellular localization and distribution of the cloned mu and kappa opioid receptors in rat gastrointestinal tract Neuroscience 81 1997 579 591
9. T.F. Burks Opioid peptides in gastrointestinal functions L.F. Tseng, The pharmacology of opioid peptides 1995 Harwood Academic Publishers Amsterdam, The Netherlands 397 409
10. A. Ho, A. Lievore, and S. Patierno Neurochemically distinct classes of myenteric neurons express the μ-opioid receptor in the guinea pig ileum J Comp Neurol 458 2003 404 411
11. C. Sternini, S. Patierno, and I.S. Selmer The opioid system in the gastrointestinal tract Neurogastroenterol Motil 16 Suppl 2 2004 3 16
12. S.J. Panchal, P. Muller-Schwefe, and J.I. Wurzelmann Opioid-induced bowel dysfunction: prevalence, pathophysiology and burden Int J Clin Pract 61 2007 1181 1187
13. M. Pappagallo Incidence, prevalence, and management of opioid bowel dysfunction Am J Surg 182 2001 11S 18S
14. S.A. Schug, D. Zech, and S. Grond Adverse effects of systemic opioid analgesics Drug Saf 7 1992 200 213
15. D. Philippe, L. Dubuquoy, and H. Groux Anti-inflammatory properties of the mu opioid receptor support its use in the treatment of colon inflammation J Clin Invest 111 2003 1329 1338
16. S. Bohm, E.F. Grady, and N.W. Bunnett Mechanisms attenuating signaling by G protein-coupled receptors Biochem J 322 1997 1 18
17. M. von Zastrow Mechanisms regulating membrane trafficking of G protein-coupled receptors in the endocytic pathway Life Sci 74 2003 217 224
18. M. von Zastrow, A. Svingos, and H. Haberstock-Debic Regulated endocytosis of opioid receptors: cellular mechanisms and proposed roles in physiological adaptation to opiate drugs Curr Opin Neurobiol 13 2003 348 353
19. Y. Qiu, P.Y. Law, and H.H. Loh Mu-opioid receptor desensitization: role of receptor phosphorylation, internalization, and representation J Biol Chem 278 2003 36733 36739
20. M. von Zastrow Role of endocytosis in signalling and regulation of G-protein-coupled receptors Biochem Soc Trans 29 2001 500 504
21. D.E. Keith, B. Anton, and S.R. Murray μ-opioid receptor internalization: opiate drugs have differential effects on a conserved endocytic mechanism in vitro and in mammalian brain Mol Pharmacol 53 1998 377 384
22. D.E. Keith, S.R. Murray, and P.A. Zaki Morphine activates opioid receptors without causing their rapid internalization J Biol Chem 271 1996 19021 19024
23. K. McConalogue, E.F. Grady, and J. Minnis Activation and internalization of the μ opioid receptor by the newly described endogenous agonists, endomorphin-1 and endomorphin-2 Neuroscience 90 1999 1051 1059
24. J. Minnis, S. Patierno, and S.E. Kohlmeier Ligand-induced μ opioid receptor endocytosis and recycling in enteric neurons Neuroscience 119 2003 33 42
25. C. Sternini, M. Spann, and B. Anton Agonist-selective endocytosis of μ opioid receptor by neurons in vivo Proc Natl Acad Sci U S A 93 1996 9241 9246
26. J.L. Whistler, H.-H. Chuang, and P. Chu Functional dissociation of μ opioid receptor signaling and endocytosis: implications for the biology of opiate tolerance and addiction Neuron 23 1999 737 746
27. J. Zhang, S.S.G. Ferguson, and L.S. Barak Role of G protein-coupled receptor kinase in agonist-specific regulation of μ-opioid receptor responsiveness Proc Natl Acad Sci U S A 95 1998 7157 7162
28. A. Duttaroy, and B.C. Yoburn The effect of intrinsic efficacy on opioid tolerance Anesthesiology 82 1995 1226 1236
29. F. Noble, M. Szuc, and B. Kieffer Overexpression of dynamin is induced by chronic stimulation of μ- but not d-opioid receptors: relationships with μ-related morphine dependence Mol Pharmacol 58 2000 159 166
30. B.C. Yoburn, V. Purohit, and K. Patel Opioid agonist and antagonist treatment differentially regulates immunoreactive mu-opioid receptors and dynamin-2 in vivo Eur J Pharmacol 498 2004 87 96
31. Q. Zhang, V. Purohit, and B.C. Yoburn Continuous opioid agonist treatment dose-dependently regulates mu-opioid receptors and dynamin-2 in mouse spinal cord Synapse 56 2005 123 128
32. S. Patierno, H.E. Raybould, and C. Sternini Abdominal surgery induces μ opioid receptor endocytosis in enteric neurons of the guinea pig ileum Neuroscience 123 2004 101 109
33. C. Sternini, N.C. Brecha, and J. Minnis Role of agonist-dependent receptor internalization in the regulation of μ opioid receptors Neuroscience 98 2000 233 241
34. W. Kromer Endogenous and exogenous opioids in the control of gastrointestinal motility and secretion Pharmacol Rev 40 1988 121 162
35. E. Macia, M. Ehrlich, and R. Massol Dynasore, a cell-permeable inhibitor of dynamin Dev Cell 10 2006 839 850
36. S. Patierno, W. Zellalem, and A. Ho N-Methyl-d-aspartate receptors mediate endogenous opioid release in enteric neurons after abdominal surgery Gastroenterology 128 2005 2009 2019
37. T. Harada, B.A. Moore, and R. Yang Ethyl pyruvate ameliorates ileus induced by bowel manipulation in mice Surgery 138 2005 530 537
38. M.S. Miller, J.J. Galligan, and T.F. Burks Accurate measurement of intestinal transit in the rat J Pharmacol Methods 6 1981 211 217
39. C. Chavkin, and A. Goldstein Opioid receptor reserve in normal and morphine-tolerant guinea pig ileum myenteric plexus Proc Natl Acad Sci U S A 81 1984 7253 7257
40. V.A. Alvarez, S. Arttamangkul, and V. Dang mu-Opioid receptors: ligand-dependent activation of potassium conductance, desensitization, and internalization J Neurosci 22 2002 5769 5776
41. A. Kovoor, J.P. Celver, and A. Wu Agonist induced homologous desensitization of mu-opioid receptors mediated by G protein-coupled receptor kinases is dependent on agonist efficacy Mol Pharmacol 54 1998 704 711
42. S. Schulz, D. Mayer, and M. Pfeiffer Morphine induces terminal micro-opioid receptor desensitization by sustained phosphorylation of serine-375 EMBO J 23 2004 3282 3289
43. Y. Yu, L. Zhang, and X. Yin Mu opioid receptor phosphorylation, desensitization, and ligand efficacy J Biol Chem 272 1997 28869 28874
44. S.L. Borgland, M. Connor, and P.B. Osborne Opioid agonists have different efficacy profiles for G protein activation, rapid desensitization, and endocytosis of mu-opioid receptors J Biol Chem 278 2003 18776 18784
45. N.T. Burford, L.M. Tolbert, and W. Sadee Specific G protein activation and mu-opioid receptor internalization caused by morphine, DAMGO and endomorphin I Eur J Pharmacol 342 1998 123 126
46. S. Arttamangkul, N. Quillinan, and M.J. Low Differential activation and trafficking of micro-opioid receptors in brain slices Mol Pharmacol 74 2008 972 979
47. J. Zhang, S.S.G. Ferguson, and L.S. Barak Dynamin and beta-arrestin reveal distinct mechanisms for G protein-coupled receptor internalization J Biol Chem 271 1996 18302 18305
48. J.L. Whistler, and M. von Zastrow Morphine-activated opioid receptors elude desensitization by β-arrestin Proc Natl Acad Sci U S A 95 1998 9914 9919
49. J.A. Trafton, and A.I. Basbaum [d-Ala2,N-MePhe4,Gly-ol5]enkephalin- induced internalization of the micro opioid receptor in the spinal cord of morphine tolerant rats Neuroscience 125 2004 541 543
50. A.C. Hanyaloglu, and M. von Zastrow Regulation of GPCRs by membrane trafficking and its potential implications Annu Rev Pharmacol Toxicol 48 2008 537 568
51. H. Haberstock-Debic, K.A. Kim, and Y.J. Yu Morphine promotes rapid, arrestin-dependent endocytosis of mu-opioid receptors in striatal neurons J Neurosci 25 2005 7847 7857
52. H. Haberstock-Debic, M. Wein, and M. Barrot Morphine acutely regulates opioid receptor trafficking selectively in dendrites of nucleus accumbens neurons J Neurosci 23 2003 4324 4332
53. J.L. Scavone, and E.J. Van Bockstaele Mu-opioid receptor redistribution in the locus coeruleus upon precipitation of withdrawal in opiate-dependent rats Anat Rec (Hoboken) 292 2009 401 411
54. M.F. Olive, M. Bertolucci, and C.J. Evans Microdialysis reveals a morphine-induced increase in pallidal opioid peptide release Neuroreport 6 1995 1093 1096