The absence of endogenous β-endorphin selectively blocks phosphorylation and desensitization of mu opioid receptors following partial sciatic nerve ligation

Neuroscience

Volumn 146, Issue 4, 2007, Pages 1795-1807

  Petraschka, M ^a   Li, S ^a   Gilbert, T L ^a   Westenbroek, R E ^a   Bruchas, M R ^a   Schreiber, S ^a   Lowe, J ^a   Low, M J ^b   Pintar, J E ^c   Chavkin, C ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^c RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

Author keywords

antinociception; dynorphins; enkephalins; neuropathic pain; opiate tolerance; opioid peptides

Indexed keywords

BETA ENDORPHIN; ENKEPHALIN[2 DEXTRO ALANINE 4 METHYLPHENYLALANINE 5 GLYCINE]; FENTANYL; MORPHINE; MU OPIATE RECEPTOR; NALOXONE; PROOPIOMELANOCORTIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY SPECIFICITY; ANTINOCICEPTION; ARTICLE; CONTROLLED STUDY; CORPUS STRIATUM; DESENSITIZATION; DOSE RESPONSE; DRUG TOLERANCE; GENE; GENE DELETION; IMMUNOREACTIVITY; MALE; MOUSE; NERVE LIGATION; NEUROPATHIC PAIN; NONHUMAN; PHOSPHORYLATION; PLACE PREFERENCE; PRIORITY JOURNAL; RECEPTOR BLOCKING; SCIATIC NERVE; TAIL FLICK TEST; WITHDRAWAL REFLEX;

ANALGESICS, OPIOID; ANALYSIS OF VARIANCE; ANIMALS; BEHAVIOR, ANIMAL; BETA-ENDORPHIN; CELL LINE, TRANSFORMED; CONDITIONING, OPERANT; CORPUS STRIATUM; DRUG INTERACTIONS; ENKEPHALIN, ALA(2)-MEPHE(4)-GLY(5)-; GREEN FLUORESCENT PROTEINS; HUMANS; HYPERALGESIA; MICE; MICE, KNOCKOUT; MUTAGENESIS; NALOXONE; NARCOTIC ANTAGONISTS; PHOSPHORYLATION; PHOSPHOTHREONINE; RECEPTORS, OPIOID, MU; SCIATICA; TRANSFECTION;

EID: 34249053249     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2007.03.029     Document Type: Article

References (48)

1. Akil H., Mayer D.J., and Liebeskind J.C. Antagonism of stimulation-produced analgesia by naloxone, a narcotic antagonist. Science 191 (1976) 961-962
2. Arden J.R., Segredo V., Wang Z., Lameh J., and Sadee W. Phosphorylation and agonist-specific intracellular trafficking of an epitope-tagged mu-opioid receptor expressed in HEK 293 cells. J Neurochem 65 (1995) 1636-1645
3. Arnér S., and Meyerson B.A. Lack of analgesic effect of opioids on neuropathic and idiopathic forms of pain. Pain 33 (1988) 11-23
4. Bach F.W., Chaplan S.R., Jang J., and Yaksh T.L. Cerebrospinal fluid beta-endorphin in models of hyperalgesia in the rat. Regul Pept 59 (1995) 79-86
5. Bhargava H.N., Matwyshyn G.A., Rattan A.K., Koo K.L., and Tejwani G.A. beta-Endorphin-like immunoreactivity in discrete brain regions, spinal cord, pituitary gland and peripheral tissues of U-50,488H-tolerant and -abstinent rats. J Pharmacol Exp Ther 268 (1994) 856-861
6. Bleeker C.P., Bremer R.C., Dongelmans D.A., van Dongen R.T., and Crul B.J. Inefficacy of high-dose transdermal fentanyl in a patient with neuropathic pain, a case report. Eur J Pain 5 (2001) 325-329
7. Bodnar R.J. Endogenous opioids and feeding behavior: a 30-year historical perspective. Peptides 25 (2004) 697-725
8. Bohn L.M., Gainetdinov R.R., Lin F.T., Lefkowitz R.J., and Caron M.G. Mu-opioid receptor desensitization by beta-arrestin-2 determines morphine tolerance but not dependence. Nature 408 (2000) 720-723
9. Bruggemann I., Schulz S., Wiborny D., and Hollt V. Colocalization of the mu-opioid receptor and calcium/calmodulin-dependent kinase II in distinct pain-processing brain regions. Brain Res Mol Brain Res 85 (2000) 239-250
10. Celver J.P., Lowe J., Kovoor A., Gurevich V.V., and Chavkin C. Threonine 180 is required for G-protein-coupled receptor kinase 3- and beta-arrestin 2-mediated desensitization of the mu-opioid receptor in Xenopus oocytes. J Biol Chem 276 (2001) 4894-4900
11. Celver J., Xu M., Jin W., Lowe J., and Chavkin C. Distinct domains of the mu-opioid receptor control uncoupling and internalization. Mol Pharmacol 65 (2004) 528-537
12. Connor M., Osborne P.B., and Christie M.J. mu-Opioid receptor desensitization: Is morphine different?. Br J Pharmacol 143 (2004) 685-696
13. Deng H.B., Yu Y., Wang H., Guang W., and Wang J.B. Agonist-induced mu opioid receptor phosphorylation and functional desensitization in rat thalamus. Brain Res 898 (2001) 204-214
14. El Kouhen R., Burd A.L., Erickson-Herbrandson L.J., Chang C.Y., Law P.Y., and Loh H.H. Phosphorylation of Ser363, Thr370, and Ser375 residues within the carboxyl tail differentially regulates mu-opioid receptor internalization. J Biol Chem 276 (2001) 12774-12780
15. Gainetdinov R.R., Premont R.T., Bohn L.M., Lefkowitz R.J., and Caron M.G. Desensitization of G protein-coupled receptors and neuronal functions. Annu Rev Neurosci 27 (2004) 107-144
16. Gudehithlu K.P., Tejwani G.A., and Bhargava H.N. Beta-endorphin and methionine-enkephalin levels in discrete brain regions, spinal cord, pituitary gland and plasma of morphine tolerant-dependent and abstinent rats. Brain Res 553 (1991) 284-290
17. Idanpaan-Heikkila J.J., Guilbaud G., and Kayser V. Prevention of tolerance to the antinociceptive effects of systemic morphine by a selective cholecystokinin-B receptor antagonist in a rat model of peripheral neuropathy. J Pharmacol Exp Ther 282 (1997) 1366-1372
18. Kaneko T., Minami M., Satoh M., and Mizuno N. Immunocytochemical localization of mu-opioid receptor in the rat caudate-putamen. Neurosci Lett 184 (1995) 149-152
19. Kieffer B.L., and Gaveriaux-Ruff C. Exploring the opioid system by gene knockout. Prog Neurobiol 66 (2002) 285-306
20. Kitchen I., Slowe S.J., Matthes H.W., and Kieffer B. Quantitative autoradiographic mapping of mu-, delta- and kappa-opioid receptors in knockout mice lacking the mu-opioid receptor gene. Brain Res 778 (1997) 73-88
21. Kovoor A., Celver J.P., Wu A., and Chavkin C. 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
22. Kupers R.C., Konings H., Adriaensen H., and Gybels J.M. Morphine differentially affects the sensory and affective pain ratings in neurogenic and idiopathic forms of pain. Pain 47 (1991) 5-12
23. Lamey M., Thompson M., Varghese G., Chi H., Sawzdargo M., George S.R., and O'Dowd B.F. Distinct residues in the carboxyl tail mediate agonist-induced desensitization and internalization of the human dopamine D1 receptor. J Biol Chem 277 (2002) 9415-9421
24. Li S., Lee M., Bruchas M., Chan G.C., Storm D.R., and Chavkin C. Reduction of morphine tolerance and reward in mice lacking calmodulin-stimulated adenylyl cyclases. Mol Pharmacol 70 (2006) 1742-1749
25. Mansour A., Fox C.A., Burke S., Meng F., Thompson R.C., Akil H., and Watson S.J. Mu, delta, and kappa opioid receptor mRNA expression in the rat CNS: an in situ hybridization study. J Comp Neurol 350 (1994) 412-438
26. McLaughlin J.P., Marton-Popovici M., and Chavkin C. Kappa opioid receptor antagonism and prodynorphin gene disruption block stress-induced behavioral responses. J Neurosci 23 (2003) 5674-5683
27. McLaughlin J.P., Xu M., Mackie K., and Chavkin C. Phosphorylation of a carboxyl-terminal serine within the kappa-opioid receptor produces desensitization and internalization. J Biol Chem 278 (2003) 34631-34640
28. McLaughlin J.P., Myers L.C., Zarek P.E., Caron M.G., Lefkowitz R.J., Czyzyk T.A., Pintar J.E., and Chavkin C. Prolonged kappa opioid receptor phosphorylation mediated by G-protein receptor kinase underlies sustained analgesic tolerance. J Biol Chem 279 (2004) 1810-1818
29. Narita M., Kuzumaki N., Suzuki M., Narita M., Oe K., Yamazaki M., Yajima Y., and Suzuki T. Increased phosphorylated-mu-opioid receptor immunoreactivity in the mouse spinal cord following sciatic nerve ligation. Neurosci Lett 354 (2004) 148-152
30. Nichols M.L., Bian D., Ossipov M.H., Malan Jr. T.P., and Porreca F. Antiallodynic effects of a CCKB antagonist in rats with nerve ligation injury: role of endogenous enkephalins. Neurosci Lett 215 (1996) 161-164
31. Ossipov M.H., Lopez Y., Nichols M.L., Bian D., and Porreca F. Inhibition by spinal morphine of the tail-flick response is attenuated in rats with nerve ligation injury. Neurosci Lett 199 (1995) 83-86
32. Ragnauth A., Schuller A., Morgan M., Chan J., Ogawa S., Pintar J., Bodnar R.J., and Pfaff D.W. Female preproenkephalin-knockout mice display altered emotional responses. Proc Natl Acad Sci U S A 98 (2001) 1958-1963
33. Rattan A.K., and Tejwani G.A. Effect of chronic treatment with morphine, midazolam, and both together on beta-endorphin levels in the rat. Brain Res Bull 41 (1996) 335-441
34. Rogers J., Shoemaker W.J., Morgan D.G., and Finch C.E. Senescent change in tissue weight and immunoreactive beta-endorphin, enkephalin, and vasopressin in eight regions of C57BL/6J mouse brain and pituitary. Neurobiol Aging 6 (1985) 1-9
35. Rubinstein M., Mogil J.S., Japón M., Chan E.C., Allen R.G., and Low M.J. Absence of opioid stress-induced analgesia in mice lacking beta-endorphin by site-directed mutagenesis. Proc Natl Acad Sci U S A 93 (1996) 3995-4000
36. Schuller A.G., King M.A., Zhang J., Bolan E., Pan Y.X., Morgan D.J., Chang A., Czick M.E., Unterwald E.M., Pasternak G.W., and Pintar J.E. Retention of heroin and morphine-6 beta-glucuronide analgesia in a new line of mice lacking exon 1 of MOR-1. Nat Neurosci 2 (1999) 151-156
37. Schulz S., Schreff M., Koch T., Zimprich A., Gramsch C., Elde R., and Hollt V. Immunolocalization of two mu-opioid receptor isoforms (MOR1 and MOR1B) in the rat central nervous system. Neuroscience 82 (1998) 613-622
38. Schulz S., Mayer D., Pfeiffer M., Stumm R., Koch T., and Hollt V. Morphine induces terminal mu-opioid receptor desensitization by sustained phosphorylation of serine-375. EMBO J 23 (2004) 3282-3289
39. Seltzer Z., Dubner R., and Shir Y. A novel behavioral model of neuropathic pain disorders produced in rats by partial sciatic nerve injury. Pain 43 (1990) 205-218
40. Sharifi N., Diehl N., Yaswen L., Brennan M.B., and Hochgeschwender U. Generation of dynorphin knockout mice. Brain Res Mol Brain Res 86 (2001) 70-75
41. Trujillo K.A. Are NMDA receptors involved in opiate-induced neural and behavioral plasticity?. A review of preclinical studies. Psychopharmacology (Berl) 151 (2000) 121-141
42. Wang H., Moriwaki A., Wang J.B., Uhl G.R., and Pickel V.M. Ultrastructural immunocytochemical localization of mu opioid receptors and Leu5-enkephalin in the patch compartment of the rat caudate-putamen nucleus. J Comp Neurol 375 (1996) 659-374
43. Wang H.L., Chang W.T., Hsu C.Y., Huang P.C., Chow Y.W., and Li A.H. Identification of two C-terminal amino acids, Ser(355) and Thr(357), required for short-term homologous desensitization of mu-opioid receptors. Biochem Pharmacol 64 (2002) 257-266
44. Xu M., Petraschka M., McLaughlin J.P., Westenbroek R.E., Caron M.G., Lefkowitz R.J., Czyzyk T.A., Pintar J.E., Terman G.W., and Chavkin C. Neuropathic pain activates the endogenous kappa opioid system in mouse spinal cord and induces opioid receptor tolerance. J Neurosci 24 (2004) 4576-4584
45. Yu Y., Zhang L., Yin X., Sun H., Uhl G.R., and Wang J.B. Mu opioid receptor phosphorylation, desensitization, and ligand efficacy. J Biol Chem 272 (1997) 28869-28874
46. Zadina J.E., Hackler L., Ge L.J., and Kastin A.J. A potent and selective endogenous agonist for the mu-opiate receptor. Nature 386 (1997) 499-502
47. Zamir N., Palkovits M., Weber E., Mezey E., and Brownstein M.J. A dynorphinergic pathway of Leu-enkephalin production in rat substantia nigra. Nature 307 (1984) 643-645
48. Zhang J., Ferguson S.S., Barak L.S., Bodduluri S.R., Laporte S.A., Law P.Y., and Caron M.G. Role for G protein-coupled receptor kinase in agonist-specific regulation of mu-opioid receptor responsiveness. Proc Natl Acad Sci U S A 95 (1998) 7157-7162