The role of mitogen-activated protein kinase (MAPK) in morphine tolerance and dependence

Molecular Neurobiology

Volumn 40, Issue 2, 2009, Pages 101-107

  Chen, Yong ^a   Sommer, Claudia ^b  

^a DUKE UNIVERSITY   (United States)

^b UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

Activation; Dependence; Downstream target; Mitogen activated protein kinase; Morphine; Tolerance

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; ACTIVATING TRANSCRIPTION FACTOR 2; ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MINOCYCLINE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE KINASE 2; MITOGEN ACTIVATED PROTEIN KINASE KINASE 4; MITOGEN ACTIVATED PROTEIN KINASE KINASE 7; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE 1; MORPHINE; MYC PROTEIN; NALOXONE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN C FOS; PROTEIN C JUN; PROTEIN KINASE C; RAF PROTEIN; SYNAPTOPHYSIN; TRANSCRIPTION FACTOR ELK 1; VANILLOID RECEPTOR 1;

ALLODYNIA; CAUDATE NUCLEUS; CHRONIC DRUG ADMINISTRATION; CORPUS STRIATUM; DRUG DOSE COMPARISON; DRUG DOSE INCREASE; DRUG IMPLANTATION; DRUG INTERMITTENT THERAPY; DRUG PELLET; DRUG WITHDRAWAL; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; FRONTAL CORTEX; HIPPOCAMPUS; HUMAN; HYPOTHALAMUS; LOCUS CERULEUS; MORPHINE ADDICTION; MORPHINE TOLERANCE; NONHUMAN; PUTAMEN; RECOMMENDED DRUG DOSE; REPEATED DRUG DOSE; REVIEW; SIGNAL TRANSDUCTION; SINGLE DRUG DOSE; SOLITARY TRACT NUCLEUS; SPINAL GANGLION;

EID: 73049103800     PISSN: 08937648     EISSN: None     Source Type: Journal    
DOI: 10.1007/s12035-009-8074-z     Document Type: Review

References (68)

1. LM Harrison AJ Kastin JE Zadina 1998 Opiate tolerance and dependence: receptors, G-proteins, and antiopiates Peptides 19 1603 1630 9864069 10.1016/S0196-9781(98)00126-0 1:CAS:528:DyaK1cXnvFyltLk%3D (Pubitemid 29015903)
2. R Seger EG Krebs 1995 The MAPK signaling cascade FASEB J 9 726 735 7601337 1:CAS:528:DyaK2MXmvFCltb0%3D
3. C Widmann S Gibson MB Jarpe GL Johnson 1999 Mitogen-activated protein kinase: conservation of a three-kinase module from yeast to human Physiol Rev 79 143 180 9922370 1:CAS:528:DyaK1MXhs1Cgu7s%3D
4. RR Ji 2004 Mitogen-activated protein kinases as potential targets for pain killers Curr Opin Investig Drugs 5 71 75 14983977
5. K Obata K Noguchi 2004 MAPK activation in nociceptive neurons and pain hypersensitivity Life Sci 74 2643 2653 15041446 10.1016/j.lfs.2004.01.007 1:CAS:528:DC%2BD2cXisVemtro%3D (Pubitemid 38369361)
6. W Ma R Quirion 2005 The ERK/MAPK pathway, as a target for the treatment of neuropathic pain Expert Opin Ther Targets 9 699 713 16083338 10.1517/14728222.9.4.699 1:CAS:528:DC%2BD2MXmvFelsrc%3D (Pubitemid 41131674)
7. Ji RR, Kawasaki Y, Zhuang ZY, Wen YR, Zhang YQ (2007) Protein kinases as potential targets for the treatment of pathological pain. Handb Exp Pharmacol (177):359-389
8. RR Ji RW Gereau M Malcangio GR Strichartz 2008 MAP kinase and pain Brain Res Rev 60 135 148 19150373 10.1016/j.brainresrev.2008.12.011
9. J Mao DD Price DJ Mayer 1995 Mechanisms of hyperalgesia and opiate tolerance: a current view of their possible interactions Pain 62 259 274 8657426 10.1016/0304-3959(95)00073-2 1:CAS:528:DyaK2MXptlajtLw%3D
10. DJ Mayer J Mao J Holt DD Price 1999 Cellular mechanisms of neuropathic pain, morphine tolerance, and their interactions Proc Natl Acad Sci U S A 96 7731 7736 10393889 10.1073/pnas.96.14.7731 1:CAS:528:DyaK1MXltVOktrg%3D (Pubitemid 29328349)
11. EJ Nestler 2001 Molecular basis of long-term plasticity underlying addiction Nat Rev Neurosci 2 119 128 11252991 10.1038/35053570 1:CAS:528:DC%2BD3MXisl2qu78%3D (Pubitemid 33673366)
12. L Li K Chang 1996 The stimulatory effects of opioids on mitogen-activated protein kinase in Chinese hamster ovary cells transfected to express μ-opioid receptors Mol Pharmacol 50 599 602 8794899 1:CAS:528: DyaK28XlslShu7g%3D
13. HB Gutstein EA Rubie A Mansour H Akil 1997 Opioid effects on mitogen-activated protein kinase signaling cascades Anesthesiology 87 1118 1126 9366464 10.1097/00000542-199711000-00016 1:CAS:528:DyaK2sXnsVeisL4%3D (Pubitemid 27469311)
14. N Trapaidze I Gomes S Cvejic M Bansinath LA Devi 2000 Opioid receptor endocytosis and activation of MAP kinase pathway Brain Res Mol Brain Res 76 220 228 10762697 10.1016/S0169-328X(00)00002-4 1:CAS:528:DC%2BD3cXitlOlsLw%3D (Pubitemid 30179758)
15. M Ferrer-Alcón MJ García-Fuster R La Harpe JA García-Sevilla 2004 Long-term regulation of signaling components of adenylyl cyclase and mitogen-activated protein kinase in the pre-frontal cortex of human opiate addicts J Neurochem 90 220 230 15198681 10.1111/j.1471-4159. 2004.02473.x (Pubitemid 38879176)
16. W Bilecki G Zapart A Ligeza A Wawrzczak-Bargiela MJ Urbański R Przewłocki 2005 Regulation of the extracellular signal-regulated kinases following acute and chronic opioid treatment Cell Mol Life Sci 62 2369 2375 16158186 10.1007/s00018-005-5277-y 1:CAS:528:DC%2BD2MXht1ShsbvP (Pubitemid 41500552)
17. Y Liu Y Wang Z Jiang C Wan W Zhou Z Wang 2007 The extracellular signal-regulated kinase signaling pathway is involved in the modulation of morphine-induced reward by mPer1 Neuroscience 146 265 271 17320300 10.1016/j.neuroscience.2007.01.009 1:CAS:528:DC%2BD2sXkslaisrk%3D (Pubitemid 46654608)
18. E Valjent C Pagès D Hervé JA Girault J Caboche 2004 Addictive and non-addictive drugs induce distinct and specific patterns of ERK activation in mouse brain Eur J Neurosci 19 1826 1836 15078556 10.1111/j.1460-9568.2004.03278.x (Pubitemid 38482570)
19. MT Berhow N Hiroi EJ Nestler 1996 Regulation of ERK (extracellular signal regulated kinase), part of the neurotrophin signal transduction cascade, in the rat mesolimbic dopamine system by chronic exposure to morphine or cocaine J Neurosci 16 4707 4715 8764658 1:CAS:528:DyaK28XksFWju7g%3D
20. JJ Hawes DH Brunzell R Narasimhaiah U Langel D Wynick MR Picciotto 2008 Galanin protects against behavioral and neurochemical correlates of opiate reward Neuropsychopharmacology 33 1864 1873 17957220 10.1038/sj.npp.1301579 1:CAS:528:DC%2BD1cXntFShs78%3D (Pubitemid 351832595)
21. M Narita M Ioka M Suzuki T Suzuki 2002 Effect of repeated administration of morphine on the activity of extracellular signal regulated kinase in the mouse brain Neurosci Lett 324 97 100 11988336 10.1016/S0304-3940(02)00141-6 1:CAS:528:DC%2BD38Xjt1Squrg%3D (Pubitemid 34457814)
22. J Ortiz HW Harris X Guitart RZ Terwilliger JW Haycock EJ Nestler 1995 Extracellular signal-regulated protein kinases (ERKs) and ERK kinase (MEK) in brain: regional distribution and regulation by chronic morphine J Neurosci 15 1285 1297 7532701 1:CAS:528:DyaK2MXjvVCgt7g%3D
23. S Eitan CD Bryant N Saliminejad YC Yang E Vojdani D Keith Jr R Polakiewicz CJ Evans 2003 Brain region-specific mechanisms for acute morphine-induced mitogen-activated protein kinase modulation and distinct patterns of activation during analgesic tolerance and locomotor sensitization J Neurosci 23 8360 8369 12967998 1:CAS:528:DC%2BD3sXnsVGgu7Y%3D
24. S Schulz V Höllt 1998 Opioid withdrawal activates MAP kinase in locus coeruleus neurons in morphine-dependent rats in vivo Eur J Neurosci 10 1196 1201 9753188 10.1046/j.1460-9568.1998.00103.x 1:STN:280: DyaK1cvisVWisg%3D%3D (Pubitemid 28375645)
25. SX Li ZR Wang J Li ZG Peng W Zhou M Zhou L Lu 2008 Inhibition of Period1 gene attenuates the morphine-induced ERK-CREB activation in frontal cortex, hippocampus, and striatum in mice Am J Drug Alcohol Abuse 34 673 682 18850497 10.1080/00952990802308197
26. DL Muller EM Unterwald 2004 In vivo regulation of extracellular signal-regulated protein kinase (ERK) and proteinkinase B (Akt) phosphorylation by acute and chronic morphine J Pharmacol Exp Ther 310 774 782 15056728 10.1124/jpet.104.066548 1:CAS:528:DC%2BD2cXmtVyktrY%3D (Pubitemid 38988924)
27. KH Jhamandas M Marsala T Ibuki T Yaksh 1996 Spinal amino acid release and precipitated withdrawal in rats chronically infused with spinal morphine J Neurosci 16 2758 2766 8786451 1:CAS:528:DyaK28XitFKgsro%3D
28. DS Rohde WR McKay C Abbadie AI Basbaum 1997 Contribution of sacral spinal cord neurons to the autonomic and somatic consequences of withdrawal from morphine in the rat Brain Res 745 83 95 9037396 10.1016/S0006-8993(96)01132-8 1:CAS:528:DyaK2sXhs1yrtQ%3D%3D (Pubitemid 27055748)
29. DS Rohde AI Basbaum 1998 Activation of coeruleospinal noradrenergic inhibitory controls during withdrawal from morphine in the rat J Neurosci 18 4393 4402 9592116 1:CAS:528:DyaK1cXjsV2qtbg%3D
30. JL Cao JH He HL Ding YM Zeng 2005 Activation of the spinal ERK signaling pathway contributes naloxone-precipitated withdrawal in morphine-dependent rats Pain 118 336 349 16289800 10.1016/j.pain.2005.09.006 1:CAS:528: DC%2BD2MXhtlSjsbrM (Pubitemid 41752991)
31. JL Cao HL Liu JK Wang YM Zeng 2006 Cross talk between nitric oxide and ERK1/2 signaling pathway in the spinal cord mediates naloxone-precipitated withdrawal in morphine-dependent rats Neuropharmacology 51 315 326 16712881 10.1016/j.neuropharm.2006.03.028 1:CAS:528:DC%2BD28XntFSnur8%3D (Pubitemid 44096879)
32. Wang Z, Ma W, Chabot JG, Quirion R (2009) Cell-type specific activation of p38 and ERK mediates calcitonin gene-related peptide involvement in tolerance to morphine-induced analgesia. FASEB J (in press)
33. Y Chen C Geis C Sommer 2008 Activation of TRPV1 contributes to morphine tolerance: involvement of the mitogen-activated protein kinase signaling pathway J Neurosci 28 5836 5845 18509045 10.1523/JNEUROSCI.4170-07.2008 1:CAS:528:DC%2BD1cXmvFWmtr8%3D
34. W Ma WH Zheng K Powell K Jhamandas R Quirion 2001 Chronic morphine exposure increases the phosphorylation of MAP kinases and the transcription factor CREB in dorsal root ganglion neurons: an in vitro and in vivo study Eur J Neurosci 14 1091 1104 11683901 10.1046/j.0953-816x.2001.01731.x 1:STN:280:DC%2BD3Mnjs1Smtg%3D%3D (Pubitemid 35463753)
35. P Almela P García-Nogales A Romero MV Milanés ML Laorden MM Puig 2009 Effects of chronic inflammation and morphine tolerance on the expression of phospho-ERK 1/2 and phospho-P38 in the injured tissue Naunyn Schmiedebergs Arch Pharmacol 379 315 323 18839150 10.1007/s00210-008-0356-x 1:CAS:528:DC%2BD1MXhtleqtr4%3D
36. Y Cui Y Chen JL Zhi RX Guo JQ Feng PX Chen 2006 Activation of p38 mitogen-activated protein kinase in spinal microglia mediates morphine antinociceptive tolerance Brain Res 1069 235 243 16403466 10.1016/j.brainres. 2005.11.066 1:CAS:528:DC%2BD28XotVGquw%3D%3D (Pubitemid 43145918)
37. W Liu CH Wang Y Cui LQ Mo JL Zhi SN Sun YL Wang HM Yu CM Zhao JQ Feng PX Chen 2006 Inhibition of neuronal nitric oxide synthase antagonizes morphine antinociceptive tolerance by decreasing activation of p38 MAPK in the spinal microglia Neurosci Lett 410 174 177 17101217 10.1016/j.neulet.2006.08.091 1:CAS:528:DC%2BD28Xht1agtrvI (Pubitemid 44750337)
38. MD Hayward RS Duman EL Nestler 1990 Induction of the c-fos proto-oncogene during opiate withdrawal in the locus coeruleus and other regions of rat brain Brain Res 525 256 266 1701330 10.1016/0006-8993(90)90872-9 1:CAS:528: DyaK3cXls1GgtLc%3D (Pubitemid 20257744)
39. P Couceyro J Douglass 1995 Precipitated morphine withdrawal stimulates multiple activator protein-1 signaling pathways in rat brain Mol Pharmacol 47 29 39 7838131 1:CAS:528:DyaK2MXjsVSntb8%3D
40. XL Fan JS Zhang XQ Zhang L Ma 2003 Chronic morphine treatment and withdrawal induce up-regulation of c-Jun N-terminal kinase 3 gene expression in rat brain Neuroscience 122 997 1002 14643766 10.1016/j.neuroscience.2003.08.062 1:CAS:528:DC%2BD3sXpt1SqtLo%3D (Pubitemid 37485849)
41. S Nishimoto E Nishida 2006 MAPK signalling: ERK5 versus ERK1/2 EMBO Rep 7 782 786 16880823 10.1038/sj.embor.7400755 1:CAS:528:DC%2BD28XnsFajsrw%3D (Pubitemid 44275395)
42. X Wang C Tournier 2006 Regulation of cellular functions by the ERK5 signalling pathway Cell Signal 18 753 760 16376520 10.1016/j.cellsig.2005.11.003 1:CAS:528:DC%2BD28Xhtlaktbo%3D (Pubitemid 43208930)
43. K Obata H Katsura T Mizushima J Sakurai K Kobayashi H Yamanaka Y Dai T Fukuoka K Noguchi 2007 Roles of extracellular signal-regulated protein kinases 5 in spinal microglia and primary sensory neurons for neuropathic pain J Neurochem 102 1569 1584 17509087 10.1111/j.1471-4159.2007.04656.x 1:CAS:528:DC%2BD2sXhtVWnt7vM (Pubitemid 47256198)
44. H Katsura K Obata T Mizushima J Sakurai K Kobayashi H Yamanaka Y Dai T Fukuoka M Sakagami K Noguchi 2007 Activation of extracellular signal-regulated protein kinases 5 in primary afferent neurons contributes to heat and cold hyperalgesia after inflammation J Neurochem 102 1614 1624 17573825 10.1111/j.1471-4159.2007.04698.x 1:CAS:528:DC%2BD2sXhtVWnt7vI (Pubitemid 47256204)
45. C Xiao L Zhang QP Cheng LC Zhang 2008 The activation of extracellular signal-regulated protein kinase 5 in spinal cord and dorsal root ganglia contributes to inflammatory pain Brain Res 1215 76 86 18486117 10.1016/j.brainres.2008.03.065 1:CAS:528:DC%2BD1cXmvVOjsLc%3D
46. S Kamakura T Moriguchi E Nishida 1999 Activation of the protein kinase ERK5/BMK1 by receptor tyrosine kinases. Identification and characterization of a signaling pathway to the nucleus J Biol Chem 274 26563 26571 10473620 10.1074/jbc.274.37.26563 1:CAS:528:DyaK1MXmtVKlsLo%3D (Pubitemid 29437114)
47. N Mody J Leitch C Armstrong J Dixon P Cohen 2001 Effects of MAP kinase cascade inhibitors on the MKK5/ERK5 pathway FEBS Lett 502 21 24 11478941 10.1016/S0014-5793(01)02651-5 1:CAS:528:DC%2BD3MXls1eisbY%3D (Pubitemid 32722053)
48. L Moulédous MF Díaz HB Gutstein 2007 Extracellular signal-regulated kinase (ERK) inhibition does not prevent the development or expression of tolerance to and dependence on morphine in the mouse Pharmacol Biochem Behav 88 39 46 17764731 10.1016/j.pbb.2007.07.002 (Pubitemid 47379821)
49. C Mazzucchelli C Vantaggiato A Ciamei S Fasano P Pakhotin W Krezel H Welzl DP Wolfer G Pagès O Valverde A Marowsky A Porrazzo PC Orban R Maldonado MU Ehrengruber V Cestari HP Lipp PF Chapman J Pouysségur R Brambilla 2002 Knockout of ERK1 MAP kinase enhances synaptic plasticity in the striatum and facilitates striatal-mediated learning and memory Neuron 34 807 820 12062026 10.1016/S0896-6273(02)00716-X 1:CAS:528:DC%2BD38XksFKjsLY%3D (Pubitemid 34628742)
50. Y Cui XX Liao W Liu RX Guo ZZ Wu CM Zhao PX Chen JQ Feng 2008 A novel role of minocycline: attenuating morphine antinociceptive tolerance by inhibition of p38 MAPK in the activated spinal microglia Brain Behav Immun 22 114 123 17919885 10.1016/j.bbi.2007.07.014 1:CAS:528:DC%2BD2sXhsVWjtL%2FE (Pubitemid 350216368)
51. T King MH Ossipov TW Vanderah F Porreca J Lai 2005 Is paradoxical pain induced by sustained opioid exposure an underlying mechanism of opioid antinociceptive tolerance? Neurosignals 14 194 205 16215302 10.1159/000087658 1:CAS:528:DC%2BD2MXhtVyksL%2FF (Pubitemid 41417108)
52. LR Watkins MR Hutchinson A Ledeboer J Wieseler-Frank ED Milligan SF Maier 2007 Norman Cousins Lecture. Glia as the "bad guys": implications for improving clinical pain control and the clinical utility of opioids Brain Behav Immun 2 131 146 10.1016/j.bbi.2006.10.011 (Pubitemid 46038918)
53. DP Menard DV Rossum S Kar S St-Pierre M Sutak K Jhamandas R Quirion 1996 A calcitonin gene-related peptide receptor antagonist prevents the development of tolerance to spinal morphine analgesia J Neurosci 16 2342 2351 8601814 1:CAS:528:DyaK28XhvVCksr4%3D
54. KJ Powell R Quirion K Jhamandas 2003 Inhibition of neurokinin-1-substance P receptor and prostanoid activity prevents and reverses the development of morphine tolerance in vivo and the morphine-induced increase in CGRP expression in cultured dorsal root ganglion neurons Eur J Neurosci 18 1572 1583 14511336 10.1046/j.1460-9568.2003.02887.x (Pubitemid 37215110)
55. T King LR Gardell R Wang A Vardanyan MH Ossipov TP Malan Jr TW Vanderah SP Hunt VJ Hruby J Lai F Porreca 2005 Role of NK-1 neurotransmission in opioid-induced hyperalgesia Pain 116 276 288 15964684 10.1016/j.pain.2005.04.014 1:CAS:528:DC%2BD2MXlvFeiurw%3D (Pubitemid 40957131)
56. PL Durham AF Russo 1998 Serotonergic repression of mitogen-activated protein kinase control of the calcitonin gene-related peptide enhancer Mol Endocrinol 12 1002 1009 9658404 10.1210/me.12.7.1002 1:CAS:528: DyaK1cXktlOitLc%3D
57. U Forstermann I Gath P Schwarz EI Closs H Kleinert 1995 Isoforms of nitric oxide synthase: properties, cellular distribution and expressional control Biochem Pharmacol 50 1321 1332 7503779 10.1016/0006-2952(95)00181-6 1:STN:280:DyaK28%2FotValtA%3D%3D
58. MJ Caterina MA Schumacher M Tominaga TA Rosen JD Levine D Julius 1997 The capsaicin receptor: a heat-activated ion channel in the pain pathway Nature 389 816 824 9349813 10.1038/39807 1:CAS:528:DyaK2sXmvFSksbs%3D (Pubitemid 27462969)
59. MJ Caterina A Leffler AB Malmberg WJ Martin J Trafton KR Petersen-Zeitz M Koltzenburg AI Basbaum D Julius 2000 Impaired nociception and pain sensation in mice lacking the capsaicin receptor Science 288 306 313 10764638 10.1126/science.288.5464.306 1:CAS:528:DC%2BD3cXislersr8%3D (Pubitemid 30226186)
60. JD Levine N Alessandri-Haber 2007 TRP channels: targets for the relief of pain Biochim Biophys Acta 1772 989 1003 17321113 1:CAS:528:DC%2BD2sXosFOjtbg%3D
61. SR Chen A Prunean HM Pan KL Welker HL Pan 2007 Resistance to morphine analgesic tolerance in rats with deleted transient receptor potential vanilloid type 1-expressing sensory neurons Neuroscience 145 676 685 17239544 10.1016/j.neuroscience.2006.12.016 1:CAS:528:DC%2BD2sXivVSju7Y%3D (Pubitemid 46341655)
62. A Vardanyan R Wang TW Vanderah MH Ossipov J Lai F Porreca T King 2008 TRPV1 Receptor in expression of opioid-induced hyperalgesia J Pain 10 243 252 18774343 10.1016/j.jpain.2008.07.004
63. C Sommer M Kress 2004 Recent findings on how proinflammatory cytokines cause pain: peripheral mechanisms in inflammatory and neuropathic hyperalgesia Neurosci Lett 361 184 187 15135924 10.1016/j.neulet.2003.12.007 1:CAS:528:DC%2BD2cXjvVGksrk%3D (Pubitemid 38609247)
64. WA Verri Jr TM Cunha CA Parada S Poole FQ Cunha SH Ferreira 2006 Hypernociceptive role of cytokines and chemokines: targets for analgesic drug development? Pharmacol Ther 112 116 138 16730375 10.1016/j.pharmthera.2006.04. 001 1:CAS:528:DC%2BD28XptFCitrw%3D (Pubitemid 44301486)
65. E McNicol N Horowicz-Mehler RA Fisk K Bennett M Gialeli-Goudas PW Chew J Lau D Carr Americal Pain Society 2003 Management of opioid side effects in cancer-related and chronic noncancer pain: a systematic review J Pain 4 231 256 14622694 10.1016/S1526-5900(03)00556-X (Pubitemid 36807905)
66. JC Ballantyne J Mao 2003 Opioid therapy for chronic pain N Engl J Med 349 1943 1953 14614170 10.1056/NEJMra025411 1:CAS:528:DC%2BD3sXptVGnu74%3D (Pubitemid 37409712)
67. L Martini JL Whistler 2007 The role of mu opioid receptor desensitization and endocytosis in morphine tolerance and dependence Curr Opin Neurobiol 17 556 564 18068348 10.1016/j.conb.2007.10.004 1:CAS:528:DC%2BD1cXislKhsw%3D%3D
68. PY Law YH Wong HH Loh 2000 Molecular mechanisms and regulation of opioid receptor signaling Annu Rev Pharmacol Toxicol 40 389 430 10836142 10.1146/annurev.pharmtox.40.1.389 1:CAS:528:DC%2BD3cXjs1yhtr0%3D (Pubitemid 30340688)