Agonist-dependent attenuation of μ-opioid receptor-mediated G-protein activation in the dorsal root ganglia of neuropathic rats

Journal of Neural Transmission

Volumn 117, Issue 4, 2010, Pages 421-429

  Obara, Ilona ^a,b,c   Gunduz Cinar, Ozge ^b,d   Starowicz, Katarzyna ^a   Benyhe, Sandor ^b   Borsodi, Anna ^b   Przewlocka, Barbara ^a  

^a INSTITUTE OF PHARMACOLOGY   (Poland)

^b INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

opioid receptor; 35S GTP S binding; Dorsal root ganglia; Morphine; Neuropathic pain; Opioid peptides

Indexed keywords

ENDORPHIN; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANOSINE 5' O (3 THIOTRIPHOSPHATE); GUANOSINE 5' O (3 THIOTRIPHOSPHATE) S 35; MESSENGER RNA; MORPHINE; MU OPIATE RECEPTOR; MU OPIATE RECEPTOR AGONIST; RADIOISOTOPE; SULFUR 35; UNCLASSIFIED DRUG;

ANALGESIC ACTIVITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; DRUG PROTEIN BINDING; GENE EXPRESSION REGULATION; ISOTOPE LABELING; MALE; NEUROPATHIC PAIN; NEUROPATHY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RAT; SPINAL GANGLION;

ANALGESICS, OPIOID; ANIMALS; FUNCTIONAL LATERALITY; GANGLIA, SPINAL; GTP-BINDING PROTEINS; MALE; MORPHINE; NEURALGIA; POSTERIOR HORN CELLS; RATS; RATS, WISTAR; RECEPTORS, OPIOID, MU; RNA, MESSENGER; SCIATIC NERVE; SCIATIC NEUROPATHY; SPINAL CORD; TIME FACTORS;

EID: 77952242527     PISSN: 03009564     EISSN: 14351463     Source Type: Journal    
DOI: 10.1007/s00702-010-0382-y     Document Type: Article

References (43)

1. C Abbadie JL Brown PW Mantyh AI Basbaum 1996 Spinal cord substance P receptor immunoreactivity increases in both inflammatory and nerve injury models of persistent pain Neuroscience 70 201 209 10.1016/0306-4522(95)00343-H 1:CAS:528:DyaK2MXpslOitr8%3D 8848125
2. S Arnér BA Meyerson 1988 Lack of analgesic effect of opioids on neuropathic and idiopathic forms of pain Pain 33 11 23 10.1016/0304-3959(88) 90198-4 2454440
3. JC Ballantyne J Mao 2003 Opioid therapy for chronic pain N Engl J Med 349 1943 1953 10.1056/NEJMra025411 1:CAS:528:DC%2BD3sXptVGnu74%3D 14614170 (Pubitemid 37409712)
4. GJ Bennett YK Xie 1988 A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man Pain 33 87 107 10.1016/0304-3959(88)90209-6 1:STN:280:DyaL1c3kslGhsw%3D%3D 2837713
5. S Benyhe J Farkas G Tóth M Wollemann 1997 Met5-enkephalin-Arg6- Phe7, an endogenous neuropeptide, binds to multiple opioid and nonopioid sites in rat brain J Neurosci Res 48 249 258 10.1002/(SICI)1097-4547(19970501)48: 3<249::AID-JNR7>3.0.CO;2-F 1:CAS:528:DyaK2sXivVKjsbc%3D 9160247 (Pubitemid 27190905)
6. NT Burford LM Tolbert W Sadee 1998 Specific G protein activation and mu-opioid receptor internalization caused by morphine, DAMGO and endomorphin Eur J Pharmacol 342 123 126 10.1016/S0014-2999(97)01556-2 1:CAS:528: DyaK1cXhvFGqsrY%3D 9544801 (Pubitemid 28131354)
7. P Chomczynski N Sacchi 1987 Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction Anal Biochem 162 156 159 10.1016/0003-2697(87)90021-2 1:CAS:528:DyaL2sXitFSns7Y%3D 2440339
8. RW Colburn JA DeLeo AJ Rickman MP Yeager P Kwon WF Hickey 1997 Dissociation of microglial activation and neuropathic pain behaviors following peripheral nerve injury in the rat J Neuroimmunol 79 163 175 10.1016/S0165-5728(97)00119-7 1:CAS:528:DyaK2sXmsVyhtb8%3D 9394789 (Pubitemid 27502035)
9. RH Dworkin AB O'Connor M Backonja JT Farrar NB Finnerup TS Jensen EA Kalso JD Loeser C Miaskowski TJ Nurmikko RK Portenoy AS Rice BR Stacey RD Treede DC Turk MS Wallace 2007 Pharmacologic management of neuropathic pain: evidence-based recommendations Pain 132 237 251 10.1016/j.pain.2007.08.033 1:CAS:528:DC%2BD2sXht1yls7nN 17920770 (Pubitemid 350051570)
10. LR Gardell TW Vanderah SE Gardell R Wang MH Ossipov J Lai F Porreca 2003 Enhanced evoked excitatory transmitter release in experimental neuropathy requires descending facilitation J Neurosci 23 8370 8379 1:CAS:528: DC%2BD3sXnsVGgu7c%3D 12967999
11. T Koch V Höllt 2008 Role of receptor internalization in opioid tolerance and dependence Pharmacol Ther 117 199 206 10.1016/j.pharmthera.2007. 10.003 18076994
12. M Koltzenburg PD Wall SB McMahon 1999 Does the right side know what the left is doing? Trends Neurosci 22 122 127 10.1016/S0166-2236(98)01302-2 1:CAS:528:DyaK1MXhvVyrs7Y%3D 10199637 (Pubitemid 29151805)
13. TM Largent-Milnes W Guo HY Wang LH Burns TW Vanderah 2008 Oxycodone plus ultra-low-dose naltrexone attenuates neuropathic pain and associated mu-opioid receptor-Gs coupling J Pain 9 700 713 10.1016/j.jpain.2008.03.005 1:CAS:528:DC%2BD1cXptVajtrY%3D 18468954
14. ZH Li LD Shan XH Jiang SY Guo GD Yu T Hisamitsu QZ Yin 2001 Analgesic effect of endomorphin-1 Acta Pharmacol Sin 22 976 980 1:CAS:528: DC%2BD3MXotlSjs7w%3D 11749786
15. CE Maher JC Eisenach HL Pan R Xiao SR Childers 2001 Chronic intrathecal morphine administration produces homologous mu receptor/G-protein desensitization specifically in spinal cord Brain Res 895 1 8 10.1016/S0006-8993(00)03093-6 1:CAS:528:DC%2BD3MXitVOgu70%3D 11259753 (Pubitemid 32231131)
16. K McConalogue EF Grady J Minnis B Balestra M Tonini NC Brecha NW Bunnett C Sternini 1999 Activation and internalization of the mu-opioid receptor by the newly discovered endogenous agonists, endomorphin-1 and endomorphin-2 Neuroscience 90 1051 1059 10.1016/S0306-4522(98)00514-4 1:CAS:528: DyaK1MXitlGgurc%3D 10218804 (Pubitemid 29156769)
17. J Mika MK Schäfer I Obara E Weihe B Przewlocka 2004 Morphine and endomorphin-1 differently influence pronociceptin/orphanin FQ system in neuropathic rats Pharmacol Biochem Behav 78 171 178 10.1016/j.pbb.2004.03.005 1:CAS:528:DC%2BD2cXkt1Srsbs%3D 15159147 (Pubitemid 38670526)
18. M Narita N Kuzumaki M Suzuki M Narita K Oe M Yamazaki Y Yajima T Suzuki 2004 Increased phosphorylated-mu-opioid receptor immunoreactivity in the mouse spinal cord following sciatic nerve ligation Neurosci Lett 354 148 152 10.1016/j.neulet.2003.09.077 1:CAS:528:DC%2BD3sXpvF2ktb4%3D 14698460 (Pubitemid 38032855)
19. ML Nichols D Bian MH Ossipov J Lai F Porreca 1995 Regulation of morphine antiallodynic efficacy by cholecystokinin in a model of neuropathic pain in rats J Pharmacol Exp Ther 275 1339 1345 1:CAS:528:DyaK28XhvVyrtg%3D%3D 8531101
20. AL Oaklander K Romans S Horasek A Stocks P Hauer RA Meyer 1998 Unilateral postherpetic neuralgia is associated with bilateral sensory neuron damage Ann Neurol 44 789 795 10.1002/ana.410440513 1:STN:280:DyaK1M%2FjsVantg%3D%3D 9818935
21. I Obara R Przewlocki B Przewlocka 2004 Local peripheral effects of mu-opioid receptor agonists in neuropathic pain in rats Neurosci Lett 360 85 89 10.1016/j.neulet.2004.01.056 1:CAS:528:DC%2BD2cXjtV2nt7c%3D 15082185 (Pubitemid 38471994)
22. I Obara JR Parkitna M Korostynski W Makuch D Kaminska B Przewlocka R Przewlocki 2009 Local peripheral opioid effects and expression of opioid genes in the spinal cord and dorsal root ganglia in neuropathic and inflammatory pain Pain 141 283 291 10.1016/j.pain.2008.12.006 1:CAS:528:DC%2BD1MXhtlSlt7w%3D 19147290
23. 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 10.1111/j.1471-4159.2007.04656.x 1:CAS:528: DC%2BD2sXhtVWnt7vM 17509087 (Pubitemid 47256198)
24. MH Ossipov Y Lopez ML Nichols D Bian F Porreca 1995 The loss of antinociceptive efficacy of spinal morphine in rats with nerve ligation injury is prevented by reducing spinal afferent drive Neurosci Lett 199 87 90 10.1016/0304-3940(95)12022-V 1:CAS:528:DyaK2MXptVemsro%3D 8584250
25. RK Portenoy NA Hagen 1990 Breakthrough pain: definition, prevalence and characteristics Pain 41 273 281 10.1016/0304-3959(90)90004-W 1:STN:280:DyaK3czls1aktw%3D%3D 1697056 (Pubitemid 20187930)
26. B Przewlocka J Mika D Labuz G Toth R Przewlocki 1999 Spinal analgesic action of endomorphins in acute, inflammatory and neuropathic pain in rats Eur J Pharmacol 367 189 196 10.1016/S0014-2999(98)00956-X 1:CAS:528: DyaK1MXhsVWnsb4%3D 10078992 (Pubitemid 29106370)
27. R Przewlocki B Przewlocka 2001 Opioids in chronic pain Eur J Pharmacol 429 79 91 10.1016/S0014-2999(01)01308-5 1:CAS:528:DC%2BD3MXotFWisL0%3D 11698029 (Pubitemid 33043984)
28. R Przewlocki D Labuz J Mika B Przewlocka C Tomboly G Toth 1999 Pain inhibition by endomorphins Ann N Y Acad Sci 897 154 164 10.1111/j.1749-6632. 1999.tb07887.x 1:CAS:528:DC%2BD3cXnt1SktQ%3D%3D 10676444
29. MH Rashid M Inoue K Toda H Ueda 2004 Loss of peripheral morphine analgesia contributes to the reduced effectiveness of systemic morphine in neuropathic pain J Pharmacol Exp Ther 309 380 387 10.1124/jpet.103.060582 1:CAS:528:DC%2BD2cXivFamur0%3D 14718584 (Pubitemid 38393151)
30. Z Saidak K Blake-Palmer DL Hay JK Northup M Glass 2006 Differential activation of G-proteins by mu-opioid receptor agonists Br J Pharmacol 147 671 680 10.1038/sj.bjp.0706661 1:CAS:528:DC%2BD28XisFOntrY%3D 16415903
31. P Sánchez-Blázquez M Rodríguez-Díaz I DeAntonio I Garzón 1999 Endomorphin-1 and endomorphin-2 show differences in their activation of mu opioid receptor-regulated G proteins in supraspinal antinociception in mice J Pharmacol Exp Ther 291 12 18 10490881
32. P Sánchez-Blázquez P Gómez-Serranillos J Garzón 2001 Agonists determine the pattern of G-protein activation in mu-opioid receptor-mediated supraspinal analgesia Brain Res Bull 54 229 235 10.1016/S0361-9230(00)00448-2 11275413 (Pubitemid 32223929)
33. LJ Sim DE Selley SR Childers 1995 In vitro autoradiography of receptor-activated G proteins in rat brain by agonist-stimulated guanylyl 5′-[gamma-[35S]thio]-triphosphate binding Proc Natl Acad Sci USA 96 7242 7246 10.1073/pnas.92.16.7242
34. LJ Sim-Selley KL Scoggins MP Cassidy LA Smith WL Dewey FL Smith DE Selley 2007 Region-dependent attenuation of mu opioid receptor-mediated G-protein activation in mouse CNS as a function of morphine tolerance Br J Pharmacol 151 1324 1333 10.1038/sj.bjp.0707328 1:CAS:528:DC%2BD2sXovFehsrc%3D 17572699 (Pubitemid 47255897)
35. M Spetea K Monory C Tömböly G Tóth E Tzavara S Benyhe J Hanoune A Borsodi 1998 In vitro binding and signaling profile of the novel mu opioid receptor agonist endomorphin 2 in rat brain membranes Biochem Biophys Res Commun 250 720 725 10.1006/bbrc.1998.9395 1:CAS:528:DyaK1cXmsF2qsb4%3D 9784412 (Pubitemid 28484794)
36. CI Svensson M Schäfers TL Jones TL Yaksh LS Sorkin 2006 Covariance among age, spinal p38 MAP kinase activation and allodynia J Pain 7 337 345 10.1016/j.jpain.2005.12.007 1:CAS:528:DC%2BD28XjvV2qsLo%3D 16632323
37. W Truong C Cheng QG Xu XQ Li DW Zochodne 2003 Mu opioid receptors and analgesia at the site of a peripheral nerve injury Ann Neurol 53 366 375 10.1002/ana.10465 1:CAS:528:DC%2BD3sXit1yntb4%3D 12601704 (Pubitemid 36258640)
38. HY Wang LH Burns 2006 Gbetagamma that interacts with adenylyl cyclase in opioid tolerance originates from a Gs protein J Neurobiol 66 1302 1330 10.1002/neu.20286 1:CAS:528:DC%2BD28Xht1WmsrvI 16967511 (Pubitemid 44713809)
39. HS Xiao QH Huang FX Zhang L Bao YJ Lu C Guo L Yang WJ Huang G Fu SH Xu XP Cheng Q Yan ZD Zhu X Zhang Z Chen ZG Han X Zhang 2002 Identification of gene expression profile of dorsal root ganglion in the rat peripheral axotomy model of neuropathic pain Proc Natl Acad Sci USA 99 8360 8365 10.1073/pnas.122231899 1:CAS:528:DC%2BD38XkvVGgu7Y%3D 12060780 (Pubitemid 34651057)
40. JT Xu HY Tu WJ Xin XG Liu GH Zhang CH Zhai 2007 Activation of phosphatidylinositol 3-kinase and protein kinase B/Akt in dorsal root ganglia and spinal cord contributes to the neuropathic pain induced by spinal nerve ligation in rats Exp Neurol 206 269 279 10.1016/j.expneurol.2007.05.029 1:CAS:528:DC%2BD2sXotlWkt7c%3D 17628541 (Pubitemid 47094771)
41. X Yu X Mao AD Blake WX Li SL Chang 2003 Morphine and endomorphins differentially regulate micro-opioid receptor mRNA in SHSY-5Y human neuroblastoma cells J Pharmacol Exp Ther 306 447 454 10.1124/jpet.103.048694 1:CAS:528:DC%2BD3sXlslGltL4%3D 12754318 (Pubitemid 36886139)
42. X Zhang L Bao TJ Shi G Ju R Elde T Hökfelt 1998 Down-regulation of mu-opioid receptors in rat and monkey dorsal root ganglion neurons and spinal cord after peripheral axotomy Neuroscience 82 223 240 10.1016/S0306-4522(97) 00240-6 1:CAS:528:DyaK2sXmvFCqtr4%3D 9483516
43. M Zimmermann 1983 Ethical guidelines for investigations of experimental pain in conscious animals Pain 16 109 110 10.1016/0304-3959(83)90201-4 1:STN:280:DyaL3s3nt1GqsQ%3D%3D 6877845 (Pubitemid 13058546)