Ultra-low dose naloxone restores the antinociceptive effect of morphine in pertussis toxin-treated rats by reversing the coupling of μ-opioid receptors from Gs-protein to coupling to Gi-protein

Neuroscience

Volumn 164, Issue 2, 2009, Pages 435-443

  Tsai, R Y ^a   Tai, Y H ^a   Tzeng, J I ^b   Cherng, C H ^a   Yeh, C C ^a   Wong, C S ^a,c  

^a TRI SERVICE GENERAL HOSPITAL   (Taiwan)

^b CHI MEI MEDICAL CENTER   (Taiwan)

^c NATIONAL DEFENSE MEDICAL CENTER   (Taiwan)

Author keywords

ADP ribosylate; G protein; immunoprecipitation; intrathecal injection; neuropathic pain; opioid

Indexed keywords

DEXTRO PHENYLALANYLCYSTEINYLTYROSYL DEXTRO TRYPTOPHYLORNITHYLTHREONYLPENICILLAMINYLTHREONINAMIDE 2,7 DISULFIDE; GLUTAMATE TRANSPORTER; INHIBITORY GUANINE NUCLEOTIDE BINDING PROTEIN; MORPHINE; MU OPIATE RECEPTOR; NALOXONE; NALTRINDOLE; PERTUSSIS TOXIN; STIMULATORY GUANINE NUCLEOTIDE BINDING PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIINFLAMMATORY ACTIVITY; ANTINOCICEPTION; ARTICLE; CONTROLLED STUDY; GENE EXPRESSION; HYPERALGESIA; IMMUNOPRECIPITATION; LOW DRUG DOSE; MALE; NERVOUS SYSTEM INFLAMMATION; NEUROPATHIC PAIN; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RAT; SIGNAL TRANSDUCTION; SPINAL CORD DORSAL HORN;

ANALGESICS, OPIOID; ANIMALS; DRUG THERAPY, COMBINATION; GTP-BINDING PROTEIN ALPHA SUBUNITS, GI-GO; GTP-BINDING PROTEIN ALPHA SUBUNITS, GS; MALE; MORPHINE; NALOXONE; NARCOTIC ANTAGONISTS; PAIN; PERTUSSIS TOXIN; RATS; RATS, WISTAR; RECEPTORS, OPIOID, MU; SPINAL CORD;

EID: 70349754718     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2009.08.015     Document Type: Article

References (46)

1. Back S.K., Lee J., Hong S.K., and Na H.S. Loss of spinal mu-opioid receptor is associated with mechanical allodynia in a rat model of peripheral neuropathy. Pain 123 (2006) 117-126
2. Bennett G.J., and Xie Y.K. A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man. Pain 33 (1988) 87-107
3. Birnbaumer L. G proteins in signal transduction. Annu Rev Pharmacol Toxicol 30 (1990) 675-705
4. Cahill C.M., Holdridge S.V., and Morinville A. Trafficking of delta-opioid receptors and other G-protein-coupled receptors: implications for pain and analgesia. Trends Pharmacol Sci 28 (2007) 23-31
5. Campbell J.N., and Meyer R.A. Mechanisms of neuropathic pain. Neuron 52 (2006) 77-92
6. Chindalore V.L., Craven R.A., Yu K.P., Butera P.G., Burns L.H., and Friedmann N. Adding ultralow-dose naltrexone to oxycodone enhances and prolongs analgesia: a randomized controlled trial of Oxytrex. J Pain 6 (2005) 392-399
7. Crain S.M., and Shen K.F. Ultra-low concentrations of naloxone selectively antagonize excitatory effects of morphine on sensory neurons, thereby increasing its antinociceptive potency and attenuating tolerance/dependence during chronic cotreatment. Proc Natl Acad Sci U S A 92 (1995) 10540-10544
8. Crain S.M., and Shen K.F. Modulation of opioid analgesia, tolerance and dependence by Gs-coupled, GM1 ganglioside-regulated opioid receptor functions. Trends Pharmacol Sci 19 (1998) 358-365
9. Crain S.M., and Shen K.F. Antagonists of excitatory opioid receptor functions enhance morphine's analgesic potency and attenuate opioid tolerance/dependence liability. Pain 84 (2000) 121-131
10. Crain S.M., and Shen K.F. Acute thermal hyperalgesia elicited by low-dose morphine in normal mice is blocked by ultra-low-dose naltrexone, unmasking potent opioid analgesia. Brain Res 888 (2001) 75-82
11. Cruciani R.A., Lussier D., Miller-Saultz D., and Arbuck D.M. Ultra-low dose oral naltrexone decreases side effects and potentiates the effect of methadone. J Pain Symptom Manage 25 (2003) 491-494
12. Dawson-Basoa M.E., and Gintzler A.R. Estrogen and progesterone activate spinal kappa-opiate receptor analgesic mechanisms. Pain 64 (1996) 169-177
13. deGroot J.F., Coggeshall R.E., and Carlton S.M. The reorganization of mu opioid receptors in the rat dorsal horn following peripheral axotomy. Neurosci Lett 233 (1997) 113-116
14. Grossman M.L., Basbaum A.I., and Fields H.L. Afferent and efferent connections of the rat tail flick reflex (a model used to analyze pain control mechanisms). J Comp Neurol 206 (1982) 9-16
15. Hille B. Modulation of ion-channel function by G-protein-coupled receptors. Trends Neurosci 17 (1994) 531-536
16. Kayser V., Lee S.H., and Guilbaud G. Evidence for a peripheral component in the enhanced antinociceptive effect of a low dose of systemic morphine in rats with peripheral mononeuropathy. Neuroscience 64 (1995) 537-545
17. Kim S.H., and Chung J.M. An experimental model for peripheral neuropathy produced by segmental spinal nerve ligation in the rat. Pain 50 (1992) 355-363
18. Kohno T., Ji R.R., Ito N., Allchorne A.J., Befort K., Karchewski L.A., and Woolf C.J. Peripheral axonal injury results in reduced Mu Opioid receptor pre- and post-synaptic action in the spinal cord. Pain 117 (2005) 77-87
19. Kolesnikov Y., El-Maarouf A., Rutishauser U., and Pasternak G. Reorganization of dorsal root ganglion neurons following chronic sciatic nerve constriction injury: correlation with morphine and lidocaine analgesia. Eur J Pharmacol 568 (2007) 124-133
20. Kong L.L., and Yu L.C. Involvement of mu- and delta-opioid receptors in the antinociceptive effects induced by AMPA receptor antagonist in the spinal cord of rats. Neurosci Lett 402 (2006) 180-183
21. Largent-Milnes T.M., Guo W., Wang H.Y., Burns L.H., and Vanderah T.W. Oxycodone plus ultra-low-dose naltrexone attenuates neuropathic pain and associated mu-opioid receptor-Gs coupling. J Pain 9 (2008) 700-713
22. Law P.Y., Wong Y.H., and Loh H.H. Molecular mechanisms and regulation of opioid receptor signaling. Annu Rev Pharmacol Toxicol 40 (2000) 389-430
23. Li C.Y., Song Y.H., Higuera E.S., and Luo Z.D. Spinal dorsal horn calcium channel alpha2delta-1 subunit upregulation contributes to peripheral nerve injury-induced tactile allodynia. J Neurosci 24 (2004) 8494-8499
24. Mansikka H., Zhao C., Sheth R.N., Sora I., Uhl G., and Raja S.N. Nerve injury induces a tonic bilateral mu-opioid receptors-mediated inhibitory effect on mechanical allodynia in mice. Anesthesiology 100 (2004) 912-921
25. Mao J., Price D.D., and Mayer D.J. Experimental mononeuropathy reduces the antinociceptive effects of morphine: implications for common intracellular mechanisms involved in morphine tolerance and neuropathic pain. Pain 61 (1995) 353-364
26. Matthes H.W., Maldonado R., Simonin F., Valverde O., Slowe S., Kitchen I., Befort K., Dierich A., Le Meur M., Dolle P., Tzavara E., Hanoune J., Roques B.P., and Kieffer B.L. Loss of morphine-induced analgesia reward effect and withdrawal symptoms in mice lacking the mu-opioid-receptor gene. Nature 383 (1996) 819-823
27. McCormack K., Prather P., and Chapleo C. Some new insights into the effects of opioids in phasic and tonic nociceptive tests. Pain 78 (1998) 79-98
28. Pasternak G.W. Multiple opiate receptors: deja vu all over again. Neuropharmacology 47 Suppl 1 (2004) 312-323
29. Petaja-Repo U.E., Hogue M., Bhalla S., Laperriere A., Morello J.P., and Bouvier M. Ligands act as pharmacological chaperones and increase the efficiency of delta Opioid receptor maturation. EMBO J 21 (2002) 1628-1637
30. Powell K.J., Abul-Husn N.S., Jhamandas A., Olmstead M.C., Beninger R.J., and Jhamandas K. Paradoxical effects of the opioid antagonist naltrexone on morphine analgesia tolerance, and reward in rats. J Pharmacol Exp Ther 300 (2002) 588-596
31. Raghavendra V., Tanga F., and Deleo J.A. Inhibition of microglial activation attenuates the development but not existing hypersensitivity in a rat model of neuropathy. J Pharmacol Exp Ther 306 (2003) 624-630
32. Raja S.N., Haythornthwaite J.A., Pappagallo M., Clark M.R., Travison T.G., Sabeen S., Royall R.M., and Max M.B. Opioids versus antidepressants in postherpetic neuralgia: a randomized placebo-controlled trial. Neurology 59 (2002) 1015-1021
33. Shah S., Duttaroy A., Davis T., and Yoburn B.C. Spinal and supraspinal effects of pertussis toxin on opioid analgesia. Pharmacol Biochem Behav 49 (1994) 773-776
34. Shen K.F., and Crain S.M. Antagonists at excitatory opioid receptors on sensory neurons in culture increase potency and specificity of opiate analgesics and attenuate development of tolerance/dependence. Brain Res 636 (1994) 286-297
35. Shen K.F., and Crain S.M. Ultra-low doses of naltrexone or etorphine increase morphine's antinociceptive potency and attenuate tolerance/dependence in mice. Brain Res 757 (1997) 176-190
36. Truong W., Cheng C., Xu Q.G., Li X.Q., and Zochodne D.W. Mu opioid receptors and analgesia at the site of a peripheral nerve injury. Ann Neurol 53 (2003) 366-375
37. Tsai R.Y., Jang F.L., Tai Y.H., Lin S.L., Shen C.H., and Wong C.S. Ultra-low-dose naloxone restores the antinociceptive effect of morphine and suppresses spinal neuroinflammation in PTX-treated rats. Neuropsychopharmacology 33 (2008) 2772-2782
38. Tsai R.Y., Tai Y.H., Tzeng J.I., Lin S.L., Shen C.H., Yang C.P., Hsin S.T., Wang C.B., and Wong C.S. Ultra-low dose naloxone restores the antinociceptive effect of morphine in pertussis toxin-treated rats and prevents glutamate transporter downregulation by suppressing the p38 mitogen-activated protein kinase signaling pathway. Neuroscience 159 (2009) 1244-1256
39. Wang H.Y., and Burns L.H. Naloxone's pentapeptide binding site on filamin A blocks Mu Opioid receptor-Gs coupling and CREB activation of acute morphine. PLoS One 4 (2009) e4282
40. Wang H.Y., Frankfurt M., and Burns L.H. High-affinity naloxone binding to filamin a prevents Mu Opioid receptor-Gs coupling underlying opioid tolerance and dependence. PLoS One 3 (2008) e1554
41. Wang H.Y., Friedman E., Olmstead M.C., and Burns L.H. Ultra-low-dose naloxone suppresses opioid tolerance dependence and associated changes in Mu Opioid receptor-G protein coupling and Gbetagamma signaling. Neuroscience 135 (2005) 247-261
42. Watson C.P., and Babul N. Efficacy of oxycodone in neuropathic pain: a randomized trial in postherpetic neuralgia. Neurology 50 (1998) 1837-1841
43. Wiesenfeld-Hallin Z. The effects of intrathecal morphine and naltrexone on autotomy in sciatic nerve sectioned rats. Pain 18 (1984) 267-278
44. Womer D.E., DeLapp N.W., and Shannon H.E. Intrathecal pertussis toxin produces hyperalgesia and allodynia in mice. Pain 70 (1997) 223-228
45. Womer D.E., and Shannon H.E. Reversal of pertussis toxin-induced thermal allodynia by muscarinic cholinergic agonists in mice. Neuropharmacology 39 (2000) 2499-2504
46. Zhang X., Bao L., Shi T.J., Ju G., Elde R., and Hokfelt T. Downregulation of mu-opioid receptors in rat and monkey dorsal root ganglion neurons and spinal cord after peripheral axotomy. Neuroscience 82 (1998) 223-240