dextro-Naloxone or levo-naloxone reverses the attenuation of morphine antinociception induced by lipopolysaccharide in the mouse spinal cord via a non-opioid mechanism

European Journal of Neuroscience

Volumn 24, Issue 9, 2006, Pages 2575-2580

  Wu, Hsiang En ^a   Sun, Han Sen ^a   Cheng, Caleb W ^a   Terashvili, Maia ^a   Tseng, Leon F ^a  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

Antianalgesia; Antinociception; dextro naloxone; Lipopolysaccharide; Opioid

Indexed keywords

LIPOPOLYSACCHARIDE; MORPHINE SULFATE; NALOXONE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINOCICEPTION; ARTICLE; CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; GLIA; MALE; MOUSE; NERVE CELL STIMULATION; NONHUMAN; PRIORITY JOURNAL; SPINAL CORD; TAIL FLICK TEST;

ANALGESICS, OPIOID; ANIMALS; INJECTIONS, SPINAL; LIPOPOLYSACCHARIDES; MALE; MICE; MORPHINE; NALOXONE; NARCOTIC ANTAGONISTS; NEUROGLIA; PAIN; SPINAL CORD; STEREOISOMERISM;

EID: 33750930263     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2006.05144.x     Document Type: Article

References (55)

1. Ali, H., Richardson, R.M., Haribabu, B. & Snyderman, R. (1999) Chemoattractant receptor cross-desensitization. J. Biol. Chem., 274, 6027-6030.
2. Alonso, G., Phan, V.L., Guillemain, I., Saunier, M., Legrand, A., Anoal, M. & Maurice, T. (2000) Immunocytochemical localization of the sigma1 receptor in the adult rat central nervous system. Neuroscience, 97, 155-170.
3. Arner, S. & Meyerson, B.A. (1988) Lack of analgesic effect of opioids on neuropathic and idiopathic forms of pain. Pain, 33, 11-23.
4. Bian, D., Nichols, M.L., Ossipov, M.H., Lai, J. & Porreca, F. (1995) Characterization of the antiallodynic efficacy of morphine in a model of neuropathic pain in rats. Neuroreport, 6, 1981-1984.
5. Chatterjie, N., Alexander, G.J., Sechzer, J.A. & Lieberman, K.W. (1996) Prevention of cocaine-induced hyperalgesia by a naloxone isomer with no opiate antagonist activity. Neurochem. Res., 21, 691-693.
6. Chatterjie, N., Sechzer, J.A., Lieberman, K.W. & Alexander, G.J. (1998) Dextro-naloxone counteracts amphetamine-induced hyperactivity. Pharmacol. Biochem. Behav., 59, 271-274.
7. Chien, C.C. & Pasternak, G.W. (1994) Selective antagonism of opioid analgesia by a sigma system. J. Pharmacol. Exp. Ther., 271, 1583-1884.
8. Chow, J.C., Young, D.W., Golenbock, D.T., Christ, W.J. & Gusovsky, F. (1999) Toll-like receptor-4 mediates lipopolysaccharide-induced signal transduction. J. Biol. Chem., 274, 10689-10692.
9. Colburn, R.W., Rickman, A.J. & DeLeo, J.A. (1999) The effects of site and type of nerve injury on spinal glial activation and neuropathic pain behavior. Exp. Neurol., 157, 289-304.
10. Couture, S. & Debonnel, G. (2001) Some of the effects of the selective sigma ligand (+) pentazocine are mediated via a naloxone-sensitive receptor. Synapse, 39, 323-331.
11. D'Amour, F.E. & Smith, D.L. (1941) A method for determining loss of pain sensation. J. Pharmacol. Exp. Ther., 72, 74-79.
12. Derocq, J.M., Bourrie, B., Segul, M., Le Fur, G. & Casellas, P. (1994) In vivo inhibition of endotoxin-induced pro-inflammatory cytokines production by the sigma ligand SR31747. J. Pharmacol. Exp. Ther., 272, 224-230.
13. Dunwiddie, T.V., Perez-Reyes, E., Rice, K.C. & Palmer, M.R. (1982) Stereoselectivity of opiate antagonists in rat hippocampus and neocortex: response to (+)- and (-)isomer of naloxone. Neuroscience, 7, 1691-1702.
14. Elmquist, J.K., Scammell, T.E. & Saper, C.B. (1997) Mechanisms of CNS response to systemic immune challenge: the febrile response. Trends Neurosci., 20, 565-570.
15. Faden, I.A. & Salzman, S. (1992) Pharmacological strategies in CNS trauma. Trends Pharmacol. Sci., 13, 29-35.
16. Fallis, R.J., Fisher, M. & Lobo, R.A. (1983) A double blind trial of naloxone in the treatment of stroke. Stroke, 15, 627-629.
17. Gadient, R.A. & Otten, U.H. (1997) Interleukin-6 (IL-6) a molecule with both beneficial and destructive potential. Prog. Neurobiol., 52, 379-390.
18. Gayle, D.A., Ling, Z., Tong, C., Landers, T., Lipton, J.W. & Carvey, P.M. (2002) Lipopolysaccharides-induced dopamine cell loss in cultures: role of tumor necrosis factor-alpha, interleukin-1 beta, and nitric oxide. Brain Res. Dev. Brain Res., 133, 27-35.
19. Gehrmann, J., Monoco, S. & Kreutzberg, G.W. (1991) Spinal cord microglia cells and DRG satellite cells rapidly respond to transection of the rat sciatic nerve. Restor. Neurol. Neurosci., 2, 181-198.
20. Gilmore, S.A. & Skinner, R.D. (1979) Intraspinal non-neuronal cellular responses to peripheral nerve injury. Anat. Rec., 194, 369-388.
21. Gul, H., Yildiz, O., Dogrul, A., Yesilyurt, O. & Isimer, A. (2000) The interaction between IL-1beta and morphine: possible mechanism of the deficiency of morphine-induced analgesia in diabetic mice. Pain, 15, 39-45.
22. Hashizume, H., Rutkowski, M.D., Weinstein, J.N. & DeLeo, J.A. (2000) Central administration of methotrexate reduces mechanical allodynia in an animal model of radiculopathy/sciatica. Pain, 87, 159-169.
23. Hosobuchi, T., Baskin, D.S. & Woo, S.K. (1982) Reversal of induced ischemic neurologic deficit in gerbil by the opiate antagonist naloxone. Science (Wash. DC), 215, 69-71.
24. Hylden, J.L.K. & Wilcox, G.L. (1980) Intrathecal morphine in mice: a new technique. Eur. J. Pharmacol., 167, 313-316.
25. Iijima, I., Minamikawa, J.-I., Jacobsen, A.E., Brossi, A. & Rice, K.E. (1978) Studies in the (+)-morphine series-5. Synthesis and biological properties of (+)-naloxone. J. Med. Chem., 21, 398-400.
26. Irwin, S., Houde, R.W., Bennett, D.R., Hendershot, L.C. & Seevers, M.H. (1951) The effects of morphine methadone and meperidine on some reflex responses of spinal animals to nociceptive stimulation. J. Pharmacol. Exp. Ther., 101, 132-143.
27. Johnston, I.N. & Westbrook, R.F. (2003) Acute and conditioned sickness reduces morphine analgesia. Behav. Brain Res., 142, 89-97.
28. Johnston, I.N. & Westbrook, R.F. (2005) Inhibition of morphine analgesia by LPS: role of opioid and NMDA receptors and spinal glia. Behav. Brain Res., 156, 75-83.
29. Kan, M.N., Chen, Y.T. & Lee, A.Y.S. (1992) Naloxone reversal of ischemic arrhythmia is stereospecific and suggesting role of endogenous opioid peptides in ischemic heart disease. Proc. Soc. Exp. Biol. Medical, 200, 518-521.
30. Kong, L.Y., McMillian, M.K., Hudson, P.M., Jin, L. & Hong, J.-S. (1997) Inhibition of lipopolysaccharide-induced nitric oxide and cytokine production by ultralow concentrations of dynorphins in mixed glia cultures. J. Pharmacol. Exp. Ther., 280, 61-66.
31. Lehnardt, S., Lachance, C., Patrizi, S., Lefebvre, S., Follet, P.L., Jensen, F.E., Rosenberg, P.A., Volpe, J.J. & Vartanian, T. (2002) The TLR4 is necessary for lipopolysaccharide-induced oligodendrocyte injury in the CNS. J. Neurosci., 22, 2478-2486.
32. Lehnardt, S., Massillon, L., Follett, P., Jensen, F.E., Ratan, R., Rosenberg, P.A., Volpe, J.J. & Vartanian, T. (2003) Activation of innate immunity in the CNS triggers neurodegeneration through a Toll-like receptor 4-dependent pathway. Proc. Natl Acad. Sci. USA, 100, 8514-8519.
33. Liu, B., Du, L. & Hong, J.S. (2000) Naloxone protects rat dopaminergic neurons against inflammatory damage through inhibition of microglia activation and superoxide generation. J. Pharmacol. Exp. Ther., 293, 607-617.
34. Marcoli, M., Ricevuti, G., Mazzone, A., Pastti, D., Lecchini, S. & Frigo, G.M. (1989) A stereoselective blockade by naloxone of opioid and non-opioid induced granulocyte activation. Int. J. Immunopharmacol., 11, 57-61.
35. Martin, W.R., Eades, C.G., Thompson, J.A., Hyppler, R.E. & Gilbert, P.E. (1976) The effects of morphine- and nalorphine-like drugs in the nondependent and morphine-dependent chronic spinal dog. J. Pharmacol. Exp. Ther., 197, 517-532.
36. 1 receptor function: behavioral consequences and therapeutic opportunities. Brain Res. Rev., 37, 116-132.
37. Mei, J. & Pasternak, G.W. (2002) σ1 Receptor modulation of opioid analgesia in the mouse. J. Pharmacol. Exp. Ther., 300, 1070-1074.
38. Meller, S.T., Dykstra, C., Grzybycki, D., Murphy, S. & Gebhart, G.F. (1994) The possible role of glia in nociceptive processing and hyperalgesia in the spinal cord of the rat. Neuropharmacology, 33, 1471-1478.
39. Murphy, P.M., Baggiolini, M., Charo, I.F., Hebert, C.A., Horuk, R., Matsushima, K., Miller, L.H., Oppenheim, J.J. & Power, C.A. (2000) International union of pharmacology XXXII, nomenclature for chemokine receptors. Pharmacol. Rev., 52, 145-176.
40. Raghavendra, V. & DeLeo, J.A. (2004) The role of astrocytes and microglia in persistent pain. In Hertz, L. (Ed.), Advances in Molecular and Cell Biology, Non-Neuronal Cells of the Nervous System: Function and Dysfunction. Part III: Pathological Conditions. Elsevier, Amsterdam, pp. 951-966.
41. Raghavendra, V., Tanga, F. & DeLeo, J.A. (2003a) Inhibition of microglial activation attenuates the development but not existing hyperalgesia in a rat model of neuropathy. J. Pharmacol. Exp. Ther., 306, 624-630.
42. Raghavendra, V., Tanga, F., Rutkowski, M.D. & DeLeo, J.A. (2003b) Antihyperalgesia and morphine-sparing actions of propentofylline following peripheral nerve injury in rats: mechanistic implications of spinal glia and proinflammatory cytokines. Pain, 104, 655-664.
43. Rogers, T.J. & Peterson, P.K. (2003) Opioid G protein-coupled receptors: signals at the crossroads of inflammation. Trends Immunol., 24, 116-121.
44. Rowbotham, M.C., Twilling, L., Davies, P.S., Reisner, L., Taylor, K. & Mohr, D. (2003) Oral opioid therapy for chronic peripheral and central neuropathic pain. N. Engl. J. Med., 348, 1223-1232.
45. Shavit, Y., Wolf, G., Goshen, I., Livshits, D. & Yirmiya, R. (2005) Interleukin-1 antagonizes morphine analgesia and underlies morphine tolerance. Pain, 115, 50-59.
46. Sinclair, J.G., Main, C.D. & Lo, G.F. (1988) Spinal vs. supraspinal actions of morphine on the rat tail-flick reflex. Pain, 33, 357-362.
47. Sweitzer, S.M., Schubert, P. & DeLeo, J.A. (2001) Propentofylline, a glial modulating agent, exhibits antiallodynic properties in a rat model of neuropathic pain. J. Pharmacol. Exp. Ther., 297, 1210-1217.
48. Terashvili, M., Wu, H., Leitermann, R.J., Sun, H., Clithero, A.D. & Tseng, L.F. (2005) Differential mechanisms of antianalgesia induced by endomorphin-1 and endomorphin-2 in the ventral periaqueductal gray of the rat. J. Pharmacol. Exp. Ther., 312, 1257-1265.
49. Tsan, M.F. & Gao, B. (2004) Cytokine function of heat shock proteins. Am. J. Physiol. Cell Physiol., 286, C739-C744.
50. Tsao, L.I. & Su, T.P. (1997) Naloxone-sensitive, haloperidol- sensitive, [3H](+)SKF-10047-binding protein partially purified from rat liver and rat brain membrane: an opioid/sigma receptor? Synapse, 25, 117-124.
51. Watkins, L.R., Maier, S.F. & Goehler, L.E. (1995) Immune activation: the role of pro-inflammatory cytokines in inflammation, illness responses and pathological pain states. Pain, 63, 289-302.
52. Watkins, L.R., Milligan, E.D. & Maier, S.F. (2001) Glial activation: a driving force for pathological pain. Trends Neurosci., 24, 450-455.
53. Wordliczek, J., Szczepanik, A.M., Banach, M., Turchan, J., Zembala, M., Siedlar, M., Przewlocki, R., Serednicki, W. & Przewlocka, B. (2000) The effect of pentoxifiline on post-injury hyperalgesia in rats and postoperative pain in patients. Life Sci., 66, 1155-1164.
54. Wu, H., Thompson, J., Sun, H., Leitermann, R.J., Fujimoto, J.M. & Tseng, L.F. (2004) Non-opioidergic mechanism mediating morphine-induced antianalgesia in the mouse spinal cord. J. Pharmacol. Exp. Ther., 310, 240-246.
55. Zhang, N. & Oppenheim, J.J. (2005) Crosstalk between chemokines and neuronal receptors bridges immune and nervous systems. J. Leukoc. Biol., 78, 1210-1214.