Ultra-low dose naloxone restores the antinocicepitve effect of morphine in PTX-treated rats: Association of IL-10 upregulation in the spinal cord

Life Sciences

Volumn 91, Issue 5-6, 2012, Pages 213-220

  Lin, Yaoh Shiang ^a   Tsai, Ru Yin ^b   Shen, Ching Hui ^c   Chien, Chih Cheng ^b   Tsai, Wei Yuan ^d   Guo, Shu Lin ^b   Wong, Chih Shung ^a,b,d  

^a TRI SERVICE GENERAL HOSPITAL   (Taiwan)

^b CATHAY GENERAL HOSPITAL   (Taiwan)

^c TAICHUNG VETERANS GENERAL HOSPITAL   (Taiwan)

^d NATIONAL DEFENSE MEDICAL CENTER   (Taiwan)

Author keywords

Antinociceptive; Cytokine; Neuroinflammation; Neuropathic; Opioid

Indexed keywords

INTERLEUKIN 1BETA; INTERLEUKIN 6; MORPHINE; NALOXONE; PERTUSSIS TOXIN; RECOMBINANT INTERLEUKIN 10; SYNAPTOPHYSIN;

ALLODYNIA; ANALGESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DRUG ACTIVITY; DRUG EFFECT; DRUG POTENTIATION; HYPERALGESIA; LOW DRUG DOSE; MALE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; SPINAL CORD; UPREGULATION;

ANALGESICS, OPIOID; ANIMALS; ANTIBODIES; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG THERAPY, COMBINATION; INFLAMMATION; INTERLEUKIN-10; MALE; MICE; MICROGLIA; MORPHINE; NALOXONE; NARCOTIC ANTAGONISTS; NEURONS; PAIN; PERTUSSIS TOXIN; RANDOM ALLOCATION; RATS; RATS, WISTAR; RECOMBINANT PROTEINS; SPINAL CORD; UP-REGULATION;

RATTUS; RATTUS NORVEGICUS;

EID: 84865230699     PISSN: 00243205     EISSN: 18790631     Source Type: Journal    
DOI: 10.1016/j.lfs.2012.07.005     Document Type: Article

References (43)

1. I. Bettoni, F. Comelli, C. Rossini, F. Granucci, G. Giagnoni, and F. Peri Glial TLR4 receptor as new target to treat neuropathic pain: efficacy of a new receptor antagonist in a model of peripheral nerve injury in mice Glia 56 2008 1312 1319
2. R.K. Bhairavabhotla, V. Verm, H. Tongaonkar, S. Shastri, K. Dinshaw, and S. Chiplunkar Role of IL-10 in immune suppression in cervical cancer Indian J Biochem Biophys 44 2007 350 356
3. J.N. Campbell, and R.A. Meyer Mechanisms of neuropathic pain Neuron 52 2006 77 92
4. Y. Dai, K. Iwata, T. Fukuoka, E. Kondo, A. Tokunaga, and H. Yamanaka Phosphorylation of extracellular signal-regulated kinase in primary afferent neurons by noxious stimuli and its involvement in peripheral sensitization J Neurosci 22 2002 7737 7745
5. J. Garnacho-Montero, T. Aldabo-Pallas, C. Garnacho-Montero, A. Cayuela, R. Jimenez, and S. Barroso Timing of adequate antibiotic therapy is a greater determinant of outcome than are TNF and IL-10 polymorphisms in patients with sepsis Crit Care 10 2006 R111
6. K.M. Greeneltch, C.C. Haudenschild, A.D. Keegan, and Y. Shi The opioid antagonist naltrexone blocks acute endotoxic shock by inhibiting tumor necrosis factor-alpha production Brain Behav Immun 18 2004 476 484
7. M.L. Grossman, A.I. Basbaum, and H.L. Fields 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
8. B. Hassel, R.E. Paulsen, A. Johnsen, and F. Fonnum Selective inhibition of glial cell metabolism in vivo by fluorocitrate Brain Res 576 1992 120 124
9. M. Howard, and A. O'Garra Biological properties of interleukin 10 Immunol Today 13 1992 198 200
10. R.R. Ji, and M.R. Suter p38 MAPK, microglial signaling, and neuropathic pain Mol Pain 3 2007 33 42
11. S.X. Jin, Z.Y. Zhuang, C.J. Woolf, and R.R. Ji p38 mitogen-activated protein kinase is activated after a spinal nerve ligation in spinal cord microglia and dorsal root ganglion neurons and contributes to the generation of neuropathic pain J Neurosci 23 2003 4017 4022
12. A.C. Johansson, A.S. Hansson, K.S. Nandakumar, J. Backlund, and R. Holmdahl IL-10-deficient B10.Q mice develop more severe collagen-induced arthritis, but are protected from arthritis induced with anti-type II collagen antibodies J Immunol 167 2001 3505 3512
13. S.A. Kanaan, S. Poole, N.E. Saade, S. Jabbur, and B. Safieh-Garabedian Interleukin-10 reduces the endotoxin-induced hyperalgesia in mice J Neuroimmunol 86 1998 142 150
14. T. Kasama, R.M. Strieter, N.W. Lukacs, P.M. Lincoln, M.D. Burdick, and S.L. Kunkel Interleukin-10 expression and chemokine regulation during the evolution of murine type II collagen-induced arthritis J Clin Invest 95 1995 2868 2876
15. T. Kohno, R.R. Ji, N. Ito, A.J. Allchorne, K. Befort, and L.A. Karchewski Peripheral axonal injury results in reduced mu opioid receptor pre- and post-synaptic action in the spinal cord Pain 117 2005 77 87
16. S.L. Liao, W.Y. Chen, S.L. Raung, and C.J. Chen Neuroprotection of naloxone against ischemic injury in rats: role of mu receptor antagonism Neurosci Lett 345 2003 169 172
17. S.L. Lin, Y.M. Lee, H.Y. Chang, Y.W. Cheng, and M.H. Yen Effects of naltrexone on lipopolysaccharide-induced sepsis in rats J Biomed Sci 12 2005 431 440
18. S.L. Lin, R.Y. Tsai, Y.H. Tai, C.H. Cherng, C.T. Wu, and C.C. Yeh Ultra-low dose naloxone upregulates interleukin-10 expression and suppresses neuroinflammation in morphine-tolerant rat spinal cords Behav Brain Res 207 2010 30 36
19. B. Liu, and J.S. Hong Role of microglia in inflammation-mediated neurodegenerative diseases: mechanisms and strategies for therapeutic intervention J Pharmacol Exp Ther 304 2003 1 7
20. Y. Liu, L. Qin, B.C. Wilson, L. An, J.S. Hong, and B. Liu Inhibition by naloxone stereoisomers of beta-amyloid peptide (1-42)-induced superoxide production in microglia and degeneration of cortical and mesencephalic neurons J Pharmacol Exp Ther 302 2002 1212 1219
21. A. Loizzo, S. Loizzo, L. Lopez, A. d'Amore, P. Renzi, and S. Spampinato Naloxone prevents cell-mediated immune alterations in adult mice following repeated mild stress in the neonatal period Br J Pharmacol 135 2002 1219 1226
22. W. Ma, and R. Quirion Partial sciatic nerve ligation induces increase in the phosphorylation of extracellular signal-regulated kinase (ERK) and c-Jun N-terminal kinase (JNK) in astrocytes in the lumbar spinal dorsal horn and the gracile nucleus Pain 99 2002 175 184
23. K. McCormack, P. Prather, and C. Chapleo Some new insights into the effects of opioids in phasic and tonic nociceptive tests Pain 78 1998 79 98
24. E.D. Milligan, S.J. Langer, E.M. Sloane, L. He, J. Wieseler-Frank, and K. O'Connor Controlling pathological pain by adenovirally driven spinal production of the anti-inflammatory cytokine, interleukin-10 Eur J Neurosci 21 2005 2136 2148
25. E.D. Milligan, R.G. Soderquist, S.M. Malone, J.H. Mahoney, T.S. Hughes, and S.J. Langer Intrathecal polymer-based interleukin-10 gene delivery for neuropathic pain Neuron Glia Biol 2 2006 293 308
26. K.J. Powell, N.S. Abul-Husn, A. Jhamandas, M.C. Olmstead, R.J. Beninger, and K. Jhamandas Paradoxical effects of the opioid antagonist naltrexone on morphine analgesia, tolerance, and reward in rats J Pharmacol Exp Ther 300 2002 588 596
27. V. Raghavendra, M.D. Rutkowski, and J.A. DeLeo The role of spinal neuroimmune activation in morphine tolerance/hyperalgesia in neuropathic and sham-operated rats J Neurosci 22 2002 9980 9989
28. V. Raghavendra, F. Tanga, and J.A. DeLeo 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
29. J. Schouenborg, H.R. Weng, J. Kalliomaki, and H. Holmberg A survey of spinal dorsal horn neurones encoding the spatial organization of withdrawal reflexes in the rat Exp Brain Res 106 1995 19 27
30. S. Shah, A. Duttaroy, T. Davis, and B.C. Yoburn Spinal and supraspinal effects of pertussis toxin on opioid analgesia Pharmacol Biochem Behav 49 1994 773 776
31. C.S. Sung, Z.H. Wen, W.K. Chang, K.H. Chan, S.T. Ho, and S.K. Tsai Inhibition of p38 mitogen-activated protein kinase attenuates interleukin-1beta-induced thermal hyperalgesia and inducible nitric oxide synthase expression in the spinal cord J Neurochem 94 2005 742 752
32. Y.H. Tai, Y.H. Wang, R.Y. Tsai, J.J. Wang, P.L. Tao, and T.M. Liu Amitriptyline preserves morphine's antinociceptive effect by regulating the glutamate transporter GLAST and GLT-1 trafficking and excitatory amino acids concentration in morphine-tolerant rats Pain 129 2007 343 354
33. R.Y. Tsai, F.L. Jang, Y.H. Tai, S.L. Lin, C.H. Shen, and C.S. Wong Ultra-low-dose naloxone restores the antinociceptive effect of morphine and suppresses spinal neuroinflammation in PTX-treated rats Neuropsychopharmacology 33 2008 2772 2782
34. R.Y. Tsai, Y.H. Tai, J.I. Tzeng, C.H. Cherng, C.C. Yeh, and C.S. Wong Ultra-low dose naloxone restores the antinociceptive effect of morphine in pertussis toxin-treated rats by reversing the coupling of mu-opioid receptors from Gs-protein to coupling to Gi-protein Neuroscience 164 2009 435 443
35. R.Y. Tsai, Y.H. Tai, J.I. Tzeng, S.L. Lin, C.H. Shen, and C.P. Yang 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
36. M. Tsuda, A. Mizokoshi, Y. Shigemoto-Mogami, S. Koizumi, and K. Inoue Activation of p38 mitogen-activated protein kinase in spinal hyperactive microglia contributes to pain hypersensitivity following peripheral nerve injury Glia 45 2004 89 95
37. B. van den Blink, N.P. Juffermans, T. ten Hove, M.J. Schultz, S.J. van Deventer, and T. van der Poll p38 mitogen-activated protein kinase inhibition increases cytokine release by macrophages in vitro and during infection in vivo J Immunol 166 2001 582 587
38. L.R. Watkins, E.D. Milligan, and S.F. Maier Glial proinflammatory cytokines mediate exaggerated pain states: implications for clinical pain Adv Exp Med Biol 521 2003 1 21
39. L.R. Watkins, M.R. Hutchinson, A. Ledeboer, J. Wieseler-Frank, E.D. Milligan, and S.F. Maier Norman Cousins Lecture. Glia as the "bad guys": implications for improving clinical pain control and the clinical utility of opioids Brain Behav Immun 21 2007 131 146
40. D.E. Womer, and H.E. Shannon Pharmacologic reversal of pertussis toxin-induced thermal allodynia in mice Neuropharmacology 39 2000 1732 1739
41. D.E. Womer, N.W. DeLapp, and H.E. Shannon Intrathecal pertussis toxin produces hyperalgesia and allodynia in mice Pain 70 1997 223 228
42. C.P. Yang, C.H. Cherng, C.T. Wu, H.Y. Huang, P.L. Tao, and C.S. Wong Intrathecal ultra-low dose naloxone enhances the antinociceptive effect of morphine by enhancing the reuptake of excitatory amino acids from the synaptic cleft in the spinal cord of partial sciatic nerve-transected rats Anesth Analg 113 2011 1490 1500
43. C. Zhang, R.A. Baumgartner, K. Yamada, and M.A. Beaven Mitogen-activated protein (MAP) kinase regulates production of tumor necrosis factor-alpha and release of arachidonic acid in mast cells. Indications of communication between p38 and p42 MAP kinases J Biol Chem 272 1997 13397 13402