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

Anesthesia and Analgesia

Volumn 113, Issue 6, 2011, Pages 1490-1500

  Yang, Chih Ping ^a,c   Cherng, Chen Hwan ^b   Wu, Ching Tang ^b   Huang, Hui Yi ^c   Tao, Pao Luh ^d   Wong, Chih Shung ^c,e  

^a TAOYUAN ARMED FORCES GENERAL HOSPITAL   (Taiwan)

^b TRI SERVICE GENERAL HOSPITAL   (Taiwan)

^c NATIONAL DEFENSE MEDICAL CENTER   (Taiwan)

^d NATIONAL HEALTH RESEARCH INSTITUTES   (Taiwan)

^e CATHAY GENERAL HOSPITAL   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARTIC ACID; EXCITATORY AMINO ACID; EXCITATORY AMINO ACID TRANSPORTER; GLUTAMATE TRANSPORTER; ISOFLURANE; MORPHINE; NALOXONE; VESICULAR GLUTAMATE TRANSPORTER 1;

ALLODYNIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINOCICEPTION; ARTICLE; ASTROCYTE; CEREBROSPINAL FLUID; CONTROLLED STUDY; DIALYSATE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HYPERALGESIA; IMMUNOHISTOCHEMISTRY; LOW DRUG DOSE; MALE; MICRODIALYSIS; NERVE TRANSECTION; NEUROPATHIC PAIN; NOCICEPTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SCIATIC NERVE; SPINAL CORD; SPINAL CORD DORSAL HORN; WESTERN BLOTTING;

ANALGESICS; ANALGESICS, OPIOID; ANIMALS; DRUG SYNERGISM; EXCITATORY AMINO ACIDS; INJECTIONS, SPINAL; MALE; MORPHINE; NALOXONE; PAIN MEASUREMENT; RATS; RATS, WISTAR; SCIATIC NEUROPATHY; SPINAL CORD; SYNAPSES;

EID: 82255179838     PISSN: 00032999     EISSN: None     Source Type: Journal    
DOI: 10.1213/ANE.0b013e31822d39c1     Document Type: Article

References (53)

1. Crain SM, Shen KF. 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 1995;92:10540-4
2. Tsai RY, Jang FL, Tai YH, Lin SL, Shen CH, Wong CS. Ultra-low-dose naloxone restores the antinociceptive effect of morphine and suppresses spinal neuroinflammation in PTXtreated rats. Neuropsychopharmacology 2008;33:2772-82
3. Sandkuhler J. Learning and memory in pain pathways. Pain 2000;88:113-8
4. Ji RR, Kohno T, Moore KA, Woolf CJ. Central sensitization and LTP: do pain and memory share similar mechanisms? Trends Neurosci 2003;26:696-705 (Pubitemid 37415022)
5. Yoshimura M, Jessell T. Amino acid-mediated EPSPs at primary afferent synapses with substantia gelatinosa neurones in the rat spinal cord. J Physiol 1990;430:315-35 (Pubitemid 20382826)
6. Randic M, Jiang MC, Cerne R. Long-term potentiation and long-term depression of primary afferent neurotransmission in the rat spinal cord. J Neurosci 1993;13:5228-41 (Pubitemid 24001008)
7. Danbolt NC. Glutamate uptake. Prog Neurobiol 2001;65:1-105 (Pubitemid 32479155)
8. Gegelashvili G, Robinson MB, Trotti D, Rauen T. Regulation of glutamate transporters in health and disease. Prog Brain Res 2001;132:267-86
9. Oliet SH, Piet R, Poulain DA. Control of glutamate clearance and synaptic efficacy by glial coverage of neurons. Science 2001;292:923-6 (Pubitemid 32422488)
10. Rothstein JD, Dykes-Hoberg M, Pardo CA, Bristol LA, Jin L, Kuncl RW, Kanai Y, Hediger MA, Wang Y, Schielke JP, Welty DF. Knockout of glutamate transporters reveals a major role for astroglial transport in excitotoxicity and clearance of glutamate. Neuron 1996;16:675-86 (Pubitemid 26103145)
11. Sung B, Lim G, Mao J. Altered expression and uptake activity of spinal glutamate transporters after nerve injury contribute to the pathogenesis of neuropathic pain in rats. J Neurosci 2003;23:2899-910 (Pubitemid 36418626)
12. Carver A, Foley K. Facts and an open mind should guide clinical practice. Curr Neurol Neurosci Rep 2001;1:97-8
13. Przewlocki R, Przewlocka B. Opioids in neuropathic pain. Curr Pharm Des 2005;11:3013-25 (Pubitemid 41158089)
14. Crain SM, Shen KF. Antagonists of excitatory opioid receptor functions enhance morphines analgesic potency and attenuate opioid tolerance/dependence liability. Pain 2000;84:121-31 (Pubitemid 30074213)
15. Ueda H, Fukushima N, Kitao T, Ge M, Takagi H. Low doses of naloxone produce analgesia in the mouse brain by blocking presynaptic autoinhibition of enkephalin release. Neurosci Lett 1986;65:247-52 (Pubitemid 16109646)
16. Mehlisch DR. The combination of low dose of naloxone and morphine in patient-controlled (PCA) does not decrease opioid requirements in the postoperative period. Pain 2003;101: 209-11
17. Cepeda MS, Alvarez H, Morales O, Carr DB. Addition of ultralow dose naloxone to postoperative morphine PCA: unchanged analgesia and opioid requirement but decreased incidence of opioid side effects. Pain 2004;107:41-6 (Pubitemid 38058697)
18. Sartain JB, Barry JJ, Richardson CA, Branagan HC. Effect of combining naloxone and morphine for intravenous patientcontrolled analgesia. Anesthesiology 2003;99:148-51 (Pubitemid 36799045)
19. Yaksh TL, Rudy TA. Chronic catheterization of the spinal subarachnoid space. Physiol Behav 1976;17:1031-6 (Pubitemid 8063691)
20. Tai YH, Wang YH, Tsai RY, Wang JJ, Tao PL, Liu TM, Wang YC, Wong CS. Amitriptyline preserves morphines antinociceptive effect by regulating the glutamate transporter GLAST and GLT-1 trafficking and excitatory amino acids concentration in morphine-tolerant rats. Pain 2007;129:343-54 (Pubitemid 46754573)
21. Tai YH, Wang YH, Wang JJ, Tao PL, Tung CS, Wong CS. Amitriptyline suppresses neuroinflammation and up-regulates glutamate transporters in morphine-tolerant rats. Pain 2006;124:77-86
22. Lindenlaub T, Sommer C. Partial sciatic nerve transection as a model of neuropathic pain: a qualitative and quantitative neuropathological study. Pain 2000;89:97-106
23. Lever I, Cunningham J, Grist J, Yip PK, Malcangio M. Release of BDNF and GABA in the dorsal horn of neuropathic rats. Eur J Neurosci 2003;18:1169-74 (Pubitemid 37115036)
24. Kalmar B, Greensmith L, Malcangio M, McMahon SB, Csermely P, Burnstock G. The effect of treatment with BRX- 220, a co-inducer of heat shock proteins, on sensory fibers of the rat following peripheral nerve injury. Exp Neurol 2003; 184:636-47 (Pubitemid 38182793)
25. Loeser JD, Treede RD. The Kyoto protocol of IASP basic pain terminology. Pain 2008;137:473-7
26. Wen ZH, Chang YC, Cherng CH, Wang JJ, Tao PL, Wong CS. Increasing of intrathecal CSF excitatory amino acids concentration following morphine challenge in morphine-tolerant rats. Brain Res 2004;995:253-9
27. Wen ZH, Wu GJ, Chang YC, Wang JJ, Wong CS. Dexamethasone modulates the development of morphine tolerance and expression of glutamate transporters in rats. Neuroscience 2005;133:807-17
28. Montiel T, Camacho A, Estrada-Sanchez A, Massieu L. Differential effects of the substrate inhibitor l-transpyrrolidine- 2,4-dicarboxylate (PDC) and the non-substrate inhibitor DL-threo-beta-benzyloxyaspartate (DL-TBOA) of glutamate transporters on neuronal damage and extracellular amino acid levels in rat brain in vivo. Neuroscience 2005;133:667-78 (Pubitemid 40798320)
29. Robinson I, Meert TF. Stability of neuropathic pain symptoms in partial sciatic nerve ligation in rats is affected by suture material. Neurosci Lett 2005;373:125-9 (Pubitemid 39572974)
30. Sommer C, Lindenlaub T, Teuteberg P, Schafers M, Hartung T, Toyka KV. Anti-TNF-neutralizing antibodies reduce painrelated behavior in two different mouse models of painful mononeuropathy. Brain Res 2001;913:86-9 (Pubitemid 32786935)
31. Mendell JR, Sahenk Z. Clinical practice: painful sensory neuropathy. N Engl J Med 2003;348:1243-55 (Pubitemid 36359301)
32. Ma W, Quirion R. 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 2002;99:175-84 (Pubitemid 35247540)
33. Back SK, Lee J, Hong SK, Na HS. Loss of spinal mu-opioid receptor is associated with mechanical allodynia in a rat model of peripheral neuropathy. Pain 2006;123:117-26 (Pubitemid 43816764)
34. Mao J, Sung B, Ji RR, Lim G. Chronic morphine induces downregulation of spinal glutamate transporters: implications in morphine tolerance and abnormal pain sensitivity. J Neurosci 2002;22:8312-23 (Pubitemid 35379137)
35. Zhu W, Pan ZZ. Mu-opioid-mediated inhibition of glutamate synaptic transmission in rat central amygdala neurons. Neuroscience 2005;133:97-103 (Pubitemid 40694161)
36. Zhang X, Bao L, Shi TJ, Ju G, Elde R, Hokfelt T. Downregulation of mu-opioid receptors in rat and monkey dorsal root ganglion neurons and spinal cord after peripheral axotomy. Neuroscience 1998;82:223-40
37. Porreca F, Tang QB, Bian D, Riedl M, Elde R, Lai J. Spinal opioid mu receptor expression in lumbar spinal cord of rats following nerve injury. Brain Res 1998;795:197-203 (Pubitemid 28337831)
38. Kohno T, Ji RR, Ito N, Allchorne AJ, Befort K, Karchewski LA, Woolf CJ. Peripheral axonal injury results in reduced mu opioid receptor pre- and post-synaptic action in the spinal cord. Pain 2005;117:77-87 (Pubitemid 41764774)
39. Swanson RA, Liu J, Miller JW, Rothstein JD, Farrell K, Stein BA, Longuemare MC. Neuronal regulation of glutamate transporter subtype expression in astrocytes. J Neurosci 1997; 17:932-40 (Pubitemid 27043952)
40. Sitcheran R, Gupta P, Fisher PB, Baldwin AS. Positive and negative regulation of EAAT2 by NF-kappaB: a role for N-myc in TNFalpha-controlled repression. EMBO J 2005;24:510-20 (Pubitemid 40343253)
41. Su ZZ, Leszczyniecka M, Kang DC, Sarkar D, Chao W, Volsky DJ, Fisher PB. Insights into glutamate transport regulation in human astrocytes: cloning of the promoter for excitatory amino acid transporter 2 (EAAT2). Proc Natl Acad Sci U S A 2003;100:1955-60 (Pubitemid 36254555)
42. Frizzo ME, Frizzo JK, Amadio S, Rodrigues JM, Perry ML, Bernardi G, Volonte C. Extracellular adenosine triphosphate induces glutamate transporter-1 expression in hippocampus. Hippocampus 2007;17:305-15 (Pubitemid 46649582)
43. Gegelashvili G, Dehnes Y, Danbolt NC, Schousboe A. The high-affinity glutamate transporters GLT1, GLAST, and EAAT4 are regulated via different signalling mechanisms. Neurochem Int 2000;37:163-70 (Pubitemid 30254148)
44. Belcheva MM, Clark AL, Haas PD, Serna JS, Hahn JW, Kiss A, Coscia CJ. Mu and kappa opioid receptors activate ERK/MAPK via different protein kinase C isoforms and secondary messengers in astrocytes. J Biol Chem 2005; 280:27662-9 (Pubitemid 41076879)
45. Zheng H, Loh HH, Law PY. Beta-arrestin-dependent mu-opioid receptor-activated extracellular signal-regulated kinases (ERKs) translocate to nucleus in contrast to G protein-dependent ERK activation. Mol Pharmacol 2008;73:178-90 (Pubitemid 350294209)
46. Verkhratsky A. Physiology and pathophysiology of the calcium store in the endoplasmic reticulum of neurons. Physiol Rev 2005;85:201-79 (Pubitemid 40173995)
47. Liu YP, Yang CS, Tzeng SF. Inhibitory regulation of glutamate aspartate transporter (GLAST) expression in astrocytes by cadmium-induced calcium influx. J Neurochem 2008;105: 137-50
48. Wang HY, Frankfurt M, Burns LH. High-affinity naloxone binding to filamin A prevents mu opioid receptor-Gs coupling underlying opioid tolerance and dependence. PLoS ONE 2008;3:e1554
49. Onoprishvili I, Andria ML, Kramer HK, Ancevska-Taneva N, Hiller JM, Simon EJ. Interaction between the mu opioid receptor and filamin A is involved in receptor regulation and trafficking. Mol Pharmacol 2003;64:1092-100 (Pubitemid 37310742)
50. Gintzler AR, Xu H. Different G proteins mediate the opioid inhibition or enhancement of evoked [5-methionine]enkephalin release. Proc Natl Acad Sci U S A 1991;88:4741-5 (Pubitemid 21914618)
51. Wang HY, Friedman E, Olmstead MC, Burns LH. Ultra-lowdose naloxone suppresses opioid tolerance, dependence and associated changes in mu opioid receptor-G protein coupling and Gbetagamma signaling. Neuroscience 2005;135:247-61 (Pubitemid 41219753)
52. Wang HY, Burns LH. Naloxones pentapeptide binding site on filamin A blocks mu opioid receptor-Gs coupling and CREB activation of acute morphine. PLoS ONE 2009;4:e4282
53. Gueler N, Kukley M, Dietrich D. TBOA-sensitive uptake limits glutamate penetration into brain slices to a few micrometers. Neurosci Lett 2007;419:269-72 (Pubitemid 46778882)