Spinal amino acid release and precipitated withdrawal in rats chronically infused with spinal morphine

Journal of Neuroscience

Volumn 16, Issue 8, 1996, Pages 2758-2766

  Jhamandas, K H ^b   Marsala, M ^a   Ibuki, T ^c   Yaksh, T L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b QUEEN S UNIVERSITY   (Canada)

^c KYOTO PREFECTURAL UNIVERSITY OF MEDICINE   (Japan)

Author keywords

AP 5; clonidine; MK 801; morphine; spinal; tolerance; withdrawal

Indexed keywords

2 AMINO 5 PHOSPHONOVALERIC ACID; CLONIDINE; DIZOCILPINE; GLUTAMATE RECEPTOR ANTAGONIST; GLUTAMIC ACID; MORPHINE; NALOXONE; TAURINE;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; INTRAPERITONEAL DRUG ADMINISTRATION; INTRATHECAL DRUG ADMINISTRATION; MALE; MICRODIALYSIS; MORPHINE ADDICTION; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; RAT; SPINAL CORD; WITHDRAWAL SYNDROME;

EID: 0029881933     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.16-08-02758.1996     Document Type: Article

References (68)

1. Aanonsen LM, Lei S, Wilcox GL (1990) Excitatory amino acid receptors and nociceptive acids in the somatosensory system. J Histochem Cytochem 38:1745-1754.
2. Advokat C, Burton P, Tyler CB (1987) Investigation of tolerance to chronic intrathecal morphine infusion in the rat. Physiol Behav 39:161-168.
3. Aghajanian GK (1978) Tolerance of locus coeruleus neurons to morphine and suppression of withdrawal response by clonidine. Nature 267:186-188.
4. Aghajanian GK, Kogan JH, Moghadam B (1994) Opiate withdrawal increases glutamate and aspartate efflux in the locus coeruleus: an in vivo microdialysis study. Brain Res 636:126-130.
5. Aimone LA, Yaksh TL (1989) Opioid modulation of capsaicin-evoked release of substance P from rat spinal cord in vivo. Peptides 10:1127-1131.
6. Akaoka H, Aston-Jones G (1991) Opiate withdrawal-induced hyperactivity of locus coeruleus neurons is substantially mediated by augmented excitatory amino acid input. J Neurosci 11:3830-3839.
7. Benson ChG, Chase MC, Potashner SJ (1991) Decreased release of D-aspartate in the guinea pig spinal cord after lesions of the red nucleus. J Neurochem 56:1174-1183.
8. Broman J, Anderson S, Ottersen OP (1993) Enrichment of glutamate-like immunoreactivity in primary afferent terminals throughout the spinal cord dorsal horn. Eur J Neurosci 5:1050-1061.
9. Chaplan SR, Pogrel J (1993) Pharmacologic modulation of tactile allodynia in a rat neuropathy model. Presented at the 7th World Congress on Pain (IASP) meeting, Paris.
10. Coderre TJ, Melzack R (1992) The contribution of excitatory amino acids to central sensitization and persistent nociception after formalin-induced tissue injury. J Neurosci 12:3665-3670.
11. Grain SM, Shen KF (1992) After chronic opioid exposure sensory neurons become supersensitive to the excitatory effects of opioid agonists and antagonists as occurs after acute elevation of GM1 ganglioside. Brain Res 575:13-24.
12. Cridland RA, Sutak M, Jhamandas K (1991) Characteristics of precipitated withdrawal from spinal morphine: changes in [Met5]enkephalin levels. Eur J Pharmacol 203:93-103.
13. DeBiasi S, Rustoni A (1990) Ultrastructural immunocytochemical localization of excitatory amino acids in the somatosensory system. J Histochem Cytochem 38:1745-1754.
14. Dunbar SA, Yaksh TL (1994) Intrathecal MK-801 attenuates intrathecal morphine tolerance and withdrawal in the rat (Abstr). Anesthesiology 81:838A.
15. Furuyama T, Kiyama H, Sato K, Park HT, Maeno H, Takagi H, Tohyama M (1993) Region-specific expression of subunits of ionotropic glutamate receptors (AMPA-type, KA-type and NMDA receptors) in the rat spinal cord with special reference to nociception. Mol Brain Res 18:141-51.
16. Go VLW, Yaksh TL (1987) Release of substance P from the cat spinal cord. J Physiol (Lond) 391:141-167.
17. Gold MS, Redmond DE, Kleber HD (1978) Clonidine in opiate withdrawal. Lancet II:599-602.
18. Higgins GA, Nguyen P, Sellers EM (1992) The NMDA antagonist dizolcipine (MK801) attenuates motivational as well as somatic aspects of naloxone precipitated opioid withdrawal. Life Sci 50:167-172.
19. Hong M, Milne B, Jhamandas K (1993) Evidence for the involvement of excitatory amino acid pathways in the development of precipitated withdrawal from acute and chronic morphine: an in vivo voltametric study in the rat locus coeruleus. Brain Res 623:131-141.
20. Ibuki T, Dunbar S, Yaksh TL (1995) Effect of transient antagonism on spinal morphine tolerance and spinal release of glutamate. Proc Soc Neurosci, in press.
21. Jhamandas K, Yaksh TL, Harty G, Szolcsanyi J, Go VLW (1984) Action of intrathecal capsaicin and its structural analogues on the content and release of spinal substance P: selectivity of action and relationship to analgesia. Brain Res 306:215-225.
22. Kamisaki Y, Hamada T, Maeda K, Ishimura M, Itoh T (1993a) Presynaptic α2 adrenoceptors inhibit glutamate release from rat spinal cord synaptosomes. J Neurochem 60:522-526.
23. Kamisaki Y, Maeda K, Ishimura M, Omura H, Itoh T (1993b) Effects of taurine on depolarization-evoked release of amino acids from rat cortical synaptosomes. Brain Res 627:181-185.
24. Kreeger JS, Yukhananov RY, Larson AA (1994) Increased N-methyl-D-aspartate (NMDA) activity in the mouse spinal cord following morphine does not mediate opioid withdrawal. Brain Res 663:101-106.
25. Lehman A, Hagberg H, Hamberger A (1984) A role for taurine in the maintenance of homeostasis in the central nervous system during hyperexcitation. Neurosci Lett 52:341-346.
26. Liu H, Wang H, Sheng M, Jan LY, Jan YN, Basbaum AI (1994) Evidence for presynaptic N-methyl-D-aspartate autoreceptors in the spinal cord dorsal horn. Proc Natl Acad Sci USA 91:8383-8387.
27. Malmberg AB, Yaksh TL (1992) Hyperalgesia mediated by spinal glutamate or substance P receptor blocked by spinal cyclooxygenase inhibition. Science 257:1276-1279.
28. Malmberg AB, Yaksh TL (1995) The effect of morphine on formalin-evoked behaviour and spinal release of excitatory amino acids and prostaglandin E2 using microdialysis in conscious rats. Br J Pharmacol 114:1069-1075.
29. Mao J, Price DD, Mayer DJ (1994) Thermal hyperalgesia in association with development of morphine tolerance in rats: role of excitatory amino acid receptors and protein kinase. J Neurosci 14:2301-2312.
30. Marsala M, Malmberg AB, Yaksh TL (1995a) The spinal loop dialysis catheter: characterization of use in the unanesthetized rat. J Neurosci Methods 62:43-53.
31. Marsala M, Yang LCh Yaksh TL (1995b) Chronic intrathecal infusion of NMDA evokes secondary excitatory amino acid release and progressive degeneration in spinal cord neurons: a spinal microdialysis study in awake animals. Soc Neurosci Abstr 21:242.
32. Merighi A, Polak JM, Theodosis DT (1991) Ultrastructural visualization of glutamate and aspartate immunoreactivity in the rat dorsal horn, with special reference to co-localization of glutamate, substance P and calcitonin-gene related peptide. Neuroscience 40:67-80.
33. Milne B, Cervenko FW, Jhamandas K, Sutak M (1985) Intrathecal clonidine: analgesia and effect on opiate withdrawal in the rat. Anesthesiology 62:34-38.
34. Paleckova V, Palecek J, McAdoo DJ, Willis WD (1992) The non-NMDA antagonist CNQX prevents release of amino acids into the rat spinal cord dorsal horn evoked by sciatic nerve stimulation. Neurosci Lett 148:19-22.
35. Potashner SJ, Dymczyk L (1986) Amino acid levels in the guinea pig spinal gray matter after axotomy of primary sensory and descending tracts. J Neurochem 47:412-422.
36. Rasmussen K, Beitner-Johnson D, Krystal JH, Aghajanian GK, Nestler EJ (1990) Opiate withdrawal and the rat locus coeruleus: behavioral, electrophysiological, and biochemical correlates. J Neurosci 10:2308-2317.
37. Rasmussen K, Fuller RW, Stockton ME, Perry KW, Swinford RM, Ornstein PL (1991) NMDA receptor antagonists suppress behaviours but not norepinephrine turnover or locus coeruleus unit activity induced by opiate withdrawal. Eur J Pharmacol 197:9-16.
38. Russell RD, Leslie JB, Su YF, Watkins WD, Chang KJ (1987) Continuous intrathecal opioid analgesia: tolerance and cross-tolerance of mu and delta spinal opioid receptors. J Pharmacol Exp Ther 240:150-158.
39. Sanghvi R, Yaksh TL (1994) Spinal amino acid release evoked by paw formalin in unanesthetized and halothane anesthetized rats (Abstr). Anesthesiology 81:836A.
40. Schneider SP, Fyffe RE (1992) Involvement of GABA and glycine in recurrent inhibition of spinal motoneurons. J Neurophysiol 68:397-406.
41. Shen KF, Crain SM (1992) Chronic selective activation of excitatory opioid receptor functions in sensory neurons results in opioid "dependence" without tolerance. Brain Res 597:74-83.
42. Shen KF, Crain SM (1994) 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 636:286-297.
43. Smullin DH, Skilling SR, Larson AA (1990) Interactions between substance P, calcitonin gene-related peptide, taurine and excitatory amino acids in the spinal cord. Pain 42:93-101.
44. Sorkin LS (1993) NMDA evokes an L-NAME sensitive spinal release of glutamate and citrulline. NeuroReport 4:479-482.
45. Sosnowski M, Yaksh TL (1990) Differential cross-tolerance between intrathecal morphine and sufentanil in the rat. Anesthesiology 73:1141-1147.
46. Stevens CW, Yaksh TL (1989a) Time course characteristics of tolerance development to continuously infused antinociceptive agents in rat spinal cord. J Pharmacol Exp Ther 251:216-223.
47. Stevens CW, Yaksh TL (1989b) Magnitude of opioid dependence after continuous intrathecal infusion of μ- and δ-selective opioids in the rat. Eur J Pharmacol 166:467-472.
48. Stevens CW, Yaksh TL (1989c) Potency of infused spinal antinociceptive agents is inversely related to magnitude of tolerance after continuous infusion. J Pharmacol Exp Ther 250:1-8.
49. Stevens CW, Yaksh TL (1992) Studies of morphine and D-ala2-D-leu5-enkephalin (DADLE) cross-tolerance after continuous intrathecal infusion in the rat. Anesthesiology 76:596-603.
50. Takano Y, Yaksh TL (1992) Characterization of the pharmacology of intrathecally administered alpha-2 agonists and antagonists in rats. J Pharmacol Exp Ther 261:764-772.
51. Tanganelli S, Antenolli T, Moriori M, Bianchi C, Beani L (1991) Glutamate antagonists prevent morphine withdrawal in mice and guinea pigs. Neurosci Lett 122:270-272.
52. Todd AJ, Sullivan AC (1990) Light microscope study of the coexistence of GABA-like and glycine-like immunoreactivities in the spinal cord of the rat. J Comp Neurol 296:496-505.
53. Tracey DJ, Debiasi S, Phend K, Rustioni A (1991) Aspartate-like immunoreactivity in primary afferent neurons. Neuroscience 40:673-686.
54. Trujillo K, Akil H (1991) Inhibition of morphine tolerance and dependence by the NMDA receptor antagonist MK-801. Science 251:85-87.
55. Tyce GM, Yaksh TL (1981) Monoamine release from cat spinal cord by somatic stimuli: an intrinsic modulatory system. J Physiol (Lond) 314:513-529.
56. Yaksh TL (1993a) The spinal actions of opioids. In: Handbook of experimental pharmacology. Vol. 104 (Herz A, ed), pp 53-90. Berlin: Springer.
57. Yaksh TL (1993b) The spinal pharmacology of facilitation of afferent processing evoked by high threshold afferent input of the postinjury pain state. Curr Opin Neurol Neurosurg 6:250-256.
58. Yaksh TL, Elde RP (1980) Release of methionine-enkephalin immunoreactivity from the rat spinal cord in vivo. Eur J Pharmacol 63:359-362.
59. Yaksh TL, Elde RP (1981) Factors governing release of methionine enkephalin-like immunoreactivity from mesencephalon and spinal cord of the cat in vivo. J Neurophysiol 46:1056-1075.
60. Yaksh TL, Stevens CW (1986) Simple catheter preparation for permitting bolus intrathecal administration during chronic intrathecal infusion. Pharmacol Biochem Behav 25:483-485.
61. Yaksh TL, Kohl RL, Rudy TL (1977) Induction of tolerance and withdrawal in rats receiving morphine in the spinal subarachnoid space. Eur J Pharmacol 42:275-284.
62. Yaksh TL, Abay EO, Go VLW (1982a) Studies on the location and release of cholecystokinin and vasoactive intestinal peptide in rat and cat spinal cord. Brain Res 242:279-290.
63. Yaksh TL, Schmauss C, Micevych PE, Abay EO, Go VLW (1982b) Pharmacological studies on the application, disposition and release of neurotensin in the spinal cord. Ann NY Acad Sci 400:228-243.
64. Yaksh TL, Jage J, Takano Y (1993) Pharmacokinetics and pharmacodynamics of medullar agents. III. The spinal actions of alpha 2-adrenergic agonists as analgesic. In: Bailliere's clinical anesthesiology, Vol 7, No 3 (Aitkenhead AR, Benad G, Brown BR, Cousins MJ, Jones JG, Strunin L, Thomson D, Van Aken H, eds), pp 597-614. London: Bailliere Tindall.
65. Yaksh TL, Pogrel JW, Lee YW, Chaplan SR (1995) Reversal of nerve ligation-induced allodynia by spinal alpha-2 adrenoreceptor agonists. J Pharmacol Exp Ther 272:207-214.
66. Yamamoto T, Yaksh TL (1992a) Comparison of the antinociceptive effects of pre- and posttreatment with intrathecal morphine and MK801, an NMDA antagonist, on the formalin test in the rat. Anesthesiology 77:757-763.
67. Yamamoto T, Yaksh TL (1992b) Spinal pharmacology of thermal hyperesthesia induced by constriction injury of sciatic nerve: excitatory amino acid antagonists. Pain 49:121-128.
68. Yang LCH, Marsala M, Yaksh TL (1995) Knee joint inflammation: a potential role of spinal PGE2 and NO release in hypersensitivity state (Abstr). Anesthesiology 83:794A.