Altered spinal arachidonic acid turnover after peripheral nerve injury regulates regional glutamate concentration and neuropathic pain behaviors in rats

Pain

Volumn 131, Issue 1-2, 2007, Pages 121-131

  Sung, Backil ^a   Wang, Shuxing ^a   Zhou, Bei ^a   Lim, Grewo ^a   Yang, Liling ^a   Zeng, Qing ^a   Lim, Jeong Ae ^a   Wang, Jing Dong ^b   Kang, Jing X ^b   Mao, Jianren ^a  

^a Pain Research Group   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

Arachidonic acid; Gas chromatography; Glutamate transporter; Glutamate uptake; High pressure liquid chromatography; Microdialysis; Nerve injury; Neuropathic pain; Phospholipase A2

Indexed keywords

ARACHIDONIC ACID; CYCLOOXYGENASE 1 INHIBITOR; CYCLOOXYGENASE 2 INHIBITOR; DICLOFENAC; GLUTAMIC ACID;

ALLODYNIA; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISEASE EXACERBATION; DOSE RESPONSE; DRUG INHIBITION; GENE CONTROL; HOMEOSTASIS; HYPERALGESIA; IN VITRO STUDY; MALE; MICRODIALYSIS; NEUROPATHIC PAIN; NONHUMAN; PERIPHERAL NERVE INJURY; POSTOPERATIVE PERIOD; PRIORITY JOURNAL; PROTEIN METABOLISM; RAT; SPINAL ROOT;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; ARACHIDONIC ACID; BEHAVIOR, ANIMAL; GLUTAMIC ACID; HYPERALGESIA; MALE; METABOLIC CLEARANCE RATE; RATS; RATS, SPRAGUE-DAWLEY; SCIATIC NERVE; SPINAL CORD;

EID: 34547587094     PISSN: 03043959     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pain.2006.12.020     Document Type: Article

References (76)

1. al Ghoul W.M., Volsi G.L., Weinberg R.J., and Rustioni A. Glutamate immunocytochemistry in the dorsal horn after injury or stimulation of the sciatic nerve of rats. Brain Res Bull 30 (1993) 453-459
2. Azbill R.D., Mu X., and Springer J.E. Riluzole increases high-affinity glutamate uptake in rat spinal cord synaptosomes. Brain Res 871 (2000) 175-180
3. Bazan N.G. Eicosanoids, Platelet-Activating Factor and Inflammation. In: Siegel G.J., Fisher S.K., Albers W.R., Agranoff B.W., and Uhler M.D. (Eds). Basic Neurochem (1998), Williams & Wilkins, Lippincott
4. 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
5. Bidlingmeyer B.A., Cohen S.A., and Tarvin T.L. Rapid analysis of amino acids using pre-column derivatization. J Chromatogr 336 (1984) 93-104
6. Binns B.C., Huang Y., Goettl V.M., Hackshaw K.V., and Stephens Jr. R.L. Glutamate uptake is attenuated in spinal deep dorsal and ventral horn in the rat spinal nerve ligation model. Brain Res 1041 (2005) 38-47
7. Breukel A.I., Besselsen E., Lopes da Silva F.H., and Ghijsen W.E. Arachidonic acid inhibits uptake of amino acids and potentiates PKC effects on glutamate, but not GABA, exocytosis in isolated hippocampal nerve terminals. Brain Res 773 (1997) 90-97
8. Broom D.C., Samad T.A., Kohno T., Tegeder I., Geisslinger G., and Woolf C.J. Cyclooxygenase 2 expression in the spared nerve injury model of neuropathic pain. Neuroscience 124 (2004) 891-900
9. Chiechio S., Copani A., Melchiorri D., Canudas A.M., Storto M., Calvani M., et al. Metabotropic receptors as targets for drugs of potential use in the treatment of neuropathic pain. J Endocrinol Invest 27 (2004) 171-176
10. Danbolt N.C. Glutamate uptake. Prog Neurobiol 65 (2001) 1-105
11. De S., Trigueros M.A., Kalyvas A., and David S. Phospholipase A2 plays an important role in myelin breakdown and phagocytosis during Wallerian degeneration. Mol Cell Neurosci 24 (2003) 753-765
12. Devor M. Nerve pathophysiology and mechanisms of pain in causalgia. J Auton Nerv Syst 7 (1983) 371-384
13. Dorandeu F., Antier D., Pernot-Marino I., Lapeyre P., and Lallement G. Venom phospholipase A2-induced impairment of glutamate uptake: an indirect and nonselective effect related to phospholipid hydrolysis. J Neurosci Res 51 (1998) 349-359
14. Farooqui A.A., and Horrocks L.A. Brain phospholipases A2: a perspective on the history. Prostaglandins Leukot Essent Fatty Acids 71 (2004) 161-169
15. Farooqui A.A., Ong W.Y., and Horrocks L.A. Biochemical aspects of neurodegeneration in human brain: involvement of neural membrane phospholipids and phospholipases A2. Neurochem Res 29 (2004) 1961-1977
16. Gil A. Polyunsaturated fatty acids and inflammatory diseases. Biomed Pharmacother 56 (2002) 388-396
17. Hargreaves K., Dubner R., Brown F., Flores C., and Joris J. A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain 32 (1988) 77-88
18. Hefferan M.P., Carter P., Haley M., and Loomis C.W. Spinal nerve injury activates prostaglandin synthesis in the spinal cord that contributes to early maintenance of tactile allodynia. Pain 101 (2003) 139-147
19. Hefferan M.P., and Loomis C.W. Interaction of spinal nitric oxide and prostaglandins after L5-L6 spinal nerve ligation in the rat: an isobolographic analysis. Anesthesiology 100 (2004) 1611-1614
20. Hua X.Y., Chen P., Marsala M., and Yaksh T.L. Intrathecal substance P-induced thermal hyperalgesia and spinal release of prostaglandin E2 and amino acids. Neuroscience 89 (1999) 525-534
21. Kanai Y., and Hediger M.A. The glutamate and neutral amino acid transporter family: physiological and pharmacological implications. Eur J Pharmacol 479 (2003) 237-247
22. Katsuki H., and Okuda S. Arachidonic acid as a neurotoxic and neurotrophic substance. Prog Neurobiol 46 (1995) 607-636
23. Kawahara H., Sakamoto A., Takeda S., Onodera H., Imaki J., and Ogawa R. A prostaglandin E2 receptor subtype EP1 receptor antagonist (ONO-8711) reduces hyperalgesia, allodynia, and c-fos gene expression in rats with chronic nerve constriction. Anesth Analg 93 (2001) 1012-1017
24. Kirchheiner J., Meineke I., Steinbach N., Meisel C., Roots I., and Brockmoller J. Pharmacokinetics of diclofenac and inhibition of cyclooxygenases 1 and 2: no relationship to the CYP2C9 genetic polymorphism in humans. Br J Clin Pharmacol 55 (2003) 51-61
25. Kuwata H., Nakatani Y., Murakami M., and Kudo I. Cytosolic phospholipase A2 is required for cytokine-induced expression of type IIA secretory phospholipase A2 that mediates optimal cyclooxygenase-2-dependent delayed prostaglandin E2 generation in rat 3Y1 fibroblasts. J Biol Chem 273 (1998) 1733-1740
26. Lievens J.C., Bernal F., Forni C., Mahy N., and Kerkerian-Le Goff L. Characterization of striatal lesions produced by glutamate uptake alteration: cell death, reactive gliosis, and changes in GLT1 and GADD45 mRNA expression. Glia 29 (2000) 222-232
27. Lucas K.K., Svensson C.I., Hua X.Y., Yaksh T.L., and Dennis E.A. Spinal phospholipase A(2) in inflammatory hyperalgesia: role of Group IVA cPLA(2). Br J Pharmacol 144 (2005) 940-952
28. Ma W., Du W., and Eisenach J.C. Role for both spinal cord COX-1 and COX-2 in maintenance of mechanical hypersensitivity following peripheral nerve injury. Brain Res 937 (2002) 94-99
29. Mabuchi T., Kojima H., Abe T., Takagi K., Sakurai M., Ohmiya Y., et al. Membrane-associated prostaglandin E synthase-1 is required for neuropathic pain. Neuroreport 15 (2004) 1395-1398
30. Malmberg A.B., and Yaksh T.L. Hyperalgesia mediated by spinal glutamate or substance P receptor blocked by spinal cyclooxygenase inhibition. Science 257 (1992) 1276-1279
31. Manzoni C., and Mennini T. Arachidonic acid inhibits 3H-glutamate uptake with different potencies in rodent central nervous system regions expressing different transporter subtypes. Pharmacol Res 35 (1997) 149-151
32. Mao J., Price D.D., Hayes R.L., Lu J., and Mayer D.J. Differential roles of NMDA and non-NMDA receptor activation in induction and maintenance of thermal hyperalgesia in rats with painful peripheral mononeuropathy. Brain Res 598 (1992) 271-278
33. Mao J., Price D.D., Hayes R.L., Lu J., and Mayer D.J. Intrathecal GM1 ganglioside and local nerve anesthesia reduce nociceptive behaviors in rats with experimental peripheral mononeuropathy. Brain Res 584 (1992) 28-53
34. Mao J., Price D.D., and Mayer D.J. Mechanisms of hyperalgesia and morphine tolerance: a current view of their possible interactions. Pain 62 (1995) 259-274
35. Mao J., Price D.D., Zhu J., Lu J., and Mayer D.J. The inhibition of nitric oxide-activated poly(ADP-ribose) synthetase attenuates transsynaptic alteration of spinal cord dorsal horn neurons and neuropathic pain in the rat. Pain 72 (1997) 355-366
36. Maragakis N.J., and Rothstein J.D. Glutamate transporters: animal models to neurologic disease. Neurobiol Dis 15 (2004) 461-473
37. Minami T., Matsumura S., Okuda-Ashitaka E., Shimamoto K., Sakimura K., Mishina M., et al. Characterization of the glutamatergic system for induction and maintenance of allodynia. Brain Res 895 (2001) 178-185
38. Minami T., Nishihara I., Uda R., Ito S., Hyodo M., and Hayaishi O. Involvement of glutamate receptors in allodynia induced by prostaglandins E2 and F2 alpha injected into conscious mice. Pain 57 (1994) 225-231
39. Mitrovic A.D., Maddison J.E., and Johnston G.A. Influence of the oestrous cycle on L-glutamate and L-aspartate transport in rat brain synaptosomes. Neurochem Int 34 (1999) 101-108
40. Molnar-Perl I. Advances in the high-performance liquid chromatographic determination of phenylthiocarbamyl amino acids. Journal of Chromatography A 661 (1994) 43-50
41. Morioka N., Takeda K., Kumagai K., Hanada T., Ikoma K., Hide I., et al. Interleukin-1beta-induced substance P release from rat cultured primary afferent neurons driven by two phospholipase A2 enzymes: secretory type IIA and cytosolic type IV. J Neurochem 80 (2002) 989-997
42. Mu X., Azbill R.D., and Springer J.E. Riluzole improves measures of oxidative stress following traumatic spinal cord injury. Brain Res 870 (2000) 66-72
43. Muja N., and DeVries G.H. Prostaglandin E(2) and 6-keto-prostaglandin F(1alpha) production is elevated following traumatic injury to sciatic nerve. Glia 46 (2004) 116-129
44. Ohkubo K., Suzuki K., and Otorii T. [Pressor and depressor responses to intracerebroventricularly administered prostaglandins and arachidonic acid in anaesthetized rabbits]. Nippon Yakurigaku Zasshi 84 (1984) 327-335
45. Okuyama S., and Aihara H. Hyperalgesic action in rats of intracerebroventricularly administered arachidonic acid, PG E2 and PG F2 alpha: effects of analgesic drugs on hyperalgesia. Arch Int Pharmacodyn Ther 278 (1985) 13-22
46. Oomagari K., Buisson B., Dumuis A., Bockaert J., and Pin J.P. Effect of Glutamate and Ionomycin on the Release of Arachidonic Acid, Prostaglandins and HETEs from Cultured Neurons and Astrocytes. Eur J Neurosci 3 (1991) 928-939
47. Ossipov M.H., Lai J., Malan Jr. T.P., and Porreca F. Spinal and supraspinal mechanisms of neuropathic pain. Ann N Y Acad Sci 909 (2000) 12-24
48. Pinardi G., Sierralta F., and Miranda H.F. Atropine reverses the antinociception of nonsteroidal anti-inflammatory drugs in the tail-flick test of mice. Pharmacol Biochem Behav 74 3 (2003) 603-608
49. Pompeia C., Lima T., and Curi R. Arachidonic acid cytotoxicity: can arachidonic acid be a physiological mediator of cell death?. Cell Biochem Funct 21 (2003) 97-104
50. Pound E.M., Kang J.X., and Leaf A. Partitioning of polyunsaturated fatty acids, which prevent cardiac arrhythmias, into phospholipid cell membranes. J Lipid Res 42 (2001) 346-351
51. Raja S.N., Meyer R.A., and Campbell J.N. Peripheral mechanisms of somatic pain. Anesthesiology 68 (1988) 571-590
52. Robinson M.B., and Dowd L.A. Heterogeneity and functional properties of subtypes of sodium-dependent glutamate transporters in the mammalian central nervous system. Adv Pharmacol 37 (1997) 69-115
53. Rychkov G.Y., Litjens T., Roberts M.L., and Barritt G.J. Arachidonic acid inhibits the store-operated Ca2+ current in rat liver cells. Biochem J 385 (2005) 551-556
54. Samad T.A., Moore K.A., Sapirstein A., Billet S., Allchorne A., Poole S., et al. Interleukin-1beta-mediated induction of Cox-2 in the CNS contributes to inflammatory pain hypersensitivity. Nature 410 (2001) 471-475
55. Sawin P.D., Traynelis V.C., Rich G., Smith B.A., Maves T.J., Follett K.A., et al. Chymopapain-induced reduction of proinflammatory phospholipase A2 activity and amelioration of neuropathic behavioral changes in an in vivo model of acute sciatica. J Neurosurg 86 (1997) 998-1006
56. Schafers M., Marziniak M., Sorkin L.S., Yaksh T.L., and Sommer C. Cyclooxygenase inhibition in nerve-injury- and TNF-induced hyperalgesia in the rat. Exp Neurol 185 (2004) 160-168
57. Scholer D.W., Ku E.C., Boettcher I., and Schweizer A. Pharmacology of diclofenac sodium. Am J Med 80 (1986) 34-38
58. Semba J., and Wakuta M.S. Regional differences in the effects of glutamate uptake inhibitor L-trans-pyrrolidine-2,4-dicarboxylic acid on extracellular amino acids and dopamine in rat brain: an in vivo microdialysis study. Gen Pharmacol 31 (1998) 399-404
59. Sung B., Lim G., and 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 23 (2003) 2899-2910
60. Syriatowicz J.P., Hu D., Walker J.S., and Tracey D.J. Hyperalgesia due to nerve injury: role of prostaglandins. Neuroscience 94 (1999) 587-594
61. Tal M., and Bennett G.J. Extra-territorial pain in rats with a peripheral mononeuropathy: mechano-hyperalgesia and mechano-allodynia in the territory of an uninjured nerve. Pain 57 (1994) 375-382
62. Trotti D., Aoki M., Pasinelli P., Berger U.V., Danbolt N.C., Brown Jr. R.H., et al. Amyotrophic lateral sclerosis-linked glutamate transporter mutant has impaired glutamate clearance capacity. J Biol Chem 276 (2001) 576-582
63. Trotti D., Volterra A., Lehre K.P., Rossi D., Gjesdal O., Racagni G., et al. Arachidonic acid inhibits a purified and reconstituted glutamate transporter directly from the water phase and not via the phospholipid membrane. J Biol Chem 270 (1995) 9890-9895
64. Urban M.O., Hama A.T., Bradbury M., Anderson J., Varney M.A., and Bristow L. Role of metabotropic glutamate receptor subtype 5 (mGluR5) in the maintenance of cold hypersensitivity following a peripheral mononeuropathy in the rat. Neuropharmacology 44 (2003) 983-993
65. Volterra A., Trotti D., Cassutti P., Tromba C., Galimberti R., Lecchi P., et al. A role for the arachidonic acid cascade in fast synaptic modulation: ion channels and transmitter uptake systems as target proteins. Adv Exp Med Biol 318 (1992) 147-158
66. Volterra A., Trotti D., and Racagni G. Glutamate uptake is inhibited by arachidonic acid and oxygen radicals via two distinct and additive mechanisms. Mol Pharmacol 46 (1994) 986-992
67. Wall P.D., Waxman S., and Basbaum A.I. Ongoing activity in peripheral nerve: injury discharge. Exp Neurol 45 (1974) 576-589
68. White B.C., Sullivan J.M., DeGracia D.J., O'Neil B.J., Neumar R.W., Grossman L.I., et al. Brain ischemia and reperfusion: molecular mechanisms of neuronal injury. J Neurol Sci 179 (2000) 1-33
69. Woolf C.J., and Mannion R.J. Neuropathic pain: aetiology, symptoms, mechanisms, and management. Lancet 353 (1999) 1959-1964
70. Yaksh T.L., and Rudy T.A. Chronic catheterization of the spinal subarachnoid space. Physiol Behav 17 (1976) 1031-1036
71. Yamamoto T., and Yaksh T.L. Spinal pharmacology of thermal hyperesthesia induced by constriction injury of sciatic nerve Excitatory amino acid antagonists. Pain 49 (1992) 121-128
72. Yeo J.F., Ong W.Y., Ling S.F., and Farooqui A.A. Intracerebroventricular injection of phospholipases A2 inhibitors modulates allodynia after facial carrageenan injection in mice. Pain 112 (2004) 148-155
73. Yue H.Y., Fujita T., and Kumamoto E. Phospholipase A2 activation by melittin enhances spontaneous glutamatergic excitatory transmission in rat substantia gelatinosa neurons. Neuroscience 135 (2005) 485-495
74. Zerangue N., Arriza J.L., Amara S.G., and Kavanaugh M.P. Differential modulation of human glutamate transporter subtypes by arachidonic acid. J Biol Chem 270 (1995) 6433-6435
75. Zhu X., and Eisenach J.C. Cyclooxygenase-1 in the spinal cord is altered after peripheral nerve injury. Anesthesiology 99 (2003) 1175-1179
76. Zimmermann M. Pathobiology of neuropathic pain. Eur J Pharmacol 429 (2001) 23-37