Effects of GCP-II inhibition on responses of dorsal horn neurones after inflammation and neuropathy: An electrophysiological study in the rat

Neuropeptides

Volumn 37, Issue 5, 2003, Pages 298-306

  Carpenter, Katherine J ^a   Sen, Sayen ^a   Matthews, Elizabeth A ^a   Flatters, Sarah L ^a   Wozniak, Krystyna M ^b   Slusher, Barbara S ^b   Dickenson, Anthony H ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b GUILFORD PHARMACEUTICALS INC   (United States)

Author keywords

Dorsal horn; GCP II; Inflammation; Metabotropic glutamate receptor; NAAG; NAALADase; Neuropathy; Nociception

Indexed keywords

2 (PHOSPHONOMETHYL)PENTANEDIOIC ACID; CARRAGEENAN; GAMMA GLUTAMYL HYDROLASE; N ACETYLASPARTYLGLUTAMIC ACID; UNCLASSIFIED DRUG; VALERIC ACID DERIVATIVE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTROPHYSIOLOGY; EVOKED CORTICAL RESPONSE; INFLAMMATION; LOW DRUG DOSE; MALE; NERVE ENDING; NERVE LIGATION; NEUROPATHY; NOCICEPTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SENSORY NERVE; SPINAL CORD DORSAL HORN; SPINAL NERVE; SYNAPTIC TRANSMISSION; UPREGULATION;

ANIMALIA;

EID: 0344441376     PISSN: 01434179     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.npep.2003.08.001     Document Type: Article

References (42)

1. Azkue, J.J., Mateos, J.M., Elezgarai, I., Benitez, R., Osorio, A., Diez, J., Bilbao, A., Bidaurrazaga, A., Grandes, P., 2000. The metabotropic glutamate receptor subtype mGluR 2/3 is located at extrasynaptic loci in rat spinal dorsal horn synapses. Neurosci. Lett. 287, 236-238.
2. Berthele, A., Boxall, S.J., Urban, A., Anneser, J.M., Zieglgansberger, W., Urban, L., Tolle, T.R., 1999. Distribution and developmental changes in metabotropic glutamate receptor messenger RNA expression in the rat lumbar spinal cord. Brain Res. Dev. Brain Res. 112, 39-53.
3. Boxall, S., Berthele, A., Laurie, D., Sommer, B., Zieglgansberger, W., Urban, L., Tolle, T., 1998. Enhanced expression of metabotropic glutamate receptor 3 messenger RNA in the rat spinal cord during ultraviolet irradiation induced peripheral inflammation. Neuroscience 82, 591-602.
4. Bruno, V., Wroblewska, B., Wroblewski, J.T., Fiore, L., Nicoletti, F., 1998. Neuroprotective activity of N-acetylaspartylglutamate in cultured cortical cells. Neuroscience 85, 751-757.
5. Cai, Z., Lin, S., Rhodes, P.G., 2002. Neuroprotective effects of N-acetylaspartylglutamate in a neonatal rat model of hypoxia-ischemia. Eur. J. Pharmacol. 437, 139-145.
6. Cangro, C.B., Namboodiri, M.A., Sklar, L.A., Corigliano Murphy, A., Neale, J.H., 1987. Immunohistochemistry and biosynthesis of N- acetylaspartylglutamate in spinal sensory ganglia. J. Neurochem. 49, 1579-1588.
7. Cassidy, M., Neale, J.H., 1993. N-Acetylaspartylglutamate catabolism is achieved by an enzyme on the cell surface of neurons and glia. Neuropeptides 24, 271-278.
8. Chaplan, S.R., Malmberg, A.B., Yaksh, T.L., 1997. Efficacy of spinal NMDA receptor antagonism in formalin hyperalgesia and nerve injury evoked allodynia in the rat. J. Pharmacol. Exp. Ther. 280, 829-838.
9. Chen, S.R., Wozniak, K.M., Slusher, B.S., Pan, H.L., 2002. Effect of 2-(phosphono-methyl)-pentanedioic acid on allodynia and afferent ectopic discharges in a rat model of neuropathic pain. J. Pharmacol. Exp. Ther. 300, 662-667.
10. Davies, S.N., Lodge, D., 1987. Evidence for involvement of N-methyl-D-aspartate receptors in 'wind-up' of class 2 neurones in the dorsal horn of the rat. Brain Res. 424, 402-406.
11. Dickenson, A.H., Sullivan, A.F., 1987. Evidence for a role of the NMDA receptor in the frequency dependent potentiation of deep rat dorsal horn nociceptive neurones following C fibre stimulation. Neuropharmacology 26, 1235-1238.
12. Dolan, S., Nolan, A.M., 2000. Behavioural evidence supporting a differential role for group I and II metabotropic glutamate receptors in spinal nociceptive transmission. Neuropharmacology 39, 1132-1138.
13. Fuhrman, S., Palkovits, M., Cassidy, M., Neale, J.H., 1994. The regional distribution of N-acetylaspartylglutamate (NAAG) and peptidase activity against NAAG in the rat nervous system. J. Neurochem. 62, 275-281.
14. Jackson, P.F., Cole, D.C, Slusher, B.S., Stetz, S.L., Ross, L.E., Donzanti, B.A., Trainor, D.A., 1996. Design, synthesis, and biological activity of a potent inhibitor of the neuropeptidase N-acetylated-alpha-linked acidic dipeptidase. J. Med. Chem. 39, 619-622.
15. Jia, H., Rustioni, A., Valtschanoff, J.G., 1999. Metabotropic glutamate receptors in superficial laminae of the rat dorsal horn. J. Comp. Neurol. 410, 627-642.
16. Kim, S.H., Chung, J.M., 1992. An experimental model for peripheral neuropathy produced by segmental spinal nerve ligation in the rat. Pain 50, 355-363.
17. Knoflach, F., Woltering, T., Adam, G., Mutel, V., Kemp, J.A., 2001. Pharmacological properties of native metabotropic glutamate receptors in freshly dissociated Golgi cells of the rat cerebellum. Neuropharmacology 40, 163-169.
18. Ohishi, H., Shigemoto, R., Nakanishi, S., Mizuno, N., 1993a. Distribution of the messenger RNA for a metabotropic glutamate receptor, mGlu receptor 2, in the central nervous system of the rat. Neuroscience 53, 1009-1018.
19. Ohishi, H., Shigemoto, R., Nakanishi, S., Mizuno, N., 1993b. Distribution of the mRNA for a metabotropic glutamate receptor (mGluR3) in the rat brain: an in situ hybridization study. J. Comp. Neurol. 335, 252-266.
20. Ottersen, O., Landsend, A., 1997. Organization of glutamate receptors at the synapse. Eur. J. Neurosci. 9, 2219-2224.
21. Petralia, R.S., Wang, Y.X., Niedzielski, A.S., Wenthold, R.J., 1996. The metabotropic glutamate receptors, mGluR2 and mGluR3, show unique postsynaptic, presynaptic and glial localizations. Neuroscience 71, 949-976.
22. 3H]norepinephrine release from rat hippocampal slices. J. Pharmacol. Exp. Ther. 266, 796-803.
23. Scanziani, M., Salin, P.A., Vogt, K.E., Malenka, R.C., Nicoll, R.A., 1997. Use dependent increases in glutamate concentration activate presynaptic metabotropic glutamate receptors. Nature 385, 630-634.
24. Sekiguchi, M., Okamoto, K., Sakai, Y., 1989. Low concentration N-acetylaspartylglutamate suppresses the climbing fiber response of Purkinje cells in guinea pig cerebellar slices and the responses to excitatory amino acids of Xenopus laevis oocytes injected with cerebellar mRNA. Brain Res. 482, 87-96.
25. Sekiguchi, M., Wada, K., Wenthold, R.J., 1992. N-Acetylaspartylglutamate acts as an agonist upon homomeric NMDA receptor (NMDAR1) expressed in Xenopus oocytes. FEBS Lett. 311, 285-289.
26. Silva, G.A., Theriault, E., Mills, L.R., Pennefather, P.S., Feeney, C.J., 1999. Group I and II metabotropic glutamate receptor expression in cultured rat spinal cord astrocytes. Neurosci. Lett. 263, 117-120.
27. Sluka, K.A., Westlund, K.N., 1992. An experimental arthritis in rats: dorsal horn aspartate and glutamate increases. Neurosci. Lett. 145, 141-144.
28. Slusher, B.S., Tsai, G., Yoo, G., Coyle, J.T., 1992. Immunocytochemical localization of the N-acetylaspartyl glutamate (NAAG) hydrolyzing enzyme N-acetylated-alpha-linked acidic dipeptidase (NAALADase). J. Comp. Neurol. 315, 217-229.
29. Slusher, B.S., Vornov, J.J., Thomas, A.G., Hurn, P.D., Harukuni, I., Bhardwaj, A., Traystman, R.J., Robinson, M.B., Britton, P., Lu, X.C., Tortella, F.C., Wozniak, K.M., Yudkoff, M., Potter, B.M., Jackson, P.F., 1999. Selective inhibition of NAALADase, which converts NAAG to glutamate, reduces ischemic brain injury. Nat. Med. 5, 1396-1402.
30. Sorkin, L.S., Westlund, K.N., Sluka, K.A., Dougherty, P.M., Willis, W.D., 1992. Neural changes in acute arthritis in monkeys. IV. Time-course of amino acid release into lumbar dorsal horn. Brain Res. Rev. 19, 39-50.
31. Tang, F.R., Sim, M.K., 1999. Pre-and/or post-synaptic localisation of metabotropic glutamate receptor 1alpha (mGluR1alpha) and 2/3 (mGluR2/3) in the rat spinal cord. Neurosci. Res. 34, 73-78.
32. Thomas, A.G., Olkowski, J.L., Slusher, B.S., 2001. Neuroprotection afforded by NAAG and NAALADase inhibition requires glial cells and metabotropic glutamate receptor activation. Eur. J. Pharmacol. 426, 35-38.
33. Valerio, A., Paterlini, M., Boifava, M., Memo, M., Spano, P., 1997. Metabotropic glutamate receptor mRNA expression in rat spinal cord. Neuroreport 8, 2695-2699.
34. Vornov, J.J., Wozniak, K., Lu, M., Jackson, P., Tsukamoto, T., Wang, E., Slusher, B., 1999. Blockade of NAALADase: a novel neuroprotective strategy based on limiting glutamate and elevating, NAAG. Ann. NY Acad. Sci. 890, 400-405.
35. Westbrook, G.L., Mayer, M.L., Namboodiri, M.A., Neale, J.H., 1986. High concentrations of N-acetylaspartylglutamate (NAAG) selectively activate NMDA receptors on mouse spinal cord neurons in cell culture. J. Neurosci. 6, 3385-3392.
36. Wroblewska, B., Wroblewski, J.T., Pshenichkin, S., Surin, A., Sullivan, S.E., Neale, J.H., 1997. N-Acetylaspartylglutamate selectively activates mGluR3 receptors in transfected cells. J. Neurochem. 69, 174-181.
37. Xi, Z.X., Baker, D.A., Shen, H., Carson, D.S., Kalivas, P.W., 2002. Group II metabotropic glutamate receptors modulate extracellular glutamate in the nucleus accumbens. J. Pharmacol. Exp. Ther. 300, 162-171.
38. Yamamoto, T., Nozaki-Taguchi, N., Sakashita, Y., 2001a. Spinal N-acetyl-alpha-linked acidic dipeptidase (NAALADase) inhibition attenuates mechanical allodynia induced by paw carrageenan injection in the rat. Brain Res. 909, 138-144.
39. Yamamoto, T., Nozaki-Taguchi, N., Sakashita, Y., 2001b. Inhibition of spinal N-acetyl-alpha-linked acidic dipeptidase produces an antinociceptive effect in the rat formalin test. Neuroscience 102, 473-479.
40. Zhang, W., Slusher, B., Murakawa, Y., Wozniak, K.M., Tsukamoto, T., Jackson, P.F., Sima, A.A., 2002. GCPII (NAALADase) inhibition prevents long-term diabetic neuropathy in type 1 diabetic BB/W or rats. J. Neurol. Sci. 194, 21-28.
41. 3H]GABA release via mGluR3, cAMP, PKA and L-type calcium conductance. Eur. J. Neurosci. 13, 340-346.
42. Zollinger, M., Brauchli Theotokis, J., Gutteck Amsler, U., Do, K.Q., Streit, P., Cuenod, M., 1994. Release of N-acetylaspartylglutamate from slices of rat cerebellum, striatum, and spinal cord, and the effect of climbing fiber deprivation. J. Neurochem. 63, 1133-1142.