Peripheral inflammation-induce increase of AMPA-mediated currents and Ca2+ transients in the presence of cylothiazide in the rat substantia gelatinosa neurons

Cell Calcium

Volumn 35, Issue 5, 2004, Pages 461-469

  Voitenko, Nana ^a,b   Gerber, G ^a,c   Youn, D ^a,d   Randic, M ^a  

^a IOWA STATE UNIVERSITY   (United States)

^b BOGOMOLETZ INSTITUTE OF PHYSIOLOGY   (Ukraine)

^c SEMMELWEIS UNIVERSITY   (Hungary)

^d MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

AMPA; Gelatinosa; Inflammation; Substantia

Indexed keywords

ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; AMPA RECEPTOR; CALCIUM ION; CARRAGEENAN; CYCLOTHIAZIDE; FURA 2; AMINO ACID RECEPTOR STIMULATING AGENT; ANTIHYPERTENSIVE AGENT; BENZOTHIADIAZINE DERIVATIVE; CALCIUM;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM TRANSPORT; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYTOSOL; DENDRITE; DESENSITIZATION; DISEASE MODEL; INFLAMMATION; LUMBAR SPINAL CORD; MEMBRANE CURRENT; NERVE CELL; NONHUMAN; PAIN; PATCH CLAMP; PRIORITY JOURNAL; RAT; RECEPTOR UPREGULATION; RODENT; SENSITIVITY ANALYSIS; SUBSTANTIA GELATINOSA; ANIMAL; CALCIUM SIGNALING; CELL MEMBRANE POTENTIAL; CHEMICALLY INDUCED DISORDER; DRUG ANTAGONISM; DRUG EFFECT; DRUG POTENTIATION; FEMALE; IN VITRO STUDY; MALE; METABOLISM; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

RODENTIA;

ALPHA-AMINO-3-HYDROXY-5-METHYL-4-ISOXAZOLEPROPIONIC ACID; ANIMALS; ANTIHYPERTENSIVE AGENTS; BENZOTHIADIAZINES; CALCIUM; CALCIUM SIGNALING; CARRAGEENAN; EXCITATORY AMINO ACID AGONISTS; FEMALE; INFLAMMATION; MALE; MEMBRANE POTENTIALS; NEURONS; PATCH-CLAMP TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, AMPA; SUBSTANTIA GELATINOSA;

EID: 1642344419     PISSN: 01434160     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ceca.2003.11.002     Document Type: Article

References (58)

1. M.J. Millan, The induction of pain: An integrative review, Prog. Neurobiol. 57 (1999) 1-164.
2. W. Zieglgansberger, T.R. Tolle, The pharmacology of pain signalling, Curr. Opin. Neurobiol. 3 (1993) 611-618.
3. T.P. Doubell, R.J. Mannion, C.J. Woolf, The dorsal horn: state-dependent sensory processing, plasticity and the generation of pain, in: Wall PD, R. Melzack (Eds.), Textbook of Pain, Churchill Livingstone, New York, 1999, pp. 165-181.
4. 2+ transients in the rat substantia gelatinosa neurons after ligation of L5-L6 spinal nerves, Neuroreport 11 (2000) 4055-4061.
5. X.M. Yu, R. Askalan, G.J. Keil, M.W. Salter, NMDA channel regulation by channel-associated protein tyrosine kinase Src, Science 275 (1997) 674-678.
6. R. Dubner, M.A. Ruda, Activity-dependent neuronal plasticity following tissue injury and inflammation, Trends Neurosci. 15 (1992) 96-103.
7. V. Neugebauer, T. Lucke, H.G. Schaible, N-Methyl-D-aspartate (NMDA) and non-NMDA receptor antagonists block the hyperexcitability of dorsal horn neurons during development of acute arthritis in rat's knee joint, J. Neurophysiol. 70 (1993) 1365-1377.
8. J.I. Szekely, K. Torok, G. Mate, The role of ionotropic glutamate receptors in nociception with special regard to the AMPA binding sites, Curr. Pharm. Des. 8 (2002) 887-912.
9. L.C. Stanfa, A.H. Dickenson, The role of non-N-methyl-D-aspartate ionotropic glutamate receptors in the spinal transmission of nociception in normal animals and animals with carrageenan inflammation, Neuroscience 93 (1999) 1391-1398.
10. T. Nishiyama, L. Gyermek, C. Lee, S. Kawasaki-Yatsugi, T. Yamaguchi, The systemically administered competitive AMPA receptor antagonist, YM872, has analgesic effects on thermal or formalin-induced pain in rats, Anesth. Analg. 89 (1999) 1534-1537.
11. C.N. Sang, M.P. Hostetter, R.H. Gracely, et al., AMPA/kainate antagonist LY293558 reduces capsaicin-evoked hyperalgesia but not pain in normal skin in humans, Anesthesiology 89 (1998) 1060-1067.
12. M. Hollmann, S. Heinemann, Cloned glutamate receptors, Annu. Rev. Neurosci. 17 (1994) 31-108.
13. 2+ permeability of AMPA receptors in principal neurons and interneurons in rat CNS, Neuron 15 (1995) 193-204.
14. H.S. Engelman, T.B. Allen, A.B. MacDermott, The distribution of neurons expressing calcium-permeable AMPA receptors in the superficial laminae of the spinal cord dorsal horn, J. Neurosci. 19 (1999) 2081-2089.
15. T. Furuyama, H. Kiyama, K. Sato, et al., 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, Brain Res. Mol. Brain Res. 18 (1993) 141-151.
16. A. Popratiloff, R.J. Weinberg, A. Rustioni, AMPA receptor subunits underlying terminals of fine-caliber primary afferent fibers, J. Neurosci. 16 (1996) 3363-3372.
17. Q.Q. Zhou, H. Imbe, S. Zou, R. Dubner, K. Ren, Selective upregulation of the flip-flop splice variants of AMPA receptor subunits in the rat spinal cord after hindpaw inflammation, Brain Res. Mol. Brain Res. 88 (2001) 186-193.
18. E.J. Fletcher, D. Lodge, New developments in the molecular pharmacology of alpha-amino-3-hydroxy-5-methyl-4-isoxazole propionate and kainate receptors, Pharmacol. Ther. 70 (1996) 65-89.
19. B. Bettler, C. Mulle, Review: Neurotransmitter receptors. II. AMPA and kainate receptors, Neuropharmacology 34 (1995) 123-139.
20. L.A. Wong, M.L. Mayer, Differential modulation by cyclothiazide and concanavalin A of desensitization at native alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid- and kainate-preferring glutamate receptors, Mol. Pharmacol. 44 (1993) 504-510.
21. C.F. Zorumski, L.L. Thio, Properties of vertebrate glutamate receptors: Calcium mobilization and desensitization, Prog. Neurobiol. 39 (1992) 295-336.
22. K.A. Yamada, C.M. Tang, Benzothiadiazides inhibit rapid glutamate receptor desensitization and enhance glutamatergic synaptic currents, J. Neurosci. 13 (1993) 3904-3915.
23. 2+ transients in dorsal horn neurons in slices of carrageenan-treated rats, Abstr. Soc. Neurosci. 24 (1998) 1870.
24. 2+ transients in substantia gelatinosa of the rat spinal dorsal horn, Abstr. Soc. Neurosci. 28 (2002) 367.
25. G. Gerber, D.H. Youn, C.H. Hsu, D. Isaev, M. Randic, Spinal dorsal horn synaptic plasticity: Involvement of group I metabotropic glutamate receptors, Prog. Brain Res. 129 (2000) 115-134.
26. V. Lev-Ram, H. Miyakawa, N. Lasser-Ross, W.N. Ross, Calcium transients in cerebellar Purkinje neurons evoked by intracellular stimulation, J. Neurophysiol. 68 (1992) 1167-1177.
27. L. Ballerini, E. Bracci, A. Nistri, Desensitization of AMPA receptors limits the amplitude of EPSPs and the excitability of motoneurons of the rat isolated spinal cord, Eur. J. Neurosci. 7 (1995) 1229-1234.
28. 2+ uptake in brain neurons, Eur. J. Pharmacol. 290 (1995) 105-115.
29. 2+ in cultured neurons from rat brain, J. Neurochem. 64 (1995) 2049-2056.
30. K.M. Partin, D.K. Patneau, M.L. Mayer, Cyclothiazide differentially modulates desensitization of alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor splice variants, Mol. Pharmacol. 46 (1994) 129-138.
31. R. Dingledine, K. Borges, D. Bowie, S.F. Traynelis, The glutamate receptor ion channels, Pharmacol. Rev. 51 (1999) 7-61.
32. Y. Stern-Bach, S. Russo, M. Neuman, C. Rosenmund, A point mutation in the glutamate binding site blocks desensitization of AMPA receptors, Neuron 21 (1998) 907-918.
33. Y. Guan, W. Guo, S.P. Zou, R. Dubner, K. Ren, Inflammation-induced upregulation of AMPA receptor subunit expression in brain stem pain modulatory circuitry, Pain 104 (2003) 401-413.
34. T.R. Tolle, A. Berthele, W. Zieglgansberger, P.H. Seeburg, W. Wisden, The differential expression of 16 NMDA and non-NMDA receptor subunits in the rat spinal cord and in periaqueductal gray, J. Neurosci. 13 (1993) 5009-5028.
35. T.R. Tolle, A. Berthele, W. Zieglgansberger, P.H. Seeburg, W. Wisden, Flip and Flop variants of AMPA receptors in the rat lumbar spinal cord, Eur. J. Neurosci. 7 (1995) 1414-1419.
36. B. Sommer, K. Keinanen, T.A. Verdoorn, et al., Flip and flop: a cell-specific functional switch in glutamate-operated channels of the CNS, Science 249 (1990) 1580-1585.
37. F. Florenzano, B. De Luca, Nociceptive stimulation induces glutamate receptor down-regulation in the trigeminal nucleus, Neuroscience 90 (1999) 201-207.
38. D.E. Pellegrini-Giampietro, S. Fan, B. Ault, B.E. Miller, R.S. Zukin, Glutamate receptor gene expression in spinal cord of arthritic rats, J. Neurosci. 14 (1994) 1576-1583.
39. N. Burnashev, H. Monyer, P.H. Seeburg, B. Sakmann, Divalent ion permeability of AMPA receptor channels is dominated by the edited form of a single subunit, Neuron 8 (1992) 189-198.
40. 2+ permeability of KA-AMPA-gated glutamate receptor channels depends on subunit composition, Science 252 (1991) 851-853.
41. i homeostasis in cultures of embryonic dopaminergic neurons, Brain Res. Mol. Brain Res. 21 (1994) 303-311.
42. M.J. Berridge, Neuronal calcium signaling, Neuron 21 (1998) 13-26.
43. M. Shimuta, M. Yoshikawa, M. Fukaya, M. Watanabe, H. Takeshima, T. Manabe, Postsynaptic modulation of AMPA receptor-mediated synaptic responses and LTP by the type 3 ryanodine receptor, Mol. Cell Neurosci. 17 (2001) 921-930.
44. T.G. Banke, D. Bowie, H. Lee, R.L. Huganir, A. Schousboe, S.F. Traynelis, Control of GluR1 AMPA receptor function by cAMP-dependent protein kinase, J. Neurosci. 20 (2000) 89-102.
45. H.K. Lee, M. Barbarosie, K. Kameyama, M.F. Bear, R.L. Huganir, Regulation of distinct AMPA receptor phosphorylation sites during bidirectional synaptic plasticity, Nature 405 (2000) 955-959.
46. B.J. McDonald, H.J. Chung, R.L. Huganir, Identification of protein kinase C phosphorylation sites within the AMPA receptor GluR2 subunit, Neuropharmacology 41 (2001) 672-679.
47. Y. Rong, X. Lu, A. Bernard, M. Khrestchatisky, M. Baudry, Tyrosine phosphorylation of ionotropic glutamate receptors by Fyn or Src differentially modulates their susceptibility to calpain and enhances their binding to spectrin and PSD-95, J. Neurochem. 79 (2001) 382-390.
48. K.M. Partin, Domain interactions regulating ampa receptor desensitization, J. Neurosci. 21 (2001) 1939-1948.
49. T.G. Banke, J.R. Greenwood, J.K. Christensen, et al., Identification of amino acid residues in GluR1 responsible for ligand binding and desensitization, J. Neurosci. 21 (2001) 3052-3062.
50. M.W. Fleck, R. Bahring, D.K. Patneau, M.L. Mayer, AMPA receptor heterogeneity in rat hippocampal neurons revealed by differential sensitivity to cyclothiazide, J. Neurophysiol. 75 (1996) 2322-2333.
51. V.S. Vorobjev, I.N. Sharonova, H.L. Haas, O.A. Sergeeva, Differential modulation of AMPA receptors by cyclothiazide in two types of striatal neurons, Eur. J. Neurosci. 12 (2000) 2871-2880.
52. T.V. Bliss, G.L. Collingridge, A synaptic model of memory: long-term potentiation in the hippocampus, Nature 361 (1993) 31-39.
53. G. Gerber, M. Randic, Participation of excitatory amino acid receptors in the slow excitatory synaptic transmission in the rat spinal dorsal horn in vitro, Neurosci. Lett. 106 (1989) 220-228.
54. M. Yoshimura, S. Nishi, Excitatory amino acid receptors involved in primary afferent-evoked polysynaptic EPSPs of substantia gelatinosa neurons in the adult rat spinal cord slice, Neurosci. Lett. 143 (1992) 131-134.
55. D.B. Reichling, A.B. MacDermott, Brief calcium transients evoked by glutamate receptor agonists in rat dorsal horn neurons: Fast kinetics and mechanisms, J. Physiol. 469 (1993) 67-88.
56. 2+-permeable AMPA receptors, Nature 381 (1996) 793-796.
57. M. Randic, M.C. Jiang, R. Cerne, Long-term potentiation and long-term depression of primary afferent neurotransmission in the rat spinal cord, J. Neurosci. 13 (1993) 5228-5241.
58. M. Randic, Plasticity of excitatory synaptic transmission in the spinal cord dorsal horn, Prog. Brain Res. 113 (1996) 463-506.