Altered long-term synaptic plasticity and kainate-induced Ca2+ transients in the substantia gelatinosa neurons in GLUK6-deficient mice

Molecular Brain Research

Volumn 142, Issue 1, 2005, Pages 9-18

  Youn, Dong Ho ^a,b   Voitenko, Nana ^a,c   Gerber, Gabor ^a,d   Park, Yun Kyung ^a   Galik, Jan ^a,e   Randić, Mirjana ^a  

^a IOWA STATE UNIVERSITY   (United States)

^b Kyungpook National University   (South Korea)

^c BOGOMOLETZ INSTITUTE OF PHYSIOLOGY   (Ukraine)

^d SEMMELWEIS UNIVERSITY OF MEDICINE   (Hungary)

^e INSTITUTE OF CHEMISTRY   (Slovakia)

Author keywords

GLUK6; Kainate receptor; LTP; Spinal cord

Indexed keywords

CALCIUM ION; GLUTAMATE RECEPTOR 5; KAINIC ACID; RECEPTOR SUBUNIT;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME DEFICIENCY; EVOKED SPINAL CORD RESPONSE; EXCITATORY POSTSYNAPTIC POTENTIAL; FREQUENCY MODULATION; GENE DELETION; GENE EXPRESSION REGULATION; GENE INDUCTION; GENE TARGETING; LONG TERM DEPRESSION; MOUSE; NERVE CELL; NERVE CELL PLASTICITY; NERVE STIMULATION; NONHUMAN; PAIN; PRIORITY JOURNAL; SENSORY NERVE; SPIKE; SUBSTANTIA GELATINOSA;

6-CYANO-7-NITROQUINOXALINE-2,3-DIONE; AGE FACTORS; ALPHA-AMINO-3-HYDROXY-5-METHYL-4-ISOXAZOLEPROPIONIC ACID; ANIMALS; BENZOATES; CADMIUM CHLORIDE; CALCIUM; DOSE-RESPONSE RELATIONSHIP, RADIATION; DRUG INTERACTIONS; ELECTRIC STIMULATION; EXCITATORY AMINO ACID AGONISTS; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; GLUTAMATES; GLYCINE; KAINIC ACID; MEMBRANE POTENTIALS; MICE; MICE, KNOCKOUT; NEURONAL PLASTICITY; NEURONS; PATCH-CLAMP TECHNIQUES; PROTEIN SUBUNITS; RECEPTORS, KAINIC ACID; SUBSTANTIA GELATINOSA;

ANIMALIA;

EID: 27844440919     PISSN: 0169328X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molbrainres.2005.09.004     Document Type: Article

References (58)

1. A. Bernard, and M. Khrestchatisky Assessing the extent of RNA editing in the TMII regions of GluR5 and GluR6 kainate receptors during rat brain development J. Neurochem. 62 1994 2057 2060
2. A. Bernard, L. Ferhat, F. Dessi, G. Charton, A. Represa, Y. Ben-Ari, and M. Khrestchatisky Q/R editing of the rat GluR5 and GluR6 kainate receptors in vivo and in vitro: evidence for independent developmental, pathological and cellular regulation Eur. J. Neurosci. 11 1999 604 616
3. D. Bleakman, A.M. Ogden, P.L. Ornstein, and K. Hoo Pharmacological characterization of a GluR6 kainate receptor in cultured hippocampal neurons Eur. J. Pharmacol. 378 1999 331 337
4. Z.A. Bortolotto, V.R. Clarke, C.M. Delany, M.C. Parry, I. Smolders, M. Vignes, K.H. Ho, P. Miu, B.T. Brinton, R. Fantaske, A. Ogden, M. Gates, P.L. Ornstein, D. Lodge, D. Bleakman, and G.L. Collingridge Kainate receptors are involved in synaptic plasticity Nature 402 1999 297 301
5. K6 at hippocampal mossy fiber synapses J. Neurosci. 24 2004 10093 10098
6. N. Burnashev, Z. Zhou, E. Neher, and B. Sakmann Fractional calcium currents through recombinant GluR channels of the NMDA, AMPA and kainate receptor subunits J. Physiol. 485 1995 403 418
7. N. Burnashev, A. Villarroel, and B. Sakmann Dimensions and ion selectivity of recombinant AMPA and kainate receptor channels and their dependence on Q/R site residues J. Physiol. 496 1996 165 173
8. J.K. Christensen, A.V. Paternain, S. Selak, P.K. Ahring, and J. Lerma A mosaic of functional kainate receptors in hippocampal interneurons J. Neurosci. 24 2004 8986 8993
9. A. Contractor, G.T. Swanson, and S.F. Heinemann Kainate receptors are involved in short- and long-term plasticity at mossy fiber synapses in the hippocampus Neuron 29 2001 209 216
10. R. Dingledine The glutamate receptor ion channels Pharmacol. Rev. 51 1999 7 61
11. S.D. Donevan, A. Beg, J.M. Gunther, and R.E. Twyman The methylglutamate, SYM 2081, is a potent and highly selective agonist at kainate receptors J. Pharmacol. Exp. Ther. 285 1998 539 545
12. 2+ permeability of unedited and edited versions of the kainate selective glutamate receptor GluR6 Proc. Natl. Acad. Sci. U. S. A. 90 1993 755 759
13. A. Frandsen, and A. Schousboe Mobilization of dantrolene-sensitive intracellular calcium pools is involved in the cytotoxicity induced by quisqualate and N-methyl-d-aspartate but not by 2-amino-3-(3-hydroxy-5- methylisoxazol-4-yl)propionate and kainate in cultured cerebral cortical neurons Proc. Natl. Acad. Sci. U. S. A. 89 1992 2590 2594
14. G. Gerber, D.H. Youn, G.T. Swanson, A. Sailer, S. Heinemann, and M. Randić Kainate receptors modulate sensory synaptic transmission in the mouse spinal cord Abstr.-Soc. Neurosci. 25 1999 920
15. 2+-permeable AMPA receptors Nature 381 1996 793 796
16. W. Guo, S. Zou, M. Tal, and K. Ren Activation of spinal kainate receptors after inflammation: behavioral hyperalgesia and subunit gene expression Eur. J. Pharmacol. 452 2002 309 318
17. M. Hollmann, and S. Heinemann Cloned glutamate receptors Annu. Rev. Neurosci. 17 1994 31 108
18. J.R. Howe Homomeric and heteromeric ion channels formed from the kainate-type subunits GluR6 and KA2 have very small, but different, unitary conductances J. Neurophysiol. 76 1996 510 519
19. S.J. Hwang, S. Pagliardini, A. Rustioni, and J.G. Valtschanoff Presynaptic kainate receptors in primary afferents to the superficial laminae of the rat spinal cord J. Comp. Neurol. 436 2001 275 289
20. H. Ikeda, B. Heinke, R. Ruscheweyh, and J. Sandkuhler Synaptic plasticity in spinal lamina I projection neurons that mediate hyperalgesia Science 299 2003 1237 1240
21. R.R. Ji, T. Kohno, K.A. Moore, and C.J. Woolf Central sensitization and LTP: do pain and memory share similar mechanisms? Trends Neurosci. 26 2003 696 705
22. Z. Jia, N. Agopyan, P. Miu, Z. Xiong, J. Henderson, R. Gerlai, F.A. Taverna, A. Velumian, J. MacDonald, P. Carlen, W. Abramow-Newerly, and J. Roder Enhance LTP in mice deficient in the AMPA receptor GluR2 Neuron 17 1996 945 956
23. K.A. Jones, T.J. Wilding, J.E. Huettner, and A.M. Costa Desensitization of kainate receptors by kainate, glutamate and diastereomers of 4-methylglutamate Neuropharmacology 36 1997 853 863
24. S. Jung, Y. Park, J. Park, J. Kwak, S. Kim, and J. Kim Role of intracellular calcium stores on long-term potentiation (LTP) in substantia gelatinosa neurons in the rat Abstr.-Soc. Neurosci. 27 2001 275.6
25. H. Kamiya Kainate receptor-dependent presynaptic modulation and plasticity Neurosci. Res. 42 2002 1 6
26. J. Kang, Q. Xu, L. Jiang, N. Kang, and J. Xu Calcium permeability of GluR5 and GluR6 in CA1 hippocampal interneurons Abstr.-Soc. Neurosci. 2004 260.13
27. G.A. Kerchner, T.J. Wilding, P. Li, M. Zhuo, and J.E. Huettner Presynaptic kainate receptors regulate spinal sensory transmission J. Neurosci. 21 2001 59 66
28. G.A. Kerchner, T.J. Wilding, J.E. Huettner, and M. Zhuo Kainate receptor subunits underlying presynaptic regulation of transmitter release in the dorsal horn J. Neurosci. 22 2002 8010 8017
29. 2+ permeability in both TM1 and TM2 of high affinity kainate receptor channels: diversity by RNA editing Neuron 10 1993 491 550
30. S. Ko, M. Zhao, H. Toyoda, C. Qiu, and M. Zhuo Altered behavioral responses to noxious stimuli and fear in glutamate receptor 5 (GluR5)- or GluR6-deficient mice J. Neurosci. 25 2005 977 984
31. S.E. Lauri, Z.A. Bortolotto, D. Bleakman, P.L. Ornstein, D. Lodge, J.T. Isaac, and G.L. Collingridge A critical role of a facilitatory presynaptic kainate receptor in mossy fiber LTP Neuron 32 2001 697 709
32. 2+ stores in kainate receptor-dependent synaptic facilitation and LTP at mossy fiber synapses in the hippocampus Neuron 39 2003 327 341
33. 2+ permeability J. Neurosci. 21 2001 4572 4581
34. V. Lev-Ram, N. Miyakawa, N. Lasser-Ross, and W.N. Ross Calcium transients in cerebellar Purkinje neurons evoked by intracellular stimulation J. Neurophysiol. 68 1992 1167 1177
35. P. Li, T.J. Wilding, S.J. Kim, A.A. Calejesan, J.E. Huettner, and M. Zhuo Kainate-receptor-mediated sensory synaptic transmission in mammalian spinal cord Nature 397 1999 161 163
36. H. Li, A. Chen, G. Xing, M.L. Wei, and M.A. Rogawski Kainate receptor-mediated heterosynaptic facilitation in the amygdale Nat. Neurosci. 4 2001 612 620
37. S. Lucifora, C. Lu, K.D. Phend, H.H. Willcockson, J.G. Valtschanoff, and A. Rustioni Presynaptic kainate receptors are expressed in terminals of nociceptive primary afferents to the rat dorsal horn Abstr.-Soc. Neurosci. 2004 291.1
38. R.C. Malenka, and R.A. Nicoll Long-term potentiation-a decade of progress? Science 285 1999 1870 1874
39. A.V. Paternain, M. Morales, and J. Lerma Selective antagonism of AMPA receptors unmasks kainate receptor-mediated responses in hippocampal neurons Neuron 14 1995 185 189
40. M. Randić Plasticity of excitatory synaptic transmission in the spinal cord dorsal horn Prog. Brain Res. 113 1996 463 506
41. M. Randić, M.C. Jiang, and R. Cerne Long-term potentiation and long-term depression of primary afferent neurotransmission in the rat spinal cord J. Neurosci. 13 1993 5228 5241
42. J.R. Savidge, D. Bleakman, and D.R. Bristow Identification of kainate receptor-mediated intracellular calcium increases in cultured rat cerebellar granule cells J. Neurochem. 69 1997 1763 1766
43. J. Schmitt, E. Dux, C. Gissel, and W. Paschen Regional analysis of developmental changes in the extent of GluR6 mRNA editing in rat brain Brain Res. Dev. Brain Res. 91 1996 153 157
44. D. Schmitz, J. Mellor, J. Breustedt, and R.A. Nicoll Presynaptic kainate receptors impart an associative property to hippocampal mossy fiber long-term potentiation Nat. Neurosci. 6 2003 1058 1063
45. P.H. Seeburg, F. Single, T. Kuner, M. Higuchi, and R. Sprengel Genetic manipulation of key determinants of ion flow in glutamate receptor channels in the mouse Brain Res. 907 2001 233 243
46. i changes in cultured rat hippocampal neurons J. Neurosci. Res. 65 2001 378 386
47. B. Sommer, M. Köhler, R. Sprengel, and P.H. Seeburg RNA editing in brain controls a determinant of ion flow in glutamate-gated channels Cell 67 1991 11 19
48. S.L. Stegenga, and R.G. Kalb Developmental regulation of N-methyl-d-aspartate- and kainate-type glutamate receptor expression in the rat spinal cord Neuroscience 105 2001 499 507
49. G.T. Swanson, D. Feldmeyer, M. Kaneda, and S.G. Cull-Candy Effect of RNA editing and subunit co-assembly on single-channel properties of recombinant kainate receptors J. Physiol. 492 1996 129 142
50. T.R. Tölle, A. Berthele, W. Zieglgänsberger, P.H. Seeburg, and 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
51. B. Vissel, G.A. Royle, B.R. Christie, H.H. Schiffer, A. Ghetti, T. Tritto, I. Perez-Otano, R.A. Radcliffe, J. Seamans, T. Sejnowski, N.K. Wehner, A.C. Collins, S. O'Gorman, and S.F. Heinemann The role of RNA editing of kainate receptors in synaptic plasticity and seizures Neuron 29 2001 217 227
52. 2+ transients in the presence of cyclothiazide in the rat substantia gelatinosa neurons Cell Calcium 35 2004 461 469
53. N. Voitenko, D. Youn, J. Galik, G. Gerber, and M. Randić Kainate receptors are involved in long-term synaptic plasticity in the spinal cord substantia gelatinosa Abstr.-Soc. Neurosci. 2004 56.8
54. W.D. Willis Long-term potentiation in spinothalamic neurons Brain Res. Brain Res. Rev. 40 2002 202 214
55. W.D. Willis Jr., and R.E. Coggeshall Sensory Mechanisms of the Spinal Cord 1991 Plenum Press New York
56. M.F. Yeckel, A. Kapur, and D. Johnston Multiple forms of LTP in hippocampal CA3 neurons use a common postsynaptic mechanism Nat. Neurosci. 2 1999 625 633
57. D. Youn, and M. Randić Modulation of excitatory synaptic transmission in the spinal substantia gelatinosa of mice deficient in the kainate receptor GluR5 and/or GluR6 subunit J. Physiol. 555.3 2004 683 698
58. D. Youn, B. Vissel, G. Royle, S.F. Heinemann, and M. Randic Enhanced LTP of primary afferent neurotransmission in mice deficient in the AMPA receptor GluR2 Abstr.-Soc. Neurosci. 26 2000 909