Zinc-induced collapse of augmented inhibition by GABA in a temporal lobe epilepsy model

Science

Volumn 271, Issue 5247, 1996, Pages 369-373

  Buhl, Eberhard H ^a   Otis, Thomas S ^b   Mody, Istvan ^c  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 AMINO 5 PHOSPHONOVALERIC ACID; 4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID B RECEPTOR; 6 CYANO 7 NITRO 2,3 QUINOXALINEDIONE; AMINO ACID RECEPTOR BLOCKING AGENT; CHLORIDE; PYRIDINE DERIVATIVE; ZINC; ZINC CHLORIDE; ZINC DERIVATIVE; ZOLPIDEM;

ANIMAL; ARTICLE; DENTATE GYRUS; DRUG ANTAGONISM; DRUG EFFECT; HUMAN; IN VITRO STUDY; INTERNEURON; KINDLING; MALE; METABOLISM; NERVE CELL INHIBITION; PATHOPHYSIOLOGY; PHYSIOLOGY; RAT; SYNAPTIC TRANSMISSION; TEMPORAL LOBE EPILEPSY; WISTAR RAT;

2-AMINO-5-PHOSPHONOVALERATE; 6-CYANO-7-NITROQUINOXALINE-2,3-DIONE; ANIMALS; CHLORIDES; DENTATE GYRUS; EPILEPSY, TEMPORAL LOBE; EXCITATORY AMINO ACID ANTAGONISTS; GAMMA-AMINOBUTYRIC ACID; HUMANS; INTERNEURONS; KINDLING, NEUROLOGIC; MALE; NEURAL INHIBITION; PYRIDINES; RATS; RATS, WISTAR; RECEPTORS, GABA-A; RECEPTORS, GABA-B; SYNAPTIC TRANSMISSION; ZINC; ZINC COMPOUNDS;

ANIMALIA;

EID: 0030593034     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.271.5247.369     Document Type: Article

References (69)

1. R L. Macdonald and R. W. Olsen, Annu. Rev. Neurosci. 17, 569 (1994).
2. I Mody, Y. De Koninck, T. S. Otis, I Soltesz, Trends Neurosci. 17, 517 (1994)
3. P. A. Schwartzkroin, Ed., Epilepsy. Models, Mechanisms, and Concepts (Cambridge Univ. Press, Cambridge, 1993).
4. R. S. Sloviter, Science 235, 73 (1987); M. Isokawa, G. Avanzini, D. M. Finch, T. L. Babb, M. F. Levesque, Epilepsy Res. 9, 242 (1991); M. Avoli, ibid. 10, 33 (1991); R S. Sloviter, Hippocampus 4. 250 (1994); K. Uruno, M J. O'Connor, L M Masukawa, ibid., p 583.
5. R. S. Sloviter, Science 235, 73 (1987); M. Isokawa, G. Avanzini, D. M. Finch, T. L. Babb, M. F. Levesque, Epilepsy Res. 9, 242 (1991); M. Avoli, ibid. 10, 33 (1991); R S. Sloviter, Hippocampus 4. 250 (1994); K. Uruno, M J. O'Connor, L M Masukawa, ibid., p 583.
6. R. S. Sloviter, Science 235, 73 (1987); M. Isokawa, G. Avanzini, D. M. Finch, T. L. Babb, M. F. Levesque, Epilepsy Res. 9, 242 (1991); M. Avoli, ibid. 10, 33 (1991); R S. Sloviter, Hippocampus 4. 250 (1994); K. Uruno, M J. O'Connor, L M Masukawa, ibid., p 583.
7. R. S. Sloviter, Science 235, 73 (1987); M. Isokawa, G. Avanzini, D. M. Finch, T. L. Babb, M. F. Levesque, Epilepsy Res. 9, 242 (1991); M. Avoli, ibid. 10, 33 (1991); R S. Sloviter, Hippocampus 4. 250 (1994); K. Uruno, M J. O'Connor, L M Masukawa, ibid., p 583.
8. R. S. Sloviter, Science 235, 73 (1987); M. Isokawa, G. Avanzini, D. M. Finch, T. L. Babb, M. F. Levesque, Epilepsy Res. 9, 242 (1991); M. Avoli, ibid. 10, 33 (1991); R S. Sloviter, Hippocampus 4. 250 (1994); K. Uruno, M J. O'Connor, L M Masukawa, ibid., p 583.
9. R. S Sloviter, Hippocampus 1, 41 (1991); J. W. Bekenstein and E. W. Lothman, Science 259, 97 (1993).
10. R. S Sloviter, Hippocampus 1, 41 (1991); J. W. Bekenstein and E. W. Lothman, Science 259, 97 (1993).
11. S. Otis, Y. De Koninck, I. Mody, Proc Natl Acad Sci. U S.A. 91, 7698 (1994).
12. T. Sutula, H. Xiao-Xian, J. Cavazos, G. Scott, Science 239, 1147 (1988).
13. J. Cronin and F. E Dudek, Brain Res. 474, 181 (1988); J. E. Cavazos, G. Golarai, T. P. Sutula, J. Neurosci. 11, 2795 (1991); M Isokawa, M F Levesque, T. L. Babb, J. J Engel, ibid 13, 1511 (1993).
14. J. Cronin and F. E Dudek, Brain Res. 474, 181 (1988); J. E. Cavazos, G. Golarai, T. P. Sutula, J. Neurosci. 11, 2795 (1991); M Isokawa, M F Levesque, T. L. Babb, J. J Engel, ibid 13, 1511 (1993).
15. J. Cronin and F. E Dudek, Brain Res. 474, 181 (1988); J. E. Cavazos, G. Golarai, T. P. Sutula, J. Neurosci. 11, 2795 (1991); M Isokawa, M F Levesque, T. L. Babb, J. J Engel, ibid 13, 1511 (1993).
16. T. P. Sutula, G Cascino, J. Cavazos, I. Paracta, L Ramirez, Ann. Neurol. 26, 321 (1989).
17. T. L. Babb, W. R Kupfer, J. K. Pretorius, P H. Crandall, M. F Levesque, Neuroscience 42, 351 (1991).
18. C E Ribak and G. M. Peterson, Hippocampus 1, 355 (1991); R. S. Sloviter, Neurosci Lett. 137, 91 (1992); M.M. Okazaki, D.A. Evenson, J V Nadler, J. Comp. Neurol. 352, 515 (1995).
19. C E Ribak and G. M. Peterson, Hippocampus 1, 355 (1991); R. S. Sloviter, Neurosci Lett. 137, 91 (1992); M.M. Okazaki, D.A. Evenson, J V Nadler, J. Comp. Neurol. 352, 515 (1995).
20. C E Ribak and G. M. Peterson, Hippocampus 1, 355 (1991); R. S. Sloviter, Neurosci Lett. 137, 91 (1992); M.M. Okazaki, D.A. Evenson, J V Nadler, J. Comp. Neurol. 352, 515 (1995).
21. T. P. Sutula, Epilepsy Res. 10, 62 (1991); J. O. McNamara, J. Neurosci. 14, 3413 (1994). Three of the 24 kindled animals in this study were prepared for Timm's stain The pattern of supragranular mossy fibers in all of the kindled animals examined was consistent with the level of sprouting described by Sutula et al. (7)
22. T. P. Sutula, Epilepsy Res. 10, 62 (1991); J. O. McNamara, J. Neurosci. 14, 3413 (1994). Three of the 24 kindled animals in this study were prepared for Timm's stain The pattern of supragranular mossy fibers in all of the kindled animals examined was consistent with the level of sprouting described by Sutula et al. (7)
23. T. P. Sutula, Epilepsy Res. 10, 62 (1991); J. O. McNamara, J. Neurosci. 14, 3413 (1994). Three of the 24 kindled animals in this study were prepared for Timm's stain The pattern of supragranular mossy fibers in all of the kindled animals examined was consistent with the level of sprouting described by Sutula et al. (7)
24. M. N. G. Titulaer, W. E. Ghijsen, W. Kamphuis, T. C. De Rijk, F. H. Lopes da Silva, J. Neurochem 64, 2615 (1995)
25. L. P. Tuff, R. J Racine, R. Adamec, Brain Res. 277, 79 (1983), M. W Oliver and J J. Miller, Exp. Brain Res 57, 443 (1985); W Kamphuis, J. A. Gorter, W J. Wadman, F. H Lopes da Silva, Neurosci. Lett. 141, 101 (1992).
26. L. P. Tuff, R. J Racine, R. Adamec, Brain Res. 277, 79 (1983), M. W Oliver and J J. Miller, Exp. Brain Res 57, 443 (1985); W Kamphuis, J. A. Gorter, W J. Wadman, F. H Lopes da Silva, Neurosci. Lett. 141, 101 (1992).
27. L. P. Tuff, R. J Racine, R. Adamec, Brain Res. 277, 79 (1983), M. W Oliver and J J. Miller, Exp. Brain Res 57, 443 (1985); W Kamphuis, J. A. Gorter, W J. Wadman, F. H Lopes da Silva, Neurosci. Lett. 141, 101 (1992).
28. E. H. Buhl, K Halasy, P Somogyi, Nature 368, 823 (1994)
29. I. Soltesz, D. K. Smetters, I. Mody, Neuron 14, 1273 (1995).
30. 2 and comparable between recordings in control and kindled granule cells. The signals were transmitted through a low-pass filter at 3 kHz (-3 dB, eight-pole Bessel filter, Frequency Devices 9002) and digitized at 20 kHz (DT 2821 MD interface). Individual events were detected and analyzed off-line [CDR software, J Dempster, University of Strathclyde, Glasgow, UK; see also (76) and (78)] . All experimental values are given as means ± SEMs. Significance was set at the 0.01 level.
31. T. S. Otis and I. Mody, Neuroscience 49, 13 (1992).
32. S. M. Thompson, Prog. Neurobiol. 42, 575 (1994).
33. Z S. Han, E. H. Buhl, Z. Lörinczi, P. Somogyi, Eur J. Neurosci. 5, 395 (1993).
34. 2- entry into the terminals [see also (2), (18), and (19)] This type of GABA release is responsible for generating IPSCs. Their frequency varies from brain region to brain region but it is consistently less than that observed in the presence of action potentials.
35. 2- entry into the terminals [see also (2), (18), and (19)] This type of GABA release is responsible for generating IPSCs. Their frequency varies from brain region to brain region but it is consistently less than that observed in the presence of action potentials.
36. N. G. Bowery et al , Nature 283, 92 (1980).
37. C. H. Davies, S. J. Starkey, M. F. Pozza, G. L Collingridge, Nature 349, 609 (1991); D. D. Matt and D. V. Lewis, Science 252, 1718 (1991); D. D. Mott, C, W. Xie, W. A. Wilson, H. S. Swartzwelder, D. V. Lewis, J. Neurophysiol. 69, 674 (1993), S. M. Thompson, M Capogna, M. Scanziani, Trends Weurosci. 16, 222 (1993).
38. C. H. Davies, S. J. Starkey, M. F. Pozza, G. L Collingridge, Nature 349, 609 (1991); D. D. Matt and D. V. Lewis, Science 252, 1718 (1991); D. D. Mott, C, W. Xie, W. A. Wilson, H. S. Swartzwelder, D. V. Lewis, J. Neurophysiol. 69, 674 (1993), S. M. Thompson, M Capogna, M. Scanziani, Trends Weurosci. 16, 222 (1993).
39. C. H. Davies, S. J. Starkey, M. F. Pozza, G. L Collingridge, Nature 349, 609 (1991); D. D. Matt and D. V. Lewis, Science 252, 1718 (1991); D. D. Mott, C, W. Xie, W. A. Wilson, H. S. Swartzwelder, D. V. Lewis, J. Neurophysiol. 69, 674 (1993), S. M. Thompson, M Capogna, M. Scanziani, Trends Weurosci. 16, 222 (1993).
40. C. H. Davies, S. J. Starkey, M. F. Pozza, G. L Collingridge, Nature 349, 609 (1991); D. D. Matt and D. V. Lewis, Science 252, 1718 (1991); D. D. Mott, C, W. Xie, W. A. Wilson, H. S. Swartzwelder, D. V. Lewis, J. Neurophysiol. 69, 674 (1993), S. M. Thompson, M Capogna, M. Scanziani, Trends Weurosci. 16, 222 (1993).
41. C H. Davies, S. N. Davies, G L. Collingridge, J Physiol. London 424, 513 (1990); N. A. Lambert and W. A Wilson, J. Neurophysiol. 72, 121 (1994)
42. C H. Davies, S. N. Davies, G L. Collingridge, J Physiol. London 424, 513 (1990); N. A. Lambert and W. A Wilson, J. Neurophysiol. 72, 121 (1994)
43. h2: 41.8 ± 2.7, 152 7 ± 10.8, 981 ± 198, 087 ± 0.02, and 0 11 ± 0.02 (control, n= 6), and 45 6 ± 1.2, 143.4 ± 7.6, 722 ± 86.9, 0.83 ± 0 06, and 0.17 ± 0.06 (kindled, n= 9).
44. I. Mody and U. Heinemann, Nature 326, 701 (1987); J. E. Kraus, G. C. Yeh, D. W. Bonhaus, J. V. Nadler, J. O. McNamara, J. Neurosci. 14, 4196 (1994).
45. I. Mody and U. Heinemann, Nature 326, 701 (1987); J. E. Kraus, G. C. Yeh, D. W. Bonhaus, J. V. Nadler, J. O. McNamara, J. Neurosci. 14, 4196 (1994).
46. S. Y. Assaf and S. H. Chung, Nature 308, 734 (1984); G A. Howell, M. G. Welch, C. J. Frederickson, Nature 308, 736 (1984), C. J. Frederickson and D. W. Moncrieff, Biol. Signals 3, 127 (1994).
47. S. Y. Assaf and S. H. Chung, Nature 308, 734 (1984); G A. Howell, M. G. Welch, C. J. Frederickson, Nature 308, 736 (1984), C. J. Frederickson and D. W. Moncrieff, Biol. Signals 3, 127 (1994).
48. S. Y. Assaf and S. H. Chung, Nature 308, 734 (1984); G A. Howell, M. G. Welch, C. J. Frederickson, Nature 308, 736 (1984), C. J. Frederickson and D. W. Moncrieff, Biol. Signals 3, 127 (1994).
49. A. Draguhn, T. A. Verdom, M. Ewert, P. H Seeburg, B. Sakmann, Neuron 5, 781 (1990); T. G. Smart, S J. Moss, X. Xie, R. L. Huganir, Br. J. Pharmacol. 103, 1837 (1991)
50. A. Draguhn, T. A. Verdom, M. Ewert, P. H Seeburg, B. Sakmann, Neuron 5, 781 (1990); T. G. Smart, S J. Moss, X. Xie, R. L. Huganir, Br. J. Pharmacol. 103, 1837 (1991)
51. G. L. Westbrook and M. L. Mayer, Nature 328, 640 (1987); T. G Smart and A. Constanti, Br. J. Pharmacol. 99, 643 (1990); N. L. Harrison and S. J. Gibbons, Neuropharmacology 33, 935 (1994); T. G. Smart, X Xie, B. J. Krishek, Prog Neurobiol. 42, 393 (1994).
52. G. L. Westbrook and M. L. Mayer, Nature 328, 640 (1987); T. G Smart and A. Constanti, Br. J. Pharmacol. 99, 643 (1990); N. L. Harrison and S. J. Gibbons, Neuropharmacology 33, 935 (1994); T. G. Smart, X Xie, B. J. Krishek, Prog Neurobiol. 42, 393 (1994).
53. G. L. Westbrook and M. L. Mayer, Nature 328, 640 (1987); T. G Smart and A. Constanti, Br. J. Pharmacol. 99, 643 (1990); N. L. Harrison and S. J. Gibbons, Neuropharmacology 33, 935 (1994); T. G. Smart, X Xie, B. J. Krishek, Prog Neurobiol. 42, 393 (1994).
54. G. L. Westbrook and M. L. Mayer, Nature 328, 640 (1987); T. G Smart and A. Constanti, Br. J. Pharmacol. 99, 643 (1990); N. L. Harrison and S. J. Gibbons, Neuropharmacology 33, 935 (1994); T. G. Smart, X Xie, B. J. Krishek, Prog Neurobiol. 42, 393 (1994).
55. Y. X. Wang and D. M. Quastel, Pflugers Arch 415, 582 (1990)
56. Y. De Koninck and I Mody, J Neurophysiol. 71, 1318 (1994); I. Soltesz and I. Mody, ibid. 73, 1763 (1995).
57. Y. De Koninck and I Mody, J Neurophysiol. 71, 1318 (1994); I. Soltesz and I. Mody, ibid. 73, 1763 (1995).
58. -1).
59. P Legendre and G. L Westbrook, Mol. Pharmacol. 39, 267 (1991), T G Smart, J. Physiol. London 447, 587 (1992)
60. P Legendre and G. L Westbrook, Mol. Pharmacol. 39, 267 (1991), T G Smart, J. Physiol. London 447, 587 (1992)
61. F. Valdes, R. M. Dasheiff, F. Birmingham, K A. Crutcher, J. O McNamara, Proc. Natl. Acad Sci. U.S.A 79, 193 (1982).
62. M Clark, G. S. Massenburg, S. R. B Weiss, R M Post, Mol Brain Res. 26, 309 (1994); W. Kamphuis, T. C. De Rijk, F. H. Lopes da Silva, Neurosci. Lett 174, 5 (1994); M. Kokaia et al., Mol Brain Res. 23, 323 (1994).
63. M Clark, G. S. Massenburg, S. R. B Weiss, R M Post, Mol Brain Res. 26, 309 (1994); W. Kamphuis, T. C. De Rijk, F. H. Lopes da Silva, Neurosci. Lett 174, 5 (1994); M. Kokaia et al., Mol Brain Res. 23, 323 (1994).
64. M Clark, G. S. Massenburg, S. R. B Weiss, R M Post, Mol Brain Res. 26, 309 (1994); W. Kamphuis, T. C. De Rijk, F. H. Lopes da Silva, Neurosci. Lett 174, 5 (1994); M. Kokaia et al., Mol Brain Res. 23, 323 (1994).
65. N. C. Saxena and R. L. Macdonald, J. Neurosci 14, 7077 (1994): G. White and D. A. Gurley, Neurorepon 6, 461 (1995).
66. N. C. Saxena and R. L. Macdonald, J. Neurosci 14, 7077 (1994): G. White and D. A. Gurley, Neurorepon 6, 461 (1995).
67. 2+ cannot be replenished (C. J. Frederickson, personal communication).
68. D J. Maconochie, J. M. Zempel, J H. Steinbach, Neuron 12, 61 (1994)
69. We thank R. W. Olsen and P Somogyi for critical comments on the manuscript, C. J. Frederickson for technical advice, J. Gruneich for technical assistance, I. Parada for the Timm's staining, and S. Vietla for carrying out some of the zolpidem experiments. This research was supported by National Institute of Neurological Disorders and Stroke grants NS 12151 and NS 30549 (I.M).