Pharmacological preconditioning with GYKI 52466: A prophylactic approach to neuroprotection

Frontiers in Neuroscience

Volumn 4, Issue AUG, 2010, Pages

  Goulton, Chelsea S ^a   Patten, Anna R ^a   Kerr, John R ^a   Kerr, D Steven ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

EEG; GYKI 52466; Metabotropic; Preconditioning; Protection; Seizures

Indexed keywords

EID: 84891155934     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/fnins.2010.00054     Document Type: Article

References (71)

1. Barton, M. E., Peters, S. C., and Shannon, H. E. (2003). Comparison of the effect of glutamate receptor modulators in the 6 Hz and maximal electroshock seizure models. Epilepsy Res. 56, 17-26.
2. Borowicz, K. K., Duda, A. M., Kleinrok, Z., and Czucwar, S. J. (2001). Interaction of GYKI 52466, a selective non- competitive antagonist of AMPA/kainate receptors, with conventional antiepileptic drugs in amygdala-kindled seizures in rats. Polish J. Pharmacol. 53, 101-108.
3. Borowicz, K. K., Gasior, M., Kleinrok, Z., and Czucwar, S. J. (1995). The noncompetitive Ampa/Kainate receptor antagonist, GYKI 52466, potentiates the activity of conventional antiepileptics. Eur. J. Pharmacol. 281, 319-326.
4. Best, N., Sundstrom, L. E., Mitchell, J., and Wheal, H. V. (1996). Pre-exposure to subtoxic levels prevents kainic acid lesions in organotypic hippocampal slice cultures: effects of kainic acid on parvalbumin-immunoreactive neurons and expression of heat shock protein 72 following the induction of tolerance. Eur. J. Neuorsci. 8, 1209-1219.
5. Centeno, J. M., Orti, M., Salom, J. B., Sick, T. J., and Pérez-Pinzon, M. A. (1999). Nitric oxide is involved in anoxic preconditioning neuroprotection in rat hippocampal slices. Brain Res. 836, 62-69.
6. Chang, A. Y., Wang, C. H., Chiu, T. H., Chi, J. W., Chen, C. F., Ho, L. T., and Lin, A. M. (2005). Hypoxic preconditioning attenuated in kainic acid-induced neurotoxicity in rat hippocampus. Exp. Neurol. 195, 40-48.
7. Chauhan, N., Zhao, Z., Barber, P. A., and Buchan, A. M. (2003). Lessons in experimental ischemia for clinical stroke medicine. Curr. Opin. Neurol. 16, 65-71.
8. Clarkson, A., Liu, H., Rahman, R., Appleton, I., Jackson, D., and Kerr, D. S. (2005). Clomethiazole: mechanisms underlying lasting neuroprotection following hypoxia-ischemia. FASEB J. 19, 1036-1038.
9. Cloyd, J., Hauser, W., Towne, A., Ramsay, R., Mattson, R., Gilliam, F., and Walczak, T. (2006). Epidemiological and medical aspects of epilepsy in the elderly. Epilepsy Res. 68S, S39-S48.
10. Cunha, R. A., Malva, J. O., and Ribeiro, J. A. (1999). Kainate receptors coupled to G(i)/G(o) proteins in the rat hippocampus. Mol. Pharmacol. 56, 429-433.
11. Dave, K. R., Lange-Asschenfeldt, C., Raval, A. P., Prado, R., Busto, R., Saul, I., and Perez-Pinzon, M. A. (2005). Ischemic preconditioning ameliorates excitotoxicity by shifting glutamate/gamma-aminobutyric acid release and biosynthesis. J. Neurosci. Res. 82, 665-673.
12. DeCoster, M. A., Mukherjee, P. K., Davis, R. J., and Bazan, N. G. (1998). Platelet-activating factor is a downstream messenger of kainate-induced activation of mitogen-activated protein kinases in primary hippocampal neurons. J. Neurosci. Res. 53, 297-303.
13. De Sarro, A., De Sarro, G., Gitto, R., Grasso, S., Micale, N., Quartaone, S., and Zappala, M. (1998a). 7,8- methylenedioxy-4H-2,3-benzodiazepin-4-ones as novel AMPA receptor antagonists. Bioorg. Med. Chem. Lett. 8, 971-976.
14. De Sarro, G., Rizzo, M., Sinopoli, V. A., Gitto, R., De Sarro, A., Zappala, M., and Chimirri, A. (1998b). Relationship between anticonvulsant activity and plasma level of some 2,3- benzodiazepines in genetically epilepsy-prone rats. Pharmacol. Biochem. Behav. 61, 215-220.
15. De Sarro, G., Ferreri, G., Gareri, P., Russo, E., De Sarro, A., and Gitto, R., and Chimirri, A. (2003). Comparative anticonvulsant activity of some 2,3-benzodiazepine derivatives in rodents. Pharmacol. Biochem. Behav. 74, 595-602.
16. De Sarro, G., Gitto, R., Russo, E., Ibbadu, G.F., Barreca, M.L., De Luca, L., and Chimirri, A. (2005). AMPA receptor antagonists as potential anticonvulsant drugs. Curr. Top. Med. Chem. 5, 31-42.
17. Denes, L., Szilagyi, G., Gal, A., and Nagy, Z. (2006). Talampanel a non-competitive AMPA-antagonist attenuates caspase-3 dependent apoptosis in mouse brain after transient focal cerebral ischemia. Brain Res. Bull. 70, 260-262.
18. Donevan, S. D., and Rogawski, M. A. (1993). Gyki 52466, a 2,3- benzodiazepine, is a highly selective, noncompetitive antagonist of Ampa/Kainate receptor responses. Neuron 10, 51-59.
19. Donevan, S. D., Yamaguchi, S., and Rogawski, M. A. (1994). Non-N-Methyl-d-Aspartate receptor antagonism by 3-N-substituted 2,3-benzodiazepines - Relationship to anticonvulsant activity. J. Pharmacol. Exp. Therap. 271, 25-29.
20. Doyle, K. P., Simon, R. P., and Stenzel-Poore, M. P. (2008). Mechanisms of ischemic brain damage. Neuropharmacology 55, 310-318.
21. Elger, B., Huth, A., Neuhaus, R., Ottow, E., Schneider, H., Seilheimer, B., and Turski, L. (2005). Novel alpha-amino-3-hydroxy-5-methyl-4-isoxazole propionate (AMPA) receptor antagonists of 2,3-benzodiazepine type: chemical synthesis, in vitro characterization, and in vivo prevention of acute neurodegeneration. J. Med. Chem. 48, 4618-4627.
22. El Bahh, B., Lurton, D., Sundstrom, L. E., and Rougier, A. (1997). Induction of tolerance and mossy fibre neuropeptide-Y expression in the contralateral hippocampus following a unilateral intrahippocampal kainic acid injection in the rat. Neurosci. Lett. 227, 135-139.
23. Epsztein, J., Ben-Ari, Y., Represa, A., and Crépel, V. (2008). Late-onset epileptogenesis and seizure genesis: lessons from models of cerebral ischemia. Neuroscientist 14, 78-90.
24. Erdo, F., Berzsenyi, P., and Andrasi, F. (2005). The AMPA-antagonist talampanel is neuroprotective in rodent models of focal cerebral ischemia. Brain Res. Bull. 66, 43-49.
25. Erdo, F., Berzsenyi, P., Nemet, L., and Andrasi, F. (2006). Talampanel improves the functional deficit after transient focal cerebral ischemia in rats. A 30-day follow up study. Brain Res. Bull. 68, 269-276.
26. Fernandes, H. B., Catches, J. S., Petralia, R. S., Copits, B. A., Xu, J., Russell, T. A., Swanson, G. T., and Contractor, A. (2009). High-affinity kainate receptor subunits are necessary for ionotropic but not metabotropic signaling. Neuron 63, 818-829.
27. Gigler, G., Moricz, K., Agoston, M., Simo, A., Albert, M., Benedek, A., Kapus, G., Kertesz, S., Vegh, M., Barkoczy, J., Marko, B., Szabo, G., Matucz, E., Gacsalyi, I., Levay, G., Harsing, L. G. Jr., and Szenasi, G. (2007). Neuroprotective and anticonvulsant effects of EGIS-8332, a non- competitive AMPA receptor antagonist, in a range of animal models. Br. J. Pharmacol. 152, 151-160.
28. Gressens, P., Spedding, M., Gigler, G., Kertesz, S., Villa, P., Medja, F., Williamson, T., Kapus, G., Levay, G., Szenasi, G., Barkoczy, J., and Harsing, L. G. Jr. (2005). The effects of AMPA receptor antagonists in models of stroke and neurodegeneration. Eur. J. Pharmacol. 519, 58-67.
29. Hazell, A. S. (2007). Excitotoxic mechanisms in stroke: an update of concepts and treatment strategies. Neurochem. Int. 50, 941-953.
30. Hesp, B. R., Clarkson, A., Sawant, P. M., and Kerr, D. S. (2007). Domoic acid pre-conditioning and seizure induction in young and aged rats. Epilepsy Res. 76, 103-112.
31. Hesp, B. R., Wrightson, T., Mullaney, I. M., and Kerr, D. S. (2004). Kainate receptors mediate tolerance to kainic acid and reduce high-affinity GTPase activity in young but not aged rat hippocampus. J. Neurochem. 90, 70-79.
32. Jung, Y. S., Lee, B. K., Park, H. S., Shim, J. K., Kim, S. U., Lee, S. H., Baik, E. J., and Moon, C. H. (2005). Activation of protein kinase C-delta attenuates kainate-induced cell death of cortical neurons. Neuroreport 16, 741-744.
33. Kapoor, M., Howard, R., Hall, I., and Appleton, I. (2004). Effects of epicatechin gallate on wound healing and scar formation in a full thickness incisional wound healing model in rats. Am. J. Pathol. 165, 299-307.
34. Karhunen, H., Bezvenyuk, Z., Nissinen, J., Sivenius, J., Jolkkonen, J., and Pitkänen, A. (2007). Epileptogenesis after cortical photothrombotic brain lesion in rats. Neuroscience 148, 314-324.
35. Kerr, D. S. (2007). In vivo pharmacological preconditioning reduces domoic acid- and kainic acid-induced seizures in rats: a role of G protein coupled receptors? ASCEPT Intern. Confer. on Neuropharmacology of Glutamate; Hunter Valley, Newcastle, Australia, July 8-11, 2007.
36. Kerr, D. S., Razak, A., and Crawford, N. (2002). Age-related changes in tolerance to the marine algal excitotoxin domoic acid. Neuropharmacol. 43, 357-366.
37. Kurkinen, K., Busto, R., Goldsteins, G., Koistinaho, J., and Perez-Pinzon, M. A. (2001). Isoform-specific membrane translocation of protein kinase C after ischemic preconditioning. Neurochem. Res. 26, 1139-1144.
38. Lerma, J. (2006), Kainate receptor physiology. Curr. Opin. Pharmacol. 6, 89-97.
39. Lere, C., El Bahh, B., Le Gal La Salle, G., and Rougier, A. (2002). A model of 'epileptic tolerance' for investigating neuroprotection, epileptic susceptibility and gene expression-related plastic changes. Brain Res. Brain Res. Protoc. 9, 49-56.
40. Matucz, E., Moricz, K., Gigler, G., Benedek, A., Barkoczy, J., Levay, G., Harsing, L. G. Jr., and Szenasi, G. (2006). Therapeutic time window of neuroprotection by non-competitive AMPA antagonists in transient and permanent focal cerebral ischemia in rats. Brain Res. 1123, 60-67.
41. Meldrum, B. S. (1993). Excitotoxicity and selective neuronal loss in epilepsy. Brain Pathol. 3, 405-412.
42. Melyan, Z., Wheal, H. V., and Lancaster, B. (2002). Metabotropic-mediated kainate receptor regulation of IsAHP and excitability in pyramidal cells. Neuron 34, 107-114.
43. Naegele, J. R. (2007). Neuroprotective strategies to avert seizure-induced neurodegeneration in epilepsy. Epilepsia 48(Suppl. 2), 107-117.
44. Najm, I. M., Hadam, J., Chakraverty, D., Mikuni, N., Penrod, C., Sopa, C., Markarian, G., Luders, H. O., Babb, T., and Baudry, M. (1998). A short episode of seizure activity protects from status epilepticus-induced neuronal damage in rat brain. Brain Res. 810, 72-75.
45. Newman, M. F., Kirchner, J. L., Phillips-Bute, B., Gaver, V., Grocott, H., Jones, R. H., Mark, D. B., Reves, J. G., and Blumenthal, J. A. (2001). Longitudinal assessment of neurocognitive function after coronary-artery bypass surgery. New England J. Med. 344, 395-402.
46. Perez-Pinzon, M. A. (2007). Mechanisms of neuroprotection during ischemic preconditioning: lessons from anoxic tolerance. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 147, 291-299.
47. Perez-Pinzon, M. A., Born, J. G., and Centeno, J. M. (1999). Calcium and increased excitability promote tolerance against anoxia in hippocampal slices. Brain Res. 833, 20-26.
48. 2+-permeable AMPA receptors induce phosphorylation of cAMP response element-binding protein through a phosphatidylinositol 3-kinase- dependent stimulation of the mitogen-activated protein kinase signaling cascade in neurons. J. Neurosci. 19, 5861-5874.
49. Pitkänen, A., and Sutula, T. P. (2002). Is epilepsy a progressive disorder? Prospects fornew therapeutic approaches in temporal-lobeepilepsy. Lancet Neurol. 1, 173-181.
50. Pohle, W., and Rauca C. (1994). Hypoxia protects against the neurotoxicity of kainic acid. Brain Res. 644, 297-304.
51. Rorick-Kehn, L. M., Hart, J. C., and McKinzie, D. L. (2005). Pharmacological characterization of stress-induced hyperthermia in DBA/2 mice using metabotropic and ionotropic glutamate receptor ligands. Psychopharmacology 183, 226-240.
52. Rodriguez-Moreno, A., Lopez-Garcia, J. C., and Lerma, J. (2000). Two populations of kainate receptors with separate signaling mechanisms in hippocampal interneurons. Proc. Natl. Acad. Sci. U.S.A. 97, 1293-1298.
53. Rodriguez-Moreno, A., and Sihra, T. S. (2004). Presynaptic kainate receptor facilitation of glutamate release involves protein kinase A in the rat hippocampus. J. Physiol. 557, 733-745.
54. Rodriguez-Moreno, A., and Sihra, T. S. (2007). Kainate receptors with a metabotropic modus operandi. Trends Neurosci. 30, 630-637.
55. Rozas, J. L., Paternain, A. V., and Lerma, J. (2003). Noncanonical signaling by ionotropic kainate receptors. Neuron 39, 543-553.
56. Sawant, P. M., Munday, R., Holland, P. T., Mountfort, D. O., and Kerr, D. S. (2008). In vivo studies of seizure induction and pharmacological preconditioning by domoic acid and isodomoic acids A, B and C. Neuropharmacology 55, 1412-1418.
57. Sawant, P. M., Munday, R., Holland, P. T., Mountfort, D. O., and Kerr, D. S. (2010a). Spectral analysis of electrocorticographic activity during pharmacological preconditioning and seizure induction by intrahippocampal domoic acid. Hippocampus 20, 994-1002.
58. Sawant, P. M., Tyndall J. D. A., Holland, P. T., Mountfort, D. O., and Kerr, D. S. (2010b). In vivo seizure induction and affinity studies of domoic acid and isodomoic acids D, E and F. Neuropharmacology 59, 129-138.
59. Sawant, P. M., Weare, B. A., Holland, P. T., Selwood, A. I., King, K. L., Mikulski, C. M., Doucette, G. J., Mountfort, D. O., and Kerr, D. S. (2007). Isodomoic acids A and C exhibit low KA receptor affinity and reduced in vitro potencyin hippocampal region CA1. Toxicon 50, 627-638.
60. Segerstråle, M., Juuri, J., Lanore, F., Piepponen, P., Lauri, S. E., Mulle, C., and Taira, T. (2010). High firing rate of neonatal hippocampal interneurons is caused by attenuation of after hyperpolarizing potassium currents by tonically active kainate receptors. J. Neurosci. 30, 6507-6514.
61. Schurr, A., Payne, R. S., Tseng, M. T., Gozal, E., and Gozal, D. (2001). Excitotoxic preconditioning elicited by both glutamate and hypoxia and abolished by lactate transport inhibition in rat hippocampal slices. Neurosci. Lett. 307, 151-154.
62. Sloviter, R. S. (1987). Decreased hippocampal inhibition and a selective loss of interneurons in experimental epilepsy. Science 235, 73-76.
63. Smith, S. E., Dürmüller, N., and Meldrum, B. S. (1991). The non-N-methyl-d-aspartate receptor antagonists, GYKI 52466 and NBQX are anticonvulsant in two animal models of reflex epilepsy. Eur. J. Pharmacol. 201, 179-183.
64. Sundquist, S. J., and Nisenbaum, L. K. (2005). Fast Fos: rapid protocols for single- and double-labeling c-Fos immunohistochemistry in fresh frozen brain sections. J. Neurosci. Meth. 141, 9-20.
65. Szabados, T., Gigler, G., Gacsályi, I., Gyertyán, I., and Lévay, G. (2001). Comparison of anticonvulsive and acute neuroprotective activity of three 2,3-benzodiazepine compounds, GYKI 52466, GYKI 53405, and GYKI 53655. Brain Res. Bull. 55, 387-391.
66. Tandon, P., Yang, Y., Stafstrom, C. E., and Holmes, G. L. (2002). Downregulation of kainate receptors in the hippocampus following repeated seizures in immature rats. Dev. Brain Res. 136, 145-150.
67. Wang, C. H., Chang, A., Tsai, M. J., Cheng, H., Liao, L. P., and Lin, A. M. (2005). Kainic acid-induced oxidative injury is attenuated by hypoxic preconditioning. Ann. N.Y. Acad. Sci. 1042, 314-324.
68. Wang, Y. Z., and Durkin, J. P. (1995). alpha-Amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid, but not N-methyl-d-aspartate, activates mitogen-activated protein kinase through G-protein beta gamma subunits in rat cortical neurons.. J. Biol. Chem. 270, 22783-22787.
69. Weiczner, R., Krisztin-Péva, B., and Mihály, A. (2008). Blockade of AMPA-receptors attenuates 4- aminopyridine seizures, decreases the activation of inhibitory neurons but is ineffective against seizure-related astrocytic swelling. Epilepsy Res. 78, 22-32.
70. Youssef, F. F., Addae, J. I., McRae, A., and Stone. T. W. (2001). Long-term potentiation protects rat hippocampal slices from the effects of acute hypoxia. Brain Res. 907, 144-150.
71. Zorumski, C. F., Yamada, K. A., Price, M. T., and Olney, J. W. (1993). A benzodiazepine recognition site associated with the non-NMDA glutamate receptor. Neuron 10, 61-67.