Mechanism of inhibition of the GluA2 AMPA receptor channel opening by talampanel and its enantiomer: The stereochemistry of the 4-methyl group on the diazepine ring of 2,3-benzodiazepine derivatives

ACS Chemical Neuroscience

Volumn 4, Issue 4, 2013, Pages 635-644

  Wang, Congzhou ^a   Niu, Li ^a  

^a STATE UNIVERSITY OF NEW YORK   (United States)

Author keywords

2,3 benzodiazepine compounds; AMPA receptors; stereoselectivity; structure activity relationship; Talampanel

Indexed keywords

1 (4 AMINOPHENYL) 4 METHYL 7,8 METHYLENEDIOXY 5H 2,3 BENZODIAZEPINE; AMPA RECEPTOR; BENZODIAZEPINE DERIVATIVE; DIAZEPINE DERIVATIVE; GLUTAMATE RECEPTOR 1; GLUTAMATE RECEPTOR 2; GLUTAMATE RECEPTOR 3; GLUTAMATE RECEPTOR 4; TALAMPANEL;

ACYLATION; ARTICLE; CONTROLLED STUDY; DRUG BINDING; DRUG SELECTIVITY; DRUG STRUCTURE; ENANTIOMER; HUMAN; HUMAN CELL; ISOMERIZATION; PHOTOLYSIS; PRIORITY JOURNAL; STEREOCHEMISTRY;

BENZODIAZEPINES; HEK293 CELLS; HUMANS; RECEPTORS, AMPA; STEREOISOMERISM; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84876573575     PISSN: None     EISSN: 19487193     Source Type: Journal    
DOI: 10.1021/cn3002398     Document Type: Article

References (63)

1. Huang, Q., He, R., and Kozikowski, A. P. (2011) Stereochemistry at the forefront in the design and discovery of novel anti-tuberculosis agents Curr. Top. Med. Chem. 11, 810-818
2. McConnell, O., Bach, A., 2nd, Balibar, C., Byrne, N., Cai, Y., Carter, G., Chlenov, M., Di, L., Fan, K., Goljer, I., He, Y., Herold, D., Kagan, M., Kerns, E., Koehn, F., Kraml, C., Marathias, V., Marquez, B., McDonald, L., Nogle, L., Petucci, C., Schlingmann, G., Tawa, G., Tischler, M., Williamson, R. T., Sutherland, A., Watts, W., Young, M., Zhang, M. Y., Zhang, Y., Zhou, D., and Ho, D. (2007) Enantiomeric separation and determination of absolute stereochemistry of asymmetric molecules in drug discovery: building chiral technology toolboxes Chirality 19, 658-682
3. Dingledine, R., Borges, K., Bowie, D., and Traynelis, S. F. (1999) The glutamate receptor ion channels Pharmacol. Rev. 51, 7-61
4. Traynelis, S. F., Wollmuth, L. P., McBain, C. J., Menniti, F. S., Vance, K. M., Ogden, K. K., Hansen, K. B., Yuan, H., Myers, S. J., and Dingledine, R. (2010) Glutamate receptor ion channels: structure, regulation, and function Pharmacol. Rev. 62, 405-496
5. Chapman, A. G. (1998) Glutamate receptors in epilepsy Prog. Brain Res. 116, 371-383
6. Meldrum, B. S., Akbar, M. T., and Chapman, A. G. (1999) Glutamate receptors and transporters in genetic and acquired models of epilepsy Epilepsy Res. 36, 189-204
7. Kawahara, Y. and Kwak, S. (2005) Excitotoxicity and ALS: what is unique about the AMPA receptors expressed on spinal motor neurons? Amyotrophic Lateral Scler. Other Mot. Neuron Disord. 6, 131-144
8. Kwak, S., Hideyama, T., Yamashita, T., and Aizawa, H. (2010) AMPA receptor-mediated neuronal death in sporadic ALS Neuropathology 30, 182-188
9. Klockgether, T., Turski, L., Honore, T., Zhang, Z. M., Gash, D. M., Kurlan, R., and Greenamyre, J. T. (1991) The AMPA receptor antagonist NBQX has antiparkinsonian effects in monoamine-depleted rats and MPTP-treated monkeys Ann. Neurol. 30, 717-723
10. Tarnawa, I., Farkas, S., Berzsenyi, P., Pataki, A., and Andrasi, F. (1989) Electrophysiological studies with a 2,3-benzodiazepine muscle relaxant: GYKI 52466 Eur. J. Pharmacol. 167, 193-199
11. Solyom, S. and Tarnawa, I. (2002) Non-competitive AMPA antagonists of 2,3-benzodiazepine type Curr. Pharm. Des. 8, 913-939
12. Szenasi, G., Vegh, M., Szabo, G., Kertesz, S., Kapus, G., Albert, M., Greff, Z., Ling, I., Barkoczy, J., Simig, G., Spedding, M., and Harsing, L. G., Jr. (2008) 2,3-Benzodiazepine-type AMPA receptor antagonists and their neuroprotective effects Neurochem. Int. 52, 166-183
13. De Sarro, A., De Sarro, G., Gitto, R., Grasso, S., Micale, N., Quartarone, S., and Zappala, M. (1998) 7,8-Methylenedioxy-4H-2,3-benzodiazepin- 4-ones as novel AMPA receptor antagonists Bioorg. Med. Chem. Lett. 8, 971-976
14. Grasso, S., De Sarro, G., De Sarro, A., Micale, N., Zappala, M., Puia, G., Baraldi, M., and De Micheli, C. (1999) Synthesis and anticonvulsant activity of novel and potent 2,3-benzodiazepine AMPA/kainate receptor antagonists J. Med. Chem. 42, 4414-4421
15. Ritz, M., Wang, C., Micale, N., Ettari, R., and Niu, L. (2011) Mechanism of Inhibition of the GluA2 AMPA Receptor Channel Opening: The Role of 4-Methyl versus 4-Carbonyl Group on the Diazepine Ring of 2,3-Benzodiazepine Derivatives ACS Chem. Neurosci. 2, 506-513
16. Wang, C., Sheng, Z., and Niu, L. (2011) Mechanism of Inhibition of the GluA2 AMPA Receptor Channel Opening: Consequences of Adding an N-3 Methylcarbamoyl Group to the Diazepine Ring of 2,3-Benzodiazepine Derivatives Biochemistry 50, 7284-7293
17. Horváth, K., Szabó, H., Pátfalusi, M., Berzsenyi, P., and Andrási, F. (1990) Pharmacological effects of GYMI 52 895, a new selective dopamine uptake Inhibitor Eur. J. Pharmacol. 183, 1416-1417
18. May, P. C., Robison, P. M., and Fuson, K. S. (1999) Stereoselective neuroprotection by novel 2,3-benzodiazepine non-competitive AMPA antagonist against non-NMDA receptor-mediated excitotoxicity in primary rat hippocampal cultures Neurosci. Lett. 262, 219-221
19. Bleakman, D., Ballyk, B. A., Schoepp, D. D., Palmer, A. J., Bath, C. P., Sharpe, E. F., Woolley, M. L., Bufton, H. R., Kamboj, R. K., Tarnawa, I., and Lodge, D. (1996) Activity of 2,3-benzodiazepines at native rat and recombinant human glutamate receptors in vitro: stereospecificity and selectivity profiles Neuropharmacology 35, 1689-1702
20. Howes, J. F. and Bell, C. (2007) Talampanel Neurotherapeutics 4, 126-129
21. Szabo, G. and Henley, J. M. (1993) Binding of the AMPA receptor antagonist [3H]GYKI 53405 to Xenopus brain membranes NeuroReport 5, 93-94
22. 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. Ther. 271, 25-29
23. Lodge, D., Bond, A., O'Neill, M. J., Hicks, C. A., and Jones, M. G. (1996) Stereoselective effects-of 2,3-benzodiazepines in vivo: electrophysiology and neuroprotection studies Neuropharmacology 35, 1681-1688
24. Chappell, A. S., Sander, J. W., Brodie, M. J., Chadwick, D., Lledo, A., Zhang, D., Bjerke, J., Kiesler, G. M., and Arroyo, S. (2002) A crossover, add-on trial of talampanel in patients with refractory partial seizures Neurology 58, 1680-1682
25. 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
26. 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
27. Aujla, P. K., Fetell, M. R., and Jensen, F. E. (2009) Talampanel suppresses the acute and chronic effects of seizures in a rodent neonatal seizure model Epilepsia 50, 694-701
28. Langan, Y. M., Lucas, R., Jewell, H., Toublanc, N., Schaefer, H., Sander, J. W., and Patsalos, P. N. (2003) Talampanel, a new antiepileptic drug: single- and multiple-dose pharmacokinetics and initial 1-week experience in patients with chronic intractable epilepsy Epilepsia 44, 46-53
29. Traynor, B. J., Bruijn, L., Conwit, R., Beal, F., O'Neill, G., Fagan, S. C., and Cudkowicz, M. E. (2006) Neuroprotective agents for clinical trials in ALS: a systematic assessment Neurology 67, 20-27
30. Pascuzzi, R. M., Shefner, J., Chappell, A. S., Bjerke, J. S., Tamura, R., Chaudhry, V., Clawson, L., Haas, L., and Rothstein, J. D. (2010) A phase II trial of talampanel in subjects with amyotrophic lateral sclerosis Amyotroph Lateral Scler. 11, 266-271
31. Ishiuchi, S., Tsuzuki, K., Yoshida, Y., Yamada, N., Hagimura, N., Okado, H., Miwa, A., Kurihara, H., Nakazato, Y., Tamura, M., Sasaki, T., and Ozawa, S. (2002) Blockage of Ca(2+)-permeable AMPA receptors suppresses migration and induces apoptosis in human glioblastoma cells Nat. Med. 8, 971-978
32. Iwamoto, F. M., Kreisl, T. N., Kim, L., Duic, J. P., Butman, J. A., Albert, P. S., and Fine, H. A. (2010) Phase 2 trial of talampanel, a glutamate receptor inhibitor, for adults with recurrent malignant gliomas Cancer 116, 1776-1782
33. Ritz, M., Micale, N., Grasso, S., and Niu, L. (2008) Mechanism of inhibition of the GluR2 AMPA receptor channel opening by 2,3-benzodiazepine derivatives Biochemistry 47, 1061-1069
34. Qneibi, M. S., Micale, N., Grasso, S., and Niu, L. (2012) Mechanism of Inhibition of the GluA2 AMPA Receptor Channel Opening by 2,3-Benzodiazepine Derivatives: Functional Consequences of Replacing 7,8-Methylenedioxy with 7,8-Ethylenedioxy Moiety Biochemistry 51, 1787-1795
35. Sommer, B., Keinanen, K., Verdoorn, T. A., Wisden, W., Burnashev, N., Herb, A., Kohler, M., Takagi, T., Sakmann, B., and Seeburg, P. H. (1990) Flip and flop: a cell-specific functional switch in glutamate-operated channels of the CNS Science 249, 1580-1585
36. Mosbacher, J., Schoepfer, R., Monyer, H., Burnashev, N., Seeburg, P. H., and Ruppersberg, J. P. (1994) A molecular determinant for submillisecond desensitization in glutamate receptors Science 266, 1059-1062
37. Koike, M., Tsukada, S., Tsuzuki, K., Kijima, H., and Ozawa, S. (2000) Regulation of kinetic properties of GluR2 AMPA receptor channels by alternative splicing J. Neurosci. 20, 2166-2174
38. Partin, K. M., Patneau, D. K., and Mayer, M. L. (1994) Cyclothiazide differentially modulates desensitization of alpha-amino-3-hydroxy-5-methyl-4- isoxazolepropionic acid receptor splice variants Mol. Pharmacol. 46, 129-138
39. Kessler, M., Rogers, G., and Arai, A. (2000) The norbornenyl moiety of cyclothiazide determines the preference for flip-flop variants of AMPA receptor subunits Neurosci. Lett. 287, 161-165
40. Pei, W., Huang, Z., Wang, C., Han, Y., Park, J. S., and Niu, L. (2009) Flip and flop: a molecular determinant for AMPA receptor channel opening Biochemistry 48, 3767-3777
41. Wieboldt, R., Gee, K. R., Niu, L., Ramesh, D., Carpenter, B. K., and Hess, G. P. (1994) Photolabile precursors of glutamate: synthesis, photochemical properties, and activation of glutamate receptors on a microsecond time scale Proc. Natl. Acad. Sci. U.S.A. 91, 8752-8756
42. Li, G., Pei, W., and Niu, L. (2003) Channel-opening kinetics of GluR2Q(flip) AMPA receptor: a laser-pulse photolysis study Biochemistry 42, 12358-12366
43. Sundaresan, V. and Abrol, R. (2002) Towards a general model for protein-substrate stereoselectivity Protein Sci. 11, 1330-1339
44. Mesecar, A. D. and Koshland, D. E., Jr. (2000) A new model for protein stereospecificity Nature 403, 614-615
45. Grimm, H. G. (1925) Structure and Size of the Non-metallic Hydrides Z Electrochemistry 474-480
46. Sun, H., Kawahara, Y., Ito, K., Kanazawa, I., and Kwak, S. (2006) Slow and selective death of spinal motor neurons in vivo by intrathecal infusion of kainic acid: implications for AMPA receptor-mediated excitotoxicity in ALS J. Neurochem. 98, 782-791
47. Spalloni, A., Pascucci, T., Albo, F., Ferrari, F., Puglisi-Allegra, S., Zona, C., Bernardi, G., and Longone, P. (2004) Altered vulnerability to kainate excitotoxicity of transgenic-Cu/Zn SOD1 neurones NeuroReport 15, 2477-2480
48. Rembach, A., Turner, B. J., Bruce, S., Cheah, I. K., Scott, R. L., Lopes, E. C., Zagami, C. J., Beart, P. M., Cheung, N. S., Langford, S. J., and Cheema, S. S. (2004) Antisense peptide nucleic acid targeting GluR3 delays disease onset and progression in the SOD1 G93A mouse model of familial ALS J. Neurosci. Res. 77, 573-582
49. Tortarolo, M., Grignaschi, G., Calvaresi, N., Zennaro, E., Spaltro, G., Colovic, M., Fracasso, C., Guiso, G., Elger, B., Schneider, H., Seilheimer, B., Caccia, S., and Bendotti, C. (2006) Glutamate AMPA receptors change in motor neurons of SOD1G93A transgenic mice and their inhibition by a noncompetitive antagonist ameliorates the progression of amytrophic lateral sclerosis-like disease J. Neurosci. Res. 83, 134-146
50. Van Den Bosch, L., Van Damme, P., Bogaert, E., and Robberecht, W. (2006) The role of excitotoxicity in the pathogenesis of amyotrophic lateral sclerosis Biochim. Biophys. Acta 1762, 1068-1082
51. Van Damme, P., Leyssen, M., Callewaert, G., Robberecht, W., and Van Den Bosch, L. (2003) The AMPA receptor antagonist NBQX prolongs survival in a transgenic mouse model of amyotrophic lateral sclerosis Neurosci. Lett. 343, 81-84
52. Rothstein, J. D., Jin, L., Dykes-Hoberg, M., and Kuncl, R. W. (1993) Chronic inhibition of glutamate uptake produces a model of slow neurotoxicity Proc. Natl. Acad. Sci. U.S.A. 90, 6591-6595
53. Leitereg, T. J., Guadagni, D. G., Harris, J., Mon, T. R., and Teranishi, R. (1971) Chemical and sensory data supporting the difference between the odors of the enantiomeric carvones J. Agric. Food Chem. 19, 3
54. Gray, S. R., Batstone, F. R., Santiapillai, N. F., and Richardson, P. J. (1991) Solubilization and purification of a putative quisqualate-sensitive glutamate receptor from crustacean muscle Biochem. J. 273 (Pt 1) 165-171
55. James, V. A., Walker, R. J., and Wheal, H. V. (1980) Structure-activity studies on an excitatory receptor for glutamate on leech Retzius neurones Br. J. Pharmacol. 68, 711-717
56. Chang, H. H. and Michaelis, E. K. (1981) L-glutamate stimulation of Na+ efflux from brain synaptic membrane vesicles J. Biol. Chem. 256, 10084-10087
57. Li, G. and Niu, L. (2004) How fast does the GluR1Qflip channel open? J. Biol. Chem. 279, 3990-3997
58. Pei, W., Huang, Z., and Niu, L. (2007) GluR3 Flip and Flop: Differences in Channel-Opening Kinetics Biochemistry 46, 2027-2036
59. Li, G., Sheng, Z., Huang, Z., and Niu, L. (2005) Kinetic mechanism of channel opening of the GluRDflip AMPA receptor Biochemistry 44, 5835-5841
60. Chen, C. and Okayama, H. (1987) High-efficiency transformation of mammalian cells by plasmid DNA Mol. Cell. Biol. 7, 2745-2752
61. Huang, Z., Li, G., Pei, W., Sosa, L. A., and Niu, L. (2005) Enhancing protein expression in single HEK 293 cells J. Neurosci. Methods 142, 159-166
62. Udgaonkar, J. B. and Hess, G. P. (1987) Chemical kinetic measurements of a mammalian acetylcholine receptor by a fast-reaction technique Proc. Natl. Acad. Sci. U.S.A. 84, 8758-8762
63. Han, Y., Wang, C., Park, J. S., and Niu, L. (2012) Channel-Opening Kinetic Mechanism of Wild-Type GluK1 Kainate Receptors and a C-Terminal Mutant Biochemistry 51, 761-768