Mechanism and site of inhibition of AMPA receptors: Pairing a thiadiazole with a 2,3-benzodiazepine scaffold

ACS Chemical Neuroscience

Volumn 5, Issue 2, 2014, Pages 138-147

  Wang, Congzhou ^a   Han, Yan ^a,c   Wu, Andrew ^a   Sólyom, Sándor ^b   Niu, Li ^a  

^a STATE UNIVERSITY OF NEW YORK   (United States)

^b CF Pharma Ltd   (Hungary)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

AMPA receptors; mechanism of inhibition; thiadiazolyl benzodiazepine compounds

Indexed keywords

BENZODIAZEPINES; BINDING SITES; HEK293 CELLS; HUMANS; RECEPTORS, AMPA; STRUCTURE-ACTIVITY RELATIONSHIP; THIADIAZOLES;

EID: 84894468158     PISSN: None     EISSN: 19487193     Source Type: Journal    
DOI: 10.1021/cn400193u     Document Type: Article

References (58)

1. 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
2. Solyom, S. and Tarnawa, I. (2002) Non-competitive AMPA antagonists of 2,3-benzodiazepine type Curr. Pharm. Des. 8, 913-939
3. Zappala, M., Pellicano, A., Micale, N., Menniti, F. S., Ferreri, G., De Sarro, G., Grasso, S., and De Micheli, C. (2006) New 7,8-ethylenedioxy-2,3- benzodiazepines as noncompetitive AMPA receptor antagonists Bioorg. Med. Chem. Lett. 16, 167-170
4. Zappala, M., Grasso, S., Micale, N., Polimeni, S., and De Micheli, C. (2001) Synthesis and structure-activity relationships of 2,3-benzodiazepines as AMPA receptor antagonists Mini Rev. Med. Chem. 1, 243-253
5. Honore, T., Davies, S. N., Drejer, J., Fletcher, E. J., Jacobsen, P., Lodge, D., and Nielsen, F. E. (1988) Quinoxalinediones: potent competitive non-NMDA glutamate receptor antagonists Science 241, 701-703
6. Turski, L., Huth, A., Sheardown, M., McDonald, F., Neuhaus, R., Schneider, H. H., Dirnagl, U., Wiegand, F., Jacobsen, P., and Ottow, E. (1998) ZK200775: a phosphonate quinoxalinedione AMPA antagonist for neuroprotection in stroke and trauma Proc. Natl. Acad. Sci. U.S.A. 95, 10960-10965
7. Stromgaard, K. and Mellor, I. (2004) AMPA receptor ligands: synthetic and pharmacological studies of polyamines and polyamine toxins Med. Res. Rev. 24, 589-620
8. Chapman, A. G., al-Zubaidy, Z., and Meldrum, B. S. (1993) Aniracetam reverses the anticonvulsant action of NBQX and GYKI 52466 in DBA/2 mice Eur. J. Pharmacol. 231, 301-303
9. Smith, S. E., Durmuller, 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
10. Chapman, A. G., Smith, S. E., and Meldrum, B. S. (1991) The anticonvulsant effect of the non-NMDA antagonists, NBQX and GYKI 52466, in mice Epilepsy Res 9, 92-96
11. 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
12. Smith, S. E. and Meldrum, B. S. (1992) Cerebroprotective effect of a non-N-methyl-D-aspartate antagonist, GYKI 52466, after focal ischemia in the rat Stroke 23, 861-864
13. Le Peillet, E., Arvin, B., Moncada, C., and Meldrum, B. S. (1992) The non-NMDA antagonists, NBQX and GYKI 52466, protect against cortical and striatal cell loss following transient global ischaemia in the rat Brain Res. 571, 115-120
14. Hollmann, M. and Heinemann, S. (1994) Cloned glutamate receptors Annu. Rev. Neurosci. 17, 31-108
15. Dingledine, R., Borges, K., Bowie, D., and Traynelis, S. F. (1999) The glutamate receptor ion channels Pharmacol. Rev. 51, 7-61
16. 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
17. Contractor, A., Mulle, C., and Swanson, G. T. (2011) Kainate receptors coming of age: milestones of two decades of research Trends Neurosci. 34, 154-163
18. Rezessy, B. and Sólyom, S. (2004) Advanced Pharmacophore Model of Non-Competitive AMPA Antagonist 2,3-benzodiazepines Lett. Drug Des. Discovery 1, 217-223
19. Abraham, G., Sólyom, S., Csuzdi, E., Berzsenyi, P., Ling, I., Tarnawa, I., Hamori, T., Pallagi, I., Horvath, K., Andrasi, F., Kapus, G., Harsing, L. G., Jr., Kiraly, I., Patthy, M., and Horvath, G. (2000) New non competitive AMPA antagonists Bioorg. Med. Chem. 8, 2127-2143
20. Solyom, S., Abraham, G., Hamori, T., Berzsenyl, P., Andrasi, F., and Kurucz, I. (2005) Substituted 2,3-benzodiazepine derivatives. U.S. Patent 6858605, February 22.
21. Solyom, S., Abraham, G., Hamori, T., Berzsenyl, P., Andrasi, F., and Kurucz, I. (2007) Novel substituted 2,3-benzodiazepine derivatives. U.S. Patent Application 2007027143 A1, February 1.
22. Wang, C. and Niu, L. (2013) 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 Chem. Neurosci. 4, 635-644
23. 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
24. Sommer, B., Kohler, M., Sprengel, R., and Seeburg, P. H. (1991) RNA editing in brain controls a determinant of ion flow in glutamate-gated channels Cell 67, 11-19
25. 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
26. 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
27. Park, J. S., Wang, C., Han, Y., Huang, Z., and Niu, L. (2011) Potent and selective inhibition of a single alpha-amino-3-hydroxy-5-methyl-4- isoxazolepropionic acid (AMPA) receptor subunit by an RNA aptamer J. Biol. Chem. 286, 15608-15617
28. Huang, Z., Han, Y., Wang, C., and Niu, L. (2010) Potent and selective inhibition of the open-channel conformation of AMPA receptors by an RNA aptamer Biochemistry 49, 5790-5798
29. 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
30. 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
31. Domingues, A., Cunha Oliveira, T., Laco, M. L., Macedo, T. R., Oliveira, C. R., and Rego, A. C. (2006) Expression of NR1/NR2B N-methyl-D-aspartate receptors enhances heroin toxicity in HEK293 cells Ann. N.Y. Acad. Sci. 1074, 458-465
32. 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
33. 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
34. Burnashev, N., Monyer, H., Seeburg, P. H., and Sakmann, B. (1992) Divalent ion permeability of AMPA receptor channels is dominated by the edited form of a single subunit Neuron 8, 189-198
35. Lomeli, H., Mosbacher, J., Melcher, T., Hoger, T., Geiger, J. R., Kuner, T., Monyer, H., Higuchi, M., Bach, A., and Seeburg, P. H. (1994) Control of kinetic properties of AMPA receptor channels by nuclear RNA editing Science 266, 1709-1713
36. Seeburg, P. H. (1996) The role of RNA editing in controlling glutamate receptor channel properties J. Neurochem. 66, 1-5
37. Greger, I. H., Khatri, L., Kong, X., and Ziff, E. B. (2003) AMPA receptor tetramerization is mediated by Q/R editing Neuron 40, 763-774
38. Pellegrini-Giampietro, D. E., Bennett, M. V., and Zukin, R. S. (1992) Are Ca(2+)-permeable kainate/AMPA receptors more abundant in immature brain? Neurosci. Lett. 144, 65-69
39. Carlson, N. G., Howard, J., Gahring, L. C., and Rogers, S. W. (2000) RNA editing (Q/R site) and flop/flip splicing of AMPA receptor transcripts in young and old brains Neurobiol. Aging 21, 599-606
40. Rogers, S. W., Hughes, T. E., Hollmann, M., Gasic, G. P., Deneris, E. S., and Heinemann, S. (1991) The characterization and localization of the glutamate receptor subunit GluR1 in the rat brain J. Neurosci. 11, 2713-2724
41. Lu, W., Shi, Y., Jackson, A. C., Bjorgan, K., During, M. J., Sprengel, R., Seeburg, P. H., and Nicoll, R. A. (2009) Subunit composition of synaptic AMPA receptors revealed by a single-cell genetic approach Neuron 62, 254-268
42. Kwak, S., Hideyama, T., Yamashita, T., and Aizawa, H. (2010) AMPA receptor-mediated neuronal death in sporadic ALS Neuropathology 30, 182-188
43. Castro, A., Castano, T., Encinas, A., Porcal, W., and Gil, C. (2006) Advances in the synthesis and recent therapeutic applications of 1,2,4-thiadiazole heterocycles Bioorg. Med. Chem. 14, 1644-1652
44. Tripathy, R., Ghose, A., Singh, J., Bacon, E. R., Angeles, T. S., Yang, S. X., Albom, M. S., Aimone, L. D., Herman, J. L., and Mallamo, J. P. (2007) 1,2,3-Thiadiazole substituted pyrazolones as potent KDR/VEGFR-2 kinase inhibitors Bioorg. Med. Chem. Lett. 17, 1793-1798
45. Kumar, D., Maruthi Kumar, N., Chang, K. H., and Shah, K. (2010) Synthesis and anticancer activity of 5-(3-indolyl)-1,3,4-thiadiazoles Eur. J. Med. Chem. 45, 4664-4668
46. Katz, I. M., Hubbard, W. A., Getson, A. J., and Gould, A. L. (1976) Intraocular pressure decrease in normal volunteers following timolol ophthalmic solution Invest. Ophthalmol. 15, 489-492
47. Volotinen, M., Hakkola, J., Pelkonen, O., Vapaatalo, H., and Maenpaa, J. (2011) Metabolism of ophthalmic timolol: new aspects of an old drug Basic Clin. Pharmacol. Toxicol. 108, 297-303
48. 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
49. Mansour, M., Nagarajan, N., Nehring, R. B., Clements, J. D., and Rosenmund, C. (2001) Heteromeric AMPA receptors assemble with a preferred subunit stoichiometry and spatial arrangement Neuron 32, 841-853
50. Burnashev, N., Villarroel, A., and Sakmann, B. (1996) Dimensions and ion selectivity of recombinant AMPA and kainate receptor channels and their dependence on Q/R site residues J. Physiol. 496, 165-173
51. Verdoorn, T. A., Burnashev, N., Monyer, H., Seeburg, P. H., and Sakmann, B. (1991) Structural determinants of ion flow through recombinant glutamate receptor channels Science 252, 1715-1718
52. Smothers, C. T., Clayton, R., Blevins, T., and Woodward, J. J. (2001) Ethanol sensitivity of recombinant human N -methyl- d -aspartate receptors Neurochem. Int. 38, 333-340
53. 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
54. Li, G., Oswald, R. E., and Niu, L. (2003) Channel opening kinetics of GluR6 kainate receptor Biochemistry 42, 12367-12375
55. Li, G. and Niu, L. (2004) How fast does the GluR1Qflip channel open? J. Biol. Chem. 279, 3990-3997
56. Pei, W., Huang, Z., and Niu, L. (2007) GluR3 Flip and Flop: Differences in Channel-Opening Kinetics Biochemistry 46, 2027-2036
57. Li, G., Sheng, Z., Huang, Z., and Niu, L. (2005) Kinetic mechanism of channel opening of the GluRDflip AMPA receptor Biochemistry 44, 5835-5841
58. Pei, W., Ritz, M., McCarthy, M., Huang, Z., and Niu, L. (2007) Receptor occupancy and channel-opening kinetics: a study of GluR1 L497Y AMPA receptor J. Biol. Chem. 282, 22731-22736