Advertisement

Neurochemical Journal

, Volume 12, Issue 4, pp 337–346 | Cite as

The Neurochemical Mechanisms of the Pharmacological Activities of Inverse Agonists of the Benzodiazepine Binding Site

  • A. I. GolovkoEmail author
  • M. B. Ivanov
  • E. S. Golovko
  • V. B. Dolgo-Saburov
  • E. P. Zatsepin
Review Articles
  • 12 Downloads

Abstract

Data on the basal (constitutive or spontaneous) activities of receptors, as well as their neurochemical and electrophysiological correlates, are presented. Inverse receptor agonists are a group of pharmacological drugs that can suppress constitutive activities. We describe the neurochemical mechanisms of the pharmacological activities of benzodiazepine binding site inverse agonists. These compounds inhibit chloride currents caused by gamma-aminobutyric acid at low non-physiological concentrations. This activity is the basis of the sobering action during the action of ethanol and the ability to suppress the addictive potential of psychoactive substances. In addition, the benzodiazepine binding site inverse agonists are able to activate memory formation processes and improve learning. The possible uses of drugs from this group in modern medicine are discussed. They may be used to treat a number of diseases in the fields of narcology, therapy, neurology, and psychiatry.

Keywords

inverse agonists for the benzodiazepine binding site reduction of the intoxicating effects of ethanol decrease in addictive potential of psychoactive substances accelerated learning and memory antidepressant actions 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Atack, J.R., Maubach, K.A., Wafford, K.A., O’Connor, D., Rodrigues, A.D., Evans, D.C., Tattersall, F.D., and Chambers, M.S., Macleod A.M., Eng, W.S., Ryan, C., Hostetler, E., Sanabria, S.M., Gibson, R.E., Krause, S., Burns, H.D., Hargreaves, R.J., Agrawal, N.G., McKernan, R.M., Murphy, M.G., Gingrich, K., Dawson, G.R., Musson, D.G., and Petty, K.J., J. Pharmacol. Exp. Ther., 2009, vol. 331, no. 2, pp. 470–484.Google Scholar
  2. 2.
    Braudeau, J., Delatour, B., Duchon, A., Pereira, P.L., Dauphinot, L., de Chaumont, F., Olivo-Marin, J.C., Dodd, R.H., Hérault, Y., and Potier, M.C., J. Psychopharmacol., 2011, vol. 25, no. 8, pp. 1030–1042.Google Scholar
  3. 3.
    Sato, J., Makita, N., and Iiri, T., Endocr. J., 2016, vol. 63, no. 6, pp. 507–514.Google Scholar
  4. 4.
    Bhowmik, M., Khanam, R., and Vohora, D., Br. J. Pharmacol., 2012, vol. 167, no. 7, pp. 1398–1414.Google Scholar
  5. 5.
    Monczor, F., Fernandez, N., Fitzsimons, C.P., Shayo, C., and Davio, C., Eur. J. Pharmacol., 2013, vol. 715, nos. 1–3, pp. 26–32.Google Scholar
  6. 6.
    Corder, G., Doolen, S., Donahue, R.R., Winter, M.K., Jutras, B.L., He, Y., Hu, X., Wieskopf, J.S., Mogil, J.S., Storm, D.R., Wang, Z.J., McCarson, K.E., and Taylor, B.K., Science, 2013, vol. 341, no. 6152, pp. 1394–1399.Google Scholar
  7. 7.
    Polter, A.M., Barcomb, K., Chen, R.W., Dingess, P.M., Graziane, N.M., Brown, T.E., and Kauer, J.A., Elife, 2017, vol. 6, article e23785.Google Scholar
  8. 8.
    Arrang, J.M., Morisset, S., and Gbahou, F., Trends Pharmacol. Sci., 2007, vol. 28, no. 7, pp. 350–357.Google Scholar
  9. 9.
    Morisset, S., Rouleau, A., Ligneau, X., Gbahou, F., Tardivel-Lacombe, J., Stark, H., Schunack, W., Ganellin, C.R., Schwartz, J.C., and Arrang, J.M., Nature, 2000, vol. 408, no. 6814, pp. 860–864.Google Scholar
  10. 10.
    Rouleau, A., Ligneau, X., Tardivel-Lacombe, J., Morisset, S., Gbahou, F., Schwartz, J.C., and Arrang, J.M., Br. J. Pharmacol., 2002, vol. 135, no. 2, pp. 383–392.Google Scholar
  11. 11.
    Meye, F.J., Ramakers, G.M., and Adan, R.A., Transl. Psychiatry, 2014, vol.4.Google Scholar
  12. 12.
    Bond, R.A., Leff, P., Johnson, T.D., Milano, C.A., Rockman, H.A., McMinn, T.R., Apparsundaram, S., Hyek, M.F., Kenakin, T.P., Allen, L.F., and Lefkowitz, R.J., Nature, 1995, vol. 374, no. 6519, pp. 272–276.Google Scholar
  13. 13.
    Walwyn, W.M., Chen, W., Kim, H., Minasyan, A., Ennes, H.S., McRoberts, J.A., and Marvizon, J.C., J. Neurosci., 2016, vol. 36, no. 1, pp. 204–221.Google Scholar
  14. 14.
    Lecker, I., Yin, Y., Wang, D.S., and Orser, B.A., Br. J. Anaest, vol. 110, no. Suppl. 1, pp. i73–i81.Google Scholar
  15. 15.
    Savic, M.M., Clayton, T., Furtmüller, R., Gavrilovic, I., Samardzic, J., Savic, S., Huck, S., Sieghart, W., and Cook, J.M., Brain Res., 2008, vol. 1208, pp. 150–159.Google Scholar
  16. 16.
    Stamenic, T., Joksimovic, S., Biawat, P., Stankovic, T., Markovic, B., Cook, J.M., and Savic, M.M., J. Psychopharmacol., 2015, vol. 29, no. 9, pp. 1013–1024.Google Scholar
  17. 17.
    Chua, H.C. and Chebib, M., Adv. Pharmacol., 2017, vol. 79, pp. 1–34.Google Scholar
  18. 18.
    Olsen, R.W. and Sieghart, W., Pharmacol. Rev., 2008, vol. 60, no. 3, pp. 243–260.Google Scholar
  19. 19.
    Olsen, R.W., Adv. Pharmacol., 2015, vol. 73, pp. 167–202.Google Scholar
  20. 20.
    Sigel, E. and Steinmann, M.E., J. Biol. Chem., 2012, vol. 287, no. 48, pp. 40224–40231.Google Scholar
  21. 21.
    Sadee, W., Wang, D., and Bilsky, E.J., Life Sci., 2005, vol. 76, no. 13, pp. 1427–1437.Google Scholar
  22. 22.
    Sirohi, S., Dighe, S.V., Madia, P.A., and Yoburn, B.C., J. Pharmacol. Exp. Ther., 2009, vol. 330, no. 2, pp. 513–519.Google Scholar
  23. 23.
    Raehal, K.M., Lowery, J.J., Bhamidipati, C.M., Paolino, R.M., Blair, J.R., Wang, D., Sadee, W., and Bilsky, E.J., J. Pharmacol. Exp. Ther., 2005, vol. 313, no. 3, pp. 1150–1162.Google Scholar
  24. 24.
    Wang, D., Raehal, K.M., Lin, E.T., Lowery, J.J., Kieffer, B.L., Bilsky, E.J., and Sadée, W., J. Pharmacol. Exp. Ther., 2004, vol. 308, no. 2, pp. 512–520.Google Scholar
  25. 25.
    Alyautdin, R.N. and Romanov, B.K., Bezopasnost’ i risk farmakoterapii (Safety and Risk of Pharmacotherapy), 2014, no. 4, pp. 6–11.Google Scholar
  26. 26.
    Hodavance, S.Y., Gareri, C., Torok, R.D., and Rockman, H.A., J. Cardiovasc. Pharmacol., 2016, vol. 67, no. 3, pp. 193–202.Google Scholar
  27. 27.
    Evans, A.K. and Lowry, C.A., CNS Drug Rev, 2007, vol. 13, no. 4, pp. 475–501.Google Scholar
  28. 28.
    Sally, E.J., Xu, H., Dersch, C.M., Hsin, L.W., Chang, L.T., Prisinzano, T.E., Simpson, D.S., Giuvelis, D., Rice, K.C., Jacobson, A.E., Cheng, K., Bilsky, E.J., and Rothman, R.B., Synapse, 2010, vol. 64, no. 4, pp. 280–288.Google Scholar
  29. 29.
    Barbalho, C.A., Nunes-de-Souza, R.L., and Cantode-Souza, A., Brain Res., 2009, vol. 1267, pp. 65–76.Google Scholar
  30. 30.
    Hashimoto, T. and Iwamura, Y., Pharmacol. Biochem. Behav., 2016, vol. 144, pp. 45–52.Google Scholar
  31. 31.
    Hashimoto, T., Kiyoshi, T., Kohayakawa, H., Iwamura, Y., and Yoshida, N., Neuroscience, 2014, vol. 256, pp. 352–359.Google Scholar
  32. 32.
    Nutt, D.J., Besson, M., Wilson, S.J., Dawson, G.R., and Lingford-Hughes, A.R., Neuropharmacology, 2007, vol. 53, no. 7, pp. 810–820.Google Scholar
  33. 33.
    Barnard, E.A., Skolnick, P., Olsen, R.W., Mohler, H., Sieghart, W., Biggio, G., Braestrup, C., Bateson, A.N., and Langer, S.Z., Pharmacol. Rev., 1998, vol. 50. no. 2, pp. 291–313.Google Scholar
  34. 34.
    Ballard, T.M., Knoflach, F., Prinssen, E., Borroni, E., Vivian, J.A., Basile, J., Gasser, R., Moreau, J.L., Wettstein, J.G., Buettelmann, B., Knust, H., Thomas, A.W., Trube, G., and Hernandez, M.C., Psychopharmacology (Berlin), 2009, vol. 202, nos. 1–3, pp. 207–223.Google Scholar
  35. 35.
    Knust, H., Achermann, G., Ballard, T., Buettelmann, B., Gasser, R., Fischer, H., Hernandez, M.C., Knoflach, F., Koblet, A., Stadler, H., Thomas, A.W., Trube, G., and Waldmeier, P., Bioorg. Med. Chem. Lett., 2009, vol. 19, no. 20, pp. 5940–5944.Google Scholar
  36. 36.
    De Min, A., Matera, C., Bock, A., Holze, J., Kloeckner, J., Muth, M., Traenkle, C., De Amici, M., Kenakin, T., Holzgrabe, U., Dallanoce, C., Kostenis, E., Mohr, K., and Schrage, R., Mol. Pharmacol., 2017, vol. 91, no. 4, pp. 348–356.Google Scholar
  37. 37.
    Gbahou, F., Rouleau, A., Morisset, S., Parmentier, R., Crochet, S., Lin, J.S., Ligneau, X., Tardivel-Lacombe, J., Stark, H., Schunack, W., Ganellin, C.R., Schwartz, J.C., and Arrang, J.M., Proc. Natl. Acad. Sci. U.S.A., 2003, vol. 100, no. 19, pp. 11086–11091.Google Scholar
  38. 38.
    Riddy, D.M., Cook, A.E., Diepenhorst, N.A., Bosnyak, S., Brady, R., Mannoury la Cour, C., Mocaer, E., Summers, R.J., Charman, W.N., Sexton, P.M., Christopoulos, A., and Langmead, C.J., Mol. Pharmacol., 2017, vol. 91, no. 2, pp. 87–99.Google Scholar
  39. 39.
    Milic, M., Timic, T., Joksimovic, S., Biawat, P., Rallapalli, S., Divljakovic, J., Radulovic, T., Cook, J.M., and Savic, M.M., Behav. Brain Res., 2013, vol. 241, pp. 206–213.Google Scholar
  40. 40.
    Wallner, M., Hanchar, H.J., and Olsen, R.W., Proc. Natl. Acad. Sci. U.S.A., 2006, vol. 103, no. 22, pp. 8540–8545.Google Scholar
  41. 41.
    Haefely, W.E., Eur. Arch. Psychiatry Neurol. Sci., 1989, vol. 238, nos 5–6, pp. 294–301.Google Scholar
  42. 42.
    Olsen, R.W., Neurochem. Res., 2014, vol. 39, no. 10, pp. 1924–1941.Google Scholar
  43. 43.
    Mehta, A.K. and Ticku, M.K., J. Pharmacol. Exp. Ther., 1988, vol. 246, no. 2, pp. 558–564.Google Scholar
  44. 44.
    Mehta, A.K. and Ticku, M.K., J. Pharmacol. Exp. Ther., 1989, vol. 249, no. 2, pp. 418–423.Google Scholar
  45. 45.
    Wang, F., Xu, Z., Yuen, C.T., Chow, C.Y., Lui, Y.L., Tsang, S.Y., and Xue, H., Neuropharmacology, 2007, vol. 53, no. 4, pp. 574–582.Google Scholar
  46. 46.
    Clayton, T., Poe, M.M., Rallapalli, S., Biawat, P., Savic, M.M., Rowlett, J.K., Gallos, G., Emala, C.W., Kaczorowski, C.C., Stafford, D.C., Arnold, L.A., and Cook, J.M., Int. J. Med. Chem., 2015, vol. 2015, article ID 430248.Google Scholar
  47. 47.
    Hashimoto, T., Hatayama, Y., Nakamichi, K., and Yoshida, N., Eur. J. Pharmacol., 2014, vol. 745, pp. 123–128.Google Scholar
  48. 48.
    Möhler, H., Adv. Pharmacol., 2015, vol. 72, pp. 1–36.Google Scholar
  49. 49.
    Venault, P. and Chapouthier, G., Scientific World Journal, 2007, vol. 7, pp. 204–223.Google Scholar
  50. 50.
    Guerrini, G. and Ciciani, G., Expert Opin. Ther. Pat., 2013, vol. 23, no. 7, pp. 843–866.Google Scholar
  51. 51.
    Farrant, M. and Nusser, Z., Nat. Rev. Neurosci., 2005, vol. 6, no. 3, pp. 215–229.Google Scholar
  52. 52.
    Hoestgaard-Jensen, K., Dalby, N.O., Krall, J., Hammer, H., Krogsgaard-Larsen, P., Frolund, B., and Jensen, A.A., J. Neurosci., 2014, vol. 34, no. 49, pp. 16256–16272.Google Scholar
  53. 53.
    Jia, F., Chandra, D., Homanics, G.E., and Harrison, N.L., J. Pharmacol. Exp. Ther., 2008, vol. 326, no. 2, pp. 475–482.Google Scholar
  54. 54.
    Atack, J.R., Curr. Top. Med. Chem., 2011, vol. 11, no. 9, pp. 1203–1214.Google Scholar
  55. 55.
    Carreno, F.R., Collins, G.T., Frazer, A., and Lodge, D.J., Int. J. Neuropsychopharmacol., 2017, vol. 20, no. 6, pp. 504–509.Google Scholar
  56. 56.
    Redrobe, J.P., Elster, L., Frederiksen, K., Bundgaard, C., de Jong, I.E., Smith, G.P., Bruun, A.T., Larsen, P.H., and Didriksen, M., Psychopharmacology (Berlin), 2012, vol. 221, no. 3, pp. 451–468.Google Scholar
  57. 57.
    Atack, J.R., Pharmacol. Ther., 2010, vol. 125, no. 1, pp. 11–26.Google Scholar
  58. 58.
    Martínez-Cué, C., Delatour, B., and Potier, M.C., Neurosci. Biobehav. Rev., 2014, vol. 46., Pt. 2, pp. 218–227.Google Scholar
  59. 59.
    Cook, J.B., Foster, K.L., Eiler, W.J. 2nd., McKay P.F., Woods J., 2nd., Harvey S.C., Garcia M., Grey C., McCane S., Mason D., Cummings R., Li X., Cook J.M., and June H.L. Alcohol. Clin. Exp. Res., 2005, vol. 29, no. 8, pp. 1390–1401.Google Scholar
  60. 60.
    June, H.L., Torres, L., Cason, C.R., Hwang, B.H., Braun, M.R., and Murphy, J.M., Brain Res., 1998, vol. 784, nos. 1–2, pp. 256–275.Google Scholar
  61. 61.
    Liu, R., Hu, R.J., Zhang, P., Skolnick, P., and Cook, J.M., J. Med. Chem., 1996, vol. 39, no. 9, pp. 1928–1934.Google Scholar
  62. 62.
    Atack, J.R., Bayley, P.J., Fletcher, S.R., McKernan, R.M., Wafford, K.A., and Dawson, G.R., Eur. J. Pharmacol., 2006, vol. 548, nos. 1–3, pp. 77–82.Google Scholar
  63. 63.
    McKay, P.F., Foster, K.L., Mason, D., Cummings, R., Garcia, M., Williams, L.S., Grey, C., McCane, S., He, X., Cook, J.M., and June, H.L., Psychopharmacology (Berlin), 2004, vol. 172, no. 4, pp. 455–462.Google Scholar
  64. 64.
    Fischell, J., Van Dyke, A.M., Kvarta, M.D., LeGates, T.A., and Thompson, S.M., Neuropsychopharmacology, 2015, vol. 40, no. 11, pp. 2499–2509.Google Scholar
  65. 65.
    Samardzic, J., Puskas, L., Obradovic, M., Lazic-Puskas, D., and Obradovic, I.D., Acta Veterinaria-Beograd, 2014, vol. 64, no. 1, pp. 52–60.Google Scholar
  66. 66.
    Zanos, P., Nelson, M.E., Highland, J.N., Krimmel, S.R., Georgiou, P., Gould, T.D., and Thompson, S.M., eNeuro, 2017, vol. 4, no. 1, article e0285-16.2017.Google Scholar
  67. 67.
    Wallner, M. and Olsen, R.W., Br. J. Pharmacol., 2008, vol. 154, no. 2, pp. 288–298.Google Scholar
  68. 68.
    Corda, M.G., Giorgi, O., Mele, S., and Biggio, G., Brain Res. Bull., 1987, vol. 19, no. 3, pp. 379–385.Google Scholar
  69. 69.
    Kubova, H. and Mares, P., Naunyn Schmiedeberg’s Arch. Pharmacol., 1994, vol. 350, no. 4, pp. 393–397.Google Scholar
  70. 70.
    Nicolas, L.B. and Prinssen, E.P., Psychopharmacology (Berlin), 2006, vol. 184, no. 1, pp. 65–74.Google Scholar
  71. 71.
    Nutt, D.J., Lister, R.G., Rusche, D., Bonetti, E.P., Reese, R.E., and Rufener, R., Eur. J. Pharmacol., 1988, vol. 151, no. 1, pp. 127–129.Google Scholar
  72. 72.
    Tracy, M.E., Banks, M.L., and Shelton, K.L., Psychopharmacology (Berlin), 2016, vol. 233, no. 4, pp. 715–725.Google Scholar
  73. 73.
    Bonetti, E.P., Burkard, W.P., Gabl, M., Hunkeler, W., Lorez, H.P., Martin, J.R., Moehler, H., Osterrieder, W., Pieri, L., Polc, P., Richards, J.G., Schaffner, R., Scherschlicht, R., Schoch, P., and Haefely, W.E., Pharmacol. Biochem. Behav., 1988, vol. 31, no. 3, pp. 733–749.Google Scholar
  74. 74.
    Lister, R.G. and Nutt, D.J., Adv. Alcohol Subst. Abuse, 1988, vol. 7, nos. 3–4, pp. 119–123.Google Scholar
  75. 75.
    Suzdak, P.D., Paul, S.M., and Crawley, J.N., J. Pharmacol. Exp. Ther., 1988, vol. 245, no. 3, pp. 880–886.Google Scholar
  76. 76.
    Dar, M.S., Pharmacol. Biochem. Behav., 1992, vol. 42, no. 3, pp. 473–479.Google Scholar
  77. 77.
    Glowa, J.R., Crawley, J., Suzdak, P.D., and Paul, S.M., Pharmacol. Biochem. Behav., 1988, vol. 31, no. 3, pp. 767–772.Google Scholar
  78. 78.
    Nabeshima, T., Tohyama, K., and Kameyama, T., Eur. J. Pharmacol., 1988, vol. 155, no. 3, pp. 211–217.Google Scholar
  79. 79.
    Syapin, P.J., Gee, K.W., and Alkana, R.L., Brain Res. Bull., 1987, vol. 19, no. 5, pp. 603–605.Google Scholar
  80. 80.
    Hoffman, P.L., Tabakoff, B., Szabó, G., Suzdak, P.D., and Paul, S.M., Life Sci., 1987, vol. 41, no. 5, pp. 611–619.Google Scholar
  81. 81.
    Hanchar, H.J., Chutsrinopkun, P., Meera, P., Supavilai, P., Sieghart, W., Wallner, M., and Olsen, R.W., Proc. Natl. Acad. Sci. U.S.A., 2006, vol. 103, no. 22, pp. 8546–8551.Google Scholar
  82. 82.
    Benson, J.A., Löw, K., Keist, R., Mohler, H., and Rudolph, U., FEBS Lett., 1998, vol. 431, no. 3, pp. 400–404.Google Scholar
  83. 83.
    Lister, R.G. and Durcan, M.J., Brain Res., 1989, vol. 482, no. 1, pp. 141–144.Google Scholar
  84. 84.
    Durcan, M.J. and Lister, R.G., Pharmacol. Biochem. Behav., 1989, vol. 32, no. 3, pp. 667–670.Google Scholar
  85. 85.
    Sternfeld, F., Carling, R.W., Jelley, R.A., Ladduwahetty, T., Merchant, K.J., Moore, K.W., Reeve, A.J., Street, L.J., O’Connor, D., Sohal, B., Atack, J.R., Cook, S., Seabrook, G., Wafford, K., Tattersall, F.D., Collinson, N., Dawson, G.R., Castro, J.L., and Macleod, A.M., J. Med. Chem., 2004, vol. 47, no. 9, pp. 2176–2179.Google Scholar
  86. 86.
    ClinicalTrials.gov, Ability of partial inverse agonist, iomazenil, to block ethanol effects in humans. NCT01590277. https://doi.org/clinicaltrials.gov/ct2/show/NCT01590277.2017.
  87. 87.
    McBride, W.J., Murphy, J.M., Lumeng, L., and Li, T.K., Pharmacol. Biochem. Behav., 1988, vol. 30, no. 4, pp. 1045–1050.Google Scholar
  88. 88.
    Melón, L.C. and Boehm, S.L. 2nd, Behav. Brain Res., 2011, vol. 220, no. 1, pp. 230–237.Google Scholar
  89. 89.
    June, H.L., Greene, T.L., Murphy, J.M., Hite, M.L., Williams, J.A., Cason, C.R., Mellon-Burke, J., Cox, R., Duemler, S.E., Torres, L., Lumeng, L., and Li, T.K., Brain Res., 1996, vol. 734, nos. 1–2, pp. 19–34.Google Scholar
  90. 90.
    June, H.L., Harvey, S.C., Foster, K.L., McKay, P.F., Cummings, R., Garcia, M., Mason, D., Grey, C., McCane, S., Williams, L.S., Johnson, T.B., He, X., Rock, S., and Cook, J.M., J. Neurosci., 2001, vol. 21, no. 6, pp. 2166–2177.Google Scholar
  91. 91.
    Rüedi-Bettschen, D., Rowlett, J.K., Rallapalli, S., Clayton, T., Cook, J.M., and Platt, D.M., Alcohol. Clin. Exp. Res., 2013, vol. 37, no. 4, pp. 624–634.Google Scholar
  92. 92.
    Griffiths, J.L. and Lovick, T.A., Neuroscience, 2005, vol. 136, no. 2, pp. 457–466.Google Scholar
  93. 93.
    Lovick, T.A., Griffiths, J.L., Dunn, S.M., and Martin, I.L., Neuroscience, 2005, vol. 131, no. 2, pp. 397–405.Google Scholar
  94. 94.
    Korpi, E.R., den Hollander, B., Farooq, U., Vashchinkina, E., Rajkumar, R., Nutt, D.J., Hyytiä, P., and Dawe, G.S., Pharmacol. Rev., 2015, vol. 67, no. 4, pp. 872–1004.Google Scholar
  95. 95.
    Buettelmann, B., Ballard, T.M., Gasser, R., Fischer, H., Hernandez, M.C., Knoflach, F., Knust, H., Stadler, H., Thomas, A.W., and Trube, G., Bioorg. Med. Chem. Lett., 2009, vol. 19, no. 20, pp. 5958–5961.Google Scholar
  96. 96.
    Hatayama, Y., Hashimoto, T., Kohayakawa, H., Kiyoshi, T., Nakamichi, K., Kinoshita, T., and Yoshida, N., Neuroscience, 2014, vol. 265, pp. 217–225.Google Scholar
  97. 97.
    Contestabile, A., Magara, S., and Cancedda, L., Front. Cell. Neurosci., 2017, vol. 11, article54.Google Scholar
  98. 98.
    Etherington, L.A., Mihalik, B., Pálvölgyi, A., Ling, I., Pallagi, K., Kertész, S., Varga, P., Gunn, B.G., Brown, A.R., Livesey, M.R., Monteiro, O., Belelli, D., Barkóczy, J., Spedding, M., Gacsályi, I., Antoni, F.A., and Lambert, J.J., Neuropharmacology, 2017, vol. 125, pp. 353–364.Google Scholar
  99. 99.
    Gacsályi, I., Móricz, K., Gigler, G., Wellmann, J., Nagy, K., Ling, I., Barkoczy, J., Haller, J., Lambert, J.J., Szénási, G., Spedding, M., and Antoni, F.A., Neuropharmacology, 2017, vol. 125, pp. 30–38.Google Scholar
  100. 100.
    Mihalik, B., Pálvölgyi, A., Bogár, F., Megyeri, K., Ling, I., Barkóczy, J., Bartha, F., Martinek, T.A., Gacsályi, I., and Antoni, F.A., Eur. J. Pharmacol., 2017, vol. 798, pp. 129–136.Google Scholar
  101. 101.
    Pálvölgyi, A., Móricz, K., Pataki, Á., Mihalik, B., Gigler, G., Megyeri, K., Udvari, S., Gacsályi, I., and Antoni, F.A., Neuropharmacology, 2018, vol. 128, pp. 408–415.Google Scholar
  102. 102.
    Atack, J.R., CNS Neurosci. Ther., 2008, vol. 14, no. 1, pp. 25–35.Google Scholar

Copyright information

© Pleiades Publishing, Ltd. 2018

Authors and Affiliations

  • A. I. Golovko
    • 1
    • 3
    Email author
  • M. B. Ivanov
    • 1
  • E. S. Golovko
    • 2
  • V. B. Dolgo-Saburov
    • 1
  • E. P. Zatsepin
    • 1
  1. 1.Institute of ToxicologyFederal Medico-Biological Agency of RussiaSt. PetersburgRussia
  2. 2.St. Petersburg State Pediatric Medical UniversitySt. PetersburgRussia
  3. 3.St. PetersburgRussia

Personalised recommendations