Histamine H3 receptor antagonism by ABT-239 attenuates kainic acid induced excitotoxicity in mice

Brain Research

Volumn 1581, Issue , 2014, Pages 129-140

  Bhowmik, Malay ^a   Saini, Neeru ^a,b   Vohora, Divya ^a  

^a HAMDARD UNIVERSITY   (India)

^b CSIR INSTITUTE OF GENOMICS AND INTEGRATIVE BIOLOGY   (India)

Author keywords

(ABT 239); 4 (2 2 (2R) 2 methylpyrrolidinyl ethyl benzofuran 5 yl)benzonitrile; cAMP response element binding protein (CREB); Histamine H3 receptor (H3R); Kainic acid (KA); Neurodegeneration; Phospho GSK3 (Ser9, pGSK3 ser9)

Indexed keywords

ABT 239; CASPASE 3; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; GLYCOGEN SYNTHASE KINASE 3 INHIBITOR; GLYCOGEN SYNTHASE KINASE 3BETA; HISTAMINE H3 RECEPTOR; HISTAMINE H3 RECEPTOR ANTAGONIST; KAINIC ACID; PROTEIN BAX; PROTEIN BCL 2; PROTEIN KINASE B; TDZD 8; UNCLASSIFIED DRUG; VALPROIC ACID; 4-BENZYL-2-METHYL-1,2,4-THIADIAZOLIDINE-3,5-DIONE; ANTICONVULSIVE AGENT; BENZOFURAN DERIVATIVE; BENZONITRILE, 4-(2-(2-((2R)-2-METHYL-1-PYRROLIDINYL)ETHYL)-5-BENZOFURANYL)-; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 BETA; NEUROPROTECTIVE AGENT; PROTEIN KINASE INHIBITOR; PYRROLIDINE DERIVATIVE; THIADIAZOLE DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DRUG DOSE COMPARISON; DRUG EFFICACY; DRUG MEGADOSE; EXCITOTOXICITY; LOW DRUG DOSE; MALE; MONOTHERAPY; MOUSE; NEUROPROTECTION; NONHUMAN; PROTEIN EXPRESSION; ANIMAL; ANTAGONISTS AND INHIBITORS; DOSE RESPONSE; DRUG COMBINATION; DRUG EFFECTS; GENE EXPRESSION; HIPPOCAMPUS; METABOLISM; NERVE CELL; NEURODEGENERATIVE DISEASES; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; RANDOMIZATION; SEIZURES;

MUS;

ANIMALS; ANTICONVULSANTS; BENZOFURANS; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG THERAPY, COMBINATION; GENE EXPRESSION; GLYCOGEN SYNTHASE KINASE 3; HIPPOCAMPUS; HISTAMINE H3 ANTAGONISTS; KAINIC ACID; MALE; MICE; NEURODEGENERATIVE DISEASES; NEURONS; NEUROPROTECTIVE AGENTS; PROTEIN KINASE INHIBITORS; PYRROLIDINES; RANDOM ALLOCATION; SEIZURES; THIADIAZOLES; VALPROIC ACID;

EID: 84907694360     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2014.06.012     Document Type: Article

References (55)

1. M.M. Acharya, B. Hattiangady, and A.K. Shetty Progress in neuroprotective strategies for preventing epilepsy Prog. Neurobiol. 84 2008 363 404
2. Y. Ben-Ari Limbic seizure and brain damage produced by kainic acid: mechanisms and relevance to human temporal lobe epilepsy Neuroscience 14 1985 375 403
3. S.A. Benkovic, J.P. O'Callaghan, and D.B. Miller Sensitive indicators of injury reveal hippocampal damage in C57BL/6J mice treated with kainic acid in the absence of tonic-clonic seizures Brain Res. 1024 2004 59 76
4. R.V. Bhat, S. Leonov, J. Luthman, C.W. Scott, and C.M. Lee Interactions between GSK3beta and caspase signalling pathways during NGF deprivation induced cell death J. Alzheimers Dis. 4 2002 291 301
5. M. Bhowmik, R. Khanam, and D. Vohora Histamine H3 receptor antagonists in relation to epilepsy and neurodegeneration: a systemic consideration of recent progress and perspectives Br. J. Pharmacol. 167 2012 1398 1414
6. R.S. Bitner, S. Markosyan, A.L. Nikkel, and J.D. Brioni In-vivo histamine H3 receptor antagonism activates cellular signaling suggestive of symptomatic and disease modifying efficacy in Alzheimer's disease Neuropharmacology 60 2011 460 466
7. G. Bongers, S. Markosyan, A.L. Nikkel, and J.D. Brioni The Akt/GSK-3beta axis as a new signaling pathway of the histamine H(3) receptor J. Neurochem. 103 2007 248 258
8. A. Chakraborty, C. Latapy, J. Xu, S.H. Snyder, and J.M. Beaulieu Inositol hexakisphosphate kinase-1 regulates behavioral responses via GSK3 signaling pathways Mol. Psychiatry 19 2014 284 293
9. P. Chang, M.C. Walker, and R.S. Williams Seizure-induced reduction in PIP3 levels contributes to seizure-activity and is rescued by valproic acid Neurobiol. Dis. 62 2014 296 306
10. Z. Chen, Z. Li, E. Sakurai, J. Izadi Mobarakeh, H. Ohtsu, T. Watanabe, T. Watanabe, K. Iinuma, and K. Yanai Chemical kindling induced by pentylenetetrazol in histamine H(1) receptor gene knockout mice (H(1)KO), histidine decarboxylase-deficient mice (HDC(-/-)) and mast cell-deficient W/W(v) mice Brain Res. 968 2003 162 166
11. O.C. Cockerell, A.L. Johnson, J.W. Sander, Y.M. Hart, and S.D. Shorvon Remission of epilepsy: results from the National General Practice Study of Epilepsy Lancet 346 1995 140 144
12. J.A. Cramer, S. Mintzer, J. Wheless, and R.H. Mattson Adverse effects of antiepileptic drugs: a brief overview of important issues Expert Rev. Neurother 10 2010 885 891
13. N. Crespo-Biel, A.M. Canudas, A. Camins, and M. Pallàs Kainate induces AKT, ERK and cdk5/GSK3beta pathway deregulation, phosphorylates tau protein in mouse hippocampus Neurochem. Int. 50 2007 435 442
14. S. Cuzzocrea, T. Genovese, E. Mazzon, C. Crisafulli, R. Di Paola, C. MuiÃ, M. Collin, E. Esposito, P. Bramanti, and C. Thiemermann Glycogen synthase kinase-3 beta inhibition reduces secondary damage in experimental spinal cord trauma J. Pharmacol. Exp. Ther. 318 2006 79 89
15. H. Dai, T. Genovese, E. Mazzon, C. Crisafulli, R. Di Paola, C. Muià, M. Collin, E. Esposito, P. Bramanti, and C. Thiemermann The histamine H3 receptor antagonist clobenpropit enhances GABA release to protect against NMDA-induced excitotoxicity through the cAMP/protein kinase A pathway in cultured cortical neurons Eur. J. Pharmacol. 563 2007 117 123
16. M.A. Dichter Emerging concepts in the pathogenesis of epilepsy and epileptogenesis Arch. Neurol. 66 2009 443 447
17. T.A. Esbenshade, G.B. Fox, K.M. Krueger, T.R. Miller, C.H. Kang, L.I. Denny, D.G. Witte, B.B. Yao, L. Pan, J. Wetter, K. Marsh, Y.L. Bennani, M.D. Cowart, J.P. Sullivan, and A.A. Hancock Pharmacological properties of ABT-239 [4-(2-{2-[(2R)-2-methylpyrrolidinyl]ethyl}-benzofuran-5-yl)benzonitrile]: I. Potent and selective histamine H3 receptor antagonist with drug-like properties J. Pharmacol. Exp. Ther. 313 2005 165 175
18. C.J. Faherty, S. Xanthoudakis, and R.J. Smeyne Caspase-3-dependent neuronal death in the hippocampus following kainic acid treatment Brain Res. Mol. Brain Res. 70 1999 159 163
19. G.B. Fox, T.A. Esbenshade, J.B. Pan, R.J. Radek, K.M. Krueger, B.B. Yao, K.E. Browman, M.J. Buckley, M.E. Ballard, V.A. Komater, H. Miner, M. Zhang, R. Faghih, L.E. Rueter, R.S. Bitner, K.U. Drescher, J. Wetter, K. Marsh, M. Lemaire, R.D. Porsolt, Y.L. Bennani, J.P. Sullivan, M.D. Cowart, M.W. Decker, and AA. Hancock Pharmacological properties of ABT-239 [4-(2-{2-[(2R)-2-methylpyrrolidinyl]ethyl}-benzofuran-5-yl)benzonitrile]: II. Neurophysiological characterization and broad preclinical efficacy in cognition and schizophrenia of a potent and selective histamine H3 receptor antagonist J. Pharmacol. Exp. Ther. 313 2005 176 190
20. D.G. Fujikawa, S.S. Shinmei, S. Zhao, and E.R. Jr. Aviles Caspase-dependent programmed cell death pathways are not activated in generalized seizure-induced neuronal death Brain Res. 1135 2007 206 218
21. F. Gillardon, H. Wickert, and M. Zimmermann Up-regulation of bax and down-regulation of bcl-2 is associated with kainate-induced apoptosis in mouse brain Neurosci. Lett. 192 1995 85 88
22. C. Harada, Y. Fujii, T. Hirai, K. Shinomiya, and C. Kamei Inhibitory effect of iodophenpropit, a selective histamine H3 antagonist, on amygdaloid kindled seizures Brain Res. Bull. 63 2004 143 146
23. T. Hirai, C. Okuma, C. Harada, M. Mio, H. Ohtsu, T. Watanabe, and C. Kamei Development of amygdaloid kindling in histidine decarboxylase - deficient and histamine H1 receptor - deficient mice Epilepsia 45 2004 309 313
24. Z. Huang, M.C. Walker, and M.M. Shah Loss of dendritic HCN1 subunits enhances cortical excitability and epileptogenesis J. Neurosci. 29 2009 10979 10988
25. B.T. Jeon, H.J. Shin, J.B. Kim, Y.K. Kim, D.H. Lee, K.H. Kim, H.J. Kim, S.S. Kang, G.J. Cho, W.S. Choi, and G.S. Roh Adiponectin protects hippocampal neurons against kainic acid-induced excitotoxicity Brain Res. Rev. 61 2009 81 88
26. C. Jin, M. Lintunen, and P. Panula Histamine H(1) and H(3) receptors in the rat thalamus and their modulation after systemic kainic acid administration Exp. Neurol. 194 2005 43 56
27. C. Kamei Involvement of central histamine in amygdaloid kindled seizures in rats Behav. Brain Res. 124 2001 243 250
28. B.S. Kim, M.Y. Kim, and Y.H. Leem Hippocampal neuronal death induced by kainic acid and restraint stress is suppressed by exercise Neuroscience 194 2011 291 301
29. Y. Kinoshita, H.J. Wenzel, C. Kinoshita, P.A. Schwartzkroin, and R.S. Morrison Acute, but reversible, kainic acid-induced DNA damage in hippocampal CA1 pyramidal cells of p53-deficient mice Epilepsia 53 Suppl. 1 2012 125 133
30. A. Kondratyev, and K. Gale Intracerebral injection of caspase-3 inhibitor prevents neuronal apoptosis after kainic acid-evoked status epilepticus Brain Res. Mol. Brain Res. 75 2000 216 224
31. T.K. Kukko-Lukjanov, S. Soini, T. Taira, K.A. Michelsen, P. Panula, and I.E. Holopainen Histaminergic neurons protect the developing hippocampus from kainic acid-induced neuronal damage in an organotypic coculture system J. Neurosci. 26 2006 1088 1097
32. B. Lee, R. Cao, Y.S. Choi, H.Y. Cho, A.D. Rhee, C.K. Hah, K.R. Hoyt, and K. Obrietan The CREB/CRE transcriptional pathway: protection against oxidative stress-mediated neuronal cell death J. Neurochem. 108 2009 1251 1265
33. D.A. Linseman, B.D. Butts, T.A. Precht, R.A. Phelps, S.S. Le, T.A. Laessig, R.J. Bouchard, M.L. Florez-McClure, and K.A. Heidenreich Glycogen synthase kinase-3beta phosphorylates Bax and promotes its mitochondrial localization during neuronal apoptosis J. Neurosci. 24 2004 9993 10002
34. M. Lintunen, T. Sallmen, K. Karlstedt, and P. Panula Transient changes in the limbic histaminergic system after systemic kainic acid-induced seizures Neurobiol. Dis. 20 2005 155 169
35. W. Loscher, and D. Schmidt Modern antiepileptic drug development has failed to deliver: ways out of the current dilemma Epilepsia 52 2011 657 678
36. T.W. Lovenberg, B.L. Roland, S.J. Wilson, X. Jiang, J. Pyati, A. Huvar, M.R. Jackson, and M.G. Erlander Cloning and functional expression of the human histamine H3 receptor Mol. Pharmacol. 55 1999 1101 1107
37. T. Mabuchi, K. Kitagawa, K. Kuwabara, K. Takasawa, T. Ohtsuki, Z. Xia, D. Storm, T. Yanagihara, M. Hori, and M. Matsumoto Phosphorylation of cAMP response element-binding protein in hippocampal neurons as a protective response after exposure to glutamate in vitro and ischemia in vivo J. Neurosci. 21 2001 9204 9213
38. C. Mariottini, T. Scartabelli, G. Bongers, S. Arrigucci, D. Nosi, R. Leurs, A. Chiarugi, P. Blandina, D.E. Pellegrini-Giampietro, and M.B. Passani Activation of the histaminergic H3 receptor induces phosphorylation of the Akt/GSK-3 beta pathway in cultured cortical neurons and protects against neurotoxic insults J. Neurochem. 110 2009 1469 1478
39. G.M. McKhann 2nd, H.J. Wenzel, C.A. Robbins, A.A. Sosunov, and P.A. Schwartzkroin Mouse strain differences in kainic acid sensitivity, seizure behavior, mortality, and hippocampal pathology Neuroscience 122 2003 551 561
40. I. Miyata, H. Saegusa, and M. Sakurai Seizure-modifying potential of histamine H1 antagonists: a clinical observation Pediatr. Int. 53 2011 706 708
41. H.S. Noh, Y.S. Kim, Y.H. Kim, J.Y. Han, C.H. Park, A.K. Kang, H.S. Shin, S.S. Kang, G.J. Cho, and W.S. Choi Ketogenic diet protects the hippocampus from kainic acid toxicity by inhibiting the dissociation of bad from 14-3-3 J. Neurosci. Res. 84 2006 1829 1836
42. G. Paxinos, and K. Franklin Paxinos Franklin's The Mouse Brain in Stereotaxic Coordinates, fourth ed 2012 Academic Press San Diego
43. P. Perucca, and F.G. Gilliam Adverse effects of antiepileptic drugs Lancet Neurol. 11 2012 792 802
44. A. Pitkanen Therapeutic approaches to epileptogenesis - hope on the horizon Epilepsia 51 Suppl. 3 2010 2 17
45. H. Pollard, C. Charriaut-Marlangue, S. Cantagrel, A. Represa, O. Robain, J. Moreau, and Y. Ben-Ari Kainate-induced apoptotic cell death in hippocampal neurons Neuroscience 63 1994 7 18
46. B. Puig, and I. Ferrer Caspase-3-associated apoptotic cell death in excitotoxic necrosis of the entorhinal cortex following intraperitoneal injection of kainic acid in the rat Neurosci. Lett. 321 2002 182 186
47. R.J. Racine Modification of seizure activity by electrical stimulation. II. Motor seizure Electroencephalogr. Clin. Neurophysiol. 32 1972 281 294
48. A.I. Rojo, P. Rada, J. Egea, A.O. Rosa, M.G. López, and A. Cuadrado Functional interference between glycogen synthase kinase-3 beta and the transcription factor Nrf2 in protection against kainate-induced hippocampal cell death Mol. Cell. Neurosci. 39 2008 125 132
49. S. Shinoda, C.K. Schindler, R. Meller, N.K. So, T. Araki, A. Yamamoto, J.Q. Lan, W. Taki, R.P. Simon, and D.C. Henshall Bim regulation may determine hippocampal vulnerability after injurious seizures and in temporal lobe epilepsy J. Clin. Invest. 113 2004 1059 1068
50. R.S. Sloviter, and B.P. Damiano On the relationship between kainic acid-induced epileptiform activity and hippocampal neuronal damage Neuropharmacology 20 1981 1003 1011
51. E. Tremblay, and Y. Ben-Ari Usefulness of parenteral kainic acid as a model of temporal lobe epilepsy Rev. Electroencephalogr. Neurophysiol. Clin. 14 1984 241 246
52. D. Vohora, S.N. Pal, and K.K. Pillai Thioperamide, a selective histamine H3 receptor antagonist, protects against PTZ-induced seizures in mice Life Sci. 66 2000 297 301
53. D. Vohora, S.N. Pal, and K.K. Pillai Histamine and selective H3-receptor ligands: a possible role in the mechanism and management of epilepsy Pharmacol. Biochem. Behav. 68 2001 735 741
54. I. Yawata, K. Tanaka, Y. Nakagawa, Y. Watanabe, Y.L. Murashima, and K. Nakano Role of histaminergic neurons in development of epileptic seizures in EL mice Brain Res. Mol. Brain Res. 132 2004 13 17
55. H. Yokoyama, K. Onodera, K. Iinuma, and T. Watanabe Proconvulsive effects of histamine H1-antagonists on electrically-induced seizure in developing mice Psychopharmacology (Berlin) 112 1993 199 203