Understanding the basic mechanisms underlying seizures in mesial temporal lobe epilepsy and possible therapeutic targets: A review

Journal of Neuroscience Research

Volumn 90, Issue 5, 2012, Pages 913-924

  O'Dell, Casey M ^a   Das, Arabinda ^a   Wallace, Gerald ^a   Ray, Swapan K ^b   Banik, Naren L ^a  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b UNIVERSITY OF SOUTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Calpain; Cytokines; Epileptogenesis; Temporal lobe epilepsy

Indexed keywords

1 (4 AMINOPHENYL) 4 METHYL 7,8 METHYLENEDIOXY 5H 2,3 BENZODIAZEPINE; 4 [5 (4 CHLOROPHENYL) 3 TRIFLUOROMETHYL 1H PYRAZOL 1 YL]BENZENESULFONAMIDE; 5 IODOTUBERCIDIN; A 438079; A 740003; ANTICONVULSIVE AGENT; ANTIMITOTIC AGENT; CARBAMAZEPINE; CELECOXIB; CYTOSINE BETA DEXTRO ARABINOFURANOSE; DEXAMETHASONE; ETHOSUXIMIDE; FLUPIRTINE; GLUTAMIC ACID; KAINIC ACID; LAMOTRIGINE; PARECOXIB; PHENOBARBITAL; PHENYTOIN; PLANT EXTRACT; POTASSIUM BROMIDE; PRIMIDONE; RAPAMYCIN; RETIGABINE; SEARSIA EXTRACT; TRIMETHADIONE; UNCLASSIFIED DRUG; VALPROIC ACID;

4 AMINOBUTYRIC ACID RELEASE; ANTICONVULSANT THERAPY; APOPTOSIS; CHILDHOOD DISEASE; CLINICAL TRIAL (TOPIC); DRUG TOLERABILITY; EPILEPTIC STATE; EPILEPTOGENESIS; GENERALIZED EPILEPSY; GLIOSIS; HUMAN; INFLAMMATION; LATENT PERIOD; MESIAL TEMPORAL LOBE EPILEPSY; MOSSY FIBER; NERVE CELL DEGENERATION; NERVE EXCITABILITY; NERVE SPROUTING; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SEDATION; SIDE EFFECT; TEMPORAL LOBE EPILEPSY; UNSPECIFIED SIDE EFFECT;

ADENOSINE KINASE; ANIMALS; COMPREHENSION; CYTOKINES; DISEASE MODELS, ANIMAL; EPILEPSY, TEMPORAL LOBE; GLIOSIS; HUMANS; MOSSY FIBERS, HIPPOCAMPAL; NERVE DEGENERATION; SEIZURES;

EID: 84858004619     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.22829     Document Type: Review

References (76)

1. Araujo IM, Carreira BP, Carvalho CM, Carvalho AP. 2010. Calpains and delayed calcium deregulation in excitotoxicity. Neurochem Res 35: 1966-1969.
2. Arganaraz GA, Konno AC, Perosa SR, Santiago JF, Boim MA, Vidotti DB, Varella PP, Costa LG, Canzian M, Porcionatto MA, Yacubian EM, Sakamoto AC, Carrete HJr, Centeno RS, Amado D, Cavalheiro EA, Junior JA, Mazzacoratti Mda G. 2008. The renin-angiotensin system is upregulated in the cortex and hippocampus of patients with temporal lobe epilepsy related to mesial temporal sclerosis. Epilepsia 49: 1348-1357.
3. Aronica E, Zurolo E, Iyer A, de Groot M, Anink J, Carbonell C, van Vliet EA, Baayen JC, Boison D, Gorter JA. 2011. Upregulation of adenosine kinase in astrocytes in experimental and human temporal lobe epilepsy. Epilepsia (in press).
4. Bae EK, Jung KH, Chu K, Lee ST, Kim JH, Park KI, Kim M, Chung CK, Lee SK, Roh JK. 2010. Neuropathologic and clinical features of human medial temporal lobe epilepsy. J Clin Neurol 6: 73-80.
5. Baram TZ, Jensen FE, Brooks-Kayal A. 2011. Does acquired epileptogenesis in the immature brain require neuronal death. Epilepsy Curr 11: 21-26.
6. Ben-Ari Y, Dudek FE. 2010. Primary and secondary mechanisms of epileptogenesis in the temporal lobe: there is a before and an after. Epilepsy Curr 10: 118-125.
7. Boison D. 2008. The adenosine kinase hypothesis of epileptogenesis. Prog Neurobiol 84: 249-262.
8. Buckmaster PS, Wen X. 2011. Rapamycin suppresses axon sprouting by somatostatin interneurons in a mouse model of temporal lobe epilepsy. Epilepsia (PMID 21883182).
9. Carson RP, Van Nielen DL, Winzenburger PA, Ess KC. 2011. Neuronal and glia abnormalities in Tsc1-deficient forebrain and partial rescue by rapamycin. Neurobiol Dis (in press).
10. Chamberlain SE, Jane DE, Jones RS. 2011. Pre- and post-synaptic functions of kainate receptors at glutamate and GABA synapses in the rat entorhinal cortex. Hippocampus (in press).
11. Chong ZZ, Shang YC, Zhang L, Wang S, Maiese K. 2010. Mammalian target of rapamycin: hitting the bull's-eye for neurological disorders. Oxid Med Cell Longev 3: 374-391.
12. Crespel A, Coubes P, Rousset MC, Brana C, Rougier A, Rondouin G, Bockaert J, Baldy-Moulinier M, Lerner-Natoli M. 2002. Inflammatory reactions in human medial temporal lobe epilepsy with hippocampal sclerosis. Brain Res 952: 159-169.
13. + channel blocker attenuates kainic acid-induced apoptosis in rat primary hippocampal neurons. Neurochem Res 35: 2175-2183.
14. de Lanerolle NC, Kim JH, Williamson A, Spencer SS, Zaveri HP, Eid T, Spencer DD. 2003. A retrospective analysis of hippocampal pathology in human temporal lobe epilepsy: evidence for distinctive patient subcategories. Epilepsia 44: 677-687.
15. A receptors in patients with mesial temporal lobe epilepsy. Hippocampus (in press).
16. Diener W, Sorni M, Ruile S, Rude P, Kruse R, Becker E, Bork K, Berg PA. 1998. Panniculitis due to potassium bromide. Brain Dev 20: 83-87.
17. + homeostasis in the human epileptogenic hippocampus. Proc Natl Acad Sci U S A 102: 1193-1198.
18. Epsztein J, Represa A, Jorquera I, Ben-Ari Y, Crepel V. 2005. Recurrent mossy fibers establish aberrant kainate receptor-operated synapses on granule cells from epileptic rats. J Neurosci 25: 8229-8239.
19. Feng ZH, Hao J, Ye L, Dayao C, Yan N, Yan Y, Chu L, Shi FD. 2011. Overexpression of mu-calpain in the anterior temporal neocortex of patients with intractable epilepsy correlates with clinicopathological characteristics. Seizure 20: 395-401.
20. Frasca A, Aalbers M, Frigerio F, Fiordaliso F, Salio M, Gobbi M, Cagnotto A, Gardoni F, Battaglia GS, Hoogland G, Di Luca M, Vezzani A. 2011. Misplaced NMDA receptors in epileptogenesis contribute to excitotoxicity. Neurobiol Dis 43: 507-515.
21. A-receptors in temporal lobe epilepsy. Neurochem Int 34: 435-445.
22. A receptor signaling by seizures. Epilepsia 48( Suppl 5): 14-18.
23. Gorter JA, van Vliet EA, Aronica E, Lopes da Silva FH. 2001. Progression of spontaneous seizures after status epilepticus is associated with mossy fibre sprouting and extensive bilateral loss of hilar parvalbumin and somatostatin-immunoreactive neurons. Eur J Neurosci 13: 657-669.
24. Gorter JA, Goncalves Pereira PM, van Vliet EA, Aronica E, Lopes da Silva FH, Lucassen PJ. 2003. Neuronal cell death in a rat model for mesial temporal lobe epilepsy is induced by the initial status epilepticus and not by later repeated spontaneous seizures. Epilepsia 44: 647-658.
25. Gouder N, Scheurer L, Fritschy JM, Boison D. 2004. Overexpression of adenosine kinase in epileptic hippocampus contributes to epileptogenesis. J Neurosci 24: 692-701.
26. Hayashi K, Ueshima S, Ouchida M, Mashimo T, Nishiki T, Sendo T, Serikawa T, Matsui H, Ohmori I. 2011. Therapy for hyperthermia-induced seizures in Scn1a mutant rats. Epilepsia 52: 1010-1017.
27. Holtman L, van Vliet EA, van Schaik R, Queiroz CM, Aronica E, Gorter JA. 2009. Effects of SC58236, a selective COX-2 inhibitor, on epileptogenesis and spontaneous seizures in a rat model for temporal lobe epilepsy. Epilepsy Res 84: 56-66.
28. Jankowsky JL, Patterson PH. 2001. The role of cytokines and growth factors in seizures and their sequelae. Prog Neurobiol 63: 125-149.
29. Jantas D, Lorenc-Koci E, Kubera M, Lason W. 2011. Neuroprotective effects of MAPK/ERK1/2 and calpain inhibitors on lactacystin-induced cell damage in primary cortical neurons. Neurotoxicology (in press).
30. Jaworska-Adamu J, Dmowska M, Cybulska R, Krawczyk A, Pawlikowska-Pawlega B. 2011. Investigations of hippocampal astrocytes in lipopolysaccharide-preconditioned rats in the pilocarpine model of epilepsy. Fol Histochem Cytobiol 49: 219-224.
31. Johannessen Landmark C, Patsalos PN. 2010. Drug interactions involving the new second- and third-generation antiepileptic drugs. Expert Rev Neurother 10: 119-140.
32. Jung KH, Chu K, Lee ST, Kim J, Sinn DI, Kim JM, Park DK, Lee JJ, Kim SU, Kim M, Lee SK, Roh JK. 2006. Cyclooxygenase-2 inhibitor, celecoxib, inhibits the altered hippocampal neurogenesis with attenuation of spontaneous recurrent seizures following pilocarpine-induced status epilepticus. Neurobiol Dis 23: 237-246.
33. Kaur J, Mencl S, Sahaboglu A, Farinelli P, van Veen T, Zrenner E, Ekstrom P, Paquet-Durand F, Arango-Gonzalez B. 2011. Calpain and PARP activation during photoreceptor cell death in P23H and S334ter rhodopsin mutant rats. PLoS One 6: e22181.
34. Kharatishvili I, Pitkanen A. 2010. Posttraumatic epilepsy. Curr Opin Neurol 23: 183-188.
35. Kharatishvili I, Nissinen JP, McIntosh TK, Pitkanen A. 2006. A model of posttraumatic epilepsy induced by lateral fluid-percussion brain injury in rats. Neuroscience 140: 685-697.
36. Krall RL, Penry JK, Kupferberg HJ, Swinyard EA. 1978. Antiepileptic drug development: I. History and a program for progress. Epilepsia 19: 393-408.
37. Lee TS, Eid T, Mane S, Kim JH, Spencer DD, Ottersen OP, de Lanerolle NC. 2004. Aquaporin-4 is increased in the sclerotic hippocampus in human temporal lobe epilepsy. Acta Neuropathol 108: 493-502.
38. Li JM, Zeng YJ, Peng F, Li L, Yang TH, Hong Z, Lei D, Chen Z, Zhou D. 2010. Aberrant glutamate receptor 5 expression in temporal lobe epilepsy lesions. Brain Res 1311: 166-174.
39. Linard B, Ferrandon A, Koning E, Nehlig A, Raffo E. 2010. Ketogenic diet exhibits neuroprotective effects in hippocampus but fails to prevent epileptogenesis in the lithium-pilocarpine model of mesial temporal lobe epilepsy in adult rats. Epilepsia 51: 1829-1836.
40. Löscher W, Schmidt D. 2011. Modern antiepileptic drug development has failed to deliver: ways out of the current dilemma. Epilepsia 52: 657-678.
41. Mantegazza M, Curia G, Biagini G, Ragsdale DS, Avoli M. 2010. Voltage-gated sodium channels as therapeutic targets in epilepsy and other neurological disorders. Lancet Neurol 9: 413-424.
42. Marchetti C, Gavazzo P, Stafford GI, Van Staden J. 2011. South African plants used in traditional medicine to treat epilepsy have an antagonistic effect on NMDA receptor currents. J Ethnopharmacol (in press).
43. Marchi N, Fan Q, Ghosh C, Fazio V, Bertolini F, Betto G, Batra A, Carlton E, Najm I, Granata T, Janigro D. 2009. Antagonism of peripheral inflammation reduces the severity of status epilepticus. Neurobiol Dis 33: 171-181.
44. Marchi N, Granata T, Freri E, Ciusani E, Ragona F, Puvenna V, Teng Q, Alexopolous A, Janigro D. 2011. Efficacy of anti-inflammatory therapy in a model of acute seizures and in a population of pediatric drug resistant epileptics. PLoS One 6: e18200.
45. Matute C. 2010. Therapeutic potential of kainate receptors. CNS Neurosci Ther (in press).
46. McDowell ML, Das A, Smith JA, Varma AK, Ray SK, Banik NL. 2011. Neuroprotective effects of genistein in VSC4.1 motoneurons exposed to activated microglial cytokines. Neurochem Int 59: 175-184.
47. v7.2 channels as a molecular target for epilepsy-causing mutations and anticonvulsants. Front Pharmacol 2: 2.
48. Mustafa AG, Wang JA, Carrico KM, Hall ED. 2011. Pharmacological inhibition of lipid peroxidation attenuates calpain-mediated cytoskeletal degradation after traumatic brain injury. J Neurochem 117: 579-588.
49. + channels in pilocarpine-treated epileptic rats. Brain Res 1348: 187-199.
50. Olkkola KT, Ahonen J. 2008. Midazolam and other benzodiazepines. Hdbk Exp Pharmacol 182: 335-360.
51. Paradiso B, Zucchini S, Su T, Bovolenta R, Berto E, Marconi P, Marzola A, Navarro Mora G, Fabene PF, Simonato M. 2011. Localized overexpression of FGF-2 and BDNF in hippocampus reduces mossy fiber sprouting and spontaneous seizures up to 4 weeks after pilocarpine-induced status epilepticus. Epilepsia 52: 572-578.
52. Pitkanen A, Sutula TP. 2002. Is epilepsy a progressive disorder? Prospects for new therapeutic approaches in temporal-lobe epilepsy. Lancet Neurol 1: 173-181.
53. Pitkanen A, Immonen RJ, Grohn OH, Kharatishvili I. 2009. From traumatic brain injury to posttraumatic epilepsy: what animal models tell us about the process and treatment options. Epilepsia 50( Suppl 2): 21-29.
54. Polascheck N, Bankstahl M, Löscher W. 2010. The COX-2 inhibitor parecoxib is neuroprotective but not antiepileptogenic in the pilocarpine model of temporal lobe epilepsy. Exp Neurol 224: 219-233.
55. Ravizza T, Balosso S, Vezzani A. 2011. Inflammation and prevention of epileptogenesis. Neurosci Lett 497: 223-230.
56. Ray SK, Samantaray S, Smith JA, Matzelle DD, Das A, Banik NL. 2011. Inhibition of cysteine proteases in acute and chronic spinal cord injury. Neurotherapeutics 8: 180-186.
57. Riazanski V, Deriy LV, Shevchenko PD, Le B, Gomez EA, Nelson DJ. 2011. Presynaptic CLC-3 determines quantal size of inhibitory transmission in the hippocampus. Nat Neurosci 14: 487-494.
58. Sandoval R, Gonzalez A, Caviedes A, Pancetti F, Smalla KH, Kaehne T, Michea L, Gundelfinger ED, Wyneken U. 2011. Homeostatic NMDA receptor down-regulation via brain derived neurotrophic factor and nitric oxide-dependent signalling in cortical but not in hippocampal neurons. J Neurochem (in press).
59. Sayyah M, Beheshti S, Shokrgozar MA, Eslami-far A, Deljoo Z, Khabiri AR, Haeri Rohani A. 2005. Antiepileptogenic and anticonvulsant activity of interleukin-1 beta in amygdala-kindled rats. Exp Neurol 191: 145-153.
60. Sharma AK, Reams RY, Jordan WH, Miller MA, Thacker HL, Snyder PW. 2007. Mesial temporal lobe epilepsy: pathogenesis, induced rodent models and lesions. Toxicol Pathol 35: 984-999.
61. Shinnar S, Hesdorffer DC, Nordli DRJr, Pellock JM, O'Dell C, Lewis DV, Frank LM, Moshe SL, Epstein LG, Marmarou A, Bagiella E. 2008. Phenomenology of prolonged febrile seizures: results of the FEBSTAT study. Neurology 71: 170-176.
62. Shorvon SD. 2009. Drug treatment of epilepsy in the century of the ILAE: the second 50 years, 1959-2009. Epilepsia 50( Suppl 3): 93-130.
63. Sieveking EH. 1857. Analysis of fifty-two cases of epilepsy observed by the author. Med Chir Trans 40: 157-166.
64. Sloviter RS. 1996. Hippocampal pathology and pathophysiology in temporal lobe epilepsy. Neurologia 11 Suppl 4: 29-32.
65. + buffering and gap junction coupling in the hippocampus. Glia 59: 973-980.
66. Stucki BL MD, Bolognani F, Perrone-Bizzozero NI, Banik NL, Griesemer DA, Ray SK. 2004. Upregulation of calpain in neuronal apoptosis in kainic acid induced seizures in rats. J Neurochem 90( Suppl 1): 8.
67. Takahashi DK, Vargas JR, Wilcox KS. 2010. Increased coupling and altered glutamate transport currents in astrocytes following kainic-acid-induced status epilepticus. Neurobiol Dis 40: 573-585.
68. Tian GF, Azmi H, Takano T, Xu Q, Peng W, Lin J, Oberheim N, Lou N, Wang X, Zielke HR, Kang J, Nedergaard M. 2005. An astrocytic basis of epilepsy. Nat Med 11: 973-981.
69. Vezzani A, Granata T. 2005. Brain inflammation in epilepsy: experimental and clinical evidence. Epilepsia 46: 1724-1743.
70. Vezzani A, Balosso S, Ravizza T. 2008. The role of cytokines in the pathophysiology of epilepsy. Brain Behav Immun 22: 797-803.
71. Wieser HG. 2004. ILAE Commission Report. Mesial temporal lobe epilepsy with hippocampal sclerosis. Epilepsia 45: 695-714.
72. Wong M. 2011. Rapamycin for treatment of epilepsy: antiseizure, antiepileptogenic, both, or neither? Epilepsy Curr 11: 66-68.
73. Yang T, Zhou D, Stefan H. 2010. Why mesial temporal lobe epilepsy with hippocampal sclerosis is progressive: uncontrolled inflammation drives disease progression? J Neurol Sci 296: 1-6.
74. Yellanki S, Jagtap S, Masareddy R. 2011. Dissofilm: a novel approach for delivery of phenobarbital; design and characterization. J Young Pharm 3: 181-188.
75. Zhang J, Yan H, Wu YP, Li C, Zhang GY. 2011. Activation of GluR6-containing kainate receptors induces ubiquitin-dependent Bcl-2 degradation via denitrosylation in the rat hippocampus after kainate treatment. J Biol Chem 286: 7669-7680.
76. Zheng XY, Zhang HL, Luo Q, Zhu J. 2011. Kainic acid-induced neurodegenerative model: potentials and limitations. J Biomed Biotechnol 2011: 457079.