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ORIGINAL RESEARCH

Ketogenic Diet Alleviates Hippocampal Neurodegeneration Possibly via ASIC1a and the Mitochondria-Mediated Apoptotic Pathway in a Rat Model of Temporal Lobe Epilepsy

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Pages 2181-2198 | Received 01 Jun 2022, Accepted 14 Sep 2022, Published online: 25 Sep 2022

References

  • Franco V, French JA, Perucca E. Challenges in the clinical development of new antiepileptic drugs. Pharmacol Res. 2016;103:95–104. doi:10.1016/j.phrs.2015.11.007
  • Hermann BP, Seidenberg M, Dow C, et al. Cognitive prognosis in chronic temporal lobe epilepsy. Ann Neurol. 2006;60:80–87. doi:10.1002/ana.20872
  • Lenck-Santini PP, Scott RC. Mechanisms responsible for cognitive impairment in epilepsy. Cold Spring Harb Perspect Med. 2015;5(10):a022772. doi:10.1101/cshperspect.a022772
  • Wang X, Huang SP, Liu Y, et al. Effects of ketogenic diet on cognitive function in pentylenetetrazol-kindled rats. Epilepsy Res. 2021;170:106534. doi:10.1016/j.eplepsyres.2020.106534
  • Murugan M, Boison D. Ketogenic diet, neuroprotection, and antiepileptogenesis. Epilepsy Res. 2020;167:106444. doi:10.1016/j.eplepsyres.2020.106444
  • Noh HS, Kim YS, Choi WS. Neuroprotective effects of the ketogenic diet. Epilepsia. 2008;49(Suppl 8):120–123. doi:10.1111/j.1528-1167.2008.01855.x
  • Blumcke I, Spreafico R, Haaker G, et al. Histopathological findings in brain tissue obtained during epilepsy surgery. N Engl J Med. 2017;377:1648–1656. doi:10.1056/NEJMoa1703784
  • Walker MC. Hippocampal sclerosis causes and prevention. Semin Neurol. 2015;35:193–200. doi:10.1055/s-0035-1552618
  • Gourmaud S, Shou HC, Irwin DJ, et al. Alzheimer-like amyloid and tau alterations associated with cognitive deficit in temporal lobe epilepsy. Brain. 2020;143:191–209. doi:10.1093/brain/awz381
  • Alvarez de la Rosa D, Krueger SR, Kolar A, et al. Distribution, subcellular localization and ontogeny of ASIC1 in the mammalian central nervous system. J Physiol. 2003;546:77–87. doi:10.1113/jphysiol.2002.030692
  • Alvarez de la Rosa D, Zhang P, Shao D, et al. Functional implications of the localization and activity of acid-sensitive channels in rat peripheral nervous system. Proc Natl Acad Sci U S A. 2002;992:326–331. doi:10.1073/pnas.042688199
  • Xiong ZG, Zhu XM, Chu XP, et al. Neuroprotection in ischemia blocking calcium-permeable acid-sensing ion channels. Cell. 2004;118:687–698. doi:10.1016/j.cell.2004.08.026
  • Xiong ZG, Pignataro G, Li MH, et al. Acid-sensing ion channels (ASICs) as pharmacological targets for neurodegenerative diseases. Curr Opin Pharmacol. 2008;8:25–32. doi:10.1016/j.coph.2007.09.001
  • Siesjo BK, von Hanwehr R, Nergelius G, et al. Extra- and intracellular pH in the brain during seizures and in the recovery period following the arrest of seizure activity. J Cereb Blood Flow Metab. 1985;5:47–57. doi:10.1038/jcbfm.1985.7
  • Somjen GG. Acidification of interstitial fluid in hippocampal formation caused by seizures and by spreading depression. Brain Res. 1984;311:186–188. doi:10.1016/0006-8993(84)91416-1
  • Lv RJ, He JS, Fu YH, et al. ASIC1a polymorphism is associated with temporal lobe epilepsy. Epilepsy Res. 2011;96:74–80. doi:10.1016/j.eplepsyres.2011.05.002
  • Yang F, Sun XL, Ding YX, et al. Astrocytic acid-sensing ion channel 1a contributes to the development of chronic epileptogenesis. Sci Rep. 2016;6:31581. doi:10.1038/srep31581
  • Ievglevskyi O, Isaev D, Netsyk O, et al. Acid-sensing ion channels regulate spontaneous inhibitory activity in the hippocampus possible implications for epilepsy. Philos Trans R Soc Lond B Biol Sci. 2016;371(1700):20150431. doi:10.1098/rstb.2015.0431
  • Wu H, Wang C, Liu B, et al. Altered expression pattern of acid-sensing ion channel isoforms in piriform cortex after seizures. Mol Neurobiol. 2016;53:1782–1793. doi:10.1007/s12035-015-9130-5
  • Savic Azoulay I, Liu F, Hu Q, et al. ASIC1a channels regulate mitochondrial ion signaling and energy homeostasis in neurons. J Neurochem. 2020;153:203–215. doi:10.1111/jnc.14971
  • Wang YZ, Zeng WZ, Xiao X, et al. Intracellular ASIC1a regulates mitochondrial permeability transition-dependent neuronal death. Cell Death Differ. 2013;201:359–369. doi:10.1038/cdd.2013.90
  • Zhu F, Shan W, Xu QL, et al. Ketone bodies inhibit the opening of Acid-Sensing Ion Channels (ASICs) in rat hippocampal excitatory neurons in vitro. Front Neurol. 2019;10:155. doi:10.3389/fneur.2019.00155
  • Curia G, Longo D, Biagini G, et al. The pilocarpine model of temporal lobe epilepsy. J Neurosci Methods. 2008;172:143–157. doi:10.1016/j.jneumeth.2008.04.019
  • Smith ZZ, Benison AM, Bercum FM, et al. Progression of convulsive and nonconvulsive seizures during epileptogenesis after pilocarpine-induced status epilepticus. J Neurophysiol. 2018;119:1818–1835. doi:10.1152/jn.00721.2017
  • Racine RJ. Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr Clin Neurophysiol. 1972;32:281–294. doi:10.1016/0013-4694(72)90177-0
  • Su SW, Cilio MR, Sogawa Y, et al. Timing of ketogenic diet initiation in an experimental epilepsy model. Brain Res Dev Brain Res. 2000;125:131–138. doi:10.1016/s0165-3806(00)00130-9
  • Sun C, Fu J, Qu ZZ, et al. Chronic mild hypoxia promotes hippocampal neurogenesis involving Notch1 signaling in epileptic rats. Brain Res. 2019;171:488–498. doi:10.1016/j.brainres.2019.02.011
  • Sun C, Fu J, Qu ZZ, et al. Chronic intermittent hypobaric hypoxia restores hippocampus function and rescues cognitive impairments in chronic epileptic rats via wnt/beta-catenin signaling. Front Mol Neurosci. 2020;13:617143. doi:10.3389/fnmol.2020.617143
  • Flameng W, Borgers M, Daenen W, et al. Ultrastructural and cytochemical correlates of myocardial protection by cardiac hypothermia in man. J Thorac Cardiovasc Surg. 1980;79:413–424.
  • Krasemann S, Madore C, Cialic R, et al. The TREM2-APOE pathway drives the transcriptional phenotype of dysfunctional microglia in neurodegenerative diseases. Immunity. 2017;47(3):566–581.e9. doi:10.1016/j.immuni.2017.08.008
  • Im EJ, Lee CH, Moon PG, et al. Sulfisoxazole inhibits the secretion of small extracellular vesicles by targeting the endothelin receptor A. Nat Commun. 2019;10(1):1387. doi:10.1038/s41467-019-09387-4
  • Yermolaieva O, Soren Leonard A, Schnizler MK, et al. Extracellular acidosis increases neuronal cell calcium by activating acid-sensing ion channel 1a. Proc Natl Acad Sci U S A. 2004;101:6752–6757. doi:10.1073/pnas.0308636100
  • Kann O, Kovacs R. Mitochondria and neuronal activity. Am J Physiol Cell Physiol. 2007;292:C641–57. doi:10.1152/ajpcell.00222.2006
  • Janson MT, Bainbridge JL. Continuing burden of refractory epilepsy. Ann Pharmacother. 2021;55(3):406–408. doi:10.1177/1060028020948056
  • Ghannad-Rezaie M, Eimon PM, Wu Y, Yanik MF. Engineering brain activity patterns by neuromodulator polytherapy for treatment of disorders. Nat Commun. 2019;10(1):2620. doi:10.1038/s41467-019-10541-1
  • Fu P, Yuan Q, Sun Y, et al. Baicalein ameliorates epilepsy symptoms in a pilocarpine-induced rat model by regulation of IGF1R. Neurochem Res. 2020;45(12):3021–3033. doi:10.1007/s11064-020-03150-8
  • Mishra P, Mittal AK, Rajput SK, Sinha JK. Cognition and memory impairment attenuation via reduction of oxidative stress in acute and chronic mice models of epilepsy using antiepileptogenic Nux vomica. J Ethnopharmacol. 2021;267:113509. doi:10.1016/j.jep.2020.113509
  • Mishra P, Sinha JK, Rajput SK. Efficacy of Cicuta virosa medicinal preparations against pentylenetetrazole-induced seizures. Epilepsy Behav. 2021;115:107653. doi:10.1016/j.yebeh.2020.107653
  • Ghosh S, Sinha JK, Khan T, et al. Pharmacological and therapeutic approaches in the treatment of epilepsy. Biomedicines. 2021;9(5):470. doi:10.3390/biomedicines9050470
  • Alese OO, Mabandla MV. Upregulation of hippocampal synaptophysin, GFAP and mGluR3 in a pilocarpine rat model of epilepsy with history of prolonged febrile seizure. J Chem Neuroanat. 2019;100:101659. doi:10.1016/j.jchemneu.2019.101659
  • Singh T, Mishra A, Goel RK. PTZ kindling model for epileptogenesis, refractory epilepsy, and associated comorbidities: relevance and reliability. Metab Brain Dis. 2021;36(7):1573–1590. doi:10.1007/s11011-021-00823-3
  • Pitkanen A, Lukasiuk K, Edward Dudek F, et al. Epileptogenesis. Cold Spring Harb Perspect Med. 2015;5(10):a022822. doi:10.1101/cshperspect.a022822
  • Lusardi TA, Akula KK, Coffman SQ, et al. Ketogenic diet prevents epileptogenesis and disease progression in adult mice and rats. Neuropharmacology. 2015;99:500–509. doi:10.1016/j.neuropharm.2015.08.007
  • Jiang Y, Yang Y, Wang S, et al. Ketogenic diet protects against epileptogenesis as well as neuronal loss in amygdaloid-kindling seizures. Neurosci Lett. 2012;508:22–26. doi:10.1016/j.neulet.2011.12.002
  • Vrinda M, Arun S, Srikumar BN, et al. Temporal lobe epilepsy-induced neurodegeneration and cognitive deficits Implications for aging. J Chem Neuroanat. 2019;95:146–153. doi:10.1016/j.jchemneu.2018.02.005
  • Bell B, Lin JJ, Seidenberg M, et al. The neurobiology of cognitive disorders in temporal lobe epilepsy. Nat Rev Neurol. 2011;7:154–164. doi:10.1038/nrneurol.2011.3
  • Lambrechts DA, Wielders LHP, Aldenkamp AP, et al. The ketogenic diet as a treatment option in adults with chronic refractory epilepsy efficacy and tolerability in clinical practice. Epilepsy Behav. 2012;23:310–314. doi:10.1016/j.yebeh.2012.01.002
  • Tai XY, Bernhardt B, Thom M, et al. Review Neurodegenerative processes in temporal lobe epilepsy with hippocampal sclerosis Clinical, pathological and neuroimaging evidence. Neuropathol Appl Neurobiol. 2018;44:70–90. doi:10.1111/nan.12458
  • Nobili P, Colciaghi F, Finardi A, et al. Continuous neurodegeneration and death pathway activation in neurons and glia in an experimental model of severe chronic epilepsy. Neurobiol Dis. 2015;83:54–66. doi:10.1016/j.nbd.2015.08.002
  • Luan G, Zhao YX, Zhai F, et al. Ketogenic diet reduces Smac/Diablo and cytochrome c release and attenuates neuronal death in a mouse model of limbic epilepsy. Brain Res Bull. 2012;89:79–85. doi:10.1016/j.brainresbull.2012.07.002
  • Zhen JL, Wang WP, Zhou JJ, et al. Chronic intermittent hypoxic preconditioning suppresses pilocarpine-induced seizures and associated hippocampal neurodegeneration. Brain Res. 2014;1563:122–130. doi:10.1016/j.brainres.2014.03.032
  • Gao S, Yu Y, Ma ZY, et al. NMDAR-mediated hippocampal neuronal death is exacerbated by activities of ASIC1a. Neurotox Res. 2015;281:22–37. doi:10.1007/s12640-015-9530-3
  • Ma CL, Sun H, Yang L, et al. Acid-sensing ion channel 1a modulates NMDA receptor function through targeting NR1/NR2A/NR2B triheteromeric receptors. Neuroscience. 2019;406:389–404. doi:10.1016/j.neuroscience.2019.03.044
  • Henshall DC. Apoptosis signalling pathways in seizure-induced neuronal death and epilepsy. Biochem Soc Trans. 2007;35:421–423. doi:10.1042/BST0350421
  • Waldbaum S, Patel M. Mitochondria, oxidative stress, and temporal lobe epilepsy. Epilepsy Res. 2010;88:23–45. doi:10.1016/j.eplepsyres.2009.09.020
  • Folbergrova J, Kunz WS. Mitochondrial dysfunction in epilepsy. Mitochondrion. 2012;12:35–40. doi:10.1016/j.mito.2011.04.004
  • Rao VK, Carlson EA, Yan SS. Mitochondrial permeability transition pore is a potential drug target for neurodegeneration. Biochim Biophys Acta. 2014;1842:1267–1272. doi:10.1016/j.bbadis.2013.09.003
  • Liu Z, Pei H, Zhang LM, et al. Mitochondria-targeted DNA nanoprobe for real-time imaging and simultaneous quantification of Ca(2+) and pH in neurons. ACS Nano. 2018;12:12357–12368. doi:10.1021/acsnano.8b06322
  • Liang JJ, Huang LF, Chen XM, et al. Amiloride suppresses pilocarpine-induced seizures via ASICs other than NHE in rats. Int J Clin Exp Pathol. 2015;8:14507–14513.
  • Ali A, Pillai KP, Ahmad FJ, et al. Anticonvulsant effect of amiloride in pentetrazole-induced status epilepticus in mice. Pharmacol Rep. 2006;58:242–245.
  • Luszczki JJ, Sawicka KM, Kozinska J, et al. Amiloride enhances the anticonvulsant action of various antiepileptic drugs in the mouse maximal electroshock seizure model. J Neural Transm. 2009;116:57–66. doi:10.1007/s00702-008-0152-2
  • Ou-Yang TP, Zhu GM, Ding YX, et al. The effects of amiloride on seizure activity, cognitive deficits and seizure-induced neurogenesis in a novel rat model of febrile seizures. Neurochem Res. 2016;41:933–942. doi:10.1007/s11064-015-1777-9
  • Biagini G, Babinski K, Avoli M, et al. Regional and subunit-specific downregulation of acid-sensing ion channels in the pilocarpine model of epilepsy. Neurobiol Dis. 2001;8:45–58. doi:10.1006/nbdi.2000.0331
  • Ziemann AE, Schnizler MK, Albert GW, et al. Seizure termination by acidosis depends on ASIC1a. Nat Neurosci. 2008;11:816–822. doi:10.1038/nn.2132
  • Becker AJ. Review Animal models of acquired epilepsy insights into mechanisms of human epileptogenesis. Neuropathol Appl Neurobiol. 2018;44:112–129. doi:10.1111/nan.12451
  • Covolan L, Mello LE. Temporal profile of neuronal injury following pilocarpine or kainic acid-induced status epilepticus. Epilepsy Res. 2000;39:133–152. doi:10.1016/s0920-1211(99)00119-9
  • Wei D, Yang F, Wang Y, et al. Degeneration and regeneration of GABAergic interneurons in the dentate gyrus of adult mice in experimental models of epilepsy. CNS Neurosci Ther. 2015;21:52–60. doi:10.1111/cns.12330
  • Magloczky Z, Freund TF. Impaired and repaired inhibitory circuits in the epileptic human hippocampus. Trends Neurosci. 2005;28:334–340. doi:10.1016/j.tins.2005.04.002