Ketogenic diet attenuates neuronal injury via autophagy and mitochondrial pathways in pentylenetetrazol-kindled seizures

Brain Research

Volumn 1678, Issue , 2018, Pages 106-115

  Wang, Bao Hui ^a   Hou, Qun ^a   Lu, Yu Qiang ^b   Jia, Meng Meng ^a   Qiu, Tao ^a   Wang, Xiao Hang ^a   Zhang, Zheng Xiang ^a   Jiang, Yan ^a  

^a ZHEJIANG CHINESE MEDICAL UNIVERSITY   (China)

^b Tongde Hospital of Zhejiang Province   (China)

Author keywords

Autophagy; Ketogenic diet; Mitochondrial pathway; Neuroprotection; Pentylenetetrazol kindled seizure

Indexed keywords

3 METHYLADENINE; AUTOPHAGY RELATED PROTEIN 5; BECLIN 1; CASPASE 3; CYTOCHROME C; MICROTUBULE ASSOCIATED PROTEIN 1; MITOCHONDRIAL PROTEIN; RAPAMYCIN; 3-METHYLADENINE; ADENINE; NEUROPROTECTIVE AGENT; PENTETRAZOLE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPHAGY; BRAIN INJURY; BRAIN MITOCHONDRION; CELL COUNT; CELL VACUOLE; CLONUS; CONTROLLED STUDY; CYTOSOL; DISEASE SEVERITY; DOWN REGULATION; EPILEPSY; HIPPOCAMPAL CA1 REGION; HIPPOCAMPUS; KETOGENIC DIET; MALE; MITOCHONDRIAL MEMBRANE; NERVE CELL DEGENERATION; NEUROPROTECTION; NONHUMAN; PENTYLENETETRAZOLE-INDUCED SEIZURE; PRIORITY JOURNAL; RAT; RIGHT HIPPOCAMPUS; UPREGULATION; ANALOGS AND DERIVATIVES; ANIMAL; APOPTOSIS; DRUG EFFECTS; METABOLISM; MITOCHONDRION; NERVE CELL; PATHOPHYSIOLOGY; PHYSIOLOGY; PROCEDURES; SEIZURE; SPRAGUE DAWLEY RAT;

ADENINE; ANIMALS; APOPTOSIS; AUTOPHAGY; CASPASE 3; CYTOCHROMES C; DIET, KETOGENIC; EPILEPSY; HIPPOCAMPUS; MALE; MITOCHONDRIA; NEURONS; NEUROPROTECTIVE AGENTS; PENTYLENETETRAZOLE; RATS; RATS, SPRAGUE-DAWLEY; SEIZURES; SIROLIMUS;

EID: 85032022287     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2017.10.009     Document Type: Article

References (40)

1. Alirezaei, M., Kemball, C.C., Flynn, C.T., Wood, M.R., Whitton, J.L., Kiosses, W.B., Short-term fasting profound neuronal autophagy. Autophagy 6 (2010), 702–710.
2. Balog, J., Mehta, S.L., Vemuganti, R., Mitochondrial fission and fusion in secondary brain damage after CNS insults. J. Cereb. Blood Flow Metab. 36 (2016), 2022–2033.
3. Bejarano, E., Rodríguez-Navarro, J.A., Autophagy and amino acid metabolism in the brain: implications for epilepsy. Amino Acids 47 (2014), 2113–2126.
4. Benz, A.P., Niquet, J., Wasterlain, C.G., Rami, A., Status epilepticus in the immature rodent brain alters the dynamics of autophagy. Curr. Neurovasc. Res. 11 (2014), 125–135.
5. Blümcke, I., Zuschratter, W., Schewe, J.C., Suter, B., Ailing, A.L., Riederer, B.M., Meyer, B., Schramm, J., Elger, C.E., Wiestler, O.D., Cellular pathology of hilar neurons in ammon's horn sclerosis. J. Comp. Neurol. 414 (1999), 437–453.
6. Bough, K.J., Eagles, D.A., A ketogenic diet increases the resistance to pentylenetetrazole-induced seizures in the rat. Epilepsia 40 (1999), 138–143.
7. Bough, K.J., Wetherington, J., Hassel, B., Pare, J.F., Gawryluk, J.W., Greene, J.G., Shaw, R., Smith, Y., Geiger, J.D., Dingledine, R.J., Mitochondrial biogenesis in the anticonvulsant mechanism of the ketogenic diet. Ann. Neurol. 60 (2006), 223–235.
8. Camberos-Luna, L., Geronimo-Olvera, C., Montiel, T., Rincon-Heredia, R., Massieu, L., The ketone body, beta-hydroxybutyrate stimulates the autophagic flux and prevents neuronal death induced by glucose deprivation in cortical cultured neurons. Neurochem. Res. 41 (2016), 600–609.
9. Finn, P.F., Dice, J.F., Ketone bodies stimulate chaperone-mediated autophagy. J. Biol. Chem. 280 (2005), 25864–25870.
10. Giorgi, F.S., Biagioni, F., Lenzi, P., Frati, A., Fornai, F., The role of autophagy in epileptogenesis and in epilepsy-induced neuronal alterations. J. Neural Transm. (Vienna) 122 (2015), 849–862.
11. Hansen, S.L., Nielsen, A.H., Knudsen, K.E., Artmann, A., Petersen, G., Kristiansen, U., Hansen, S.H., Hansen, H.S., Ketogenic diet is antiepileptogenic in pentylenetetrazole kindled mice and decrease levels of N-acylethanolamines in hippocampus. Neurochem. Int. 54 (2009), 199–204.
12. He, C., Sumpter, R. Jr., Levine, B., Exercise induces autophagy in peripheral tissues and in the brain. Autophagy 8 (2012), 1548–1551.
13. Hori, A., Tandon, P., Holmes, G.L., Stafstrom, C.E., Ketogenic diet effects on expression of kindled seizures and behavior in adult rats. Epilepsia 38 (1997), 750–758.
14. Hu, Z.G., Wang, H.D., Jin, W., Yin, H.X., Ketogenic diet reduces cytochrome c release and cellular apoptosis following traumatic brain injury in juvenile rats. Ann. Clin. Lab. Sci. 39 (2009), 76–83.
15. Jiang, Y., Yang, Y., Wang, S., Ding, Y., Guo, Y., Zhang, M.M., Wen, S.Q., Ding, M.P., Ketogenic diet protects against epileptogenesis as well as neuronal loss in amygdaloid-kindling seizures. Neurosci. Lett. 508 (2012), 22–26.
16. Jiang, Y., Lu, Y., Jia, M., Wang, X., Zhang, Z., Hou, Q., Wang, B., Ketogenic diet attenuates spatial and item memory impairment in pentylenetetrazol-kindled rats. Brain Res. 1646 (2016), 451–458.
17. Jing, C.H., Wang, L., Liu, P.P., Wu, C., Ruan, D., Chen, G., Autophagy activation is associated with neuroprotection against apoptosis via a mitochondrial pathway in a rat model of subarachnoid hemorrhage. Neuroscience 213 (2012), 144–153.
18. Kim, Y.C., Guan, K.-L., mTOR_ a pharmacologic target for autophagy. J. Clin. Invest. 125 (2015), 25–32.
19. Knecht, E., Aguado, C., Sarkar, S., Korolchuk, V.I., Criado-Garcia, O., Vernia, S., Boya, P., Sanz, P., Rodriguez de Cordoba, S., Rubinsztein, D.C., Impaired autophagy in Lafora disease. Autophagy 6 (2010), 991–993.
20. Kundu, M., Thompson, C.B., Macroautophagy versus mitochondrial autophagy: a question of fate?. Cell Death Differ. 12 (2005), 1484–1489.
21. Levine, B., Klionsky, D.J., Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev. Cell 6 (2004), 463–477.
22. Linard, B., Ferrandon, A., Koning, E., Nehlig, A., Raffo, E., 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 (2010), 1829–1836.
23. Maiese, K., Targeting molecules to medicine with mTOR, autophagy, and neurodegenerative disorders. Br. J. Clin. Pharmacol. 82 (2015), 1245–1266.
24. McMahon, J., Huang, X., Yang, J., Komatsu, M., Yue, Z., Qian, J., Zhu, X., Huang, Y., Impaired autophagy in neurons after disinhibition of mammalian target of rapamycin and its contribution to epileptogenesis. J. Neurosci. 32 (2012), 15704–15714.
25. Mizushima, N., Methods for monitoring autophagy. Int. J. Biochem. Cell Biol. 36 (2004), 2491–2502.
26. Ni, H., Zhao, D.J., Tian, T., Ketogenic diet change cPLA2/clusterin and autophagy related gene expression and correlate with cognitive deficits and hippocampal MFs sprouting following neonatal seizures. Epilepsy Res. 120 (2016), 13–18.
27. Noh, H., The protective effect of a ketogenic diet on kainic acid-induced hippocampal cell death in the male ICR mice. Epilepsy Res. 53 (2003), 119–128.
28. Otabe, H., Nibuya, M., Shimazaki, K., Toda, H., Suzuki, G., Nomura, S., Shimizu, K., Electroconvulsive seizures enhance autophagy signaling in rat hippocampus. Prog. Neuropsychopharmacol. Biol. Psychiatry 50 (2014), 37–43.
29. Racine, R.J., Gartner, J.G., Burnham, W.M., Epileptiform activity and neural plasticity in limbic structures. Brain Res. 47 (1972), 262–268.
30. Ratliff, E.P., Barekat, A., Lipinski, M.M., Finley, K.D., Brain trauma and autophagy: what flies and mice can teach us about conserved responses. Autophagy 12 (2016), 2256–2257.
31. Rowley, S., Patel, M., Mitochondrial involvement and oxidative stress in temporal lobe epilepsy. Free Radical Biol. Med. 62 (2013), 121–131.
32. Shi, R., Weng, J., Zhao, L., Li, X.M., Gao, T.M., Kong, J., Excessive autophagy contributes to neuron death in cerebral ischemia. CNS Neurosci. Ther. 18 (2012), 250–260.
33. Tait, S.W.G., Green, D.R., Mitochondria and cell death: outer membrane permeabilization and beyond. Nat. Rev. Mol. Cell Biol. 11 (2010), 621–632.
34. Takagi, A., Kume, S., Maegawa, H., Uzu, T., Emerging role of mammalian autophagy in ketogenesis to overcome starvation. Autophagy 12 (2016), 709–710.
35. Wang, S., Ding, Y., Ding, X.Y., Liu, Z.R., Shen, C.H., Jin, B., Guo, Y., Wang, S., Ding, M.P., Effectiveness of ketogenic diet in pentylenetetrazol-induced and kindling rats as well as its potential mechanisms. Neurosci. Lett. 614 (2016), 1–6.
36. Wong, M., Cleaning up epilepsy and neurodegeneration: the role of autophagy in epileptogenesis. Epilepsy Curr. 13 (2013), 177–178.
37. Xu, L., Kanasaki, M., He, J., Kitada, M., Nagao, K., Jinzu, H., Noguchi, Y., Maegawa, H., Kanasaki, K., Koya, D., Ketogenic essential amino acids replacement diet ameliorated hepatosteatosis with altering autophagy-associated molecules. Biochim. Biophys. Acta 1832 (2013), 1605–1612.
38. Zeng, L.H., Rensing, N.R., Wong, M., The mammalian target of rapamycin signaling pathway mediates epileptogenesis in a model of temporal lobe epilepsy. J. Neurosci. 29 (2009), 6964–6972.
39. Zhang, X., Yan, H., Yuan, Y., Gao, J., Shen, Z., Cheng, Y., Shen, Y., Wang, R.R., Wang, X., Hu, W.W., Wang, G., Chen, Z., Cerebral ischemia-reperfusion-induced autophagy protects against neuronal injury by mitochondrial clearance. Autophagy 9 (2013), 1321–1333.
40. Zsurka, G., Kunz, W.S., Mitochondrial dysfunction and seizures: the neuronal energy crisis. Lancet Neurol. 14 (2015), 956–966.