Epigenetic Suppression of GADs Expression is Involved in Temporal Lobe Epilepsy and Pilocarpine-Induced Mice Epilepsy

Neurochemical Research

Volumn 41, Issue 7, 2016, Pages 1751-1760

  Wang, Jin Gang ^a   Cai, Qing ^b   Zheng, Jun ^a   Dong, Yu Shu ^c   Li, Jin Jiang ^c   Li, Jing Chen ^c   Hao, Guang Zhi ^c   Wang, Chao ^b   Wang, Ju Lei ^b  

^a The 463 Hospital of Chinese PLA   (China)

^b FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^c GENERAL HOSPITAL OF NORTHERN THEATER COMMAND   (China)

Author keywords

Epilepsy; GAD; HDAC; Histone acetylation; JNJ 26481585; Single cell PCR

Indexed keywords

GLUTAMATE DECARBOXYLASE; HYDROXAMIC ACID; PILOCARPINE; QUISINOSTAT;

ADOLESCENT; ADULT; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CHEMICALLY INDUCED; ENZYMOLOGY; EPILEPSY, TEMPORAL LOBE; FEMALE; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; HUMAN; MALE; MOUSE; PHYSIOLOGY; YOUNG ADULT;

ADOLESCENT; ADULT; ANIMALS; EPIGENESIS, GENETIC; EPILEPSY, TEMPORAL LOBE; FEMALE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLUTAMATE DECARBOXYLASE; HUMANS; HYDROXAMIC ACIDS; MALE; MICE; MICE, INBRED C57BL; PILOCARPINE; YOUNG ADULT;

EID: 84970021169     PISSN: 03643190     EISSN: 15736903     Source Type: Journal    
DOI: 10.1007/s11064-016-1891-3     Document Type: Article

References (44)

1. Dulac O, Milh M, Holmes GL (2013) Brain maturation and epilepsy. Handb Clin Neurol 111:441–446
2. Holmes GL, Milh MD, Dulac O (2012) Maturation of the human brain and epilepsy. Handb Clin Neurol 107:135–143
3. Mizielinska S, Greenwood S, Connolly CN (2006) The role of GABAA receptor biogenesis, structure and function in epilepsy. Biochem Soc Trans 34:863–867
4. Jagirdar R, Drexel M, Kirchmair E, Tasan RO, Sperk G (2015) Rapid changes in expression of class I and IV histone deacetylases during epileptogenesis in mouse models of temporal lobe epilepsy. Exp Neurol 273:92–104
5. Lusardi TA, Akula KK, Coffman SQ, Ruskin DN, Masino SA, Boison D (2015) Ketogenic diet prevents epileptogenesis and disease progression in adult mice and rats. Neuropharmacology 99:500–509
6. Ritter C, Gobel CH, Liebig T, Kaminksy E, Fink GR, Lehmann HC (2015) An epigenetic cause of seizures and brain calcification: pseudohypoparathyroidism. Lancet 385:1802
7. Parrish RR, Buckingham SC, Mascia KL, Johnson JJ, Matyjasik MM, Lockhart RM, Lubin FD (2015) Methionine increases BDNF DNA methylation and improves memory in epilepsy. Ann Clin Transl Neurol 2:401–416
8. Miller-Delaney SF, Bryan K, Das S, McKiernan RC, Bray IM, Reynolds JP, Gwinn R, Stallings RL, Henshall DC (2015) Differential DNA methylation profiles of coding and non-coding genes define hippocampal sclerosis in human temporal lobe epilepsy. Brain J Neurol 138:616–631
9. Kobow K, Blumcke I (2014) Epigenetic mechanisms in epilepsy. Prog Brain Res 213:279–316
10. Hwang JY, Aromolaran KA, Zukin RS (2013) Epigenetic mechanisms in stroke and epilepsy. Neuropsychopharmacol Off Publ Am Coll Neuropsychopharmacol 38:167–182
11. Roopra A, Dingledine R, Hsieh J (2012) Epigenetics and epilepsy. Epilepsia 53(Suppl 9):2–10
12. Belhedi N, Perroud N, Karege F, Vessaz M, Malafosse A, Salzmann A (2014) Increased CPA6 promoter methylation in focal epilepsy and in febrile seizures. Epilepsy Res 108:144–148
13. Fukuchi M, Nii T, Ishimaru N, Minamino A, Hara D, Takasaki I, Tabuchi A, Tsuda M (2009) Valproic acid induces up- or down-regulation of gene expression responsible for the neuronal excitation and inhibition in rat cortical neurons through its epigenetic actions. Neurosci Res 65:35–43
14. Zhang Z, Cai YQ, Zou F, Bie B, Pan ZZ (2011) Epigenetic suppression of GAD65 expression mediates persistent pain. Nat Med 17:1448–1455
15. Banerjee K, Akiba Y, Baker H, Cave JW (2013) Epigenetic control of neurotransmitter expression in olfactory bulb interneurons. Int J Dev Neurosci Off J Int Soc Dev Neurosci 31:415–423
16. Ueki N, Lee S, Sampson NS, Hayman MJ (2013) Selective cancer targeting with prodrugs activated by histone deacetylases and a tumour-associated protease. Nat Commun 4:2735
17. Benson MJ, Manzanero S, Borges K (2015) Complex alterations in microglial M1/M2 markers during the development of epilepsy in two mouse models. Epilepsia 56:895–905
18. Oliveira CV, Grigoletto J, Funck VR, Ribeiro LR, Royes LF, Fighera MR, Furian AF, Oliveira MS (2015) Evaluation of potential gender-related differences in behavioral and cognitive alterations following pilocarpine-induced status epilepticus in C57BL/6 mice. Physiol Behav 143:142–150
19. Leung A, Ahn S, Savvidis G, Kim Y, Iskandar D, Luna MJ, Kim KS, Cunningham M, Chung S (2015) Optimization of pilocarpine-mediated seizure induction in immunodeficient NodScid mice. Epilepsy Res 109:114–118
20. Castillo CG, Mendoza S, Freed WJ, Giordano M (2006) Intranigral transplants of immortalized GABAergic cells decrease the expression of kainic acid-induced seizures in the rat. Behav Brain Res 171:109–115
21. Racine RJ (1972) Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr Clin Neurophysiol 32:281–294
22. Racine R, Okujava V, Chipashvili S (1972) Modification of seizure activity by electrical stimulation. 3 Mechanisms. Electroencephalogr Clin Neurophysiol 32:295–299
23. Fang M, Shen L, Yin H, Pan YM, Wang L, Chen D, Xi ZQ, Xiao Z, Wang XF, Zhou SN (2011) Downregulation of gephyrin in temporal lobe epilepsy neurons in humans and a rat model. Synapse 65:1006–1014
24. Kash SF, Johnson RS, Tecott LH, Noebels JL, Mayfield RD, Hanahan D, Baekkeskov S (1997) Epilepsy in mice deficient in the 65-kDa isoform of glutamic acid decarboxylase. Proc Natl Acad Sci USA 94:14060–14065
25. Mathew J, Balakrishnan S, Antony S, Abraham PM, Paulose CS (2012) Decreased GABA receptor in the cerebral cortex of epileptic rats: effect of Bacopa monnieri and Bacoside-A. J Biomed Sci 19:25
26. Sakakibara T, Sukigara S, Otsuki T, Takahashi A, Kaneko Y, Kaido T, Saito Y, Sato N, Nakagawa E, Sugai K, Sasaki M, Goto Y, Itoh M (2012) Imbalance of interneuron distribution between neocortex and basal ganglia: consideration of epileptogenesis of focal cortical dysplasia. J Neurol Sci 323:128–133
27. Darrah SD, Miller MA, Ren D, Hoh NZ, Scanlon JM, Conley YP, Wagner AK (2013) Genetic variability in glutamic acid decarboxylase genes: associations with post-traumatic seizures after severe TBI. Epilepsy Res 103:180–194
28. Malter MP, Frisch C, Zeitler H, Surges R, Urbach H, Helmstaedter C, Elger CE, Bien CG (2015) Treatment of immune-mediated temporal lobe epilepsy with GAD antibodies. Seizure 30:57–63
29. He S, Bausch SB (2014) Synaptic plasticity in glutamatergic and GABAergic neurotransmission following chronic memantine treatment in an in vitro model of limbic epileptogenesis. Neuropharmacology 77:379–386
30. Alvestad S, Hammer J, Qu H, Haberg A, Ottersen OP, Sonnewald U (2011) Reduced astrocytic contribution to the turnover of glutamate, glutamine, and GABA characterizes the latent phase in the kainate model of temporal lobe epilepsy. J Cereb Blood Flow Metab Off J Int Soc Cereb Blood Flow Metab 31:1675–1686
31. Rajasekaran K, Kapur J, Bertram EH (2007) Alterations in GABA(A) receptor mediated inhibition in adjacent dorsal midline thalamic nuclei in a rat model of chronic limbic epilepsy. J Neurophysiol 98:2501–2508
32. Austin JE, Buckmaster PS (2004) Recurrent excitation of granule cells with basal dendrites and low interneuron density and inhibitory postsynaptic current frequency in the dentate gyrus of macaque monkeys. J Comp Neurol 476:205–218
33. Kobayashi M, Buckmaster PS (2003) Reduced inhibition of dentate granule cells in a model of temporal lobe epilepsy. J Neurosci Off J Soc Neurosci 23:2440–2452
34. Georgieva Z, Parton M (2014) Cerebellar ataxia and epilepsy with anti-GAD antibodies treatment with IVIG and plasmapheresis. BMJ Case Rep 2014:bcr2013202314
35. Leke R, Silveira TR, Escobar TD, Schousboe A (2014) Expression of Glutamate Decarboxylase (GAD) mRNA in the brain of bile duct ligated rats serving as a model of hepatic encephalopathy. Neurochem Res 39:605–611
36. Nasreen Z, Jameel T, Hasan A, Parveen N, Sadasivudu B (2012) Glutamate decarboxylase and GABA aminotransferase levels in different regions of rat brain on the onset of Leptazol induced convulsions. Neurochem Res 37:202–204
37. Erlander MG, Tillakaratne NJ, Feldblum S, Patel N, Tobin AJ (1991) Two genes encode distinct glutamate decarboxylases. Neuron 7:91–100
38. Esclapez M, Tillakaratne NJ, Kaufman DL, Tobin AJ, Houser CR (1994) Comparative localization of two forms of glutamic acid decarboxylase and their mRNAs in rat brain supports the concept of functional differences between the forms. J Neurosci Off J Soc Neurosci 14:1834–1855
39. Shen X, Liu Y, Xu S, Zhao Q, Wu H, Guo X, Shen R, Wang F (2014) Menin regulates spinal glutamate-GABA balance through GAD65 contributing to neuropathic pain. Pharmacol Rep PR 66:49–55
40. Kundakovic M, Chen Y, Guidotti A, Grayson DR (2009) The reelin and GAD67 promoters are activated by epigenetic drugs that facilitate the disruption of local repressor complexes. Mol Pharmacol 75:342–354
41. Krumholz A, Wiebe S, Gronseth G, Shinnar S, Levisohn P, Ting T, Hopp J, Shafer P, Morris H, Seiden L, Barkley G, French J, Quality Standards Subcommittee of the American Academy of N, American Epilepsy S (2007) Practice parameter: evaluating an apparent unprovoked first seizure in adults (an evidence-based review): report of the Quality Standards Subcommittee of the American Academy of Neurology and the American Epilepsy Society. Neurology 69:1996–2007
42. Stuhmer T, Arts J, Chatterjee M, Borawski J, Wolff A, King P, Einsele H, Leo E, Bargou RC (2010) Preclinical anti-myeloma activity of the novel HDAC-inhibitor JNJ-26481585. Br J Haematol 149:529–536
43. Capasso KE, Manners MT, Quershi RA, Tian Y, Gao R, Hu H, Barrett JE, Sacan A, Ajit SK (2015) Effect of histone deacetylase inhibitor JNJ-26481585 in pain. J Mol Neurosci MN 55:570–578
44. Arts J, King P, Marien A, Floren W, Belien A, Janssen L, Pilatte I, Roux B, Decrane L, Gilissen R, Hickson I, Vreys V, Cox E, Bol K, Talloen W, Goris I, Andries L, Du Jardin M, Janicot M, Page M, van Emelen K, Angibaud P (2009) JNJ-26481585, a novel “second-generation” oral histone deacetylase inhibitor, shows broad-spectrum preclinical antitumoral activity. Clin Cancer Res Off J Am Assoc Cancer Res 15:6841–6851