Methionine increases BDNF DNA methylation and improves memory in epilepsy

Annals of Clinical and Translational Neurology

Volumn 2, Issue 4, 2015, Pages 401-416

  Parrish, R Ryley ^a   Buckingham, Susan C ^a   Mascia, Katherine L ^a   Johnson, Jarvis J ^a   Matyjasik, Michal M ^b   Lockhart, Roxanne M ^a   Lubin, Farah D ^a  

^a University of Alabama at Birmingham   (United States)

^b WEBER STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; DECITABINE; DNA METHYLTRANSFERASE; KAINIC ACID; METHIONINE;

ADULT; AMNESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY; ARTICLE; CONTROLLED STUDY; DIET SUPPLEMENTATION; DNA METHYLATION; DNA SEQUENCE; ELECTROENCEPHALOGRAPHY; EPIGENETICS; EPILEPTIC STATE; FEAR CONDITIONING TEST; GENE EXPRESSION; GENETIC TRANSCRIPTION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; LEARNING; MALE; MEMORY; MEMORY CONSOLIDATION; MEMORY DISORDER; NONHUMAN; OPEN FIELD TEST; POWER SPECTRUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION; SEIZURE; SPIKE WAVE; TEMPORAL LOBE EPILEPSY; WESTERN BLOTTING;

EID: 85030779616     PISSN: None     EISSN: 23289503     Source Type: Journal    
DOI: 10.1002/acn3.183     Document Type: Article

References (69)

1. Kleen JK, Scott RC, Lenck-Santini PP, Holmes GL. Cognitive and behavioral co-morbidities of epilepsy. In: Noebels JL, Avoli M, Rogawski MA, Olsen RW, Delgado-Escueta AV, eds. Jasper’s basic mechanisms of the epilepsies. 4th ed. Bethesda, MD: Oxford University Press, 2012; pp. 915-929.
2. Levenson JM, Roth TL, Lubin FD, et al. Evidence that DNA (cytosine-5) methyltransferase regulates synaptic plasticity in the hippocampus. J Biol Chem 2006;281:15763-15773.
3. Lubin FD, Roth TL, Sweatt JD. Epigenetic regulation of BDNF gene transcription in the consolidation of fear memory. J Neurosci 2008;28:10576-10586.
4. Nelson ED, Kavalali ET, Monteggia LM. Activitydependent suppression of miniature neurotransmission through the regulation of DNA methylation. J Neurosci 2008;28:395-406.
5. Guo JU, Ma DK, Mo H, et al. Neuronal activity modifies the DNA methylation landscape in the adult brain. Nat Neurosci 2011;14:1345-1351.
6. Feng J, Fan G. The role of DNA methylation in the central nervous system and neuropsychiatric disorders. Int Rev Neurobiol 2009;89:67-84.
7. Kobow K, Jeske I, Hildebrandt M, et al. Increased reelin promoter methylation is associated with granule cell dispersion in human temporal lobe epilepsy. J Neuropathol Exp Neurol 2009;68:356-364.
8. Miller-Delaney SF, Das S, Sano T, et al. Differential DNA methylation patterns define status epilepticus and epileptic tolerance. J Neurosci 2012;32:1577-1588.
9. Kobow K, Kaspi A, Harikrishnan KN, et al. Deep sequencing reveals increased DNA methylation in chronic rat epilepsy. Acta Neuropathol 2013;126:741-756.
10. Ryley Parrish R, Albertson AJ, Buckingham SC, et al. Status epilepticus triggers early and late alterations in brain-derived neurotrophic factor and NMDA glutamate receptor Grin2b DNA methylation levels in the hippocampus. Neuroscience 2013;248C:602-619.
11. Williams-Karnesky RL, Sandau US, Lusardi TA, et al. Epigenetic changes induced by adenosine augmentation therapy prevent epileptogenesis. J Clin Invest 2013;123:3552-3563.
12. Scharfman HE, Goodman JH, Sollas AL, Croll SD. Spontaneous limbic seizures after intrahippocampal infusion of brain-derived neurotrophic factor. Exp Neurol 2002;174:201-214.
13. Binder DK. The role of BDNF in epilepsy and other diseases of the mature nervous system. Adv Exp Med Biol 2004;548:34-56.
14. McNamara JO, Huang YZ, Leonard AS. Molecular signaling mechanisms underlying epileptogenesis. Science’s STKE: signal transduction knowledge environment. 2006;2006:re12.
15. Liu IY, Lyons WE, Mamounas LA, Thompson RF. Brainderived neurotrophic factor plays a critical role in contextual fear conditioning. J Neurosci 2004;24:7958-7963.
16. Cunha C, Angelucci A, D’Antoni A, et al. Brain-derived neurotrophic factor (BDNF) overexpression in the forebrain results in learning and memory impairments. Neurobiol Dis 2009;33:358-368.
17. Martinowich K, Hattori D, Wu H, et al. DNA methylationrelated chromatin remodeling in activity-dependent BDNF gene regulation. Science 2003;302:890-893.
18. Bekinschtein P, Cammarota M, Izquierdo I, Medina JH. BDNF and memory formation and storage. Neuroscientist 2008;14:147-156.
19. Racine RJ. Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr Clin Neurophysiol. 1972;32:281-294.
20. Rubin RA, Ordonez LA, Wurtman RJ. Physiological dependence of brain methionine and Sadenosylmethionine concentrations on serum amino acid pattern. J Neurochem 1974;23:227-231.
21. Roth TL, Lubin FD, Funk AJ, Sweatt JD. Lasting epigenetic influence of early-life adversity on the BDNF gene. Biol Psychiatry 2009;65:760-769.
22. Parrish RR, Day JJ, Lubin FD. Direct bisulfite sequencing for examination of DNA methylation with gene and nucleotide resolution from brain tissues. Curr Protoc Neurosci. 2012;Chapter 7:Unit 7 24.
23. Jiang M, Zhang Y, Fei J, et al. Rapid quantification of DNA methylation by measuring relative peak heights in direct bisulfite-PCR sequencing traces. Lab Invest 2010;90:282-290.
24. Assini FL, Duzzioni M, Takahashi RN. Object location memory in mice: pharmacological validation and further evidence of hippocampal CA1 participation. Behav Brain Res 2009;204:206-211.
25. Ennaceur A, Neave N, Aggleton JP. Spontaneous object recognition and object location memory in rats: the effects of lesions in the cingulate cortices, the medial prefrontal cortex, the cingulum bundle and the fornix. Exp Brain Res 1997;113:509-519.
26. Kim JJ, Rison RA, Fanselow MS. Effects of amygdala, hippocampus, and periaqueductal gray lesions on shortand long-term contextual fear. Behav Neurosci 1993;107:1093-1098.
27. Phillips RG, LeDoux JE. Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav Neurosci 1992;106:274-285.
28. Binder DK, Scharfman HE. Brain-derived neurotrophic factor. Growth Factors 2004;22:123-131.
29. Alonso M, Vianna MR, Izquierdo I, Medina JH. Signaling mechanisms mediating BDNF modulation of memory formation in vivo in the hippocampus. Cell Mol Neurobiol 2002;22:663-674.
30. Shao LR, Dudek FE. Increased excitatory synaptic activity and local connectivity of hippocampal CA1 pyramidal cells in rats with kainate-induced epilepsy. J Neurophysiol 2004;92:1366-1373.
31. Smith BN, Dudek FE. Short- and long-term changes in CA1 network excitability after kainate treatment in rats. J Neurophysiol 2001;85:1-9.
32. Sakata K, Martinowich K, Woo NH, et al. Role of activitydependent BDNF expression in hippocampal-prefrontal cortical regulation of behavioral perseverance. Proc Natl Acad Sci USA 2013;110:15103-15108.
33. Martinowich K, Schloesser RJ, Jimenez DV, et al. Activitydependent brain-derived neurotrophic factor expression regulates cortistatin-interneurons and sleep behavior. Mol Brain 2011;4:11.
34. Fan G, Feng C, Wu F, et al. Methionine choline reverses lead-induced cognitive and N-methyl-d-aspartate receptor subunit 1 deficits. Toxicology 2010;272:23-31.
35. LaPlant Q, Vialou V, Covington HE III, et al. Dnmt3a regulates emotional behavior and spine plasticity in the nucleus accumbens. Nat Neurosci 2010;13:1137-1143.
36. Tian W, Zhao M, Li M, et al. Reversal of cocaineconditioned place preference through methyl supplementation in mice: altering global DNA methylation in the prefrontal cortex. PLoS One 2012;7:e33435.
37. Weaver IC, Champagne FA, Brown SE, et al. Reversal of maternal programming of stress responses in adult offspring through methyl supplementation: altering epigenetic marking later in life. J Neurosci 2005;25:11045-11054.
38. Weaver IC, Meaney MJ, Szyf M. Maternal care effects on the hippocampal transcriptome and anxiety-mediated behaviors in the offspring that are reversible in adulthood. Proc Natl Acad Sci USA 2006;103:3480-3485.
39. Khan OI, Zhao Q, Miller F, Holmes GL. Interictal spikes in developing rats cause long-standing cognitive deficits. Neurobiol Dis 2010;39:362-371.
40. Kleen JK, Scott RC, Holmes GL, Lenck-Santini PP. Hippocampal interictal spikes disrupt cognition in rats. Ann Neurol 2010;67:250-257.
41. Chauviere L, Rafrafi N, Thinus-Blanc C, et al. Early deficits in spatial memory and theta rhythm in experimental temporal lobe epilepsy. J Neurosci 2009;29:5402-5410.
42. Ge M, Wang D, Dong G, et al. Transient impact of spike on theta rhythm in temporal lobe epilepsy. Exp Neurol 2013;250:136-142.
43. Matsumoto JY, Stead M, Kucewicz MT, et al. Network oscillations modulate interictal epileptiform spike rate during human memory. Brain 2013;136(Pt 8):2444-2456.
44. Duzel E, Penny WD, Burgess N. Brain oscillations and memory. Curr Opin Neurobiol 2010;20:143-149.
45. Saletu B, Anderer P, Di Padova C, et al. Electrophysiological neuroimaging of the central effects of S-adenosyl-L-methionine by mapping of electroencephalograms and event-related potentials and low-resolution brain electromagnetic tomography. Am J Clin Nutr 2002;76:1162S-1171S.
46. Sales AJ, Biojone C, Terceti MS, et al. Antidepressant-like effect induced by systemic and intra-hippocampal administration of DNA methylation inhibitors. Br J Pharmacol 2011;164:1711-1721.
47. Tao X, Finkbeiner S, Arnold DB, et al. Ca2+ influx regulates BDNF transcription by a CREB family transcription factor-dependent mechanism. Neuron 1998;20:709-726.
48. Binder DK, Croll SD, Gall CM, Scharfman HE. BDNF and epilepsy: too much of a good thing? Trends Neurosci 2001;24:47-53.
49. Heinrich C, Lahteinen S, Suzuki F, et al. Increase in BDNF-mediated TrkB signaling promotes epileptogenesis in a mouse model of mesial temporal lobe epilepsy. Neurobiol Dis 2011;42:35-47.
50. Miller CA, Sweatt JD. Covalent modification of DNA regulates memory formation. Neuron 2007;53:857-869.
51. Papaleo F, Silverman JL, Aney J, et al. Working memory deficits, increased anxiety-like traits, and seizure susceptibility in BDNF overexpressing mice. Learn Mem 2011;18:534-544.
52. Zhang L, Benedek DM, Fullerton CS, et al. PTSD risk is associated with BDNF Val66Met and BDNF overexpression. Mol Psychiatry 2014;19:8-10.
53. Cao XJ, Huang SH, Wang M, et al. S-adenosyl-Lmethionine improves impaired hippocampal long-term potentiation and water maze performance induced by developmental lead exposure in rats. Eur J Pharmacol 2008;595:30-34.
54. Perry S, Levasseur J, Chan A, Shea TB. Dietary supplementation with S-adenosyl methionine was associated with protracted reduction of seizures in a line of transgenic mice. Comp Med 2008;58:604-606.
55. Tremolizzo L, Carboni G, Ruzicka WB, et al. An epigenetic mouse model for molecular and behavioral neuropathologies related to schizophrenia vulnerability. Proc Natl Acad Sci USA 2002;99:17095-17100.
56. Zhu Q, Wang L, Zhang Y, et al. Increased expression of DNA methyltransferase 1 and 3a in human temporal lobe epilepsy. J Mol Neurosci 2012;46:420-426.
57. Cao XJ, Wang M, Chen JT, Ruan DY. Protection effects of S-adenosyl-L-methionine on lead-exposed rats during development and its mechanism of long-term potentiation. Zhonghua Yu Fang Yi Xue Za Zhi 2008;42:151-155.
58. Holmes GL, Lenck-Santini PP. Role of interictal epileptiform abnormalities in cognitive impairment. Epilepsy Behav 2006;8:504-515.
59. Buzsaki G. Theta rhythm of navigation: link between path integration and landmark navigation, episodic and semantic memory. Hippocampus 2005;15:827-840.
60. Hyman JM, Wyble BP, Goyal V, et al. Stimulation in hippocampal region CA1 in behaving rats yields long-term potentiation when delivered to the peak of theta and longterm depression when delivered to the trough. J Neurosci 2003;23:11725-11731.
61. Richard GR, Titiz A, Tyler A, et al. Speed modulation of hippocampal theta frequency correlates with spatial memory performance. Hippocampus 2013;23:1269-1279.
62. Klimesch W, Sauseng P, Hanslmayr S. EEG alpha oscillations: the inhibition-timing hypothesis. Brain Res Rev 2007;53:63-88.
63. Lahteinen S, Pitkanen A, Saarelainen T, et al. Decreased BDNF signalling in transgenic mice reduces epileptogenesis. Eur J Neurosci 2002;15:721-734.
64. Liu X, Liu J, Liu J, et al. BDNF-TrkB signaling pathway is involved in pentylenetetrazole-evoked progression of epileptiform activity in hippocampal neurons in anesthetized rats. Neurosci Bull 2013;29:565-575.
65. McNamara JO, Scharfman HE. Temporal lobe epilepsy and the BDNF receptor, Trk. In: Noebels JL, Avoli M, Rogawski MA, Olsen RW, Delgado-Escueta AV, eds. Jasper’s basic mechanisms of the epilepsies. 4th ed. Bethesda, MD: Oxford University Press, 2012; pp. 514-531.
66. Mudd SH, Brosnan JT, Brosnan ME, et al. Methyl balance and transmethylation fluxes in humans. Am J Clin Nutr 2007;85:19-25.
67. Takeuchi Y, Miyamoto E, Fukunaga K. Analysis on the promoter region of exon IV brain-derived neurotrophic factor in NG108-15 cells. J Neurochem 2002;83:67-79.
68. Stefanello FM, Matte C, Scherer EB, et al. Chemically induced model of hypermethioninemia in rats. J Neurosci Methods 2007;160:1-4.
69. Vuaden FC, Savio LE, Piato AL, et al. Long-term methionine exposure induces memory impairment on inhibitory avoidance task and alters acetylcholinesterase activity and expression in zebrafish (Danio rerio). Neurochem Res 2012;37:1545-1553.