Epigenetic regulation of reelin and brain-derived neurotrophic factor genes in long-term potentiation in rat medial prefrontal cortex

Neurobiology of Learning and Memory

Volumn 97, Issue 4, 2012, Pages 425-440

  Sui, Li ^a   Wang, Yan ^a   Ju, Li Hua ^a   Chen, Meng ^b  

^a UNIVERSITY OF SHANGHAI FOR SCIENCE AND TECHNOLOGY   (China)

^b FUDAN UNIVERSITY   (China)

Author keywords

DNA methylation demethylation; Epigenetics; Histone acetylation; Medial prefrontal cortex (mPFC); Synaptic plasticity; Trace fear memory

Indexed keywords

AZACITIDINE; BRAIN DERIVED NEUROTROPHIC FACTOR; BUTYRIC ACID; DNA METHYLTRANSFERASE; HISTONE ACETYLTRANSFERASE; HISTONE H3; HISTONE H4; MESSENGER RNA; REELIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DERIVED NEUROTROPHIC FACTOR GENE; CONDITIONING; CONTROLLED STUDY; DEMETHYLATION; DNA METHYLATION; EPIGENETICS; FEAR; GENE; GENE EXPRESSION; HISTONE ACETYLATION; LONG TERM POTENTIATION; MALE; MEDIAL PREFRONTAL CORTEX; MEMORY CONSOLIDATION; NERVE CELL PLASTICITY; NONHUMAN; PREFRONTAL CORTEX; PROMOTER REGION; PROTEIN EXPRESSION; RAT; REELIN GENE; TRACE FEAR;

ACETYLATION; ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELL ADHESION MOLECULES, NEURONAL; DNA METHYLATION; DNA MODIFICATION METHYLASES; EPIGENESIS, GENETIC; EXTRACELLULAR MATRIX PROTEINS; FEAR; HISTONE ACETYLTRANSFERASES; HISTONES; LONG-TERM POTENTIATION; MALE; MEMORY; NERVE TISSUE PROTEINS; NEURONAL PLASTICITY; PREFRONTAL CORTEX; RATS; RATS, SPRAGUE-DAWLEY; SERINE ENDOPEPTIDASES;

EID: 84861189663     PISSN: 10747427     EISSN: 10959564     Source Type: Journal    
DOI: 10.1016/j.nlm.2012.03.007     Document Type: Article

References (77)

1. Alarcón J.M., Malleret G., Touzani K., Vronskaya S., Ishii S., Kandel E.R., et al. Chromatin acetylation, memory, and LTP are impaired in CBP+/- mice: A model for the cognitive deficit in Rubinstein-Taybi syndrome and its amelioration. Neuron 2004, 42:947-959.
2. Aoki E., Ohashi H., Uchida T., Murate T., Saito H., Kinoshita T. Expression levels of DNA methyltransferase genes do not correlate with p15INK4B gene methylation in myelodysplastic syndromes. Leukemia 2003, 17:1903-1904.
3. Ben-Porath I., Cedar H. Epigenetic crosstalk. Molecular Cell 2001, 8:933-935.
4. Bestor T.H. The DNA methyltransferases of mammals. Human Molecular Genetics 2000, 9:2395-2402. [Review].
5. Bird A. DNA methylation patterns and epigenetic memory. Genes & Development 2002, 16:6-21. [Review].
6. Bird A. Perceptions of epigenetics. Nature 2007, 477:396-398. [Review].
7. Branchi I., Karpova N.N., D'andrea I., Castrén E., Alleva E. Epigenetic modifications induced by early enrichment are associated with changes in timing of induction of BDNF expression. Neuroscience Letter 2011, 495:168-172.
8. Bredy T.W., Wu H., Crego C., Zellhoefer J., Sun Y.E., Barad M. Histone modifications around individual BDNF gene promoters in prefrontal cortex are associated with extinction of conditioned fear. Learning & Memory 2007, 14:268-276.
9. Brown S.E., Weaver I.C., Meaney M.J., Szyf M. Regional-specific global cytosine methylation and DNA methyltransferase expression in the adult rat hippocampus. Neuroscience Letter 2008, 440:49-53.
10. Brownell J.E., Allis C.D. Special HATs for special occasions: Linking histone acetylation to chromatin assembly and gene activation. Current Opinion in Genetics & Development 1996, 6:176-184. [Review].
11. Chahrour M., Jung S.Y., Shaw C., Zhou X., Wong S.T., Qin J., et al. MeCP2, a key contributor to neurological disease, activates and represses transcription. Science 2008, 320:1224-1229.
12. Chakrabarti S.K., James J.C., Mirmira R.G. Quantitative assessment of gene targeting in vitro and in vivo by the pancreatic transcription factor, Pdx1. Importance of chromatin structure in directing promoter binding. Journal of Biological Chemistry 2002, 277:13286-13293.
13. Chen P.S., Wang C.C., Bortner C.D., Peng G.S., Wu X., Pang H., et al. Valproic acid and other histone deacetylase inhibitors induce microglial apoptosis and attenuate lipopolysaccharide-induced dopaminergic neurotoxicity. Neuroscience 2007, 149:203-212.
14. Chwang W.B., O'riordan K.J., Levenson J.M., Sweatt J.D. ERK/MAPK regulates hippocampal histone phosphorylation following contextual fear conditioning. Learning & Memory 2006, 13:322-328.
15. Dokmanovic M., Marks P.A. Prospects: Histone deacetylase inhibitors. Journal of Cellular Biochemistry 2005, 96:293-304. [Review].
16. Eden S., Hashimshony T., Keshet I., Cedar H., Thorne A.W. DNA methylation models histone acetylation. Nature 1998, 394:842.
17. Endres M., Meisel A., Biniszkiewicz D., Namura S., Prass K., Ruscher K., et al. DNA methyltransferase contributes to delayed ischemic brain injury. Journal of Neuroscience 2000, 20:3175-3181.
18. Fan G., Hutnick L. Methyl-CpG binding proteins in the nervous system. Cell Research 2005, 15:255-261. [Review].
19. Feng J., Fouse S., Fan G. Epigenetic regulation of neural gene expression and neuronal function. Pediatric Research 2007, 61:58R-63R. [Review].
20. Gemmell C., O'mara S.M. Long-term potentiation and paired-pulse facilitation in the prelimbic cortex of the rat following stimulation in the contralateral hemisphere in vivo. Experimental Brain Research 2000, 132:223-229.
21. Goldman-Rakic P.S. Architecture of the prefrontal cortex and the central executive. Annals of the New York Academy of Sciences 1995, 769:71-83. [Review].
22. Guan Z., Giustetto M., Lomvardas S., Kim J.H., Miniaci M.C., Schwartz J.H., et al. Integration of long-term-memory-related synaptic plasticity involves bidirectional regulation of gene expression and chromatin structure. Cell 2002, 111:483-493.
23. Gupta S., Kim S.Y., Artis S., Molfese D.L., Schumacher A., Sweatt J.D., et al. Histone methylation regulates memory formation. Journal of Neuroscience 2010, 30:3589-3599.
24. Herz J., Chen Y. Reelin, lipoprotein receptors and synaptic plasticity. Nature Reviews of Neuroscience 2006, 7:850-859. [Review].
25. Hsieh J., Gage F.H. Chromatin remodeling in neural development and plasticity. Current Opinion in Cell Biology 2005, 17:664-671. [Review].
26. Kawamoto K., Okino S.T., Place R.F., Urakami S., Hirata H., Kikuno N., et al. Epigenetic modifications of RASSF1A gene through chromatin remodeling in prostate cancer. Clinical Cancer Research 2007, 13:2541-2548.
27. Kelly W.K., Marks P.A. Drug insight: Histone deacetylase inhibitors - Development of the new targeted anticancer agent suberoylanilide hydroxamic acid. Nature Clinical Practice Oncology 2005, 2:150-157. [Review].
28. Klose R.J., Bird A.P. Genomic DNA methylation: The mark and its mediators. Trends in Biochemical Sciences 2006, 31:89-97. [Review].
29. Korzus E., Rosenfeld M.G., Mayford M. CBP histone acetyltransferase activity is a critical component of memory consolidation. Neuron 2004, 42:961-972.
30. Koshibu K., Gräff J., Mansuy I.M. Nuclear protein phosphatase-1: An epigenetic regulator of fear memory and amygdala long-term potentiation. Neuroscience 2011, 173:30-36.
31. Lattal K.M., Barrett R.M., Wood M.A. Systemic or intrahippocampal delivery of histone deacetylase inhibitors facilitates fear extinction. Behavioral Neuroscience 2007, 121:1125-1131.
32. Levenson J.M., O'riordan K.J., Brown K.D., Trinh M.A., Molfese D.L., Sweatt J.D. Regulation of histone acetylation during memory formation in the hippocampus. Journal of Biological Chemistry 2004, 279:40545-40559.
33. Levenson J.M., Qiu S., Weeber E.J. The role of reelin in adult synaptic function and the genetic and epigenetic regulation of the reelin gene. BBA - Biochimica et Biophysica Acta 2008, 1779:422-431. [Review].
34. Levenson J.M., Roth T.L., Lubin F.D., Miller C.A., Huang I.C., Desai P., et al. Evidence that DNA (cytosine-5) methyltransferase regulates synaptic plasticity in the hippocampus. Journal of Biological Chemistry 2006, 281:15763-15773.
35. Levenson J.M., Sweatt J.D. Epigenetic mechanisms in memory formation. Nature Reviews in Neuroscience 2005, 6:108-118. [Review].
36. Levenson J.M., Sweatt J.D. Epigenetic mechanisms: A common theme in vertebrate and invertebrate memory formation. CMLS - Cellular and Molecular, Life Sciences 2006, 63:1009-1016. [Review].
37. Li L.C., Dahiya R. MethPrimer: Designing primers for methylation PCRs. Bioinformatics 2002, 18:1427-1431.
38. Lu B. Pro-region of neurotrophins: Role in synaptic modulation. Neuron 2003, 39:735-738. [Review].
39. Lu B., Figurov A. Role of neurotrophins in synapse development and plasticity. Reviews in the Neurosciences 1997, 8:1-12. [Review].
40. Lubin F.D., Gupta S., Parrish R.R., Grissom N.M., Davis R.L. Epigenetic mechanisms: Critical contributors to long-term memory formation. Neuroscientist 2011, 17:616-632.
41. Lubin F.D., Roth T.L., Sweatt J.D. Epigenetic regulation of BDNF gene transcription in the consolidation of fear memory. Journal of Neuroscience 2008, 28:10576-10586.
42. Maddox S.A., Schafe G.E. Epigenetic alterations in the lateral amygdala are required for reconsolidation of a Pavlovian fear memory. Learning & Memory 2011, 18:579-593.
43. Marutha Ravindran C.R., Ticku M.K. Effect of 5-azacytidine on the methylation aspects of NMDA receptor NR2B gene in the cultured cortical neurons of mice. Neurochemical Research 2009, 34:342-350.
44. Métivier R., Gallais R., Tiffoche C., Le Péron C., Jurkowska R.Z., Carmouche R.P., et al. Cyclical DNA methylation of a transcriptionally active promoter. Nature 2008, 452:45-50.
45. Mikaelsson M.A., Miller C.A. DNA methylation: A transcriptional mechanism co-opted by the developed mammalian brain?. Epigenetics 2011, 6:548-551.
46. Miller C.A., Campbell S.L., Sweatt J.D. DNA methylation and histone acetylation work in concert to regulate memory formation and synaptic plasticity. Neurobiology of Learning and Memory 2008, 89:599-603.
47. Miller C.A., Gavin C.F., White J.A., Parrish R.R., Honasoge A., Yancey C.R., et al. Cortical DNA methylation maintains remote memory. Nature Neuroscience 2010, 13:664-666.
48. Miller C.A., Sweatt J.D. Covalent modification of DNA regulates memory formation. Neuron 2007, 53:857-869.
49. Milutinovic S., D'alessio A.C., Detich N., Szyf M. Valproate induces widespread epigenetic reprogramming which involves demethylation of specific genes. Carcinogenesis 2007, 28:560-571.
50. Monsey M.S., Ota K.T., Akingbade I.F., Hong E.S., Schafe G.E. Epigenetic alterations are critical for fear memory consolidation and synaptic plasticity in the lateral amygdala. PLoS One 2011, 6:e19958.
51. Nabel C.S., Kohli R.M. Demystifying DNA demethylation. Science 2011, 333:1229-1230.
52. Nelson E.D., Kavalali E.T., Monteggia L.M. Activity-dependent suppression of miniature neurotransmission through the regulation of DNA methylation. Journal of Neuroscience 2008, 28:395-406.
53. Ono T., Uehara Y., Kurishita A., Tawa R., Sakurai H. Biological significance of DNA methylation in the ageing process. Age and Ageing 1993, 22:S34-S43.
54. Ou J.N., Torrisani J., Unterberger A., Provençal N., Shikimi K., Karimi M., et al. Histone deacetylase inhibitor Trichostatin A induces global and gene-specific DNA demethylation in human cancer cell lines. Biochemical Pharmacology 2007, 73:1297-1307.
55. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 1986, Academic Press, New York. 2nd ed.
56. Rampon C., Tang Y.P., Goodhouse J., Shimizu E., Kyin M., Tsien J.Z. Enrichment induces structural changes and recovery from nonspatial memory deficits in CA1 NMDAR1-knockout mice. Nature Neuroscience 2000, 3:238-244.
57. Robertson K.D., Jones P.A. DNA methylation: Past, present and future directions. Carcinogenesis 2000, 21:461-467. [Review].
58. Robertson K.D., Wolffe A.P. DNA methylation in health and disease. Nature Reviews Genetics 2000, 1:11-19. [Review].
59. Roder S., Danober L., Pozza M.F., Lingenhoehl K., Wiederhold K.H., Olpe H.R. Electrophysiological studies on the hippocampus and prefrontal cortex assessing the effects of amyloidosis in amyloid precursor protein 23 transgenic mice. Neuroscience 2003, 120:705-720.
60. Roth T.L., Zoladz P.R., Sweatt J.D., Diamond D.M. Epigenetic modification of hippocampal Bdnf DNA in adult rats in an animal model of post-traumatic stress disorder. Journal of Psychiatric Research 2011, 45:919-926.
61. Runyan J.D., Dash P.K. Intra-medial prefrontal administration of SCH-23390 attenuates ERK phosphorylation and long-term memory for trace fear conditioning in rats. Neurobiology of Learning and Memory 2004, 82:65-70.
62. Runyan J.D., Moore A.N., Dash P.K. A role for prefrontal cortex in memory storage for trace fear conditioning. Journal of Neuroscience 2004, 24:1288-1295.
63. Shilatifard A. Chromatin modifications by methylation and ubiquitination: Implications in the regulation of gene expression. Annual Review of Biochemistry 2006, 75:243-269. [Review].
64. Sui L., Li B.M. Effects of perinatal hypothyroidism on regulation of reelin and brain-derived neurotrophic factor gene expression in rat hippocampus: Role of DNA methylation and histone acetylation. Steroids 2010, 75:988-997.
65. Sui L., Ren W.W., Li B.M. Administration of thyroid hormone increases reelin and brain-derived neurotrophic factor expression in rat hippocampus in vivo. Brain Research 2010, 1313:9-24.
66. Sui L., Wang J., Li B.M. Administration of triiodo-l-thyronine into dorsal hippocampus alters phosphorylation of Akt, mammalian target of rapamycin, p70S6 kinase and 4E-BP1 in rats. Neurochemical Research 2008, 33:1065-1076.
67. Sui L., Wang J., Li B.M. Role of the phosphoinositide 3-kinase-Akt-mammalian target of the rapamycin signaling pathway in long-term potentiation and trace fear conditioning memory in rat medial prefrontal cortex. Learning & Memory 2008, 15:762-776.
68. Swank M.W., Sweatt J.D. Increased histone acetyltransferase and lysine acetyltransferase activity and biphasic activation of the ERK/RSK cascade in insular cortex during novel taste learning. Journal of Neuroscience 2001, 21:3383-3391.
69. Vaissière T., Sawan C., Herceg Z. Epigenetic interplay between histone modifications and DNA methylation in gene silencing. Mutation Research 2008, 659:40-48. [Review].
70. Varga-Weisz P.D., Becker P.B. Chromatin-remodeling factors: Machines that regulate?. Current Opinion in Cell Biology 1998, 10:346-353. [Review].
71. Vecsey C.G., Hawk J.D., Lattal K.M., Stein J.M., Fabian S.A., Attner M.A., et al. Histone deacetylase inhibitors enhance memory and synaptic plasticity via CREB:CBP-dependent transcriptional activation. Journal of Neuroscience 2007, 27:6128-6140.
72. Vidali G., Boffa L.C., Mann R.S., Allfrey V.G. Reversible effects of Na-butyrate on histone acetylation. Biochemical and Biophysical Research Communications 1978, 82:223-227.
73. Watt F., Molloy P.L. Cytosine methylation prevents binding to DNA of a HeLa cell transcription factor required for optimal expression of the adenovirus major late promoter. Genes & Development 1988, 2:1136-1143.
74. Wilson V.L., Smith R.A., Ma S., Cutler R.G. Genomic 5-methyldeoxycytidine decreases with age. Journal of Biological Chemistry 1987, 262:9948-9951.
75. Wu H., Sun Y.E. Epigenetic regulation of stem cell differentiation. Pediatric Research 2006, 59:21R-25R. [Review].
76. Yasuda S., Liang M.H., Marinova Z., Yahyavi A., Chuang D.M. The mood stabilizers lithium and valproate selectively activate the promoter IV of brain-derived neurotrophic factor in neurons. Molecular Psychiatry 2009, 14:51-59.
77. Yeh S.H., Lin C.H., Gean P.W. Acetylation of nuclear factor-kappaB in rat amygdala improves long-term but not short-term retention of fear memory. Molecular Pharmacology 2004, 65:1286-1292.