Epigenetic regulation of Arc and c-Fos in the hippocampus after acute electroconvulsive stimulation in the rat

Brain Research Bulletin

Volumn 88, Issue 5, 2012, Pages 507-513

  Dyrvig, Mads ^a   Hansen, Henrik H ^b   Christiansen, Søren H ^c   Woldbye, David P D ^c   Mikkelsen, Jens D ^a,b,d   Lichota, Jacek ^a  

^a AALBORG UNIVERSITY   (Denmark)

^b NEUROSEARCH A S   (Denmark)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d Rigshospitalet   (Denmark)

Author keywords

Depression; DNA methylation; Electroconvulsive seizure; Histone acetylation

Indexed keywords

ARC PROTEIN; DNA; HISTONE H4; PROTEIN; PROTEIN C FOS; UNCLASSIFIED DRUG;

AMNESIA; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; DNA METHYLATION; DNA MODIFICATION; ELECTROCONVULSIVE THERAPY; GENE ACTIVATION; GENE EXPRESSION REGULATION; GENE SILENCING; GENETIC MARKER; HISTONE ACETYLATION; LONG TERM POTENTIATION; MALE; MEMORY CONSOLIDATION; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FUNCTION; RAT; REACTION TIME;

ANIMALS; CYTOSKELETAL PROTEINS; DNA METHYLATION; ELECTROSHOCK; EPIGENESIS, GENETIC; HIPPOCAMPUS; MALE; NERVE TISSUE PROTEINS; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, SPRAGUE-DAWLEY; TIME FACTORS;

EID: 84862560054     PISSN: 03619230     EISSN: 18732747     Source Type: Journal    
DOI: 10.1016/j.brainresbull.2012.05.004     Document Type: Article

References (54)

1. Abraham W.C., Christie B.R., Logan B., Lawlor P., Dragunow M. Immediate early gene expression associated with the persistence of heterosynaptic long-term depression in the hippocampus. Proceedings of the National Academy of Sciences of the United States of America 1994, 91:10049-10053.
2. Amir R.E., Van den Veyver I.B., Wan M., Tran C.Q., Francke U., Zoghbi H.Y. Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2. Nature Genetics 1999, 23:185-188.
3. Andrade C., Shaikh S.A., Narayan L., Blasey C., Belanoff J. Administration of a selective glucocorticoid antagonist attenuates electroconvulsive shock-induced retrograde amnesia. Journal of Neural Transmission 2011.
4. Arzenani M.K., Zade A.E., Ming Y., Vijverberg S.J.H., Zhang Z., Khan Z., et al. Genomic DNA hypomethylation by histone deacetylase inhibition implicates DNMT1 nuclear dynamics. Molecular and Cellular Biology 2011, 31:4119-4128.
5. +/calmodulin-dependent protein kinase II mRNA association to polysomes. Journal of Neuroscience 2000, 20:RC76.
6. Berton O., Nestler E.J. New approaches to antidepressant drug discovery: beyond monoamines. Nature Reviews Neuroscience 2006, 7:137-151.
7. Bramham C.R., Alme M.N., Bittins M., Kuipers S.D., Nair R.R., Pai B., et al. The Arc of synaptic memory. Experimental Brain Research 2009, 200:125-140.
8. Brooks P.J., Marietta C., Goldman D. DNA mismatch repair and DNA methylation in adult brain neurons. Journal of Neuroscience 1996, 16:939-945.
9. Chowdhury S., Shepherd J.D., Okuno H., Lyford G., Petralia R.S., Plath N., et al. Arc/Arg3.1 interacts with the endocytic machinery to regulate AMPA receptor trafficking. Neuron 2006, 52:445-459.
10. Donai H., Sugiura H., Ara D., Yoshimura Y., Yamagata K., Yamauchi T. Interaction of Arc with CaM kinase II and stimulation of neurite extension by Arc in neuroblastoma cells expressing CaM kinase II. Neuroscience Research 2003, 47:399-408.
11. Dulac C. Brain function and chromatin plasticity. Nature 2010, 465:728-735.
12. Endres M., Fan G., Meisel A., Dirnagl U., Jaenisch R. Effects of cerebral ischemia in mice lacking DNA methyltransferase 1 in post-mitotic neurons. Neuroreport 2001, 12:3763-3766.
13. 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.
14. Fan G., Beard C., Chen R.Z., Csankovszki G., Sun Y., Siniaia M., et al. DNA hypomethylation perturbs the function and survival of CNS neurons in postnatal animals. Journal of Neuroscience 2001, 21:788-797.
15. Fava M., Kendler K.S. Major depressive disorder. Neuron 2000, 28:335-341.
16. Feng J., Zhou Y., Campbell S.L., Le T., Li E., Sweatt J.D., et al. Dnmt1 and Dnmt3a maintain DNA methylation and regulate synaptic function in adult forebrain neurons. Nature Publishing Group 2010, 13:423-430.
17. Fleischmann A., Hvalby O., Jensen V., Strekalova T., Zacher C., Layer L.E., et al. Impaired long-term memory and NR2A-type NMDA receptor-dependent synaptic plasticity in mice lacking c-Fos in the CNS. Journal of Neuroscience 2003, 23:9116-9122.
18. Fujimoto T., Tanaka H., Kumamaru E., Okamura K., Miki N. Arc interacts with microtubules/microtubule-associated protein 2 and attenuates microtubule-associated protein 2 immunoreactivity in the dendrites. Journal of Neuroscience Research 2004, 76:51-63.
19. Greer P.L., Hanayama R., Bloodgood B.L., Mardinly A.R., Lipton D.M., Flavell S.W., et al. The Angelman Syndrome protein Ube3A regulates synapse development by ubiquitinating Arc. Cell 2010, 140:704-716.
20. Guo J.U., Ma D.K., Mo H., Ball M.P., Jang M-H., Bonaguidi M.A., et al. Neuronal activity modifies the DNA methylation landscape in the adult brain. Nature Publishing Group 2011, 14:1345-1351.
21. Guzowski J.F., Lyford G.L., Stevenson G.D., Houston F.P., McGaugh J.L., Worley P.F., et al. Inhibition of activity-dependent Arc protein expression in the rat hippocampus impairs the maintenance of long-term potentiation and the consolidation of long-term memory. Journal of Neuroscience 2000, 20:3993-4001.
22. Guzowski J.F., McNaughton B.L., Barnes C.A., Worley P.F. Environment-specific expression of the immediate-early gene Arc in hippocampal neuronal ensembles. Nature Neuroscience 1999, 2:1120-1124.
23. Jenuwein T., Allis C.D. Translating the histone code. Science 2001, 293:1074-1080.
24. Kaczmarek L. Expression of c-Fos and other genes encoding transcription factors in long-term potentiation. Behavioral and Neural Biology 1992, 57:263-266.
25. Larsen M.H., Olesen M., Woldbye D.P.D., Hay-Schmidt A., Hansen H.H., Rønn L.C.B., et al. Regulation of activity-regulated cytoskeleton protein (Arc) mRNA after acute and chronic electroconvulsive stimulation in the rat. Brain Research 2005, 1064:161-165.
26. 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.
27. 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.
28. Link W., Konietzko U., Kauselmann G., Krug M., Schwanke B., Frey U., et al. Somatodendritic expression of an immediate early gene is regulated by synaptic activity. Proceedings of the National Academy of Sciences of the United States of America 1995, 92:5734-5738.
29. Luo J., Min S., Wei K., Li P., Dong J., Liu Y-F. Propofol protects against impairment of learning-memory and imbalance of hippocampal Glu/GABA induced by electroconvulsive shock in depressed rats. Journal of Anaesthesia 2011, 25:657-665.
30. Lyford G.L., Yamagata K., Kaufmann W.E., Barnes C.A., Sanders L.K., Copeland N.G., et al. Arc, a growth factor and activity-regulated gene, encodes a novel cytoskeleton-associated protein that is enriched in neuronal dendrites. Neuron 1995, 14:433-445.
31. Madsen T.M., Woldbye D.P., Bolwig T.G., Mikkelsen J.D. Kainic acid seizure suppression by neuropeptide Y is not correlated to immediate early gene mRNA levels in rats. Neuroscience Letters 1999, 271:21-24.
32. Martinowich K., Hattori D., Wu H., Fouse S., He F., Hu Y., et al. DNA methylation-related chromatin remodeling in activity-dependent BDNF gene regulation. Science 2003, 302:890-893.
33. Miller C.A., Sweatt J.D. Covalent modification of DNA regulates memory formation. Neuron 2007, 53:857-869.
34. Pei Q., Tordera R., Sprakes M., Sharp T. Glutamate receptor activation is involved in 5-HT2 agonist-induced Arc gene expression in the rat cortex. Neuropharmacology 2004, 46:331-339.
35. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research 2001, 29:e45.
36. Plath N., Ohana O., Dammermann B., Errington M.L., Schmitz D., Gross C., et al. Arc/Arg3.1 is essential for the consolidation of synaptic plasticity and memories. Neuron 2006, 52:437-444.
37. Ramirez-Amaya V. Spatial exploration-induced Arc mRNA and protein expression: evidence for selective, network-specific reactivation. Journal of Neuroscience 2005, 25:1761-1768.
38. Renthal W., Maze I., Krishnan V., Covington HE -III, Xiao G., Kumar A. Histone deacetylase 5 epigenetically controls behavioral adaptations to chronic emotional stimuli. Neuron 2007, 56:517-529.
39. Rial Verde E.M., Lee-Osbourne J., Worley P.F., Malinow R., Cline H.T. Increased expression of the immediate-early gene Arc/Arg3.1 reduces AMPA receptor-mediated synaptic transmission. Neuron 2006, 52:461-474.
40. Rodríguez J.J., Davies H.A., Silva A.T., De Souza I.E.J., Peddie C.J., Colyer F.M., et al. Long-term potentiation in the rat dentate gyrus is associated with enhanced Arc/Arg3.1 protein expression in spines, dendrites and glia. European Journal of Neuroscience 2005, 21:2384-2396.
41. Semkovska M., McLoughlin D.M. Objective cognitive performance associated with electroconvulsive therapy for depression: a systematic review and meta-analysis. Biological Psychiatry 2010, 68:568-577.
42. Steward O., Worley P.F. Selective targeting of newly synthesized Arc mRNA to active synapses requires NMDA receptor activation. Neuron 2001, 30:227-240.
43. Sutcliffe J.S., Nelson D.L., Zhang F., Pieretti M., Caskey C.T., Saxe D., et al. DNA methylation represses FMR-1 transcription in fragile X syndrome. Human Molecular Genetics 1992, 1:397-400.
44. Thomsen M.S., Mikkelsen J.D., Timmermann D.B., Peters D., Hay-Schmidt A., Martens H., et al. The selective alpha7 nicotinic acetylcholine receptor agonist A-582941 activates immediate early genes in limbic regions of the forebrain: differential effects in the juvenile and adult rat. Neuroscience 2008, 154:741-753.
45. Tsankova N.M., Kumar A., Nestler E.J. Histone modifications at gene promoter regions in rat hippocampus after acute and chronic electroconvulsive seizures. Journal of Neuroscience 2004, 24:5603-5610.
46. Tzingounis A.V., Nicoll R.A. Arc/Arg3.1: linking gene expression to synaptic plasticity and memory. Neuron 2006, 52:403-407.
47. Vazdarjanova A., Ramirez-Amaya V., Insel N., Plummer T.K., Rosi S., Chowdhury S., et al. Spatial exploration induces Arc, a plasticity-related immediate-early gene, only in calcium/calmodulin-dependent protein kinase II-positive principal excitatory and inhibitory neurons of the rat forebrain. Journal of Comparative Neurology 2006, 498:317-329.
48. Veldic M., Caruncho H.J., Liu W.S., Davis J., Satta R., Grayson D.R., et al. DNA-methyltransferase 1 mRNA is selectively overexpressed in telencephalic GABAergic interneurons of schizophrenia brains. Proceedings of the National Academy of Sciences of the United States of America 2004, 101:348-353.
49. Wallace C.S., Lyford G.L., Worley P.F., Steward O. Differential intracellular sorting of immediate early gene mRNAs depends on signals in the mRNA sequence. Journal of Neuroscience 1998, 18:26-35.
50. + and cAMP requires protein kinase A and mitogen-activated protein kinase/extracellular regulated kinase activation. Journal of Neuroscience 2001, 21:5484-5493.
51. Woldbye D.P., Greisen M.H., Bolwig T.G., Larsen P.J., Mikkelsen J.D. Prolonged induction of c-Fos in neuropeptide Y- and somatostatin-immunoreactive neurons of the rat dentate gyrus after electroconvulsive stimulation. Brain Research 1996, 720:111-119.
52. Woldbye D.P., Larsen P.J., Mikkelsen J.D., Klemp K., Madsen T.M., Bolwig T.G. Powerful inhibition of kainic acid seizures by neuropeptide Y via Y5-like receptors. Nature Medicine 1997, 3:761-764.
53. Yao Z., Guo Z., Yang C., Tian Q., Gong C.X., Liu G., et al. Phenylbutyric acid prevents rats from electroconvulsion-induced memory deficit with alterations of memory-related proteins and tau hyperphosphorylation. Neuroscience 2010, 168:405-415.
54. Yasuda M., Fukuchi M., Tabuchi A., Kawahara M., Tsuneki H., Azuma Y., et al. Robust stimulation of TrkB induces delayed increases in BDNF and Arc mRNA expressions in cultured rat cortical neurons via distinct mechanisms. Journal of Neurochemistry 2007, 103:626-636.