Tet1 oxidase regulates neuronal gene transcription, active DNA hydroxymethylation, object location memory, and threat recognition memory

Neuroepigenetics

Volumn 4, Issue , 2015, Pages 12-27

  Kumar, Dinesh ^a,d,e   Aggarwal, Milan ^a   Kaas, Garrett A ^a   Lewis, John ^a   Wang, Jing ^a   Ross, Daniel L ^b   Zhong, Chun ^c   Kennedy, Andrew ^a   Song, Hongjun ^c   Sweatt, J David ^a  

^a University of Alabama at Birmingham   (United States)

^b University of Alabama at Birmingham   (United States)

^c Institute for Cell Engineering   (United States)

^d MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^e BROAD INSTITUTE OF MIT AND HARVARD   (United States)

Author keywords

Active demethylation; Cytosine methylation; Epigenetic; Fear conditioning; HDAC; Homeostatic plasticity; Hydroxymethylcytosine; Learning; Memory; Neuroepigenetics; TET; Threat conditioning

Indexed keywords

5 HYDROXYMETHYLCYTOSINE; CYTOSINE; OXIDOREDUCTASE; TET 1 OXIDASE; TET 2 OXIDASE; TET 3 OXIDASE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN ELECTROPHYSIOLOGY; CENTRAL NERVOUS SYSTEM; CEREBELLUM; CONDITIONING; CONTROLLED STUDY; DEMETHYLATION; DNA METHYLATION; ELECTROPHYSIOLOGICAL PROCEDURES; EPIGENETICS; FEAR; GENE CONTROL; GENE DELETION; GENE EXPRESSION; GENETIC TRANSCRIPTION; HIPPOCAMPUS; MALE; MASS SPECTROMETRY; MEMORY; MEMORY CONSOLIDATION; NERVE CELL PLASTICITY; NERVE CONDUCTION; NONHUMAN; PRIORITY JOURNAL; RECOGNITION; STEREOTAXIC SURGERY; SYNAPTIC TRANSMISSION; THREAT; UPREGULATION;

EID: 84946737005     PISSN: None     EISSN: 22147845     Source Type: Journal    
DOI: 10.1016/j.nepig.2015.10.002     Document Type: Article

References (58)

1. Almonte A.G., Qadri L.H., Sultan F.A., Watson J.A., Mount D.J., Rumbaugh G., Sweatt J.D. Protease-activated receptor-1 modulates hippocampal memory formation and synaptic plasticity. J Neurochem 2013, 124:109-122.
2. Bahar Halpern K., Vana T., Walker M.D. Paradoxical role of DNA methylation in activation of FoxA2 gene expression during endoderm development. J Biol Chem 2014, 289:23882-23892.
3. Bartsch D., Casadio A., Karl K.A., Serodio P., Kandel E.R. CREB1 encodes a nuclear activator, a repressor, and a cytoplasmic modulator that form a regulatory unit critical for long-term facilitation. Cell 1998, 95:211-223.
4. Bloodgood B.L., Sharma N., Browne H.A., Trepman A.Z., Greenberg M.E. The activity-dependent transcription factor NPAS4 regulates domain-specific inhibition. Nature 2013, 503:121-125.
5. Bonasio R., Tu S., Reinberg D. Molecular signals of epigenetic states. Science 2010, 330:612-616.
6. Chwang W.B., Arthur J.S., Schumacher A., Sweatt J.D. The nuclear kinase mitogen- and stress-activated protein kinase 1 regulates hippocampal chromatin remodeling in memory formation. J Neurosci 2007, 27:12732-12742.
7. Dash P.K., Hochner B., Kandel E.R. Injection of the cAMP-responsive element into the nucleus of Aplysia sensory neurons blocks long-term facilitation. Nature 1990, 345:718-721.
8. Dawlaty M.M., Ganz K., Powell B.E., Hu Y.C., Markoulaki S., Cheng A.W., Gao Q., Kim J., Choi S.W., Page D.C., et al. Tet1 is dispensable for maintaining pluripotency and its loss is compatible with embryonic and postnatal development. Cell Stem Cell 2011, 9:166-175.
9. Dudai Y. The neurobiology of consolidations, or, how stable is the engram?. Annu Rev Psychol 2004, 55:51-86.
10. Ellegood J., Babineau B.A., Henkelman R.M., Lerch J.P., Crawley J.N. Neuroanatomical analysis of the BTBR mouse model of autism using magnetic resonance imaging and diffusion tensor imaging. Neuroimage 2013, 70:288-300.
11. Feng J., Zhou Y., Campbell S.L., Le T., Li E., Sweatt J.D., Silva A.J., Fan G. Dnmt1 and Dnmt3a maintain DNA methylation and regulate synaptic function in adult forebrain neurons. Nat Neurosci 2010, 13:423-430.
12. Feng S., Jacobsen S.E., Reik W. Epigenetic reprogramming in plant and animal development. Science 2010, 330:622-627.
13. Feng J., Shao N., Szulwach K.E., Vialou V., Huynh J., Zhong C., Le T., Ferguson D., Cahill M.E., Li Y., et al. Role of Tet1 and 5-hydroxymethylcytosine in cocaine action. Nat Neurosci 2015, 18:536-544.
14. Globisch D., Munzel M., Muller M., Michalakis S., Wagner M., Koch S., Bruckl T., Biel M., Carell T. Tissue distribution of 5-hydroxymethylcytosine and search for active demethylation intermediates. PLoS One 2010, 5:e15367.
15. Guan J.S., Su S.C., Gao J., Joseph N., Xie Z., Zhou Y., Durak O., Zhang L., Zhu J.J., Clauser K.R., et al. Cdk5 is required for memory function and hippocampal plasticity via the cAMP signaling pathway. PLoS One 2011, 6:e25735.
16. Guo J.U., Su Y., Zhong C., Ming G.L., Song H. Hydroxylation of 5-methylcytosine by TET1 promotes active DNA demethylation in the adult brain. Cell 2011, 145:423-434.
17. Haettig J., Stefanko D.P., Multani M.L., Figueroa D.X., McQuown S.C., Wood M.A. HDAC inhibition modulates hippocampus-dependent long-term memory for object location in a CBP-dependent manner. Learn Mem 2011, 18:71-79.
18. Hawk J.D., Bookout A.L., Poplawski S.G., Bridi M., Rao A.J., Sulewski M.E., Kroener B.T., Manglesdorf D.J., Abel T. NR4A nuclear receptors support memory enhancement by histone deacetylase inhibitors. J Clin Invest 2012, 122:3593-3602.
19. Huang Y., Chavez L., Chang X., Wang X., Pastor W.A., Kang J., Zepeda-Martinez J.A., Pape U.J., Jacobsen S.E., Peters B., et al. Distinct roles of the methylcytosine oxidases Tet1 and Tet2 in mouse embryonic stem cells. Proc Natl Acad Sci U S A 2014, 111:1361-1366.
20. Iurlaro M., Ficz G., Oxley D., Raiber E.A., Bachman M., Booth M.J., Andrews S., Balasubramanian S., Reik W. A screen for hydroxymethylcytosine and formylcytosine binding proteins suggests functions in transcription and chromatin regulation. Genome Biol 2013, 14:R119.
21. Iyer L.M., Tahiliani M., Rao A., Aravind L. Prediction of novel families of enzymes involved in oxidative and other complex modifications of bases in nucleic acids. Cell Cycle 2009, 8:1698-1710.
22. Jaenisch R., Bird A. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet 2003, 33 Suppl.:245-254.
23. Jeltsch A., Jurkowska R.Z. New concepts in DNA methylation. Trends Biochem Sci 2014, 39:310-318.
24. Kaas G.A., Zhong C., Eason D.E., Ross D.L., Vachhani R.V., Ming G.L., King J.R., Song H., Sweatt J.D. TET1 controls CNS 5-methylcytosine hydroxylation, active DNA demethylation, gene transcription, and memory formation. Neuron 2013, 79:1086-1093.
25. Khare T., Pai S., Koncevicius K., Pal M., Kriukiene E., Liutkeviciute Z., Irimia M., Jia P., Ptak C., Xia M., et al. 5-hmC in the brain is abundant in synaptic genes and shows differences at the exon-intron boundary. Nat Struct Mol Biol 2012, 19:1037-1043.
26. Kriaucionis S., Heintz N. The nuclear DNA base 5-hydroxymethylcytosine is present in Purkinje neurons and the brain. Science 2009, 324:929-930.
27. Ledoux J.E. Coming to terms with fear. Proc Natl Acad Sci U S A 2014, 111:2871-2878.
28. Lein E.S., Zhao X., Gage F.H. Defining a molecular atlas of the hippocampus using DNA microarrays and high-throughput in situ hybridization. J Neurosci 2004, 24:3879-3889.
29. Lesburgueres E., Gobbo O.L., Alaux-Cantin S., Hambucken A., Trifilieff P., Bontempi B. Early tagging of cortical networks is required for the formation of enduring associative memory. Science 2011, 331:924-928.
30. Leslie J.H., Nedivi E. Activity-regulated genes as mediators of neural circuit plasticity. Prog Neurobiol 2011, 94:223-237.
31. Li X., Wei W., Zhao Q.Y., Widagdo J., Baker-Andresen D., Flavell C.R., D'Alessio A., Zhang Y., Bredy T.W. Neocortical Tet3-mediated accumulation of 5-hydroxymethylcytosine promotes rapid behavioral adaptation. Proc Natl Acad Sci U S A 2014, 111:7120-7125.
32. Lin Y., Bloodgood B.L., Hauser J.L., Lapan A.D., Koon A.C., Kim T.K., Hu L.S., Malik A.N., Greenberg M.E. Activity-dependent regulation of inhibitory synapse development by Npas4. Nature 2008, 455:1198-1204.
33. Lister R., Mukamel E.A., Nery J.R., Urich M., Puddifoot C.A., Johnson N.D., Lucero J., Huang Y., Dwork A.J., Schultz M.D., et al. Global epigenomic reconfiguration during mammalian brain development. Science 2013, 341:1237905.
34. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25:402-408.
35. Lubin F.D., Roth T.L., Sweatt J.D. Epigenetic regulation of BDNF gene transcription in the consolidation of fear memory. J Neurosci 2008, 28:10576-10586.
36. Ma D.K., Jang M.H., Guo J.U., Kitabatake Y., Chang M.L., Pow-Anpongkul N., Flavell R.A., Lu B., Ming G.L., Song H. Neuronal activity-induced Gadd45b promotes epigenetic DNA demethylation and adult neurogenesis. Science 2009, 323:1074-1077.
37. Meadows J.P., Guzman-Karlsson M.C., Phillips S., Holleman C., Posey J.L., Day J.J., Hablitz J.J., Sweatt J.D. DNA methylation regulates neuronal glutamatergic synaptic scaling. Sci Signal 2015, 8:ra61.
38. Miller C.A., Sweatt J.D. Covalent modification of DNA regulates memory formation. Neuron 2007, 53:857-869.
39. Miller C.A., Gavin C.F., White J.A., Parrish R.R., Honasoge A., Yancey C.R., Rivera I.M., Rubio M.D., Rumbaugh G., Sweatt J.D. Cortical DNA methylation maintains remote memory. Nat Neurosci 2010, 13:664-666.
40. 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.
41. Munzel M., Globisch D., Bruckl T., Wagner M., Welzmiller V., Michalakis S., Muller M., Biel M., Carell T. Quantification of the sixth DNA base hydroxymethylcytosine in the brain. Angew Chem Int Ed Engl 2010, 49:5375-5377.
42. Penn N.W., Suwalski R., O'Riley C., Bojanowski K., Yura R. The presence of 5-hydroxymethylcytosine in animal deoxyribonucleic acid. Biochem J 1972, 126:781-790.
43. Penner M.R., Roth T.L., Chawla M.K., Hoang L.T., Roth E.D., Lubin F.D., Sweatt J.D., Worley P.F., Barnes C.A. Age-related changes in Arc transcription and DNA methylation within the hippocampus. Neurobiol Aging 2011, 32:2198-2210.
44. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001, 29:e45.
45. Rudenko A., Dawlaty M.M., Seo J., Cheng A.W., Meng J., Le T., Faull K.F., Jaenisch R., Tsai L.H. Tet1 is critical for neuronal activity-regulated gene expression and memory extinction. Neuron 2013, 79:1109-1122.
46. Silverman J.L., Yang M., Lord C., Crawley J.N. Behavioural phenotyping assays for mouse models of autism. Nat Rev Neurosci 2010, 11:490-502.
47. Spruijt C.G., Gnerlich F., Smits A.H., Pfaffeneder T., Jansen P.W., Bauer C., Munzel M., Wagner M., Muller M., Khan F., et al. Dynamic readers for 5-(hydroxy)methylcytosine and its oxidized derivatives. Cell 2013, 152:1146-1159.
48. Stefanko D.P., Barrett R.M., Ly A.R., Reolon G.K., Wood M.A. Modulation of long-term memory for object recognition via HDAC inhibition. Proc Natl Acad Sci U S A 2009, 106:9447-9452.
49. Sweatt J.D. The emerging field of neuroepigenetics. Neuron 2013, 80:624-632.
50. Tahiliani M., Koh K.P., Shen Y., Pastor W.A., Bandukwala H., Brudno Y., Agarwal S., Iyer L.M., Liu D.R., Aravind L., et al. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 2009, 324:930-935.
51. Varley K.E., Gertz J., Bowling K.M., Parker S.L., Reddy T.E., Pauli-Behn F., Cross M.K., Williams B.A., Stamatoyannopoulos J.A., Crawford G.E., et al. Dynamic DNA methylation across diverse human cell lines and tissues. Genome Res 2013, 23:555-567.
52. Vecsey C.G., Hawk J.D., Lattal K.M., Stein J.M., Fabian S.A., Attner M.A., Cabrera S.M., McDonough C.B., Brindle P.K., Abel T., et al. Histone deacetylase inhibitors enhance memory and synaptic plasticity via CREB:CBP-dependent transcriptional activation. J Neurosci 2007, 27:6128-6140.
53. West A.E., Greenberg M.E. Neuronal activity-regulated gene transcription in synapse development and cognitive function. Cold Spring Harb. Perspect. Biol. 2011, 3.
54. Wu H., Zhang Y. Reversing DNA methylation: mechanisms, genomics, and biological functions. Cell 2014, 156:45-68.
55. Xie W., Barr C.L., Kim A., Yue F., Lee A.Y., Eubanks J., Dempster E.L., Ren B. Base-resolution analyses of sequence and parent-of-origin dependent DNA methylation in the mouse genome. Cell 2012, 148:816-831.
56. Yu D.H., Ware C., Waterland R.A., Zhang J., Chen M.H., Gadkari M., Kunde-Ramamoorthy G., Nosavanh L.M., Shen L. Developmentally programmed 3' CpG island methylation confers tissue- and cell-type-specific transcriptional activation. Mol Cell Biol 2013, 33:1845-1858.
57. Yu H., Su Y., Shin J., Zhong C., Guo J.U., Weng Y.L., Gao F., Geschwind D.H., Coppola G., Ming G.L., et al. Tet3 regulates synaptic transmission and homeostatic plasticity via DNA oxidation and repair. Nat Neurosci 2015, 18:836-843.
58. Zhang R.R., Cui Q.Y., Murai K., Lim Y.C., Smith Z.D., Jin S., Ye P., Rosa L., Lee Y.K., Wu H.P., et al. Tet1 regulates adult hippocampal neurogenesis and cognition. Cell Stem Cell 2013, 13:237-245.