Genomic distribution and possible functions of DNA hydroxymethylation in the brain

Genomics

Volumn 104, Issue 5, 2014, Pages 341-346

  Wen, Lu ^a   Tang, Fuchou ^a  

^a PEKING UNIVERSITY   (China)

Author keywords

5 Hydroxymethylcytosine; Active DNA demethylation; Brain; DNA methylation; MeCP2; TET

Indexed keywords

5 HYDROXYMETHYLCYTOSINE; 5 METHYLCYTOSINE; PROTEIN; TEN ELEVEN TRANSLOCATION PROTEIN; UNCLASSIFIED DRUG; 5-HYDROXYMETHYLCYTOSINE; CYTOSINE; DNA BINDING PROTEIN;

BRAIN; BRAIN DEVELOPMENT; DNA HYDROXYMETHYLATION; DNA METABOLISM; DNA METHYLATION; EPIGENETICS; GENE INACTIVATION; GENE MAPPING; GENE SILENCING; GENETIC ASSOCIATION; GENOMICS; HUMAN; MEMORY; NONHUMAN; OXIDATION; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; ANALOGS AND DERIVATIVES; ANIMAL; GENETIC EPIGENESIS; GENETICS; GENOME; METABOLISM; OXIDATION REDUCTION REACTION;

5-METHYLCYTOSINE; ANIMALS; BRAIN; CYTOSINE; DNA METHYLATION; DNA-BINDING PROTEINS; EPIGENESIS, GENETIC; GENOME; HUMANS; OXIDATION-REDUCTION;

EID: 84927695541     PISSN: 08887543     EISSN: 10898646     Source Type: Journal    
DOI: 10.1016/j.ygeno.2014.08.020     Document Type: Review

References (57)

1. Kriaucionis S., Heintz N. The nuclear DNA base 5-hydroxymethylcytosine is present in Purkinje neurons and the brain. Science 2009, 324:929-930.
2. Tahiliani M., Koh K.P., Shen Y., Pastor W.A., Bandukwala H., Brudno Y., Agarwal S., Iyer L.M., Liu D.R., Aravind L., Rao A. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 2009, 324:930-935.
3. Shen L., Song C.X., He C., Zhang Y. Mechanism and function of oxidative reversal of DNA and RNA methylation. Annu. Rev. Biochem. 2014, 83:585-614.
4. Mellen M., Ayata P., Dewell S., Kriaucionis S., Heintz N. MeCP2 binds to 5hmC enriched within active genes and accessible chromatin in the nervous system. Cell 2012, 151:1417-1430.
5. Day J.J., Sweatt J.D. DNA methylation and memory formation. Nat. Neurosci. 2010, 13:1319-1323.
6. 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.
7. 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.
8. Song C.X., Szulwach K.E., Fu Y., Dai Q., Yi C., Li X., Li Y., Chen C.H., Zhang W., Jian X., Wang J., Zhang L., Looney T.J., Zhang B., Godley L.A., Hicks L.M., Lahn B.T., Jin P., He C. Selective chemical labeling reveals the genome-wide distribution of 5-hydroxymethylcytosine. Nat. Biotechnol. 2011, 29:68-72.
9. Ito S., Shen L., Dai Q., Wu S.C., Collins L.B., Swenberg J.A., He C., Zhang Y. Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine. Science 2011, 333:1300-1303.
10. Almeida R.D., Sottile V., Loose M., De Sousa P.A., Johnson A.D., Ruzov A. Semi-quantitative immunohistochemical detection of 5-hydroxymethyl-cytosine reveals conservation of its tissue distribution between amphibians and mammals. Epigenetics 2012, 7:137-140.
11. Szulwach K.E., Li X., Li Y., Song C.X., Wu H., Dai Q., Irier H., Upadhyay A.K., Gearing M., Levey A.I., Vasanthakumar A., Godley L.A., Chang Q., Cheng X., He C., Jin P. 5-hmC-mediated epigenetic dynamics during postnatal neurodevelopment and aging. Nat. Neurosci. 2011, 14:1607-1616.
12. Hahn M.A., Qiu R., Wu X., Li A.X., Zhang H., Wang J., Jui J., Jin S.G., Jiang Y., Pfeifer G.P., Lu Q. Dynamics of 5-hydroxymethylcytosine and chromatin marks in mammalian neurogenesis. Cell Rep. 2013, 3:291-300.
13. Stroud H., Feng S., Morey Kinney S., Pradhan S., Jacobsen S.E. 5-Hydroxymethylcytosine is associated with enhancers and gene bodies in human embryonic stem cells. Genome Biol. 2011, 12:R54.
14. Jin S.G., Wu X., Li A.X., Pfeifer G.P. Genomic mapping of 5-hydroxymethylcytosine in the human brain. Nucleic Acids Res. 2011, 39:5015-5024.
15. Khare T., Pai S., Koncevicius K., Pal M., Kriukiene E., Liutkeviciute Z., Irimia M., Jia P., Ptak C., Xia M., Tice R., Tochigi M., Morera S., Nazarians A., Belsham D., Wong A.H., Blencowe B.J., Wang S.C., Kapranov P., Kustra R., Labrie V., Klimasauskas S., Petronis A. 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.
16. Wang T., Pan Q., Lin L., Szulwach K.E., Song C.X., He C., Wu H., Warren S.T., Jin P., Duan R., Li X. Genome-wide DNA hydroxymethylation changes are associated with neurodevelopmental genes in the developing human cerebellum. Hum. Mol. Genet. 2012, 21:5500-5510.
17. Wen L., Li X., Yan L., Tan Y., Li R., Zhao Y., Wang Y., Xie J., Zhang Y., Song C., Yu M., Liu X., Zhu P., Hou Y., Guo H., Wu X., He C., Tang F., Qiao J. Whole-genome analysis of 5-hydroxymethylcytosine and 5-methylcytosine at base resolution in the human brain. Genome Biol. 2014, 15:R49.
18. 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., Yu M., Tonti-Filippini J., Heyn H., Hu S., Wu J.C., Rao A., Esteller M., He C., Haghighi F.G., Sejnowski T.J., Behrens M.M., Ecker J.R. Global epigenomic reconfiguration during mammalian brain development. Science 2013, 341:1237905.
19. Yu M., Hon G.C., Szulwach K.E., Song C.X., Zhang L., Kim A., Li X., Dai Q., Shen Y., Park B., Min J.H., Jin P., Ren B., He C. Base-resolution analysis of 5-hydroxymethylcytosine in the mammalian genome. Cell 2012, 149:1368-1380.
20. Guo J.U., Ma D.K., Mo H., Ball M.P., Jang M.H., Bonaguidi M.A., Balazer J.A., Eaves H.L., Xie B., Ford E., Zhang K., Ming G.L., Gao Y., Song H. Neuronal activity modifies the DNA methylation landscape in the adult brain. Nat. Neurosci. 2011, 14:1345-1351.
21. Jones P.A. Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat. Rev. Genet. 2012, 13:484-492.
22. Gan H., Wen L., Liao S., Lin X., Ma T., Liu J., Song C.X., Wang M., He C., Han C., Tang F. Dynamics of 5-hydroxymethylcytosine during mouse spermatogenesis. Nat. Commun. 2013, 4:1995.
23. Ivanov M., Kals M., Kacevska M., Barragan I., Kasuga K., Rane A., Metspalu A., Milani L., Ingelman-Sundberg M. Ontogeny, distribution and potential roles of 5-hydroxymethylcytosine in human liver function. Genome Biol. 2013, 14:R83.
24. Zemach A., McDaniel I.E., Silva P., Zilberman D. Genome-wide evolutionary analysis of eukaryotic DNA methylation. Science 2010, 328:916-919.
25. Coleman-Derr D., Zilberman D. DNA methylation, H2A.Z, and the regulation of constitutive expression. Cold Spring Harb. Symp. Quant. Biol. 2012, 77:147-154.
26. Lister R., Pelizzola M., Dowen R.H., Hawkins R.D., Hon G., Tonti-Filippini J., Nery J.R., Lee L., Ye Z., Ngo Q.M., Edsall L., Antosiewicz-Bourget J., Stewart R., Ruotti V., Millar A.H., Thomson J.A., Ren B., Ecker J.R. Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 2009, 462:315-322.
27. Laurent L., Wong E., Li G., Huynh T., Tsirigos A., Ong C.T., Low H.M., Kin Sung K.W., Rigoutsos I., Loring J., Wei C.L. Dynamic changes in the human methylome during differentiation. Genome Res. 2010, 20:320-331.
28. Maunakea A.K., Chepelev I., Cui K., Zhao K. Intragenic DNA methylation modulates alternative splicing by recruiting MeCP2 to promote exon recognition. Cell Res. 2013, 23:1256-1269.
29. Chodavarapu R.K., Feng S., Bernatavichute Y.V., Chen P.Y., Stroud H., Yu Y., Hetzel J.A., Kuo F., Kim J., Cokus S.J., Casero D., Bernal M., Huijser P., Clark A.T., Kramer U., Merchant S.S., Zhang X., Jacobsen S.E., Pellegrini M. Relationship between nucleosome positioning and DNA methylation. Nature 2010, 466:388-392.
30. Kellinger M.W., Song C.X., Chong J., Lu X.Y., He C., Wang D. 5-Formylcytosine and 5-carboxylcytosine reduce the rate and substrate specificity of RNA polymerase II transcription. Nat. Struct. Mol. Biol. 2012, 19:831-833.
31. Song C.X., Szulwach K.E., Dai Q., Fu Y., Mao S.Q., Lin L., Street C., Li Y., Poidevin M., Wu H., Gao J., Liu P., Li L., Xu G.L., Jin P., He C. Genome-wide profiling of 5-formylcytosine reveals its roles in epigenetic priming. Cell 2013, 153:678-691.
32. Shen L., Wu H., Diep D., Yamaguchi S., D'Alessio A.C., Fung H.L., Zhang K., Zhang Y. Genome-wide analysis reveals TET- and TDG-dependent 5-methylcytosine oxidation dynamics. Cell 2013, 153:692-706.
33. Pfaffeneder T., Spada F., Wagner M., Brandmayr C., Laube S.K., Eisen D., Truss M., Steinbacher J., Hackner B., Kotljarova O., Schuermann D., Michalakis S., Kosmatchev O., Schiesser S., Steigenberger B., Raddaoui N., Kashiwazaki G., Muller U., Spruijt C.G., Vermeulen M., Leonhardt H., Schar P., Muller M., Carell T. Tet oxidizes thymine to 5-hydroxymethyluracil in mouse embryonic stem cell DNA. Nat. Chem. Biol. 2014, 10:574-581.
34. Wu H., D'Alessio A.C., Ito S., Wang Z., Cui K., Zhao K., Sun Y.E., Zhang Y. Genome-wide analysis of 5-hydroxymethylcytosine distribution reveals its dual function in transcriptional regulation in mouse embryonic stem cells. Genes Dev. 2011, 25:679-684.
35. Baubec T., Ivanek R., Lienert F., Schubeler D. Methylation-dependent and -independent genomic targeting principles of the MBD protein family. Cell 2013, 153:480-492.
36. Hackett J.A., Sengupta R., Zylicz J.J., Murakami K., Lee C., Down T.A., Surani M.A. Germline DNA demethylation dynamics and imprint erasure through 5-hydroxymethylcytosine. Science 2013, 339:448-452.
37. Jakovcevski M., Akbarian S. Epigenetic mechanisms in neurological disease. Nat. Med. 2012, 18:1194-1204.
38. 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.
39. LaPlant Q., Vialou V., Covington H.E., Dumitriu D., Feng J., Warren B.L., Maze I., Dietz D.M., Watts E.L., Iniguez S.D., Koo J.W., Mouzon E., Renthal W., Hollis F., Wang H., Noonan M.A., Ren Y., Eisch A.J., Bolanos C.A., Kabbaj M., Xiao G., Neve R.L., Hurd Y.L., Oosting R.S., Fan G., Morrison J.H., Nestler E.J. Dnmt3a regulates emotional behavior and spine plasticity in the nucleus accumbens. Nat. Neurosci. 2010, 13:1137-1143.
40. Miller C.A., Sweatt J.D. Covalent modification of DNA regulates memory formation. Neuron 2007, 53:857-869.
41. 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.
42. 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.
43. Ito S., D'Alessio A.C., Taranova O.V., Hong K., Sowers L.C., Zhang Y. Role of Tet proteins in 5mC to 5hmC conversion, ES-cell self-renewal and inner cell mass specification. Nature 2010, 466:1129-1133.
44. 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., Liu W., Xu Z.M., Yang L., Ding Y.Q., Tang F., Meissner A., Ding C., Shi Y., Xu G.L. Tet1 regulates adult hippocampal neurogenesis and cognition. Cell Stem Cell 2013, 13:237-245.
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. 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.
47. 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.
48. Xu Y., Xu C., Kato A., Tempel W., Abreu J.G., Bian C., Hu Y., Hu D., Zhao B., Cerovina T., Diao J., Wu F., He H.H., Cui Q., Clark E., Ma C., Barbara A., Veenstra G.J., Xu G., Kaiser U.B., Liu X.S., Sugrue S.P., He X., Min J., Kato Y., Shi Y.G. Tet3 CXXC domain and dioxygenase activity cooperatively regulate key genes for Xenopus eye and neural development. Cell 2012, 151:1200-1213.
49. Spruijt C.G., Gnerlich F., Smits A.H., Pfaffeneder T., Jansen P.W., Bauer C., Munzel M., Wagner M., Muller M., Khan F., Eberl H.C., Mensinga A., Brinkman A.B., Lephikov K., Muller U., Walter J., Boelens R., van Ingen H., Leonhardt H., Carell T., Vermeulen M. Dynamic readers for 5-(hydroxy)methylcytosine and its oxidized derivatives. Cell 2013, 152:1146-1159.
50. Frauer C., Hoffmann T., Bultmann S., Casa V., Cardoso M.C., Antes I., Leonhardt H. Recognition of 5-hydroxymethylcytosine by the Uhrf1 SRA domain. PLoS One 2011, 6:e21306.
51. Guy J., Cheval H., Selfridge J., Bird A. The role of MeCP2 in the brain. Annu. Rev. Cell Dev. Biol. 2011, 27:631-652.
52. Skene P.J., Illingworth R.S., Webb S., Kerr A.R., James K.D., Turner D.J., Andrews R., Bird A.P. Neuronal MeCP2 is expressed at near histone-octamer levels and globally alters the chromatin state. Mol. Cell 2010, 37:457-468.
53. Valinluck V., Tsai H.H., Rogstad D.K., Burdzy A., Bird A., Sowers L.C. Oxidative damage to methyl-CpG sequences inhibits the binding of the methyl-CpG binding domain (MBD) of methyl-CpG binding protein 2 (MeCP2). Nucleic Acids Res. 2004, 32:4100-4108.
54. Khrapunov S., Warren C., Cheng H., Berko E.R., Greally J.M., Brenowitz M. Unusual characteristics of the DNA binding domain of epigenetic regulatory protein MeCP2 determine its binding specificity. Biochemistry 2014, 53:3379-3391.
55. Chahrour M., Jung S.Y., Shaw C., Zhou X., Wong S.T., Qin J., Zoghbi H.Y. MeCP2, a key contributor to neurological disease, activates and represses transcription. Science 2008, 320:1224-1229.
56. Li Y., Wang H., Muffat J., Cheng A.W., Orlando D.A., Loven J., Kwok S.M., Feldman D.A., Bateup H.S., Gao Q., Hockemeyer D., Mitalipova M., Lewis C.A., Vander Heiden M.G., Sur M., Young R.A., Jaenisch R. Global transcriptional and translational repression in human-embryonic-stem-cell-derived Rett syndrome neurons. Cell Stem Cell 2013, 13:446-458.
57. Young J.I., Hong E.P., Castle J.C., Crespo-Barreto J., Bowman A.B., Rose M.F., Kang D., Richman R., Johnson J.M., Berget S., Zoghbi H.Y. Regulation of RNA splicing by the methylation-dependent transcriptional repressor methyl-CpG binding protein 2. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:17551-17558.