Molecular epigenetic switches in neurodevelopment in health and disease

Frontiers in Behavioral Neuroscience

Volumn 9, Issue MAY, 2015, Pages

  Hoffmann, Anke ^a   Zimmermann, Christoph A ^a   Spengler, Dietmar ^a  

^a MAX PLANCK INSTITUTE OF PSYCHIATRY   (Germany)

Author keywords

Avp; Bivalent domains; Early life stress; Genomic imprinting; Molecular clocks; NSC; Polycomb; Transposons

Indexed keywords

DNA;

AVP GENE; BRAIN DEVELOPMENT; CIRCADIAN RHYTHM; DEVELOPMENTAL GENE; DNA METHYLATION; EARLY LIFE STRESS; EMBRYONIC STEM CELL; EPIGENETICS; GENE; GENE EXPRESSION; GENE SWITCHING; GENETIC REGULATION; GENOME IMPRINTING; GENOTYPE ENVIRONMENT INTERACTION; HISTONE MODIFICATION; HUMAN; KISS1 GENE; MOLECULAR DYNAMICS; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NONHUMAN; PHENOTYPE; PUBERTY; RETROPOSON; REVIEW;

EID: 84929332970     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2015.00120     Document Type: Review

References (119)

1. Allis, C.D.(2009). Epigenetics. Cold Spring Harbor NY: ColdSpringHarbor Laboratory Press.
2. Armstrong, L.(2013). Epigenetic. 1st dn. NewYork, NY: Garland Science, Taylor & Francis Group, LLC.
3. Athanikar, J.N., Badge, R.M., and Moran, J.V. (2004). AYY1-bindingsiteis required foraccuratehumanLINE-1transcriptioninitiation. Nucleic AcidsRes. 32, 3846-3855. doi:10.1093/nar/gkh698
4. Auger, C.J., Coss, D., Auger, A.P., and Forbes-Lorman, R.M. (2011). Epigenetic control ofvasopressinexpressionismaintainedbysteroidhormonesinthe adult maleratbrain. Proc. Natl.Acad.Sci.USA 108, 4242-4247.doi:10.1073/pnas.1100314108
5. Azzi, A., Dallmann, R., Casserly, A., Rehrauer, H., Patrignani, A., Maier, B., etal. (2014). Circadianbehaviorislight-reprogrammedbyplastic DNAmethylation. Nat. Neurosci. 17, 377-382.doi:10.1038/nn.3651
6. Badcock, C., and Crespi, B. (2008). Battleofthesexesmaysetthebrain. Nature 454, 1054-1055.doi:10.1038/4541054a
7. Barrett, P., Ebling, F.J.P., Schuhler, S., Wilson, D., Ross, A.W., Warner, A., et al. (2007). Hypothalamicthyroidhormonecatabolismactsasagatekeeper for theseasonalcontrolofbodyweightandreproduction. Endocrinology 148, 3608-3617. doi:10.3410/f.1086035.538993
8. Bellini, E., Pavesi, G., Barbiero, I., Bergo, A., Chandola, C., Nawaz, M. S., et al. (2014). MeCP2 post-translational modifications: a mechanism to control its involvement in synaptic plasticity and homeostasis? Front. Cell. Neurosci. 8:236. doi: 10.3389/fncel.2014.00236
9. Bernstein, B. E., Mikkelsen, T. S., Xie, X., Kamal, M., Huebert, D. J., Cuff, J., et al. (2006). A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125, 315-326. doi: 10.1016/j.cell.2006.02.041
10. Bird, A. (2002). DNA methylation patterns and epigenetic memory. Genes Dev. 16, 6-21. doi: 10.1101/gad.947102
11. Bird, A. (2007). Perceptions of epigenetics. Nature 447, 396-398. doi: 10.1038/nature05913
12. Bundo, M., Toyoshima, M., Okada, Y., Akamatsu, W., Ueda, J., Nemoto- Miyauchi, T., et al. (2014). Increased l1 retrotransposition in the neuronal genome in schizophrenia. Neuron 81, 306-313. doi: 10.1016/j.neuron.2013.10.053
13. Cairns, B. R. (2007). Chromatin remodeling: insights and intrigue from single-molecule studies. Nat. Struct. Mol. Biol. 14, 989-996. doi: 10.1038/nsmb1333
14. Ciarleglio, C. M., Axley, J. C., Strauss, B. R., Gamble, K. L., and McMahon, D. G. (2011). Perinatal photoperiod imprints the circadian clock. Nat. Neurosci. 14, 25-27. doi: 10.1038/nn.2699
15. Constância, M., Kelsey, G., and Reik, W. (2004). Resourceful imprinting. Nature432, 53-57. doi: 10.1038/432053a
16. Cortellino, S., Xu, J., Sannai, M., Moore, R., Caretti, E., Cigliano, A., et al. (2011). Thymine DNA glycosylase is essential for active DNA demethylation by linked deamination-base excision repair. Cell 146, 67-79. doi: 10.1016/j.cell.2011.06.020
17. Coufal, N. G., Garcia-Perez, J. L., Peng, G. E., Marchetto, M. C. N., Muotri, A. R., Mu, Y., et al. (2011). Ataxia telangiectasia mutated (ATM) modulates long interspersed element-1 (L1) retrotransposition in human neural stem cells. Proc. Natl. Acad. Sci. USA 108, 20382-20387. doi: 10.1073/pnas.1100273108
18. Coufal, N. G., Garcia-Perez, J. L., Peng, G. E., Yeo, G. W., Mu, Y., Lovci, M. T., et al. (2009). L1 retrotransposition in human neural progenitor cells. Nature 460, 1127-1131. doi: 10.1038/nature08248
19. Crone, E. A., and Dahl, R. E. (2012). Understanding adolescence as a period of social-affective engagement and goal flexibility. Nat. Rev. Neurosci. 13, 636-650. doi: 10.1038/nrn3313
20. Cubas, P., Vincent, C., and Coen, E. (1999). An epigenetic mutation responsible for natural variation in floral symmetry. Nature 401, 157-161. doi: 10.1038/43657
21. Daniel, G., Schmidt-Edelkraut, U., Spengler, D., and Hoffmann, A. (2015). Imprinted Zac1 in neural stem cells. World J. Stem Cells 7, 300-314. doi: 10.4252/wjsc.v7.i2.300
22. da Rocha, S. T., Edwards, C. A., Ito, M., Ogata, T., and Ferguson-Smith, A. C. (2008). Genomic imprinting at the mammalian Dlk1-Dio3 domain. Trends Genet. 24, 306-316. doi: 10.1016/j.tig.2008.03.011
23. Dawkins, R. (2006). The Selfish Gene. 30th anniversary ed. Oxford, NY: Oxford University Press.
24. Deaton, A. M., and Bird, A. (2011). CpG islands and the regulation of transcription. Genes Dev. 25, 1010-1022. doi: 10.1101/gad.2037511
25. Djebali, S., Davis, C. A., Merkel, A., Dobin, A., Lassmann, T., Mortazavi, A., et al. (2012). Landscape of transcription in human cells. Nature 489, 101-108. doi: 10.1038/nature11233
26. Edwards, C. A., and Ferguson-Smith, A. C. (2007). Mechanisms regulating imprinted genes in clusters. Curr. Opin. Cell Biol. 19, 281-289. doi: 10.1016/j.ceb.2007.04.013
27. Edwards, V. J., Holden, G. W., Felitti, V. J., and Anda, R. F. (2003). Relationship between multiple forms of childhood maltreatment and adult mental health in community respondents: results from the adverse childhood experiences study. Am. J. Psychiatry 160, 1453-1460. doi: 10.1176/appi.ajp.160.8.1453
28. Evrony, G. D., Cai, X., Lee, E., Hills, L. B., Elhosary, P. C., Lehmann, H. S., et al. (2012). Single-neuron sequencing analysis ofL1 retrotransposition and somatic mutation in the human brain. Cell 151, 483-496. doi: 10.1016/j.cell.2012.09.035
29. Faulkner, G. J., Kimura, Y., Daub, C. O., Wani, S., Plessy, C., Irvine, K. M., et al. (2009). The regulated retrotransposon transcriptome of mammalian cells. Nat. Genet. 41, 563-571. doi: 10.1038/ng.368
30. Feinberg, A. P. (2007). Phenotypic plasticity and the epigenetics of human disease.Nature 447, 433-440. doi: 10.1038/nature05919
31. Felitti, V. J., Anda, R. F., Nordenberg, D., Williamson, D. F., Spitz, A. M., Edwards, V., et al. (1998). Relationship of childhood abuse and household dysfunction to many of the leading causes of death in adults. The Adverse Childhood Experiences (ACE) study. Am. J. Prev. Med. 14, 245-258. doi: 10.1016/s0749-3797(98)00017-8
32. Feng, J., Chang, H., Li, E., and Fan, G. (2005). Dynamic expression of de novo DNA methyltransferases Dnmt3a and Dnmt3b in the central nervous system. J. Neurosci. Res. 79, 734-746. doi: 10.1002/jnr.20404
33. Ferrón, S. R., Charalambous, M., Radford, E., McEwen, K., Wildner, H., Hind, E., et al. (2011). Postnatal loss of Dlk1 imprinting in stem cells and niche astrocytes regulates neurogenesis. Nature 475, 381-385. doi: 10.1038/nature10229
34. Fournier, A., Sasai, N., Nakao, M., and Defossez, P.-A. (2012). The role of methyl- binding proteins in chromatin organization and epigenome maintenance. Brief. Funct. Genomics 11, 251-264. doi: 10.1093/bfgp/elr040
35. Furey, T. S., and Sethupathy, P. (2013). Genetics. Genetics driving epigenetics.Science 342,705-706. doi: 10.1126/science.1246755
36. Gallego, M., and Virshup, D. M. (2007). Post-translational modifications regulate the ticking of the circadian clock. Nat. Rev. Mol. Cell Biol. 8, 139-148. doi: 10.1038/nrm2106
37. Gottschling, D. E. (2004). Summary: epigenetics--from phenomenon to field. Cold Spring Harb. Symp. Quant. Biol. 69, 507-519. doi: 10.1101/sqb.2004.69.507
38. Green, J. G., McLaughlin, K. A., Berglund, P. A., Gruber, M. J., Sampson, N. A., Zaslavsky, A. M., et al. (2010). Childhood adversities and adult psychiatric disorders in the national comorbidity survey replication I: associations with first onset of DSM-IV disorders. Arch. Gen. Psychiatry 67, 113-123. doi: 10.1001/archgenpsychiatry.2009.186
39. Guo, J. U., Su, Y., Zhong, C., Ming, G., and Song, H. (2011). Hydroxylation of 5-methylcytosine by TET1 promotes active DNA demethylation in the adult brain. Cell145, 423-434. doi: 10.1016/j.cell.2011.03.022
40. He, Y.-F., Li, B.-Z., Li, Z., Liu, P., Wang, Y., Tang, Q., et al. (2011). Tet-mediated formation of 5-carboxylcytosine and its excision by TDG in mammalian DNA. Science 333, 1303-1307. doi: 10.1126/science.1210944
41. Heim, C., and Binder, E. B. (2012). Current research trends in early life stress and depression: review of human studies on sensitive periods, gene- environment interactions and epigenetics. Exp. Neurol. 233, 102-111. doi: 10.1016/j.expneurol.2011.10.032
42. Heim, C., Newport, D. J., Mletzko, T., Miller, A. H., and Nemeroff, C. B. (2008). The link between childhood trauma and depression: insights from HPA axis studies in humans. Psychoneuroendocrinology 33, 693-710. doi: 10.1016/j.psyneuen.2008.03.008
43. Henikoff, S., and Shilatifard, A. (2011). Histone modification: cause or cog? Trends Genet. 27, 389-396. doi: 10.1016/j.tig.2011.06.006
44. Hoffmann, A., Guillaume, D., Schmidt-Edelkraut, U., and Spengler, D. (2014). Roles of imprinted genes in neural stem cells. Epigenomics 6, 515-532. doi: 10.2217/epi.14.42
45. Hoffmann, A., and Spengler, D. (2012). The lasting legacy of social stress on the epigenome of the hypothalamic-pituitary-adrenal axis. Epigenomics 4,431-444. doi: 10.2217/epi.12.34
46. Hoffmann, A., and Spengler, D. (2014). DNA memories of early social life. Neuroscience 264, 64-75. doi: 10.1016/j.neuroscience.2012.04.003
47. Holliday, R. (1991). Mutations and epimutations in mammalian cells. Mutat. Res. 250, 351-363. doi: 10.1016/0027-5107(91)90192-q
48. Holliday, R., and Pugh, J. E. (1975). DNA modification mechanisms and gene activity during development. Science 187, 226-232. doi: 10.1126/science.1111098
49. Hunter, R. G., Murakami, G., Dewell, S., Seligsohn, M., Baker, M. E. R., Datson, N. A., et al. (2012). Acute stress and hippocampal histone H3 lysine 9 trimethylation, a retrotransposon silencing response. Proc. Natl. Acad. Sci. USA 109, 17657-17662. doi: 10.1073/pnas.1215810109
50. Ito, S., D’Alessio, A. C., Taranova, O. V., Hong, K., Sowers, L. C., and Zhang, Y. (2010). Role of Tet proteins in 5mC to 5hmC conversion, ES-cell self­renewal and inner cell mass specification. Nature 466, 1129-1133. doi: 10.1038/nature09303
51. Ito, S., Shen, L., Dai, Q., Wu, S. C., Collins, L. B., Swenberg, J. A., et al. (2011). Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5- carboxylcytosine. Science 333, 1300-1303. doi: 10.1126/science.1210597
52. Jirtle, R. L. (2012). Geneimprint. Available online at: http://www.geneimprint.org/
53. Katada, S., Imhof, A., and Sassone-Corsi, P. (2012). Connecting threads: epigenetics and metabolism. Cell 148, 24-28. doi: 10.1016/j.cell.2012.01.001
54. Ko, M., An, J., Bandukwala, H. S., Chavez, L., Aijo, T., Pastor, W. A., et al. (2013). Modulation of TET2 expression and 5-methylcytosine oxidation by the CXXC domain protein IDAX. Nature 497, 122-126. doi: 10.1038/nature12052
55. Kouzarides, T. (2007). Chromatin modifications and their function. Cell 128, 693-705. doi: 10.1016/j.cell.2007.02.005
56. Kuwabara, T., Hsieh, J., Muotri, A., Yeo, G., Warashina, M., Lie, D. C., et al. (2009). Wnt-mediated activation of NeuroD1 and retro-elements during adult neurogenesis. Nat. Neurosci. 12, 1097-1105. doi: 10.1038/nn.2360
57. Lander, E. S., Linton, L. M., Birren, B., Nusbaum, C., Zody, M. C., Baldwin, J., et al. (2001). Initial sequencing and analysis of the human genome. Nature 409, 860-921. doi: 10.1038/35057062
58. Levin, H. L., and Moran, J. V. (2011). Dynamic interactions between transposable elements and their hosts. Nat. Rev. Genet. 12, 615-627. doi: 10.1038/nrg3030
59. Li, B., Carey, M., and Workman, J. L. (2007). The role of chromatin during transcription. Cell 128,707-719. doi: 10.1016/j.cell.2007.01.015
60. Lister, R., Mukamel, E. A., Nery, J. R., Urich, M., Puddifoot, C. A., Johnson, N. D., et al. (2013). Global epigenomic reconfiguration during mammalian brain development. Science 341:1237905. doi: 10.1126/science.1237905
61. Lister, R., Pelizzola, M., Dowen, R. H., Hawkins, R. D., Hon, G., Tonti-Filippini, J., et al. (2009). Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 462, 315-322. doi: 10.1038/nature08514
62. Lomniczi, A., Loche, A., Castellano, J. M., Ronnekleiv, O. K., Bosch, M., Kaidar, G., et al. (2013). Epigenetic control of female puberty. Nat. Neurosci. 16, 281-289. doi: 10.1038/nn.3319
63. Lupien, S. J., McEwen, B. S., Gunnar, M. R., and Heim, C. (2009). Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat. Rev. Neurosci. 10, 434-445. doi: 10.1038/nrn2639
64. Maiti, A., and Drohat, A. C. (2011). Thymine DNA glycosylase can rapidly excise 5-formylcytosine and 5-carboxylcytosine: potential implications for active demethylation of CpG sites. J. Biol. Chem. 286, 35334-35338. doi: 10.1074/jbc.c111.284620
65. Martello, G., and Smith, A. (2014). The nature ofembryonic stem cells. Annu. Rev. Cell Dev. Biol. 30, 647-675. doi: 10.1146/annurev-cellbio-100913-013116
66. Maunakea, A. K., Nagarajan, R. P., Bilenky, M., Ballinger, T. J., D’Souza, C., Fouse, S. D., et al. (2010). Conserved role of intragenic DNA methylation in regulating alternative promoters. Nature 466, 253-257. doi: 10.1038/nature09165
67. McClintock, B. (1951). Chromosome organization and genic expression. Cold SpringHarb. Symp. Quant. Biol. 16, 13-47. doi: 10.1101/sqb.1951.016.01.004
68. McClintock, B. (1984). The significance of responses of the genome to challenge.Science 226, 792-801. doi: 10.1126/science.15739260
69. Meaney, M. J., and Ferguson-Smith, A. C. (2010). Epigenetic regulation of the neural transcriptome: the meaning of the marks. Nat. Neurosci. 13, 1313-1318. doi: 10.1038/nn1110-1313
70. Melmed, S., and Williams, R. (2011). Williams Textbook of Endocrinology. 12th Edn. Philadelphia Pa.: Saunders Elsevier.
71. Mikkelsen, T. S., Ku, M., Jaffe, D. B., Issac, B., Lieberman, E., Giannoukos, G., et al. (2007). Genome-wide maps ofchromatin state in pluripotent and lineage- committed cells. Nature 448, 553-560. doi: 10.1038/nature06008
72. Misteli, T. (2007). Beyond the sequence: cellular organization ofgenome function.Cell 128, 787-800. doi: 10.1016/j.cell.2007.01.028
73. Mohn, F., Weber, M., Rebhan, M., Roloff, T. C., Richter, J., Stadler, M. B., et al. (2008). Lineage-specific polycomb targets and denovo DNA methylation define restriction and potential ofneuronal progenitors. Mol. Cell 30,755-766. doi: 10.1016/j.molcel.2008.05.007
74. Moore, T., and Haig, D. (1991). Genomic imprinting in mammalian development: aparentaltug-of-war. Trends Genet. 7,45-49. doi: 10.1016/0168-9525(91)90040-w
75. Morison, I. M., Ramsay, J. P., and Spencer, H. G. (2005). A census of mammalian imprinting. Trends Genet. 21, 457-465. doi: 10.1016/j.tig.2005.06.008
76. Muotri, A. R., Chu, V. T., Marchetto, M. C. N., Deng, W., Moran, J. V., and Gage,H. (2005). Somatic mosaicism in neuronal precursor cells mediated by L1 retrotransposition. Nature 435, 903-910. doi: 10.1038/nature03663
77. Muotri, A. R., Marchetto, M. C. N., Coufal, N. G., Oefner, R., Yeo, G., Nakashima, K., et al. (2010). L1 retrotransposition in neurons is modulated by MeCP2. Nature 468, 443-446. doi: 10.1038/nature09544
78. Murgatroyd, C., Patchev, A. V., Wu, Y., Micale, V., Bockmühl, Y., Fischer, D., et al. (2009). Dynamic DNA methylation programs persistent adverse effects of early-life stress. Nat. Neurosci. 12, 1559-1566. doi: 10.1038/nn.2436
79. Murgatroyd, C., and Spengler, D. (2011). Epigenetic programming of the HPA axis: early life decides. Stress 14, 581-589. doi: 10.3109/10253890.2011.602146
80. Murgatroyd, C., and Spengler, D. (2014). Polycomb binding precedes early-life stress responsive DNA methylation at the Avp enhancer. PloS One 9:e90277. doi: 10.1371/journal.pone.0090277
81. Murgatroyd, C., Wu, Y., Bockmühl, Y., and Spengler, D. (2010). Genes learn from stress: howinfantile trauma programs us for depression. Epigenetics 5,194-199. doi: 10.4161/epi.5.3.11375
82. Neri, F., Krepelova, A., Incarnato, D., Maldotti, M., Parlato, C., Galvagni, F., et al. (2013). Dnmt3L antagonizes DNA methylation at bivalent promoters and favors DNA methylation at gene bodies in ESCs. Cell 155, 121-134. doi: 10.1016/j.cell.2013.08.056
83. O’Jile, J. R., and Bartness, T. J. (1992). Effects of thyroxine on the photoperiodic controlofenergybalance and reproductive status in Siberian hamsters. Physiol. Behav. 52, 267-270. doi: 10.1016/0031-9384(92)90269-8
84. Ono, H., Hoshino, Y., Yasuo, S., Watanabe, M., Nakane, Y., Murai, A., et al. (2008). Involvement of thyrotropin in photoperiodic signal transduction in mice. Proc. Natl. Acad. Sci. USA 105, 18238-18242. doi: 10.1073/pnas.0808952105
85. Ooi, S. K. T., O’Donnell, A. H., and Bestor, T. H. (2009). Mammalian cytosine methylation at a glance. J. Cell Sci. 122, 2787-2791. doi: 10.1242/jcs.015123
86. Patchev, A. V., Rodrigues, A. J., Sousa, N., Spengler, D., and Almeida, O. F. X. (2014). The future is now: earlylife events preset adult behaviour. Acta Physiol. (Oxf) 210,46-57. doi: 10.1111/apha.12140
87. Peters, J. (2014). The role of genomic imprinting in biology and disease: an expanding view. Nat. Rev. Genet. 15, 517-530. doi: 10.1038/nrg3766
88. Piet, R., de Croft, S., Liu, X., and Herbison, A. E. (2015). Electrical properties of kisspeptin neurons and their regulation of GnRH neurons. Front. Neuroendocrinol. 36, 15-27. doi: 10.1016/j.yfrne.2014.05.006
89. Ponomarev, I., Rau, V., Eger, E. I., Harris, R. A., and Fanselow, M. S. (2010). Amygdala transcriptome and cellular mechanisms underlying stress- enhanced fear learning in a rat model of posttraumatic stress disorder. Neuropsychopharmacology 35, 1402-1411. doi: 10.1038/npp.2010.10
90. Ptashne, M. (2004). A Genetic Switch. 3rd Edn. Cold Spring Harbor N.Y.: Cold Spring Harbor Laboratory Press.
91. Ptashne, M. (2007). On the use of the word ‘‘epigenetic’’. Curr. Biol. 17, R233-R236. doi: 10.1016/j.cub.2007.02.030
92. Ptashne, M. (2013). Epigenetics: core misconcept. Proc. Natl. Acad. Sci. USA 110, 7101-7103. doi: 10.1073/pnas.1305399110
93. Ptashne, M. (2014). The chemistry of regulation of genes and other things. J. Biol. Chem. 289, 5417-5435. doi: 10.1074/jbc.x114.547323
94. Raabe, F. J., and Spengler, D. (2013). Epigenetic risk factors in PTSD and depression. Front. Psychiatry 4:80. doi: 10.3389/fpsyt.2013.00080
95. Reilly, M. T., Faulkner, G. J., Dubnau, J., Ponomarev, I., and Gage, F. H. (2013). The role of transposable elements in health and diseases of the central nervous system. J. Neurosci. 33, 17577-17586. doi: 10.1523/jneurosci.3369-13.2013
96. Reiter, R. J. (1980). The pineal and its hormones in the control ofreproduction in mammals. Endocr. Rev. 1, 109-131. doi: 10.1210/edrv-1-2-109
97. Schroeder, D. I., Lott, P., Korf, I., and LaSalle, J. M. (2011). Large-scale methylation domains mark a functional subset of neuronally expressed genes. Genome Res. 21, 1583-1591. doi: 10.1101/gr.119131.110
98. Schuettengruber, B., Chourrout, D., Vervoort, M., Leblanc, B., and Cavalli, G. (2007). Genome regulation by polycomb and trithorax proteins. Cell 128, 735-745. doi: 10.1016/j.cell.2007.02.009
99. Sharif, J., Muto, M., Takebayashi, S., Suetake, I., Iwamatsu, A., Endo, T. A., et al. (2007). The SRA protein Np95 mediates epigenetic inheritance by recruiting Dnmt1 to methylated DNA. Nature 450, 908-912. doi: 10.1038/nature06397
100. Shilatifard, A. (2012). The COMPASS family of histone H3K4 methylases: mechanisms of regulation in development and disease pathogenesis. Annu. Rev. Biochem. 81, 65-95. doi: 10.1146/annurev-biochem-051710-134100
101. Simon, J. A., and Kingston, R. E. (2013). Occupying chromatin: polycomb mechanisms for getting to genomic targets, stopping transcriptional traffic and staying put. Mol. Cell 49, 808-824. doi: 10.1016/j.molcel.2013.02.013
102. Speicher, M. R., Antonarakis, S. E., Motulsky, A. G., and Vogel, F. (eds) (2010). Vogel and Motulsky’s Human Genetics: Problems and Approaches. 4th completely rev. ed. Heidelberg; NewYork: Springer.
103. Spruijt, C. G., Gnerlich, F., Smits, A. H., Pfaffeneder, T., Jansen, P. W. T. C., Bauer, C., et al. (2013). Dynamic readers for 5-(hydroxy)methylcytosine and its oxidized derivatives. Cell 152, 1146-1159. doi: 10.1016/j.cell.2013.02.004
104. Stevenson, T. J., and Prendergast, B. J. (2013). Reversible DNA methylation regulates seasonal photoperiodic time measurement. Proc. Natl. Acad. Sci. USA 110, 16651-16656. doi: 10.1073/pnas.1310643110
105. Sweatt, J. D. (2013). The emerging field of neuroepigenetics. Neuron 80, 624-632. doi: 10.1016/j.neuron.2013.10.023
106. Szyf, M., and Bick, J. (2013). DNA methylation: a mechanism for embeddingearly lifeexperiences inthegenome. ChildDev. 84,49-57. doi: 10.1111/j.1467-8624.2012.01793.x
107. Tahiliani, M., Koh, K. P., Shen, Y., Pastor, W. A., Bandukwala, H., Brudno, Y., et al. (2009). Conversion of 5-methylcytosine to 5-hydroxymethylcytosinein mammalian DNA by MLL partner TET1. Science 324, 930-935. doi: 10.1126/science.1170116
108. Takada, S., Paulsen, M., Tevendale, M., Tsai, C.-E., Kelsey, G., Cattanach, B. M., et al. (2002). Epigenetic analysis of the Dlk1-Gtl2 imprinted domain on mouse chromosome 12: implications for imprinting control from comparison with Igf2-H19. Hum. Mol. Genet. 11, 77-86. doi: 10.1093/hmg/11.1.77
109. Takahashi, J. S., Hong, H.-K., Ko, C. H., and McDearmon, E. L. (2008). The genetics of mammalian circadian order and disorder: implications for physiology and disease. Nat. Rev. Genet. 9,764-775. doi: 10.1038/nrg2430
110. Tchénio, T., Casella, J. F., and Heidmann, T. (2000). Members of the SRY family regulate the human LINE retrotransposons. Nucleic Acids Res. 28, 411-415. doi: 10.1093/nar/28.2.411
111. Thurman, R. E., Rynes, E., Humbert, R., Vierstra, J., Maurano, M. T., Haugen, E., et al. (2012). The accessible chromatin landscape of the human genome. Nature 489, 75-82. doi: 10.1038/nature11232
112. Tollefsbol, T. (2011). Handbook of Epigenetics. 1st Edn. Amsterdam: Elsevier.
113. Tuite, M. F., and Serio, T. R. (2010). The prion hypothesis: from biological anomaly to basic regulatory mechanism. Nat. Rev. Mol. Cell Biol. 11, 823-833. doi: 10.1038/nrm3007
114. Voigt, P., Tee, W.-W., and Reinberg, D. (2013). A double take on bivalent promoters. Genes Dev. 27, 1318-1338. doi: 10.1101/gad.219626.113
115. Weber, M., Hellmann, I., Stadler, M. B., Ramos, L., Paabo, S., Rebhan, M., et al. (2007). Distribution, silencing potential and evolutionary impact of promoter DNA methylation in the human genome. Nat. Genet. 39, 457-466. doi: 10.3410/f.1071721.524633
116. Wu, H., and Zhang, Y. (2014). Reversing DNA methylation: mechanisms, genomics and biological functions. Cell 156, 45-68. doi: 10.1016/j.cell.2013.12.019
117. Xie, W., Barr, C. L., Kim, A., Yue, F., Lee, A. Y., Eubanks, J., et al. (2012). Base-resolution analyses of sequence and parent-of-origin dependent DNA methylation in the mouse genome. Cell 148, 816-831. doi: 10.1016/j.cell.2011.12.035
118. Yang, N., Zhang, L., Zhang, Y., and Kazazian, H. H. (2003). An important role for RUNX3 in human L1 transcription and retrotransposition. Nucleic Acids Res. 31,4929-4940. doi: 10.1093/nar/gkg663
119. Zannas, A. S., and Binder, E. B. (2014). Gene-environment interactions at the FKBP5 locus: sensitive periods, mechanisms and pleiotropism. Genes Brain Behav. 13,25-37. doi: 10.1111/gbb.12104