Transposable elements and DNA methylation create in embryonic stem cells human-specific regulatory sequences associated with distal enhancers and noncoding RNAs

Genome Biology and Evolution

Volumn 7, Issue 6, 2015, Pages 1432-1454

  Glinsky, Gennadi V ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

CTCF; Evolution of Modern Humans; Human ESC; L1 retrotransposition; LINE; LTR; LTR7 RNAs; LTR7 HERVH; Methyl cytosine deamination; NANOG; Pluripotent state regulators; POU5F1 (OCT4); Primate evolution; Repetitive elements; Retrotransposons

Indexed keywords

CHROMATIN; HOMEODOMAIN PROTEIN; LONG UNTRANSLATED RNA; NANOG PROTEIN, HUMAN; RETROPOSON; TRANSCRIPTION FACTOR; UNTRANSLATED RNA;

ANIMAL; BINDING SITE; BRAIN; CELL DIFFERENTIATION; CHROMATIN; DNA METHYLATION; EMBRYONIC STEM CELL; ENHANCER REGION; GENETIC TRANSCRIPTION; GENETICS; HUMAN; HUMAN GENOME; METABOLISM; MOLECULAR EVOLUTION; MOUSE; MUTATION; NUCLEAR LAMINA; PRIMATE; REGULATORY SEQUENCE; RETROPOSON;

ANIMALS; BINDING SITES; BRAIN; CELL DIFFERENTIATION; CHROMATIN; DNA METHYLATION; EMBRYONIC STEM CELLS; ENHANCER ELEMENTS, GENETIC; EVOLUTION, MOLECULAR; GENOME, HUMAN; HOMEODOMAIN PROTEINS; HUMANS; MICE; MUTATION; NUCLEAR LAMINA; PRIMATES; REGULATORY ELEMENTS, TRANSCRIPTIONAL; RETROELEMENTS; RNA, LONG NONCODING; RNA, UNTRANSLATED; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84979851107     PISSN: None     EISSN: 17596653     Source Type: Journal    
DOI: 10.1093/gbe/evv081     Document Type: Article

References (64)

1. Baillie JK, et al. 2011. Somatic retrotransposition alters the genetic landscape of the human brain. Nature 479:534-537.
2. Balakrishnan SK, WitcherM, Berggren TW, Emerson BM. 2012. Functional and molecular characterization of the role of CTCF in human embryonic stem cell biology. PLoS One 7:e42424.
3. Barbieri M, et al. 2012. Complexity of chromatin folding is captured by the strings and binders switch model. Proc Natl Acad Sci U S A. 109:16173-16178.
4. Bourque G, et al. 2008. Evolution of the mammalian transcription factor binding repertoire via transposable elements. Genome Res. 18:1752-1762.
5. Bulmer M. 1986. Neighboring base effects on substitution rates in pseudogenes. Mol Biol Evol. 3:322-329.
6. Chen X, et al. 2008 Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell 133:1106-1117.
7. Coulondre C, Miller JH, Farabaugh PJ, Gilbert W. 1978. Molecular basis of base substitution hotspots in Escherichia coli. Nature 274:775-780.
8. De Koning AP, GuW, Castoe TA, Batzer MA, Pollock DD. 2011. Repetitive elements may comprise over two-thirds of the human genome. PLoS Genet. 7:e1002384.
9. Dorus S, et al. 2004. Accelerated evolution of nervous system genes in the origin of Homo sapiens. Cell 119:1027-1040.
10. Duncan BK, Miller JH. 1980. Mutagenic deamination of cytosine residues in DNA. Nature 287:560-561.
11. Ehrlich M, Wang RY. 1981. 5-Methylcytosine in eukaryotic DNA. Science 212:1350-1357.
12. Ernst J, Kellis M. 2013. Interplay between chromatin state, regulator binding, and regulatory motifs in six human cell types. Genome Res. 23:1142-1154.
13. Fort A, et al. 2014. Deep transcriptome profiling of mammalian stem cells supports a regulatory role for retrotransposons in pluripotency maintenance.Nat Genet. 46:558-566.
14. Garcia-Perez JL, et al. 2007. LINE-1 retrotransposition in human embryonic stem cells. Hum Mol Genet. 16:1569-1577.
15. Glinsky GV. 2013. RNA-guided diagnostics and therapeutics for next-generation individualized nanomedicine. J Clin Invest. 123:2350-2352.
16. Guelen L, et al. 2008. Domain organization of human chromosomes revealed by mapping of nuclear lamina interactions. Nature 453:948-951.
17. Guttman M, et al. 2011. lincRNAs act in the circuitry controlling pluripotency and differentiation. Nature 477:295-300.
18. Hwang DG, Green P. 2004. Bayesian Markov chainMonte Carlo sequence analysis reveals varying neutral substitution patterns in mammalian evolution. Proc Natl Acad Sci U S A. 101:13994-14001.
19. Jacques P-E, Jeyakani J, Bourque G. 2013. The majority of primate-specific regulatory sequences are derived from transposable elements. PLoS Genet. 9(5):e1003504.
20. Jordan IK, Rogozin IB, Glazko GV, Koonin EV. 2003. Origin of a substantial fraction of human regulatory sequences from transposable elements. Trends Genet. 19(2):68-72.
21. Kapusta A, et al. 2013. Transposable elements are major contributors to the origin, diversification, and regulation of vertebrate long noncoding RNAs. PLoS Genet. 9:e1003470.
22. Kelley D, Rinn J. 2012. Transposable elements reveal a stem cell-specific class of long noncoding RNAs. Genome Biol. 13:R107.
23. Kent WJ. 2002. BLAT-the BLAST-like alignment tool. Genome Res. 12:656-664.
24. Koyanagi-Aoi M, et al. 2013. Differentiation-defective phenotypes revealed by large-scale analyses of human pluripotent stem cells. Proc Natl Acad Sci U S A. 110:20569-20574.
25. Kunarso G, et al. 2010. Transposable elements have rewired the core regulatory network of human embryonic stem cells. Nat Genet. 42:631-634.
26. Landon PB, et al. 2014. Energetically biased DNA motor containing a thermodynamically stable partial strand displacement state. Langmuir 30:14073-14078.
27. Li G, et al. 2012. Extensive promoter-centered chromatin interactions provide a topological basis for transcription regulation. Cell 148:84-98.
28. Lister R, et al. 2009. Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 462:315-322.
29. Lister R, et al. 2013. Global epigenomic reconfiguration during mammalian brain development. Science 341:1237905.
30. Lu X, et al. 2014. The retrovirus HERVH is a long noncoding RNA required for human embryonic stem cell identity. Nat Struct Mol Biol. 21:423-425.
31. Macia A, et al. 2011. Epigenetic control of retrotransposon expression in human embryonic stem cells. Mol Cell Biol. 31:300-316.
32. Marchetto MC, et al. 2013. Differential LINE-1 regulation in pluripotent stem cells of humans and other great apes. Nature 503:525-529.
33. MeyerM, et al. 2012. A high-coverage genome sequence from an archaic Denisovan individual. Science 338:222-226.
34. Meyer LR, et al. 2013. The UCSC Genome Browser database: extensions and updates 2013. Nucleic Acids Res. 41:D64-D69.
35. Mo AH, et al. 2014. An on-demand four-way junction DNAzyme nanoswitch driven by inosine-based partial strand displacement. Nanoscale 6:1462-1466.
36. Noonan JP, et al. 2006. Sequencing and analysis of Neanderthal genomic DNA. Science 314:1113-1118.
37. Ohnuki M, et al. 2014. Dynamic regulation of human endogenous retroviruses mediates factor-induced reprogramming and differentiation potential. Proc Natl Acad Sci U S A. 111:12426-12431.
38. Peric-Hupkes D, et al. 2010. Molecular maps of the reorganization of genome-nuclear lamina interactions during differentiation. Mol Cell. 38:603-613.
39. Rada-Iglesias A, et al. 2011. A unique chromatin signature uncovers early developmental enhancers in humans. Nature 470:279-283.
40. Razin A, Riggs AD. 1980. DNA methylation and gene function. Science 210:604-610.
41. Reich D, et al. 2010. Genetic history of an archaic hominin group from Denisova Cave in Siberia. Nature 468:1053-1060.
42. Rosenbloom KR, et al. 2013. ENCODE data in the UCSC Genome Browser: year 5 update. Nucleic Acids Res. 41:D56-D63.
43. Santoni FA, Guerra J, Luban J. 2012. HERV-H RNA is abundant in human embryonic stem cells and a precise marker for pluripotency. Retrovirology 9:111.
44. Schmidt D, et al. 2012. Waves of retrotransposon expansion remodel genome organization and CTCF binding in multiple mammalian lineages. Cell 148:335-348.
45. Schroeder DI, et al. 2013. The human placenta methylome. Proc Natl Acad Sci U S A. 110:6037-6042.
46. Schwartz S, et al. 2003. Human-mouse alignments with BLASTZ. Genome Res. 13:103-107.
47. Shulha HP, et al. 2012 Human-specific histone methylation signatures at transcription start sites in prefrontal neurons. PLoS Biol. 10(11):e1001427.
48. Smith ZD, et al. 2014. DNA methylation dynamics of the human preimplantation embryo. Nature 511:611-615.
49. Somel M, et al. 2011. MicroRNA-driven developmental remodeling in the brain distinguishes humans fromother primates. PLoS Biol. 9:e1001214.
50. Sved J, Bird A. 1990.The expected equilibrium of the CpG dinucleotide in vertebrate genomes under a mutation model. Proc Natl Acad Sci U S A. 87:4692-4696.
51. Tavazoie S, Hughes JD, Campbell MJ, Cho RJ, Church GM. 1999. Systematic determination of genetic network architecture. Nat Genet. 22:281-285.
52. Tay SK, Blythe J, Lipovich L. 2009.Global discovery of primate-specific genes in the human genome. Proc Natl Acad Sci U S A. 106:12019-12024.
53. Toll-Riera M, et al. 2012. Origin of primate orphan genes: a comparative genomics approach. Mol Biol Evol. 26:603-612.
54. Venn O, et al. 2014. Nonhuman genetics. Strong male bias drives germline mutation in chimpanzees. Science 344:1272-1275.
55. Wang J, et al. 2012. Sequence features and chromatin structure around the genomic regions bound by 119 human transcription factors. Genome Res. 22:1798-1812.
56. Wang T, et al. 2007. Species-specific endogenous retroviruses shape the transcriptional network of the human tumor suppressor protein p53. Proc Natl Acad Sci U S A. 104:18613-18618.
57. Wissing S, et al. 2012. Reprogramming somatic cells into iPS cells activates LINE-1 retroelement mobility. Hum Mol Genet. 21:208-218.
58. Xie W, et al. 2013. Epigenomic analysis of multilineage differentiation of human embryonic stem cells. Cell 153:1134-1148.
59. Xu C, et al. 2012 Nanog-like regulates endoderm formation through the Mxtx2-Nodal pathway. Dev Cell. 22:625-638.
60. Yoder JA, Walsh CP, Bestor TH. 1997. Cytosine methylation and the ecology of intragenomic parasites. Trends Genet. 13:335-340.
61. Yu M, et al. 2012. Base-resolution analysis of 5-hydroxymethylcytosine in the mammalian genome. Cell 149:1368-1380.
62. Zemojtel T, et al. 2011. CpG deamination creates transcription factorbinding sites with high efficiency. Genome Biol Evol. 3:1304-1311.
63. Zemojtel T, Kielbasa SM, Arndt PF, Chung HR, Vingron M. 2009. Methylation and deamination of CpGs generate p53-binding sites on a genomic scale. Trends Genet. 25:63-66.
64. Zhang YE, Landback P, Vibranovski MD, Long M. 2011. Accelerated recruitment of new brain development genes into the human genome. PLoS Biol. 9:e1001179.