Massive contribution of transposable elements to mammalian regulatory sequences

Seminars in Cell and Developmental Biology

Volumn 57, Issue , 2016, Pages 51-56

  Rayan, Nirmala Arul ^a   del Rosario, Ricardo C H ^b   Prabhakar, Shyam ^a  

^a GENOME INSTITUTE OF SINGAPORE   (Singapore)

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

Author keywords

Primate specific; Regulatory elements; Transposable element functionalization; Transposons

Indexed keywords

DNA;

GENE CONTROL; GENE SEQUENCE; GENOME; GENOME-WIDE ASSOCIATION STUDY; HUMAN; HUMAN GENOME; NONHUMAN; PRIMATE; PROMOTER REGION; REVIEW; TRANSPOSON; ANIMAL; BIOLOGICAL MODEL; GENETICS; MAMMAL; PHYLOGENY; REGULATORY SEQUENCE;

ANIMALS; DNA TRANSPOSABLE ELEMENTS; GENOME; HUMANS; MAMMALS; MODELS, GENETIC; PHYLOGENY; REGULATORY SEQUENCES, NUCLEIC ACID;

EID: 84975507678     PISSN: 10849521     EISSN: 10963634     Source Type: Journal    
DOI: 10.1016/j.semcdb.2016.05.004     Document Type: Review

References (64)

1. [1] A.F.A. Smit, R. Hubley, P. Green, RepeatMasker at: http://repeatmasker.org.
2. [2] McClintock, B., Chromosome organization and genic expression. Cold Spring Harb. Symp. Quant. Biol. 16 (1951), 13–47.
3. [3] McClintock, B., Controlling elements and the gene. Cold Spring Harb. Symp. Quant. Biol. 21 (1956), 197–216.
4. [4] Britten, R.J., Davidson, E.H., Gene regulation for higher cells. A theory. Science 25 (1969), 349–357.
5. [5] Britten, R.J., Davidson, E.H., Repetitive and non-repetitive DNA sequences and a speculation on the origins of evolutionary novelty. Q. Rev. Biol. 46:2 (1971), 111–138.
6. [6] Ohno, S., So much junk DNA in our genome. Brookhaven Symp. Biol. 23 (1972), 366–370.
7. [7] Orgel, L.E., Crick, F.H.C., Selfish DNA: the ultimate parasite. Nature 284 (1980), 604–607.
8. [8] Doolittle, W.F., Sapienza, C., Selfish genes, the phenotype paradigm and genome evolution. Nature 284 (1980), 601–603.
9. [9] International Human Genome Sequencing Consortium, Initial sequencing and analysis of the human genome. Nature 409 (2001), 860–921.
10. [10] Mouse Genome Sequencing Consortium, Initial sequencing and comparative analysis of the mouse genome. Nature 420 (2002), 520–562.
11. [11] Silva, J.C., Shabalina, S.A., Harris, D.G., Spouge, J.L., Kondrashovi, A.S., Conserved fragments of transposable elements in intergenic regions: evidence for widespread recruitment of MIR- and L2-derived sequences within the mouse and human genomes. Genet. Res. 82 (2003), 1–18.
12. [12] Jordan, I.K., Rogozin, I.B., Glazko, G.V., Koonin, E.V., Origin of a substantial fraction of human regulatory sequences from transposable elements. Trends Genet. 19 (2003), 68–72.
13. [13] Kamal, M., Xie, X., Lander, E.S., A large family of ancient repeat elements in the human genome is under strong selection. Proc. Natl. Acad. Sci. U. S. A. 103 (2006), 2740–2745.
14. [14] Lowe, C.B., Bejerano, G., Haussler, D., Thousands of human mobile element fragments undergo strong purifying selection near developmental genes. Proc. Natl. Acad. Sci. U. S. A. 104:19 (2007), 8005–8010.
15. [15] Bejerano, G., Lowe, C.B., Ahituv, N., King, B., Siepel, A., Salama, S.R., Rubin, E.M., Kent, W.J., Haussler, D., A distal enhancer and an ultraconserved exon are derived from a novel retroposon. Nature 441:7089 (2006), 87–90.
16. [16] Santangelo, A.M., de Souza, F.S., Franchini, L.F., Bumaschny, V.F., Low, M.J., Rubinstein, M., Ancient exaptation of a CORE-SINE retroposon into a highly conserved mammalian neuronal enhancer of the proopiomelanocortin gene. PLoS Genet. 3 (2007), 1813–1826.
17. [17] Sasaki, T., Nishihara, H., Hirakawa, M., Fujimura, K., Tanaka, M., Kokubo, N., Kimura-Yoshida, C., Matsuo, I., Sumiyama, K., Saitou, N., et al. Possible involvement of SINEs in mammalian-specific brain formation. Proc. Natl. Acad. Sci. U. S. A. 105 (2008), 4220–4225.
18. [18] Mikkelsen, T.S., Wakefield, M.J., Aken, B., Amemiya, C.T., Chang, J.L., Duke, S., Garber, M., Gentles, A.J., Goodstadt, L., Heger, A., et al. Genome of the marsupial Monodelphis domestica reveals innovation in non-coding sequences. Nature 447:7141 (2007), 167–177.
19. [19] Gentles, A.J., Wakefield, M.J., Kohany, O., Gu, W., Batzer, M.A., Pollock, D.D., Jurka, J., Evolutionary dynamics of transposable elements in the short-tailed opossum Monodelphis domestica. Genome Res. 17:7 (2007), 992–1004.
20. [20] Lindblad-Toh, K., Garber, M., Zuk, O., Lin, M.F., Parker, B.J., Washietl, S., Kheradpour, P., Ernst, J., et al. A high-resolution map of human evolutionary constraint using 29 mammals. Nature 478:7370 (2011), 476–482.
21. [21] Kunarso, G., Chia, N.Y., Jeyakani, J., Hwang, C., Lu, X., Chan, Y.S., Ng, H.H., Bourque, G., Transposable elements have rewired the core regulatory network of human embryonic stem cells. Nat. Genet. 42:7 (2010), 631–634.
22. [22] Sundaram, V., Cheng, Y., Ma, Z., Li, D., Xing, X., Edge, P., Snyder, M.P., Wang, T., Widespread contribution of transposable elements to the innovation of gene regulatory networks. Genome Res. 24:12 (2014), 1963–1976.
23. [23] Schmidt, D., Schwalie, P.C., Wilson, M.D., Ballester, B., Gonçalves, A., Kutter, C., Brown, G.D., Marshall, A., Flicek, P., Odom, D.T., Waves of retrotransposon expansion remodel genome organization and CTCF binding in multiple mammalian lineages?. Cell 148:1-2 (2012), 335–348.
24. [24] Jacques, P.É., Jeyakani, J., Bourque, G., The majority of primate-specific regulatory sequences are derived from transposable elements. PLoS Genet., 9, 2013, e1003504.
25. [25] Kapusta, A., Kronenberg, Z., Lynch, V.J., Zhuo, X., Ramsay, L., Bourque, G., Yandell, M., Feschotte, C., Transposable elements are major contributors to the origin, diversification, and regulation of vertebrate long noncoding RNAs. PLoS Genet., 9(4), 2013, e1003470.
26. [26] Feschotte, C., Transposable elements and the evolution of regulatory networks. Nat. Rev. Genet. 9:5 (2008), 397–405.
27. [27] Feschotte, C., Gilbert, C., Endogenous viruses: insights into viral evolution and impact on host biology. Nat. Rev. Genet. 13 (2012), 283–296.
28. [28] Rebollo, R., Farivar, S., Mager, D.L., C-GATE: catalogue of genes affected by transposable elements. Mob. DNA, 3(9), 2012.
29. [29] Lynch, V.J., Leclerc, R.D., May, G., Wagner, G.P., Transposon-mediated rewiring of gene regulatory networks contributed to the evolution of pregnancy in mammals. Nat. Genet. 43 (2011), 1154–1159.
30. [30] Chuong, E.B., Rumi, M.A., Soares, M.J., Baker, J.C., Endogenous retroviruses function as species-specific enhancer elements in the placenta. Nat. Genet. 45 (2013), 325–329.
31. [31] del Rosario, R.C., Rayan, N.A., Prabhakar, S., Noncoding origins of anthropoid traits and a new null model of transposon functionalization. Genome Res. 24 (2014), 1469–1484.
32. [32] Wu, J., Grindlay, G.J., et al. Negative regulation of the human epsilon-globin gene by transcriptional interference: role of an Alu repetitive element. Mol. Cell. Biol. 10:3 (1990), 1209–1216.
33. [33] Samuelson, L.C., Wiebauer, K., Snow, C.M., Meisler, M.H., Retroviral and pseudogene insertion sites reveal the lineage of human salivary and pancreatic amylase genes from a single gene during primate evolution. Mol. Cell. Biol. 10:6 (1990), 2513–2520.
34. [34] Brini, A.T., Lee, G.M., Kinet, J.P., Involvement of Alu sequences in the cell-specific regulation of transcription of the gamma chain of Fc and T cell receptors. J. Biol. Chem. 268:2 (1993), 1355–1361.
35. [35] Hambor, J.E., Mennone, J., Coon, M.E., Hanke, J.H., Kavathas, P., Identification and characterization of an Alu-containing, T-cell-specific enhancer located in the last intron of the human CD8 alpha gene. Mol. Cell. Biol. 13:11 (1993), 7056–7070.
36. [36] Thorey, I.S., Cecena, G., Reynolds, W., Oshima, R.G., Alu sequence involvement in transcriptional insulation of the keratin 18 gene in transgenic mice. Mol. Cell. Biol. 13:11 (1993), 6742–6751.
37. [37] Vansant, G., Reynolds, W.F., The consensus sequence of a major Alu subfamily contains a functional retinoic acid response element. Proc. Natl. Acad. Sci. U. S. A. 92:18 (1995), 8229–8233.
38. [38] Laperriere, D., Wang, T.T., White, J.H., Mader, S., Widespread Alu repeat-driven expansion of consensus DR2 retinoic acid response elements during primate evolution. BMC Genom., 8, 2007, 23.
39. [39] Su, M., Han, D., Boyd-Kirkup, J., Yu, X., Han, J.D., Evolution of Alu elements toward enhancers. Cell Rep. 7:2 (2014), 376–385.
40. [40] Schulte, A.M., Lai, S., Kurtz, A., Czubayko, F., Riegel, A.T., Wellstein, A., Human trophoblast and choriocarcinoma expression of the growth factor pleiotrophin attributable to germ-line insertion of an endogenous retrovirus. Proc. Natl. Acad. Sci. U. S. A. 93:25 (1996), 14759–14764.
41. [41] Ramsey, E.M., Houston, M.L., Harris, J.W., Interactions of the trophoblast and maternal tissues in three closely related primate species. Am. J. Obstet. Gynecol. 124:6 (1976), 647–652.
42. [42] Carter, A.M., Pijnenborg, R., Evolution of invasive placentation with special reference to non-human primates. Best Pract. Res. Clin. Obstet. 25:3 (2011), 249–257.
43. [43] Cohen, C.J., Lock, W.M., Mager, D.L., Endogenous retroviral LTRs as promoters for human genes: a critical assessment. Gene 448:2 (2009), 105–114.
44. [44] Hewitt, S.M., Fraizer, G.C., Saunders, G.F., Transcriptional silencer of the Wilms’ tumor gene WT1 contains an Alu repeat. J. Biol. Chem. 270:30 (1995), 17908–17912.
45. [45] Fornasari, D., Battaglioli, E., Flora, A., Terzano, S., Clementi, F., Structural and functional characterization of the human a3 nicotinic subunit gene promoter. Mol. Pharmacol. 51 (1997), 250–261.
46. [46] Medstrand, P., Landry, J.R., Mager, D.L., Long terminal repeats are used as alternative promoters for the endothelin B receptor and apolipoprotein C-I genes in humans. J. Biol. Chem. 276 (2001), 1896–1903.
47. [47] Landry, J.R., Rouhi, A., Medstrand, P., Mager, D.L., The Opitz syndrome gene MID1 is transcribed from a human endogenous retroviral promoter. Mol. Biol. Evol. 19 (2002), 1934–1942.
48. [48] Le Goff, W., Guerin, M., Chapman, M.J., Thillet, J., A CPF site and ALU repeat in the distal promoter region are implicated in regulation of human CETP gene expression. J. Lipid Res., 16, 2003, 16.
49. [49] Gombart, A.F., Borregaard, N., Koeffler, H.P., Human cathelicidin antimicrobial peptide (CAMP) gene is a direct target of the vitamin D receptor and is strongly up-regulated in myeloid cells by 1,25-dihydroxyvitamin D3. FASEB J. 19:9 (2005), 1067–1077.
50. [50] Huh, J.W., Kim, Y.H., Lee, S.R., Kim, H., Kim, D.S., Kim, H.S., Kang, H.S., Chang, K.T., Gain of new exons and promoters by lineage-specific transposable elements-integration and conservation event on CHRM3 gene. Mol. Cells 28:2 (2009), 111–117.
51. [51] Pi, W., Zhu, X., Wu, M., Wang, Y., Fulzele, S., Eroglu, A., Ling, J., Tuan, D., Long-range function of an intergenic retrotransposon. Proc. Natl. Acad. Sci. U. S. A. 107:29 (2010), 12992–12997.
52. [52] Emera, D., Casola, C., Lynch, V.J., Wildman, D.E., Agnew, D., Wagner, G.P., Convergent evolution of endometrial prolactin expression in primates, mice, and elephants through the independent recruitment of transposable elements. Mol. Biol. Evol. 29:1 (2012), 239–247.
53. [53] Contente, A., Zischler, H., Einspanier, A., Dobbelstein, M., A promoter that acquired p53 responsiveness during primate evolution. Cancer Res. 63:8 (2003), 1756–1758.
54. [54] Wang, T., Zeng, J., Lowe, C.B., Sellers, R.G., Salama, S.R., Yang, M., Burgess, S.M., Brachmann, R.K., Haussler, D., Species-specific endogenous retroviruses shape the transcriptional network of the human tumor suppressor protein p53. Proc. Natl. Acad. Sci. U. S. A. 104:47 (2007), 18613–18618.
55. [55] Eddy, S.R., The C-value paradox, junk DNA and ENCODE. Curr. Biol. 22:21 (2012), R898–899.
56. [56] Niu, D.K., Jiang, L., Can ENCODE tell us how much junk DNA we carry in our genome?. Biochem. Biophys. Res. Commun. 430:4 (2013), 1340–1343.
57. [57] Doolittle, W.F., Is junk DNA bunk? a critique of ENCODE. Proc. Natl. Acad. Sci. U. S. A. 110:14 (2013), 5294–5300.
58. [58] de Souza, F.S., Franchini, L.F., Rubinstein, M., Exaptation of transposable elements into novel cis-regulatory elements: is the evidence always strong?. Mol. Biol. Evol. 30:6 (2013), 1239–1251.
59. [59] Cowley, M., Oakey, R.J., Transposable elements re-wire and fine-tune the transcriptome. PLoS Genet., 9(1), 2013, e1003234.
60. [60] Le, T.N., Miyazaki, Y., Takuno, S., Saze, H., Epigenetic regulation of intragenic transposable elements impacts gene transcription in Arabidopsis thaliana. Nucleic Acids Res. 43:8 (2015), 3911–3921.
61. [61] Shapiro, E., Biezuner, T., Linnarsson, S., Single-cell sequencing-based technologies will revolutionize whole-organism science. Nat. Rev. Genet. 14:9 (2013), 618–630.
62. [62] Singer, T., McConnell, M.J., Marchetto, M.C., Coufal, N.G., Gage, F.H., LINE-1 retrotransposons: mediators of somatic variation in neuronal genomes?. Trends Neurosci. 33:8 (2010), 345–354.
63. [63] Kazazian, H.H. Jr., Wong, C., Youssoufian, H., Scott, A.F., Phillips, D.G., Antonarakis, S.E., Haemophilia A resulting from de novo insertion of L1 sequences represents a novel mechanism for mutation in man. Nature 332 (1988), 164–166.
64. [64] Ward, M.C., Wilson, M.D., Barbosa-Morais, N.L., Schmidt, D., Stark, R., Pan, Q., Schwalie, P.C., Menon, S., Lukk, M., Watt, S., et al. Latent regulatory potential of human-specific repetitive elements. Mol. Cell 49:2 (2013), 262–272.