Transposable elements and the evolution of regulatory networks (original) (raw)
Britten, R. J. & Kohne, D. E. Repeated sequences in DNA. Hundreds of thousands of copies of DNA sequences have been incorporated into the genomes of higher organisms. Science161, 529–540 (1968). CASPubMed Google Scholar
Wicker, T. et al. A unified classification system for eukaryotic transposable elements. Nature Rev. Genet.8, 973–982 (2007). ArticleCASPubMed Google Scholar
Brookfield, J. F. The ecology of the genome — mobile DNA elements and their hosts. Nature Rev. Genet.6, 128–136 (2005). ArticleCASPubMed Google Scholar
Kidwell, M. G. & Lisch, D. R. Perspective: transposable elements, parasitic DNA, and genome evolution. Evolution Int. J. Org. Evolution55, 1–24 (2001). ArticleCAS Google Scholar
Deininger, P. L., Moran, J. V., Batzer, M. A. & Kazazian, H. H. Jr. Mobile elements and mammalian genome evolution. Curr. Opin. Genet. Dev.13, 651–658 (2003). ArticleCASPubMed Google Scholar
Gould, S. J. & Vrba, E. S. Exaptation — a missing term in the science of form. Paleobiology8, 4–15 (1983). Article Google Scholar
Britten, R. J. Cases of ancient mobile element DNA insertions that now affect gene regulation. Mol. Phylogenet. Evol.5, 13–17 (1996). ArticleCASPubMed Google Scholar
Miller, W. J., McDonald, J. F., Nouaud, D. & Anxolabehere, D. Molecular domestication — more than a sporadic episode in evolution. Genetica107, 197–207 (1999). ArticleCASPubMed Google Scholar
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, 1–18 (2003). ArticleCASPubMed Google Scholar
Lowe, C. B., Bejerano, G. & Haussler, D. Thousands of human mobile element fragments undergo strong purifying selection near developmental genes. Proc. Natl Acad. Sci. USA104, 8005–8010 (2007). ArticleCASPubMedPubMed Central Google Scholar
Mikkelsen, T. S. et al. Genome of the marsupial Monodelphis domestica reveals innovation in non-coding sequences. Nature447, 167–177 (2007). ArticleCASPubMed Google Scholar
Bejerano, G., Haussler, D. & Blanchette, M. Into the heart of darkness: large-scale clustering of human non-coding DNA. Bioinformatics20 (Suppl. 1), i40–i48 (2004). ArticleCASPubMed Google Scholar
Xie, X., Kamal, M. & Lander, E. S. A family of conserved noncoding elements derived from an ancient transposable element. Proc. Natl Acad. Sci. USA103, 11659–11664 (2006). ArticleCASPubMedPubMed Central Google Scholar
Bejerano, G. et al. A distal enhancer and an ultraconserved exon are derived from a novel retroposon. Nature441, 87–90 (2006). ArticleCASPubMed Google Scholar
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. USA103, 2740–2745 (2006). ArticleCASPubMedPubMed Central Google Scholar
Nishihara, H., Smit, A. F. & Okada, N. Functional noncoding sequences derived from SINEs in the mammalian genome. Genome Res.16, 864–874 (2006). ArticleCASPubMedPubMed Central Google Scholar
Santangelo, A. M. et al. Ancient exaptation of a CORE-SINE retroposon into a highly conserved mammalian neuronal enhancer of the proopiomelanocortin gene. PLoS Genet.3, 1813–1826 (2007). ArticleCASPubMed Google Scholar
Maside, X., Bartolome, C. & Charlesworth, B. S-element insertions are associated with the evolution of the HSP70 genes in Drosophila melanogaster. Curr. Biol.12, 1686–1691 (2002). ArticleCASPubMed Google Scholar
Schlenke, T. A. & Begun, D. J. Strong selective sweep associated with a transposon insertion in Drosophila simulans. Proc. Natl Acad. Sci. USA101, 1626–1631 (2004). ArticleCASPubMedPubMed Central Google Scholar
Chung, H. et al. _Cis_-regulatory elements in the Accord retrotransposon result in tissue-specific expression of the Drosophila melanogaster insecticide resistance gene Cyp6g1. Genetics175, 1071–1077 (2007). ArticleCASPubMedPubMed Central Google Scholar
Brosius, J. The contribution of RNAs and retroposition to evolutionary novelties. Genetica118, 99–116 (2003). ArticleCASPubMed Google Scholar
Marino-Ramirez, L., Lewis, K. C., Landsman, D. & Jordan, I. K. Transposable elements donate lineage-specific regulatory sequences to host genomes. Cytogenet. Genome Res.110, 333–341 (2005). ArticleCASPubMed Google Scholar
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, 68–72 (2003). ArticleCASPubMed Google Scholar
van de Lagemaat, L. N., Landry, J. R., Mager, D. L. & Medstrand, P. Transposable elements in mammals promote regulatory variation and diversification of genes with specialized functions. Trends Genet.19, 530–536 (2003). ArticleCASPubMed Google Scholar
Marino-Ramirez, L. & Jordan, I. K. Transposable element derived DNaseI-hypersensitive sites in the human genome. Biol. Direct1, 20 (2006). ArticlePubMedPubMed CentralCAS Google Scholar
Gentles, A. J. et al. Evolutionary dynamics of transposable elements in the short-tailed opossum Monodelphis domestica. Genome Res.17, 992–1004 (2007). ArticleCASPubMedPubMed Central Google Scholar
Ni, J. Z. et al. Ultraconserved elements are associated with homeostatic control of splicing regulators by alternative splicing and nonsense-mediated decay. Genes Dev.21, 708–718 (2007). ArticleCASPubMedPubMed Central Google Scholar
Wray, G. A. et al. The evolution of transcriptional regulation in eukaryotes. Mol. Biol. Evol.20, 1377–1419 (2003). ArticleCASPubMed Google Scholar
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, 7056–7070 (1993). ArticleCASPubMedPubMed Central Google Scholar
Zhou, Y. H., Zheng, J. B., Gu, X., Saunders, G. F. & Yung, W. K. Novel PAX6 binding sites in the human genome and the role of repetitive elements in the evolution of gene regulation. Genome Res.12, 1716–1722 (2002). ArticleCASPubMedPubMed Central Google Scholar
Medstrand, P. et al. Impact of transposable elements on the evolution of mammalian gene regulation. Cytogenet. Genome Res.110, 342–352 (2005). ArticleCASPubMed Google Scholar
Thornburg, B. G., Gotea, V. & Makalowski, W. Transposable elements as a significant source of transcription regulating signals. Gene365, 104–110 (2006). ArticleCASPubMed Google Scholar
Polak, P. & Domany, E. Alu elements contain many binding sites for transcription factors and may play a role in regulation of developmental processes. BMC Genomics7, 133 (2006). ArticlePubMedPubMed CentralCAS Google Scholar
Johnson, R. et al. Identification of the REST regulon reveals extensive transposable element-mediated binding site duplication. Nucleic Acids Res.34, 3862–3877 (2006). ArticleCASPubMedPubMed Central Google Scholar
Wang, T. et al. Species-specific endogenous retroviruses shape the transcriptional network of the human tumor suppressor protein p53. Proc. Natl Acad. Sci. USA104, 18613–18618 (2007). ArticleCASPubMedPubMed Central Google Scholar
Wessler, S. R., Bureau, T. E. & White, S. E. LTR-retrotransposons and MITEs: important players in the evolution of plant genomes. Curr. Opin. Genet. Dev.5, 814–821 (1995). ArticleCASPubMed Google Scholar
Ferrigno, O. et al. Transposable B2 SINE elements can provide mobile RNA polymerase II promoters. Nature Genet.28, 77–81 (2001). CASPubMed Google Scholar
Romanish, M. T., Lock, W. M., van de Lagemaat, L. N., Dunn, C. A. & Mager, D. L. Repeated recruitment of LTR retrotransposons as promoters by the anti-apoptotic locus NAIP during mammalian evolution. PLoS Genet.3, e10 (2007). ArticlePubMedPubMed CentralCAS Google Scholar
Borchert, G. M., Lanier, W. & Davidson, B. L. RNA polymerase III transcribes human microRNAs. Nature Struct. Mol. Biol.13, 1097–1101 (2006). ArticleCAS Google Scholar
Britten, R. J. & Davidson, E. H. Gene regulation for higher cells: a theory. Science165, 349–357 (1969). ArticleCASPubMed Google Scholar
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, 111–138 (1971). ArticleCASPubMed Google Scholar
Peaston, A. E. et al. Retrotransposons regulate host genes in mouse oocytes and preimplantation embryos. Dev. Cell7, 597–606 (2004). ArticleCASPubMed Google Scholar
Bringaud, F. et al. Members of a large retroposon family are determinants of post-transcriptional gene expression in Leishmania. PLoS Pathog.3, 1291–1307 (2007). ArticleCASPubMed Google Scholar
Wilkins, A. S. The Evolution of Developmental Pathways (Sinauer, Sunderland, Massachusetts, 2002). Google Scholar
Davidson, E. H. The Regulatory Genome: Gene Regulatory Networks in Development and Evolution (Academic, New York, 2006). Google Scholar
Mattick, J. S. A new paradigm for developmental biology. J. Exp. Biol.210, 1526–1547 (2007). ArticlePubMed Google Scholar
Chen, K. & Rajewsky, N. The evolution of gene regulation by transcription factors and microRNAs. Nature Rev. Genet.8, 93–103 (2007). ArticleCASPubMed Google Scholar
Slotkin, R. K. & Martienssen, R. Transposable elements and the epigenetic regulation of the genome. Nature Rev. Genet.8, 272–285 (2007). ArticleCASPubMed Google Scholar
Aravin, A. A., Hannon, G. J. & Brennecke, J. The Piwi-piRNA pathway provides an adaptive defense in the transposon arms race. Science318, 761–764 (2007). ArticleCASPubMed Google Scholar
He, L. & Hannon, G. J. MicroRNAs: small RNAs with a big role in gene regulation. Nature Rev. Genet.5, 522–531 (2004). ArticleCASPubMed Google Scholar
Smalheiser, N. R. & Torvik, V. I. Mammalian microRNAs derived from genomic repeats. Trends Genet.21, 322–326 (2005). ArticleCASPubMed Google Scholar
Piriyapongsa, J., Marino-Ramirez, L. & Jordan, I. K. Origin and evolution of human microRNAs from transposable elements. Genetics176, 1323–1337 (2007). ArticleCASPubMedPubMed Central Google Scholar
Smalheiser, N. R. & Torvik, V. I. Alu elements within human mRNAs are probable microRNA targets. Trends Genet.22, 532–536 (2006). ArticleCASPubMed Google Scholar
Feschotte, C., Jiang, N. & Wessler, S. R. Plant transposable elements: where genetics meets genomics. Nature Rev. Genet.3, 329–341 (2002). ArticleCASPubMed Google Scholar
Sijen, T. & Plasterk, R. H. Transposon silencing in the Caenorhabditis elegans germ line by natural RNAi. Nature426, 310–314 (2003). ArticleCASPubMed Google Scholar
Piriyapongsa, J. & Jordan, I. K. A family of human microRNA genes from miniature inverted-repeat transposable elements. PLoS ONE2, e203 (2007). ArticlePubMedPubMed CentralCAS Google Scholar
Levine, M. & Tjian, R. Transcription regulation and animal diversity. Nature424, 147–151 (2003). ArticleCASPubMed Google Scholar
Volff, J. N. Turning junk into gold: domestication of transposable elements and the creation of new genes in eukaryotes. Bioessays28, 913–922 (2006). ArticleCASPubMed Google Scholar
Lander, E. S. et al. Initial sequencing and analysis of the human genome. Nature409, 860–921 (2001). ArticleCASPubMed Google Scholar
Pace, J. K. & Feschotte, C. The evolutionary history of human DNA transposons: evidence for intense activity in the primate lineage. Genome Res.17, 422–432 (2007). ArticleCASPubMedPubMed Central Google Scholar
Zdobnov, E. M., Campillos, M., Harrington, E. D., Torrents, D. & Bork, P. Protein coding potential of retroviruses and other transposable elements in vertebrate genomes. Nucleic Acids Res.33, 946–954 (2005). ArticleCASPubMedPubMed Central Google Scholar
Casola, C., Lawing, A. M., Betran, E. & Feschotte, C. _PIF_-like transposons are common in Drosophila and have been repeatedly domesticated to generate new host genes. Mol. Biol. Evol.24, 1872–1888 (2007). ArticleCASPubMed Google Scholar
Campillos, M., Doerks, T., Shah, P. K. & Bork, P. Computational characterization of multiple _gag_-like human proteins. Trends Genet.22, 585–589 (2006). ArticleCASPubMed Google Scholar
Muehlbauer, G. J. et al. A hAT superfamily transposase recruited by the cereal grass genome. Mol. Genet. Genomics275, 553–563 (2006). ArticleCASPubMed Google Scholar
Craig, N. L., Craigie, R., Gellert, M. & Lambowitz, A. M. Mobile DNA II, (American Society for Microbiology, Washington, 2002). Book Google Scholar
Makarova, K. S., Aravind, L. & Koonin, E. V. SWIM, a novel Zn-chelating domain present in bacteria, archaea and eukaryotes. Trends Biochem. Sci.27, 384–386 (2002). ArticleCASPubMed Google Scholar
Ros, F. & Kunze, R. Regulation of activator/dissociation transposition by replication and DNA methylation. Genetics157, 1723–1733 (2001). CASPubMedPubMed Central Google Scholar
Aravind, L. The BED finger, a novel DNA-binding domain in chromatin-boundary-element-binding proteins and transposases. Trends Biochem. Sci.25, 421–423 (2000). ArticleCASPubMed Google Scholar
Siegmund, T. & Lehmann, M. The Drosophila Pipsqueak protein defines a new family of helix-turn-helix DNA-binding proteins. Dev. Genes Evol.212, 152–157 (2002). ArticleCASPubMed Google Scholar
Roussigne, M. et al. The THAP domain: a novel protein motif with similarity to the DNA-binding domain of P element transposase. Trends Biochem. Sci.28, 66–69 (2003). ArticleCASPubMed Google Scholar
Kapitonov, V. V. & Jurka, J. Harbinger transposons and an ancient HARBI1 gene derived from a transposase. DNA Cell Biol.23, 311–324 (2004). ArticleCASPubMed Google Scholar
Babu, M. M., Iyer, L. M., Balaji, S. & Aravind, L. The natural history of the WRKY-GCM1 zinc fingers and the relationship between transcription factors and transposons. Nucleic Acids Res.34, 6505–6520 (2006). ArticleCASPubMedPubMed Central Google Scholar
Tudor, M., Lobocka, M., Goodwell, M., Pettitt, J. & O'Hare, K. The pogo transposable element family of Drosophila melanogaster. Mol. Gen. Genet.232, 126–134 (1992). ArticleCASPubMed Google Scholar
Franz, G., Loukeris, T. G., Dialektaki, G., Thompson, C. R. & Savakis, C. Mobile Minos elements from Drosophila hydei encode a two-exon transposase with similarity to the paired DNA-binding domain. Proc. Natl Acad. Sci. USA91, 4746–4750 (1994). ArticleCASPubMedPubMed Central Google Scholar
Breitling, R. & Gerber, J. K. Origin of the paired domain. Dev. Genes Evol.210, 644–650 (2000). ArticleCASPubMed Google Scholar
Quesneville, H., Nouaud, D. & Anxolabehere, D. Recurrent recruitment of the THAP DNA-binding domain and molecular domestication of the P-transposable element. Mol. Biol. Evol.22, 741–746 (2005). ArticleCASPubMed Google Scholar
Casola, C., Hucks, D. & Feschotte, C. Convergent domestication of _pogo_-like transposases into centromere-binding proteins in fission yeast and mammals. Mol. Biol. Evol., 25, 29–41 (2008). ArticleCASPubMed Google Scholar
Piriyapongsa, J., Rutledge, M. T., Patel, S., Borodovsky, M. & Jordan, I. K. Evaluating the protein coding potential of exonized transposable element sequences. Biol. Direct2, 31 (2007). ArticlePubMedPubMed CentralCAS Google Scholar
Cowan, R. K., Hoen, D. R., Schoen, D. J. & Bureau, T. E. MUSTANG is a novel family of domesticated transposase genes found in diverse angiosperms. Mol. Biol. Evol.22, 2084–2089 (2005). ArticleCASPubMed Google Scholar
Cordaux, R., Udit, S., Batzer, M. A. & Feschotte, C. Birth of a chimeric primate gene by capture of the transposase gene from a mobile element. Proc. Natl Acad. Sci. USA103, 8101–8106 (2006). ArticleCASPubMedPubMed Central Google Scholar
Liu, D. et al. The human SETMAR protein preserves most of the activities of the ancestral Hsmar1 transposase. Mol. Cell Biol.27, 1125–1132 (2007). ArticlePubMedCAS Google Scholar
Miskey, C. et al. The ancient mariner sails again: transposition of the human Hsmar1 element by a reconstructed transposase and activities of the SETMAR protein on transposon ends. Mol. Cell Biol.27, 4589–4600 (2007). ArticleCASPubMedPubMed Central Google Scholar
Pathak, R. U., Rangaraj, N., Kallappagoudar, S., Mishra, K. & Mishra, R. K. Boundary element-associated factor 32B connects chromatin domains to the nuclear matrix. Mol. Cell Biol.27, 4796–4806 (2007). ArticleCASPubMedPubMed Central Google Scholar
Cam, H. P., Noma, K. I., Ebina, H., Levin, H. L. & Grewal, S. I. Host genome surveillance for retrotransposons by transposon-derived proteins. Nature451, 431–436 (2008). ArticleCASPubMed Google Scholar
Hudson, M. E., Lisch, D. R. & Quail, P. H. The FHY3 and FAR1 genes encode transposase-related proteins involved in regulation of gene expression by the phytochrome A-signaling pathway. Plant J.34, 453–471 (2003). ArticleCASPubMed Google Scholar
Raizada, M. N., Brewer, K. V. & Walbot, V. A maize MuDR transposon promoter shows limited autoregulation. Mol. Genet. Genomics265, 82–94 (2001). ArticleCASPubMed Google Scholar
Cui, H. & Fedoroff, N. V. Inducible DNA demethylation mediated by the maize Suppressor-mutator transposon-encoded TnpA protein. Plant Cell14, 2883–2899 (2002). ArticleCASPubMedPubMed Central Google Scholar
Atkinson, P. W., Warren, W. D. & O'Brochta, D. A. The hobo transposable element of Drosophila can be cross-mobilized in houseflies and excises like the Ac element of maize. Proc. Natl Acad. Sci. USA90, 9693–9697 (1993). ArticleCASPubMedPubMed Central Google Scholar
Rezsohazy, R., van Luenen, H. G. A. M., Durbin, R. M. & Plasterk, R. H. A. Tc_7_, a _Tc1_-hitch hiking transposon in Caenorhabditis elegans. Nucleic Acids Res.25, 4048–4054 (1997). ArticleCASPubMedPubMed Central Google Scholar
Lampe, D. J., Walden, K. K. & Robertson, H. M. Loss of transposase–DNA interaction may underlie the divergence of mariner family transposable elements and the ability of more than one mariner to occupy the same genome. Mol. Biol. Evol.18, 954–961 (2001). ArticleCASPubMed Google Scholar
Feschotte, C., Osterlund, M. T., Peeler, R. & Wessler, S. R. DNA-binding specificity of rice _mariner_-like transposases and interactions with Stowaway MITEs. Nucleic Acids Res.33, 2153–2165 (2005). ArticleCASPubMedPubMed Central Google Scholar
Wallace, M. R. et al. A de novo Alu insertion results in neurofibromatosis type 1. Nature353, 864–866 (1991). ArticleCASPubMed Google Scholar
Girard, L. & Freeling, M. Regulatory changes as a consequence of transposon insertion. Dev. Genet.25, 291–296 (1999). ArticleCASPubMed Google Scholar
Simons, C., Pheasant, M., Makunin, I. V. & Mattick, J. S. Transposon-free regions in mammalian genomes. Genome Res.16, 164–172 (2006). ArticleCASPubMedPubMed Central Google Scholar
Lerman, D. N. & Feder, M. E. Naturally occurring transposable elements disrupt hsp70 promoter function in Drosophila melanogaster. Mol. Biol. Evol.22, 776–783 (2005). ArticleCASPubMed Google Scholar
Walser, J. C., Chen, B. & Feder, M. E. Heat-shock promoters: targets for evolution by P transposable elements in Drosophila. PLoS Genet.2, e165 (2006). ArticlePubMedPubMed CentralCAS Google Scholar
Ackerman, H., Udalova, I., Hull, J. & Kwiatkowski, D. Evolution of a polymorphic regulatory element in interferon-gamma through transposition and mutation. Mol. Biol. Evol.19, 884–890 (2002). ArticleCASPubMed Google Scholar
Martin, C. & Lister, C. Genome juggling by transposons: Tam3-induced rearrangements in Antirrhinum majus. Dev. Genet.10, 438–451 (1989). ArticleCASPubMed Google Scholar
Koga, A., Iida, A., Hori, H., Shimada, A. & Shima, A. Vertebrate DNA transposon as a natural mutator: the medaka fish Tol2 element contributes to genetic variation without recognizable traces. Mol. Biol. Evol.23, 1414–1419 (2006). ArticleCASPubMed Google Scholar