Journal of Life Science (생명과학회지)

Korean Society of Life Science (한국생명과학회)
권호 표지
DOI QR코드

DOI QR Code

Biological Function and Structure of Transposable Elements

이동성 유전인자의 구조 및 생물학적 기능

  • Kim, So-Won (Department of Biological Sciences, College of Natural Sciences, Pusan National University) ;
  • Kim, Woo Ryung (Department of Biological Sciences, College of Natural Sciences, Pusan National University) ;
  • Kim, Heui-Soo (Department of Biological Sciences, College of Natural Sciences, Pusan National University)
  • Received : 2019.08.15
  • Accepted : 2019.09.19
  • Published : 2019.09.30
Download PDF
⟨ Previous Next ⟩

Abstract

Transposable elements (TEs) occupy approximately 45% of the human genome and can enter functional genes randomly. During evolutionary radiation, multiple copies of TEs are produced by duplication events. Those elements contribute to biodiversity and phylogenomics. Most of them are controlled by epigenetic regulation, such as methylation or acetylation. Every species contains their own specific mobile elements, and they are divided into DNA transposons and retrotransposons. Retrotransposons can be divided by the presence of a long terminal repeat (LTR). They show various biological functions, such as promoter, enhancer, exonization, rearrangement, and alternative splicing. Also, they are strongly implicated to genomic instability, causing various diseases. Therefore, they could be used as biomarkers for the diagnosis and prognosis of diseases such as cancers. Recently, it was found that TEs could produce miRNAs, which play roles in gene inhibition through mRNA cleavage or translational repression, binding seed regions of target genes. Studies of TE-derived miRNAs offer a potential for the expression of functional genes. Comparative analyses of different types of miRNAs in various species and tissues could be of interest in the fields of evolution and phylogeny. Those events allow us to understand the importance of TEs in relation to biological roles and various diseases.

이동성 유전인자는 인간 유전체의 45%를 차지하며 기능성 유전자 내부로 자유롭게 들어갈 수 있다. 이들은 진화과정에서 중복현상으로 다수의 복사수로 생성되며, 생물종다양성 및 계통유전체학 분야에 기여한다. 이동성 유전인자의 대부분은 메틸화 또는 아세틸화 현상과 같은 후성유전학적 조절에 의해 제어된다. 다양한 생물종은 그들만의 고유의 이동성 유전인자를 가지고 있으며, 일반적으로 DNA트란스포존과 레트로트란스포존으로 나뉜다. 레트로트란스포존은 LTR의 유무에 따라 다시 HERV와 LINE으로 구분된다. 이동성 유전인자는 프로모터, 인핸서, 엑손화, 재배열 및 선택적 스플라이싱과 같은 다양한 생물학적 기능을 수행한다. 또한 이들은 유전체의 불안정성을 야기시켜 다양한 질병을 유발하기도 한다. 따라서, 암과 같은 질병을 진단하는 바이오 마커로 사용될 수 있다. 최근, 이동성 유전인자는 miRNA를 만들어 내는 것으로 밝혀졌으며, 이러한 miRNA는 타겟 유전자의 seed 영역에 결합함으로서 mRNA의 분해 및 번역을 억제하는 역할을 수행한다. 이동성 유전인자 유래의 miRNA는 기능성 유전자의 발현에 큰 영향을 미친다. 다양한 생물종과 조직에서 서로 다른 miRNA의 비교 분석 연구는 생물학적 기능과 관련하여 진화학과 계통학 영역에서 흥미 있는 연구 분야라 할 수 있겠다.

Keywords

References

  1. Ahmed, M. and Liang, P. 2012. Transposable elements are a significant contributor to tandem repeats in the human genome. Comp. Funct. Genomics 2012, 1-8. https://doi.org/10.1155/2012/947089
  2. Ardeljan, D., Taylor, M. S., Ting, D. T. and Burns, K. H. 2017. The human long interspersed element-1 retrotransposon: an emerging biomarker of neoplasia. Clin. Chem. 63, 816-822. https://doi.org/10.1373/clinchem.2016.257444
  3. Bekpen, C., Xavier, R. J. and Eichler, E. E. 2010. "Human IRGM gene "to be or not to be". Semin. Immunopathol. 32., 437-444. https://doi.org/10.1007/s00281-010-0224-x
  4. Bennett, E. A., Coleman, L. E., Tsui, C., Pittard, W. S. and Devine, S. E. 2004. Natural genetic variation caused by transposable elements in humans. Genetics 168, 933-951. https://doi.org/10.1534/genetics.104.031757
  5. Bennetzen, J. L. and Wang, H. 2014. The contributions of transposable elements to the structure, function, and evolution of plant genomes. Annu. Rev. Plant. Biol. 65, 505-530. https://doi.org/10.1146/annurev-arplant-050213-035811
  6. Blumenstiel, J. P. 2019. Birth, school, work, death, and resurrection: The life stages and dynamics of transposable element proliferation. Genes (Basel) 10, 1-14. https://doi.org/10.3390/genes10010001
  7. Boeke, J. D. 1997. LINEs and Alus: the polyA connection. Nat. Genet. 16, 6-7. https://doi.org/10.1038/ng0597-6
  8. Bourque, G., Burns, K. H., Gehring, M., Gorbunova, V., Seluanov, A., Hammell, M., Imbeault, M., Izsvák, Z., Levin, H. L., Macfarlan, T. S., Mager, D. L. and Feschotte, C. 2018. Ten things you should know about transposable elements. Genome Biol. 19, 1-12. https://doi.org/10.1186/s13059-017-1381-1
  9. Burns, K. H. 2017. Transposable elements in cancer. Nat. Rev. Cancer 17, 415-424. https://doi.org/10.1038/nrc.2017.35
  10. Callinan, P. A. and Batzer, M. A. 2006. Retrotransposable elements and human disease. Genome Dyn. 1, 104-115. https://doi.org/10.1159/000092503
  11. Carter, A. B., Salem, A. H., Hedges, D. J., Keegan, C. N., Kimball, B., Walker, J. A., Watkins, W. S., Jorde, L. B. and Batzer, M. A. 2004. Genome-wide analysis of the human Alu Yb-lineage. Hum. Genomics 1, 167-178. https://doi.org/10.1186/1479-7364-1-3-167
  12. Chiappinelli, K. B., Strissel, P. L., Desrichard, A., Li, H., Henke, C., Akman, B., Hein, A., Rote, N. S., Cope, L. M., Snyder, A., Makarov, V., Budhu, S., Slamon, D. J., Wolchok, J. D., Pardoll, D. M., Beckmann, M. W., Zahnow, C. A., Merghoub, T., Chan, T. A., Baylin, S. B. and Strick, R. 2015. Inhibiting DNA methylation causes an interferon response in cancer via dsRNA including endogenous retroviruses. Cell 162, 974-986. https://doi.org/10.1016/j.cell.2015.07.011
  13. Chien, T. Y., Liu, L. Y. and Charng, Y. C. 2013. Analysis of new functional profiles of protein isoforms yielded by ds exonization in rice. Evol. Bioinform. Online 9, 417-427. https://doi.org/10.4137/EBO.S12757
  14. Clayton, E. A., Wang, L., Rishishwar, L., Wang, J., McDonald, J. F. and Jordan, I. K. 2016. Patterns of transposable element expression and insertion in cancer. Front. Mol. Biosci. 3, 1-11.
  15. Cordaux, R. and Batzer, M. A. 2009. The impact of retrotransposons on human genome evolution. Nat. Rev. Genet. 10, 691-703. https://doi.org/10.1038/nrg2640
  16. Dewannieux, M., Esnault, C. and Heidmann, T. 2003. LINEmediated retrotransposition of marked Alu sequences. Nat. Genet. 35, 41-48. https://doi.org/10.1038/ng1223
  17. Domansky, A. N., Kopantzev, E. P., Snezhkov, E. V., Lebedev, Y. B., Leib-Mosch, C. and Sverdlov, E. D. 2000. Solitary HERV-K LTRs possess bi-directional promoter activity and contain a negative regulatory element in the U5 region. FEBS Lett. 472, 191-195. https://doi.org/10.1016/S0014-5793(00)01460-5
  18. Dupressoir, A., Lavialle, C. and Heidmann, T. 2012. From ancestral infectious retroviruses to bona fide cellular genes: role of the captured syncytins in placentation. Placenta 33, 663-671. https://doi.org/10.1016/j.placenta.2012.05.005
  19. Faustino, N. A. and Cooper, T. A. 2003. Pre-mRNA splicing and human disease. Genes Dev. 17, 419-437. https://doi.org/10.1101/gad.1048803
  20. Feschotte, C. 2008. Transposable elements and the evolution of regulatory networks. Nat. Rev. Genet. 9, 397-405. https://doi.org/10.1038/nrg2337
  21. Furano, A. V. 2000. The biological properties and evolutionary dynamics of mammalian LINE-1 retrotransposons. Prog. Nucleic Acid Res. Mol. Biol. 64, 255-294. https://doi.org/10.1016/S0079-6603(00)64007-2
  22. Ge, S. X. 2017. Exploratory bioinformatics investigation reveals importance of "junk" DNA in early embryo development. BMC Genomics 18, 1-19. https://doi.org/10.1186/s12864-016-3406-7
  23. Gentles, A. J., Wakefield, M. J., Kohany, O., Gu, W., Batzer, M. A., Pollock, D. D. and Jurka, J. 2007. Evolutionary dynamics of transposable elements in the short-tailed opossum Monodelphis domestica. Genome Res. 17, 992-1004. https://doi.org/10.1101/gr.6070707
  24. Gogvadze, E. and Buzdin, A. 2009. Retroelements and their impact on genome evolution and functioning. Cell Mol. Life Sci. 66, 3727-3742. https://doi.org/10.1007/s00018-009-0107-2
  25. Guffanti, G., Bartlett, A., Klengel, T., Klengel, C., Hunter, R., Glinsky, G. and Macciardi, F. 2018. Novel bioinformatics approach identifies transcriptional profiles of lineagespecific transposable elements at distinct loci in the human dorsolateral prefrontal cortex. Mol. Biol. Evol. 35, 2435-2453. https://doi.org/10.1093/molbev/msy143
  26. Guffanti, G., Gaudi, S., Klengel, T., Fallon, J. H., Mangalam, H., Madduri, R., Rodriguez, A., DeCrescenzo, P., Glovienka, E., Sobell, J., Klengel, C., Pato, M., Ressler, K. J., Pato, C. and Macciardi, F. 2016. LINE1 insertions as a genomic risk factor for schizophrenia: preliminary evidence from an affected family. Am. J Med. Genet. B Neuropsychiatr. Genet. 171, 534-545. https://doi.org/10.1002/ajmg.b.32437
  27. Han, K., Lee, J., Meyer, T. J., Wang, J., Sen, S. K., Srikanta, D., Liang, P. and Batzer, M. A. 2007. Alu recombinationmediated structural deletions in the chimpanzee genome. PLoS Genet. 3, 1939-1949.
  28. Han, K., Sen, S. K., Wang, J., Callinan, P. A., Lee, J., Cordaux, R., Liang, P. and Batzer, M. A. 2005. Genomic rearrangements by LINE-1 insertion-mediated deletion in the human and chimpanzee lineages. Nucleic Acids Res. 33, 4040-4052. https://doi.org/10.1093/nar/gki718
  29. Henssen, A. G., Koche, R., Zhuang, J., Jiang, E., Reed, C., Eisenberg, A., Still, E., MacArthur, I. C., Rodriguez-Fos, E., Gonzalez, S., Puiggros, M., Blackford, A. N., Mason, C. E., de Stanchina, E., Gönen, M., Emde, A. K., Shah, M., Arora, K., Reeves, C., Socci, N. D., Perlman, E., Antonescu, C. R., Roberts, C. W. M., Steen, H., Mullen, E., Jackson, S. P., Torrents, D., Weng, Z., Armstrong, S. A. and Kentsis, A. 2017. PGBD5 promotes site-specific oncogenic mutations in human tumors. Nat. Genet. 49, 1005-1014. https://doi.org/10.1038/ng.3866
  30. Horvath, V., Merenciano, M. and Gonzalez, J. 2017. Revisiting the relationship between transposable elements and the eukaryotic stress response. Trends Genet. 33, 832-841. https://doi.org/10.1016/j.tig.2017.08.007
  31. Huang, C. R., Burns, K. H. and Boeke, J. D. 2012. Active transposition in genomes. Annu. Rev. Genet. 46, 651-675. https://doi.org/10.1146/annurev-genet-110711-155616
  32. Huda, A, Bowen, N. J., Conley, A. B. and Jordan, I. K. 2011. Epigenetic regulation of transposable element derived human gene promoters. Gene 475, 39-48. https://doi.org/10.1016/j.gene.2010.12.010
  33. Huda, A., Mariño-Ramírez, L. and Jordan, I. K. 2010. Epigenetic histone modifications of human transposable elements: genome defense versus exaptation. Mob. DNA 1, 1-12. https://doi.org/10.1186/1759-8753-1-1
  34. Jung, Y. D., Huh, J. W., Kim, D. S., Kim, Y. J., Ahn, K., Ha, H. S., Lee, J. R., Yi, J. M., Moon, J. W., Kim, T. O., Song, G. A., Han, K. and Kim, H. S. 2011. Quantitative analysis of transcript variants of CHM gene containing LTR12C element in humans. Gene 489, 1-5. https://doi.org/10.1016/j.gene.2011.09.001
  35. Kaer, K., Branovets, J., Hallikma, A., Nigumann, P. and Speek, M. 2011. Intronic L1 retrotransposons and nested genes cause transcriptional interference by inducing intron retention, exonization and cryptic polyadenylation. PLoS One 6, e26099. https://doi.org/10.1371/journal.pone.0026099
  36. Kajikawa, M. and Okada, N. 2002. LINEs mobilize SINEs in the eel through a shared 3' sequence. Cell 111, 433-444. https://doi.org/10.1016/S0092-8674(02)01041-3
  37. Kazazian, H. H. Jr. 2000. Genetics. L1 retrotransposons shape the mammalian genome. Science 289, 1152-1153. https://doi.org/10.1126/science.289.5482.1152
  38. Kazazian, H. H. Jr. 2004. Mobile elements: drivers of genome evolution. Science 303, 1626-1632. https://doi.org/10.1126/science.1089670
  39. Kidwell, M. G. 1983. Evolution of hybrid dysgenesis determinants in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA. 80, 1655-1659. https://doi.org/10.1073/pnas.80.6.1655
  40. Kim, Y. J., Lee, J. and Han, K. 2012. Transposable Elements: No More 'Junk DNA'. Genomics Inform. 10, 226-233. https://doi.org/10.5808/GI.2012.10.4.226
  41. Kofler, R., Hill, T., Nolte, V., Betancourt, A. J. and Schlotterer, C. 2015. The recent invasion of natural Drosophila simulans populations by the P-element. Proc. Natl. Acad. Sci. USA. 112, 6659-6663. https://doi.org/10.1073/pnas.1500758112
  42. Lanciano, S. and Mirouze, M. 2018. Transposable elements: all mobile, all different, some stress responsive, some adaptive? Curr. Opin. Genet. Dev. 49, 106-114. https://doi.org/10.1016/j.gde.2018.04.002
  43. Lander, E. S., Linton, L. M., Birren, B., Nusbaum, C., Zody, M. C., Baldwin, J., Devon, K., Dewar, K., Doyle, M., Fitz Hugh, W., Funke, R., Gage, D., Harris, K., Heaford, A., Howland, J., Kann, L., Lehoczky, J., LeVine, R., McEwan, P., McKernan, K., Meldrim, J., Mesirov, J. P., Miranda, C. and Morris, W., International Human Genome Sequencing Consortium. 2001. Initial sequencing and analysis of the human genome. Nature 409, 860-921. https://doi.org/10.1038/35057062
  44. Lee, H. E., Ayarpadikannan, S. and Kim, H. S. 2015. Role of transposable elements in genomic rearrangement, evolution, gene regulation and epigenetics in primates. Genes Genet. Syst. 90, 245-257. https://doi.org/10.1266/ggs.15-00016
  45. Lee, J., Han, K., Meyer, T. J., Kim, H. S. and Batzer, M. A. 2008. Chromosomal inversions between human and chimpanzee lineages caused by retrotransposons. PLoS One 3, e4047. https://doi.org/10.1371/journal.pone.0004047
  46. Legrand, S., Caron, T., Maumus, F., Schvartzman, S., Quadrana, L., Durand, E., Gallina, S., Pauwels, M., Mazoyer, C., Huyghe, L., Colot V., Hanikenne, M. and Castric, V. 2019. Differential retention of transposable element-derived sequences in outcrossing Arabidopsis genomes. Mob. DNA 10, 1-17. https://doi.org/10.1186/s13100-018-0144-1
  47. Levin, H. L. and Moran, J. V. 2011. Dynamic interactions between transposable elements and their hosts. Nat. Rev. Genet. 12, 615-627. https://doi.org/10.1038/nrg3030
  48. Li, W., Lee, M. H., Henderson, L., Tyagi, R., Bachani, M., Steiner, J., Campanac, E., Hoffman, D. A., von Geldern, G., Johnson, K., Maric, D., Morris, H. D., Lentz, M., Pak, K., Mammen, A., Ostrow, L., Rothstein, J. and Nath, A. 2015. Human endogenous retrovirus-K contributes to motor neuron disease. Sci. Transl. Med. 7, 1-13.
  49. Linker, S. B., Marchetto, M. C., Narvaiza, I., Denli, A. M. and Gage, F. H. 2017. Examining non-LTR retrotransposons in the context of the evolving primate brain. BMC Biol. 15, 1-8. https://doi.org/10.1186/s12915-016-0343-5
  50. Lynch, V. J., Nnamani, M. C., Kapusta, A., Brayer, K., Plaza, S. L., Mazur, E. C., Emera, D., Sheikh, S. Z., Grützner, F., Bauersachs, S., Graf, A., Young, S. L., Lieb, J. D., DeMayo, F. J., Feschotte, C. and Wagner, G. P. 2015. Ancient transposable elements transformed the uterine regulatory landscape and transcriptome during the evolution of mammalian pregnancy. Cell Rep. 10, 551-561. https://doi.org/10.1016/j.celrep.2014.12.052
  51. Mager, D. L. and Stoye, J. P. 2015. Mammalian endogenous retroviruses. Microbiol. Spectr. 3, 1-20.
  52. Matlik, K., Redik, K. and Speek, M. 2006. L1 antisense promoter drives tissue-specific transcription of human genes. J. Biomed. Biotechnol. 2006, 1-16. https://doi.org/10.1155/JBB/2006/71753
  53. Mills, R. E., Bennett, E. A., Iskow, R. C., Luttig, C. T., Tsui, C., Pittard, W. S. and Devine, S. E. 2006. Recently mobilized transposons in the human and chimpanzee genomes. Am. J. Hum. Genet. 78, 671-679. https://doi.org/10.1086/501028
  54. Mouse Genome Sequencing Consortium, Waterston, R. H., Lindblad-Toh, K., Birney, E., Rogers, J., Abril, J. F., Agarwal, P., Agarwala, R., Ainscough, R., Alexandersson, M., An, P., Antonarakis, S. E., Attwood, J., Baertsch, R., Bailey, J., Barlow, K., Beck, S., Berry, E., Birren, B., Bloom, T. and Bork, P. 2002. Initial sequencing and comparative analysis of the mouse genome. Nature 420, 520-562. https://doi.org/10.1038/nature01262
  55. Peccoud, J., Loiseau, V., Cordaux, R. and Gilbert, C. 2017. Massive horizontal transfer of transposable elements in insects. Proc. Natl. Acad. Sci. USA. 114, 4721-4726. https://doi.org/10.1073/pnas.1621178114
  56. Percharde, M., Lin, C. J., Yin, Y., Guan, J., Peixoto, G. A., Bulut-Karslioglu, A., Biechele, S., Huang, B., Shen, X. and Ramalho-Santos, M. 2018. A LINE1-nucleolin partnership regulates early development and ESC identity. Cell 174, 391-405. e19. https://doi.org/10.1016/j.cell.2018.05.043
  57. Plohl, M., Meštrović, N. and Mravinac, B. 2014. Composition and evolutionary importance of transposable elements in humans and primates. Chromosoma 123, 313-325. https://doi.org/10.1007/s00412-014-0462-0
  58. Ramsay, L., Marchetto, M. C., Caron, M., Chen, S. H., Busche, S., Kwan, T., Pastinen, T., Gage, F. H. and Bourque, G. 2017. Conserved expression of transposon-derived non-coding transcripts in primate stem cells. BMC Genomics 18, 1-13. https://doi.org/10.1186/s12864-016-3406-7
  59. Rebollo, R., Romanish, M. T. and Mager, D. L. 2012. Transposable elements: An abundant and natural source of regulatory sequences for host genes. Annu. Rev. Genet. 46, 21-42. https://doi.org/10.1146/annurev-genet-110711-155621
  60. Reik, W., Dean, W. and Walter, J. 2001. Epigenetic reprogramming in mammalian development. 2001. Science 293, 1089-1093. https://doi.org/10.1126/science.1063443
  61. Richard, C. and Mark, A. B., 2009. The impact of retrotransposons on human genome evolution Nat. Rev. Genet. 10, 691-703 https://doi.org/10.1038/nrg2640
  62. Roulois, D., Loo Yau, H., Singhania, R., Wang, Y., Danesh, A., Shen, S. Y., Han, H., Liang, G., Jones, P. A., Pugh, T. J., O'Brien, C. and De Carvalho, D. D. 2015. DNA-demethylating agents target colorectal cancer cells by inducing viral mimicry by endogenous transcripts. Cell 162, 961-973. https://doi.org/10.1016/j.cell.2015.07.056
  63. Rowe, H. M. and Trono, D. 2011. Dynamic control of endogenous retroviruses during development. Virology 411, 273-287. https://doi.org/10.1016/j.virol.2010.12.007
  64. Schmitz, J. and Brosius, J. 2011. Exonization of transposed elements: a challenge and opportunity for evolution. Biochimie 93, 1928-1934. https://doi.org/10.1016/j.biochi.2011.07.014
  65. Sen, S. K., Han, K., Wang, J., Lee, J., Wang, H., Callinan, P. A., Dyer, M., Cordaux, R., Liang, P. and Batzer, M. A. 2006. Human genomic deletions mediated by recombination between Alu elements. Am. J Hum. Genet. 79, 41-53. https://doi.org/10.1086/504600
  66. Sundaram, V., Cheng, Y., Ma, Z., Li, D., Xing, X., Edge, P., Snyder, M. P. and Wang, T. 2014. Widespread contribution of transposable elements to the innovation of gene regulatory networks. Genome Res. 24, 1963-1976. https://doi.org/10.1101/gr.168872.113
  67. Tang, Z., Steranka, J. P., Ma, S., Grivainis, M., Rodić, N., Huang, C. R., Shih, I. M., Wang, T. L., Boeke, J. D., Fenyö, D. and Burns, K. H. 2017. Human transposon insertion profiling: analysis, visualization and identification of somatic LINE-1 insertions in ovarian cancer. Proc. Natl. Acad. Sci. USA. 114, E733-E740. https://doi.org/10.1073/pnas.1619797114
  68. Tarailo-Graovac, M. and Chen, N. 2009. Using RepeatMasker to identify repetitive elements in genomic sequences. Curr. Protoc. Bioinformatics 25, 4.10.1-4.10.14.
  69. Tempel, S. 2012. Using and understanding RepeatMasker. Methods Mol. Biol. 859, 29-51. https://doi.org/10.1007/978-1-61779-603-6_2
  70. Thompson, P. J., Macfarlan, T. S. and Lorincz, M. C. 2016. Long terminal repeats: from parasitic elements to building blocks of the transcriptional regulatory repertoire. Mol. Cell 62, 766-776. https://doi.org/10.1016/j.molcel.2016.03.029
  71. Tokuyama, M., Kong, Y., Song, E., Jayewickreme, T., Kang, I. and Iwasaki, A. 2018. ERV map analysis reveals genomewide transcription of human endogenous retroviruses. Proc. Natl. Acad. Sci. USA. 115, 12565-12572. https://doi.org/10.1073/pnas.1814589115
  72. Vitte, C., Fustier, M. A., Alix, K. and Tenaillon, M. I. 2014. The bright side of transposons in crop evolution. Brief. Funct. Genomics 13, 276-295. https://doi.org/10.1093/bfgp/elu002
  73. Warnefors, M., Pereira, V. and Eyre-Walker, A. 2010. Transposable elements: insertion pattern and impact on gene expression evolution in hominids. Mol. Biol. Evol. 27, 1955-1962. https://doi.org/10.1093/molbev/msq084
  74. Wicker, T., Sabot, F., Hua-Van, A., Bennetzen, J. L., Capy, P., Chalhoub, B., Flavell, A., Leroy, P., Morgante, M., Panaud, O., Paux, E., SanMiguel, P. and Schulman, A. H. 2007. A unified classification system for eukaryotic transposable elements. Nat. Rev. Genet. 8, 973-982. https://doi.org/10.1038/nrg2165
  75. Xing, J., Zhang, Y., Han, K., Salem, A. H., Sen, S. K., Huff, C. D., Zhou, Q., Kirkness, E. F., Levy, S., Batzer, M. A. and Jorde, L. B. 2009. Mobile elements create structural variation: analysis of a complete human genome. Genome Res. 19, 1516-1526. https://doi.org/10.1101/gr.091827.109
  76. Yuan, Z., Sun, X., Liu, H. and Xie, J. 2011. MicroRNA genes derived from repetitive elements and expanded by segmental duplication events in mammalian genomes. PLoS One 6, e17666. https://doi.org/10.1371/journal.pone.0017666
  77. Yum, S. Y., Lee, S. J., Kim, H. M., Choi, W. J., Park, J. H., Lee, W. W., Kim, H. S., Kim, H. J., Bae, S. H., Lee, J. H., Moon, J. Y., Lee, J. H., Lee, C. I., Son, B. J., Song, S. H., Ji, S. M., Kim, S. J. and Jang, G. 2016. Efficient generation of transgenic cattle using the DNA transposon and their analysis by next-generation sequencing. Sci. Rep. 6, 1-12. https://doi.org/10.1038/s41598-016-0001-8