Advertisement

Biochemistry (Moscow)

, Volume 83, Issue 3, pp 185–199 | Cite as

The Role of Transposable Elements in Emergence of Metazoa

  • R. N. MustafinEmail author
  • E. K. Khusnutdinova
Review

Abstract

Systems initially emerged for protecting genomes against insertions of transposable elements and represented by mechanisms of splicing regulation, RNA–interference, and epigenetic factors have played a key role in the evolution of animals. Many studies have shown inherited transpositions of mobile elements in embryogenesis and preservation of their activities in certain tissues of adult organisms. It was supposed that on the emergence of Metazoa the self–regulation mechanisms of transposons related with the gene networks controlling their activity could be involved in intercellular cell coordination in the cascade of successive divisions with differentiated gene expression for generation of tissues and organs. It was supposed that during evolution species–specific features of transposons in the genomes of eukaryotes could form the basis for creation of dynamically related complexes of systems for epigenetic regulation of gene expression. These complexes could be produced due to the influence of noncoding transposon–derived RNAs on DNA methylation, histone modifications, and processing of alternative splicing variants, whereas the mobile elements themselves could be directly involved in the regulation of gene expression in cis and in trans. Transposons are widely distributed in the genomes of eukaryotes; therefore, their activation can change the expression of specific genes. In turn, this can play an important role in cell differentiation during ontogenesis. It is supposed that transposons can form a species–specific pattern for control of gene expression, and that some variants of this pattern can be favorable for adaptation. The presented data indicate the possible influence of transposons in karyotype formation. It is supposed that transposon localization relative to one another and to protein–coding genes can influence the species–specific epigenetic regulation of ontogenesis.

Keywords

alternative splicing differentiation noncoding RNAs ontogenesis RNA interference transposons evolution 

Abbreviations

AS

alternative splicing

CNS

central nervous system

ERV

endogenous retroviruses

ESC

embryonic stem cells

lincRNA

long intergenic noncoding RNA

LINE

long interspersed nuclear element

lncRNAs

long noncoding RNAs

LTR

long terminal repeats

ME

mobile element

MIR

mammalian wide interspersed repeat

ncRNAs

noncoding RNAs

piRNAs

piwi–interacting RNAs

RdRP

RNA–dependent RNA polymerase

RNAi

RNA interference

SINE

short interspersed nuclear element

siRNAs

small interfering RNAs

UTR

untranslated region

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Casas–Mollano, J. A., Rohr, J., Kim, E. J., Balassa, E, van Dijk, K., and Cerutti, H. (2008) Diversification of the core RNA interference machinery in Chlamydomonas reinhardtii and the role of DCL1 in transposon silencing, Genetics, 179, 69–81.PubMedPubMedCentralCrossRefGoogle Scholar
  2. 2.
    Moran, Y., Praher, D., Fredman, D., and Technau, U. (2013) The evolution of microRNA pathway protein components in Cnidaria, Mol. Biol. Evol., 30, 2541–2552.PubMedPubMedCentralCrossRefGoogle Scholar
  3. 3.
    Liew, Y. J., Aranda, M., Carr, A., Baumgarten, S., Zoccola, D., Tambutte, S., Allemand, D., Micklem, G., and Voolstra, C. R. (2014) Identification of microRNA in the coral Styphora pistillata, PLoS One, 9, e91101.PubMedPubMedCentralCrossRefGoogle Scholar
  4. 4.
    Kubiak, M. R., and Makalowska, I. (2017) Protein–coding genes’ retrocopies and their functions, Viruses, 9, pii: E80.PubMedCrossRefGoogle Scholar
  5. 5.
    Smalheiser, N. R., and Torvik, V. I. (2005) Mammalian microRNAs derived from genomic repeats, Trends Genet., 21, 322–326.PubMedCrossRefGoogle Scholar
  6. 6.
    Piriyapongsa, J., and Jordan, I. K. (2007) Family of human microRNA genes from miniature inverted–repeat transposable elements, PLoS One, 14, e203.CrossRefGoogle Scholar
  7. 7.
    Piriyapongsa, J., Marino–Ramirez, L., and Jordan, I. K. (2007) Origin and evolution of human microRNAs from transposable elements, Genetics, 176, 1323–1337.PubMedPubMedCentralCrossRefGoogle Scholar
  8. 8.
    Devor, E. J., Peek, A. S., Lanier, W., and Samollow, P. B. (2009) Marsupial–specific microRNAs evolved from marsupial–specific transposable elements, Gene, 448, 187–191.PubMedPubMedCentralCrossRefGoogle Scholar
  9. 9.
    Yuan, Z., Sun, X., Jiang, D., Ding, Y., Lu, Z., Gong, L., Liu, H., and Xie, J. (2010) Origin and evolution of a placental–specific microRNA family in the human genome, BMC Evol. Biol., 10, 346–348.PubMedPubMedCentralCrossRefGoogle Scholar
  10. 10.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  11. 11.
    Borchert, G. M., Holton, N. W., Williams, J. D., Hernan, W. L., Bishop, I. P., Dembosky, J. A., Elste, J. E., Gregoire, N. S., Kim, J. A., Koehler, W. W., Lengerich, J. C., Medema, A. A., Nguyen, M. A., Ower, G. D., Rarick, M. A., Strong, B. N., Tardi, N. J., Tasker, N. M., Wozniak, D. J., Gatto, C., and Larson, E. D. (2011) Comprehensive analysis of microRNA genomic loci identifies pervasive repetitive–element origins, Mob. Genet. Elements, 1, 8–17.PubMedPubMedCentralCrossRefGoogle Scholar
  12. 12.
    Tempel, S., Pollet, N., and Tahi, F. (2012) NcRNA classifier: a tool for detection and classification of transposable element sequences in RNA hairpins, BMC Bioinformatics, 13, 246–258.PubMedPubMedCentralCrossRefGoogle Scholar
  13. 13.
    Roberts, J. T., Cooper, E. A., and Favreau, C. J. (2013) Formation from transposable element insertions and noncoding RNA mutations, Mob. Genet. Elements, 1, e27755.CrossRefGoogle Scholar
  14. 14.
    Gim, J., Ha, H., Ahn, K., Kim, D. S., and Kim, H. S. (2014) Genome–wide identification and classification of microRNAs derived from repetitive elements, Genom. Inform., 12, 261–267.CrossRefGoogle Scholar
  15. 15.
    Platt, R. N., Vandewege, M. W., Kern, C., Schmidt, C. J., Hoffmann, F. G., and Ray, D. A. (2014) Large number of novel miRNAs originate from DNA transposons and are coincident with a large species radiation in bats, Mol. Biol. Evol., 31, 1536–1545.PubMedCrossRefGoogle Scholar
  16. 16.
    Lei, H., and Vorechovsky, I. (2005) Identification of splicing silencers and enhancers in sense Alus: a role for pseudoacceptors in splice site repression, Mol. Cell. Biol., 25, 6912–6920.PubMedPubMedCentralCrossRefGoogle Scholar
  17. 17.
    Pastor, T., Talotti, G., Lewandowska, M. A., and Pagani, F. (2009) An Alu–derived intronic splicing enhancer facilitates intronic processing and modulates aberrant splicing in ATM, Nucleic Acids Res., 37, 7258–7267.PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Watanabe, T., Cheng, E., Zhong, M., and Lin, H. (2015) Retrotransposons and pseudogenes regulate mRNAs and lncRNAs via the piRNA pathway in the germline, Genome Res., 25, 368–380.PubMedPubMedCentralCrossRefGoogle Scholar
  19. 19.
    Hadjiargyrou, M., and Delihas, N. (2013) The intertwining of transposable elements and non–coding RNAs, Int. J. Mol. Sci., 14, 13307–13328.PubMedPubMedCentralCrossRefGoogle Scholar
  20. 20.
    Johnson, R., and Guigo, R. J. (2014) The RIDL hypothesis: transposable elements as functional domains of long noncoding RNAs, RNA, 20, 959–976.PubMedPubMedCentralCrossRefGoogle Scholar
  21. 21.
    Gerdes, P., Richardson, S. R., Mager, D. L., and Faulkner, G. J. (2016) Transposable elements in the mammalian embryo: pioneers surviving through stealth and service, Genome Biol., 17, 100–116.PubMedPubMedCentralCrossRefGoogle Scholar
  22. 22.
    De Koning, A. P., Gu, W., Castoe, T. A., Batzer, M. A., and Pollock, D. D. (2011) Repetitive elements may comprise over two–thirds of the human genome, PLoS Genet., 7, e1002384.PubMedPubMedCentralCrossRefGoogle Scholar
  23. 23.
    Mersch, B., Sela, N., Ast, G., Suhai, S., and Hotz-Wagenblatt, A. (2007) SERpredict: detection of tissueor tumor–specific isoforms generated through exonization of transposable elements, BMC Genet., 8, 78.PubMedPubMedCentralCrossRefGoogle Scholar
  24. 24.
    Novikova, O., and Belfort, M. (2017) Mobile group II introns as ancestral eukaryotic elements, Trends Genet., 33, 773–783.PubMedCrossRefGoogle Scholar
  25. 25.
    Yenerall, P., and Zhou, L. (2012) Identifying the mechanisms of intron gain: progress and trends, Biol. Direct., 7, 29.PubMedPubMedCentralCrossRefGoogle Scholar
  26. 26.
    Amit, M., Sela, N., Keren, H., Melamed, Z., Muler, I., Shomron, N., Izraeli, S., and Ast, G. (2007) Biased exonization of transposed elements in duplicated genes: a lesson from the TIF–IA gene, BMC Mol. Biol., 8, 109.PubMedPubMedCentralCrossRefGoogle Scholar
  27. 27.
    Du, Z., Yang, C., Rothschild, M. F., and Ross, J. (2013) Novel microRNA families expanded in the human genome, BMC Genom., 14, 98–105.CrossRefGoogle Scholar
  28. 28.
    Tan, S., Cardoso–Moreira, M., Shi, W., Zhang, D., Huang, J., Mao, Y., Jia, H., Zhang, Y., Chen, C., Shao, Y., Leng, L., Liu, Z., Huang, X., Long, M., and Zhang, Y. E. (2016) LTR–mediated retroposition as a mechanism of RNA–based duplication in metazoans, Genome Res., 26, 1663–1675.PubMedPubMedCentralCrossRefGoogle Scholar
  29. 29.
    Lin, L., Shen, S., Tye, A., Cai, J. J., Jiang, P., Davidson, B. L., and Xing, Y. (2008) Diverse splicing patterns of exonized Alu elements in human tissues, PLoS Genet., 4, e1000225.PubMedPubMedCentralCrossRefGoogle Scholar
  30. 30.
    Sela, N., Kim, E., and Ast, G. (2010) The role of transposable elements in the evolution of non–mammalian vertebrates and invertebrates, Genome Biol., 11, R59.PubMedPubMedCentralCrossRefGoogle Scholar
  31. 31.
    Belancio, V. P., Roy–Engel, A. M., and Deininger, P. L. (2010) All y’all need to know ‘bout retroelements in cancer, Semin. Cancer Biol., 20, 200–210.PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    Baskaev, K. K. (2015) New Method of Large–Scale Search for Hypomethylated Regulatory Sites in Eukaryotic Genomes: PhD in Biology [in Russian], Moscow.Google Scholar
  33. 33.
    Schmitz, J., and Brosius, J. (2011) Exonization of transposed elements: a challenge and opportunity for evolution, Biochimie, 93, 1928–1934.PubMedCrossRefGoogle Scholar
  34. 34.
    Hadjiargyrou, M., and Delihas, N. (2013) The intertwining of transposable elements and non–coding RNAs, Int. J. Mol. Sci., 14, 13307–13328.PubMedPubMedCentralCrossRefGoogle Scholar
  35. 35.
    Wang, D., Su, Y., Wang, X., Lei, H., and Yu, J. (2012) Transposon–derived and satellite–derived repetitive sequences play distinct functional roles in mammalian intron size expansion, Evol. Bioinform. Online, 8, 301–319.PubMedPubMedCentralGoogle Scholar
  36. 36.
    Li, W., Prazak, L., Chatterjee, N., Gruninger, S., Krug, L., Theodorou, D., and Dubnau, J. (2013) Activation of transposable elements during aging and neuronal decline in Drosophila, Nat. Neurosci., 16, 529–531.PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    Kralovicova, J., Patel, A., Searle, M., and Vorechovsky, I. (2015) The role of short RNA loops in recognition of a single–hairpin exon derived from a mammalian–wide interspersed repeat, RNA Biol., 12, 54–69.PubMedPubMedCentralCrossRefGoogle Scholar
  38. 38.
    Nozu, K., Lijima, K., Igarashi, T., Yamada, S., Kralovicova, J., Nozu, Y., Yamamura, T., Minamikawa, S., Morioka, I., Ninchoji, T., Kaito, H., Nakanishi, K., and Vorechovsky, I. (2017) A birth of bipartite exon by intragenic deletion, Mol. Genet. Genom. Med., 5, 287–294.CrossRefGoogle Scholar
  39. 39.
    Kovalskaya, O. N., Sergiev, P. V., Bogdanov, A. A., and Dontsova, O. A. (2007) Structurally functional anatomy of the signal–recognizing particle: from bacteria to mammals, Usp. Biol. Khim., 47, 129–188.Google Scholar
  40. 40.
    McClintock, B. (1984) The significance of responses of the genome to challenge, Science, 226, 792–801.PubMedCrossRefPubMedCentralGoogle Scholar
  41. 41.
    Vasil’eva, L. A., Vykhristyuk, O. V., Antonenko, O. V., and Zakharov, I. K. (2007) Induction of transpositions of mobile genetic elements in the Drosophila melanogaster genome by different stress factors, Vestnik VOGiS, 11, 662–671.Google Scholar
  42. 42.
    Lukash, L. L. (2007) Mutagenesis induced by integration processes and evolution of nuclear genome, Biopolym. Cell, 23, 172–187.CrossRefGoogle Scholar
  43. 43.
    Yurchenko, N. N., Kovalenko, L. V., and Zakharov, I. K. (2011) Mobile genetic elements: instability of genes and genomes, Vavilov Zh. Genet. Selektsii, 15, 261–270.Google Scholar
  44. 44.
    Masuta, Y., Nozawa, K., Takagi, H., Yaegashi, H., Tanaka, K., Ito, T., Saito, H., Kobayashi, H., Matsunaga, W., Masuda, S., Kato, A., and Ito, H. (2017) Inducible transposition of a heat–activated retrotransposon in tissue culture, Plant. Cell Physiol., 58, 375–384.PubMedGoogle Scholar
  45. 45.
    Kiselev, O. I. (2013) Endogenous retroviruses: structure and functions in the human genome, Vopr. Virusol., 1, 102–115.Google Scholar
  46. 46.
    Kitkumthorn, N., and Mutirangura, A. (2011) Long interspersed nuclear element–1 hypomethylation in cancer: biology and clinical applications, Clin. Epigenet., 2, 315–330.CrossRefGoogle Scholar
  47. 47.
    Khowutthitham, S., Ngamphiw, C., Wanichnopparat, W., Suwanwongse, K., Tongsima, S., Aporntewan, C., and Mutirangura, A. (2012) Intragenic long interspersed element–1 sequences promote promoter hypermethylation in lung adenocarcinoma, multiple myeloma and prostate cancer, Genes Genom., 34, 517–528.Google Scholar
  48. 48.
    Polavarapu, N., Marino–Ramirez, L., Landsman, D., McDonald, J. F., and Jordan, I. K. (2008) Evolutionary rates and patterns for human transcription factor binding sites derived from repetitive DNA, BMC Genom., 9, 226–235.CrossRefGoogle Scholar
  49. 49.
    Feschotte, C. (2008) The contribution of transposable elements to the evolution of regulatory networks, Nat. Rev. Genet., 9, 397–405.PubMedPubMedCentralCrossRefGoogle Scholar
  50. 50.
    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.PubMedCrossRefGoogle Scholar
  51. 51.
    Castellano, L., Rizzi, E., Krell, J., Di Cristina, M., Galizi, R., Mori, A., Tam, J., De Bellis, G., Stebbing, J., Crisanti, A., and Nolan, T. (2015) The germline of the malaria mosquito produces abundant miRNAs, endo–siRNAs and 29–nt small RNAs, BMC Genom., 16, 100–106.Google Scholar
  52. 52.
    Aziz, R. K., Breitbart, M., and Edwards, R. A. (2010) Transposase are the most abundant, most ubiquitous genes in nature, Nucleic Acids Res., 38, 4207–4217.PubMedCrossRefGoogle Scholar
  53. 53.
    Duan, C. G., Wang, X., Pan, L., Miki, D., Tang, K., Hsu, C. C., Lei, M., Zhong, Y., Hou, Y. J., Wang, Z., Zhang, Z., Mangrauthia, S. K., Xu, H., Zhang, H., Dilkes, B., Tao, W. A., and Zhu, J. K. (2017) A pair of transposon–derived proteins function in a histone acetyltransferase complex for active DNA demethylation, Cell Res., 27, 226–240.PubMedCrossRefGoogle Scholar
  54. 54.
    Kurnosov, A. A., Ustyugova, S. V., Nazarov, V., Minervina, A. A., Komkov, A. Y., Shugay, M., Pogorelyy, M. V., Khodosevich, K. V., Mamedov, I. Z., and Lebedev, Y. B. (2015) The evidence for increased L1 activity in the site of human adult brain neurogenesis, PLoS One, 10, e0117854.PubMedPubMedCentralCrossRefGoogle Scholar
  55. 55.
    Casacuberta, E. (2017) Drosophila: retrotransposons making up telomeres, Viruses, 9, pii: E192.PubMedCrossRefGoogle Scholar
  56. 56.
    Titov, I. I., and Vorozheikin, P. S. (2011) MiRNA–containing human transposons, Vavilov Zh. Genet. Selektsii, 15, 323–326.Google Scholar
  57. 57.
    Wang, J., Vicente–Garcia, C., Seruggia, D., Molto, E., Fernandez–Minan, A., Neto, A., Lee, E., Gomez–Skarmeta, J. L., Montoliu, L., Lunyak, V. V., and Jordan, I. K. (2015) MIR retrotransposons sequences provide insulators to the human genome, Proc. Natl. Acad. Sci. USA, 112, 4428–4437.CrossRefGoogle Scholar
  58. 58.
    Buzdin, A. A. (2002) High–throughput Comparison of the Retroelement Distribution in DNA of Human and Chimpanzee: PhD in Biology [in Russain], Moscow.Google Scholar
  59. 59.
    Kramerov, D. A., and Vassetzky, N. S. (2011) SINEs, Wiley Interdiscip. Rev. RNA, 2, 772–786.PubMedCrossRefGoogle Scholar
  60. 60.
    McClintock, B. (1951) Chromosome organization and genic expression, Cold Spring Harb. Symp. Quant. Biol., 16, 13–47.PubMedCrossRefGoogle Scholar
  61. 61.
    Grandi, F. C., Rosser, J. M., Newkirk, S. J., Yin, J., Jiang, X., Xing, Z., Whitmore, L., Bashir, S., Ivics, Z., Izsvak, Z., Ye, P., Yu, Y. E., and An, W. (2015) Retrotransposition creates sloping shores: a graded influence of hypomethylated CpG islands on flanking CpG sites, Genome Res., 25, 1135–1146.PubMedPubMedCentralCrossRefGoogle Scholar
  62. 62.
    Glazko, V. I. (2013) Problems of “marker–aided selection”, Genetika, 2, 16–22.Google Scholar
  63. 63.
    Iniguez, L. P., and Hernandez, G. (2017) The evolutionary relationship between alternative splicing and gene duplication, Front. Genet., 8, 14.PubMedPubMedCentralCrossRefGoogle Scholar
  64. 64.
    Baskaev, K. K., and Buzdin, A. A. (2011) Evolutionary recent groups of genetic mobile elements in human genome, Vavilov Zh. Genet. Selektsii, 15, 313–322.Google Scholar
  65. 65.
    Suntsova, M., Garazha, A., Ivanova, A., Kaminsky, D., Zhavoronkov, A., and Buzdin, A. (2015) Molecular functions of human endogenous retroviruses in health and disease, Cell. Mol. Life Sci., 72, 3653–3675.PubMedCrossRefGoogle Scholar
  66. 66.
    Lippman, Z., May, B., Yordan, C., Singer, T., and Martienssen, R. (2003) Distinct mechanisms determine transposon inheritance and methylation via small interfering RNA and histone modification, PLoS Biol., 1, 420–428.CrossRefGoogle Scholar
  67. 67.
    Upadhyay, U., Srivastava, S., Khatri, I., Nanda, J. S., Subramanian, S., Arora, A., and Singh, J. (2017) Ablation of RNA interference and retrotransposons accompany acquisition and evolution of transposases to heterochromatin protein CENPB, Mol. Biol. Cell, 28, 1132–1146.PubMedPubMedCentralCrossRefGoogle Scholar
  68. 68.
    Xu, C., Tian, J., and Mo, B. (2013) SiRNA–mediated DNA methylation and H3K9 dimethylation in plants, Protein Cell, 4, 656–663.PubMedPubMedCentralCrossRefGoogle Scholar
  69. 69.
    Spengler, R. M., Oakley, C. K., and Davidson, B. L. (2014) Functional microRNAs and target sites are created by line–age–specific transposition, Hum. Mol. Genet., 23, 1783–1793.PubMedCrossRefGoogle Scholar
  70. 70.
    Lu, D., Davis, M. P., Abreu–Goodger, C., Wang, W., Campos, L. S., Siede, J., Vigorito, E., Skarnes, W. C., Dunham, I., Enright, A. J., and Liu, P. (2012) miR–25 regulates Wwp2 and Fbxw7 and promotes reprogramming of mouse fibroblast cells to iPSCs, PLoS One, 7, e40938.PubMedPubMedCentralCrossRefGoogle Scholar
  71. 71.
    Nozawa, M., Miura, S., and Nei, M. (2012) Origins and evolution of microRNA genes in plant species, Genome Biol. Evol., 4, 230–239.PubMedPubMedCentralCrossRefGoogle Scholar
  72. 72.
    Samantarrai, D., Dash, S., Chhetri, B., and Mallick, B. (2013) Genomic and epigenomic cross–talks in the regulatory landscape of miRNAs in breast cancer, Mol. Cancer Res., 11, 315–328.PubMedCrossRefGoogle Scholar
  73. 73.
    Zhang, G., Esteve, P., Chin, H. G., Terragni, J., Dai, N., Correa, I. R., Jr., and Pradhan, S. (2015) Small RNA–mediated DNA (cytosine–5) methyltransferase 1 inhibition leads to aberrant DNA methylation, Nucleic Acids Res., 43, 6112–6124.PubMedPubMedCentralCrossRefGoogle Scholar
  74. 74.
    Morita, S., Horii, T., Kimura, M., Ochiya, T., Tajima, S., and Hatada, I. (2013) MiR–29 represses the activities of DNA methyltransferases and DNA demethylases, Int. J. Mol. Sci., 14, 14647–14658.PubMedPubMedCentralCrossRefGoogle Scholar
  75. 75.
    Zhang, H., Tao, Z., Hong, H., Chen, Z., Wu, C., Li, X., Xiao, J., and Wang, S. (2016) Transposon–derived small RNA is responsible for modified function of WRKY45 locus, Nat. Plants, 2, 16016–16023.PubMedCrossRefPubMedCentralGoogle Scholar
  76. 76.
    Molaro, A., Falciatori, I., Hodges, E., Aravin, A. A., Marran, K., Rafii, S., McCombie, W. R., Smith, A. D., and Hannon, G. J. (2014) Two waves of de novo methylation during mouse germ cell development, Genes Dev., 28, 1544–1549.PubMedPubMedCentralCrossRefGoogle Scholar
  77. 77.
    Fu, A., Jacobs, D. I., and Zhu, Y. (2014) Epigenome–wide analysis of piRNAs in gene–specific DNA methylation, RNA Biol., 11, 1301–1312.PubMedCrossRefGoogle Scholar
  78. 78.
    Shao, P., Liao, J., Guan, D. G., Yang, J. H., Zheng, L. L., Jing, Q., Zhou, H., and Qu, L. H. (2012) Drastic expression change of transposon–derived piRNA–like RNAs and microRNAs in early stages of chicken embryos implies a role in gastrulation, RNA Biol., 9, 212–227.PubMedCrossRefGoogle Scholar
  79. 79.
    Kapusta, A., Kronenberg, Z., Lynch, V. J., Zhuo, X., Ramsay, L., Bourgue, G., Yandell, M., and Feschotte, C. (2013) Transposable elements are major contributors to the origin, diversification, and regulation of vertebrate long noncoding RNAs, PLoS Genet., 9, e1003470.PubMedGoogle Scholar
  80. 80.
    Long, Y., Wang, X., Youmans, D. T., and Cech, T. R. (2017) How do lncRNAs regulate transcription, Sci. Adv., 3, eaao2110.PubMedPubMedCentralCrossRefGoogle Scholar
  81. 81.
    Lisitsyn, N. A., Chernyi, A. A., and Karpov, V. L. (2015) The role of long noncoding RNAs in carcinogenesis, Mol. Biol., 49, 561–570.CrossRefGoogle Scholar
  82. 82.
    Ramsay, L., Marchetto, M. C., Caron, M., Chen, S. H., Busche, S., Kwan, T., Pastinen, T., Gage, F. H., and Bourgue, G. (2017) Conserved expression of transposon–derived non–coding transcripts in primate stem cells, BMC Genom., 18, 214–226.CrossRefGoogle Scholar
  83. 83.
    Iwakiri, J., Terai, G., and Hamada, M. (2017) Computational prediction of lncRNA–mRNA interactions by integrating tissue specificity in human transcriptome, Biol. Direct., 12, 15.PubMedPubMedCentralCrossRefGoogle Scholar
  84. 84.
    Deng, B., Cheng, X., Li, H., Qin, J., Tian, M., and Jin, G. (2017) Microarray expression profiling in the denervated hippocampus identifies long noncoding RNAs functionally involved in neurogenesis, BMC Mol. Biol., 18, 15.PubMedPubMedCentralCrossRefGoogle Scholar
  85. 85.
    Faulkner, G. J. (2011) Retrotransposons: mobile and mutagenic from conception to death, FEBS Lett., 585, 1589–1594.PubMedCrossRefGoogle Scholar
  86. 86.
    Richardson, S. R., Morell, S., and Faulkner, G. J. (2014) L1 retrotransposons and somatic mosaicism in the brain, Annu. Rev. Genet., 48, 1–27.PubMedCrossRefGoogle Scholar
  87. 87.
    Upton, K. R., Gerhardt, D. J., Jesuadian, J. S., Richardson, S. R., Sanchez–Lugue, F. J., Bodea, G. O., Ewing, A. D., Salvador–Palmoegue, C., van der Knaap, M. S., Brennan, P. M., Vanderver, A., and Faulkner, G. J. (2015) Ubiquitous L1 mosaicism in hippocampal neurons, Cell, 161, 22–39.CrossRefGoogle Scholar
  88. 88.
    Patel, T., and Hobert, O. (2017) Coordinated control of terminal differentiation and restriction of cellular plasticity, eLife, 6, e24100.PubMedPubMedCentralCrossRefGoogle Scholar
  89. 89.
    Wissing, S., Munoz–Lopez, M., Macia, A., Yang, Z., Montano, M., Collins, W., Garcia–Perez, J. L., Moran, J. V., and Green, W. C. (2012) Reprogramming somatic cells into iPS cell activates LINE–1 retroelement mobility, Hum. Mol. Genet., 21, 208–218.PubMedCrossRefGoogle Scholar
  90. 90.
    Klawitter, S., Fuchs, N. V., Upton, K. R., Munoz–Lopez, M., Shukkla, R., Wang, J., Faulkner, G. J., and Schumann, G. G. (2016) Reprogramming triggers endogenous L1 and Alu retrotransposition in human induced pluripotent stem cells, Nat. Commun., 7, 10286–10301.PubMedPubMedCentralCrossRefGoogle Scholar
  91. 91.
    Baranov, V. S., and Kuznetsova, T. V. (2007) Cytogenetics of Human Embryonic Development [in Russian], Izdatelstvo N–L, St. Petersburg.Google Scholar
  92. 92.
    Haig, D. (2016) Transposable elements: self–seekers of the germline, team–players of the soma, Bioessays, 38, 1158–1166.PubMedGoogle Scholar
  93. 93.
    Wang, J., Li, X., Wang, L., Li, J., Zhao, Y., Bou, G., Li, Y., Jiao, G., Shen, X., Wei, R., Liu, S., Xie, B., Lei, L., Li, W., Zhou, Q., and Liu, Z. (2016) A novel long intergenic noncoding RNA indispensable for the cleavage of mouse two–cell embryos, EMBO Rep., 17, 1452–1470.PubMedPubMedCentralCrossRefGoogle Scholar
  94. 94.
    Wu, Y., Qi, X., Gong, L., Xing, G., Chen, M., Miao, L., Yao, J., Suzuki, T., Furihata, C., Luan, Y., and Ren, J. (2012) Identification of BC005512 as a DNA damage responsive murine endogenous retrovirus of GLN family involved in cell growth regulation, PLoS One, 7, e35010.PubMedPubMedCentralCrossRefGoogle Scholar
  95. 95.
    Eckersley–Maslin, M. A., Svensson, V., Krueger, C., Stubbs, T. M., Giehr, P., Krueger, F., Miragaia, R. J., Kyriakopoulos, C., Berrrens, R. V., Milagre, I., Walter, J., Teichmann, S. A., and Reik, W. (2016) MERVL/Zscan4 network activation results in transient genome–wide DNA demethylation of mESCs, Cell Rep., 17, 179–192.PubMedPubMedCentralCrossRefGoogle Scholar
  96. 96.
    Bray, S., Turnbull, M., Hebert, S., and Douville, R. N. (2016) Insight into the ERVK integrase–propensity for DNA damage, Front. Microbiol., 7, 1941.PubMedPubMedCentralCrossRefGoogle Scholar
  97. 97.
    Galli, U. M., Sauter, M., Lecher, B., Maurer, S., Herbst, H., Roemer, K., and Mueller–Lantzsch, N. (2005) Human endogenous retrovirus rec interferes with germ cell development in mice and may cause carcinoma in situ, the predecessor lesion of germ cell tumors, Oncogene, 24, 3223–3228.PubMedGoogle Scholar
  98. 98.
    Moran, J. V., Holmes, S. E., Naas, T. P., DeBerardinis, R. J., Boeke, J. D., and Kazazian, H. H., Jr. (1996) High frequency retrotransposition in cultured mammalian cells, Cell, 87, 917–927.PubMedCrossRefPubMedCentralGoogle Scholar
  99. 99.
    De Berardinis, R. J., Goodier, J. L., Ostertag, E. M., and Kazazian, H. H. (1998) Rapid amplification of a retrotransposons subfamily is evolving the mouse genome, Nat. Genet., 20, 288–290.CrossRefGoogle Scholar
  100. 100.
    Wei, W., Morrish, T. A., and Alisch, R. S. (2000) A transient assay reveals that cultured human cells can accommodate multiple LINE–1 retrotransposition events, Anal. Biochem., 284, 435–438.PubMedCrossRefGoogle Scholar
  101. 101.
    Morrish, T. A., Gilbert, N., Myers, J. S., Vincent, B. J., Stamato, T. D., Taccioli, G. E., Batzer, M. A., and Moran, J. V. (2002) DNA repair mediated by endonuclease–independent LINE–1 retrotransposition, Nat. Genet., 31, 159–165.PubMedCrossRefPubMedCentralGoogle Scholar
  102. 102.
    Han, J. S., and Boeke, J. D. (2004) A highly active synthetic mammalian retrotransposons, Nature, 429, 314–318.PubMedCrossRefGoogle Scholar
  103. 103.
    Ostertag, E. M., De Berardinis, R. J., Goodier, J. L., Zhang, Y., Yang, N., Gerton, G. L., and Kazazian, H. H., Jr. (2002) A mouse model of human L1 retrotransposition, Nat. Genet., 32, 655–660.PubMedCrossRefGoogle Scholar
  104. 104.
    Prak, E. T., Dodson, A. W., Farkash, E. A., and Kazazian, H. H. (2003) Tracking an embryonic L1 retrotransposition event, Proc. Natl. Acad. Sci. USA, 100, 1832–1837.PubMedPubMedCentralCrossRefGoogle Scholar
  105. 105.
    Muotri, A. R., Chu, V. T., Marchetto, M. C., Deng, W., Moran, J. V., and Gage, F. H. (2005) Somatic mosaicism in neuronal precursor cells mediated by L1 retrotransposition, Nature, 435, 903–910.PubMedCrossRefGoogle Scholar
  106. 106.
    Van den Hurk, J. A., Meij, I. C., and Seleme, M. C. (2007) L1 retrotransposition can occur early in human embryonic development, Hum. Mol. Genet., 16, 1587–1592.PubMedCrossRefGoogle Scholar
  107. 107.
    Coufal, N. G., Garcia–Perez, J. L., Peng, G. E., Yeo, G. W., Mu, Y., Lovci, M. T., Morell, M., O’Shea, K. S., Moran, J. V., and Gage, F. H. (2009) L1 retrotransposition in human neural progenitor cells, Nature, 460, 1127–1131.PubMedPubMedCentralCrossRefGoogle Scholar
  108. 108.
    Macia, A., Munoz–Lopez, M., Cortes, J. L., Hastings, R. K., Morell, S., Lucena–Aguilar, G., Marchal, J. A., Badge, R. M., and Garcia–Perez, J. L. (2011) Epigenetic control of retrotransposons expression in human embryonic stem cells, Mol. Cell. Biol., 31, 300–316.PubMedCrossRefGoogle Scholar
  109. 109.
    Marchetto, M. C., Narvaiza, I., Denli, A. M., Benner, C., Lazzarini, T. A., Nathanson, J. L., Paguola, A. C. M., Desai, K. N., Herai, R. H., Weitzman, M. D., Yeo, G. W., Muotri, A. R., and Gage, F. H. (2013) Differential L1 regulation in pluripotent stem cells of humans and apes, Nature, 503, 525–529.PubMedPubMedCentralCrossRefGoogle Scholar
  110. 110.
    Pavlicev, M., Hiratsuka, K., Swaggart, K. A., Dunn, C., and Muglia, L. (2015) Detecting endogenous retrovirusdriven tissue–specific gene transcription, Genome Biol. Evol., 7, 1082–1097.PubMedPubMedCentralCrossRefGoogle Scholar
  111. 111.
    Lee, K. H., Chiu, S., Lee, Y. K., Greenhalgh, D. G., and Cho, K. (2012) Age–dependent and tissue–specific structural changes in the C57BL/6J mouse genome, Exp. Mol. Pathol., 93, 167–172.PubMedCrossRefGoogle Scholar
  112. 112.
    Lee, K. H., Yee, L., Lim, D., Greenhalgh, D., and Cho, K. (2015) Temporal and spatial rearrangements of a repetitive element array on C57BL/6J mouse genome, Exp. Mol. Pathol., 98, 439–445.PubMedPubMedCentralCrossRefGoogle Scholar
  113. 113.
    Evrony, G. D., Cai, X., Lee, E., Hills, L. B., Elhosary, P. C., Lehmann, H. S., Parker, J. J., Atabay, K. D., Gilmore, E. C., Poduri, A., Park, P. J., and Walsh, C. A. (2012) Singleneuron sequencing analysis of L1 retrotransposition and somatic mutation in the human brain, Cell, 151, 483–496.PubMedPubMedCentralCrossRefGoogle Scholar
  114. 114.
    Garcia–Perez, J. L., Marchetto, M. C., Muotri, A. R., Coufal, N. G., Gage, F. H., O’Shea, K. S., and Moran, J. V. (2007) LINE–1 retrotransposition in human embryonic stem cells, Hum. Mol. Genet., 16, 1569–1577.PubMedCrossRefGoogle Scholar
  115. 115.
    Kubo, S., Seleme, M. C., Soifer, H. S., Perez, J. L., Moran, J. V., Kazazian, H. H., Jr., and Kasahara, N. (2006) L1 retrotransposition in non–dividing and primary human somatic cells, Proc. Natl. Acad. Sci. USA, 103, 8036–8041.PubMedPubMedCentralCrossRefGoogle Scholar
  116. 116.
    Shi, X., Seluanov, A., and Gorbunova, V. (2007) Cell divisions are required for L1 retrotransposition, Mol. Cell. Biol., 27, 1264–1270.PubMedCrossRefGoogle Scholar
  117. 117.
    Gottesman, S., and Storz, G. (2015) RNA reflections: converging of Hfq, RNA, 21, 511–512.PubMedPubMedCentralCrossRefGoogle Scholar
  118. 118.
    Lee, R. C., Feinbaum, R. L., and Ambro, V. (1993) The C. elegans heterochronic gene lin–4 encodes small RNAs with antisense complementarity to lin–14, Cell, 75, 843–854.PubMedCrossRefGoogle Scholar
  119. 119.
    Shabalina, S. A., and Koonin, E. V. (2008) Origins and evolution of eukaryotic RNA interference, Trends Ecol. Evol., 23, 578–587.PubMedPubMedCentralCrossRefGoogle Scholar
  120. 120.
    Avesson, L., Reimegard, J., Wagner, E. G. H., and Soderbom, F. (2012) MicroRNAs in Amoebozoa: deep sequencing of the small RNA population in the social amoeba Dictyostelium discoideum reveals developmentally regulated microRNAs, RNA, 18, 1771–1782.PubMedPubMedCentralCrossRefGoogle Scholar
  121. 121.
    Pashkovskiy, P. P., and Ryazansky, S. S. (2013) Biogenesis, evolution, and functions of plant microRNAs, Biochemistry (Moscow), 78, 627–637.CrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2018

Authors and Affiliations

  1. 1.Bashkir State UniversityUfaRussia
  2. 2.Institute of Biochemistry and GeneticsUfa Research CenterUfaRussia

Personalised recommendations