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Korean Society for Biochemistry and Molecular Biology (생화학분자생물학회)
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Ongoing endeavors to detect mobilization of transposable elements

  • Lee, Yujeong (Department of Biological Sciences, Kangwon National University) ;
  • Ha, Una (Department of Biological Sciences, Kangwon National University) ;
  • Moon, Sungjin (Department of Biological Sciences, Kangwon National University)
  • Received : 2022.04.23
  • Accepted : 2022.06.14
  • Published : 2022.07.31
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Abstract

Transposable elements (TEs) are DNA sequences capable of mobilization from one location to another in the genome. Since the discovery of 'Dissociation (Dc) locus' by Barbara McClintock in maize (1), mounting evidence in the era of genomics indicates that a significant fraction of most eukaryotic genomes is composed of TE sequences, involving in various aspects of biological processes such as development, physiology, diseases and evolution. Although technical advances in genomics have discovered numerous functional impacts of TE across species, our understanding of TEs is still ongoing process due to challenges resulted from complexity and abundance of TEs in the genome. In this mini-review, we briefly summarize biology of TEs and their impacts on the host genome, emphasizing importance of understanding TE landscape in the genome. Then, we introduce recent endeavors especially in vivo retrotransposition assays and long read sequencing technology for identifying de novo insertions/TE polymorphism, which will broaden our knowledge of extraordinary relationship between genomic cohabitants and their host.

Keywords

Acknowledgement

Authors in this work sincerely apologize for presenting a minuscule fraction of colleagues' work due to page limitations. We deeply thank to Dr. Yun Doo Chung and Dr. Sim Namkoong for comments on the manuscript. SM, YL and UH drafted this manuscript and all agreed the submitted version. This work was supported by the National Research Foundation of Korea (NRF) grant funded by the Korea government (2020R1C1C1007050) and by 2020 Research Grant from Kangwon National University (520200047) given to SM.

References

  1. Mc CB (1950) The origin and behavior of mutable loci in maize. Proc Natl Acad Sci U S A 36, 344-355 https://doi.org/10.1073/pnas.36.6.344
  2. Kazazian HH Jr and Moran JV (2017) Mobile DNA in health and disease. N Engl J Med 377, 361-370 https://doi.org/10.1056/NEJMra1510092
  3. Richardson SR, Doucet AJ, Kopera HC, Moldovan JB, Garcia-Perez JL and Moran JV (2015) The Influence of LINE-1 and SINE retrotransposons on mammalian genomes. Microbiol Spectr 3, MDNA3-0061-2014
  4. Cordaux R and Batzer MA (2009) The impact of retrotransposons on human genome evolution. Nat Rev Genet 10, 691-703 https://doi.org/10.1038/nrg2640
  5. Hancks DC and Kazazian HH Jr (2016) Roles for retrotransposon insertions in human disease. Mob DNA 7, 9 https://doi.org/10.1186/s13100-016-0065-9
  6. Ostertag EM and Kazazian HH Jr (2001) Biology of mammalian L1 retrotransposons. Annu Rev Genet 35, 501-538 https://doi.org/10.1146/annurev.genet.35.102401.091032
  7. Ewing AD and Kazazian HH Jr (2010) High-throughput sequencing reveals extensive variation in human-specific L1 content in individual human genomes. Genome Res 20, 1262-1270 https://doi.org/10.1101/gr.106419.110
  8. Mager DL and Stoye JP (2015) Mammalian endogenous retroviruses. Microbiol Spectr 3, MDNA3-0009-2014
  9. Tarlinton RE, Meers J and Young PR (2006) Retroviral invasion of the koala genome. Nature 442, 79-81 https://doi.org/10.1038/nature04841
  10. Lander ES, Linton LM, Birren B et al (2001) Initial sequencing and analysis of the human genome. Nature 409, 860-921 https://doi.org/10.1038/35057062
  11. Clark JB and Kidwell MG (1997) A phylogenetic perspective on P transposable element evolution in Drosophila. Proc Natl Acad Sci U S A 94, 11428-11433 https://doi.org/10.1073/pnas.94.21.11428
  12. Khurana JS, Wang J, Xu J et al (2011) Adaptation to P element transposon invasion in Drosophila melanogaster. Cell 147, 1551-1563 https://doi.org/10.1016/j.cell.2011.11.042
  13. Moon S, Cassani M, Lin YA, Wang L, Dou K and Zhang ZZ (2018) A robust transposon-endogenizing response from germline stem cells. Dev Cell 47, 660-671 e663 https://doi.org/10.1016/j.devcel.2018.10.011
  14. Kofler R, Senti KA, Nolte V, Tobler R and Schlotterer C (2018) Molecular dissection of a natural transposable element invasion. Genome Res 28, 824-835 https://doi.org/10.1101/gr.228627.117
  15. Kofler R, Hill T, Nolte V, Betancourt AJ and Schlotterer C (2015) The recent invasion of natural Drosophila simulans populations by the P-element. Proc Natl Acad Sci U S A 112, 6659-6663 https://doi.org/10.1073/pnas.1500758112
  16. Hill T, Schlotterer C and Betancourt AJ (2016) Hybrid dysgenesis in Drosophila simulans associated with a rapid invasion of the P-element. PLoS Genet 12, e1005920 https://doi.org/10.1371/journal.pgen.1005920
  17. Bellen HJ, Levis RW, He Y et al (2011) The Drosophila gene disruption project: progress using transposons with distinctive site specificities. Genetics 188, 731-743 https://doi.org/10.1534/genetics.111.126995
  18. Spradling AC, Bellen HJ and Hoskins RA (2011) Drosophila P elements preferentially transpose to replication origins. Proc Natl Acad Sci U S A 108, 15948-15953 https://doi.org/10.1073/pnas.1112960108
  19. Eickbush TH and Eickbush DG (2015) Integration, regulation, and long-term stability of R2 retrotransposons. Microbiol Spectr 3, MDNA3-0011-2014
  20. Huang CR, Burns KH and Boeke JD (2012) Active transposition in genomes. Annu Rev Genet 46, 651-675 https://doi.org/10.1146/annurev-genet-110711-155616
  21. Sotero-Caio CG, Platt RN 2nd, Suh A and Ray DA (2017) Evolution and diversity of transposable elements in vertebrate genomes. Genome Biol Evol 9, 161-177 https://doi.org/10.1093/gbe/evw264
  22. Kissinger JC and DeBarry J (2011) Genome cartography: charting the apicomplexan genome. Trends Parasitol 27, 345-354 https://doi.org/10.1016/j.pt.2011.03.006
  23. Van't Hof AE, Campagne P, Rigden DJ et al (2016) The industrial melanism mutation in British peppered moths is a transposable element. Nature 534, 102-105 https://doi.org/10.1038/nature17951
  24. Lisch D (2013) How important are transposons for plant evolution? Nat Rev Genet 14, 49-61 https://doi.org/10.1038/nrg3374
  25. Studer A, Zhao Q, Ross-Ibarra J and Doebley J (2011) Identification of a functional transposon insertion in the maize domestication gene tb1. Nat Genet 43, 1160-1163 https://doi.org/10.1038/ng.942
  26. Rebollo R, Farivar S and Mager DL (2012) C-GATE - catalogue of genes affected by transposable elements. Mob DNA 3, 9 https://doi.org/10.1186/1759-8753-3-9
  27. de Souza FS, Franchini LF and Rubinstein M (2013) Exaptation of transposable elements into novel cis-regulatory elements: is the evidence always strong? Mol Biol Evol 30, 1239-1251 https://doi.org/10.1093/molbev/mst045
  28. Sundaram V, Cheng Y, Ma Z et al (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
  29. Notwell JH, Chung T, Heavner W and Bejerano G (2015) A family of transposable elements co-opted into developmental enhancers in the mouse neocortex. Nat Commun 6, 6644 https://doi.org/10.1038/ncomms7644
  30. Lynch VJ, Leclerc RD, May G and Wagner GP (2011) Transposon-mediated rewiring of gene regulatory networks contributed to the evolution of pregnancy in mammals. Nat Genet 43, 1154-1159 https://doi.org/10.1038/ng.917
  31. Kapitonov VV and Jurka J (2005) RAG1 core and V(D)J recombination signal sequences were derived from Transib transposons. PLoS Biol 3, e181 https://doi.org/10.1371/journal.pbio.0030181
  32. Huang S, Tao X, Yuan S et al (2016) Discovery of an active RAG transposon illuminates the origins of V(D)J recombination. Cell 166, 102-114 https://doi.org/10.1016/j.cell.2016.05.032
  33. Traverse KL and Pardue ML (1988) A spontaneously opened ring chromosome of Drosophila melanogaster has acquired He-T DNA sequences at both new telomeres. Proc Natl Acad Sci U S A 85, 8116-8120 https://doi.org/10.1073/pnas.85.21.8116
  34. Levis RW, Ganesan R, Houtchens K, Tolar LA and Sheen FM (1993) Transposons in place of telomeric repeats at a Drosophila telomere. Cell 75, 1083-1093 https://doi.org/10.1016/0092-8674(93)90318-k
  35. Abad JP, De Pablos B, Osoegawa K, De Jong PJ, Martin-Gallardo A and Villasante A (2004) TAHRE, a novel telomeric retrotransposon from Drosophila melanogaster, reveals the origin of Drosophila telomeres. Mol Biol Evol 21, 1620-1624 https://doi.org/10.1093/molbev/msh180
  36. Villasante A, Abad JP, Planello R, Mendez-Lago M, Celniker SE and de Pablos B (2007) Drosophila telomeric retrotransposons derived from an ancestral element that was recruited to replace telomerase. Genome Res 17, 1909-1918 https://doi.org/10.1101/gr.6365107
  37. Agudo M, Losada A, Abad JP, Pimpinelli S, Ripoll P and Villasante A (1999) Centromeres from telomeres? The centromeric region of the Y chromosome of Drosophila melanogaster contains a tandem array of telomeric HeT-A-and TART-related sequences. Nucleic Acids Res 27, 3318-3324 https://doi.org/10.1093/nar/27.16.3318
  38. Chang CH, Chavan A, Palladino J et al (2019) Islands of retroelements are major components of Drosophila centromeres. PLoS Biol 17, e3000241 https://doi.org/10.1371/journal.pbio.3000241
  39. Neumann P, Navratilova A, Koblizkova A et al (2011) Plant centromeric retrotransposons: a structural and cytogenetic perspective. Mob DNA 2, 4 https://doi.org/10.1186/1759-8753-2-4
  40. Glockner G and Heidel AJ (2009) Centromere sequence and dynamics in Dictyostelium discoideum. Nucleic Acids Res 37, 1809-1816 https://doi.org/10.1093/nar/gkp017
  41. Ferreri GC, Brown JD, Obergfell C et al (2011) Recent amplification of the kangaroo endogenous retrovirus, KERV, limited to the centromere. J Virol 85, 4761-4771 https://doi.org/10.1128/JVI.01604-10
  42. Rad R, Rad L, Wang W et al (2010) PiggyBac transposon mutagenesis: a tool for cancer gene discovery in mice. Science 330, 1104-1107 https://doi.org/10.1126/science.1193004
  43. Dupuy AJ, Akagi K, Largaespada DA, Copeland NG and Jenkins NA (2005) Mammalian mutagenesis using a highly mobile somatic Sleeping Beauty transposon system. Nature 436, 221-226 https://doi.org/10.1038/nature03691
  44. Lee E, Iskow R, Yang L et al (2012) Landscape of somatic retrotransposition in human cancers. Science 337, 967-971 https://doi.org/10.1126/science.1222077
  45. Babaian A and Mager DL (2016) Endogenous retroviral promoter exaptation in human cancer. Mob DNA 7, 24 https://doi.org/10.1186/s13100-016-0080-x
  46. Shukla R, Upton KR, Munoz-Lopez M et al (2013) Endogenous retrotransposition activates oncogenic pathways in hepatocellular carcinoma. Cell 153, 101-111 https://doi.org/10.1016/j.cell.2013.02.032
  47. Bailey JA, Liu G and Eichler EE (2003) An Alu transposition model for the origin and expansion of human segmental duplications. Am J Hum Genet 73, 823-834 https://doi.org/10.1086/378594
  48. Montgomery EA, Huang SM, Langley CH and Judd BH (1991) Chromosome rearrangement by ectopic recombination in Drosophila melanogaster: genome structure and evolution. Genetics 129, 1085-1098 https://doi.org/10.1093/genetics/129.4.1085
  49. Deininger PL and Batzer MA (1999) Alu repeats and human disease. Mol Genet Metab 67, 183-193 https://doi.org/10.1006/mgme.1999.2864
  50. Deniz O, Frost JM and Branco MR (2019) Regulation of transposable elements by DNA modifications. Nat Rev Genet 20, 417-431 https://doi.org/10.1038/s41576-019-0106-6
  51. Ozata DM, Gainetdinov I, Zoch A, O'Carroll D and Zamore PD (2019) PIWI-interacting RNAs: small RNAs with big functions. Nat Rev Genet 20, 89-108 https://doi.org/10.1038/s41576-018-0073-3
  52. Yang P, Wang Y and Macfarlan TS (2017) The role of KRAB-ZFPs in transposable element repression and mammalian evolution. Trends Genet 33, 871-881 https://doi.org/10.1016/j.tig.2017.08.006
  53. Wang L, Dou K, Moon S, Tan FJ and Zhang ZZ (2018) Hijacking oogenesis enables massive propagation of LINE and retroviral transposons. Cell 174, 1082-1094 e1012 https://doi.org/10.1016/j.cell.2018.06.040
  54. Nagirnaja L, Morup N, Nielsen JE et al (2021) Variant PNLDC1, defective piRNA processing, and azoospermia. N Engl J Med 385, 707-719 https://doi.org/10.1056/NEJMoa2028973
  55. Houwing S, Kamminga LM, Berezikov E et al (2007) A role for Piwi and piRNAs in germ cell maintenance and transposon silencing in Zebrafish. Cell 129, 69-82 https://doi.org/10.1016/j.cell.2007.03.026
  56. Carmell MA, Girard A, van de Kant HJ et al (2007) MIWI2 is essential for spermatogenesis and repression of transposons in the mouse male germline. Dev Cell 12, 503-514 https://doi.org/10.1016/j.devcel.2007.03.001
  57. Bourc'his D and Bestor TH (2004) Meiotic catastrophe and retrotransposon reactivation in male germ cells lacking Dnmt3L. Nature 431, 96-99 https://doi.org/10.1038/nature02886
  58. Siudeja K, van den Beek M, Riddiford N et al (2021) Unraveling the features of somatic transposition in the Drosophila intestine. EMBO J 40, e106388 https://doi.org/10.15252/embj.2020106388
  59. Brouha B, Schustak J, Badge RM et al (2003) Hot L1s account for the bulk of retrotransposition in the human population. Proc Natl Acad Sci U S A 100, 5280-5285 https://doi.org/10.1073/pnas.0831042100
  60. Beck CR, Collier P, Macfarlane C et al (2010) LINE-1 retrotransposition activity in human genomes. Cell 141, 1159-1170 https://doi.org/10.1016/j.cell.2010.05.021
  61. Hancks DC, Goodier JL, Mandal PK, Cheung LE and Kazazian HH Jr (2011) Retrotransposition of marked SVA elements by human L1s in cultured cells. Hum Mol Genet 20, 3386-3400 https://doi.org/10.1093/hmg/ddr245
  62. Raiz J, Damert A, Chira S et al (2012) The non-autonomous retrotransposon SVA is trans-mobilized by the human LINE-1 protein machinery. Nucleic Acids Res 40, 1666-1683 https://doi.org/10.1093/nar/gkr863
  63. Boeke JD, Garfinkel DJ, Styles CA and Fink GR (1985) Ty elements transpose through an RNA intermediate. Cell 40, 491-500 https://doi.org/10.1016/0092-8674(85)90197-7
  64. Moran JV, Holmes SE, Naas TP, DeBerardinis RJ, Boeke JD and Kazazian HH Jr (1996) High frequency retrotrans-position in cultured mammalian cells. Cell 87, 917-927 https://doi.org/10.1016/S0092-8674(00)81998-4
  65. Ostertag EM, Prak ET, DeBerardinis RJ, Moran JV and Kazazian HH Jr (2000) Determination of L1 retrotransposition kinetics in cultured cells. Nucleic Acids Res 28, 1418-1423 https://doi.org/10.1093/nar/28.6.1418
  66. Xie Y, Rosser JM, Thompson TL, Boeke JD and An W (2011) Characterization of L1 retrotransposition with highthroughput dual-luciferase assays. Nucleic Acids Res 39, e16 https://doi.org/10.1093/nar/gkq1076
  67. Kannan M, Li J, Fritz SE et al (2017) Dynamic silencing of somatic L1 retrotransposon insertions reflects the developmental and cellular contexts of their genomic integration. Mob DNA 8, 8 https://doi.org/10.1186/s13100-017-0091-2
  68. Kopera HC, Larson PA, Moldovan JB, Richardson SR, Liu Y and Moran JV (2016) LINE-1 cultured cell retrotransposition assay. Methods Mol Biol 1400, 139-156 https://doi.org/10.1007/978-1-4939-3372-3_10
  69. Wei W, Morrish TA, Alisch RS and Moran JV (2000) A transient assay reveals that cultured human cells can accommodate multiple LINE-1 retrotransposition events. Anal Biochem 284, 435-438 https://doi.org/10.1006/abio.2000.4675
  70. Morrish TA, Gilbert N, Myers JS et al (2002) DNA repair mediated by endonuclease-independent LINE-1 retrotransposition. Nat Genet 31, 159-165 https://doi.org/10.1038/ng898
  71. Feng Q, Moran JV, Kazazian HH Jr and Boeke JD (1996) Human L1 retrotransposon encodes a conserved endonuclease required for retrotransposition. Cell 87, 905-916 https://doi.org/10.1016/S0092-8674(00)81997-2
  72. An W, Han JS, Wheelan SJ et al (2006) Active retrotransposition by a synthetic L1 element in mice. Proc Natl Acad Sci U S A 103, 18662-18667 https://doi.org/10.1073/pnas.0605300103
  73. Muotri AR, Chu VT, Marchetto MC, Deng W, Moran JV and Gage FH (2005) Somatic mosaicism in neuronal precursor cells mediated by L1 retrotransposition. Nature 435, 903-910 https://doi.org/10.1038/nature03663
  74. Newkirk SJ, Lee S, Grandi FC et al (2017) Intact piRNA pathway prevents L1 mobilization in male meiosis. Proc Natl Acad Sci U S A 114, E5635-E5644
  75. Jensen S and Heidmann T (1991) An indicator gene for detection of germline retrotransposition in transgenic Drosophila demonstrates RNA-mediated transposition of the LINE I element. EMBO J 10, 1927-1937 https://doi.org/10.1002/j.1460-2075.1991.tb07719.x
  76. Sultana T, van Essen D, Siol O et al (2019) The landscape of L1 retrotransposons in the human genome is shaped by pre-insertion sequence biases and post-insertion selection. Mol Cell 74, 555-570 e557 https://doi.org/10.1016/j.molcel.2019.02.036
  77. Flasch DA, Macia A, Sanchez L et al (2019) Genomewide de novo L1 retrotransposition connects endonuclease activity with replication. Cell 177, 837-851 e828 https://doi.org/10.1016/j.cell.2019.02.050
  78. Marlor RL, Parkhurst SM and Corces VG (1986) The Drosophila melanogaster gypsy transposable element encodes putative gene products homologous to retroviral proteins. Mol Cell Biol 6, 1129-1134 https://doi.org/10.1128/MCB.6.4.1129
  79. Kim A, Terzian C, Santamaria P, Pelisson A, Purd'homme N and Bucheton A (1994) Retroviruses in invertebrates: the gypsy retrotransposon is apparently an infectious retrovirus of Drosophila melanogaster. Proc Natl Acad Sci U S A 91, 1285-1289 https://doi.org/10.1073/pnas.91.4.1285
  80. Song SU, Gerasimova T, Kurkulos M, Boeke JD and Corces VG (1994) An env-like protein encoded by a Drosophila retroelement: evidence that gypsy is an infectious retrovirus. Genes Dev 8, 2046-2057 https://doi.org/10.1101/gad.8.17.2046
  81. Mevel-Ninio M, Mariol MC and Gans M (1989) Mobilization of the gypsy and copia retrotransposons in Drosophila melanogaster induces reversion of the ovo dominant female-sterile mutations: molecular analysis of revertant alleles. EMBO J 8, 1549-1558 https://doi.org/10.1002/j.1460-2075.1989.tb03539.x
  82. Dej KJ, Gerasimova T, Corces VG and Boeke JD (1998) A hotspot for the Drosophila gypsy retroelement in the ovo locus. Nucleic Acids Res 26, 4019-4025 https://doi.org/10.1093/nar/26.17.4019
  83. Labrador M, Sha K, Li A and Corces VG (2008) Insulator and Ovo proteins determine the frequency and specificity of insertion of the gypsy retrotransposon in Drosophila melanogaster. Genetics 180, 1367-1378 https://doi.org/10.1534/genetics.108.094318
  84. Li W, Prazak L, Chatterjee N et al (2013) Activation of transposable elements during aging and neuronal decline in Drosophila. Nat Neurosci 16, 529-531 https://doi.org/10.1038/nn.3368
  85. Duffy JB (2002) GAL4 system in Drosophila: a fly geneticist's Swiss army knife. Genesis 34, 1-15 https://doi.org/10.1002/gene.10150
  86. Jones BC, Wood JG, Chang C et al (2016) A somatic piRNA pathway in the Drosophila fat body ensures metabolic homeostasis and normal lifespan. Nat Commun 7, 13856 https://doi.org/10.1038/ncomms13856
  87. Wood JG, Jones BC, Jiang N et al (2016) Chromatin-modifying genetic interventions suppress age-associated transposable element activation and extend life span in Drosophila. Proc Natl Acad Sci U S A 113, 11277-11282 https://doi.org/10.1073/pnas.1604621113
  88. Sousa-Victor P, Ayyaz A, Hayashi R et al (2017) Piwi is required to limit exhaustion of aging somatic stem cells. Cell Rep 20, 2527-2537 https://doi.org/10.1016/j.celrep.2017.08.059
  89. Sun W, Samimi H, Gamez M, Zare H and Frost B (2018) Pathogenic tau-induced piRNA depletion promotes neuronal death through transposable element dysregulation in neurodegenerative tauopathies. Nat Neurosci 21, 1038-1048 https://doi.org/10.1038/s41593-018-0194-1
  90. Fort-Aznar L, Ugbode C and Sweeney ST (2020) Retrovirus reactivation in CHMP2BIntron5 models of frontotemporal dementia. Hum Mol Genet 29, 2637-2646 https://doi.org/10.1093/hmg/ddaa142
  91. Penke TJ, McKay DJ, Strahl BD, Matera AG and Duronio RJ (2016) Direct interrogation of the role of H3K9 in metazoan heterochromatin function. Genes Dev 30, 1866-1880 https://doi.org/10.1101/gad.286278.116
  92. Chang YH, Keegan RM, Prazak L and Dubnau J (2019) Cellular labeling of endogenous retrovirus replication (CLEVR) reveals de novo insertions of the gypsy retrotransposable element in cell culture and in both neurons and glial cells of aging fruit flies. PLoS Biol 17, e3000278 https://doi.org/10.1371/journal.pbio.3000278
  93. Keegan RM, Talbot LR, Chang YH, Metzger MJ and Dubnau J (2021) Intercellular viral spread and intracellular transposition of Drosophila gypsy. PLoS Genet 17, e1009535 https://doi.org/10.1371/journal.pgen.1009535
  94. Song SU, Kurkulos M, Boeke JD and Corces VG (1997) Infection of the germ line by retroviral particles produced in the follicle cells: a possible mechanism for the mobilization of the gypsy retroelement of Drosophila. Development 124, 2789-2798 https://doi.org/10.1242/dev.124.14.2789
  95. Chang YH and Dubnau J (2019) The gypsy endogenous retrovirus drives non-cell-autonomous propagation in a Drosophila TDP-43 model of neurodegeneration. Curr Biol 29, 3135-3152 e3134 https://doi.org/10.1016/j.cub.2019.07.071
  96. Wensink PC, Tabata S and Pachl C (1979) The clustered and scrambled arrangement of moderately repetitive elements in Drosophila DNA. Cell 18, 1231-1246 https://doi.org/10.1016/0092-8674(79)90235-6
  97. Potter S, Truett M, Phillips M and Maher A (1980) Eucaryotic transposable genetic elements with inverted terminal repeats. Cell 20, 639-647 https://doi.org/10.1016/0092-8674(80)90310-4
  98. Biemont C, Ronsseray S, Anxolabehere D, Izaabel H and Gautier C (1990) Localization of P elements, copy number regulation, and cytotype determination in Drosophila melanogaster. Genet Res 56, 3-14 https://doi.org/10.1017/S0016672300028822
  99. Badge RM, Alisch RS and Moran JV (2003) ATLAS: a system to selectively identify human-specific L1 insertions. Am J Hum Genet 72, 823-838 https://doi.org/10.1086/373939
  100. Sheen FM, Sherry ST, Risch GM et al (2000) Reading between the LINEs: human genomic variation induced by LINE-1 retrotransposition. Genome Res 10, 1496-1508 https://doi.org/10.1101/gr.149400
  101. Pornthanakasem W and Mutirangura A (2004) LINE-1 insertion dimorphisms identification by PCR. Biotechniques 37, 750, 752
  102. Kim EY, Fan W and Cho J (2021) Determination of TE insertion positions using transposon display. Methods Mol Biol 2250, 115-121 https://doi.org/10.1007/978-1-0716-1134-0_11
  103. Goerner-Potvin P and Bourque G (2018) Computational tools to unmask transposable elements. Nat Rev Genet 19, 688-704 https://doi.org/10.1038/s41576-018-0050-x
  104. Tubio JMC, Li Y, Ju YS et al (2014) Mobile DNA in cancer. Extensive transduction of nonrepetitive DNA mediated by L1 retrotransposition in cancer genomes. Science 345, 1251343 https://doi.org/10.1126/science.1251343
  105. Treiber CD and Waddell S (2017) Resolving the prevalence of somatic transposition in Drosophila. Elife 6, e28297 https://doi.org/10.7554/elife.28297
  106. Kim J, Hu C, Moufawad El Achkar C et al (2019) Patient-customized oligonucleotide therapy for a rare genetic disease. N Engl J Med 381, 1644-1652 https://doi.org/10.1056/NEJMoa1813279
  107. van Dijk EL, Jaszczyszyn Y, Naquin D and Thermes C (2018) The third revolution in sequencing technology. Trends Genet 34, 666-681 https://doi.org/10.1016/j.tig.2018.05.008
  108. Wang Y, Zhao Y, Bollas A, Wang Y and Au KF (2021) Nanopore sequencing technology, bioinformatics and applications. Nat Biotechnol 39, 1348-1365 https://doi.org/10.1038/s41587-021-01108-x
  109. Logsdon GA, Vollger MR and Eichler EE (2020) Long-read human genome sequencing and its applications. Nat Rev Genet 21, 597-614 https://doi.org/10.1038/s41576-020-0236-x
  110. Kasianowicz JJ, Brandin E, Branton D and Deamer DW (1996) Characterization of individual polynucleotide molecules using a membrane channel. Proc Natl Acad Sci U S A 93, 13770-13773 https://doi.org/10.1073/pnas.93.24.13770
  111. Song L, Hobaugh MR, Shustak C, Cheley S, Bayley H and Gouaux JE (1996) Structure of staphylococcal alpha-hemolysin, a heptameric transmembrane pore. Science 274, 1859-1866 https://doi.org/10.1126/science.274.5294.1859
  112. Jain M, Olsen HE, Paten B and Akeson M (2016) The Oxford Nanopore MinION: delivery of nanopore sequencing to the genomics community. Genome Biol 17, 239 https://doi.org/10.1186/s13059-016-1103-0
  113. Manrao EA, Derrington IM, Laszlo AH et al (2012) Reading DNA at single-nucleotide resolution with a mutant MspA nanopore and phi29 DNA polymerase. Nat Biotechnol 30, 349-353 https://doi.org/10.1038/nbt.2171
  114. Cherf GM, Lieberman KR, Rashid H, Lam CE, Karplus K and Akeson M (2012) Automated forward and reverse ratcheting of DNA in a nanopore at 5-A precision. Nat Biotechnol 30, 344-348 https://doi.org/10.1038/nbt.2147
  115. Amarasinghe SL, Ritchie ME and Gouil Q (2021) longread-tools.org: an interactive catalogue of analysis methods for long-read sequencing data. Gigascience 10, giab003 https://doi.org/10.1093/gigascience/giab003
  116. Gong L, Wong CH, Cheng WC et al (2018) Picky comprehensively detects high-resolution structural variants in nanopore long reads. Nat Methods 15, 455-460 https://doi.org/10.1038/s41592-018-0002-6
  117. Goodwin S, Gurtowski J, Ethe-Sayers S, Deshpande P, Schatz MC and McCombie WR (2015) Oxford Nanopore sequencing, hybrid error correction, and de novo assembly of a eukaryotic genome. Genome Res 25, 1750-1756 https://doi.org/10.1101/gr.191395.115
  118. David M, Dursi LJ, Yao D, Boutros PC and Simpson JT (2017) Nanocall: an open source basecaller for Oxford Nanopore sequencing data. Bioinformatics 33, 49-55 https://doi.org/10.1093/bioinformatics/btw569
  119. Boza V, Brejova B and Vinar T (2017) DeepNano: deep recurrent neural networks for base calling in MinION nanopore reads. PLoS One 12, e0178751 https://doi.org/10.1371/journal.pone.0178751
  120. Gong L, Wong CH, Idol J, Ngan CY and Wei CL (2019) Ultra-long read sequencing for whole genomic DNA analysis. J Vis Exp 145, e58954
  121. Branton D and Deamer DW (2018) Nanopore sequencing: an introduction, World Scientific, New Jersey.
  122. De Coster W, De Rijk P, De Roeck A et al (2019) Structural variants identified by Oxford Nanopore PromethION sequencing of the human genome. Genome Res 29, 1178-1187 https://doi.org/10.1101/gr.244939.118
  123. De Roeck A, De Coster W, Bossaerts L et al (2019) NanoSatellite: accurate characterization of expanded tandem repeat length and sequence through whole genome long-read sequencing on PromethION. Genome Biol 20, 239 https://doi.org/10.1186/s13059-019-1856-3
  124. Kim HS, Jeon S, Kim C et al (2019) Chromosome-scale assembly comparison of the Korean Reference Genome KOREF from PromethION and PacBio with Hi-C mapping information. Gigascience 8, giz125 https://doi.org/10.1093/gigascience/giz125
  125. Nicholls SM, Quick JC, Tang S and Loman NJ (2019) Ultra-deep, long-read nanopore sequencing of mock microbial community standards. Gigascience 8, giz043 https://doi.org/10.1093/gigascience/giz043
  126. Payne A, Holmes N, Rakyan V and Loose M (2019) BulkVis: a graphical viewer for Oxford nanopore bulk FAST5 files. Bioinformatics 35, 2193-2198 https://doi.org/10.1093/bioinformatics/bty841
  127. Jain M, Koren S, Miga KH et al (2018) Nanopore sequencing and assembly of a human genome with ultralong reads. Nat Biotechnol 36, 338-345 https://doi.org/10.1038/nbt.4060
  128. Solares EA, Chakraborty M, Miller DE et al (2018) Rapid low-cost assembly of the Drosophila melanogaster reference genome using low-coverage, long-read sequencing. G3 (Bethesda) 8, 3143-3154 https://doi.org/10.1534/g3.118.200162
  129. Tyson JR, O'Neil NJ, Jain M, Olsen HE, Hieter P and Snutch TP (2018) MinION-based long-read sequencing and assembly extends the Caenorhabditis elegans reference genome. Genome Res 28, 266-274 https://doi.org/10.1101/gr.221184.117
  130. Jain M, Olsen HE, Turner DJ et al (2018) Linear assembly of a human centromere on the Y chromosome. Nat Biotechnol 36, 321-323 https://doi.org/10.1038/nbt.4109
  131. Miga KH, Koren S, Rhie A et al (2020) Telomere-to-telomere assembly of a complete human X chromosome. Nature 585, 79-84 https://doi.org/10.1038/s41586-020-2547-7
  132. Michael TP, Jupe F, Bemm F et al (2018) High contiguity Arabidopsis thaliana genome assembly with a single nanopore flow cell. Nat Commun 9, 541 https://doi.org/10.1038/s41467-018-03016-2
  133. Chernyavskaya Y, Zhang X, Liu J and Blackburn J (2022) Long-read sequencing of the zebrafish genome reorganizes genomic architecture. BMC Genomics 23, 116 https://doi.org/10.1186/s12864-022-08349-3
  134. Garg S, Fungtammasan A, Carroll A et al (2021) Chromosome-scale, haplotype-resolved assembly of human genomes. Nat Biotechnol 39, 309-312 https://doi.org/10.1038/s41587-020-0711-0
  135. Kirov I, Merkulov P, Dudnikov M et al (2021) Transposons hidden in Arabidopsis thaliana genome assembly gaps and mobilization of non-autonomous LTR retrotransposons unravelled by nanotei pipeline. Plants (Basel) 10, 2681
  136. Mohamed M, Dang NT, Ogyama Y et al (2020) A transposon story: from TE content to TE dynamic invasion of Drosophila genomes using the single-molecule sequencing technology from Oxford Nanopore. Cells 9, 1776 https://doi.org/10.3390/cells9081776
  137. Miller DE, Staber C, Zeitlinger J and Hawley RS (2018) Highly contiguous genome assemblies of 15 Drosophila species generated using Nanopore sequencing. G3 (Bethesda) 8, 3131-3141 https://doi.org/10.1534/g3.118.200160
  138. Pradhan B, Cajuso T, Katainen R et al (2017) Detection of subclonal L1 transductions in colorectal cancer by long-distance inverse-PCR and Nanopore sequencing. Sci Rep 7, 14521 https://doi.org/10.1038/s41598-017-15076-3
  139. Fujimoto A, Wong JH, Yoshii Y et al (2021) Whole-genome sequencing with long reads reveals complex structure and origin of structural variation in human genetic variations and somatic mutations in cancer. Genome Med 13, 65 https://doi.org/10.1186/s13073-021-00883-1
  140. Ellison CE and Cao W (2020) Nanopore sequencing and Hi-C scaffolding provide insight into the evolutionary dynamics of transposable elements and piRNA production in wild strains of Drosophila melanogaster. Nucleic Acids Res 48, 290-303 https://doi.org/10.1093/nar/gkz1080
  141. Siudeja K, van den Beek M, Riddiford N et al (2021) Unraveling the features of somatic transposition in the Drosophila intestine. EMBO J 40, e106388 https://doi.org/10.15252/embj.2020106388
  142. Frommer M, McDonald LE, Millar DS et al (1992) A genomic sequencing protocol that yields a positive display of 5-methylcytosine residues in individual DNA strands. Proc Natl Acad Sci U S A 89, 1827-1831 https://doi.org/10.1073/pnas.89.5.1827
  143. Ewing AD, Smits N, Sanchez-Luque FJ et al (2020) Nano-pore sequencing enables comprehensive transposable element epigenomic profiling. Mol Cell 80, 915-928 e915 https://doi.org/10.1016/j.molcel.2020.10.024
  144. Haggerty C, Kretzmer H, Riemenschneider C et al (2021) Dnmt1 has de novo activity targeted to transposable elements. Nat Struct Mol Biol 28, 594-603 https://doi.org/10.1038/s41594-021-00603-8
  145. Jiang F, Zhang J, Liu Q et al (2019) Long-read direct RNA sequencing by 5'-Cap capturing reveals the impact of Piwi on the widespread exonization of transposable elements in locusts. RNA Biol 16, 950-959 https://doi.org/10.1080/15476286.2019.1602437
  146. Kirov I, Dudnikov M, Merkulov P et al (2020) Nanopore RNA sequencing revealed long non-coding and LTR retrotransposon-related RNAs expressed at early stages of triticale SEED development. Plants (Basel) 9, 1794
  147. Lee SC, Ernst E, Berube B et al (2020) Arabidopsis retrotransposon virus-like particles and their regulation by epigenetically activated small RNA. Genome Res 30, 576-588 https://doi.org/10.1101/gr.259044.119
  148. Panda K and Slotkin RK (2020) Long-read cDNA sequencing enables a "gene-like" transcript annotation of transposable elements. Plant Cell 32, 2687-2698 https://doi.org/10.1105/tpc.20.00115
  149. Berrens RV, Yang A, Laumer CE et al (2021) Locus-specific expression of transposable elements in single cells with CELLO-seq. Nat Biotechnol 40, 546-554 https://doi.org/10.1038/s41587-021-01093-1
  150. Maringer K, Yousuf A, Heesom KJ et al (2017) Proteomics informed by transcriptomics for characterising active transposable elements and genome annotation in Aedes aegypti. BMC Genomics 18, 101 https://doi.org/10.1186/s12864-016-3432-5