Nanopore sequencing enables comprehensive transposable element epigenomic profiling

We apply long-read nanopore sequencing and a new tool, TLDR (Transposons from Long Dirty Reads), to directly infer CpG methylation of new and extant human transposable element (TE) insertions in hippocampus, heart, and liver, as well as paired tumour and non-tumour liver. Whole genome TLDR analysis greatly facilitates studies of TE biology as complete insertion sequences and their epigenetic modifications are readily obtainable.

[1]  G. Cristofari,et al.  Measuring and interpreting transposable element expression , 2020, Nature Reviews Genetics.

[2]  L. Jorde,et al.  The Simons Genome Diversity Project: A Global Analysis of Mobile Element Diversity , 2020, Genome biology and evolution.

[3]  Kathryn O'Neill,et al.  Mobile genomics: tools and techniques for tackling transposons , 2020, Philosophical Transactions of the Royal Society B.

[4]  David T. W. Jones,et al.  Pan-cancer analysis of whole genomes identifies driver rearrangements promoted by LINE-1 retrotransposition , 2020, Nature Genetics.

[5]  Weichen Zhou,et al.  Identification and characterization of occult human-specific LINE-1 insertions using long-read sequencing technology , 2019, Nucleic acids research.

[6]  T. Macfarlan,et al.  The Arms Race Between KRAB-Zinc Finger Proteins and Endogenous Retroelements and Its Impact on Mammals. , 2019, Annual review of genetics.

[7]  Erica C. Pehrsson,et al.  The epigenomic landscape of transposable elements across normal human development and anatomy , 2019, Nature Communications.

[8]  Guillaume Holley,et al.  Long read sequencing of 1,817 Icelanders provides insight into the role of structural variants in human disease , 2019, bioRxiv.

[9]  Mark J. P. Chaisson,et al.  Human-specific tandem repeat expansion and differential gene expression during primate evolution , 2019, Proceedings of the National Academy of Sciences.

[10]  Jinkuk Kim,et al.  Patient-Customized Oligonucleotide Therapy for a Rare Genetic Disease. , 2019, The New England journal of medicine.

[11]  Sergey Koren,et al.  Telomere-to-telomere assembly of a complete human X chromosome , 2019, bioRxiv.

[12]  G. Faulkner,et al.  LINE-1 Evasion of Epigenetic Repression in Humans. , 2019, Molecular cell.

[13]  A. Meissner,et al.  Activation of neuronal genes via LINE-1 elements upon global DNA demethylation in human neural progenitors , 2019, Nature Communications.

[14]  Nakul M. Shah,et al.  Transposable elements drive widespread expression of oncogenes in human cancers , 2019, Nature Genetics.

[15]  G. Faulkner,et al.  Dynamic Methylation of an L1 Transduction Family during Reprogramming and Neurodifferentiation , 2019, Molecular and Cellular Biology.

[16]  J. Boeke,et al.  LINE-1 derepression in senescent cells triggers interferon and inflammaging , 2018, Nature.

[17]  A. Ferguson-Smith,et al.  Identification, Characterization, and Heritability of Murine Metastable Epialleles: Implications for Non-genetic Inheritance , 2018, Cell.

[18]  A. Ferguson-Smith,et al.  The discovery and importance of genomic imprinting , 2018, eLife.

[19]  Matthew E. Ritchie,et al.  Using long-read sequencing to detect imprinted DNA methylation , 2018, bioRxiv.

[20]  G. Bourque,et al.  Computational tools to unmask transposable elements , 2018, Nature Reviews Genetics.

[21]  J. Flowers,et al.  Origins and geographic diversification of African rice (Oryza glaberrima) , 2018, bioRxiv.

[22]  Mohammad M. Karimi,et al.  LTR retrotransposons transcribed in oocytes drive species-specific and heritable changes in DNA methylation , 2018, Nature Communications.

[23]  H. Woodrow,et al.  : A Review of the , 2018 .

[24]  G. Faulkner,et al.  L1 retrotransposition in the soma: a field jumping ahead , 2018, Mobile DNA.

[25]  G. Faulkner,et al.  L1 retrotransposition is a common feature of mammalian hepatocarcinogenesis , 2018, Genome research.

[26]  Kazunori D. Yamada,et al.  Parallelization of MAFFT for large-scale multiple sequence alignments , 2018, Bioinform..

[27]  Trisha J. Multhaupt-Buell,et al.  Disease onset in X-linked dystonia-parkinsonism correlates with expansion of a hexameric repeat within an SVA retrotransposon in TAF1 , 2017, Proceedings of the National Academy of Sciences.

[28]  Esa Pitkänen,et al.  Detection of subclonal L1 transductions in colorectal cancer by long-distance inverse-PCR and Nanopore sequencing , 2017, Scientific Reports.

[29]  Ryan E. Mills,et al.  The Mobile Element Locator Tool (MELT): population-scale mobile element discovery and biology , 2017, Genome research.

[30]  Heng Li,et al.  Minimap2: pairwise alignment for nucleotide sequences , 2017, Bioinform..

[31]  J. V. Moran,et al.  Mobile DNA in Health and Disease , 2017, The New England journal of medicine.

[32]  K. Burns Transposable elements in cancer , 2017, Nature Reviews Cancer.

[33]  G. Faulkner,et al.  Heritable L1 retrotransposition in the mouse primordial germline and early embryo , 2017, Genome research.

[34]  Brent S. Pedersen,et al.  Nanopore sequencing and assembly of a human genome with ultra-long reads , 2017, Nature Biotechnology.

[35]  D. Trono,et al.  KRAB zinc-finger proteins contribute to the evolution of gene regulatory networks , 2017, Nature.

[36]  Winston Timp,et al.  Detecting DNA cytosine methylation using nanopore sequencing , 2017, Nature Methods.

[37]  C. Feschotte,et al.  Regulatory activities of transposable elements: from conflicts to benefits , 2016, Nature Reviews Genetics.

[38]  J. Houseley,et al.  TET-dependent regulation of retrotransposable elements in mouse embryonic stem cells , 2016, Genome Biology.

[39]  Jun Wang,et al.  Evidence for L1-associated DNA rearrangements and negligible L1 retrotransposition in glioblastoma multiforme , 2016, Mobile DNA.

[40]  F. Gage,et al.  L1-associated genomic regions are deleted in somatic cells of the healthy human brain , 2016, Nature Neuroscience.

[41]  J. Goodier Restricting retrotransposons: a review , 2016, Mobile DNA.

[42]  S. Devine,et al.  A hot L1 retrotransposon evades somatic repression and initiates human colorectal cancer , 2016, Genome research.

[43]  H. Kazazian,et al.  Roles for retrotransposon insertions in human disease , 2016, Mobile DNA.

[44]  J. Vera-Otarola,et al.  Activation of individual L1 retrotransposon instances is restricted to cell-type dependent permissive loci , 2016, eLife.

[45]  Aurélie Teissandier,et al.  An epigenetic switch ensures transposon repression upon dynamic loss of DNA methylation in embryonic stem cells , 2016, eLife.

[46]  A. Ewing Transposable element detection from whole genome sequence data , 2015, Mobile DNA.

[47]  Gabor T. Marth,et al.  An integrated map of structural variation in 2,504 human genomes , 2015, Nature.

[48]  Zhaohui S. Qin,et al.  Detection of differentially methylated regions from whole-genome bisulfite sequencing data without replicates , 2015, Nucleic acids research.

[49]  Leo van Iersel,et al.  WhatsHap: Weighted Haplotype Assembly for Future-Generation Sequencing Reads , 2015, J. Comput. Biol..

[50]  Leanne S. Whitmore,et al.  Retrotransposition creates sloping shores: a graded influence of hypomethylated CpG islands on flanking CpG sites , 2015, Genome research.

[51]  C. Walsh,et al.  Cell Lineage Analysis in Human Brain Using Endogenous Retroelements , 2015, Neuron.

[52]  David Haussler,et al.  An evolutionary arms race between KRAB zinc finger genes 91/93 and SVA/L1 retrotransposons , 2014, Nature.

[53]  D. Trono,et al.  Evolutionally dynamic L1 regulation in embryonic stem cells , 2014, Genes & development.

[54]  Heng Li Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM , 2013, 1303.3997.

[55]  Roderic Guigó,et al.  The GEM mapper: fast, accurate and versatile alignment by filtration , 2012, Nature Methods.

[56]  R. Löwer,et al.  The non-autonomous retrotransposon SVA is trans-mobilized by the human LINE-1 protein machinery , 2011, Nucleic acids research.

[57]  S. Dimauro,et al.  Pathogenic exon-trapping by SVA retrotransposon and rescue in Fukuyama muscular dystrophy , 2011, Nature.

[58]  H. Kazazian,et al.  Retrotransposition of marked SVA elements by human L1s in cultured cells. , 2011, Human molecular genetics.

[59]  Adrian M. Stütz,et al.  A Comprehensive Map of Mobile Element Insertion Polymorphisms in Humans , 2011, PLoS genetics.

[60]  H. Kazazian,et al.  Whole-genome resequencing allows detection of many rare LINE-1 insertion alleles in humans. , 2011, Genome research.

[61]  M. DePristo,et al.  A framework for variation discovery and genotyping using next-generation DNA sequencing data , 2011, Nature Genetics.

[62]  Heng Li,et al.  Tabix: fast retrieval of sequence features from generic TAB-delimited files , 2011, Bioinform..

[63]  H. Kazazian,et al.  High-throughput sequencing reveals extensive variation in human-specific L1 content in individual human genomes. , 2010, Genome research.

[64]  Evan E. Eichler,et al.  LINE-1 Retrotransposition Activity in Human Genomes , 2010, Cell.

[65]  Helen M. Rowe,et al.  KAP1 controls endogenous retroviruses in embryonic stem cells , 2010, Nature.

[66]  Katsushi Tokunaga,et al.  Exon-trapping mediated by the human retrotransposon SVA. , 2009, Genome research.

[67]  E. Ostertag,et al.  L1 retrotransposition occurs mainly in embryogenesis and creates somatic mosaicism. , 2009, Genes & development.

[68]  P. D. de Jong,et al.  L1 retrotransposition can occur early in human embryonic development. , 2007, Human molecular genetics.

[69]  Ryan E. Mills,et al.  Which transposable elements are active in the human genome? , 2007, Trends in genetics : TIG.

[70]  M. Batzer,et al.  Extensive individual variation in L1 retrotransposition capability contributes to human genetic diversity. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[71]  Michael Q. Zhang,et al.  Large-scale structure of genomic methylation patterns. , 2005, Genome research.

[72]  Stéphane Boissinot,et al.  Molecular evolution and tempo of amplification of human LINE-1 retrotransposons since the origin of primates. , 2005, Genome research.

[73]  Jeffrey S. Han,et al.  Gene-breaking: a new paradigm for human retrotransposon-mediated gene evolution. , 2005, Genome research.

[74]  Ewan Birney,et al.  Automated generation of heuristics for biological sequence comparison , 2005, BMC Bioinformatics.

[75]  Thierry Heidmann,et al.  LINE-mediated retrotransposition of marked Alu sequences , 2003, Nature Genetics.

[76]  J. V. Moran,et al.  Hot L1s account for the bulk of retrotransposition in the human population , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[77]  J. V. Moran,et al.  ATLAS: a system to selectively identify human-specific L1 insertions. , 2003, American journal of human genetics.

[78]  Tom H. Pringle,et al.  The human genome browser at UCSC. , 2002, Genome research.

[79]  E. Ostertag,et al.  Twin priming: a proposed mechanism for the creation of inversions in L1 retrotransposition. , 2001, Genome research.

[80]  Jef D. Boeke,et al.  Human L1 Retrotransposition: cisPreference versus trans Complementation , 2001, Molecular and Cellular Biology.

[81]  Thierry Heidmann,et al.  Human LINE retrotransposons generate processed pseudogenes , 2000, Nature Genetics.

[82]  M. Boguski,et al.  Frequent human genomic DNA transduction driven by LINE-1 retrotransposition. , 2000, Genome research.

[83]  E. Ostertag,et al.  Transduction of 3'-flanking sequences is common in L1 retrotransposition. , 2000, Human molecular genetics.

[84]  J. V. Moran,et al.  Exon shuffling by L1 retrotransposition. , 1999, Science.

[85]  C. Walsh,et al.  Cytosine methylation and the ecology of intragenomic parasites. , 1997, Trends in genetics : TIG.

[86]  J. Jurka,et al.  Sequence patterns indicate an enzymatic involvement in integration of mammalian retroposons. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[87]  Jef D Boeke,et al.  High Frequency Retrotransposition in Cultured Mammalian Cells , 1996, Cell.

[88]  T. Fanning,et al.  Differential methylation of human LINE-1 retrotransposons in malignant cells. , 1996, Gene.

[89]  M. Surani,et al.  Peg1/Mest imprinted gene on chromosome 6 identified by cDNA subtraction hybridization , 1995, Nature Genetics.

[90]  R. E. Thayer,et al.  Undermethylation of specific LINE-1 sequences in human cells producing a LINE-1-encoded protein. , 1993, Gene.

[91]  T. Eickbush,et al.  Reverse transcription of R2Bm RNA is primed by a nick at the chromosomal target site: A mechanism for non-LTR retrotransposition , 1993, Cell.

[92]  S. Davies,et al.  Imprinting in Albright's hereditary osteodystrophy. , 1993, Journal of medical genetics.

[93]  A. F. Scott,et al.  Isolation of an active human transposable element. , 1991, Science.

[94]  D. Mager,et al.  Homologous recombination between the LTRs of a human retrovirus-like element causes a 5-kb deletion in two siblings. , 1989, American journal of human genetics.

[95]  S. Antonarakis,et al.  Haemophilia A resulting from de novo insertion of L1 sequences represents a novel mechanism for mutation in man , 1988, Nature.

[96]  G. Fink,et al.  Ty elements transpose through an RNA intermediate , 1985, Cell.

[97]  Piero Carninci,et al.  Edinburgh Research Explorer Endogenous Retrotransposition Activates Oncogenic Pathways in Hepatocellular Carcinoma Endogenous Retrotransposition Activates Oncogenic Pathways in Hepatocellular Carcinoma , 2022 .

[98]  Elizabeth M. Smigielski,et al.  dbSNP: the NCBI database of genetic variation , 2001, Nucleic Acids Res..