Discovery and characterization of Alu repeat sequences via precise local read assembly

Nucleic Acids Research

Volumn 43, Issue 21, 2015, Pages 10292-10307

  Wildschutte, Julia H ^a   Baron, Alayna ^a   Diroff, Nicolette M ^a   Kidd, Jeffrey M ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RNA;

ALU GENE; ARTICLE; CONTROLLED STUDY; DE NOVO ASSEMBLY; DNA TRANSPOSITION; GENE; GENE INSERTION; GENE SEQUENCE; GENETIC ANALYSIS; GENETIC VARIABILITY; GENOTYPE; HAPLOTYPE; HUMAN; NUCLEOTIDE BINDING SITE; OPEN READING FRAME; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; WHOLE GENOME SEQUENCE; ALU SEQUENCE; CHROMOSOME BREAKAGE; DNA SEQUENCE; GENOMICS; GENOTYPING TECHNIQUE; HUMAN GENOME; PROCEDURES;

ALU ELEMENTS; CHROMOSOME BREAKPOINTS; GENOME, HUMAN; GENOMICS; GENOTYPING TECHNIQUES; HUMANS; SEQUENCE ANALYSIS, DNA;

EID: 84964372657     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv1089     Document Type: Article

References (94)

1. Kazazian, H.H. Jr (2004) Mobile elements: drivers of genome evolution. Science, 303, 1626-1632.
2. Batzer, M.A. and Deininger, P.L. (2002) Alu repeats and human genomic diversity. Nat. Rev. Genet., 3, 370-379.
3. McPherson, J.D., Marra, M., Hillier, L., Waterston, R.H., Chinwalla, A., Wallis, J., Sekhon, M., Wylie, K., Mardis, E.R., Wilson, R.K. et al. (2001) A physical map of the human genome. Nature, 409, 934-941.
4. Kano, H., Godoy, I., Courtney, C., Vetter, M.R., Gerton, G.L., Ostertag, E.M. and Kazazian, H.H. Jr (2009) L1 retrotransposition occurs mainly in embryogenesis and creates somatic mosaicism. Genes Dev., 23, 1303-1312.
5. Mills, R.E., Bennett, E.A., Iskow, R.C. and Devine, S.E. (2007) Which transposable elements are active in the human genome? Trends Genet., 23, 183-191.
6. Richardson, S.R., Morell, S. and Faulkner, G.J. (2014) L1 retrotransposons and somatic mosaicism in the brain. Annu. Rev. Genet., 48, 1-27.
7. Deininger, P. (2011) Alu elements: know the SINEs. Genome Biol., 12, 236.
8. Jurka, J. and Smith, T. (1988) A fundamental division in the Alu family of repeated sequences. Proc. Natl. Acad. Sci. U.S.A., 85, 4775-4778.
9. Bennett, E.A., Keller, H., Mills, R.E., Schmidt, S., Moran, J.V., Weichenrieder, O. and Devine, S.E. (2008) Active Alu retrotransposons in the human genome. Genome Res., 18, 1875-1883.
10. Stewart, C., Kural, D., Stromberg, M.P., Walker, J.A., Konkel, M.K., Stutz, A.M., Urban, A.E., Grubert, F., Lam, H.Y., Lee, W.P. et al. (2011) A comprehensive map of mobile element insertion polymorphisms in humans. PLoS Genet., 7, e1002236.
11. 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. et al. (2009) Mobile elements create structural variation: analysis of a complete human genome. Genome Res., 19, 1516-1526.
12. 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.
13. Wang, J., Song, L., Gonder, M.K., Azrak, S., Ray, D.A., Batzer, M.A., Tishkoff, S.A. and Liang, P. (2006) Whole genome computational comparative genomics: A fruitful approach for ascertaining Alu insertion polymorphisms. Gene, 365, 11-20.
14. Mustafa, H., David, M. and Brudno, M. (2015) Assembly and characterization of novel Alu inserts detected from next-generation sequencing data. Moile Genet. Elem., 4, 1-7.
15. Carroll, M.L., Roy-Engel, A.M., Nguyen, S.V., Salem, A.H., Vogel, E., Vincent, B., Myers, J., Ahmad, Z., Nguyen, L., Sammarco, M. et al. (2001) Large-scale analysis of the Alu Ya5 and Yb8 subfamilies and their contribution to human genomic diversity. J. Mol. Biol., 311, 17-40.
16. Cordaux, R., Hedges, D.J., Herke, S.W. and Batzer, M.A. (2006) Estimating the retrotransposition rate of human Alu elements. Gene, 373, 134-137.
17. Callinan, P.A. and Batzer, M.A. (2006) Retrotransposable elements and human disease. Genome Dyn., 1, 104-115.
18. Hancks, D.C. and Kazazian, H.H. Jr (2012) Active human retrotransposons: Variation and disease. Curr. Opin. Genet. Dev., 22, 191-203.
19. Solyom, S. and Kazazian, H.H. Jr (2012) Mobile elements in the human genome: implications for disease. Genome Med., 4, 12.
20. 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.
21. Callinan, P.A., Wang, J., Herke, S.W., Garber, R.K., Liang, P. and Batzer, M.A. (2005) Alu retrotransposition-mediated deletion. J. Mol. Biol., 348, 791-800.
22. Franke, G., Bausch, B., Hoffmann, M.M., Cybulla, M., Wilhelm, C., Kohlhase, J., Scherer, G. and Neumann, H.P. (2009) Alu-Alu recombination underlies the vast majority of large VHL germline deletions: Molecular characterization and genotype-phenotype correlations in VHL patients. Hum. Mutat., 30, 776-786.
23. Ade, C., Roy-Engel, A.M. and Deininger, P.L. (2013) Alu elements: an intrinsic source of human genome instability. Curr. Opin. Virol., 3, 639-645.
24. Vissers, L.E., Bhatt, S.S., Janssen, I.M., Xia, Z., Lalani, S.R., Pfundt, R., Derwinska, K., de Vries, B.B., Gilissen, C., Hoischen, A. et al. (2009) Rare pathogenic microdeletions and tandem duplications are microhomology-mediated and stimulated by local genomic architecture. Hum. Mol. Genet., 18, 3579-3593.
25. Hedges, D.J. and Deininger, P.L. (2007) Inviting instability: Transposable elements, double-strand breaks, and the maintenance of genome integrity. Mutat. Res., 616, 46-59.
26. Morales, M.E., White, T.B., Streva, V.A., DeFreece, C.B., Hedges, D.J. and Deininger, P.L. (2015) The contribution of alu elements to mutagenic DNA double-strand break repair. PLoS Genet., 11, e1005016.
27. Fuhrman, S.A., Deininger, P.L., LaPorte, P., Friedmann, T. and Geiduschek, E.P. (1981) Analysis of transcription of the human Alu family ubiquitous repeating element by eukaryotic RNA polymerase III. Nucleic Acids Res., 9, 6439-6456.
28. Dewannieux, M., Esnault, C. and Heidmann, T. (2003) LINE-mediated retrotransposition of marked Alu sequences. Nat. Genet., 35, 41-48.
29. van de Lagemaat, L.N., Gagnier, L., Medstrand, P. and Mager, D.L. (2005) Genomic deletions and precise removal of transposable elements mediated by short identical DNA segments in primates. Genome Res., 15, 1243-1249.
30. Srikanta, D., Sen, S.K., Conlin, E.M. and Batzer, M.A. (2009) Internal priming: an opportunistic pathway for L1 and Alu retrotransposition in hominins. Gene, 448, 233-241.
31. Chen, J.M., Ferec, C. and Cooper, D.N. (2007) Mechanism of Alu integration into the human genome. Genomic Med., 1, 9-17.
32. Iskow, R.C., McCabe, M.T., Mills, R.E., Torene, S., Pittard, W.S., Neuwald, A.F., Van Meir, E.G., Vertino, P.M. and Devine, S.E. (2010) Natural mutagenesis of human genomes by endogenous retrotransposons. Cell, 141, 1253-1261.
33. Witherspoon, D.J., Xing, J., Zhang, Y., Watkins, W.S., Batzer, M.A. and Jorde, L.B. (2010) Mobile element scanning (ME-Scan) by targeted high-throughput sequencing. BMC Genomics, 11, 410.
34. Witherspoon, D.J., Zhang, Y., Xing, J., Watkins, W.S., Ha, H., Batzer, M.A. and Jorde, L.B. (2013) Mobile element scanning (ME-Scan) identifies thousands of novel Alu insertions in diverse human populations. Genome Res., 23, 1170-1181.
35. Hormozdiari, F., Alkan, C., Ventura, M., Hajirasouliha, I., Malig, M., Hach, F., Yorukoglu, D., Dao, P., Bakhshi, M., Sahinalp, S.C. et al. (2011) Alu repeat discovery and characterization within human genomes. Genome Res., 21, 840-849.
36. Keane, T.M., Wong, K. and Adams, D.J. (2013) RetroSeq: transposable element discovery from next-generation sequencing data. Bioinformatics, 29, 389-390.
37. David, M., Mustafa, H. and Brudno, M. (2013) Detecting Alu insertions from high-throughput sequencing data. Nucleic Acids Res., 41, e169.
38. Lee, E., Iskow, R., Yang, L., Gokcumen, O., Haseley, P., Luquette, L.J. 3rd, Lohr, J.G., Harris, C.C., Ding, L., Wilson, R.K. et al. (2012) Landscape of somatic retrotransposition in human cancers. Science, 337, 967-971.
39. Thung, D., de Ligt, J., Vissers, L., Steehouwer, M., Kroon, M., de Vries, P., Slagboom, E.P., Ye, K., Veltman, J.A. and Hehir-Kwa, J.Y. (2014) Mobster: Accurate detection of mobile element insertions in next generation sequencing data. Genome Biol., 15, 488.
40. Wu, J., Lee, W.P., Ward, A., Walker, J.A., Konkel, M.K., Batzer, M.A. and Marth, G.T. (2014) Tangram: a comprehensive toolbox for mobile element insertion detection. BMC Genomics, 15, 795.
41. Tubio, J.M., Li, Y., Ju, Y.S., Martincorena, I., Cooke, S.L., Tojo, M., Gundem, G., Pipinikas, C.P., Zamora, J., Raine, K. et al. (2014) Mobile DNA in cancer. Extensive transduction of nonrepetitive DNA mediated by L1 retrotransposition in cancer genomes. Science, 345, 1251343.
42. Chen, K., Chen, L., Fan, X., Wallis, J., Ding, L. and Weinstock, G. (2014) TIGRA: A targeted iterative graph routing assembler for breakpoint assembly. Genome Res., 24, 310-317.
43. Malhotra, A., Lindberg, M., Faust, G.G., Leibowitz, M.L., Clark, R.A., Layer, R.M., Quinlan, A.R. and Hall, I.M. (2013) Breakpoint profiling of 64 cancer genomes reveals numerous complex rearrangements spawned by homology-independent mechanisms. Genome Res., 23, 762-776.
44. Simpson, J.T. and Durbin, R. (2012) Efficient de novo assembly of large genomes using compressed data structures. Genome Res., 22, 549-556.
45. Wong, K., Keane, T.M., Stalker, J. and Adams, D.J. (2010) Enhanced structural variant and breakpoint detection using SVMerge by integration of multiple detection methods and local assembly. Genome Biol., 11, R128.
46. Narzisi, G., O'Rawe, J.A., Iossifov, I., Fang, H., Lee, Y.H., Wang, Z., Wu, Y., Lyon, G.J., Wigler, M. and Schatz, M.C. (2014) Accurate de novo and transmitted indel detection in exome-capture data using microassembly. Nat. Methods, 11, 1033-1036.
47. Li, S., Li, R., Li, H., Lu, J., Li, Y., Bolund, L., Schierup, M.H. and Wang, J. (2013) SOAPindel: Efficient identification of indels from short paired reads. Genome Res., 23, 195-200.
48. Iqbal, Z., Caccamo, M., Turner, I., Flicek, P. and McVean, G. (2012) De novo assembly and genotyping of variants using colored de Bruijn graphs. Nat. Genet., 44, 226-232.
49. Li, H. (2012) Exploring single-sample SNP and INDEL calling with whole-genome de novo assembly. Bioinformatics, 28, 1838-1844.
50. Rimmer, A., Phan, H., Mathieson, I., Iqbal, Z., Twigg, S.R., Consortium, W.G.S., Wilkie, A.O., McVean, G. and Lunter, G. (2014) Integrating mapping-, assembly- and haplotype-based approaches for calling variants in clinical sequencing applications. Nat. Genet., 46, 912-918.
51. Cann, H.M., de Toma, C., Cazes, L., Legrand, M.F., Morel, V., Piouffre, L., Bodmer, J., Bodmer, W.F., Bonne-Tamir, B., Cambon-Thomsen, A. et al. (2002) A human genome diversity cell line panel. Science, 296, 261-262.
52. Martin, A.R., Costa, H.A., Lappalainen, T., Henn, B.M., Kidd, J.M., Yee, M.C., Grubert, F., Cann, H.M., Snyder, M., Montgomery, S.B. et al. (2014) Transcriptome sequencing from diverse human populations reveals differentiated regulatory architecture. PLoS Genet., 10, e1004549.
53. Chaisson, M.J., Huddleston, J., Dennis, M.Y., Sudmant, P.H., Malig, M., Hormozdiari, F., Antonacci, F., Surti, U., Sandstrom, R., Boitano, M. et al. (2015) Resolving the complexity of the human genome using single-molecule sequencing. Nature, 517, 608-611.
54. McKenna, A., Hanna, M., Banks, E., Sivachenko, A., Cibulskis, K., Kernytsky, A., Garimella, K., Altshuler, D., Gabriel, S., Daly, M. et al. (2010) The genome Analysis toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res., 20, 1297-1303.
55. Jurka, J., Kapitonov, V.V., Pavlicek, A., Klonowski, P., Kohany, O. and Walichiewicz, J. (2005) Repbase Update, a database of eukaryotic repetitive elements. Cytogenetic Genome Res., 110, 462-467.
56. Smit, A.F., Hubley, R. and Green, P. (2013) RepeatMasker Open-4.0, 4.0 ed, http://www.repeatmasker.org.
57. Quinlan, A.R. (2014) BEDTools: The Swiss-Army Tool for Genome Feature Analysis. Baxevanis, AD (ed). Current protocols in bioinformatics. Vol. 47, pp. 11-34.
58. Huang, X. and Madan, A. (1999) CAP3: A DNA sequence assembly program. Genome Res., 9, 868-877.
59. Kidd, J.M., Graves, T., Newman, T.L., Fulton, R., Hayden, H.S., Malig, M., Kallicki, J., Kaul, R., Wilson, R.K. and Eichler, E.E. (2010) A human genome structural variation sequencing resource reveals insights into mutational mechanisms. Cell, 143, 837-847.
60. Kidd, J.M., Sampas, N., Antonacci, F., Graves, T., Fulton, R., Hayden, H.S., Alkan, C., Malig, M., Ventura, M., Giannuzzi, G. et al. (2010) Characterization of missing human genome sequences and copy-number polymorphic insertions. Nat. Methods, 7, 365-371.
61. Kent, W.J. (2002) BLAT-the BLAST-like alignment tool. Genome Res., 12, 656-664.
62. Parsons, J. (1995) Miropeats: graphical DNA sequence comparisons. Comput. Appl. Biosci., 11, 615-619.
63. Rice, P., Longden, I. and Bleasby, A. (2000) EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet., 16, 276-277.
64. Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res., 32, 1792-1797.
65. Koressaar, T. and Remm, M. (2007) Enhancements and modifications of primer design program Primer3. Bioinformatics, 23, 1289-1291.
66. Kent, W.J., Sugnet, C.W., Furey, T.S., Roskin, K.M., Pringle, T.H., Zahler, A.M. and Haussler, D. (2002) The human genome browser at UCSC. Genome Res., 12, 996-1006.
67. Hormozdiari, F., Konkel, M.K., Prado-Martinez, J., Chiatante, G., Herraez, I.H., Walker, J.A., Nelson, B., Alkan, C., Sudmant, P.H., Huddleston, J. et al. (2013) Rates and patterns of great ape retrotransposition. Proc. Natl. Acad. Sci. U.S.A., 110, 13457-13462.
68. Gilbert, N., Lutz, S., Morrish, T.A. and Moran, J.V. (2005) Multiple fates of L1 retrotransposition intermediates in cultured human cells. Mol. Cell. Biol., 25, 7780-7795.
69. Li, H. (2011) A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data. Bioinformatics, 27, 2987-2993.
70. Browning, S.R. and Browning, B.L. (2007) Rapid and accurate haplotype phasing and missing-data inference for whole-genome association studies by use of localized haplotype clustering. Am. J. Hum. Genet., 81, 1084-1097.
71. Browning, B.L. and Browning, S.R. (2009) A unified approach to genotype imputation and haplotype-phase inference for large data sets of trios and unrelated individuals. Am. J. Hum. Genet., 84, 210-223.
72. DePristo, M.A., Banks, E., Poplin, R., Garimella, K.V., Maguire, J.R., Hartl, C., Philippakis, A.A., del Angel, G., Rivas, M.A., Hanna, M. et al. (2011) A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat. Genet., 43, 491-498.
73. Patterson, N., Price, A.L. and Reich, D. (2006) Population structure and eigenanalysis. PLoS Genet., 2, e190.
74. Lee, H. and Tang, H. (2012) Next-generation sequencing technologies and fragment assembly algorithms. Methods Mol. Biol., 855, 155-174.
75. Li, H. and Homer, N. (2010) A survey of sequence alignment algorithms for next-generation sequencing. Brief. Bioinform., 11, 473-483.
76. Miller, J.R., Koren, S. and Sutton, G. (2010) Assembly algorithms for next-generation sequencing data. Genomics, 95, 315-327.
77. Yang, Y. and Smith, S.A. (2013) Optimizing de novo assembly of short-read RNA-seq data for phylogenomics. BMC Genomics, 14, 328.
78. Reddy, R.M., Mohammed, M.H. and Mande, S.S. (2014) MetaCAA: A clustering-aided methodology for efficient assembly of metagenomic datasets. Genomics, 103, 161-168.
79. Lander, E.S., Linton, L.M., Birren, B., Nusbaum, C., Zody, M.C., Baldwin, J., Devon, K., Dewar, K., Doyle, M., FitzHugh, W. et al. (2001) Initial sequencing and analysis of the human genome. Nature, 409, 860-921.
80. 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.
81. Klein, J., Sato, A., Nagl, S. and O'hiUigin. (1998) Molecular trans-species polymorphism. Annu. Rev. Ecol. Syst., 29, 1-21.
82. Zingler, N., Willhoeft, U., Brose, H.P., Schoder, V., Jahns, T., Hanschmann, K.M., Morrish, T.A., Lower, J. and Schumann, G.G. (2005) Analysis of 5′ junctions of human LINE-1 and Alu retrotransposons suggests an alternative model for 5′-end attachment requiring microhomology-mediated end-joining. Genome Res., 15, 780-789.
83. Srikanta, D., Sen, S.K., Huang, C.T., Conlin, E.M., Rhodes, R.M. and Batzer, M.A. (2009) An alternative pathway for Alu retrotransposition suggests a role in DNA double-strand break repair. Genomics, 93, 205-212.
84. Harrow, J., Frankish, A., Gonzalez, J.M., Tapanari, E., Diekhans, M., Kokocinski, F., Aken, B.L., Barrell, D., Zadissa, A., Searle, S. et al. (2012) GENCODE: the reference human genome annotation for The ENCODE Project. Genome Res., 22, 1760-1774.
85. Nielsen, R., Paul, J.S., Albrechtsen, A. and Song, Y.S. (2011) Genotype and SNP calling from next-generation sequencing data. Nat. Rev. Genet., 12, 443-451.
86. Hammer, M.F. (1994) A recent insertion of an alu element on the Y chromosome is a useful marker for human population studies. Mol. Biol. Evol., 11, 749-761.
87. Lee, J.A., Carvalho, C.M. and Lupski, J.R. (2007) A DNA replication mechanism for generating nonrecurrent rearrangements associated with genomic disorders. Cell, 131, 1235-1247.
88. Smith, C.E., Llorente, B. and Symington, L.S. (2007) Template switching during break-induced replication. Nature, 447, 102-105.
89. Onozawa, M., Zhang, Z., Kim, Y.J., Goldberg, L., Varga, T., Bergsagel, P.L., Kuehl, W.M. and Aplan, P.D. (2014) Repair of DNA double-strand breaks by templated nucleotide sequence insertions derived from distant regions of the genome. Proc. Natl. Acad. Sci. U.S.A., 111, 7729-7734.
90. Ono, R., Ishii, M., Fujihara, Y., Kitazawa, M., Usami, T., Kaneko-Ishino, T., Kanno, J., Ikawa, M. and Ishino, F. (2015) Double strand break repair by capture of retrotransposon sequences and reverse-transcribed spliced mRNA sequences in mouse zygotes. Scientific Rep., 5, 12281.
91. Feng, Q., Moran, J.V., Kazazian, H.H. Jr and Boeke, J.D. (1996) Human L1 retrotransposon encodes a conserved endonuclease required for retrotransposition. Cell, 87, 905-916.
92. Cost, G.J. and Boeke, J.D. (1998) Targeting of human retrotransposon integration is directed by the specificity of the L1 endonuclease for regions of unusual DNA structure. Biochemistry, 37, 18081-18093.
93. Piskareva, O. and Schmatchenko, V. (2006) DNA polymerization by the reverse transcriptase of the human L1 retrotransposon on its own template in vitro. FEBS Lett., 580, 661-668.
94. Weichenrieder, O., Wild, K., Strub, K. and Cusack, S. (2000) Structure and assembly of the Alu domain of the mammalian signal recognition particle. Nature, 408, 167-173.