Mobile element scanning (ME-Scan) identifies thousands of novel Alu insertions in diverse human populations

Genome Research

Volumn 23, Issue 7, 2013, Pages 1170-1181

  Witherspoon, David J ^a   Zhang, Yuhua ^b   Xing, Jinchuan ^b   Watkins, W Scott ^a   Ha, Hongseok ^b   Batzer, Mark A ^c   Jorde, Lynn B ^a  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^b Life Sciences Building Rutgers University   (United States)

^c LOUISIANA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALUMINUM;

AFRICA; ARTICLE; ELECTROPHORESIS; EUROPE; GENE INSERTION SEQUENCE; GENE SEQUENCE; GENETIC VARIABILITY; HUMAN; MOBILE ELEMENT INSERTION; MOBILE ELEMENT SCANNING; POLYMERASE CHAIN REACTION; POPULATION GENETICS; PRIORITY JOURNAL; RETROPOSON; SENSITIVITY AND SPECIFICITY; SOUTH ASIA;

ALU ELEMENTS; DNA REPLICATION; EXONS; GENETIC LOCI; GENOME, HUMAN; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; MUTAGENESIS, INSERTIONAL; POLYMORPHISM, GENETIC; POPULATION GROUPS; REPRODUCIBILITY OF RESULTS; RETROELEMENTS; SENSITIVITY AND SPECIFICITY; TRANSCRIPTION, GENETIC;

EID: 84880066634     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.148973.112     Document Type: Article

References (58)

1. The 1000 Genomes Project Consortium. 2010. Amap of human genome variation from population-scale sequencing. Nature 467: 1061-1073.
2. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J Mol Biol 215: 403-410.
3. Altshuler DM, Gibbs RA, Peltonen L, Dermitzakis E, Schaffner SF, Yu F, Bonnen PE, de Bakker PI, Deloukas P, Gabriel SB, et al. 2010. Integrating common and rare genetic variation in diverse human populations. Nature 467: 52-58.
4. Badge RM, Alisch RS, Moran JV. 2003. ATLAS: A system to selectively identify human-specific L1 insertions. Am J Hum Genet 72: 823-838.
5. Baillie JK, Barnett MW, Upton KR, Gerhardt DJ, Richmond TA, De Sapio F, Brennan PM, Rizzu P, Smith S, Fell M, et al. 2011. Somatic retrotransposition alters the genetic landscape of the human brain. Nature 479: 534-537.
6. Bamshad MJ, Watkins WS, Dixon ME, Jorde LB, Rao BB, Naidu JM, Prasad BV, Rasanayagam A, Hammer MF. 1998. Female gene flow stratifies Hindu castes. Nature 395: 651-652.
7. Beck CR, Garcia-Perez JL, Badge RM, Moran JV. 2011. LINE-1 elements in structural variation and disease. Annu Rev Genomics Hum Genet 12: 187-215.
8. Boissinot S, Entezam A, Young L, Munson PJ, Furano AV. 2004. The insertional history of an active family of L1 retrotransposons in humans. Genome Res 14: 1221-1231.
9. Buzdin A, Khodosevich K, Mamedov I, Vinogradova T, Lebedev Y, Hunsmann G, Sverdlov E. 2002. A technique for genome-wide identification of differences in the interspersed repeats integrations between closely related genomes and its application to detection of human-specific integrations of HERV-K LTRs. Genomics 79: 413-422.
10. Cordaux R, Batzer MA. 2009. The impact of retrotransposons on human genome evolution. Nat Rev Genet 10: 691-703.
11. Cordaux R, Srikanta D, Lee J, Stoneking M, Batzer MA. 2007. In search of polymorphic Alu insertions with restricted geographic distributions. Genomics 90: 154-158.
12. Coufal NG, Garcia-Perez JL, Peng GE, Yeo GW, Mu Y, Lovci MT, Morell M, O'Shea KS, Moran JV, Gage FH. 2009. L1 retrotransposition in human neural progenitor cells. Nature 460: 1127-1131.
13. De Cecco M, Criscione SW, Peckham EJ, Hillenmeyer S, Hamm EA, Manivannan J, Peterson AL, Kreiling JA, Neretti N, Sedivy JM. 2013. Genomes of replicatively senescent cells undergo global epigenetic changes leading to gene silencing and activation of transposable elements. Aging Cell 12: 247-256.
14. de Koning AP, Gu W, Castoe TA, Batzer MA, Pollock DD. 2011. Repetitive elements may comprise over two-thirds of the human genome. PLoS Genet 7: e1002384.
15. Derrien T, Estelle J, Marco Sola S, Knowles DG, Raineri E, Guigo R, Ribeca P. 2012. Fast computation and applications of genome mappability. PLoS ONE 7: e30377.
16. Evrony GD, Cai X, Lee E, Hills LB, Elhosary PC, Lehmann HS, Parker JJ, Atabay KD, Gilmore EC, Poduri A, et al. 2012. Single-neuron sequencing analysis of L1 retrotransposition and somatic mutation in the human brain. Cell 151: 483-496.
17. Ewing AD, Kazazian HH Jr. 2010. High-throughput sequencing reveals extensive variation in human-specific L1 content in individual human genomes. Genome Res 20: 1262-1270.
18. Genome 10K Community of Scientists. 2009. Genome 10K: A proposal to obtain whole-genome sequence for 10,000 vertebrate species. J Hered 100: 659-674.
19. Gravel S, Henn BM, Gutenkunst RN, Indap AR, Marth GT, Clark AG, Yu F, Gibbs RA, Bustamante CD. 2011. Demographic history and rare allele sharing among human populations. Proc Natl Acad Sci 108: 11983-11988.
20. Hormozdiari F, Alkan C, Ventura M, Hajirasouliha I, Malig M, Hach F, Yorukoglu D, Dao P, Bakhshi M, Sahinalp SC, et al. 2011. Alu repeat discovery and characterization within human genomes. Genome Res 21: 840-849.
21. Huang CR, Schneider AM, Lu Y, Niranjan T, Shen P, RobinsonMA, Steranka JP, Valle D, Civin CI,Wang T, et al. 2010.Mobile interspersed repeats are major structural variants in the human genome. Cell 141: 1171-1182.
22. International Human Genome Sequencing Consortium. 2001. Initial sequencing and analysis of the human genome. Nature 409: 860-921.
23. Iskow RC, McCabe MT, Mills RE, Torene S, Pittard WS, Neuwald AF, Van Meir EG, Vertino PM, Devine SE. 2010. Natural mutagenesis of human genomes by endogenous retrotransposons. Cell 141: 1253-1261.
24. Jiang N, Bao Z, Zhang X, Hirochika H, Eddy SR, McCouch SR, Wessler SR. 2003. An active DNA transposon family in rice. Nature 421: 163-167.
25. Jorde LB, Bamshad MJ, Watkins WS, Zenger R, Fraley AE, Krakowiak PA, Carpenter KD, Soodyall H, Jenkins T, Rogers AR. 1995. Origins and affinities of modern humans: A comparison of mitochondrial and nuclear genetic data. Am J Hum Genet 57: 523-538.
26. Jurka J. 1997. Sequence patterns indicate an enzymatic involvement in integration of mammalian retroposons. Proc Natl Acad Sci 94: 1872-1877.
27. Jurka J, Kohany O, Pavlicek A, Kapitonov VV, Jurka MV. 2004. Duplication, coclustering, and selection of human Alu retrotransposons. Proc Natl Acad Sci 101: 1268-1272.
28. Lee E, Iskow R, Yang L, Gokcumen O, Haseley P, Luquette LJ III, Lohr JG, Harris CC, Ding L, Wilson RK, et al. 2012. Landscape of somatic retrotransposition in human cancers. Science 337: 967-971.
29. Levy S, Sutton G, Ng PC, Feuk L, Halpern AL,Walenz BP, Axelrod N, Huang J, Kirkness EF, Denisov G, et al. 2007. The diploid genome sequence of an individual human. PLoS Biol 5: e254.
30. Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754-1760.
31. Li H, Durbin R. 2011. Inference of human population history from individual whole-genome sequences. Nature 475: 493-496.
32. Li JZ, Absher DM, Tang H, Southwick AM, Casto AM, Ramachandran S, Cann HM, Barsh GS, Feldman M, Cavalli-Sforza LL, et al. 2008. Worldwide human relationships inferred from genome-wide patterns of variation. Science 319: 1100-1104.
33. Lockton S, Ross-Ibarra J, Gaut BS. 2008. Demography and weak selection drive patterns of transposable element diversity in natural populations of Arabidopsis lyrata. Proc Natl Acad Sci 105: 13965-13970.
34. Macko A, Grzebelus D. 2008. DcMaster transposon display markers as a tool for diversity evaluation of carrot breeding materials and for hybrid seed purity testing. J Appl Genet 49: 33-39.
35. Mamedov IZ, Arzumanyan ES, Amosova AL, Lebedev YB, Sverdlov ED. 2005. Whole-genome experimental identification of insertion/deletion polymorphisms of interspersed repeats by a new general approach. Nucleic Acids Res 33: e16.
36. Medstrand P, van de Lagemaat LN, Mager DL. 2002. Retroelement distributions in the human genome: Variations associated with age and proximity to genes. Genome Res 12: 1483-1495.
37. Mitchell RS, Beitzel BF, Schroder AR, Shinn P, Chen H, Berry CC, Ecker JR, Bushman FD. 2004. Retroviral DNA integration: ASLV, HIV, and MLV show distinct target site preferences. PLoS Biol 2: E234.
38. Naito K, Zhang F, Tsukiyama T, Saito H, Hancock CN, Richardson AO, Okumoto Y, Tanisaka T, Wessler SR. 2009. Unexpected consequences of a sudden and massive transposon amplification on rice gene expression. Nature 461: 1130-1134.
39. Ovchinnikov I, Troxel AB, Swergold GD. 2001. Genomic characterization of recent human LINE-1 insertions: Evidence supporting random insertion. Genome Res 11: 2050-2058.
40. R Development Core Team. 2012. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
41. Rho M, Schaack S, Gao X, Kim S, Lynch M, Tang H. 2010. LTR retroelements in the genome of Daphnia pulex. BMC Genomics 11: 425.
42. Roy AM, Carroll ML, Kass DH, Nguyen SV, Salem AH, Batzer MA, Deininger PL. 1999. Recently integrated human Alu repeats: Finding needles in the haystack. Genetica 107: 149-161.
43. Schaack S, Pritham EJ, Wolf A, Lynch M. 2010. DNA transposon dynamics in populations of Daphnia pulex with and without sex. Proc Biol Sci 277: 2381-2387.
44. Schröder AR, Shinn P, Chen H, Berry C, Ecker JR, Bushman F. 2002. HIV-1 integration in the human genome favors active genes and local hotspots. Cell 110: 521-529.
45. Sheen FM, Sherry ST, Risch GM, Robichaux M, Nasidze I, Stoneking M, Batzer MA, Swergold GD. 2000. Reading between the LINEs: Human genomic variation induced by LINE-1 retrotransposition. Genome Res 10: 1496-1508.
46. Stewart C, Kural D, Stromberg MP, Walker JA, Konkel MK, Stutz AM, Urban AE, Grubert F, Lam HY, Lee WP, et al. 2011. A comprehensive map of mobile element insertion polymorphisms in humans. PLoS Genet 7: e1002236.
47. Toda Y, Saito R, Tomita M. 1998. Comprehensive sequence analyses of 59 flanking regions of primate Alu elements. Genome Inform Ser Workshop Genome Inform 9: 41-48.
48. Van den Broeck D, Maes T, Sauer M, Zethof J, De Keukeleire P, D'Hauw M, Van Montagu M, Gerats T. 1998. Transposon Display identifies individual transposable elements in high copy number lines. Plant J 13: 121-129.
49. Wang J, Song L, Grover D, Azrak S, Batzer MA, Liang P. 2006. dbRIP: A highly integrated database of retrotransposon insertion polymorphisms in humans. Hum Mutat 27: 323-329.
50. Wang GP, Ciuffi A, Leipzig J, Berry CC, Bushman FD. 2007. HIV integration site selection: Analysis by massively parallel pyrosequencing reveals association with epigenetic modifications. Genome Res 17: 1186-1194.
51. Watkins WS, Rogers AR, Ostler CT, Wooding S, Bamshad MJ, Brassington AM, Carroll ML, Nguyen SV, Walker JA, Prasad BV, et al. 2003. Genetic variation among world populations: Inferences from 100 Alu insertion polymorphisms. Genome Res 13: 1607-1618.
52. Wheelan SJ, Scheifele LZ, Martinez-Murillo F, Irizarry RA, Boeke JD. 2006. Transposon insertion site profiling chip (TIP-chip). Proc Natl Acad Sci 103: 17632-17637.
53. Witherspoon DJ, Marchani EE,Watkins WS, Ostler CT,Wooding SP, Anders BA, Fowlkes JD, Boissinot S, Furano AV, Ray DA, et al. 2006. Human population genetic structure and diversity inferred from polymorphic L1(LINE-1) and Alu insertions. Hum Hered 62: 30-46.
54. Witherspoon DJ, Xing J, Zhang Y, Watkins WS, Batzer MA, Jorde LB. 2010. Mobile element scanning (ME-Scan) by targeted high-throughput sequencing. BMC Genomics 11: 410.
55. Wu X, Li Y, Crise B, Burgess SM. 2003. Transcription start regions in the human genome are favored targets for MLV integration. Science 300: 1749-1751.
56. Xing J, Watkins WS, Witherspoon DJ, Zhang Y, Guthery SL, Thara R, Mowry BJ, Bulayeva K, Weiss RB, Jorde LB. 2009a. Fine-scaled human genetic structure revealed by SNP microarrays. Genome Res 19: 815-825.
57. Xing J, Zhang Y, Han K, Salem AH, Sen SK, Huff CD, Zhou Q, Kirkness EF, Levy S, Batzer MA, et al. 2009b. Mobile elements create structural variation: Analysis of a complete human genome. Genome Res 19: 1516-1526.
58. Xing J, Witherspoon DJ, Jorde LB. 2013. Mobile element biology: New possibilities with high-throughput sequencing. Trends Genet 29: 280-289.