Evidence for L1-associated DNA rearrangements and negligible L1 retrotransposition in glioblastoma multiforme

Mobile DNA

Volumn 7, Issue 1, 2016, Pages 1-14

  Carreira, Patricia E ^a   Ewing, Adam D ^a   Li, Guibo ^b,c   Schauer, Stephanie N ^a   Upton, Kyle R ^a   Fagg, Allister C ^a   Morell, Santiago ^a   Kindlova, Michaela ^a   Gerdes, Patricia ^a   Richardson, Sandra R ^a   Li, Bo ^b   Gerhardt, Daniel J ^a   Wang, Jun ^b,c   Brennan, Paul M ^d   Faulkner, Geoffrey J ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b BGI SHENZHEN   (China)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ENDONUCLEASE; EPIDERMAL GROWTH FACTOR RECEPTOR; METHYL CPG BINDING PROTEIN 2;

ALU SEQUENCE; ARTICLE; CLINICAL ARTICLE; DNA REARRANGEMENT; DNA RECOMBINATION; DNA STRUCTURE; DNA TRANSPOSITION; GENE INSERTION; GENE MUTATION; GENE SEQUENCE; GLIOBLASTOMA; GLIOMA; HUMAN; HUMAN CELL; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RETROPOSON;

EID: 84999622498     PISSN: None     EISSN: 17598753     Source Type: Journal    
DOI: 10.1186/s13100-016-0076-6     Document Type: Article

References (77)

1. Wen PY, Kesari S. Malignant gliomas in adults. N Engl J Med. 2008;359:492-507.
2. Bleeker FE, Molenaar RJ, Leenstra S. Recent advances in the molecular understanding of glioblastoma. J Neuro-Oncol. 2012;108:11-27.
3. Ohgaki H, Kleihues P. Genetic pathways to primary and secondary glioblastoma. Am J Pathol. 2007;170:1445-53.
4. Parsons DW, Jones S, Zhang X, Lin JC, Leary RJ, Angenendt P, Mankoo P, Carter H, Siu IM, Gallia GL, et al. An integrated genomic analysis of human glioblastoma multiforme. Science. 2008;321:1807-12.
5. Sottoriva A, Spiteri I, Piccirillo SG, Touloumis A, Collins VP, Marioni JC, Curtis C, Watts C, Tavare S. Intratumor heterogeneity in human glioblastoma reflects cancer evolutionary dynamics. Proc Natl Acad Sci U S A. 2013;110:4009-14.
6. Brennan Cameron W, Verhaak Roel GW, McKenna A, Campos B, Noushmehr H, Salama Sofie R, Zheng S, Chakravarty D, Sanborn JZ, Berman Samuel H, et al. The somatic genomic landscape of glioblastoma. Cell. 2013;155:462-77.
7. Maher EA, Brennan C, Wen PY, Durso L, Ligon KL, Richardson A, Khatry D, Feng B, Sinha R, Louis DN, et al. Marked genomic differences characterize primary and secondary glioblastoma subtypes and identify two distinct molecular and clinical secondary glioblastoma entities. Cancer Res. 2006;66:11502-13.
8. Fischer U, Meese E. Glioblastoma multiforme: the role of DSB repair between genotype and phenotype. Oncogene. 2007;26:7809-15.
9. Miki Y, Nishisho I, Horii A, Miyoshi Y, Utsunomiya J, Kinzler KW, Vogelstein B, Nakamura Y. Disruption of the APC gene by a retrotransposal insertion of L1 sequence in a colon cancer. Cancer Res. 1992;52:643-5.
10. Grimaldi G, Skowronski J, Singer MF. Defining the beginning and end of KpnI family segments. EMBO J. 1984;3:1753-9.
11. Scott AF, Schmeckpeper BJ, Abdelrazik M, Comey CT, O'Hara B, Rossiter JP, Cooley T, Heath P, Smith KD, Margolet L. Origin of the human L1 elements: proposed progenitor genes deduced from a consensus DNA sequence. Genomics. 1987;1:113-25.
12. Hohjoh H, Singer MF. Cytoplasmic ribonucleoprotein complexes containing human LINE-1 protein and RNA. EMBO J. 1996;15:630-9.
13. Kolosha VO, Martin SL. In vitro properties of the first ORF protein from mouse LINE-1 support its role in ribonucleoprotein particle formation during retrotransposition. Proc Natl Acad Sci U S A. 1997;94:10155-60.
14. Mathias SL, Scott AF, Kazazian Jr HH, Boeke JD, Gabriel A. Reverse transcriptase encoded by a human transposable element. Science. 1991;254:1808-10.
15. Feng Q, Moran JV, Kazazian Jr HH, Boeke JD. Human L1 retrotransposon encodes a conserved endonuclease required for retrotransposition. Cell. 1996;87:905-16.
16. Swergold GD. Identification, characterization, and cell specificity of a human LINE-1 promoter. Mol Cell Biol. 1990;10:6718-29.
17. Speek M. Antisense promoter of human L1 retrotransposon drives transcription of adjacent cellular genes. Mol Cell Biol. 2001;21:1973-85.
18. Denli AM, Narvaiza I, Kerman BE, Pena M, Benner C, Marchetto MC, Diedrich JK, Aslanian A, Ma J, Moresco JJ, et al. Primate-specific ORF0 contributes to retrotransposon-mediated diversity. Cell. 2015;163:583-93.
19. Luan DD, Korman MH, Jakubczak JL, Eickbush TH. Reverse transcription of R2Bm RNA is primed by a nick at the chromosomal target site: a mechanism for non-LTR retrotransposition. Cell. 1993;72:595-605.
20. Jurka J. Sequence patterns indicate an enzymatic involvement in integration of mammalian retroposons. Proc Natl Acad Sci U S A. 1997;94:1872-7.
21. Morrish TA, Garcia-Perez JL, Stamato TD, Taccioli GE, Sekiguchi J, Moran JV. Endonuclease-independent LINE-1 retrotransposition at mammalian telomeres. Nature. 2007;446:208-12.
22. Symer DE, Connelly C, Szak ST, Caputo EM, Cost GJ, Parmigiani G, Boeke JD. Human l1 retrotransposition is associated with genetic instability in vivo. Cell. 2002;110:327-38.
23. Morrish TA, Gilbert N, Myers JS, Vincent BJ, Stamato TD, Taccioli GE, Batzer MA, Moran JV. DNA repair mediated by endonuclease-independent LINE-1 retrotransposition. Nat Genet. 2002;31:159-65.
24. Sen SK, Huang CT, Han K, Batzer MA. Endonuclease-independent insertion provides an alternative pathway for L1 retrotransposition in the human genome. Nucleic Acids Res. 2007;35:3741-51.
25. Ahl V, Keller H, Schmidt S, Weichenrieder O. Retrotransposition and crystal structure of an Alu RNP in the ribosome-stalling conformation. Mol Cell. 2015;60:715-27.
26. Dewannieux M, Esnault C, Heidmann T. LINE-mediated retrotransposition of marked Alu sequences. Nat Genet. 2003;35:41-8.
27. Doucet AJ, Wilusz JE, Miyoshi T, Liu Y, Moran JV. A 3' Poly(A) tract is required for LINE-1 retrotransposition. Mol Cell. 2015;60:728-41.
28. Han K, Lee J, Meyer TJ, Remedios P, Goodwin L, Batzer MA. L1 recombination-associated deletions generate human genomic variation. Proc Natl Acad Sci U S A. 2008;105:19366-71.
29. Sen SK, Han K, Wang J, Lee J, Wang H, Callinan PA, Dyer M, Cordaux R, Liang P, Batzer MA. Human genomic deletions mediated by recombination between Alu elements. Am J Hum Genet. 2006;79:41-53.
30. Iskow RC, McCabe MT, Mills RE, Torene S, Pittard WS, Neuwald AF, Van Meir EG, Vertino PM, Devine SE. Natural mutagenesis of human genomes by endogenous retrotransposons. Cell. 2010;141:1253-61.
31. Tubio JM, Li Y, Ju YS, Martincorena I, Cooke SL, Tojo M, Gundem G, Pipinikas CP, Zamora J, Raine K, et al. Mobile DNA in cancer. Extensive transduction of nonrepetitive DNA mediated by L1 retrotransposition in cancer genomes. Science. 2014;345:1251343.
32. Lee E, Iskow R, Yang L, Gokcumen O, Haseley P, Luquette 3rd LJ, Lohr JG, Harris CC, Ding L, Wilson RK, et al. Landscape of somatic retrotransposition in human cancers. Science. 2012;337:967-71.
33. Solyom S, Ewing AD, Rahrmann EP, Doucet T, Nelson HH, Burns MB, Harris RS, Sigmon DF, Casella A, Erlanger B, et al. Extensive somatic L1 retrotransposition in colorectal tumors. Genome Res. 2012;22:2328-38.
34. Shukla R, Upton KR, Munoz-Lopez M, Gerhardt DJ, Fisher ME, Nguyen T, Brennan PM, Baillie JK, Collino A, Ghisletti S, et al. Endogenous retrotransposition activates oncogenic pathways in hepatocellular carcinoma. Cell. 2013;153:101-11.
35. Helman E, Lawrence ML, Stewart C, Sougnez C, Getz G, Meyerson M. Somatic retrotransposition in human cancer revealed by whole-genome and exome sequencing. Genome Res. 2014;24(7):1053-63.
36. Ewing AD, Gacita A, Wood LD, Ma F, Xing D, Kim MS, Manda SS, Abril G, Pereira G, Makohon-Moore A, et al. Widespread somatic L1 retrotransposition occurs early during gastrointestinal cancer evolution. Genome Res. 2015;25:1536-45.
37. Rodic N, Steranka JP, Makohon-Moore A, Moyer A, Shen P, Sharma R, Kohutek ZA, Huang CR, Ahn D, Mita P, et al. Retrotransposon insertions in the clonal evolution of pancreatic ductal adenocarcinoma. Nat Med. 2015;21:1060-4.
38. Doucet-O'Hare TT, Rodić N, Sharma R, Darbari I, Abril G, Choi JA, Young Ahn J, Cheng Y, Anders RA, Burns KH, et al. LINE-1 expression and retrotransposition in Barrett's esophagus and esophageal carcinoma. Proc Natl Acad Sci. 2015;112:E4894-900.
39. Baillie JK, Barnett MW, Upton KR, Gerhardt DJ, Richmond TA, De Sapio F, Brennan PM, Rizzu P, Smith S, Fell M, et al. Somatic retrotransposition alters the genetic landscape of the human brain. Nature. 2011;479:534-7.
40. Coufal NG, Garcia-Perez JL, Peng GE, Yeo GW, Mu Y, Lovci MT, Morell M, O'Shea KS, Moran JV, Gage FH. L1 retrotransposition in human neural progenitor cells. Nature. 2009;460:1127-31.
41. Evrony GD, Cai X, Lee E, Hills LB, Elhosary PC, Lehmann HS, Parker JJ, Atabay KD, Gilmore EC, Poduri A, et al. Single-neuron sequencing analysis of L1 retrotransposition and somatic mutation in the human brain. Cell. 2012;151:483-96.
42. Upton KR, Gerhardt DJ, Jesuadian JS, Richardson SR, Sanchez-Luque FJ, Bodea GO, Ewing AD, Salvador-Palomeque C, van der Knaap MS, Brennan PM, et al. Ubiquitous L1 mosaicism in hippocampal neurons. Cell. 2015;161:228-39.
43. Moran JV, Holmes SE, Naas TP, DeBerardinis RJ, Boeke JD, Kazazian Jr HH. High frequency retrotransposition in cultured mammalian cells. Cell. 1996;87:917-27.
44. Dombroski BA, Mathias SL, Nanthakumar E, Scott AF, Kazazian Jr HH. Isolation of an active human transposable element. Science. 1991;254:1805-8.
45. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R. The Sequence Alignment/Map format and SAMtools. Bioinformatics. 2009;25:2078-9.
46. Kent WJ. BLAT--the BLAST-like alignment tool. Genome Res. 2002;12:656-64.
47. Beck CR, Collier P, Macfarlane C, Malig M, Kidd JM, Eichler EE, Badge RM, Moran JV. LINE-1 retrotransposition activity in human genomes. Cell. 2010;141:1159-70.
48. Ewing AD, Kazazian Jr HH. High-throughput sequencing reveals extensive variation in human-specific L1 content in individual human genomes. Genome Res. 2010;20:1262-70.
49. Ewing AD, Kazazian Jr HH. Whole-genome resequencing allows detection of many rare LINE-1 insertion alleles in humans. Genome Res. 2011;21:985-90.
50. Kuhn A, Ong YM, Cheng CY, Wong TY, Quake SR, Burkholder WF. Linkage disequilibrium and signatures of positive selection around LINE-1 retrotransposons in the human genome. Proc Natl Acad Sci U S A. 2014;111:8131-6.
51. Wang J, Song L, Grover D, Azrak S, Batzer MA, Liang P. dbRIP: a highly integrated database of retrotransposon insertion polymorphisms in humans. Hum Mutat. 2006;27:323-9.
52. Rozen S, Skaletsky H. Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol. 2000;132:365-86.
53. Magoc T, Salzberg SL. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics. 2011;27:2957-63.
54. Saunders CT, Wong WS, Swamy S, Becq J, Murray LJ, Cheetham RK. Strelka: accurate somatic small-variant calling from sequenced tumor-normal sample pairs. Bioinformatics. 2012;28:1811-7.
55. Rimmer A, Phan H, Mathieson I, Iqbal Z, Twigg SR, Wilkie AO, McVean G, Lunter G. Integrating mapping-, assembly- and haplotype-based approaches for calling variants in clinical sequencing applications. Nat Genet. 2014;46:912-8.
56. Rausch T, Zichner T, Schlattl A, Stutz AM, Benes V, Korbel JO. DELLY: structural variant discovery by integrated paired-end and split-read analysis. Bioinformatics. 2012;28:i333-9.
57. Chen X, Schulz-Trieglaff O, Shaw R, Barnes B, Schlesinger F, Kallberg M, Cox AJ, Kruglyak S, Saunders CT. Manta: Rapid detection of structural variants and indels for germline and cancer sequencing applications. Bioinformatics. 2016;32(8):1220-2.
58. Klambauer G, Schwarzbauer K, Mayr A, Clevert DA, Mitterecker A, Bodenhofer U, Hochreiter S. cn.MOPS: mixture of Poissons for discovering copy number variations in next-generation sequencing data with a low false discovery rate. Nucleic Acids Res. 2012;40:e69.
59. Wei W, Morrish TA, Alisch RS, Moran JV. A transient assay reveals that cultured human cells can accommodate multiple LINE-1 retrotransposition events. Anal Biochem. 2000;284:435-8.
60. Kopera HC, Moldovan JB, Morrish TA, Garcia-Perez JL, Moran JV. Similarities between long interspersed element-1 (LINE-1) reverse transcriptase and telomerase. Proc Natl Acad Sci U S A. 2011;108:20345-50.
61. Dombroski BA, Scott AF, Kazazian Jr HH. Two additional potential retrotransposons isolated from a human L1 subfamily that contains an active retrotransposable element. Proc Natl Acad Sci U S A. 1993;90:6513-7.
62. Mills RE, Bennett EA, Iskow RC, Devine SE. Which transposable elements are active in the human genome? Trends Genet. 2007;23:183-91.
63. Guy J, Hendrich B, Holmes M, Martin JE, Bird A. A mouse Mecp2-null mutation causes neurological symptoms that mimic Rett syndrome. Nat Genet. 2001;27:322-6.
64. Muotri AR, Marchetto MC, Coufal NG, Oefner R, Yeo G, Nakashima K, Gage FH. L1 retrotransposition in neurons is modulated by MeCP2. Nature. 2010;468:443-6.
65. Han JS, Szak ST, Boeke JD. Transcriptional disruption by the L1 retrotransposon and implications for mammalian transcriptomes. Nature. 2004;429:268-74.
66. Sanborn JZ, Salama SR, Grifford M, Brennan CW, Mikkelsen T, Jhanwar S, Katzman S, Chin L, Haussler D. Double minute chromosomes in glioblastoma multiforme are revealed by precise reconstruction of oncogenic amplicons. Cancer Res. 2013;73:6036-45.
67. Joensuu H, Puputti M, Sihto H, Tynninen O, Nupponen NN. Amplification of genes encoding KIT, PDGFRalpha and VEGFR2 receptor tyrosine kinases is frequent in glioblastoma multiforme. J Pathol. 2005;207:224-31.
68. Carvalho S, Vitor AC, Sridhara SC, Martins FB, Raposo AC, Desterro JM, Ferreira J, de Almeida SF. SETD2 is required for DNA double-strand break repair and activation of the p53-mediated checkpoint. Elife. 2014;3:e02482.
69. Pfister SX, Ahrabi S, Zalmas LP, Sarkar S, Aymard F, Bachrati CZ, Helleday T, Legube G, La Thangue NB, Porter AC, Humphrey TC. SETD2-dependent histone H3K36 trimethylation is required for homologous recombination repair and genome stability. Cell Rep. 2014;7:2006-18.
70. Sassaman DM, Dombroski BA, Moran JV, Kimberland ML, Naas TP, DeBerardinis RJ, Gabriel A, Swergold GD, Kazazian Jr HH. Many human L1 elements are capable of retrotransposition. Nat Genet. 1997;16:37-43.
71. Brouha B, Schustak J, Badge RM, Lutz-Prigge S, Farley AH, Moran JV, Kazazian Jr HH. Hot L1s account for the bulk of retrotransposition in the human population. Proc Natl Acad Sci U S A. 2003;100:5280-5.
72. Gilbert N, Lutz S, Morrish TA, Moran JV. Multiple fates of L1 retrotransposition intermediates in cultured human cells. Mol Cell Biol. 2005;25:7780-95.
73. Gilbert N, Lutz-Prigge S, Moran JV. Genomic deletions created upon LINE-1 retrotransposition. Cell. 2002;110:315-25.
74. Morse B, Rotherg PG, South VJ, Spandorfer JM, Astrin SM. Insertional mutagenesis of the myc locus by a LINE-1 sequence in a human breast carcinoma. Nature. 1988;333:87-90.
75. McVey M, Lee SE. MMEJ repair of double-strand breaks (director's cut): deleted sequences and alternative endings. Trends Genet. 2008;24:529-38.
76. Goodier JL, Cheung LE, Kazazian Jr HH. MOV10 RNA helicase is a potent inhibitor of retrotransposition in cells. PLoS Genet. 2012;8:e1002941.
77. Short SC, Martindale C, Bourne S, Brand G, Woodcock M, Johnston P. DNA repair after irradiation in glioma cells and normal human astrocytes. Neuro Oncol. 2007;9:404-11.