Chromatin Landscapes of Retroviral and Transposon Integration Profiles

PLoS Genetics

Volumn 10, Issue 4, 2014, Pages

  de Jong, Johann ^a,b   Akhtar, Waseem ^a,b   Badhai, Jitendra ^a   Rust, Alistair G ^c   Rad, Roland ^d   Hilkens, John ^a   Berns, Anton ^a,e   van Lohuizen, Maarten ^a,b   Wessels, Lodewyk F A ^a,b,f   de Ridder, Jeroen ^f  

^a NETHERLANDS CANCER INSTITUTE   (Netherlands)

^b Netherlands Consortium for Systems Biology   (Netherlands)

^c WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^d TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^e SKOLKOVO INSTITUTE OF SCIENCE AND TECHNOLOGY   (Russian Federation)

^f DELFT UNIVERSITY OF TECHNOLOGY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

STAT3 PROTEIN; TRANSCRIPTION FACTOR AP 2; TRANSCRIPTION FACTOR AP 2A; TRANSCRIPTION FACTOR AP 2E; UNCLASSIFIED DRUG; CHROMATIN; TRANSPOSON;

ANIMAL CELL; ARTICLE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONTROLLED STUDY; CPG ISLAND; DNA INTEGRATION; DNA MODIFICATION; DNA REPLICATION TIMING; DNA SEQUENCE; EXON; GENE CASSETTE; GENE INSERTION; GENE LOCUS; GENETIC DISTANCE; HETEROCHROMATIN; INTRON; MOUSE; MOUSE MAMMARY TUMOR ONCOVIRUS; NONHUMAN; NUCLEOTIDE MOTIF; PIGGYBAC TRANSPOSON; PROTEIN BINDING; PROTEIN DOMAIN; SLEEPING BEAUTY TRANSPOSON; TRANSPOSON; ANIMAL; CHROMATIN; GENE EXPRESSION REGULATION; GENETICS; GENOME; ONCOGENE; PROCEDURES; RETROVIRIDAE;

ANIMALS; CHROMATIN; CPG ISLANDS; DNA TRANSPOSABLE ELEMENTS; GENOME; MICE; MUTAGENESIS, INSERTIONAL; ONCOGENES; RETROVIRIDAE;

EID: 84901361283     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004250     Document Type: Article

References (100)

1. Cartier N, Hacein-Bey-Abina S, Bartholomae CC, Veres G, Schmidt M, et al. (2009) Hematopoietic stem cell gene therapy with a lentiviral vector in X-Linked adrenoleukodystrophy. Science 326: 818-823.
2. Fischer A, Hacein-Bey-Abina S, Cavazzana-Calvo M, (2010) 20 years of gene therapy for SCID. Nat Immunol 11: 457-460.
3. Uren AG, Kool J, Matentzoglu K, de Ridder J, Mattison J, et al. (2008) Large-scale mutagenesis in p19(ARF)- and p53-deficient mice identifies cancer genes and their collaborative networks. Cell 133: 727-741.
4. Mattison J, Kool J, Uren AG, de Ridder J, Wessels L, et al. (2010) Novel candidate cancer genes identified by a large-scale cross-species comparative oncogenomics approach. Cancer Res 70: 883-895.
5. Akhtar W, de Jong J, Pindyurin AV, Pagie L, Meuleman W, et al. (2013) Chromatin position effects assayed by thousands of reporters integrated in parallel. Cell 154: 914-27.
6. Ruf S, Symmons O, Uslu VV, Dolle D, Hot C, et al. (2011) Large-scale analysis of the regulatory architecture of the mouse genome with a transposon-associated sensor. Nat Genet 43: 379-386.
7. Miller EH, Obernosterer G, Raaben M, Herbert AS, Deffieu MS, et al. (2012) Ebola virus entry requires the host-programmed recognition of an intracellular receptor. EMBO J 31 (8) (): 1947-60.
8. Bouwman P, Aly A, Escandell JM, Pieterse M, Bartkova J, et al. (2010) 53BP1 loss rescues BRCA1 deficiency and is associated with triple-negative and BRCA-mutated breast cancers. Nat Struct & Mol Biol 17: 688-695.
9. Hacein-Bey-Abina S, Garrigue A, Wang GP, Soulier J, Lim A, et al. (2008) Insertional oncogenesis in 4 patients after retrovirus-mediated gene therapy of scid-x1. J Clin Invest 118: 3132-3142.
10. Liu G, Geurts AM, Yae K, Srinivasan AR, Fahrenkrug SC, et al. (2005) Target-site preferences of sleeping beauty transposons. J Mol Biol 346: 161-73.
11. Geurts AM, Hackett CS, Bell JB, Bergemann TL, Collier LS, et al. (2006) Structure-based prediction of insertionsite preferences of transposons into chromosomes. Nucleic acids research 34: 2803-2811.
12. Copeland NG, Jenkins NA, (2010) Harnessing transposons for cancer gene discovery. Nat Rev Cancer 10: 696-706.
13. Vandendriessche T, Ivics Z, Izsvak Z, Chuah MK, (2009) Emerging potential of transposons for gene therapy and generation of induced pluripotent stem cells. Blood 114: 1461-1468.
14. Liang Q, Kong J, Stalker J, Bradley A, (2009) Chromosomal mobilization and reintegration of sleeping beauty and piggybac transposons. Genesis 47: 404-8.
15. Berry C, Hannenhalli S, Leipzig J, Bushman FD, (2006) Selection of target sites for mobile DNA integration in the human genome. PLoS Comput Biol 2: e157.
16. Balu B, Chauhan C, Maher S, Shoue D, Kissinger J, et al. (2009) piggyBac is an effective tool for functional analysis of the plasmodium falciparum genome. BMC Microbiol 9: 83+.
17. Galvan DL, Nakazawa Y, Kaja A, Kettlun C, Cooper LJ, et al. (2009) Genome-wide mapping of PiggyBac transposon integrations in primary human T cells. J Immunother 32: 837-844.
18. Li MA, Pettitt SJ, Eckert S, Ning Z, Rice S, et al. (2013) The piggybac transposon displays local and distant reintegration preferences and can cause mutations at non-canonical integration sites. Mol Cell Biol 33 (7) (): 1317-30.
19. Wang W, Lin C, Lu D, Ning Z, Cox T, et al. (2008) Chromosomal transposition of PiggyBac in mouse embryonic stem cells. P Natl Acad of Sci USA 105: 9290-9295.
20. Faschinger A, Rouault F, Johannes S, Lukas A, Salmons B, et al. (2007) Mouse Mammary Tumor Virus integration site selection in human and mouse genomes. J Virol 82: 1360-1367.
21. Felice B, Cattoglio C, Cittaro D, Testa A, Miccio A, et al. (2009) Transcription factor binding sites are genetic determinants of retroviral integration in the human genome. PLoS One 4: e4571.
22. Santoni FA, Hartley O, Luban J, (2010) Deciphering the code for retroviral integration target site selection. PLoS Comput Biol 6: e1001008.
23. Brady T, Lee YN, Ronen K, Malani N, Berry CC, et al. (2009) Integration target site selection by a resurrected human endogenous retrovirus. Genes & Development 23: 633-642.
24. Kodama Y, Shumway M, Leinonen R, (2012) International Nucleotide Sequence Database Collaboration (2012) The sequence read archive: explosive growth of sequencing data. Nucleic acids research 40: D54-6.
25. Bergemann TL, Starr TK, Yu H, Steinbach M, Erdmann J, et al. (2012) New methods for finding common insertion sites and co-occurring common insertion sites in transposon- and virus-based genetic screens. Nucleic Acids Res 40: 3822-33.
26. Abel U, Deichmann A, Nowrouzi A, Gabriel R, Bartholomae CC, et al. (2011) Analyzing the number of common integration sites of viral vectors new methods and computer programs. PLoS ONE 6: e24247.
27. Biffi A, Bartolomae C, Cesana D, Cartier N, Aubourg P, et al. (2011) Lentiviral vector common integration sites in preclinical models and a clinical trial reect a benign integration bias and not oncogenic selection. Blood 117: 5332-5339.
28. Wu X, Luke B, Burgess S, (2006) Redefining the common insertion site. Virology 344: 292-295.
29. Starr TK, Allaei R, Silverstein KAT, Staggs RA, Sarver AL, et al. (2009) A Transposon-Based genetic screen in mice identifies genes altered in colorectal cancer. Science 323: 1747-1750.
30. de Jong J, de Ridder J, van der Weyden L, Sun N, van Uitert M, et al. (2011) Computational identification of insertional mutagenesis targets for cancer gene discovery. Nucleic Acids Res 39: e105.
31. Koudijs MJ, Klijn C, van der Weyden L, Kool J, ten Hoeve J, et al. (2011) High-throughput semiquantitative analysis of insertional mutations in heterogeneous tumors. Genome Res 21: 2181-2189.
32. Rad R, Rad L, Wang W, Cadinanos J, Vassiliou G, et al. (2010) PiggyBac transposon mutagenesis: A tool for cancer gene discovery in mice. Science 330: 1104-1107.
33. de Ridder J, Uren A, Kool J, Reinders M, Wessels L, (2006) Detecting statistically significant common insertion sites in retroviral insertional mutagenesis screens. PLoS Comput Biol 2: e166.
34. Heinz S, Benner C, Spann N, Bertolino E, Lin YC, et al. (2010) Simple combinations of Lineage-Determining transcription factors prime cis-Regulatory elements required for macrophage and b cell identities. Mol Cell 38: 576-589.
35. Mitchell RS, Beitzel BF, Schroder AR, Shinn P, Chen H, et al. (2004) Retroviral DNA integration: ASLV, HIV, and MLV show distinct target site preferences. PLoS Biol 2: e234.
36. 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.
37. Kool J, Uren AG, Martins CP, Sie D, de Ridder J, et al. (2010) Insertional mutagenesis in mice deficient for p15Ink4b, p16Ink4a, p21Cip1, and p27Kip1 reveals cancer gene interactions and correlations with tumor phenotypes. Cancer Res 70: 520-531.
38. Belton JMM, McCord RPP, Gibcus JHH, Naumova N, Zhan Y, et al. (2012) Hi-C: A comprehensive technique to capture the conformation of genomes. Methods 58: 268-276.
39. Dixon JR, Selvaraj S, Yue F, Kim A, Li Y, et al. (2012) Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 485: 376-380.
40. Hartemink AJ, (2005) Reverse engineering gene regulatory networks. Nat Biotechnol 23: 554-555.
41. Pearl J (1985) Bayesian networks: A model of self-activated memory for evidential reasoning. In: Proceedings of the 7th Conference of the Cognitive Science Society, University of California, Irvine. pp. 329-334.
42. Mikkers H, Allen J, Knipscheer P, Romeijn L, Hart A, et al. (2002) High-throughput retroviral tagging to identify components of specific signaling pathways in cancer. Nat Genet 32: 153-159.
43. Lund AH, Turner G, Trubetskoy A, Verhoeven E, Wientjens E, et al. (2002) Genome-wide retro-viral insertional tagging of genes involved in cancer in Cdkn2a-deficient mice. Nat Genet 32: 160-165.
44. Uren AG, Kool J, Berns A, van Lohuizen M, (2005) Retroviral insertional mutagenesis: past, present and future. Oncogene 24: 7656-7672.
45. Collier LS, Carlson CM, Ravimohan S, Dupuy AJ, Largaespada DA, (2005) Cancer gene discovery in solid tumours using transposon-based somatic mutagenesis in the mouse. Nature 436: 272-276.
46. Robertson ES (2011) Cancer Associated Viruses. Current Cancer Research. Springer.
47. Theodorou V, Kimm MA, Boer M, Wessels L, Theelen W, et al. (2007) MMTV insertional mutagenesis identifies genes, gene families and pathways involved in mammary cancer. Nature Genetics 39: 759-769.
48. Kagey MH, Newman JJ, Bilodeau S, Zhan Y, Orlando DA, et al. (2010) Mediator and cohesin connect gene expression and chromatin architecture. Nature 467: 430-435.
49. Mikkelsen TS, Ku M, Jaffe DB, Issac B, Lieberman E, et al. (2007) Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448: 553-560.
50. Bilodeau S, Young R (2010) ChIPSeq for H3K79me2 (unpublished). GSE accession: GSE26680.
51. Creyghton MP, Cheng AW, Welstead GG, Kooistra T, Carey BW, et al. (2010) Histone H3K27ac separates active from poised enhancers and predicts developmental state. P Natl Acad Sci USA 107: 21931-21936.
52. Shen Y, Yue F, McCleary DF, Ye Z, Edsall L, et al. (2012) A map of the cis-regulatory sequences in the mouse genome. Nature 488: 116-120.
53. Masui S, Shimosato D, Toyooka Y, Yagi R, Takahashi K, et al. (2005) An efficient system to establish multiple embryonic stem cell lines carrying an inducible expression unit. Nucleic Acids Res 33: e43.
54. Ying QL, Wray J, Nichols J, Batlle-Morera L, Doble B, et al. (2008) The ground state of embryonic stem cell self-renewal. Nature 453: 519-23.
55. Wang W, Yang J, Liu H, Lu D, Chen X, et al. (2011) Rapid and efficient reprogramming of somatic cells to induced pluripotent stem cells by retinoic acid receptor gamma and liver receptor homolog 1. P Natl Acad Sci USA.
56. Cadinanos J, Bradley A, (2007) Generation of an inducible and optimized piggybac transposon system. Nucleic Acids Res 35: e87.
57. Mates L, Chuah MKL, Belay E, Jerchow B, Manoj N, et al. (2009) Molecular evolution of a novel hyperactive sleeping beauty transposase enables robust stable gene transfer in vertebrates. Nat Genet 41: 753-761.
58. Langmead B, Salzberg SL, (2012) Fast gapped-read alignment with bowtie 2. Nat Meth 9: 357-359.
59. Langmead B, Trapnell C, Pop M, Salzberg S, (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25-10.
60. Barrett T, Troup DB, Wilhite SE, Ledoux P, Evangelista C, et al. (2010) NCBI GEO: archive for functional genomics data sets-10 years on. Nucleic Acids Res 39: D1005-D1010.
61. Xu Y, Wu F, Tan L, Kong L, Xiong L, et al. (2011) Genome-wide regulation of 5hmC, 5mC, and gene expression by tet1 hydroxylase in mouse embryonic stem cells. Mol Cell 42: 451-464.
62. Pedersen B, Hsieh TF, Ibarra C, Fischer RL, (2011) MethylCoder: software pipeline for bisulfitetreated sequences. Bioinformatics 27: 2435-2436.
63. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, et al. (2010) Transcript assembly and quantification by RNA-seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28: 511-515.
64. Lienert F, Mohn F, Tiwari VK, Baubec T, Roloff TC, et al. (2011) Genomic prevalence of heterochromatic H3K9me2 and transcription do not discriminate pluripotent from terminally differentiated cells. PLoS Genet 7: e1002090+.
65. Hiratani I, Ryba T, Itoh M, Yokochi T, Schwaiger M, et al. (2008) Global reorganization of replication domains during embryonic stem cell differentiation. PLoS Biol 6: e245+.
66. Peric-Hupkes D, Meuleman W, Pagie L, Bruggeman SWM, Solovei I, et al. (2010) Molecular maps of the reorganization of genome-nuclear lamina interactions during differentiation. Mol Cell 38: 603-613.
67. Chang C, Yang X, Pursell B, Mercurio AM, (2013) Id2 complexes with the snag domain of snai1 inhibiting snai1-mediated repression of integrin beta-4. Mol Cell Biol 33 (19) (): 3795-804.
68. Flicek P, Amode MR, Barrell D, Beal K, Brent S, et al. (2012) Ensembl 2012. Nucleic Acids Res 40: D84-D90.
69. Stamatoyannopoulos J, Snyder M, Hardison R, Ren B, Gingeras T, et al. (2012) An encyclopedia of mouse DNA elements (mouse ENCODE). Genome Biol 13: 418+.
70. Karimi MM, Goyal P, Maksakova IA, Bilenky M, Leung D, et al. (2011) DNA methylation and SETDB1/H3K9me3 regulate predominantly distinct sets of genes, retroelements, and chimeric transcripts in mESCs. Cell Stem Cell 8: 676-687.
71. Xiao S, Xie D, Cao X, Yu P, Xing X, et al. (2012) Comparative epigenomic annotation of regulatory DNA. Cell 149: 1381-1392.
72. Law MJ, Lower KM, Voon HPJ, Hughes JR, Garrick D, et al. (2010) ATR-x syndrome protein targets tandem repeats and inuences Allele-Specific expression in a Size-Dependent manner. Cell 143: 367-378.
73. Ho L, Jothi R, Ronan JL, Cui K, Zhao K, et al. (2009) An embryonic stem cell chromatin remodeling complex, esBAF, is an essential component of the core pluripotency transcriptional network. P Natl Acad Sci USA 106: 5187-5191.
74. Chen X, Xu H, Yuan P, Fang F, Huss M, et al. (2008) Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell 133: 1106-1117.
75. Marson A, Levine SS, Cole MF, Frampton GM, Brambrink T, et al. (2008) Connecting microRNA genes to the core transcriptional regulatory circuitry of embryonic stem cells. Cell 134: 521-533.
76. Ku M, Koche RP, Rheinbay E, Mendenhall EM, Endoh M, et al. (2008) Genomewide analysis of PRC1 and PRC2 occupancy identifies two classes of bivalent domains. PLoS Genet 4: e1000242+.
77. Bilodeau S, Kagey MH, Frampton GM, Rahl PB, Young RA, (2009) SetDB1 contributes to repression of genes encoding developmental regulators and maintenance of ES cell state. Gene Dev 23: 2484-2489.
78. Li G, Margueron R, Ku M, Chambon P, Bernstein BE, et al. (2010) Jarid2 and PRC2, partners in regulating gene expression. Gene Dev 24: 368-380.
79. Han J, Yuan P, Yang H, Zhang J, Soh BS, et al. (2010) Tbx3 improves the germ-line competency of induced pluripotent stem cells. Nature 463: 1096-100.
80. Rahl PB, Lin CY, Seila AC, Flynn RA, McCuine S, et al. (2010) c-Myc regulates transcriptional pause release. Cell 141: 432-445.
81. Krebs AR, Demmers J, Karmodiya K, Chang NC, Chang AC, et al. (2010) ATAC and mediator coactivators form a stable complex and regulate a set of non-coding RNA genes. EMBO Rep 11: 541-7.
82. Schnetz MP, Handoko L, Akhtar-Zaidi B, Bartels CF, Pereira CF, et al. (2010) CHD7 targets active gene enhancer elements to modulate ES cell-specific gene expression. PLoS Genet 6.
83. Mendenhall EM, Koche RP, Truong T, Zhou VW, Issac B, et al. (2010) GC-rich sequence elements recruit PRC2 in mammalian ES cells. PLoS Genet 6: e1001244+.
84. Handoko L, Xu H, Li G, Ngan CYY, Chew E, et al. (2011) CTCF-mediated functional chromatin interactome in pluripotent cells. Nat Genet 43: 630-638.
85. Hezroni H, Sailaja BS, Meshorer E, (2011) Pluripotency-related, valproic acid (VPA)-induced genome-wide histone h3 lysine 9 (H3K9) acetylation patterns in embryonic stem cells. J Biol Chem 286: 35977-35988.
86. Liu Z, Scannell DR, Eisen MB, Tjian R, (2011) Control of embryonic stem cell lineage commitment by core promoter factor, TAF3. Cell 146: 720-731.
87. Schmitz SU, Albert M, Malatesta M, Morey L, Johansen JV, et al. (2011) Jarid1b targets genes regulating development and is involved in neural differentiation. EMBO J 30 (22) (): 4586-600.
88. Mullen AC, Orlando DA, Newman JJ, Lovén J, Kumar RM, et al. (2011) Master transcription factors determine cell-type-specific responses to TGF-? signaling. Cell 147: 565-576.
89. Quenneville S, Verde G, Corsinotti A, Kapopoulou A, Jakobsson J, et al. (2011) In embryonic stem cells, ZFP57/KAP1 recognize a methylated hexanucleotide to affect chromatin and DNA methylation of imprinting control regions. Mol Cell 44: 361-372.
90. Stadler MB, Murr R, Burger L, Ivanek R, Lienert F, et al. (2011) DNA-binding factors shape the mouse methylome at distal regulatory regions. Nature 480: 490-495.
91. Creppe C, Janich P, Cantarino N, Noguera M, Valero V, et al. (2012) Macroh2a1 regulates the balance between self-renewal and differentiation commitment in embryonic and adult stem cells. Mol Cell Biol 32: 1442-52.
92. Li M, He Y, Dubois W, Wu X, Shi J, et al. (2012) Distinct regulatory mechanisms and functions for p53-Activated and p53-Repressed DNA damage response genes in embryonic stem cells. Mol Cell 46: 30-42.
93. Tavares L, Dimitrova E, Oxley D, Webster J, Poot R, et al. (2012) RYBP-PRC1 complexes mediate H2A ubiquitylation at polycomb target sites independently of PRC2 and H3K27me3. Cell 148: 664-678.
94. Whyte WA, Bilodeau S, Orlando DA, Hoke HA, Frampton GM, et al. (2012) Enhancer decommissioning by LSD1 during embryonic stem cell differentiation. Nature 482 (7384) (): 221-5.
95. Jiang H, Shukla A, Wang X, Chen Wy, Bernstein BE, et al. (2011) Role for dpy-30 in ES Cell-Fate specification by regulation of H3K4 methylation within bivalent domains. Cell 144: 825.
96. Yildirim O, Li R, Hung JHH, Chen PB, Dong X, et al. (2011) Mbd3/NURD complex regulates expression of 5-hydroxymethylcytosine marked genes in embryonic stem cells. Cell 147: 1498-1510.
97. Young R (2011) ChIPSeq for Mcaf1 (unpublished). GSE accession: GSE26680.
98. Young R (2010) ChIPSeq for Tbp (unpublished). GSE accession: GSE22303.
99. Young R (2010) ChIPSeq for PolII-Ser18P (unpublished). GSE accession: GSE21917.
100. Smith ER, Lin C, Garrett AS, Thornton J, Mohaghegh N, et al. (2011) The little elongation complex regulates small nuclear RNA transcription. Mol Cell 44: 954-965.