Cancer translocations in human cells induced by zinc finger and TALE nucleases

Genome Research

Volumn 23, Issue 7, 2013, Pages 1182-1193

  Piganeau, Marion ^a   Ghezraoui, Hind ^a   De Cian, Anne ^a   Guittat, Lionel ^b   Tomishima, Mark ^c   Perrouault, Loic ^a   René, Oliver ^a   Katibah, George E ^d   Zhang, Lei ^d   Holmes, Michael C ^d   Doyon, Yannick ^d   Concordet, Jean Paul ^e   Giovannangeli, Carine ^a   Jasin, Maria ^c   Brunet, Erika ^a  

^a MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

^b UNIVERSITÉ PARIS 13   (France)

^c MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^d SANGAMO BIOSCIENCES INC   (United States)

^e INSTITUT COCHIN   (France)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION ACTIVATOR LIKE EFFECTO NUCLEASE; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN;

ARTICLE; CANCER CELL; CELLS; CHROMOSOME ABERRATION; CHROMOSOME TRANSLOCATION; EWING SARCOMA; FUSION GENE; GENOME; HUMAN; HUMAN CELL; LARGE CELL LYMPHOMA; ONCOGENE; PRIORITY JOURNAL;

CELL LINE; CHROMOSOME BREAKPOINTS; ENDONUCLEASES; HUMANS; NEOPLASMS; PROTEIN-TYROSINE KINASES; SARCOMA, EWING; TRANSLOCATION, GENETIC; ZINC FINGERS;

EID: 84880062591     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.147314.112     Document Type: Article

References (43)

1. Barberi T, Willis LM, Socci ND, Studer L. 2005. Derivation of multipotent mesenchymal precursors from human embryonic stem cells. PLoS Med 2: e161.
2. Brunet E, Simsek D, Tomishima M, DeKelver R, Choi VM, Gregory P, Urnov F, Weinstock DM, Jasin M. 2009. Chromosomal translocations induced at specified loci in human stem cells. Proc Natl Acad Sci 106: 10620-10625.
3. Carroll D. 2011. Genome engineering with zinc-finger nucleases. Genetics 188: 773-782.
4. Chansky HA, Barahmand-Pour F, Mei Q, Kahn-Farooqi W, Zielinska- Kwiatkowska A, Blackburn M, Chansky K, Conrad EU III, Bruckner JD, Greenlee TK, et al. 2004. Targeting of EWS/FLI-1 by RNA interference attenuates the tumor phenotype of Ewing's sarcoma cells in vitro. J Orthop Res 22: 910-917.
5. Colombo E, Martinelli P, Zamponi R, Shing DC, Bonetti P, Luzi L, Volorio S, Bernard L, Pruneri G, Alcalay M, et al. 2006. Delocalization and destabilization of the Arf tumor suppressor by the leukemia-associated NPM mutant. Cancer Res 66: 3044-3050.
6. Doyon Y, Vo TD, Mendel MC, Greenberg SG, Wang J, Xia DF, Miller JC, Urnov FD, Gregory PD, Holmes MC. 2011. Enhancing zinc-fingernuclease activity with improved obligate heterodimeric architectures. Nat Methods 8: 74-79.
7. Elmberger PG, Lozano MD,Weisenburger DD, SangerW, ChanWC. 1995. Transcripts of the npm-alk fusion gene in anaplastic large cell lymphoma, Hodgkin's disease, and reactive lymphoid lesions. Blood 86: 3517-3521.
8. Gillis S, Watson J. 1980. Biochemical and biological characterization of lymphocyte regulatorymolecules. V. Identification of an interleukin 2-producing human leukemia T cell line. J Exp Med 152: 1709-1719.
9. Greenland C, Touriol C, Chevillard G, Morris SW, Bai R, Duyster J, Delsol G, Allouche M. 2001. Expression of the oncogenic NPM-ALK chimeric protein in human lymphoid T-cells inhibits drug-induced, but not Fasinduced apoptosis. Oncogene 20: 7386-7397.
10. Grisendi S, Pandolfi PP. 2005. NPM mutations in acute myelogenous leukemia. N Engl JMed 352: 291-292.
11. Guschin DY, Waite AJ, Katibah GE, Miller JC, Holmes MC, Rebar EJ. 2010. A rapid and general assay for monitoring endogenous gene modification. Methods Mol Biol 649: 247-256.
12. Hockemeyer D,Wang H, Kiani S, Lai CS, Gao Q, Cassady JP, Cost GJ, Zhang L, Santiago Y, Miller JC, et al. 2011. Genetic engineering of human pluripotent cells using TALE nucleases. Nat Biotechnol 29: 731-734.
13. Kasprzycka M, Marzec M, Liu X, Zhang Q, Wasik MA. 2006. Nucleophosmin/anaplastic lymphoma kinase (NPM/ALK) oncoprotein induces the T regulatory cell phenotype by activating STAT3. Proc Natl Acad Sci 103: 9964-9969.
14. Kuefer MU, Look AT, Pulford K, Behm FG, Pattengale PK, Mason DY, Morris SW. 1997. Retrovirus-mediated gene transfer of NPM-ALK causes lymphoid malignancy in mice. Blood 90: 2901-2910.
15. Kurki S, Peltonen K, Latonen L, Kiviharju TM, Ojala PM, Meek D, Laiho M. 2004. Nucleolar protein NPM interacts with HDM2 and protects tumor suppressor protein p53 from HDM2-mediated degradation. Cancer Cell 5: 465-475.
16. LeeHJ, Kim E, Kim JS. 2010. Targeted chromosomal deletions in human cells using zinc finger nucleases. Genome Res 20: 81-89.
17. Lee HJ, Kweon J, Kim E, Kim S, Kim JS. 2012. Targeted chromosomal duplications and inversions in the human genome using zinc finger nucleases. Genome Res 22: 539-548.
18. Lessnick SL, Ladanyi M. 2012. Molecular pathogenesis of Ewing sarcoma: New therapeutic and transcriptional targets. Annu Rev Pathol 7: 145-159.
19. Li Z, Boone D, Hann SR. 2008. Nucleophosmin interacts directly with c-Myc and controls c-Myc-induced hyperproliferation and transformation. Proc Natl Acad Sci 105: 18794-18799.
20. Mani RS, Chinnaiyan AM. 2010. Triggers for genomic rearrangements: Insights into genomic, cellular and environmental influences. Nat Rev Genet 11: 819-829.
21. Mathas S, Kreher S, Meaburn KJ, Johrens K, Lamprecht B, Assaf C, SterryW, Kadin ME, Daibata M, Joos S, et al. 2009. Gene deregulation and spatial genome reorganization near breakpoints prior to formation of translocations in anaplastic large cell lymphoma. Proc Natl Acad Sci 106: 5831-5836.
22. Miller JC, Tan S, Qiao G, Barlow KA, Wang J, Xia DF, Meng X, Paschon DE, Leung E, Hinkley SJ, et al. 2011. A TALE nuclease architecture for efficient genome editing. Nat Biotechnol 29: 143-148.
23. Mitelman F, Johansson B, Mertens F. 2007. The impact of translocations and gene fusions on cancer causation. Nat Rev Cancer 7: 233-245.
24. Morris SW, KirsteinMN, ValentineMB, DittmerKG, ShapiroDN, SaltmanDL, Look AT. 1994. Fusion of a kinase gene, ALK, to a nucleolar protein gene, NPM, in non-Hodgkin's lymphoma. Science 263: 1281-1284.
25. Mussolino C, Cathomen T. 2012. TALE nucleases: Tailored genome engineering made easy. Curr Opin Biotechnol 23: 644-650.
26. Mussolino C, Morbitzer R, Lutge F, Dannemann N, Lahaye T, Cathomen T. 2011. A novel TALE nuclease scaffold enables high genome editing activity in combinationwith low toxicity. Nucleic Acids Res 39: 9283-9293.
27. Plougastel B, Zucman J, Peter M, Thomas G, Delattre O. 1993. Genomic structure of the EWS gene and its relationship to EWSR1, a site of tumorassociated chromosome translocation. Genomics 18: 609-615.
28. Prieur A, Tirode F, Cohen P, Delattre O. 2004. EWS/FLI-1 silencing and gene profiling of Ewing cells reveal downstream oncogenic pathways and a crucial role for repression of insulin-like growth factor binding protein 3. Mol Cell Biol 24: 7275-7283.
29. Reyon D, Tsai SQ, Khayter C, Foden JA, Sander JD, Joung JK. 2012. FLASH assembly of TALENs for high-throughput genome editing. Nat Biotechnol 30: 460-465.
30. Richardson C, Jasin M. 2000. Frequent chromosomal translocations induced by DNA double-strand breaks. Nature 405: 697-700.
31. Riggi N, Suva ML, Suva D, Cironi L, Provero P, Tercier S, Joseph JM, Stehle JC, Baumer K, Kindler V, et al. 2008. EWS-FLI-1 expression triggers a Ewing's sarcoma initiation program in primary humanmesenchymal stem cells. Cancer Res 68: 2176-2185.
32. Riggi N, Suva ML, De Vito C, Provero P, Stehle JC, Baumer K, Cironi L, Janiszewska M, Petricevic T, Suva D, et al. 2010. EWS-FLI-1 modulates miRNA145 and SOX2 expression to initiate mesenchymal stem cell reprogramming toward Ewing sarcoma cancer stem cells. Genes Dev 24: 916-932.
33. Roth DB, Porter TN, Wilson JH. 1985. Mechanisms of nonhomologous recombination in mammalian cells. Mol Cell Biol 5: 2599-2607.
34. Simsek D, Jasin M. 2010. Alternative end-joining is suppressed by the canonical NHEJ component Xrcc4-ligase IV during chromosomal translocation formation. Nat Struct Mol Biol 17: 410-416.
35. Simsek D, Brunet E,Wong SY, Katyal S, Gao Y, McKinnon PJ, Lou J, Zhang L, Li J, Rebar EJ, et al. 2011. DNA ligase III promotes alternative nonhomologous end-joining during chromosomal translocation formation. PLoS Genet 7: e1002080.
36. Smith J, Bibikova M, Whitby FG, Reddy AR, Chandrasegaran S, Carroll D. 2000. Requirements for double-strand cleavage by chimeric restriction enzymes with zinc finger DNA-recognition domains. Nucleic Acids Res 28: 3361-3369.
37. Smith R, Owen LA, Trem DJ,Wong JS, Whangbo JS, Golub TR, Lessnick SL. 2006. Expression profiling of EWS/FLI identifies NKX2.2 as a critical target gene in Ewing's sarcoma. Cancer Cell 9: 405-416.
38. Tirode F, Laud-Duval K, Prieur A, Delorme B, Charbord P, Delattre O. 2007. Mesenchymal stemcell features of Ewing tumors. Cancer Cell 11: 421-429.
39. Urnov FD, Rebar EJ, Holmes MC, Zhang HS, Gregory PD. 2010. Genome editing with engineered zinc finger nucleases. Nat Rev Genet 11: 636-646.
40. Wang W, Budhu A, Forgues M, Wang XW. 2005. Temporal and spatial control of nucleophosmin by the Ran-Crm1 complex in centrosome duplication. Nat Cell Biol 7: 823-830.
41. Weinstock DM, Brunet E, Jasin M. 2007. Formation of NHEJ-derived reciprocal chromosomal translocations does not require Ku70. Nat Cell Biol 9: 978-981.
42. Yan CT, Boboila C, Souza EK, Franco S, Hickernell TR, Murphy M, Gumaste S, Geyer M, Zarrin AA, Manis JP, et al. 2007. IgH class switching and translocations use a robust non-classical end-joining pathway. Nature 449: 478-482.
43. Zucman-Rossi J, Legoix P, Victor JM, Lopez B, Thomas G. 1998. Chromosome translocation based on illegitimate recombination in human tumors. Proc Natl Acad Sci 95: 11786-11791.