Infection with retroviral vectors leads to perturbed DNA replication increasing vector integrations into fragile sites

Scientific Reports

Volumn 3, Issue , 2013, Pages

  Bester, Assaf C ^a   Kafri, Moshe ^a,b   Maoz, Karin ^a   Kerem, Batsheva ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CELL LINE; CHROMOSOME 11; CHROMOSOME FRAGILE SITE; DNA REPLICATION; DOUBLE STRANDED DNA BREAK; GENE ORDER; GENE VECTOR; GENETIC TRANSFECTION; GENETICS; GENOMIC INSTABILITY; HUMAN; METAPHASE; MURINE LEUKEMIA VIRUS; VIRUS DNA CELL DNA INTERACTION;

CELL LINE; CHROMOSOME FRAGILE SITES; CHROMOSOMES, HUMAN, PAIR 11; DNA BREAKS, DOUBLE-STRANDED; DNA REPLICATION; GENE ORDER; GENETIC VECTORS; GENOMIC INSTABILITY; HUMANS; LEUKEMIA VIRUS, MURINE; METAPHASE; TRANSFECTION; VIRUS INTEGRATION;

EID: 84880386029     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep02189     Document Type: Article

References (47)

1. Glover, T. W., Berger, C., Coyle, J., Echo, B.DNApolymerase alpha inhibition by aphidicolin induces gaps and breaks at common fragile sites in human chromosomes. Hum Genet 67, 136-142 (1984). (Pubitemid 14095149)
2. Cheng, C. H., Kuchta, R.D.DNApolymerase epsilon: aphidicolin inhibition and the relationship between polymerase and exonuclease activity. Biochemistry 32, 8568-8574 (1993). (Pubitemid 23270441)
3. Ikegami, S. et al. Aphidicolin prevents mitotic cell division by interfering with the activity of DNA polymerase-alpha. Nature 275, 458-460 (1978). (Pubitemid 9021221)
4. Glover, T. W. & Stein, C. K. Induction of sister chromatid exchanges at common fragile sites. Am J Hum Genet 41, 882-890 (1987).
5. Glover, T. W. & Stein, C. K. Chromosome breakage and recombination at fragile sites. Am J Hum Genet 43, 265-273 (1988).
6. Wang, L. et al. Aphidicolin-induced FRA3B breakpoints cluster in two distinct regions. Genomics 41, 485-488 (1997). (Pubitemid 27194806)
7. Bignell, G. R. et al. Signatures of mutation and selection in the cancer genome. Nature 463, 893-8 (2010).
8. Hecht, F., Morgan, R., Hecht, B. K. & Smith, S. D. Common region on chromosome 14 in T-cell leukemia and lymphoma. Science (New York, N.Y.) 226, 1445-7 (1984). (Pubitemid 15161280)
9. Yunis, J. J. J. & Soreng, A. L. Constitutive Fragile Sites and Cancer. Science 226, 1199-1204 (1984). (Pubitemid 15221736)
10. Bester, A. C. et al. Nucleotide deficiency promotes genomic instability in early stages of cancer development. Cell 145, 435-46 (2011).
11. Bartkova, J. et al.DNAdamage response as a candidate anti-cancer barrier in early human tumorigenesis. Nature 434, 864-870 (2005). (Pubitemid 40558993)
12. Hellman, A. et al. A role for common fragile site induction in amplification of human oncogenes. Cancer Cell 1, 89-97 (2002). (Pubitemid 41039179)
13. Kotzot, D. et al. Parental origin and mechanisms of formation of cytogenetically recognisable de novo direct and inverted duplications. J Med Genet 37, 281-286 (2000). (Pubitemid 30245933)
14. Miller, C. T. et al. Genomic amplification of MET with boundaries within fragile site FRA7G and upregulation of MET pathways in esophageal adenocarcinoma. Oncogene 25, 409-418 (2006). (Pubitemid 43117626)
15. Di Micco, R. et al. Oncogene-induced senescence is a DNA damage response triggered by DNA hyper-replication. Nature 444, 638-42 (2006). (Pubitemid 44864443)
16. Gorgoulis, V. G. et al. Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions. Nature 434, 907-13 (2005). (Pubitemid 40559004)
17. Rassool, F. V. et al. Preferential integration of marker DNA into the chromosomal fragile site at 3p14: an approach to cloning fragile sites. Proceedings of the National Academy of Sciences of the United States of America 88, 6657-61 (1991). (Pubitemid 21915008)
18. Lehoux, M., D'Abramo, C. M. & Archambault, J. Molecular mechanisms of human papillomavirus-induced carcinogenesis. Public health genomics 12, 268-80 (2009).
19. Kim, S. et al. Integration site preference of xenotropic murine leukemia virusrelated virus, a new human retrovirus associated with prostate cancer. J Virol 82, 9964-9977 (2008).
20. Urisman, A. et al. Identification of a novel Gammaretrovirus in prostate tumors of patients homozygous for R462Q RNASEL variant. PLoS pathogens 2, e25 (2006).
21. Bester, A. C. et al. Fragile sites are preferential targets for integrations of MLV vectors in gene therapy. Gene therapy 13, 1057-9 (2006). (Pubitemid 43905859)
22. Howe, S. J. et al. Insertional mutagenesis combined with acquired somatic mutations causes leukemogenesis following gene therapy of SCID-X1 patients. The Journal of clinical investigation 118, 3143-50 (2008).
23. Hacein-Bey-Abina, S. et al. Insertional oncogenesis in 4 patients after retrovirusmediated gene therapy of SCID-X1. The Journal of clinical investigation 118, 3132 (2008).
24. Huang, X., Gollin, S. M., Raja, S. & Godfrey, T. E. High-resolution mapping of the 11q13 amplicon and identification of a gene, TAOS1, that is amplified and overexpressed in oral cancer cells. Proc Natl Acad Sci USA 99, 11369-11374 (2002). (Pubitemid 34920932)
25. Zhang, D. et al. Analysis of DNA copy number aberrations by multiple ligationdependent probe amplification on 50 intestinal type gastric cancers. Journal of surgical oncology 103, 124-32 (2011).
26. Deichmann, A. et al. Vector integration is nonrandom and clustered and influences the fate of lymphopoiesis in SCID-X1 gene therapy. J Clin Invest 117, 2225-2232 (2007). (Pubitemid 47219567)
27. Schwarzwaelder, K. et al. Gammaretrovirus-mediated correction of SCID-X1 is associated with skewed vector integration site distribution in vivo. J Clin Invest 117, 2241-2249 (2007). (Pubitemid 47219569)
28. Cattoglio, C. et al. High-definition mapping of retroviral integration sites identifies active regulatory elements in human multipotent hematopoietic progenitors. Blood 116, 5507-17 (2010).
29. Panet, A. & Cedar, H. Selective degradation of integrated murine leukemia proviral DNA by deoxyribonucleases. Cell 11, 933-940 (1977). (Pubitemid 8186415)
30. Wang, B., Matsuoka, S., Carpenter, P. B. & Elledge, S. J. 53BP1, a mediator of the DNA damage checkpoint. Science (New York, N.Y.) 298, 1435-8 (2002). (Pubitemid 35346146)
31. Rogakou, E. P., Pilch, D. R., Orr, A. H., Ivanova, V. S. & Bonner, W. M. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 273, 5858-5868 (1998). (Pubitemid 28124064)
32. Musgrove, E. A., Caldon, C. E., Barraclough, J., Stone, A. & Sutherland, R. L. Cyclin D as a therapeutic target in cancer. Nature reviews. Cancer 11, 558-72 (2011).
33. Coquelle, A., Pipiras, E., Toledo, F., Buttin, G. & Debatisse, M. Expression of fragile sites triggers intrachromosomal mammalian gene amplification and sets boundaries to early amplicons. Cell 89, 215-225 (1997). (Pubitemid 27199894)
34. Ciullo, M. et al. Initiation of the breakage-fusion-bridge mechanism through common fragile site activation in human breast cancer cells: the model of PIP gene duplication from a break at FRA7I. Human molecular genetics 11, 2887-94 (2002).
35. Zimonjic, D. B. et al. SMAD5 gene expression, rearrangements, copy number, and amplification at fragile site FRA5C in human hepatocellular carcinoma. Neoplasia (New York, N.Y.) 5, 390-6 (2003). (Pubitemid 37475647)
36. Pelliccia, F., Bosco, N. & Rocchi, A. Breakages at common fragile sites set boundaries of amplified regions in two leukemia cell lines K562-Molecular characterization of FRA2H and localization of a new CFS FRA2S. Cancer letters 299, 37-44 (2010).
37. Reshmi, S. C. et al. Relationship between FRA11F and 11q13 gene amplification in oral cancer. Genes Chromosomes Cancer 46, 143-154 (2007). (Pubitemid 44913379)
38. Tsantoulis, P. K. et al. Oncogene-induced replication stress preferentially targets common fragile sites in preneoplastic lesions. A genome-wide study. Oncogene 27, 3256-64 (2008). (Pubitemid 351733389)
39. Bartkova, J. et al. Oncogene-induced senescence is part of the tumorigenesis barrier imposed by DNA damage checkpoints. Nature 444, 633-7 (2006). (Pubitemid 44864442)
40. Wu, X., Li, Y., Crise, B. & Burgess, S. M. Transcription start regions in the human genome are favored targets for MLV integration. Science (New York, N.Y.) 300, 1749-51 (2003). (Pubitemid 36712571)
41. Mitchell, R. S. et al. Retroviral DNA integration: ASLV, HIV, and MLV show distinct target site preferences. PLoS Biol 2, E234 (2004).
42. Rohdewohld, H., Weiher, H., Reik, W., Jaenisch, R. & Breindl, M. Retrovirus integration and chromatin structure: Moloney murine leukemia proviral integration sites map near DNase I-hypersensitive sites. Journal of virology 61, 336-43 (1987). (Pubitemid 17001729)
43. Koren, B. et al. Efficient transduction and seeding of human endothelial cells onto metallic stents using bicistronic pseudo-typed retroviral vectors encoding vascular endothelial growth factor. Cardiovascular Revascularization Medicine 7, 173-178 (2006). (Pubitemid 44292063)
44. Lichter, P., Cremer, T., Borden, J., Manuelidis, L. & Ward, D. C. Delineation of individual human chromosomes in metaphase and interphase cells by in situ suppression hybridization using recombinant DNA libraries. Hum Genet 80, 224-234 (1988).
45. Mishmar, D. et al. Molecular characterization of a common fragile site (FRA7H) on human chromosome 7 by the cloning of a simian virus 40 integration site. Proceedings of the National Academy of Sciences of the United States of America 95, 8141-6 (1998). (Pubitemid 28326080)
46. Herrick, J., Bensimon, A. Single molecule analysis ofDNAreplication. Biochimie 81, 859-871 (1999).
47. Lebofsky, R., Heilig, R., Sonnleitner, M., Weissenbach, J. & Bensimon, A. DNA replication origin interference increases the spacing between initiation events in human cells. Molecular biology of the cell 17, 5337-45 (2006). (Pubitemid 44907373)