High-throughput insertional mutagenesis screens in mice to identify oncogenic networks (original) (raw)
Uren, A. G., Kool, J., Berns, A. & van Lohuizen, M. Retroviral insertional mutagenesis: past, present and future. Oncogene24, 7656–7672 (2005). This review provides an historical overview of retroviral insertional mutagenesis screens and the different mechanisms in which genes can be mutated by retroviral integrations. ArticleCAS Google Scholar
Jonkers, J. & Berns, A. Retroviral insertional mutagenesis as a strategy to identify cancer genes. Biochim. Biophys. Acta1287, 29–57 (1996). PubMed Google Scholar
Uren, A. G. et al. Large-scale mutagenesis in p19ARF- and p53-deficient mice identifies cancer genes and their collaborative networks. Cell133, 727–741 (2008). ArticleCAS Google Scholar
Jonkers, J., Korswagen, H. C., Acton, D., Breuer, M. & Berns, A. Activation of a novel proto-oncogene, Frat1, contributes to progression of mouse T-cell lymphomas. EMBO J.16, 441–450 (1997). ArticleCAS Google Scholar
Nihrane, A., Fujita, K., Willey, R., Lyu, M. S. & Silver, J. Murine leukemia virus envelope protein in transgenic-mouse serum blocks infection in vitro. J. Virol.70, 1882–1889 (1996). CASPubMedPubMed Central Google Scholar
Ikeda, H. & Sugimura, H. Fv-4 resistance gene: a truncated endogenous murine leukemia virus with ecotropic interference properties. J. Virol.63, 5405–5412 (1989). CASPubMedPubMed Central Google Scholar
Ott, D. & Rein, A. Basis for receptor specificity of nonecotropic murine leukemia virus surface glycoprotein gp70SU. J. Virol.66, 4632–4638 (1992). CASPubMedPubMed Central Google Scholar
Heidmann, T., Heidmann, O. & Nicolas, J. F. An indicator gene to demonstrate intracellular transposition of defective retroviruses. Proc. Natl Acad. Sci. USA85, 2219–2223 (1988). ArticleCAS Google Scholar
Tchenio, T. & Heidmann, T. Defective retroviruses can disperse in the human genome by intracellular transposition. J. Virol.65, 2113–2118 (1991). CASPubMedPubMed Central Google Scholar
Dzuris, J. L., Zhu, W., Kapkov, D., Golovkina, T. V. & Ross, S. R. Expression of mouse mammary tumour virus envelope protein does not prevent superinfection in vivo or in vitro. Virology263, 418–426 (1999). ArticleCAS Google Scholar
Suzuki, T., Minehata, K., Akagi, K., Jenkins, N. A. & Copeland, N. G. Tumour suppressor gene identification using retroviral insertional mutagenesis in _Blm_-deficient mice. EMBO J.25, 3422–3431 (2006). ArticleCAS Google Scholar
Suzuki, T. et al. New genes involved in cancer identified by retroviral tagging. Nature Genet.32, 166–174 (2002). An elegant study in which a hypomorphicBlmallele is used to induce LOH of retrovirally inactivated tumour suppressor genes. ArticleCAS Google Scholar
Stewart, M. et al. Insertional mutagenesis reveals progression genes and checkpoints in MYC/Runx2 lymphomas. Cancer Res.67, 5126–5133 (2007). ArticleCAS Google Scholar
Mikkers, H. et al. High-throughput retroviral tagging to identify components of specific signaling pathways in cancer. Nature Genet.32, 153–159 (2002). ArticleCAS Google Scholar
Erkeland, S. J. et al. Large-scale identification of disease genes involved in acute myeloid leukemia. J. Virol.78, 1971–1980 (2004). ArticleCAS Google Scholar
Lund, A. H. et al. Genome-wide retroviral insertional tagging of genes involved in cancer in _Cdkn2a_-deficient mice. Nature Genet.32, 160–165 (2002). ArticleCAS Google Scholar
Theodorou, V. et al. MMTV insertional mutagenesis identifies genes, gene families and pathways involved in mammary cancer. Nature Genet.39, 759–769 (2007). The first large-scale MMTV insertional mutagenesis screen to identify new cancer genes in mammary tumours. ArticleCAS Google Scholar
Kim, R. et al. Genome-based identification of cancer genes by proviral tagging in mouse retrovirus-induced T-cell lymphomas. J. Virol.77, 2056–2062 (2003). ArticleCAS Google Scholar
Hasemann, M. S. et al. Mutation of C/EBPα predisposes to the development of myeloid leukemia in a retroviral insertional mutagenesis screen. Blood111, 4309–4321 (2008). ArticleCAS Google Scholar
Shendure, J. & Ji, H. Next-generation DNA sequencing. Nature Biotechnol.26, 1135–1145 (2008). An introduction to, and overview of, next-generation massive parallel sequencing technologies. ArticleCAS Google Scholar
Dupuy, A. J., Akagi, K., Largaespada, D. A., Copeland, N. G. & Jenkins, N. A. Mammalian mutagenesis using a highly mobile somatic Sleeping Beauty transposon system. Nature436, 221–226 (2005). ArticleCAS Google Scholar
Collier, L. S., Carlson, C. M., Ravimohan, S., Dupuy, A. J. & Largaespada, D. A. Cancer gene discovery in solid tumours using transposon-based somatic mutagenesis in the mouse. Nature436, 272–276 (2005). The first two papers, which were published back-to-back, to report transposon mutagenesis systems that efficiently induce tumours in mice. ArticleCAS Google Scholar
Carlson, C. M. & Largaespada, D. A. Insertional mutagenesis in mice: new perspectives and tools. Nature Rev. Genet.6, 568–580 (2005). ArticleCAS Google Scholar
Keng, V. W. et al. A conditional transposon-based insertional mutagenesis screen for genes associated with mouse hepatocellular carcinoma. Nature Biotechnol.27, 264–274 (2009). ArticleCAS Google Scholar
Starr, T. K. et al. A transposon-based genetic screen in mice identifies genes altered in colorectal cancer. Science323, 1747–1750 (2009). ArticleCAS Google Scholar
Beverly, L. J., Felsher, D. W. & Capobianco, A. J. Suppression of p53 by Notch in lymphomagenesis: implications for initiation and regression. Cancer Res.65, 7159–7168 (2005). ArticleCAS Google Scholar
Beverly, L. J. & Capobianco, A. J. Perturbation of Ikaros isoform selection by MLV integration is a cooperative event in NotchIC-induced T cell leukemogenesis. Cancer Cell3, 551–564 (2003). ArticleCAS Google Scholar
Iwasaki, M. et al. Identification of cooperative genes for NUP98–HOXA9 in myeloid leukemogenesis using a mouse model. Blood105, 784–793 (2005). ArticleCAS Google Scholar
Castilla, L. H. et al. Identification of genes that synergize with Cbfb–MYH11 in the pathogenesis of acute myeloid leukemia. Proc. Natl Acad. Sci. USA101, 4924–4929 (2004). ArticleCAS Google Scholar
Feldman, B. J., Reid, T. R. & Cleary, M. L. Pim1 cooperates with E2a–Pbx1 to facilitate the progression of thymic lymphomas in transgenic mice. Oncogene15, 2735–2742 (1997). ArticleCAS Google Scholar
Slape, C. et al. Retroviral insertional mutagenesis identifies genes that collaborate with NUP98_–_HOXD13 during leukemic transformation. Cancer Res.67, 5148–5155 (2007). ArticleCAS Google Scholar
Li, J. et al. Leukaemia disease genes: large-scale cloning and pathway predictions. Nature Genet.23, 348–353 (1999). ArticleCAS Google Scholar
Erkeland, S. J. et al. Significance of murine retroviral mutagenesis for identification of disease genes in human acute myeloid leukemia. Cancer Res.66, 622–626 (2006). ArticleCAS Google Scholar
Adams, J. M. et al. The c-myc oncogene driven by immunoglobulin enhancers induces lymphoid malignancy in transgenic mice. Nature318, 533–538 (1985). ArticleCAS Google Scholar
Ellwood-Yen, K. et al. Myc-driven murine prostate cancer shares molecular features with human prostate tumours. Cancer Cell4, 223–238 (2003). ArticleCAS Google Scholar
Jacobs, J. J. et al. Bmi-1 collaborates with c-Myc in tumourigenesis by inhibiting c-Myc- induced apoptosis via INK4a/ARF. Genes Dev.13, 2678–2690 (1999). ArticleCAS Google Scholar
van der Lugt, N. M. et al. Proviral tagging in E mu-myc transgenic mice lacking the Pim-1 proto-oncogene leads to compensatory activation of Pim-2. EMBO J.14, 2536–2544 (1995). ArticleCAS Google Scholar
Soucek, L. et al. Modelling Myc inhibition as a cancer therapy. Nature455, 679–683 (2008). ArticleCAS Google Scholar
Lazo, P. A., Lee, J. S. & Tsichlis, P. N. Long-distance activation of the Myc protooncogene by provirus insertion in Mlvi-1 or Mlvi-4 in rat T-cell lymphomas. Proc. Natl Acad. Sci. USA87, 170–173 (1990). ArticleCAS Google Scholar
Hickson, I. D. RecQ helicases: caretakers of the genome. Nature Rev. Cancer3, 169–178 (2003). ArticleCAS Google Scholar
Luo, G. et al. Cancer predisposition caused by elevated mitotic recombination in Bloom mice. Nature Genet.26, 424–429 (2000). ArticleCAS Google Scholar
Garrett-Engele, C. M. et al. A mechanism misregulating p27 in tumours discovered in a functional genomic screen. PLoS Genet.3, e219 (2007). Article Google Scholar
Tsihlias, J., Kapusta, L. & Slingerland, J. The prognostic significance of altered cyclin-dependent kinase inhibitors in human cancer. Annu. Rev. Med.50, 401–423 (1999). ArticleCAS Google Scholar
Park, M. S. et al. p27 and Rb are on overlapping pathways suppressing tumourigenesis in mice. Proc. Natl Acad. Sci. USA96, 6382–6387 (1999). ArticleCAS Google Scholar
Pinkel, D. & Albertson, D. G. Array comparative genomic hybridization and its applications in cancer. Nature Genet.37, S11–S17 (2005). ArticleCAS Google Scholar
Carrasco, D. R. et al. High-resolution genomic profiles define distinct clinico-pathogenetic subgroups of multiple myeloma patients. Cancer Cell9, 313–325 (2006). ArticleCAS Google Scholar
Wood, L. D. et al. The genomic landscapes of human breast and colorectal cancers. Science318, 1108–1113 (2007). A paper describing mutations that were identified by sequencing a panel of human breast cancers. Multiple genes that are mutated in humans were also found to be CISs in MMTV-induced tumours in mice. ArticleCAS Google Scholar
Sjoblom, T. et al. The consensus coding sequences of human breast and colorectal cancers. Science314, 268–274 (2006). Article Google Scholar
Parsons, D. W. et al. An integrated genomic analysis of human glioblastoma multiforme. Science321, 1807–1812 (2008). ArticleCAS Google Scholar
Jones, S. et al. Core signaling pathways in human pancreatic cancers revealed by global genomic analyses. Science321, 1801–1806 (2008). ArticleCAS Google Scholar
Fujino, Y., Ohno, K. & Tsujimoto, H. Molecular pathogenesis of feline leukemia virus-induced malignancies: insertional mutagenesis. Vet. Immunol. Immunopathol.123, 138–143 (2008). ArticleCAS Google Scholar
Kanter, M. R., Smith, R. E. & Hayward, W. S. Rapid induction of B-cell lymphomas: insertional activation of c-myb by avian leukosis virus. J. Virol.62, 1423–1432 (1988). CASPubMedPubMed Central Google Scholar
van Agthoven, T. et al. Functional identification of genes causing estrogen independence of human breast cancer cells. Breast Cancer Res. Treat.114, 23–30 (2009). Article Google Scholar
Dorssers, L. C., van, A. T., Dekker, A., van Agthoven, T. L. & Kok, E. M. Induction of antiestrogen resistance in human breast cancer cells by random insertional mutagenesis using defective retroviruses: identification of bcar-1, a common integration site. Mol. Endocrinol.7, 870–878 (1993). These authors demonstrate that insertional mutagenesis can be used to screen for genes that confer resistance to therapeutic agentsin vivo. CASPubMed Google Scholar
van der, F. S. et al. Bcar1/p130Cas protein and primary breast cancer: prognosis and response to tamoxifen treatment. J. Natl Cancer Inst.92, 120–127 (2000). Article Google Scholar
Miething, C. et al. Retroviral insertional mutagenesis identifies RUNX genes involved in chronic myeloid leukemia disease persistence under imatinib treatment. Proc. Natl Acad. Sci. USA104, 4594–4599 (2007). ArticleCAS Google Scholar
Johansson, F. K., Goransson, H. & Westermark, B. Expression analysis of genes involved in brain tumour progression driven by retroviral insertional mutagenesis in mice. Oncogene24, 3896–3905 (2005). ArticleCAS Google Scholar
Hanai, S. et al. Integration of human T-cell leukemia virus type 1 in genes of leukemia cells of patients with adult T-cell leukemia. Cancer Sci.95, 306–310 (2004). ArticleCAS Google Scholar
Killebrew, D. & Shiramizu, B. Pathogenesis of HIV-associated non-Hodgkin lymphoma. Curr. HIV Res.2, 215–221 (2004). ArticleCAS Google Scholar
Thrasher, A. J. et al. Gene therapy: X-SCID transgene leukaemogenicity. Nature443, E5–E6; discussion E6–E7 (2006). Article Google Scholar
de Ridder, J., Uren, A., Kool, J., Reinders, M. & Wessels, L. Detecting statistically significant common insertion sites in retroviral insertional mutagenesis screens. PLoS Comput. Biol.2, e166 (2006). Article Google Scholar
Wu, X., Li, Y., Crise, B. & Burgess, S. M. Transcription start regions in the human genome are favored targets for MLV integration. Science300, 1749–1751 (2003). ArticleCAS Google Scholar
Berry, C., Hannenhalli, S., Leipzig, J. & Bushman, F. D. Selection of target sites for mobile DNA integration in the human genome. PLoS Comput. Biol.2, e157 (2006). Article Google Scholar
Lewinski, M. K. et al. Retroviral DNA integration: viral and cellular determinants of target-site selection. PLoS Pathog.2, e60 (2006). Article Google Scholar
Mitchell, R. S. et al. Retroviral DNA integration: ASLV, HIV, and MLV show distinct target site preferences. PLoS Biol.2, e234 (2004). Article Google Scholar
Felice, B. et al. Transcription factor binding sites are genetic determinants of retroviral integration in the human genome. PLoS ONE4, e4571 (2009). Article Google Scholar
Sauvageau, M. et al. Quantitative expression profiling guided by common retroviral insertion sites reveals novel and cell type specific cancer genes in leukemia. Blood111, 790–799 (2008). ArticleCAS Google Scholar
Su, Q. et al. A DNA transposon-based approach to validate oncogenic mutations in the mouse. Proc. Natl Acad. Sci. USA105, 19904–19909 (2008). ArticleCAS Google Scholar
Wilson, M. H., Coates, C. J. & George, A. L. Jr. PiggyBac transposon-mediated gene transfer in human cells. Mol. Ther.15, 139–145 (2007). ArticleCAS Google Scholar
van Lohuizen, M., Breuer, M. & Berns, A. N-myc is frequently activated by proviral insertion in MuLV-induced T cell lymphomas. EMBO J.8, 133–136 (1989). ArticleCAS Google Scholar
Girard, L. & Jolicoeur, P. A full-length Notch1 allele is dispensable for transformation associated with a provirally activated truncated Notch1 allele in Moloney MuLV-infected MMTVD/myc transgenic mice. Oncogene16, 517–522 (1998). ArticleCAS Google Scholar
Weng, A. P. et al. Activating mutations of NOTCH1 in human T cell acute lymphoblastic leukemia. Science306, 269–271 (2004). ArticleCAS Google Scholar
Yang, L. T. et al. Fringe glycosyltransferases differentially modulate Notch1 proteolysis induced by Delta1 and Jagged1. Mol. Biol. Cell16, 927–942 (2005). ArticleCAS Google Scholar
Haines, N. & Irvine, K. D. Glycosylation regulates Notch signalling. Nature Rev. Mol. Cell Biol.4, 786–797 (2003). ArticleCAS Google Scholar
Moloney, D. J. et al. Fringe is a glycosyltransferase that modifies Notch. Nature406, 369–375 (2000). ArticleCAS Google Scholar
Largaespada, D. A., Shaughnessy, J. D. Jr, Jenkins, N. A. & Copeland, N. G. Retroviral integration at the Evi-2 locus in BXH-2 myeloid leukemia cell lines disrupts Nf1 expression without changes in steady-state Ras-GTP levels. J. Virol.69, 5095–5102 (1995). CASPubMedPubMed Central Google Scholar
Cho, B. C. et al. Frequent disruption of the Nf1 gene by a novel murine AIDS virus-related provirus in BXH-2 murine myeloid lymphomas. J. Virol.69, 7138–7146 (1995). CASPubMedPubMed Central Google Scholar