Somatic CRISPR/Cas9-mediated tumour suppressor disruption enables versatile brain tumour modelling

Nature Communications

Volumn 6, Issue , 2015, Pages

  Zuckermann, Marc ^a   Hovestadt, Volker ^a   Knobbe Thomsen, Christiane B ^a,b   Zapatka, Marc ^a   Northcott, Paul A ^a   Schramm, Kathrin ^a   Belic, Jelena ^a   Jones, David T W ^a   Tschida, Barbara ^c   Moriarity, Branden ^c   Largaespada, David ^c   Roussel, Martine F ^d   Korshunov, Andrey ^a,e   Reifenberger, Guido ^a,b   Pfister, Stefan M ^a   Lichter, Peter ^a   Kawauchi, Daisuke ^a   Gronych, Jan ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b HEINRICH HEINE UNIVERSITY   (Germany)

^c UNIVERSITY OF MINNESOTA   (United States)

^d ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^e UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; BRAIN; GENOME; MODEL VALIDATION; TUMOR;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN TUMOR; CARCINOGENESIS; CONTROLLED STUDY; CRISPR CAS SYSTEM; FEMALE; GENE DELETION; GENE DISRUPTION; GENE SEQUENCE; GENE TARGETING; GLIOBLASTOMA; IN VITRO STUDY; IN VIVO STUDY; MALE; MEDULLOBLASTOMA; MOUSE; NF1 GENE; NONHUMAN; PTEN GENE; TRP53 GENE; TUMOR SUPPRESSOR GENE; ANIMAL; DISEASE MODEL; DNA SEQUENCE; EXPERIMENTAL NEOPLASM; GENE EXPRESSION PROFILING; GENE INACTIVATION; GENETICS; PATHOLOGY; PROCEDURES;

ANIMALIA;

CELL SURFACE RECEPTOR; NEUROFIBROMIN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN P53; PROTEIN PATCHED; PROTEIN PATCHED 1; PTCH PROTEIN, HUMAN; PTCH1 PROTEIN, MOUSE; PTEN PROTEIN, MOUSE;

ANIMALS; BRAIN NEOPLASMS; CRISPR-CAS SYSTEMS; DISEASE MODELS, ANIMAL; GENE EXPRESSION PROFILING; GENE KNOCKOUT TECHNIQUES; GLIOBLASTOMA; MEDULLOBLASTOMA; MICE; NEOPLASMS, EXPERIMENTAL; NEUROFIBROMIN 1; PATCHED RECEPTORS; PATCHED-1 RECEPTOR; PTEN PHOSPHOHYDROLASE; RECEPTORS, CELL SURFACE; SEQUENCE ANALYSIS, DNA; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84931291649     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms8391     Document Type: Article

References (48)

1. Garraway, L. A., Lander, E. S. Lessons from the cancer genome. Cell 153, 17-37 (2013).
2. Cong, L. et al. Multiplex genome engineering using CRISPR/Cas systems. Science 339, 819-823 (2013).
3. Mali, P. et al. RNA-guided human genome engineering via Cas9. Science 339, 823-826 (2013).
4. Jinek, M. et al. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337, 816-821 (2012).
5. Valerie, K., Povirk, L. F. Regulation and mechanisms of mammalian double-strand break repair. Oncogene 22, 5792-5812 (2003).
6. Platt, R. J. et al. CRISPR-Cas9 knockin mice for genome editing and cancer modeling. Cell 159, 440-455 (2014).
7. Xue, W. et al. CRISPR-mediated direct mutation of cancer genes in the mouse liver. Nature 514, 380-384 (2014).
8. Abdallah, B. et al. A powerful nonviral vector for in vivo gene transfer into the adult mammalian brain: polyethylenimine. Hum. Gene Ther. 7, 1947-1954 (1996).
9. Saito, T. In vivo electroporation in the embryonic mouse central nervous system. Nat. Protoc. 1, 1552-1558 (2006).
10. Taylor, M. D. et al. Molecular subgroups of medulloblastoma: the current consensus. Acta. Neuropathol. 123, 465-472 (2012).
11. Ostrom, Q. T. et al. CBTRUS statistical report: Primary brain and central nervous system tumors diagnosed in the United States in 2006-2010. Neuro-oncol. 15(Suppl 2): 1-56 (2013).
12. Northcott, P. A. et al. Medulloblastomics: the end of the beginning. Nat. Rev. Cancer 12, 818-834 (2012).
13. Wechsler-Reya, R. J., Scott, M. P. Control of neuronal precursor proliferation in the cerebellum by Sonic Hedgehog. Neuron 22, 103-114 (1999).
14. Goodrich, L. V., Milenkovic, L., Higgins, K. M., Scott, M. P. Altered neural cell fates and medulloblastoma in mouse patched mutants. Science 277, 1109-1113 (1997).
15. Wetmore, C., Eberhart, D. E., Curran, T. The normal patched allele is expressed in medulloblastomas from mice with heterozygous germ-line mutation of patched. Cancer Res. 60, 2239-2246 (2000).
16. Yang, Z. J. et al. Medulloblastoma can be initiated by deletion of Patched in lineage-restricted progenitors or stem cells. Cancer Cell 14, 135-145 (2008).
17. Schuller, U. et al. Acquisition of granule neuron precursor identity is a critical determinant of progenitor cell competence to form Shh-induced medulloblastoma. Cancer Cell 14, 123-134 (2008).
18. Wetmore, C., Eberhart, D. E., Curran, T. Loss of p53 but not ARF accelerates medulloblastoma in mice heterozygous for patched. Cancer Res. 61, 513-516 (2001).
19. Kool, M. et al. Genome sequencing of SHH medulloblastoma predicts genotype-related response to smoothened inhibition. Cancer Cell 25, 393-405 (2014).
20. Gonzales, M. The 2000 World Health Organization classification of tumours of the nervous system. J. Clin. Neurosci. 8, 1-3 (2001).
21. Zong, H., Parada, L. F., Baker, S. J. Cell of origin for malignant gliomas and its implication in therapeutic development. Cold Spring Harb. Perspect. Biol. 7, a020610 (2015).
22. Alcantara Llaguno, S. et al. Malignant astrocytomas originate from neural stem/progenitor cells in a somatic tumor suppressor mouse model. Cancer Cell 15, 45-56 (2009).
23. Verhaak, R. G. et al. Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell 17, 98-110 (2010).
24. Brennan, C. W. et al. The somatic genomic landscape of glioblastoma. Cell 155, 462-477 (2013).
25. Chen, J. et al. A restricted cell population propagates glioblastoma growth after chemotherapy. Nature 488, 522-526 (2012).
26. Zhu, Y. et al. Early inactivation of p53 tumor suppressor gene cooperating with NF1 loss induces malignant astrocytoma. Cancer Cell 8, 119-130 (2005).
27. Oliver, T. G. et al. Loss of patched and disruption of granule cell development in a pre-neoplastic stage of medulloblastoma. Development 132, 2425-2439 (2005).
28. Duan, D., Fu, Y., Paxinos, G., Watson, C. Spatiotemporal expression patterns of Pax6 in the brain of embryonic, newborn, and adult mice. Brain Struct. Funct. 218, 353-372 (2013).
29. Akazawa, C., Ishibashi, M., Shimizu, C., Nakanishi, S., Kageyama, R. A mammalian helix-loop-helix factor structurally related to the product of Drosophila proneural gene atonal is a positive transcriptional regulator expressed in the developing nervous system. J. Biol. Chem. 270, 8730-8738 (1995).
30. Northcott, P. A. et al. Medulloblastoma comprises four distinct molecular variants. J. Clin. Oncol. 29, 1408-1414 (2011).
31. Gibson, P. et al. Subtypes of medulloblastoma have distinct developmental origins. Nature 468, 1095-1099 (2010).
32. Kawauchi, D. et al. A mouse model of the most aggressive subgroup of human medulloblastoma. Cancer Cell 21, 168-180 (2012).
33. Pei, Y. et al. An animal model of MYC-driven medulloblastoma. Cancer Cell 21, 155-167 (2012).
34. Swartling, F. J. et al. Pleiotropic role for MYCN in medulloblastoma. Genes Dev. 24, 1059-1072 (2010).
35. Cho, S. W., Kim, S., Kim, J. M., Kim, J. S. Targeted genome engineering in human cells with the Cas9 RNA-guided endonuclease. Nat. Biotechnol. 31, 230-232 (2013).
36. Jinek, M. et al. RNA-programmed genome editing in human cells. eLife 2, e00471 (2013).
37. Fu, Y. et al. High-frequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells. Nat. Biotechnol. 31, 822-826 (2013).
38. Hsu, P. D. et al. DNA targeting specificity of RNA-guided Cas9 nucleases. Nat. Biotechnol. 31, 827-832 (2013).
39. Pattanayak, V. et al. High-throughput profiling of off-target DNA cleavage reveals RNA-programmed Cas9 nuclease specificity. Nat. Biotechnol. 31, 839-843 (2013).
40. Cho, S. W. et al. Analysis of off-target effects of CRISPR/Cas-derived RNA-guided endonucleases and nickases. Genome Res. 24, 132-141 (2014).
41. Jiang, H., Wong, W. H. SeqMap: mapping massive amount of oligonucleotides to the genome. Bioinformatics 24, 2395-2396 (2008).
42. Muguruma, K. et al. Ontogeny-recapitulating generation and tissue integration of ES cell-derived Purkinje cells. Nat. Neurosci. 13, 1171-1180 (2010).
43. Sato, Y. et al. Stable integration and conditional expression of electroporated transgenes in chicken embryos. Dev. Biol. 305, 616-624 (2007).
44. Guschin, D. Y. et al. A rapid and general assay for monitoring endogenous gene modification. Methods Mol. Biol. 649, 247-256 (2010).
45. Zhang, J., Kobert, K., Flouri, T., Stamatakis, A. PEAR: a fast and accurate Illumina Paired-End reAd mergeR. Bioinformatics 30, 614-620 (2014).
46. Keane, T. M. et al. Mouse genomic variation and its effect on phenotypes and gene regulation. Nature 477, 289-294 (2011).
47. Robinson, G. et al. Novel mutations target distinct subgroups of medulloblastoma. Nature 488, 43-48 (2012).
48. Saeed, A. I. et al. TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34, 374-378 (2003).