Genome-wide CRISPR screen in a mouse model of tumor growth and metastasis

Cell

Volumn 160, Issue 6, 2015, Pages 1246-1260

  Chen, Sidi ^a,b,c   Sanjana, Neville E ^b,c,d,e,f   Zheng, Kaijie ^c,d   Shalem, Ophir ^c,d   Lee, Kyungheon ^g   Shi, Xi ^c,d   Scott, David A ^c,d   Song, Jun ^g   Pan, Jen Q ^c,d   Weissleder, Ralph ^g,h   Lee, Hakho ^g   Zhang, Feng ^b,c,d,e,f   Sharp, Phillip A ^a,b  

^a David H Koch Institute for Integrative Cancer Research   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^d Stanley Center for Psychiatric Research   (United States)

^e MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^f Massachusetts Institute of Technology Cambridge   (United States)

^g MASSACHUSETTS GENERAL HOSPITAL   (United States)

^h HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RNA; SINGLE GUIDE RNA; UNCLASSIFIED DRUG; GUIDE RNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CELL LINE; CANCER GRAFT; CELL MUTANT; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; GENETIC ASSOCIATION; GENETIC SCREENING; HUMAN; IN VIVO STUDY; LOSS OF FUNCTION MUTATION; METASTASIS; MOLECULAR CLONING; MOUSE; MUTAGENESIS; NON SMALL CELL LUNG CANCER; NONHUMAN; PHENOTYPE; PRIMARY TUMOR; PRIORITY JOURNAL; TUMOR GROWTH; ANIMAL; CRISPR CAS SYSTEM; GENE INACTIVATION; GENETICS; GENOME-WIDE ASSOCIATION STUDY; LUNG TUMOR; PATHOLOGY;

ANIMALS; CARCINOMA, NON-SMALL-CELL LUNG; CRISPR-CAS SYSTEMS; GENE KNOCKOUT TECHNIQUES; GENOME-WIDE ASSOCIATION STUDY; HUMANS; LUNG NEOPLASMS; MICE; NEOPLASM METASTASIS; RNA, GUIDE;

EID: 84925008880     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2015.02.038     Document Type: Article

References (58)

1. N. Aceto, A. Bardia, D.T. Miyamoto, M.C. Donaldson, B.S. Wittner, J.A. Spencer, M. Yu, A. Pely, A. Engstrom, and H. Zhu Circulating tumor cell clusters are oligoclonal precursors of breast cancer metastasis Cell 158 2014 1110 1122
2. R. Barrangou, C. Fremaux, H. Deveau, M. Richards, P. Boyaval, S. Moineau, D.A. Romero, and P. Horvath CRISPR provides acquired resistance against viruses in prokaryotes Science 315 2007 1709 1712
3. J. Barretina, G. Caponigro, N. Stransky, K. Venkatesan, A.A. Margolin, S. Kim, C.J. Wilson, J. Lehár, G.V. Kryukov, and D. Sonkin The Cancer Cell Line Encyclopedia enables predictive modelling of anticancer drug sensitivity Nature 483 2012 603 607
4. A. Bolotin, B. Quinquis, A. Sorokin, and S.D. Ehrlich Clustered regularly interspaced short palindrome repeats (CRISPRs) have spacers of extrachromosomal origin Microbiology 151 2005 2551 2561
5. Cancer Genome Atlas Research Network Comprehensive genomic characterization of squamous cell lung cancers Nature 489 2012 519 525
6. Cancer Genome Atlas Research Network Comprehensive molecular profiling of lung adenocarcinoma Nature 511 2014 543 550
7. E. Cerami, J. Gao, U. Dogrusoz, B.E. Gross, S.O. Sumer, B.A. Aksoy, A. Jacobsen, C.J. Byrne, M.L. Heuer, and E. Larsson The cBiol. cancer genomics portal: an open platform for exploring multidimensional cancer genomics data Cancer Discovery 2 2012 401 404
8. S. Chen, Y. Xue, X. Wu, C. Le, A. Bhutkar, E.L. Bell, F. Zhang, R. Langer, and P.A. Sharp Global microRNA depletion suppresses tumor angiogenesis Genes Dev. 28 2014 1054 1067
9. Z. Cheng, R. Ma, W. Tan, and L. Zhang MiR-152 suppresses the proliferation and invasion of NSCLC cells by inhibiting FGF2 Exp. Mol. Med. 46 2014 e112
10. K. Chylinski, A. Le Rhun, and E. Charpentier The tracrRNA and Cas9 families of type II CRISPR-Cas immunity systems RNA Biol. 10 2013 726 737
11. K. Chylinski, K.S. Makarova, E. Charpentier, and E.V. Koonin Classification and evolution of type II CRISPR-Cas systems Nucleic Acids Res. 42 2014 6091 6105
12. L. Cong, F.A. Ran, D. Cox, S. Lin, R. Barretto, N. Habib, P.D. Hsu, X. Wu, W. Jiang, L.A. Marraffini, and F. Zhang Multiplex genome engineering using CRISPR/Cas systems Science 339 2013 819 823
13. E. Deltcheva, K. Chylinski, C.M. Sharma, K. Gonzales, Y. Chao, Z.A. Pirzada, M.R. Eckert, J. Vogel, and E. Charpentier CRISPR RNA maturation by trans-encoded small RNA and host factor RNase III Nature 471 2011 602 607
14. G. Francia, W. Cruz-Munoz, S. Man, P. Xu, and R.S. Kerbel Mouse models of advanced spontaneous metastasis for experimental therapeutics Nat. Rev. Cancer 11 2011 135 141
15. J. Gao, B.A. Aksoy, U. Dogrusoz, G. Dresdner, B. Gross, S.O. Sumer, Y. Sun, A. Jacobsen, R. Sinha, and E. Larsson Integrative analysis of complex cancer genomics and clinical profiles using the cBioPortal Sci. Signal. 6 2013 p11
16. J.E. Garneau, M.E. Dupuis, M. Villion, D.A. Romero, R. Barrangou, P. Boyaval, C. Fremaux, P. Horvath, A.H. Magadán, and S. Moineau The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA Nature 468 2010 67 71
17. L.A. Garraway, and E.S. Lander Lessons from the cancer genome Cell 153 2013 17 37
18. G. Gasiunas, R. Barrangou, P. Horvath, and V. Siksnys Cas9-crRNA ribonucleoprotein complex mediates specific DNA cleavage for adaptive immunity in bacteria Proc. Natl. Acad. Sci. USA 109 2012 E2579 E2586
19. L.A. Gilbert, M.A. Horlbeck, B. Adamson, J.E. Villalta, Y. Chen, E.H. Whitehead, C. Guimaraes, B. Panning, H.L. Ploegh, and M.C. Bassik Genome-scale CRISPR-mediated control of gene repression and activation Cell 159 2014 647 661
20. D. Hanahan, and R.A. Weinberg Hallmarks of cancer: the next generation Cell 144 2011 646 674
21. R. Heimann, and S. Hellman Aging, progression, and phenotype in breast cancer J. Clin. Oncol. 16 1998 2686 2692
22. P.D. Hsu, D.A. Scott, J.A. Weinstein, F.A. Ran, S. Konermann, V. Agarwala, Y. Li, E.J. Fine, X. Wu, and O. Shalem DNA targeting specificity of RNA-guided Cas9 nucleases Nat. Biotechnol. 31 2013 827 832
23. S. Huang, M. Hölzel, T. Knijnenburg, A. Schlicker, P. Roepman, U. McDermott, M. Garnett, W. Grernrum, C. Sun, and A. Prahallad MED12 controls the response to multiple cancer drugs through regulation of TGF-β receptor signaling Cell 151 2012 937 950
24. E. Jesien-Lewandowicz, D. Jesionek-Kupnicka, I. Zawlik, M. Szybka, D. Kulczycka-Wojdala, P. Rieske, M. Sieruta, D. Jaskolski, W. Och, and W. Skowronski High incidence of MGMT promoter methylation in primary glioblastomas without correlation with TP53 gene mutations Cancer Genet. Cytogenet. 188 2009 77 82
25. M. Jinek, K. Chylinski, I. Fonfara, M. Hauer, J.A. Doudna, and E. Charpentier A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity Science 337 2012 816 821
26. G. Kaczmarczyk, R. Lewandowski, W. Trautsolt, A. Ziółkowski, and J. Kozielski Cytological examination of pleural cavity lavage accompanied by the study of gene promoter hypermethylation of p16 and O6-methylguanine-DNA-methyltransferase genes in diagnostics of non-small cell lung cancer metastatic changes into pleura Contemp Oncol (Pozn) 16 2012 322 327
27. H. Koike-Yusa, Y. Li, E.P. Tan, Mdel.C. Velasco-Herrera, and K. Yusa Genome-wide recessive genetic screening in mammalian cells with a lentiviral CRISPR-guide RNA library Nat. Biotechnol. 32 2014 267 273
28. S. Konermann, M.D. Brigham, A.E. Trevino, J. Joung, O.O. Abudayyeh, C. Barcena, P.D. Hsu, N. Habib, J.S. Gootenberg, and H. Nishimasu Genome-scale transcriptional activation by an engineered CRISPR-Cas9 complex Nature 517 2015 583 588
29. B. Korczak, I.B. Robson, C. Lamarche, A. Bernstein, and R.S. Kerbel Genetic tagging of tumor cells with retrovirus vectors: clonal analysis of tumor growth and metastasis in vivo Mol. Cell. Biol. 8 1988 3143 3149
30. M.S. Kumar, R.E. Pester, C.Y. Chen, K. Lane, C. Chin, J. Lu, D.G. Kirsch, T.R. Golub, and T. Jacks Dicer1 functions as a haploinsufficient tumor suppressor Genes Dev. 23 2009 2700 2704
31. M.S. Lawrence, P. Stojanov, P. Polak, G.V. Kryukov, K. Cibulskis, A. Sivachenko, S.L. Carter, C. Stewart, C.H. Mermel, and S.A. Roberts Mutational heterogeneity in cancer and the search for new cancer-associated genes Nature 499 2013 214 218
32. J.G. Lohr, V.A. Adalsteinsson, K. Cibulskis, A.D. Choudhury, M. Rosenberg, P. Cruz-Gordillo, J.M. Francis, C.Z. Zhang, A.K. Shalek, and R. Satija Whole-exome sequencing of circulating tumor cells provides a window into metastatic prostate cancer Nat. Biotechnol. 32 2014 479 484
33. P. Mali, L. Yang, K.M. Esvelt, J. Aach, M. Guell, J.E. DiCarlo, J.E. Norville, and G.M. Church RNA-guided human genome engineering via Cas9 Science 339 2013 823 826
34. A.I. McClatchey, I. Saotome, K. Mercer, D. Crowley, J.F. Gusella, R.T. Bronson, and T. Jacks Mice heterozygous for a mutation at the Nf2 tumor suppressor locus develop a range of highly metastatic tumors Genes Dev. 12 1998 1121 1133
35. D.G. McFadden, T. Papagiannakopoulos, A. Taylor-Weiner, C. Stewart, S.L. Carter, K. Cibulskis, A. Bhutkar, A. McKenna, A. Dooley, and A. Vernon Genetic and clonal dissection of murine small cell lung carcinoma progression by genome sequencing Cell 156 2014 1298 1311
36. D.X. Nguyen, P.D. Bos, and J. Massagué Metastasis: from dissemination to organ-specific colonization Nat. Rev. Cancer 9 2009 274 284
37. P. Rouet, F. Smih, and M. Jasin Introduction of double-strand breaks into the genome of mouse cells by expression of a rare-cutting endonuclease Mol. Cell. Biol. 14 1994 8096 8106
38. N.E. Sanjana, O. Shalem, and F. Zhang Improved vectors and genome-wide libraries for CRISPR screening Nat. Methods 11 2014 783 784
39. R. Sapranauskas, G. Gasiunas, C. Fremaux, R. Barrangou, P. Horvath, and V. Siksnys The Streptococcus thermophilus CRISPR/Cas system provides immunity in Escherichia coli Nucleic Acids Res. 39 2011 9275 9282
40. C. Schiano, A. Casamassimi, M. Rienzo, F. de Nigris, L. Sommese, and C. Napoli Involvement of Mediator complex in malignancy Biochim. Biophys. Acta 1845 2014 66 83
41. D. Schramek, A. Sendoel, J.P. Segal, S. Beronja, E. Heller, D. Oristian, B. Reva, and E. Fuchs Direct in vivo RNAi screen unveils myosin IIa as a tumor suppressor of squamous cell carcinomas Science 343 2014 309 313
42. O. Shalem, N.E. Sanjana, E. Hartenian, X. Shi, D.A. Scott, T.S. Mikkelsen, D. Heckl, B.L. Ebert, D.E. Root, J.G. Doench, and F. Zhang Genome-scale CRISPR-Cas9 knockout screening in human cells Science 343 2014 84 87
43. D.D. Shao, W. Xue, E.B. Krall, A. Bhutkar, F. Piccioni, X. Wang, A.C. Schinzel, S. Sood, J. Rosenbluh, and J.W. Kim KRAS and YAP1 converge to regulate EMT and tumor survival Cell 158 2014 171 184
44. J.T. Tang, J.L. Wang, W. Du, J. Hong, S.L. Zhao, Y.C. Wang, H. Xiong, H.M. Chen, and J.Y. Fang MicroRNA 345, a methylation-sensitive microRNA is involved in cell proliferation and invasion in human colorectal cancer Carcinogenesis 32 2011 1207 1215
45. K. Tano, S. Shiota, J. Collier, R.S. Foote, and S. Mitra Isolation and structural characterization of a cDNA clone encoding the human DNA repair protein for O6-alkylguanine Proc. Natl. Acad. Sci. USA 87 1990 686 690
46. S. Valastyan, and R.A. Weinberg Tumor metastasis: molecular insights and evolving paradigms Cell 147 2011 275 292
47. S. Vanharanta, and J. Massagué Origins of metastatic traits Cancer Cell 24 2013 410 421
48. C. Waghorne, M. Thomas, A. Lagarde, R.S. Kerbel, and M.L. Breitman Genetic evidence for progressive selection and overgrowth of primary tumors by metastatic cell subpopulations Cancer Res. 48 1988 6109 6114
49. T. Wang, J.J. Wei, D.M. Sabatini, and E.S. Lander Genetic screens in human cells using the CRISPR-Cas9 system Science 343 2014 80 84
50. R.A. Weinberg The Biology of Cancer 2007 Garland Science
51. J. Yokota, M. Nishioka, M. Tani, and T. Kohno Genetic alterations responsible for metastatic phenotypes of lung cancer cells Clin. Exp. Metastasis 20 2003 189 193
52. L. Zender, W. Xue, J. Zuber, C.P. Semighini, A. Krasnitz, B. Ma, P. Zender, S. Kubicka, J.M. Luk, and P. Schirmacher An oncogenomics-based in vivo RNAi screen identifies tumor suppressors in liver cancer Cell 135 2008 852 864
53. Y. Zhou, S. Zhu, C. Cai, P. Yuan, C. Li, Y. Huang, and W. Wei High-throughput screening of a CRISPR/Cas9 library for functional genomics in human cells Nature 509 2014 487 491
54. J. Chung, D. Issadore, A. Ullal, K. Lee, R. Weissleder, and H. Lee Rare cell isolation and profiling on a hybrid magnetic/size-sorting chip Biomicrofluidics 7 2013 54107
55. B. Langmead, C. Trapnell, M. Pop, and S.L. Salzberg Ultrafast and memory-efficient alignment of short DNA sequences to the human genome Genome Biol. 10 2009 R25
56. M. Martin Cutadapt removes adapter sequences from high-throughput sequencing reads EMBnet 17 2011 10 12
57. R.J. Platt, S. Chen, Y. Zhou, M.J. Yim, L. Swiech, H.R. Kempton, J.E. Dahlman, O. Parnas, T.M. Eisenhaure, and M. Jovanovic CRISPR-Cas9 knockin mice for genome editing and cancer modeling Cell 159 2014 440 455
58. A. Subramanian, P. Tamayo, V.K. Mootha, S. Mukherjee, B.L. Ebert, M.A. Gillette, A. Paulovich, S.L. Pomeroy, T.R. Golub, E.S. Lander, and J.P. Mesirov Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles Proc. Natl. Acad. Sci. USA 102 2005 15545 15550