In vivo transcriptional activation using CRISPR/Cas9 in Drosophila

Genetics

Volumn 201, Issue 2, 2015, Pages 433-442

  Lin, Shuailiang ^a,b   Ewen Campen, Ben ^b   Ni, Xiaochun ^b   Housden, Benjamin E ^b   Perrimon, Norbert ^b,c  

^a TSINGHUA UNIVERSITY   (China)

^b HARVARD MEDICAL SCHOOL   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

CRISPR Cas9; Gain of function; Gene activation; Overexpression

Indexed keywords

GUIDE RNA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR DCAS9 VPR; TRANSCRIPTION FACTOR SNAIL; TRANSCRIPTION FACTOR TWIST; UNCLASSIFIED DRUG; DROSOPHILA PROTEIN; SNA PROTEIN, DROSOPHILA; TWI PROTEIN, DROSOPHILA; TWIST RELATED PROTEIN 1;

ANIMAL CELL; ARTICLE; CELL CULTURE; CONTROLLED STUDY; CRISPR CAS SYSTEM; DNA BASE COMPOSITION; DROSOPHILA; DROSOPHILA MELANOGASTER; GAIN OF FUNCTION MUTATION; GENE ACTIVATION; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; MESODERM; MOLECULAR CLONING; NONHUMAN; PRIORITY JOURNAL; START CODON; TRANSCRIPTION INITIATION; TRANSCRIPTION INITIATION SITE; ANIMAL; BIOSYNTHESIS; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN;

ANIMALS; CRISPR-CAS SYSTEMS; DROSOPHILA; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; MESODERM; RNA, GUIDE; SNAIL FAMILY TRANSCRIPTION FACTORS; TRANSCRIPTION FACTORS; TRANSCRIPTIONAL ACTIVATION; TWIST-RELATED PROTEIN 1;

EID: 84943638166     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.115.181065     Document Type: Article

References (44)

1. Anders, S., and W. Huber, 2010 Differential expression analysis for sequence count data. Genome Biol. 11: R106.
2. Anders, S., P. T. Pyl, and W. Huber, 2015 HTSeq: a Python framework to work with high-throughput sequencing data. Bioinformatics 31: 166-169.
3. Barrallo-Gimeno, A., and M. A. Nieto, 2005 The Snail genes as inducers of cell movement and survival: implications in development and cancer. Development 132: 3151-3161.
4. Bischof, J., M. Bjorklund, E. Furger, C. Schertel, J. Taipale et al., 2013 A versatile platform for creating a comprehensive UASORFeome library in Drosophila. Development 140: 2434-2442.
5. Boulay, J. L., C. Dennefeld, and A. Alberga, 1987 The Drosophila developmental gene snail encodes a protein with nucleic acid binding fingers. Nature 330: 395-398.
6. Chavez, A., J. Scheiman, S. Vora, B. W. Pruitt, and M. Tuttle et al., 2015 Highly efficient Cas9-mediated transcriptional programming. Nat. Methods 12: 326-328.
7. Chen, S., N. E. Sanjana, K. Zheng, O. Shalem, K. Lee et al., 2015 Genome-wide CRISPR screen in a mouse model of tumor growth and metastasis. Cell 160: 1-16.
8. Cheng, A. W., H. Wang, H. Yang, L. Shi, Y. Katz et al., 2013 Multiplexed activation of endogenous genes by CRISPRon, an RNA-guided transcriptional activator system. Cell Res. 23: 1163-1171.
9. Fuse, N., S. Hirose, and S. Hayashi, 1996 Determination of wing cell fate by the escargot and snail genes in Drosophila. Development 122: 1059-1067.
10. Gibson, D. G., 2011 Enzymatic assembly of overlapping DNA fragments. Methods Enzymol. 498: 349-361.
11. Gibson, D. G., L. Young, R.-Y. Chuang, J. C. Venter, C. A. Hutchison et al., 2009 Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat. Methods 6: 343-345.
12. Gilbert, L. A., M. H. Larson, L. Morsut, Z. Liu, G. A. Brar et al., 2013 CRISPR-mediated modular RNA-guided regulation of transcription in eukaryotes. Cell 154: 442-451.
13. Gilbert, L. A., M. A. Horlbeck, B. Adamson, J. E. Villalta, Y. Chen et al., 2014 Genome-scale CRISPR-mediated control of gene repression and activation. Cell 159: 1-15.
14. Gratz, S. J., F. P. Ukken, C. D. Rubinstein, G. Thiede, L. K. Donohue et al., 2014 Highly specific and efficient CRISPR/Cas9-catalyzed homology-directed repair in Drosophila. Genetics 196: 961-971.
15. Housden, B. E., S. Lin, and N. Perrimon, 2014 Cas9-based genome editing in Drosophila. Methods Enzymol. 546: 415-439.
16. Housden, B. E., A. J. Valvezan, C. Kelley, R. Sopko, S. Lin et al., 2015 Identification of potential drug targets for Tuberous Sclerosis Complex by synthetic screens combining CRISPRbased knockouts with RNAi. Science Signaling (in press).
17. Konermann, S., M. D. Brigham, A. E. Trevino, J. Joung, O. O. Abudayyeh et al., 2015 Genome-scale transcriptional activation by an engineered CRISPR-Cas9 complex. Nature 517: 583-588.
18. Kuscu, C., S. Arslan, R. Singh, J. Thorpe, and M. Adli, 2014 Genomewide analysis reveals characteristics of off-target sites bound by the Cas9 endonuclease. Nat. Biotechnol. 32: 1-9.
19. Leptin, M., 1991 Twist and snail as positive and negative regulators during Drosophila mesoderm development. Genes Dev. 5: 1568-1576.
20. Livak, K. J., and T. D. Schmittgen, 2001 Analysis of relative gene expression data using real-time quantitative PCR and the 22DDCT method. Methods 25: 402-408.
21. MacArthur, S., X.-Y. Li, J. Li, J. B. Brown, H. C. Chu et al., 2009 Developmental roles of 21 Drosophila transcription factors are determined by quantitative differences in binding to an overlapping set of thousands of genomic regions. Genome Biol. 10: R80.
22. Maeder, M. L., S. J. Linder, V. M. Cascio, Y. Fu, Q. H. Ho et al., 2013 CRISPR RNA-guided activation of endogenous human genes. Nat. Methods 10: 977-979.
23. Mali, P., J. Aach, P. B. Stranges, K. M. Esvelt, M. Moosburner et al., 2013 CAS9 transcriptional activators for target specificity screening and paired nickases for cooperative genome engineering. Nat. Biotechnol. 31: 833-838.
24. Markstein, M., C. Pitsouli, C. Villalta, S. E. Celniker, and N. Perrimon, 2008 Exploiting position effects and the gypsy retrovirus insulator to engineer precisely expressed transgenes. Nat. Genet. 40: 476-483.
25. Murre, C., P. S. McCaw, and D. Baltimore, 1989 A new DNA binding and dimerization motif in immunoglobulin enhancer binding, daughterless, MyoD, and myc proteins. Cell 56: 777-783.
26. Ng, M., F. J. Diaz-Benjumea, J. P. Vincent, J. Wu, and S. M. Cohen, 1996 Specification of the wing by localized expression of wingless protein. Nature 381: 316-318.
27. Ni, J.-Q., R. Zhou, B. Czech, L.-P. Liu, L. Holderbaum et al., 2011 A genome-scale shRNA resource for transgenic RNAi in Drosophila. Nat. Methods 8: 405-407.
28. Nieto, M. A., 2002 The snail superfamily of zinc-finger transcription factors. Nat. Rev. Mol. Cell Biol. 3: 155-166.
29. Perez-Pinera, P., D. D. Kocak, C. M. Vockley, A. F. Adler, A. M. Kabadi et al., 2013 RNA-guided gene activation by CRISPRCas9-based transcription factors. Nat. Methods 10: 973-976.
30. Port, F., H.-M. Chen, T. Lee, and S. L. Bullock, 2014 Optimized CRISPR/Cas tools for efficient germline and somatic genome engineering in Drosophila. Proc. Natl. Acad. Sci. USA 111: E2967-E2976.
31. Qi, L. S. M. H. Larson, L. A. Gilbert, J. A. Doudna, J. S. Weissman et al., 2013 Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression. Cell 152: 1173-1183.
32. Rembold, M., L. Ciglar, J. O. Yanez-Cuna, R. P. Zinzen, C. Girardot et al., 2014 A conserved role for Snail as a potentiator of active transcription. Genes Dev. 28: 167-181.
33. Robinson, J. T., H. Thorvaldsdóttir, W. Winckler, M. Guttman, E. S. Lander et al., 2011 Integrative genomics viewer. Nat. Biotechnol. 29: 24-26.
34. Rørth, P., 1996 A modular misexpression screen in Drosophila detecting tissue-specific phenotypes. Proc. Natl. Acad. Sci. USA 93: 12418-12422.
35. Sandmann, T., C. Girardot, M. Brehme, W. Tongprasit, V. Stolc et al., 2007 A core transcriptional network for early mesoderm development in Drosophila melanogaster. Genes Dev. 21: 436-449.
36. Shishido, E., S. Higashijima, Y. Emori, and K. Saigo, 1993 Two FGF-receptor homologues of Drosophila: one is expressed in mesodermal primordium in early embryos. Development 117: 751-761.
37. Staudt, N., A. Molitor, K. Somogyi, J. Mata, S. Curado et al., 2005 Gain-of-function screen for genes that affect Drosophila muscle pattern formation. PLoS Genet. 1: e55.
38. Tanenbaum, M. E., L. A. Gilbert, L. S. Qi, J. S. Weissman, and R. D. Vale, 2014 A protein-tagging system for signal amplification in gene expression and fluorescence imaging. Cell 159: 635-646.
39. Thisse, B., C. Stoetzel, C. Gorostiza-Thisse, and F. Perrin-Schmitt, 1988 Sequence of the twist gene and nuclear localization of its protein in endomesodermal cells of early Drosophila embryos. EMBO J. 7: 2175-2183.
40. Trapnell, C., L. Pachter, and S. L. Salzberg, 2009 TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25: 1105-1111.
41. Trapnell, C., B. A. Williams, G. Pertea, A. Mortazavi, G. Kwan et al., 2010 Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 28: 511-515.
42. Wu, X., D. A. Scott, A. J. Kriz, A. C. Chiu, P. D. Hsu et al., 2014 Genome-wide binding of the CRISPR endonuclease Cas9 in mammalian cells. Nat. Biotechnol. 32: 1-9.
43. Zalatan, J. G., M. E. Lee, R. Almeida, L. A. Gilbert, E. H. Whitehead et al., 2014 Engineering complex synthetic transcriptional programs with CRISPR RNA scaffolds. Cell 160: 1-12.
44. Zeitlinger, J., R. P. Zinzen, A. Stark, M. Kellis, H. Zhang et al., 2007 Whole-genome ChIP-chip analysis of Dorsal, Twist, and Snail suggests integration of diverse patterning processes in the Drosophila embryo. Genes Dev. 21: 385-390.