A rapid and effective method for screening, sequencing and reporter verification of engineered frameshift mutations in zebrafish

DMM Disease Models and Mechanisms

Volumn 10, Issue 6, 2017, Pages 811-822

  Prykhozhij, Sergey V ^a   Steele, Shelby L ^a   Razaghi, Babak ^a   Berman, Jason N ^a  

^a DALHOUSIE UNIVERSITY   (Canada)

Author keywords

Cas9; CRISPR; Mutation; Reporter; SgRNA; Zebrafish

Indexed keywords

CHROMODOMAIN HELICASE DNA BINDING PROTEIN 7; DNA BINDING PROTEIN; E3 UBIQUITIN PROTEIN LIGASE 1; MESSENGER RNA; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; ZEBRAFISH PROTEIN;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY DETECTION; ARTICLE; CONTROLLED STUDY; CRISPR CAS SYSTEM; EMBRYO; EXON SKIPPING; FRAMESHIFT MUTATION; GENE DELETION; GENE EXPRESSION; GENETIC ENGINEERING; HETEROZYGOSITY; HETEROZYGOTE; LOSS OF FUNCTION MUTATION; MISSENSE MUTATION; MOLECULAR CLONING; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; RESTRICTION SITE; SANGER SEQUENCING; START CODON; ZEBRA FISH; ANIMAL; DNA SEQUENCE; EXON; FLUORESCENCE; GENETIC SCREENING; GENETICS; NUCLEOTIDE SEQUENCE; PHENOTYPE; PROCEDURES; REPORTER GENE; REPRODUCIBILITY; RNA SPLICING;

ANIMALS; BASE SEQUENCE; CLONING, MOLECULAR; EXONS; FLUORESCENCE; FRAMESHIFT MUTATION; GENES, REPORTER; GENETIC ENGINEERING; GENETIC TESTING; PHENOTYPE; REPRODUCIBILITY OF RESULTS; RNA SPLICING; SEQUENCE ANALYSIS, DNA; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 85020461642     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.026765     Document Type: Article

References (55)

1. Adriao, A., Conceicao, N. and Cancela, M. L. (2016). MEF2C orthologues from zebrafi sh: evolution, expression and promoter regulation. Arch. Biochem. Biophys. 591, 43-56.
2. Barbosa, C., Peixeiro, I. and Romao, L. (2013). Gene expression regulation by upstream open reading frames and human disease. PLoS Genet. 9, 1-12.
3. Bazykin, G. A. and Kochetov, A. V. (2011). Alternative translation start sites are conserved in eukaryotic genomes. Nucleic Acids Res. 39, 567-577.
4. Bergman, J. E. H., Janssen, N., Hoefsloot, L. H., Jongmans, M. C. J., Hofstra, R. M. W. and van Ravenswaaij-Arts, C. M. A. (2011). CHD7 mutations and CHARGE syndrome: the clinical implications of an expanding phenotype. J. Med. Genet. 48, 334-342.
5. Blake, K. D. and Prasad, C. (2006). CHARGE syndrome. Orphanet J. Rare Dis. 1, 34.
6. Cáceres, E. F. and Hurst, L. D. (2013). The evolution, impact and properties of exonic splice enhancers. Genome Biol. 14, R143.
7. Carrington, B., Varshney, G. K., Burgess, S. M. and Sood, R. (2015). CRISPRSTAT: an easy and reliable PCR-based method to evaluate target-specific sgRNA activity. Nucleic Acids Res. 43, e157.
8. Cartegni, L. and Krainer, A. R. (2002). Disruption of an SF2/ASF-dependent exonic splicing enhancer in SMN2 causes spinal muscular atrophy in the absence of SMN1. Nat. Genet. 30, 377-384.
9. Cartegni, L., Chew, S. L. and Krainer, A. R. (2002). Listening to silence and understanding nonsense: exonic mutations that affect splicing. Nat. Rev. Genet. 3, 285-298.
10. Cartegni, L.,Wang, J., Zhu, Z., Zhang, M. Q. and Krainer, A. R. (2003). ESEfinder: a web resource to identify exonic splicing enhancers. Nucleic Acids Res. 31, 3568-3571.
11. Carter, B. S., Cortés-Campos, C., Chen, X., McCammon, J. M. and Sive, H. L. (2016). Validation of protein knockout in mutant zebrafish lines using in vitro translation assays. Zebrafish 10-13.
12. Chen, Y. C., Wu, B. K., Chu, C. Y., Cheng, C. H., Han, H. W., Chen, G.-D., Lee, M. T., Hwang, P. P., Kawakami, K., Chang, C. C. et al. (2010). Identification and characterization of alternative promoters of zebrafish Rtn-4/Nogo genes in cultured cells and zebrafish embryos. Nucleic Acids Res. 38, 4635-4650.
13. Chen, J., Zhang, X., Wang, T., Li, Z., Guan, G. and Hong, Y. (2012). Efficient detection, quantification and enrichment of subtle allelic alterations. DNA Res. 19, 423-433.
14. Cho, S. W., Kim, S., Kim, J. M. and Kim, J.-S. (2013). Targeted genome engineering in human cells with the Cas9 RNA-guided endonuclease. Nat. Biotechnol. 31, 230-232.
15. Cong, L., Ran, F. A., Cox, D., Lin, S., Barretto, R., Hsu, P. D., Wu, X., Jiang, W. and Marraffini, L. A. (2013). Multiplex genome engineering using CRISPR/Cas systems. Science 339, 819-823.
16. Cotter, K. A., Yershov, A., Novillo, A. and Callard, G. V. (2013). Multiple structurally distinct ERa mRNAvariants in zebrafish are differentially expressed by tissue type, stage of development and estrogen exposure. Gen. Comp. Endocrinol. 194, 217-229.
17. D'Agostino, Y., Locascio, A., Ristoratore, F., Sordino, P., Spagnuolo, A., Borra, M. and D'Aniello, S. (2015). A rapid and cheap methodology for CRISPR/Cas9 zebrafish mutant screening. Mol. Biotechnol. 58, 1-6.
18. Dahlem, T. J., Hoshijima, K., Jurynec, M. J., Gunther, D., Starker, C. G., Locke, A. S.,Weis, A. M., Voytas, D. F. and Grunwald, D. J. (2012). Simple methods for generating and detecting locus-specific mutations induced with TALENs in the zebrafish genome. PLoS Genet. 8, e1002861.
19. Daugaard, M., Nitsch, R., Razaghi, B., McDonald, L., Jarrar, A., Torrino, S., Castillo-Lluva, S., Rotblat, B., Li, L., Malliri, A. et al. (2013). Hace1 controls ROS generation of vertebrate Rac1-dependent NADPH oxidase complexes. Nat. Commun. 4, 2180.
20. Desmet, F. O. and Beroud, C. (2012). Bioinformatics and mutations leading to exon skipping. Methods Mol. Biol. 867, 17-35.
21. Fairbrother, W. G., Yeh, R.-F., Sharp, P. A. and Burge, C. B. (2002). Predictive identification of exonic splicing enhancers inhuman genes.Science 297, 1007-1013.
22. Fairbrother, W. G., Yeo, G. W., Yeh, R., Goldstein, P., Mawson, M., Sharp, P. A. and Burge, C. B. (2004). RESCUE-ESE identifies candidate exonic splicing enhancers in vertebrate exons. Nucleic Acids Res. 32, 187-190.
23. Gagnon, J. A., Valen, E., Thyme, S. B., Huang, P., Ahkmetova, L., Pauli, A., Montague, T. G., Zimmerman, S., Richter, C. and Schier, A. F. (2014). Efficient mutagenesis by Cas9 protein-mediated oligonucleotide insertion and large-scale assessment of single-guide RNAs. PLoS ONE 9, e98186.
24. Gao, X., Wan, J., Liu, B., Ma, M., Shen, B. and Qian, S.-B. (2015). Quantitative profiling of initiating ribosomes in vivo. Nat. Methods 12, 147-153.
25. Gasiunas, G., Barrangou, R., Horvath, P. and Siksnys, V. (2012). Cas9-crRNA ribonucleoprotein complex mediates specific DNA cleavage for adaptive immunity in bacteria. Proc. Natl. Acad. Sci. USA 109, E2579-E2586.
26. Gonçalves, V., Theisen, P., Antunes, O., Medeira, A., Ramos, J. S., Jordan, P. and Isidro, G. (2009). A missense mutation in the APC tumor suppressor gene disrupts an ASF/SF2 splicing enhancer motif and causes pathogenic skipping of exon 14. Mutat. Res.-Fundam. Mol. Mech. Mutagen. 662, 33-36.
27. Gonzales, A. P. W. and Yeh, J. J.-R. (2014). Cas9-based genome editing in zebrafish. Methods Enzymol. 546, 377-413.
28. Hahn, M. A., McDonnell, J. and Marsh, D. J. (2009). The effect of diseaseassociated HRPT2 mutations on splicing. J. Endocrinol. 201, 387-396.
29. Hill, J. T., Demarest, B. L., Bisgrove, B. W., Su, Y. C., Smith, M. and Yost, H. J. (2014). Poly peak parser: method and software for identification of unknown indels using sanger sequencing of polymerase chain reaction products. Dev. Dyn. 243, 1632-1636.
30. Hinnebusch, A. G. (2011). Molecular mechanism of scanning and start codon selection in eukaryotes. Microbiol. Mol. Biol. Rev. 75, 434-467.
31. Ingolia, N. T., Lareau, L. F. and Weissman, J. S. (2011). Ribosome profiling of mouse embryonic stem cells reveals the complexity and dynamics of mammalian proteomes. Cell 147, 789-802.
32. Jinek, M., Chylinski, K., Fonfara, I., Hauer, M., Doudna, J. A. and Charpentier, E. (2012). A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337, 816-821.
33. Kim, J. H., Lee, S.-R., Li, L.-H., Park, H.-J., Park, J.-H., Lee, K. Y., Kim, M.-K., Shin, B. A. and Choi, S.-Y. (2011). High cleavage efficiency of a 2A peptide derived from porcine teschovirus-1 in human cell lines, zebrafish and mice. PLoS ONE 6, e18556.
34. Kochetov, A. V. (2008). Alternative translation start sites and hidden coding potential of eukaryotic mRNAs. BioEssays 30, 683-691.
35. Law, S. H.W. and Sargent, T. D. (2014). The serine-threonine protein kinase PAK4 is dispensable in zebrafish: identification of a morpholino-generated pseudophenotype. PLoS ONE 9, e100268.
36. Mali, P., Yang, L., Esvelt, K. M., Aach, J., Guell, M., DiCarlo, J. E., Norville, J. E. and Church, G. M. (2013). RNA-guided human genome engineering via Cas9. Science 339, 823-826.
37. McGookin, R. (1988). Electrophoresis of DNA in nondenaturing polyacrylamide gels. Methods Mol. Biol. 4, 75-79.
38. Moreno-Mateos, M. A., Vejnar, C. E., Beaudoin, J.-D., Fernandez, J. P., Mis, E. K., Khokha, M. K. and Giraldez, A. J. (2015). CRISPRscan: designing highly efficient sgRNAs for CRISPR-Cas9 targeting in vivo. Nat. Methods 12, 982-988.
39. Ota, S., Hisano, Y., Muraki, M., Hoshijima, K., Dahlem, T. J., Grunwald, D. J., Okada, Y. and Kawahara, A. (2013). Efficient identification of TALEN-mediated genome modifications using heteroduplex mobility assays. Genes Cells 18, 450-458.
40. Ota, S., Hisano, Y., Ikawa, Y. and Kawahara, A. (2014). Multiple genome modifications by the CRISPR/Cas9 system in zebrafish. Genes Cells 19, 555-564.
41. Rodgers, K. and McVey, M. (2016). Error-prone repair of DNA double-strand breaks. J. Cell. Physiol. 231, 15-24.
42. Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B. et al. (2012). Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676-682.
43. Smith, P. J., Zhang, C., Wang, J., Chew, S. L., Zhang, M. Q. and Krainer, A. R. (2006). An increased specificity score matrix for the prediction of SF2/ASFspecific exonic splicing enhancers. Hum. Mol. Genet. 15, 2490-2508.
44. Sorek, R., Lawrence, C. M. andWiedenheft, B. (2013). CRISPR-mediated adaptive immune systems in bacteria and archaea. Annu. Rev. Biochem. 82, 237-266.
45. Talbot, J. C. and Amacher, S. L. (2014). A streamlined CRISPR pipeline to reliably generate zebrafish frameshifting alleles. Zebrafish 11, 583-585.
46. Thomas, H. R., Percival, S. M., Yoder, B. K. and Parant, J. M. (2014). Highthroughput genome editing and phenotyping facilitated by high resolution melting curve analysis. PLoS ONE 9, e114632.
47. Uddin, B., Chen, N.-P., Panic, M. and Schiebel, E. (2015). Genome editing through large insertion leads to the skipping of targeted exon. BMC Genomics 16, 1082.
48. Varshney, G. K., Pei, W., LaFave, M. C., Idol, J., Xu, L., Gallardo, V., Carrington, B., Bishop, K., Jones, M., Li, M. et al. (2015a). High-throughput gene targeting and phenotyping in zebrafish using CRISPR/Cas9. Genome Res. 25, 1030-1042.
49. Varshney, G. K., Sood, R. and Burgess, S. M. (2015b). Understanding and editing the zebrafish genome. Methods Mol. Biol. 92, 1-52.
50. Vissers, L. E. L. M., van Ravenswaaij, C. M. A., Admiraal, R., Hurst, J. A., de Vries, B. B. A., Janssen, I. M., van der Vliet, W. A., Huys, E. H. L. P. G., de Jong, P. J., Hamel, B. C. J. et al. (2004). Mutations in a new member of the chromodomain gene family cause CHARGE syndrome. Nat. Genet. 36, 955-957.
51. Westerfield, M. (2007) The Zebrafish Book. A Guide for the Laboratory Use of Zebrafish (Danio rerio), 5th Edn. University of Oregon Press: Eugene Close.
52. White, R. M., Sessa, A., Burke, C., Bowman, T., LeBlanc, J., Ceol, C., Bourque, C., Dovey, M., Goessling, W., Burns, E. et al. (2008). Transparent adult zebrafish as a tool for in vivo transplantation analysis. Cell Stem Cell 2, 183-189.
53. Xiao, A., Wang, Z., Hu, Y., Wu, Y., Luo, Z., Yang, Z., Zu, Y., Li, W., Huang, P., Tong, X. et al. (2013). Chromosomal deletions and inversions mediated by TALENs and CRISPR/Cas in zebrafish. Nucleic Acids Res. 41, 1-11.
54. Yeo, G., Hoon, S., Venkatesh, B. and Burge, C. B. (2004). Variation in sequence and organization of splicing regulatory elements in vertebrate genes. Proc. Natl. Acad. Sci. USA 101, 15700-15705.
55. Zatkova, A., Messiaen, L., Vandenbroucke, I., Wieser, R., Fonatsch, C., Krainer, A. R. and Wimmer, K. (2004). Disruption of exonic splicing enhancer elements is the principal cause of exon skipping associated with seven nonsense or missense alleles of NF1. Hum. Mutat. 24, 491-501.