CRISPR-mediated genetic interaction profiling identifies RNA binding proteins controlling metazoan fitness

eLife

Volumn 6, Issue , 2017, Pages

  Norris, Adam D ^a,b   Gracida, Xicotencatl ^a   Calarco, John A ^a,c  

^a HARVARD UNIVERSITY   (United States)

^b SOUTHERN METHODIST UNIVERSITY   (United States)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN EAT 2; PROTEIN EXC 7; PROTEIN MBL 1; RNA BINDING PROTEIN; TRANSCRIPTOME; UNCLASSIFIED DRUG; CAENORHABDITIS ELEGANS PROTEIN; EXC-7 PROTEIN, C ELEGANS; MBL-1 PROTEIN, C ELEGANS;

ARTICLE; CAENORHABDITIS ELEGANS; COMPETITIVE BINDING ASSAY; CONTROLLED STUDY; CRISPR CAS SYSTEM; EMBRYO; FLUORESCENCE MICROSCOPY; GENE DISRUPTION; GENE EXPRESSION; GENE INTERACTION; GENE REGULATORY NETWORK; GENETIC ANALYSIS; HOMOLOGOUS RECOMBINATION; LIFESPAN; MUTANT; NONHUMAN; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ANIMAL; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; EPISTASIS; GENETICS; GROWTH, DEVELOPMENT AND AGING; HIGH THROUGHPUT SCREENING; MUTATION; PHENOTYPE; PROCEDURES; RNA INTERFERENCE;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEATS; EPISTASIS, GENETIC; HIGH-THROUGHPUT SCREENING ASSAYS; MUTATION; PHENOTYPE; RNA INTERFERENCE; RNA-BINDING PROTEINS;

EID: 85026896815     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.28129     Document Type: Article

References (54)

1. Anders S, Huber W. 2010. Differential expression analysis for sequence count data. Genome Biology 11:R106. doi: 10.1186/gb-2010-11-10-r106, PMID: 20979621
2. Anyanful A, Ono K, Johnsen RC, Ly H, Jensen V, Baillie DL, Ono S. 2004. The RNA-binding protein SUP-12 controls muscle-specific splicing of the ADF/cofilin pre-mRNA in C. elegans. The Journal of Cell Biology 167: 639-647. doi: 10.1083/jcb.200407085, PMID: 15545320
3. Asikainen S, Vartiainen S, Lakso M, Nass R, Wong G. 2005. Selective sensitivity of Caenorhabditis elegans neurons to RNA interference. NeuroReport 16:1995-1999. doi: 10.1097/00001756-200512190-00005, PMID: 16317341
4. Barberan-Soler S, Medina P, Estella J, Williams J, Zahler AM. 2011. Co-regulation of alternative splicing by diverse splicing factors in Caenorhabditis elegans. Nucleic Acids Research 39:666-674. doi: 10.1093/nar/gkq767, PMID: 20805248
5. Baryshnikova A, Costanzo M, Kim Y, Ding H, Koh J, Toufighi K, Youn JY, Ou J, San Luis BJ, Bandyopadhyay S, Hibbs M, Hess D, Gingras AC, Bader GD, Troyanskaya OG, Brown GW, Andrews B, Boone C, Myers CL. 2010. Quantitative analysis of fitness and genetic interactions in yeast on a genome scale. Nature Methods 7:1017-1024. doi: 10.1038/nmeth.1534, PMID: 21076421
6. Baugh LR, Wen JC, Hill AA, Slonim DK, Brown EL, Hunter CP. 2005. Synthetic lethal analysis of Caenorhabditis elegans posterior embryonic patterning genes identifies conserved genetic interactions. Genome Biology 6: R45. doi: 10.1186/gb-2005-6-5-r45, PMID: 15892873
7. Brenner S. 1974. The genetics of Caenorhabditis elegans. Genetics 77:71-94. PMID: 4366476
8. Brooks AN, Duff MO, May G, Yang L, Bolisetty M, Landolin J, Wan K, Sandler J, Booth BW, Celniker SE, Graveley BR, Brenner SE. 2015. Regulation of alternative splicing in Drosophila by 56 RNA binding proteins. Genome Research 25:1771-1780. doi: 10.1101/gr.192518.115, PMID: 26294686
9. Butland G, Babu M, Díaz-Mejía JJ, Bohdana F, Phanse S, Gold B, Yang W, Li J, Gagarinova AG, Pogoutse O, Mori H, Wanner BL, Lo H, Wasniewski J, Christopolous C, Ali M, Venn P, Safavi-Naini A, Sourour N, Caron S, et al. 2008. eSGA: E. coli synthetic genetic array analysis. Nature Methods 5:789-795. doi: 10.1038/nmeth.1239, PMID: 18677321
10. Byrne AB, Weirauch MT, Wong V, Koeva M, Dixon SJ, Stuart JM, Roy PJ. 2007. A global analysis of genetic interactions in Caenorhabditis elegans. Journal of Biology 6:8. doi: 10.1186/jbiol58, PMID: 17897480
11. Calixto A, Chelur D, Topalidou I, Chen X, Chalfie M. 2010. Enhanced neuronal RNAi in C. elegans using SID-1. Nature Methods 7:554-559. doi: 10.1038/nmeth.1463, PMID: 20512143
12. Carbon S, Ireland A, Mungall CJ, Shu S, Marshall B, Lewis S, Ami GOH, Ami GO HubWeb Presence Working Group. 2009. AmiGO: online access to ontology and annotation data. Bioinformatics 25:288-289. doi: 10.1093/bioinformatics/btn615, PMID: 19033274
13. Castello A, Fischer B, Hentze MW, Preiss T. 2013. RNA-binding proteins in mendelian disease. Trends in Genetics 29:318-327. doi: 10.1016/j.tig.2013.01.004, PMID: 23415593
14. Chalfie M, Sulston J. 1981. Developmental genetics of the mechanosensory neurons of Caenorhabditis elegans. Developmental Biology 82:358-370. doi: 10.1016/0012-1606(81)90459-0, PMID: 7227647
15. Chen M, Manley JL. 2009. Mechanisms of alternative splicing regulation: insights from molecular and genomics approaches. Nature Reviews Molecular Cell Biology 10:741-754. doi: 10.1038/nrm2777, PMID: 19773805
16. Collins SR, Schuldiner M, Krogan NJ, Weissman JS. 2006. A strategy for extracting and analyzing large-scale quantitative epistatic interaction data. Genome Biology 7:R63. doi: 10.1186/gb-2006-7-7-r63, PMID: 16859555
17. Costanzo M, Baryshnikova A, Bellay J, Kim Y, Spear ED, Sevier CS, Ding H, Koh JL, Toufighi K, Mostafavi S, Prinz J, St Onge RP, VanderSluis B, Makhnevych T, Vizeacoumar FJ, Alizadeh S, Bahr S, Brost RL, Chen Y, Cokol M, et al. 2010. The genetic landscape of a cell. Science 327:425-431. doi: 10.1126/science.1180823, PMID: 20093466
18. Dickinson DJ, Goldstein B. 2016. CRISPR-Based methods for Caenorhabditis elegans Genome Engineering. Genetics 202:885-901. doi: 10.1534/genetics.115.182162, PMID: 26953268
19. Dixon SJ, Costanzo M, Baryshnikova A, Andrews B, Boone C. 2009. Systematic mapping of genetic interaction networks. Annual Review of Genetics 43:601-625. doi: 10.1146/annurev.genet.39.073003.114751, PMID: 19712041
20. Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, Batut P, Chaisson M, Gingeras TR. 2013. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29:15-21. doi: 10.1093/bioinformatics/bts635, PMID: 23104
21. Elkon R, Ugalde AP, Agami R. 2013. Alternative cleavage and polyadenylation: extent, regulation and function. Nature Reviews Genetics 14:496-506. doi: 10.1038/nrg3482, PMID: 23774734
22. Firnhaber C, Hammarlund M. 2013. Neuron-specific feeding RNAi in C. elegans and its use in a screen for essential genes required for GABA neuron function. PLoS Genetics 9:e1003921. doi: 10.1371/journal.pgen.1003921, PMID: 24244189
23. Fujita M, Hawkinson D, King KV, Hall DH, Sakamoto H, Buechner M. 2003. The role of the ELAV homologue EXC-7 in the development of the Caenorhabditis elegans excretory canals. Developmental Biology 256:290-301. doi: 10.1016/S0012-1606(03)00040-X, PMID: 12679103
24. Gehman LT, Meera P, Stoilov P, Shiue L, O’Brien JE, Meisler MH, Ares M, Otis TS, Black DL. 2012. The splicing regulator Rbfox2 is required for both cerebellar development and mature motor function. Genes & Development 26:445-460. doi: 10.1101/gad.182477.111, PMID: 22357600
25. Gerstberger S, Hafner M, Ascano M, Tuschl T. 2014a. Evolutionary conservation and expression of human RNA- binding proteins and their role in human genetic disease. Advances in Experimental Medicine and Biology 825: 1-55. doi: 10.1007/978-1-4939-1221-6_1, PMID: 25201102
26. Gerstberger S, Hafner M, Tuschl T. 2014b. A census of human RNA-binding proteins. Nature Reviews Genetics 15:829-845. doi: 10.1038/nrg3813, PMID: 25365966
27. Heintz C, Doktor TK, Lanjuin A, Escoubas C, Zhang Y, Weir HJ, Dutta S, Silva-García CG, Bruun GH, Morantte I, Hoxhaj G, Manning BD, Andresen BS, Mair WB. 2017. Splicing factor 1 modulates dietary restriction and TORC1 pathway longevity in C. elegans. Nature 541:102-106. doi: 10.1038/nature20789, PMID: 27919065
28. Hulsen T, de Vlieg J, Alkema W. 2008. BioVenn - a web application for the comparison and visualization of biological lists using area-proportional Venn diagrams. BMC Genomics 9:488. doi: 10.1186/1471-2164-9-488, PMID: 18925949
29. Kamath RS, Ahringer J. 2003. Genome-wide RNAi screening in Caenorhabditis elegans. Methods 30:313-321. doi: 10.1016/S1046-2023(03)00050-1, PMID: 12828945
30. Kimura KD, Tissenbaum HA, Liu Y, Ruvkun G. 1997. daf-2, an insulin receptor-like gene that regulates longevity and diapause in Caenorhabditis elegans. Science 277:942-946. doi: 10.1126/science.277.5328.942, PMID: 9252323
31. Lakowski B, Hekimi S. 1998. The genetics of caloric restriction in Caenorhabditis elegans. PNAS 95:13091-13096. doi: 10.1073/pnas.95.22.13091, PMID: 9789046
32. Lehner B, Crombie C, Tischler J, Fortunato A, Fraser AG. 2006. Systematic mapping of genetic interactions in Caenorhabditis elegans identifies common modifiers of diverse signaling pathways. Nature Genetics 38:896-903. doi: 10.1038/ng1844, PMID: 16845399
33. Lin K, Dorman JB, Rodan A, Kenyon C. 1997. daf-16: an HNF-3/forkhead family member that can function to double the life-span of Caenorhabditis elegans. Science 278:1319-1322. doi: 10.1126/science.278.5341.1319, PMID: 9360933
34. Lukong KE, Chang KW, Khandjian EW, Richard S. 2008. RNA-binding proteins in human genetic disease. Trends in Genetics 24:416-425. doi: 10.1016/j.tig.2008.05.004, PMID: 18597886
35. Lundquist EA, Herman RK. 1994. The mec-8 gene of Caenorhabditis elegans affects muscle and sensory neuron function and interacts with three other genes: unc-52, smu-1 and smu-2. Genetics 138:83-101. PMID: 8001796
36. Mani R, St Onge RP, Hartman JL, Giaever G, Roth FP. 2008. Defining genetic interaction. PNAS 105:3461-3466. doi: 10.1073/pnas.0712255105, PMID: 18305163
37. Muñoz MJ, Riddle DL. 2003. Positive selection of Caenorhabditis elegans mutants with increased stress resistance and longevity. Genetics 163:171-180. PMID: 12586705
38. Norris AD, Gao S, Norris ML, Ray D, Ramani AK, Fraser AG, Morris Q, Hughes TR, Zhen M, Calarco JA. 2014. A pair of RNA-binding proteins controls networks of splicing events contributing to specialization of neural cell types. Molecular Cell 54:946-959. doi: 10.1016/j.molcel.2014.05.004, PMID: 24910101
39. Norris AD, Kim HM, Colaiácovo MP, Calarco JA. 2015. Efficient Genome Editing in Caenorhabditis elegans with a toolkit of Dual-Marker selection cassettes. Genetics 201:449-458. doi: 10.1534/genetics.115.180679, PMID: 26232410
40. Nussbacher JK, Batra R, Lagier-Tourenne C, Yeo GW. 2015. RNA-binding proteins in neurodegeneration: seq and you shall receive. Trends in Neurosciences 38:226-236. doi: 10.1016/j.tins.2015.02.003, PMID: 25765321
41. Ogg S, Paradis S, Gottlieb S, Patterson GI, Lee L, Tissenbaum HA, Ruvkun G. 1997. The Fork head transcription factor DAF-16 transduces insulin-like metabolic and longevity signals in C. elegans. Nature 389:994-999. doi: 10.1038/40194, PMID: 9353126
42. Ramani AK, Calarco JA, Pan Q, Mavandadi S, Wang Y, Nelson AC, Lee LJ, Morris Q, Blencowe BJ, Zhen M, Fraser AG. 2011. Genome-wide analysis of alternative splicing in Caenorhabditis elegans. Genome Research 21:342-348. doi: 10.1101/gr.114645.110, PMID: 21177968
43. Ray D, Kazan H, Cook KB, Weirauch MT, Najafabadi HS, Li X, Gueroussov S, Albu M, Zheng H, Yang A, Na H, Irimia M, Matzat LH, Dale RK, Smith SA, Yarosh CA, Kelly SM, Nabet B, Mecenas D, Li W, et al. 2013. A compendium of RNA-binding motifs for decoding gene regulation. Nature 499:172-177. doi: 10.1038/nature12311, PMID: 23846655
44. Schoenberg DR, Maquat LE. 2012. Regulation of cytoplasmic mRNA decay. Nature Reviews Genetics 13:448-259. doi: 10.1038/nrg3254, PMID: 22392217
45. Schuldiner M, Collins SR, Thompson NJ, Denic V, Bhamidipati A, Punna T, Ihmels J, Andrews B, Boone C, Greenblatt JF, Weissman JS, Krogan NJ. 2005. Exploration of the function and organization of the yeast early secretory pathway through an epistatic miniarray profile. Cell 123:507-519. doi: 10.1016/j.cell.2005.08.031, PMID: 16269340
46. Sieburth D, Ch’ng Q, Dybbs M, Tavazoie M, Kennedy S, Wang D, Dupuy D, Rual JF, Hill DE, Vidal M, Ruvkun G, Kaplan JM. 2005. Systematic analysis of genes required for synapse structure and function. Nature 436:510-517. doi: 10.1038/nature03809, PMID: 16049479
47. Simone LE, Keene JD. 2013. Mechanisms coordinating ELAV/Hu mRNA regulons. Current Opinion in Genetics & Development 23:35-43. doi: 10.1016/j.gde.2012.12.006, PMID: 23312841
48. Spilker KA, Wang GJ, Tugizova MS, Shen K. 2012. Caenorhabditis elegans muscleblind homolog mbl-1 functions in neurons to regulate synapse formation. Neural Development 7:7, 7. doi: 10.1186/1749-8104-7-7, PMID: 22314215
49. Sreedharan J, Blair IP, Tripathi VB, Hu X, Vance C, Rogelj B, Ackerley S, Durnall JC, Williams KL, Buratti E, Baralle F, de Belleroche J, Mitchell JD, Leigh PN, Al-Chalabi A, Miller CC, Nicholson G, Shaw CE. 2008. TDP-43 mutations in familial and sporadic amyotrophic lateral sclerosis. Science 319:1668-1672. doi: 10.1126/science.1154584, PMID: 18309045
50. Ule J, Stefani G, Mele A, Ruggiu M, Wang X, Taneri B, Gaasterland T, Blencowe BJ, Darnell RB. 2006. An RNA map predicting Nova-dependent splicing regulation. Nature 444:580-586. doi: 10.1038/nature05304, PMID: 17065982
51. Van Nostrand EL, Sá nchez-Blanco A, Wu B, Nguyen A, Kim SK. 2013. Roles of the developmental regulator unc- 62/Homothorax in limiting longevity in Caenorhabditis elegans. PLoS Genetics 9:e1003325. doi: 10.1371/journal.pgen.1003325, PMID: 23468654
52. Vance C, Rogelj B, Hortobá gyi T, De Vos KJ, Nishimura AL, Sreedharan J, Hu X, Smith B, Ruddy D, Wright P, Ganesalingam J, Williams KL, Tripathi V, Al-Saraj S, Al-Chalabi A, Leigh PN, Blair IP, Nicholson G, de Belleroche J, Gallo JM, et al. 2009. Mutations in FUS, an RNA processing protein, cause familial amyotrophic lateral sclerosis type 6. Science 323:1208-1211. doi: 10.1126/science.1165942, PMID: 19251628
53. Wang ET, Cody NA, Jog S, Biancolella M, Wang TT, Treacy DJ, Luo S, Schroth GP, Housman DE, Reddy S, Lécuyer E, Burge CB. 2012. Transcriptome-wide regulation of pre-mRNA splicing and mRNA localization by muscleblind proteins. Cell 150:710-724. doi: 10.1016/j.cell.2012.06.041, PMID: 22901804
54. Wang ET, Ward AJ, Cherone JM, Giudice J, Wang TT, Treacy DJ, Lambert NJ, Freese P, Saxena T, Cooper TA, Burge CB. 2015. Antagonistic regulation of mRNA expression and splicing by CELF and MBNL proteins. Genome Research 25:858-871. doi: 10.1101/gr.184390.114, PMID: 25883322