Implementation of the CRISPR-Cas13a system in fission yeast and its repurposing for precise RNA editing

Nucleic Acids Research

Volumn 46, Issue 15, 2018, Pages E90-

  Jing, Xinyun ^a   Xie, Bingran ^a   Chen, Longxian ^a   Zhang, Niubing ^a,b   Jiang, Yiyi ^c   Qin, Hang ^a   Wang, Hongbing ^d   Hao, Pei ^c   Yang, Sheng ^a   Li, Xuan ^a  

^a INSTITUTE OF PLANT PHYSIOLOGY AND ECOLOGY   (China)

^b HENAN UNIVERSITY   (China)

^c INSTITUTE PASTEUR OF SHANGHAI   (China)

^d MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DEAMINASE; BACTERIAL PROTEIN; FUNGAL RNA; RIBONUCLEASE;

ARTICLE; CONTROLLED STUDY; CRISPR CAS SYSTEM; CRISPR CAS13A SYSTEM; ENZYME ACTIVE SITE; FLOW CYTOMETRY; FUNGAL CELL; FUNGAL STRAIN; GENETIC TRANSCRIPTION; NONHUMAN; PLASMID; RESIDUE ANALYSIS; RETROPOSON; RNA EDITING; SANGER SEQUENCING; SCHIZOSACCHAROMYCES POMBE; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; LEPTOTRICHIA; METABOLISM; REPRODUCIBILITY; SCHIZOSACCHAROMYCES;

BACTERIAL PROTEINS; CRISPR-CAS SYSTEMS; GENE EXPRESSION REGULATION, FUNGAL; LEPTOTRICHIA; MUTAGENESIS, INSERTIONAL; REPRODUCIBILITY OF RESULTS; RETROELEMENTS; RIBONUCLEASES; RNA EDITING; RNA, FUNGAL; SCHIZOSACCHAROMYCES;

EID: 85052877430     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gky433     Document Type: Article

References (52)

1. Shalem,O., Sanjana,N.E. and Zhang,F. (2015) High-throughput functional genomics using CRISPR–Cas9. Nat. Rev. Genet., 16, 299–311.
2. Wright,A.V., Nunez,J.K. and Doudna,J.A. (2016) Biology and applications of CRISPR systems: harnessing nature’s toolbox for genome engineering. Cell, 164, 29–44.
3. Dominguez,A.A., Lim,W.A. and Qi,L.S. (2016) Beyond editing: repurposing CRISPR-Cas9 for precision genome regulation and interrogation. Nat. Rev. Mol. Cell Biol., 17, 5–15.
4. Shmakov,S., Abudayyeh,O.O., Makarova,K.S., Wolf,Y.I., Gootenberg,J.S., Semenova,E., Minakhin,L., Joung,J., Konermann,S. and Severinov,K. (2015) Discovery and functional characterization of diverse Class 2 CRISPR-Cas systems. Mol. Cell, 60, 385–397.
5. Makarova,K.S., Wolf,Y.I., Alkhnbashi,O.S., Costa,F., Shah,S.A., Saunders,S.J., Barrangou,R., Brouns,S.J., Charpentier,E. and Haft,D.H. (2015) An updated evolutionary classification of CRISPR-Cas systems. Nat. Rev. Microbiol., 13, 722–736.
6. Lewis,K.M. and Ke,A. (2017) Building the Class 2 CRISPR-Cas arsenal. Mol. Cell, 65, 377–379.
7. Abudayyeh,O.O., Gootenberg,J.S., Konermann,S., Joung,J., Slaymaker,I.M., Cox,D.B., Shmakov,S., Makarova,K.S., Semenova,E., Minakhin,L. et al. (2016) C2c2 is a single-component programmable RNA-guided RNA-targeting CRISPR effector. Science, 353, aaf5573.
8. East-Seletsky,A., O’Connell,M.R., Knight,S.C., Burstein,D., Cate,J.H., Tjian,R. and Doudna,J.A. (2016) Two distinct RNase activities of CRISPR-C2c2 enable guide-RNA processing and RNA detection. Nature, 538, 270–273.
9. Knott,G.J., East-Seletsky,A., Cofsky,J.C., Holton,J.M., Charles,E., O’Connell,M.R. and Doudna,J.A. (2017) Guide-bound structures of an RNA-targeting A-cleaving CRISPR-Cas13a enzyme. Nat. Struct. Mol. Biol., 24, 825–833.
10. Smargon,A.A., Cox,D.B., Pyzocha,N.K., Zheng,K., Slaymaker,I.M., Gootenberg,J.S., Abudayyeh,O.A., Essletzbichler,P., Shmakov,S., Makarova,K.S. et al. (2017) Cas13b is a type VI-B CRISPR-Associated RNA-Guided RNase differentially regulated by accessory proteins Csx27 and Csx28. Mol. Cell, 65, 618–630.
11. Gootenberg,J.S., Abudayyeh,O.O., Lee,J.W., Essletzbichler,P., Dy,A.J., Joung,J., Verdine,V., Donghia,N., Daringer,N.M. and Freije,C.A. (2017) Nucleic acid detection with CRISPR-Cas13a/C2c2. Science, 356, 438–442.
12. Abudayyeh,O.O., Gootenberg,J.S., Essletzbichler,P., Han,S., Joung,J., Belanto,J.J., Verdine,V., Cox,D.B.T., Kellner,M.J., Regev,A. et al. (2017) RNA targeting with CRISPR-Cas13. Nature, 550, 280–284.
13. Nurse,P. and Bissett,Y. (1981) Gene required in G1 for commitment to cell cycle and in G2 for control of mitosis in fission yeast. Nature, 292, 558–560.
14. Petersen,J. and Nurse,P. (2007) TOR signalling regulates mitotic commitment through the stress MAP kinase pathway and the Polo and Cdc2 kinases. Nat. Cell Biol., 9, 1263–1272.
15. Goshima,G., Saitoh,S. and Yanagida,M. (1999) Proper metaphase spindle length is determined by centromere proteins Mis12 and Mis6 required for faithful chromosome segregation. Genes Dev., 13, 1664–1677.
16. Kitajima,T.S., Kawashima,S.A. and Watanabe,Y. (2004) The conserved kinetochore protein shugoshin protects centromeric cohesion during meiosis. Nature, 427, 510–517.
17. Jenuwein,T. and Allis,C.D. (2001) Translating the histone code. Science, 293, 1074–1080.
18. Allshire,R.C. and Ekwall,K. (2015) Epigenetic regulation of chromatin states in schizosaccharomyces pombe. Cold Spring Harb. Perspect. Biol., 7, a018770.
19. Mulholland,J., Preuss,D., Moon,A., Wong,A., Drubin,D. and Botstein,D. (1994) Ultrastructure of the yeast actin cytoskeleton and its association with the plasma membrane. J. Cell Biol., 125, 381–391.
20. Chang,F., Drubin,D. and Nurse,P. (1997) cdc12p, a protein required for cytokinesis in fission yeast, is a component of the cell division ring and interacts with profilin. J. Cell Biol., 137, 169–182.
21. Bass,B.L. (2002) RNA editing by adenosine deaminases that act on RNA. Annu. Rev. Biochem., 71, 817–846.
22. Qi,L.S., Larson,M.H., Gilbert,L.A., Doudna,J.A., Weissman,J.S., Arkin,A.P. and Lim,W.A. (2013) Repurposing CRISPR as an RNA-Guided platform for sequence-specific control of gene expression. Cell, 152, 1173–1183.
23. Gilbert,L.A., Larson,M.H., Morsut,L., Liu,Z., Brar,G.A., Torres,S.E., Sternginossar,N., Brandman,O., Whitehead,E.H. and Doudna,J.A. (2013) CRISPR-mediated modular RNA-Guided regulation of transcription in eukaryotes. Cell, 154, 442–451.
24. Sabatinos,S.A. and Forsburg,S.L. (2010) Molecular genetics of Schizosaccharomyces pombe. Methods Enzymol., 470, 759–795.
25. Rinkevich,F.D., Schweitzer,P.A. and Scott,J.G. (2012) Antisense sequencing improves the accuracy and precision of A-to-I editing measurements using the peak height ratio method. BMC Res. Notes, 5, 1–6.
26. Levin,H.L., Weaver,D.C. and Boeke,J.D. (1993) Novel gene expression mechanism in a fission yeast retroelement: Tf1 proteins are derived from a single primary translation product. EMBO J., 12, 4885–4895.
27. Jacobs,J.Z., Rosado-Lugo,J.D., Cranz-Mileva,S., Ciccaglione,K.M., Tournier,V. and Zaratiegui,M. (2015) Arrested replication forks guide retrotransposon integration. Science, 349, 1549–1553.
28. Jacobs,J.Z., Ciccaglione,K.M., Tournier,V. and Zaratiegui,M. (2014) Implementation of the CRISPR-Cas9 system in fission yeast. Nat. Commun., 5, 5344–5348.
29. Matsuyama,A., Shirai,A., Yashiroda,Y., Kamata,A., Horinouchi,S. and Yoshida,M. (2004) pDUAL, a multipurpose, multicopy vector capable of chromosomal integration in fission yeast. Yeast, 21, 1289–1305.
30. Verma,H.K., Shukla,P., Alfatah,M., Khare,A.K., Upadhyay,U., Ganesan,K. and Singh,J. (2014) High level constitutive expression of luciferase reporter by lsd90 promoter in fission yeast. PLoS One, 9, e101201.
31. Ruijter,J.C., Koskela,E.V., Nandania,J., Frey,A.D. and Velagapudi,V. (2017) Understanding the metabolic burden of recombinant antibody production in Saccharomyces cerevisiae using a quantitative metabolomics approach. Yeast, 35, 331–341.
32. Hayles,J., Wood,V., Jeffery,L., Hoe,K.L., Kim,D.U., Park,H.O., Salas-Pino,S., Heichinger,C. and Nurse,P. (2013) A genome-wide resource of cell cycle and cell shape genes of fission yeast. Open Biol., 3, 130053.
33. Zhou,X., Ma,Y., Fang,Y., gerile,W., Jaiseng,W., Yamada,Y. and Kuno,T. (2013) A genome-wide screening of potential target genes to enhance the antifungal activity of micafungin in Schizosaccharomyces pombe. PLoS One, 8, e65904.
34. Rueter,S.M., Burns,C.M., Coode,S.A., Mookherjee,P. and Emeson,R.B. (1995) Glutamate receptor RNA editing in vitro by enzymatic conversion of adenosine to inosine. Science, 267, 1491–1494.
35. Melcher,T., Maas,S., Herb,A., Sprengel,R., Seeburg,P.H. and Higuchi,M. (1996) A mammalian RNA editing enzyme. Nature, 379, 460–464.
36. Komor,A.C., Kim,Y.B., Packer,M.S., Zuris,J.A. and Liu,D.R. (2016) Programmable editing of a target base in genomic DNA without double-stranded DNA cleavage. Nature, 533, 420–424.
37. Phelps,K.J., Tran,K., Eifler,T., Erickson,A.I., Fisher,A.J. and Beal,P.A. (2015) Recognition of duplex RNA by the deaminase domain of the RNA editing enzyme ADAR2. Nucleic Acids Res., 43, 1123–1132.
38. Cox,D.B.T., Gootenberg,J.S., Abudayyeh,O.O., Franklin,B., Kellner,M.J., Joung,J. and Zhang,F. (2017) RNA editing with CRISPR-Cas13. Science, 358, 1019–1027.
39. Montielgonzález,M.F., Vallecilloviejo,I.C. and Rosenthal,J.J. (2016) An efficient system for selectively altering genetic information within mRNAs. Nucleic Acids Res., 44, e157.
40. Marguerat,S., Schmidt,A., Codlin,S., Chen,W., Aebersold,R. and Bähler,J. (2012) Quantitative analysis of fission yeast transcriptomes and proteomes in proliferating and quiescent cells. Cell, 151, 671–683.
41. Mcdowall,M.D., Harris,M.A., Lock,A., Rutherford,K., Staines,D.M., Bähler,J., Kersey,P.J., Oliver,S.G. and Wood,V. (2015) PomBase 2015: updates to the fission yeast database. Nucleic Acids Res., 43, D656–D661.
42. Liu,L., Li,X., Ma,J., Li,Z., You,L., Wang,J., Wang,M., Zhang,X. and Wang,Y. (2017) The molecular architecture for RNA-Guided RNA cleavage by Cas13a. Cell, 170, 714–726.
43. Wettengel,J., Reautschnig,P., Geisler,S., Kahle,P.J. and Stafforst,T. (2017) Harnessing human ADAR2 for RNA repair––recoding a PINK1 mutation rescues mitophagy. Nucleic Acids Res., 45, 2797–2808.
44. Montiel-Gonzalez,M.F., Vallecillo-Viejo,I., Yudowski,G.A. and Rosenthal,J.J.C. (2013) Correction of mutations within the cystic fibrosis transmembrane conductance regulator by site-directed RNA editing. Proc. Natl. Acad. Sci. U.S.A., 110, 18285–18290.
45. Austin,R.J., Xia,T., Ren,J., Takahashi,T.T. and Roberts,R.W. (2002) Designed arginine-rich RNA-binding peptides with picomolar affinity. J. Am. Chem. Soc., 124, 10966–10967.
46. Vogel,P., Schneider,M.F., Wettengel,J. and Stafforst,T. (2014) Improving site-directed RNA editing in vitro and in cell culture by chemical modification of the guideRNA. Angew. Chem., 53, 6267–6271.
47. Stafforst,T. and Schneider,M.F. (2012) An RNA–deaminase conjugate selectively repairs point mutations. Angew. Chem., 51, 11166–11169.
48. Vogel,P., Hanswillemenke,A. and Stafforst,T. (2017) Switching protein localization by site-directed RNA editing under control of light. ACS Synth. Biol., 6, 1642–1649.
49. Yu,Y., Zhou,H., Kong,Y., Pan,B., Chen,L., Wang,H., Hao,P. and Li,X. (2016) The landscape of A-to-I RNA editome is shaped by both positive and purifying selection. PLoS Genet., 12, e1006191.
50. Tan,M.H., Li,Q., Shanmugam,R., Piskol,R., Kohler,J., Young,A.N., Liu,K.I., Zhang,R., Ramaswami,G., Ariyoshi,K. et al. (2017) Dynamic landscape and regulation of RNA editing in mammals. Nature, 550, 249–254.
51. Eifler,T., Pokharel,S. and Beal,P.A. (2013) RNA-Seq analysis identifies a novel set of editing substrates for human ADAR2 present in Saccharomyces cerevisiae. Biochemistry, 52, 7857–7869.
52. Gao,Y. and Zhao,Y. (2014) Self-processing of ribozyme-flanked RNAs into guide RNAs in vitro and in vivo for CRISPR-mediated genome editing. J. Integr. Plant Biol., 56, 343–349.