Probing RNA recognition by human ADAR2 using a high-throughput mutagenesis method

Nucleic Acids Research

Volumn 44, Issue 20, 2016, Pages 9872-9880

  Wang, Yuru ^a   Beal, Peter A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DEAMINASE; PROTEIN ADAR2; UNCLASSIFIED DRUG; ADARB1 PROTEIN, HUMAN; PROTEIN BINDING; RNA; RNA BINDING PROTEIN;

5' UNTRANSLATED REGION; ARTICLE; BINDING AFFINITY; CATALYSIS; CONTROLLED STUDY; ENZYME ACTIVITY; GENETIC PROCEDURES; GENETIC SCREENING; GENETIC VARIABILITY; HIGH THROUGHPUT MUTAGENESIS METHOD; MOLECULAR PROBE; MOLECULAR RECOGNITION; NONHUMAN; PROCESS DEVELOPMENT; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; RNA BINDING; RNA EDITING; RNA RECOGNITION; RNA SEQUENCE; STRUCTURE ACTIVITY RELATION; YEAST CELL; AMINO ACID SEQUENCE; BINDING SITE; CHEMISTRY; CONFORMATION; FLOW CYTOMETRY; GENE EXPRESSION; GENETICS; HUMAN; METABOLISM; MOLECULAR MODEL; MUTAGENESIS; NUCLEOTIDE SEQUENCE; POSITION WEIGHT MATRIX; REPORTER GENE; SINGLE CELL ANALYSIS; YEAST;

ADENOSINE DEAMINASE; AMINO ACID SEQUENCE; BASE SEQUENCE; BINDING SITES; FLOW CYTOMETRY; GENE EXPRESSION; GENES, REPORTER; HUMANS; MODELS, MOLECULAR; MOLECULAR CONFORMATION; MUTAGENESIS; NUCLEIC ACID CONFORMATION; POSITION-SPECIFIC SCORING MATRICES; PROTEIN BINDING; RNA; RNA EDITING; RNA-BINDING PROTEINS; SINGLE-CELL ANALYSIS; STRUCTURE-ACTIVITY RELATIONSHIP; YEASTS;

EID: 85015617514     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkw799     Document Type: Article

References (45)

1. Carlile,T.M., Rojas-Duran,M.F., Zinshteyn,B., Shin,H., Bartoli,K.M. and Gilbert,W.V. (2014) Pseudouridine profiling reveals regulated mRNA pseudouridylation in yeast and human cells. Nature, 515, 143-146.
2. 1-methyladenosine methylome. Nat. Chem. Biol., 12, 311-316.
3. Gilbert,W.V., Bell,T.A. and Schaening,C. (2016) Messenger RNA modifications: form, distribution, and function. Science, 352, 1048-1412.
4. Chen,K., Zhao,B.S. and He,C. (2016) Nucleic acid modifications in regulation of gene expression. Cell Chem. Biol., 23, 74-85.
5. O'Connell,M.A., Mannion,N.M. and Keegan,L.P. (2015) The epitranscriptome and innate immunity. PLoS Genet., 11, e1005687.
6. Keegan,L.P., Gallo,A. and O'Connell,M.A. (2001) The many roles of an RNA editor. Genetics 2, 869-878.
7. Bass,B.L., Nishikura,K., Keller,W., Seeburg,P.H., Emeson,R.B., O'Connell,M.A., Samuel,C.E. and Herbert,A. (1997) A standardized nomenclature for adenosine deaminases that act on RNA. RNA, 3, 947-949.
8. Bass,B.L. (2002) RNA editing by adenosine deaminases that act on RNA. Annu. Rev. Biochem., 71, 817-846.
9. Melcher,T., Maas,S., Herb,A., Sprengel,R., Higuchi,M. and Seeburg,P.H. (1996) Communication - RED2, a brain-specific member of the RNA-specific adenosine deaminase family. J. Biol. Chem., 271, 31795-31798.
10. Chen,C., Cho,D., Wang,Q., Lai,F., Carter,K. and Nishikura,K. (2000) A third member of the RNA-specific adenosine deaminase gene family, ADAR3, contains both single- and double-stranded RNA binding domains. RNA, 6, 755-767.
11. Maas,S., Kawahara,Y., Tamburro,K.M. and Nishikura,K. (2006) A-to-I RNA editing and human disease. RNA Biol., 3, 1-9.
12. Li,M., Yang,L., Li,C., Jin,C., Lai,M., Zhang,G., Hu,Y., Ji,J. and Yao,Z. (2010) Mutational spectrum of the ADAR1 gene in dyschromatosis symmetrica hereditaria. Arch. Dermatol. Res., 302, 469-476.
13. Miyamura,Y., Suzuki,T., Kono,M., Inagaki,K., Ito,S., Suzuki,N. and Tomita,Y. (2003) Mutations of the RNA-specific adenosine deaminase gene (DSRAD) are involved in dyschromatosis symmetrica hereditaria. Am. J. Hum. Genet., 73, 693-699.
14. Rice,G.I., Kasher,P.R., Forte,G.M., Mannion,N.M., Greenwood,S.M., Szynkiewicz,M., Dickerson,J.E., Bhaskar,S.S., Zampini,M., Briggs,T.A. et al. (2012) Mutations in ADAR1 cause Aicardi-Goutieres syndrome associated with a type I interferon signature. Nat. Genet., 44, 1243-1248.
15. Zhang,X.J., He,P.P., Li,M., He,C.D., Yan,K.L., Cui,Y., Yang,S., Zhang,K.Y., Gao,M., Chen,J.J. et al. (2004) Seven novel mutations of the ADAR gene in Chinese families and sporadic patients with dyschromatosis symmetrica hereditaria (DSH). Hum. Mutat., 23, 629-630.
16. Eggington,J.M., Greene,T. and Bass,B.L. (2011) Predicting sites of ADAR editing in double-stranded RNA. Nat. Commun., 2, 319-327.
17. Lehmann,K.A. and Bass,B.L. (2000) Double-stranded RNA adenosine deaminases ADAR1 and ADAR2 have overlapping specificities. Biochemistry, 39, 12875-12884.
18. Maas,S., Melcher,T., Herb,A., Seeburg,P.H., Keller,W., Krause,S., Higuchi,M. and O'Connell,M.A. (1996) Structural requirements for RNA editing in glutamate receptor pre-mRNAs by recombinant double-stranded RNA adenosine deaminase. J. Biol. Chem., 271, 12221-12226.
19. Melcher,T., Maas,S., Herb,A., Sprengel,R., Seeburg,P.H. and Higuchi,M. (1996) A mammalian RNA editing enzyme. Nature, 379, 460-464.
20. Wong,S., Sato,S. and Lazinski,D.W. (2001) Substrate recognition by ADAR1 and ADAR2. RNA, 7, 846-858.
21. Yeo,J., Goodman,R.A., Schirle,N.T., David,S.S. and Beal,P.A. (2010) RNA editing changes the lesion specificity for the DNA repair enzyme NEIL1. Proc. Natl. Acad. Sci. U.S.A., 107, 20715-20719.
22. Goodman,R.A., Macbeth,M.R. and Beal,P.A. (2012) ADAR proteins: structure and catalytic mechanism. Curr. Top. Microbiol. Immunol., 353, 1-33.
23. Barraud,P. and Allain,F.H. (2012) ADAR proteins: double-stranded RNA and Z-DNA binding domains. Curr. Top. Microbiol. Immunol., 353, 35-60.
24. Bass,B.L., Hurst,S.R. and Singer,J.D. (1994) Binding properties of newly identified Xenopus proteins containing dsRNA binding motifs. Curr. Biol., 4, 301-314.
25. Doyle,M. and Jantsch,M.F. (2002) New and old roles of the double-stranded RNA-binding domain. J. Struct. Biol., 140, 147-153.
26. Ryter,J.M. and Schultz,S.C. (1998) Molecular basis of double-stranded RNA-protein interactions: structure of a dsRNA binding domain complexed with dsRNA. EMBO J., 17, 7505-7513.
27. Matthews,M.M., Thomas,J.M., Zheng,Y., Tran,K., Phelps,K.J., Scott,A.I., Havel,J., Fisher,A.J. and Beal,P.A. (2016) Structures of human ADAR2 bound to dsRNA reveal base-flipping mechanism and basis for site selectivity. Nat. Struct. Mol. Biol., 23, 426-433.
28. Gietz,R.D. and Schiestl,R.H. (2007) High-efficiency yeast transformation using the LiAc/SS carrier DNA/PEG method. Nat. Protoc., 2, 31-34.
29. Macbeth,M.R. and Bass,B.L. (2007) Large-scale overexpression and purification of ADARs from Saccharomyces cerevisiae for biophysical and biochemical studies. Methods Enzymol., 424, 319-331.
30. Wang,Y., Havel,J. and Beal,P.A. (2015) A phenotypic screen for functional mutants of human adenosine deaminase acting on RNA 1. ACS Chem. Biol., 10, 2512-2519.
31. Pokharel,S. and Beal,P.A. (2006) High-throughput screening for functional adenosine to inosine RNA editing systems. ACS Chem. Biol., 1, 761-765.
32. 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.
33. Kuttan,A. and Bass,B.L. (2012) Mechanistic insights into editing-site specificity of ADARs. Proc. Natl. Acad. Sci. U.S.A., 109, E3295-E3304.
34. Pokharel,S., Jayalath,P., Maydanovych,O., Goodman,R.A., Wang,S.C., Tantillo,D.J. and Beal,P.A. (2009) Matching active site and substrate structures for an RNA editing reaction. J. Am. Chem. Soc., 131, 11882-11891.
35. Cormack,B. (1998) Green fluorescent protein as a reporter of transcription and protein localization in fungi. Curr. Opin. Microbiol., 1, 406-410.
36. Michener,J.K. and Smolke,C.D. (2012) High-throughput enzyme evolution in Saccharomyces cerevisiae using a synthetic RNA switch. Metab. Eng., 14, 306-316.
37. Shiroishi,M. and Kobayashi,T. (2015) Screening of stable G-protein-coupled receptor variants in Saccharomyces cerevisiae. Methods Mol. Biol., 1261, 159-170.
38. 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.
39. Gajula,K.S., Huwe,P.J., Mo,C.Y., Crawford,D.J., Stivers,J.T., Radhakrishnan,R. and Kohli,R.M. (2014) High-throughput mutagenesis reveals functional determinants for DNA targeting by activation-induced deaminase. Nucleic Acids Res., 42, 9964-9975.
40. Palladino,M.J., Keegan,L.P., O'Connell,M.A. and Reenan,R.A. (2000) dADAR,a Drosophila double-stranded RNA-specific adenosine deaminase is highly developmentally regulated and is itself a target for RNA editing. RNA, 6, 1004-1018.
41. Savva,Y.A., Jepson,J.E., Sahin,A., Sugden,A.U., Dorsky,J.S., Alpert,L., Lawrence,C. and Reenan,R.A. (2012) Auto-regulatory RNA editing fine-tunes mRNA re-coding and complex behaviour in Drosophila. Nat. Commun., 3, 790-799.
42. Deffit,S.N. and Hundley,H.A. (2016) To edit or not to edit: regulation of ADAR editing specificity and efficiency. Wiley Interdiscip. Rev. RNA, 7, 113-127.
43. Garncarz,W., Tariq,A., Handl,C., Pusch,O. and Jantsch,M.F. (2013) A high throughput screen to identify enhancers of ADAR-mediated RNA-editing. RNA Biol., 10, 192-204.
44. Marcucci,R., Brindle,J., Paro,S., Casadio,A., Hempel,S., Morrice,N., Bisso,A., Keegan,L.P., Del Sal,G. and O'Connell,M.A. (2011) Pin1 and WWP2 regulate GluR2 Q/R site RNA editing by ADAR2 with opposing effects. EMBO J., 30, 4211-4222.
45. Tariq,A., Garncarz,W., Handl,C., Balik,A., Pusch,O. and Jantsch,M.F. (2013) RNA-interacting proteins act as site-specific repressors of ADAR2-mediated RNA editing and fluctuate upon neuronal stimulation. Nucleic Acids Res., 41, 2581-2593.