Advances in methods for native expression and purification of RNA for structural studies

Current Opinion in Structural Biology

Volumn 26, Issue 1, 2014, Pages 1-8

  Batey, Robert T ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RIBONUCLEOPROTEIN; RNA; RNA POLYMERASE; TRANSFER RNA;

ANION EXCHANGE; GEL PERMEATION CHROMATOGRAPHY; HUMAN; INTRON; MOLECULAR GENETICS; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; REVIEW; RNA DEGRADATION; RNA EXPRESSION; RNA PURIFICATION; RNA SEQUENCE; RNA STRUCTURE; RNA SYNTHESIS; RNA TRANSCRIPTION; CHEMISTRY; FRACTIONATION; GENE EXPRESSION; GENETICS; ISOLATION AND PURIFICATION; PROCEDURES;

CHEMICAL FRACTIONATION; GENE EXPRESSION; HUMANS; RNA; RNA, TRANSFER;

EID: 84896821946     PISSN: 0959440X     EISSN: 1879033X     Source Type: Journal    
DOI: 10.1016/j.sbi.2014.01.014     Document Type: Review

References (64)

1. Serganov A., Patel D.J. Ribozymes, riboswitches and beyond: regulation of gene expression without proteins. Nat Rev Genet 2007, 8:776-790.
2. Edwards A.L., Garst A.D., Batey R.T. Determining structures of RNA aptamers and riboswitches by X-ray crystallography. Methods Mol Biol 2009, 535:135-163.
3. Milligan J.F., Uhlenbeck O.C. Synthesis of small RNAs using T7 RNA polymerase. Methods Enzymol 1989, 180:51-62.
4. Pleiss J.A., Derrick M.L., Uhlenbeck O.C. T7 RNA polymerase produces 5' end heterogeneity during in vitro transcription from certain templates. RNA 1998, 4:1313-1317.
5. Reyes F.E., Garst A.D., Batey R.T. Strategies in RNA crystallography. Methods Enzymol 2009, 469:119-139.
6. Uhlenbeck O.C. Keeping RNA happy. RNA 1995, 1:4-6.
7. Kladwang W., Hum J., Das R. Ultraviolet shadowing of RNA can cause significant chemical damage in seconds. Sci Rep 2012, 2:517.
8. Greenfeld M., Solomatin S.V., Herschlag D. Removal of covalent heterogeneity reveals simple folding behavior for P4-P6 RNA. J Biol Chem 2011, 286:19872-19879.
9. Lukavsky P.J., Puglisi J.D. Large-scale preparation and purification of polyacrylamide-free RNA oligonucleotides. RNA 2004, 10:889-893.
10. Milligan J.F., Groebe D.R., Witherell G.W., Uhlenbeck O.C. Oligoribonucleotide synthesis using T7 RNA polymerase and synthetic DNA templates. Nucleic Acids Res 1987, 15:8783-8798.
11. Ponchon L., Dardel F. Recombinant RNA technology: the tRNA scaffold. Nat Methods 2007, 4:571-576.
12. Ponchon L., Beauvais G., Nonin-Lecomte S., Dardel F. A generic protocol for the expression and purification of recombinant RNA in Escherichia coli using a tRNA scaffold. Nat Protoc 2009, 4:947-959.
13. Ponchon L., Catala M., Seijo B., El Khouri M., Dardel F., Nonin-Lecomte S., Tisne C. Co-expression of RNA-protein complexes in Escherichia coli and applications to RNA biology. Nucleic Acids Res 2013, 41:e150.
14. Ponchon L., Beauvais G., Nonin-Lecomte S., Dardel F. Selective RNase H cleavage of target RNAs from a tRNA scaffold. Methods Mol Biol 2012, 941:9-18.
15. Nelissen F.H., Leunissen E.H., van de Laar L., Tessari M., Heus H.A., Wijmenga S.S. Fast production of homogeneous recombinant RNA-towards large-scale production of RNA. Nucleic Acids Res 2012, 40:e102.
16. Chui H.M., Desaulniers J.P., Scaringe S.A., Chow C.S. Synthesis of helix 69 of Escherichia coli 23S rRNA containing its natural modified nucleosides, m(3)Psi and Psi. J Org Chem 2002, 67:8847-8854.
17. Vendeix F.A., Murphy F.Vt., Cantara W.A., Leszczynska G., Gustilo E.M., Sproat B., Malkiewicz A., Agris P.F. Human tRNA(Lys3)(UUU) is pre-structured by natural modifications for cognate and wobble codon binding through keto-enol tautomerism. J Mol Biol 2012, 416:467-485.
18. Paige J.S., Nguyen-Duc T., Song W., Jaffrey S.R. Fluorescence imaging of cellular metabolites with RNA. Science 2012, 335:1194.
19. Nakayama S., Luo Y., Zhou J., Dayie T.K., Sintim H.O. Nanomolar fluorescent detection of c-di-GMP using a modular aptamer strategy. Chem Commun (Camb) 2012, 48:9059-9061.
20. Kellenberger C.A., Wilson S.C., Sales-Lee J., Hammond M.C. RNA-based fluorescent biosensors for live cell imaging of second messengers cyclic di-GMP and cyclic AMP-GMP. J Am Chem Soc 2013, 135:4906-4909.
21. Song W., Strack R.L., Jaffrey S.R. Imaging bacterial protein expression using genetically encoded RNA sensors. Nat Methods 2013, 10:873-875.
22. Kieft J.S., Batey R.T. A general method for rapid and nondenaturing purification of RNAs. RNA 2004, 10:988-995.
23. Aviv H., Leder P. Purification of biologically active globin messenger RNA by chromatography on oligothymidylic acid-cellulose. Proc Natl Acad Sci U S A 1972, 69:1408-1412.
24. Pereira M.J., Behera V., Walter N.G. Nondenaturing purification of co-transcriptionally folded RNA avoids common folding heterogeneity. PLoS ONE 2010, 5:e12953.
25. Srisawat C., Engelke D.R. Streptavidin aptamers: affinity tags for the study of RNAs and ribonucleoproteins. RNA 2001, 7:632-641.
26. Srisawat C., Goldstein I.J., Engelke D.R. Sephadex-binding RNA ligands: rapid affinity purification of RNA from complex RNA mixtures. Nucleic Acids Res 2001, 29:E4.
27. Walker S.C., Scott F.H., Srisawat C., Engelke D.R. RNA affinity tags for the rapid purification and investigation of RNAs and RNA-protein complexes. Methods Mol Biol 2008, 488:23-40.
28. Butter F., Scheibe M., Morl M., Mann M. Unbiased RNA-protein interaction screen by quantitative proteomics. Proc Natl Acad Sci U S A 2009, 106:10626-10631.
29. Iioka H., Loiselle D., Haystead T.A., Macara I.G. Efficient detection of RNA-protein interactions using tethered RNAs. Nucleic Acids Res 2011, 39:e53.
30. Lemay V., Hossain A., Osheim Y.N., Beyer A.L., Dragon F. Identification of novel proteins associated with yeast snR30 small nucleolar RNA. Nucleic Acids Res 2011, 39:9659-9670.
31. Johansson H.E., Liljas L., Uhlenbeck O.C. RNA recognition by the MS2 phage coat protein. Semin Virol 1997, 8:176-185.
32. Coller J., Wickens M. Tethered function assays: an adaptable approach to study RNA regulatory proteins. Methods Enzymol 2007, 429:299-321.
33. Jurica M.S., Licklider L.J., Gygi S.P., Grigorieff N., Moore M.J. Purification and characterization of native spliceosomes suitable for three-dimensional structural analysis. RNA 2002, 8:426-439.
34. Said N., Rieder R., Hurwitz R., Deckert J., Urlaub H., Vogel J. In vivo expression and purification of aptamer-tagged small RNA regulators. Nucleic Acids Res 2009, 37.
35. Di Tomasso G., Lampron P., Dagenais P., Omichinski J.G., Legault P. The ARiBo tag: a reliable tool for affinity purification of RNAs under native conditions. Nucleic Acids Res 2011, 39:e18.
36. Lee H.Y., Haurwitz R.E., Apffel A., Zhou K., Smart B., Wenger C.D., Laderman S., Bruhn L., Doudna J.A. RNA-protein analysis using a conditional CRISPR nuclease. Proc Natl Acad Sci U S A 2013, 110:5416-5421.
37. Batey R.T., Kieft J.S. Improved native affinity purification of RNA. RNA 2007, 13:1384-1389.
38. Salvail-Lacoste A., Di Tomasso G., Piette B.L., Legault P. Affinity purification of T7 RNA transcripts with homogeneous ends using ARiBo and CRISPR tags. RNA 2013, 19:1003-1014.
39. Winkler W.C., Nahvi A., Roth A., Collins J.A., Breaker R.R. Control of gene expression by a natural metabolite-responsive ribozyme. Nature 2004, 428:281-286.
40. Huang F., Wang G., Coleman T., Li N. Synthesis of adenosine derivatives as transcription initiators and preparation of 5' fluorescein- and biotin-labeled RNA through one-step in vitro transcription. RNA 2003, 9:1562-1570.
41. Huang F., He J., Zhang Y., Guo Y. Synthesis of biotin-AMP conjugate for 5' biotin labeling of RNA through one-step in vitro transcription. Nat Protoc 2008, 3:1848-1861.
42. Kirby R., Cho E.J., Gehrke B., Bayer T., Park Y.S., Neikirk D.P., McDevitt J.T., Ellington A.D. Aptamer-based sensor arrays for the detection and quantitation of proteins. Anal Chem 2004, 76:4066-4075.
43. Collett J.R., Cho E.J., Lee J.F., Levy M., Hood A.J., Wan C., Ellington A.D. Functional RNA microarrays for high-throughput screening of antiprotein aptamers. Anal Biochem 2005, 338:113-123.
44. Coleman T.M., Wang G., Huang F. Superior 5' homogeneity of RNA from ATP-initiated transcription under the T7 phi 2.5 promoter. Nucleic Acids Res 2004, 32:e14.
45. Dunn J.J., Studier F.W. Complete nucleotide sequence of bacteriophage T7 DNA and the locations of T7 genetic elements. J Mol Biol 1983, 166:477-535.
46. Luo Y., Eldho N.V., Sintim H.O., Dayie T.K. RNAs synthesized using photocleavable biotinylated nucleotides have dramatically improved catalytic efficiency. Nucleic Acids Res 2011, 39:8559-8571.
47. Kao C., Rudisser S., Zheng M. A simple and efficient method to transcribe RNAs with reduced 3' heterogeneity. Methods 2001, 23:201-205.
48. Kao C., Zheng M., Rudisser S. A simple and efficient method to reduce nontemplated nucleotide addition at the 3 terminus of RNAs transcribed by T7 RNA polymerase. RNA 1999, 5:1268-1272.
49. Kim I., McKenna S.A., Viani Puglisi E., Puglisi J.D. Rapid purification of RNAs using fast performance liquid chromatography (FPLC). RNA 2007, 13:289-294.
50. McKenna S.A., Kim I., Puglisi E.V., Lindhout D.A., Aitken C.E., Marshall R.A., Puglisi J.D. Purification and characterization of transcribed RNAs using gel filtration chromatography. Nat Protoc 2007, 2:3270-3277.
51. Easton L.E., Shibata Y., Lukavsky P.J. Rapid, nondenaturing RNA purification using weak anion-exchange fast performance liquid chromatography. RNA 2010, 16:647-653.
52. Keel A.Y., Easton L.E., Lukavsky P.J., Kieft J.S. Large-scale native preparation of in vitro transcribed RNA. Methods Enzymol 2009, 469:3-25.
53. Sosnick T.R., Pan T. RNA folding: models and perspectives. Curr Opin Struct Biol 2003, 13:309-316.
54. Novikova I.V., Hennelly S.P., Sanbonmatsu K.Y. Structural architecture of the human long non-coding RNA, steroid receptor RNA activator. Nucleic Acids Res 2012, 40:5034-5051.
55. Xayaphoummine A., Viasnoff V., Harlepp S., Isambert H. Encoding folding paths of RNA switches. Nucleic Acids Res 2007, 35:614-622.
56. Shajani Z., Sykes M.T., Williamson J.R. Assembly of bacterial ribosomes. Annu Rev Biochem 2011, 80:501-526.
57. Vogel U., Jensen K.F. The RNA chain elongation rate in Escherichia coli depends on the growth rate. J Bacteriol 1994, 176:2807-2813.
58. Darzacq X., Shav-Tal Y., de Turris V., Brody Y., Shenoy S.M., Phair R.D., Singer R.H. In vivo dynamics of RNA polymerase II transcription. Nat Struct Mol Biol 2007, 14:796-806.
59. Makarova O.V., Makarov E.M., Sousa R., Dreyfus M. Transcribing of Escherichia coli genes with mutant T7 RNA polymerases: stability of lacZ mRNA inversely correlates with polymerase speed. Proc Natl Acad Sci U S A 1995, 92:12250-12254.
60. Bonner G., Patra D., Lafer E.M., Sousa R. Mutations in T7 RNA polymerase that support the proposal for a common polymerase active site structure. EMBO J 1992, 11:3767-3775.
61. Bonner G., Lafer E.M., Sousa R. Characterization of a set of T7 RNA polymerase active site mutants. J Biol Chem 1994, 269:25120-25128.
62. Toor N., Keating K.S., Taylor S.D., Pyle A.M. Crystal structure of a self-spliced group II intron. Science 2008, 320:77-82.
63. Swisher J.F., Su L.J., Brenowitz M., Anderson V.E., Pyle A.M. Productive folding to the native state by a group II intron ribozyme. J Mol Biol 2002, 315:297-310.
64. Kieft J.S., Costantino D.A., Filbin M.E., Hammond J., Pfingsten J.S. Structural methods for studying IRES function. Methods Enzymol 2007, 430:333-371.