Co-expression of RNA-protein complexes in Escherichia coli and applications to RNA biology

Nucleic Acids Research

Volumn 41, Issue 15, 2013, Pages

  Ponchon, Luc ^a,b   Catala, Marjorie ^a,b   Seijo, Bili ^a,b   El Khouri, Marguerite ^a,b   Dardel, Frédéric ^a,b   Nonin Lecomte, Sylvie ^a,b   Tisné, Carine ^a,b  

^a CNRS   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; COAT PROTEIN; MESSENGER RNA; MOLECULAR SCAFFOLD; MS2 COAT PROTEIN; NICKEL; NUCLEASE; PEPTIDES AND PROTEINS; POLYHISTIDINE TAG; PROTEIN HFQ; PSEUDOPEPTIDE; RECOMBINANT RNA; TRANSFER MESSENGER RNA; TRANSFER RNA; UNCLASSIFIED DRUG; UNTRANSLATED RNA;

AFFINITY CHROMATOGRAPHY; ARTICLE; CHEMONUCLEOLYSIS; CONTROLLED STUDY; CRYSTALLOGRAPHY; ENCAPSULATION; ENZYME MODIFICATION; ESCHERICHIA COLI; GENE OVEREXPRESSION; INTERACTIONS WITH RNA; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMID; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROCESSING; PROTEIN PURIFICATION; PROTEIN SYNTHESIS; RIBONUCLEIC ACID PROTEIN COMPLEX; RNA BINDING; RNA PURIFICATION; RNA SYNTHESIS; VIRUS LIKE AGENT;

BASE SEQUENCE; CAPSID PROTEINS; ESCHERICHIA COLI; GENETIC VECTORS; LEVIVIRUS; METHYLATION; PLASMIDS; PROTEIN INTERACTION MAPPING; RECOMBINANT PROTEINS; RNA; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, BACTERIAL; RNA, TRANSFER, LYS; RNA-BINDING PROTEINS;

EID: 84883480063     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt576     Document Type: Article

References (67)

1. Breaker,R.R. (2004) Natural and engineered nucleic acids as tools to explore biology. Nature, 432, 838-845.
2. Roth,A. and Breaker,R.R. (2009) The structural and functional diversity of metabolite-binding riboswitches. Annu. Rev. Biochem., 78, 305-334.
3. Guo,P. (2005) RNA nanotechnology: engineering, assembly and applications in detection, gene delivery and therapy. J. Nanosci. Nanotechnol., 5, 1964-1982.
4. Guo,P. (2010) The emerging field of RNA nanotechnology. Nat. Nanotechnol., 5, 833-842.
5. Gumireddy,K., Young,D.D., Xiong,X., Hogenesch,J.B., Huang,Q. and Deiters,A. (2008) Small-molecule inhibitors of microrna miR-21 function. Angew. Chem. Int. Ed Engl., 47, 7482-7484.
6. Wahlestedt,C. (2006) Natural antisense and noncoding RNA transcripts as potential drug targets. Drug Discov. Today, 11, 503-508.
7. Jovanovic,M. and Hengartner,M.O. (2006) miRNAs and apoptosis: RNAs to die for. Oncogene, 25, 6176-6187.
8. Faghihi,M.A., Modarresi,F., Khalil,A.M., Wood,D.E., Sahagan,B.G., Morgan,T.E., Finch,C.E. St, Laurent,G. 3rd, Kenny,P.J. and Wahlestedt,C. (2008) Expression of a noncoding RNA is elevated in Alzheimer s disease and drives rapid feedforward regulation of beta-secretase. Na. Med., 14, 723-730.
9. Roshan,R., Ghosh,T., Scaria,V. and Pillai,B. (2009) MicroRNAs: novel therapeutic targets in neurodegenerative diseases. Drug Discov. Today, 14, 1123-1129.
10. Thomas,J.R. and Hergenrother,P.J. (2008) Targeting RNA with small molecules. Chem. Rev., 108, 1171-1224.
11. Ponchon,L. and Dardel,F. (2011) Large scale expression and purification of recombinant RNA in Escherichia coli. Methods, 54, 267-273.
12. Ponchon,L. and Dardel,F. (2007) Recombinant RNA technology: the tRNA scaffold. Nat. Methods, 4, 571-576.
13. Nonin-Lecomte,S., Germain-Amiot,N., Gillet,R., Hallier,M., Ponchon,L., Dardel,F. and Felden,B. (2009) Ribosome hijacking: a role for small protein B during trans-translation. EMBO Rep., 10, 160-165.
14. Benitez-Paez,A., Villarroya,M., Douthwaite,S., Gabaldon,T. and Armengod,M.E. (2010) YibK is the 2 -O-methyltransferase TrmL that modifies the wobble nucleotide in Escherichia coli tRNA(Leu) isoacceptors. RNA, 16, 2131-2143.
15. Iioka,H., Loiselle,D., Haystead,T.A. and Macara,I.G. (2011) Efficient detection of RNA-protein interactions using tethered RNAs. Nucleic Acids Res., 39, e53.
16. Paige,J.S., Wu,K.Y. and Jaffrey,S.R. (2011) RNA mimics of green fluorescent protein. Science, 333, 642-646.
17. Umekage,S. and Kikuchi,Y. (2009) In vivo circular RNA production using a constitutive promoter for high-level expression. J. Biosci. Bioeng., 108, 354-356.
18. Umekage,S. and Kikuchi,Y. (2009) In vitro and in vivo production and purification of circular RNA aptamer. J. Biotechnol., 139, 265-272.
19. Ponchon,L., Beauvais,G., Nonin-Lecomte,S. and Dardel,F. (2009) A generic protocol for the expression and purification of recombinant RNA in Escherichia coli using a tRNA scaffold. Nat. Protoc., 4, 947-959.
20. Nelissen,F.H., Leunissen,E.H., van de Laar,L., Tessari,M., Heus,H.A. and Wijmenga,S.S. (2012) Fast production of homogeneous recombinant RNA towards large-scale production of RNA. Nucleic Acids Res., 40, e102.
21. Zhang,X., Potty,A.S., Jackson,G.W., Stepanov,V., Tang,A., Liu,Y., Kourentzi,K., Strych,U., Fox,G.E. and Willson,R.C. (2009) Engineered 5S ribosomal RNAs displaying aptamers recognizing vascular endothelial growth factor and malachite green. J. Mol. Recognit., 22, 154-161.
22. Pasloske,B.L., Walkerpeach,C.R., Obermoeller,R.D., Winkler,M. and DuBois,D.B. (1998) Armored RNA technology for production of ribonuclease- resistant viral RNA controls and standards. J. Clin. Microbiol., 36, 3590-3594.
23. Meinnel,T., Mechulam,Y. and Fayat,G. (1988) Fast purification of a functional elongator tRNAmet expressed from a synthetic gene in vivo. Nucleic Acids Res., 16, 8095-8096.
24. Xue,H., Shen,W. and Wong,J.T. (1993) Purification of hyperexpressed Bacillus subtilis tRNA(Trp) cloned in Escherichia coli. J. Chromatogr., 613, 247-255.
25. Wallis,N.G., Dardel,F. and Blanquet,S. (1995) Heteronuclear NMR studies of the interactions of 15N-labeled methioninespecific transfer RNAs with methionyl-tRNA transformylase. Biochemistry, 34, 7668-7677.
26. Tisne,C., Rigourd,M., Marquet,R., Ehresmann,C. and Dardel,F. (2000) NMR and biochemical characterization of recombinant human tRNA(Lys)3 expressed in Escherichia coli: identification of posttranscriptional nucleotide modifications required for efficient initiation of HIV-1 reverse transcription. RNA, 6, 1403-1412.
27. Norrander,J., Kempe,T. and Messing,J. (1983) Construction of improved M13 vectors using oligodeoxynucleotide-directed mutagenesis. Gene, 26, 101-106.
28. Cheng,Y., Niu,J., Zhang,Y., Huang,J. and Li,Q. (2006) Preparation of His-tagged armored RNA phage particles as a control for real-time reverse transcription-PCR detection of severe acute respiratory syndrome coronavirus. J. Clin. Microbiol., 44, 3557-3561.
29. Droogmans,L., Roovers,M., Bujnicki,J.M., Tricot,C., Hartsch,T., Stalon,V. and Grosjean,H. (2003) Cloning and characterization of tRNA (m1A58) methyltransferase (TrmI) from thermus thermophilus HB27, a protein required for cell growth at extreme temperatures. Nucleic Acids Res., 31, 2148-2156.
30. Barraud,P., Golinelli-Pimpaneau,B., Atmanene,C., Sanglier,S., Van Dorsselaer,A., Droogmans,L., Dardel,F. and Tisne,C. (2008) Crystal structure of thermus thermophilus tRNA m1A58 methyltransferase and biophysical characterization of its interaction with tRNA. J. Mol. Biol., 377, 535-550.
31. Piotto,M., Saudek,V. and Sklenar,V. (1992) Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions. J. Biomol. NMR, 2, 661-665.
32. Nakamura,K. and Inouye,M. (1979) DNA sequence of the gene for the outer membrane lipoprotein of E coli: an extremely ATrich promoter. Cell, 18, 1109-1117.
33. Selzer,G., Som,T., Itoh,T. and Tomizawa,J. (1983) The origin of replication of plasmid p15A and comparative studies on the nucleotide sequences around the origin of related plasmids. Cell, 32, 119-129.
34. Davison,J. (1984) Mechanism of control of DNA replication and incompatibility in ColE1-type plasmids-a review. Gene, 28, 1-15.
35. de Boer,H.A., Comstock,L.J. and Vasser,M. (1983) The tac promoter: a functional hybrid derived from the trp and lac promoters. Proc. Natl Acad. Sci. USA, 80, 21-25.
36. Guo,P.X., Erickson,S. and Anderson,D. (1987) A small viral RNA is required for in vitro packaging of bacteriophage phi 29 DNA. Science, 236, 690-694.
37. Xiao,F., Moll,W.D., Guo,S. and Guo,P. (2005) Binding of pRNA to the N-terminal 14 amino acids of connector protein of bacteriophage phi29. Nucleic Acids Res., 33, 2640-2649.
38. Tisne,C., Roques,B.P. and Dardel,F. (2001) Heteronuclear NMR studies of the interaction of tRNA(Lys)3 with HIV-1 nucleocapsid protein. J. Mol. Biol., 306, 443-454.
39. Tisne,C., Roques,B.P. and Dardel,F. (2004) The annealing mechanism of HIV-1 reverse transcription primer onto the viral genome. J. Biol. Chem., 279, 3588-3595.
40. Auxilien,S., Keith,G., Le Grice,S.F. and Darlix,J.L. (1999) Role of post-transcriptional modifications of primer tRNALys,3 in the fidelity and efficacy of plus strand DNA transfer during HIV-1 reverse transcription. J. Biol. Chem., 274, 4412-4420.
41. Guelorget,A., Barraud,P., Tisne,C. and Golinelli-Pimpaneau,B. (2011) Structural comparison of tRNA m(1)A58 methyltransferases revealed different molecular strategies to maintain their oligomeric architecture under extreme conditions. BMC Struct. Biol., 11, 48.
42. Peabody,D.S. (1990) Translational repression by bacteriophage MS2 coat protein expressed from a plasmid. A system for genetic analysis of a protein-RNA interaction. J. Biol. Chem., 265, 5684-5689.
43. Pickett,G.G. and Peabody,D.S. (1993) Encapsidation of heterologous RNAs by bacteriophage MS2 coat protein. Nucleic Acids Res., 21, 4621-4626.
44. Peabody,D.S. (1993) The RNA binding site of bacteriophage MS2 coat protein. EMBO J., 12, 595-600.
45. Valegard,K., Murray,J.B., Stockley,P.G., Stonehouse,N.J. and Liljas,L. (1994) Crystal structure of an RNA bacteriophage coat protein-operator complex. Nature, 371, 623-626.
46. Helgstrand,C., Grahn,E., Moss,T., Stonehouse,N.J., Tars,K., Stockley,P.G. and Liljas,L. (2002) Investigating the structural basis of purine specificity in the structures of MS2 coat protein RNA translational operator hairpins. Nucleic Acids Res., 30, 2678-2685.
47. Grate,D. and Wilson,C. (1999) Laser-mediated, site-specific inactivation of RNA transcripts. Proc. Natl Acad. Sci. USA, 96, 6131-6136.
48. Kurita,D., Muto,A. and Himeno,H. (2011) tRNA/mRNA Mimicry by tmRNA and SmpB in Trans-Translation. J. Nucleic Acids., 2011, 130581.
49. Lukavsky,P.J. and Puglisi,J.D. (2004) Large-scale preparation and purification of polyacrylamide-free RNA oligonucleotides. RNA, 10, 889-893.
50. Jorgensen,M.G., Nielsen,J.S., Boysen,A., Franch,T., Moller-Jensen,J. and Valentin-Hansen,P. (2012) Small regulatory RNAs control the multi-cellular adhesive lifestyle of Escherichia coli. Mol. Microbiol., 84, 36-50.
51. Mika,F., Busse,S., Possling,A., Berkholz,J., Tschowri,N., Sommerfeldt,N., Pruteanu,M. and Hengge,R. (2012) Targeting of csgD by the small regulatory RNA RprA links stationary phase, biofilm formation and cell envelope stress in Escherichia coli. Mol. Microbiol., 84, 51-65.
52. Thomason,M.K., Fontaine,F., De Lay,N. and Storz,G. (2012) A small RNA that regulates motility and biofilm formation in response to changes in nutrient availability in Escherichia coli. Mol. Microbiol., 84, 17-35.
53. Moon,K. and Gottesman,S. (2009) A PhoQ/P-regulated small RNA regulates sensitivity of Escherichia coli to antimicrobial peptides. Mol. Microbiol., 74, 1314-1330.
54. Corcoran,C.P., Podkaminski,D., Papenfort,K., Urban,J.H., Hinton,J.C. and Vogel,J. (2012) Superfolder GFP reporters validate diverse new mRNA targets of the classic porin regulator, MicF RNA. Mol. Microbiol., 84, 428-445.
55. Holmqvist,E., Unoson,C., Reimegard,J. and Wagner,E.G. (2012) A mixed double negative feedback loop between the sRNA MicF and the global regulator Lrp. Mol. Microbiol., 84, 414-427.
56. Maki,K., Morita,T., Otaka,H. and Aiba,H. (2010) A minimal base-pairing region of a bacterial small RNA SgrS required for translational repression of ptsG mRNA. Mol. Microbiol., 76, 782-792.
57. Rice,J.B. and Vanderpool,C.K. (2011) The small RNA SgrS controls sugar-phosphate accumulation by regulating multiple PTS genes. Nucleic Acids Res., 39, 3806-3819.
58. Sonnleitner,E., Gonzalez,N., Sorger-Domenigg,T., Heeb,S., Richter,A.S., Backofen,R., Williams,P., Huttenhofer,A., Haas,D. and Blasi,U. (2011) The small RNA PhrS stimulates synthesis of the Pseudomonas aeruginosa quinolone signal. Mol. Microbiol., 80, 868-885.
59. Shao,Y. and Bassler,B.L. (2012) Quorum-sensing non-coding small RNAs use unique pairing regions to differentially control mRNA targets. Mol. Microbiol., 83, 599-611.
60. Boysen,A., Moller-Jensen,J., Kallipolitis,B., Valentin-Hansen,P. and Overgaard,M. (2010) Translational regulation of gene expression by an anaerobically induced small non-coding RNA in Escherichia coli. J. Biol. Chem., 285, 10690-10702.
61. Durand,S. and Storz,G. (2010) Reprogramming of anaerobic metabolism by the FnrS small RNA. Mol. Microbiol., 75, 1215-1231.
62. Papenfort,K., Podkaminski,D., Hinton,J.C. and Vogel,J. (2012) The ancestral SgrS RNA discriminates horizontally acquired Salmonella mRNAs through a single G-U wobble pair. Proc. Natl Acad. Sci. USA, 109, E757-E764.
63. Vanderpool,C.K. and Gottesman,S. (2004) Involvement of a novel transcriptional activator and small RNA in post-transcriptional regulation of the glucose phosphoenolpyruvate phosphotransferase system. Mol. Microbiol., 54, 1076-1089.
64. Otaka,H., Ishikawa,H., Morita,T. and Aiba,H. (2011) PolyU tail of rho-independent terminator of bacterial small RNAs is essential for Hfq action. Proc. Natl Acad. Sci. USA, 108, 13059-13064.
65. Ishikawa,H., Otaka,H., Maki,K., Morita,T. and Aiba,H. (2012) The functional Hfq-binding module of bacterial sRNAs consists of a double or single hairpin preceded by a U-rich sequence and followed by a 3 poly(U) tail. RNA, 18, 1062-1074.
66. Zuker,M. (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res., 31, 3406-3415.
67. Donia,D., Divizia,M. and Pana,A. (2005) Use of armored RNA as a standard to construct a calibration curve for real-time RT-PCR. J. Virol. Methods, 126, 157-163.