In vivo expression and purification of aptamer-tagged small RNA regulators

Nucleic Acids Research

Volumn 37, Issue 20, 2009, Pages

  Said, Nelly ^a   Rieder, Renate ^a   Hurwitz, Robert ^b   Deckert, Jochen ^c,d   Urlaub, Henning ^e   Vogel, Jörg ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b MAX PLANCK INSTITUTE FOR INFECTION BIOLOGY   (Germany)

^c Department of Cellular Biochemistry ^*  (Germany)

^d Roche Kulmbach GmbH   (Germany)

^e MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

APTAMER; BACTERIAL PROTEIN; MESSENGER RNA; PROTEIN GCVB; PROTEIN HFQ; PROTEIN INVR; PROTEIN MS2; PROTEIN OMPN; PROTEIN RYBB; REPRESSOR PROTEIN; RNA BINDING PROTEIN; TRANSFER RNA; UNCLASSIFIED DRUG; UNTRANSLATED RNA;

AFFINITY CHROMATOGRAPHY; ARTICLE; BACTERIAL CHROMOSOME; BACTERIAL GROWTH; BACTERIAL STRAIN; GENE EXPRESSION; IN VIVO STUDY; MASS SPECTROMETRY; NONHUMAN; NORTHERN BLOTTING; NUCLEOTIDE SEQUENCE; PLASMID; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN PURIFICATION; SALMONELLA TYPHIMURIUM; WESTERN BLOTTING; CHEMISTRY; CHROMOSOME; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MOLECULAR GENETICS;

BACTERIA (MICROORGANISMS); SALMONELLA;

APTAMERS, NUCLEOTIDE; BASE SEQUENCE; CHROMATOGRAPHY, AFFINITY; CHROMOSOMES; MOLECULAR SEQUENCE DATA; RNA, UNTRANSLATED;

EID: 76149125466     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkp719     Document Type: Article

References (64)

1. Gerber, C.A., Relich, A. and Driscoll, D.M. (2004) Isolation of an mRNA-binding protein involved in C-to-U editing. Methods Mol. Biol., 265, 239-249.
2. Allerson, C.R., Martinez, A., Yikilmaz, E. and Rouault, T.A. (2003) A high-capacity RNA affinity column for the purification of human IRP1 and IRP2 overexpressed in Pichia pastoris. RNA, 9, 364-374.
3. Caputi, M., Mayeda, A., Krainer, A.R. and Zahler, A.M. (1999) hnRNP A/B proteins are required for inhibition of HIV-1 pre-mRNA splicing. EMBO J., 18, 4060-4067.
4. Bindereif, A. and Green, M.R. (1987) An ordered pathway of snRNP binding during mammalian pre-mRNA splicing complex assembly. EMBO J., 6, 2415-2424.
5. Grabowski, P.J. and Sharp, P.A. (1986) Affinity chromatography of splicing complexes: U2, U5, and U4 + U6 small nuclear ribonucleoprotein particles in the spliceosome. Science, 233, 1294-1299.
6. Blencowe, B.J., Sproat, B.S., Ryder, U., Barabino, S. and Lamond, A.I. (1989) Antisense probing of the human U4/U6 snRNP with biotinylated 2'-OMe RNA oligonucleotides. Cell, 59, 531-539.
7. Lingner, J. and Cech, T.R. (1996) Purification of telomerase from Euplotes aediculatus: requirement of a primer 3' overhang. Proc. Natl Acad. Sci. USA, 93, 10712-10717.
8. Srisawat, C. and Engelke, D.R. (2001) Streptavidin aptamers: affinity tags for the study of RNAs and ribonucleoproteins. RNA, 7, 632-641.
9. Windbichler, N. and Schroeder, R. (2006) Isolation of specific RNA-binding proteins using the streptomycin-binding RNA aptamer. Nature Protoc., 1, 637-640.
10. Locker, N., Easton, L.E. and Lukavsky, P.J. (2006) Affinity purification of eukaryotic 48S initiation complexes. RNA, 12, 683-690.
11. Hartmuth, K., Urlaub, H., Vornlocher, H.P., Will, C.L., Gentzel, M., Wilm, M. and Luhrmann, R. (2002) Protein composition of human prespliceosomes isolated by a tobramycin affinity-selection method. Proc. Natl Acad. Sci. USA, 99, 16719-16724.
12. Bardwell, V.J. and Wickens, M. (1990) Purification of RNA and RNA-protein complexes by an R17 coat protein affinity method. Nucleic Acids Res., 18, 6587-6594.
13. Zhou, Z., Sim, J., Griffith, J. and Reed, R. (2002) Purification and electron microscopic visualization of functional human spliceosomes. Proc. Natl Acad. Sci. USA, 99, 12203-12207.
14. Bessonov, S., Anokhina, M., Will, C.L., Urlaub, H. and Luhrmann, R. (2008) Isolation of an active step I spliceosome and composition of its RNP core. Nature, 452, 846-850.
15. Czaplinski, K., Kocher, T., Schelder, M., Segref, A., Wilm, M. and Mattaj, I.W. (2005) Identification of 40LoVe, a Xenopus hnRNP D family protein involved in localizing a TGF-beta-related mRNA during oogenesis. Dev. Cell, 8, 505-515.
16. Duncan, K., Grskovic, M., Strein, C., Beckmann, K., Niggeweg, R., Abaza, I., Gebauer, F., Wilm, M. and Hentze, M.W. (2006) Sex-lethal imparts a sex-specific function to UNR by recruiting it to the msl-2 mRNA 3' UTR: translational repression for dosage compensation. Genes Dev., 20, 368-379.
17. Hogg, J.R. and Collins, K. (2007) RNA-based affinity purification reveals 7SK RNPs with distinct composition and regulation. RNA, 13, 868-880.
18. Majdalani, N., Vanderpool, C.K. and Gottesman, S. (2005) Bacterial small RNA regulators. Crit. Rev. Biochem. Mol. Biol., 40, 93-113.
19. Romby, P., Vandenesch, F. and Wagner, E.G. (2006) The role of RNAs in the regulation of virulence-gene expression. Curr. Opin. Microbiol., 9, 229-236.
20. Görke, B. and Vogel, J. (2008) Noncoding RNA control of the making and breaking of sugars. Genes Dev., 22, 2914-2925.
21. Waters, L.S. and Storz, G. (2009) Regulatory RNAs in bacteria. Cell, 136, 615-628.
22. Massé, E., Salvail, H., Desnoyers, G. and Arguin, M. (2007) Small RNAs controlling iron metabolism. Curr. Opin. Microbiol., 10, 140-145.
23. Livny, J. and Waldor, M.K. (2007) Identification of small RNAs in diverse bacterial species. Curr. Opin. Microbiol., 10, 96-101.
24. Wassarman, K.M. (2007) 6S RNA: a regulator of transcription. Mol. Microbiol., 65, 1425-1431.
25. Lapouge, K., Schubert, M., Allain, F.H. and Haas, D. (2008) Gac/Rsm signal transduction pathway of gamma-proteobacteria: from RNA recognition to regulation of social behaviour. Mol. Microbiol., 67, 241-253.
26. Babitzke, P. and Romeo, T. (2007) CsrB sRNA family: sequestration of RNA-binding regulatory proteins. Curr. Opin. Microbiol., 10, 156-163.
27. Vogel, J. and Wagner, E.G. (2007) Target identification of regulatory sRNAs in bacteria. Curr. Opin. Microbiol., 10, 262-270.
28. Aiba, H. (2007) Mechanism of RNA silencing by Hfq-binding small RNAs. Curr. Opin. Microbiol., 10, 134-139.
29. Valentin-Hansen, P., Eriksen, M. and Udesen, C. (2004) The bacterial Sm-like protein Hfq: a key player in RNA transactions. Mol. Microbiol., 51, 1525-1533.
30. Sittka, A., Lucchini, S., Papenfort, K., Sharma, C.M., Rolle, K., Binnewies, T.T., Hinton, J.C. and Vogel, J. (2008) Deep sequencing analysis of small noncoding RNA and mRNA targets of the global post-transcriptional regulator, Hfq. PLoS Genet., 4, e1000163.
31. Zhang, A., Wassarman, K.M., Rosenow, C., Tjaden, B.C., Storz, G. and Gottesman, S. (2003) Global analysis of small RNA and mRNA targets of Hfq. Mol. Microbiol., 50, 1111-1124.
32. Sittka, A., Sharma, C.M., Rolle, K. and Vogel, J. (2009) Deep sequencing of Salmonella RNA associated with heterologous Hfq proteins in vivo reveals small RNAs as a major target class and identifies RNA processing phenotypes. RNA Biol., 6, e1000163.
33. Pichon, C. and Felden, B. (2007) Proteins that interact with bacterial small RNA regulators. FEMS Microbiol. Rev., 31, 614-625.
34. Urbanowski, M.L., Stauffer, L.T. and Stauffer, G.V. (2000) The gcvB gene encodes a small untranslated RNA involved in expression of the dipeptide and oligopeptide transport systems in Escherichia coli. Mol. Microbiol., 37, 856-868.
35. Sharma, C.M., Darfeuille, F., Plantinga, T.H. and Vogel, J. (2007) A small RNA regulates multiple ABC transporter mRNAs by targeting C/A-rich elements inside and upstream of ribosome-binding sites. Genes Dev., 21, 2804-2817.
36. Pfeiffer, V., Sittka, A., Tomer, R., Tedin, K., Brinkmann, V. and Vogel, J. (2007) A small non-coding RNA of the invasion gene island (SPI-1) represses outer membrane protein synthesis from the Salmonella core genome. Mol. Microbiol., 66, 1174-1191.
37. Papenfort, K., Pfeiffer, V., Mika, F., Lucchini, S., Hinton, J.C. and Vogel, J. (2006) sigma(E)-dependent small RNAs of Salmonella respond to membrane stress by accelerating global omp mRNA decay. Mol. Microbiol., 62, 1674-1688.
38. Sittka, A., Pfeiffer, V., Tedin, K. and Vogel, J. (2007) The RNA chaperone Hfq is essential for the virulence of Salmonella typhimurium. Mol. Microbiol., 63, 193-217.
39. Hoiseth, S.K. and Stocker, B.A. (1981) Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines. Nature, 291, 238-239.
40. Datsenko, K.A. and Wanner, B.L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl Acad. Sci. USA, 97, 6640-6645.
41. LeCuyer, K.A., Behlen, L.S. and Uhlenbeck, O.C. (1995) Mutants of the bacteriophage MS2 coat protein that alter its cooperative binding to RNA. Biochemistry, 34, 10600-10606.
42. Jurica, M.S., Licklider, L.J., Gygi, S.R., Grigorieff, N. and Moore, M.J. (2002) Purification and characterization of native spliceosomes suitable for three-dimensional structural analysis. RNA, 8, 426-439.
43. Shevchenko, A., Wilm, M., Vorm, O. and Mann, M. (1996) Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem., 68, 850-858.
44. Jungblut, P.R. and Seifert, R. (1990) Analysis by high-resolution two-dimensional electrophoresis of differentiation-dependent alterations in cytosolic protein pattern of HL-60 leukemic cells. J. Biochem. Biophys. Methods, 21, 47-58.
45. Batey, R.T. and Kieft, J.S. (2007) Improved native affinity purification of RNA. RNA, 13, 1384-1389.
46. Das, R., Zhou, Z. and Reed, R. (2000) Functional association of U2 snRNP with the ATP-independent spliceosomal complex E. Mol. Cell, 5, 779-787.
47. Deckert, J., Hartmuth, K., Boehringer, D., Behzadnia, N., Will, C.L., Kastner, B., Stark, H., Urlaub, H. and Luhrmann, R. (2006) Protein composition and electron microscopy structure of affinity-purified human spliceosomal B complexes isolated under physiological conditions. Mol. Cell Biol., 26, 5528-5543.
48. Daigle, N. and Ellenberg, J. (2007) LambdaN-GFP: an RNA reporter system for live-cell imaging. Nat. Methods, 4, 633-636.
49. Valencia-Burton, M., McCullough, R.M., Cantor, C.R. and Broude, N.E. (2007) RNA visualization in live bacterial cells using fluorescent protein complementation. Nat. Methods, 4, 421-427.
50. Song, T., Mika, F., Lindmark, B., Liu, Z., Schild, S., Bishop, A., Zhu, J., Camilli, A., Johansson, J., Vogel, J. et al. (2008) A new Vibrio cholerae sRNA modulates colonization and affects release of outer membrane vesicles. Mol. Microbiol., 70, 100-111.
51. Bouvier, M., Sharma, C.M., Mika, F., Nierhaus, K.H. and Vogel, J. (2008) Small RNA binding to 5' mRNA coding region inhibits translational initiation. Mol. Cell, 32, 827-837.
52. Lutz, R. and Bujard, H. (1997) Independent and tight regulation of transcriptional units in Escherichia coli via the LacR/O, the TetR/O and AraC/I1-I2 regulatory elements. Nucleic Acids Res., 25, 1203-1210.
53. Zhou, Z. and Reed, R. (2003) Purification of functional RNA-protein complexes using MS2-MBP. In Ausubel, F.M. (ed.), Current Protocols in Molecular Biology. John Wiley & Sons, Inc, New York. Chapter 27, Unit 27.
54. Johansen, J., Rasmussen, A.A., Overgaard, M. and Valentin-Hansen, P. (2006) Conserved small non-coding RNAs that belong to the sigma(E) regulon: role in down-regulation of outer membrane proteins. J. Mol. Biol., 364, 1-8.
55. Wassarman, K.M., Repoila, F., Rosenow, C., Storz, G. and Gottesman, S. (2001) Identification of novel small RNAs using comparative genomics and microarrays. Genes Dev., 15, 1637-1651.
56. Talbot, S.J. and Altman, S. (1994) Kinetic and thermodynamic analysis of RNA-protein interactions in the RNase P holoenzyme from Escherichia coli. Biochemistry, 33, 1406-1411.
57. Lohman, T.M., Overman, L.B., Ferrari, M.E. and Kozlov, A.G. (1996) A highly salt-dependent enthalpy change for Escherichia coli SSB protein-nucleic acid binding due to ion-protein interactions. Biochemistry, 35, 5272-5279.
58. Baumann, C., Otridge, J. and Gollnick, P. (1996) Kinetic and thermodynamic analysis of the interaction between TRAP (trp RNA-binding attenuation protein) of Bacillus subtilis and trp leader RNA. J. Biol. Chem., 271, 12269-12274.
59. Wassarman, K.M. and Storz, G. (2000) 6S RNA regulates E. coli RNA polymerase activity. Cell, 101, 613-623.
60. Windbichler, N., von Pelchrzim, F., Mayer, O., Csaszar, E. and Schroeder, R. (2008) Isolation of small RNA-binding proteins from E. coli: evidence for frequent interaction of RNAs with RNA polymerase. RNA Biol., 5, 30-40.
61. Chant, E.L. and Summers, D.K. (2007) Indole signalling contributes to the stable maintenance of Escherichia coli multicopy plasmids. Mol. Microbiol., 63, 35-43.
62. Hershberg, R., Altuvia, S. and Margalit, H. (2003) A survey of small RNA-encoding genes in Escherichia coli. Nucleic Acids Res., 31, 1813-1820.
63. Golding, I. and Cox, E.C. (2004) RNA dynamics in live Escherichia coli cells. Proc. Natl Acad. Sci. USA, 101, 11310-11315.
64. Winkler, C., Denker, K., Wortelkamp, S. and Sickmann, A. (2007) Silver- and Coomassie-staining protocols: detection limits and compatibility with ESI MS. Electrophoresis, 28, 2095-2099.