Imaging metabolite dynamics in living cells using a Spinach-based riboswitch

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 21, 2015, Pages E2756-E2765

  You, Mingxu ^a   Litke, Jacob L ^a   Jaffrey, Samie R ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

Cellular imaging; Fluorescence; Metabolite; Riboswitch; RNA probes

Indexed keywords

BACILLUS SUBTILIS; BINDING SITE; BIOSYNTHESIS; ESCHERICHIA COLI; FLUORESCENCE; METABOLITE; NONHUMAN; POPULATION; PRIORITY JOURNAL; PROMOTER REGION; REVIEW; RIBOSWITCH; SPINACH; TRANSDUCER; UPREGULATION; GENETICS; METABOLISM; SINGLE CELL ANALYSIS; SPECTROFLUOROMETRY;

BACILLUS SUBTILIS; ESCHERICHIA COLI; SPINACIA OLERACEA;

APTAMER; COCARBOXYLASE; GREEN FLUORESCENT PROTEIN; RIBOSWITCH;

APTAMERS, NUCLEOTIDE; BACILLUS SUBTILIS; ESCHERICHIA COLI; GREEN FLUORESCENT PROTEINS; RIBOSWITCH; SINGLE-CELL ANALYSIS; SPECTROMETRY, FLUORESCENCE; THIAMINE PYROPHOSPHATE;

EID: 84930227077     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1504354112     Document Type: Review

References (59)

1. Zhang J, Campbell RE, Ting AY, Tsien RY (2002) Creating new fluorescent probes for cell biology. Nat Rev Mol Cell Biol 3(12):906-918.
2. Frommer WB, Davidson MW, Campbell RE (2009) Genetically encoded biosensors based on engineered fluorescent proteins. Chem Soc Rev 38(10):2833-2841.
3. Lakowicz JR (2006) Principles of Fluorescence Spectroscopy (Springer, New York) 3rd Ed.
4. Lindenburg L, Merkx M (2014) Engineering genetically encoded FRET sensors. Sensors (Basel) 14(7):11691-11713.
5. Paige JS, Nguyen-Duc T, Song W, Jaffrey SR (2012) Fluorescence imaging of cellular metabolites with RNA. Science 335(6073):1194.
6. Paige JS, Wu KY, Jaffrey SR (2011) RNA mimics of green fluorescent protein. Science 333(6042):642-646.
7. Song W, Strack RL, Svensen N, Jaffrey SR (2014) Plug-and-play fluorophores extend the spectral properties of Spinach. J Am Chem Soc 136(4):1198-1201.
8. Song W, Strack RL, Jaffrey SR (2013) Imaging bacterial protein expression using genetically encoded RNA sensors. Nat Methods 10(9):873-875.
9. Kellenberger CA, Wilson SC, Sales-Lee J, Hammond MC (2013) RNA-based fluorescent biosensors for live cell imaging of second messengers cyclic di-GMP and cyclic AMP-GMP. J Am Chem Soc 135(13):4906-4909.
10. Tuerk C, Gold L (1990) Systematic evolution of ligands by exponential enrichment: RNA ligands to bacteriophage T4 DNA polymerase. Science 249(4968):505-510.
11. Ellington AD, Szostak JW (1990) In vitro selection of RNA molecules that bind specific ligands. Nature 346(6287):818-822.
12. Stoltenburg R, Reinemann C, Strehlitz B (2007) SELEX - a (r)evolutionary method to generate high-affinity nucleic acid ligands. Biomol Eng 24(4):381-403.
13. Strack RL, Jaffrey SR (2013) New approaches for sensing metabolites and proteins in live cells using RNA. Curr Opin Chem Biol 17(4):651-655.
14. Klug SJ, Famulok M (1994) All you wanted to know about SELEX. Mol Biol Rep 20(2): 97-107.
15. Nahvi A, et al. (2002) Genetic control by a metabolite binding mRNA. Chem Biol 9(9):1043.
16. Serganov A, Nudler E (2013) A decade of riboswitches. Cell 152(1-2):17-24.
17. Weinberg Z, et al. (2010) Comparative genomics reveals 104 candidate structured RNAs from bacteria, archaea, and their metagenomes. Genome Biol 11(3):R31.
18. Barrick JE, et al. (2004) New RNA motifs suggest an expanded scope for riboswitches in bacterial genetic control. Proc Natl Acad Sci USA 101(17):6421-6426.
19. Baker JL, et al. (2012) Widespread genetic switches and toxicity resistance proteins for fluoride. Science 335(6065):233-235.
20. Weinberg Z, et al. (2007) Identification of 22 candidate structured RNAs in bacteria using the CMfinder comparative genomics pipeline. Nucleic Acids Res 35(14): 4809-4819.
21. Mandal M, et al. (2004) A glycine-dependent riboswitch that uses cooperative binding to control gene expression. Science 306(5694):275-279.
22. Nelson JW, et al. (2013) Riboswitches in eubacteria sense the second messenger c-di-AMP. Nat Chem Biol 9(12):834-839.
23. Jurgenson CT, Begley TP, Ealick SE (2009) The structural and biochemical foundations of thiamin biosynthesis. Annu Rev Biochem 78:569-603.
24. Winkler W, Nahvi A, Breaker RR (2002) Thiamine derivatives bind messenger RNAs directly to regulate bacterial gene expression. Nature 419(6910):952-956.
25. Serganov A, Polonskaia A, Phan AT, Breaker RR, Patel DJ (2006) Structural basis for gene regulation by a thiamine pyrophosphate-sensing riboswitch. Nature 441(7097): 1167-1171.
26. Edwards TE, Ferré-D'Amaré AR (2006) Crystal structures of the thi-box riboswitch bound to thiamine pyrophosphate analogs reveal adaptive RNA-small molecule recognition. Structure 14(9):1459-1468.
27. Serganov A, Patel DJ (2012) Metabolite recognition principles and molecular mechanisms underlying riboswitch function. Annu Rev Biophys 41:343-370.
28. Ceres P, Garst AD, Marcano-Velázquez JG, Batey RT (2013) Modularity of select riboswitch expression platforms enables facile engineering of novel genetic regulatory devices. ACS Synth Biol 2(8):463-472.
29. Warner KD, et al. (2014) Structural basis for activity of highly efficient RNA mimics of green fluorescent protein. Nat Struct Mol Biol 21(8):658-663.
30. Huang H, et al. (2014) A G-quadruplex-containing RNA activates fluorescence in a GFP-like fluorophore. Nat Chem Biol 10(8):686-691.
31. Nakayama H, Hayashi R (1972) Biosynthesis of thiamine pyrophosphate in Escherichia coli. J Bacteriol 109(2):936-938.
32. Kulshina N, Edwards TE, Ferré-D'Amaré AR (2010) Thermodynamic analysis of ligand binding and ligand binding-induced tertiary structure formation by the thiamine pyrophosphate riboswitch. RNA 16(1):186-196.
33. Deigan KE, Ferré-D'Amaré AR (2011) Riboswitches: Discovery of drugs that target bacterial gene-regulatory RNAs. Acc Chem Res 44(12):1329-1338.
34. Du Q, Wang H, Xie J (2011) Thiamin (vitamin B1) biosynthesis and regulation: A rich source of antimicrobial drug targets? Int J Biol Sci 7(1):41-52.
35. Sudarsan N, Cohen-Chalamish S, Nakamura S, Emilsson GM, Breaker RR (2005) Thiamine pyrophosphate riboswitches are targets for the antimicrobial compound pyrithiamine. Chem Biol 12(12):1325-1335.
36. Elena C, Liuhong C, Chris A, Finian LJ, Smith GA (2011) Fragment screening against the thiamine pyrophosphate riboswitch thiM. Chem Sci 2:157-165.
37. Chen L, Cressina E, Leeper FJ, Smith AG, Abell C (2010) A fragment-based approach to identifying ligands for riboswitches. ACS Chem Biol 5(4):355-358.
38. Warner KD, et al. (2014) Validating fragment-based drug discovery for biological RNAs: Lead fragments bind and remodel the TPP riboswitch specifically. Chem Biol 21(5):591-595.
39. Lang K, Rieder R, Micura R (2007) Ligand-induced folding of the thiM TPP riboswitch investigated by a structure-based fluorescence spectroscopic approach. Nucleic Acids Res 35(16):5370-5378.
40. Leonardi R, Roach PL (2004) Thiamine biosynthesis in Escherichia coli: In vitro reconstitution of the thiazole synthase activity. J Biol Chem 279(17):17054-17062.
41. Gerrits J, Eidhof H, Brunnekreeft JW, Hessels J (1997) Determination of thiamin and thiamin phosphates in whole blood by reversed-phase liquid chromatography with precolumn derivatization. Methods Enzymol 279:74-82.
42. Kawasi T, Iwashima A, Nose Y (1969) Regulation of thiamine biosynthesis in Escherichia coli. J Biochem 65(3):407-416.
43. Cerecedo LP, Soodak M, Eusebi AJ (1951) Studies on thiamine analogues. I. Experiments in vivo. J Biol Chem 189(1):293-299.
44. Shcherbo D, et al. (2010) Near-infrared fluorescent proteins. Nat Methods 7(10): 827-829.
45. Filonov GS, Moon JD, Svensen N, Jaffrey SR (2014) Broccoli: Rapid selection of an RNA mimic of green fluorescent protein by fluorescence-based selection and directed evolution. J Am Chem Soc 136(46):16299-16308.
46. Mandal M, Boese B, Barrick JE, Winkler WC, Breaker RR (2003) Riboswitches control fundamental biochemical pathways in Bacillus subtilis and other bacteria. Cell 113(5): 577-586.
47. Serganov A, et al. (2004) Structural basis for discriminative regulation of gene expression by adenine- and guanine-sensing mRNAs. Chem Biol 11(12):1729-1741.
48. Winkler WC, Nahvi A, Sudarsan N, Barrick JE, Breaker RR (2003) An mRNA structure that controls gene expression by binding S-adenosylmethionine. Nat Struct Biol 10(9): 701-707.
49. Topp S, et al. (2010) Synthetic riboswitches that induce gene expression in diverse bacterial species. Appl Environ Microbiol 76(23):7881-7884.
50. Wachter A, et al. (2007) Riboswitch control of gene expression in plants by splicing and alternative 3? end processing of mRNAs. Plant Cell 19(11):3437-3450.
51. Haller A, Altman RB, Soulière MF, Blanchard SC, Micura R (2013) Folding and ligand recognition of the TPP riboswitch aptamer at single-molecule resolution. Proc Natl Acad Sci USA 110(11):4188-4193.
52. McKeague M, Derosa MC (2012) Challenges and opportunities for small molecule aptamer development. J Nucleic Acids 2012:748913.
53. Bennett BD, et al. (2009) Absolute metabolite concentrations and implied enzyme active site occupancy in Escherichia coli. Nat Chem Biol 5(8):593-599.
54. Kellenberger CA, Hammond MC (2015) In vitro analysis of riboswitch-Spinach aptamer fusions as metabolite-sensing fluorescent biosensors. Methods Enzymol 550: 147-172.
55. Corbino KA, et al. (2005) Evidence for a second class of S-adenosylmethionine riboswitches and other regulatory RNA motifs in alpha-proteobacteria. Genome Biol 6(8):R70.
56. Meyer MM, Roth A, Chervin SM, Garcia GA, Breaker RR (2008) Confirmation of a second natural preQ1 aptamer class in Streptococcaceae bacteria. RNA 14(4):685-695.
57. Wang JX, Lee ER, Morales DR, Lim J, Breaker RR (2008) Riboswitches that sense S-adenosylhomocysteine and activate genes involved in coenzyme recycling. Mol Cell 29(6):691-702.
58. Strack RL, Disney MD, Jaffrey SR (2013) A superfolding Spinach2 reveals the dynamic nature of trinucleotide repeat-containing RNA. Nat Methods 10(12):1219-1224.
59. Alatossava T, Jütte H, Kuhn A, Kellenberger E (1985) Manipulation of intracellular magnesium content in polymyxin B nonapeptide-sensitized Escherichia coli by ionophore A23187. J Bacteriol 162(1):413-419.