An evaluation of genetically encoded FRET-based biosensors for quantitative metabolite analyses in vivo

Journal of Biotechnology

Volumn 191, Issue , 2014, Pages 250-259

  Moussa, Roland ^a   Baierl, Anna ^a   Steffen, Victoria ^a   Kubitzki, Tina ^a   Wiechert, Wolfgang ^a   Pohl, Martina ^a  

^a FORSCHUNGSZENTRUM JÜLICH   (Germany)

Author keywords

Citrine; ECFP; EYFP; GFP; Intracellular metabolite analysis

Indexed keywords

BINDING ENERGY; BIOMOLECULES; ENERGY TRANSFER; ENZYME ACTIVITY; FLUORESCENCE; IONIC STRENGTH; METABOLITES; PROTEINS;

CITRINE; ECFP; EYFP; GFP; INTRACELLULAR METABOLITES;

BIOSENSORS;

4 (2 HYDROXYETHYL) 1 PIPERAZINEETHANESULFONIC ACID; ADENOSINE DIPHOSPHATE; ADENOSINE PHOSPHATE; ADENOSINE TRIPHOSPHATE; AMINO ACID; CARBOHYDRATE BINDING PROTEIN; CYCLIC GMP; GLUCOSE; GREEN FLUORESCENT PROTEIN; GUANOSINE TRIPHOSPHATE; HISTIDINE; MALTOSE; MANGANESE CHLORIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; POTASSIUM SALT; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; SODIUM CHLORIDE; SODIUM DIHYDROGEN PHOSPHATE; TROMETAMOL; PROTEIN; PROTEIN BINDING;

ARTICLE; BINDING AFFINITY; BIOSENSOR; CALCIUM BINDING; CHROMATOPHORE; CRYSTAL STRUCTURE; FLUORESCENCE; FLUORESCENCE RESONANCE ENERGY TRANSFER; GLUCOSE SENSOR; IN VIVO STUDY; IONIC STRENGTH; METABOLITE; MICROENVIRONMENT; PH; QUANTITATIVE ANALYSIS; QUANTITATIVE METABOLITE ANALYSIS; STATIC ELECTRICITY; TEMPERATURE; GENETIC PROCEDURES; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; PROTEIN TERTIARY STRUCTURE;

BIOSENSING TECHNIQUES; FLUORESCENCE RESONANCE ENERGY TRANSFER; GREEN FLUORESCENT PROTEINS; HYDROGEN-ION CONCENTRATION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEINS;

EID: 84911926312     PISSN: 01681656     EISSN: 18734863     Source Type: Journal    
DOI: 10.1016/j.jbiotec.2014.07.007     Document Type: Article

References (46)

1. Anjem A., Varghese S., Imlay J.A. Manganese import is a key element of the OxyR response to hydrogen peroxide in Escherichia coli. Mol. Microbiol. 2009, 72:844-858.
2. Bennett B.D., Kimball E.H., Gao M., Osterhout R., Van Dien S.J., Rabinowitz J.D. Absolute metabolite concentrations and implied enzyme active site occupancy in Escherichia coli. Nat. Chem. Biol. 2009, 5:593-599.
3. Bermejo C., Haerizadeh F., Takanaga H., Chermak D., Frommer W.B. Optical sensors for measuring dynamic changes of cytosolic metabolite levels in yeast. Nat. Prot. 2011, 6:1806-1817.
4. Bizzarri R., Serresi M., Luin S., Beltram F. Green fluorescent protein based pH indicators for in vivo use: a review. Anal. Bioanal. Chem. 2009, 393:1107-1122.
5. Borst J.W., Willemse M., Slijkhuis R., van der Krogt G., Laptenok S.P., Jalink K., Wieringa B., Fransen J.A. ATP changes the fluorescence lifetime of cyan fluorescent protein via an interaction with His148. PLoS One 2010, 5:e13862.
6. Campanini B., Pioselli B., Raboni S., Felici P., Giordano I., D'Alfonso L., Collini M., Chirico G., Bettati S. Role of histidine 148 in stability and dynamics of a highly fluorescent GFP variant. Biochim. Biophys. Acta 2013, 1834:770-779.
7. Cossins B.P., Jacobson M.P., Guallar V. A new view of the bacterial cytosol environment. PLoS Comp. Biol. 2011, 7:e1002066.
8. Dale R.E., Eisinger J., Blumberg W.E. The orientational freedom of molecular probes. The orientation factor in intramolecular energy transfer. Biophys. J. 1979, 26:161-193.
9. Deuschle K., Okumoto S., Fehr M., Looger L.L., Kozhukh L., Frommer W.B. Construction and optimization of a family of genetically encoded metabolite sensors by semirational protein engineering. Protein Sci. 2005, 14:2304-2314.
10. Drepper T., Gensch T., Pohl M. Advanced in vivo applications of blue light photoreceptors as alternative fluorescent proteins. Photochem. Photobiol. Sci. 2013, 12:1125-1134.
11. Fehr M., Frommer W.B., Lalonde S. Visualization of maltose uptake in living yeast cells by fluorescent nanosensors. Proc. Nat. Acad. Sci. 2002, 99:9846-9851.
12. Fehr M., Lalonde S., Lager I., Wolff M.W., Frommer W.B. In vivo imaging of the dynamics of glucose uptake in the cytosol of COS-7 cells by fluorescent nanosensors. J. Biol. Chem. 2003, 278:19127-19133.
13. Fehr M., Takanaga H., Ehrhardt D.W., Frommer W.B. Evidence for high-capacity bidirectional glucose transport across the endoplasmic reticulum membrane by genetically encoded fluorescence resonance energy transfer nanosensors. Mol. Cell. Biol. 2005, 25:11102-11112.
14. Förster T. Zwischenmolekulare Energiewanderung und Fluoreszenz. Annalen der Physik 1948, 437:55-75.
15. Griesbeck O., Baird G.S., Campbell R.E., Zacharias D.A., Tsien R.Y. Reducing the environmental sensitivity of yellow fluorescent protein: mechanism and applications. J. Biol. Chem. 2001, 276:29188-29194.
16. Hou B.H., Takanaga H., Grossmann G., Chen L.Q., Qu X.Q., Jones A.M., Lalonde S., Schweissgut O., Wiechert W., Frommer W.B. Optical sensors for monitoring dynamic changes of intracellular metabolite levels in mammalian cells. Nat. Prot. 2011, 6:1818-1833.
17. Hurwitz C., Rosano C.L. The intracellular concentration of bound and unbound magnesium ions in Escherichia coli. J. Biol. Chem. 1967, 242:3719-3722.
18. Jones A.M., Danielson J.A.H., ManojKumar S.N., Lanquar V., Grossmann G., Frommer W.B. Abscisic acid dynamics in roots detected with genetically encoded FRET sensors. Elife 2014, 3:e01741.
19. Kremers G.J., Goedhart J., van Munster E.B., Gadella T.W.J. Cyan and yellow super fluorescent proteins with improved brightness, protein folding, and FRET Forster radius. Biochemistry 2006, 45:6570-6580.
20. Liemburg-Apers D.C., Imamura H., Forkink M., Nooteboom M., Swarts H.G., Brock R., Smeitink J.A., Willems P.H., Koopman W.J. Quantitative glucose and ATP sensing in mammalian cells. Pharmaceut. Res. 2011, 28:2745-2757.
21. Llopis J., McCaffery J.M., Miyawaki A., Farquhar M.G., Tsien R.Y. Measurement of cytosolic, mitochondrial, and Golgi pH in single living cells with green fluorescent proteins. Proc. Nat. Acad. Sci. 1998, 95:6803-6808.
22. Lo C.J., Leake M.C., Berry R.M. Fluorescence measurement of intracellular sodium concentration in single Escherichia coli cells. Biophys. J. 2006, 90:357-365.
23. Martinière A., Debrosses G., Sentenac H., Paris N. Development and properties of genetically encoded pH sensors in plants. Front. Plant Sci. 2013, 4:523.
24. 2+ measurements using improved cameleons. Proc. Nat. Acad. Sci. 1999, 96:2135-2140.
25. 2+ based on green fluorescent proteins and calmodulin. Nature 1997, 388:882-887.
26. Newman R.H., Fosbrink M.D., Zhang J. Genetically encodable fluorescent biosensors for tracking signaling dynamics in living cells. Chem. Rev. 2011, 111:3614-3666.
27. Okumoto S., Jones A., Frommer W.B. Quantitative imaging with fluorescent biosensors. Ann. Rev. Plant Biol. 2012, 63:663-706.
28. Ormö M., Cubitt A.B., Kallio K., Gross L.A., Tsien R.Y., Remington S.J. Crystal structure of the Aequorea victoria green fluorescent protein. Science 1996, 273:1392-1395.
29. 2+ indicators based on computationally redesigned calmodulin-peptide pairs. Chem. Biol. 2006, 13:521-530.
30. Palmer A.E., Tsien R.Y. Measuring calcium signaling using genetically targetable fluorescent indicators. Nat. Prot. 2006, 1:1057-1065.
31. Potzkei J., Kunze M., Drepper T., Gensch T., Jaeger K.E., Büchs J. Real-time determination of intracellular oxygen in bacteria using a genetically encoded FRET-based biosensor. BMC Biol. 2012, 10:28.
32. Rizzo M.A., Springer G.H., Granada B., Piston D.W. An improved cyan fluorescent protein variant useful for FRET. Nat. Biotechnol. 2004, 22:445-449.
33. 2+ in organelles. Proc. Natl. Acad. Sci. 2014, 111:2584-2589.
34. San Martin A., Ceballo S., Baeza-Lehnert F., Lerchundi R., Valdebenito R., Contreras-Baeza Y., Alegria K., Barros L.F. Imaging mitochondrial flux in single cells with a FRET sensor for pyruvate. PLoS One 2014, 9:e85780.
35. San Martin A., Ceballo S., Ruminot I., Lerchundi R., Frommer W.B., Barros L.F. A genetically encoded FRET lactate sensor and its use to detect the Warburg effect in single cancer cells. PLoS One 2013, 8:e57712.
36. Schilling K., Cumme G.A., Hoffmann-Blume E., Hoppe H., Horn A. Multiwavelength photometry of thermochromic indicator solutions for temperature determination in multicuvettes. Clin. Chem. 1993, 39:251-256.
37. Shabala L., Bowman J., Brown J., Ross T., McMeekin T., Shabala S. Ion transport and osmotic adjustment in Escherichia coli in response to ionic and non-ionic osmotica. Environ. Microbiol. 2009, 11:137-148.
38. Spiering D., Bravo-Cordero J.J., Moshfegh Y., Miskolci V., Hogdson L. Quantitative ratiometric imaging of FRET-biosensors in living cells. Methods Cell Biol. 2013, 114:593-609.
39. 2+. Phys. Chem. Chem. Phys. 2011, 13:17852-17863.
40. Stryer L., Haugland R.P. Energy transfer: a spectroscopic ruler. Proc. Natl. Acad. Sci. U. S. A. 1967, 58:719-726.
41. Takanaga H., Chaudhuri B., Frommer W.B. GLUT1 and GLUT9 as major contributors to glucose influx in HepG2 cells identified by a high sensitivity intramolecular FRET glucose sensor. Biochim. Biophys. Acta: Biomembranes 2008, 1778:1091-1099.
42. Vyas N.K., Vyas M.N., Quiocho F.A. A novel calcium binding site in the galactose-binding protein of bacterial transport and chemotaxis. Nature 1987, 327:635-638.
43. Wachter R.M., Elsliger M.A., Kallio K., Hanson G.T., Remington S.J. Structural basis of spectral shifts in the yellow-emission variants of green fluorescent protein. Structure 1998, 6:1267-1277.
44. Watkins N.J., Knight M.R., Trewavas A.J., Campbell A.K. Free calcium transients in chemotactic and non-chemotactic strains of Escherichia coli determined by using recombinant aequorin. Biochem. J. 1995, 306:865-869.
45. Willemse M., Janssen E., Lange F.d., Wieringa B., Fransen J. ATP and FRET - a cautionary note. Nat. Biotech. 2007, 25:170-172.
46. Zhang J., Campbell R.E., Ting A.Y., Tsien R.Y. Creating new fluorescent probes for cell biology. Nat. Rev. Mol. Cell Biol. 2003, 3:906-918.