The Single T65S Mutation Generates Brighter Cyan Fluorescent Proteins with Increased Photostability and pH Insensitivity

PLoS ONE

Volumn 7, Issue 11, 2012, Pages

  Fredj, Asma ^a   Pasquier, Hélène ^a   Demachy, Isabelle ^a   Jonasson, Gabriella ^a   Levy, Bernard ^a   Derrien, Valérie ^a   Bousmah, Yasmina ^a   Manoussaris, Gallia ^a   Wien, Frank ^b   Ridard, Jacqueline ^a   Erard, Marie ^a   Merola, Fabienne ^a  

^a UNIVERSITÉ PARIS SUD   (France)

^b SYNCHROTRON SOLEIL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CYAN FLUORESCENT PROTEIN; GREEN FLUORESCENT PROTEIN;

ARTICLE; BLEACHING; CHROMATOPHORE; CONCENTRATION (PARAMETERS); CRYSTAL STRUCTURE; ENTROPY; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENE MUTATION; MUTATION RATE; PH; PHOTODYNAMICS; PHOTOREACTIVITY; PHOTOSTABILITY; PROTEIN SECONDARY STRUCTURE; PROTON TRANSPORT; QUANTUM YIELD; STEADY STATE; THERMODYNAMICS;

ANIMALS; BASE SEQUENCE; CELL LINE; CIRCULAR DICHROISM; DOGS; FLUORESCENCE RESONANCE ENERGY TRANSFER; FLUORESCENT DYES; GREEN FLUORESCENT PROTEINS; HYDROGEN-ION CONCENTRATION; MODELS, CHEMICAL; MOLECULAR SEQUENCE DATA; MUTAGENESIS; MUTATION; PHOTOCHEMISTRY; PHYSICS; SPECTROMETRY, FLUORESCENCE; SPECTROPHOTOMETRY, ULTRAVIOLET; SYNCHROTRONS; TIME FACTORS;

AEQUOREA VICTORIA;

EID: 84868305301     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0049149     Document Type: Article

References (62)

1. Zhang J, Allen MD, (2007) FRET-based biosensors for protein kinases: illuminating the kinome. Molecular Biosyst 3: 759-765.
2. Balla T, (2009) Green light to illuminate signal transduction events. Trends Cell Biol 19: 575-586.
3. Lu S, Wang Y, (2010) Fluorescence resonance energy transfer biosensors for cancer detection and evaluation of drug efficacy. Clin Cancer Res 16: 3822-3824.
4. Tian L, Looger LL, (2008) Genetically encoded fluorescent sensors for studying healthy and diseased nervous systems. Drug Discov Today Dis Models 5: 27-35.
5. Newman RH, Fosbrink MD, Zhang J, (2011) Genetically encodable fluorescent biosensors for tracking signaling dynamics in living cells. Chem Rev 111: 3614-3666.
6. Miyawaki A, (2011) Development of probes for cellular functions using fluorescent proteins and fluorescence resonance energy transfer. Annu Rev Biochem 80: 357-373.
7. Heim R, Prasher DC, Tsien RY, (1994) Wavelength mutations and posttranslational autoxidation of green fluorescent protein. Proc Natl Acad Sci U S A 91: 12501-12504.
8. Heim R, Tsien RY, (1996) Engineering green fluorescent protein for improved brightness, longer wavelengths and fluorescence resonance energy transfer. Curr Biol 6: 178-182.
9. Tsien RY, (1998) The green fluorescent protein. Annu Rev Biochem 67: 509-544.
10. Villoing A, Ridhoir M, Cinquin B, Erard M, Alvarez L, et al. (2008) Complex fluorescence of the cyan fluorescent protein: comparisons with the H148D variant and consequences for quantitative cell imaging. Biochemistry 47: 12483-12492.
11. Rizzo MA, Springer GH, Granada B, Piston DW, (2004) An improved cyan fluorescent protein variant useful for FRET. Nat Biotechnol 29: 445-449.
12. Shaner NC, Patterson GH, Davidson MW, (2007) Advances in fluorescent protein technology. J Cell Sci 120: 4247-4260.
13. Goedhart J, van Weeren L, Hink MA, Vischer NO, Jalink K, et al. (2010) Bright cyan fluorescent protein variants identified by fluorescence lifetime screening. Nat Methods 7: 137-139.
14. Markwardt ML, Kremers GJ, Kraft CA, Ray K, Cranfill PJ, et al. (2011) An improved cerulean fluorescent protein with enhanced brightness and reduced reversible photoswitching. PLoS One 6: e17896.
15. Goedhart J, von Stetten D, Noirclerc-Savoye M, Lelimousin M, Joosen L, et al. (2012) Structure-guided evolution of cyan fluorescent proteins towards a quantum yield of 93%. Nat Commun 3: doi: 10.1038.
16. Alvarez L, Levin CH, Merola F, Bizouarn T, Pasquier H, et al. (2009) Are the Fluorescent Properties of the Cyan Fluorescent Protein Sensitive to Conditions of Oxidative Stress? Photochem Photobiol 86: 55-61.
17. Patterson G, Day RN, Piston D, (2001) Fluorescent protein spectra. J Cell Sci 114: 837-838.
18. Mérola F, Rigler R, Holmgren A, Brochon JC, (1989) Picosecond tryptophan fluorescence of thioredoxin: evidence for discrete species in slow exchange. Biochemistry 28: 3383-3398.
19. Couprie ME, Mérola F, Tauc P, Garzella D, Delboulbé A, et al. (1994) First use of the UV Super-ACO free electron laser: fluorescence decays and rotational dynamics of the NADH coenzyme. Rev Sci Instrum 65: 1485-1495.
20. Valeur B (2002) Molecular Fluorescence. Principles and applications. Weinheim: Wiley-VCH. 402 p.
21. Giuliani A, Jamme F, Rouam V, Wien F, Giorgetta JL, et al. (2009) DISCO: a low-energy multipurpose beamline at synchrotron SOLEIL. J Synchrotron Radiat 16: 835-841.
22. Wien F, Wallace BA, (2005) Calcium fluoride micro cells for synchrotron radiation circular dichroism spectroscopy. Appl Spectrosc 59: 1109-1113.
23. Lees JG, Smith BR, Wien F, Miles AJ, Wallace BA, (2004) CDtool-an integrated software package for circular dichroism spectroscopic data processing, analysis, and archiving. Anal Biochem 332: 285-289.
24. Kelly SM, Jess TJ, Price NC, (2005) How to study proteins by circular dichroism. Biochim Biophys Acta 1751: 119-139.
25. Whitmore L, Wallace BA, (2004) DICHROWEB, an online server for protein secondary structure analyses from circular dichroism spectroscopic data. Nucleic Acids Res 32: W668-673.
26. Lees JG, Miles AJ, Wien F, Wallace BA, (2006) A reference database for circular dichroism spectroscopy covering fold and secondary structure space. Bioinformatics 22: 1955-1962.
27. Chudakov DM, Matz MV, Lukyanov S, Lukyanov KA (2010) Fluorescent Proteins and Their Applications in Imaging Living Cells and Tissues. Physiol Rev: 1103-1163.
28. Bell-Upp P, Robinson AC, Whitten ST, Wheeler EL, Lin J, et al. (2011) Thermodynamic principles for the engineering of pH-driven conformational switches and acid insensitive proteins. Biophys Chem 159: 217-226.
29. Malo GD, Pouwels LJ, Wang M, Weichsel A, Montfort WR, et al. (2007) X-ray structure of Cerulean GFP: a tryptophan-based chromophore useful for fluorescence lifetime imaging. Biochemistry 46: 9865-9873.
30. Vallverdu G, Demachy I, Merola F, Pasquier H, Ridard J, et al. (2010) Relation between pH, structure, and absorption spectrum of Cerulean: A study by molecular dynamics and TD DFT calculations. Proteins 78: 1040-1054.
31. Adam V, Moeyaert B, David CC, Mizuno H, Lelimousin M, et al. (2011) Rational design of photoconvertible and biphotochromic fluorescent proteins for advanced microscopy applications. Chem Biol 18: 1241-1251.
32. Sinnecker D, Voigt P, Hellwig N, Schaefer M, (2005) Reversible photobleaching of enhanced green fluorescent proteins. Biochemistry 44: 7085-7094.
33. Shaner NC, Lin MZ, McKeown MR, Steinbach PA, Hazelwood KL, et al. (2008) Improving the photostability of bright monomeric orange and red fluorescent proteins. Nat Methods 5: 545-551.
34. Ando R, Mizuno H, Miyawaki A, (2004) Regulated fast nucleocytoplasmic shuttling observed by reversible protein highlighting. Science 306: 1370-1373.
35. Bizzarri R, Serresi M, Cardarelli F, Abbruzzetti S, Campanini B, et al. (2010) Single Amino Acid Replacement Makes Aequorea victoria Fluorescent Proteins Reversibly Photoswitchable. J Am Chem Soc 132: 85-95.
36. Merola F, Levy B, Demachy I, Pasquier H (2010) Photophysics and Spectroscopy of Fluorophores in the Green Fluorescent Protein Family. In: Demchenko AP, editor. Advanced Fluorescence Reporters in Chemistry and Biology Vol I Fundamentals and Molecular Design, Springer Series on Fluorescence. Berlin: Springer. 347-383.
37. Meech SR, (2009) Excited state reactions in fluorescent proteins. Chem Soc Rev 38: 2922-2934.
38. Jonasson G, Teuler JM, Vallverdu G, Mérola F, Ridard J, et al. (2011) Excited State Dynamics of the Green Fluorescent Protein at the Nanosecond Timescale. J of Chem Theory Comput 7: 1990-1997.
39. Bae JH, Rubini M, Jung G, Wiegand G, Seifert MHJ, et al. (2003) Expansion of the genetic code enables design of a novel "gold" class of green fluorescent proteins. J Mol Biol 328: 1071-1081.
40. Lelimousin M, Noirclerc-Savoye M, Lazareno-Saez C, Paetzold B, Le Vot S, et al. (2009) Intrinsic Dynamics in ECFP and Cerulean Control Fluorescence Quantum Yield. Biochemistry 48: 10038-10046.
41. Seifert MH, Ksiazek D, Azim MK, Smialowski P, Budisa N, et al. (2002) Slow exchange in the chromophore of a green fluorescent protein variant. J Am Chem Soc 124: 7932-7942.
42. Voliani V, Bizzarri R, Nifosi R, Abbruzzetti S, Grandi E, et al. (2008) Cis-trans photoisomerization of fluorescent-protein chromophores. J Phys Chem B 112: 10714-10722.
43. Abbandonato G, Signore G, Nifosi R, Voliani V, Bizzarri R, et al. (2011) Cis-trans photoisomerization properties of GFP chromophore analogs. Eur Biophys J 40: 1205-1214.
44. Adam V, Lelimousin M, Boehme S, Desfonds G, Nienhaus K, et al. (2008) Structural characterization of IrisFP, an optical highlighter undergoing multiple photo-induced transformations. Proc Natl Acad Sci U S A 105: 18343-18348.
45. Andresen M, Stiel AC, Trowitzsch S, Weber G, Eggeling C, et al. (2007) Structural basis for reversible photoswitching in Dronpa. Proc Natl Acad Sci U S A 104: 13005-13009.
46. Andresen M, Wahl MC, Stiel AC, Grater F, Schafer LV, et al. (2005) Structure and mechanism of the reversible photoswitch of a fluorescent protein. Proc Natl Acad Sci U S A 102: 13070-13074.
47. Henderson JN, Ai HW, Campbell RE, Remington SJ, (2007) Structural basis for reversible photobleaching of a green fluorescent protein homologue. Proc Natl Acad Sci U S A 104: 6672-6677.
48. Luin S, Voliani V, Lanza G, Bizzarri R, Nifosi R, et al. (2009) Raman study of chromophore states in photochromic fluorescent proteins. J Am Chem Soc 131: 96-103.
49. Jung G, Wiehler J, Zumbusch A, (2005) The photophysics of green fluorescent protein: influence of the key amino acids at positions 65, 203, and 222. Biophys J 88: 1932-1947.
50. Kremers GJ, Goedhart J, van den Heuvel DJ, Gerritsen HC, Gadella TWJ, (2007) Improved green and blue fluorescent proteins for expression in bacteria and mammalian cells. Biochemistry 46: 3775-3783.
51. Ai HW, Shaner NC, Cheng Z, Tsien RY, Campbell RE, (2007) Exploration of new chromophore structures leads to the identification of improved blue fluorescent proteins. Biochemistry 46: 5904-5910.
52. Brejc K, Sixma TK, Kitts PA, Kain SR, Tsien RY, et al. (1997) Structural basis for dual excitation and photoisomerization of the Aequorea victoria green fluorescent protein. Proc Natl Acad Sci U S A 94: 2306-2311.
53. Shinobu A, Palm GJ, Schierbeek AJ, Agmon N, (2010) Visualizing proton antenna in a high-resolution green fluorescent protein structure. J Am Chem Soc 132: 11093-11102.
54. van Thor JJ, Zanetti G, Ronayne KL, Towrie M, (2005) Structural events in the photocycle of green fluorescent protein. J Phys Chem B 109: 16099-16108.
55. Yang F, Moss LG, Phillips GN Jr, (1996) The molecular structure of green fluorescent protein. Nat Biotechnol 14: 1246-1251.
56. Elsliger MA, Wachter RM, Hanson GT, Kallio K, Remington SJ, (1999) Structural and spectral response of green fluorescent protein variants to changes in pH. Biochemistry 38: 5296-5301.
57. Jain RK, Ranganathan R, (2004) Local complexity of amino acid interactions in a protein core. Proc Natl Acad Sci U S A 101: 111-116.
58. Ormo M, Cubitt AB, Kallio K, Gross LA, Tsien RY, et al. (1996) Crystal structure of the Aequorea victoria green fluorescent protein. Science 273: 1392-1395.
59. Loening AM, Fenn TD, Gambhir SS, (2007) Crystal structures of the luciferase and green fluorescent protein from Renilla reniformis. J Mol Biol 374: 1017-1028.
60. Yarbrough D, Wachter RM, Kallio K, Matz MV, Remington SJ, (2001) Refined crystal structure of DsRed, a red fluorescent protein from coral, at 2.0-A resolution. Proc Natl Acad Sci U S A 98: 462-467.
61. Henderson JN, Remington SJ, (2005) Crystal structures and mutational analysis of amFP486, a cyan fluorescent protein from Anemonia majano. Proc Natl Acad Sci U S A. 102: 12712-12717.
62. van Thor JJ, Georgiev GY, Towrie M, Sage JT, (2005) Ultrafast and low barrier motions in the photoreactions of the green fluorescent protein. J Biol Chem 280: 33652-33659.