The Impact of Heterogeneity and Dark Acceptor States on FRET: Implications for Using Fluorescent Protein Donors and Acceptors

PLoS ONE

Volumn 7, Issue 11, 2012, Pages

  Vogel, Steven S ^a   Nguyen, Tuan A ^a   van der Meer, B Wieb ^b   Blank, Paul S ^c  

^a NATIONAL INSTITUTE ON ALCOHOL ABUSE AND ALCOHOLISM   (United States)

^b WESTERN KENTUCKY UNIVERSITY   (United States)

^c EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GREEN FLUORESCENT PROTEIN;

ARTICLE; BINDING SITE; CONTROLLED STUDY; DONOR; ENERGY TRANSFER; FLUORESCENCE RESONANCE ENERGY TRANSFER; KERNEL METHOD; MONTE CARLO METHOD; PROBABILITY; PROTEIN AGGREGATION; PROTEIN EXPRESSION; PROTEIN POLYMORPHISM; PROTEIN TRANSPORT;

COMPUTER SIMULATION; DARKNESS; FLUORESCENCE RESONANCE ENERGY TRANSFER; GREEN FLUORESCENT PROTEINS; MONTE CARLO METHOD;

EID: 84869021496     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0049593     Document Type: Article

References (54)

1. Clegg RM (2009) Forster resonance energy transfer-FRET what it is, why do it, and how it's done. In: Gadella TWJ, editor. FRET and FLIM Techniques. 1 ed. Amsterdam: Elsevier. 1-57.
2. Vogel SS, Thaler C, Koushik SV, (2006) Fanciful FRET. Sci STKE 2006: re2.
3. Jares-Erijman EA, Jovin TM, (2006) Imaging molecular interactions in living cells by FRET microscopy. Curr Opin Chem Biol 10: 409-416.
4. Sekar RB, Periasamy A, (2003) Fluorescence resonance energy transfer (FRET) microscopy imaging of live cell protein localizations. J Cell Biol 160: 629-633.
5. Piston DW, Kremers GJ, (2007) Fluorescent protein FRET: the good, the bad and the ugly. Trends Biochem Sci 32: 407-414.
6. Förster T (1951) Fluoreszenz Organischer Verbindungen. Göttingen: Vandenhoeck & Ruprecht.
7. Stryer L, Haugland RP, (1967) Energy transfer: a spectroscopic ruler. Proc Natl Acad Sci U S A 58: 719-726.
8. Hoppe A, Christensen K, Swanson JA, (2002) Fluorescence resonance energy transfer-based stoichiometry in living cells. Biophys J 83: 3652-3664.
9. Chalfie M, Tu Y, Euskirchen G, Ward WW, Prasher DC, (1994) Green fluorescent protein as a marker for gene expression. Science 263: 802-805.
10. 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.
11. Koushik SV, Blank PS, Vogel SS, (2009) Anomalous surplus energy transfer observed with multiple FRET acceptors. PLoS One 4: e8031.
12. Ha T, (2001) Single-molecule fluorescence resonance energy transfer. Methods 25: 78-86.
13. Padilla-Parra S, Auduge N, Lalucque H, Mevel JC, Coppey-Moisan M, et al. (2009) Quantitative comparison of different fluorescent protein couples for fast FRET-FLIM acquisition. Biophys J 97: 2368-2376.
14. Koushik SV, Chen H, Thaler C, Puhl HL, 3rd, Vogel SS (2006) Cerulean, Venus, and VenusY67C FRET reference standards. Biophys J 91: L99-L101.
15. Thaler C, Koushik SV, Blank PS, Vogel SS, (2005) Quantitative multiphoton spectral imaging and its use for measuring resonance energy transfer. Biophys J 89: 2736-2749.
16. Sun Y, Day RN, Periasamy A, (2011) Investigating protein-protein interactions in living cells using fluorescence lifetime imaging microscopy. Nat Protocols 6: 1324-1340.
17. Rizzo MA, Springer GH, Granada B, Piston DW, (2004) An improved cyan fluorescent protein variant useful for FRET. Nat Biotechnol 22: 445-449.
18. Heikal A, Hess ST, Webb WW, (2001) Multiphoton molecular spectroscopy and excited state dynamics of enhanced green fluorescent protein (EGFP): acid-base specificity. Chemical Physics 274: 37-55.
19. Volkmer A, Subramaniam V, Birch DJ, Jovin TM, (2000) One- and two-photon excited fluorescence lifetimes and anisotropy decays of green fluorescent proteins. Biophys J 78: 1589-1598.
20. Knox RS, van Amerongen H, (2002) Refractive index dependence of the Förster resonance excitatoion transfer rate. J Phys Chem B 106: 5289-5293.
21. Sarkar P, Koushik SV, Vogel SS, Gryczynski I, Gryczynski Z, (2009) Photophysical properties of Cerulean and Venus fluorescent proteins. J Biomed Opt 14: 034047.
22. Liu Y, Kim HR, Heikal AA, (2006) Structural basis of fluorescence fluctuation dynamics of green fluorescent proteins in acidic environments. J Phys Chem B 110: 24138-24146.
23. Schwille P, Kummer S, Heikal AA, Moerner WE, Webb WW, (2000) Fluorescence correlation spectroscopy reveals fast optical excitation-driven intramolecular dynamics of yellow fluorescent proteins. Proc Natl Acad Sci U S A 97: 151-156.
24. Dickson RM, Cubitt AB, Tsien RY, Moerner WE, (1997) On/off blinking and switching behaviour of single molecules of green fluorescent protein. Nature 388: 355-358.
25. Dale RE, Eisinger J, Blumberg WE, (1979) The orientational freedom of molecular probes. The orientation factor in intramolecular energy transfer. Biophys J 26: 161-193.
26. van der Meer BW, (2002) Kappa-squared: from nuisance to new sense. J Biotechnol 82: 181-196.
27. Eisinger J, Dale RE, (1974) Letter: interpretation of intramolecular energy transfer experiments. J Mol Biol 84: 643-647.
28. Dale RE, Eisinger J, (1976) Intramolecular energy transfer and molecular conformation. Proc Natl Acad Sci U S A 73: 271-273.
29. Haas E, Katchalski-Katzir E, Steinberg IZ, (1978) Effect of the orientation of donor and acceptor on the probability of energy transfer involving electronic transitions of mixed polarization. Biochemistry 17: 5064-5070.
30. Steinberg IZ, Haas E, Katchalski-Katzir E (1983) Long-rangeTransfer of Electronic Excitation Energy. In: Cundall RB, Dale RE, editors. Time-Resolved Fluorescence Spectroscopy in Biochemistry and Biology. New York: Plenum Press. 411-450.
31. Pham E, Chiang J, Li I, Shum W, Truong K, (2007) A computational tool for designing FRET protein biosensors by rigid-body sampling of their conformational space. Structure 15: 515-523.
32. Chiang JJ, Truong K, (2006) Computational modeling of a new fluorescent biosensor for caspase proteolytic activity improves dynamic range. IEEE Trans Nanobioscience 5: 41-45.
33. Hunt J, Keeble AH, Dale RE, Corbett MK, Beavil RL, et al. (2012) A fluorescent biosensor reveals conformational changes in human immunoglobulin E Fc: implications for mechanisms of receptor binding, inhibition and allergen recognition. J Biol Chem.
34. Rizzo MA, Springer G, Segawa K, Zipfel WR, Piston DW, (2006) Optimization of pairings and detection conditions for measurement of FRET between cyan and yellow fluorescent proteins. Microsc Microanal 12: 238-254.
35. Heikal AA, Hess ST, Baird GS, Tsien RY, Webb WW, (2000) Molecular spectroscopy and dynamics of intrinsically fluorescent proteins: coral red (dsRed) and yellow (Citrine). Proc Natl Acad Sci U S A 97: 11996-12001.
36. Tompa H, Englert A, (1979) The frequency distribution of the orientation factor of dipole-dipole interaction. Biophys Chem 9: 211-214.
37. Gautier I, Tramier M, Durieux C, Coppey J, Pansu RB, et al. (2001) Homo-FRET microscopy in living cells to measure monomer-dimer transition of GFP-tagged proteins. Biophys J 80: 3000-3008.
38. Tramier M, Piolot T, Gautier I, Mignotte V, Coppey J, et al. (2003) Homo-FRET versus hetero-FRET to probe homodimers in living cells. Methods Enzymol 360: 580-597.
39. Thaler C, Koushik SV, Puhl HL, 3rd, Blank PS, Vogel SS (2009) Structural rearrangement of CaMKIIalpha catalytic domains encodes activation. Proc Natl Acad Sci U S A 106: 6369-6374.
40. Vogel SS, Thaler C, Blank PS, Koushik SV (2010) Time Resolved Fluorescence Anisotropy. In: Periasamy A, Clegg RM, editors. FLIM Microscopy in Biology and Medicine. Boca Raton: Taylor & Francis. 245-290.
41. Suhling K, Davis D, Phillips D, (2002) The Influence of Solvent Viscosity on the Fluorescence Decay and Time-Resolved Anisotropy of Green Fluorescent Protein. J Fluores 12: 91-95.
42. Yuan H, Xia T, Schuler B, Orrit M, (2011) Temperature-cycle single-molecule FRET microscopy on polyprolines. Phys Chem Chem Phys 13: 1762-1769.
43. 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.
44. Rekas A, Alattia JR, Nagai T, Miyawaki A, Ikura M, (2002) Crystal structure of venus, a yellow fluorescent protein with improved maturation and reduced environmental sensitivity. J Biol Chem 277: 50573-50578.
45. Cantor CR, Schimmel PR (1980) Biophysical Chemistry Part II: Techniques for the study of biological structure and function. San Francisco: W.H. Freeman & Co. 846 p.
46. Gryczynski I, Wiczk W, Johnson ML, Cheung HC, Wang CK, et al. (1988) Resolution of end-to-end distance distributions of flexible molecules using quenching-induced variations of the Forster distance for fluorescence energy transfer. Biophys J 54: 577-586.
47. Steinberg IZ, (1971) Long-range nonradiative transfer of electronic excitation energy in proteins and polypeptides. Annu Rev Biochem 40: 83-114.
48. VanBeek DB, Zwier MC, Shorb JM, Krueger BP, (2007) Fretting about FRET: correlation between kappa and R. Biophys J. 92: 4168-4178.
49. Yasuda R, Harvey CD, Zhong H, Sobczyk A, van Aelst L, et al. (2006) Supersensitive Ras activation in dendrites and spines revealed by two-photon fluorescence lifetime imaging. Nat Neurosci 9: 283-291.
50. Wlodarczyk J, Woehler A, Kobe F, Ponimaskin E, Zeug A, et al. (2008) Analysis of FRET signals in the presence of free donors and acceptors. Biophys J 94: 986-1000.
51. Ganesan S, Ameer-Beg SM, Ng TT, Vojnovic B, Wouters FS, (2006) A dark yellow fluorescent protein (YFP)-based Resonance Energy-Accepting Chromoprotein (REACh) for Forster resonance energy transfer with GFP. Proc Natl Acad Sci U S A 103: 4089-4094.
52. Chen Y, Johnson J, Macdonald P, Wu B, Mueller JD, (2010) Observing protein interactions and their stoichiometry in living cells by brightness analysis of fluorescence fluctuation experiments. Methods Enzymol 472: 345-363.
53. Nguyen TA, Sarkar P, Veetil JV, Koushik SV, Vogel SS, (2012) Fluorescence Polarization and Fluctuation Analysis Monitors Subunit Proximity, Stoichiometry, and Protein Complex Hydrodynamics. PLoS One 7: e38209.
54. Gell C, Brockwell D, Smith A (2006) Handbook of Single Molecule Fluorescence Spectroscopy. Oxford, New York: Oxford University Press. 262 p.