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An Orange Fluorescent Protein with a Large Stokes Shift for Single-Excitation Multicolor FCCS and FRET Imaging

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    An Orange Fluorescent Protein with a Large Stokes Shift for Single-Excitation Multicolor FCCS and FRET Imaging
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    † Department of Anatomy and Structural Biology and Gruss-Lipper Biophotonics Center, Albert Einstein College of Medicine, 1300 Morris Park Avenue, Bronx, New York 10461, United States
    ‡ Swammerdam Institute for Life Sciences, Section of Molecular Cytology, van Leeuwenhoek Centre for Advanced Microscopy, University of Amsterdam, Science Park 904, NL-1098 XH, Amsterdam, The Netherlands
    [email protected]
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    Cite this: J. Am. Chem. Soc. 2012, 134, 18, 7913–7923
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    https://doi.org/10.1021/ja3018972
    Published April 9, 2012
    Copyright © 2012 American Chemical Society
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    Abstract

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    Multicolor imaging based on genetically encoded fluorescent proteins (FPs) is a powerful approach to study several dynamic processes in a live cell. We report a monomeric orange FP with a large Stokes shift (LSS), called LSSmOrange (excitation/emission at 437/572 nm), which fills up an existing spectral gap between the green-yellow and red LSSFPs. Brightness of LSSmOrange is five-fold larger than that of the brightest red LSSFP and similar to the green-yellow LSSFPs. LSSmOrange allows numerous multicolor applications using a single-excitation wavelength that was not possible before. Using LSSmOrange we developed four-color single-laser fluorescence cross-correlation spectroscopy, solely based on FPs. The quadruple cross-correlation combined with photon counting histogram techniques allowed quantitative single-molecule analysis of particles labeled with four FPs. LSSmOrange was further applied to simultaneously image two Förster resonance energy transfer pairs, one of which is the commonly used CFP-YFP pair, with a single-excitation laser line. The combination of LSSmOrange-mKate2 and CFP-YFP biosensors enabled imaging of apoptotic activity and calcium fluctuations in real time. The LSSmOrange mutagenesis, low-temperature, and isotope effect studies revealed a proton relay for the excited-state proton transfer responsible for the LSS phenotype.

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    Supporting Information

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    Six supporting figures and three supporting tables are available. Alignment of the amino acid sequences of LSSmOrange, mOrange, and EGFP. Biochemical and photobleaching properties of LSSmOrange and other available LSSFPs. Polyacrylamide gel with purified LSSmOrange, mOrange, and LSSmKate2. Fluorescence images of the LSSmOrange fusion constructs in live mammalian cells. Single-wavelength excitation dual FRET with the YC3.6 sensor and control noncleavable caspase-3 biosensor. Alignment of the amino acid sequences of red-shifted LSSFPs. Molecular brightness and cross-talk factors of FPs used in four-color FCCS analysis. Multicolor FCCS analysis of 100 nm beads labeled with four FPs in different ratios. Spectral properties of the LSSmOrange/S148A and LSSmOrange/D165A mutants. This material is available free of charge via Internet at http://pubs.acs.org.

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    Cite this: J. Am. Chem. Soc. 2012, 134, 18, 7913–7923
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