Commonly used FRET fluorophores promote collapse of an otherwise disordered protein
Abstract
The dimensions that unfolded proteins, including intrinsically disordered proteins (IDPs), adopt in the absence of denaturant remain controversial. We developed an analysis procedure for small-angle X-ray scattering (SAXS) profiles and used it to demonstrate that even relatively hydrophobic IDPs remain nearly as expanded in water as they are in high denaturant concentrations. In contrast, as demonstrated here, most fluorescence resonance energy transfer (FRET) measurements have indicated that relatively hydrophobic IDPs contract significantly in the absence of denaturant. Here, we use two independent approaches to further explore this controversy. First, using SAXS we show that fluorophores employed in FRET can contribute to the observed discrepancy. Specifically, we find that addition of Alexa-488 to a normally expanded IDP causes contraction by an additional 15%, a value in reasonable accord with the contraction reported in FRET-based studies. Second, using our simulations and analysis procedure to accurately extract both the radius of gyration (Rg) and end-to-end distance (Ree) from SAXS profiles, we tested the recent suggestion that FRET and SAXS results can be reconciled if the Rg and Ree are “uncoupled” (i.e., no longer simply proportional), in contrast to the case for random walk homopolymers. We find, however, that even for unfolded proteins, thesemore »
- Authors:
-
- Univ. of Chicago, IL (United States)
- Univ. of Notre Dame, IN (United States)
- Univ. of California, Santa Barbara, CA (United States)
- Publication Date:
- Research Org.:
- Argonne National Laboratory (ANL), Argonne, IL (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities Division; National Institutes of Health (NIH); W. M. Keck Foundation; National Science Foundation (NSF)
- OSTI Identifier:
- 1513009
- Grant/Contract Number:
- AC02- 06CH11357; GM055694; GM130122; GRF DGE-1144082; MCB 1516959; NIH 2P41RR008630-18; 9 P41 GM103622-18
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Proceedings of the National Academy of Sciences of the United States of America
- Additional Journal Information:
- Journal Volume: 116; Journal Issue: 18; Journal ID: ISSN 0027-8424
- Publisher:
- National Academy of Sciences
- Country of Publication:
- United States
- Language:
- ENGLISH
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; protein folding; SAXS; IDP; Flory exponent; unfolded state
Citation Formats
Riback, Joshua A., Bowman, Micayla A., Zmyslowski, Adam M., Plaxco, Kevin W., Clark, Patricia L., and Sosnick, Tobin R. Commonly used FRET fluorophores promote collapse of an otherwise disordered protein. United States: N. p., 2019.
Web. doi:10.1073/pnas.1813038116.
Riback, Joshua A., Bowman, Micayla A., Zmyslowski, Adam M., Plaxco, Kevin W., Clark, Patricia L., & Sosnick, Tobin R. Commonly used FRET fluorophores promote collapse of an otherwise disordered protein. United States. https://doi.org/10.1073/pnas.1813038116
Riback, Joshua A., Bowman, Micayla A., Zmyslowski, Adam M., Plaxco, Kevin W., Clark, Patricia L., and Sosnick, Tobin R. Tue .
"Commonly used FRET fluorophores promote collapse of an otherwise disordered protein". United States. https://doi.org/10.1073/pnas.1813038116. https://www.osti.gov/servlets/purl/1513009.
@article{osti_1513009,
title = {Commonly used FRET fluorophores promote collapse of an otherwise disordered protein},
author = {Riback, Joshua A. and Bowman, Micayla A. and Zmyslowski, Adam M. and Plaxco, Kevin W. and Clark, Patricia L. and Sosnick, Tobin R.},
abstractNote = {The dimensions that unfolded proteins, including intrinsically disordered proteins (IDPs), adopt in the absence of denaturant remain controversial. We developed an analysis procedure for small-angle X-ray scattering (SAXS) profiles and used it to demonstrate that even relatively hydrophobic IDPs remain nearly as expanded in water as they are in high denaturant concentrations. In contrast, as demonstrated here, most fluorescence resonance energy transfer (FRET) measurements have indicated that relatively hydrophobic IDPs contract significantly in the absence of denaturant. Here, we use two independent approaches to further explore this controversy. First, using SAXS we show that fluorophores employed in FRET can contribute to the observed discrepancy. Specifically, we find that addition of Alexa-488 to a normally expanded IDP causes contraction by an additional 15%, a value in reasonable accord with the contraction reported in FRET-based studies. Second, using our simulations and analysis procedure to accurately extract both the radius of gyration (Rg) and end-to-end distance (Ree) from SAXS profiles, we tested the recent suggestion that FRET and SAXS results can be reconciled if the Rg and Ree are “uncoupled” (i.e., no longer simply proportional), in contrast to the case for random walk homopolymers. We find, however, that even for unfolded proteins, these two measures of unfolded state dimensions remain proportional. Together, these results suggest that improved analysis procedures and a correction for significant, fluorophore-driven interactions are sufficient to reconcile prior SAXS and FRET studies, thus providing a unified picture of the nature of unfolded polypeptide chains in the absence of denaturant.},
doi = {10.1073/pnas.1813038116},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 18,
volume = 116,
place = {United States},
year = {Tue Apr 16 00:00:00 EDT 2019},
month = {Tue Apr 16 00:00:00 EDT 2019}
}
Web of Science
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