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Quantification of Membrane Protein-Detergent Complex Interactions

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Department of Physics, Syracuse University, 201 Physics Building, Syracuse, New York 13244-1130, United States
Structural Biology, Biochemistry, and Biophysics Program, Syracuse University, 111 College Place, Syracuse, New York 13244-4100, United States
§ Jiangsu Key Laboratory for Design and Manufacture of Micro-Nano Biomedical Instruments and School of Mechanical Engineering, Southeast University, Nanjing 210096, China
Department of Physics, University of Illinois at Urbana−Champaign, Urbana, Illinois 61801, United States
Department of Chemistry and Biochemistry, University of Delaware, 136 Brown Laboratory, Newark, Delaware 19716, United States
# Department of Biochemistry and Molecular Biology, State University of New York Upstate Medical University, 4249 Weiskotten Hall, 766 Irving Av., Syracuse, New York 13210, United States
Department of Chemistry, University of Massachusetts, 820 LGRT, 710 North Pleasant Street, Amherst, Massachusetts 01003-9336, United States
Department of Biomedical and Chemical Engineering, Syracuse University, 329 Link Hall, Syracuse, New York 13244, United States
*Phone: 315-443-8078; Fax: 315-443-9103; E-mail: [email protected]
Cite this: J. Phys. Chem. B 2017, 121, 44, 10228–10241
Publication Date (Web):October 16, 2017
https://doi.org/10.1021/acs.jpcb.7b08045
Copyright © 2017 American Chemical Society

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    Abstract

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    Although fundamentally significant in structural, chemical, and membrane biology, the interfacial protein-detergent complex (PDC) interactions have been modestly examined because of the complicated behavior of both detergents and membrane proteins in aqueous phase. Membrane proteins are prone to unproductive aggregation resulting from poor detergent solvation, but the participating forces in this phenomenon remain ambiguous. Here, we show that using rational membrane protein design, targeted chemical modification, and steady-state fluorescence polarization spectroscopy, the detergent desolvation of membrane proteins can be quantitatively evaluated. We demonstrate that depleting the detergent in the sample well produced a two-state transition of membrane proteins between a fully detergent-solvated state and a detergent-desolvated state, the nature of which depended on the interfacial PDC interactions. Using a panel of six membrane proteins of varying hydrophobic topography, structural fingerprint, and charge distribution on the solvent-accessible surface, we provide direct experimental evidence for the contributions of the electrostatic and hydrophobic interactions to the protein solvation properties. Moreover, all-atom molecular dynamics simulations report the major contribution of the hydrophobic forces exerted at the PDC interface. This semiquantitative approach might be extended in the future to include studies of the interfacial PDC interactions of other challenging membrane protein systems of unknown structure. This would have practical importance in protein extraction, solubilization, stabilization, and crystallization.

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    The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.jpcb.7b08045.

    • Characterization of selenoproteins prior to and following labeling with Texas Red; example of steady-state FP traces illustrating no time-dependent alterations in the anisotropy readout at detergent concentrations much greater than the CMC; example of steady-state FP traces showing no time-dependent alterations in the anisotropy readout after 24 h; hydrodynamic changes of the proteomicelles during the transition of detergent desolvation; table that summarizes the recorded minima and maxima of the anisotropy with maltoside-containing detergents; summary of the fitting results of the two-state, concentration-dependent anisotropy curves acquired with maltoside-containing detergents; time-dependent changes in the FP anisotropy acquired with CHAPS; time-dependent FP anisotropy acquired with LD; table that summarizes the recorded minima and maxima of the anisotropy readout with DM at various pH values; summary of the fitting results of the two-state desolvation curves acquired with DM at various pH values; MD simulations of DDM molecules binding to β-barrel proteins; differential affinity of DDM molecules to residues of β-barrels; DDM binding versus residue type; biophysical properties of the selenoproteins; table that summarizes the recorded minima and maxima of the anisotropy readout with the α-helical membrane proteins solubilized in DDM; and summary of the fitting results of the two-state, concentration-dependent anisotropy curves acquired with α-helical transmembrane proteins (PDF)

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