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Depletion Interactions Modulate the Binding Between Disordered Proteins in Crowded Environments

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Depletion Interactions Modulate the Binding Between Disordered Proteins in Crowded Environments Washington University School of Medicine Digital Commons@Becker Open Access Publications 2020 Depletion interactions modulate the binding between disordered proteins in crowded environments Franziska Zosel Andrea Soranno Karin J. Buholzer Daniel Nettels Benjamin Schuler Follow this and additional works at: https://digitalcommons.wustl.edu/open_access_pubs Depletion interactions modulate the binding between disordered proteins in crowded environments Franziska Zosela,1,2, Andrea Sorannoa,b,2, Karin J. Buholzera, Daniel Nettelsa, and Benjamin Schulera,c,2 aDepartment of Biochemistry, University of Zurich, 8057 Zurich, Switzerland; bDepartment of Biochemistry and Molecular Biophysics, Washington University in St. Louis, St. Louis, MO 63130; and cDepartment of Physics, University of Zurich, 8057 Zurich, Switzerland Edited by Martin Gruebele, University of Illinois at Urbana–Champaign, Urbana, IL, and approved April 7, 2020 (received for review December 14, 2019) Intrinsically disordered proteins (IDPs) abound in cellular regulation. effects on all these observables can be rationalized quantitatively Their interactions are often transitory and highly sensitive to salt within the framework of depletion interactions, the effective attractive concentration and posttranslational modifications. However, little force that arises between particles in a solution of solutes that are is known about the effect of macromolecular crowding on the preferentially excluded from the vicinity of the particles (37–39). interactions of IDPs with their cellular targets. Here, we investigate The depletion effects that cause the interaction between two the influence of crowding on the interaction between two IDPs that proteins in a crowded solution have the same entropic origin as fold upon binding, with polyethylene glycol as a crowding agent. those leading to the conformational collapse of IDPs in the Single-molecule spectroscopy allows us to quantify the effects of presence of crowding agents (20, 40). It is worth noting that our crowding on a comprehensive set of observables simultaneously: use of terminology, especially regarding “depletion interactions” the equilibrium stability of the complex, the association and dissoci- and “crowding,” is influenced by different schools of thought that ation kinetics, and the microviscosity, which governs translational have traditionally been separated, but the underlying quantitative diffusion. We show that a quantitative and coherent explanation of concepts are equivalent (40). The coherent framework we use is all observables is possible within the framework of depletion inter- enabled by theoretical developments, some of them quite recent, actions if the polymeric nature of IDPs and crowders is incorporated that allow us to combine the influence of polymer physics (19) based on recent theoretical developments. The resulting integrated with the enhanced attractive interactions between the proteins in a framework can also rationalize important functional consequences, crowded solution (39). for example, that the interaction between the two IDPs is less en- hanced by crowding than expected for folded proteins of the Results same size. Single-Molecule Spectroscopy Enables a Comprehensive Investigation of Crowding Effects. We investigate the interaction between the single-molecule spectroscopy | macromolecular crowding | intrinsically intrinsically disordered activation domain of the steroid recep- disordered proteins tor coactivator 3 (ACTR) and the molten-globule-like nuclear coactivator binding domain of CBP/p300 (NCBD), a paradigm of ntrinsic disorder is a widespread phenomenon among eukary- coupled folding and binding (41, 42). Upon binding to each other, Iotic proteins, manifesting itself in unstructured segments of larger proteins or proteins that are entirely disordered under Significance physiological conditions (1). Such intrinsically disordered pro- teins (IDPs) are particularly prevalent in the context of signaling The molecular environment in a biological cell is much more and regulation (2), where they form complex interaction net- crowded than the conditions commonly used in biochemical works (3), often involving many partners (4). IDPs lack the stable and biophysical experiments in vitro. It is therefore important tertiary structure familiar from folded proteins—instead, they to understand how the conformations and interactions of biological sample a heterogeneous ensemble of conformations on time- macromolecules are affected by such crowding. Addressing these scales from nanoseconds to seconds (5–8). Their disorder and questions quantitatively, however, has been challenging owing the lack of pronounced minima in their conformational free to a lack of sufficiently detailed experimental information and energy landscapes makes the ensembles particularly sensitive to theoretical concepts suitable for describing crowding, especially external factors such as ligands (9), posttranslational modifica- when polymeric crowding agents and biomolecules are in- tions (10), and salt concentration (11), which can even induce volved. Here, we use the combination of extensive single- the folding of IDPs. The cellular milieu, densely packed with molecule experiments with established and recent theoretical globular and polymeric macromolecules (12–14), is thus also concepts to investigate the interaction between two intrinsically expected to influence the conformational distributions and disordered proteins. We observe pronounced effects of crowd- dynamics of IDPs. Experimental evidence, simulations, and ing on their interactions and provide a quantitative framework theory suggest that the effects of such macromolecular crowd- for rationalizing these effects. ing are moderate but detectable, including the compaction and local structure formation of unfolded proteins and IDPs (8, 11, Author contributions: F.Z., A.S., and B.S. designed research; F.Z., A.S., K.J.B., and D.N. – performed research; D.N. contributed new reagents/analytic tools; F.Z., A.S., K.J.B., and 15 31), which may have important effects on their function. D.N. analyzed data; and F.Z., A.S., and B.S. wrote the paper. However, a quantitative understanding of the effects of crowding The authors declare no competing interest. on IDPs is largely lacking. This article is a PNAS Direct Submission. The influence of macromolecular crowding on the conforma- This open access article is distributed under Creative Commons Attribution-NonCommercial- tional properties of individual IDPs and on the binding interactions NoDerivatives License 4.0 (CC BY-NC-ND). of folded proteins has been studied (32–35), but little is known 1Present address: Department of Biophysics and Injectable Formulation 2, Novo Nordisk about the effect of crowding on the binding process involving IDPs, A/S, 2760 Måløv, Denmark. which is essential for many of their functions (9, 36). Here, we aim 2To whom correspondence may be addressed. Email: [email protected], to fill this gap with a systematic investigation of the effects of the [email protected], or [email protected]. size and concentration of polymeric crowding agents on the in- This article contains supporting information online at https://www.pnas.org/lookup/suppl/ teraction between two IDPs by simultaneously monitoring com- doi:10.1073/pnas.1921617117/-/DCSupplemental. plex stability, kinetics, and translational diffusion. We find that the First published June 2, 2020. 13480–13489 | PNAS | June 16, 2020 | vol. 117 | no. 24 www.pnas.org/cgi/doi/10.1073/pnas.1921617117 Downloaded at SERIALS DEPARTMENT, WASHINGTON UNIVERSITY on August 27, 2020 A B No PEG C No PEG 10 K 200 D 5 0 3 0 41% PEG 400 41% PEG 400 τ 200 on 10 k τ ACTR on 5 0 0 k Photons/50ms 13.5% PEG 6000 13.5% PEG 6000 ff Number of events/10 o 200 15 NCBD 10 5 0 0 0 5 10 15 20 0.0 0.2 0.4 0.6 0.8 1.0 Time (s) Apparent transfer efficiency DE 1 k k 2.0 No PEG on off τ 1.8 D 41% PEG 400 0.1 13.5% PEG 6000 1.6 0.01 G(τ ) 1.4 O H (normalized) 1.2 H O Number of events 0.001 P 1.0 0.0 0.5 1.0 2.0 2.0 3.0 0.0 0.5 1.0 2.0 2.0 3.0 3.0 -6 -5 -4 -3 -2 -1 τoff (s) τon (s) log τ/s Fig. 1. Probing IDP interactions and crowding in single-molecule experiments. (A) Schematic representation of acceptor-labeled NCBD (orange, Protein Data Bank ID code 2KKJ) binding to surface-immobilized donor-labeled ACTR (blue, Protein DataBank ID code 1KBH) in the presence of polymeric crowders (gray). (B) Examples of single-molecule time traces recorded at different PEG concentrations (first 20 s each, binning: 50 ms, donor signal: magenta, acceptor signal: BIOPHYSICS AND COMPUTATIONAL BIOLOGY light blue; not corrected for background, quantum yields, detection efficiencies, etc.). The most likely state trajectory identified by the Viterbi algorithm is depicted in gray. Note that the quantitative trajectory analysis is based on 1-ms binning to avoid averaging over fast events (Materials and Methods). From top to bottom: buffer without PEG; 41% PEG 400; 13.5% PEG 6000. (C) Histograms of the apparent transfer efficiency (from time traces binned at 20 ms) can be used to quantify the equilibrium dissociation constant, KD. Apparent efficiencies at 13.5% PEG 6000 are shifted to higher values because of the increased background in the acceptor channel owing to residual nonspecific surface adsorption of NCBD. (D) Normalized dwell-time distributions (conditions and color code as in B) from the state trajectories of 30 to 40 ACTR molecules each (gray: 9,300 transitions, green: 3,475 transitions, orange: 12,192
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