The ins and outs of membrane bending by intrinsically disordered proteins

Membrane curvature is essential to diverse cellular functions. While classically attributed to structured domains, recent work illustrates that intrinsically disordered proteins are also potent drivers of membrane bending. Specifically, repulsive interactions among disordered domains drive convex bending, while attractive interactions, which lead to liquid-like condensates, drive concave bending. How might disordered domains that contain both repulsive and attractive domains impact curvature? Here we examine chimeras that combine attractive and repulsive interactions. When the attractive domain was closer to the membrane, its condensation amplified steric pressure among repulsive domains, leading to convex curvature. In contrast, when the repulsive domain was closer to the membrane, attractive interactions dominated, resulting in concave curvature. Further, a transition from convex to concave curvature occurred with increasing ionic strength, which reduced repulsion while enhancing condensation. In agreement with a simple mechanical model, these results illustrate a set of design rules for membrane bending by disordered proteins.

[1]  V. Uversky,et al.  Phase separation of FG-nucleoporins in nuclear pore complexes. , 2022, Biochimica et biophysica acta. Molecular cell research.

[2]  P. Rangamani,et al.  Mem3DG: Modeling membrane mechanochemical dynamics in 3D using discrete differential geometry , 2021, Biophysical Reports.

[3]  Nicolas L. Fawzi,et al.  Membrane bending by protein phase separation , 2020, Proceedings of the National Academy of Sciences.

[4]  R. Pappu,et al.  Valence and patterning of aromatic residues determine the phase behavior of prion-like domains , 2020, Science.

[5]  E. Lafer,et al.  Molecular Mechanisms of Membrane Curvature Sensing by a Disordered Protein. , 2019, Journal of the American Chemical Society.

[6]  L. Kourkoutis,et al.  Physical Principles of Membrane Shape Regulation by the Glycocalyx , 2019, Cell.

[7]  Vladimir N. Uversky,et al.  Intrinsically Disordered Proteins and Their “Mysterious” (Meta)Physics , 2019, Front. Phys..

[8]  D. Thirumalai,et al.  Synergy between intrinsically disordered domains and structured proteins amplifies membrane curvature sensing , 2018, Nature Communications.

[9]  J. Stachowiak,et al.  Structure Versus Stochasticity-The Role of Molecular Crowding and Intrinsic Disorder in Membrane Fission. , 2018, Journal of molecular biology.

[10]  Matthew C. Good,et al.  Controllable protein phase separation and modular recruitment to form responsive membraneless organelles , 2018, Nature Communications.

[11]  Nicolas L. Fawzi,et al.  Protein Phase Separation: A New Phase in Cell Biology. , 2018, Trends in cell biology.

[12]  Anne-Florence Bitbol,et al.  pH sensing by lipids in membranes: The fundamentals of pH-driven migration, polarization and deformations of lipid bilayer assemblies. , 2018, Biochimica et biophysica acta. Biomembranes.

[13]  E. Lafer,et al.  BAR scaffolds drive membrane fission by crowding disordered domains , 2018, bioRxiv.

[14]  Evan Evans,et al.  Mechanics and Thermodynamics of Biomembranes , 2017 .

[15]  W. Weissenhorn,et al.  The Matrix protein M1 from influenza C virus induces tubular membrane invaginations in an in vitro cell membrane model , 2017, Scientific Reports.

[16]  J. Gallop,et al.  Membrane curvature in cell biology: An integration of molecular mechanisms , 2016, The Journal of cell biology.

[17]  Peter Tompa,et al.  Polymer physics of intracellular phase transitions , 2015, Nature Physics.

[18]  Nicolas L. Fawzi,et al.  Residue-by-Residue View of In Vitro FUS Granules that Bind the C-Terminal Domain of RNA Polymerase II. , 2015, Molecular cell.

[19]  A. Quigley,et al.  The second virial coefficient as a predictor of protein aggregation propensity: A self-interaction chromatography study , 2015, European journal of pharmaceutics and biopharmaceutics : official journal of Arbeitsgemeinschaft fur Pharmazeutische Verfahrenstechnik e.V.

[20]  M. Sherman,et al.  Intrinsically disordered proteins drive membrane curvature , 2015, Nature Communications.

[21]  C. Brangwynne,et al.  The disordered P granule protein LAF-1 drives phase separation into droplets with tunable viscosity and dynamics , 2015, Proceedings of the National Academy of Sciences.

[22]  G. Bachand,et al.  Designing lipids for selective partitioning into liquid ordered membrane domains. , 2015, Soft matter.

[23]  E. Boucrot,et al.  Membrane curvature at a glance , 2015, Journal of Cell Science.

[24]  V. Haucke,et al.  BAR Domain Scaffolds in Dynamin-Mediated Membrane Fission , 2014, Cell.

[25]  Christopher J. Ryan,et al.  Membrane bending by protein–protein crowding , 2012, Nature Cell Biology.

[26]  A. Dunker,et al.  Orderly order in protein intrinsic disorder distribution: disorder in 3500 proteomes from viruses and the three domains of life , 2012, Journal of biomolecular structure & dynamics.

[27]  K. Weninger,et al.  Beyond the random coil: stochastic conformational switching in intrinsically disordered proteins. , 2011, Structure.

[28]  M. Niepel,et al.  The nuclear pore complex: bridging nuclear transport and gene regulation , 2010, Nature Reviews Molecular Cell Biology.

[29]  G. Drin,et al.  Amphipathic helices and membrane curvature , 2010, FEBS letters.

[30]  D. Sasaki,et al.  Steric confinement of proteins on lipid membranes can drive curvature and tubulation , 2010, Proceedings of the National Academy of Sciences.

[31]  B. Różycki,et al.  Membrane Budding , 2010, Cell.

[32]  O. Borisov,et al.  Curved polymer and polyelectrolyte brushes beyond the Daoud-Cotton model , 2006, The European physical journal. E, Soft matter.

[33]  Michael M. Kozlov,et al.  How proteins produce cellular membrane curvature , 2006, Nature Reviews Molecular Cell Biology.

[34]  Harvey T. McMahon,et al.  Membrane curvature and mechanisms of dynamic cell membrane remodelling , 2005, Nature.

[35]  P. Evans,et al.  Adaptors for clathrin coats: structure and function. , 2004, Annual review of cell and developmental biology.

[36]  V. Uversky,et al.  Disorder in the nuclear pore complex: The FG repeat regions of nucleoporins are natively unfolded , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[37]  I. Derényi,et al.  Formation and interaction of membrane tubes. , 2002, Physical review letters.

[38]  O. Borisov,et al.  Effect of Salt on Self-Assembly in Charged Block Copolymer Micelles , 2002 .

[39]  P. Gómez-Puertas,et al.  Influenza Virus Matrix Protein Is the Major Driving Force in Virus Budding , 2000, Journal of Virology.

[40]  B. Chait,et al.  The Yeast Nuclear Pore Complex: Composition, Architecture, and Transport Mechanism , 2000 .

[41]  A. Lenhoff,et al.  Molecular origins of osmotic second virial coefficients of proteins. , 1998, Biophysical journal.

[42]  O. Borisov,et al.  Polyelectrolytes Grafted to Curved Surfaces , 1996 .

[43]  G. J. Fleer,et al.  Charged polymeric brushes: structure and scaling relations. , 1994 .

[44]  E. Evans,et al.  Bending resistance and chemically induced moments in membrane bilayers. , 1974, Biophysical journal.

[45]  P. Canham The minimum energy of bending as a possible explanation of the biconcave shape of the human red blood cell. , 1970, Journal of theoretical biology.

[46]  O. Kratky,et al.  Röntgenuntersuchung gelöster Fadenmoleküle , 1949 .

[47]  H. Kowarzyk Structure and Function. , 1910, Nature.