Flow arrest in the plasma membrane

The arrangement of receptors in the plasma membrane strongly affects the ability of a cell to sense its environment both in terms of sensitivity and in terms of spatial resolution. The spatial and temporal arrangement of the receptors is affected in turn by the mechanical properties and the structure of the cell membrane. Here we focus on characterizing the flow of the membrane in response to the motion of a protein embedded in it. We do so by measuring the correlated diffusion of extracellularly tagged transmembrane neurotrophin receptors TrkB and p75 on transfected neuronal cells. In accord with previous reports, we find that the motion of single receptors exhibits transient confinement to sub-micron domains. We confirm predictions based on hydrodynamics of fluid membranes, finding long-range correlations in the motion of the receptors in the plasma membrane. However, we discover that these correlations do not persist for long ranges, as predicted, but decay exponentially, with a typical decay length on the scale of the average confining domain size.

[1]  Akihiro Kusumi,et al.  Rapid hop diffusion of a G-protein-coupled receptor in the plasma membrane as revealed by single-molecule techniques. , 2005, Biophysical journal.

[2]  Andrey G. Cherstvy,et al.  Non-Brownian diffusion in lipid membranes: Experiments and simulations. , 2016, Biochimica et biophysica acta.

[3]  M. Saxton.  Anomalous diffusion due to binding: a Monte Carlo study. , 1996, Biophysical journal.

[4]  M. Garcia-Parajo,et al.  Uncovering homo-and hetero-interactions on the cell membrane using single particle tracking approaches , 2016 .

[5]  In-plane dynamics of membranes with immobile inclusions. , 2011, Physical review letters.

[6]  P. Saffman,et al.  Brownian motion in biological membranes. , 1975, Proceedings of the National Academy of Sciences of the United States of America.

[7]  D. Krapf,et al.  Plasma Membrane is Compartmentalized by a Self-Similar Cortical Actin Meshwork , 2017, Physical review. X.

[8]  D A Weitz,et al.  Two-point microrheology of inhomogeneous soft materials. , 2000, Physical review letters.

[9]  M. Sheetz,et al.  Lateral mobility of integral membrane proteins is increased in spherocytic erythrocytes , 1980, Nature.

[10]  M. Dahan,et al.  Cytoskeleton Regulation of Glycine Receptor Number at Synapses and Diffusion in the Plasma Membrane , 2006, The Journal of Neuroscience.

[11]  M. Kozlov,et al.  Front-to-rear membrane tension gradient in rapidly moving cells. , 2015, Biophysical journal.

[12]  Jung Kyung Kim,et al.  Tracking of quantum dot-labeled CFTR shows near immobilization by C-terminal PDZ interactions. , 2006, Molecular biology of the cell.

[13]  Alexandra Jilkine,et al.  Membrane Tension Maintains Cell Polarity by Confining Signals to the Leading Edge during Neutrophil Migration , 2012, Cell.

[14]  Michael Chein,et al.  The receptor tyrosine kinase TrkB signals without dimerization at the plasma membrane , 2018, Science Signaling.

[15]  H. Stone,et al.  Cell Membranes Resist Flow , 2018, Cell.

[16]  Deirdre R Meldrum,et al.  Measurement of the cell-substrate separation and the projected area of an individual adherent cell using electric cell-substrate impedance sensing. , 2008, Analytical chemistry.

[17]  P. A. Friedman,et al.  NHERF-1 and the Cytoskeleton Regulate the Traffic and Membrane Dynamics of G Protein-coupled Receptors* , 2007, Journal of Biological Chemistry.

[18]  M. Sheetz,et al.  Mechanical feedback between membrane tension and dynamics. , 2012, Trends in cell biology.

[19]  Yael Roichman,et al.  Viscoelastic Response of a Complex Fluid at Intermediate Distances , 2013, 1307.4278.

[20]  Akihiro Kusumi,et al.  Three-dimensional reconstruction of the membrane skeleton at the plasma membrane interface by electron tomography , 2006, The Journal of cell biology.

[21]  C Bechinger,et al.  Imaging of cell/substrate contacts of living cells with surface plasmon resonance microscopy. , 1999, Biophysical journal.

[22]  Akihiro Kusumi,et al.  Paradigm shift of the plasma membrane concept from the two-dimensional continuum fluid to the partitioned fluid: high-speed single-molecule tracking of membrane molecules. , 2005, Annual review of biophysics and biomolecular structure.

[23]  Anomalous hydrodynamic interaction in a quasi-two-dimensional suspension. , 2003, Physical review letters.

[24]  Weiyang Jin,et al.  Cytotoxic T Cells Use Mechanical Force to Potentiate Target Cell Killing , 2016, Cell.

[25]  D A Weitz,et al.  Microrheology probes length scale dependent rheology. , 2006, Physical review letters.

[26]  F. Goñi,et al.  The basic structure and dynamics of cell membranes: an update of the Singer-Nicolson model. , 2014, Biochimica et biophysica acta.

[27]  H. Diamant,et al.  Screened hydrodynamic interaction in a narrow channel. , 2002, Physical review letters.

[28]  G. Stuart,et al.  Direct measurement of specific membrane capacitance in neurons. , 2000, Biophysical journal.

[29]  C. Henderson,et al.  Rapid purification of embryonic rat motoneurons: An in vitro model for studying MND/ALS pathogenesis , 1994, Journal of the Neurological Sciences.

[30]  H. Diamant,et al.  Correlated dynamics of inclusions in a supported membrane. , 2010, Physical review. E, Statistical, nonlinear, and soft matter physics.

[31]  T C Lubensky,et al.  Rheological microscopy: local mechanical properties from microrheology. , 2003, Physical review letters.

[32]  G. Nicolson,et al.  The Fluid-Mosaic Model of Membrane Structure: still relevant to understanding the structure, function and dynamics of biological membranes after more than 40 years. , 2014, Biochimica et biophysica acta.

[33]  B. Heit,et al.  Short-Lived Cages Restrict Protein Diffusion in the Plasma Membrane , 2016, Scientific Reports.

[34]  Hervé Rigneault,et al.  Dynamic molecular confinement in the plasma membrane by microdomains and the cytoskeleton meshwork , 2006, The EMBO journal.

[35]  A. Leier,et al.  Receptor dimer stabilization by hierarchical plasma membrane microcompartments regulates cytokine signaling , 2016, Science Advances.

[36]  Alba Diz-Muñoz,et al.  Use the force: membrane tension as an organizer of cell shape and motility. , 2013, Trends in cell biology.

[37]  Frank Moss,et al.  Experiments and simulations , 2009 .

[38]  A. Gottlob,et al.  Monte-Carlo study , 1998 .

[39]  S. Singer,et al.  The Fluid Mosaic Model of the Structure of Cell Membranes , 1972, Science.

[40]  F. MacKintosh,et al.  Dynamics of viscoelastic membranes. , 2001, Physical review. E, Statistical, nonlinear, and soft matter physics.

[41]  H. Diamant,et al.  Correlated diffusion of membrane proteins and their effect on membrane viscosity. , 2008, Biophysical journal.

[42]  K. Jacobson,et al.  Single-particle tracking: applications to membrane dynamics. , 1997, Annual review of biophysics and biomolecular structure.

[43]  Ralf Metzler,et al.  Single particle tracking in systems showing anomalous diffusion: the role of weak ergodicity breaking. , 2010, Physical chemistry chemical physics : PCCP.

[44]  K. Jacobson,et al.  Revisiting the fluid mosaic model of membranes. , 1995, Science.

[45]  Y. Roichman,et al.  Dynamics in steady state in vitro acto-myosin networks , 2016, Journal of physics. Condensed matter : an Institute of Physics journal.

[46]  Aubrey V. Weigel,et al.  Ergodic and nonergodic processes coexist in the plasma membrane as observed by single-molecule tracking , 2011, Proceedings of the National Academy of Sciences.

[47]  A. Mogilner,et al.  Computational Estimates of Membrane Flow and Tension Gradient in Motile Cells , 2014, PloS one.

[48]  M. Sheetz.  Membrane skeletal dynamics: role in modulation of red cell deformability, mobility of transmembrane proteins, and shape. , 1983, Seminars in hematology.

[49]  D. Neeleman,et al.  A Monte-Carlo study , 1973 .

[50]  M. Huse.  Mechanical forces in the immune system , 2017, Nature Reviews Immunology.

[51]  Pere Roca-Cusachs,et al.  Temporary increase in plasma membrane tension coordinates the activation of exocytosis and contraction during cell spreading , 2011, Proceedings of the National Academy of Sciences.

[52]  Levine,et al.  One- and two-particle microrheology , 2000, Physical review letters.

[53]  D. Engelman.  Membranes are more mosaic than fluid , 2005, Nature.

[54]  Yael Roichman,et al.  Extracting the dynamic correlation length of actin networks from microrheology experiments. , 2014, Soft matter.

[55]  A. Cambi,et al.  Enhanced receptor–clathrin interactions induced by N-glycan–mediated membrane micropatterning , 2014, Proceedings of the National Academy of Sciences.

[56]  A. Verkman,et al.  Crowding effects on diffusion in solutions and cells. , 2008, Annual review of biophysics.

[57]  D. Grier,et al.  Methods of Digital Video Microscopy for Colloidal Studies , 1996 .

[58]  Ken Jacobson,et al.  Nanoclustering as a dominant feature of plasma membrane organization , 2014, Journal of Cell Science.