Dynamics in the plasma membrane: how to combine fluidity and order

Cell membranes are fascinating supramolecular aggregates that not only form a barrier between compartments but also harbor many chemical reactions essential to the existence and functioning of a cell. Here, it is proposed to review the molecular dynamics and mosaic organization of the plasma membrane, which are thought to have important functional implications. We will first summarize the basic concepts of Brownian diffusion and lipid domain formation in model membranes and then track the development of ideas and tools in this field, outlining key results obtained on the dynamic processes at work in membrane structure and assembly. We will focus in particular on findings made using fluorescent labeling and imaging procedures to record these dynamic processes. We will also discuss a few examples showing the impact of lateral diffusion on cell signal transduction, and outline some future methodological challenges which must be met before we can answer some of the questions arising in this field of research.

[1]  P. Sluijs,et al.  How proteins move lipids and lipids move proteins , 2001, Nature Reviews Molecular Cell Biology.

[2]  P. Verkade,et al.  Phase coexistence and connectivity in the apical membrane of polarized epithelial cells. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[3]  W. R. Wiley,et al.  Three-Dimensional Vibrational Imaging by Coherent Anti-Stokes Raman Scattering , 1999 .

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

[5]  D. Choquet,et al.  Single metallic nanoparticle imaging for protein detection in cells , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[6]  Tetsuo Yamazaki,et al.  T cell receptor ligation induces the formation of dynamically regulated signaling assemblies , 2002, The Journal of cell biology.

[7]  M. Roth,et al.  Differently anchored influenza hemagglutinin mutants display distinct interaction dynamics with mutual rafts , 2003, The Journal of cell biology.

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

[9]  E Gratton,et al.  Lipid rafts reconstituted in model membranes. , 2001, Biophysical journal.

[10]  M. Sheetz,et al.  Truncation mutants define and locate cytoplasmic barriers to lateral mobility of membrane glycoproteins. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[11]  J. Lippincott-Schwartz,et al.  Secretory protein trafficking and organelle dynamics in living cells. , 2000, Annual review of cell and developmental biology.

[12]  Petra Schwille,et al.  Fluorescence correlation spectroscopy relates rafts in model and native membranes. , 2004, Biophysical journal.

[13]  Hervé Rigneault,et al.  Fluorescence correlation spectroscopy diffusion laws to probe the submicron cell membrane organization. , 2005, Biophysical journal.

[14]  Kai Simons,et al.  Model systems, lipid rafts, and cell membranes. , 2004, Annual review of biophysics and biomolecular structure.

[15]  Watt W. Webb,et al.  Temporally resolved interactions between antigen-stimulated IgE receptors and Lyn kinase on living cells , 2005, The Journal of cell biology.

[16]  M. Edidin,et al.  Micrometer-scale domains in fibroblast plasma membranes , 1987, The Journal of cell biology.

[17]  R D Klausner,et al.  The concept of lipid domains in membranes , 1982, The Journal of cell biology.

[18]  L. Johnston,et al.  Imaging nanometer domains of β-adrenergic receptor complexes on the surface of cardiac myocytes , 2005, Nature chemical biology.

[19]  K. Jacobson,et al.  Detecting microdomains in intact cell membranes. , 2005, Annual review of physical chemistry.

[20]  Enrico Gratton,et al.  Measuring fast dynamics in solutions and cells with a laser scanning microscope. , 2005, Biophysical journal.

[21]  D. Axelrod Total Internal Reflection Fluorescence Microscopy in Cell Biology , 2001, Traffic.

[22]  Eric O Potma,et al.  Direct visualization of lipid phase segregation in single lipid bilayers with coherent anti-Stokes Raman scattering microscopy. , 2005, ChemPhysChem.

[23]  Daniel Choquet,et al.  Direct imaging of lateral movements of AMPA receptors inside synapses , 2003, The EMBO journal.

[24]  Doyun Lee,et al.  Low mobility of phosphatidylinositol 4,5-bisphosphate underlies receptor specificity of Gq-mediated ion channel regulation in atrial myocytes. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[25]  M. Edidin,et al.  The rapid intermixing of cell surface antigens after formation of mouse-human heterokaryons. , 1970, Journal of cell science.

[26]  Shuichi Takayama,et al.  Lateral propagation of EGF signaling after local stimulation is dependent on receptor density. , 2002, Developmental cell.

[27]  Li Li,et al.  Quantitative coherent anti-Stokes Raman scattering imaging of lipid distribution in coexisting domains. , 2005, Biophysical journal.

[28]  Christian Eggeling,et al.  Breaking the diffraction barrier in fluorescence microscopy at low light intensities by using reversibly photoswitchable proteins. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

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

[30]  Santiago Costantino,et al.  Accuracy and dynamic range of spatial image correlation and cross-correlation spectroscopy. , 2005, Biophysical journal.

[31]  Jerome Mertz,et al.  Mechanisms of membrane potential sensing with second-harmonic generation microscopy. , 2003, Journal of biomedical optics.

[32]  M. Saxton,et al.  The spectrin network as a barrier to lateral diffusion in erythrocytes. A percolation analysis. , 1989, Biophysical journal.

[33]  S. Karnik,et al.  G-protein-dependent cell surface dynamics of the human serotonin1A receptor tagged to yellow fluorescent protein. , 2004, Biochemistry.

[34]  Troy Shinbrot,et al.  Noise to order , 2001, Nature.

[35]  M. Edidin,et al.  Vesicle trafficking and cell surface membrane patchiness. , 2001, Biophysical journal.

[36]  Thomas Schmidt,et al.  Single-molecule imaging of the H-ras membrane-anchor reveals domains in the cytoplasmic leaflet of the cell membrane. , 2007, Biophysical journal.

[37]  S. Hell,et al.  Fluorescence microscopy with diffraction resolution barrier broken by stimulated emission. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[38]  Akihiro Kusumi,et al.  Phospholipids undergo hop diffusion in compartmentalized cell membrane , 2002, The Journal of cell biology.

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

[40]  Levi A. Gheber,et al.  A model for membrane patchiness: lateral diffusion in the presence of barriers and vesicle traffic. , 1999, Biophysical journal.

[41]  H. Berg Random Walks in Biology , 2018 .

[42]  N. Socci,et al.  Nonequilibrium raftlike membrane domains under continuous recycling. , 2005, Physical review letters.

[43]  E. London How principles of domain formation in model membranes may explain ambiguities concerning lipid raft formation in cells. , 2005, Biochimica et biophysica acta.

[44]  A. Pokorny,et al.  Thermodynamics of membrane domains. , 2005, Biochimica et biophysica acta.

[45]  S. Singer,et al.  The fluid mosaic model of the structure of cell membranes. , 1972, Science.

[46]  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.

[47]  M. Edidin The state of lipid rafts: from model membranes to cells. , 2003, Annual review of biophysics and biomolecular structure.

[48]  R. S. Hodges,et al.  Lateral mobility of proteins in liquid membranes revisited , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[49]  S. Hell,et al.  Properties of a 4Pi confocal fluorescence microscope , 1992 .

[50]  X. Xie,et al.  Near-field fluorescence microscopy based on two-photon excitation with metal tips , 1999 .

[51]  H. A. Rinia,et al.  Imaging orientational order and lipid density in multilamellar vesicles with multiplex CARS microscopy , 2005, Journal of microscopy.

[52]  G. van Meer,et al.  Cellular lipidomics , 2005, The EMBO journal.

[53]  P. Cuatrecasas Membrane receptors. , 1974, Annual review of biochemistry.

[54]  Nathan C Shaner,et al.  A guide to choosing fluorescent proteins , 2005, Nature Methods.

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

[56]  K. Gaus,et al.  Condensation of the plasma membrane at the site of T lymphocyte activation , 2005, The Journal of cell biology.

[57]  N O Petersen,et al.  Quantitation of membrane receptor distributions by image correlation spectroscopy: concept and application. , 1993, Biophysical journal.

[58]  Levi A. Gheber,et al.  Domains in cell plasma membranes investigated by near-field scanning optical microscopy. , 1998, Biophysical journal.

[59]  M Edidin,et al.  Lateral diffusion of GFP-tagged H2Ld molecules and of GFP-TAP1 reports on the assembly and retention of these molecules in the endoplasmic reticulum. , 1999, Immunity.

[60]  Ronald D. Vale,et al.  Single-Molecule Microscopy Reveals Plasma Membrane Microdomains Created by Protein-Protein Networks that Exclude or Trap Signaling Molecules in T Cells , 2005, Cell.

[61]  Jennifer Lippincott-Schwartz,et al.  Dynamics of putative raft-associated proteins at the cell surface , 2004, The Journal of cell biology.

[62]  P. Schwille,et al.  Fluorescence cross-correlation spectroscopy in living cells , 2006, Nature Methods.

[63]  P J Verveer,et al.  Quantitative imaging of lateral ErbB1 receptor signal propagation in the plasma membrane. , 2000, Science.

[64]  Yan Chen,et al.  Molecular brightness determined from a generalized form of Mandel's Q-parameter. , 2005, Biophysical journal.

[65]  Gerald Kada,et al.  Properties of lipid microdomains in a muscle cell membrane visualized by single molecule microscopy , 2000, The EMBO journal.

[66]  Igor L. Medintz,et al.  Quantum dot bioconjugates for imaging, labelling and sensing , 2005, Nature materials.

[67]  J. Hörber,et al.  Sphingolipid–Cholesterol Rafts Diffuse as Small Entities in the Plasma Membrane of Mammalian Cells , 2000, The Journal of cell biology.

[68]  A Kusumi,et al.  Compartmentalized structure of the plasma membrane for receptor movements as revealed by a nanometer-level motion analysis , 1994, The Journal of cell biology.

[69]  M. Bonn,et al.  Vibrational spectroscopic investigation of the phase diagram of a biomimetic lipid monolayer. , 2003, Physical review letters.

[70]  S. Gambhir,et al.  Quantum Dots for Live Cells, in Vivo Imaging, and Diagnostics , 2005, Science.

[71]  J. Lippincott-Schwartz,et al.  Diffusional Mobility of Golgi Proteins in Membranes of Living Cells , 1996, Science.

[72]  J. Korlach,et al.  Characterization of lipid bilayer phases by confocal microscopy and fluorescence correlation spectroscopy. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[73]  E. Gratton,et al.  Visualizing association of N-ras in lipid microdomains: influence of domain structure and interfacial adsorption. , 2006, Journal of the American Chemical Society.

[74]  M. Vrljic,et al.  Liquid-liquid immiscibility in membranes. , 2003, Annual review of biophysics and biomolecular structure.

[75]  Deborah A. Brown,et al.  Structure and Function of Sphingolipid- and Cholesterol-rich Membrane Rafts* , 2000, The Journal of Biological Chemistry.