Abstract
The membrane skeleton is a specialized part of the cytoskeleton that is in close proximity to the cell membrane with a protein composition and structure that differs from that of the bulk cytoskeleton. The membrane skeleton and various transmembrane proteins bound to it form a mosaic of compartments in the membrane that is responsible for the temporary confinement of membrane proteins and lipids and controls the rate of their repetitive hop movements between these membrane skeleton-based compartments, known as “hop diffusion”, found by observation of single-molecule diffusion. Such hop diffusion has been found to be universal with compartment sizes that range from 30 to 700 nm, depending on the cell type. The part of the membrane skeleton that is directly involved in temporal confinement of membrane molecules has been successfully imaged by raster scanning a single membrane molecule using an optical trap (single molecule scanning optical force imaging). Such compartmentalization enables dynamic spatial regulation of signal transduction in the plasma membrane, by arresting signaling complexes of activated receptor molecules and enlarged, stabilized rafts within a compartment. Furthermore, high concentrations of the membrane skeleton and its associated immobile transmembrane proteins are involved in formation of the cell membrane polarity such as is found across the initial segment between the axon and the cell body in neurons. Argument is advanced that the creation of various membrane domains in the cell membrane must be influenced by the membrane skeleton.
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References
Almeida, P. E, Vaz, W. L. and Thompson, T. E., 1992, Lateral diffusion and percolation in two-phase, two-component lipid bilayers. Topology of the solid-phase domains in-plane and across the lipid bilayer. Biochemistry, 31, 7198–7210.
Bussell, S. J., Koch, D. L. and Hammer, D. A., 1995, Effect of Hydrodynamic Interactions on the Diffusion of Integral Membrane-Proteins — Diffusion in Plasma-Membranes. Biophys J, 68, 1836–1849.
de Brabander, M., Geuens, G., Nuydens, R., Moeremans, M. and Demey, J., 1985, Probing Microtubule-Dependent Intracellular Motility with Nanometer Particle Video Ultramicroscopy (Nanovid Ultramicroscopy). Cytobios, 43, 273–283.
Dodd, T. L., Hammer, D. A., Sangani, A. S. and Koch, D. L., 1995, Numerical Simulations of the Effect of Hydrodynamic Interactions on Diffusivities of Integral Membrane-Proteins. JFluid Mech, 293, 147–180.
East, J. M., Melville, D. and Lee, A. G., 1985, Exchange rates and numbers of annular lipids for the calcium and magnesium ion dependent adenosinetriphosphatase. Biochemistry, 24, 2615–2623.
Fujiwara, T., Ritchie, K., Murakoshi, H., Jacobson, K. and Kusumi, A., 2002, Phospholipids undergo hop diffusion in compartmentalized cell membrane. J Cell Biol, 157, 1071 1081.
Gelles, J., Schnapp, B. J. and Sheetz, M. P., 1988, Tracking Kinesin-Driven Movements with Nanometre-Scale Precision. Nature, 331, 450–453.
lino, R., Koyama, I. and Kusumi, A., 2001, Single molecule imaging of green fluorescent proteins in living cells: E-cadherin forms oligomers on the free cell surface. Biophys J, 80, 2667–2677.
Jacobson, K., Sheets, E. D. and Simson, R., 1995, Revisiting the fluid mosaic model of membranes. Science, 268, 1441–1442.
Kucik, D. F., Elson, E. L. and Sheetz, M. E, 1989, Forward Transport of Glycoproteins on Leading Lamellipodia in Locomoting Cells. Nature, 340, 315–317.
Kusumi, A. and Sako, Y., 1996, Cell surface organization by the membrane skeleton. Curr Opin Cell Biol, 8, 566–574.
Kusumi, A., Sako, Y. and Yamamoto, M., 1993, Confined Lateral Diffusion of Membrane-Receptors as Studied by Single-Particle Tracking (Nanovid Microscopy) — Effects of Calcium-Induced Differentiation in Cultured Epithelial-Cells. Biophys J, 65, 2021–2040.
Murase, K., Fujiwara, T., Iino, R., Murakoshi, H., Ritchie, K. P. and Kusumi, A., 2001, Compartmentalization of the plasma membrane into 40 nm compartments which induce hop diffusion of phospholipids as visualized by single molecule techniques. Mol Biol Cell, 12, 470a.
Nakada, C., Ritchie, K., Fujiwara, T., Yamaguchi, K. and Kusumi, A., 2001, Formation of a diffusion barrier in the plasma membrane of the neuronal initial segment; A single molecule study. Biophys J, 80, 179a.
Powles, J. G., Mallett, M. J. D., Rickayzen, G. and Evans, W. A. B., 1992, Exact Analytic Solutions for Diffusion Impeded by an Infinite Array of Partially Permeable Barriers. Proc. R. Soc. Lond. (A. Maths), 436, 391–403.
Ritchie, K. and Kusumi, A., 2002, Single molecule probe scanning optical force imaging microscope for viewing live cells. JBiol Phys, 28, 619–626.
Ryba, N. J., Horvath, L. I., Watts, A. and Marsh, D., 1987, Molecular exchange at the lipidrhodopsin interface: spin-label electron spin resonance studies of rhodopsindimyristoylphosphatidylcholine recombinants. Biochemistry, 26, 3234–3240.
Sako, Y. and Kusumi, A., 1994, Compartmentalized Structure of the Plasma-Membrane for Receptor Movements as Revealed by a Nanometer-Level Motion Analysis. J Cell Biol, 125, 1251–1264.
Sako, Y., Nagafuchi, A., Tsukita, S., Takeichi, M. and Kusumi, A., 1998, Cytoplasmic regulation of the movement of E-cadherin on the free cell surface as studied by optical tweezers and single particle tracking: Corralling and tethering by the membrane skeleton. JCell Biol, 140, 1227–1240.
Saxton, M. J., 1995, Single-Particle Tracking — Effects of Corrals. Biophys J, 69, 389–398. Sheetz, M. P., Turney, S., Qian, H. and Elson, E. L., 1989, Nanometer-Level Analysis
Demonstrates That Lipid Flow Does Not Drive Membrane Glycoprotein Movements. Nature,340 284–288.
Singer, S. J. and Nicolson, G. L., 1972, Fluid Mosaic Model of Structure of Cell-Membranes. Science, 175, 720–731.
Sperotto, M. M. and Mouritsen, O. G., 1991, Monte Carlo simulation studies of lipid order parameter profiles near integral membrane proteins. Biophys J, 59, 261–270.
Suzuki, K., Sanematsu, F., Fujiwara, T., Edidin, M. and Kusumi, A., 2001, A GPI-anchored membrane protein, CD59, frequently visits/forms rafts in signaling: A single molecule study. Biophys J, 80, 252a.
Tomishige, M., Sako, Y. and Kusumi, A., 1998, Regulation mechanism of the lateral diffusion of band 3 in erythrocyte membranes by the membrane skeleton. J Cell Biol, 142, 989–1000.
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Ritchie, K., Kusumi, A. (2004). Role of the Membrane Skeleton in Creation of Microdomains. In: Quinn, P.J. (eds) Membrane Dynamics and Domains. Subcellular Biochemistry, vol 37. Springer, Boston, MA. https://doi.org/10.1007/978-1-4757-5806-1_7
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DOI: https://doi.org/10.1007/978-1-4757-5806-1_7
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