Barriers for lateral diffusion of transferrin receptor in the plasma membrane as characterized by receptor dragging by laser tweezers: fence versus tether

doi:10.1083/jcb.129.6.1559

This Article

	Full Text (PDF, 2409K)
	Alert me when this article is cited
	Citation Map

Services

	Email this article
	Similar articles in this journal
	Similar articles in PubMed
	Alert me to new content in the JCB
	Download to citation manager

Citing Articles

	Citing Articles via HighWire
	Citing Articles via CrossRef
	Citing Articles via Google Scholar

Google Scholar

	Articles by Sako, Y.
	Articles by Kusumi, A.
	Search for Related Content

PubMed

	PubMed Citation
	Articles by Sako, Y.
	Articles by Kusumi, A.

Social Bookmarking

	What's this?

ARTICLES

Barriers for lateral diffusion of transferrin receptor in the plasma membrane as characterized by receptor dragging by laser tweezers: fence versus tether

Y Sako and A Kusumi
Department of Life Sciences, Graduate School of Arts and Sciences, University of Tokyo, Japan.

Our previous results indicated that the plasma membrane of cultured normal rat kidney fibroblastic cell is compartmentalized for diffusion of receptor molecules, and that long-range diffusion is the result of successive intercompartmental jumps (Sako, Y. and Kusumi, A. 1994. J. Cell Biol. 125:1251-1264). In the present study, we characterized the properties of intercompartmental boundaries by tagging transferrin receptor (TR) with either 210-nm-phi latex or 40-nm-phi colloidal gold particles, and by dragging the particle-TR complexes laterally along the plasma membrane using laser tweezers. Approximately 90% of the TR- particle complexes showed confined-type diffusion with a microscopic diffusion coefficient (Dmicro) of approximately 10(-9) cm2/s and could be dragged past the intercompartmental boundaries in their path by laser tweezers at a trapping force of 0.25 pN for gold-tagged TR and 0.8 pN for latex-tagged TR. At lower dragging forces between 0.05 and 0.1 pN, particle-TR complexes tended to escape from the laser trap at the boundaries, and such escape occurred in both the forward and backward directions of dragging. The average distance dragged was half of the confined distance of TR, which further indicates that particle- TR complexes escape at the compartment boundaries. Since variation in the particle size (40 and 210 nm, the particles are on the extracellular surface of the plasma membrane) hardly affects the diffusion rate and behavior of the particle-TR complexes at the compartment boundaries, and since treatment with cytochalasin D or vinblastin affects the movements of TR (Sako and Kusumi as cited above), argument has been advanced that the boundaries are present in the cytoplasmic domain. Rebound of the particle-TR complexes when they escape from the laser tweezers at the compartment boundaries suggests that the boundaries are elastic structures. These results are consistent with the proposal that the compartment boundaries consist of membrane skeleton or a membrane-associated part of the cytoskeleton (membrane skeleton fence model). Approximately 10% of TR exhibited slower diffusion (Dmicro approximately 10(-10)-10(-11) cm2/s) and binding to elastic structures.
Add to CiteULike CiteULike Add to Complore Complore Add to Connotea Connotea Add to Del.icio.us Del.icio.us Add to Digg Digg Facebook Add to Reddit Reddit Add to Technorati Technorati Twitter What's this?

This article has been cited by other articles:

Simek, J., Churko, J., Shao, Q., Laird, D. W. (2009). Cx43 has distinct mobility within plasma-membrane domains, indicative of progressive formation of gap-junction plaques. J. Cell Sci. 122: 554-562 [Abstract] [Full Text]
Tamkun, M. M., O'Connell, K. M. S., Rolig, A. S. (2007). A cytoskeletal-based perimeter fence selectively corrals a sub-population of cell surface Kv2.1 channels. J. Cell Sci. 120: 2413-2423 [Abstract] [Full Text]
Lee, S., Mandic, J., Van Vliet, K. J. (2007). From the Cover: Chemomechanical mapping of ligand-receptor binding kinetics on cells. Proc. Natl. Acad. Sci. USA 104: 9609-9614 [Abstract] [Full Text]
Chen, Y., Thelin, W. R., Yang, B., Milgram, S. L., Jacobson, K. (2006). Transient anchorage of cross-linked glycosyl-phosphatidylinositol-anchored proteins depends on cholesterol, Src family kinases, caveolin, and phosphoinositides. JCB 175: 169-178 [Abstract] [Full Text]
Morone, N., Fujiwara, T., Murase, K., Kasai, R. S., Ike, H., Yuasa, S., Usukura, J., Kusumi, A. (2006). Three-dimensional reconstruction of the membrane skeleton at the plasma membrane interface by electron tomography. JCB 174: 851-862 [Abstract] [Full Text]
Weisswange, I., Bretschneider, T., Anderson, K. I. (2005). The leading edge is a lipid diffusion barrier. J. Cell Sci. 118: 4375-4380 [Abstract] [Full Text]
Thi, M. M., Tarbell, J. M., Weinbaum, S., Spray, D. C. (2004). The role of the glycocalyx in reorganization of the actin cytoskeleton under fluid shear stress: A "bumper-car" model. Proc. Natl. Acad. Sci. USA 101: 16483-16488 [Abstract] [Full Text]
Cezanne, L., Lecat, S., Lagane, B., Millot, C., Vollmer, J.-Y., Matthes, H., Galzi, J.-L., Lopez, A. (2004). Dynamic Confinement of NK2 Receptors in the Plasma Membrane: IMPROVED FRAP ANALYSIS AND BIOLOGICAL RELEVANCE. J. Biol. Chem. 279: 45057-45067 [Abstract] [Full Text]
Williams, J. A., MacIver, B., Klipfell, E. A., Thomas, G. H. (2004). The C-terminal domain of Drosophila {beta}Heavy-spectrin exhibits autonomous membrane association and modulates membrane area. J. Cell Sci. 117: 771-782 [Abstract] [Full Text]
Vereb, G., Szollosi, J., Matko, J., Nagy, P., Farkas, T., Vigh, L., Matyus, L., Waldmann, T. A., Damjanovich, S. (2003). Dynamic, yet structured: The cell membrane three decades after the Singer-Nicolson model. Proc. Natl. Acad. Sci. USA 100: 8053-8058 [Abstract] [Full Text]
Weinbaum, S., Zhang, X., Han, Y., Vink, H., Cowin, S. C. (2003). Inaugural Article: Mechanotransduction and flow across the endothelial glycocalyx. Proc. Natl. Acad. Sci. USA 100: 7988-7995 [Abstract] [Full Text]
Fujiwara, T., Ritchie, K., Murakoshi, H., Jacobson, K., Kusumi, A. (2002). Phospholipids undergo hop diffusion in compartmentalized cell membrane. JCB 157: 1071-1082 [Abstract] [Full Text]
Serge, A., Fourgeaud, L., Hemar, A., Choquet, D. (2002). Receptor Activation and Homer Differentially Control the Lateral Mobility of Metabotropic Glutamate Receptor 5 in the Neuronal Membrane. J. Neurosci. 22: 3910-3920 [Abstract] [Full Text]
Varadhachary, A. S., Edidin, M., Hanlon, A. M., Peter, M. E., Krammer, P. H., Salgame, P. (2001). Phosphatidylinositol 3'-Kinase Blocks CD95 Aggregation and Caspase-8 Cleavage at the Death-Inducing Signaling Complex by Modulating Lateral Diffusion of CD95. J. Immunol. 166: 6564-6569 [Abstract] [Full Text]
Kucik, D. F., O'Toole, T. E., Zheleznyak, A., Busettini, D. K., Brown, E. J. (2001). Activation-enhanced {alpha}IIb{beta}3-Integrin-Cytoskeleton Interactions Outside of Focal Contacts Require the {alpha}-Subunit. Mol. Biol. Cell 12: 1509-1518 [Abstract] [Full Text]
Toomre, D., Steyer, J. A., Keller, P., Almers, W., Simons, K. (2000). Fusion of Constitutive Membrane Traffic with the Cell Surface Observed by Evanescent Wave Microscopy. JCB 149: 33-40 [Abstract] [Full Text]
Pralle, A., Keller, P., Florin, E.-L., Simons, K., Horber, J.K.H. (2000). Sphingolipid-Cholesterol Rafts Diffuse as Small Entities in the Plasma Membrane of Mammalian Cells. JCB 148: 997-1008 [Abstract] [Full Text]
Mordue, D. G., Desai, N., Dustin, M., Sibley, L. D. (1999). Invasion by Toxoplasma gondii Establishes a Moving Junction That Selectively Excludes Host Cell Plasma Membrane Proteins on the Basis of Their Membrane Anchoring. JEM 190: 1783-1792 [Abstract] [Full Text]
Tomishige, M., Kusumi, A. (1999). Compartmentalization of the Erythrocyte Membrane by the Membrane Skeleton: Intercompartmental Hop Diffusion of Band 3. Mol. Biol. Cell 10: 2475-2479 [Full Text]
Edwards, S. W., Limbird, L. E. (1999). Role for the Third Intracellular Loop in Cell Surface Stabilization of the alpha 2A-Adrenergic Receptor. J. Biol. Chem. 274: 16331-16336 [Abstract] [Full Text]
Tomishige, M., Sako, Y., Kusumi, A. (1998). Regulation Mechanism of the Lateral Diffusion of Band 3 in Erythrocyte Membranes by the Membrane Skeleton. JCB 142: 989-1000 [Abstract] [Full Text]
Sako, Y., Nagafuchi, A., Tsukita, S., Takeichi, M., 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. JCB 140: 1227-1240 [Abstract] [Full Text]
West, A. E., Neve, R. L., Buckley, K. M. (1997). Identification of a Somatodendritic Targeting Signal in the Cytoplasmic Domain of the Transferrin Receptor. J. Neurosci. 17: 6038-6047 [Abstract] [Full Text]
Subtil, A, Dautry-Varsat, A (1997). Microtubule depolymerization inhibits clathrin coated-pit internalization in non-adherent cell lines while interleukin 2 endocytosis is not affected. J. Cell Sci. 110: 2441-2447 [Abstract]
Wilson, K., Morrison, I., Smith, P., Fernandez, N, Cherry, R. (1996). Single particle tracking of cell-surface HLA-DR molecules using R-phycoerythrin labeled monoclonal antibodies and fluorescence digital imaging. J. Cell Sci. 109: 2101-2109 [Abstract]