Rapid hop diffusion of a G-protein-coupled receptor in the plasma membrane as revealed by single-molecule techniques

Biophysical Journal

Volumn 88, Issue 5, 2005, Pages 3659-3680

  Suzuki, Kenichi ^a   Ritchie, Ken ^a   Kajikawa, Eriko ^a   Fujiwara, Takahiro ^a   Kusumi, Akihiro ^a  

^a NAGOYA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

G PROTEIN COUPLED RECEPTOR; MU OPIATE RECEPTOR; TRANSFERRIN RECEPTOR;

ACTIN FILAMENT; ANIMAL CELL; ARTICLE; CELL COMPARTMENTALIZATION; CYTOSKELETON; DIFFUSION; FLUORESCENCE; MEMBRANE COMPONENT; MEMBRANE TRANSPORT; MOLECULAR IMAGING; NONHUMAN; PROTEIN TRANSPORT; VIDEORECORDING;

EID: 17844389341     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.104.048538     Document Type: Article

References (79)

1. Bray, D. 1998. Signaling complexes: biophysical constraints on intracellular communication. Annu. Rev. Biophys. Biomol. Struct. 27: 59-75.
2. Bussell, S. J., D. L. Koch, and D. A. Hammer. 1995. Effect of hydrodynamic interactions on the diffusion of integral membrane proteins: tracer diffusion in organelle and reconstituted membranes. Biophys. J. 68:1828-1835.
3. Chang, C-H., H. Takeuchi, T. Ito, K. Machida, and S. Ohnishi. 1981. Lateral mobility of erythrocyte membrane proteins studied by the fluorescence photobleaching recovery technique. J. Biochem. 90:997-1004.
4. Daumas, F., H. Mazarguil, C. Millot, A. Lopez, and L. Salome. 2002. Probing functionalized gold colloids for signal particle tracking experiments. Biochem. Biophys. Res. Commun. 295:610-615.
5. Daumas, F., N. Destainville, C. Millot, A. Lopez, D. Dean, and L. Salome. 2003. Confined diffusion without fences of a G-protein-coupled receptor as revealed by single particle tracking. Biophys. J. 84:356-366.
6. De Mey, J. 1983. Colloidal gold probes in immunocytochemistry. In Immunocytochemistry (Practical Applications in Pathology and Biology). J. M. Polak and S. van Noorden, editors. Wright PSG, Bristol, UK. 83-112.
7. Derrick, J. P., and D. B. Wigley. 1994. The third IgG-binding domain from Streptococcal protein G. J. Mol. Biol. 243:906-918.
8. Dietrich, C., B. Yang, T. Fujiwara, A. Kusumi, and K. Jacobson. 2002. Relationship of lipid rafts to transient confinement zones detected by single particle tracking. Biophys. J. 82:274-284.
9. Dodd, T. L., D. A. Hammer, A. S. Sangani, and D. L. Koch. 1995. Numerical simulations of the effect of hydrodynamic interactions on diffusivities of integral membrane proteins. J. Fluid Mech. 293: 147-180.
10. Edidin, M., S. C. Kuo, and M. P. Sheetz. 1991. Lateral movements of membrane glycoproteins restricted by dynamic cytoplasmic barriers. Science. 254:1379-1382.
11. Edidin, M., M. C. Zuniga, and M. P. Sheetz. 1994. Truncation mutants define and locate cytoplasmic barriers to lateral mobility of membrane glycoproteins. Proc. Natl. Acad. Sci. USA. 91:3378-3382.
12. Edidin, M. 2003. Lipids on the frontier: a century of cell-membrane bilayers. Nat. Rev. Mol. Cell Biol. 4:414-418.
13. Feder, T. J., I. Brust-Mascher, J. P. Slattery, B. Baird, and W. W. Webb. 1996. Constrained diffusion or immobile fraction on cell surfaces: a new interpretation. Biophys. J. 70:2767-2773.
14. Felsenfeld, D., D. Choquet, and M. P. Sheetz. 1996. Ligand binding regulates the directed movement of beta 1 integrins on fibroblasts. Nature. 383:438-440.
15. Fujiwara, T., K. Ritchie, H. Murakoshi, K. Jacobson, and A. Kusumi. 2002. Phospholipids undergo hop diffusion in compartmentalized cell membrane. J. Cell Biol. 157:1071-1081.
16. Gelles, J., B. J. Schnapp, and M. P. Sheetz. 1988. Tracking kinesin-driven movements with nanometer-scale precision. Nature. 331:450-453.
17. Gittes, F., B. Mickey, J. Nettleton, and J. Howard. 1993. Flexural rigidity of microtubules and actin filaments measured from thermal fluctuations in shape. J. Cell. Biol. 120:923-934.
18. Holowka, D., and B. Baird. 1996. Antigen-mediated IGE receptor aggregation and signaling: a window on cell surface structure and dynamics. Annu. Rev. Biophys. Biomol. Struct. 25:79-112.
19. Horvat, R. D., S. Nelson, C. M. Clay, B. G. Barisas, and D. A. Roess. 1999. Intrinsically fluorescent luteinizing hormone receptor demonstrates hormone-driven aggregation. Biochem. Biophys. Res. Commun. 255:382-385.
20. Iino, R., I. Koyama, and A. Kusumi. 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.
21. Jacobson, K., E. D. Sheets, and R. Simson. 1995. Revisiting the fluid mosaic model of membranes. Science. 268:1441-1442.
22. Kenworthy, A. K., B. J. Nichols, C. L. Remmert, G. M. Hendrix, M. Kumar, J. Zimmerberg, and J. Lippincott-Schwartz. 2004. Dynamics of putative raft-associated proteins at the cell surface. J. Cell Biol. 165:735-746.
23. Kusumi, A., Y. Sako, and M. Yamamoto. 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.
24. Kusumi, A., and Y. Sako. 1996. Cell surface organization by the membrane skeleton. Curr. Opin. Cell Biol. 8:566-574.
25. Kusumi, A., I. Koyama-Honda, and K. Suzuki. 2004. Molecular dynamics and interactions for creation of stimulation-induced stabilized rafts from small unstable steady-state rafts. Traffic. 5:213-230.
26. Kusumi, A., C. Nakada, K. Ritchie, K. Murase, K. Suzuki, H. Murakoshi, R. S. Kasai, J. Kondo, and T. Fujiwara. 2005. 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. Annu. Rev. Biophys. Biomol. Struct. In press.
27. Ladha, S., P. S. James, D. C. Clark, E. A. Howes, and R. Jones. 1997. Lateral mobility of plasma membrane lipids in bull spermatozoa: heterogeneity between surface domains and rigidification following cell death. J. Cell Sci. 110:1041-1050.
28. Laporte, S. A., R. H. Oakley, J. Zhang, J. A. Holt, S. S. Ferguson, M. G. Caron, and L. S. Barak. 1999. The β2-adrenergic receptor/βarrestin complex recruits the clathrin adaptor AP-2 during endocytosis. Proc. Natl. Acad. Sci. USA. 96:3712-3717.
29. Lee, G. M., F. Zhang, A. Ishihara, C. L. McNeil, and K. Jacobson. 1993. Unconfined lateral diffusion and an estimate of pericellular matrix viscosity revealed by measuring the mobility of gold-tagged lipids. J. Cell Biol. 120:25-35.
30. Leunissen, J. L. M., and J. R. D. Mey. 1989. Preparation of gold probes. In Immuno-Gold Labeling in Cell Biology. A. J. Verkleij and J. L. M. Leunissen, editors. CRC Press, Boca Raton, FL. 3-16.
31. Lindblom, G., L. B. Johansson, and G. Arvidson. 1981. Effect of cholesterol in membranes. Pulsed nuclear magnetic resonance measurements of lipid lateral diffusion. Biochemistry. 20:2204-2207.
32. Liu, X., and G. H. Pollack. 2002. Mechanics of F-actin characterized with microfabricated cantilevers. Biophys. J. 83:2705-2715.
33. Lommerse, P. H., G. A. Blab, L. Congnet, G. S. Harms, B. E. Snaar-Jagalska, H. P. Spaink, and T. Schmidt. 2004. Single-molecule imaging of the H-ras membrane-anchor reveals domains in the cytoplasmic leaflet of the cell membrane. Biophys. J. 86:609-616.
34. Murakoshi, H., R. Iino, T. Kobayashi, T. Fujiwara, C. Ohshima, A. Yoshimura, and A. Kusumi. 2004. Single molecule imaging analysis of Ras activation in living cells. Proc. Natl. Acad. Sci. USA. 101:7317-7322.
35. Murase, K., T. Fujiwara, Y. Uemura, K. Suzuki, R. Iino, H. Yamashita, M. Saito, H. Murakoshi, K. Ritchie, and A. Kusumi. 2004. Ultrafine membrane compartments for molecular diffusion as revealed by single molecule techniques. Biophys. J. 86:4075-4093.
36. Nagle, J. F. 1992. Looking tail kinetics in biophysics? Biophys. J. 63:366-370.
37. Nakada, C., K. Ritchie, Y. Oba, M. Nakamura, Y. Hotta, R. Iino, R. S. Kasai, K. Yamaguchi, T. Fujiwara, and A. Kusumi. 2003. Accumulation of anchored proteins forms membrane diffusion barriers during neuronal polarization. Nat. Cell Biol. 5:626-632.
38. Nelson, S., R. D. Horvat, J. Malvey, D. A. Roess, B. G. Barisas, and C. M. Clay. 1999. Characterization of an intrinsically fluorescent gonadotropin-releasing hormone receptor and effects of ligand binding on receptor lateral diffusion. Endocrinology. 140:950-957.
39. Powles, J. G., M. J. D. Mallett, G. Rickayzen, and W. A. B. Evans. 1992. Exact analytic solutions for diffusion impeded by an infinite array of partially permeable barriers. Proc. R. Soc. Lond. A. 436:391-403.
40. Perosa, F., G. Luccarelli, M. Neri, and F. Dammacco. 1997. The Fab region of IgG2 human myeloma proteins does not bear the streptococcal protein G-specific determinant. J. Immunol. Methods. 203:153-155.
41. Peters, R., and R. J. Cherry. 1982. Lateral and rotational diffusion of bacteriorhodopsin in lipid bilayers: Experimental test of the Saffman-Delbrück equations. Proc. Natl. Acad. Sci. USA. 79:4317-4321.
42. Pralle, A., P. Keller, E. L. Florin, K. Simons, and J. K. Horber. 2000. Sphingolipid-cholesterol rafts diffuse as small entities in the plasma membrane of mammalian cells. J. Cell Biol. 148:997-1008.
43. Qian, H., M. P. Sheetz, and E. L. Elson. 1991. Single particle tracking Analysis of diffusion and flow in two-dimensional systems. Biophys. J. 60:910-921.
44. Saffman, P. G., and M. Delbruck. 1975. Brownian motion in biological membranes. Proc. Natl. Acad. Sci. USA. 72:3111-3113.
45. Sako, Y., and A. Kusumi. 1994. Compartmentalized structure of the plasma membrane for receptor movements as revealed by a nanometer-level motion analysis. J. Cell Biol. 125:1251-1264.
46. Sako, Y., and A. Kusumi. 1995. Barriers for lateral diffusion of transferrin receptor in the plasma membrane as characterized by receptor dragging by laser tweezers: fence versus tether. J. Cell Biol. 129:1559-1574.
47. Sako, Y., A. Nagafuchi, S. Tsukita, M. Takeichi, and A. Kusumi. 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. J. Cell Biol. 140: 1227-1240.
48. Sako, Y., S. Mizoguchi, and T. Yanagida. 2001. Single molecule imaging of EGFR signalling on the surface of living cells. Nat. Cell Biol. 2:168-172.
49. Santini, F., I. Gaidarov, and J. H. Keen. 2002. G protein-coupled receptor/ arrestin3 modulation of the endocytic machinery. J. Cell Biol. 156:665-676.
50. Saxton, M. J. 1989a. Lateral diffusion in an archipelago. Distance dependence of the diffusion coefficient. Biophys. J. 56:615-622.
51. Saxton, M. J. 1989b. The spectrin network as a barrier to lateral diffusion in erythrocytes. A percolation analysis. Biophys. J. 55:21-28.
52. Saxton, M. J. 1990. The membrane skeleton of erythrocytes. A percolation model. Biophys. J. 57:1167-1177.
53. Saxton, M. J. 1994. Anomalous diffusion due to obstacles: a Monte Carlo study. Biophys. J. 66:394-401.
54. Saxton, M. J. 1996. Anomalous diffusion due to binding: a Monte Carlo study. Biophys. J. 70:1250-1262.
55. Saxton, M. J. 1997. Anomalous diffusion due to binding: The distribution of diffusion coefficients. Biophys. J. 72:1744-1753.
56. Saxton, M. J. 2001. Anomalous subdiffusion in fluorescence photobleaching recovery: a Monte Carlo study. Biophys. J. 81:2226-2240.
57. Saxton, M. J., and K. Jacobson. 1997. Single-particle tracking: applications to membrane dynamics. Annu. Rev. Biophys. Biomol. Struct. 26:373-399.
58. Schiweck, W., B. Buxbaum, C. Schatzlein, H. G. Neiss, and A. Skerra. 1997. Sequence analysis and bacterial production of the anti-c-myc antibody 9E10: the V(H) domain has an extended CDR-H3 and exhibits unusual solubility. FEBS Lett. 414:33-38.
59. Schulz, R., A. Wehmeyer, and K. Schulz. 2002. Opioid receptor types selectively cointernalize with G protein-coupled receptor kinases 2 and 3. J. Pharmacol. Exp. Ther. 300:376-384.
60. Schütz, G. J., G. Kada, V. P. Pastushenko, and H. Schindler. 2000. Properties of lipid microdomains in a muscle cell membrane visualized by single molecule microscopy. EMBO J. 19:892-901.
61. Sheets, E. D., G. M. Lee, R. Simson, and K. Jacobson. 1997. Transient confinement of a glycosylphosphatidylinositol-anchored protein in the plasma membrane. Biochemistry. 36:12449-12458.
62. Sheetz, M. P. 1983. Membrane skeleton dynamics: role in modulation of red cell deformability, mobility of transmembrane proteins, and shape. Semin. Hematol. 20:175-188.
63. Sheetz, M. P., S. Turney, H. Qian, and E. L. Elson. 1989. Nanometre-level analysis demonstrates that lipid flow does not drive membrane glycoprotein movements. Nature. 340:284-288.
64. Sheetz, M. P. 1993. Glycoprotein motility and dynamic domains in fluid plasma membranes. Annu. Rev. Biophys. Biomol. Struct. 22:417-431.
65. Shvartsman, D. E., M. Kotler, R. D. Tall, M. G. Roth, and Y. I. Henis. 2003. Differently anchored influenza hemagglutinin mutants display distinct interaction dynamics with mutual rafts. J. Cell Biol. 163:879-888.
66. Simson, R., E. D. Sheets, and K. Jacobson. 1995. Detection of temporary lateral confinement of membrane proteins using single-particle tracking analysis. Biophys. J. 69:989-993.
67. Singer, S. J., and G. L. Nicolson. 1972. The fluid mosaic model of the structure of cell membranes. Science. 175:720-731.
68. Spector, I., N. R. Shochet, Y. Kashman, and A. Groweiss. 1983. Latrunculins: noyel marine toxins that disrupt microfilament organization in cultured cells. Science. 219:493-495.
69. Steinmetz, M. O., K. N. Goldie, and U. Aebi. 1997. A correlation analysis of actin filament assembly, structure, and dynamics. J. Cell Biol. 138:559-574.
70. Suzuki, K., and M. P. Sheetz. 2001. Binding of cross-linked glycosylphosphatidylinositol-anchored proteins to discrete actin-associated sites and cholesterol-dependent domains. Biophys. J. 81:2181-2189.
71. Swaisgood, M., and M. Schindler. 1989. Lateral diffusion of lectin receptors in fibroblast membranes as a function of cell shape. Exp. Cell Res. 180:515-528.
72. Tomishige, M., Y. Sako, and A. Kusumi. 1998. Regulation mechanism of the lateral diffusion of band 3 in erythrocyte membranes by the membrane skeleton. J. Cell Biol. 142:989-1000.
73. Tsuji, A., K. Kawasaki, S.-I. Ohnishi, H. Merkle, and A. Kusumi. 1988. Regulation of band 3 mobilities in erythrocyte ghost membranes by protein association and cytoskeletal meshwork. Biochemistry. 27:7447-7452.
74. Tsuji, A., and S.-I. Ohnishi. 1986. Restriction of the lateral motion of band 3 in the erythrocyte membrane by the cytoskeletal network: dependence on spectrin association state. Biochemistry. 25:6133-6139.
75. Vaz, W. L. C., M. Criado, V. M. C. Madeir, G. Schoellman, and T. M. Jovin. 1982. Size dependence of the translational diffusion of large integral membrane proteins in liquid-crystalline phase lipid bilayers. A study using fluorescence recovery after photobleaching. Biochemistry. 21:5608-5612.
76. Vrljic, M., S. Y. Nishimura, S. Brasselet, W. E. Moemer, and H. M. McConnell. 2002. Translational diffusion of individual class II MHC membrane proteins in cells. Biophys. J. 83:2681-2692.
77. Vrljic, M., S. Y. Nishimura, W. E. Moemer, and H. M. McConnell. 2005. Cholesterol depletion suppresses the translational diffusion of class II major histocompatibility complex proteins in the plasma membrane. Biophys. J. 88:334-347.
78. Yanagida, T., M. Nakase, K. Nishiyama, and F. Oosawa. 1984. Direct observation of motion of single F-actin filaments in the presence of myosin. Nature. 307:58-60.
79. Young, S. H., J. H. Walsh, E. Rozengurt, and L. W. Slice. 2001. Agonist-dependent immobilization of chimeric bombesin/GRP receptors: dependence on c-Src activity and dissociation from internalization. Exp. Cell Res. 267:37-44.