Both MHC class II and its GPI-anchored form undergo hop diffusion as observed by single-molecule tracking

Biophysical Journal

Volumn 95, Issue 1, 2008, Pages 435-450

  Umemura, Yasuhiro M ^a   Vrljic, Marija ^b   Nishimura, Stefanie Y ^b   Fujiwara, Takahiro K ^a   Suzuki, Kenichi G N ^a   Kusumi, Akihiro ^a  

^a KYOTO UNIVERSITY   (Japan)

^b STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOSYLPHOSPHATIDYLINOSITOL; HLA ANTIGEN CLASS 2;

ANIMAL; ARTICLE; CHEMISTRY; CHO CELL; CRICETULUS; DIFFUSION; FLUORESCENCE MICROSCOPY; GENETIC PROCEDURES; HAMSTER; METABOLISM; METHODOLOGY;

ANIMALS; CHO CELLS; CRICETINAE; CRICETULUS; DIFFUSION; GLYCOSYLPHOSPHATIDYLINOSITOLS; HISTOCOMPATIBILITY ANTIGENS CLASS II; MICROSCOPY, FLUORESCENCE; MOLECULAR PROBE TECHNIQUES;

EID: 46749128544     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1529/biophysj.107.123018     Document Type: Article

References (72)

1. Vrljic, M., S. Y. Nishimura, S. Brasselet, W. E. Moerner, and H. M. McConnell. 2002. Translational diffusion of individual class II MHC membrane proteins in cells. Biophys. J. 83:2681-2692.
2. Vrljic, M., S. Y. Nishimura, W. E. Moerner, 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.
3. Nishimura, S. Y., M. Vrljic, L. O. Klein, H. M. McConnell, and W. E. Moerner. 2006. Cholesterol depletion induces solid-like regions in the plasma membrane. Biophys. J. 90:927-938.
4. Kusumi, A., and Y. Sako. 1996. Cell surface organization by the membrane skeleton. Curr. Opin. Cell Biol. 8:566-574.
5. 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.
6. Murase, K., T. Fujiwara, Y. Umemura, 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.
7. Sheetz, M. P. 1983. Membrane skeletal dynamics: role in modulation of red cell deformability, mobility of transmembrane proteins, and shape. Semin. Hematol. 20:175-188.
8. Tsuji, A., K. Kawasaki, S. 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.
9. Tsuji, A., and S. 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.
10. Saxton, M. J. 1989. The spectrin network as a barrier to lateral diffusion in erythrocytes. A percolation analysis. Biophys. J. 55:21-28.
11. Saxton, M. J. 1990. The membrane skeleton of erythrocytes. A percolation model. Biophys. J. 57:1167-1177.
12. 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.
13. 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.
14. 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.
15. Jacobson, K., E. D. Sheets, and R. Simson. 1995. Revisiting the fluid mosaic model of membranes. Science. 268:1441-1442.
16. 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.
17. Saxton, M. J., and K. Jacobson. 1997. Single-particle tracking: applications to membrane dynamics. Annu. Rev. Biophys. Biomol. Struct. 26:373-399.
18. 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.
19. Suzuki, K., K. Ritchie, E. Kajikawa, T. Fujiwara, and A. Kusumi. 2005. Rapid hop diffusion of a G-protein-coupled receptor in the plasma membrane as revealed by single-molecule techniques. Biophys. J. 88:3659-3680.
20. 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.
21. 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. 34:351-378.
22. Dodd, T. L., D. A. Hammer, A. S. Sangani, and D. L. Koch. 1995. Numerical simulations of the effect of hydrodynamic interactions on the diffusivities of integral membrane proteins. J. Fluid Mech. 293:147-180.
23. Bussell, S. J., D. L. Koch, and D. A. Hammer. 1995. Effect of hydrodynamic interactions on the diffusion of integral membrane proteins: diffusion in plasma membranes. Biophys. J. 68:1836-1849.
24. Almeida, P. F., W. L. Vaz, and T. E. Thompson. 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.
25. Sperotto, M. M., and O. G. Mouritsen. 1991. Monte Carlo simulation studies of lipid order parameter profiles near integral membrane proteins. Biophys. J. 59:261-270.
26. 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.
27. Morone, N., T. Fujiwara, K. Murase, R. S. Kasai, H. Ike, S. Yuasa, J. Usukura, and A. Kusumi. 2006. Three-dimensional reconstruction of the membrane skeleton at the plasma membrane interface by electron tomography. J. Cell Biol. 174:851-862.
28. Gaus, K., E. Gratton, E. P. Kable, A. S. Jones, I. Gelissen, L. Kritharides, and W. Jessup. 2003. Visualizing lipid structure and raft domains in living cells with two-photon microscopy. Proc. Natl. Acad. Sci. USA. 100:15554-15559.
29. Gaus, K., M. Rodriguez, K. R. Ruberu, I. Gelissen, T. M. Sloane, L. Kritharides, and W. Jessup. 2005. Domain-specific lipid distribution in macrophage plasma membranes. J. Lipid Res. 46:1526-1538.
30. Ishihara, A., Y. Hou, and K. Jacobson. 1987. The Thy-1 antigen exhibits rapid lateral diffusion in the plasma membrane of rodent lymphoid cells and fibroblasts. Proc. Natl. Acad. Sci. USA. 84:1290-1293.
31. Edidin, M., and I. Stroynowski. 1991. Differences between the lateral organization of conventional and inositol phospholipid-anchored membrane proteins. A further definition of micrometer scale membrane domains. J. Cell Biol. 112:1143-1150.
32. Zhang, F., B. Crise, B. Su, Y. Hou, J. K. Rose, A. Bothwell, and K. Jacobson. 1991. Lateral diffusion of membrane-spanning and glycosylphosphatidylinositol-linked proteins: toward establishing rules governing the lateral mobility of membrane proteins. J. Cell Biol. 115:75-84.
33. Subczynski, W. K., and A. Kusumi. 2003. Dynamics of raft molecules in the cell and artificial membranes: approaches by pulse EPR spin labeling and single molecule optical microscopy. Biochim. Biophys. Acta. 1610:231-243.
34. 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.
35. Wieser, S., M. Moertelmaier, E. Furtbauer, H. Stockinger, and G. J. Schutz. 2007. (Un)confined diffusion of CD59 in the plasma membrane determined by high-resolution single molecule microscopy. Biophys. J. 92:3719-3728.
36. 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.
37. 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.
38. Lenne, P. F., L. Wawrezinieck, F. Conchonaud, O. Wurtz, A. Boned, X. J. Guo, H. Rigneault, H. T. He, and D. Marguet. 2006. Dynamic molecular confinement in the plasma membrane by microdomains and the cytoskeleton meshwork. EMBO J. 25:3245-3256.
39. Wenger, J., F. Conchonaud, J. Dintinger, L. Wawrezinieck, T. W. Ebbesen, H. Rigneault, D. Marguet, and P. F. Lenne. 2007. Diffusion analysis within single nanometric apertures reveals the ultrafine cell membrane organization. Biophys. J. 92:913-919.
40. 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.
41. Leunissen, J. L. M., and J. R. De 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.
42. 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.
43. Koyama-Honda, I., K. Ritchie, T. Fujiwara, R. Iino, H. Murakoshi, R. S. Kasai, and A. Kusumi. 2005. Fluorescence imaging for monitoring the colocalization of two single molecules in living cells. Biophys. J. 88:2126-2136.
44. 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.
45. Dickson, R. M., A. B. Cubitt, R. Y. Tsien, and W. E. Moerner. 1997. On/off blinking and switching behavior of single molecules of green fluorescent protein. Nature. 388:355-358.
46. Gelles, J., B. J. Schnapp, and M. P. Sheetz. 1988. Tracking kinesin-driven movements with nanometer-scale precision. Nature. 331:450-453.
47. Sheetz, M. P., S. Turney, H. Qian, and E. L. Elson. 1989. Nanometer-level analysis demonstrates that lipid flow does not drive membrane glycoprotein movements. Nature. 340:284-288.
48. 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.
49. Saxton, M. J. 1994. Anomalous diffusion due to obstacles: a Monte Carlo study. Biophys. J. 66:394-401.
50. Saxton, M. J. 1996. Anomalous diffusion due to binding: a Monte Carlo study. Biophys. J. 70:1250-1262.
51. Saxton, M. J. 1997. Single-particle tracking: the distribution of diffusion coefficients. Biophys. J. 72:1744-1753.
52. 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.
53. Ayscough, K. 1998. Use of latrunculin-A, an actin monomer-binding drug. Methods Enzymol. 298:18-25.
54. Spector, I., N. R. Shochet, Y. Kashman, and A. Groweiss. 1983. Latrunculins: novel marine toxins that disrupt microfilament organization in cultured cells. Science. 219:493-495.
55. Sampath, P., and T. D. Pollard. 1991. Effects of cytochalasin, phalloidin, and pH on the elongation of actin filaments. Biochemistry. 30:1973-1980.
56. Marguet, D., P. F. Lenne, H. Rigneault, and H. T. He. 2006. Dynamics in the plasma membrane: how to combine fluidity and order. EMBO J. 25:3446-3457.
57. 2+ signaling: single-molecule tracking study 2. J. Cell Biol. 177:731-742.
58. Suzuki, K. G., T. K. Fujiwara, F. Sanematsu, R. Iino, M. Edidin, and A. Kusumi. 2007. GPI-anchored receptor clusters transiently recruit Lyn and Gα for temporary cluster immobilization and Lyn activation: single-molecule tracking study 1. J. Cell Biol. 177:717-730.
59. Frick, M., K. Schmidt, and B. J. Nichols. 2007. Modulation of lateral diffusion in the plasma membrane by protein density. Curr. Biol. 17:462-467.
60. Schmidt, K., and B. J. Nichols. 2004. A barrier to lateral diffusion in the cleavage furrow of dividing mammalian cells. Curr. Biol. 14:1002-1006.
61. Wilson, K. M., I. E. Morrison, P. R. Smith, N. Fernandez, and R. J. Cherry. 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.
62. Magnusson, K. E., M. Gustafsson, K. Holmgren, and B. Johansson. 1990. Small intestinal differentiation in human colon carcinoma HT29 cells has distinct effects on the lateral diffusion of lipids (ganglioside GM1) and proteins (HLA class 1, HLA class 2, and neoplastic epithelial antigens) in the apical cell membrane. J. Cell. Physiol. 143:381-390.
63. Barisas, B. G., W. F. Wade, T. M. Jovin, D. Arndt-Jovin, and D. A. Roess. 1999. Dynamics of molecules involved in antigen presentation: effects of fixation. Mol. Immunol. 36:701-708.
64. Munnelly, H. M., C. J. Brady, G. M. Hagen, R. D. Horvat, W. F. Wade, D. A. Roess, and B. G. Barisas. 2001. Molecular dynamics of point mutated I-A(k) molecules expressed on lymphocytes. Immunol. Lett. 77:187-196.
65. Wade, W. F., Z. Z. Chen, R. Maki, S. McKercher, E. Palmer, J. C. Cambier, and J. H. Freed. 1989. Altered I-A protein-mediated transmembrane signaling in B cells that express truncated I-Ak protein. Proc. Natl. Acad. Sci. USA. 86:6297-6301.
66. Griffith, I. J., N. Nabavi, Z. Ghogawala, C. G. Chase, M. Rodriguez, D. J. McKean, and L. H. Glimcher. 1988. Structural mutation affecting intracellular transport and cell surface expression of murine class II molecules. J. Exp. Med. 167:541-555.
67. Mecheri, S., M. Edidin, G. Dannecker, R. S. Mittler, and M. K. Hoffmann. 1990. Immunogenic Ia-binding peptides immobilize the Ia molecule and facilitate its aggregation on the B cell membrane. Control by the M1s-1 gene. J. Immunol. 144:1361-1368.
68. de Brabander, M., R. Nuydens, A. Ishihara, B. Holifield, K. Jacobson, and H. Geerts. 1991. Lateral diffusion and retrograde movements of individual cell surface components on single motile cells observed with Nanovid microscopy. J. Cell Biol. 112:111-124.
69. 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.
70. Thoumine, O., E. Saint-Michel, C. Dequidt, J. Falk, R. Rudge, T. Galli, C. Faivre-Sarrailh, and D. Choquet. 2005. Weak effect of membrane diffusion on the rate of receptor accumulation at adhesive contacts. Biophys. J. 89:L40-L42.
71. Kemble, G. W., Y. I. Henis, and J. M. White. 1993. GPI- and transmembrane-anchored influenza hemagglutinin differ in structure and receptor binding activity. J. Cell Biol. 122:1253-1265.
72. Wettstein, D. A., J. J. Boniface, P. A. Reay, H. Schild, and M. M. Davis. 1991. Expression of a class II major histocompatibility complex (MHC) heterodimer in a lipid-linked form with enhanced peptide/soluble MHC complex formation at low pH. J. Exp. Med. 174:219-228.