Abstract
We consider the possibility of inferring the nature of cytoskeletal interaction with transmembrane proteins via optical experiments such as single-particle tracking (SPT) and near-field scanning optical microscopy (NSOM). In particular, we demonstrate that it may be possible to differentiate between static and dynamic barriers to diffusion by examining the time-dependent variance and higher moments of protein population inside cytoskeletal "corrals." Simulations modeling Band 3 diffusion on the surface of erythrocytes provide a concrete demonstration that these statistical tools might prove useful in the study of biological systems.
Full Text
The Full Text of this article is available as a PDF (210.9 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Berg H. C., Purcell E. M. Physics of chemoreception. Biophys J. 1977 Nov;20(2):193–219. doi: 10.1016/S0006-3495(77)85544-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Boal D. H., Boey S. K. Barrier-free paths of directed protein motion in the erythrocyte plasma membrane. Biophys J. 1995 Aug;69(2):372–379. doi: 10.1016/S0006-3495(95)79909-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Boal D. H. Computer simulation of a model network for the erythrocyte cytoskeleton. Biophys J. 1994 Aug;67(2):521–529. doi: 10.1016/S0006-3495(94)80511-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cherry R. J. Rotational and lateral diffusion of membrane proteins. Biochim Biophys Acta. 1979 Dec 20;559(4):289–327. doi: 10.1016/0304-4157(79)90009-1. [DOI] [PubMed] [Google Scholar]
- Corbett J. D., Agre P., Palek J., Golan D. E. Differential control of band 3 lateral and rotational mobility in intact red cells. J Clin Invest. 1994 Aug;94(2):683–688. doi: 10.1172/JCI117385. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Edidin M., Kuo S. C., Sheetz M. P. Lateral movements of membrane glycoproteins restricted by dynamic cytoplasmic barriers. Science. 1991 Nov 29;254(5036):1379–1382. doi: 10.1126/science.1835798. [DOI] [PubMed] [Google Scholar]
- Fleming T. P. Trapped by a skeleton--the maintenance of epithelial membrane domains. Bioessays. 1987 Oct;7(4):179–181. doi: 10.1002/bies.950070410. [DOI] [PubMed] [Google Scholar]
- Giancotti F. G., Ruoslahti E. Integrin signaling. Science. 1999 Aug 13;285(5430):1028–1032. doi: 10.1126/science.285.5430.1028. [DOI] [PubMed] [Google Scholar]
- Jacobson K., Sheets E. D., Simson R. Revisiting the fluid mosaic model of membranes. Science. 1995 Jun 9;268(5216):1441–1442. doi: 10.1126/science.7770769. [DOI] [PubMed] [Google Scholar]
- Koppel D. E., Sheetz M. P., Schindler M. Matrix control of protein diffusion in biological membranes. Proc Natl Acad Sci U S A. 1981 Jun;78(6):3576–3580. doi: 10.1073/pnas.78.6.3576. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kusumi A., Sako Y. Cell surface organization by the membrane skeleton. Curr Opin Cell Biol. 1996 Aug;8(4):566–574. doi: 10.1016/s0955-0674(96)80036-6. [DOI] [PubMed] [Google Scholar]
- Kusumi A., Sako Y., Fujiwara T., Tomishige M. Application of laser tweezers to studies of the fences and tethers of the membrane skeleton that regulate the movements of plasma membrane proteins. Methods Cell Biol. 1998;55:173–194. doi: 10.1016/s0091-679x(08)60408-2. [DOI] [PubMed] [Google Scholar]
- Leitner D. M., Brown F. L., Wilson K. R. Regulation of protein mobility in cell membranes: a dynamic corral model. Biophys J. 2000 Jan;78(1):125–135. doi: 10.1016/S0006-3495(00)76579-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Qian H., Sheetz M. P., Elson E. L. Single particle tracking. Analysis of diffusion and flow in two-dimensional systems. Biophys J. 1991 Oct;60(4):910–921. doi: 10.1016/S0006-3495(91)82125-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sako Y., Kusumi A. 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. 1995 Jun;129(6):1559–1574. doi: 10.1083/jcb.129.6.1559. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Saxton M. J., Jacobson K. Single-particle tracking: applications to membrane dynamics. Annu Rev Biophys Biomol Struct. 1997;26:373–399. doi: 10.1146/annurev.biophys.26.1.373. [DOI] [PubMed] [Google Scholar]
- Saxton M. J. Single-particle tracking: effects of corrals. Biophys J. 1995 Aug;69(2):389–398. doi: 10.1016/S0006-3495(95)79911-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Saxton M. J. The membrane skeleton of erythrocytes. A percolation model. Biophys J. 1990 Jun;57(6):1167–1177. doi: 10.1016/S0006-3495(90)82636-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Saxton M. J. The membrane skeleton of erythrocytes: models of its effect on lateral diffusion. Int J Biochem. 1990;22(8):801–809. doi: 10.1016/0020-711x(90)90283-9. [DOI] [PubMed] [Google Scholar]
- Saxton M. J. The spectrin network as a barrier to lateral diffusion in erythrocytes. A percolation analysis. Biophys J. 1989 Jan;55(1):21–28. doi: 10.1016/S0006-3495(89)82776-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schindler M., Koppel D. E., Sheetz M. P. Modulation of membrane protein lateral mobility by polyphosphates and polyamines. Proc Natl Acad Sci U S A. 1980 Mar;77(3):1457–1461. doi: 10.1073/pnas.77.3.1457. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sheetz M. P. Membrane skeletal dynamics: role in modulation of red cell deformability, mobility of transmembrane proteins, and shape. Semin Hematol. 1983 Jul;20(3):175–188. [PubMed] [Google Scholar]
- Sheetz M. P., Schindler M., Koppel D. E. Lateral mobility of integral membrane proteins is increased in spherocytic erythrocytes. Nature. 1980 Jun 12;285(5765):510–511. doi: 10.1038/285510a0. [DOI] [PubMed] [Google Scholar]
- Singer S. J., Nicolson G. L. The fluid mosaic model of the structure of cell membranes. Science. 1972 Feb 18;175(4023):720–731. doi: 10.1126/science.175.4023.720. [DOI] [PubMed] [Google Scholar]
- Tomishige M., Sako Y., Kusumi A. Regulation mechanism of the lateral diffusion of band 3 in erythrocyte membranes by the membrane skeleton. J Cell Biol. 1998 Aug 24;142(4):989–1000. doi: 10.1083/jcb.142.4.989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tsuji A., Kawasaki K., Ohnishi S., Merkle H., Kusumi A. Regulation of band 3 mobilities in erythrocyte ghost membranes by protein association and cytoskeletal meshwork. Biochemistry. 1988 Sep 20;27(19):7447–7452. doi: 10.1021/bi00419a041. [DOI] [PubMed] [Google Scholar]
- Tsuji A., Ohnishi S. Restriction of the lateral motion of band 3 in the erythrocyte membrane by the cytoskeletal network: dependence on spectrin association state. Biochemistry. 1986 Oct 7;25(20):6133–6139. doi: 10.1021/bi00368a045. [DOI] [PubMed] [Google Scholar]
- Wang J, Wolynes P. Intermittency of single molecule reaction dynamics in fluctuating environments. Phys Rev Lett. 1995 May 22;74(21):4317–4320. doi: 10.1103/PhysRevLett.74.4317. [DOI] [PubMed] [Google Scholar]
- Winckler B., Forscher P., Mellman I. A diffusion barrier maintains distribution of membrane proteins in polarized neurons. Nature. 1999 Feb 25;397(6721):698–701. doi: 10.1038/17806. [DOI] [PubMed] [Google Scholar]