Skip to main content
Biophysical Journal logoLink to Biophysical Journal
. 1995 May;68(5):1828–1835. doi: 10.1016/S0006-3495(95)80359-0

Effect of hydrodynamic interactions on the diffusion of integral membrane proteins: tracer diffusion in organelle and reconstituted membranes.

S J Bussell 1, D L Koch 1, D A Hammer 1
PMCID: PMC1282085  PMID: 7612824

Abstract

A persistent discrepancy exists between theoretical predictions and experimental observations for the diffusion coefficients of integral membrane proteins in lipid bilayers free of immobilized proteins. Current thermodynamic theories overestimate tracer diffusion coefficients at high area fractions. We explore the hypothesis that the combined effect of hydrodynamic and thermodynamic interactions reconciles theory with experiment. We have determined previously the short- and long-time tracer diffusivities, Ds and Dl, respectively, of integral membrane proteins in lipid bilayers as a function of their area fraction, phi. The results are based on two-particle hydrodynamic and thermodynamic interactions and are precise to O(phi). Here we extend the results for Dl to high phi by combining the hydrodynamic results for Ds into theories for Dl based on many-particle thermodynamic interactions. The results compare favorably with the experimental measurements of Dl as a function of protein area fraction for bacteriorhodopsin in reconstituted membranes and for complex III of the mitochondrial inner membrane. The agreement suggests that both hydrodynamic and thermodynamic interactions are important determinants of diffusion coefficients of proteins in lipid bilayers. Additional experiments are required to verify the role of hydrodynamic interactions in protein diffusion in reconstituted systems.

Full text

PDF
1828

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Abney J. R., Scalettar B. A., Owicki J. C. Mutual diffusion of interacting membrane proteins. Biophys J. 1989 Aug;56(2):315–326. doi: 10.1016/S0006-3495(89)82678-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Abney J. R., Scalettar B. A., Owicki J. C. Self diffusion of interacting membrane proteins. Biophys J. 1989 May;55(5):817–833. doi: 10.1016/S0006-3495(89)82882-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Axelrod D., Koppel D. E., Schlessinger J., Elson E., Webb W. W. Mobility measurement by analysis of fluorescence photobleaching recovery kinetics. Biophys J. 1976 Sep;16(9):1055–1069. doi: 10.1016/S0006-3495(76)85755-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bussell S. J., Koch D. L., Hammer D. A. Effect of hydrodynamic interactions on the diffusion of integral membrane proteins: diffusion in plasma membranes. Biophys J. 1995 May;68(5):1836–1849. doi: 10.1016/S0006-3495(95)80360-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Chazotte B., Hackenbrock C. R. The multicollisional, obstructed, long-range diffusional nature of mitochondrial electron transport. J Biol Chem. 1988 Oct 5;263(28):14359–14367. [PubMed] [Google Scholar]
  6. Cherry R. J., Godfrey R. E. Anisotropic rotation of bacteriorhodopsin in lipid membranes. Comparison of theory with experiment. Biophys J. 1981 Oct;36(1):257–276. doi: 10.1016/S0006-3495(81)84727-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Deatherage J. F., Henderson R., Capaldi R. A. Relationship between membrane and cytoplasmic domains in cytochrome c oxidase by electron microscopy in media of different density. J Mol Biol. 1982 Jul 5;158(3):501–514. doi: 10.1016/0022-2836(82)90211-x. [DOI] [PubMed] [Google Scholar]
  8. Henderson R., Unwin P. N. Three-dimensional model of purple membrane obtained by electron microscopy. Nature. 1975 Sep 4;257(5521):28–32. doi: 10.1038/257028a0. [DOI] [PubMed] [Google Scholar]
  9. Henis Y. I., Elson E. L. Inhibition of the mobility of mouse lymphocyte surface immunoglobulins by locally bound concanavalin A. Proc Natl Acad Sci U S A. 1981 Feb;78(2):1072–1076. doi: 10.1073/pnas.78.2.1072. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Leonard K., Haiker H., Weiss H. Three-dimensional structure of NADH: ubiquinone reductase (complex I) from Neurospora mitochondria determined by electron microscopy of membrane crystals. J Mol Biol. 1987 Mar 20;194(2):277–286. doi: 10.1016/0022-2836(87)90375-5. [DOI] [PubMed] [Google Scholar]
  11. Medina-Noyola M. Long-time self-diffusion in concentrated colloidal dispersions. Phys Rev Lett. 1988 Jun 27;60(26):2705–2708. doi: 10.1103/PhysRevLett.60.2705. [DOI] [PubMed] [Google Scholar]
  12. Minton A. P. Lateral diffusion of membrane proteins in protein-rich membranes. A simple hard particle model for concentration dependence of the two-dimensional diffusion coefficient. Biophys J. 1989 Apr;55(4):805–808. doi: 10.1016/S0006-3495(89)82880-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Peters R., Cherry R. J. Lateral and rotational diffusion of bacteriorhodopsin in lipid bilayers: experimental test of the Saffman-Delbrück equations. Proc Natl Acad Sci U S A. 1982 Jul;79(14):4317–4321. doi: 10.1073/pnas.79.14.4317. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Saffman P. G., Delbrück M. Brownian motion in biological membranes. Proc Natl Acad Sci U S A. 1975 Aug;72(8):3111–3113. doi: 10.1073/pnas.72.8.3111. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Saxton M. J. Lateral diffusion in an archipelago. The effect of mobile obstacles. Biophys J. 1987 Dec;52(6):989–997. doi: 10.1016/S0006-3495(87)83291-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. 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]
  17. Tank D. W., Wu E. S., Meers P. R., Webb W. W. Lateral diffusion of gramicidin C in phospholipid multibilayers. Effects of cholesterol and high gramicidin concentration. Biophys J. 1982 Nov;40(2):129–135. doi: 10.1016/S0006-3495(82)84467-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Tank D. W., Wu E. S., Webb W. W. Enhanced molecular diffusibility in muscle membrane blebs: release of lateral constraints. J Cell Biol. 1982 Jan;92(1):207–212. doi: 10.1083/jcb.92.1.207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Wu E. S., Tank D. W., Webb W. W. Unconstrained lateral diffusion of concanavalin A receptors on bulbous lymphocytes. Proc Natl Acad Sci U S A. 1982 Aug;79(16):4962–4966. doi: 10.1073/pnas.79.16.4962. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Biophysical Journal are provided here courtesy of The Biophysical Society

RESOURCES