Home LiteratureArticle Details
PMID: 16113107 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Anomalous diffusion of proteins due to molecular crowding.

Biophysical journal ·Vol. 89 ·No. 5 ·2005-11-00 ·Pages 2960-71

Banks DS, Fradin C

Abstract

We have studied the diffusion of tracer proteins in highly concentrated random-coil polymer and globular protein solutions imitating the crowded conditions encountered in cellular environments. Using fluorescence correlation spectroscopy, we measured the anomalous diffusion exponent alpha characterizing the dependence of the mean-square displacement of the tracer proteins on time, r(2)(t) approximately t(alpha). We observed that the diffusion of proteins in dextran solutions with concentrations up to 400 g/l is subdiffusive (alpha < 1) even at low obstacle concentration. The anomalous diffusion exponent alpha decreases continuously with increasing obstacle concentration and molecular weight, but does not depend on buffer ionic strength, and neither does it depend strongly on solution temperature. At very high random-coil polymer concentrations, alpha reaches a limit value of alpha(l) approximately 3/4, which we take to be the signature of a coupling between the motions of the tracer proteins and the segments of the dextran chains. A similar, although less pronounced, subdiffusive behavior is observed for the diffusion of streptavidin in concentrated globular protein solutions. These observations indicate that protein diffusion in the cell cytoplasm and nucleus should be anomalous as well, with consequences for measurements of solute diffusion coefficients in cells and for the modeling of cellular processes relying on diffusion.

MeSH Terms
Biophysics/methods Buffers Dextrans/chemistry Diffusion Fluorescent Dyes/pharmacology Ions Macromolecular Substances Models, Biological Models, Chemical Models, Statistical Monte Carlo Method Proteins/chemistry Spectrometry, Fluorescence/methods Temperature Time Factors
Chemicals
Buffers Dextrans Fluorescent Dyes Ions Macromolecular Substances Proteins
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Banks Daniel S
Department of Physics and Astronomy, McMaster University, Hamilton, Ontario, Canada.
Fradin Cécile
References (65)
65 references, click to expand
  1. Maximum-entropy decomposition of fluorescence correlation spectroscopy data: application to liposome-human serum albumin association.
    Eur Biophys J. 2004 Feb;33(1):59-67 PMID: 12955361
  2. Effect of dextran on protein stability and conformation attributed to macromolecular crowding.
    J Mol Biol. 2003 Feb 28;326(4):1227-37 PMID: 12589765
  3. Protein mobility in the cytoplasm of Escherichia coli.
    J Bacteriol. 1999 Jan;181(1):197-203 PMID: 9864330
  4. Fluorescence correlation spectroscopy in small cytosolic compartments depends critically on the diffusion model used.
    Biophys J. 2000 Dec;79(6):3294-306 PMID: 11106632
  5. Anomalous diffusion of fluorescent probes inside living cell nuclei investigated by spatially-resolved fluorescence correlation spectroscopy.
    J Mol Biol. 2000 May 12;298(4):677-89 PMID: 10788329
  6. Visualization and tracking of single protein molecules in the cell nucleus.
    Biophys J. 2001 Jun;80(6):2954-67 PMID: 11371468
  7. Anomalous diffusion probes microstructure dynamics of entangled F-actin networks.
    Phys Rev Lett. 2004 Apr 30;92(17):178101 PMID: 15169197
  8. Brownian dynamics simulations of probe and self-diffusion in concentrated protein and DNA solutions.
    Biophys J. 1993 Nov;65(5):1810-6 PMID: 8298014
  9. Analysis of fluorophore diffusion by continuous distributions of diffusion coefficients: application to photobleaching measurements of multicomponent and anomalous diffusion.
    Biophys J. 1998 Jul;75(1):557-67 PMID: 9649418
  10. New fluorescence correlation spectroscopy enabling direct observation of spatiotemporal dependence of diffusion constants as an evidence of anomalous transport in extracellular matrices.
    Biophys J. 2005 May;88(5):3584-91 PMID: 15695633
  11. Macromolecular crowding and molecular recognition.
    J Mol Recognit. 1993 Dec;6(4):211-4 PMID: 7917416
  12. Solute and macromolecule diffusion in cellular aqueous compartments.
    Trends Biochem Sci. 2002 Jan;27(1):27-33 PMID: 11796221
  13. Properties of cage rearrangements observed near the colloidal glass transition.
    Phys Rev Lett. 2002 Aug 26;89(9):095704 PMID: 12190415
  14. Direct molecular level measurements of the electrostatic properties of a protein surface.
    Proc Natl Acad Sci U S A. 1998 Oct 27;95(22):12961-6 PMID: 9789023
  15. Diffusion of green fluorescent protein in the aqueous-phase lumen of endoplasmic reticulum.
    Biophys J. 1999 May;76(5):2843-51 PMID: 10233100
  16. Monte carlo simulations of enzyme reactions in two dimensions: fractal kinetics and spatial segregation.
    Biophys J. 2002 Oct;83(4):1891-901 PMID: 12324410
  17. Fluorescence correlation spectroscopy close to a fluctuating membrane.
    Biophys J. 2003 Mar;84(3):2005-20 PMID: 12609903
  18. Anomalous diffusion due to obstacles: a Monte Carlo study.
    Biophys J. 1994 Feb;66(2 Pt 1):394-401 PMID: 8161693
  19. Diffusion of a small molecule in the cytoplasm of mammalian cells.
    Proc Natl Acad Sci U S A. 1984 Jun;81(11):3414-8 PMID: 6328515
  20. The amyloid beta peptide (Abeta(1-40)) is thermodynamically soluble at physiological concentrations.
    Biochemistry. 2003 Sep 9;42(35):10506-13 PMID: 12950178
  21. Estimation of macromolecule concentrations and excluded volume effects for the cytoplasm of Escherichia coli.
    J Mol Biol. 1991 Dec 5;222(3):599-620 PMID: 1748995
  22. Fluorescence correlation spectroscopy: inception, biophysical experimentations, and prospectus.
    Appl Opt. 2001 Aug 20;40(24):3969-83 PMID: 18360431
  23. Anomalous diffusion due to binding: a Monte Carlo study.
    Biophys J. 1996 Mar;70(3):1250-62 PMID: 8785281
  24. Physical properties of cytoplasm.
    Curr Opin Cell Biol. 1994 Feb;6(1):3-9 PMID: 8167023
  25. Microbiology. Action at a distance--bacterial flagellar assembly.
    Science. 2000 Dec 15;290(5499):2086-7 PMID: 11187835
  26. Measuring size distribution in highly heterogeneous systems with fluorescence correlation spectroscopy.
    Biophys J. 2003 Mar;84(3):1977-84 PMID: 12609900
  27. Hierarchical assembly of cell-matrix adhesion complexes.
    Biochem Soc Trans. 2004 Jun;32(Pt3):416-20 PMID: 15157150
  28. Molecular crowding reduces to a similar extent the diffusion of small solutes and macromolecules: measurement by fluorescence correlation spectroscopy.
    J Mol Recognit. 2004 Sep-Oct;17(5):441-7 PMID: 15362103
  29. Fluorescence correlation spectroscopy with single-molecule sensitivity on cell and model membranes.
    Cytometry. 1999 Jul 1;36(3):176-82 PMID: 10404965
  30. A biodegradable polymer scaffold for delivery of osteotropic factors.
    Biomaterials. 2000 Dec;21(24):2545-51 PMID: 11071604
  31. Molecular interactions in biofilms.
    Chem Biol. 2002 Aug;9(8):859-71 PMID: 12204685
  32. Direct observation of the enhancement of noncooperative protein self-assembly by macromolecular crowding: indefinite linear self-association of bacterial cell division protein FtsZ.
    Proc Natl Acad Sci U S A. 2001 Mar 13;98(6):3150-5 PMID: 11248047
  33. Stabilizing Turing patterns with subdiffusion in systems with low particle numbers.
    Phys Rev E Stat Nonlin Soft Matter Phys. 2003 Sep;68(3 Pt 2):036213 PMID: 14524874
  34. Fluorescence correlation spectroscopy and its potential for intracellular applications.
    Cell Biochem Biophys. 2001;34(3):383-408 PMID: 11898862
  35. Diffusional protein transport within the nucleus: a message in the medium.
    Nat Cell Biol. 2000 May;2(5):E73-4 PMID: 10806486
  36. The influence of macromolecular crowding and macromolecular confinement on biochemical reactions in physiological media.
    J Biol Chem. 2001 Apr 6;276(14):10577-80 PMID: 11279227
  37. Rational design of green fluorescent protein mutants as biosensor for bacterial endotoxin.
    Protein Eng. 2002 Jun;15(6):493-502 PMID: 12082168
  38. Diffusion and thermal diffusion of semidilute to concentrated solutions of polystyrene in toluene in the vicinity of the glass transition.
    Phys Rev Lett. 2002 May 6;88(18):185901 PMID: 12005700
  39. Size effects on diffusion processes within agarose gels.
    Biophys J. 2004 May;86(5):2710-9 PMID: 15111390
  40. Highly crosslinked, PEG-containing copolymers for sustained solute delivery.
    Biomaterials. 1999 Aug;20(15):1371-80 PMID: 10454008
  41. How crowded is the cytoplasm?
    Cell. 1982 Sep;30(2):345-7 PMID: 6754085
  42. Constrained diffusion or immobile fraction on cell surfaces: a new interpretation.
    Biophys J. 1996 Jun;70(6):2767-73 PMID: 8744314
  43. Diffusion in embryogenesis.
    Nature. 1970 Jan 31;225(5231):420-2 PMID: 5411117
  44. Probing the structure of cytoplasm.
    J Cell Biol. 1986 Jun;102(6):2015-22 PMID: 2423529
  45. Macromolecular crowding: biochemical, biophysical, and physiological consequences.
    Annu Rev Biophys Biomol Struct. 1993;22:27-65 PMID: 7688609
  46. Diffusion and directed motion in cellular transport.
    Phys Rev E Stat Nonlin Soft Matter Phys. 2002 Jul;66(1 Pt 1):011916 PMID: 12241393
  47. Subdiffusion and Anomalous Local Viscoelasticity in Actin Networks.
    Phys Rev Lett. 1996 Nov 18;77(21):4470-4473 PMID: 10062546
  48. Photobleaching recovery and anisotropy decay of green fluorescent protein GFP-S65T in solution and cells: cytoplasmic viscosity probed by green fluorescent protein translational and rotational diffusion.
    Biophys J. 1997 Apr;72(4):1900-7 PMID: 9083693
  49. Translational diffusion of macromolecule-sized solutes in cytoplasm and nucleus.
    J Cell Biol. 1997 Jul 14;138(1):131-42 PMID: 9214387
  50. Direct observation of one-dimensional diffusion and transcription by Escherichia coli RNA polymerase.
    Biophys J. 1999 Oct;77(4):2284-94 PMID: 10512846
  51. Dynamics of fluorescence fluctuations in green fluorescent protein observed by fluorescence correlation spectroscopy.
    Proc Natl Acad Sci U S A. 1998 Nov 10;95(23):13573-8 PMID: 9811841
  52. Long tail kinetics in biophysics?
    Biophys J. 1992 Aug;63(2):366-70 PMID: 1420883
  53. Measurement of normal and anomalous diffusion of dyes within protein structures fabricated via multiphoton excited cross-linking.
    Biomacromolecules. 2004 Nov-Dec;5(6):2347-57 PMID: 15530051
  54. Measurement of molecular diffusion in solution by multiphoton fluorescence photobleaching recovery.
    Biophys J. 1999 Nov;77(5):2837-49 PMID: 10545381
  55. Size-dependent DNA mobility in cytoplasm and nucleus.
    J Biol Chem. 2000 Jan 21;275(3):1625-9 PMID: 10636854
  56. Diffusion of injected macromolecules within the cytoplasm of living cells.
    Proc Natl Acad Sci U S A. 1981 Jul;78(7):4407-10 PMID: 6945591
  57. Statistical analysis of fluorescence correlation spectroscopy: the standard deviation and bias.
    Biophys J. 2003 Mar;84(3):2030-42 PMID: 12609905
  58. An ultrasensitive bacterial motor revealed by monitoring signaling proteins in single cells.
    Science. 2000 Mar 3;287(5458):1652-5 PMID: 10698740
  59. Microscopic viscosity and rotational diffusion of proteins in a macromolecular environment.
    Biophys J. 1999 May;76(5):2744-51 PMID: 10233089
  60. Anomalous subdiffusion is a measure for cytoplasmic crowding in living cells.
    Biophys J. 2004 Nov;87(5):3518-24 PMID: 15339818
  61. Slow diffusion of proteins in the yeast plasma membrane allows polarity to be maintained by endocytic cycling.
    Curr Biol. 2003 Sep 16;13(18):1636-40 PMID: 13678596
  62. Lateral diffusion of proteins in membranes.
    Annu Rev Physiol. 1987;49:163-75 PMID: 3551795
  63. Macromolecular crowding: qualitative and semiquantitative successes, quantitative challenges.
    Biochim Biophys Acta. 2003 Jul 30;1649(2):127-39 PMID: 12878031
  64. Direct observation of dynamical heterogeneities in colloidal hard-sphere suspensions
    Science. 2000 Jan 14;287(5451):290-3 PMID: 10634780
  65. Physico-chemical characterization of Ca-alginate microparticles produced with different methods.
    Biomaterials. 1999 Aug;20(15):1427-35 PMID: 10454015
Article Info
Journal
Biophysical journal
Abbr.
Biophys J
ISSN
0006-3495
Published
2005-11-00
Epub
2005-00-19
Pages
2960-71
Language
English
Region
United States
NLM ID
0370626
PMCID
PMC1366794
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com