Effects of macromolecular crowding on intracellular diffusion from a single particle perspective

Biophysical Reviews

Volumn 2, Issue 1, 2010, Pages 39-53

  Hall, Damien ^a   Hoshino, Masaru ^b  

^a UNIVERSITY OF TSUKUBA   (Japan)

^b KYOTO UNIVERSITY   (Japan)

Author keywords

'Crowded' solutions; Bio molecules; Brownian motion; In vitro reactions; intracellular diffusion; Single particle

Indexed keywords

EID: 79959721346     PISSN: 18672450     EISSN: 18672469     Source Type: Journal    
DOI: 10.1007/s12551-010-0029-0     Document Type: Review

References (120)

1. Alcor D, Gouzer G, Triller A (2009) Single-particle tracking methods for the study of membrane receptors dynamics. Eur J Neurosci 30: 987-997.
2. Andrews SS, Bray D (2004) Stochastic simulation of chemical reactions with spatial resolution and single molecule detail. Phys Biol 1: 137-151.
3. Arrio-Dupont M, Foucault G, Vacher M, Devaux PF, Cribier S (2000) Translational diffusion of globular proteins in the cytoplasm of cultured muscle cells. Biophys J 78: 901-907.
4. Banks DS, Fradin C (2005) Anomalous diffusion of proteins due to molecular crowding. Biophys J 89: 2960-2971.
5. Batchelor GK (1982) Sedimentation in a dilute polydisperse system of interacting spheres. Part 1. General theory. J Fluid Mech 119: 379-408.
6. Batchelor GK (2000) An introduction to fluid dynamics. Cambridge University Press, Cambridge.
7. Baumeister W (2004) Mapping molecular landscapes inside cells. Biol Chem 385: 865-872.
8. Berg HC (1993) Random walks in biology. Princeton University Press, Princeton.
9. Bernadó P, García de la Torre J, Pons M (2004) Macromolecular crowding in biological systems: hydrodynamics and NMR methods. J Mol Recognition 17: 397-407.
10. Bicout DJ, Field MJ (1996) Stochastic dynamics simulations of macromolecular diffusion in a model of the cytoplasm of E. coli. J Phys Chem 100: 2489-2497.
11. Blum JJ, Lawler G, Reed M, Shin I (1989) Effect of cytoskeletal geometry on intracellular diffusion. Biophys J 56: 995-1005.
12. Bray D (1998) Signalling complexes: biophysical constraints on intracellular communication. Annu Rev Biophys Biomol Struct 27: 59-75.
13. Burdzy K, Hołyst R. (2001) Mechanisms for facilitated target location and the optimal number of molecules in the diffusion search process. Phys Rev E Stat Nonlin Soft Matter Phys 64: 011914-011915.
14. Burz DS, Dutta K, Cowburn D, Shekhtman A (2006) Mapping structural interactions using in-cell NMR spectroscopy (STINT-NMR). Nat Methods 3: 91-93.
15. Bussell SJ, Koch DL, Hammer DA (1995) Effect of hydrodynamic interactions on the diffusion of integral membrane proteins: tracer diffusion in organelle and reconstituted membranes. Biophys J 68: 1828-1835.
16. Byron Bird R, Stewart WE, Lightfoot EN (2002) Chapter 2 of Transport phenomena, 2nd edn. John Wiley and Sons, London.
17. Chiantia S, Ries J, Schwille P (2009) Fluorescence correlation spectroscopy in membrane structure elucidation. Biochim Biophys Acta 1788: 225-233.
18. Czech J, Dittrich M, Stiles JR (2009) Rapid creation, Monte Carlo simulation, and visualization of realistic 3D cell models. Methods Mol Biol 500: 237-287.
19. de Brabander M, Nuydens R, Ishihara A, Holifield B, Jacobsen K, Geerts H (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.
20. Dhont JKG (1996) An introduction to dynamics of colloids. In: Möbius D, Miller R (eds) Studies of interface science. Elsevier, Amsterdam, pp 327-329.
21. Diaspro A (ed) (2002) Confocal and two-photon microscopy: foundations, applications and advances. Wiley Liss, London.
22. Dix J, Verkman A (2008) Crowding effects on diffusion in solutions and cells. Annu Rev Biophys 37: 247-263.
23. Doi M, Edwards S (1999) Theory of polymer dynamics. Clarendon Press, Oxford.
24. Doster W, Longeville S (2007) Microscopic diffusion and hydrodynamic interactions of hemoglobin in red blood cells. Biophys J 93: 1360-1368.
25. Einstein A (1956) Investigations on the theory of the Brownian movement. Dover Publ, New York.
26. Elcock AH (2003) Atomic-level observation of macromolecular crowding effects. Proc Natl Acad Sci USA 100: 2340-2344.
27. Elimelech M, Gregory J, Jia X, Williams R (1995) Particle deposition and aggregation: measurement modelling and simulation. Butterworth and Heinemann, Oxford.
28. Elson EL (2004) A quick tour of fluorescence correlation spectroscopy from its inception. J Biomed Opt 9: 857-864.
29. Ermak DL (1975) A computer simulation of charged particles in solution I. Technique and equilibrium properties. J Chem Phys 62: 4189-4196.
30. Ermak DL, McCammon JA (1978) Brownian dynamics with hydrodynamic interactions. J Chem Phys 69: 1352-1360.
31. Falck E, Lahtinen JM, Vattulainen I, Ala-Nissila T (2004) Influence of hydrodynamics on many particle diffusion in 2D colloidal suspensions. Eur Phys J E 13: 267-275.
32. Fernandes MX, de la Torre JG (2002) Brownian dynamics simulation of rigid particles of arbitrary shape in external fields. Biophys J 83: 3039-3048.
33. Frey E, Kroy K (2005) Brownian motion: a paradigm of soft matter and biological physics. Ann Phys 14: 20-50.
34. Fulinski A (1998) On Marain Smoluchowski's life and contribution to physics. Acta Phys Polonica B 29: 1523-1537.
35. Geerts H, de Brabander M, Nuydens R (1991) Nanovid microscopy. Nature 331: 450-453.
36. Gershon ND, Porter KR, Trans BL (1985) The cytoplasmic matrix: its volume and surface area and the diffusion of molecules through it. Proc Natl Acad Sci USA 82: 030-5034.
37. 2) approximation for hydrodynamic interactions in Brownian dynamics simulations. J Chem Phys 21: 130: 114905.
38. 2O. Biochemistry 32: 11878-11885.
39. Goulian M, Simon SM (2000) Tracking single proteins within cells. Biophys J 79: 2188-2198.
40. Guo L, Har JY, Sankaran J, Hong Y, Kannan B, Wohland T (2008) Molecular diffusion measurement in lipid bilayers over wide concentration ranges: a comparative study. Chem Physchem 9: 721-728.
41. Haggie PM, Verkman AS (2002) Diffusion of tricarboxylic acid cycle enzymes in the mitochondrial matrix in vivo. Evidence for restricted mobility of a multienzyme complex. J Biol Chem 277: 40782-40788.
42. Hall D (2008) Analysis and interpretation of two-dimensional single-particle tracking microscopy measurements: effect of local surface roughness. Anal Biochem 377: 24-32.
43. Hall D (2010) Effect of heterogeneity on the characterization of cell membrane compartments: I. Uniform size and permeability. Anal Biochem (in press).
44. Hall D, Dobson CM (2006) Expanding to fill the gap: a possible role for inert biopolymers in regulating the extent of the 'macromolecular crowding' effect. FEBS Lett 580: 2584-2590.
45. Hall D, Minton AP (2003) Macromolecular crowding: qualitative and semiquantitative successes, quantitative challenges. Biochim Biophys Acta 1649: 127-139.
46. Han J, Herzfeld J (1993) Macromolecular diffusion in crowded solutions. Biophys J 65: 1155-1161.
47. Harris SJ, Winzor DJ (1985) Effect of thermodynamic nonideality on the subcellular distribution of enzymes: adsorption of aldolase to muscle myofibrils. Arch Biochem Biophys 243: 598-604.
48. Hellriegel C, Gratton E (2009) Real-time multi-parameter spectroscopy and localization in three-dimensional single-particle tracking. J R Soc Interface 6[Suppl 1]: S3-S14.
49. Hentschke R, Herzfeld J (1989) Nematic behaviour of reversibly of reversibly polymerising proteins. J Chem Phys 90: 5094-5101.
50. Herzfeld J (2004) Crowding-induced organization in cells: spontaneous alignment and sorting of filaments with physiological control points. J Mol Recognition 17: 376-381.
51. Hibino K, Hiroshima M, Takahashi M, Sako Y (2009) Single-molecule imaging of fluorescent proteins expressed in living cells. Methods Mol Biol 544: 451-460.
52. Heyes DM (1995) Mean-field hydrodynamics Brownian dynamics simulations of viscosity and self diffusion of near-hard-sphere colloidal liquids. J Phys Condens Matter 7: 8857-8865.
53. Hoshino M, Yumoto N, Yoshikawa S, Goto Y (1997) Design and characterization of the anion-sensitive coiled-coil peptide. Protein Sci 6: 1396-1404.
54. Iwahara J, Clore GM (2006) Detecting transient intermediates in macromolecular binding by paramagnetic NMR. Nature 440: 1227-1230.
55. Jacobson K, Wojcieszyn J (1984) The translational mobility of substances within the cytoplasmic matrix. Proc Natl Acad Sci USA 81: 6747-6751.
56. Jameson DM, Ross JA, Albanesi JP (2009) Fluorescence fluctuation spectroscopy: ushering in a new age of enlightenment for cellular dynamics. Biophys Rev 3: 105-118.
57. Jeschke M (2008) Multi-resolution spatial simulation for molecular crowding. In: Proc 40th Conf Winter Simulation, pp1384-1392.
58. Jin S, Verkmann AS (2007) Single particle tracking of complex diffusion in membranes: simulation and detection of barrier, raft and interaction phenomena. J Phys Chem B 111: 3625-3632.
59. Jones RAL (2002) Soft condensed matter. Oxford University Press, Oxford.
60. Kao HP, Verkman AS (1994) Tracking of single fluorescent particles in three dimensions: use of cylindrical optics to encode particle position. Biophys J 67: 1291-1300.
61. Kang K, Wilk A, Patkowski A, Dhont JK (2007) Diffusion of spheres in isotropic and nematic networks of rods: electrostatic interactions and hydrodynamic screening. J Chem Phys 126(214501): 1-17.
62. Klann MT, Lapin A, Reuss M (2009) Stochastic simulation of signal transduction: impact of the cellular architecture on diffusion. Biophys J 96: 5122-5129.
63. Konopka MC, Shkel IA, Cayley S, Record MT, Weisshaar JC (2006) Crowding and confinement effects on protein diffusion in vivo. J Bacteriol 188: 6115-6123.
64. Kubo R (1966) The fluctuation dissipation theorem. Rep Prog Phys 29: 255-284.
65. Kurganov BI, Sugrobova NP, Mil'man LS (1985) Supramolecular organization of glycolytic enzymes. J Theor Biol 116: 509-526.
66. Kusumi A, Nakada C, Ritchie K, Murase K, Suzuki K, Murakoshi H, Kasai RS, Kondo J, Fujiwara T (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.
67. Langevin P (1908) Sur la thėorie du mouvement brownien. C. R. Acad. Sci. (Paris) 146: 530-533 [As translated by Lemons DS, Gythiel A (1995) Paul Langevin's 1908 paper "On the Theory of Brownian Motion". Am J Phys 65: 1079-1081].
68. Lax M (1966) Classical noise. IV. Langevin methods. Rev Mod Phys 38: 541-566.
69. Leach AR (2001) Molecular modelling: principles and applications, 2nd edn. Pearson-Prentice Hall, Upper Saddle River.
70. Leis A, Rockel B, Andrees L, Baumeister W (2009) Visualizing cells at the nanoscale. Trends Biochem Sci 34: 60-70.
71. Lorén N, Nydén M, Hermansson AM (2009) Determination of local diffusion properties in heterogeneous biomaterials. Adv Colloid Interface Sci 150: 5-15.
72. Luby-Phelps K, Lanni F, Taylor DL (1988) The submicroscopic properties of cytoplasm as a determinant of cellular function. Annu Rev Biophys Biophys Chem 17: 369-396.
73. Ma'ayan A, Blitzer RD, Iyengar R (2005) Toward predictive models of mammalian cells. Annu Rev Biophys Biomol Struct 34: 319-349.
74. McGuffee SR, Elcock AH (2006) Atomically detailed simulations of concentrated protein solutions: the effects of salt, pH, point mutations, and protein concentration in simulations of 1000-molecule systems. J Am Chem Soc 128: 12098-12110.
75. Minton AP (1989) 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 55: 805-808.
76. Minton AP (1992) Confinement as a determinant of macromolecular structure and reactivity. Biophys J 63: 1090-1100.
77. Minton AP, Wilf J (1981) Effect of macromolecular crowding upon the structure and function of an enzyme: glyceraldehyde-3-phosphate dehydrogenase. Biochemistry 20: 4821-4826.
78. Mirosavljević K, Noethig-Laslo V (2008) Spin labelling study of interfacial properties of egg-phosphatidylcholine liposomes as a function of cholesterol concentrations. Chem Phys Lipids 155: 74-79.
79. Moraru II, Schaff JC, Slepchenko BM, Blinov ML, Morgan F, Lakshminarayana A, Gao F, Li Y, Loew LM (2009) Virtual Cell modelling and simulation software environment. IET Syst Biol 2: 352-362.
80. Morris KF, Johnson Jr. CS (1992) Diffusion-ordered two-dimensional nuclear magnetic resonance spectroscopy. J Am Chem Soc 114: 3139-3141.
81. Muramatsu N, Minton AP (1988) Tracer diffusion of globular proteins in concentrated protein solutions. Proc Natl Acad Sci USA 85: 2984-2988.
82. Murcia MJ, Garg S, Naumann CA (2007) Single-molecule fluorescence microscopy to determine phospholipid lateral diffusion. Methods Mol Biol 400: 277-294.
83. Padding JT, Louis AA (2006) Hydrodynamic interactions and Brownian forces in colloidal suspensions: coarse graining over time and length scales. Phys Rev E 74031402: 1-29.
84. Peetermans JA, Foy BD, Tanaka T (1987) Accumulation and diffusion of crystallin inside single fiber cells in intact chicken embryo lenses. Proc Natl Acad Sci USA 84(7): 1727-1730.
85. Perrin J (1910) Brownian movement and molecular reality (translated edition published by Taylor and Francis, London, 1910).
86. Peskir G (2003) On the diffusion coefficient: the Einstein relation and beyond. Stochastic Models 19: 383-405.
87. Philibert J (2006) One and a half century of diffusion: Fick, Einstein, before and beyond. Diffusion-Fundamentals 6: 1-19.
88. Provance DW Jr, McDowall A, Marko M, Luby-Phelps K (1993) Cytoarchitecture of size-excluding compartments in living cells. J Cell Sci 106: 565-578.
89. Qin S, Zhou HX (2009) Atomistic modeling of macromolecular crowding predicts modest increases in protein folding and binding stability. Biophys J 97: 12-19.
90. Regan DG, Kuchel PW (2003) Simulations of NMR-detected diffusion in suspensions of red cells: the effects of variation in membrane permeability and observation time. Eur Biophys J 32: 671-675.
91. Ridgway D, Broderick G, Lopez-Campistrous A, Ru'aini M, Winter P, Hamilton M, Boulanger P, Kovalenko P, Ellison M (2008) Coarse-grained molecularsimulation of diffusion and reaction kinetics in a crowdedvirtual cytoplasm. Biophys J 17(5): 493-498.
92. Rotne J, Prager S (1969) Variational treatment of hydrodynamic interaction in polymers. J Chem Phys 50: 4831-4841.
93. Saffman PG, Delbru{double acute}ck M (1975) Brownian motion in biological membranes. Proc Natl Acad Sci USA 72: 3111-3113.
94. Sakaki T, Tsuji A, Chang CH, Ohnishi S (1982) Rotational mobility of an erythrocyte membrane integral protein band 3 in dimyristoylphosphatidylcholine reconstituted vesicles and effect of binding of cytoskeletal peripheral proteins. Biochemistry 21: 2366-2372.
95. Sanabria H, Kubota Y, Waxham MN (2007) Multiple diffusion mechanisms due to nanostructuring in crowded environments. Biophys J 92: 313-322.
96. Saxton MJ (1995) Single-particle tracking: effects of corrals. Biophys J 69: 389-398.
97. Saxton MJ (2007) A biological interpretation of transient anomalous subdiffusion. I. Qualitative model. Biophys J 92: 1178-1191.
98. Saxton MJ (2008) Modeling 2D and 3D diffusion. Methods Mol Biol 400: 295-321.
99. Saxton MJ, Jacobson K (1997) Single Particle Tracking: applications and membrane dynamics. Annu Rev Biophys Biomol Struct 26: 373-399.
100. Schlessinger J, Elson EL, Webb WW, Yahara I, Rutishauser U, Edelmane GM (1977) Receptor diffusion on cell surfaces modulated by locally bound concanavalin A. Proc Natl Acad Sci 74: 1110-1114.
101. Schnell S, Turner TE (2004) Reaction kinetics in intracellular environments with macromolecular crowding: simulations and rate laws. Progr Biophys Mol Biol 85: 235-260.
102. Sear RP (2005) The cytoplasm of living cells: a functional mixture of thousands of components. J Phys Condens Matter 17: S3587-S3595.
103. Sheetz MP, Schindler M, Koppel DE (1980) Lateral mobility of integral membrane proteins is increased in spherocytic erythrocytes. Nature 285: 510-511.
104. Snook I (2006) The Langevin and generalized Langevin approaches to the dynamics of atomic, polymeric and colloidal systems, 1st edn. Elsevier, Amsterdam.
105. Spooner P Jr, Friesen RHE, Knol J, Poolman B, Watts A (2000) Rotational mobility and orientational stability of a transport protein in lipid membranes. Biophys J 79(2): 756-766.
106. Stejskal EO, Tanner JE (1965) Spin diffusion measurements: spin echoes in the presence of a time-dependent field gradient. J Chem Phys 42: 288-292.
107. Sun J, Weinstein H (2007) Towards realistic modelling of dynamic processes in cell signalling: quantification of macromolecular crowding effects. J Chem Phys 127(155105): 1-10.
108. Svedberg T, Pederson KO (1940) The ultracentrifuge. Clarendon Press, Oxford.
109. Szymanski J, Weiss M (2009) Elucidating the origin of anomalous diffusion in crowded fluids. Phys Rev Lett 103: 038102-1-4.
110. Takahashi K, Arjunan SN, Tomita M (2005) Space in systems biology of signaling pathways-towards intracellular molecular crowding in silico. FEBS Lett 579: 1783-1788.
111. Tang C, Iwahara J, Clore GM (2006) Visualization of transient encounter complexes in protein-protein association. Nature 444: 383-386.
112. Tokuyama M, Oppenheim I (1994) Dynamics of hard-sphere suspensions. Phys Rev E 50: R16-R19.
113. Urbina-Villalba G, García-Sucre M, Toro-Mendoza J (2003) Average hydrodynamic correction for the Brownian dynamics calculation of flocculation rates in concentrated dispersions. Phys Rev E Stat Nonlin Soft Matter Phys 68: 061408-1-9.
114. Wade RC (1996) Brownian dynamics simulations of enzyme substrate encounter. Biochem Soc Trans 24: 254-259.
115. Weiss M (2008) Probing the interior of living cells with fluorescence correlation spectroscopy. Ann N Y Acad Sci 1130: 21-27.
116. Wils S, De Schutter E (2009) STEPS: modelling and simulating complex reaction-diffusion systems with python. Front Neuroinformatics 3: 15-23.
117. Zhou HX, Rivas G, Minton AP (2008) Macromolecular crowding and confinement: biochemical, biophysical, and potential physiological consequences. Annu Rev Biophys 37: 375-397.
118. Zimmerman SB, Minton AP (1993) Macromolecular crowding: biochemical, biophysical, and physiological consequences. Annu Rev Biophys Biomol Struct 22: 27-65.
119. Zimmerman SB, Trach SO (1991) Estimation of macromolecule concentrations and excluded volume effects for the cytoplasm of Escherichia coli. J Mol Biol 222: 599-620.
120. Zwanzig R (1969) Langevin theory of polymer dynamics in dilute solution. Adv Chem Phys 15: 325-331.