Confining domains lead to reaction bursts: Reaction kinetics in the plasma membrane

PLoS ONE

Volumn 7, Issue 3, 2012, Pages

  Kalay, Ziya ^a   Fujiwara, Takahiro K ^a   Kusumi, Akihiro ^a,b  

^a KYOTO UNIVERSITY   (Japan)

^b KYOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

DIMER; MONOMER; MEMBRANE LIPID; MEMBRANE PROTEIN;

ACTIN FILAMENT; ARTICLE; CELL COMPARTMENTALIZATION; CELL FUNCTION; CELL KINETICS; CELL MEMBRANE; CELL SEPARATION; CELL SURFACE; CELLULAR DISTRIBUTION; CELLULAR PARAMETERS; CHEMICAL REACTION KINETICS; CONTROLLED STUDY; DIFFUSION; EQUILIBRIUM CONSTANT; INTRACELLULAR SIGNALING; MATHEMATICAL COMPUTING; MEMBRANE POTENTIAL; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; MONTE CARLO METHOD; PERMEABILITY BARRIER; PREDICTIVE VALUE; REACTION TIME; ALGORITHM; BIOLOGICAL MODEL; CHEMISTRY; COMPUTER SIMULATION; KINETICS; METABOLISM; TIME;

ALGORITHMS; CELL MEMBRANE; COMPUTER SIMULATION; DIFFUSION; KINETICS; MEMBRANE LIPIDS; MEMBRANE MICRODOMAINS; MEMBRANE PROTEINS; MODELS, BIOLOGICAL; TIME FACTORS;

EID: 84858980359     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0032948     Document Type: Article

References (44)

1. Eldar A, Elowitz MB, (2010) Functional roles for noise in genetic circuits. Nature 467: 167-73.
2. Grecco H, Schmick M, Bastiaens P, (2011) Signaling from the living plasma membrane. Cell 144: 897-909.
3. Mears M, Tarmey DS, Geoghegan M, (2011) Single macromolecule diffusion in confined environments. Macromol Rapid Commun 32: 1411-1418.
4. Nicolau DV, Burrage K, Parton RG, Hancock JF, (2006) Identifying optimal lipid raft characteristics required to promote nanoscale protein-protein interactions on the plasma membrane. Mol Cell Biol 26: 313-323.
5. Wang G, Yau S, (2007) Spatial confinement induced enzyme stability for bioelectronic applications. J Phys Chem C 111: 11921-11926.
6. Schoen I, Krammer H, Braun D, (2009) Hybridization kinetics is different inside cells. Proc Natl Acad Sci USA 106: 21649-54.
7. Ryan T, Myers J, Holowka D, Baird B, Webb W, (1988) Molecular crowding on the cell surface. Science 239: 61-64.
8. Schnell S, Turner T, (2004) Reaction kinetics in intracellular environments with macromolecular crowding: simulations and rate laws. Prog Biophys and Mol Biol 85: 235-260.
9. Grima R, Schnell S, (2006) A systematic investigation of the rate laws valid in intracellular envi- ronments. Biophys Chem 124: 1-10.
10. Singer SJ, Nicolson GL, (1972) The fluid mosaic model of the structure of cell membranes. Science 175: 720-731.
11. Nabi IR, (2011) Cellular Membrane Domains Hoboken, N.J Wiley-Blackwell.
12. Lingwood D, Simons K, (2010) Lipid rafts as a membrane-organizing principle. Science 327: 46-50.
13. Kusumi A, Nakada C, Ritchie K, Murase K, Suzuki K, et al. (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.
14. Chung I, Akita R, Vandlen R, Toomre D, Schlessinger J, et al. (2010) Spatial control of EGF receptor activation by reversible dimerization on living cells. Nature 464: 783-787.
15. Costa MN, Radhakrishnan K, Wilson BS, Vlachos DG, Edwards JS, (2009) Coupled stochastic spatial and non-spatial simulations of ErbB1 signaling pathways demonstrate the importance of spatial organization in signal transduction. PLoS ONE 4: e6316.
16. Costa MN, Radhakrishnan K, Edwards JS, (2011) Monte carlo simulations of plasma membrane corral-induced EGFR clustering. J Biotechnol 151: 261-270.
17. Treanor B, Depoil D, Gonzalez-Granja A, Barral P, Weber M, et al. (2010) The membrane skeleton controls diffusion dynamics and signaling through the b cell receptor. Immunity 32: 187-199.
18. Suzuki KG, Fujiwara TK, Sanematsu F, Iino R, Edidin M, et al. (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.
19. Suzuki KG, Fujiwara TK, Edidin M, Kusumi A, (2007) Dynamic recruitment of phospholipase c at transiently immobilized GPI-anchored receptor clusters induces IP3Ca2+ signaling: single-molecule tracking study 2. J Cell Biol 177: 731-742.
20. Goswami D, Gowrishankar K, Bilgrami S, Ghosh S, Raghupathy R, et al. (2008) Nanoclusters of GPI-anchored proteins are formed by cortical actin-driven activity. Cell 135: 1085-1097.
21. Chaudhuri A, Bhattacharya B, Gowrishankar K, Mayor S, Rao M, (2011) Spatiotemporal regulation of chemical reactions by active cytoskeletal remodeling. Proc Natl Acad Sci USA 108: 14825-14830.
22. Riley M, Buettner H, Muzzio F, Reyes S, (1995) Monte Carlo simulation of diffusion and reaction in two-dimensional cell structures. Biophys J 68: 1716-1726.
23. Saxton MJ, (2002) Chemically limited reactions on a percolation cluster. J Chem Phys 116: 203-208.
24. Fujiwara T, Ritchie K, Murakoshi H, Jacobson K, Kusumi A, (2002) Phospholipids undergo hop diffusion in compartmentalized cell membrane. J Cell Biol 157: 1071-1082.
25. Murase K, Fujiwara T, Umemura Y, Suzuki K, Iino R, et al. (2004) Ultrafine membrane compart- ments for molecular diffusion as revealed by single molecule techniques. Biophys J 86: 4075-4093.
26. Morone N, Fujiwara T, Murase K, Kasai RS, Ike H, et al. (2006) Three-dimensional reconstruction of the membrane skeleton at the plasma membrane interface by electron tomography. J Cell Biol 174: 851-862.
27. Kalay Z, Fujiwara TK, Kusumi A, (2011) pp. 3-22 Cellular Domains, Wiley-Blackwell (Hoboken, NJ), chapter 1.
28. Kusumi A, Suzuki KG, Kasai RS, Ritchie K, Fujiwara TK, (2011) Hierarchical mesoscale domain organization of the plasma membrane. Trends Biochem Sci 36: 604-615.
29. Melo E, Martins J, (2006) Kinetics of bimolecular reactions in model bilayers and biological membranes. a critical review. Biophys Chem 123: 77-94.
30. Fange D, Berg OG, Sjoberg P, Elf J, (2010) Stochastic reaction-diffusion kinetics in the microscopic limit. Proc Natl Acad Sci USA 107: 19820-19825.
31. Grima R, (2010) Intrinsic biochemical noise in crowded intracellular conditions. J Chem Phys 132: 185102-9.
32. Powles JG, Mallett MJD, Rickayzen G, Evans WAB, (1992) Exact analytic solutions for diffusion impeded by an infinite array of partially permeable barriers. Proc R Soc Lond A 436: 391-403.
33. Kenkre VM, Giuggioli L, Kalay Z, (2008) Molecular motion in cell membranes: Analytic study of fence-hindered random walks. Phys Rev E 77: 051907.
34. Calvert PD, Govardovskii VI, Krasnoperova N, Anderson RE, Lem J, et al. (2001) Membrane protein diffusion sets the speed of rod phototransduction. Nature 411: 90-94.
35. Landau LD, Lifshitz EM, (1980) Statistical Physics, Third Edition, Part 1: Volume 5. Butterworth- Heinemann, 3 edition.
36. Mocciaro A, Schiebel E, (2010) Cdc14: a highly conserved family of phosphatases with non-conserved functions? J Cell Sci 123: 2867-2876.
37. Klarlund JK, (1985) Transformation of cells by an inhibitor of phosphatases acting on phosphoty-rosine in proteins. Cell 41: 707-717.
38. Lerea KM, Tonks NK, Krebs EG, Fischer EH, Glomset JA, (1989) Vanadate and molybdate increase tyrosine phosphorylation in a 50-kilodalton protein and stimulate secretion in electropermeabilized platelets. Biochemistry 28: 9286-9292.
39. Heinrich R, Neel BG, Rapoport TA, (2002) Mathematical models of protein kinase signal transduction. Biol Direct 9: 957-970.
40. Cai L, Dalal CK, Elowitz MB, (2008) Frequency-modulated nuclear localization bursts coordinate gene regulation. Nature 455: 485-90.
41. Grima R, (2009) Investigating the robustness of the classical enzyme kinetic equations in small intracellular compartments. BMC Sys Biol 3: 101.
42. Krishnamurthy S, Smith E, Krakauer D, Fontana W, (2007) The stochastic behavior of a molecular switching circuit with feedback. Biology Direct 2: 13.
43. Tyson JJ, Albert R, Goldbeter A, Ruoff P, Sible J, (2008) Biological switches and clocks. Interface Focus 5 (Suppl 1): S1-8.
44. Kasai RS, Suzuki KGN, Prossnitz ER, Koyama-Honda I, Nakada C, et al. (2011) Full characterization of GPCR monomer-dimer dynamic equilibrium by single molecule imaging. J Cell Biol 192: 463-480.