Monte Carlo simulations of plasma membrane corral-induced EGFR clustering

Journal of Biotechnology

Volumn 151, Issue 3, 2011, Pages 261-270

  Costa, Michelle N ^a,d   Radhakrishnan, Krishnan ^b   Edwards, Jeremy S ^a,c  

^a University of New Mexico   (United States)

^b UNIVERSITY OF NEW MEXICO HEALTH SCIENCES CENTER   (United States)

^c UNIVERSITY OF NEW MEXICO SCHOOL OF MEDICINE   (United States)

^d PACIFIC NORTHWEST NATIONAL LABORATORY   (United States)

Author keywords

Clustering; EGFR; Membrane cytoskeleton; Picket fence; Plasma membrane; Spatial modeling

Indexed keywords

CLUSTERING; EGFR; PICKET FENCES; PLASMA MEMBRANE; SPATIAL MODELING;

CELL MEMBRANES; COMPUTER SIMULATION; CYTOLOGY; DIMERIZATION; FENCES; MONTE CARLO METHODS; PRESSURE EFFECTS; SIGNALING;

MEMBRANES;

DIMER; EPIDERMAL GROWTH FACTOR RECEPTOR; MONOMER;

ARTICLE; CELL COMPARTMENTALIZATION; CELL MEMBRANE; CYTOSKELETON; DIMERIZATION; MATHEMATICAL COMPUTING; MONTE CARLO METHOD; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN PHOSPHORYLATION; SIMULATION;

ALGORITHMS; CELL MEMBRANE; CLUSTER ANALYSIS; COMPUTATIONAL BIOLOGY; FUZZY LOGIC; HUMANS; MEMBRANE MICRODOMAINS; MODELS, BIOLOGICAL; MONTE CARLO METHOD; RECEPTOR, EPIDERMAL GROWTH FACTOR;

EID: 79151468802     PISSN: 01681656     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jbiotec.2010.12.009     Document Type: Article

References (71)

1. Abulrob A., Lu Z., Baumann E., Vobornik D., Taylor R., Stanimirovic D., Johnston L.J. Nanoscale imaging of epidermal growth factor receptor clustering. Effects of inhibitors. J. Biol. Chem. 2010, 285:3145-3156.
2. Allen J.A., Halverson-Tamboli R.A., Rasenick M.M. Lipid raft microdomains and neurotransmitter signalling. Nat. Rev. Neurosci. 2007, 8:128-140.
3. Andrews N.L., Lidke K.A., Pfeiffer J.R., Burns A.R., Wilson B.S., Oliver J.M., Lidke D.S. Actin restricts FcepsilonRI diffusion and facilitates antigen-induced receptor immobilization. Nat. Cell. Biol. 2008, 10:955-963.
4. Bénéteau M., Pizon M., Chaigne-Delalande B., Daburon S., Moreau P., De Giorgi F., Ichas F., Rebillard A., Dimanche-Boitrel M.T., Taupin J.L., Moreau J.F., Legembre P. Localization of Fas/CD95 into the lipid rafts on down-modulation of the phosphatidylinositol-3-kinase signaling pathway. Mol. Can. Res. 2008, 6:604-613.
5. Beres S.B., Sylva G.L., Sturdevant D.E., Granville C.N., Liu M., Ricklefs S.M., Whitney A.R., Parkins L.D., Hoe N.P., Adams G.J., Low D.E., DeLeo F.R., McGeer A., Musser J.M. Genome-wide molecular dissection of serotype M3 group A Streptococcus strains causing two epidemics of invasive infections. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:11833-11838.
6. Bezdek J.C. Pattern Recognition with Fuzzy Objective Function Algorithms (Advanced Applications in Pattern Recognition) 1981, Plenum Press, NY.
7. Brinkerhoff C.J., Woolf P.J., Linderman J.J. Monte Carlo simulations of receptor dynamics: insights into cell signaling. J. Mol. Histol. 2004, 35:667-677.
8. Bublil E.M., Yarden Y. The EGF receptor family: spearheading a merger of signaling and therapeutics. Curr. Opin. Cell. Biol. 2007, 19:124-134.
9. Casalini P.C., Iorio M.V., Galmozzi E., Ménard S. Role of HER receptors family in development and differentiation. J. Cell. Physiol. 2004, 200:343-350.
10. Cherry R.J., Godfrey R.E., Peters R. Mobility of bacteriorhodopsin in lipid vesicles. Biochem. Soc. Trans. 1982, 10:342-343.
11. Chichili G.R., Rodgers W. Clustering of membrane raft proteins by the actin cytoskeleton. J. Biol. Chem. 2007, 282:36682-36691.
12. Clayton A.H.A., Walker F., Orchard S.G., Henderson C., Fuchs D., Rothacker J., Nice E.C., Burgess A.W. Ligand-induced dimer-tetramer transition during the activation of the cell surface epidermal growth factor receptor - a multidimensional microscopy analysis. J. Biol. Chem. 2005, 280:30392-30399.
13. Clayton A.H.A., Tavarnesi M.L., Johns T.G. Unligated epidermal growth factor receptor forms higher order oligomers within microclusters on A431 cells that are sensitive to tyrosine kinase inhibitor binding. Biochemistry 2007, 46:4589-4597.
14. Collins S., Stamatakis M., Vlachos D.G. Adaptive coarse-grained Monte Carlo simulation of reaction and diffusion dynamics in heterogenous plasma membranes. BMC Bioinformatics 2010, 11:218.
15. Danuser G., Waterman-Storer C.M. Quantitative fluorescent speckle microscopy: where it came from and where it is going. J. Microsc. 2003, 211:191-207.
16. Danuser G., Waterman-Storer C.M. Quantitative fluorescent speckle microscopy of cytoskeleton dynamics. Annu. Rev. Biophys. Biomol. Struct. 2006, 35:361-387.
17. Deshpande V.S., McMeeking R.M., Evans A.G. A bio-chemo-mechanical model for cell contractility. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:14015-14020.
18. Dietrich C., Bagatolli L.A., Volovyk Z.N., Thompson N.L., Levi M., Jacobson K., Gratton E. Lipid rafts reconstituted in model membranes. Biophys. J. 2001, 80:1417-1428.
19. Douglass A.D., Vale C.M. Single-molecule microscopy reveals plasma membrane microdomains created by protein-protein networks that exclude or trap signaling molecules in T cells. Cell 2005, 121:937-950.
20. Duke T., Graham I. Equilibrium mechanisms of receptor clustering. Prog. Biophys. Mol. Biol. 2009, 100:18-24.
21. Fujiwara T., Ritchie K., Murakoshi H., Jacobson K., Kusumi A. Phospholipids undergo hop diffusion in compartmentalized cell membrane. J. Cell. Biol. 2002, 157:1071-1081.
22. Ganguly S., Pucadyil T.J., Chattopadhyay A. Actin cytoskeleton-dependent dynamics of the human serotonin1A receptor correlates with receptor signaling. Biophys. J. 2008, 95:451-463.
23. Gopalakrishnan M., Forsten-Williams K., Nugent M.A., Täuber U.W. Effects of receptor clustering on ligand dissociation kinetics: theory and simulations. Biophys. J. 2005, 89:3686-3700.
24. Guo C., Levine H. A thermodynamic model for receptor clustering. Biophys. J. 1999, 77:2358-2365.
25. Hegener O., Prenner L., Runkel F., Baader S.L., Kappler J., Haberlein H. Dynamics of beta2-adrenergic receptor-ligand complexes on living cells. Biochemistry 2004, 43:6190-6199.
26. Heneberg P., Lebduska P., Draberova L., Korb J., Draber P. Topography of plasma membrane microdomains and its consequences for mast cell signaling. Eur. J. Immunol. 2006, 36:2795-2806.
27. Hopkins B., Skellam J.G. A new method for determining the type of distribution of plant individuals. Ann. Bot. 1954, 18(2):213-227.
28. Hynes N.E., MacDonald G. ErbB receptors and signaling pathways in cancer. Curr. Opin. Cell. Biol. 2009, 21:177-184.
29. Jia C., Zhou Z., Liu R., Chen S., Xia R. EGF receptor clustering is induced by a 0.4mT power frequency magnetic field and blocked by the EGF receptor tyrosine kinase inhibitor PD153035. Bioelectromagnetics 2007, 28:197-207.
30. Kholodenko B.N., Demin O.V., Moehren G., Hoek J.B. Quantification of short term signaling by the epidermal growth factor receptor. J. Biol. Chem. 1999, 274:30169-30181.
31. Koyama-Honda I., Ritchie K., Fujiwara T., Iino R., Murakoshi H., Kasai R.S., Kusumi A. Fluorescence imaging for monitoring the colocalization of two single molecules in living cells. Biophys. J. 2005, 88:2126-2136.
32. Kusumi A., Nakada C., Ritchie K., Murase K., Suzuki K., Murakoshi H., Kasai R.S., Kondo J., Fujiwara T. 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. 2005, 34:351-378.
33. Kusumi A., Shira Y.M., Koyama-Honda I., Suzuki K.G.N., Fujiwara T.K. Hierarchial organization of the plasma membrane: investigations by single-molecule tracking vs. fluorescence correlation spectroscopy. FEBS Lett. 2010, 584:1814-1823.
34. Lim K.I., Yin J. Localization of receptors in lipid rafts can inhibit signal transduction. Biotechnol. Bioeng. 2005, 90:694-702.
35. Lo H.W. Nuclear mode of the EGFR signaling network: biology, prognostic value, and therapeutic involvement. Discov. Medc. 2010, 10:44-51.
36. Marmor M.D., Julius M. Role for lipid rafts in regulating interleukin-2 receptor signaling. Blood 2001, 98:1489-1497.
37. Mayawala K., Vlachos D.G., Edwards J.S. Computational modeling reveals molecular details of epidermal growth factor binding. BMC Cell. Biol. 2005, 6:41.
38. Mayawala K., Vlachos D.G., Edwards J.S. Heterogeneities in EGF receptor density at the cell surface can lead to concave up scatchard plot of EGF binding. FEBS Lett. 2005, 579:3043-3047.
39. Miura Y., Hanada K., Jones T.L. G(s) signaling is intact after disruption of lipid rafts. Biochemistry 2001, 18:15418-15423.
40. Morone N., Fujiwara T., Murase K., Kasai R.S., Ike H., Yuasa S., Usukura J., Kusumi A. Three-dimensional reconstruction of the membrane skeleton at the plasma membrane interface by electron tomography. J. Cell. Biol. 2006, 174:851-862.
41. Morone N., Nakada C., Umemura Y., Usukura J., Kusumi A. Three-dimensional molecular architecture of the plasma-membrane-associated cytoskeleton as reconstructed by freeze-etch electron tomography. Methods Cell. Biol. 2008, 88:207-236.
42. Murase K., Fujiwara T., Umemura Y., Suzuki K., Iino R., Yamashita H., Saito M., Murakoshi H., Ritchie K., Kusumi A. Ultrafine membrane compartments for molecular diffusion as revealed by single molecule techniques. Biophys. J. 2004, 86:4075-4093.
43. Nagy P., Vereb G., Sebestyen Z., Horvath G., Lockett S.J., Damjanovich S., Park J.W., Jovin T.M., Szollosi J. Lipid rafts and the local density of ErbB proteins influence the biological role of homo- and heteroassociations of ErbB2. J. Cell. Sci. 2002, 115:4251-4262.
44. Nakada C., Ritchie K., Oba Y., Nakamura M., Hotta Y., Iino R., Kasai R.S., Yamaguchi K., Fujiwara T., Kusumi A. Accumulation of anchored proteins forms membrane diffusion barriers during neuronal polarization. Nat. Cell. Biol. 2003, 5:626-632.
45. Nelson S., Horvat R.D., Malvey J., Roess D.A., Barisas B.G., Clay C.M. Characterization of an intrinsically fluorescent gonadotropin-releasing hormone receptor and effects of ligand binding on receptor lateral diffusion. Endocrinology 1999, 140:950-957.
46. Niehaus A.M., Vlachos D.G., Edwards J.S., Plechac P., Tribe R. Microscopic simulation of membrane molecule diffusion on corralled membrane surfaces. Biophys. J. 2008, 94:1551-1564.
47. Olayioue M.A., Neve R.M., Lane H.A., Hynes N.E. The ErbB signaling network: receptor heterodimerization in development and cancer. EMBO J. 2000, 19:3159-3167.
48. Peters R., Cherry R.J. Lateral and rotational diffusion of bacteriorhodopsin in lipid bilayers: experimental test of the Saffman-Delbruck equations. Proc. Natl. Acad. Sci. U.S.A. 1982, 79:4317-4321.
49. Pike L.J. Lipid rafts: bringing order to chaos. J. Lipid. Res. 2003, 44:655-667.
50. Ritchie K., Iino R., Fujiwara T., Murase K., Kusumi A. The fence and picket structure of the plasma membrane of live cells as revealed by single molecule techniques (Review). Mol. Membr. Biol. 2003, 20:13-18.
51. Ritchie K., Shan X.Y., Kondo J., Iwasawa K., Fujiwara T., Kusumi A. Detection of non-Brownian diffusion in the cell membrane in single molecule tracking. Biophys. J. 2005, 88:2266-2277.
52. Roess D.A., Horvat R.D., Munnelly H., Barisas B.G. Luteinizing hormone receptors are self-associated in the plasma membrane. Endocrinology 2000, 141:4518-4523.
53. Saffarian S., Li Y., Elson E.L., Pike L.J. Oligomerization of the EGF receptor investigated by live cell fluorescence intensity distribution analysis. Biophys. J. 2007, 93:1021-1031.
54. Saffman P.G., Delbruck M. Brownian motion in biological membranes. Proc. Natl. Acad. Sci. U.S.A. 1975, 72:3111-3113.
55. Sasagawa S., Ozaki Y., Fujita K., Kuroda S. Prediction and validation of the distinct dynamics of transient and sustained ERK activation. Nat. Cell. Biol. 2005, 7:365-373.
56. Sebastian S., Settleman J., Reshkin S.J., Azzariti A., Bellizzi A., Paradiso A. The complexity of targeting EGFR signaling in cancer: from expression to turnover. Biochem. Biophys. Acta 2006, 1766:120-139.
57. Sheetz M.P., Sable J.E., Dobereiner H.G. Continuous membrane-cytoskeleton adhesion requires continuous accommodation to lipid and cytoskeleton dynamics. Annu. Rev. Biophys. Biomol. Struct. 2006, 35:417-434.
58. Shi Y. Clustering and signaling of cell receptors. Physica A 2002, 311:199-212.
59. Singer S.J., Nicolson G.L. The fluid mosaic model of the structure of cell membranes. Science 1972, 175:720-731.
60. Snedecor G.W., Cochran W.G. Statistical Methods 1989, Iowa State University Press, Ames.
61. Suzuki K., Ritchie K., Kajikawa E., Fujiwara T., Kusumi A. Rapid hop diffusion of a G-protein-coupled receptor in the plasma membrane as revealed by single-molecule techniques. Biophys. J. 2005, 88:3659-3680.
62. Szabo A., Horvath G., Szollosi J., Nagy P. Quantitative characterization of the large-scale association of ErbB1 and ErbB2 by flow cytometeric homo-FRET measurements. Biophys. J. 2008, 95:2086-2096.
63. Thrane E.V., Schwarze P.E., Thoresen G.H., Lag M., Refsnes M. Persistent versus transient map kinase (ERK) activation in the proliferation of lung epithelial type 2 cells. Exp. Lung. Res. 2001, 27:387-400.
64. Vallotton P., Gupton S.L., Waterman-Storer C.M., Danuser G. Simultaneous mapping of filamentous actin flow and turnover in migrating cells by quantitative fluorescent speckle microscopy. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:9660-9665.
65. Vereb G., Szollosi J., Matko J., Nagy P., Farkas T., Vigh L., Matyus L., Waldmann T.A., Damjanovich S. Dynamic, yet structured: the cell membrane three decades after the Singer-Nicolson model. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:8053-8058.
66. Wilson B.S., Pfeiffer J.R., Raymond-Stintz M.A., Lidke D., Andrews N., Zhang J., Yin W., Steinberg S., Oliver J.M. Exploring membrane domains using native membrane sheets and transmission electron microscopy. Methods Mol. Biol. 2007, 398:245-261.
67. Wisniewska A., Draus J., Subczynski W.K. Is a fluid-mosaic model of biological membranes fully relevant? Studies on lipid organization in model and biological membranes. Cell. Mol. Biol. Lett. 2003, 1(8):7-159.
68. Woolf P.J., Linderman J.J. Self organization of membrane proteins via dimerization. Biophys. Chem. 2003, 104:217-227.
69. Xiao Z., Zhang W., Yang Y., Xu L., Fang X. Single-molecule diffusion study of activated EGFR implicates its endocytic pathway. Biochem. Biophys. Res. Commun. 2008, 369:730-734.
70. Yu C., Hale J., Ritchie K., Prasad N.K., Irudayaraj J. Receptor overexpression or inhibition alters cell surface dynamics of EGF-EGFR interaction: new insights from real-time single molecule analysis. Biochem. Biophys. Res. Commun. 2008, 378:376-382.
71. Zhang J., Leiderman K., Pfeiffer J.R., Wilson B.S., Oliver J.M., Steinberg S.L. Characterizing the topography of membrane receptors and signaling molecules from spatial patterns obtained using nanometer-scale electron-dense probes and electron microscopy. Micron 2006, 37:14-24.