Lateral dynamics of proteins with polybasic domain on anionic membranes: A dynamic Monte-Carlo study

Biophysical Journal

Volumn 100, Issue 5, 2011, Pages 1261-1270

  Kiselev, Vladimir Yu ^a   Marenduzzo, Davide ^a   Goryachev, Andrew B ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 79953841393     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2011.01.025     Document Type: Article

References (65)

1. Kiessling, V., C. Wan, and L. K. Tamm. 2009. Domain coupling in asymmetric lipid bilayers. Biochim. Biophys. Acta. 1788:64-71.
2. Mulgrew-Nesbitt, A., K. Diraviyam, D. Murray. 2006. The role of electrostatics in protein-membrane interactions. Biochim. Biophys. Acta. 1761:812-826. (Pubitemid 44332331)
3. McLaughlin, S., and D. Murray. 2005. Plasma membrane phosphoinositide organization by protein electrostatics. Nature. 438:605-611. (Pubitemid 41740564)
4. Fivaz, M., and T. Meyer. 2003. Specific localization and timing in neuronal signal transduction mediated by protein-lipid interactions. Neuron. 40:319-330. (Pubitemid 37244098)
5. Hammond, G. R., Y. Sim, .. , R. F. Irvine. 2009. Reversible binding and rapid diffusion of proteins in complex with inositol lipids serves to coordinate free movement with spatial information. J. Cell Biol. 184:297-308.
6. Hancock, J. F., H. Paterson, and C. J. Marshall. 1990. A polybasic domain or palmitoylation is required in addition to the CAAX motif to localize p21ras to the plasma membrane. Cell. 63:133-139.
7. Murray, D., L. Hermida-Matsumoto, S. McLaughlin. 1998. Electrostatics and the membrane association of Src: theory and experiment. Biochemistry. 37:2145-2159. (Pubitemid 28119288)
8. McLaughlin, S., and A. Aderem. 1995. The myristoyl-electrostatic switch: a modulator of reversible protein-membrane interactions. Trends Biochem. Sci. 20:272-276.
9. Wang, J., A. Gambhir, ..., S. McLaughlin. 2002. Lateral sequestration of phosphatidylinositol 4,5-bisphosphate by the basic effector domain of myristoylated alanine-rich C kinase substrate is due to nonspecific electrostatic interactions. J. Biol. Chem. 277:34401-34412.
10. Das, S., J. E. Dixon, and W. Cho. 2003. Membrane-binding and activation mechanism of PTEN. Proc. Natl. Acad. Sci. USA. 100:7491-7496. (Pubitemid 36759997)
11. Heo, W. D., T. Inoue, T. Meyer. 2006. PI(3,4,5)P3 and PI(4,5)P2 lipids target proteins with polybasic clusters to the plasma membrane. Science. 314:1458-1461. (Pubitemid 44871952)
12. Magalhaes, M. A., and M. Glogauer. 2010. Pivotal advance: phospholipids determine net membrane surface charge resulting in differential localization of active Rac1 and Rac2. J. Leukoc. Biol. 87:545-555.
13. Abankwa, D., A. A. Gorfe, and J. F. Hancock. 2007. Ras nanoclusters: molecular structure and assembly. Semin. Cell Dev. Biol. 18:599-607. (Pubitemid 350026427)
14. Kenworthy, A. K. 2007. Nanoclusters digitize Ras signalling. Nat. Cell Biol. 9:875-877. (Pubitemid 47190440)
15. Day, C. A., and A. K. Kenworthy. 2009. Tracking microdomain dynamics in cell membranes. Biochim. Biophys. Acta. 1788:245-253.
16. Goryachev, A. B., and A. V. Pokhilko. 2008. Dynamics of Cdc42 network embodies a Turing-type mechanism of yeast cell polarity. FEBS Lett. 582:1437-1443.
17. Singer, S. J., and G. L. Nicolson. 1972. The fluid mosaic model of the structure of cell membranes. Science. 175:720-731.
18. Saffman, P. G., and M. Delbruck. 1975. Brownian motion in biological membranes. Proc. Natl. Acad. Sci. USA. 72:3111-3113.
19. Axelrod, D. 1983. Lateral motion of membrane proteins and biological function. J. Membr. Biol. 75:1-10.
20. Chen, Y., B. C. Lagerholm, ..., K. Jacobson. 2006. Methods to measure the lateral diffusion of membrane lipids and proteins. Methods. 39:147-153. (Pubitemid 44107712)
21. Tamm, L. K., and H. M. McConnell. 1985. Supported phospholipid bilayers. Biophys. J. 47:105-113.
22. Zhang, F., B. Crise, K. Jacobson. 1991. Lateral diffusion of membrane-spanning and glycosylphosphatidylinositol-linked proteins: toward establishing rules governing the lateral mobility of membrane proteins. J. Cell Biol. 115:75-84. (Pubitemid 21909895)
23. Tamm, L. K. 1988. Lateral diffusion and fluorescence microscope studies on a monoclonal antibody specifically bound to supported phospholipid bilayers. Biochemistry. 27:1450-1457. (Pubitemid 18077442)
24. Stefl, M., A. Kulakowska, and M. Hof. 2009. Simultaneous characterization of lateral lipid and prothrombin diffusion coefficients by z-scan fluorescence correlation spectroscopy. Biophys. J. 97, L01-L03.
25. Gilmanshin, R., C. E. Creutz, and L. K. Tamm. 1994. Annexin IV reduces the rate of lateral lipid diffusion and changes the fluid phase structure of the lipid bilayer when it binds to negatively charged membranes in the presence of calcium. Biochemistry. 33:8225-8232. (Pubitemid 24241055)
26. Golebiewska, U., M. Nyako, ..., S. McLaughlin. 2008. Diffusion coefficient of fluorescent phosphatidylinositol 4,5-bisphosphate in the plasma membrane of cells. Mol. Biol. Cell. 19:1663-1669. (Pubitemid 351805118)
27. Haugh, J. M., F. Codazzi, ..., T. Meyer. 2000. Spatial sensing in fibroblasts mediated by 3' phosphoinositides. J. Cell Biol. 151:1269-1280.
28. Yaradanakul, A., and D. W. Hilgemann. 2007. Unrestricted diffusion of exogenous and endogenous PIP(2)in baby hamster kidney and Chinese hamster ovary cell plasmalemma. J. Membr. Biol. 220:53-67. (Pubitemid 50003532)
29. Golebiewska, U., A. Gambhir, . , S. McLaughlin. 2006. Membranebound basic peptides sequester multivalent (PIP2), but not monovalent (PS), acidic lipids. Biophys. J. 91:588-599.
30. Shvartsman, D. E., J. C. Donaldson, . , Y. I. Henis. 2007. Src kinase activity and SH2 domain regulate the dynamics of Src association with lipid and protein targets. J. Cell Biol. 178:675-686. (Pubitemid 47267278)
31. Lu, S., M. Ouyang, Y. Wang. 2008. The spatiotemporal pattern of Src activation at lipid rafts revealed by diffusion-corrected FRET imaging. PLOS Comput. Biol. 4:e1000127.
32. Larson, D. R., J. A. Gosse, ..., W. W. Webb. 2005. Temporally resolved interactions between antigen-stimulated IgE receptors and Lyn kinase on living cells. J. Cell Biol. 171:527-536. (Pubitemid 41586941)
33. Frick, M., K. Schmidt, and B. J. Nichols. 2007. Modulation of lateral diffusion in the plasma membrane by protein density. Curr. Biol. 17:462-467.
34. Pyenta, P. S., P. Schwille, B. Baird. 2003. Lateral diffusion of membrane lipid-anchored probes before and after aggregation of cell surface IgE-receptors. J. Phys. Chem. A. 107:8310-8318.
35. Zimmermann, L., W. Paster, ..., G. J. Schutz. 2010. Direct observation and quantitative analysis of Lck exchange between plasma membrane and cytosol in living T cells. J. Biol. Chem. 285:6063-6070.
36. Niv, H., O. Gutman, ..., Y. I. Henis. 2002. Activated K-Ras and H-Ras display different interactions with saturable nonraft sites at the surface of live cells. J. Cell Biol. 157:865-872. (Pubitemid 34847823)
37. Goodwin, J. S., K. R. Drake, . , A. K. Kenworthy. 2005. Ras diffusion is sensitive to plasma membrane viscosity. Biophys. J. 89:1398-1410. (Pubitemid 41099021)
38. Gambhir, A., G. Hangyas-Mihalyne, . , S. McLaughlin. 2004. Electrostatic sequestration of PIP2 on phospholipid membranes by basic/aromatic regions of proteins. Biophys. J. 86:2188-2207. (Pubitemid 38524409)
39. Saxton, M. J. 1989. Lateral diffusion in an archipelago. Distance dependence of the diffusion coefficient. Biophys. J. 56:615-622.
40. Sung, B. J., and A. Yethiraj. 2009. Computer simulations of protein diffusion in compartmentalized cell membranes. Biophys. J. 97: 472-479.
41. Haugh, J. M. 2009. Analysis of reaction-diffusion systems with anomalous subdiffusion. Biophys. J. 97:435-442.
42. Gil, T., J. H. Ipsen, . , M. J. Zuckermann. 1998. Theoretical analysis of protein organization in lipid membranes. Biochim. Biophys. Acta. 1376:245-266. (Pubitemid 28517880)
43. Wang, J., A. Gambhir, . , D. Murray. 2004. A computational model for the electrostatic sequestration of PI(4,5)P2 by membrane-adsorbed basic peptides. Biophys. J. 86:1969-1986. (Pubitemid 38524391)
44. Tzlil, S., D. Murray, and A. Ben-Shaul. 2008. The " electrostaticswitch" mechanism: Monte Carlo study of MARCKS-membrane interaction. Biophys. J. 95:1745-1757.
45. Tzlil, S., and A. Ben-Shaul. 2005. Flexible charged macromolecules on mixed fluid lipid membranes: theory and Monte Carlo simulations. Biophys. J. 89:2972-2987. (Pubitemid 41636054)
46. Murray, D., A. Arbuzova, . , S. McLaughlin. 1999. Electrostatic properties of membranes containing acidic lipids and adsorbed basic peptides: theory and experiment. Biophys. J. 77:3176-3188.
47. Haleva, E., N. Ben-Tal, and H. Diamant. 2004. Increased concentration of polyvalent phospholipids in the adsorption domain of a charged protein. Biophys. J. 86:2165-2178. (Pubitemid 38524407)
48. Denisov, G., S. Wanaski, . , S. McLaughlin. 1998. Binding of basic peptides to membranes produces lateral domains enriched in the acidic lipids phosphatidylserine and phosphatidylinositol 4,5-bisphosphate: an electrostatic model and experimental results. Biophys. J. 74:731-744. (Pubitemid 28345268)
49. BenTal, N., B. Honig, S. McLaughlin. 1996. Binding of small basic peptides to membranes containing acidic lipids: Theoretical models and experimental results. Biophys. J. 71:561-575. (Pubitemid 26289141)
50. Heimburg, T., B. Angerstein, and D. Marsh. 1999. Binding of peripheral proteins to mixed lipid membranes: Effect of lipid demixing upon binding. Biophys. J. 76:2575-2586. (Pubitemid 29264617)
51. May, S., D. Harries, and A. Ben-Shaul. 2000. Lipid demixing and protein-protein interactions in the adsorption of charged proteins on mixed membranes. Biophys. J. 79:1747-1760.
52. Mbamala, E. C., A. Ben-Shaul, and S. May. 2005. Domain formation induced by the adsorption of charged proteins on mixed lipid membranes. Biophys. J. 88:1702-1714. (Pubitemid 40976187)
53. Hinderliter, A., P. F. F. Almeida, R. L. Biltonen. 2001. Domain formation in a fluid mixed lipid bilayer modulated through binding of the C2 protein motif. Biochemistry. 40:4181-4191. (Pubitemid 32280456)
54. Khelashvili, G., H. Weinstein, and D. Harries. 2008. Protein diffusion on charged membranes: a dynamic mean-field model describes time evolution and lipid reorganization. Biophys. J. 94:2580-2597.
55. Petrache, H. I., S. W. Dodd, and M. F. Brown. 2000. Area per lipid and acyl length distributions in fluid phosphatidylcholines determined by H-2 NMR spectroscopy. Biophys. J. 79:3172-3192.
56. Murray, D., N. Ben-Tal, S. McLaughlin. 1997. Electrostatic interaction of myristoylated proteins with membranes: simple physics, complicated biology. Structure. 5:985-989. (Pubitemid 27393084)
57. Kawasaki, K. 1972. In Phase Transition and Critical Phenomena, Vol. 2, C. Domb and M. S. Green, editors. Academic Press, New York.
58. Jan, N., T. Lookman, and D. A. Pink. 1984. On computer-simulation methods used to study models of 2-component lipid bilayers. Biochemistry. 23:3227-3231.
59. Whitelam, S., and P. L. Geissler. 2007. Avoiding unphysical kinetic traps in Monte Carlo simulations of strongly attractive particles. J. Chem. Phys. 127:154101.
60. Kunitz, M. 1926. An empirical formula for the relation between viscosity of solution and volume of solute. J. Gen. Physiol. 9:715-725.
61. Golestanian, R., T. B. Liverpool, and A. Ajdari. 2005. Propulsion of a molecular machine by asymmetric distribution of reaction products. Phys. Rev. Lett. 94:220801.
62. Anderson, J. L. 1989. Colloid transport by interfacial forces. Annu. Rev. Fluid Mech. 21:61-99.
63. Marsh, D. 2008. Protein modulation of lipids, and vice-versa, in membranes. Biochim. Biophys. Acta. 1778:75.
64. Han, J. J., and D. W. Boo. 2009. Reversible immobilization of diffusive membrane-associated proteins using a liquid-gel bilayer phase transition: a case study of Annexin V monomers. Langmuir. 25:3083-3088.
65. Cazzolli, R., A. N. Shemon, . , W. E. Hughes. 2006. Phospholipid signalling through phospholipase D and phosphatidic acid. IUBMB Life. 58:457-461. (Pubitemid 44266905)