Molecular dynamics simulations of PIP2 and PIP3 in lipid bilayers: Determination of ring orientation, and the effects of surface roughness on a Poisson-Boltzmann description

Biophysical Journal

Volumn 97, Issue 1, 2009, Pages 155-163

  Li, Zheng ^a   Venable, Richard M ^b   Rogers, Laura A ^a   Murray, Diana ^a   Pastor, Richard W ^b  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1 PALMITOYL 2 OLEOYL PHOSPHATIDYLCHOLINE; CHOLINE DERIVATIVE; INOSITOL; LYSINE DERIVATIVE; PENTALYSINE; PHOSPHATIDYLINOSITIDE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; UNCLASSIFIED DRUG;

ARTICLE; CELL MEMBRANE; ELECTRICITY; ENERGY; LIPID BILAYER; MICROSCOPE; MOLECULAR DYNAMICS; SIGNAL TRANSDUCTION;

CHLORIDES; COMPUTER SIMULATION; LIPID BILAYERS; MODELS, CHEMICAL; MODELS, MOLECULAR; PHOSPHATIDYLCHOLINES; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE; PHOSPHATIDYLINOSITOL PHOSPHATES; SODIUM; STATIC ELECTRICITY; SURFACE PROPERTIES; TIME FACTORS;

EID: 68949110664     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2009.04.037     Document Type: Article

References (52)

1. Langner, M., D. Cafiso, S. Marcelja, and S. McLaughlin. 1990. Electrostatics of phosphoinositide bilayer membranes-theoretical and experimental results. Biophys. J. 57:335-349.
2. McLaughlin, S., and D. Murray. 2005. Plasma membrane phosphoinositide organization by protein electrostatics. Nature. 438:605-611.
3. Muller, M., O. Zschornig, S. Ohki, and K. Arnold. 2003. Fusion, leakage and surface hydrophobicity of vesicles containing phosphoinositides: influence of steric and electrostatic effects. J. Membr. Biol. 193:33-43.
4. Yeung, T., G. E. Gilbert, J. Shi, J. Silvius, A. Kapus, et al. 2008. Membrane phosphatidylserine regulates surface charge and protein localization. Science. 319:210-213.
5. Ritter, B., and P. S. McPherson. 2006. There's a GAP in the ENTH domain. Proc. Natl. Acad. Sci. USA. 103:3953-3954.
6. Freed, E. O. 2006. HIV-1 Gag: flipped out for PI(4,5)P-2. Proc. Natl. Acad. Sci. USA. 103:11101-11102.
7. McLaughlin, S. 1989. The electrostatic properties of membranes. Annu. Rev. Biophys. Biophys. Chem. 18:113-136.
8. Heimburg, T., and D. Marsh. 1996. Thermodynamics of the Interaction of Proteins with Lipid Membranes. Birkhauser, Boston.
9. Kim, J., L. Mosio, L. A. Chung, H. Wu, and A. McLaughlin. 1991. Binding of peptides with basic residues to membranes containing acidic phospholipids. Biophys. J. 60:135-148.
10. Wang, J. Y., A. Gambhir, S. McLaughlin, and 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.
11. Bhuiyan, L. B., and C. W. Outhwaite. 2004. Comparison of the modi-fied Poisson-Boltzmann theory with recent density functional theory and simulation results in the planar electric double layer. Phys. Chem. Chem. Phys. 6:3467-3473.
12. Sperotto, M. M., S. May, and A. Baumgaertner. 2006. Modelling of proteins in membranes. Chem. Phys. Lipids. 141:2-29.
13. Baker, N. A., D. Sept, S. Joseph, M. J. Holst, and J. A. McCammon. 2001. Electrostatics of nanosystems: Application to microtubules and the ribosome. Proc. Natl. Acad. Sci. USA. 98:10037-10041.
14. Davis, M. E., and J. A. McCammon. 1990. Electrostatics in biomolecular structure and dynamics. Chem. Rev. 90:509-521.
15. Honig, B., and A. Nicholls. 1995. Classical electrostatics in biology and chemistry. Science. 268:1144-1149.
16. Prabhu, N. V., P. J. Zhu, and K. A. Sharp. 2004. Implementation and testing of stable, fast implicit solvation in molecular dynamics using the smooth-permittivity finite difference Poisson-Boltzmann method. J. Comput. Chem. 25:2049-2064.
17. Sharp, K. A., and B. Honig. 1990. Electrostatic interactions in macromolecules: theory and applications. Annu. Rev. Biophys. Biophys. Chem. 19:301-332.
18. Arbuzova, A., L. Wang, J. Wang, G. Hangyas-Mihalyne, D. Murray, et al. 2000. Membrane binding of peptides containing both basic and aromatic residues. Experimental studies with peptides corresponding to the scaffolding region of caveolin and the effector region of MARCKS. Biochemistry. 39:10330-10339.
19. Ben-Tal, N., B. Honig, C. Miller, and S. McLaughlin. 1997. Electrostatic binding of proteins to membranes: theoretical prediction and experimental results with charybdotoxin and phospholipid vesicles. Biophys. J. 73:1717-1727.
20. Ben-Tal, N., B. Honig, and R. M. Peitzsch. 1996. Binding of small basic peptides to membranes containing acidic lipids: theoretical models and experimental results. Biophys. J. 71:561-575.
21. Bradshaw, J. P., R. J. Bushby, C. C. D. Giles, and M. R. Saunders. 1999. Orientation of the headgroup of phosphatidylinositol in a model biomembrane as determined by neutron diffraction. Biochemistry. 38:8393-8401.
22. Diraviyam, K., R. Stahelin, W. Cho, and D. Murray. 2003. Computer modeling of the membrane interaction of FYVE domains. J. Mol. Biol. 328:721-736.
23. Murray, D., and B. Honig. 2002. Electrostatic control of the membrane targeting of C2 domains. Mol. Cell. 9:145-154.
24. Murray, D., L. H. Matsumoto, C. A. Buser, J. Tsang, C. T. Sigal, et al. 1998. Electrostatics and the membrane association of Src: theory and experiment. Biochemistry. 37:2145-2159.
25. Bradshaw, J. P., R. J. Bushby, C. C. D. Giles, M. R. Saunders, and D. G. Reid. 1996. Neutron diffraction reveals the orientation of the headgroup of inositol lipids in model membranes. Nat. Struct. Biol. 3:125-127.
26. Fisher, S. K., A. M. Heacock, and B. W. Agranoff. 1992. Inositol lipids and signal transduction in the nervous system-an update. J. Neurochem. 58:18-38.
27. Martinez-Seara, H., T. Rog, M. Pasenkiewicz-Gierula, I. Vattulainen, M. Karttunen, et al. 2007. Effect of double bond position on lipid bilayer properties: insight through atomistic simulations. J. Phys. Chem. B. 111:1162-1168.
28. Skibinsky, A., R. M. Venable, and R. W. Pastor. 2005. A molecular dynamics study of the response of lipid bilayers and monolayers to trehalose. Biophys. J. 89:4111-4121.
29. Zhang, Y. H., S. E. Feller, B. R. Brooks, and R. W. Pastor. 1995. Computer-simulation of liquid/liquid interfaces. 1. Theory and application to octane/water. J. Chem. Phys. 103:10252-10266.
30. Feller, S. E., Y. H. Zhang, and R. W. Pastor. 1995. Computer-simulation of liquid/liquid interfaces. 2. Surface-tension area dependence of a bilayer and monolayer. J. Chem. Phys. 103:10267-10276.
31. Kucerka, N., S. Tristram-Nagle, and J. F. Nagle. 2006. Structure of fully hydrated fluid phase lipid bilayers with monounsaturated chains. J. Membr. Biol. 208:193-202.
32. Brooks, B. R., R. E. Bruccoleri, B. D. Olafson, D. J. States, S. Swaminathan, et al. 1983. CHARMM - a program for macromolecular energy, minimization, and dynamics calculations. J. Comput. Chem. 4:187-217.
33. Klauda, J. B., B. R. Brooks, A. D. MacKerell, R. M. Venable, and R. W. Pastor. 2005. An ab initio study on the torsional surface of alkanes and its effect on molecular simulations of alkanes and a DPPC bilayer. J. Phys. Chem. B. 109:5300-5311.
34. Jorgensen, W. L., J. Chandrasekhar, J. D. Madura, R. W. Impey, and M. L. Klein. 1983. Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79:926-935.
35. Durell, S. R., B. R. Brooks, and A. Bennaim. 1994. Solvent-induced forces between 2 hydrophilic groups. J. Phys. Chem. 98:2198-2202.
36. Feller, S. E., and A. D. MacKerell. 2000. An improved empirical potential energy function for molecular dynamics simulations of phospholipids. J. Phys. Chem. B. 104:7510-7515.
37. Klauda, J. B., R. M. Venable, A. D. MacKerell, and R. W. Pastor. 2008. Considerations for lipid force field development. In Current Topics in Membranes: Computational Modeling of Membrane Bilayers. S. E. Feller, editor, Vol. 60. Elsevier, Amsterdam. 1-48.
38. Klauda, J. B., M. F. Roberts, A. G. Redfield, B. R. Brooks, and R. W. Pastor. 2008. Rotation of lipids in membranes: molecular dynamics simulation, P-31 spin-lattice relaxation, and rigid-body dynamics. Biophys. J. 94:3074-3083.
39. Feller, S. E., K. Gawrisch, and A. D. MacKerell. 2002. Polyunsaturated fatty acids in lipid bilayers: intrinsic and environmental contributions to their unique physical properties. J. Am. Chem. Soc. 124:318-326.
40. Darden, T., D. York, and L. Pedersen. 1993. Particle mesh Ewald-an N.Log(N) method for Ewald sums in large systems. J. Chem. Phys. 98:10089-10092.
41. Ryckaert, J. P., G. Ciccotti, and H. J. C. Berendsen. 1977. Numerical integration of Cartesian equations of motion of a system with constraints-molecular dynamics of N-alkanes. J. Comput. Phys. 23:327-341.
42. Gallagher, K., and K. Sharp. 1998. Electrostatic contributions to heat capacity changes of DNA-ligand binding. Biophys. J. 75:769-776.
43. Peitzsch, R. M., M. Eisenberg, K. A. Sharp, and S. McLaughlin. 1995. Calculations of the electrostatic potential adjacent to model phospholipid bilayers. Biophys. J. 68:729-738.
44. Sharp, K. A., and B. Honig. 1990. Calculating total electrostatic energies with the nonlinear Poisson-Boltzmann equation. J. Phys. Chem. 94:7684-7692.
45. Klauda, J. B., N. Kucerka, B. R. Brooks, R. W. Pastor, and J. F. Nagle. 2006. Simulation-based methods for interpreting X-ray data from lipid bilayers. Biophys. J. 90:2796-2807.
46. Freyssingeas, E., D. Roux, and F. Nallet. 1996. The effect of water thickness on the bending rigidity of inverted bilayers. J. Phys. Condens. Matter. 8:2801-2806.
47. Lee, S., Y. Song, and N. A. Baker. 2008. Molecular dynamics simulations of asymmetric NaCl and KCl solutions separated by phosphatidylcholine bilayers: potential drops and structural changes induced by strong Na1-lipid interactions and finite size effects. Biophys. J. 94:3565-3576.
48. Klauda, J. B., B. R. Brooks, and R. W. Pastor. 2006. Dynamical motions of lipids and a finite size effect in simulations of bilayers. J. Chem. Phys. 125:144710.
49. Gambhir, A., G. Hangyas-Mihalyne, I. Zaitseva, D. S. Cafiso, J. Y. Wang, et al. 2004. Electrostatic sequestration of PIP2 on phospholipid membranes by basic/aromatic regions of proteins. Biophys. J. 86:2188-2207.
50. Mulgrew-Nesbitt, A., K. Diraviyam, J. Y. Wang, S. Singh, P. Murray, et al. 2006. The role of electrostatics in protein-membrane interactions. Biochim. Biophys. Acta. 1761:812-826.
51. Lemmon, M. A. 2003. Phosphoinositide recognition domains. Traffic. 4:201-213.
52. Petrey, D., and B. Honig. 2003. GRASP2: visualization, surface properties, and electrostatics of macromolecular structures and sequences. Methods Enzymol. 374:492-509.