Effect of polyelectrolyte adsorption on lateral distribution and dynamics of anionic lipids: a Monte Carlo study of a coarse-grain model

European Biophysics Journal - Tập 43 - Trang 377-391 - 2014
Xiaozheng Duan1, Ran Zhang1, Yunqi Li1, Yongbiao Yang1, Tongfei Shi1, Lijia An1, Qingrong Huang2
1State Key Laboratory of Polymer Physics and Chemistry, Changchun Institute of Applied Chemistry, Chinese Academy of Sciences, Changchun, People’s Republic of China
2Department of Food Science, Rutgers University, New Brunswick, USA

Tóm tắt

We employ Monte Carlo simulations to investigate the interaction between an adsorbing linear flexible cationic polyelectrolyte and a ternary mixed fluid membrane containing neutral (phosphatidylcholine, PC), monovalent (phosphatidylserine, PS), and multivalent (phosphatidylinositol, PIP2) anionic lipids. We systematically explore the influences of polyelectrolyte chain length, polyelectrolyte charge density, polyelectrolyte total charge amount, and salt solution ionic strength on the static and dynamic properties of different anionic lipid species. Our results show that the multivalent PIP2 lipids dominate the polyelectrolyte–membrane interaction and competitively inhibit polyelectrolyte–PS binding. When the total charge amount of the polyelectrolyte is less than that of the local oppositely charged PIP2 lipids, the polyelectrolyte can drag the bound multivalent lipids to diffuse on the membrane, but cannot interact with the PS lipids. Under this condition, the diffusion behaviors of the polyelectrolyte closely follow the prediction of the Rouse model, and the polyelectrolyte chain properties determine the adsorption amount, concentration gradients, and hierarchical mobility of the bound PIP2 lipids. However, when the total charge amount of the polyelectrolyte is larger than that of the local PIP2 lipids, the polyelectrolyte further binds the PS lipids around the polyelectrolyte–PIP2 complex to achieve local electrical neutrality. In this condition, parts of the polyelectrolyte desorb from the membrane and show faster mobility, and the bound PS presents much faster mobility than the segregated PIP2. This work provides an explanation for heterogeneity formation in different anionic lipids induced by polyelectrolyte adsorption.

Tài liệu tham khảo

Akesson T, Woodward C, Jonsson B (1989) Electric double-layer forces in the presence of poly-electrolytes. J Chem Phys 91:2461–2469 Bazzi MD, Nelsestuen GL (1991) Extensive segregation of acidic phospholipids in membranes induced by protein-kinase-C and related proteins. Biochemistry 30:7961–7969 Cai XM, Lietha D, Ceccarelli DF, Karginov AV, Rajfur Z, Jacobson K, Hahn KM, Eck MJ, Schaller MD (2008) Spatial and temporal regulation of focal adhesion kinase activity in living cells. Mol Cell Biol 28:201–214 Cicchetti G, Biernacki M, Farquharson J, Allen PG (2004) A ratiometric expressible FRET sensor for phosphoinositides displays a signal change in highly dynamic membrane structures in fibroblasts. Biochemistry 43:1939–1949 Clausen-Schaumann H, Gaub HE (1999) DNA adsorption to laterally structured charged lipid membranes. Langmuir 15:8246–8251 Czech MP (2000) PIP2 and PIP3: complex roles at the cell surface. Cell 100:603–606 Deme B, Hess D, Tristl M, Lee LT, Sackmann E (2000) Binding of actin filaments to charged lipid monolayers: film balance experiments combined with neutron reflectivity. Eur Phys J E 2:125–136 deMeijere K, Brezesinski G, Mohwald H (1997) Polyelectrolyte coupling to a charged lipid monolayer. Macromolecules 30:2337–2342 Di Paolo G, De Camilli P (2006) Phosphoinositides in cell regulation and membrane dynamics. Nature 443:651–657 Dias RS, Pais A, Linse P, Miguel MG, Lindman B (2005) Polyion adsorption onto catanionic surfaces. A Monte Carlo study. J Phys Chem B 109:11781–11788 Diederich A, Bahr G, Winterhalter M (1998) Influence of polylysine on the rupture of negatively charged membranes. Langmuir 14:4597–4605 Dietrich U, Kruger P, Gutberlet T, Kas JA (2009) Interaction of the MARCKS peptide with PIP(2) in phospholipid monolayers. Biochim Biophys Acta Biomembr 1788:1474–1481 Ding LP, Chi EY, Schanze KS, Lopez GP, Whitten DG (2010) Insight into the mechanism of antimicrobial conjugated polyelectrolytes: lipid headgroup charge and membrane fluidity effects. Langmuir 26:5544–5550 Duan XZ, Li YQ, Zhang R, Shi TF, An LJ, Huang QR (2013a) Regulation of anionic lipids in binary membrane upon the adsorption of polyelectrolyte: a Monte Carlo simulation. AIP Adv 3:062128 Duan XZ, Zhang R, Li YQ, Shi TF, An LJ, Huang QR (2013b) Monte Carlo study of polyelectrolyte adsorption on mixed lipid membrane. J Phys Chem B 117:989–1002 Ferguson CG, James RD, Bigman CS, Shepard DA, Abdiche Y, Katsamba PS, Myszka DG, Prestwich GD (2005) Phosphoinositide-containing polymerized liposomes: stable membrane-mimetic vesicles for protein–lipid binding analysis. Bioconjug Chem 16:1475–1483 Gambhir A, Hangyas-Mihalyne G, Zaitseva I, Cafiso DS, Wang JY, Murray D, Pentyala SN, Smith SO, McLaughlin S (2004) Electrostatic sequestration of PIP2 on phospholipid membranes by basic/aromatic regions of proteins. Biophys J 86:2188–2207 Garnier-Lhomme M, Byrne RD, Hobday TMC, Gschmeissner S, Woscholski R, Poccia DL, Dufourc EJ, Larijani B (2009) Nuclear envelope remnants: fluid membranes enriched in sterols and polyphosphoinositides. PLOS ONE 4(1):e4255 Goldenberg NM, Steinberg BE (2010) Surface charge: a key determinant of protein localization and function. Cancer Res 70:1277–1280 Golebiewska U, Gambhir A, Hangyas-Mihalyne G, Zaitseva I, Radler J, McLaughlin S (2006) Membrane-bound basic peptides sequester multivalent (PIP2), but not monovalent (PS), acidic lipids. Biophys J 91:588–599 Golebiewska U, Nyako M, Woturski W, Zaitseva I, McLaughlin S (2008) Diffusion coefficient of fluorescent phosphatidylinositol 4,5-bisphosphate in the plasma membrane of cells. Mol Biol Cell 19:1663–1669 Haleva E, Ben-Tal N, Diamant H (2004) Increased concentration of polyvalent phospholipids in the adsorption domain of a charged protein. Biophys J 86:2165–2178 Heo WD, Inoue T, Park WS, Kim ML, Park BO, Wandless TJ, Meyer T (2006) PI(3,4,5)P-3 and PI(4,5)P-2 lipids target proteins with polybasic clusters to the plasma membrane. Science 314:1458–1461 Honda A, Nogami M, Yokozeki T, Yamazaki M, Nakamura H, Watanabe H, Kawamoto K, Nakayama K, Morris AJ, Frohman MA, Kanaho Y (1999) Phosphatidylinositol 4-phosphate 5-kinase alpha is a downstream effector of the small G protein ARF6 in membrane ruffle formation. Cell 99:521–532 Im YJ, Perera IY, Brglez I, Davis AJ, Stevenson-Paulik J, Phillippy BQ, Johannes E, Allen NS, Boss WF (2007) Increasing plasma membrane phosphatidylinositol(4,5)bisphosphate biosynthesis increases phosphoinositide metabolism in Nicotiana tabacum. Plant Cell 19:1603–1616 Jan N, Lookman T, Pink DA (1984) On computer-simulation methods used to study models of 2-component lipid bilayers. Biochemistry 23:3227–3231 Kawasaki K (1972) In: Domb C, Greenphase MS (eds) Phase transition and critical phenomena, vol 2. Academic, New York Khelashvili G, Weinstein H, Harries D (2008) Protein diffusion on charged membranes: a dynamic mean-field model describes time evolution and lipid reorganization. Biophys J 94:2580–2597 Kiselev VY, Marenduzzo D, Goryachev AB (2011) Lateral dynamics of proteins with polybasic domain on anionic membranes: a dynamic Monte-Carlo study. Biophys J 100:1261–1270 Kleijn JM, Barten D, Stuart MAC (2004) Adsorption of charged macromolecules at a gold electrode. Langmuir 20:9703–9713 Lemmon MA (2003) Phosphoinositide recognition domains. Traffic 4:201–213 Liu S, Muthukumar M (2002) Langevin dynamics simulation of counterion distribution around isolated flexible polyelectrolyte chains. J Chem Phys 116:9975–9982 Loew S, Hinderliter A, May S (2009) Stability of protein-decorated mixed lipid membranes: the interplay of lipid–lipid, lipid–protein, and protein–protein interactions. J Chem Phys 130(4):045102 Lorenz CD, Faraudo J, Travesset A (2008) Hydrogen bonding and binding of polybasic residues with negatively charged mixed lipid monolayers. Langmuir 24:1654–1658 Maier B, Radler JO (1999) Conformation and self-diffusion of single DNA molecules confined to two dimensions. Phys Rev Lett 82:1911–1914 May S, Harries D, Ben-Shaul A (2000) Lipid demixing and protein–protein interactions in the adsorption of charged proteins on mixed membranes. Biophys J 79:1747–1760 May S, Harries D, Ben-Shaul A (2002) Macroion-induced compositional instability of binary fluid membranes. Phys Rev Lett 89(26):268102 Mbamala EC, Ben-Shaul A, May S (2005) Domain formation induced by the adsorption of charged proteins on mixed lipid membranes. Biophys J 88:1702–1714 McLaughlin S, Murray D (2005) Plasma membrane phosphoinositide organization by protein electrostatics. Nature 438:605–611 McLaughlin S, Wang JY, Gambhir A, Murray D (2002) PIP2 and proteins: interactions, organization, and information flow. Annu Rev Biophys Biomol Struct 31:151–175 Metropolis N, Rosenbluth AW, Rosenbluth MN, Teller AH, Teller E (1953) Equation of state calculations by fast computing machines. J Chem Phys 21:1087–1092 Mitrakos P, Macdonald PM (2000) Polyelectrolyte molecular weight and electrostatically-induced domains in lipid bilayer membranes. Biomacromolecules 1:365–376 Mollapour M, Phelan JP, Millson SH, Piper PW, Cooke FT (2006) Weak acid and alkali stress regulate phosphatidylinositol bisphosphate synthesis in Saccharomyces cerevisiae. Biochem J 395:73–80 Murray D, Arbuzova A, Honig B, McLaughlin S (2002) The role of electrostatic and nonpolar interactions in the association of peripheral proteins with membranes. Pept Lipid Interact 52:277–307 Porcar I, Gomez CM, Perezpaya E, Soria V, Campos A (1994) Macromolecules in ordered media. 1. Interfacial interactions between a cationic polymer and oppositely charged liposomes. Polymer 35:4627–4637 Porcar I, Garcia R, Gomez C, Campos A, Abad C (1997a) Macromolecules in ordered media: 7. Influence of ionic strength and bilayer composition on the association of polyelectrolytes to mixed liposomes. Polymer 38:5107–5113 Porcar I, Garcia R, Soria V, Campos A (1997b) Macromolecules in ordered media: 4. Poly(2-vinyl pyridine)–liposome association induced by electrostatic interactions. Polymer 38:3545–3552 Porcar I, Garcia R, Soria V, Campos A (1997c) Macromolecules in ordered media: 5. Poly(4-vinyl pyridine)–liposome association induced by electrostatic interactions. Polymer 38:3553–3560 Ranaldi G, Marigliano I, Vespignani I, Perozzi G, Sambuy Y (2002) The effect of chitosan and other polycations on tight junction permeability in the human intestinal Caco-2 cell line. J Nutr Biochem 13:157–167 Raudino A, Castelli F (1997) Polyelectrolyte–multicomponent lipid bilayer interactions. Unusual effects on going from the dilute to the semidilute regime. Macromolecules 30:2495–2502 Rouse PE (1953) A theory of the linear viscoelastic properties of dilute solutions of coiling polymers. J Chem Phys 21:1272–1280 Rusu L, Gambhir A, McLaughlin S, Radler J (2004) Fluorescence correlation spectroscopy studies of peptide and protein binding to phospholipid vesicles. Biophys J 87:1044–1053 Santin M, Rhys-Williams W, O’Reilly J, Davies MC, Shakesheff K, Love WG, Lloyd AW, Denyer SP (2006) Calcium-binding phospholipids as a coating material for implant osteointegration. J R Soc Interface 3:277–281 Sarkar J, Annepu H, Sharma A (2011) Contact instability of a soft elastic film bonded to a patterned substrate. J Adhes 87:214–234 Shafir A, Andelman D (2006) Phase behavior of polyelectrolyte–surfactant complexes at planar surfaces. Phys Rev E 74(2):021803 Tall EG, Spector I, Pentyala SN, Bitter I, Rebecchi MJ (2000) Dynamics of phosphatidylinositol 4,5-bisphosphate in actin-rich structures. Curr Biol 10:743–746 Tian WD, Ma YQ (2012) Insights into the endosomal escape mechanism via investigation of dendrimer–membrane interactions. Soft Matter 8:6378–6384 Tzlil S, Ben-Shaul A (2005) Flexible charged macromolecules on mixed fluid lipid membranes: theory and Monte Carlo simulations. Biophys J 89:2972–2987 Tzlil S, Murray D, Ben-Shaul A (2008) The “electrostatic-switch” mechanism: Monte Carlo study of MARCKS–membrane interaction. Biophys J 95:1745–1757 Vance JE, Steenbergen R (2005) Metabolism and functions of phosphatidylserine. Prog Lipid Res 44:207–234 Wang JY, Gambhir A, Hangyas-Mihalyne G, Murray D, Golebiewska U, McLaughlin S (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 Wang JY, Gambhir A, McLaughlin S, Murray D (2004) A computational model for the electrostatic sequestration of PI(4,5)P-2 by membrane-adsorbed basic peptides. Biophys J 86:1969–1986 Wang L, Liang HJ, Wu JZ (2010) Electrostatic origins of polyelectrolyte adsorption: theory and Monte Carlo simulations. J Chem Phys 133(4):044906 Watt SA, Kular G, Fleming IN, Downes CP, Lucocq JM (2002) Subcellular localization of phosphatidylinositol 4,5-bisphosphate using the pleckstrin homology domain of phospholipase C delta(1). Biochem J 363:657–666 Wu CM, Liou W, Chen HL, Lin TL, Jeng US (2004) Self-assembled structure of the binary complex of DNA with cationic lipid. Macromolecules 37:4974–4980 Yan HD, Villalobos C, Andrade R (2009) TRPC channels mediate a muscarinic receptor-induced afterdepolarization in cerebral cortex. J Neurosci 29:10038–10046 Yeh LH, Xue S, Joo SW, Qian S, Hsu JP (2012) Field effect control of surface charge property and electroosmotic flow in nanofluidics. J Phys Chem C 116:4209–4216 Yeung T, Gilbert GE, Shi J, Silvius J, Kapus A, Grinstein S (2008) Membrane phosphatidylserine regulates surface charge and protein localization. Science 319:210–213 Zhdanov VP, Kasemo B (2010) Adsorption of proteins on a lipid bilayer. Eur Biophys J Biophys Lett 39:1477–1482