Semihydrophobic nanoparticle-induced disruption of supported lipid bilayers: Specific ion effect

Journal of Physical Chemistry B

Volumn 118, Issue 46, 2014, Pages 13175-13182

  Jing, Benxin ^a   Abot, Rosary C T ^a   Zhu, Yingxi ^a,b  

^a University of Notre Dame   (United States)

^b UNIVERSITY OF NOTRE DAME   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MEMBRANES; CYTOLOGY; DIAGNOSIS; DRUG DELIVERY; HYDROPHOBICITY; NANOPARTICLES; NEGATIVE IONS; PHOSPHOLIPIDS; POSITIVE IONS;

CARBOXYL-FUNCTIONALIZED; HYDROPHOBIC INTERACTIONS; IONIC CONCENTRATIONS; MOLECULAR TRANSPORT; PHOSPHOLIPID BILAYER; POLYSTYRENE NANOPARTICLES; SPECIFIC ION EFFECTS; SUPPORTED LIPID BILAYERS;

LIPID BILAYERS;

ANION; CATION; LIPID BILAYER; NANOPARTICLE; PHOSPHATIDYLCHOLINE;

ATOMIC FORCE MICROSCOPY; CHEMICAL PHENOMENA; CHEMISTRY; LIPID BILAYER; QUARTZ CRYSTAL MICROBALANCE;

ANIONS; CATIONS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; LIPID BILAYERS; MICROSCOPY, ATOMIC FORCE; NANOPARTICLES; PHOSPHATIDYLCHOLINES; QUARTZ CRYSTAL MICROBALANCE TECHNIQUES;

EID: 84912535752     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp5074945     Document Type: Article

References (80)

1. Hofmeister, F. Zur Lehre von der Wirkung der Salze. Naunyn-Schmiedeberg's Arch. Pharmacol. 1888, 24 (4), 247-260.
2. Kunz, W.; Henle, J.; Ninham, B. W. 'Zur Lehre von der Wirkung der Salze' (about the science of the effect of salts): Franz Hofmeister's historical papers. Curr. Opin. Colloid Interface Sci. 2004, 9 (1-2), 19-37.
3. Zhang, F.; Skoda, M. W. A.; Jacobs, R. M. J.; Dressen, D. G.; Martin, R. A.; Martin, C. M.; Clark, G. F.; Lamkemeyer, T.; Schreiber, F. Gold Nanoparticles Decorated with Oligo(ethylene glycol) Thiols: Enhanced Hofmeister Effects in Colloid- Protein Mixtures. J. Phys. Chem. C 2009, 113 (12), 4839-4847.
4. Eggers, D. K.; Valentine, J. S. Molecular confinement influences protein structure and enhances thermal protein stability. Protein Sci. 2001, 10 (2), 250-261.
5. Crevenna, A. H.; Naredi-Rainer, N.; Lamb, D. C.; Wedlich-Söldner, R.; Dzubiella, J. Effects of Hofmeister Ions on the α-Helical Structure of Proteins. Biophys. J. 2012, 102 (4), 907-915.
6. Lo Nostro, P.; Ninham, B. W. Hofmeister Phenomena: An Update on Ion Specificity in Biology. Chem. Rev. 2012, 112 (4), 2286-2322.
7. Petrache, H. I.; Zemb, T.; Belloni, L.; Parsegian, V. A. Salt screening and specific ion adsorption determine neutral-lipid membrane interactions. Proc. Natl. Acad. Sci. U.S.A. 2006, 103 (21), 7982-7987.
8. Clarke, R. J.; Lüpfert, C. Influence of Anions and Cations on the Dipole Potential of Phosphatidylcholine Vesicles: A Basis for the Hofmeister Effect. Biophys. J. 1999, 76 (5), 2614-2624.
9. Binder, H.; Zschörnig, O. The effect of metal cations on the phase behavior and hydration characteristics of phospholipid membranes. Chem. Phys. Lipids 2002, 115 (1-2), 39-61.
10. Leontidis, E.; Aroti, A. Liquid Expanded Monolayers of Lipids As Model Systems to Understand the Anionic Hofmeister Series: 2. Ion Partitioning Is Mostly a Matter of Size. J. Phys. Chem. B 2009, 113 (5), 1460-1467.
11. Leontidis, E.; Aroti, A.; Belloni, L. Liquid Expanded Monolayers of Lipids As Model Systems to Understand the Anionic Hofmeister Series: 1. A Tale of Models. J. Phys. Chem. B 2009, 113 (5), 1447-1459.
12. Vácha, R.; Siu, S. W. I.; Petrov, M.; Böckmann, R. A.; Barucha-Kraszewska, J.; Jurkiewicz, P.; Hof, M.; Berkowitz, M. L.; Jungwirth, P. Effects of Alkali Cations and Halide Anions on the DOPC Lipid Membrane. J. Phys. Chem. A 2009, 113 (26), 7235-7243.
13. Vácha, R.; Jurkiewicz, P.; Petrov, M.; Berkowitz, M. L.; Böckmann, R. A.; Barucha-Kraszewska, J.; Hof, M.; Jungwirth, P. Mechanism of Interaction of Monovalent Ions with Phosphatidylcholine Lipid Membranes. J. Phys. Chem. B 2010, 114 (29), 9504-9509.
14. Aroti, A.; Leontidis, E.; Maltseva, E.; Brezesinski, G. Effects of Hofmeister Anions on DPPC Langmuir Monolayers at the Air-Water Interface. J. Phys. Chem. B 2004, 108 (39), 15238-15245.
15. Sachs, J. N.; Nanda, H.; Petrache, H. I.; Woolf, T. B. Changes in Phosphatidylcholine Headgroup Tilt and Water Order Induced by Monovalent Salts: Molecular Dynamics Simulations. Biophys. J. 2004, 86 (6), 3772-3782.
16. Sachs, J. N.; Woolf, T. B. Understanding the Hofmeister Effect in Interactions between Chaotropic Anions and Lipid Bilayers: Molecular Dynamics Simulations. J. Am. Chem. Soc. 2003, 125 (29), 8742-8743.
17. Garcia-Celma, J. J.; Hatahet, L.; Kunz, W.; Fendler, K. Specific Anion and Cation Binding to Lipid Membranes Investigated on a Solid Supported Membrane. Langmuir 2007, 23 (20), 10074-10080.
18. Leontidis, E.; Aroti, A.; Belloni, L.; Dubois, M.; Zemb, T. Effects of Monovalent Anions of the Hofmeister Series on DPPC Lipid Bilayers Part II: Modeling the Perpendicular and Lateral Equation-of-State. Biophys. J. 2007, 93 (5), 1591-1607.
19. Klasczyk, B.; Knecht, V.; Lipowsky, R.; Dimova, R. Interactions of Alkali Metal Chlorides with Phosphatidylcholine Vesicles. Langmuir 2010, 26 (24), 18951-18958.
20. McLaughlin, S.; Bruder, A.; Chen, S.; Moser, C. Chaotropic anions and the surface potential of bilayer membranes. Biochim. Biophys. Acta, Biomembr. 1975, 394 (2), 304-313.
21. Pabst, G.; Kucerka, N.; Nieh, M. P.; Rheinstädter, M. C.; Katsaras, J. Applications of neutron and X-ray scattering to the study of biologically relevant model membranes. Chem. Phys. Lipids 2010, 163 (6), 460-479.
22. Jungwirth, P.; Tobias, D. J. Specific Ion Effects at the Air/Water Interface. Chem. Rev. 2006, 106 (4), 1259-1281.
23. Collins, K. D.; Washabaugh, M. W. The Hofmeister effect and the behaviour of water at interfaces. Q. Rev. Biophys. 1985, 18 (4), 323-422.
24. Kunz, W.; Lo Nostro, P.; Ninham, B. W. The present state of affairs with Hofmeister effects. Curr. Opin. Colloid Interface Sci. 2004, 9 (1-2), 1-18.
25. Blachechen, L.; Silva, J.; Barbosa, L. S.; Itri, R.; Petri, D. S. Hofmeister effects on the colloidal stability of poly(ethylene glycol)-decorated nanoparticles. Colloid Polym. Sci. 2012, 290 (15), 1537-1546.
26. Tan, S.; Erol, M.; Sukhishvili, S.; Du, H. Substrates with Discretely Immobilized Silver Nanoparticles for Ultrasensitive Detection of Anions in Water Using Surface-Enhanced Raman Scattering. Langmuir 2008, 24 (9), 4765-4771.
27. Deniz, V.; Boström, M.; Bratko, D.; Tavares, F. W.; Ninham, B. W. Specific ion effects: Interaction between nanoparticles in electrolyte solutions. Colloids Surf., A 2008, 319 (1-3), 98-102.
28. Tanaka, T.; Sakai, R.; Kobayashi, R.; Hatakeyama, K.; Matsunaga, T. Contributions of Phosphate to DNA Adsorption/Desorption Behaviors on Aminosilane-Modified Magnetic Nanoparticles. Langmuir 2009, 25 (5), 2956-2961.
29. Nelson, E. M.; Rothberg, L. J. Kinetics and Mechanism of Single-Stranded DNA Adsorption onto Citrate-Stabilized Gold Nanoparticles in Colloidal Solution. Langmuir 2011, 27 (5), 1770-1777.
30. López-León, T.; Jódar-Reyes, A. B.; Bastos-González, D.; Ortega-Vinuesa, J. L. Hofmeister Effects in the Stability and Electrophoretic Mobility of Polystyrene Latex Particles. J. Phys. Chem. B 2003, 107 (24), 5696-5708.
31. Zhang, Y.; Cremer, P. S. Chemistry of Hofmeister Anions and Osmolytes. Annu. Rev. Phys. Chem. 2010, 61 (1), 63-83.
32. Yang, Q.; Zhao, J. Hofmeister Effect on the Interfacial Dynamics of Single Polymer Molecules. Langmuir 2011, 27 (19), 11757-11760.
33. Cacace, M. G.; Landau, E. M.; Ramsden, J. J. The Hofmeister series: salt and solvent effects on interfacial phenomena. Q. Rev. Biophys. 1997, 30 (03), 241-277.
34. López-León, T.; Ortega-Vinuesa, J. L.; Bastos-González, D. Ion-Specific Aggregation of Hydrophobic Particles. ChemPhysChem 2012, 13 (9), 2382-2391.
35. López-León, T.; Santander-Ortega, M. J.; Ortega-Vinuesa, J. L.; Bastos- González, D. Hofmeister Effects in Colloidal Systems: Influence of the Surface Nature. J. Phys. Chem. C 2008, 112 (41), 16060-16069.
36. Schwierz, N.; Horinek, D.; Netz, R. R. Reversed Anionic Hofmeister Series: The Interplay of Surface Charge and Surface Polarity. Langmuir 2010, 26 (10), 7370-7379.
37. Calero, C.; Faraudo, J.; Bastos-González, D. Interaction of Monovalent Ions with Hydrophobic and Hydrophilic Colloids: Charge Inversion and Ionic Specificity. J. Am. Chem. Soc. 2011, 133 (38), 15025-15035.
38. Tobias, D. J.; Hemminger, J. C. Getting specific about specific ion effects. Science 2008, 319 (5867), 1197-1198.
39. Smith, J. D.; Saykally, R. J.; Geissler, P. L. The Effects of Dissolved Halide Anions on Hydrogen Bonding in Liquid Water. J. Am. Chem. Soc. 2007, 129 (45), 13847-13856.
40. Zangi, R. Can Salting-In/Salting-Out Ions be Classified as Chaotropes/Kosmotropes? J. Phys. Chem. B 2010, 114 (1), 643-650.
41. Mancinelli, R.; Botti, A.; Bruni, F.; Ricci, M. A.; Soper, A. K. Hydration of Sodium, Potassium, and Chloride Ions in Solution and the Concept of Structure Maker/Breaker. J. Phys. Chem. B 2007, 111 (48), 13570-13577.
42. Zangi, R.; Hagen, M.; Berne, B. J. Effect of Ions on the Hydrophobic Interaction between Two Plates. J. Am. Chem. Soc. 2007, 129 (15), 4678-4686.
43. Lund, M.; Jungwirth, P.; Woodward, C. E. Ion Specific Protein Assembly and Hydrophobic Surface Forces. Phys. Rev. Lett. 2008, 100 (25), 258105.
44. Peula-García, J. M.; Ortega-Vinuesa, J. L.; Bastos-González, D. Inversion of Hofmeister Series by Changing the Surface of Colloidal Particles from Hydrophobic to Hydrophilic. J. Phys. Chem. C 2010, 114 (25), 11133-11139.
45. dos Santos, A. P.; Levin, Y. Ion Specificity and the Theory of Stability of Colloidal Suspensions. Phys. Rev. Lett. 2011, 106 (16), 167801.
46. An Inventory of Nanotechnology-based Consumer Products Currently on the Market. http://www.nanotechproject.org/cpi/about/analysis/, accessed Nov 6, 2014.
47. Lewinski, N.; Colvin, V.; Drezek, R. Cytotoxicity of nanoparticles. Small 2008, 4 (1), 26-49.
48. Schulz, M.; Olubummo, A.; Binder, W. H. Beyond the lipidbilayer: interaction of polymers and nanoparticles with membranes. Soft Matter 2012, 8 (18), 4849-4864.
49. Moghimi, S. M.; Hunter, A. C.; Murray, J. C. Nanomedicine: current status and future prospects. FASEB J. 2005, 19 (3), 311-330.
50. Von White, G.; Chen, Y.; Roder-Hanna, J.; Bothun, G. D.; Kitchens, C. L. Structural and Thermal Analysis of Lipid Vesicles Encapsulating Hydrophobic Gold Nanoparticles. ACS Nano 2012, 6 (6), 4678-4685.
51. Li, Y.; Chen, X.; Gu, N. Computational Investigation of Interaction between Nanoparticles and Membranes: Hydrophobic/Hydrophilic Effect. J. Phys. Chem. B 2008, 112 (51), 16647-16653.
52. Hong, S.; Bielinska, A. U.; Mecke, A.; Keszler, B.; Beals, J. L.; Shi, X.; Balogh, L.; Orr, B. G.; Baker, J. R.; Banaszak Holl, M. M. Interaction of Poly(amidoamine) Dendrimers with Supported Lipid Bilayers and Cells: Hole Formation and the Relation to Transport. Bioconjugate Chem. 2004, 15 (4), 774-782.
53. Mecke, A.; Uppuluri, S.; Sassanella, T. M.; Lee, D.-K.; Ramamoorthy, A.; Baker, J. J. R.; Orr, B. G.; Banaszak Holl, M. M. Direct observation of lipid bilayer disruption by poly(amidoamine) dendrimers. Chem. Phys. Lipids 2004, 132 (1), 3-14.
54. Wang, B.; Zhang, L.; Bae, S. C.; Granick, S. Nanoparticleinduced surface reconstruction of phospholipid membranes. Proc. Natl. Acad. Sci. U.S.A. 2008, 105 (47), 18171-18175.
55. Grillo, D.; Olvera de la Cruz, M.; Szleifer, I. Theoretical studies of the phase behavior of DPPC bilayers in the presence of macroions. Soft Matter 2011, 7 (10), 4672-4679.
56. Prates Ramalho, J. P.; Gkeka, P.; Sarkisov, L. Structure and Phase Transformations of DPPC Lipid Bilayers in the Presence of Nanoparticles: Insights from Coarse-Grained Molecular Dynamics Simulations. Langmuir 2011, 27 (7), 3723-3730.
57. Jing, B.; Hutin, M.; Connor, E.; Cronin, L.; Zhu, Y. Polyoxometalate Macroion Induced Phase and Morphology Instability of Lipid Membrane. Chem. Sci. 2012, 4 (10), 3818-3826.
58. Jing, B.; Zhu, Y. Disruption of Supported Lipid Bilayers by Semihydrophobic Nanoparticles. J. Am. Chem. Soc. 2011, 133 (28), 10983-10989.
59. Morrissey, J. H. Morrissey Lab Protocol for Preparing Phospholipid Vesicles (SUV) by Sonication. http://avantilipids.com/images/PDF/MorrisseyLabProtocolForPrepSuvBySonication.pdf.
60. Wang, L.; Friesner, R. A.; Berne, B. J. Competition of Electrostatic and Hydrophobic Interactions between Small Hydrophobes and Model Enclosures. J. Phys. Chem. B 2010, 114 (21), 7294-7301.
61. Avrami, M. Kinetics of Phase Change. I General Theory. J. Chem. Phys. 1939, 7 (12), 1103-1112.
62. Avrami, M. Kinetics of Phase Change. II Transformation-Time Relations for Random Distribution of Nuclei. J. Chem. Phys. 1940, 8 (2), 212-224.
63. Avrami, M. Granulation, Phase Change, and Microstructure Kinetics of Phase Change. III. J. Chem. Phys. 1941, 9 (2), 177-184.
64. Nagle, J. F.; Tristram-Nagle, S. Structure of lipid bilayers. Biochim. Biophys. Acta, Rev. Biomembr. 2000, 1469 (3), 159-195.
65. Meyer, E. E.; Rosenberg, K. J.; Israelachvili, J. Recent progress in understanding hydrophobic interactions. Proc. Natl. Acad. Sci. U.S.A. 2006, 103 (43), 15739-15746.
66. Israelachvili, J.; Pashley, R. The hydrophobic interaction is long range, decaying exponentially with distance. Nature 1982, 300 (5890), 341-342.
67. Zavitsas, A. A. Properties of Water Solutions of Electrolytes and Nonelectrolytes. J. Phys. Chem. B 2001, 105 (32), 7805-7817.
68. Pegram, L. M.; Record, M. T., Jr. Quantifying accumulation or exclusion of H+, HO-, and Hofmeister salt ions near interfaces. Chem. Phys. Lett. 2008, 467 (1-3), 1-8.
69. Haverd, V. E.; Warr, G. G. Cation Selectivity at Air/Anionic Surfactant Solution Interfaces. Langmuir 2000, 16 (1), 157-160.
70. Klein, R.; Kellermeier, M.; Drechsler, M.; Touraud, D.; Kunz, W. Solubilisation of stearic acid by the organic base choline hydroxide. Colloids Surf., A 2009, 338 (1-3), 129-134.
71. Annapureddy, H. V. R.; Dang, L. X. Molecular Mechanism of Specific Ion Interactions between Alkali Cations and Acetate Anion in Aqueous Solution: A Molecular Dynamics Study. J. Phys. Chem. B 2012, 116 (25), 7492-7498.
72. Hess, B.; van der Vegt, N. F. A. Cation specific binding with protein surface charges. Proc. Natl. Acad. Sci. U.S.A. 2009, 106 (32), 13296-13300.
73. Kherb, J.; Flores, S. C.; Cremer, P. S. Role of Carboxylate Side Chains in the Cation Hofmeister Series. J. Phys. Chem. B 2012, 116 (25), 7389-7397.
74. Uejio, J. S.; Schwartz, C. P.; Duffin, A. M.; Drisdell, W. S.; Cohen, R. C.; Saykally, R. J. Characterization of selective binding of alkali cations with carboxylate by x-ray absorption spectroscopy of liquid microjets. Proc. Natl. Acad. Sci. U.S.A. 2008, 105 (19), 6809-6812.
75. Aziz, E. F.; Ottosson, N.; Eisebitt, S.; Eberhardt, W.; Jagoda-Cwiklik, B.; Vácha, R.; Jungwirth, P.; Winter, B. Cation-Specific Interactions with Carboxylate in Amino Acid and Acetate Aqueous Solutions: X-ray Absorption and ab initio Calculations. J. Phys. Chem. B 2008, 112 (40), 12567-12570.
76. Vrbka, L.; Vondrášek, J.; Jagoda-Cwiklik, B.; Vácha, R.; Jungwirth, P. Quantification and rationalization of the higher affinity of sodium over potassium to protein surfaces. Proc. Natl. Acad. Sci. U.S.A. 2006, 103 (42), 15440-15444.
77. Collins, K. D. Ions from the Hofmeister series and osmolytes: effects on proteins in solution and in the crystallization process. Methods 2004, 34 (3), 300-311.
78. Collins, K. D. Ion hydration: Implications for cellular function, polyelectrolytes, and protein crystallization. Biophys. Chem. 2006, 119 (3), 271-281.
79. Marcus, Y.; Loewenschuss, A. Chapter 4. Standard entropies of hydration of ions. Annu. Rep. Prog. Chem., Sect. C: Phys. Chem. 1984, 81, 81-135.
80. Graziano, G. On the salting in effect of tetraalkylammonium bromides. Chem. Phys. Lett. 2011, 505 (1-3), 26-30.