Effects of detergent β-octylglucoside and phosphate salt solutions on phase behavior of monoolein mesophases.

Using small-angle x-ray scattering (SAXS), we investigated the phase behavior of mesophases of monoolein (MO) mixed with additives commonly used for the crystallization of membrane proteins from lipidic mesophases. In particular, we examined the effect of sodium and potassium phosphate salts and the detergent β-octylglucoside (βOG) over a wide range of compositions relevant for the crystallization of membrane proteins in lipidic mesophases. We studied two types of systems: 1), ternary mixtures of MO with salt solutions above the hydration boundary; and 2), quaternary mixtures of MO with βOG and salt solutions over a wide range of hydration conditions. All quaternary mixtures showed highly regular lyotropic phase behavior with the same sequence of phases (Lα, Ia3d, and Pn3m) as MO/water mixtures at similar temperatures. The effects of additives in quaternary systems agreed qualitatively with those found in ternary mixtures in which only one additive is present. However, quantitative differences in the effects of additives on the lattice parameters of fully hydrated mesophases were found between ternary and quaternary mixtures. We discuss the implications of these findings for mechanistic investigations of membrane protein crystallization in lipidic mesophases and for studies of the suitability of precipitants for mesophase-based crystallization methods.

[1]  C. Kulkarni,et al.  Monoolein: a magic lipid? , 2011, Physical chemistry chemical physics : PCCP.

[2]  D. Harries,et al.  Measured depletion of ions at the biomembrane interface. , 2005, Journal of the American Chemical Society.

[3]  P. Cremer,et al.  Chemistry of Hofmeister anions and osmolytes. , 2010, Annual review of physical chemistry.

[4]  Martin Caffrey,et al.  The Temperature-Composition Phase Diagram and Mesophase Structure Characterization of the Monoolein/Water System , 1996 .

[5]  K. Fendler,et al.  Specific anion and cation binding to lipid membranes investigated on a solid supported membrane. , 2007, Langmuir : the ACS journal of surfaces and colloids.

[6]  T. McIntosh,et al.  A bicontinuous tetrahedral structure in a liquid-crystalline lipid , 1983, Nature.

[7]  R. Stevens,et al.  Development of an Automated High Throughput LCP-FRAP Assay to Guide Membrane Protein Crystallization in Lipid Mesophases. , 2011, Crystal growth & design.

[8]  R. Templer,et al.  Modeling the Phase Behavior of the Inverse Hexagonal and Inverse Bicontinuous Cubic Phases in 2:1 Fatty Acid/Phosphatidylcholine Mixtures , 1998 .

[9]  S. Mizrahi,et al.  Hydration forces underlie the exclusion of salts and of neutral polar solutes from hydroxypropylcellulose. , 2005, The journal of physical chemistry. B.

[10]  J. Rosenbusch,et al.  Molecular mechanism for the crystallization of bacteriorhodopsin in lipidic cubic phases , 2001, FEBS letters.

[11]  K. Meguro,et al.  The effects of inorganic salts and urea on the micellar structure of nonionic surfactant , 1975 .

[12]  E. Sparr,et al.  The effect of bacteriorhodopsin, detergent and hydration on the cubic-to-lamellar phase transition in the monoolein-distearoyl phosphatidyl glycerol-water system. , 2004, Biochimica et biophysica acta.

[13]  B. Ninham,et al.  Possible origin of the inverse and direct Hofmeister series for lysozyme at low and high salt concentrations. , 2011, Langmuir : the ACS journal of surfaces and colloids.

[14]  R. Templer,et al.  Membrane-protein crystallization in cubo: temperature-dependent phase behaviour of monoolein-detergent mixtures. , 2003, Acta crystallographica. Section D, Biological crystallography.

[15]  V. Parsegian,et al.  Measurement of Forces between Hydroxypropylcellulose Polymers: Temperature Favored Assembly and Salt Exclusion , 2001 .

[16]  R. Templer,et al.  Calculations of and evidence for chain packing stress in inverse lyotropic bicontinuous cubic phases. , 2007, Langmuir : the ACS journal of surfaces and colloids.

[17]  S. Gruner,et al.  Structural study of the inverted cubic phases of di-dodecyl alkyl-β-D-glucopyranosyl-rac-glycerol , 1992 .

[18]  V. Cherezov,et al.  Crystallizing membrane proteins using lipidic mesophases , 2009, Nature Protocols.

[19]  T. C. Huang,et al.  X‐ray powder diffraction analysis of silver behenate, a possible low‐angle diffraction standard , 1993 .

[20]  R. Hołyst,et al.  Scattering patterns of self-assembled cubic phases. 1. The model , 2002 .

[21]  R. Templer,et al.  Inverse lyotropic phases of lipids and membrane curvature , 2006, Journal of physics. Condensed matter : an Institute of Physics journal.

[22]  M. Caffrey,et al.  Detergents destabilize the cubic phase of monoolein: implications for membrane protein crystallization. , 2003, Biophysical journal.

[23]  V. Cherezov,et al.  Membrane protein crystallization in lipidic mesophases. A mechanism study using X-ray microdiffraction. , 2007, Faraday discussions.

[24]  Daniel Blankschtein,et al.  Salt effects on intramicellar interactions and micellization of nonionic surfactants in aqueous solutions , 1994 .

[25]  Joshua M. Kunken,et al.  Characterization of lipid matrices for membrane protein crystallization by high-throughput small angle X-ray scattering. , 2011, Methods.

[26]  K. Fontell Cubic phases in surfactant and surfactant-like lipid systems , 1990 .

[27]  V. Gordeliy,et al.  SANS investigations of the lipidic cubic phase behaviour in course of bacteriorhodopsin crystallization , 2005 .

[28]  Towards an understanding of phase transitions between inverse bicontinuous cubic lyotropic liquid crystalline phases , 2010 .

[29]  S. Hyde Microstructure of bicontinuous surfactant aggregates , 1989 .

[30]  Barry W. Ninham,et al.  ‘Zur Lehre von der Wirkung der Salze’ (about the science of the effect of salts): Franz Hofmeister's historical papers , 2004 .

[31]  Michael Grabe,et al.  Protein interactions and membrane geometry. , 2003, Biophysical journal.

[32]  Martin Caffrey,et al.  Membrane protein crystallization in meso: lipid type-tailoring of the cubic phase. , 2002, Biophysical journal.

[33]  D. Sands Introduction to crystallography , 1975 .

[34]  M. Hato,et al.  New lipid family that forms inverted cubic phases in equilibrium with excess water: molecular structure-aqueous phase structure relationship for lipids with 5,9,13,17-tetramethyloctadecyl and 5,9,13,17-tetramethyloctadecanoyl chains. , 2008, The journal of physical chemistry. B.

[35]  R. Stevens,et al.  LCP-FRAP Assay for Pre-Screening Membrane Proteins for in Meso Crystallization. , 2008, Crystal growth & design.

[36]  Chun-Chieh Chan,et al.  Effects of High Salt Concentrations on the Micellization of Octyl Glucoside: Salting-Out of Monomers and Electrolyte Effects on the Micelle−Water Interfacial Tension1 , 2002 .

[37]  V. Cherezov Lipidic cubic phase technologies for membrane protein structural studies. , 2011, Current opinion in structural biology.

[38]  W. N. Maclay Factors affecting the solubility of nonionic emulsifiers , 1956 .

[39]  P. Kenis,et al.  Using macromolecular-crystallography beamline and microfluidic platform for small-angle diffraction studies of lipidic matrices for membrane-protein crystallization. , 2013, Journal of physics. Conference series.

[40]  M. Caffrey,et al.  The curvature elastic-energy function of the lipid–water cubic mesophase , 1994, Nature.

[41]  V. Cherezov,et al.  Crystallization screens: compatibility with the lipidic cubic phase for in meso crystallization of membrane proteins. , 2001, Biophysical journal.

[42]  G. S. Pawley,et al.  Unit-cell refinement from powder diffraction scans , 1981 .

[43]  P. Nollert,et al.  Monoolein Lipid Phases as Incorporation and Enrichment Materials for Membrane Protein Crystallization , 2011, PloS one.

[44]  B. Ninham,et al.  Theory of self-assembly of hydrocarbon amphiphiles into micelles and bilayers , 1976 .

[45]  A. Romero,et al.  The effect of increasing concentrations of precipitating salts used to crystallize proteins on the structure of the lipidic Q224 cubic phase. , 2004, Chemistry and physics of lipids.

[46]  Sophie Le Cann,et al.  High-throughput analysis of the structural evolution of the monoolein cubic phase in situ under crystallogenesis conditions , 2012 .

[47]  R. Aveyard,et al.  Interfacial tensions at alkane-aqueous electrolyte interfaces , 1976 .

[48]  A. Angelova,et al.  X-ray Diffraction Study of the Effect of the Detergent Octyl Glucoside on the Structure of Lamellar and Nonlamellar Lipid/Water Phases of Use for Membrane Protein Reconstitution , 1999 .

[49]  Armel Le Bail,et al.  Ab-initio structure determination of LiSbWO6 by X-ray powder diffraction , 1988 .

[50]  Hiroshi Takahashi,et al.  Effects of salt on the lamellar and bicontinuous cubic phases of fully hydrated monoacylglycerol (monoelaidin) , 2002 .

[51]  C. Kulkarni In Cubo Crystallization of Membrane Proteins , 2010 .

[52]  M. Caffrey Kinetics and mechanism of transitions involving the lamellar, cubic, inverted hexagonal, and fluid isotropic phases of hydrated monoacylglycerides monitored by time-resolved X-ray diffraction. , 1987, Biochemistry.

[53]  V. Cherezov,et al.  Room to move: crystallizing membrane proteins in swollen lipidic mesophases. , 2006, Journal of molecular biology.

[54]  T. Hahn International tables for crystallography , 2002 .

[55]  A. Angelova,et al.  Diamond-type lipid cubic phase with large water channels. , 2003, Journal of the American Chemical Society.

[56]  Sarah L Perry,et al.  An X-ray transparent microfluidic platform for screening of the phase behavior of lipidic mesophases. , 2013, The Analyst.

[57]  V. Cherezov,et al.  Too hot to handle? Synchrotron X-ray damage of lipid membranes and mesophases. , 2002, Journal of synchrotron radiation.

[58]  K. Larsson,et al.  Two cubic phases in monoolein–water system , 1983, Nature.

[59]  P. Garstecki,et al.  Scattering patterns of self-assembled cubic phases. 2. Analysis of the experimental spectra , 2002 .

[60]  C. Baeken,et al.  Controlled In Meso Phase Crystallization – A Method for the Structural Investigation of Membrane Proteins , 2012, PloS one.

[61]  J. Lyons,et al.  Chapter 4 Monoacylglycerols: The Workhorse Lipids for Crystallizing Membrane Proteins in Mesophases , 2009 .

[62]  M. Caffrey,et al.  The phase diagram of the monoolein/water system: metastability and equilibrium aspects. , 2000, Biomaterials.

[63]  M. Caffrey,et al.  Membrane protein crystallization in lipidic mesophases: detergent effects. , 2000, Biophysical journal.

[64]  Hiroshi Takahashi,et al.  Effects of Chaotropic and Kosmotropic Solutes on the Structure of Lipid Cubic Phase: Monoolein-Water Systems , 2000 .

[65]  V. Parsegian,et al.  Salt screening and specific ion adsorption determine neutral-lipid membrane interactions. , 2006, Proceedings of the National Academy of Sciences of the United States of America.