Using small-angle neutron scattering to detect nanoscopic lipid domains

Chemistry and Physics of Lipids

Volumn 170-171, Issue , 2013, Pages 19-32

  Pan, Jianjun ^a   Heberle, Frederick A ^a   Petruzielo, Robin S ^b   Katsaras, John ^a,c  

^a OAK RIDGE NATIONAL LABORATORY   (United States)

^b Cornell University   (United States)

^c NATIONAL RESEARCH COUNCIL CANADA   (Canada)

Author keywords

Contrast matching; Domain size; Line tension; Phase coexistence; Phase separation; Thickness mismatch

Indexed keywords

LIPID;

CELL MEMBRANE; LIPID COMPOSITION; MEMBRANE MODEL; MONTE CARLO METHOD; MORPHOLOGY; NEUTRON SCATTERING; PHASE SEPARATION; PRIORITY JOURNAL; REVIEW;

LIPIDS; MONTE CARLO METHOD; NANOSTRUCTURES; NEUTRON DIFFRACTION; SCATTERING, SMALL ANGLE;

EID: 84875920852     PISSN: 00093084     EISSN: 18732941     Source Type: Journal    
DOI: 10.1016/j.chemphyslip.2013.02.012     Document Type: Review

References (109)

1. S.N. Ahmed, D.A. Brown, and E. London On the origin of sphingolipid/cholesterol-rich detergent-insoluble cell membranes: physiological concentrations of cholesterol and sphingolipid induce formation of a detergent-insoluble, liquid-ordered lipid phase in model membranes Biochemistry 36 1997 10944 10953
2. K. Akashi, H. Miyata, H. Itoh, and K. Kinosita Preparation of giant liposomes in physiological conditions and their characterization under an optical microscope Biophysical Journal 71 1996 3242 3250
3. R.G. Anderson, and K. Jacobson A role for lipid shells in targeting proteins to caveolae, rafts, and other lipid domains Science 296 2002 1821 1825
4. V.N.P. Anghel, N. Kučerka, J. Pencer, and J. Katsaras Scattering from laterally heterogeneous vesicles. II. The form factor Journal of Applied Crystallography 40 2007 513 525
5. A.G. Ayuyan, and F.S. Cohen Lipid peroxides promote large rafts: effects of excitation of probes in fluorescence microscopy and electrochemical reactions during vesicle formation Biophysical Journal 91 2006 2172 2183
6. L. Bagatolli, and P.B.S. Kumar Phase behavior of multicomponent membranes: experimental and computational techniques Soft Matter 5 2009 3234 3248
7. J.A. Balmer, O.O. Mykhaylyk, A. Schmid, S.P. Armes, J.P.A. Fairclough, and A.J. Ryan Characterization of polymer-silica nanocomposite particles with core-shell morphologies using Monte Carlo simulations and small angle X-ray scattering Langmuir 27 2011 8075 8089
8. I.S. Barnes, and T.N. Zemb Calculation of small-angle scattering from models for surfactant systems Journal of Applied Crystallography 21 1988 373 379
9. B. Boulgaropoulos, M. Rappolt, B. Sartori, H. Amenitsch, and G. Pabst Lipid Sorting by Ceramide and the Consequences for Membrane Proteins Biophysical Journal 102 2012 2031 2038
10. D.A. Brown, and J.K. Rose Sorting of Gpi-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell-surface Cell 68 1992 533 544
11. J.T. Buboltz, C. Bwalya, K. Williams, and M. Schutzer High-resolution mapping of phase behavior in a ternary lipid mixture: do lipid-raft phase boundaries depend on the sample preparation procedure? Langmuir 23 2007 11968 11971
12. L. Chen, Z. Yu, and P.J. Quinn The partition of cholesterol between ordered and fluid bilayers of phosphatidylcholine: a synchrotron X-ray diffraction study Biochimica et Biophysica Acta 1768 2007 2873 2881
13. J.M. Crane, and L.K. Tamm Role of cholesterol in the formation and nature of lipid rafts in planar and spherical model membranes Biophysical Journal 86 2004 2965 2979
14. C. Czeslik, J. Erbes, and R. Winter Lateral organization of binary-lipid membranes - evidence for fractal-like behaviour in the gel-fluid coexistence region Europhysics Letters 37 1997 577 582
15. R.F.M. de Almeida, A. Fedorov, and M. Prieto Sphingomyelin/ phosphatidylcholine/cholesterol phase diagram: boundaries and composition of lipid rafts Biophysical Journal 85 2003 2406 2416
16. A.R.G. Dibble, M.D. Yeager, and G.W. Feigenson Partitioning of gramicidin A' between coexisting fluid and gel phospholipid phases Biochimica Et Biophysica Acta 1153 1993 155 162
17. C. Dietrich, L.A. Bagatolli, Z.N. Volovyk, N.L. Thompson, M. Levi, K. Jacobson, and E. Gratton Lipid rafts reconstituted in model membranes Biophysical Journal 80 2001 1417 1428
18. C. Eggeling, C. Ringemann, R. Medda, G. Schwarzmann, K. Sandhoff, S. Polyakova, V.N. Belov, B. Hein, C. von Middendorff, A. Schonle, and S.W. Hell Direct observation of the nanoscale dynamics of membrane lipids in a living cell Nature 457 2009 1159 1162
19. E.L. Elson, E. Fried, J.E. Dolbow, and G.M. Genin Phase separation in biological membranes: integration of theory and experiment Annual Review of Biophysics 39 2010 207 226
20. S. Fahsel, E.M. Pospiech, M. Zein, T.L. Hazlet, E. Gratton, and R. Winter Modulation of concentration fluctuations in phase-separated lipid membranes by polypeptide insertion Biophysical Journal 83 2002 334 344
21. E.R. Farkas, and W.W. Webb Precise and millidegree stable temperature control for fluorescence imaging: application to phase transitions in lipid membranes Review of Scientific Instruments 81 2010 093704
22. G.W. Feigenson Phase diagrams and lipid domains in multicomponent lipid bilayer mixtures Biochimica et Biophysica Acta 1788 2009 47 52
23. G.W. Feigenson, and J.T. Buboltz Ternary phase diagram of dipalmitoyl-PC/dilauroyl-PC/cholesterol: nanoscopic domain formation driven by cholesterol Biophysical Journal 80 2001 2775 2788
24. K.I. Florine, and G.W. Feigenson Protein redistribution in model membranes - clearing of M13 coat protein from calcium-induced gel-phase regions in phosphatidylserine phosphatidylcholine multilamellar vesicles Biochemistry 26 1987 2978 2983
25. L.J. Foster, C.L. de Hoog, and M. Mann Unbiased quantitative proteomics of lipid rafts reveals high specificity for signaling factors Proceedings of the National Academy of Sciences of the United States of America 100 2003 5813 5818
26. E.K. Fridriksson, P.A. Shipkova, E.D. Sheets, D. Holowka, B. Baird, and F.W. McLafferty Quantitative analysis of phospholipids in functionally important membrane domains from RBL-2H3 mast cells using tandem high-resolution mass spectrometry Biochemistry 38 1999 8056 8063
27. S.L. Goh, J.J. Amazon, and G.W. Feigenson Toward a better raft model: modulated phases in the 4-component bilayer, DSPC/DOPC/POPC/CHOL Biophysical Journal 104 2013 853 863
28. K.K. Halling, B. Ramstedt, J.H. Nystrom, J.P. Slotte, and T.K.M. Nyholm Cholesterol interactions with fluid-phase phospholipids: effect on the lateral organization of the bilayer Biophysical Journal 95 2008 3861 3871
29. S. Hansen Calculation of small-angle scattering profiles using Monte-Carlo simulation Journal of Applied Crystallography 23 1990 344 346
30. F.A. Heberle, J.J. Pan, R.F. Standaert, P. Drazba, N. Kučerka, and J. Katsaras Model-based approaches for the determination of lipid bilayer structure from small-angle neutron and X-ray scattering data European Biophysics Journal with Biophysics Letters 41 2012 875 890
31. F.A. Heberle, J. Wu, S.L. Goh, R.S. Petruzielo, and G.W. Feigenson Comparison of three ternary lipid bilayer mixtures: FRET and ESR reveal nanodomains Biophysical Journal 99 2010 3309 3318
32. F.A. Heberle, R.S. Petruzielo, J.J. Pan, P. Drazba, N. Kučerka, R.F. Standaert, G. Feigenson, and J. Katsaras Bilayer thickness mismatch controls domain size in model membranes Journal of the American Chemical Society 2013 10.1021/ja3113615
33. S.J. Henderson Monte Carlo modeling of small-angle scattering data from non-interacting homogeneous and heterogeneous particles in solution Biophysical Journal 70 1996 1618 1627
34. T. Henkel, S. Mittler, W. Pfeiffer, H. Rotzer, H.J. Apell, and W. Knoll Lateral order in mixed lipid bilayers and its influence on ion translocation by gramicidin - a model for the structure-function relationship in membranes Biochimie 71 1989 89 98
35. S.T. Hess, T.P.K. Girirajan, and M.D. Mason Ultra-high resolution imaging by fluorescence photoactivation localization microscopy Biophysical Journal 91 2006 4258 4272
36. M. Hirai, H. Hirai, M. Koizumi, K. Kasahara, K. Yuyama, and N. Suzuki Structure of raft-model membrane by using the inverse contrast variation neutron scattering method Physica B-Condensed Matter 385-386 2006 868 870
37. I.V. Ionova, V.A. Livshits, and D. Marsh Phase diagram of ternary cholesterol/palmitoylsphingomyelin/palmitoyloleoyl-phosphatidylcholine mixtures: spin-label EPR study of lipid-raft formation Biophysical Journal 102 2012 1856 1865
38. M.O. Jensen, and O.G. Mouritsen Lipids do influence protein function - the hydrophobic matching hypothesis revisited Biochimica Et Biophysica Acta-Biomembranes 1666 2004 205 226
39. N. Kahya, D. Scherfeld, K. Bacia, and P. Schwille Lipid domain formation and dynamics in giant unilamellar vesicles explored by fluorescence correlation spectroscopy Journal of Structural Biology 147 2004 77 89
40. M.J. Karnovsky, A.M. Kleinfeld, R.L. Hoover, and R.D. Klausner The concept of lipid domains in membranes Journal of Cell Biology 94 1982 1 6
41. J.J.K. Kirkensgaard, J.K. Holm, J.K. Larsen, and D. Posselt Simulation of small-angle X-ray scattering from thylakoid membranes Journal of Applied Crystallography 42 2009 649 659
42. W. Knoll, J. Haas, H.B. Stuhrmann, H.H. Fuldner, H. Vogel, and E. Sackmann Small-angle neutron-scattering of aqueous dispersions of lipids and lipid mixtures - a contrast variation study Journal of Applied Crystallography 14 1981 191 202
43. W. Knoll, K. Ibel, and E. Sackmann Small-angle neutron-scattering study of lipid phase-diagrams by the contrast variation method Biochemistry 20 1981 6379 6383
44. W. Knoll, G. Schmidt, and K. Ibel The inverse contrast variation in small-angle neutron-scattering - a sensitive technique for the evaluation of lipid phase-diagrams Journal of Applied Crystallography 18 1985 65 70
45. W. Knoll, G. Schmidt, K. Ibel, and E. Sackmann Small-angle neutron-scattering study of lateral phase-separation in dimyristoylphosphatidylcholine cholesterol mixed membranes Biochemistry 24 1985 5240 5246
46. W. Knoll, G. Schmidt, E. Sackmann, and K. Ibel Critical demixing in fluid bilayers of phospholipid mixtures: a neutron diffraction study Journal of Chemical Physics 79 1983 3439 3442
47. W. Knoll, G. Schmidt, H. Rotzer, T. Henkel, W. Pfeiffer, E. Sackmann, S. Mittlerneher, and J. Spinke Lateral order in binary lipid alloys and its coupling to membrane functions Chemistry and Physics of Lipids 57 1991 363 374
48. T.M. Konyakhina, S.L. Goh, J. Amazon, F.A. Heberle, J. Wu, and G.W. Feigenson Control of a nanoscopic-to-macroscopic transition: modulated phases in four-component DSPC/DOPC/POPC/Chol giant unilamellar vesicles Biophysical Journal 101 2011 L8 L10
49. J. Korlach, P. Schwille, W.W. Webb, and G.W. Feigenson Characterization of lipid bilayer phases by confocal microscopy and fluorescence correlation spectroscopy Proceedings of the National Academy of Sciences of the United States of America 96 1999 8461 8466
50. R. Krivanek, C. Jeworrek, C. Czeslik, and R. Winter Composition fluctuations in phospholipid-sterol vesicles - a small-angle neutron scattering study Zeitschrift Fur Physikalische Chemie-International Journal of Research in Physical Chemistry & Chemical Physics 222 2008 1679 1692
51. N. Kučerka, M.P. Nieh, and J. Katsaras Fluid phase lipid areas and bilayer thicknesses of commonly used phosphatidylcholines as a function of temperature Biochimica Et Biophysica Acta-Biomembranes 1808 2011 2761 2771
52. A.G. Lee, N.J. Birdsall, J.C. Metcalfe, P.A. Toon, and G.B. Warren Clusters in lipid bilayers and interpretation of thermal effects in biological-membranes Biochemistry 13 1974 3699 3705
53. L. Li, and J.X. Cheng Coexisting stripe- and patch-shaped domains in giant unilamellar vesicles Biochemistry 45 2006 11819 11826
54. D. Lingwood, and K. Simons Lipid rafts as a membrane-organizing principle Science 327 2010 46 50
55. D. Marsh Cholesterol-induced fluid membrane domains: a compendium of lipid raft ternary phase diagrams Biochimica et Biophysica Acta 1788 2009 2114 2123
56. D. Marsh Liquid-ordered phases induced by cholesterol: a compendium of binary phase diagrams Biochimica et Biophysica Acta 1789 2010 688 699
57. T. Masui, M. Imai, and N. Urakami Microdomain formation in model biomembranes Physica B-Condensed Matter 385 2006 821 823
58. T. Masui, N. Urakami, and M. Imai Nano-meter-sized domain formation in lipid membranes observed by small angle neutron scattering European Physical Journal E 27 2008 379 389
59. B.C. McAlister, and B.P. Grady The use of Monte-Carlo simulations to calculate small-angle scattering patterns Macromolecular Symposia 190 2002 117 129
60. T.T. Mills, G.E.S. Toombes, S. Tristram-Nagle, D.M. Smilgies, G.W. Feigenson, and J.F. Nagle Order parameters and areas in fluid-phase oriented lipid membranes using wide angle X-ray scattering Biophysical Journal 95 2008 669 681
61. T.T. Mills, S. Tristram-Nagle, F.A. Heberle, N.F. Morales, J. Zhao, J. Wu, G.E.S. Toombes, J.F. Nagle, and G.W. Feigenson Liquid-liquid domains in bilayers detected by wide angle X-ray scattering Biophysical Journal 95 2008 682 690
62. C. Nicolini, P. Thiyagarajan, and R. Winter Small-scale composition fluctuations and microdomain formation in lipid raft models as revealed by small-angle neutron scattering Physical Chemistry Chemical Physics 6 2004 5531 5534
63. T.K.M. Nyholm, D. Lindroos, B. Westerlund, and J.P. Slotte Construction of a DOPC/PSM/cholesterol phase diagram based on the fluorescence properties of trans-Parinaric acid Langmuir 27 2011 8339 8350
64. J.J. Pan, T.T. Mills, S. Tristram-Nagle, and J.F. Nagle Cholesterol perturbs lipid bilayers nonuniversally Physical Review Letters 100 2008 198103
65. J.J. Pan, S. Tristram-Nagle, and J.F. Nagle Effect of cholesterol on structural and mechanical properties of membranes depends on lipid chain saturation Physical Review E 80 2009 021931
66. J.J. Pan, X.L. Cheng, F.A. Heberle, B. Mostofian, N. Kučerka, P. Drazba, and J. Katsaras Interactions between ether phospholipids and cholesterol as determined by scattering and molecular dynamics simulations Journal of Physical Chemistry B 116 2012 14829 14838
67. J.J. Pan, F.A. Heberle, J.R. Carmichael, J.F. Ankner, and J. Katsaras Time-of-flight Bragg scattering from aligned stacks of lipid bilayers using the liquids reflectometer at the spallation neutron source Journal of Applied Crystallography 45 2012 1219 1227
68. J.J. Pan, F.A. Heberle, S. Tristram-Nagle, M. Szymanski, M. Koepfinger, J. Katsaras, and N. Kučerka Molecular structures of fluid phase phosphatidylglycerol bilayers as determined by small angle neutron and X-ray scattering Biochimica Et Biophysica Acta-Biomembranes 1818 2012 2135 2148
69. E. Pantos, H.F. vanGarderen, P.A.J. Hilbers, T.P.M. Beelen, and R.A. vanSanten Simulation of small-angle scattering from large assemblies of multi-type scatterer particles Journal of Molecular Structure 383 1996 303 308
70. J.S. Pedersen Analysis of small-angle scattering data from colloids and polymer solutions: modeling and least-squares fitting Advances in Colloid and Interface Science 70 1997 171 210
71. J.S. Pedersen, and P. Schurtenberger Scattering functions of semiflexible polymers with and without excluded volume effects Macromolecules 29 1996 7602 7612
72. J.S. Pedersen, C.L.P. Oliveira, H.B. Hubschmann, L. Arleth, S. Manniche, N. Kirkby, and H.M. Nielsen Structure of immune stimulating complex matrices and immune stimulating complexes in suspension determined by small-angle X-ray scattering Biophysical Journal 102 2012 2372 2380
73. J. Pencer, V.N.P. Anghel, N. Kučerka, and J. Katsaras Scattering from laterally heterogeneous vesicles. I. Model-independent analysis Journal of Applied Crystallography 39 2006 791 796
74. J. Pencer, T. Mills, V. Anghel, S. Krueger, R.M. Epand, and J. Katsaras Detection of submicron-sized raft-like domains in membranes by small-angle neutron scattering European Physical Journal E 18 2005 447 458
75. J. Pencer, V.N.P. Anghel, N. Kučerka, and J. Katsaras Scattering from laterally heterogeneous vesicles. III. Reconciling past and present work Journal of Applied Crystallography 40 2007 771 772
76. J. Pencer, T.T. Mills, N. Kučerka, M.P. Nieh, and J. Katsaras Small-angle neutron scattering to detect rafts and lipid domains T.J. McIntosh, Methods in Molecular Biology 2008/01/25 ed. 2007 Humana Press Inc. Totowa, NJ 231 244
77. R.S. Petruzielo, F.A. Heberle, P. Drazba, J. Katsaras, and G.W. Feigenson Phase behavior and domain size in sphingomyelin-containing lipid bilayers Biochimica et Biophysica Acta 1828 2013 1302 1313
78. L.J. Pike, X.L. Han, K.N. Chung, and R.W. Gross Lipid rafts are enriched in arachidonic acid and plasmenylethanolamine and their composition is independent of caveolin-1 expression: a quantitative electrospray ionization/mass spectrometric analysis Biochemistry 41 2002 2075 2088
79. A. Pokorny, L.E. Yandek, A.I. Elegbede, A. Hinderliter, and P.F.F. Almeida Temperature and composition dependence of the interaction of delta-lysin with ternary mixtures of sphingomyelin/cholesterol/POPC Biophysical Journal 91 2006 2184 2197
80. D. Potschke, P. Hickl, M. Ballauff, P.O. Astrand, and J.S. Pedersen Analysis of the conformation of worm-like chains by small-angle scattering: Monte-Carlo simulations in comparison to analytical theory Macromolecular Theory and Simulations 9 2000 345 353
81. H.J. Risselada, and S.J. Marrink Curvature effects on lipid packing and dynamics in liposomes revealed by coarse grained molecular dynamics simulations Physical Chemistry Chemical Physics 11 2009 2056 2067
82. A.V. Samsonov, I. Mihalyov, and F.S. Cohen Characterization of cholesterol-sphingomyelin domains and their dynamics in bilayer membranes Biophysical Journal 81 2001 1486 1500
83. D. Scherfeld, N. Kahya, and P. Schwille Lipid dynamics and domain formation in model membranes composed of ternary mixtures of unsaturated and saturated phosphatidylcholines and cholesterol Biophysical Journal 85 2003 3758 3768
84. P. Sengupta, D. Holowka, and B. Baird Fluorescence resonance energy transfer between lipid probes detects nanoscopic heterogeneity in the plasma membrane of live cells Biophysical Journal 92 2007 3564 3574
85. P. Sharma, R. Varma, R.C. Sarasij, K. Ira Gousset, G. Krishnamoorthy, M. Rao, and S. Mayor Nanoscale organization of multiple GPI-anchored proteins in living cell membranes Cell 116 2004 577 589
86. J.R. Silvius, D. delGiudice, and M. Lafleur Cholesterol at different bilayer concentrations can promote or antagonize lateral segregation of phospholipids of differing acyl chain length Biochemistry 35 1996 15198 15208
87. K. Simons, and M.J. Gerl Revitalizing membrane rafts: new tools and insights Nature Reviews Molecular Cell Biology 11 2010 688 699
88. K. Simons, and E. Ikonen Functional rafts in cell membranes Nature 387 1997 569 572
89. K. Simons, and D. Toomre Lipid rafts and signal transduction Nature Reviews Molecular Cell Biology 1 2000 31 39
90. K. Simons, and G. Vanmeer Lipid sorting in epithelial-cells Biochemistry 27 1988 6197 6202
91. S.J. Singer, and G.L. Nicolson The fluid mosaic model of the structure of cell membranes Science 175 1972 720 731
92. N. Skar-Gislinge, J.B. Simonsen, K. Mortensen, R. Feidenhans'l, S.G. Sligar, B.L. Moller, T. Bjornholm, and L. Arleth Elliptical structure of phospholipid bilayer nanodiscs encapsulated by scaffold proteins: casting the roles of the lipids and the protein Journal of the American Chemical Society 132 2010 13713 13722
93. A.K. Smith, and J.H. Freed Determination of tie-line fields for coexisting lipid phases: an ESR study Journal of Physical Chemistry B 113 2009 3957 3971
94. B. Su, L. Gao, F. Meng, L.W. Guo, J. Rothschild, and I.H. Gelman Adhesion-mediated cytoskeletal remodeling is controlled by the direct scaffolding of Src from FAK complexes to lipid rafts by SSeCKS/AKAP12 Oncogene 2012 10.1038/onc.2012.218
95. D.I. Svergun, and M.H.J. Koch Small-angle scattering studies of biological macromolecules in solution Reports on Progress in Physics 66 2003 1735 1782
96. M.J. Swamy, L. Ciani, M.T. Ge, A.K. Smith, D. Holowka, B. Baird, and J.H. Freed Coexisting domains in the plasma membranes of live cells characterized by spin-label ESR spectroscopy Biophysical Journal 90 2006 4452 4465
97. B.G. Tenchov Nonuniform lipid distribution in membranes Progress in Surface Science 20 1985 273 340
98. S.L. Veatch, and S.L. Keller Separation of liquid phases in giant vesicles of ternary mixtures of phospholipids and cholesterol Biophysical Journal 85 2003 3074 3083
99. S.L. Veatch, and S.L. Keller Miscibility phase diagrams of giant vesicles containing sphingomyelin Physical Review Letters 94 2005 148101
100. S.L. Veatch, and S.L. Keller Seeing spots: Complex phase behavior in simple membranes Biochimica Et Biophysica Acta-Molecular Cell Research 1746 2005 172 185
101. S.L. Veatch, K. Gawrisch, and S.L. Keller Closed-loop miscibility gap and quantitative tie-lines in ternary membranes containing diphytanoyl PC Biophysical Journal 90 2006 4428 4436
102. S.L. Veatch, O. Soubias, S.L. Keller, and K. Gawrisch Critical fluctuations in domain-forming lipid mixtures Proceedings of the National Academy of Sciences of the United States of America 104 2007 17650 17655
103. K. Vogtt, C. Jeworrek, V.M. Garamus, and R. Winter Microdomains in lipid vesicles: structure and distribution assessed by small-angle neutron scattering Journal of Physical Chemistry B 114 2010 5643 5648
104. R. Winter, A. Gabke, C. Czeslik, and P. Pfeifer Power-law fluctuations in phase-separated lipid membranes Physical Review E 60 1999 7354 7359
105. F. Wunderlich, W. Kreutz, P. Mahler, A. Ronai, and G. Heppeler Thermotropic fluid ordered discontinuous phase separation in microsomal lipids of tetrahymena: an X-ray-diffraction study Biochemistry 17 1978 2005 2010
106. J. Yuan, A. Kiss, Y.H. Pramudya, L.T. Nguyen, and L.S. Hirst Solution synchrotron x-ray diffraction reveals structural details of lipid domains in ternary mixtures Physical Review E 79 2009 031924
107. J. Zhao, J. Wu, F.A. Heberle, T.T. Mills, P. Klawitter, G. Huang, G. Costanza, and G.W. Feigenson Phase studies of model biomembranes: complex behavior of DSPC/DOPC/cholesterol Biochimica Et Biophysica Acta-Biomembranes 1768 2007 2764 2776
108. J. Zhao, J. Wu, H.L. Shao, F. Kong, N. Jain, G. Hunt, and G. Feigenson Phase studies of model biomembranes: macroscopic coexistence of L alpha plus L beta, with light-induced coexistence of L alpha plus Lo Phases Biochimica Et Biophysica Acta-Biomembranes 1768 2007 2777 2786
109. J. Zhou, S.K. Gregurick, S. Krueger, and F.P. Schwarz Conformational changes in single-strand DNA as a function of temperature by SANS Biophysical Journal 90 2006 544 551