Molecular insight into the effect of lipid bilayer environments on thrombospondin-1 and calreticulin interactions

Biochemistry

Volumn 53, Issue 40, 2014, Pages 6309-6322

  Wang, Lingyun ^a   Murphy Ullrich, Joanne E ^b   Song, Yuhua ^a  

^a and Radiation Oncology   (United States)

^b University of Alabama at Birmingham   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESION; CELL MEMBRANES; CONFORMATIONS; COORDINATION REACTIONS; LIPIDS; MECHANICAL PROPERTIES; MOLECULAR DYNAMICS; MOLECULES;

CELLULAR ACTIVITIES; CONFORMATIONAL CHANGE; DIRECT INTERACTIONS; ELECTROSTATIC POTENTIALS; LOW DENSITY LIPOPROTEINS; MOLECULAR DYNAMICS SIMULATIONS; MOLECULAR INSIGHTS; RECEPTOR-RELATED PROTEINS;

LIPID BILAYERS;

2 OLEOYL 1 PALMITOYLPHOSPHATIDYLCHOLINE; CALRETICULIN; CHOLESTEROL; SPHINGOMYELIN; THROMBOSPONDIN 1; 1-PALMITOYL-2-OLEOYLPHOSPHATIDYLCHOLINE; LIPID BILAYER; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; PHOSPHATIDYLCHOLINE;

ARTICLE; BILAYER MEMBRANE; BINDING AFFINITY; CONFORMATION; CONFORMATIONAL TRANSITION; LIPID BILAYER; MOLECULAR DYNAMICS; PROTEIN PROTEIN INTERACTION; STATIC ELECTRICITY; BINDING SITE; CHEMISTRY; HUMAN; HYDROGEN BOND; PROTEIN DOMAIN; PROTEIN QUATERNARY STRUCTURE;

BINDING SITES; CALRETICULIN; HUMANS; HYDROGEN BONDING; LIPID BILAYERS; LOW DENSITY LIPOPROTEIN RECEPTOR-RELATED PROTEIN-1; MOLECULAR DYNAMICS SIMULATION; PHOSPHATIDYLCHOLINES; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN STRUCTURE, QUATERNARY; THROMBOSPONDIN 1;

EID: 84908025142     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi500662v     Document Type: Article

References (111)

1. Falanga, V. (2005) Wound healing and its impairment in the diabetic foot Lancet 366, 1736-1743
2. Cheng, C. F., Fan, J., Fedesco, M., Guan, S., Li, Y., Bandyopadhyay, B., Bright, A. M., Yerushalmi, D., Liang, M., Chen, M., Han, Y. P., Woodley, D. T., and Li, W. (2008) Transforming growth factor α (TGFα)-stimulated secretion of HSP90α: Using the receptor LRP-1/CD91 to promote human skin cell migration against a TGFβ-rich environment during wound healing Mol. Cell. Biol. 28, 3344-3358
3. Jung, M. Y., Thapa, N., Kim, J. E., Yang, J. D., Cho, B. C., and Kim, I. S. (2007) Recombinant tetra-cell adhesion motifs supports adhesion, migration and proliferation of keratinocytes/fibroblasts, and promotes wound healing Exp. Mol. Med. 39, 663-672
4. Hara-Chikuma, M. and Verkman, A. S. (2008) Aquaporin-3 facilitates epidermal cell migration and proliferation during wound healing J. Mol. Med. 86, 221-231
5. Rieck, P. W., Cholidis, S., and Hartmann, C. (2001) Intracellular signaling pathway of FGF-2-modulated corneal endothelial cell migration during wound healing in vitro Exp. Eye Res. 73, 639-650
6. Ellis, I. R. and Schor, S. L. (1996) Differential effects of TGF-β1 on hyaluronan synthesis by fetal and adult skin fibroblasts: Implications for cell migration and wound healing Exp. Cell Res. 228, 326-333
7. Grinnell, F. (1990) The activated keratinocyte: Up regulation of cell adhesion and migration during wound healing J. Trauma 30, S144-S149
8. Seiler, W. O., Stahelin, H. B., Zolliker, R., Kallenberger, A., and Luscher, N. J. (1989) Impaired migration of epidermal cells from decubitus ulcers in cell cultures. A cause of protracted wound healing? Am. J. Clin. Pathol. 92, 430-434
9. Sweetwyne, M. T., Pallero, M. A., Lu, A., Van Duyn Graham, L., and Murphy-Ullrich, J. E. (2010) The calreticulin-binding sequence of thrombospondin 1 regulates collagen expression and organization during tissue remodeling Am. J. Pathol. 177, 1710-1724
10. Pallero, M. A., Elzie, C. A., Chen, J., Mosher, D. F., and Murphy-Ullrich, J. E. (2008) Thrombospondin 1 binding to calreticulin-LRP1 signals resistance to anoikis FASEB J. 22, 3968-3979
11. Barker, T. H., Pallero, M. A., MacEwen, M. W., Tilden, S. G., Woods, A., Murphy-Ullrich, J. E., and Hagood, J. S. (2004) Thrombospondin-1-induced focal adhesion disassembly in fibroblasts requires Thy-1 surface expression, lipid raft integrity, and Src activation J. Biol. Chem. 279, 23510-23516
12. Orr, A. W., Pedraza, C. E., Pallero, M. A., Elzie, C. A., Goicoechea, S., Strickland, D. K., and Murphy-Ullrich, J. E. (2003) Low density lipoprotein receptor-related protein is a calreticulin coreceptor that signals focal adhesion disassembly J. Cell Biol. 161, 1179-1189
13. Orr, A. W., Elzie, C. A., Kucik, D. F., and Murphy-Ullrich, J. E. (2003) Thrombospondin signaling through the calreticulin/LDL receptor-related protein co-complex stimulates random and directed cell migration J. Cell Sci. 116, 2917-2927
14. Goicoechea, S., Pallero, M. A., Eggleton, P., Michalak, M., and Murphy-Ullrich, J. E. (2002) The anti-adhesive activity of thrombospondin is mediated by the N-terminal domain of cell surface calreticulin J. Biol. Chem. 277, 37219-37228
15. Goicoechea, S., Orr, A. W., Pallero, M. A., Eggleton, P., and Murphy-Ullrich, J. E. (2000) Thrombospondin mediates focal adhesion disassembly through interactions with cell surface calreticulin J. Biol. Chem. 275, 36358-36368
16. Li, S. S., Forslow, A., and Sundqvist, K. G. (2005) Autocrine regulation of T cell motility by calreticulin-thrombospondin-1 interaction J. Immunol. 174, 654-661
17. Talme, T., Bergdahl, E., and Sundqvist, K. G. (2014) Regulation of T-lymphocyte motility, adhesion and de-adhesion by a cell surface mechanism directed by low density lipoprotein receptor-related protein 1 and endogenous thrombospondin-1 Immunology 142, 176-192
18. DiPietro, L. A. and Polverini, P. J. (1993) Angiogenic macrophages produce the angiogenic inhibitor thrombospondin 1 Am. J. Pathol. 143, 678-684
19. Reed, M. J., Iruela-Arispe, L., OBrien, E. R., Truong, T., LaBell, T., Bornstein, P., and Sage, E. H. (1995) Expression of thrombospondins by endothelial cells. Injury is correlated with TSP-1 Am. J. Pathol. 147, 1068-1080
20. Majack, R. A., Cook, S. C., and Bornstein, P. (1986) Control of smooth muscle cell growth by components of the extracellular matrix: Autocrine role for thrombospondin Proc. Natl. Acad. Sci. U.S.A. 83, 9050-9054
21. Frangogiannis, N. G., Ren, G., Dewald, O., Zymek, P., Haudek, S., Koerting, A., Winkelmann, K., Michael, L. H., Lawler, J., and Entman, M. L. (2005) Critical role of endogenous thrombospondin-1 in preventing expansion of healing myocardial infarcts Circulation 111, 2935-2942
22. Bornstein, P. (2001) Thrombospondins as matricellular modulators of cell function J. Clin. Invest. 107, 929-934
23. Mosher, D. F., Doyle, M. J., and Jaffe, E. A. (1982) Synthesis and secretion of thrombospondin by cultured human endothelial cells J. Cell Biol. 93, 343-348
24. Lawler, J. W., Slayter, H. S., and Coligan, J. E. (1978) Isolation and characterization of a high molecular weight glycoprotein from human blood platelets J. Biol. Chem. 253, 8609-8616
25. Jaffe, E. A., Ruggiero, J. T., Leung, L. K., Doyle, M. J., McKeown-Longo, P. J., and Mosher, D. F. (1983) Cultured human fibroblasts synthesize and secrete thrombospondin and incorporate it into extracellular matrix Proc. Natl. Acad. Sci. U.S.A. 80, 998-1002
26. Jaffe, E. A., Ruggiero, J. T., and Falcone, D. J. (1985) Monocytes and macrophages synthesize and secrete thrombospondin Blood 65, 79-84
27. Raugi, G. J., Mumby, S. M., Abbott-Brown, D., and Bornstein, P. (1982) Thrombospondin: Synthesis and secretion by cells in culture J. Cell Biol. 95, 351-354
28. Adams, J. C. and Lawler, J. (2004) The thrombospondins Int. J. Biochem. Cell Biol. 36, 961-968
29. Adams, J. C. (2001) Thrombospondins: Multifunctional regulators of cell interactions Annu. Rev. Cell Dev. Biol. 17, 25-51
30. Sweetwyne, M. T. and Murphy-Ullrich, J. E. (2012) Thrombospondin1 in tissue repair and fibrosis: TGF-β-dependent and independent mechanisms Matrix Biol. 31, 178-186
31. Li, S. S., Ivanoff, A., Bergstrom, S. E., Sandstrom, A., Christensson, B., van Nerven, J., Holgersson, J., Hauzenberger, D., Arencibia, I., and Sundqvist, K. G. (2002) T lymphocyte expression of thrombospondin-1 and adhesion to extracellular matrix components Eur. J. Immunol. 32, 1069-1079
32. Li, S. S., Liu, Z., Uzunel, M., and Sundqvist, K. G. (2006) Endogenous thrombospondin-1 is a cell-surface ligand for regulation of integrin-dependent T-lymphocyte adhesion Blood 108, 3112-3120
33. Murphy-Ullrich, J. E., Gurusiddappa, S., Frazier, W. A., and Hook, M. (1993) Heparin-binding peptides from thrombospondins 1 and 2 contain focal adhesion-labilizing activity J. Biol. Chem. 268, 26784-26789
34. Tan, K., Duquette, M., Liu, J. H., Zhang, R., Joachimiak, A., Wang, J. H., and Lawler, J. (2006) The structures of the thrombospondin-1 N-terminal domain and its complex with a synthetic pentameric heparin Structure 14, 33-42
35. Johnson, S., Michalak, M., Opas, M., and Eggleton, P. (2001) The ins and outs of calreticulin: From the ER lumen to the extracellular space Trends Cell Biol. 11, 122-129
36. Ling, S., Pi, X., and Holoshitz, J. (2007) The rheumatoid arthritis shared epitope triggers innate immune signaling via cell surface calreticulin J. Immunol. 179, 6359-6367
37. Gold, L. I., Eggleton, P., Sweetwyne, M. T., Van Duyn, L. B., Greives, M. R., Naylor, S. M., Michalak, M., and Murphy-Ullrich, J. E. (2010) Calreticulin: Non-endoplasmic reticulum functions in physiology and disease FASEB J. 24, 665-683
38. Arosa, F. A., de Jesus, O., Carmo, A. M., Porto, G., and de Sousa, M. (1999) Calreticulin is expressed on the T cell surface of activated human peripheral blood T lymphocytes in association with MHC-class I molecules FASEB J. 13, A274
39. Arosa, F. A., de Jesus, O., Porto, G., Carmo, A. M., and de Sousa, M. (1999) Calreticulin is expressed on the cell surface of activated human peripheral blood T lymphocytes in association with major histocompatibility complex class I molecules J. Biol. Chem. 274, 16917-16922
40. Zimmerman, K. A., Graham, L. V., Pallero, M. A., and Murphy-Ullrich, J. E. (2013) Calreticulin regulates transforming growth factor-β-stimulated extracellular matrix production J. Biol. Chem. 288, 14584-14598
41. Zhu, Q., Zelinka, P., White, T., and Tanzer, M. L. (1997) Calreticulin-integrin bidirectional signaling complex Biochem. Biophys. Res. Commun. 232, 354-358
42. Kwon, M. S., Park, C. S., Choi, K., Ahnn, J., Kim, J. I., Eom, S. H., Kaufman, S. J., and Song, W. K. (2000) Calreticulin couples calcium release and calcium influx in integrin-mediated calcium signaling Mol. Biol. Cell 11, 1433-1443
43. Gold, L. I., Rahman, M., Blechman, K. M., Greives, M. R., Churgin, S., Michaels, J., Callaghan, M. J., Cardwell, N. L., Pollins, A. C., Michalak, M., Siebert, J. W., Levine, J. P., Gurtner, G. C., Nanney, L. B., Galiano, R. D., and Cadacio, C. L. (2006) Overview of the role for calreticulin in the enhancement of wound healing through multiple biological effects J. Invest. Dermatol. Symp. Proc. 11, 57-65
44. Norgaard, T. K., Larsen, N., Steen Jørgensen, F., Hojrup, P., Houen, G., and Vestergaard, B. (2008) Small angle X-ray scattering study of calreticulin reveals conformational plasticity Biochim. Biophys. Acta 1784, 1265-1270
45. Yan, Q., Murphy-Ullrich, J. E., and Song, Y. H. (2010) Structural Insight into the Role of Thrombospondin-1 Binding to Calreticulin in Calreticulin-Induced Focal Adhesion Disassembly Biochemistry 49, 3685-3694
46. Pike, L. J. (2006) Rafts defined: A report on the Keystone Symposium on Lipid Rafts and Cell Function J. Lipid Res. 47, 1597-1598
47. Simons, K. and Ikonen, E. (1997) Functional rafts in cell membranes Nature 387, 569-572
48. Ostrom, R. S. and Insel, P. A. (2004) The evolving role of lipid rafts and caveolae in G protein-coupled receptor signaling: Implications for molecular pharmacology Br. J. Pharmacol. 143, 235-245
49. Maguy, A., Hebert, T. E., and Nattel, S. (2006) Involvement of lipid rafts and caveolae in cardiac ion channel function Cardiovasc. Res. 69, 798-807
50. Barker, T. H., Pallero, M. A., MacEwen, M. W., Tilden, S. G., Woods, A., Murphy-Ullrich, J. E., and Hagood, J. S. (2004) Thrombospondin-1-induced focal adhesion disassembly in fibroblasts requires Thy-1 surface expression, lipid raft integrity, and Src activation J. Biol. Chem. 279, 23510-23516
51. DeBruin, L. S. and Harauz, G. (2007) White matter rafting: Membrane microdomains in myelin Neurochem. Res. 32, 213-228
52. Berkowitz, M. L. (2009) Detailed molecular dynamics simulations of model biological membranes containing cholesterol Biochim. Biophys. Acta 1788, 86-96
53. Bennett, W. F. D. and Tieleman, D. P. (2013) Computer simulations of lipid membrane domains Biochim. Biophys. Acta 1828, 1765-1776
54. Hess, B., Kutzner, C., van der Spoel, D., and Lindahl, E. (2008) GROMACS 4: Algorithms for highly efficient, load-balanced, and scalable molecular simulation J. Chem. Theory Comput 4, 435-447
55. Kaiser, H. J., Lingwood, D., Levental, I., Sampaio, J. L., Kalvodova, L., Rajendran, L., and Simons, K. (2009) Order of lipid phases in model and plasma membranes Proc. Natl. Acad. Sci. U.S.A. 106, 16645-16650
56. Epand, R. F., Sayer, B. G., and Epand, R. M. (2005) Induction of raft-like domains by a myristoylated NAP-22 peptide and its Tyr mutant FEBS J. 272, 1792-1803
57. Bennett, W. F. D. and Tieleman, D. P. (2012) Molecular simulation of rapid translocation of cholesterol, diacylglycerol, and ceramide in model raft and nonraft membranes J. Lipid Res. 53, 421-429
58. Crane, J. M. and Tamm, L. K. (2004) Role of cholesterol in the formation and nature of lipid rafts in planar and spherical model membranes Biophys. J. 86, 2965-2979
59. McMullen, T. P. W., Lewis, R. N. A. H., and McElhaney, R. N. (2004) Cholesterol-phospholipid interactions, the liquid-ordered phase and lipid rafts in model and biological membranes Curr. Opin. Colloid Interface Sci. 8, 459-468
60. Forrest, L. R., Tieleman, D. P., and Sansom, M. S. P. (1999) Defining the transmembrane helix of M2 protein from influenza A by molecular dynamics simulations in a lipid bilayer Biophys. J. 76, 1886-1896
61. Law, R. J., Tieleman, D. P., and Sansom, M. S. P. (2003) Pores formed by the nicotinic receptor M2 delta peptide: A molecular dynamics simulation study Biophys. J. 84, 14-27
62. Hub, J. S., Winkler, F. K., Merrick, M., and de Groot, B. L. (2010) Potentials of Mean Force and Permeabilities for Carbon Dioxide, Ammonia, and Water Flux across a Rhesus Protein Channel and Lipid Membranes J. Am. Chem. Soc. 132, 13251-13263
63. Wennberg, C. L., van der Spoel, D., and Hub, J. S. (2012) Large Influence of Cholesterol on Solute Partitioning into Lipid Membranes J. Am. Chem. Soc. 134, 5351-5361
64. Niemela, P. S., Ollila, S., Hyvonen, M. T., Karttunen, M., and Vattulainen, I. (2007) Assessing the nature of lipid raft membranes PLoS Comput. Biol. 3, 304-312
65. Schrag, J. D., Bergeron, J. J., Li, Y., Borisova, S., Hahn, M., Thomas, D. Y., and Cygler, M. (2001) The Structure of calnexin, an ER chaperone involved in quality control of protein folding Mol. Cell 8, 633-644
66. Ellgaard, L., Riek, R., Braun, D., Herrmann, T., Helenius, A., and Wuthrich, K. (2001) Three-dimensional structure topology of the calreticulin P-domain based on NMR assignment FEBS Lett. 488, 69-73
67. Guo, L., Groenendyk, J., Papp, S., Dabrowska, M., Knoblach, B., Kay, C., Parker, J. M., Opas, M., and Michalak, M. (2003) Identification of an N-domain histidine essential for chaperone function in calreticulin J. Biol. Chem. 278, 50645-50653
68. Humphrey, W., Dalke, A., and Schulten, K. (1996) VMD: Visual molecular dynamics J. Mol. Graphics Modell. 14, 33-38
69. Berger, O., Edholm, O., and Jahnig, F. (1997) Molecular dynamics simulations of a fluid bilayer of dipalmitoylphosphatidylcholine at full hydration, constant pressure, and constant temperature Biophys. J. 72, 2002-2013
70. Poger, D. and Mark, A. E. (2012) Lipid bilayers: The effect of force field on ordering and dynamics J. Chem. Theory Comput. 8, 4807-4817
71. Scott, W. R. P., Hunenberger, P. H., Tironi, I. G., Mark, A. E., Billeter, S. R., Fennen, J., Torda, A. E., Huber, T., Kruger, P., and van Gunsteren, W. F. (1999) The GROMOS biomolecular simulation program package J. Phys. Chem. A 103, 3596-3607
72. Berendsen, H. J. C., Postma, J. P. M., van Gunsteren, W. F., and Hermans, J. (1981) Interaction models for water in relation to protein hydration. In Intermolecular Forces (Pullman, B., Ed.) pp 331-342, Springer, Dordrecht, The Netherlands.
73. Yan, Q., McDonald, J. M., Zhou, T., and Song, Y. (2013) Structural insight for the roles of fas death domain binding to FADD and oligomerization degree of the Fas-FADD complex in the death-inducing signaling complex formation: A computational study Proteins 81, 377-385
74. Yan, Q., Murphy-Ullrich, J. E., and Song, Y. (2011) Molecular and structural insight into the role of key residues of thrombospondin-1 and calreticulin in thrombospondin-1-calreticulin binding Biochemistry 50, 566-573
75. Pan, D., Yan, Q., Chen, Y., McDonald, J. M., and Song, Y. (2011) Trifluoperazine regulation of calmodulin binding to Fas: A computational study Proteins 79, 2543-2556
76. Pan, D. and Song, Y. (2010) Role of altered sialylation of the I-like domain of β1 integrin in the binding of fibronectin to β1 integrin: Thermodynamics and conformational analyses Biophys. J. 99, 208-217
77. Suever, J. D., Chen, Y., McDonald, J. M., and Song, Y. (2008) Conformation and free energy analyses of the complex of calcium-bound calmodulin and the Fas death domain Biophys. J. 95, 5913-5921
78. Liu, Y., Pan, D., Bellis, S. L., and Song, Y. (2008) Effect of altered glycosylation on the structure of the I-like domain of β1 integrin: A molecular dynamics study Proteins 73, 989-1000
79. +-lipid interactions and finite size effects Biophys. J. 94, 3565-3576
80. Song, Y., Guallar, V., and Baker, N. A. (2005) Molecular dynamics simulations of salicylate effects on the micro- and mesoscopic properties of a dipalmitoylphosphatidylcholine bilayer Biochemistry 44, 13425-13438
81. Hess, B., Bekker, H., Berendsen, H. J. C., and Fraaije, J. G. E. M. (1997) LINCS: A linear constraint solver for molecular simulations J. Comput. Chem. 18, 1463-1472
82. Nose, S. (1984) A unified formulation of the constant temperature molecular-dynamics methods J. Chem. Phys. 81, 511-519
83. Hoover, W. G. (1985) Canonical dynamics: Equilibrium phase-space distributions Phys. Rev. A 31, 1695-1697
84. Parrinello, M. and Rahman, A. (1981) Polymorphic transitions in single crystals: A new molecular dynamics J. Appl. Phys. 52, 7182-7190
85. de Almeida, R. F. M., Fedorov, A., and Prieto, M. (2003) Sphingomyelin/phosphatidylcholine/cholesterol phase diagram: Boundaries and composition of lipid rafts Biophys. J. 85, 2406-2416
86. Darden, T., York, D., and Pedersen, L. (1993) Particle Mesh Ewald: An N.Log(N) Method for Ewald Sums in Large Systems J. Chem. Phys. 98, 10089-10092
87. Essmann, U., Perera, L., Berkowitz, M. L., Darden, T., Lee, H., and Pedersen, L. G. (1995) A Smooth Particle Mesh Ewald Method J. Chem. Phys. 103, 8577-8593
88. Allen, M. P. and Tildesley, D. J. (1987) Computer Simulation of Liquids, Oxford University Press, New York.
89. Efron, B. and Tibshirani, R. J. (1998) An Introduction to the Bootstrap, Chapman & Hall, New York.
90. Bailey, N. T. J. (1995) Statistical methods in biology, 3rd ed., Cambridge University Press, New York.
91. Gurtovenko, A. A. and Vattulainen, I. (2008) Effect of NaCl and KCl on phosphatidylcholine and phosphatidylethanolamine lipid membranes: Insight from atomic-scale simulations for understanding salt-induced effects in the plasma membrane J. Phys. Chem. B 112, 1953-1962
92. Hyslop, P. A., Morel, B., and Sauerheber, R. D. (1990) Organization and Interaction of Cholesterol and Phosphatidylcholine in Model Bilayer-Membranes Biochemistry 29, 1025-1038
93. Kucerka, N., Tristram-Nagle, S., and Nagle, J. F. (2005) Structure of fully hydrated fluid phase lipid bilayers with monounsaturated chains J. Membr. Biol. 208, 193-202
94. n membranes. A time-resolved fluorescence study Biophys. Chem. 58, 289-302
95. Smaby, J. M., Momsen, M. M., Brockman, H. L., and Brown, R. E. (1997) Phosphatidylcholine acyl unsaturation modulates the decrease in interfacial elasticity induced by cholesterol Biophys. J. 73, 1492-1505
96. Egberts, E. and Berendsen, H. J. C. (1988) Molecular-dynamics simulation of a smectic liquid crystal with atomic detail J. Chem. Phys. 89, 3718-3732
97. Roux, B. and Schulten, K. (2004) Computational studies of membrane channels Structure 12, 1343-1351
98. Feller, S. E. and Pastor, R. W. (1999) Constant surface tension simulations of lipid bilayers: The sensitivity of surface areas and compressibilities J. Chem. Phys. 111, 1281-1287
99. Lindahl, E. and Edholm, O. (2000) Mesoscopic undulations and thickness fluctuations in lipid bilayers from molecular dynamics simulations Biophys. J. 79, 426-433
100. Lingwood, D. and Simons, K. (2010) Lipid Rafts As a Membrane-Organizing Principle Science 327, 46-50
101. Vereb, G., Szollosi, J., Matko, J., Nagy, P., Farkas, T., Vigh, L., Matyus, L., Waldmann, T. A., and Damjanovich, S. (2003) Dynamic, yet structured: The cell membrane three decades after the Singer-Nicolson model Proc. Natl. Acad. Sci. U.S.A. 100, 8053-8058
102. Korade, Z. and Kenworthy, A. K. (2008) Lipid rafts, cholesterol, and the brain Neuropharmacology 55, 1265-1273
103. Simons, K. and Ehehalt, R. (2002) Cholesterol, lipid rafts, and disease J. Clin. Invest. 110, 597-603
104. London, E. (2002) Insights into lipid raft structure and formation from experiments in model membranes Curr. Opin. Struct. Biol. 12, 480-486
105. Dupree, J. L. and Pomicter, A. D. (2010) Myelin, DIGs, and membrane rafts in the central nervous system Prostaglandins Other Lipid Mediators 91, 118-129
106. Samsonov, A. V., Mihalyov, I., and Cohen, F. S. (2001) Characterization of cholesterol-sphingomyelin domains and their dynamics in bilayer membranes Biophys. J. 81, 1486-1500
107. Kucerka, N., Perlmutter, J. D., Pan, J., Tristram-Nagle, S., Katsaras, J., and Sachs, J. N. (2008) The effect of cholesterol on short- and long-chain monounsaturated lipid bilayers as determined by molecular dynamics simulations and X-ray scattering Biophys. J. 95, 2792-2805
108. Huang, J. Y. and Feigenson, G. W. (1999) A microscopic interaction model of maximum solubility of cholesterol in lipid bilayers Biophys. J. 76, 2142-2157
109. Feig, M., Karanicolas, J., and Brooks, C. L. I. (2004) MMTSB Tool Set: Enhanced sampling and multiscale modeling methods for applications in structural biology J. Mol. Graphics Modell. 22, 377-395
110. Hartigan, J. A. (1975) Clustering algorithms, John Wiley & Sons, Inc., New York.
111. Herz, J. and Strickland, D. K. (2001) LRP: A multifunctional scavenger and signaling receptor J. Clin. Invest. 108, 779-784