The influence of cholesterol on membrane protein structure, function, and dynamics studied by molecular dynamics simulations

Biochimica et Biophysica Acta - Biomembranes

Volumn 1848, Issue 9, 2015, Pages 1783-1795

  Grouleff, Julie ^a   Irudayam, Sheeba Jem ^a   Skeby, Katrine K ^a   Schiøtt, Birgit ^a  

^a AARHUS UNIVERSITY   (Denmark)

Author keywords

Amyloid peptide; Cholesterol; Lipid protein interaction; MD simulation; Membrane protein

Indexed keywords

CHOLESTEROL; LIPID BILAYER; MEMBRANE PROTEIN; PEPTIDE; PROTEIN BINDING;

CELL MEMBRANE; CHEMICAL STRUCTURE; CHEMISTRY; HUMAN; LIPID BILAYER; METABOLISM; MOLECULAR DYNAMICS; PROTEIN TERTIARY STRUCTURE;

CELL MEMBRANE; CHOLESTEROL; HUMANS; LIPID BILAYERS; MEMBRANE PROTEINS; MOLECULAR DYNAMICS SIMULATION; MOLECULAR STRUCTURE; PEPTIDES; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY;

EID: 84936892311     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2015.03.029     Document Type: Review

References (147)

1. K. Simons, and G. Van Meer Lipid sorting in epithelial cells Biochemistry 27 1988 6197 6202
2. J.S. O'Brien, and G. Rouser The fatty acid composition of brain sphingolipids: sphingomyelin, ceramide, cerebroside, and cerebroside sulfate J. Lipid Res. 5 1964 339 342
3. S. Sonnino, L. Mauri, V. Chigorno, and A. Prinetti Gangliosides as components of lipid membrane domains Glycobiology 17 2007 1R 13R
4. S.J. Singer, and G.L. Nicolson The fluid mosaic model of the structure of cell membranes Science 175 1972 720 731
5. C. Schengrund Lipid rafts: keys to neurodegeneration Brain Res. Bull. 82 2010 7 17
6. R. Sheng, Y. Chen, H. Yung Gee, E. Stec, H.R. Melowic, N.R. Blatner, M.P. Tun, Y. Kim, M. Källberg, T.K. Fujiwara, J. Hye Hong, K. Pyo Kim, H. Lu, A. Kusumi, M. Goo Lee, and W. Cho Cholesterol modulates cell signaling and protein networking by specifically interacting with PDZ domain-containing scaffold proteins Nat. Commun. 3 2012 1249
7. J.A. Lundbæk, O.S. Andersen, T. Werge, and C. Nielsen Cholesterol-induced protein sorting: an analysis of energetic feasibility Biophys. J. 84 2003 2080 2089
8. H. Kaiser, A. Orlowski, T. Róg, T.K.M. Nyholm, W. Chai, T. Feizi, D. Lingwood, I. Vattulainen, and K. Simons Lateral sorting in model membranes by cholesterol-mediated hydrophobic matching Proc. Natl. Acad. Sci. U. S. A. 108 2011 16628 16633
9. J. Montero, A. Morales, L. Llacuna, J.M. Lluis, O. Terrones, G. Basañez, B. Antonsson, J. Prieto, C. García-Ruiz, A. Colell, and J.C. Fernández-Checa Mitochondrial cholesterol contributes to chemotherapy resistance in hepatocellular carcinoma Cancer Res. 68 2008 5246 5256
10. W. Cho, S. Trikha, and A.M. Jeremic Cholesterol regulates assembly of human islet amyloid polypeptide on model membranes J. Mol. Biol. 393 2009 765 775
11. N. Arispe, and M. Doh Plasma membrane cholesterol controls the cytotoxicity of Alzheimer's disease AßP (1-40) and (1-42) peptides FASEB J. 16 2002 1526 1536
12. L.A. Shobab, G.Y.R. Hsiung, and H.H. Feldman Cholesterol in Alzheimer's disease Lancet Neurol. 4 2005 841 852
13. B. Alberts, A. Johnson, J. Lewis, M. Raff, K. Roberts, and P. Walter Membrane Structure, Molecular Biology of the Cell 5th ed. 2008 Garland Science New York, NY 617 650
14. R. Phillips, T. Ursell, P. Wiggins, and P. Sens Emerging roles for lipids in shaping membrane-protein function Nature 459 2009 379 385
15. P.L. Yeagle Non-covalent binding of membrane lipids to membrane proteins Biochim. Biophys. Acta Biomembr. 1838 2014 1548 1559
16. T. Shinoda, H. Ogawa, F. Cornelius, and C. Toyoshima Crystal structure of the sodium-potassium pump at 2.4 Å resolution Nature 459 2009 446 450
17. A. Penmatsa, K.H. Wang, and E. Gouaux X-ray structure of dopamine transporter elucidates antidepressant mechanism Nature 503 2013 85 90
18. 2+ bound in the cation binding site Proc. Natl. Acad. Sci. U. S. A. 110 2013 10958 10963
19. D. Lingwood, and K. Simons Lipid rafts as a membrane-organizing principle Science 327 2010 46 50
20. C.L. Armstrong, D. Marquardt, H. Dies, N. Kučerka, Z. Yamani, T.A. Harroun, J. Katsaras, A. Shi, and M.C. Rheinstädter The observation of highly ordered domains in membranes with cholesterol PLoS One 8 2013 e66162
21. S. Munro Lipid rafts: elusive or illusive? Cell 115 2003 377 388
22. K. Simons, and R. Ehehalt Cholesterol, lipid rafts, and disease J. Clin. Invest. 110 2002 597 603
23. J.A. Allen, R. Halverson-Tamboli, and M.M. Rasenick Lipid raft microdomains and neurotransmitter signalling Nat. Rev. Neurosci. 8 2007 128 140
24. Z. Korade, and A.K. Kenworthy Lipid rafts, cholesterol, and the brain Neuropharmacology 55 2008 1265 1273
25. M. Bucciantini, S. Rigacci, and M. Stefani Amyloid aggregation: role of biological membranes and the aggregate-membrane system J. Phys. Chem. Lett. 5 2014 517 527
26. F. Contreras, A.M. Ernst, F. Wieland, and B. Brügger Specificity of intramembrane protein-lipid interactions Cold Spring Harb. Perspect. Biol. 3 2011 a004705
27. Y.D. Paila, and A. Chattopadhyay Membrane Cholesterol in the Function and Organization of G-Protein Coupled Receptors J.R. Harris, 2010 Springer Netherlands 439 466
28. O.S. Andersen, and R.E. Koeppe Bilayer thickness and membrane protein function: an energetic perspective Annu. Rev. Biophys. Biomol. Struct. 36 2007 107 130
29. G.A. Petsko, and D. Ringe Protein Structure and Function 2004 New Science Press London
30. M. Liao, E. Cao, D. Julius, and Y. Cheng Structure of the TRPV1 ion channel determined by electron cryo-microscopy Nature 504 2013 107 112
31. W. Liu, D. Wacker, C. Gati, G.W. Han, D. James, D. Wang, G. Nelson, U. Weierstall, V. Katritch, A. Barty, N.A. Zatsepin, D. Li, M. Messerschmidt, S. Boutet, G.J. Williams, J.E. Koglin, M.M. Seibert, C. Wang, S.T.A. Shah, S. Basu, R. Fromme, C. Kupitz, K.N. Rendek, I. Grotjohann, P. Fromme, R.A. Kirian, K.R. Beyerlein, T.A. White, H.N. Chapman, M. Caffrey, J.C.H. Spence, R.C. Stevens, and V. Cherezov Serial femtosecond crystallography of G protein-coupled receptors Science 342 2013 1521 1524
32. H. Koldsø, D. Shorthouse, J. Hélie, and M.S.P. Sansom Lipid clustering correlates with membrane curvature as revealed by molecular simulations of complex lipid bilayers PLoS Comput. Biol. 10 2014 e1003911
33. H.I. Ingólfsson, M.N. Melo, F.J. van Eerden, C. Arnarez, C.A. Lopez, T.A. Wassenaar, X. Periole, A.H. de Vries, D.P. Tieleman, and S.J. Marrink Lipid organization of the plasma membrane J. Am. Chem. Soc. 136 2014 14554 14559
34. S. Mondal, G. Khelashvili, and H. Weinstein Not just an oil slick: how the energetics of protein-membrane interactions impacts the function and organization of transmembrane proteins Biophys. J. 106 2014 2305 2316
35. D.E. Shaw, M.M. Deneroff, R.O. Dror, J.S. Kuskin, R.H. Larson, J.K. Salmon, C. Young, B. Batson, K.J. Bowers, J.C. Chao, M.P. Eastwood, J. Gagliardo, J.P. Grossman, C.R. Ho, D.J. Ierardi, I. Kolossváry, J.L. Klepeis, T. Layman, C. McLeavey, M.A. Moraes, R. Mueller, E.C. Priest, Y. Shan, J. Spengler, M. Theobald, B. Towles, and S.C. Wang Anton, a special-purpose machine for molecular dynamics simulation Commun. ACM 51 2008 91 97
36. J.E. Stone, J.C. Phillips, P.L. Freddolino, D.J. Hardy, L.G. Trabuco, and K. Schulten Accelerating molecular modeling applications with graphics processors J. Comput. Chem. 28 2007 2618 2640
37. Y. Song, A.K. Kenworthy, and C.R. Sanders Cholesterol as a co-solvent and a ligand for membrane proteins Protein Sci. 23 2014 1 22
38. I. Levitan, D.K. Singh, and A. Rosenhouse-Dantsker Cholesterol binding to ion channels Front. Physiol. 5 2014 65
39. P.L. Yeagle, J. Young, and D. Rice Effects of cholesterol on sodium-potassium ATPase ATP hydrolyzing activity in bovine kidney Biochemistry 27 1988 6449 6452
40. W.C. Hong, and S.G. Amara Membrane cholesterol modulates the outward facing conformation of the dopamine transporter and alters cocaine binding J. Biol. Chem. 285 2010 32616 32626
41. S. Trikha, and A.M. Jeremic Clustering and internalization of toxic amylin oligomers in pancreatic cells require plasma membrane cholesterol J. Biol. Chem. 286 2011 36086 36097
42. G.P. Eckert, C. Kirsch, S. Leutz, W.G. Wood, and W.E. Müller Cholesterol modulates amyloid beta-peptide's membrane interactions Pharmacopsychiatry 36 2003 136 143
43. G. Gimpl, and K. Gehrig-Burger Probes for studying cholesterol binding and cell biology Steroids 76 2011 216 231
44. H. Li, and V. Papadopoulos Peripheral-type benzodiazepine receptor function in cholesterol transport. Identification of a putative cholesterol recognition/interaction amino acid sequence and consensus pattern Endocrinology 139 1998 4991 4997
45. C.J. Baier, J. Fantini, and F.J. Barrantes Disclosure of cholesterol recognition motifs in transmembrane domains of the human nicotinic acetylcholine receptor Sci. Rep. 1 2011 69
46. R.M. Epand, A. Thomas, R. Brasseur, and R.F. Epand Cholesterol interaction with proteins that partition into membrane domains: an overview J.R. Harris, Cholesterol Binding and Cholesterol Transport Proteins 2010 Springer Netherlands 253 278
47. M.A. Hanson, V. Cherezov, M.T. Griffith, C.B. Roth, V. Jaakola, E.Y.T. Chien, J. Velasquez, P. Kuhn, and R.C. Stevens A specific cholesterol binding site is established by the 2.8 Å structure of the human β2-adrenergic receptor Structure 16 2008 897 905
48. J. Oates, and A. Watts Uncovering the intimate relationship between lipids, cholesterol and GPCR activation Curr. Opin. Struct. Biol. 21 2011 802 807
49. A receptor Biophys. J. 106 2014 1938 1949
50. S. Hiller, R.G. Garces, T.J. Malia, V.Y. Orekhov, M. Colombini, and G. Wagner Solution structure of the integral human membrane protein VDAC-1 in detergent micelles Science 321 2008 1206 1210
51. A. Laganowsky, E. Reading, T.M. Allison, M.B. Ulmschneider, M.T. Degiacomi, A.J. Baldwin, and C.V. Robinson Membrane proteins bind lipids selectively to modulate their structure and function Nature 510 2014 172 175
52. J.J. Hulce, A.B. Cognetta, M.J. Niphakis, S.E. Tully, and B.F. Cravatt Proteome-wide mapping of cholesterol-interacting proteins in mammalian cells Nat. Methods 10 2013 259 264
53. G. Brannigan, J. Hénin, R. Law, R. Eckenhoff, and M.L. Klein Embedded cholesterol in the nicotinic acetylcholine receptor Proc. Natl. Acad. Sci. U. S. A. 105 2008 14418 14423
54. B.P. Weiser, R. Salari, R.G. Eckenhoff, and G. Brannigan Computational investigation of cholesterol binding sites on mitochondrial VDAC J. Phys. Chem. B 118 2014 9852 9860
55. G.M. Morris, and M. Lim-Wilby Molecular Docking A. Kukol, 2008 Humana Press 365 382
56. M.K. Baker, and C.F. Abrams Dynamics of lipids, cholesterol, and transmembrane α-helices from microsecond molecular dynamics simulations J. Phys. Chem. B 118 2014 13590 13600
57. O.M. Becker, J. MacKerell, D. Alexander, B. Roux, and M. Watanabe Computational Biochemistry and Biophysics 2001 Marcel Dekker, Inc. New York
58. K. Lindorff-Larsen, N. Trbovic, P. Maragakis, S. Piana, and D.E. Shaw Structure and dynamics of an unfolded protein examined by molecular dynamics simulation J. Am. Chem. Soc. 134 2012 3787 3791
59. P. Stansfeld, and M.P. Sansom Molecular simulation approaches to membrane proteins Structure 19 2011 1562 1572
60. V. Tozzini Coarse-grained models for proteins Curr. Opin. Struct. Biol. 15 2005 144 150
61. V. Tozzini Multiscale modeling of proteins Acc. Chem. Res. 43 2010 220 230
62. T. Schlick Molecular dynamics-based approaches for enhanced sampling of long-time, large-scale conformational changes in biomolecules F1000 Biol. Rep. 1 2009 51
63. L. Thøgersen, B. Schiøtt, T. Vosegaard, N.C. Nielsen, and E. Tajkhorshid Peptide aggregation and pore formation in a lipid bilayer: a combined coarse-grained and all atom molecular dynamics study Biophys. J. 95 2008 4337 4347
64. P.J. Stansfeld, and M.S.P. Sansom From coarse grained to atomistic: a serial multiscale approach to membrane protein simulations J. Chem. Theory Comput. 7 2011 1157 1166
65. P.J. Stansfeld, R. Hopkinson, F.M. Ashcroft, and M.S. Sansom PIP2-binding site in Kir channels: definition by multiscale biomolecular simulations Biochemistry 48 2009 10926 10933
66. J.B. Klauda, R.M. Venable, J.A. Freites, J.W. O'Connor, D.J. Tobias, C. Mondragon-Ramirez, I. Vorobyov, A.D. MacKerell, and R.W. Pastor Update of the CHARMM all-atom additive force field for lipids: validation on six lipid types J. Phys. Chem. B 114 2010 7830 7843
67. 2 dihedral angles J. Chem. Theory Comput. 8 2012 3257 3273
68. C.J. Dickson, B.D. Madej, Å. Skjevik, R.M. Betz, K. Teigen, I.R. Gould, and R.C. Walker Lipid14: the amber lipid force field J. Chem. Theory Comput. 10 2014 865 879
69. V. Hornak, R. Abel, A. Okur, B. Strockbine, A. Roitberg, and C. Simmerling Comparison of multiple amber force fields and development of improved protein backbone parameters Proteins Struct. Funct. Genet. 65 2006 712 725
70. D.H. de Jong, G. Singh, W.F.D. Bennett, C. Arnarez, T.A. Wassenaar, L.V. Schäfer, X. Periole, D.P. Tieleman, and S.J. Marrink Improved parameters for the Martini coarse-grained protein force field J. Chem. Theory Comput. 9 2013 687 697
71. S.J. Marrink, H.J. Risselada, S. Yefimov, D.P. Tieleman, and A.H. de Vries The MARTINI force field: coarse grained model for biomolecular simulations J. Phys. Chem. B 111 2007 7812 7824
72. J.B. Lim, B. Rogaski, and J.B. Klauda Update of the cholesterol force field parameters in CHARMM J. Phys. Chem. B 116 2012 203 210
73. Å. Skjevik, B.D. Madej, R.C. Walker, and K. Teigen LIPID11: a modular framework for lipid simulations using amber J. Phys. Chem. B 116 2012 11124 11136
74. A. Chattopadhyay, and D. Sengupta Biochim. Biophys. Acta Biomembr. 2015
75. F.J. Barrantes Cholesterol effects on nicotinic acetylcholine receptor J. Neurochem. 103 2007 72 80
76. A receptor to GABA in acutely dissociated rat hippocampal neurones Neuropharmacology 40 2001 178 184
77. R. Hurst, H. Rollema, and D. Bertrand Nicotinic acetylcholine receptors: from basic science to therapeutics Pharmacol. Ther. 137 2013 22 54
78. J.E. Baenziger, M. Morris, T.E. Darsaut, and S.E. Ryan Effect of membrane lipid composition on the conformational equilibria of the nicotinic acetylcholine receptor J. Biol. Chem. 275 2000 777 784
79. 3H]azicholesterol Biochemistry 45 2006 976 986
80. M.H. Cheng, Y. Xu, and P. Tang Anionic lipid and cholesterol interactions with α4β2 nAChR: insights from MD simulations J. Phys. Chem. B 113 2009 6964 6970
81. R. Søgaard, T.M. Werge, C. Bertelsen, C. Lundbye, K.L. Madsen, and C.H. Nielsen GABAA receptor function is regulated by lipid bilayer elasticity Biochemistry 45 2006 13118 13129
82. R.E. Hibbs, and E. Gouaux Principles of activation and permeation in an anion-selective Cys-loop receptor Nature 474 2011 54
83. V.K. Gribkoff, J.E. Starrett, and S.I. Dworetzky Maxi-K potassium channels: form, function, and modulation of a class of endogenous regulators of intracellular calcium Neuroscientist 7 2001 166 177
84. + channel Nature 466 2010 393 397
85. + (BK) channels J. Biol. Chem. 287 2012 20509 20521
86. B. Popp, A. Schmid, and R. Benz Role of sterols in the functional reconstitution of water-soluble mitochondrial porins from different organisms Biochemistry 34 1995 3352 3361
87. V. de Pinto, R. Benz, and F. Palmieri Interaction of non-classical detergents with the mitochondrial porin Biophys. J. 183 1989 179 187
88. P.R.L. Markwick, and J.A. McCammon Studying functional dynamics in bio-molecules using accelerated molecular dynamics Phys. Chem. Chem. Phys. 13 2011 20053 20065
89. H. Hibino, A. Inanobe, K. Furutani, S. Murakami, I. Findlay, and Y. Kurachi Inwardly rectifying potassium channels: their structure, function, and physiological roles Physiol. Rev. 90 2010 291 366
90. + current by optical isomers of cholesterol Biophys. J. 83 2002 3211 3222
91. D. Singh, T. Shentu, D. Enkvetchakul, and I. Levitan Cholesterol regulates prokaryotic Kir channel by direct binding to channel protein Biochim. Biophys. Acta Biomembr. 1808 2011 2527 2533
92. + channels by cholesterol PLoS One 6 2011 e19393
93. A. Rosenhouse-Dantsker, S. Noskov, S. Durdagi, D.E. Logothetis, and I. Levitan Identification of novel cholesterol-binding regions in Kir2 channels J. Biol. Chem. 288 2013 31154 31164
94. M. Nishida, M. Cadene, B.T. Chait, and R. MacKinnon Crystal structure of a Kir3.1 prokaryotic Kir channel chimera EMBO J. 26 2007 4005 4015
95. W.E.C. Harries, D. Akhavan, L.J.W. Miercke, S. Khademi, and R.M. Stroud The channel architecture of aquaporin 0 at a 2.2-Å resolution Proc. Natl. Acad. Sci. U. S. A. 101 2004 14045 14050
96. R.F. Jacob, R.J. Cenedella, and R.P. Mason Direct evidence for immiscible cholesterol domains in human ocular lens fiber cell plasma membranes J. Biol. Chem. 274 1999 31613 31618
97. J.W. O'Connor, and J.B. Klauda Lipid membranes with a majority of cholesterol: applications to the ocular lens and Aquaporin 0 J. Phys. Chem. B 115 2011 6455 6464
98. 2 + ATPase 2 (SERCA2) activity: cell biological implications Cell Calcium 38 2005 291 302
99. Y. Li, M. Ge, L. Ciani, G. Kuriakose, E.J. Westover, M. Dura, D.F. Covey, J.H. Freed, F.R. Maxfield, J. Lytton, and I. Tabas Enrichment of endoplasmic reticulum with cholesterol inhibits sarcoplasmic-endoplasmic reticulum calcium ATPase-2b activity in parallel with increased order of membrane lipids: implications for depletion of endoplasmic reticulum calcium stores and apoptosis in cholesterol-loaded macrophages Biol. Chem. 279 2004 37030 37039
100. 2+ -ATPase by cholesterol: a direct or indirect effect? 2015 (under revision)
101. A.L. Jensen, T.L. Sørensen, C. Olesen, J.V. Møller, and P. Nissen Modulatory and catalytic modes of ATP binding by the calcium pump EMBO J. 25 2006 2305 2314
102. L. Frasca, and R. Lande Role of defensins and cathelicidin LL37 in auto-immune and auto-inflammatory diseases Curr. Pharm. Biotechnol. 13 2012 1882 1897
103. M. Pasupuleti, A. Schmidtchen, and M. Malmsten Antimicrobial peptides: key components of the innate immune system Crit. Rev. Biotechnol. 32 2012 143 171
104. A. Quist, L. Doudevski, H. Lin, R. Azimova, D. Ng, B. Frangione, B. Kagan, J. Ghiso, and R. Lal Amyloid ion channels: a common structural link for protein-misfolding disease Proc. Natl. Acad. Sci. U. S. A. 102 2005 10427 10432
105. Y. Porat, S. Kolusheva, R. Jelinek, and E. Gazit The human islet amyloid polypeptide forms transient membrane-active prefibrillar assemblies Biochemistry 42 2003 10971 10977
106. M. Wakabayashi, and K. Matsuzaki Ganglioside-induced amyloid formation by human islet amyloid polypeptide in lipid rafts FEBS Lett. 583 2009 2854 2858
107. J.R. Brender, A.J. McHenry, and A. Ramamoorthy Does cholesterol play a role in the bacterial selectivity of antimicrobial peptides? Front. Immunol. 3 2012 (Article 195)
108. E. Cerf, A. Gustot, E. Goormaghtigh, J. Ruysschaert, and V. Raussens High ability of apolipoprotein E4 to stabilize amyloid-β peptide oligomers, the pathological entities responsible for Alzheimer's disease FASEB J. 25 2011 1585 1595
109. E. Karran, M. Mercken, and B. De Strooper The amyloid cascade hypothesis for Alzheimer's disease: an appraisal for the development of therapeutics Nat. Rev. Drug Discov. 10 2011 698 712
110. I. Benilova, E. Karran, and B. De Strooper The toxic Aβ oligomer and Alzheimer's disease: an emperor in need of clothes Nat. Neurosci. 15 2012 349 357
111. L.N. Zhao, S. Chiu, J. Benoit, L.Y. Chew, and Y. Mu Amyloid β peptides aggregation in a mixed membrane bilayer: a molecular dynamics study J. Phys. Chem. B 115 2011 12247 12256
112. C. Di Scala, J. Troadec, C. Lelievre, N. Garmy, J. Fantini, and H. Chahinian Mechanism of cholesterol-assisted oligomeric channel formation by a short Alzheimer β-amyloid peptide J. Neurochem. 128 2014 186 195
113. X. Zhou, and J. Xu Free cholesterol induces higher β-sheet content in Aβ peptide oligomers by aromatic interaction with Phe19 PLoS One 7 2012 e46245
114. C. Di Scala, H. Chahinian, N. Yahi, N. Garmy, and J. Fantini Interaction of Alzheimer's β-amyloid peptides with cholesterol: mechanistic insights into amyloid pore formation Biochemistry 53 2014 4489 4502
115. L. Qiu, C. Buie, A. Reay, M.W. Vaughn, and K.H. Cheng Molecular dynamics simulations reveal the protective role of cholesterol in β-amyloid protein-induced membrane disruptions in neuronal membrane mimics J. Phys. Chem. B 115 2011 9795 9812
116. X. Yu, and J. Zheng Cholesterol promotes the interaction of Alzheimer β-amyloid monomer with lipid bilayer J. Mol. Biol. 421 2012 561 571
117. C. Di Scala, N. Yahi, C. Lelievre, N. Garmy, H. Chahinian, and J. Fantini Biochemical identification of a linear cholesterol-binding domain within Alzheimer's β amyloid peptide ACS Chem. Neurosci. 4 2013 509 517
118. N. Liguori, P.S. Nerenberg, and T. Head-Gordon Embedding Aβ42 in heterogeneous membranes depends on cholesterol asymmetries Biophys. J. 105 2013 899 910
119. A. Kakio, S. Nishimoto, K. Yanagisawa, Y. Kozutsumi, and K. Matsuzaki Cholesterol-dependent formation of GM1 ganglioside-bound amyloid β-protein, an endogenous seed for Alzheimer amyloid J. Biol. Chem. 276 2001 24985 24990
120. J. Fantini, N. Yahi, and N. Garmy Cholesterol accelerates the binding of Alzheimer's β-amyloid peptide to ganglioside GM1 through a universal hydrogen-bond-dependent sterol tuning of glycolipid conformation Front. Physiol. 4 2013 120
121. M. Burns, K. Gaynor, V. Olm, M. Mercken, J. LaFrancois, L.L. Wang, P.M. Mathews, W. Noble, Y. Matsuoka, and K. Duff Presenilin redistribution associated with aberrant cholesterol transport enhances β-amyloid production in vivo J. Neurosci. 23 2003 5645 5649
122. K. Fassbender, M. Simons, C. Bergmann, M. Stroick, D. Lutjohann, P. Keller, H. Runz, S. Kuhl, T. Bertsch, K. von Bergmannn, M. Hennerici, K. Beyreuther, and T. Hartmann Simvastatin strongly reduces levels of Alzheimer's disease β-amyloid peptides Aβ42 and Aβ40 in vitro and in vivo Proc. Natl. Acad. Sci. U. S. A. 98 2001 5856 5861
123. S.R. Ji, Y. Wu, and S.F. Sui Cholesterol is an important factor affecting the membrane insertion of β-amyloid peptide (Aβ1-40), which may potentially inhibit the fibril formation J. Biol. Chem. 277 2002 6273 6279
124. S. Micelli, D. Meleleo, V. Picciarelli, and E. Gallucci Effect of sterols on β-amyloid peptide (AβP 1-40) channel formation and their properties in planar lipid membranes Biophys. J. 86 2004 2231 2237
125. J. Fantini, C. Di Scala, N. Yahi, J. Troadec, K. Sadelli, H. Chahinian, and N. Garmy Bexarotene blocks calcium-permeable ion channels formed by neurotoxic Alzheimer's β-amyloid peptides ACS Chem. Neurosci. 5 2014 216 224
126. Z. Niu, W. Zhao, Z. Zhang, F. Xiao, X. Tang, and J. Yang The molecular structure of Alzheimer β-amyloid fibrils formed in the presence of phospholipid vesicles Angew. Chem. Int. Ed. 53 2014 9294 9297
127. A.T. Alexandrescu Amyloid accomplices and enforcers Protein Sci. 14 2005 1 12
128. G.P. Gellermann, T.R. Appel, A. Tannert, A. Radestock, P. Hortschansky, V. Schroeckh, C. Leisner, T. Lütkepohl, S. Shtrasburg, C. Röcken, M. Pras, R.P. Linke, S. Diekmann, and M. Fändrich Raft lipids as common components of human extracellular amyloid fibrils Proc. Natl. Acad. Sci. U. S. A. 102 2005 6297 6302
129. J.D. Knight, J.A. Hebda, and A.D. Miranker Conserved and cooperative assembly of membrane-bound α-helical states of islet amyloid polypeptide Biochemistry 45 2006 9496 9508
130. M.F.M. Engel, H. Yigittop, R.C. Elgersma, D.T.S. Rijkers, R.M.J. Liskamp, B. de Kruijff, J.W.M. Höppener, and J.A. Killian Islet amyloid polypeptide inserts into phospholipid monolayers as monomer J. Mol. Biol. 356 2006 783 789
131. S. Shim, R. Gupta, Y.L. Ling, D.B. Strasfeld, D.P. Raleigh, and M.T. Zanni Two-dimensional IR spectroscopy and isotope labeling defines the pathway of amyloid formation with residue-specific resolution Proc. Natl. Acad. Sci. U. S. A. 106 2009 6614 6619
132. W. Xu, G. Wei, H. Su, L. Nordenskiöld, and Y. Mu Effects of cholesterol on pore formation in lipid bilayers induced by human islet amyloid polypeptide fragments: a coarse-grained molecular dynamics study Phys. Rev. E 84 2011 051922
133. 1-19 in micelles by NMR spectroscopy Biochemistry 47 2008 12689 12697
134. N. Normanno, A. De Luca, C. Bianco, L. Strizzi, M. Mancino, M.R. Maiello, A. Carotenuto, G. De Feo, F. Caponigro, and D.S. Salomon Epidermal growth factor receptor (EGFR) signaling in cancer Gene 366 2006 2 16
135. J. Schlessinger Cell signaling by receptor tyrosine kinases Cell 103 2000 211 225
136. E.V. Bocharov, K.S. Mineev, P.E. Volynsky, Y.S. Ermolyuk, E.N. Tkach, A.G. Sobol, V.V. Chupin, M.P. Kirpichnikov, R.G. Efremov, and A.S. Arseniev Spatial structure of the dimeric transmembrane domain of the growth factor receptor ErbB2 presumably corresponding to the receptor active state J. Biol. Chem. 283 2008 6950 6956
137. L.J. Pike Growth factor receptors, lipid rafts and caveolae: an evolving story Biochim. Biophys. Acta 1746 2005 260 273
138. A. Prakash, L. Janosi, and M. Doxastakis GxxxG motifs, phenylalanine, and cholesterol guide the self-association of transmembrane domains of ErbB2 receptors Biophys. J. 101 2011 1949 1958
139. Y. Sonntag, M. Musgaard, C. Olesen, B. Schiøtt, J.V. Møller, P. Nissen, and L. Thøgersen Mutual adaptation of a membrane protein and its lipid bilayer during conformational changes Nat. Commun. 2 2011 304
140. D.H. MacLennan, and E.G. Kranias Phospholamban: a crucial regulator of cardiac contractility Nat. Rev. Mol. Cell Biol. 4 2003 566 577
141. M. Manna, and C. Mukhopadhyay Cholesterol driven alteration of the conformation and dynamics of phospholamban in model membranes Phys. Chem. Chem. Phys. 13 2011 20188 20198
142. N.J. Traaseth, L. Shi, R. Verardi, D.G. Mullen, G. Barany, and G. Veglia Structure and topology of monomeric phospholamban in lipid membranes determined by a hybrid solution and solid-state NMR approach Proc. Natl. Acad. Sci. U. S. A. 106 2009 10165 10170
143. R. Verardi, L. Shi, N.J. Traaseth, N. Walsh, and G. Veglia Structural topology of phospholamban pentamer in lipid bilayers by a hybrid solution and solid-state NMR method Proc. Natl. Acad. Sci. U. S. A. 108 2011 9101 9106
144. A. De Simone, M. Gustavsson, R.W. Montalvao, L. Shi, G. Veglia, and M. Vendruscolo Structures of the excited states of phospholamban and shifts in their populations upon phosphorylation Biochemistry 52 2013 6684 6694
145. C.M. Miller, A.C. Brown, and J. Mittal Disorder in cholesterol-binding functionality of CRAC peptides: a molecular dynamics study J. Phys. Chem. B 118 2014 13169 13174
146. G.L. Nicolson, and M.E. Ash Lipid Replacement Therapy: a natural medicine approach to replacing damaged lipids in cellular membranes and organelles and restoring function Biochim. Biophys. Acta Biomembr. 1838 2014 1657 1679
147. E.S. Paulsen, J. Villadsen, E. Tenori, H. Liu, D.F. Bonde, M.A. Lie, M. Bublitz, C. Olesen, H.E. Autzen, I. Dach, P. Sehgal, P. Nissen, J.V. Møller, B. Schiøtt, and S.B. Christensen Water-mediated interactions influence the binding of thapsigargin to sarco/endoplasmic reticulum calcium adenosinetriphosphatase J. Med. Chem. 56 2013 3609 3619