Where Biology Meets Physics—A Converging View on Membrane Microdomain Dynamics

Current Topics in Membranes

Volumn 77, Issue , 2016, Pages 27-65

  Destainville, Nicolas ^a   Schmidt, Thomas H ^b   Lang, Thorsten ^b  

^a CNRS   (France)

^b UNIVERSITY OF BONN   (Germany)

Author keywords

Cluster phases; Equilibrium model; Fence and picket model; Membrane proteins; Membrane rafts; Microdomains; Out of equilibrium model; Syntaxin

Indexed keywords

SNARE PROTEIN;

BIOLOGICAL MODEL; BIOPHYSICS; CHEMISTRY; MEMBRANE MICRODOMAIN; METABOLISM;

BIOPHYSICAL PHENOMENA; MEMBRANE MICRODOMAINS; MODELS, BIOLOGICAL; SNARE PROTEINS;

EID: 84961175328     PISSN: 10635823     EISSN: None     Source Type: Book Series    
DOI: 10.1016/bs.ctm.2015.10.004     Document Type: Article

References (136)

1. Abney, J.R., Scalettar, B.A., Molecular crowding and protein organization. Jackson, M.B., (eds.) Thermodynamics of membrane receptors and channels, 1993, CRC Press, Boca Raton, 183–225.
2. Abney, J.R., Scalettar, B.A., Fluctuations and membrane heterogeneity. Biophysical Chemistry 57 (1995), 27–36.
3. Anderson, R.G., Jacobson, K., A role for lipid shells in targeting proteins to caveolae, rafts, and other lipid domains. Science 296 (2002), 1821–1825.
4. Antoku, Y., Dedecker, P., Pinheiro, P.S., Vosch, T., Sørensen, J.B., Spatial distribution and temporal evolution of DRONPA-fused SNAP25 clusters in adrenal chromaffin cells. Photochemical and Photobiological Sciences 14 (2015), 1005–1012.
5. Aoyagi, K., Sugaya, T., Umeda, M., Yamamoto, S., Terakawa, S., Takahashi, M., The activation of exocytotic sites by the formation of phosphatidylinositol 4,5-bisphosphate microdomains at syntaxin clusters. The Journal of Biological Chemistry 280 (2005), 17346–17352.
6. Banjade, S., Rosen, M.K., Phase transitions of multivalent proteins can promote clustering of membrane receptors. eLife, 3, 2014, e04123.
7. Barg, S., Knowles, M.K., Chen, X., Midorikawa, M., Almers, W., Syntaxin clusters assemble reversibly at sites of secretory granules in live cells. Proceedings of the National Academy of Sciences of the United States of America 107 (2010), 20804–20809.
8. Bar-On, D., Gutman, M., Mezer, A., Ashery, U., Lang, T., Nachliel, E., Evaluation of the heterogeneous reactivity of the syntaxin molecules on the inner leaflet of the plasma membrane. Journal of Neuroscience 29 (2009), 12292–12301.
9. Bar-On, D., Winter, U., Nachliel, E., Gutman, M., Fasshauer, D., Lang, T., et al. Imaging the assembly and disassembly kinetics of cis-SNARE complexes on native plasma membranes. FEBS Letters 582 (2008), 3563–3568.
10. Bar-On, D., Wolter, S., van de Linde, S., Heilemann, M., Nudelman, G., Nachliel, E., et al. Super-resolution imaging reveals the internal architecture of nano-sized syntaxin clusters. The Journal of Biological Chemistry 287 (2012), 27158–27167.
11. Bass, R.B., Strop, P., Barclay, M., Rees, D.C., Crystal structure of Escherichia coli MscS, a voltage-modulated and mechanosensitive channel. Science 298 (2002), 1582–1587.
12. Bennett, V., Lorenzo, D.N., Spectrin- and ankyrin-based membrane domains and the evolution of vertebrates. Current Topics in Membranes 72 (2013), 1–37.
13. Blood, P.D., Voth, G.A., Direct observation of Bin/amphiphysin/Rvs (BAR) domain-induced membrane curvature by means of molecular dynamics simulations. Proceedings of the National Academy of Sciences of the United States of America 103 (2006), 15068–15072.
14. van den Bogaart, G., Lang, T., Jahn, R., Microdomains of SNARE proteins in the plasma membrane. Current Topics in Membranes 72 (2013), 193–230.
15. van den Bogaart, G., Meyenberg, K., Risselada, H.J., Amin, H., Willig, K.I., Hubrich, B.E., et al. Membrane protein sequestering by ionic protein-lipid interactions. Nature 479 (2011), 552–555.
16. Borodich, A., Rojdestvenski, I., Cottam, M., Lateral heterogeneity of photosystems in thylakoid membranes studied by brownian dynamics simulations. Biophysical Journal 85 (2003), 774–789.
17. Bray, A.J., Theory of phase ordering kinetics. Advances in Physics 43 (1994), 357–459.
18. Buyukdagli, S., Manghi, M., Palmeri, J., Ionic capillary evaporation in weakly charged nanopores. Physical Review Letters, 105, 2010, 158103.
19. Campelo, F., Kozlov, M.M., Sensing membrane stresses by protein insertions. PLoS Computational Biology, 10, 2014, e1003556.
20. Casuso, I., Sens, P., Rico, F., Scheuring, S., Experimental evidence for membrane-mediated protein–protein interaction. Biophysical Journal 99 (2010), L47–L49.
21. Chaikin, P.M., Lubensky, T.C., Principles of condensed matter physics. 1995, Cambridge University Press, Cambridge.
22. Chamberlain, L.H., Burgoyne, R.D., Gould, G.W., SNARE proteins are highly enriched in lipid rafts in PC12 cells: implications for the spatial control of exocytosis. Proceedings of the National Academy of Sciences of the United States of America 98 (2001), 5619–5624.
23. Contreras, F.X., Ernst, A.M., Wieland, F., Brügger, B., Specificity of intramembrane protein–lipid interactions. Cold Spring Harbor Perspectives in Biology, 3, 2011, a004705.
24. Dan, N., Pincus, P., Safran, S.A., Membrane-induced interactions between inclusions. Langmuir 9 (1993), 2768–2771.
25. Daumas, F., Destainville, N., Millot, C., Lopez, A., Dean, D., Salome, L., Confined diffusion without fences of a G-protein-coupled receptor as revealed by single particle tracking. Biophysical Journal 84 (2003), 356–366.
26. Destainville, N., Cluster phases of membrane proteins. Physical Review E: Statistical, Nonlinear, and Soft Matter Physics, 77, 2008, 011905.
27. Destainville, N., An alternative scenario for the formation of specialized protein nano-domains (cluster phases) in biomembranes. Europhysics Letters, 91, 2010, 58001.
28. Destainville, N., Foret, L., Thermodynamics of nano-cluster phases: a unifying theory. Physical Review E: Statistical, Nonlinear, and Soft Matter Physics, 77, 2008, 051403.
29. + conduction and selectivity. Science 280 (1998), 69–77.
30. Dupuy, A.D., Engelman, D.M., Protein area occupancy at the center of the red blood cell membrane. Proceedings of the National Academy of Sciences of the United States of America 105 (2008), 2848–2852.
31. Espenel, C., Margeat, E., Dosset, P., Arduise, C., Le Grimellec, C., Royer, C.A., et al. Single-molecule analysis of CD9 dynamics and partitioning reveals multiple modes of interaction in the tetraspanin web. Journal of Cell Biology 182 (2008), 765–776.
32. Fan, J., Sammalkorpi, M., Haataja, M., Formation and regulation of lipid microdomains in cell membranes: theory, modeling, and speculation. FEBS Letters 584 (2010), 1678–1684.
33. Fan, J., Sammalkorpi, M., Haataja, M., Influence of nonequilibrium lipid transport, membrane compartmentalization, and membrane proteins on the lateral organization of the plasma membrane. Physical Review E: Statistical, Nonlinear, and Soft Matter Physics, 81, 2010, 011908.
34. Fan, J., Sammalkorpi, M., Haataja, M., Lipid microdomains: structural correlations, fluctuations, and formation mechanisms. Physical Review Letters, 104, 2010, 118101.
35. Fasshauer, D., Margittai, M., A transient N-terminal interaction of SNAP-25 and syntaxin nucleates SNARE assembly. The Journal of Biological Chemistry 279 (2004), 7613–7621.
36. Foret, L., A simple mechanism of raft formation in two-component fluid membranes. Europhysics Letters 71 (2005), 508–514.
37. Foret, L., Aggregation on a membrane of particles undergoing active exchange with a reservoir. European Physical Journal E Soft Matter, 35, 2012, 12.
38. de Gennes, P.G., Scaling concepts in polymer physics. 1979, Cornell University Press, Ithaca.
39. Gheber, L.A., Edidin, M., A model for membrane patchiness: lateral diffusion in the presence of barriers and vesicle traffic. Biophysical Journal 77 (1999), 3163–3175.
40. Gil, T., Ipsen, J.H., Mouritsen, O.G., Sabra, M.C., Sperotto, M.M., Zuckermann, M.J., Theoretical analysis of protein organization in lipid membranes. Biochimica et Biophysica Acta Biomembranes 1376 (1998), 245–266.
41. Gil, T., Ipsen, J.H., Tejero, C.F., Wetting controlled phase transitions in two-dimensional systems of colloids. Physical Review E: Statistical, Nonlinear, and Soft Matter Physics 57 (1998), 3123–3133.
42. Gil, T., Sabra, M.C., Ipsen, J.H., Mouritsen, O.G., Wetting and capillary condensation as means of protein organization in membranes. Biophysical Journal 73 (1997), 1728–1741.
43. Goh, S.L., Amazon, J.J., Feigenson, G.W., Toward a better raft model: modulated phases in the four-component bilayer, DSPC/DOPC/POPC/CHOL. Biophysical Journal 104 (2013), 853–862.
44. Gómez, J., Sagués, F., Reigada, R., Nonequilibrium patterns in phase-separating ternary membranes. Physical Review E: Statistical, Nonlinear, and Soft Matter Physics, 80, 2009, 011920.
45. Goulian, M., Bruinsma, R., Pincus, P., Long-range forces in heterogeneous fluid membranes. Europhysics Letters 22 (1993), 145–150.
46. Gueguen, G., Destainville, N., Manghi, M., Mixed lipid bilayers with locally varying spontaneous curvature and bending. European Physical Journal E Soft matter, 37, 2014, 76.
47. Gulik-Krzywicki, T., Seigneuret, M., Rigaud, J.L., Monomer-oligomer equilibrium of bacteriorhodopsin in reconstituted proteoliposomes. The Journal of Biological Chemistry 262 (1987), 15580–15588.
48. Gurry, T., Kahramanogullari, O., Endres, R.G., Biophysical mechanism for Ras-nanocluster formation and signaling in plasma membrane. PLoS One, 4, 2009, e6148.
49. Halemani, N.D., Bethani, I., Rizzoli, S.O., Lang, T., Structure and dynamics of a two-helix SNARE complex in live cells. Traffic 11 (2010), 394–404.
50. Hancock, J.F., Ras proteins: different signals from different locations. Nature Review Molecular Cell Biology 4 (2003), 373–384.
51. Hancock, J.F., Lipid rafts: contentious only from simplistic standpoints. Nature Review Molecular Cell Biology 7 (2006), 456–462.
52. Harder, T., Formation of functional cell membrane domains: the interplay of lipid- and protein-mediated interactions. Philosophical Transactions of the Royal Society of London B 358 (2003), 863–868.
53. He, M., Abdi, K.M., Bennett, V.J., Ankyrin-G palmitoylation and βII-spectrin binding to phosphoinositide lipids drive lateral membrane assembly. Journal of Cell Biology 206 (2014), 273–288.
54. Henis, Y.I., Hancock, J.F., Prior, I.A., Ras acylation, compartmentalization and signaling nanoclusters (Review). Molecular Membrane Biology 26 (2009), 80–92.
55. Homsi, Y., Schloetel, J., Scheffer, K.D., Schmidt, T.H., Destainville, N., Florin, L., et al. The extracellular δ-domain is essential for the formation of CD81 tetraspanin webs. Biophysical Journal 107 (2014), 100–113.
56. Honigmann, A., van den Bogaart, G., Iraheta, E., Risselada, H.J., Milovanovic, D., Mueller, V., et al. Phosphatidylinositol 4,5-bisphosphate clusters act as molecular beacons for vesicle recruitment. Nature Structural and Molecular Biology 20 (2013), 679–686.
57. Jacobson, K., Mouritsen, O.G., Anderson, R.G.W., Lipid rafts: at a crossroad between cell biology and physics. Nature Cell Biology 9 (2007), 7–14.
58. Jahn, R., Fasshauer, D., Molecular machines governing exocytosis of synaptic vesicles. Nature 490 (2012), 201–207.
59. James, D.J., Khodthong, C., Kowalchyk, J.A., Martin, T.F.J., Phosphatidylinositol 4,5-bisphosphate regulates SNARE-dependent membrane fusion. Journal of Cell Biology 182 (2008), 355–366.
60. James, D.J., Kowalchyk, J., Daily, N., Petrie, M., Martin, T.F.J., CAPS drives trans-SNARE complex formation and membrane fusion through syntaxin interactions. PNAS 106 (2009), 17308–17313, 10.1073/pnas.0900755106.
61. Kai, M., Sakane, F., Jia, Y.F., Imai, S., Yasuda, S., Hanoh, H., Lipid phosphate phosphatases 1 and 3 locate in distinct lipid rafts. Journal of Biochemistry 140 (2006), 677–686.
62. Khuong, T.M., Habets, R.L., Kuenen, S., Witkowska, A., Kasprowicz, J., Swerts, J., et al. Synaptic PI(3,4,5)P3 is required for Syntaxin1A clustering and neurotransmitter release. Neuron 77 (2013), 1097–10108.
63. Knowles, M.K., Barg, S., Wan, L., Midorikawa, M., Chen, X., Almers, W., Single secretory granules of live cells recruit syntaxin-1 and synaptosomal associated protein 25 (SNAP-25) in large copy numbers. Proceedings of the National Academy of Sciences of the United States of America 107 (2010), 20810–20815.
64. Kusumi, A., Nakada, C., Ritchie, K., Murase, K., Suzuki, K., Murakoshi, H., et al. Paradigm shift of the plasma membrane concept from the two-dimensional continuum fluid to the partitioned fluid: high-speed single-molecule tracking of membrane molecules. Annual Review of Biophysics and Biomolecular Structure 34 (2005), 351–378.
65. Kusumi, A., Sako, Y., Yamamoto, M., Confined lateral diffusion of membrane receptors as studied by single particle tracking (nanovid microscopy). Effects of calcium-induced differentiation in cultured epithelial cells. Biophysical Journal 65 (1993), 2021–2040.
66. Lai, E.C., Lipid rafts make for slippery platforms. Journal of Cell Biology 162 (2003), 365–370.
67. Lang, T., SNARE proteins and ‘membrane rafts’. The Journal of Physiology 585 (2007), 693–698.
68. Lang, T., Bruns, D., Wenzel, D., Riedel, D., Holroyd, P., Thiele, C., et al. SNAREs are concentrated in cholesterol-dependent clusters that define docking and fusion sites for exocytosis. The EMBO Journal 20 (2001), 2202–2213.
69. Lang, T., Margittai, M., Hölzler, H., Jahn, R., SNAREs in native plasma membranes are active and readily form core complexes with endogenous and exogenous SNAREs. Journal of Cell Biology 158 (2002), 751–760.
70. Lang, T., Rizzoli, S.O., Membrane protein clusters at nanoscale resolution: more than pretty pictures. Physiology 25 (2010), 116–124.
71. Lee, A.G., Lipid–protein interactions in biological membranes: a structural perspective. Biochimica et Biophysica Acta Biomembranes 1612 (2003), 1–40.
72. Lee, A.G., Birdsall, N.J., Metcalfe, J.C., Toon, P.A., Warren, G.B., Clusters in lipid bilayers and the interpretation of thermal effects in biological membranes. Biochemistry 13 (1974), 3699–3705.
73. Lenne, P.F., Nicolas, A., Physics puzzles on membrane domains posed by cell biology. Soft Matter 5 (2009), 2841–2848.
74. Lerman, J.C., Robblee, J., Fairman, R., Hughson, F.M., Structural analysis of the neuronal SNARE protein syntaxin-1A. Biochemistry 39 (2000), 8470–8479.
75. Lillemeier, B.F., Pfeiffer, J.R., Surviladze, Z., Wilson, B.S., Davis, M.M., Plasma membrane-associated proteins are clustered into islands attached to the cytoskeleton. Proceedings of the National Academy of Sciences of the United States of America 103 (2006), 18992–18997.
76. Lingwood, D., Simons, K., Lipid rafts as a membrane-organizing principle. Science 327 (2010), 46–50.
77. Lipowsky, R., Domain-induced budding of fluid membranes. Biophysical Journal 64 (1993), 1133–1138.
78. Low, S.H., Vasanji, A., Nanduri, J., He, M., Sharma, N., Koo, M., et al. Syntaxins 3 and 4 are concentrated in separate clusters on the plasma membrane before the establishment of cell polarity. Molecular Biology of the Cell 17 (2006), 977–989.
79. Manglik, A., Kruse, A.C., Kobilka, T.S., Thian, F.S., Mathiesen, J.M., Sunahara, R.K., et al. Crystal structure of the μ-opioid receptor bound to a morphinan antagonist. Nature 485 (2012), 321–326.
80. Meilhac, N., Destainville, N., Clusters of proteins in bio-membranes: insights into the roles of interaction potential shapes and of protein diversity. Journal of Physical Chemistry B 115 (2011), 7190–7199.
81. de Meyer, F.J.M., Venturoli, M., Smit, B., Molecular simulations of lipid-mediated protein–protein interactions. Biophysical Journal 95 (2008), 1851–1865.
82. Milovanovic, D., Honigmann, A., Koike, S., Göttfert, F., Pähler, G., Junius, M., et al. Hydrophobic mismatch sorts SNARE proteins into distinct membrane domains. Nature Communications, 6, 2015, 5984.
83. Milovanovic, D., Jahn, R., Organization and dynamics of SNARE proteins in the presynaptic membrane. Frontiers in Physiology, 6, 2015, 89.
84. Mouritsen, O.G., Life—As a matter of fat. 2005, Springer, Berlin.
85. Munro, S., Lipid rafts: elusive or illusive?. Cell 115 (2003), 377–388.
86. Murase, K., Fujiwara, T., Umemura, Y., Suzuki, K., Iino, R., Yamashita, H., et al. Ultrafine membrane compartments for molecular diffusion as revealed by single molecule techniques. Biophysical Journal 86 (2004), 4075–4093.
87. Murray, D.H., Tamm, L.K., Clustering of syntaxin-1A in model membranes is modulated by phosphatidylinositol 4,5-bisphosphate and cholesterol. Biochemistry 48 (2009), 4617–4625.
88. Murray, D.H., Tamm, L.K., Molecular mechanism of cholesterol- and polyphosphoinositide-mediated syntaxin clustering. Biochemistry 50 (2011), 9014–9022.
89. Neder, J., West, B., Nielaba, P., Schmidt, F., Membrane-mediated protein-protein interaction: a Monte Carlo study. Current Nanoscience 7 (2011), 656–666.
90. Nielsen, C., Goulian, M., Andersen, O.S., Energetics of inclusion-induced bilayer deformations. Biophysical Journal 74 (1998), 1966–1983.
91. Ohara-Imaizumi, M., Nishiwaki, C., Nakamichi, Y., Kikuta, T., Nagai, S., Nagamatsu, S., Correlation of syntaxin-1 and SNAP-25 clusters with docking and fusion of insulin granules analysed by total internal reflection fluorescence microscopy. Diabetologia 47 (2004), 2200–2207.
92. Onuki, A., Phase transition dynamics. 2002, Cambridge University Press, Cambridge.
93. Park, J.H., Scheerer, P., Hofmann, K.P., Choe, H.W., Ernst, O.P., Crystal structure of the ligand-free G-protein-coupled receptor opsin. Nature 454 (2008), 183–187.
94. Periole, X., Knepp, A.M., Sakmar, T.P., Marrink, S.J., Hubert, T., Structural determinants of the supramolecular organization of G protein-coupled receptors in bilayers. Journal of the American Chemical Society 134 (2012), 10959–10965.
95. Pertsinidis, A., Mukherjee, K., Sharma, M., Pang, Z.P., Park, S.R., Zhang, Y., et al. Ultrahigh-resolution imaging reveals formation of neuronal SNARE/Munc18 complexes in situ. Proceedings of the National Academy of Sciences of the United States of America 110 (2013), E2812–E2820.
96. Pierce, S.K., To cluster or not to cluster: FRETting over rafts. Nature Cell Biology 6 (2004), 180–181.
97. Pike, L.J., Rafts defined: a report on the Keystone Symposium on Lipid Rafts and Cell Function. Journal of Lipid Research 47 (2006), 1597–1598.
98. Plowman, S.J., Ariotti, N., Goodall, A., Parton, R.G., Hancock, J.F., Electrostatic interactions positively regulate K-Ras nanocluster formation and function. Molecular and Cellular Biology 28 (2008), 4377–4385.
99. Pobbati, A.V., Stein, A., Fasshauer, D., N- to C-terminal SNARE complex assembly promotes rapid membrane fusion. Science 313 (2006), 673–676.
100. Reynwar, B.J., Deserno, M., Membrane composition-mediated protein-protein interactions. Biointerphases 3 (2009), FA117–FA124.
101. Ribrault, C., Reingruber, J., Petković, M., Galli, T., Ziv, N.E., Holcman, D., et al. Syntaxin1A lateral diffusion reveals transient and local SNARE interactions. Journal of Neuroscience 31 (2011), 17590–17602.
102. Rickman, C., Medine, C.N., Dun, A.R., Moulton, D.J., Mandula, O., Halemani, N.D., et al. t-SNARE protein conformations patterned by the lipid microenvironment. The Journal of Biological Chemistry 285 (2010), 13535–13541.
103. Sabra, M.C., Mouritsen, O.G., Steady-state compartmentalization of lipid membranes by active proteins. Biophysical Journal 74 (1998), 745–752.
104. Safran, S.A., Statistical thermodynamics of surfaces, interfaces, and membranes. 1994, Perseus, Cambridge.
105. Saka, S.K., Honigmann, A., Eggeling, C., Hell, S.W., Lang, T., Rizzoli, S.O., Multi-protein assemblies underlie the mesoscale organization of the plasma membrane. Nature Communications, 5, 2014, 4509.
106. Salaün, C., James, D.J., Chamberlain, L.H., Lipid rafts and the regulation of exocytosis. Traffic 5 (2004), 255–264.
107. Saric, A., Cacciuto, A., Self-assembly of nanoparticles adsorbed on fluid and elastic membranes. Soft Matter 9 (2013), 6677–6695.
108. Schmidt, U., Guigas, G., Weiss, M., Cluster formation of transmembrane proteins due to hydrophobic mismatching. Physical Review Letters, 101, 2008, 128104.
109. Schreiber, A., Fischer, S., Lang, T., The amyloid precursor protein forms plasmalemmal clusters via its pathogenic amyloid-β domain. Biophysical Journal 102 (2012), 1411–1417.
110. Seul, M., Andelman, D., Domain shapes and patterns: the phenomenology of modulated phases. Science 267 (1995), 476–483.
111. Sharma, P., Varma, R., Sarasij, R.C., Ira, Gousset, K., Krishnamoorthy, G., et al. Nanoscale organization of multiple GPI-anchored proteins in living cell membranes. Cell 116 (2004), 577–589.
112. Shimobayashi, S.F., Ichikawa, M., Taniguchi, T., Phase-separation transitions in asymmetric lipid bilayers. 2015 Preprint http://arxiv.org/abs/1504.03038.
113. Sieber, J.J., Willig, K.I., Heintzmann, R., Hell, S.W., Lang, T., The SNARE motif is essential for the formation of syntaxin clusters in the plasma membrane. Biophysical Journal 90 (2006), 2843–2851.
114. Sieber, J.J., Willig, K.I., Kutzner, C., Gerding-Reimers, C., Harke, B., Donnert, G., et al. Anatomy and dynamics of a supramolecular membrane protein cluster. Science 317 (2007), 1072–1076.
115. Simons, K., Ikonen, E., Functional rafts in cell membranes. Nature 387 (1997), 569–572.
116. Singer, S.J., Nicolson, G.L., The fluid mosaic model of the structure of cell membranes. Science 175 (1972), 720–731.
117. Stradner, A., Sedgwick, H., Cardinaux, F., Poon, W.C.K., Egelhaaf, S.U., Schurtenberger, P., Equilibrium cluster formation in concentrated protein solutions and colloids. Nature 432 (2004), 492–495.
118. Sumino, A., Yamamoto, D., Iwamoto, M., Dewa, T., Oiki, S., Gating-associated clustering-dispersion dynamics of the KcsA potassium channel in a lipid membrane. Physical Chemistry Letters 5 (2014), 578–584.
119. Takamori, S., Holt, M., Stenius, K., Lemke, E.A., Grønborg, M., Riedel, D., et al. Molecular anatomy of a trafficking organelle. Cell 127 (2006), 831–846.
120. Turner, M.S., Sens, P., Socci, N.D., Nonequilibrium raftlike membrane domains under continuous recycling. Physical Review Letters, 95, 2005, 168301.
121. Uhles, S., Moede, T., Leibiger, B., Berggren, P.O., Leibiger, I.B., Isoform-specific insulin receptor signaling involves different plasma membrane domains. Journal of Cell Biology 163 (2003), 1327–1337.
122. Ursell, T.S., Klug, W.S., Phillips, R., Morphology and interaction between lipid domains. Proceedings of the National Academy of Sciences of the United States of America 106 (2009), 13301–13306.
123. Veatch, S.L., Cicuta, P., Sengupta, P., Honerkamp-Smith, A., Holowka, D., Baird, B., Critical fluctuations in plasma membrane vesicles. ACS Chemical Biology 3 (2008), 287–293.
124. Vereb, G., Szollosi, J., Matko, J., Nagy, P., Farkas, T., Vigh, L., et al. Dynamic, yet structured: the cell membrane three decades after the Singer–Nicolson model. Proceedings of the National Academy of Sciences of the United States of America 100 (2003), 8053–8058.
125. Wasnik, V., Wingreen, N.S., Mukhopadhyay, R., Modeling curvature-dependent subcellular localization of the small sporulation protein SpoVM in bacillus subtilis. PLoS One, 10, 2015, e0111971.
126. Weikl, T.R., Kozlov, M.M., Helfrich, W., Interaction of conical membrane inclusions: effect of lateral tension. Physical Review E: Statistical, Nonlinear, and Soft Matter Physics 57 (1998), 6988–6995.
127. Weitz, S., Destainville, N., Attractive asymmetric inclusions in elastic membranes under tension: cluster phases and membrane invaginations. Soft Matter 9 (2013), 7804–7816.
128. Wilhelm, B.G., Mandad, S., Truckenbrodt, S., Kröhnert, K., Schäfer, C., Rammner, B., et al. Composition of isolated synaptic boutons reveals the amounts of vesicle trafficking proteins. Science 344 (2014), 1023–1028.
129. Willig, K., Keller, J., Bossi, M., Hell, S.W., STED microscopy resolves nanoparticle assemblies. New Journal of Physics, 8, 2006, 106.
130. Wunderlich, F., Kreutz, W., Mahler, P., Ronai, A., Heppeler, G., Thermotropic fluid goes to ordered “discontinuous” phase separation in microsomal lipids of Tetrahymena. An X-ray diffraction study. Biochemistry 17 (1978), 2005–2010.
131. Xu, K., Zhong, G., Zhuang, X., Actin, spectrin, and associated proteins form a periodic cytoskeletal structure in axons. Science 339 (2013), 452–456.
132. Yang, L., Dun, A.R., Martin, K.J., Qiu, Z., Dunn, A., Lord, G.J., et al. Secretory vesicles are preferentially targeted to areas of low molecular SNARE density. PLoS One, 7, 2012, e49514.
133. Zhong, G., He, J., Zhou, R., Lorenzo, D., Babcock, H.P., Bennett, V., et al. Developmental mechanism of the periodic membrane skeleton in axons. eLife, 3, 2014, 04581.
134. 2+ induces clustering of membrane proteins in the plasma membrane via electrostatic interactions. The EMBO Journal 30 (2011), 1209–1220.
135. Zimmerberg, J., Kozlov, M.M., How proteins produce cellular membrane curvature. Nature Review Molecular Cell Biology 7 (2006), 9–19.
136. Zuidscherwoude, M., Gottfert, F., Dunlock, V.M.E., Fidgor, C.G., van den Bogaart, G., van Spriel, A.B., The tetraspanin web revisited by super-resolution microscopy. Scientific Reports, 5, 2015, 12201.