Compartmentalization of the Cell Membrane

Journal of Molecular Biology

Volumn 428, Issue 24, 2016, Pages 4739-4748

  Honigmann, Alf ^a   Pralle, Arnd ^b  

^a MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

^b UNIVERSITY AT BUFFALO   (United States)

Author keywords

cell membrane ultrastructure; cortical actin; lipid raft; nano cluster; network

Indexed keywords

ANKYRIN; G PROTEIN COUPLED RECEPTOR; ION CHANNEL; MEMBRANE LIPID; MEMBRANE PROTEIN; PHOSPHATIDYLINOSITIDE; PHOSPHATIDYLSERINE; SCAFFOLD PROTEIN; SPECTRIN;

ACTIN FILAMENT; CELL COMPARTMENTALIZATION; CELL MEMBRANE; DIMERIZATION; EXOCYTOSIS; HUMAN; INTRACELLULAR SIGNALING; LIGAND BINDING; MEMBRANE COMPONENT; MEMBRANE STRUCTURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; REVIEW; BIOLOGICAL MODEL; MEMBRANE MICRODOMAIN; METABOLISM; PHYSIOLOGY;

CELL MEMBRANE; MEMBRANE LIPIDS; MEMBRANE MICRODOMAINS; MEMBRANE PROTEINS; MODELS, BIOLOGICAL;

EID: 84998885574     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2016.09.022     Document Type: Review

References (92)

1. [1] Kusumi, A., Suzuki, K.G.N., Kasai, R.S., Ritchie, K., Fujiwara, T.K., Hierarchical mesoscale domain organization of the plasma membrane. Trends Biochem. Sci. 36 (2011), 604–615, 10.1016/j.tibs.2011.08.001.
2. [2] Klotzsch, E., Schütz, G.J., A critical survey of methods to detect plasma membrane rafts. Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci., 368, 2013, 2,0120,033, 10.1098/rstb.2012.0033.
3. [3] Bennett, W.F.D., Tieleman, D.P., Computer simulations of lipid membrane domains. Biochim. Biophys. Acta Biomembr. 1828 (2013), 1765–1776, 10.1016/j.bbamem.2013.03.004.
4. [4] Eggeling, C., Honigmann, A., Closing the gap: the approach of optical and computational microscopy to uncover biomembrane organization. Biochim. Biophys. Acta Biomembr., 2016, 2558–2568, 10.1016/j.bbamem.2016.03.025.
5. [5] Schmick, M., Bastiaens, P.I.H., The interdependence of membrane shape and cellular signal processing. Cell 156 (2014), 1132–1138, 10.1016/j.cell.2014.02.007.
6. [6] Jackson, L.P., Kelly, B.T., McCoy, A.J., Gaffry, T., James, L.C., Collins, B.M., Höning, S., Evans, P.R., Owen, D.J., A large-scale conformational change couples membrane recruitment to cargo binding in the AP2 clathrin adaptor complex. Cell 141 (2010), 1220–1229, 10.1016/j.cell.2010.05.006.
7. [7] Pólya, G., Über eine Aufgabe der Wahrscheinlichkeitsrechnung betreffend die Irrfahrt im Straßennetz. Math. Ann. 84 (1921), 149–160.
8. [8] Almeida, P.F.F., Pokorny, A., Hinderliter, A., Thermodynamics of membrane domains. Biochim. Biophys. Acta Biomembr. 1720 (2005), 1–13, 10.1016/j.bbamem.2005.12.004.
9. [9] Baumgart, T., Capraro, B.R., Zhu, C., Das, S.L., Thermodynamics and mechanics of membrane curvature generation and sensing by proteins and lipids. Annu. Rev. Phys. Chem. 62 (2011), 483–506, 10.1146/annurev.physchem.012809.103450.
10. [10] Alberts, B., Johnson, A., Lewis, J., Raff, M., Roberts, K., Walter, P., Mol. Biol. Cell, 2008, 10.1002/1521-3773(20010316)40:6<9823::AID-ANIE9823>3.3.CO;2-C.
11. [11] Dupuy, A.D., Engelman, D.M., Protein area occupancy at the center of the red blood cell membrane. Proc. Natl. Acad. Sci. U. S. A. 105 (2008), 2848–2852, 10.1073/pnas.0712379105.
12. [12] Sowers, a.E., Hackenbrock, C.R., Rate of lateral diffusion of intramembrane particles: measurement by electrophoretic displacement and rerandomization. Proc. Natl. Acad. Sci. U. S. A. 78 (1981), 6246–6250.
13. [13] Kaiser, H.-J., Lingwood, D., Levental, I., Sampaio, J.L., Kalvodova, L., Rajendran, L., Simons, K., Order of lipid phases in model and plasma membranes. Proc. Natl. Acad. Sci. U. S. A. 106 (2009), 16,645–16,650, 10.1073/pnas.0908987106.
14. [14] Owen, D.M., Williamson, D.J., Magenau, A., Gaus, K., Sub-resolution lipid domains exist in the plasma membrane and regulate protein diffusion and distribution. Nat. Commun., 3, 2012, 1256, 10.1038/ncomms2273.
15. [15] Sako, Y., Kusumi, A., Barriers for lateral diffusion of transferrin receptor in the plasma membrane as characterized by receptor dragging by laser tweezers: fence versus tether. J. Cell Biol. 129 (1995), 1559–1574.
16. [16] Varma, R., Mayor, S., GPI-anchored proteins are organized in submicron domains at the cell surface. Nature 394 (1998), 798–801 [ http://www.nature.com.gate.lib.buffalo.edu/nature/journal/v394/n6695/full/394798a0.html (accessed May 17, 2016)].
17. [17] Lenne, P.-F., Wawrezinieck, L., Conchonaud, F., Wurtz, O., Boned, A., Guo, X.-J., Rigneault, H., He, H.-T., Marguet, D., Dynamic molecular confinement in the plasma membrane by microdomains and the cytoskeleton meshwork. EMBO J. 25 (2006), 3245–3256, 10.1038/sj.emboj.7601214.
18. [18] Eggeling, C., Ringemann, C., Medda, R., Schwarzmann, G., Sandhoff, K., Polyakova, S., Belov, V.N., Hein, B., von Middendorff, C., Schönle, A., Hell, S.W., Direct observation of the nanoscale dynamics of membrane lipids in a living cell. Nature 457 (2009), 1159–1162, 10.1038/nature07596.
19. [19] Honigmann, A., Mueller, V., Ta, H., Schoenle, A., Sezgin, E., Hell, S.W., Eggeling, C., Scanning STED-FCS reveals spatiotemporal heterogeneity of lipid interaction in the plasma membrane of living cells. Nat. Commun., 5, 2014, 5412, 10.1038/ncomms6412.
20. [20] Huang, H., Simsek, M.F., Jin, W., Pralle, A., Effect of receptor dimerization on membrane lipid raft structure continuously quantified on single cells by camera based fluorescence correlation spectroscopy. PLoS One, 10, 2015, e0121777, 10.1371/journal.pone.0121777.
21. [21] 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. Nat. Commun., 5, 2014, 4509, 10.1038/ncomms5509.
22. [22] Kusumi, A., Nakada, C., Ritchie, K., Murase, K., Suzuki, K., Murakoshi, H., Kasai, R.S., Kondo, J., Fujiwara, T., 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. Annu. Rev. Biophys. Biomol. Struct. 34 (2005), 351–378, 10.1146/annurev.biophys.34.040204.144637.
23. [23] Pralle, A., Keller, P., Florin, E.-L., Simons, K., Hörber, J.K.H., Sphingolipid-cholesterol rafts diffuse as small entities in the plasma membrane of mammalian cells. J. Cell Biol. 148 (2000), 997–1007, 10.1083/jcb.148.5.997.
24. [24] Kukura, P., Ewers, H., Muller, C., Renn, A., Helenius, A., Sandoghdar, V., High-speed nanoscopic tracking of the position and orientation of a single virus. Nat. Methods 6 (2009), 923–927, 10.1038/nmeth.1395.
25. [25] Ortega Arroyo, J., Cole, D., Kukura, P., Interferometric scattering microscopy and its combination with single-molecule fluorescence imaging. Nat. Protoc. 11 (2016), 617–633, 10.1038/nprot.2016.022.
26. [26] Krieger, J.W., Singh, A.P., Bag, N., Garbe, C.S., Saunders, T.E., Langowski, J., Wohland, T., Imaging fluorescence (cross-) correlation spectroscopy in live cells and organisms. Nat. Protoc. 10 (2015), 1948–1974, 10.1038/nprot.2015.100.
27. [27] Di Rienzo, C., Gratton, E., Beltram, F., Cardarelli, F., Fast spatiotemporal correlation spectroscopy to determine protein lateral diffusion laws in live cell membranes. Proc. Natl. Acad. Sci. U. S. A. 110 (2013), 12,307–12,312, 10.1073/pnas.1222097110.
28. [28] Simons, K., Gerl, M.J., Revitalizing membrane rafts: new tools and insights. Nat. Rev. Mol. Cell Biol. 11 (2010), 688–699, 10.1038/nrm2977.
29. [29] Rao, M., Mayor, S., Use of Forster's resonance energy transfer microscopy to study lipid rafts. Biochim. Biophys. Acta 1746 (2005), 221–233 [ http://www.sciencedirect.com/science/article/pii/S0167488905001667 (accessed May 17, 2016)].
30. [30] Goswami, D., Gowrishankar, K., Bilgrami, S., Ghosh, S., Raghupathy, R., Chadda, R., Vishwakarma, R., Rao, M., Mayor, S., Nanoclusters of GPI-anchored proteins are formed by cortical actin-driven activity. Cell 135 (2008), 1085–1097 [ http://www.sciencedirect.com/science/article/pii/S0092867408015079(accessed May 17, 2016)].
31. [31] Veatch, S.L., Keller, S.L., Seeing spots: complex phase behavior in simple membranes. Biochim. Biophys. Acta, Mol. Cell Res. 1746 (2005), 172–185, 10.1016/j.bbamcr.2005.06.010.
32. [32] Hancock, J.F., Lipid rafts: contentious only from simplistic standpoints. Nat. Rev. Mol. Cell Biol. 7 (2006), 456–462, 10.1038/nrm1925.
33. [33] Lingwood, D., Ries, J., Schwille, P., Simons, K., Plasma membranes are poised for activation of raft phase coalescence at physiological temperature. Proc. Natl. Acad. Sci. U. S. A. 105 (2008), 10,005–10,010, 10.1073/pnas.0804374105.
34. [34] Veatch, S.L., Cicuta, P., Sengupta, P., Honerkamp-Smith, A., Holowka, D., Baird, B., Critical fluctuations in plasma membrane vesicles. ACS Chem. Biol. 3 (2008), 287–293, 10.1021/cb800012x.
35. [35] Levental, K.R., Levental, I., Giant plasma membrane vesicles: models for understanding membrane organization. Curr. Top. Membr. 75 (2015), 25–57, 10.1016/bs.ctm.2015.03.009.
36. [36] Machta, B.B., Papanikolaou, S., Sethna, J.P., Veatch, S.L., Minimal model of plasma membrane heterogeneity requires coupling cortical actin to criticality. Biophys. J. 100 (2011), 1668–1677, 10.1016/j.bpj.2011.02.029.
37. [37] Holthuis, J.C.M., Menon, A.K., Lipid landscapes and pipelines in membrane homeostasis. Nature 510 (2014), 48–57, 10.1038/nature13474.
38. [38] Sebastian, T.T., Baldridge, R.D., Xu, P., Graham, T.R., Phospholipid flippases: building asymmetric membranes and transport vesicles. Biochim. Biophys. Acta Mol. Cell Biol. Lipids 1821 (2012), 1068–1077, 10.1016/j.bbalip.2011.12.007.
39. [39] van den Bogaart, G., Meyenberg, K., Risselada, H.J., Amin, H., Willig, K.I., Hubrich, B.E., Dier, M., Hell, S.W., Grubmüller, H., Diederichsen, U., Jahn, R., Membrane protein sequestering by ionic protein–lipid interactions. Nature 479 (2011), 552–555, 10.1038/nature10545.
40. [40] Honigmann, A., van den Bogaart, G., Iraheta, E., Risselada, H.J., Milovanovic, D., Mueller, V., Müllar, S., Diederichsen, U., Fasshauer, D., Grubmüller, H., Hell, S.W., Eggeling, C., Kühnel, K., Jahn, R., Phosphatidylinositol 4,5-bisphosphate clusters act as molecular beacons for vesicle recruitment. Nat. Struct. Mol. Biol. 20 (2013), 679–686, 10.1038/nsmb.2570.
41. [41] Ellenbroek, W.G., Wang, Y.H., Christian, D.A., Discher, D.E., Janmey, P.A., Liu, A.J., Divalent cation-dependent formation of electrostatic PIP2 clusters in lipid monolayers. Biophys. J. 101 (2011), 2178–2184, 10.1016/j.bpj.2011.09.039.
42. [42] Xiong, D., Xiao, S., Guo, S., Lin, Q., Nakatsu, F., Wu, M., Oscillations by phosphoinositide waves. Nat. Chem. Biol. 12 (2016), 1–10, 10.1038/nchembio.2000.
43. [43] van Rheenen, J., Achame, E.M., Janssen, H., Calafat, J., Jalink, K., PIP2 signaling in lipid domains: a critical re-evaluation. EMBO J. 24 (2005), 1664–1673, 10.1038/sj.emboj.7600655.
44. [44] Abd Halim, K.B., Koldsø, H., Sansom, M.S.P., Interactions of the EGFR juxtamembrane domain with PIP2-containing lipid bilayers: insights from multiscale molecular dynamics simulations. Biochim. Biophys. Acta 1850 (2015), 1017–1025, 10.1016/j.bbagen.2014.09.006.
45. [45] A. Kapus, P. Janmey, Plasma membrane—cortical cytoskeleton interactions: a cell biology approach with biophysical considerations, In: Compr. Physiol., John Wiley & Sons, Inc., 3 (3), 2013, 1231–1281. http://dx.doi.org/10.1002/cphy.c120015.
46. [46] Fowler, V.M., The human erythrocyte plasma membrane: a Rosetta stone for decoding membrane–cytoskeleton structure. Curr. Top. Membr. 72 (2013), 39–88, 10.1016/B978-0-12-417027-8.00002-7.
47. [47] Xu, K., Zhong, G., Zhuang, X., Actin, spectrin, and associated proteins form a periodic cytoskeletal structure in axons. Science 339 (2013), 452–456, 10.1126/science.1232251.
48. [48] D'Este, E., Kamin, D., Velte, C., Göttfert, F., Simons, M., Hell, S.W., Subcortical cytoskeleton periodicity throughout the nervous system. Sci. Rep., 6, 2016, 22,741, 10.1038/srep22741.
49. [49] Dotti, C.G., Poo, M., Neuronal polarization: building fences for molecular segregation. Nat. Cell Biol. 5 (2003), 591–594.
50. [50] Wang, Y.-H., Bucki, R., Janmey, P.A., Cholesterol-dependent phase-demixing in lipid bilayers as a switch for the activity of the phosphoinositide-binding cytoskeletal protein gelsolin. Biochemistry 55 (2016), 3361–3369, 10.1021/acs.biochem.5b01363.
51. [51] Mkrtschjan, M., Li, J., Russell, B., Substrate stiffness and microtopography in PIP2 regulation of the actin cytoskeleton in primary cardiac fibroblasts. FASEB J., 29, 2015.
52. [52] Sako, Y., Kusumi, A., Barriers for lateral diffusion of transferrin receptor in the plasma membrane as characterized by receptor dragging by laser tweezers: fence versus tether. J. Cell Biol. 129 (1995), 1559–1574 [ http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2291191&tool=pmcentrez&rendertype=abstract (accessed February 7, 2015]).
53. [53] Suzuki, K., Ritchie, K., Kajikawa, E., Fujiwara, T., Kusumi, A., Rapid hop diffusion of a G-protein-coupled receptor in the plasma membrane as revealed by single-molecule techniques. Biophys. J. 88 (2005), 3659–3680, 10.1529/biophysj.104.048538.
54. [54] Ehrig, J., Petrov, E.P., Schwille, P., Near-critical fluctuations and cytoskeleton-assisted phase separation lead to subdiffusion in cell membranes. Biophys. J. 100 (2011), 80–89, 10.1016/j.bpj.2010.11.002.
55. [55] Speck, T., Vink, R.L.C., Random pinning limits the size of membrane adhesion domains. Phys. Rev. E Stat. Nonlinear Soft Matter Phys., 86, 2012, 31,923, 10.1103/PhysRevE.86.031923.
56. [56] Zhao, J., Wu, J., Veatch, S.L., Adhesion stabilizes robust lipid heterogeneity in supercritical membranes at physiological temperature. Biophys. J. 104 (2013), 825–834, 10.1016/j.bpj.2012.12.047.
57. [57] Honigmann, A., Sadeghi, S., Keller, J., Hell, S.W., Eggeling, C., Vink, R., A lipid bound actin meshwork organizes liquid phase separation in model membranes. 2014 eLife 2014;3:e01671.
58. [58] Arumugam, S., Petrov, E.P., Schwille, P., Cytoskeletal pinning controls phase separation in multicomponent lipid membranes. Biophys. J. 108 (2015), 1104–1113, 10.1016/j.bpj.2014.12.050.
59. [59] Andrade, D.M., Clausen, M.P., Keller, J., Mueller, V., Wu, C., Bear, J.E., Hell, S.W., Lagerholm, B.C., Eggeling, C., Cortical actin networks induce spatio-temporal confinement of phospholipids in the plasma membrane—a minimally invasive investigation by STED-FCS. Sci. Rep., 5, 2015, 11,454, 10.1038/srep11454.
60. [60] Mueller, V., Ringemann, C., Honigmann, A., Schwarzmann, G., Medda, R., Leutenegger, M., Polyakova, S., Belov, V.N., Hell, S.W., Eggeling, C., STED nanoscopy reveals molecular details of cholesterol- and cytoskeleton-modulated lipid interactions in living cells. Biophys. J. 101 (2011), 1651–1660.
61. [61] Raghupathy, R., Anilkumar, A.A., Polley, A., Singh, P.P., Yadav, M., Johnson, C., Suryawanshi, S., Saikam, V., Sawant, S.D., Panda, A., Guo, Z., Vishwakarma, R.A., Rao, M., Mayor, S., Transbilayer lipid interactions mediate nanoclustering of lipid-anchored proteins. Cell 161 (2015), 581–594, 10.1016/j.cell.2015.03.048.
62. [62] Bodenmiller, B., Wanka, S., Kraft, C., Urban, J., Campbell, D., Pedrioli, P.G., Gerrits, B., Picotti, P., Lam, H., Vitek, O., Brusniak, M.-Y., Roschitzki, B., Zhang, C., Shokat, K.M., Schlapbach, R., Colman-Lerner, A., Nolan, G.P., Nesvizhskii, A.I., Peter, M., Loewith, R., von Mering, C., Aebersold, R., Phosphoproteomic analysis reveals interconnected system-wide responses to perturbations of kinases and phosphatases in yeast. Sci. Signal., 3, 2010, rs4, 10.1126/scisignal.2001182.
63. [63] Breitkreutz, A., Choi, H., Sharom, J.R., Boucher, L., Neduva, V., Larsen, B., Lin, Z.-Y.Y., Breitkreutz, B.-J.J., Stark, C., Liu, G., Ahn, J., Dewar-Darch, D., Reguly, T., Tang, X., Almeida, R., Qin, Z.S., Pawson, T., Gingras, A.-C.C., Nesvizhskii, A.I., Tyers, M., A global protein kinase and phosphatase interaction network in yeast. Science 328 (2010), 1043–1046, 10.1126/science.1176495.
64. [64] Dustin, M.L., Groves, J.T., Receptor signaling clusters in the immune synapse. Annu. Rev. Biophys. 41 (2012), 543–556, 10.1146/annurev-biophys-042910-155238.
65. [65] Lemmon, M.A., Schlessinger, J., Cell signaling by receptor tyrosine kinases. Cell 141 (2010), 1117–1134, 10.1016/j.cell.2010.06.011.
66. [66] Coskun, Ü., Grzybek, M., Drechsel, D., Simons, K., Regulation of human EGF receptor by lipids. Proc. Natl. Acad. Sci. U. S. A. 108 (2011), 9044–9048, 10.1073/pnas.1105666108.
67. [67] Gowrishankar, K., Ghosh, S., Saha, S., R. C, Mayor, S., Rao, M., Active remodeling of cortical actin regulates spatiotemporal organization of cell surface molecules. Cell 149 (2012), 1353–1367, 10.1016/j.cell.2012.05.008.
68. [68] Kholodenko, B.N., Hancock, J.F., Kolch, W., Signalling ballet in space and time. Nat. Rev. Mol. Cell Biol. 11 (2010), 414–426, 10.1038/nrm2901.
69. [69] Tian, T., Harding, A., Inder, K., Plowman, S., Parton, R.G., Hancock, J.F., Plasma membrane nanoswitches generate high-fidelity Ras signal transduction. Nat. Cell Biol. 9 (2007), 905–914, 10.1038/ncb1615.
70. [70] Goswami, D., Gowrishankar, K., Bilgrami, S., Ghosh, S., Raghupathy, R., Chadda, R., Vishwakarma, R., Rao, M., Mayor, S., Nanoclusters of GPI-anchored proteins are formed by cortical actin-driven activity. Cell 135 (2008), 1085–1097, 10.1016/j.cell.2008.11.032.
71. [71] Hancock, J.F., Parton, R.G., Ras plasma membrane signalling platforms. Biochem. J. 389 (2005), 1–11, 10.1042/BJ20050231.
72. [72] Janosi, L., Li, Z., Hancock, J.F., Gorfe, A.a., Organization, dynamics, and segregation of Ras nanoclusters in membrane domains. Proc. Natl. Acad. Sci. U. S. A. 109 (2012), 8097–8102, 10.1073/pnas.1200773109.
73. [73] Iversen, L., Tu, H., Lin, W., Christensen, S.M., Abel, S.M., Iwig, J., Wu, H.-J., Gureasko, J., Rhodes, C., Petit, R.S., Hansen, S.D., Thill, P., Yu, C.-H., Stamou, D., Chakraborty, A.K., Kuriyan, J., Groves, J.T., Ras activation by SOS: allosteric regulation by altered fluctuation dynamics. Science 345 (2014), 50–54, 10.1126/science.1250373 (80-. ).
74. [74] Baumgart, T., Hess, S.T., Webb, W.W., Imaging coexisting fluid domains in biomembrane models coupling curvature and line tension. Nature 425 (2003), 821–824, 10.1038/nature02013.
75. [75] Simons, K., Sampaio, J.L., Membrane organization and lipid rafts. Cold Spring Harb. Perspect. Biol. 3 (2011), 1–17, 10.1101/cshperspect.a004697.
76. [76] Simons, K., Ikonen, E., Functional rafts in cell membranes. Nature 387 (1997), 569–572, 10.1038/42408.
77. [77] Iversen, L., Tu, H.-L., Lin, W.-C., Christensen, S.M., Abel, S.M., Iwig, J., Wu, H.-J., Gureasko, J., Rhodes, C., Petit, R.S., Hansen, S.D., Thill, P., Yu, C.-H., Stamou, D., Chakraborty, A.K., Kuriyan, J., Groves, J.T., Ras activation by SOS: allosteric regulation by altered fluctuation dynamics. Science 345 (2014), 50–54 [ http://science.sciencemag.org/content/345/6192/50.abstract (80-.)].
78. [78] Saha, S., Lee, I.-H., Polley, A., Groves, J.T., Rao, M., Mayor, S., Diffusion of GPI-anchored proteins is influenced by the activity of dynamic cortical actin. Mol. Biol. Cell 26 (2015), 4033–4045, 10.1091/mbc.E15-06-0397.
79. [79] Köster, D.V., Husain, K., Iljazi, E., Bhat, A., Bieling, P., Mullins, R.D., Rao, M., Mayor, S., Actomyosin dynamics drive local membrane component organization in an in vitro active composite layer. Proc. Natl. Acad. Sci. U. S. A. 113 (2016), E1645–E1654, 10.1073/pnas.1514030113.
80. [80] Su, X., Ditlev, J.A., Hui, E., Xing, W., Banjade, S., Okrut, J., King, D.S., Taunton, J., Rosen, M.K., Vale, R.D., Phase separation of signaling molecules promotes T cell receptor signal transduction. Science, 2016, 595–599, aad9964, 10.1126/science.aad9964.
81. [81] Banjade, S., Rosen, M.K., Phase transitions of multivalent proteins can promote clustering of membrane receptors. Elife, 3, 2014, e04123, 10.7554/eLife 2014;3:e04123.
82. [82] Li, P., Banjade, S., Cheng, H.-C., Kim, S., Chen, B., Guo, L., Llaguno, M., Hollingsworth, J.V., King, D.S., Banani, S.F., Russo, P.S., Jiang, Q.-X., Nixon, B.T., Rosen, M.K., Phase transitions in the assembly of multivalent signalling proteins. Nature 483 (2012), 336–340, 10.1038/nature10879.
83. [83] Xie, J., Tato, C.M., Davis, M.M., How the immune system talks to itself: the varied role of synapses. Immunol. Rev. 251 (2013), 65–79, 10.1111/imr.12017.
84. [84] Lemmon, M.A., Membrane recognition by phospholipid-binding domains. Nat. Rev. Mol. Cell Biol. 9 (2008), 99–111, 10.1038/nrm2328.
85. [85] Wawrzyniak, A.M., Kashyap, R., Zimmermann, P., Phosphoinositides and PDZ domain scaffolds. Adv. Exp. Med. Biol. 991 (2013), 41–57, 10.1007/978-94-007-6331-9_4.
86. [86] Milovanovic, D., Platen, M., Junius, M., Diederichsen, U., Schaap, I.A.T., Honigmann, A., Jahn, R., van den Bogaart, G., Calcium promotes the formation of syntaxin 1 mesoscale domains through phosphatidylinositol 4,5-bisphosphate. J. Biol. Chem., 2016, 10.1074/jbc.M116.716225.
87. [87] Sorkin, A., von Zastrow, M., Endocytosis and signalling: intertwining molecular networks. Nat. Rev. Mol. Cell Biol. 10 (2009), 609–622, 10.1038/nrm2748.
88. [88] Silvius, J.R., Role of cholesterol in lipid raft formation: lessons from lipid model systems. Biochim. Biophys. Acta Biomembr. 1610 (2003), 174–183 [ http://www.sciencedirect.com/science/article/pii/S0005273603000166 (accessed May 17, 2016)].
89. [89] Maxfield, F.R., Tabas, I., Role of cholesterol and lipid organization in disease. Nature 438 (2005), 612–621, 10.1038/nature04399 (accessed March 20, 2016).
90. [90] Simons, K., Toomre, D., Lipid rafts and signal transduction. Nat. Rev. Mol. Cell Biol. 1 (2000), 31–39, 10.1038/35036052 (accessed August 19, 2015).
91. [91] Pike, L.J., Lipid rafts: bringing order to chaos. J. Lipid Res. 44 (2003), 655–667 [ http://www.jlr.org/content/44/4/655.full (accessed April 5, 2016)].
92. [92] Hanzal-Bayer, M.F., Hancock, J.F., Lipid rafts and membrane traffic. FEBS Lett. 581 (2007), 2098–2104, 10.1016/j.febslet.2007.03.019.