1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Biophysics
  4. Volume 49, 2020
  5. Article

Annual Review of Biophysics

Volume 49, 2020

Principles and Applications of Biological Membrane Organization

Abstract

Many critical biological events, including biochemical signaling, membrane traffic, and cell motility, originate at membrane surfaces. Each such event requires that members of a specific group of proteins and lipids rapidly assemble together at a specific site on the membrane surface. Understanding the biophysical mechanisms that stabilize these assemblies is critical to decoding and controlling cellular functions. In this article, we review progress toward a quantitative biophysical understanding of the mechanisms that drive membrane heterogeneity and organization. We begin from a physical perspective, reviewing the fundamental principles and key experimental evidence behind each proposed mechanism. We then shift to a biological perspective, presenting key examples of the role of heterogeneity in biology and asking which physical mechanisms may be responsible. We close with an applied perspective, noting that membrane heterogeneity provides a novel therapeutic target that is being exploited by a growing number of studies at the interface of biology, physics, and engineering.

Keyword(s): biological membrane, lipid biophysics, membrane heterogeneity, membrane organization, phase separation
Loading

Article metrics loading...

/content/journals/10.1146/annurev-biophys-121219-081637
2020-05-06
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/biophys/49/1/annurev-biophys-121219-081637.html?itemId=/content/journals/10.1146/annurev-biophys-121219-081637&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Aimon S, Callan-Jones A, Berthaud A, Pinot M, Toombes GES, Bassereau P 2014. Membrane shape modulates transmembrane protein distribution. Dev. Cell 28:212–18
     [Google Scholar]
  2. 2. 
    Albelda SM, Buck CA. 1990. Integrins and other cell adhesion molecules. FASEB J 4:2868–80
     [Google Scholar]
  3. 3. 
    Albersdörfer A, Feder T, Sackmann E 1997. Adhesion-induced domain formation by interplay of long-range repulsion and short-range attraction force: a model membrane study. Biophys. J. 73:245–57
     [Google Scholar]
  4. 4. 
    Almen MS, Nordstrom KJ, Fredriksson R, Schioth HB 2009. Mapping the human membrane proteome: a majority of the human membrane proteins can be classified according to function and evolutionary origin. BMC Biol 7:50
     [Google Scholar]
  5. 5. 
    Amjad OA, Mognetti BM, Cicuta P, Di Michele L 2017. Membrane adhesion through bridging by multimeric ligands. Langmuir 33:1139–46
     [Google Scholar]
  6. 6. 
    Antonny B. 2011. Mechanisms of membrane curvature sensing. Annu. Rev. Biochem. 80:101–23
     [Google Scholar]
  7. 7. 
    Bacia K, Schwille P, Kurzchalia T 2005. Sterol structure determines the separation of phases and the curvature of the liquid-ordered phase in model membranes. PNAS 102:3272–77
     [Google Scholar]
  8. 8. 
    Banani SF, Lee HO, Hyman AA, Rosen MK 2017. Biomolecular condensates: organizers of cellular biochemistry. Nat. Rev. Mol. Cell Biol. 18:285–98
     [Google Scholar]
  9. 9. 
    Banjade S, Rosen MK. 2014. Phase transitions of multivalent proteins can promote clustering of membrane receptors. eLife 3:e04123
     [Google Scholar]
  10. 10. 
    Bareford LM, Swaan PW. 2007. Endocytic mechanisms for targeted drug delivery. Adv. Drug Deliv. Rev. 59:748–58
     [Google Scholar]
  11. 11. 
    Barriga H, Law R, Seddon J, Ces O, Brooks N 2016. The effect of hydrostatic pressure on model membrane domain composition and lateral compressibility. Phys. Chem. Chem. Phys. 18:149–55
     [Google Scholar]
  12. 12. 
    Baumgart T, Capraro BR, Zhu C, Das SL 2011. Thermodynamics and mechanics of membrane curvature generation and sensing by proteins and lipids. Annu. Rev. Phys. Chem. 62:483–506
     [Google Scholar]
  13. 13. 
    Baumgart T, Hess ST, Webb WW 2003. Imaging coexisting fluid domains in biomembrane models coupling curvature and line tension. Nature 425:821–24
     [Google Scholar]
  14. 14. 
    Bezlyepkina N, Gracià RS, Shchelokovskyy P, Lipowsky R, Dimova R 2013. Phase diagram and tie-line determination for the ternary mixture DOPC/eSM/cholesterol. Biophys. J. 104:1456–64
     [Google Scholar]
  15. 15. 
    Bhatia T, Husen P, Brewer J, Bagatolli LA, Hansen PL et al. 2015. Preparing giant unilamellar vesicles (GUVs) of complex lipid mixtures on demand: mixing small unilamellar vesicles of compositionally heterogeneous mixtures. Biochim. Biophys. Acta Biomembr. 1848:3175–80
     [Google Scholar]
  16. 16. 
    Bigay J, Gounon P, Robineau S, Antonny B 2003. Lipid packing sensed by ArfGAP1 couples COPI coat disassembly to membrane bilayer curvature. Nature 426:563–66
     [Google Scholar]
  17. 17. 
    Blosser MC, Starr JB, Turtle CW, Ashcraft J, Keller SL 2013. Minimal effect of lipid charge on membrane miscibility phase behavior in three ternary systems. Biophys. J. 104:2629–38
     [Google Scholar]
  18. 18. 
    Boke E, Ruer M, Wühr M, Coughlin M, Lemaitre R et al. 2016. Amyloid-like self-assembly of a cellular compartment. Cell 166:637–50
     [Google Scholar]
  19. 19. 
    Bouvier M. 2001. Oligomerization of G-protein-coupled transmitter receptors. Nat. Rev. Neurosci. 2:274–86
     [Google Scholar]
  20. 20. 
    Brangwynne CP, Eckmann CR, Courson DS, Rybarska A, Hoege C et al. 2009. Germline P granules are liquid droplets that localize by controlled dissolution/condensation. Science 324:1729–32
     [Google Scholar]
  21. 21. 
    Brodsky FM, Chen C-Y, Knuehl C, Towler MC, Wakeham DE 2001. Biological basket weaving: formation and function of clathrin-coated vesicles. Annu. Rev. Cell Dev. Biol. 17:517–68
     [Google Scholar]
  22. 22. 
    Bruinsma R, Goulian M, Pincus P 1994. Self-assembly of membrane junctions. Biophys. J. 67:746–50
     [Google Scholar]
  23. 23. 
    Bunge A, Müller P, Stöckl M, Herrmann A, Huster D 2008. Characterization of the ternary mixture of sphingomyelin, POPC, and cholesterol: support for an inhomogeneous lipid distribution at high temperatures. Biophys. J. 94:2680–90
     [Google Scholar]
  24. 24. 
    Bussell SJ, Koch DL, Hammer DA 1995. Effect of hydrodynamic interactions on the diffusion of integral membrane proteins: diffusion in plasma membranes. Biophys. J. 68:1836–49
     [Google Scholar]
  25. 25. 
    Caffrey M, Hogan J. 1992. LIPIDAT: a database of lipid phase transition temperatures and enthalpy changes. DMPC data subset analysis. Chem. Phys. Lipids 61:1–109
     [Google Scholar]
  26. 26. 
    Cahuzac N, Baum W, Kirkin V, Conchonaud F, Wawrezinieck L et al. 2006. Fas ligand is localized to membrane rafts, where it displays increased cell death–inducing activity. Blood 107:2384–91
     [Google Scholar]
  27. 27. 
    Caltagarone J, Ma S, Sorkin A 2015. Dopamine transporter is enriched in filopodia and induces filopodia formation. Mol. Cell. Neurosci. 68:120–30
     [Google Scholar]
  28. 28. 
    Carbone CB, Kern N, Fernandes RA, Hui E, Su X et al. 2017. In vitro reconstitution of T cell receptor-mediated segregation of the CD45 phosphatase. PNAS 114:E9338–45
     [Google Scholar]
  29. 29. 
    Case LB, Ditlev JA, Rosen MK 2019. Regulation of transmembrane signaling by phase separation. Annu. Rev. Biophys. 48:465–94
     [Google Scholar]
  30. 30. 
    Causeret M, Taulet N, Comunale F, Favard C, Gauthier-Rouviere C 2005. N-cadherin association with lipid rafts regulates its dynamic assembly at cell-cell junctions in C2C12 myoblasts. Mol. Biol. Cell 16:2168–80
     [Google Scholar]
  31. 31. 
    Chong PA, Forman-Kay JD. 2016. Liquid–liquid phase separation in cellular signaling systems. Curr. Opin. Struct. Biol. 41:180–86
     [Google Scholar]
  32. 32. 
    Chun M, Liyanage UK, Lisanti MP, Lodish HF 1994. Signal transduction of a G protein-coupled receptor in caveolae: colocalization of endothelin and its receptor with caveolin. PNAS 91:11728–32
     [Google Scholar]
  33. 33. 
    Conner SD, Schmid SL. 2003. Regulated portals of entry into the cell. Nature 422:37–44
     [Google Scholar]
  34. 34. 
    Cullis PR, Hope MJ, Tilcock CPS 1986. Lipid polymorphism and the roles of lipids in membranes. Chem. Phys. Lipids 40:127–44
     [Google Scholar]
  35. 35. 
    Curk T, Dobnikar J, Frenkel D 2017. Optimal multivalent targeting of membranes with many distinct receptors. PNAS 114:7210–15
     [Google Scholar]
  36. 36. 
    Das S, Tian A, Baumgart T 2008. Mechanical stability of micropipet-aspirated giant vesicles with fluid phase coexistence. J. Phys. Chem. B 112:11625–30
     [Google Scholar]
  37. 37. 
    de Almeida RFM, Borst J, Fedorov A, Prieto M, Visser AJWG 2007. Complexity of lipid domains and rafts in giant unilamellar vesicles revealed by combining imaging and microscopic and macroscopic time-resolved fluorescence. Biophys. J. 93:539–53
     [Google Scholar]
  38. 38. 
    Defamie N, Mesnil M. 2012. The modulation of gap-junctional intercellular communication by lipid rafts. Biochim. Biophys. Acta Biomembr. 1818:1866–69
     [Google Scholar]
  39. 39. 
    Ditlev JA, Case LB, Rosen MK 2018. Who's in and who's out—compositional control of biomolecular condensates. J. Mol. Biol. 430:4666–84
     [Google Scholar]
  40. 40. 
    Edidin M, Kuo SC, Sheetz MP 1991. Lateral movements of membrane glycoproteins restricted by dynamic cytoplasmic barriers. Science 254:1379–82
     [Google Scholar]
  41. 41. 
    Edidin M, Zuniga MC, Sheetz MP 1994. Truncation mutants define and locate cytoplasmic barriers to lateral mobility of membrane glycoproteins. PNAS 91:3378–82
     [Google Scholar]
  42. 42. 
    Evans E, Rawicz W. 1990. Entropy-driven tension and bending elasticity in condensed-fluid membranes. Phys. Rev. Lett. 64:2094–97
     [Google Scholar]
  43. 43. 
    Fenz SF, Merkel R, Sengupta K 2009. Diffusion and intermembrane distance: case study of avidin and E-cadherin mediated adhesion. Langmuir 25:1074–85
     [Google Scholar]
  44. 44. 
    Fenz SF, Smith A-S, Merkel R, Sengupta K 2011. Inter-membrane adhesion mediated by mobile linkers: effect of receptor shortage. Soft Matter 7:952–62
     [Google Scholar]
  45. 45. 
    Filion MC, Phillips NC. 1997. Toxicity and immunomodulatory activity of liposomal vectors formulated with cationic lipids toward immune effector cells. Biochim. Biophys. Acta Biomembr. 1329:345–56
     [Google Scholar]
  46. 46. 
    Ford MG, Mills IG, Peter BJ, Vallis Y, Praefcke GJ et al. 2002. Curvature of clathrin-coated pits driven by epsin. Nature 419:361–66
     [Google Scholar]
  47. 47. 
    Fritzsching KJ, Kim J, Holland GP 2013. Probing lipid–cholesterol interactions in DOPC/eSM/Chol and DOPC/DPPC/Chol model lipid rafts with DSC and 13C solid-state NMR. Biochim. Biophys. Acta Biomembr. 1828:1889–98
     [Google Scholar]
  48. 48. 
    Fujiwara T, Ritchie K, Murakoshi H, Jacobson K, Kusumi A 2002. Phospholipids undergo hop diffusion in compartmentalized cell membrane. J. Cell Biol. 157:1071–82
     [Google Scholar]
  49. 49. 
    Garcia-Saez AJ, Chiantia S, Schwille P 2007. Effect of line tension on the lateral organization of lipid membranes. J. Biol. Chem. 282:33537–44
     [Google Scholar]
  50. 50. 
    Goldstein B, Perelson AS. 1984. Equilibrium theory for the clustering of bivalent cell surface receptors by trivalent ligands: application to histamine release from basophils. Biophys. J. 45:1109–23
     [Google Scholar]
  51. 51. 
    Gómez-Moutón C, Lacalle RA, Mira E, Jiménez-Baranda S, Barber DF et al. 2004. Dynamic redistribution of raft domains as an organizing platform for signaling during cell chemotaxis. J. Cell Biol. 164:759–68
     [Google Scholar]
  52. 52. 
    Goodenough DA, Paul DL. 2009. Gap junctions. Cold Spring Harb. Perspect. Biol. 1:a002576
     [Google Scholar]
  53. 53. 
    Gordon VD, Deserno M, Andrew CMJ, Egelhaaf SU, Poon WCK 2008. Adhesion promotes phase separation in mixed-lipid membranes. EPL 84:48003
     [Google Scholar]
  54. 54. 
    Gordon VD, O'Halloran TJ, Shindell O 2015. Membrane adhesion and the formation of heterogeneities: biology, biophysics, and biotechnology. Phys. Chem. Chem. Phys. 17:15522–33
     [Google Scholar]
  55. 55. 
    Groves JT. 2007. Bending mechanics and molecular organization in biological membranes. Annu. Rev. Phys. Chem. 58:697–717
     [Google Scholar]
  56. 56. 
    Gureasko J, Kuchment O, Makino DL, Sondermann H, Bar-Sagi D, Kuriyan J 2010. Role of the histone domain in the autoinhibition and activation of the Ras activator Son of Sevenless. PNAS 107:3430–35
     [Google Scholar]
  57. 57. 
    Hamada T, Kishimoto Y, Nagasaki T, Takagi M 2011. Lateral phase separation in tense membranes. Soft Matter 7:9061–68
     [Google Scholar]
  58. 58. 
    Hand AR, Gobel S. 1972. The structural organization of the septate and gap junctions of Hydra. J. Cell Biol. 52:397–408
     [Google Scholar]
  59. 59. 
    Hansen JS, Thompson JR, Hélix-Nielsen C, Malmstadt N 2013. Lipid directed intrinsic membrane protein segregation. J. Am. Chem. Soc. 135:17294–97
     [Google Scholar]
  60. 60. 
    Harmon TS, Holehouse AS, Rosen MK, Pappu RV 2017. Intrinsically disordered linkers determine the interplay between phase separation and gelation in multivalent proteins. eLife 6:e30294
     [Google Scholar]
  61. 61. 
    Harris TJ, Tepass U. 2010. Adherens junctions: from molecules to morphogenesis. Nat. Rev. Mol. Cell Biol. 11:502–14
     [Google Scholar]
  62. 62. 
    Hatzakis NS, Bhatia VK, Larsen J, Madsen KL, Bolinger PY et al. 2009. How curved membranes recruit amphipathic helices and protein anchoring motifs. Nat. Chem. Biol. 5:835–41
     [Google Scholar]
  63. 63. 
    Hayashi T, Fujimoto M. 2010. Detergent-resistant microdomains determine the localization of σ-1 receptors to the endoplasmic reticulum-mitochondria junction. Mol. Pharmacol. 77:517–28
     [Google Scholar]
  64. 64. 
    Heinrich M, Tian A, Esposito C, Baumgart T 2010. Dynamic sorting of lipids and proteins in membrane tubes with a moving phase boundary. PNAS 107:7208–13
     [Google Scholar]
  65. 65. 
    Henkler F, Behrle E, Dennehy KM, Wicovsky A, Peters N et al. 2005. The extracellular domains of FasL and Fas are sufficient for the formation of supramolecular FasL-Fas clusters of high stability. J. Cell Biol. 168:1087–98
     [Google Scholar]
  66. 66. 
    Honerkamp-Smith AR, Cicuta P, Collins MD, Veatch SL, den Nijs M et al. 2008. Line tensions, correlation lengths, and critical exponents in lipid membranes near critical points. Biophys. J. 95:236–46
     [Google Scholar]
  67. 67. 
    Honerkamp-Smith AR, Veatch SL, Keller SL 2009. An introduction to critical points for biophysicists; observations of compositional heterogeneity in lipid membranes. Biochim. Biophys. Acta Biomembr. 1788:53–63
     [Google Scholar]
  68. 68. 
    Houtman JC, Yamaguchi H, Barda-Saad M, Braiman A, Bowden B et al. 2006. Oligomerization of signaling complexes by the multipoint binding of GRB2 to both LAT and SOS1. Nat. Struct. Mol. Biol. 13:798–805
     [Google Scholar]
  69. 69. 
    Huang WY, Alvarez S, Kondo Y, Lee YK, Chung JK et al. 2019. A molecular assembly phase transition and kinetic proofreading modulate Ras activation by SOS. Science 363:1098–103
     [Google Scholar]
  70. 70. 
    Huang WY, Yan Q, Lin W-C, Chung JK, Hansen SD et al. 2016. Phosphotyrosine-mediated LAT assembly on membranes drives kinetic bifurcation in recruitment dynamics of the Ras activator SOS. PNAS 113:8218–23
     [Google Scholar]
  71. 71. 
    Hurley JH, Boura E, Carlson L-A, Różycki B 2010. Membrane budding. Cell 143:875–87
     [Google Scholar]
  72. 72. 
    Husen P, Arriaga LR, Monroy F, Ipsen JH, Bagatolli LA 2012. Morphometric image analysis of giant vesicles: a new tool for quantitative thermodynamics studies of phase separation in lipid membranes. Biophys. J. 103:2304–10
     [Google Scholar]
  73. 73. 
    Imam ZI, Kenyon LE, Ashby G, Nagib F, Mendicino M et al. 2017. Phase-separated liposomes enhance the efficiency of macromolecular delivery to the cellular cytoplasm. Cell. Mol. Bioeng. 10:387–403
     [Google Scholar]
  74. 74. 
    Ionova IV, Livshits VA, Marsh D 2012. Phase diagram of ternary cholesterol/palmitoylsphingomyelin/palmitoyloleoyl-phosphatidylcholine mixtures: spin-label EPR study of lipid-raft formation. Biophys. J. 102:1856–65
     [Google Scholar]
  75. 75. 
    Jensen MH, Morris EJ, Simonsen AC 2007. Domain shapes, coarsening, and random patterns in ternary membranes. Langmuir 23:8135–41
     [Google Scholar]
  76. 76. 
    Juhasz J, Davis JH, Sharom FJ 2010. Fluorescent probe partitioning in giant unilamellar vesicles of ‘lipid raft’ mixtures. Biochem. J. 430:415–23
     [Google Scholar]
  77. 77. 
    Juhasz J, Sharom FJ, Davis JH 2009. Quantitative characterization of coexisting phases in DOPC/DPPC/cholesterol mixtures: comparing confocal fluorescence microscopy and deuterium nuclear magnetic resonance. Biochim. Biophys. Acta Biomembr. 1788:2541–52
     [Google Scholar]
  78. 78. 
    Kim JV, Latouche JB, Riviere I, Sadelain M 2004. The ABCs of artificial antigen presentation. Nat. Biotechnol. 22:403–10
     [Google Scholar]
  79. 79. 
    Kloboucek A, Behrisch A, Faix J, Sackmann E 1999. Adhesion-induced receptor segregation and adhesion plaque formation: a model membrane study. Biophys. J. 77:2311–28
     [Google Scholar]
  80. 80. 
    Konyakhina TM, Feigenson GW. 2016. Phase diagram of a polyunsaturated lipid mixture: brain sphingomyelin/1-stearoyl-2-docosahexaenoyl-sn-glycero-3-phosphocholine/cholesterol. Biochim. Biophys. Acta Biomembr. 1858:153–61
     [Google Scholar]
  81. 81. 
    Koynova R, Caffrey M. 2002. An index of lipid phase diagrams. Chem. Phys. Lipids 115:107–219
     [Google Scholar]
  82. 82. 
    Kusumi A, Fujiwara TK, Morone N, Yoshida KJ, Chadda R et al. 2012. Membrane mechanisms for signal transduction: the coupling of the meso-scale raft domains to membrane-skeleton-induced compartments and dynamic protein complexes. Semin. Cell Dev. Biol. 23:126–44
     [Google Scholar]
  83. 83. 
    Kusumi A, Nakada C, Ritchie K, Murase K, Suzuki K et al. 2005. 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. 34:351–78
     [Google Scholar]
  84. 84. 
    Kusumi A, Sako Y. 1996. Cell surface organization by the membrane skeleton. Curr. Opin. Cell Biol. 8:566–74
     [Google Scholar]
  85. 85. 
    Kusumi A, Sako Y, Yamamoto M 1993. Confined lateral diffusion of membrane receptors as studied by single particle tracking (nanovid microscopy): effects of calcium-induced differentiation in cultured epithelial cells. Biophys. J. 65:2021–40
     [Google Scholar]
  86. 86. 
    Lee K, Yu Y. 2017. Janus nanoparticles for T cell activation: clustering ligands to enhance stimulation. J. Mater. Chem. B 5:4410–15
     [Google Scholar]
  87. 87. 
    Leung SSW, Thewalt J. 2017. Link between fluorescent probe partitioning and molecular order of liquid ordered-liquid disordered membranes. J. Phys. Chem. B 121:1176–85
     [Google Scholar]
  88. 88. 
    Levental I, Veatch SL. 2016. The continuing mystery of lipid rafts. J. Mol. Biol. 428:4749–64
     [Google Scholar]
  89. 89. 
    Levine AJ, MacKintosh FC. 2002. Dynamics of viscoelastic membranes. Phys. Rev. E 66:061606
     [Google Scholar]
  90. 90. 
    Li M, Khursigara CM, Subramaniam S, Hazelbauer GL 2011. Chemotaxis kinase CheA is activated by three neighbouring chemoreceptor dimers as effectively as by receptor clusters. Mol. Microbiol. 79:677–85
     [Google Scholar]
  91. 91. 
    Liang X, Li L, Qiu F, Yang Y 2010. Domain growth dynamics in multicomponent vesicles composed of BSM/DOPC/cholesterol. Phys. A Stat. Mech. Appl. 389:3965–71
     [Google Scholar]
  92. 92. 
    Liu YW, Neumann S, Ramachandran R, Ferguson SM, Pucadyil TJ, Schmid SL 2011. Differential curvature sensing and generating activities of dynamin isoforms provide opportunities for tissue-specific regulation. PNAS 108:E234–42
     [Google Scholar]
  93. 93. 
    Maeda S, Nakagawa S, Suga M, Yamashita E, Oshima A et al. 2009. Structure of the connexin 26 gap junction channel at 3.5 Å resolution. Nature 458:597–602
     [Google Scholar]
  94. 94. 
    Maléth J, Choi S, Muallem S, Ahuja M 2014. Translocation between PI(4,5) P2-poor and PI(4,5)P2-rich microdomains during store depletion determines STIM1 conformation and Orai1 gating. Nat. Commun. 5:5843
     [Google Scholar]
  95. 95. 
    Mansourian M, Badiee A, Jalali SA, Shariat S, Yazdani M et al. 2014. Effective induction of anti-tumor immunity using p5 HER-2/neu derived peptide encapsulated in fusogenic DOTAP cationic liposomes co-administrated with CpG-ODN. Immunol. Lett. 162:87–93
     [Google Scholar]
  96. 96. 
    Margineanu A, Hotta J-I, Van der Auweraer M, Ameloot M, Stefan A et al. 2007. Visualization of membrane rafts using a perylene monoimide derivative and fluorescence lifetime imaging. Biophys. J. 93:2877–91
     [Google Scholar]
  97. 97. 
    Marquês JT, Viana AS, De Almeida RFM 2011. Ethanol effects on binary and ternary supported lipid bilayers with gel/fluid domains and lipid rafts. Biochim. Biophys. Acta Biomembr. 1808:405–14
     [Google Scholar]
  98. 98. 
    Marsh D. 2009. Cholesterol-induced fluid membrane domains: a compendium of lipid-raft ternary phase diagrams. Biochim. Biophys. Acta Biomembr. 1788:2114–23
     [Google Scholar]
  99. 99. 
    McMahon HT, Gallop JL. 2005. Membrane curvature and mechanisms of dynamic cell membrane remodelling. Nature 438:590–96
     [Google Scholar]
  100. 100. 
    Mierzwa B, Gerlich DW. 2014. Cytokinetic abscission: molecular mechanisms and temporal control. Dev. Cell 31:525–38
     [Google Scholar]
  101. 101. 
    Miller SE, Mathiasen S, Bright NA, Pierre F, Kelly BT et al. 2015. CALM regulates clathrin-coated vesicle size and maturation by directly sensing and driving membrane curvature. Dev. Cell 33:163–75
     [Google Scholar]
  102. 102. 
    Muallem S, Chung WY, Jha A, Ahuja M 2017. Lipids at membrane contact sites: cell signaling and ion transport. EMBO Rep 18:1893–904
     [Google Scholar]
  103. 103. 
    Nusrat A, Parkos CA, Verkade P, Foley CS, Liang TW et al. 2000. Tight junctions are membrane microdomains. J. Cell Sci. 113:Pt. 101771–81
     [Google Scholar]
  104. 104. 
    Parthasarathy R, Groves JT. 2007. Curvature and spatial organization in biological membranes. Soft Matter 3:24–33
     [Google Scholar]
  105. 105. 
    Parthasarathy R, Yu CH, Groves JT 2006. Curvature-modulated phase separation in lipid bilayer membranes. Langmuir 22:5095–99
     [Google Scholar]
  106. 106. 
    Peter BJ, Kent HM, Mills IG, Vallis Y, Butler PJG et al. 2004. BAR domains as sensors of membrane curvature: the amphiphysin BAR structure. Science 303:495–99
     [Google Scholar]
  107. 107. 
    Phillips MJ, Voeltz GK. 2016. Structure and function of ER membrane contact sites with other organelles. Nat. Rev. Mol. Cell Biol. 17:69–82
     [Google Scholar]
  108. 108. 
    Pike LJ. 2003. Lipid rafts bringing order to chaos. J. Lipid Res. 44:655–67
     [Google Scholar]
  109. 109. 
    Popescu G, Park Y, Dasari RR, Badizadegan K, Feld MS 2007. Coherence properties of red blood cell membrane motions. Phys. Rev. E 76:031902
     [Google Scholar]
  110. 110. 
    Portet T, Gordon SE, Keller SL 2012. Increasing membrane tension decreases miscibility temperatures: an experimental demonstration via micropipette aspiration. Biophys. J. 103:L35–37
     [Google Scholar]
  111. 111. 
    Roux A, Cuvelier D, Nassoy P, Prost J, Bassereau P, Goud B 2005. Role of curvature and phase transition in lipid sorting and fission of membrane tubules. EMBO J 24:1537–45
     [Google Scholar]
  112. 112. 
    Rowland AA, Chitwood PJ, Phillips MJ, Voeltz GK 2014. ER contact sites define the position and timing of endosome fission. Cell 159:1027–41
     [Google Scholar]
  113. 113. 
    Rozovsky S, Kaizuka Y, Groves JT 2005. Formation and spatio-temporal evolution of periodic structures in lipid bilayers. J. Am. Chem. Soc. 127:36–37
     [Google Scholar]
  114. 114. 
    Sahay G, Alakhova DY, Kabanov AV 2010. Endocytosis of nanomedicines. J. Control Release 145:182–95
     [Google Scholar]
  115. 115. 
    Sako Y, Kusumi A. 1994. Compartmentalized structure of the plasma membrane for receptor movements as revealed by a nanometer-level motion analysis. J. Cell Biol. 125:1251–64
     [Google Scholar]
  116. 116. 
    Sano R, Annunziata I, Patterson A, Moshiach S, Gomero E et al. 2009. GM1-ganglioside accumulation at the mitochondria-associated ER membranes links ER stress to Ca2+-dependent mitochondrial apoptosis. Mol. Cell 36:500–11
     [Google Scholar]
  117. 117. 
    Schlessinger J. 1988. Signal transduction by allosteric receptor oligomerization. Trends Biochem. Sci. 13:443–47
     [Google Scholar]
  118. 118. 
    Schmidt D, Bihr T, Fenz S, Merkel R, Seifert U et al. 2015. Crowding of receptors induces ring-like adhesions in model membranes. Biochim. Biophys. Acta Mol. Cell Res. 1853:2984–91
     [Google Scholar]
  119. 119. 
    Scorrano L, De Matteis MA, Emr S, Giordano F, Hajnóczky G et al. 2019. Coming together to define membrane contact sites. Nat. Commun. 10:1287
     [Google Scholar]
  120. 120. 
    Sengupta K, Smith A-S. 2018. Adhesion of biological membranes. Physics of Biological Membranes P Bassereau, P Sens 499–535 Berlin: Springer
     [Google Scholar]
  121. 121. 
    Sezgin E, Levental I, Mayor S, Eggeling C 2017. The mystery of membrane organization: composition, regulation and roles of lipid rafts. Nat. Rev. Mol. Cell Biol. 18:361–74
     [Google Scholar]
  122. 122. 
    Simons K, Gerl MJ. 2010. Revitalizing membrane rafts: new tools and insights. Nat. Rev. Mol. Cell Biol. 11:688–99
     [Google Scholar]
  123. 123. 
    Simons K, Ikonen E. 1997. Functional rafts in cell membranes. Nature 387:569–72
     [Google Scholar]
  124. 124. 
    Simons K, Toomre D. 2000. Lipid rafts and signal transduction. Nat. Rev. Mol. Cell Biol. 1:31–39
     [Google Scholar]
  125. 125. 
    Sorre B, Callan-Jones A, Manzi J, Goud B, Prost J et al. 2012. Nature of curvature coupling of amphiphysin with membranes depends on its bound density. PNAS 109:173–78
     [Google Scholar]
  126. 126. 
    Staehelin LA. 1973. Further observations on the fine structure of freeze-cleaved tight junctions. J. Cell Sci. 13:763–86
     [Google Scholar]
  127. 127. 
    Staneva G, Seigneuret M, Conjeaud H, Puff N, Angelova MI 2011. Making a tool of an artifact: the application of photoinduced Lo domains in giant unilamellar vesicles to the study of Lo/Ld phase spinodal decomposition and its modulation by the ganglioside GM1. Langmuir 27:15074–82
     [Google Scholar]
  128. 128. 
    Stanich CA, Honerkamp-Smith AR, Putzel GG, Warth CS, Lamprecht AK et al. 2013. Coarsening dynamics of domains in lipid membranes. Biophys. J. 105:444–54
     [Google Scholar]
  129. 129. 
    Su X, Ditlev JA, Hui E, Xing W, Banjade S et al. 2016. Phase separation of signaling molecules promotes T cell receptor signal transduction. Science 352:595–99
     [Google Scholar]
  130. 130. 
    Subramanian K, Jochem A, Le Vasseur M, Lewis S, Paulson BR et al. 2019. Coenzyme Q biosynthetic proteins assemble in a substrate-dependent manner into domains at ER–mitochondria contacts. J. Cell Biol. 218:1353–69
     [Google Scholar]
  131. 131. 
    Sud M, Fahy E, Cotter D, Brown A, Dennis EA et al. 2007. LMSD: LIPID MAPS structure database. Nucleic Acids Res 35:D527–32
     [Google Scholar]
  132. 132. 
    Tian A, Baumgart T. 2009. Sorting of lipids and proteins in membrane curvature gradients. Biophys. J. 96:2676–88
     [Google Scholar]
  133. 133. 
    Tsai W-C, Feigenson GW. 2019. Lowering line tension with high cholesterol content induces a transition from macroscopic to nanoscopic phase domains in model biomembranes. Biochim. Biophys. Acta Biomembr. 1861:478–85
     [Google Scholar]
  134. 134. 
    Tsukita S, Furuse M, Itoh M 2001. Multifunctional strands in tight junctions. Nat. Rev. Mol. Cell Biol. 2:285–93
     [Google Scholar]
  135. 135. 
    Varela ARP, Couto AS, Fedorov A, Futerman AH, Prieto M, Silva LC 2016. Glucosylceramide reorganizes cholesterol-containing domains in a fluid phospholipid membrane. Biophys. J. 110:612–22
     [Google Scholar]
  136. 136. 
    Veatch SL, Cicuta P, Sengupta P, Honerkamp-Smith A, Holowka D, Baird B 2008. Critical fluctuations in plasma membrane vesicles. ACS Chem. Biol. 3:287–93
     [Google Scholar]
  137. 137. 
    Veatch SL, Gawrisch K, Keller SL 2006. Closed-loop miscibility gap and quantitative tie-lines in ternary membranes containing diphytanoyl PC. Biophys. J. 90:4428–36
     [Google Scholar]
  138. 138. 
    Veatch SL, Keller SL. 2005. Seeing spots: complex phase behavior in simple membranes. Biochim. Biophys. Acta Mol. Cell Res. 1746:172–85
     [Google Scholar]
  139. 139. 
    Veatch SL, Polozov IV, Gawrisch K, Keller SL 2004. Liquid domains in vesicles investigated by NMR and fluorescence microscopy. Biophys. J. 86:2910–22
     [Google Scholar]
  140. 140. 
    Veatch SL, Soubias O, Keller SL, Gawrisch K 2007. Critical fluctuations in domain-forming lipid mixtures. PNAS 104:17650–55
     [Google Scholar]
  141. 141. 
    Vequi-Suplicy CC, Riske KA, Knorr RL, Dimova R 2010. Vesicles with charged domains. Biochim. Biophys. Acta Biomembr. 1798:1338–47
     [Google Scholar]
  142. 142. 
    Wieber A, Selzer T, Kreuter J 2012. Physico-chemical characterisation of cationic DOTAP liposomes as drug delivery system for a hydrophilic decapeptide before and after freeze-drying. Eur. J. Pharm. Biopharm. 80:358–67
     [Google Scholar]
  143. 143. 
    Wilhelm S, Tavares AJ, Dai Q, Ohta S, Audet J et al. 2016. Analysis of nanoparticle delivery to tumours. Nat. Rev. Mater. 1:16014
     [Google Scholar]
  144. 144. 
    Xu K, Zhong G, Zhuang X 2013. Actin, spectrin, and associated proteins form a periodic cytoskeletal structure in axons. Science 339:452–56
     [Google Scholar]
  145. 145. 
    Xu S, Olenyuk BZ, Okamoto CT, Hamm-Alvarez SF 2013. Targeting receptor-mediated endocytotic pathways with nanoparticles: rationale and advances. Adv. Drug Deliv. Rev. 65:121–38
     [Google Scholar]
  146. 146. 
    Yanagisawa M, Shimokawa N, Ichikawa M, Yoshikawa K 2012. Micro-segregation induced by bulky-head lipids: formation of characteristic patterns in a giant vesicle. Soft Matter 8:488–95
     [Google Scholar]
  147. 147. 
    Yokota K, Toyoki A, Yamazaki K, Ogino T 2014. Behavior of raft-like domain in stacked structures of ternary lipid bilayers prepared by self-spreading method. Jpn. J. Appl. Phys. 53:05FA11
     [Google Scholar]
  148. 148. 
    Yoon YZ, Hale JP, Petrov PG, Cicuta P 2010. Mechanical properties of ternary lipid membranes near a liquid–liquid phase separation boundary. J. Phys. Condensed Matter 22:062101
     [Google Scholar]
  149. 149. 
    Yuan J, Kiss A, Pramudya YH, Nguyen LT, Hirst LS 2009. Solution synchrotron x-ray diffraction reveals structural details of lipid domains in ternary mixtures. Phys. Rev. E 79:031924
     [Google Scholar]
  150. 150. 
    Zeno WF, Baul U, Snead WT, DeGroot AC, Wang L et al. 2018. Synergy between intrinsically disordered domains and structured proteins amplifies membrane curvature sensing. Nat. Commun. 9:4152
     [Google Scholar]
  151. 151. 
    Zeno WF, Thatte AS, Wang L, Snead WT, Lafer EM, Stachowiak JC 2019. Molecular mechanisms of membrane curvature sensing by a disordered protein. J. Am. Chem. Soc. 141:10361–71
     [Google Scholar]
  152. 152. 
    Zhang Q, Reinhard BM. 2018. Ligand density and nanoparticle clustering cooperate in the multivalent amplification of epidermal growth factor receptor activation. ACS Nano 12:10473–85
     [Google Scholar]
  153. 153. 
    Zhao J, Wu J, Heberle FA, Mills TT, Klawitter P et al. 2007. Phase studies of model biomembranes: complex behavior of DSPC/DOPC/cholesterol. Biochim. Biophys. Acta Biomembr. 1768:2764–76
     [Google Scholar]
/content/journals/10.1146/annurev-biophys-121219-081637
Loading
Principles and Applications of Biological Membrane Organization
Annual Review of Biophysics 49, 19 (2020); https://doi.org/10.1146/annurev-biophys-121219-081637
/content/journals/10.1146/annurev-biophys-121219-081637
/content/journals/10.1146/annurev-biophys-121219-081637
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error