1932

Abstract

Besides direct protein–protein interactions, indirect interactions mediated by membranes play an important role for the assembly and cooperative function of proteins in membrane shaping and adhesion. The intricate shapes of biological membranes are generated by proteins that locally induce membrane curvature. Indirect curvature-mediated interactions between these proteins arise because the proteins jointly affect the bending energy of the membranes. These curvature-mediated interactions are attractive for crescent-shaped proteins and are a driving force in the assembly of the proteins during membrane tubulation. Membrane adhesion results from the binding of receptor and ligand proteins that are anchored in the apposing membranes. The binding of these proteins strongly depends on nanoscale shape fluctuations of the membranes, leading to a fluctuation-mediated binding cooperativity. A length mismatch between receptor–ligand complexes in membrane adhesion zones causes repulsive curvature-mediated interactions that are a driving force for the length-based segregation of proteins during membrane adhesion.

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2018-04-20
2024-04-16
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Literature Cited

  1. Shoemaker BA, Panchenko AR. 1.  2007. Deciphering protein–protein interactions. Part I. Experimental techniques and databases. PLOS Comput. Biol. 3:e42 [Google Scholar]
  2. Marsh JA, Hernández H, Hall Z, Ahnert SE, Perica T. 2.  et al. 2013. Protein complexes are under evolutionary selection to assemble via ordered pathways. Cell 153:461–70 [Google Scholar]
  3. Motlagh HN, Wrabl JO, Li J, Hilser VJ. 3.  2014. The ensemble nature of allostery. Nature 508:331–39 [Google Scholar]
  4. Phillips R, Ursell T, Wiggins P, Sens P. 4.  2009. Emerging roles for lipids in shaping membrane-protein function. Nature 459:379–85 [Google Scholar]
  5. Kozlov MM, Campelo F, Liska N, Chernomordik LV, Marrink SJ, McMahon HT. 5.  2014. Mechanisms shaping cell membranes. Curr. Opin. Cell Biol. 29:53–60 [Google Scholar]
  6. Weikl TR, Asfaw M, Krobath H, Rozycki B, Lipowsky R. 6.  2009. Adhesion of membranes via receptor-ligand complexes: domain formation, binding cooperativity, and active processes. Soft Matter 5:3213–24 [Google Scholar]
  7. Peter BJ, Kent HM, Mills IG, Vallis Y, Butler PJG. 7.  et al. 2004. BAR domains as sensors of membrane curvature: the amphiphysin BAR structure. Science 303:495–99 [Google Scholar]
  8. Frost A, Perera R, Roux A, Spasov K, Destaing O. 8.  et al. 2008. Structural basis of membrane invagination by F-BAR domains. Cell 132:807–17 [Google Scholar]
  9. Daum B, Auerswald A, Gruber T, Hause G, Balbach J. 9.  et al. 2016. Supramolecular organization of the human N-BAR domain in shaping the sarcolemma membrane. J. Struct. Biol. 194:375–82 [Google Scholar]
  10. Schweitzer Y, Kozlov MM. 10.  2015. Membrane-mediated interaction between strongly anisotropic protein scaffolds. PLOS Comput. Biol. 11:e1004054 [Google Scholar]
  11. Shaw AS, Dustin ML. 11.  1997. Making the T cell receptor go the distance: a topological view of T cell activation. Immunity 6:361–69 [Google Scholar]
  12. Qi SY, Groves JT, Chakraborty AK. 12.  2001. Synaptic pattern formation during cellular recognition. PNAS 98:6548–53 [Google Scholar]
  13. Weikl TR, Lipowsky R. 13.  2004. Pattern formation during T-cell adhesion. Biophys. J. 87:3665–78 [Google Scholar]
  14. Pezeshkian W, Gao H, Arumugam S, Becken U, Bassereau P. 14.  et al. 2017. Mechanism of Shiga toxin clustering on membranes. ACS Nano 11:314–24 [Google Scholar]
  15. Netz RR. 15.  1997. Inclusions in fluctuating membranes: exact results. J. Phys. I 7:833–52 [Google Scholar]
  16. Dommersnes PG, Fournier JB. 16.  1999. N-body study of anisotropic membrane inclusions: membrane mediated interactions and ordered aggregation. Eur. Phys. J. B 12:9–12 [Google Scholar]
  17. Yolcu C, Deserno M. 17.  2012. Membrane-mediated interactions between rigid inclusions: an effective field theory. Phys. Rev. E 86:031906 [Google Scholar]
  18. McMahon HT, Boucrot E. 18.  2015. Membrane curvature at a glance. J. Cell Sci. 128:1065–70 [Google Scholar]
  19. Baumgart T, Capraro BR, Zhu C, Das SL, Leone SR. 19.  et al. 2011. Thermodynamics and mechanics of membrane curvature generation and sensing by proteins and lipids. Annu. Rev. Phys. Chem. 62:483–506 [Google Scholar]
  20. Zimmerberg J, Kozlov MM. 20.  2006. How proteins produce cellular membrane curvature. Nat. Rev. Mol. Cell Biol. 7:9–19 [Google Scholar]
  21. Aimon S, Callan-Jones A, Berthaud A, Pinot M, Toombes GES, Bassereau P. 21.  2014. Membrane shape modulates transmembrane protein distribution. Dev. Cell 28:212–18 [Google Scholar]
  22. Mim C, Unger VM. 22.  2012. Membrane curvature and its generation by BAR proteins. Trends Biochem. Sci. 37:526–33 [Google Scholar]
  23. Rao Y, Haucke V. 23.  2011. Membrane shaping by the Bin/amphiphysin/Rvs (BAR) domain protein superfamily. Cell. Mol. Life Sci. 68:3983–93 [Google Scholar]
  24. Campelo F, McMahon HT, Kozlov MM. 24.  2008. The hydrophobic insertion mechanism of membrane curvature generation by proteins. Biophys. J. 95:2325–39 [Google Scholar]
  25. Boucrot E, Pick A, Çamdere G, Liska N, Evergren E. 25.  et al. 2012. Membrane fission is promoted by insertion of amphipathic helices and is restricted by crescent BAR domains. Cell 149:124–36 [Google Scholar]
  26. Helfrich W. 26.  1973. Elastic properties of lipid bilayers: theory and possible experiments. Z. Naturforsch. C 28:693–703 [Google Scholar]
  27. Lipowsky R. 27.  2013. Spontaneous tubulation of membranes and vesicles reveals membrane tension generated by spontaneous curvature. Faraday Discuss 161:305–31 [Google Scholar]
  28. Nagle JF. 28.  2013. Introductory lecture: basic quantities in model biomembranes. Faraday Discuss 161:11–29 [Google Scholar]
  29. Dimova R. 29.  2014. Recent developments in the field of bending rigidity measurements on membranes. Adv. Colloid Interface Sci. 208:225–34 [Google Scholar]
  30. Hu M, Briguglio JJ, Deserno M. 30.  2012. Determining the Gaussian curvature modulus of lipid membranes in simulations. Biophys. J. 102:1403–10 [Google Scholar]
  31. Siegel DP, Kozlov MM. 31.  2004. The Gaussian curvature elastic modulus of N-monomethylated dioleoylphosphatidylethanolamine: relevance to membrane fusion and lipid phase behavior. Biophys. J. 87:366–74 [Google Scholar]
  32. Safran SA. 32.  1994. Statistical Thermodynamics of Surfaces, Interfaces, and Membranes Reading, MA: Addison-Wesley
  33. Morone N, Fujiwara T, Murase K, Kasai RS, Ike H. 33.  et al. 2006. Three-dimensional reconstruction of the membrane skeleton at the plasma membrane interface by electron tomography. J. Cell Biol. 174:851–62 [Google Scholar]
  34. Brown ACN, Dobbie IM, Alakoskela JM, Davis I, Davis DM. 34.  2012. Super-resolution imaging of remodeled synaptic actin reveals different synergies between NK cell receptors and integrins. Blood 120:3729–40 [Google Scholar]
  35. Etoc F, Vicario C, Lisse D, Siaugue JM, Piehler J. 35.  et al. 2015. Magnetogenetic control of protein gradients inside living cells with high spatial and temporal resolution. Nano Lett 15:3487–94 [Google Scholar]
  36. Simson R, Wallraff E, Faix J, Niewohner J, Gerisch G, Sackmann E. 36.  1998. Membrane bending modulus and adhesion energy of wild-type and mutant cells of dictyostelium lacking talin or cortexillins. Biophys. J. 74:514–22 [Google Scholar]
  37. Popescu G, Ikeda T, Goda K, Best-Popescu CA, Laposata M. 37.  et al. 2006. Optical measurement of cell membrane tension. Phys. Rev. Lett. 97:218101 [Google Scholar]
  38. Betz T, Lenz M, Joanny JF, Sykes C. 38.  2009. ATP-dependent mechanics of red blood cells. PNAS 106:15320–25 [Google Scholar]
  39. Goulian M, Bruinsma R, Pincus P. 39.  1993. Long-range forces in heterogeneous fluid membranes. Europhys. Lett. 22:145–50 [Google Scholar]
  40. Weikl TR, Kozlov MM, Helfrich W. 40.  1998. Interaction of conical membrane inclusions: effect of lateral tension. Phys. Rev. E 57:6988–95 [Google Scholar]
  41. Goulian M, Bruinsma R, Pincus P. 41.  1993. Long-range forces in heterogeneous fluid membranes (erratum). Europhys. Lett. 23:155 [Google Scholar]
  42. Park JM, Lubensky TC. 42.  1996. Interactions between membrane inclusions on fluctuating membranes. J. Phys. I 6:1217–35 [Google Scholar]
  43. Fournier JB, Dommersnes PG. 43.  1997. Long-range forces in heterogeneous fluid membranes—comment. Europhys. Lett. 39:681–82 [Google Scholar]
  44. Reynwar BJ, Deserno M. 44.  2011. Membrane-mediated interactions between circular particles in the strongly curved regime. Soft Matter 7:8567–75 [Google Scholar]
  45. Fournier JB, Galatola P. 45.  2015. High-order power series expansion of the elastic interaction between conical membrane inclusions. Eur. Phys. J. E 38:86 [Google Scholar]
  46. Reynwar BJ, Illya G, Harmandaris VA, Müller MM, Kremer K, Deserno M. 46.  2007. Aggregation and vesiculation of membrane proteins by curvature-mediated interactions. Nature 447:461–64 [Google Scholar]
  47. Auth T, Gompper G. 47.  2009. Budding and vesiculation induced by conical membrane inclusions. Phys. Rev. E 80:031901 [Google Scholar]
  48. Kim KS, Neu J, Oster G. 48.  1998. Curvature-mediated interactions between membrane proteins. Biophys. J. 75:2274–91 [Google Scholar]
  49. Hurley JH, Boura E, Carlson LA, Różycki B. 49.  2010. Membrane budding. Cell 143:875–87 [Google Scholar]
  50. Faini M, Beck R, Wieland FT, Briggs JAG. 50.  2013. Vesicle coats: structure, function, and general principles of assembly. Trends Cell Biol 23:279–88 [Google Scholar]
  51. Takei K, Slepnev VI, Haucke V, De Camilli P. 51.  1999. Functional partnership between amphiphysin and dynamin in clathrin-mediated endocytosis. Nat. Cell Biol. 1:33–39 [Google Scholar]
  52. Kim KS, Neu J, Oster G. 52.  2000. Effect of protein shape on multibody interactions between membrane inclusions. Phys. Rev. E 61:4281–85 [Google Scholar]
  53. Mim C, Cui H, Gawronski-Salerno JA, Frost A, Lyman E. 53.  et al. 2012. Structural basis of membrane bending by the N-BAR protein endophilin. Cell 149:137–45 [Google Scholar]
  54. Adam J, Basnet N, Mizuno N. 54.  2015. Structural insights into the cooperative remodeling of membranes by amphiphysin/BIN1. Sci. Rep. 5:15452 [Google Scholar]
  55. Sorre B, Callan-Jones A, Manzi J, Goud B, Prost J. 55.  et al. 2012. Nature of curvature coupling of amphiphysin with membranes depends on its bound density. PNAS 109:173–78 [Google Scholar]
  56. Simunovic M, Evergren E, Golushko I, Prévost C, Renard HF. 56.  et al. 2016. How curvature-generating proteins build scaffolds on membrane nanotubes. PNAS 113:11226–31 [Google Scholar]
  57. Ayton GS, Blood PD, Voth GA. 57.  2007. Membrane remodeling from N-BAR domain interactions: insights from multi-scale simulation. Biophys. J. 92:3595–602 [Google Scholar]
  58. Simunovic M, Srivastava A, Voth GA. 58.  2013. Linear aggregation of proteins on the membrane as a prelude to membrane remodeling. PNAS 110:20396–401 [Google Scholar]
  59. Ramakrishnan N, Kumar PBS, Radhakrishnan R. 59.  2014. Mesoscale computational studies of membrane bilayer remodeling by curvature-inducing proteins. Phys. Rep. 543:1–60 [Google Scholar]
  60. Noguchi H. 60.  2016. Membrane tubule formation by banana-shaped proteins with or without transient network structure. Sci. Rep. 6:20935 [Google Scholar]
  61. Olinger AD, Spangler EJ, Kumar PBS, Laradji M. 61.  2016. Membrane-mediated aggregation of anisotropically curved nanoparticles. Faraday Discuss 186:265–75 [Google Scholar]
  62. Stachowiak JC, Schmid EM, Ryan CJ, Ann HS, Sasaki DY. 62.  et al. 2012. Membrane bending by protein–protein crowding. Nat. Cell Biol. 14:944–49 [Google Scholar]
  63. Chen Z, Atefi E, Baumgart T. 63.  2016. Membrane shape instability induced by protein crowding. Biophys. J. 111:1823–26 [Google Scholar]
  64. Derganc J, Čopič A. 64.  2016. Membrane bending by protein crowding is affected by protein lateral confinement. Biochim. Biophys. Acta 1858:1152–59 [Google Scholar]
  65. Golestanian R, Goulian M, Kardar M. 65.  1996. Fluctuation-induced interactions between rods on a membrane. Phys. Rev. E 54:6725–34 [Google Scholar]
  66. Dommersnes PG, Fournier JB. 66.  1999. Casimir and mean-field interactions between membrane inclusions subject to external torques. Europhys. Lett. 46:256–61 [Google Scholar]
  67. Lin HK, Zandi R, Mohideen U, Pryadko LP. 67.  2011. Fluctuation-induced forces between inclusions in a fluid membrane under tension. Phys. Rev. Lett. 107:228104 [Google Scholar]
  68. Goetz R, Gompper G, Lipowsky R. 68.  1999. Mobility and elasticity of self-assembled membranes. Phys. Rev. Lett. 82:221–24 [Google Scholar]
  69. Weikl TR. 69.  2002. Dynamic phase separation of fluid membranes with rigid inclusions. Phys. Rev. E 66:061915 [Google Scholar]
  70. Sintes T, Baumgartner A. 70.  1997. Protein attraction in membranes induced by lipid fluctuations. Biophys. J. 73:2251–59 [Google Scholar]
  71. Jafarinia H, Khoshnood A, Jalali MA. 71.  2016. Rigidity of transmembrane proteins determines their cluster shape. Phys. Rev. E 93:012403 [Google Scholar]
  72. Lipowsky R. 72.  1988. Lines of renormalization group fixed points for fluid and crystalline membranes. Europhys. Lett. 7:255–61 [Google Scholar]
  73. Xu GK, Hu J, Lipowsky R, Weikl TR. 73.  2015. Binding constants of membrane-anchored receptors and ligands: a general theory corroborated by Monte Carlo simulations. J. Chem. Phys. 143:243136 [Google Scholar]
  74. Netz RR, Pincus P. 74.  1995. Inhomogeneous fluid membranes: segregation, ordering, and effective rigidity. Phys. Rev. E 52:4114–28 [Google Scholar]
  75. Bruinsma R, Goulian M, Pincus P. 75.  1994. Self-assembly of membrane junctions. Biophys. J. 67:746–50 [Google Scholar]
  76. Weikl TR, Lipowsky R. 76.  2001. Adhesion-induced phase behavior of multicomponent membranes. Phys. Rev. E. 64:011903 [Google Scholar]
  77. Speck T, Reister E, Seifert U. 77.  2010. Specific adhesion of membranes: mapping to an effective bond lattice gas. Phys. Rev. E 82:021923 [Google Scholar]
  78. Dembo M, Torney DC, Saxman K, Hammer D. 78.  1988. The reaction-limited kinetics of membrane-to-surface adhesion and detachment. Proc. R. Soc. Lond. B 234:55–83 [Google Scholar]
  79. Gao H, Qian J, Chen B. 79.  2011. Probing mechanical principles of focal contacts in cell-matrix adhesion with a coupled stochastic-elastic modelling framework. J. R. Soc. Interface 8:1217–32 [Google Scholar]
  80. Bihr T, Seifert U, Smith AS. 80.  2012. Nucleation of ligand-receptor domains in membrane adhesion. Phys. Rev. Lett. 109:258101 [Google Scholar]
  81. Helfrich W. 81.  1978. Steric interaction of fluid membranes in multilayer systems. Z. Naturforsch. A 33:305–15 [Google Scholar]
  82. Lipowsky R, Leibler S. 82.  1986. Unbinding transitions of interacting membranes. Phys. Rev. Lett. 56:2541–44 [Google Scholar]
  83. Farago O. 83.  2010. Fluctuation-induced attraction between adhesion sites of supported membranes. Phys. Rev. E 81:050902(R) [Google Scholar]
  84. Weikl TR, Netz RR, Lipowsky R. 84.  2000. Unbinding transitions and phase separation of multicomponent membranes. Phys. Rev. E. 62:R45–48 [Google Scholar]
  85. Weikl TR, Lipowsky R. 85.  2006. Membrane adhesion and domain formation. Advances in Planar Lipid Bilayers and Liposomes 5 AL Liu 63–127 Cambridge, MA: Academic Press [Google Scholar]
  86. Weil N, Farago O. 86.  2010. Entropy-driven aggregation of adhesion sites of supported membranes. Eur. Phys. J. E 33:81–87 [Google Scholar]
  87. Weikl TR. 87.  2001. Fluctuation-induced aggregation of rigid membrane inclusions. Europhys. Lett. 54:547–53 [Google Scholar]
  88. Hu J, Lipowsky R, Weikl TR. 88.  2013. Binding constants of membrane-anchored receptors and ligands depend strongly on the nanoscale roughness of membranes. PNAS 110:15283–88 [Google Scholar]
  89. Hu J, Xu GK, Lipowsky R, Weikl TR. 89.  2015. Binding kinetics of membrane-anchored receptors and ligands: molecular dynamics simulations and theory. J. Chem. Phys. 143:243137 [Google Scholar]
  90. Pierres A, Benoliel AM, Touchard D, Bongrand P. 90.  2008. How cells tiptoe on adhesive surfaces before sticking. Biophys. J. 94:4114–22 [Google Scholar]
  91. Lin CC, Seikowski J, Pérez-Lara A, Jahn R, Höbartner C, Walla PJ. 91.  2014. Control of membrane gaps by synaptotagmin-Ca2+ measured with a novel membrane distance ruler. Nat. Commun. 5:5859 [Google Scholar]
  92. Monzel C, Schmidt D, Kleusch C, Kirchenbuechler D, Seifert U. 92.  et al. 2015. Measuring fast stochastic displacements of bio-membranes with dynamic optical displacement spectroscopy. Nat. Commun. 6:8162 [Google Scholar]
  93. Steinkühler J, Rozycki B, Alvey C, Lipowsky R, Weikl TR. 93.  et al. 2017. Membrane fluctuations and acidosis regulate cooperative interactions of “Marker of Self” CD47 to macrophage receptor SIRPA. Unpublished manuscript
  94. Krobath H, Rozycki B, Lipowsky R, Weikl TR. 94.  2009. Binding cooperativity of membrane adhesion receptors. Soft Matter 5:3354–61 [Google Scholar]
  95. Davis DM, Dustin ML. 95.  2004. What is the importance of the immunological synapse. Trends Immunol 25:323–27 [Google Scholar]
  96. Monks CR, Freiberg BA, Kupfer H, Sciaky N, Kupfer A. 96.  1998. Three-dimensional segregation of supramolecular activation clusters in T cells. Nature 395:82–86 [Google Scholar]
  97. Grakoui A, Bromley SK, Sumen C, Davis MM, Shaw AS. 97.  et al. 1999. The immunological synapse: a molecular machine controlling T cell activation. Science 285:221–27 [Google Scholar]
  98. Davis DM, Chiu I, Fassett M, Cohen GB, Mandelboim O, Strominger JL. 98.  1999. The human natural killer cell immune synapse. PNAS 96:15062–67 [Google Scholar]
  99. Batista FD, Iber D, Neuberger MS. 99.  2001. B cells acquire antigen from target cells after synapse formation. Nature 411:489–94 [Google Scholar]
  100. Taylor MJ, Husain K, Gartner ZJ, Mayor S, Vale RD. 100.  2017. A DNA-based T cell receptor reveals a role for receptor clustering in ligand discrimination. Cell 169:108–119.e20 [Google Scholar]
  101. Asfaw M, Rozycki B, Lipowsky R, Weikl TR. 101.  2006. Membrane adhesion via competing receptor/ligand bonds. Europhys. Lett. 76:703–9 [Google Scholar]
  102. Dustin ML, Cooper JA. 102.  2000. The immunological synapse and the actin cytoskeleton: molecular hardware for T cell signaling. Nat. Immunol. 1:23–29 [Google Scholar]
  103. Mossman KD, Campi G, Groves JT, Dustin ML. 103.  2005. Altered TCR signaling from geometrically repatterned immunological synapses. Science 310:1191–93 [Google Scholar]
  104. Burroughs NJ, Wülfing C. 104.  2002. Differential segregation in a cell–cell contact interface: the dynamics of the immunological synapse. Biophys. J. 83:1784–96 [Google Scholar]
  105. Raychaudhuri S, Chakraborty AK, Kardar M. 105.  2003. Effective membrane model of the immunological synapse. Phys. Rev. Lett. 91:208101 [Google Scholar]
  106. Weikl TR, Groves JT, Lipowsky R. 106.  2002. Pattern formation during adhesion of multicomponent membranes. Europhys. Lett. 59:916–22 [Google Scholar]
  107. Tsourkas PK, Baumgarth N, Simon SI, Raychaudhuri S. 107.  2007. Mechanisms of B-cell synapse formation predicted by Monte Carlo simulation. Biophys. J. 92:4196–208 [Google Scholar]
  108. Chung M, Koo BJ, Boxer SG. 108.  2013. Formation and analysis of topographical domains between lipid membranes tethered by DNA hybrids of different lengths. Faraday Discuss 161:333–45 discuss. 419–59 [Google Scholar]
  109. Schmid EM, Bakalar MH, Choudhuri K, Weichsel J, Ann HS. 109.  et al. 2016. Size-dependent protein segregation at membrane interfaces. Nat. Phys. 12:704–11 [Google Scholar]
  110. Atilgan E, Ovryn B. 110.  2009. Nucleation and growth of integrin adhesions. Biophys. J. 96:3555–72 [Google Scholar]
  111. Paszek MJ, Boettiger D, Weaver VM, Hammer DA. 111.  2009. Integrin clustering is driven by mechanical resistance from the glycocalyx and the substrate. PLOS Comput. Biol. 5:e1000604 [Google Scholar]
  112. Paszek MJ, DuFort CC, Rossier O, Bainer R, Mouw JK. 112.  et al. 2014. The cancer glycocalyx mechanically primes integrin-mediated growth and survival. Nature 511:319–25 [Google Scholar]
  113. Xu GK, Qian J, Hu J. 113.  2016. The glycocalyx promotes cooperative binding and clustering of adhesion receptors. Soft Matter 12:4572–83 [Google Scholar]
  114. Andersen OS, 2nd Koeppe RE. 114.  2007. Bilayer thickness and membrane protein function: an energetic perspective. Annu. Rev. Biophys. Biomol. Struct. 36:107–30 [Google Scholar]
  115. Brown MF. 115.  2012. Curvature forces in membrane lipid-protein interactions. Biochemistry 51:9782–95 [Google Scholar]
  116. Mondal S, Khelashvili G, Weinstein H. 116.  2014. Not just an oil slick: how the energetics of protein-membrane interactions impacts the function and organization of transmembrane proteins. Biophys. J. 106:2305–16 [Google Scholar]
  117. Dan N, Pincus P, Safran SA. 117.  1993. Membrane-induced interactions between inclusions. Langmuir 9:2768–71 [Google Scholar]
  118. Harroun TA, Heller WT, Weiss TM, Yang L, Huang HW. 118.  1999. Experimental evidence for hydrophobic matching and membrane-mediated interactions in lipid bilayers containing gramicidin. Biophys. J. 76:937–45 [Google Scholar]
  119. Schmidt U, Guigas G, Weiss M. 119.  2008. Cluster formation of transmembrane proteins due to hydrophobic mismatching. Phys. Rev. Lett. 101:128104 [Google Scholar]
  120. West B, Brown FLH, Schmid F. 120.  2009. Membrane-protein interactions in a generic coarse-grained model for lipid bilayers. Biophys. J. 96:101–15 [Google Scholar]
  121. Kahraman O, Koch PD, Klug WS, Haselwandter CA. 121.  2016. Bilayer-thickness-mediated interactions between integral membrane proteins. Phys. Rev. E 93:042410 [Google Scholar]
  122. Ursell T, Huang KC, Peterson E, Phillips R. 122.  2007. Cooperative gating and spatial organization of membrane proteins through elastic interactions. PLOS Comput. Biol. 3:e81 [Google Scholar]
  123. Nomura T, Cranfield CG, Deplazes E, Owen DM, Macmillan A. 123.  et al. 2012. Differential effects of lipids and lyso-lipids on the mechanosensitivity of the mechanosensitive channels MscL and MscS. PNAS 109:8770–75 [Google Scholar]
  124. Haselwandter CA, Phillips R. 124.  2013. Directional interactions and cooperativity between mechanosensitive membrane proteins. Europhys. Lett. 101:68002 [Google Scholar]
  125. Periole X, Huber T, Marrink SJ, Sakmar TP. 125.  2007. G protein-coupled receptors self-assemble in dynamics simulations of model bilayers. J. Am. Chem. Soc. 129:10126–32 [Google Scholar]
  126. Mondal S, Johnston JM, Wang H, Khelashvili G, Filizola M, Weinstein H. 126.  2013. Membrane driven spatial organization of GPCRs. Sci. Rep. 3:2909 [Google Scholar]
  127. Parton DL, Klingelhoefer JW, Sansom MSP. 127.  2011. Aggregation of model membrane proteins, modulated by hydrophobic mismatch, membrane curvature, and protein class. Biophys. J. 101:691–99 [Google Scholar]
  128. Yoo J, Cui Q. 128.  2013. Membrane-mediated protein-protein interactions and connection to elastic models: a coarse-grained simulation analysis of gramicidin A association. Biophys. J. 104:128–38 [Google Scholar]
  129. Botelho AV, Huber T, Sakmar TP, Brown MF. 129.  2006. Curvature and hydrophobic forces drive oligomerization and modulate activity of rhodopsin in membranes. Biophys. J. 91:4464–77 [Google Scholar]
  130. Casuso I, Sens P, Rico F, Scheuring S. 130.  2010. Experimental evidence for membrane-mediated protein–protein interaction. Biophys. J. 99:L47–49 [Google Scholar]
  131. Lee AG. 131.  2003. Lipid–protein interactions in biological membranes: a structural perspective. Biochim. Biophys. Acta 1612:1–40 [Google Scholar]
  132. Lee AG. 132.  2011. Biological membranes: the importance of molecular detail. Trends Biochem. Sci. 36:493–500 [Google Scholar]
  133. Contreras FX, Ernst AM, Wieland F, Bruegger B. 133.  2011. Specificity of intramembrane protein–lipid interactions. Cold Spring Harb. Perspect. Biol. 3:a004705 [Google Scholar]
  134. Niemelä PS, Miettinen MS, Monticelli L, Hammaren H, Bjelkmar P. 134.  et al. 2010. Membrane proteins diffuse as dynamic complexes with lipids. J. Am. Chem. Soc. 132:7574–75 [Google Scholar]
  135. Saric A, Cacciuto A. 135.  2012. Fluid membranes can drive linear aggregation of adsorbed spherical nanoparticles. Phys. Rev. Lett. 108:118101 [Google Scholar]
  136. Bahrami AH, Lipowsky R, Weikl TR. 136.  2012. Tubulation and aggregation of spherical nanoparticles adsorbed on vesicles. Phys. Rev. Lett. 109:188102 [Google Scholar]
  137. Saric A, Cacciuto A. 137.  2012. Mechanism of membrane tube formation induced by adhesive nanocomponents. Phys. Rev. Lett. 109:188101 [Google Scholar]
  138. van der Wel C, Vahid A, Saric A, Idema T, Heinrich D, Kraft DJ. 138.  2016. Lipid membrane-mediated attraction between curvature inducing objects. Sci. Rep. 6:32825 [Google Scholar]
  139. Yue T, Zhang X. 139.  2012. Cooperative effect in receptor-mediated endocytosis of multiple nanoparticles. ACS Nano 6:3196–205 [Google Scholar]
  140. Raatz M, Lipowsky R, Weikl TR. 140.  2014. Cooperative wrapping of nanoparticles by membrane tubes. Soft Matter 10:3570–77 [Google Scholar]
  141. Raatz M, Weikl TR. 141.  2017. Membrane tubulation by elongated and patchy nanoparticles. Adv. Mater. Interfaces 4:1600325 [Google Scholar]
  142. Xiong K, Zhao J, Yang D, Cheng Q, Wang J, Ji H. 142.  2017. Cooperative wrapping of nanoparticles of various sizes and shapes by lipid membranes. Soft Matter 13:4644–52 [Google Scholar]
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