1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Biophysics
  4. Volume 51, 2022
  5. Article

Annual Review of Biophysics

Volume 51, 2022

Molecular Shape Solution for Mesoscopic Remodeling of Cellular Membranes

Abstract

Cellular membranes self-assemble from and interact with various molecular species. Each molecule locally shapes the lipid bilayer, the soft elastic core of cellular membranes. The dynamic architecture of intracellular membrane systems is based on elastic transformations and lateral redistribution of these elementary shapes, driven by chemical and curvature stress gradients. The minimization of the total elastic stress by such redistribution composes the most basic, primordial mechanism of membrane curvature-composition coupling (CCC). Although CCC is generally considered in the context of dynamic compositional heterogeneity of cellular membrane systems, in this article we discuss a broader involvement of CCC in controlling membrane deformations. We focus specifically on the mesoscale membrane transformations in open, reservoir-governed systems, such as membrane budding, tubulation, and the emergence of highly curved sites of membrane fusion and fission. We reveal that the reshuffling of molecular shapes constitutes an independent deformation mode with complex rheological properties.This mode controls effective elasticity of local deformations as well as stationary elastic stress, thus emerging as a major regulator of intracellular membrane remodeling.

Keyword(s): curvature-composition coupling, membrane curvature, membrane elasticity, molecular shape, thermodynamics
Loading

Article metrics loading...

/content/journals/10.1146/annurev-biophys-011422-100054
2022-05-09
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/biophys/51/1/annurev-biophys-011422-100054.html?itemId=/content/journals/10.1146/annurev-biophys-011422-100054&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Aguado-Velasco C, Bretscher MS. 1999. Circulation of the plasma membrane in Dictyostelium. Mol. Biol. Cell 10:124419–27
     [Google Scholar]
  2. 2.
    Aimon S, Callan-Jones A, Berthaud A, Pinot M, Toombes GES, Bassereau P. 2014. Membrane shape modulates transmembrane protein distribution. Dev. Cell 28:2212–18
     [Google Scholar]
  3. 3.
    Alimohamadi H, Rangamani P. 2018. Modeling membrane curvature generation due to membrane–protein interactions. Biomolecules 8:4120
     [Google Scholar]
  4. 4.
    Almendro-Vedia VG, Natale P, Mell M, Bonneau S, Monroy F et al. 2017. Nonequilibrium fluctuations of lipid membranes by the rotating motor protein F1F0-ATP synthase. PNAS 114:4311291–96
     [Google Scholar]
  5. 5.
    Antonny B. 2011. Mechanisms of membrane curvature sensing. Annu. Rev. Biochem. 80:101–23
     [Google Scholar]
  6. 6.
    Ayee MAA, Levitan I. 2018. Membrane stiffening in osmotic swelling: analysis of membrane tension and elastic modulus. Curr. Top. Membr. 81:97–123
     [Google Scholar]
  7. 7.
    Baoukina S, Ingólfsson HI, Marrink SJ, Tieleman DP. 2018. Curvature-induced sorting of lipids in plasma membrane tethers. Adv. Theory Simul. 1:81800034
     [Google Scholar]
  8. 8.
    Bashkirov PV. 2007. Membrane nanotubes in the electric field as a model for measurement of mechanical parameters of the lipid bilayer. Biochem. Suppl. Ser. A Membr. Cell Biol. 1:2176–84
     [Google Scholar]
  9. 9.
    Bashkirov PV, Chekashkina KV, Akimov SA, Kuzmin PI, Frolov VA. 2011. Variation of lipid membrane composition caused by strong bending. Biochem. Suppl. Ser. A Membr. Cell Biol. 5:2205–11
     [Google Scholar]
  10. 10.
    Bashkirov PV, Kuzmin PI, Chekashkina K, Arrasate P, Vera Lillo J et al. 2020. Reconstitution and real-time quantification of membrane remodeling by single proteins and protein complexes. Nat. Protoc. 15:82443–69
     [Google Scholar]
  11. 11.
    Bassereau P, Jin R, Baumgart T, Deserno M, Dimova R et al. 2018. The 2018 biomembrane curvature and remodeling roadmap. J. Phys. D Appl. Phys. 51:34343001
     [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.
    Bayley H, Cronin B, Heron A, Holden MA, Hwang WL et al. 2008. Droplet interface bilayers. Mol. Biosyst 4:121191–208
     [Google Scholar]
  14. 14.
    Beltrán-Heredia E, Tsai F-C, Salinas-Almaguer S, Cao FJ, Bassereau P, Monroy F. 2019. Membrane curvature induces cardiolipin sorting. Commun. Biol. 2:1225
     [Google Scholar]
  15. 15.
    Ben M'barek K, Ajjaji D, Chorlay A, Vanni S, Forêt L, Thiam AR. 2017. ER membrane phospholipids and surface tension control cellular lipid droplet formation. Dev. Cell 41:6591–604.e7
     [Google Scholar]
  16. 16.
    Bhaskara RM, Grumati P, Garcia-Pardo J, Kalayil S, Covarrubias-Pinto A et al. 2019. Curvature induction and membrane remodeling by FAM134B reticulon homology domain assist selective ER-phagy. Nat. Commun. 10:2370
     [Google Scholar]
  17. 17.
    Black JC, Cheney PP, Campbell T, Knowles MK. 2014. Membrane curvature based lipid sorting using a nanoparticle patterned substrate. Soft Matter 10:122016–23
     [Google Scholar]
  18. 18.
    Bouvrais H, Méléard P, Pott T, Jensen KJ, Brask J, Ipsen JH. 2008. Softening of POPC membranes by magainin. Biophys. Chem. 137:17–12
     [Google Scholar]
  19. 19.
    Božič B, Das SL, Svetina S. 2015. Sorting of integral membrane proteins mediated by curvature-dependent protein-lipid bilayer interaction. Soft Matter 11:122479–87
     [Google Scholar]
  20. 20.
    Brannigan G, Brown FLH. 2005. Composition dependence of bilayer elasticity. J. Chem. Phys. 122:7074905
     [Google Scholar]
  21. 21.
    Breuer A, Lauritsen L, Bertseva E, Vonkova I, Stamou D. 2019. Quantitative investigation of negative membrane curvature sensing and generation by I-BARs in filopodia of living cells. Soft Matter 15:489829–39
     [Google Scholar]
  22. 22.
    Bubnis G, Risselada HJ, Grubmüller H. 2016. Exploiting lipid permutation symmetry to compute membrane remodeling free energies. Phys. Rev. Lett. 117:18188102
     [Google Scholar]
  23. 23.
    Callan-Jones A, Sorre B, Bassereau P 2011. Curvature-driven lipid sorting in biomembranes. Cold Spring Harb. Perspect. Biol. 3:2a004648
     [Google Scholar]
  24. 24.
    Campelo F, Arnarez C, Marrink SJ, Kozlov MM. 2014. Helfrich model of membrane bending: from Gibbs theory of liquid interfaces to membranes as thick anisotropic elastic layers. Adv. Colloid Interface Sci. 208:25–33
     [Google Scholar]
  25. 25.
    Campelo F, McMahon HT, Kozlov MM. 2008. The hydrophobic insertion mechanism of membrane curvature generation by proteins. Biophys. J. 95:52325–39
     [Google Scholar]
  26. 26.
    Canham PB. 1970. The minimum energy of bending as a possible explanation of the biconcave shape of the human red blood cell. J. Theor. Biol. 26:161–81
     [Google Scholar]
  27. 27.
    Cantin R, Méthot S, Tremblay MJ 2005. Plunder and stowaways: incorporation of cellular proteins by enveloped viruses. J. Virol. 79:116577–87
     [Google Scholar]
  28. 28.
    Capraro BR, Yoon Y, Cho W, Baumgart T. 2010. Curvature sensing by the epsin N-terminal homology domain measured on cylindrical lipid membrane tethers. J. Am. Chem. Soc. 132:41200–1
     [Google Scholar]
  29. 29.
    Castellana ET, Cremer PS. 2006. Solid supported lipid bilayers: from biophysical studies to sensor design. Surf. Sci. Rep. 61:10429–44
     [Google Scholar]
  30. 30.
    Chanaday NL, Cousin MA, Milosevic I, Watanabe S, Morgan JR 2019. The synaptic vesicle cycle revisited: new insights into the modes and mechanisms. J. Neurosci. 39:428209–16
     [Google Scholar]
  31. 31.
    Cheney PP, Weisgerber AW, Feuerbach AM, Knowles MK. 2017. Single lipid molecule dynamics on supported lipid bilayers with membrane curvature. Membranes 7:115
     [Google Scholar]
  32. 32.
    Cooke IR, Deserno M. 2006. Coupling between lipid shape and membrane curvature. Biophys. J. 91:2487–95
     [Google Scholar]
  33. 33.
    Deuling HJ, Helfrich W. 1976. Red blood cell shapes as explained on the basis of curvature elasticity. Biophys. J. 16:8861–68
     [Google Scholar]
  34. 34.
    Dimova R. 2014. Recent developments in the field of bending rigidity measurements on membranes. Adv. Colloid Interface Sci. 208:225–34
     [Google Scholar]
  35. 35.
    Drin G, Casella J-F, Gautier R, Boehmer T, Schwartz TU, Antonny B. 2007. A general amphipathic α-helical motif for sensing membrane curvature. Nat. Struct. Mol. Biol. 14:2138–46
     [Google Scholar]
  36. 36.
    Elías-Wolff F, Lindén M, Lyubartsev AP, Brandt EG. 2019. Curvature sensing by cardiolipin in simulated buckled membranes. Soft Matter 15:4792–802
     [Google Scholar]
  37. 37.
    Espadas J, Pendin D, Bocanegra R, Escalada A, Misticoni G et al. 2019. Dynamic constriction and fission of endoplasmic reticulum membranes by reticulon. Nat. Commun. 10:5327
     [Google Scholar]
  38. 38.
    Faini M, Beck R, Wieland FT, Briggs JAG. 2013. Vesicle coats: structure, function, and general principles of assembly. Trends Cell Biol 23:6279–88
     [Google Scholar]
  39. 39.
    Fošnarič M, Bohinc K, Gauger DR, Iglič A, Kralj-Iglič V, May S. 2005. The influence of anisotropic membrane inclusions on curvature elastic properties of lipid membranes. J. Chem. Inf. Model. 45:61652–61
     [Google Scholar]
  40. 40.
    Fournier JB. 1996. Nontopological saddle-splay and curvature instabilities from anisotropic membrane inclusions. Phys. Rev. Lett. 76:234436–39
     [Google Scholar]
  41. 41.
    Frolov VA, Escalada A, Akimov SA, Shnyrova AV. 2015. Geometry of membrane fission. Chem. Phys. Lipids 185:129–40
     [Google Scholar]
  42. 42.
    Frolov VA, Lizunov VA, Dunina-Barkovskaya AY, Samsonov AV, Zimmerberg J. 2003. Shape bistability of a membrane neck: a toggle switch to control vesicle content release. PNAS 100:158698–703
     [Google Scholar]
  43. 43.
    Frolov VA, Shnyrova AV, Zimmerberg J. 2011. Lipid polymorphisms and membrane shape. Cold Spring Harb. Perspect. Biol. 3:11a004747
     [Google Scholar]
  44. 44.
    Fuller N, Rand RP. 2001. The influence of lysolipids on the spontaneous curvature and bending elasticity of phospholipid membranes. Biophys. J. 81:1243–54
     [Google Scholar]
  45. 45.
    Galimzyanov TR, Bashkirov PV, Blank PS, Zimmerberg J, Batishchev OV, Akimov SA. 2020. Monolayerwise application of linear elasticity theory well describes strongly deformed lipid membranes and the effect of solvent. Soft Matter 16:51179–89
     [Google Scholar]
  46. 46.
    Galvez JMM, Garcia-Hernando M, Benito-Lopez F, Basabe-Desmonts L, Shnyrova AV. 2020. Microfluidic chip with pillar arrays for controlled production and observation of lipid membrane nanotubes. Lab Chip 20:152748–55
     [Google Scholar]
  47. 47.
    Garoff H, Hewson R, Opstelten DJ. 1998. Virus maturation by budding. Microbiol. Mol. Biol. Rev. 62:41171–90
     [Google Scholar]
  48. 48.
    Girard P, Prost J, Bassereau P. 2005. Passive or active fluctuations in membranes containing proteins. Phys. Rev. Lett. 94:8088102
     [Google Scholar]
  49. 49.
    Gómez-Llobregat J, Elías-Wolff F, Lindén M. 2016. Anisotropic membrane curvature sensing by amphipathic peptides. Biophys. J. 110:1197–204
     [Google Scholar]
  50. 50.
    Habermann B. 2004. The BAR-domain family of proteins: a case of bending and binding?. EMBO Rep 5:3250–55
     [Google Scholar]
  51. 51.
    Hao M, Maxfield FR. 2000. Characterization of rapid membrane internalization and recycling. J. Biol. Chem. 275:2015279–86
     [Google Scholar]
  52. 52.
    Harmandaris VA, Deserno M. 2006. A novel method for measuring the bending rigidity of model lipid membranes by simulating tethers. J. Chem. Phys. 125:20204905
     [Google Scholar]
  53. 53.
    Has C, Das SL. 2021. Recent developments in membrane curvature sensing and induction by proteins. Biochim. Biophys. Acta Gen. Subj. 1865:10129971
     [Google Scholar]
  54. 54.
    Haucke V, Kozlov MM. 2018. Membrane remodeling in clathrin-mediated endocytosis. J. Cell Sci. 131:17jcs216812
     [Google Scholar]
  55. 55.
    Heinrich M, Tian A, Esposito C, Baumgart T. 2010. Dynamic sorting of lipids and proteins in membrane tubes with a moving phase boundary. PNAS 107:167208–13
     [Google Scholar]
  56. 56.
    Heinrich MC, Capraro BR, Tian A, Isas JM, Langen R, Baumgart T 2010. Quantifying membrane curvature generation of Drosophila amphiphysin N-BAR domains. J. Phys. Chem. Lett. 1:233401–6
     [Google Scholar]
  57. 57.
    Helfrich W. 1973. Elastic properties of lipid bilayers: theory and possible experiments. Z. Naturforsch. C 28:11–12693–703
     [Google Scholar]
  58. 58.
    Henriksen JR, Andresen TL, Feldborg LN, Duelund L, Ipsen JH 2010. Understanding detergent effects on lipid membranes: a model study of lysolipids. Biophys. J. 98:102199–205
     [Google Scholar]
  59. 59.
    Hirschberg K, Miller CM, Ellenberg J, Presley JF, Siggia ED et al. 1998. Kinetic analysis of secretory protein traffic and characterization of Golgi to plasma membrane transport intermediates in living cells. J. Cell Biol. 143:61485–503
     [Google Scholar]
  60. 60.
    Hochmuth RM, Mohandas N, Blackshear PL. 1973. Measurement of the elastic modulus for red cell membrane using a fluid mechanical technique. Biophys. J. 13:8747–62
     [Google Scholar]
  61. 61.
    Honigmann A, Walter C, Erdmann F, Eggeling C, Wagner R. 2010. Characterization of horizontal lipid bilayers as a model system to study lipid phase separation. Biophys. J. 98:122886–94
     [Google Scholar]
  62. 62.
    Hossein A, Deserno M. 2020. Spontaneous curvature, differential stress, and bending modulus of asymmetric lipid membranes. Biophys. J 118:3624–42
     [Google Scholar]
  63. 63.
    Hsieh WT, Hsu CJ, Capraro BR, Wu T, Chen CM et al. 2012. Curvature sorting of peripheral proteins on solid-supported wavy membranes. Langmuir 28:3512838–43
     [Google Scholar]
  64. 64.
    Hu J, Shibata Y, Voss C, Shemesh T, Li Z et al. 2008. Membrane proteins of the endoplasmic reticulum induce high-curvature tubules. Science 319:58671247–50
     [Google Scholar]
  65. 65.
    Israelachvili JN. 2011. Intermolecular and Surface Forces Amsterdam: Elsevier. , 3rd ed..
  66. 66.
    Ivchenkov DV, Kuzmin PI, Galimzyanov TR, Shnyrova AV, Bashkirov PV, Frolov VA. 2021. Nonlinear material and ionic transport through membrane nanotubes. Biochim. Biophys. Acta Biomembr. 1863:10183677
     [Google Scholar]
  67. 67.
    Jarin Z, Tsai F-C, Davtyan A, Pak AJ, Bassereau P, Voth GA. 2019. Unusual organization of I-BAR proteins on tubular and vesicular membranes. Biophys. J. 117:3553–62
     [Google Scholar]
  68. 68.
    Jensen MB, Bhatia VK, Jao CC, Rasmussen JE, Pedersen SL et al. 2011. Membrane curvature sensing by amphipathic helices: a single liposome study using α-synuclein and annexin B12. J. Biol. Chem 286:4942603–14
     [Google Scholar]
  69. 69.
    Kamal MM, Mills D, Grzybek M, Howard J 2009. Measurement of the membrane curvature preference of phospholipids reveals only weak coupling between lipid shape and leaflet curvature. PNAS 106:5222245–50
     [Google Scholar]
  70. 70.
    Kawamoto S, Klein ML, Shinoda W. 2015. Coarse-grained molecular dynamics study of membrane fusion: curvature effects on free energy barriers along the stalk mechanism. J. Chem. Phys. 143:24243112
     [Google Scholar]
  71. 71.
    Kozlov MM 2018. Spontaneous and intrinsic curvature of lipid membranes: back to the origins. Physics of Biological Membranes P Bassereau, P Sens 287–309 Cham, Switz: Springer
     [Google Scholar]
  72. 72.
    Kozlov MM, Campelo F, Liska N, Chernomordik LV, Marrink SJ, McMahon HT. 2014. Mechanisms shaping cell membranes. Curr. Opin. Cell Biol. 29:53–60
     [Google Scholar]
  73. 73.
    Kozlov MM, Helfrich W. 1992. Effects of a cosurfactant on the stretching and bending elasticities of a surfactant monolayer. Langmuir 8:112792–97
     [Google Scholar]
  74. 74.
    Kozlov MM, Leikin SL, Markin VS. 1989. Elastic properties of interfaces. Elasticity moduli and spontaneous geometric characteristics. J. Chem. Soc. Faraday Trans. 2 Mol. Chem. Phys. 85:4277–92
     [Google Scholar]
  75. 75.
    Kozlov MM, McMahon HT, Chernomordik LV. 2010. Protein-driven membrane stresses in fusion and fission. Trends Biochem. Sci. 35:12699–706
     [Google Scholar]
  76. 76.
    Kralj-Iglič V, Svetina S, Žekž B. 1996. Shapes of bilayer vesicles with membrane embedded molecules. Eur. Biophys. J. 24:5311–21
     [Google Scholar]
  77. 77.
    Larsen JB, Rosholm KR, Kennard C, Pedersen SL, Munch HK et al. 2020. How membrane geometry regulates protein sorting independently of mean curvature. ACS Cent. Sci. 6:71159–68
     [Google Scholar]
  78. 78.
    Lavi I, Goudarzi M, Raz E, Gov NS, Voituriez R, Sens P. 2019. Cellular blebs and membrane invaginations are coupled through membrane tension buffering. Biophys. J. 117:81485–95
     [Google Scholar]
  79. 79.
    Leibler S. 1986. Curvature instability in membranes. J. Phys. 47:3507–16
     [Google Scholar]
  80. 80.
    Li N, Sharifi-Mood N, Tu F, Lee D, Radhakrishnan R et al. 2017. Curvature-driven migration of colloids on tense lipid bilayers. Langmuir 33:2600–10
     [Google Scholar]
  81. 81.
    Lipowsky R. 2013. Spontaneous tubulation of membranes and vesicles reveals membrane tension generated by spontaneous curvature. Faraday Discuss 161:305–31
     [Google Scholar]
  82. 82.
    Lipowsky R. 2014. Coupling of bending and stretching deformations in vesicle membranes. Adv. Colloid Interface Sci. 208:14–24
     [Google Scholar]
  83. 83.
    Markin VS. 1981. Lateral organization of membranes and cell shapes. Biophys. J. 36:11–19
     [Google Scholar]
  84. 84.
    Markin VS, Kozlov MM, Leikin SL. 1988. Definition of surface tension at a non-spherical interface. J. Chem. Soc. Faraday Trans. 2 Mol. Chem. Phys. 84:81149–62
     [Google Scholar]
  85. 85.
    Martyna A, Bahsoun B, Badham MD, Srinivasan S, Howard MJ, Rossman JS 2017. Membrane remodeling by the M2 amphipathic helix drives influenza virus membrane scission. Sci. Rep. 7:44695
     [Google Scholar]
  86. 86.
    McMahon HT, Gallop JL. 2005. Membrane curvature and mechanisms of dynamic cell membrane remodelling. Nature 438:7068590–96
     [Google Scholar]
  87. 87.
    Melero A, Chiaruttini N, Karashima T, Riezman I, Funato K et al. 2018. Lysophospholipids facilitate COPII vesicle formation. Curr. Biol. 28:121950–58.e6
     [Google Scholar]
  88. 88.
    Netz RR, Pincus P 1995. Inhomogeneous fluid membranes: segregation, ordering, and effective rigidity. Phys. Rev. E 52:44114
     [Google Scholar]
  89. 89.
    Nguyen N, Shteyn V, Melia TJ. 2017. Sensing membrane curvature in macroautophagy. J. Mol. Biol. 429:4457–72
     [Google Scholar]
  90. 90.
    Nishizawa M, Nishizawa K. 2010. Curvature-driven lipid sorting: coarse-grained dynamics simulations of a membrane mimicking a hemifusion intermediate. J. Biophys. Chem. 1:286–95
     [Google Scholar]
  91. 91.
    Olzmann JA, Carvalho P. 2019. Dynamics and functions of lipid droplets. Nat. Rev. Mol. Cell Biol. 20:3137–55
     [Google Scholar]
  92. 92.
    Otten D, Brown MF, Beyer K. 2000. Softening of membrane bilayers by detergents elucidated by deuterium NMR spectroscopy. J. Phys. Chem. B 104:5112119–29
     [Google Scholar]
  93. 93.
    Pabst G, Danner S, Podgornik R, Katsaras J 2007. Entropy-driven softening of fluid lipid bilayers by alamethicin. Langmuir 23:2311705–11
     [Google Scholar]
  94. 94.
    Pak AJ, Grime JMA, Sengupta P, Chen AK, Durumeric AEP et al. 2017. Immature HIV-1 lattice assembly dynamics are regulated by scaffolding from nucleic acid and the plasma membrane. PNAS 114:47E10056–65
     [Google Scholar]
  95. 95.
    Pan J, Tieleman DP, Nagle JF, Kucerka N, Tristram-Nagle S. 2009. Alamethicin in lipid bilayers: combined use of X-ray scattering and MD simulations. Biochim. Biophys. Acta Biomembr. 1788:61387–97
     [Google Scholar]
  96. 96.
    Parton RG, Kozlov MM, Ariotti N. 2020. Caveolae and lipid sorting: shaping the cellular response to stress. J. Cell Biol. 219:4e201905071
     [Google Scholar]
  97. 97.
    Pfeffer S. 2003. Membrane domains in the secretory and endocytic pathways. Cell 112:4507–17
     [Google Scholar]
  98. 98.
    Pichot R, Watson RL, Norton IT. 2013. Phospholipids at the interface: current trends and challenges. Int. J. Mol. Sci. 14:611767–94
     [Google Scholar]
  99. 99.
    Pinot M, Vanni S, Pagnotta S, Lacas-Gervais S, Payet L-A et al. 2014. Lipid cell biology. Polyunsaturated phospholipids facilitate membrane deformation and fission by endocytic proteins. Science 345:6197693–97
     [Google Scholar]
  100. 100.
    Prévost C, Tsai F-C, Bassereau P, Simunovic M. 2017. Pulling membrane nanotubes from giant unilamellar vesicles. J. Vis. Exp. 2017 13056086
     [Google Scholar]
  101. 101.
    Prévost C, Zhao H, Manzi J, Lemichez E, Lappalainen P et al. 2015. IRSp53 senses negative membrane curvature and phase separates along membrane tubules. Nat. Commun. 6:8529
     [Google Scholar]
  102. 102.
    Ramamurthi KS, Lecuyer S, Stone HA, Losick R. 2009. Geometric cue for protein localization in a bacterium. Science 323:59191354–57
     [Google Scholar]
  103. 103.
    Raucher D, Sheetz MP. 1999. Characteristics of a membrane reservoir buffering membrane tension. Biophys. J. 77:41992–2002
     [Google Scholar]
  104. 104.
    Reubold TF, Faelber K, Plattner N, Posor Y, Ketel K et al. 2015. Crystal structure of the dynamin tetramer. Nature 525:7569404–8
     [Google Scholar]
  105. 105.
    Reynwar BJ, Illya G, Harmandaris VA, Müller MM, Kremer K, Deserno M. 2007. Aggregation and vesiculation of membrane proteins by curvature-mediated interactions. Nature 447:7143461–64
     [Google Scholar]
  106. 106.
    Roux A. 2013. The physics of membrane tubes: soft templates for studying cellular membranes. Soft Matter 9:6726–36
     [Google Scholar]
  107. 107.
    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 24:81537–45
     [Google Scholar]
  108. 108.
    Roux A, Koster G, Lenz M, Sorre B, Manneville J-B et al. 2010. Membrane curvature controls dynamin polymerization. PNAS 107:94141–46
     [Google Scholar]
  109. 109.
    Safouane M, Berland L, Callan-Jones A, Sorre B, Römer W et al. 2010. Lipid cosorting mediated by Shiga toxin induced tubulation. Traffic 11:121519–29
     [Google Scholar]
  110. 110.
    Saheki Y, De Camilli P. 2012. Synaptic vesicle endocytosis. Cold Spring Harb. Perspect. Biol. 4:9a005645
     [Google Scholar]
  111. 111.
    Santinho A, Salo VT, Chorlay A, Li S, Zhou X et al. 2020. Membrane curvature catalyzes lipid droplet assembly. Curr. Biol. 30:132481–94.e6
     [Google Scholar]
  112. 112.
    Šarić A, Cacciuto A. 2013. Self-assembly of nanoparticles adsorbed on fluid and elastic membranes. Soft Matter 9:6677–95
     [Google Scholar]
  113. 113.
    Seifert U, Berndl K, Lipowsky R. 1991. Shape transformations of vesicles: phase diagram for spontaneous-curvature and bilayer-coupling models. Phys. Rev. A 44:21182–202
     [Google Scholar]
  114. 114.
    Settles EI, Loftus AF, McKeown AN, Parthasarathy R. 2010. The vesicle trafficking protein Sar1 lowers lipid membrane rigidity. Biophys. J. 99:51539–45
     [Google Scholar]
  115. 115.
    Shaw ML, Stone KL, Colangelo CM, Gulcicek EE, Palese P. 2008. Cellular proteins in influenza virus particles. PLOS Pathog 4:6e1000085
     [Google Scholar]
  116. 116.
    Shemesh T, Luini A, Malhotra V, Burger KNJ, Kozlov MM. 2003. Prefission constriction of Golgi tubular carriers driven by local lipid metabolism: a theoretical model. Biophys. J. 85:63813–27
     [Google Scholar]
  117. 117.
    Shi Z, Baumgart T. 2015. Membrane tension and peripheral protein density mediate membrane shape transitions. Nat. Commun. 6:5974
     [Google Scholar]
  118. 118.
    Shnyrova AV, Frolov VA, Zimmerberg J. 2009. Domain-driven morphogenesis of cellular membranes. Curr. Biol. 19:17R772–80
     [Google Scholar]
  119. 119.
    Simunovic M, Evergren E, Callan-Jones A, Bassereau P. 2019. Curving cells inside and out: roles of BAR domain proteins in membrane shaping and its cellular implications. Annu. Rev. Cell Dev. Biol. 35:111–29
     [Google Scholar]
  120. 120.
    Simunovic M, Evergren E, Golushko I, Prévost C, Renard H-F et al. 2016. How curvature-generating proteins build scaffolds on membrane nanotubes. PNAS 113:4011226–31
     [Google Scholar]
  121. 121.
    Simunovic M, Manneville JB, Renard HF, Evergren E, Raghunathan K et al. 2017. Friction mediates scission of tubular membranes scaffolded by BAR proteins. Cell 170:1172–84.e11
     [Google Scholar]
  122. 122.
    Simunovic M, Šarić A, Henderson JM, Lee KYC, Voth GA 2017. Long-range organization of membrane-curving proteins. ACS Cent. Sci. 3:121246–53
     [Google Scholar]
  123. 123.
    Simunovic M, Voth GA, Callan-Jones A, Bassereau P 2015. When physics takes over: BAR proteins and membrane curvature. Trends Cell Biol 25:12780–92
     [Google Scholar]
  124. 124.
    Snead WT, Hayden CC, Gadok AK, Zhao C, Lafer EM et al. 2017. Membrane fission by protein crowding. PNAS 114:16E3258–67
     [Google Scholar]
  125. 125.
    Sodt AJ, Pastor RW. 2013. Bending free energy from simulation: correspondence of planar and inverse hexagonal lipid phases. Biophys. J. 104:102202–11
     [Google Scholar]
  126. 126.
    Sodt AJ, Venable RM, Lyman E, Pastor RW 2016. Nonadditive compositional curvature energetics of lipid bilayers. Phys. Rev. Lett. 117:13138104
     [Google Scholar]
  127. 127.
    Sorre B, Callan-Jones A, Manneville JB, Nassoy P, Joanny JF et al. 2009. Curvature-driven lipid sorting needs proximity to a demixing point and is aided by proteins. PNAS 106:145622–26
     [Google Scholar]
  128. 128.
    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 109:1173–78
     [Google Scholar]
  129. 129.
    Steinem C, Meinecke M. 2021. ENTH domain-dependent membrane remodelling. Soft Matter 17:2233–40
     [Google Scholar]
  130. 130.
    Strahl H, Ronneau S, González BS, Klutsch D, Schaffner-Barbero C, Hamoen LW. 2015. Transmembrane protein sorting driven by membrane curvature. Nat. Commun. 6:8728
     [Google Scholar]
  131. 131.
    Suezaki Y. 1978. Statistical mechanical analysis of interfacial tension of black lipid membrane. J. Theor. Biol. 71:3279–94
     [Google Scholar]
  132. 132.
    Sun M, Graham JS, Hegedüs B, Marga F, Zhang Y et al. 2005. Multiple membrane tethers probed by atomic force microscopy. Biophys. J. 89:64320–29
     [Google Scholar]
  133. 133.
    Svetina S, Kralj-Iglič V, Žekš B 1990. Cell shape and lateral distribution of mobile membrane constituents. Biophysics of Membrane Transport: Tenth School on Biophysics of Membrane Transport, Part II J Kuczera, S Przestalski 139–55 Wrocław, Pol.: Agric. Univ. Wrocław
     [Google Scholar]
  134. 134.
    Svetina S, Sekš B. 1990. The mechanical behaviour of cell membranes as a possible physical origin of cell polarity. J. Theor. Biol. 146:1115–22
     [Google Scholar]
  135. 135.
    Tanaka M, Kikuchi T, Uno H, Okita K, Kitanishi-Yumura T, Yumura S. 2017. Turnover and flow of the cell membrane for cell migration. Sci. Rep. 7:112970
     [Google Scholar]
  136. 136.
    Tanaka M, Komikawa T, Yanai K, Okochi M 2020. Proteomic exploration of membrane curvature sensors using a series of spherical supported lipid bilayers. Anal. Chem. 92:2416197–203
     [Google Scholar]
  137. 137.
    Tian A, Baumgart T. 2009. Sorting of lipids and proteins in membrane curvature gradients. Biophys. J. 96:72676–88
     [Google Scholar]
  138. 138.
    Tian A, Capraro BR, Esposito C, Baumgart T. 2009. Bending stiffness depends on curvature of ternary lipid mixture tubular membranes. Biophys. J. 97:61636–46
     [Google Scholar]
  139. 139.
    Tien HT. 1967. Black lipid membranes in aqueous media: interfacial free energy measurements and effect of surfactants on film formation and stability. J. Phys. Chem. 71:113395–401
     [Google Scholar]
  140. 140.
    Tozzi C, Walani N, Le Roux AL, Roca-Cusachs P, Arroyo M 2021. A theory of ordering of elongated and curved proteins on membranes driven by density and curvature. Soft Matter 17:123367–79
     [Google Scholar]
  141. 141.
    Tsai F-C, Simunovic M, Sorre B, Bertin A, Manzi J et al. 2021. Comparing physical mechanisms for membrane curvature-driven sorting of BAR-domain proteins. Soft Matter 17:164254–65
     [Google Scholar]
  142. 142.
    Upadhyaya A, Sheetz MP. 2004. Tension in tubulovesicular networks of Golgi and endoplasmic reticulum membranes. Biophys. J. 86:52923–28
     [Google Scholar]
  143. 143.
    Walani N, Torres J, Agrawal A. 2014. Anisotropic spontaneous curvatures in lipid membranes. Phys. Rev. E 89:6062715
     [Google Scholar]
  144. 144.
    Watanabe S, Rost BR, Camacho-Pérez M, Davis MW, Söhl-Kielczynski B et al. 2013. Ultrafast endocytosis at mouse hippocampal synapses. Nature 504:7479242–47
     [Google Scholar]
  145. 145.
    Watanabe S, Trimbuch T, Camacho-Pérez M, Rost BR, Brokowski B et al. 2014. Clathrin regenerates synaptic vesicles from endosomes. Nature 515:7526228–33
     [Google Scholar]
  146. 146.
    Wilhelm BG, Mandad S, Truckenbrodt S, Kröhnert K, Schäfer C et al. 2014. Composition of isolated synaptic boutons reveals the amounts of vesicle trafficking proteins. Science 344:61871023–28
     [Google Scholar]
  147. 147.
    Woodward X, Stimpson EE, Kelly CV. 2018. Single-lipid tracking on nanoscale membrane buds: the effects of curvature on lipid diffusion and sorting. Biochim. Biophys. Acta Biomembr. 1860:102064–75
     [Google Scholar]
  148. 148.
    Wu QY, Liang Q. 2014. Interplay between curvature and lateral organization of lipids and peptides/proteins in model membranes. Langmuir 30:41116–22
     [Google Scholar]
  149. 149.
    Zeno WF, Day KJ, Gordon VD, Stachowiak JC 2020. Principles and applications of biological membrane organization. Annu. Rev. Biophys. 49:19–39
     [Google Scholar]
  150. 150.
    Zeno WF, Snead WT, Thatte AS, Stachowiak JC. 2019. Structured and intrinsically disordered domains within Amphiphysin1 work together to sense and drive membrane curvature. Soft Matter 15:438706–17
     [Google Scholar]
  151. 151.
    Zhan H, Lazaridis T. 2013. Inclusion of lateral pressure/curvature stress effects in implicit membrane models. Biophys. J. 104:3643–54
     [Google Scholar]
  152. 152.
    Zhu C, Das SL, Baumgart T. 2012. Nonlinear sorting, curvature generation, and crowding of endophilin N-BAR on tubular membranes. Biophys. J. 102:81837–45
     [Google Scholar]
  153. 153.
    Zimmerberg J, Kozlov MM. 2005. How proteins produce cellular membrane curvature. Nat. Rev. Mol. Cell Biol. 7:19–19
     [Google Scholar]
  154. 154.
    Zimmerberg J, McLaughlin S. 2004. Membrane curvature: how BAR domains bend bilayers. Curr. Biol. 14:6R250–52
     [Google Scholar]
/content/journals/10.1146/annurev-biophys-011422-100054
Loading
Molecular Shape Solution for Mesoscopic Remodeling of Cellular Membranes
Annual Review of Biophysics 51, 473 (2022); https://doi.org/10.1146/annurev-biophys-011422-100054
/content/journals/10.1146/annurev-biophys-011422-100054
/content/journals/10.1146/annurev-biophys-011422-100054
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