ACS Publications. Most Trusted. Most Cited. Most Read
My Activity
CONTENT TYPES

Figure 1Loading Img

Steric Pressure between Membrane-Bound Proteins Opposes Lipid Phase Separation

View Author Information
Department of Biomedical Engineering, The University of Texas at Austin, Austin, Texas 78712, United States
Cite this: J. Am. Chem. Soc. 2013, 135, 4, 1185–1188
Publication Date (Web):January 15, 2013
https://doi.org/10.1021/ja3099867
Copyright © 2013 American Chemical Society

    Article Views

    2718

    Altmetric

    -

    Citations

    LEARN ABOUT THESE METRICS
    Read OnlinePDF (2 MB)
    Supporting Info (2)»

    Abstract

    Abstract Image

    Cellular membranes are densely crowded with a diverse population of integral and membrane-associated proteins. In this complex environment, lipid rafts, which are phase-separated membrane domains enriched in cholesterol and saturated lipids, are thought to organize the membrane surface. Specifically, rafts may help to concentrate proteins and lipids locally, enabling cellular processes such as assembly of caveolae, budding of enveloped viruses, and sorting of lipids and proteins in the Golgi. However, the ability of rafts to concentrate protein species has not been quantified experimentally. Here we show that when membrane-bound proteins become densely crowded within liquid-ordered membrane regions, steric pressure arising from collisions between proteins can destabilize lipid phase separations, resulting in a homogeneous distribution of proteins and lipids over the membrane surface. Using a reconstituted system of lipid vesicles and recombinant proteins, we demonstrate that protein–protein steric pressure creates an energetic barrier to the stability of phase-separated membrane domains that increases in significance as the molecular weight of the proteins increases. Comparison with a simple analytical model reveals that domains are destabilized when the steric pressure exceeds the approximate enthalpy of membrane mixing. These results suggest that a subtle balance of free energies governs the stability of phase-separated cellular membranes, providing a new perspective on the role of lipid rafts as concentrators of membrane proteins.

    Supporting Information

    ARTICLE SECTIONS
    Jump To

    Materials and methods and supporting figures, video, and discussion. This material is available free of charge via the Internet at http://pubs.acs.org.

    Terms & Conditions

    Most electronic Supporting Information files are available without a subscription to ACS Web Editions. Such files may be downloaded by article for research use (if there is a public use license linked to the relevant article, that license may permit other uses). Permission may be obtained from ACS for other uses through requests via the RightsLink permission system: http://pubs.acs.org/page/copyright/permissions.html.

    Cited By

    This article is cited by 70 publications.

    1. Yifei Wang, Sheereen Majd. Charged Lipids Modulate the Phase Separation in Multicomponent Membranes. Langmuir 2023, 39 (32) , 11371-11378. https://doi.org/10.1021/acs.langmuir.3c01199
    2. Juan Ureña, Ashlynn Knight, Il-Hyung Lee. Membrane Cargo Density-Dependent Interaction between Protein and Lipid Domains on the Giant Unilamellar Vesicles. Langmuir 2022, 38 (15) , 4702-4712. https://doi.org/10.1021/acs.langmuir.2c00247
    3. Ryou Kubota, Wataru Tanaka, Itaru Hamachi. Microscopic Imaging Techniques for Molecular Assemblies: Electron, Atomic Force, and Confocal Microscopies. Chemical Reviews 2021, 121 (22) , 14281-14347. https://doi.org/10.1021/acs.chemrev.0c01334
    4. Justin R. Houser, Carl C. Hayden, D. Thirumalai, Jeanne C. Stachowiak. A Förster Resonance Energy Transfer-Based Sensor of Steric Pressure on Membrane Surfaces. Journal of the American Chemical Society 2020, 142 (49) , 20796-20805. https://doi.org/10.1021/jacs.0c09802
    5. Dima Bolmatov, Dmytro Soloviov, Mikhail Zhernenkov, Dmitry Zav’yalov, Eugene Mamontov, Alexey Suvorov, Yong Q. Cai, John Katsaras. Molecular Picture of the Transient Nature of Lipid Rafts. Langmuir 2020, 36 (18) , 4887-4896. https://doi.org/10.1021/acs.langmuir.0c00125
    6. Navneet Dogra, Rajesh P. Balaraman, Punit Kohli. Chemically Engineered Synthetic Lipid Vesicles for Sensing and Visualization of Protein–Bilayer Interactions. Bioconjugate Chemistry 2019, 30 (8) , 2136-2149. https://doi.org/10.1021/acs.bioconjchem.9b00366
    7. Wade F. Zeno, Ajay S. Thatte, Liping Wang, Wilton T. Snead, Eileen M. Lafer, Jeanne C. Stachowiak. Molecular Mechanisms of Membrane Curvature Sensing by a Disordered Protein. Journal of the American Chemical Society 2019, 141 (26) , 10361-10371. https://doi.org/10.1021/jacs.9b03927
    8. Il-Hyung Lee, Matthew Y. Imanaka, Emmi H. Modahl, Ana P. Torres-Ocampo. Lipid Raft Phase Modulation by Membrane-Anchored Proteins with Inherent Phase Separation Properties. ACS Omega 2019, 4 (4) , 6551-6559. https://doi.org/10.1021/acsomega.9b00327
    9. Arielle C. Mensch, Joseph T. Buchman, Christy L. Haynes, Joel A. Pedersen, Robert J. Hamers. Quaternary Amine-Terminated Quantum Dots Induce Structural Changes to Supported Lipid Bilayers. Langmuir 2018, 34 (41) , 12369-12378. https://doi.org/10.1021/acs.langmuir.8b02047
    10. Avinash K. Gadok, Chi Zhao, Amanda I. Meriwether, Silvia Ferrati, Tanner G. Rowley, Janet Zoldan, Hugh D. C. Smyth, and Jeanne C. Stachowiak . The Display of Single-Domain Antibodies on the Surfaces of Connectosomes Enables Gap Junction-Mediated Drug Delivery to Specific Cell Populations. Biochemistry 2018, 57 (1) , 81-90. https://doi.org/10.1021/acs.biochem.7b00688
    11. Wade F. Zeno, Kaitlin E. Johnson, Darryl Y. Sasaki, Subhash H. Risbud, and Marjorie L. Longo . Dynamics of Crowding-Induced Mixing in Phase Separated Lipid Bilayers. The Journal of Physical Chemistry B 2016, 120 (43) , 11180-11190. https://doi.org/10.1021/acs.jpcb.6b07119
    12. Wade F. Zeno, Alice Rystov, Darryl Y. Sasaki, Subhash H. Risbud, and Marjorie L. Longo . Crowding-Induced Mixing Behavior of Lipid Bilayers: Examination of Mixing Energy, Phase, Packing Geometry, and Reversibility. Langmuir 2016, 32 (18) , 4688-4697. https://doi.org/10.1021/acs.langmuir.6b00831
    13. Zachary I. Imam, Laura E. Kenyon, Adelita Carrillo, Isai Espinoza, Fatema Nagib, and Jeanne C. Stachowiak . Steric Pressure among Membrane-Bound Polymers Opposes Lipid Phase Separation. Langmuir 2016, 32 (15) , 3774-3784. https://doi.org/10.1021/acs.langmuir.6b00170
    14. James C. S. Ho, Padmini Rangamani, Bo Liedberg, and Atul N. Parikh . Mixing Water, Transducing Energy, and Shaping Membranes: Autonomously Self-Regulating Giant Vesicles. Langmuir 2016, 32 (9) , 2151-2163. https://doi.org/10.1021/acs.langmuir.5b04470
    15. Myungshim Kang and Sharon M. Loverde . Molecular Simulation of the Concentration-Dependent Interaction of Hydrophobic Drugs with Model Cellular Membranes. The Journal of Physical Chemistry B 2014, 118 (41) , 11965-11972. https://doi.org/10.1021/jp5047613
    16. Jesper S. Hansen, James R. Thompson, Claus Hélix-Nielsen, and Noah Malmstadt . Lipid Directed Intrinsic Membrane Protein Segregation. Journal of the American Chemical Society 2013, 135 (46) , 17294-17297. https://doi.org/10.1021/ja409708e
    17. Andreas Santamaria, Krishna C. Batchu, Giovanna Fragneto, Valérie Laux, Michael Haertlein, Tamim A. Darwish, Robert A. Russell, Nathan R. Zaccai, Eduardo Guzmán, Armando Maestro. Investigation on the relationship between lipid composition and structure in model membranes composed of extracted natural phospholipids. Journal of Colloid and Interface Science 2023, 637 , 55-66. https://doi.org/10.1016/j.jcis.2023.01.043
    18. Naofumi Shimokawa, Tsutomu Hamada. Physical Concept to Explain the Regulation of Lipid Membrane Phase Separation under Isothermal Conditions. Life 2023, 13 (5) , 1105. https://doi.org/10.3390/life13051105
    19. Junliang Shen, Pengfei Jiang, Ting Chen, Hua Ding, Weihong Huang, Wenming Yang. Selective enrichment and extraction of trace dibutyl phthalate by photo‐controlled molecularly imprinting polymers based on SiO 2 nanoparticles. Journal of Applied Polymer Science 2023, 140 (11) https://doi.org/10.1002/app.53613
    20. Tsutomu Hamada, Shino Mizuno, Hiroyuki Kitahata. Domain dynamics of phase-separated lipid membranes under shear flow. Soft Matter 2022, 18 (47) , 9069-9075. https://doi.org/10.1039/D2SM00825D
    21. Anup Parchure, Meng Tian, Danièle Stalder, Cierra K. Boyer, Shelby C. Bearrows, Kristen E. Rohli, Jianchao Zhang, Felix Rivera-Molina, Bulat R. Ramazanov, Sushil K. Mahata, Yanzhuang Wang, Samuel B. Stephens, David C. Gershlick, Julia von Blume. Liquid–liquid phase separation facilitates the biogenesis of secretory storage granules. Journal of Cell Biology 2022, 221 (12) https://doi.org/10.1083/jcb.202206132
    22. Il-Hyung Lee, Sam Passaro, Selin Ozturk, Juan Ureña, Weitian Wang. Intelligent fluorescence image analysis of giant unilamellar vesicles using convolutional neural network. BMC Bioinformatics 2022, 23 (1) https://doi.org/10.1186/s12859-022-04577-2
    23. Wenming Yang, Junliang Shen, Shengjie Zhu, Haojie Si, Fei Song, Wenwen Zhang, Hua Ding, Weihong Huang. Preparation and characterisation of photoresponsive molecularly imprinted polymer based on 5-[(4-(methacryloyloxy) phenyl) diazenyl] isophthalic acid for the determination of sulfamethazine. Microchemical Journal 2022, 182 , 107823. https://doi.org/10.1016/j.microc.2022.107823
    24. Victoria Thusgaard Ruhoff, Guillermo Moreno-Pescador, Weria Pezeshkian, Poul Martin Bendix. Strength in numbers: effect of protein crowding on the shape of cell membranes. Biochemical Society Transactions 2022, 50 (5) , 1257-1267. https://doi.org/10.1042/BST20210883
    25. Justin R. Houser, Hyun Woo Cho, Carl C. Hayden, Noel X. Yang, Liping Wang, Eileen M. Lafer, Dave Thirumalai, Jeanne C. Stachowiak. Molecular mechanisms of steric pressure generation and membrane remodeling by disordered proteins. Biophysical Journal 2022, 121 (18) , 3320-3333. https://doi.org/10.1016/j.bpj.2022.08.028
    26. Cuncheng Zhu, Christopher T. Lee, Padmini Rangamani. Mem3DG: Modeling membrane mechanochemical dynamics in 3D using discrete differential geometry. Biophysical Reports 2022, 2 (3) , 100062. https://doi.org/10.1016/j.bpr.2022.100062
    27. Chandra Has, P. Sivadas, Sovan Lal Das. Insights into Membrane Curvature Sensing and Membrane Remodeling by Intrinsically Disordered Proteins and Protein Regions. The Journal of Membrane Biology 2022, 255 (2-3) , 237-259. https://doi.org/10.1007/s00232-022-00237-x
    28. Jian Zhang, Lingling Liang, Yanqing Miao, Yang Yang, Xin Bao, Chunye Liu. Open-tubular capillary electrochromatography with hydroxypropyl-β-cyclodextrin imprinted polymers: hybrid polyhedral oligomeric silsesquioxane as a coating for enantioseparation. RSC Advances 2022, 12 (16) , 9637-9644. https://doi.org/10.1039/D2RA00079B
    29. Kamila Sofińska, Dawid Lupa, Anna Chachaj-Brekiesz, Michał Czaja, Jan Kobierski, Sara Seweryn, Katarzyna Skirlińska-Nosek, Marek Szymonski, Natalia Wilkosz, Anita Wnętrzak, Ewelina Lipiec. Revealing local molecular distribution, orientation, phase separation, and formation of domains in artificial lipid layers: Towards comprehensive characterization of biological membranes. Advances in Colloid and Interface Science 2022, 301 , 102614. https://doi.org/10.1016/j.cis.2022.102614
    30. Kayla Sapp, Alexander J. Sodt. Observed steric crowding at modest coverage requires a particular membrane-binding scheme or a complementary mechanism. Biophysical Journal 2022, 121 (3) , 430-438. https://doi.org/10.1016/j.bpj.2021.12.036
    31. Maryna Löwe, Milara Kalacheva, Arnold J. Boersma, Alexej Kedrov. The more the merrier: effects of macromolecular crowding on the structure and dynamics of biological membranes. The FEBS Journal 2020, 287 (23) , 5039-5067. https://doi.org/10.1111/febs.15429
    32. Ishier Raote, Morgan Chabanon, Nikhil Walani, Marino Arroyo, Maria F Garcia-Parajo, Vivek Malhotra, Felix Campelo. A physical mechanism of TANGO1-mediated bulky cargo export. eLife 2020, 9 https://doi.org/10.7554/eLife.59426
    33. Paweł Borowicz, Hanna Chan, Anette Hauge, Anne Spurkland. Adaptor proteins: Flexible and dynamic modulators of immune cell signalling. Scandinavian Journal of Immunology 2020, 92 (5) https://doi.org/10.1111/sji.12951
    34. Ester Canepa, Sebastian Salassi, Anna Lucia de Marco, Chiara Lambruschini, Davide Odino, Davide Bochicchio, Fabio Canepa, Claudio Canale, Silvia Dante, Rosaria Brescia, Francesco Stellacci, Giulia Rossi, Annalisa Relini. Amphiphilic gold nanoparticles perturb phase separation in multidomain lipid membranes. Nanoscale 2020, 12 (38) , 19746-19759. https://doi.org/10.1039/D0NR05366J
    35. Hyun‐Ro Lee, Yohan Lee, Seung Soo Oh, Siyoung Q. Choi. Ultra‐Stable Freestanding Lipid Membrane Array: Direct Visualization of Dynamic Membrane Remodeling with Cholesterol Transport and Enzymatic Reactions. Small 2020, 16 (40) https://doi.org/10.1002/smll.202002541
    36. Ming Li, William T. Heller, Chung-Hao Liu, Carrie Y. Gao, Yutian Cai, Yiming Hou, Mu-Ping Nieh. Effects of fluidity and charge density on the morphology of a bicellar mixture – A SANS study. Biochimica et Biophysica Acta (BBA) - Biomembranes 2020, 1862 (9) , 183315. https://doi.org/10.1016/j.bbamem.2020.183315
    37. Caitlin E. Cornell, Alexander Mileant, Niket Thakkar, Kelly K. Lee, Sarah L. Keller. Direct imaging of liquid domains in membranes by cryo-electron tomography. Proceedings of the National Academy of Sciences 2020, 117 (33) , 19713-19719. https://doi.org/10.1073/pnas.2002245117
    38. Wenming Yang, Yujie Qing, Yunfei Cao, Yu Luan, Yi Lu, Tianshu Liu, Wanzhen Xu, Weihong Huang, Tianzhu Li, Xiaoni Ni. A stimuli response, core-shell structured and surface molecularly imprinted polymers with specific pH for rapid and selective detection of sulfamethoxazole from milk sample. Reactive and Functional Polymers 2020, 151 , 104578. https://doi.org/10.1016/j.reactfunctpolym.2020.104578
    39. Yu-Zhen Zhang, Bei Qin, Bo Zhang, Jin-Ge Ma, Ya-Qi Hu, Lu Han, Mao-Fang He, Chun-Ye Liu. Specific enrichment of caffeic acid from Taraxacum mon-golicum Hand.-Mazz. by pH and magnetic dual-responsive molecularly imprinted polymers. Analytica Chimica Acta 2020, 1096 , 193-202. https://doi.org/10.1016/j.aca.2019.10.060
    40. Naofumi Shimokawa, Hiroaki Ito, Yuji Higuchi. Coarse-grained molecular dynamics simulation for uptake of nanoparticles into a charged lipid vesicle dominated by electrostatic interactions. Physical Review E 2019, 100 (1) https://doi.org/10.1103/PhysRevE.100.012407
    41. Wade F. Zeno, Maria O. Ogunyankin, Marjorie L. Longo. Scaling relationships for translational diffusion constants applied to membrane domain dissolution and growth. Biochimica et Biophysica Acta (BBA) - Biomembranes 2018, 1860 (10) , 1994-2003. https://doi.org/10.1016/j.bbamem.2018.02.028
    42. Kenichi Morigaki, Yasushi Tanimoto. Evolution and development of model membranes for physicochemical and functional studies of the membrane lateral heterogeneity. Biochimica et Biophysica Acta (BBA) - Biomembranes 2018, 1860 (10) , 2012-2017. https://doi.org/10.1016/j.bbamem.2018.03.010
    43. Wilton T. Snead, Jeanne C. Stachowiak. Structure Versus Stochasticity—The Role of Molecular Crowding and Intrinsic Disorder in Membrane Fission. Journal of Molecular Biology 2018, 430 (16) , 2293-2308. https://doi.org/10.1016/j.jmb.2018.03.024
    44. Wade F. Zeno, Maria O. Ogunyankin, Marjorie L. Longo. Curvature Sorting and Crowding-Induced Mixing in Experimental Model Membranes. 2018, 223-250. https://doi.org/10.1016/bs.abl.2017.12.007
    45. Jianchang Xu, Shuangqing Sun, Zhikun Wang, Shiyuan Peng, Songqing Hu, Lijuan Zhang. pH-Induced evolution of surface patterns in micelles assembled from dirhamnolipids: dissipative particle dynamics simulation. Physical Chemistry Chemical Physics 2018, 20 (14) , 9460-9470. https://doi.org/10.1039/C8CP00751A
    46. Marco M. Manni, Jure Derganc, Alenka Čopič. Crowd-Sourcing of Membrane Fission. BioEssays 2017, 39 (12) , 1700117. https://doi.org/10.1002/bies.201700117
    47. Morgan Chabanon, Jeanne C. Stachowiak, Padmini Rangamani. Systems biology of cellular membranes: a convergence with biophysics. WIREs Systems Biology and Medicine 2017, 9 (5) https://doi.org/10.1002/wsbm.1386
    48. Mariola Szenk, Ken A. Dill, Adam M.R. de Graff. Why Do Fast-Growing Bacteria Enter Overflow Metabolism? Testing the Membrane Real Estate Hypothesis. Cell Systems 2017, 5 (2) , 95-104. https://doi.org/10.1016/j.cels.2017.06.005
    49. Jingfan Xie, Guanqun Zhong, Changqun Cai, Chunyan Chen, Xiaoming Chen. Rapid and efficient separation of glycoprotein using pH double-responsive imprinted magnetic microsphere. Talanta 2017, 169 , 98-103. https://doi.org/10.1016/j.talanta.2017.03.065
    50. Aidan I. Brown, Andrew D. Rutenberg. A Model of Autophagy Size Selectivity by Receptor Clustering on Peroxisomes. Frontiers in Physics 2017, 5 https://doi.org/10.3389/fphy.2017.00014
    51. Wilton T. Snead, Carl C. Hayden, Avinash K. Gadok, Chi Zhao, Eileen M. Lafer, Padmini Rangamani, Jeanne C. Stachowiak. Membrane fission by protein crowding. Proceedings of the National Academy of Sciences 2017, 114 (16) https://doi.org/10.1073/pnas.1616199114
    52. Xubo Lin, Siya Zhang, Hui Ding, Ilya Levental, Alemayehu A. Gorfe. The aliphatic chain of cholesterol modulates bilayer interleaflet coupling and domain registration. FEBS Letters 2016, 590 (19) , 3368-3374. https://doi.org/10.1002/1873-3468.12383
    53. Chi Zhao, David J. Busch, Connor P. Vershel, Jeanne C. Stachowiak. Multifunctional Transmembrane Protein Ligands for Cell-Specific Targeting of Plasma Membrane-Derived Vesicles. Small 2016, 12 (28) , 3837-3848. https://doi.org/10.1002/smll.201600493
    54. Jure Derganc, Alenka Čopič. Membrane bending by protein crowding is affected by protein lateral confinement. Biochimica et Biophysica Acta (BBA) - Biomembranes 2016, 1858 (6) , 1152-1159. https://doi.org/10.1016/j.bbamem.2016.03.009
    55. Shunsuke F. Shimobayashi, Masatoshi Ichikawa, Takashi Taniguchi. Direct observations of transition dynamics from macro- to micro-phase separation in asymmetric lipid bilayers induced by externally added glycolipids. EPL (Europhysics Letters) 2016, 113 (5) , 56005. https://doi.org/10.1209/0295-5075/113/56005
    56. Eva Sevcsik, Gerhard J. Schütz. With or without rafts? Alternative views on cell membranes. BioEssays 2016, 38 (2) , 129-139. https://doi.org/10.1002/bies.201500150
    57. Justin R. Houser, David J. Busch, David R. Bell, Brian Li, Pengyu Ren, Jeanne C. Stachowiak. The impact of physiological crowding on the diffusivity of membrane bound proteins. Soft Matter 2016, 12 (7) , 2127-2134. https://doi.org/10.1039/C5SM02572A
    58. Xiaoming Deng, Chunyan Chen, Jingfan Xie, Changqun Cai, Xiaoming Chen. Selective adsorption of elastase by surface molecular imprinting materials prepared with novel monomer. RSC Advances 2016, 6 (49) , 43223-43227. https://doi.org/10.1039/C6RA04805F
    59. David J. Busch, Justin R. Houser, Carl C. Hayden, Michael B. Sherman, Eileen M. Lafer, Jeanne C. Stachowiak. Intrinsically disordered proteins drive membrane curvature. Nature Communications 2015, 6 (1) https://doi.org/10.1038/ncomms8875
    60. Yijing Liu, Ben Liu, Zhihong Nie. Concurrent self-assembly of amphiphiles into nanoarchitectures with increasing complexity. Nano Today 2015, 10 (3) , 278-300. https://doi.org/10.1016/j.nantod.2015.04.001
    61. Sharon E. Miller, Signe Mathiasen, Nicholas A. Bright, Fabienne Pierre, Bernard T. Kelly, Nikolay Kladt, Astrid Schauss, Christien J. Merrifield, Dimitrios Stamou, Stefan Höning, David J. Owen. CALM Regulates Clathrin-Coated Vesicle Size and Maturation by Directly Sensing and Driving Membrane Curvature. Developmental Cell 2015, 33 (2) , 163-175. https://doi.org/10.1016/j.devcel.2015.03.002
    62. Noor Momin, Stacey Lee, Avinash K. Gadok, David J. Busch, George D. Bachand, Carl C. Hayden, Jeanne C. Stachowiak, Darryl Y. Sasaki. Designing lipids for selective partitioning into liquid ordered membrane domains. Soft Matter 2015, 11 (16) , 3241-3250. https://doi.org/10.1039/C4SM02856B
    63. Kenichi G.N. Suzuki. New Insights into the Organization of Plasma Membrane and Its Role in Signal Transduction. 2015, 67-96. https://doi.org/10.1016/bs.ircmb.2015.02.004
    64. Janely Pae, Pille Säälik, Laura Liivamägi, Dmitri Lubenets, Piret Arukuusk, Ülo Langel, Margus Pooga. Translocation of cell-penetrating peptides across the plasma membrane is controlled by cholesterol and microenvironment created by membranous proteins. Journal of Controlled Release 2014, 192 , 103-113. https://doi.org/10.1016/j.jconrel.2014.07.002
    65. N. G. Almarza, J. Pȩkalski, A. Ciach. Periodic ordering of clusters and stripes in a two-dimensional lattice model. II. Results of Monte Carlo simulation. The Journal of Chemical Physics 2014, 140 (16) https://doi.org/10.1063/1.4871901
    66. J. Pȩkalski, A. Ciach, N. G. Almarza. Periodic ordering of clusters and stripes in a two-dimensional lattice model. I. Ground state, mean-field phase diagram and structure of the disordered phases. The Journal of Chemical Physics 2014, 140 (11) https://doi.org/10.1063/1.4868001
    67. Ole M. Schütte, Annika Ries, Alexander Orth, Lukas J. Patalag, Winfried Römer, Claudia Steinem, Daniel B. Werz. Influence of Gb3 glycosphingolipids differing in their fatty acid chain on the phase behaviour of solid supported membranes: chemical syntheses and impact of Shiga toxin binding. Chemical Science 2014, 5 (8) , 3104. https://doi.org/10.1039/c4sc01290a
    68. Jure Derganc, Bruno Antonny, Alenka Čopič. Membrane bending: the power of protein imbalance. Trends in Biochemical Sciences 2013, 38 (11) , 576-584. https://doi.org/10.1016/j.tibs.2013.08.006
    69. Jeanne C. Stachowiak, Frances M. Brodsky, Elizabeth A. Miller. A cost–benefit analysis of the physical mechanisms of membrane curvature. Nature Cell Biology 2013, 15 (9) , 1019-1027. https://doi.org/10.1038/ncb2832
    70. Miho Yanagisawa, Taka-aki Yoshida, Miyuki Furuta, Satoshi Nakata, Masayuki Tokita. Adhesive force between paired microdroplets coated with lipid monolayers. Soft Matter 2013, 9 (25) , 5891. https://doi.org/10.1039/c3sm50938a

    Pair your accounts.

    Export articles to Mendeley

    Get article recommendations from ACS based on references in your Mendeley library.

    Pair your accounts.

    Export articles to Mendeley

    Get article recommendations from ACS based on references in your Mendeley library.

    You’ve supercharged your research process with ACS and Mendeley!

    STEP 1:
    Click to create an ACS ID

    Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

    Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

    Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

    MENDELEY PAIRING EXPIRED
    Your Mendeley pairing has expired. Please reconnect