{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,30]],"date-time":"2026-09-30T13:56:28Z","timestamp":1790776588295,"version":"4.1.0"},"reference-count":44,"publisher":"American Chemical Society (ACS)","issue":"5","license":[{"start":{"date-parts":[[2018,4,25]],"date-time":"2018-04-25T00:00:00Z","timestamp":1524614400000},"content-version":"vor","delay-in-days":9,"URL":"https:\/\/pubs.acs.org\/page\/policy\/authorchoice_ccby_termsofuse.html"}],"funder":[{"DOI":"10.13039\/501100001659","name":"Deutsche Forschungsgemeinschaft","doi-asserted-by":"publisher","award":["IRTG 1524"],"award-info":[{"award-number":["IRTG 1524"]}],"id":[{"id":"10.13039\/501100001659","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100002347","name":"Bundesministerium f\u00fcr Bildung und Forschung","doi-asserted-by":"publisher","award":["NA"],"award-info":[{"award-number":["NA"]}],"id":[{"id":"10.13039\/501100002347","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100004189","name":"Max-Planck-Gesellschaft","doi-asserted-by":"publisher","award":["NA"],"award-info":[{"award-number":["NA"]}],"id":[{"id":"10.13039\/501100004189","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2018,5,22]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>Giant unilamellar vesicles (GUVs) provide a direct connection between the nano- and the microregime. On the one hand, these vesicles represent biomimetic compartments with linear dimensions of many micrometers. On the other hand, the vesicle walls are provided by single molecular bilayers that have a thickness of a few nanometers and respond sensitively to molecular interactions with small solutes, biopolymers, and nanoparticles. These nanoscopic responses are amplified by the GUVs and can then be studied on much larger scales. Therefore, GUVs are increasingly used as a versatile research tool for basic membrane science, bioengineering, and synthetic biology. Conventional GUVs have one major drawback, however: they have only a limited capability to cope with external perturbations such as osmotic inflation, adhesion, or micropipette aspiration that tend to rupture the membranes. In contrast, cell membranes tolerate the same kinds of mechanical perturbations without rupture because the latter membranes are coupled to reservoirs of membrane area. Here, we introduce GUVs with membrane nanotubes as model systems that include such area reservoirs. To demonstrate the increased robustness of these tubulated vesicles, we use micropipette aspiration and changes in the osmotic conditions applied to phospholipid membranes doped with the glycolipid GM1. A quantitative comparison between theory and experiment reveals that the response of the GUVs is governed by the membranes\u2019 spontaneous tension, a curvature-elastic material parameter that describes the bilayer asymmetry on the nanoscale. Because of their increased robustness, GUVs with nanotubes represent improved research tools for membrane science, in general, with potential applications as storage and delivery systems and as cell-like microcompartments in bioengineering, pharmacology, and synthetic biology.<\/jats:p>","DOI":"10.1021\/acsnano.8b00640","type":"journal-article","created":{"date-parts":[[2018,4,16]],"date-time":"2018-04-16T15:21:39Z","timestamp":1523892099000},"page":"4478-4485","source":"Crossref","is-referenced-by-count":71,"title":["Membrane Nanotubes Increase\nthe Robustness of Giant\nVesicles"],"prefix":"10.1021","volume":"12","author":[{"given":"Tripta","family":"Bhatia","sequence":"first","affiliation":[{"name":"Max Planck Institute of Colloids and Interfaces , , ,","place":["Potsdam, Germany, 14424"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jaime","family":"Agudo-Canalejo","sequence":"additional","affiliation":[{"name":"University of Oxford , , ,","place":["Oxford, U.K., OX1 3NP"]},{"name":"The Pennsylvania State University , , , ,","place":["University Park, Pennsylvania, United States, 16802"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rumiana","family":"Dimova","sequence":"additional","affiliation":[{"name":"Max Planck Institute of Colloids and Interfaces , , ,","place":["Potsdam, Germany, 14424"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8417-8567","authenticated-orcid":true,"given":"Reinhard","family":"Lipowsky","sequence":"additional","affiliation":[{"name":"Max Planck Institute of Colloids and Interfaces , , ,","place":["Potsdam, Germany, 14424"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"316","published-online":{"date-parts":[[2018,4,16]]},"reference":[{"key":"2026090110235885100_cit1","doi-asserted-by":"publisher","first-page":"S1151","DOI":"10.1088\/0953-8984\/18\/28\/S04","article-title":"A Practical Guide to\nGiant Vesicles: Probing the Membrane\nNanoregime via Optical Microscopy","volume":"18","author":"Dimova","year":"2006","journal-title":"J. Phys.: Condens. Matter"},{"key":"2026090110235885100_cit2","doi-asserted-by":"publisher","first-page":"463","DOI":"10.1021\/acsnano.5b05377","article-title":"Patterns of\nFlexible Nanotubes Formed by Liquid-Ordered and Liquid-Disordered\nMembranes","volume":"10","author":"Liu","year":"2016","journal-title":"ACS Nano"},{"key":"2026090110235885100_cit3","doi-asserted-by":"publisher","first-page":"314","DOI":"10.1021\/acsnano.6b05706","article-title":"Mechanism\nof Shiga Toxin Clustering on Membranes","volume":"11","author":"Pezeshkian","year":"2017","journal-title":"ACS\nNano"},{"key":"2026090110235885100_cit4","doi-asserted-by":"publisher","first-page":"704","DOI":"10.1038\/nphys3678","article-title":"Size-Dependent Protein\nSegregation at Membrane Interfaces","volume":"12","author":"Schmid","year":"2016","journal-title":"Nat. Phys."},{"key":"2026090110235885100_cit5","doi-asserted-by":"publisher","first-page":"14616","DOI":"10.1021\/jacs.6b06820","article-title":"The N-Terminal Amphipathic\nHelix of Endophilin Does Not Contribute to Its Molecular Curvature\nGeneration Capacity","volume":"138","author":"Chen","year":"2016","journal-title":"J. Am. Chem. Soc."},{"key":"2026090110235885100_cit6","doi-asserted-by":"publisher","first-page":"846","DOI":"10.1073\/pnas.1613525114","article-title":"Thermal-Driven Domain and Cargo Transport\nin Lipid\nMembranes","volume":"114","author":"Talbot","year":"2017","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"2026090110235885100_cit7","doi-asserted-by":"publisher","first-page":"E3258","DOI":"10.1073\/pnas.1616199114","article-title":"Membrane Fission by Protein Crowding","volume":"114","author":"Snead","year":"2017","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"2026090110235885100_cit8","doi-asserted-by":"publisher","first-page":"982","DOI":"10.1039\/c2ib00188h","article-title":"Giant Vesicles as Cell\nModels","volume":"4","author":"Fenz","year":"2012","journal-title":"Integr. Biol."},{"key":"2026090110235885100_cit9","doi-asserted-by":"publisher","first-page":"687","DOI":"10.1083\/jcb.201506125","article-title":"Jump-Starting\nLife? Fundamental Aspects of Synthetic Biology","volume":"210","author":"Schwille","year":"2015","journal-title":"J. Cell Biol."},{"key":"2026090110235885100_cit10","doi-asserted-by":"publisher","first-page":"89","DOI":"10.1038\/nmat5005","article-title":"Sequential Bottom-up\nAssembly of Mechanically Stabilized Synthetic Cells by Microfluidics","volume":"17","author":"Weiss","year":"2017","journal-title":"Nat. Mater."},{"key":"2026090110235885100_cit11","doi-asserted-by":"publisher","first-page":"848","DOI":"10.1002\/cbic.201000010","article-title":"Giant Vesicles: Preparations\nand Applications","volume":"11","author":"Walde","year":"2010","journal-title":"ChemBioChem"},{"key":"2026090110235885100_cit12","doi-asserted-by":"publisher","first-page":"752","DOI":"10.1039\/c2lc41121k","article-title":"Microfluidic Methods for Forming\nLiposomes","volume":"13","author":"van Swaay","year":"2013","journal-title":"Lab Chip"},{"key":"2026090110235885100_cit13","doi-asserted-by":"publisher","first-page":"950","DOI":"10.1002\/smll.201301904","article-title":"Ultrathin\nShell Double Emulsion Templated\nGiant Unilamellar Lipid Vesicles with Controlled Microdomain Formation","volume":"10","author":"Arriaga","year":"2014","journal-title":"Small"},{"key":"2026090110235885100_cit14","doi-asserted-by":"publisher","first-page":"16059","DOI":"10.1140\/epje\/i2016-16059-8","article-title":"Vesicles-on-a-chip: A Universal Microfluidic Platform\nfor the Assembly of Liposomes and Polymersomes","volume":"39","author":"Petit","year":"2016","journal-title":"Eur. Phys. J. E: Soft Matter Biol. Phys."},{"key":"2026090110235885100_cit15","doi-asserted-by":"publisher","first-page":"7364","DOI":"10.1039\/C6SM00868B","article-title":"cDICE Method Produces\nGiant Lipid\nVesicles under Physiological Conditions of Charged Lipids and Ionic\nSolutions","volume":"12","author":"Blosser","year":"2016","journal-title":"Soft Matter"},{"key":"2026090110235885100_cit16","doi-asserted-by":"publisher","first-page":"034106","DOI":"10.1063\/1.4983174","article-title":"On-Chip Density-Based\nPurification\nof Liposomes","volume":"11","author":"Deshpande","year":"2017","journal-title":"Biomicrofluidics"},{"key":"2026090110235885100_cit17","doi-asserted-by":"publisher","first-page":"2190","DOI":"10.1016\/j.bpj.2016.09.043","article-title":"Experimental Estimation of Membrane\nTension Induced by Osmotic Pressure","volume":"111","author":"Alam Shibly","year":"2016","journal-title":"Biophys.\nJ."},{"key":"2026090110235885100_cit18","doi-asserted-by":"publisher","first-page":"3065","DOI":"10.1039\/C5CP06786C","article-title":"Relationship between\nVesicle Size and Steric Hindrance Influences Vesicle Rupture on Solid\nSupports","volume":"18","author":"Jackman","year":"2016","journal-title":"Phys. Chem. Chem. Phys."},{"key":"2026090110235885100_cit19","doi-asserted-by":"publisher","first-page":"321","DOI":"10.1016\/S0006-3495(00)76294-1","article-title":"Water Permeability\nand Mechanical Strength of Polyunsaturated Lipid Bilayers","volume":"79","author":"Olbrich","year":"2000","journal-title":"Biophys. J."},{"key":"2026090110235885100_cit20","doi-asserted-by":"publisher","first-page":"527","DOI":"10.1016\/j.tcb.2012.07.005","article-title":"Mechanical Feedback\nbetween Membrane\nTension and Dynamics","volume":"22","author":"Gauthier","year":"2012","journal-title":"Trends Cell Biol."},{"key":"2026090110235885100_cit21","doi-asserted-by":"publisher","first-page":"47","DOI":"10.1016\/j.tcb.2012.09.006","article-title":"Use the\nForce: Membrane Tension as\nan Organizer of Cell Shape and Motility","volume":"23","author":"Diz-Mun\u0303oz","year":"2013","journal-title":"Trends\nCell Biol."},{"key":"2026090110235885100_cit22","doi-asserted-by":"publisher","first-page":"305","DOI":"10.1039\/C2FD20105D","article-title":"Spontaneous\nTubulation of Membranes and Vesicles Reveals Membrane Tension Generated\nby Spontaneous Curvature","volume":"161","author":"Lipowsky","year":"2013","journal-title":"Faraday Discuss."},{"key":"2026090110235885100_cit23","doi-asserted-by":"publisher","first-page":"4731","DOI":"10.1073\/pnas.1015892108","article-title":"Membrane Nanotubes\nInduced by Aqueous\nPhase Separation and Stabilized by Spontaneous Curvature","volume":"108","author":"Li","year":"2011","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"2026090110235885100_cit24","doi-asserted-by":"publisher","first-page":"1824","DOI":"10.1007\/s12035-015-9136-z","article-title":"GM1 Ganglioside: Past Studies and\nFuture Potential","volume":"53","author":"Aureli","year":"2016","journal-title":"Mol. Neurobiol."},{"key":"2026090110235885100_cit25","doi-asserted-by":"publisher","first-page":"397","DOI":"10.1016\/j.tibs.2015.03.007","article-title":"Gangliosides:\nGlycosphingolipids Essential for Normal Neural Development and Function","volume":"40","author":"Schengrund","year":"2015","journal-title":"Trends Biochem. Sci."},{"key":"2026090110235885100_cit26","doi-asserted-by":"publisher","first-page":"11","DOI":"10.1038\/ncb1999","article-title":"GM1 Structure Determines SV40-Induced\nMembraneInvagination and Infection","volume":"12","author":"Ewers","year":"2010","journal-title":"Nat. Cell\nBiol."},{"key":"2026090110235885100_cit27","doi-asserted-by":"publisher","first-page":"9558","DOI":"10.1021\/acsnano.7b05542","article-title":"Formation\nand Stability of Lipid Membrane Nanotubes","volume":"11","author":"Bahrami","year":"2017","journal-title":"ACS\nNano"},{"key":"2026090110235885100_cit28","doi-asserted-by":"publisher","first-page":"303","DOI":"10.1039\/dc9868100303","article-title":"Liposome Electroformation","volume":"81","author":"Angelova","year":"1986","journal-title":"Faraday\nDiscuss. Chem. Soc."},{"key":"2026090110235885100_cit29","doi-asserted-by":"publisher","first-page":"1935","DOI":"10.1016\/j.bpj.2016.09.028","article-title":"GM1 Softens POPC Membranes and Induces the Formation\nof Micron-Sized Domains","volume":"111","author":"Fricke","year":"2016","journal-title":"Biophys. J."},{"key":"2026090110235885100_cit30","doi-asserted-by":"publisher","first-page":"693","DOI":"10.1515\/znc-1973-11-1209","article-title":"Elastic Properties\nof Lipid Bilayers: Theory and Possible Experiments","volume":"28","author":"Helfrich","year":"1973","journal-title":"Z. Naturforsch., C: J. Biosci."},{"key":"2026090110235885100_cit31","doi-asserted-by":"publisher","first-page":"1182","DOI":"10.1103\/PhysRevA.44.1182","article-title":"Shape Transformations\nof Vesicles:\nPhase Diagram for Spontaneous Curvature and Bilayer Coupling Model","volume":"44","author":"Seifert","year":"1991","journal-title":"Phys. Rev. A: At., Mol., Opt. Phys."},{"key":"2026090110235885100_cit32","doi-asserted-by":"publisher","first-page":"115","DOI":"10.1016\/S0006-3495(64)86773-4","article-title":"Mechanical Properties\nof the Red Cell Membrane I. Membrane\nStiffness and Intracellular Pressure","volume":"4","author":"Rand","year":"1964","journal-title":"Biophys.\nJ."},{"key":"2026090110235885100_cit33","doi-asserted-by":"publisher","first-page":"15","DOI":"10.1016\/S0021-9290(99)00175-X","article-title":"Micropipette\nAspiration of Living Cells","volume":"33","author":"Hochmuth","year":"2000","journal-title":"J. Biomech."},{"key":"2026090110235885100_cit34","doi-asserted-by":"publisher","first-page":"012805","DOI":"10.1103\/PhysRevE.95.012805","article-title":"Mechanical Stability\nof Particle-Stabilized Droplets under Micropipette Aspiration","volume":"95","author":"Samudrala","year":"2017","journal-title":"Phys. Rev. E: Stat. Phys., Plasmas, Fluids, Relat. Interdiscip.\nTop."},{"key":"2026090110235885100_cit35","doi-asserted-by":"publisher","first-page":"151","DOI":"10.1016\/S0006-3495(89)82660-8","article-title":"Apparent Viscosity\nand Cortical Tension of Blood Granulocytes Determined\nby Micropipet Aspiration","volume":"56","author":"Evans","year":"1989","journal-title":"Biophys. J."},{"key":"2026090110235885100_cit36","doi-asserted-by":"publisher","first-page":"18581","DOI":"10.1073\/pnas.0903353106","article-title":"Role of Cortical Tension\nin Bleb Growth","volume":"106","author":"Tinevez","year":"2009","journal-title":"Proc. Natl. Acad. Sci. U. S.\nA."},{"key":"2026090110235885100_cit37","doi-asserted-by":"publisher","first-page":"2155","DOI":"10.1039\/C6SM02796B","article-title":"Uniform and Janus-Like Nanoparticles in Contact with\nVesicles: Energy Landscapes and Curvature-Induced Forces","volume":"13","author":"Agudo-Canalejo","year":"2017","journal-title":"Soft Matter"},{"key":"2026090110235885100_cit38","doi-asserted-by":"publisher","first-page":"113","DOI":"10.1002\/anie.198801131","article-title":"Molecular Architecture and Function\nof Polymeric Oriented Systems: Models for the Study of Organization,\nSurface Recognition, and Dynamics of Biomembranes","volume":"27","author":"Ringsdorf","year":"1988","journal-title":"Angew. Chem., Int. Ed. Engl."},{"key":"2026090110235885100_cit39","doi-asserted-by":"publisher","first-page":"997","DOI":"10.1016\/S0006-3495(90)82444-9","article-title":"Elastic Deformation\nand Failure of Lipid Bilayer Membranes\nContaining Cholesterol","volume":"58","author":"Needham","year":"1990","journal-title":"Biophys. J."},{"key":"2026090110235885100_cit40","doi-asserted-by":"publisher","first-page":"1143","DOI":"10.1126\/science.284.5417.1143","article-title":"Polymersomes:\nTough Vesicles Made\nfrom Diblock Copolymers","volume":"284","author":"Discher","year":"1999","journal-title":"Science"},{"key":"2026090110235885100_cit41","doi-asserted-by":"publisher","first-page":"7254","DOI":"10.1021\/nn302367m","article-title":"Incorporation of Nanoparticles\ninto Polymersomes: Size and Concentration Effects","volume":"6","author":"Jaskiewicz","year":"2012","journal-title":"ACS Nano"},{"key":"2026090110235885100_cit42","doi-asserted-by":"publisher","first-page":"241","DOI":"10.1140\/epje\/i200101032","article-title":"Hyperviscous Diblock Copolymer Vesicles","volume":"7","author":"Dimova","year":"2002","journal-title":"Eur. Phys. J. E: Soft Matter Biol. Phys."},{"key":"2026090110235885100_cit43","doi-asserted-by":"publisher","first-page":"328","DOI":"10.1073\/pnas.1609142114","article-title":"Whole-GUV Patch-Clamping","volume":"114","author":"Garten","year":"2017","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"2026090110235885100_cit44","doi-asserted-by":"publisher","first-page":"025004","DOI":"10.1088\/1367-2630\/13\/2\/025004","article-title":"Effect of the HIV-1 Fusion Peptide\non the Mechanical Properties and Leaflet Coupling of Lipid Bilayers","volume":"13","author":"Shchelokovskyy","year":"2011","journal-title":"New J. Phys."}],"container-title":["ACS Nano"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/pubs.acs.org\/doi\/pdf\/10.1021\/acsnano.8b00640","content-type":"application\/pdf","content-version":"vor","intended-application":"unspecified"},{"URL":"https:\/\/pubs.acs.org\/ancac3\/article-pdf\/12\/5\/4478\/67457260\/acsnano.8b00640.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/pubs.acs.org\/ancac3\/article-pdf\/12\/5\/4478\/67457260\/acsnano.8b00640.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,9,1]],"date-time":"2026-09-01T14:53:30Z","timestamp":1788274410000},"score":1,"resource":{"primary":{"URL":"https:\/\/pubs.acs.org\/ancac3\/article\/12\/5\/4478\/745791\/Membrane-Nanotubes-Increase-the-Robustness-of"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2018,4,16]]},"references-count":44,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2018,4,16]]},"published-print":{"date-parts":[[2018,5,22]]}},"URL":"https:\/\/doi.org\/10.1021\/acsnano.8b00640","relation":{},"ISSN":["1936-0851","1936-086X"],"issn-type":[{"value":"1936-0851","type":"print"},{"value":"1936-086X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2018,4,16]]}}}