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Double-emulsion templated lipid vesicles as minimal cell mimics for assembling tissue-like vesicular materials

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Abstract

Lipid vesicles formed using double-emulsion drops as templates exhibit uniform sizes and compositions. Despite these important advantages, conventional electroformation continues to be the selected approach for vesicle fabrication to understand biophysical processes in cells using simplified model systems. Here, we address critical aspects that could be hindering the extensive use of emulsion-templating strategies for vesicle fabrication and emphasize certain systematic studies that would help demonstrate further the advantages of microfluidic technologies. Besides the importance of controlling size and composition, we envision that the high throughput of this technology will allow the construction of vesicular materials with controlled architectures.

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Abbreviations

CAM:

Cell adhesion molecule

DOPC:

1,2-Dioleoyl-sn-glycero-3-phosphocholine

DPPC:

1,2-Dipalmitoyl-sn-glycero-3-phosphocholine

DOPE-biotinyl:

1,2-Dioleoyl-sn-glycero-3-phosphoethanolamine-N-(biotinyl) (sodium salt)

IVTT:

In vitro Transcription-translation

RICM:

Reflection interference contrast microscopy

W/O:

Water-in-oil

W/O/W:

Water-in-oil-in-water

W/O/O/W:

Water-in-oil-in-oil-in-water

References

  1. D. Perrais, C.J. Merrifield, Dynamics of endocytic vesicle creation. Dev. Cell 9, 581–592 (2005)

    Article  CAS  Google Scholar 

  2. A. Spang, The life cycle of a transport vesicle. Cell. Mol. Life Sci. 65, 2781–2789 (2008)

    Article  CAS  Google Scholar 

  3. G. Raposo, P.D. Stahl, Extracellular vesicles: a new communication paradigm? Nat. Rev. Mol. Cell. Biol. 20, 509–510 (2019)

    Article  CAS  Google Scholar 

  4. R. van der Meel, M.H.A.M. Fens, P. Vader, W.W. van Solinge, O. Eniola-Adefeso, R.M. Schiffelers, Extracellular vesicles as drug delivery systems: lessons from the liposome field. J. Control. Release 195, 72–85 (2014)

    Article  Google Scholar 

  5. M.I. Angelova, D.S. Dimitrov, Liposome electroformation. Faraday Discuss. Chem. Soc. 81, 303–311 (1986)

    Article  CAS  Google Scholar 

  6. C. Martino, A.J. deMello, Droplet-based microfluidics for artificial cell generation: a brief review. Interface Focus 6, 20160011 (2016)

    Article  Google Scholar 

  7. Y. Huang, S.-H. Kim, L.R. Arriaga, Emulsion templated vesicles with symmetric or asymmetric membranes. Adv. Colloid Interface Sci. 247, 413–425 (2017)

    Article  CAS  Google Scholar 

  8. K. Kamiya, Development of artificial cell models using microfluidic technology and synthetic biology. Micromachines 11, 559 (2020)

    Article  Google Scholar 

  9. L.R. Arriaga, S.S. Datta, S.-H. Kim, E. Amstad, T.E. Kodger, F. Monroy, D.A. Weitz, Ultra-thin shell double emulsion templated giant unilamellar lipid vesicles with controlled microdomain formation. Small 10, 950–956 (2014)

    Article  CAS  Google Scholar 

  10. S.-H. Kim, J.W. Kim, J.-C. Cho, D.A. Weitz, Double-emulsion drops with ultra-thin shells for capsule templates. Lab Chip 11, 3162–3166 (2011)

    Article  CAS  Google Scholar 

  11. L.R. Arriaga, E. Amstad, D.A. Weitz, Scalable single-step microfluidic production of single-core double emulsions with ultra-thin shells. Lab Chip 15, 3335–3340 (2015)

    Article  CAS  Google Scholar 

  12. M. Michelon, Y. Huang, L. Gaziola de la Torre, D.A. Weitz, R. Lopes Cunha, Single-step microfluidic production of W/O/W double emulsions as templates for β-carotene loaded giant liposomes formation. Chem. Eng. J. 336, 27–32 (2019)

    Article  Google Scholar 

  13. S.-Y. The, R. Khnouf, H. Fan, A.P. Lee, Stable, biocompatible lipid vesicle generation by solvent extraction-based droplet microfluidics. Biomicrofluidics 5, 044113 (2011)

    Article  Google Scholar 

  14. L.R. Arriaga, Y. Huang, S.-H. Kim, J.L. Aragones, R. Ziblat, S.A. Koehler, D.A. Weitz, Single-step assembly of asymmetric vesicles. Lab Chip 19, 749–756 (2019)

    Article  CAS  Google Scholar 

  15. A.G. Ayuyan, F.S. Cohen, Lipid peroxides promote large rafts: Effects of excitation of probes in fluorescence microscopy and electrochemical reactions during vesicle formation. Biophys. J. 91, 2172–2183 (2006)

    Article  CAS  Google Scholar 

  16. J. Steinkuhler, P. De Tillieux, R.L. Knorr, R. Lipowsky, R. Dimova, Charged giant unilamellar vesicles prepared by electroformation exhibit nanotubes and transbilayer lipid asymmetry. Sci. Rep. 8, 11838 (2018)

    Article  Google Scholar 

  17. C. Tanford, The Hydrophobic Effect: Formation of Micelles and Biological Membranes (Wiley, New York, 1973).

    Google Scholar 

  18. E.E. Meyer, K.J. Rosenberg, J. Israelachvili, Recent progress in understanding hydrophobic interactions. Proc. Natl Acad. Sci. U.S.A. 103, 15739–15746 (2006)

    Article  CAS  Google Scholar 

  19. R. Lipowsky, E. Sackmann, Structure and dynamics of membranes: from cells to vesicles, in Handbook of Biological Physics (Elsevier, Amsterdam, 1995)

  20. G. van Meer, D.R. Voelker, G.W. Feigenson, Membrane lipids: where they are and how they behave. Nat. Rev. Mol. Cell. Biol. 9, 112–124 (2008)

    Article  Google Scholar 

  21. S.L. Veatch, S.L. Keller, Seeing spots: complex phase behavior in simple membranes. Biochim. Biophys. Acta Mol. Cell Res. 1746, 172–185 (2005)

    Article  CAS  Google Scholar 

  22. J.H. Ipsen, K. Jørgensen, O.G. Mouritsen, Density fluctuations in saturated phospholipid bilayers increase as the acyl-chain length decreases. Biophys J. 58, 1099–1107 (1990)

    Article  CAS  Google Scholar 

  23. L.A. Bagatolli, E. Gratton, Two photon fluorescence microscopy of coexisting lipid domains in giant unilamellar vesicles of binary phospholipid mixtures. Biophys. J. 78, 290–305 (2000)

    Article  CAS  Google Scholar 

  24. R.F.M. de Almeida, A. Fedorov, M. Prieto, Sphingomyelin/phosphatidylcholine/cholesterol phase diagram: boundaries and composition of lipid rafts. Biophys. J. 85, 2406–2416 (2003)

    Article  Google Scholar 

  25. J. Perrotton, R. Ahijado-Guzman, L.H. Moleiro, B. Tinao, A. Guerrero-Martinez, E. Amstad, F. Monroy, L.R. Arriaga, Microfluidic fabrication of vesicles with hybrid lipid/nanoparticle bilayer membranes. Soft Matter 15, 1388–1395 (2019)

    Article  CAS  Google Scholar 

  26. P. Husen, L.R. Arriaga, F. Monroy, J.H. Ipsen, L.A. Bagatolli, Morphometric image analysis of giant vesicles: a new tool for quantitative thermodynamics studies of phase separation in lipid membranes. Biophys. J. 103, 2304–2310 (2012)

    Article  CAS  Google Scholar 

  27. E. Sezgin, P. Schwille, Fluorescence techniques to study lipid dynamics. Cold Spring Harb. Perspect. Biol. 3, a009803 (2011)

    Google Scholar 

  28. K. Simons, E. Ikonen, Functional rafts in cell membranes. Nature 387, 569–572 (1997)

    Article  CAS  Google Scholar 

  29. F.D. Ferguson, T.K. Jones, The Phase Rule (Butterworth and Co., London, 1966).

    Google Scholar 

  30. K. Simons, J.L. Sampaio, Membrane organization and lipid rafts. Cold Spring Harb. Perspect. Biol. 3, a004697 (2011)

    Article  Google Scholar 

  31. N. Kahya, E.-I. Pecheur, W.P. de Boeij, D.A. Wiersma, D. Hoekstra, Reconstitution of membrane proteins into giant unilamellar vesicles via peptide-induced fusion. Biophys. J. 81, 1464–1474 (2001)

    Article  CAS  Google Scholar 

  32. J.-B. Manneville, P. Bassereau, S. Ramaswamy, J. Prost, Active membrane fluctuations studied by micropipet aspiration. Phys. Rev. E 64, 021908 (2001)

    Article  CAS  Google Scholar 

  33. P. Girard, J. Pécréaux, G. Lenoir, P. Falson, J.-L. Rigaud, P. Bassereau, A new method for the reconstitution of membrane proteins into giant unilamellar vesicles. Biophys. J. 87, 419–429 (2004)

    Article  CAS  Google Scholar 

  34. K. Karamdad, R.V. Law, J.M. Seddon, N.J. Brooks, O. Ces, Preparation and mechanical characterisation of giant unilamellar vesicles by a microfluidic method. Lab Chip 15, 557–562 (2015)

    Article  CAS  Google Scholar 

  35. V. Romanov, J. McCullough, B.K. Gale, A. Frost, A tunable microfluidic device enables cargo encapsulation by cell- or organelle-sized lipid vesicles comprising asymmetric lipid bilayers. Adv. Biosyst. 3, 1900010 (2019)

    Article  Google Scholar 

  36. R. Cochereau, D. Renard, C. Noûs, A. Boire, Semi-permeable vesicles produced by microfluidics to tune the phase behaviour of encapsulated macromolecules. J. Colloid Interface Sci. 580, 709–719 (2020)

    Article  CAS  Google Scholar 

  37. F. Katzen, T.C. Peterson, W. Kudlicki, Membrane protein expression: no cells required. Trends Biotechnol. 27, 455–460 (2009)

    Article  CAS  Google Scholar 

  38. N. Shadiac, Y. Nagarajan, S. Waters, M. Hrmova, Close allies in membrane protein research: cell-free synthesis and nanotechnology. Mol. Membr. Biol. 30, 229–245 (2013)

    Article  CAS  Google Scholar 

  39. F. Junge, B. Schneider, S. Reckel, D. Schwarz, V. Dotsch, F. Bernhard, Large-scale production of functional membrane proteins. Cell Mol. Life Sci. 65, 1729–1755 (2008)

    Article  CAS  Google Scholar 

  40. C. Martino, S.-H. Kim, L. Horsfall, A. Abbaspourrad, S.J. Rosser, J. Cooper, D.A. Weitz, Protein expression, aggregation, and triggered release from polymersomes as artificial cell-like structures. Angew. Chem. Int. Ed. 51, 6416–6420 (2012)

    Article  CAS  Google Scholar 

  41. P.J. Yunker, H. Asahara, K.-C. Hung, C. Landry, L.R. Arriaga, I. Akartuna, S. Chong, D.A. Weitz, One-pot system for synthesis, assembly, and display of functional single-span membrane proteins on oil-water interfaces. Proc. Natl Acad. Sci. U.S.A. 113, 608–613 (2015)

    Article  Google Scholar 

  42. J. Pérez-Gil, A. Cruz, C. Casals, Solubility of hydrophobic surfactant proteins in organic solvent/water mixtures. Structural studies on SP-B and SP-C in aqueous organic solvents and lipids. Biochim. Biophys. Acta 1168, 261–270 (1993)

    Article  Google Scholar 

  43. J. Bernardino de la Serna, J. Perez-Gil, A.C. Simonsen, L.A. Bagatolli, Cholesterol rules: direct observation of the coexistence of two fluid phases in native pulmonary surfactant membranes at physiological temperatures. J. Biol. Chem. 279, 40715–40722 (2004)

    Article  Google Scholar 

  44. G. van Meer, Dynamic transbilayer lipid asymmetry. Cold Spring Harb. Perspect. Biol. 3, a004671 (2011)

    Google Scholar 

  45. S. Pautot, B.J. Frisken, D.A. Weitz, Engineering asymmetric vesicles. Proc. Natl. Acad. Sci. U.S.A. 100, 10718–10721 (2003)

    Article  CAS  Google Scholar 

  46. P.C. Hu, S. Li, N. Malmstadt, Microfluidic fabrication of asymmetric giant vesicles. ACS Appl. Mater. Interfaces 3, 1434–1440 (2011)

    Article  CAS  Google Scholar 

  47. K. Nishimura, H. Suzuki, T. Toyota, T. Yomo, Size control of giant unilamellar vesicles prepared from inverted emulsions. J. Colloid Interface Sci. 376, 119–125 (2012)

    Article  CAS  Google Scholar 

  48. S. Matosevic, B.M. Paegel, Layer-by-layer cell membrane assembly. Nat. Chem. 5, 958–963 (2013)

    Article  CAS  Google Scholar 

  49. L. Lu, J.W. Schertzer, P.R. Chiarot, Continuous microfluidic fabrication of synthetic asymmetric vesicles. Lab Chip 15, 3591–3599 (2015)

    Article  CAS  Google Scholar 

  50. K. Karamdad, R.V. Law, J.M. Seddon, N.J. Brooks, O. Ces, Studying the effects of asymmetry on the bending rigidity of lipid membranes formed by microfluidics. Chem. Commun. 52, 5277–5280 (2016)

    Article  CAS  Google Scholar 

  51. F.X. Contreras, L. Sánchez-Magraner, A. Alonso, F.M. Goñi, Transbilayer (flip-flop) lipid motion and lipid scrambling in membranes. FEBS Lett. 584, 1779–1786 (2010)

    Article  CAS  Google Scholar 

  52. S. Garg, J. Rühe, K. Lüdtke, R. Jordan, C.A. Naumann, Domain registration in raft-mimicking lipid mixtures studied using polymer-tethered lipid bilayers. Biophys. J. 92, 1263–1270 (2007)

    Article  CAS  Google Scholar 

  53. M.C. Blosser, A.R. Honerkamp-Smith, T. Han, M. Haataja, S.L. Keller, Transbilayer colocalization of lipid domains explained via measurement of strong coupling parameters. Biophys. J. 109, 2317–2327 (2015)

    Article  CAS  Google Scholar 

  54. M.D. Collins, S.L. Keller, Tuning lipid mixtures to induce or suppress domain formation across leaflets of unsupported asymmetric bilayers. Proc. Natl. Acad. Sci. U.S.A. 105, 124–128 (2008)

    Article  CAS  Google Scholar 

  55. N.P. Kamat, M.H. Lee, D. Lee, D.A. Hammer, Micropipette aspiration of double-emulsion templated polymersomes. Soft Matter 7, 9863–9866 (2011)

    Article  CAS  Google Scholar 

  56. S.-H. Kim, J. Nam, J.W. Kim, D.-H. Kim, S.-H. Han, D.A. Weitz, Formation of polymersomes with double bilayers templated by quadruple emulsions. Lab Chip 13, 1351–1356 (2013)

    Article  CAS  Google Scholar 

  57. S. Maktabi, J.W. Schertzer, P.R. Chiarot, Dewetting-induced formation and mechanical properties of synthetic bacterial outer membrane models (GUVs) with controlled inner-leaflet lipid composition. Soft Matter 15, 3938–3948 (2019)

    Article  CAS  Google Scholar 

  58. J. Drazenovic, H. Wang, K. Roth, J. Zhang, S. Ahmed, Y. Chen, G. Bothun, S.L. Wunder, Effect of lamellarity and size on calorimetric phase transitions in single component phosphatidylcholine vesicles. Biochim Biophys. Acta 1848, 532–543 (2015)

    Article  CAS  Google Scholar 

  59. M.A. Tahir, Z.P. Guven, L.R. Arriaga, B. Tinao, Y.-S.S. Yang, A. Bekdemir, J.T. Martin, A.N. Bhanji, D. Irvine, F. Stellacci, A. Alexander-Katz, Calcium-triggered fusion of lipid membranes is enabled by amphiphilic nanoparticles. Proc. Natl. Acad. Sci. U.S.A. 117, 18470–18476 (2020)

    Article  CAS  Google Scholar 

  60. H.G. Dobereiner, J. Kas, D. Noppl, I. Sprenger, E. Sackmann, Budding and fission of vesicles. Biophys. J. 65, 1396–1403 (1993)

    Article  CAS  Google Scholar 

  61. S. Deshpande, W.K. Spoelstra, M. van Doorn, J. Kerssemakers, C. Dekker, Mechanical division of cell-sized liposomes. ACS Nano 12, 2560–2568 (2018)

    Article  CAS  Google Scholar 

  62. Y. Matsushita-Ishiodori, M.M. Hanczync, A. Wang, J.W. Szostak, T. Yomo, Using imaging flow cytometry to quantify and optimize giant vesicle production by water-in-oil emulsion transfer methods. Langmuir 35, 2375–2382 (2019)

    Article  CAS  Google Scholar 

  63. K. Nishimura, T. Matsuura, K. Nishimura, T. Sunami, H. Suzuki, T. Yomo, Cell-free protein synthesis inside giant unilamellar vesicles analyzed by flow cytometry. Langmuir 28, 8426–8432 (2012)

    Article  CAS  Google Scholar 

  64. J. Ovadi, V. Saks, On the origin of intracellular compartmentation and organized metabolic systems. Mol. Cell. Biochem. 256(257), 5–12 (2004)

    Article  Google Scholar 

  65. C.D. Keating, Aqueous phase separations as a possible route to compartmentalization of biological molecules. Acc. Chem. Res. 45, 2114–2124 (2012)

    Article  CAS  Google Scholar 

  66. Y. Li, R. Lipowsky, R. Dimova, Membrane nanotubes induced by aqueous phase separation and stabilized by spontaneous curvature. Proc. Natl. Acad. Sci. U.S.A. 108, 4731–4736 (2011)

    Article  CAS  Google Scholar 

  67. M.S. Long, C.D. Jones, M.R. Helfrich, L.K. Mangeney-Slavin, C.D. Keating, Dynamic microcompartmentation in synthetic cells. Proc. Natl. Acad. Sci. U.S.A. 102, 5920–5925 (2005)

    Article  CAS  Google Scholar 

  68. M. Andes-Koback, C.D. Keating, Complete budding and asymmetric division of primitive model cells to produce daughter vesicles with different interior and membrane compositions. J. Am. Chem. Soc. 133, 9545–9555 (2011)

    Article  CAS  Google Scholar 

  69. Y. Li, R. Lipowsky, R. Dimova, Transition from complete to partial wetting within membrane compartments. J. Am. Chem. Soc. 130, 12252–12253 (2008)

    Article  CAS  Google Scholar 

  70. M.S. Long, A.-S. Cans, C.D. Keating, Budding and asymmetric protein microcompartmentation in giant vesicles containing two aqueous phases. J. Am. Chem. Soc. 130, 756–762 (2008)

    Article  CAS  Google Scholar 

  71. J. Fels, S.N. Orlov, R. Grygorczyk, The hydrogel nature of mammalian cytoplasm contributes to osmosensing and extracellular pH sensing. Biophys. J. 96, 4276–4285 (2009)

    Article  CAS  Google Scholar 

  72. S.-H. Kim, J.W. Kim, D.H. Kim, S.H. Han, D.A. Weitz, Polymersomes containing a hydrogel network for high stability and controlled release. Small 9, 124–131 (2013)

    Article  CAS  Google Scholar 

  73. C. Martino, T.Y. Lee, S.-H. Kim, A.J. DeMello, Microfluidic generation of PEG-b-PLA polymersomes containing alginate-based core hydrogel. Biomicrofluidics 9, 024101 (2015)

    Article  Google Scholar 

  74. G.C.R. Ellis-Davies, Useful caged compounds for cell physiology. Acc. Chem. Res. 53, 1593–1604 (2020)

    Article  CAS  Google Scholar 

  75. P. Hess, J.B. Lansman, R.W. Tsien, Calcium channel selectivity for divalent and monovalent cations. J. Gen. Phys. 88, 293–319 (1986)

    Article  CAS  Google Scholar 

  76. D. Bruggemann, J.P. Frohnmayer, J.P. Spatz, Model systems for studying cell adhesion and biomimetic actin networks. Beilstein J. Nanotechnol. 5, 1193–1202 (2014)

    Article  Google Scholar 

  77. A.P. Liu, D.L. Richmond, L. Maibaum, S. Pronk, P.L. Geissler, D.A. Fletcher, Membrane-induced bundling of actin filaments. Nat. Phys. 4, 789–793 (2008)

    Article  CAS  Google Scholar 

  78. F.-C. Tsai, B. Stuhrmann, G.H. Koenderink, Encapsulation of active cytoskeletal protein networks in cell-sized liposomes. Langmuir 27, 10061–10071 (2011)

    Article  CAS  Google Scholar 

  79. S. Kaufmann, J. Käs, W.H. Goldmann, E. Sackmann, G. Isenberg, Talin anchors and nucleates actin filaments at lipid membranes. FEBS Lett. 314, 203–205 (1992)

    Article  CAS  Google Scholar 

  80. H. Heise, T. Bayerl, G. Isenberg, E. Sackmann, Human platelet P-235, a talin-like actin binding protein, binds selectively to mixed lipid bilayers. Biochim. Biophys. Acta 1061, 121–131 (1991)

    Article  CAS  Google Scholar 

  81. R. Rodríguez-García, V.A. Volkov, C.-Y. Chen, E.A. Katrukha, N. Olieric, A. Aher, I. Grigoriev, M. Preciado López, M.O. Steinmetz, L.C. Kapitein, G. Koenderink, M. Dogterom, A. Akhmanova, Mechanisms of motor-independent membrane remodeling driven by dynamic microtubules. Curr. Biol. 30, 972–987 (2020)

    Article  Google Scholar 

  82. M. Hayashi, M. Nishiyama, Y. Kazayama, T. Toyota, Y. Harada, K. Takiguchi, Reversible morphological control of tubulin-encapsulating giant liposomes by hydrostatic pressure. Langmuir 32, 3794–3802 (2016)

    Article  Google Scholar 

  83. A. Doostmohammadi, J. Ignés-Mullol, J.M. Yeomans, F. Sagués, Active nematics. Nat. Commun. 9, 3246 (2018)

    Article  Google Scholar 

  84. R. Omidvar, W. Romer, Glycan-decorated protocells: novel features for rebuilding cellular processes. Interface Focus 9, 20180084 (2019)

    Article  Google Scholar 

  85. A. Huerre, V. Miralles, M.G. Jullien, Bubbles and foams in microfludics. Soft Matter 10, 6888–6902 (2014)

    Article  CAS  Google Scholar 

  86. G. Villar, A.D. Graham, H. Bayley, A tissue-like printed material. Science 340, 48–52 (2013)

    Article  CAS  Google Scholar 

  87. Q. Li, S. Li, X. Zhang, W. Xu, X. Han, Programmed magnetic manipulation of vesicles into spatially coded prototissue architectures arrays. Nat. Commun. 11, 232 (2020)

    Article  CAS  Google Scholar 

  88. H. Jin, Y. Zheng, Y. Liu, H. Cheng, Y. Zhou, D. Yan, Reversible and large-scale cytomimetic vesicle aggregation: light-responsive host-guest interactions. Angew. Chem. Int. Ed. 50, 10352–10356 (2011)

    Article  CAS  Google Scholar 

  89. P. Gobbo, A.J. Patil, M. Li, R. Harniman, W.H. Briscoe, S. Mann, Programmed assembly of synthetic protocells into thermoresponsive prototissues. Nat. Mater. 17, 1145–1153 (2018)

    Article  CAS  Google Scholar 

  90. P.H. Puech, H. Feracci, F. Brochard-Wyart, Adhesion between giant vesicles and supported bilayers decorated with chelated E-cadherin fragments. Langmuir 20, 9763–9768 (2009)

    Article  Google Scholar 

  91. S.F. Fenz, R. Merkel, K. Sengupta, Diffussion and intermembrane distance: case study of avidin and E-cadherin mediated adhesion. Langmuir 25, 1074–1085 (2009)

    Article  CAS  Google Scholar 

  92. P. Carrara, P. Stano, P.L. Luisi, Giant vesicles ‘colonies’: a model for primitive cell communities. ChemBioChem 13, 1497–1502 (2012)

    Article  CAS  Google Scholar 

  93. T.P. De Souza, G.V. Bossa, P. Stano, F. Steiniger, S. May, P.L. Luisi, A. Fahr, Vesicle aggregates as a model for primitive cellular assemblies. Phys. Chem. Chem. Phys. 19, 20082–20092 (2017)

    Article  Google Scholar 

  94. S. Villringer, J. Madl, T. Sych, C. Manner, A. Imberty, Lectin-mediated protocell crosslinking to mimic cell–cell junctions and adhesion. Sci. Rep. 8, 1932 (2018)

    Article  Google Scholar 

  95. J.P. Ribeiro, S. Villringer, D. Goyard, L. Coche-Guerente, M. Hoferlin, O. Renaudet, W. Romer, A. Imberty, Tailor-made Janus lectin with dual avidity assembles glycoconjugate multilayers and crosslinks protocells. Chem. Sci. 9, 7634–7641 (2018)

    Article  CAS  Google Scholar 

  96. S. Michaud, R. Marin, J.T. Westwood, R.M. Tanguay, The tail of integrin activation. Trends Biochem. Sci. 36, 191–198 (2011)

    Article  Google Scholar 

  97. A. Huttlenlocher, R.R. Sandborg, A.F. Horwitz, Adhesion in cell migration. Curr. Opin. Cell Biol. 7, 697–706 (1995)

    Article  Google Scholar 

  98. P. Streicher, P. Nassoy, M. Barmann, A. Dif, V. Marchi-Artzner, F. Brochard-Wyart, J. Spatz, P. Bassereau, Integrin reconstituted in GUVs: a biomimetic system to study initial steps of cell spreading. Biochim. Biophys. Acta Biomembr. 1788, 2291–2300 (2009)

    Article  CAS  Google Scholar 

  99. V. Gaul, S.G. Lopez, B.R. Lentz, N. Moran, R.J. Forster, T.E. Keyes, The lateral diffusion and fibrinogen induced clustering of platelet integrin αIIbβ3 reconstituted into physiologically mimetic GUVs. Integr. Biol. 7, 402–411 (2015)

    Article  CAS  Google Scholar 

  100. B. Herranz-Blanco, L.R. Arriaga, E. Makila, A. Correia, N. Shrestha, S. Mirza, D.A. Weitz, J. Salonen, J. Hirvonen, H.A. Santos, Microfluidic assembly of multistage porous silicon-lipid vesicles for controlled drug release. Lab Chip 14, 1083–1086 (2014)

    Article  CAS  Google Scholar 

  101. K. Gopfrich, B. Haller, O. Staufer, Y. Dreher, U. Mersdorf, I. Platzman, J.P. Spatz, One-pot assembly of complex giant unilamellar vesicle-based synthetic cells. ACS Synth. Biol. 8, 937–947 (2019)

    Article  Google Scholar 

  102. Y. Elani, R.V. Law, O. Ces, Vesicle-based artificial cells as chemical microreactors with spatially segregated reaction pathways. Nat. Commun. 5, 5305 (2014)

    Article  CAS  Google Scholar 

  103. H.H. Zepik, P. Walde, E.L. Kostoryz, J. Code, D.M. Yourtee, Lipid vesicles as membrane models for toxicological assessment of xenobiotics. Crit. Rev. Toxicol. 38, 1–11 (2008)

    Article  CAS  Google Scholar 

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Acknowledgments

LRA and JLA acknowledge financial support from the Spanish Ministry of Science and Innovation (MCI), through the María de Maeztu Programme for Units of Excellence in R&D (CEX2018-000805-M), and through the project (RTI2018-101953-A-I00; MCI/AEI/FEDER, UE). LRA also acknowledges financial support from MCI through the Ramón y Cajal Programme (RYC2018-025575-I; MCI/AEI/FSE, UE).

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Tinao, B., Magrinya, P., Aragones, J.L. et al. Double-emulsion templated lipid vesicles as minimal cell mimics for assembling tissue-like vesicular materials. MRS Communications 11, 18–30 (2021). https://doi.org/10.1557/s43579-020-00002-y

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