Budding-like division of all-aqueous emulsion droplets modulated by networks of protein nanofibrils

Networks of natural protein nanofibrils, such as cytoskeletal filaments, control the shape and the division of cells, yet mimicking this functionality in a synthetic setting has proved challenging. Here, we demonstrate that artificial networks of protein nanofibrils can induce controlled deformation and division of all-aqueous emulsion droplets with budding-like morphologies. We show that this process is driven by the difference in the immersional wetting energy of the nanofibril network, and that both the size and the number of the daughter droplets formed during division can be controlled by modulating the fibril concentration and the chemical properties of the fibril network. Our results demonstrate a route for achieving biomimetic division with synthetic self-assembling fibrils and offer an engineered approach to regulate the morphology of protein gels.The cytoskeleton, a network of fibrils, controls how cells divide. Here, the authors show that synthetic protein fibrils added to an emulsion can control the division of droplets and that this method can be used to control the morphology of microparticles during biomaterial preparation.

[1]  Petra Schwille,et al.  Ceramide Triggers Budding of Exosome Vesicles into Multivesicular Endosomes , 2008, Science.

[2]  M. Textor,et al.  Differential regulation of osteogenic differentiation of stem cells on surface roughness gradients. , 2014, Biomaterials.

[3]  R. Hayward,et al.  Hierarchically structured microparticles formed by interfacial instabilities of emulsion droplets containing amphiphilic block copolymers. , 2008, Angewandte Chemie.

[4]  Daniel A. Fletcher,et al.  Cell mechanics and the cytoskeleton , 2010, Nature.

[5]  R. Tannenbaum,et al.  The effects of combined micron-/submicron-scale surface roughness and nanoscale features on cell proliferation and differentiation. , 2011, Biomaterials.

[6]  David A Weitz,et al.  Microfluidic fabrication of water-in-water (w/w) jets and emulsions. , 2012, Biomicrofluidics.

[7]  Hossein Tavana,et al.  Ultralow interfacial tensions of aqueous two-phase systems measured using drop shape. , 2014, Langmuir : the ACS journal of surfaces and colloids.

[8]  Christine D. Keating,et al.  Complete Budding and Asymmetric Division of Primitive Model Cells To Produce Daughter Vesicles with Different Interior and Membrane Compositions , 2011, Journal of the American Chemical Society.

[9]  C. Keating,et al.  Budding and asymmetric protein microcompartmentation in giant vesicles containing two aqueous phases. , 2008, Journal of the American Chemical Society.

[10]  A. Hyman,et al.  Growth and division of active droplets provides a model for protocells , 2016, Nature Physics.

[11]  Donald E Ingber,et al.  Cytoskeletal control of growth and cell fate switching. , 2009, Current opinion in cell biology.

[12]  Reinhard Lipowsky,et al.  Wetting-Induced Budding of Vesicles in Contact with Several Aqueous Phases , 2012, The journal of physical chemistry. B.

[13]  Daniel T. N. Chen,et al.  Spontaneous motion in hierarchically assembled active matter , 2012, Nature.

[14]  Keith Gull,et al.  The evolution of the cytoskeleton , 2011, The Journal of cell biology.

[15]  S. Granick,et al.  Vesicle budding induced by a pore-forming peptide. , 2010, Journal of the American Chemical Society.

[16]  Zhiyuan Zhong,et al.  Polymersomes Spanning from Nano- to Microscales: Advanced Vehicles for Controlled Drug Delivery and Robust Vesicles for Virus and Cell Mimicking , 2011 .

[17]  D. Brooks,et al.  Phase separation in cytoplasm, due to macromolecular crowding, is the basis for microcompartmentation , 1995, FEBS letters.

[18]  D. S. Weiss,et al.  Bacterial cell division and the septal ring , 2004, Molecular microbiology.

[19]  Stephen Mann,et al.  Spontaneous growth and division in self-reproducing inorganic colloidosomes. , 2014, Small.

[20]  S. Takayama,et al.  Aqueous two‐phase system‐mediated antibody micropatterning enables multiplexed immunostaining of cell monolayers and tissues , 2015, Biotechnology journal.

[21]  Brian D. Slaughter,et al.  Symmetry breaking in the life cycle of the budding yeast. , 2009, Cold Spring Harbor perspectives in biology.

[22]  H. Kueh,et al.  Structural Plasticity in Actin and Tubulin Polymer Dynamics , 2009, Science.

[23]  Jean-Pierre Delville,et al.  An optical toolbox for total control of droplet microfluidics. , 2007, Lab on a chip.

[24]  D. Weitz,et al.  Electric control of droplets in microfluidic devices. , 2006, Angewandte Chemie.

[25]  Sean X. Sun,et al.  Condensation of FtsZ filaments can drive bacterial cell division , 2009, Proceedings of the National Academy of Sciences.

[26]  V. Hasırcı,et al.  Novel surface patterning approaches for tissue engineering and their effect on cell behavior. , 2006, Nanomedicine.

[27]  R. Steinbrecht,et al.  Cryotechniques in Biological Electron Microscopy , 1987, Springer Berlin Heidelberg.

[28]  Watt W. Webb,et al.  Imaging coexisting fluid domains in biomembrane models coupling curvature and line tension , 2003, Nature.

[29]  Ho Cheung Shum,et al.  Osmo-solidification of all-aqueous emulsion with enhanced preservation of protein activity. , 2016, Journal of materials chemistry. B.

[30]  Yang Song,et al.  All-Aqueous Electrosprayed Emulsion for Templated Fabrication of Cytocompatible Microcapsules. , 2015, ACS applied materials & interfaces.

[31]  C. P. Whitby,et al.  Some general features of limited coalescence in solid-stabilized emulsions , 2003, The European physical journal. E, Soft matter.

[32]  Yang Song,et al.  Fabrication of fibrillosomes from droplets stabilized by protein nanofibrils at all-aqueous interfaces , 2016, Nature Communications.

[33]  Alexander K. Buell,et al.  Protein microgels from amyloid fibril networks. , 2015, ACS nano.

[34]  Andrew W. Murray,et al.  Feedback control of mitosis in budding yeast , 1991, Cell.

[35]  M. Waldor,et al.  A dynamic, mitotic-like mechanism for bacterial chromosome segregation. , 2006, Genes & development.

[36]  Taco Nicolai,et al.  Stabilization of water-in-water emulsions by addition of protein particles. , 2013, Langmuir : the ACS journal of surfaces and colloids.

[37]  R. Leapman,et al.  A structural model for Alzheimer's β-amyloid fibrils based on experimental constraints from solid state NMR , 2002, Proceedings of the National Academy of Sciences of the United States of America.