Controlled division of cell-sized vesicles by low densities of membrane-bound proteins.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
14 02 2020
14 02 2020
Historique:
received:
04
07
2019
accepted:
24
01
2020
entrez:
16
2
2020
pubmed:
16
2
2020
medline:
2
6
2020
Statut:
epublish
Résumé
The proliferation of life on earth is based on the ability of single cells to divide into two daughter cells. During cell division, the plasma membrane undergoes a series of morphological transformations which ultimately lead to membrane fission. Here, we show that analogous remodeling processes can be induced by low densities of proteins bound to the membranes of cell-sized lipid vesicles. Using His-tagged fluorescent proteins, we are able to precisely control the spontaneous curvature of the vesicle membranes. By fine-tuning this curvature, we obtain dumbbell-shaped vesicles with closed membrane necks as well as neck fission and complete vesicle division. Our results demonstrate that the spontaneous curvature generates constriction forces around the membrane necks and that these forces can easily cover the force range found in vivo. Our approach involves only one species of membrane-bound proteins at low densities, thereby providing a simple and extendible module for bottom-up synthetic biology.
Identifiants
pubmed: 32060284
doi: 10.1038/s41467-020-14696-0
pii: 10.1038/s41467-020-14696-0
pmc: PMC7021675
doi:
Substances chimiques
Membrane Proteins
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
905Références
Osawa, M. & Erickson, H. P. Liposome division by a simple bacterial division machinery. PNAS 110, 11000–1004 (2013).
doi: 10.1073/pnas.1222254110
Snead, W. T. et al. Membrane fission by protein crowding. Proc. Natl Acad. Sci. USA 114, E3258–E3267 (2017).
doi: 10.1073/pnas.1616199114
Deshpande, S., Spoelstra, W. K., van Doorn J. Kerssemakers, M. & Dekker, C. Mechanical division of cell-sized liposomes. ACS Nano 12, 2560–2568 (2018).
doi: 10.1021/acsnano.7b08411
Roux, A. et al. Membrane curvature controls dynamin polymerization. PNAS 107, 4242–4146 (2010).
doi: 10.1073/pnas.0913734107
Schoeneberg, J. et al. ATP-dependent force generation and membrane scission by ESCRT-III and Vps4. Science 362, 1423–1428 (2018).
doi: 10.1126/science.aat1839
Xiao, J. & Goley, E. D. Redefining the roles of the FtsZ-ring in bacterial cytokinesis. Curr. Opin. Microbiol. 34, 90–96 (2016).
doi: 10.1016/j.mib.2016.08.008
Arpino, J. A. J., Rizkallah, P. J. & Jones, D. D. Crystal structure of enhanced green fluorescent protein to 1.35 a resolution reveals alternative conformations for Glu222. PLoS ONE 7, e47132 (2012).
doi: 10.1371/journal.pone.0047132
Sorre, B. et al. Nature of curvature coupling of amphiphysin with membranes depends on its bound density. Proc. Natl Acad. Sci. USA 109, 173–178 (2012).
doi: 10.1073/pnas.1103594108
Vrhovec, S., Mally, M., Kav̆cic̆, B. & Derganc, J. A microfluidic diffusion chamber or reversible environmental changes around flaccid lipid vesicles. Lab Chip 11, 4200–4206 (2011).
doi: 10.1039/c1lc20531e
Nye, J. A. & Groves, J. T. Kinetic control of histidine-tagged protein surface density on supported lipid bilayers. Langmuir 24, 4145–4149 (2008).
doi: 10.1021/la703788h
Müller, J. D., Chen, Y. & Gratton, E. Resolving heterogeneity on the single molecular level with the photon-counting histogram. Biophys. J. 78, 474–486 (2000).
doi: 10.1016/S0006-3495(00)76610-0
Zacharias, D. A., Violin, J. D., Newton, A. C. & Tsien, R. Y. Partitioning of lipid-modified monomeric GFPs into membrane microdomains of live cells. Science 296, 913–916 (2002).
doi: 10.1126/science.1068539
Seifert, U., Berndl, K. & Lipowsky, R. Shape transformations of vesicles: phase diagram for spontaneous curvature and bilayer coupling model. Phys. Rev. A 44, 1182–1202 (1991).
doi: 10.1103/PhysRevA.44.1182
Lipowsky, R. Understanding giant vesicles: a theoretical perspective. In The Giant Vesicle Book (eds Dimova, R. & Marques, C.) Ch. 5 (Taylor & Francis, 2019).
Chen, Z., Atafi, E. & Baumgart, T. Membrane shape instability induced by protein crowding. Biophys. J. 111, 1823–1826 (2016).
doi: 10.1016/j.bpj.2016.09.039
Helfrich, W. Elastic properties of lipid bilayers: theory and possible experiments. Z. Naturforsch. 28c, 693–703 (1973).
doi: 10.1515/znc-1973-11-1209
Bhatia, T., Agudo-Canalejo, J., Dimova, R. & Lipowsky, R. Membrane nanotubes increase the robustness of giant vesicles. ACS Nano 12, 4478–4485 (2018).
doi: 10.1021/acsnano.8b00640
Karimi, M. et al. Asymmetric ionic conditions generate large membrane curvatures. Nano Lett. 18, 7816–7821 (2018).
doi: 10.1021/acs.nanolett.8b03584
Bartelt, S. M. et al. Dynamic blue light-switchable protein patterns on giant unilamellar vesicles. Chem. Commun. 54, 948–951 (2018).
doi: 10.1039/C7CC08758F
Różycki, B. & Lipowsky, R. Membrane curvature generated by asymmetric depletion layers of ions, small molecules, and nanoparticles. J. Chem. Phys. 145, 074117 (2016).
doi: 10.1063/1.4960772
Fenz, S. F. & Sengupta, K. Giant vesicles as cell models. Integr. Biol. 4, 982–995 (2012).
doi: 10.1039/c2ib00188h
Weiss, M. et al. Sequential bottom-up assembly of mechanically stabilized synthetic cells by microfluidics. Nat. Mater. 17, 89–95 (2018).
doi: 10.1038/nmat5005
Kretschmer, S., Ganzinger, K. A., Franquelim, H. G. & Schwille, P. Synthetic cell division via membrane-transforming molecular assemblies. BMC Biol. 17, 43 (2019).
doi: 10.1186/s12915-019-0665-1
Weinberger, A. et al. Gel-assisted formation of giant unilamellar vesicles. Biophys. J. 105, 154–164 (2013).
doi: 10.1016/j.bpj.2013.05.024
Pott, T., Bouvrais, H. & Méléard, P. Giant unilamellar vesicle formation under physiologically relevant conditions. Chem. Phys. Lipids 154, 115–119 (2008).
doi: 10.1016/j.chemphyslip.2008.03.008
Steinkühler, J., Tillieux, P. D., Knorr, R. L., Lipowsky, R. & Dimova, R. Charged giant unilamellar vesicles prepared by electroformation exhibit nanotubes and transbilayer lipid asymmetry. Sci. Rep. 8, 11838 (2018).
doi: 10.1038/s41598-018-30286-z
Bahrami, A. H. & Hummer, G. Formation and stability of lipid membrane nanotubes. ACS Nano 11, 9558–9565 (2017).
doi: 10.1021/acsnano.7b05542
Fourcade, B., Miao, L., Rao, M., Wortis, M. & Zia, R. Scaling analysis of narrow necks in curvature models of fluid lipid-bilayer vesicles. Phys. Rev. E 49, 5276–5286 (1994).
doi: 10.1103/PhysRevE.49.5276
Derzhanski, A., Petrov, A. G. & Mitov, M. D. Molecular asymmetry and saddle-splay elasticity in lipid bilayers. Ann. Phys. 3, 297 (1978).
doi: 10.1051/anphys/197803030297
Lorenzen, S., Servuss, R.-M. & Helfrich, W. Elastic torques about membrane edges: a study of pierced egg lecithin vesicles. Biophys. J. 50, 565–572 (1986).
doi: 10.1016/S0006-3495(86)83496-8
Hu, M., Briguglio, J. J. & Deserno, M. Determining the gaussian curvature modulus of lipid membranes in simulations. Biophys. J. 102, 1403–1410 (2012).
doi: 10.1016/j.bpj.2012.02.013
Portet, T. & Dimova, R. A new method for measuring edge tensions and stability of lipid bilayers: effect of membrane composition. Biophys. J. 99, 3264–3273 (2010).
doi: 10.1016/j.bpj.2010.09.032
Gracia, R., Bezlyepkina, N., Knorr, R. L., Lipowsky, R. & Dimova., R. Effect of cholesterol on the rigidity of saturated and unsaturated membranes: fluctuation and electrodeformation analysis of giant vesicles. Soft Matter 6, 1472–1482 (2010).
doi: 10.1039/b920629a
Nahas, K. A. et al. A microfluidic platform for the characterisation of membrane active antimicrobials. Lab Chip 19, 837–844 (2019).
doi: 10.1039/C8LC00932E
Rueden, C. T. et al. ImageJ2: image J for the next generation of scientific image data. BMC Bioinform. 18, 529 (2017).
doi: 10.1186/s12859-017-1934-z
Weinberger, A. et al. Cargo self-assembly rescues affinity of cell-penetrating peptides to lipid membranes. Sci. Rep. 7, 43963 (2017).
doi: 10.1038/srep43963
Leftin, A., Molugu, T. R., Job, C., Beyer, K. & Brown, M. F. Area per lipid and cholesterol interactions in membranes from separated local-field
doi: 10.1016/j.bpj.2014.07.044