Dynamin A as a one-component division machinery for synthetic cells.


Journal

Nature nanotechnology
ISSN: 1748-3395
Titre abrégé: Nat Nanotechnol
Pays: England
ID NLM: 101283273

Informations de publication

Date de publication:
05 Oct 2023
Historique:
received: 05 12 2022
accepted: 08 08 2023
pubmed: 6 10 2023
medline: 6 10 2023
entrez: 5 10 2023
Statut: aheadofprint

Résumé

Membrane abscission, the final cut of the last connection between emerging daughter cells, is an indispensable event in the last stage of cell division and in other cellular processes such as endocytosis, virus release or bacterial sporulation. However, its mechanism remains poorly understood, impeding its application as a cell-division machinery for synthetic cells. Here we use fluorescence microscopy and fluorescence recovery after photobleaching measurements to study the in vitro reconstitution of the bacterial protein dynamin A inside liposomes. Upon external reshaping of the liposomes into dumbbells, dynamin A self-assembles at the membrane neck, resulting in membrane hemi-scission and even full scission. Dynamin A proteins constitute a simple one-component division machinery capable of splitting dumbbell-shaped liposomes, marking an important step towards building a synthetic cell.

Identifiants

pubmed: 37798563
doi: 10.1038/s41565-023-01510-3
pii: 10.1038/s41565-023-01510-3
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2023. The Author(s), under exclusive licence to Springer Nature Limited.

Références

Spira, F. et al. Cytokinesis in vertebrate cells initiates by contraction of an equatorial actomyosin network composed of randomly oriented filaments. eLife 6, e30867 (2017).
doi: 10.7554/eLife.30867
Allard, J. F. & Cytrynbaum, E. N. Force generation by a dynamic Z-ring in Escherichia coli cell division. Proc. Natl Acad. Sci. USA 106, 145–150 (2009).
doi: 10.1073/pnas.0808657106
Bisson-Filho, A. W. et al. Treadmilling by FtsZ filaments drives peptidoglycan synthesis and bacterial cell division. Science 355, 739–743 (2017).
doi: 10.1126/science.aak9973
Pfitzner, A.-K., Moser von Filseck, J. & Roux, A. Principles of membrane remodeling by dynamic ESCRT-III polymers. Trends Cell Biol. 31, 856–868 (2021).
doi: 10.1016/j.tcb.2021.04.005
Caspi, Y. & Dekker, C. Dividing the archaeal way: the ancient Cdv cell-division machinery. Front. Microbiol. 9, 174 (2018).
doi: 10.3389/fmicb.2018.00174
Bassereau, P. et al. The 2018 biomembrane curvature and remodeling roadmap. J. Phys. D: Appl. Phys. 51, 343001 (2018).
doi: 10.1088/1361-6463/aacb98
Hurley, J. H. ESCRTs are everywhere. EMBO J. 34, 2398–2407 (2015).
doi: 10.15252/embj.201592484
Sundborger, A. C. & Hinshaw, J. E. Regulating dynamin dynamics during endocytosis. F1000Prime Rep. 6, 85 (2014).
doi: 10.12703/P6-85
Lemus, L. & Goder, V. Membrane trafficking: ESCRTs act here, there, and everywhere. Curr. Biol. 32, R292–R294 (2022).
doi: 10.1016/j.cub.2022.02.043
Bohuszewicz, O., Liu, J. & Low, H. H. Membrane remodelling in bacteria. J. Struct. Biol. 196, 3–14 (2016).
doi: 10.1016/j.jsb.2016.05.010
Olivi, L. et al. Towards a synthetic cell cycle. Nat. Commun. 12, 4531 (2021).
doi: 10.1038/s41467-021-24772-8
Schlimpert, S. et al. Two dynamin-like proteins stabilize FtsZ rings during Streptomyces sporulation. Proc. Natl Acad. Sci. USA 114, E6176–E6183 (2017).
doi: 10.1073/pnas.1704612114
Bramkamp, M. Structure and function of bacterial dynamin-like proteins. Biol. Chem. 393, 1203–1214 (2012).
doi: 10.1515/hsz-2012-0185
Guo, L. & Bramkamp, M. Bacterial dynamin-like protein DynA mediates lipid and content mixing. FASEB J. 33, 11746–11757 (2019).
doi: 10.1096/fj.201900844RR
Bürmann, F., Ebert, N., van Baarle, S. & Bramkamp, M. A bacterial dynamin-like protein mediating nucleotide-independent membrane fusion. Mol. Microbiol. 79, 1294–1304 (2011).
doi: 10.1111/j.1365-2958.2011.07523.x
Sawant, P., Eissenberger, K., Karier, L., Mascher, T. & Bramkamp, M. A dynamin-like protein involved in bacterial cell membrane surveillance under environmental stress. Environ. Microbiol. 18, 2705–2720 (2016).
doi: 10.1111/1462-2920.13110
Guo, L., Sattler, L., Shafqat, S., Graumann, P. L. & Bramkamp, M. A bacterial dynamin-like protein confers a novel phage resistance strategy on the population level in Bacillus subtilis. mBio 13, e0375321 (2022).
doi: 10.1128/mbio.03753-21
De Franceschi, N. et al. Synthetic membrane shaper for controlled liposome deformation. ACS Nano. 17, 966–978 (2022).
doi: 10.1021/acsnano.2c06125
Bhatia, T., Christ, S., Steinkühler, J., Dimova, R. & Lipowsky, R. Simple sugars shape giant vesicles into multispheres with many membrane necks. Soft Matter 16, 1246–1258 (2020).
doi: 10.1039/C9SM01890E
Antonny, B. et al. Membrane fission by dynamin: what we know and what we need to know. EMBO J. 35, 2270–2284 (2016).
doi: 10.15252/embj.201694613
Mattila, J.-P. et al. A hemi-fission intermediate links two mechanistically distinct stages of membrane fission. Nature 524, 109–113 (2015).
doi: 10.1038/nature14509
Dreher, Y., Jahnke, K., Schröter, M. & Göpfrich, K. Light-triggered cargo loading and division of DNA-containing giant unilamellar lipid vesicles. Nano Lett. 21, 5952–5957 (2021).
doi: 10.1021/acs.nanolett.1c00822
Steinkühler, J. et al. Controlled division of cell-sized vesicles by low densities of membrane-bound proteins. Nat. Commun. 11, 905 (2020).
doi: 10.1038/s41467-020-14696-0
Kozlovsky, Y. & Kozlov, M. M. Membrane fission: model for intermediate structures. Biophys. J. 85, 85–96 (2003).
doi: 10.1016/S0006-3495(03)74457-9
Fabrikant, G. et al. Computational model of membrane fission catalyzed by ESCRT-III. PLoS Comput. Biol. 5, e1000575 (2009).
doi: 10.1371/journal.pcbi.1000575
Zhang, G. & Müller, M. Rupturing the hemi-fission intermediate in membrane fission under tension: reaction coordinates, kinetic pathways, and free-energy barriers. J. Chem. Phys. 147, 064906 (2017).
doi: 10.1063/1.4997575
Gao, M., Huang, X., Song, B. L. & Yang, H. The biogenesis of lipid droplets: lipids take center stage. Prog. Lipid Res. 75, 100989 (2019).
doi: 10.1016/j.plipres.2019.100989
De Franceschi, N. et al. The ESCRT protein CHMP2B acts as a diffusion barrier on reconstituted membrane necks. J. Cell Sci. 132, jcs217968 (2018).
doi: 10.1242/jcs.217968
Bertin, A. et al. Human ESCRT-III polymers assemble on positively curved membranes and induce helical membrane tube formation. Nat. Commun. 11, 2663 (2020).
doi: 10.1038/s41467-020-16368-5
Pfitzner, A.-K. et al. An ESCRT-III polymerization sequence drives membrane deformation and fission. Cell 182, 1140–1155.e18 (2020).
doi: 10.1016/j.cell.2020.07.021
Schöneberg, 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
Remec Pavlin, M. & Hurley, J. H. The ESCRTs—converging on mechanism. J. Cell Sci. 133, jcs240333 (2020).
doi: 10.1242/jcs.240333
Abil, Z. & Danelon, C. Roadmap to building a cell: an evolutionary approach. Front. Bioeng. Biotechnol. 8, 927 (2020).
doi: 10.3389/fbioe.2020.00927
Cada, A. K. et al. Friction-driven membrane scission by the human ESCRT-III proteins CHMP1B and IST1. Proc. Natl Acad. Sci. USA 119, e2204536119 (2022).
doi: 10.1073/pnas.2204536119
Roux, A., Uyhazi, K., Frost, A. & de Camilli, P. GTP-dependent twisting of dynamin implicates constriction and tension in membrane fission. Nature 441, 528–531 (2006).
doi: 10.1038/nature04718
Tucker, W. C., Weber, T. & Chapman, E. R. Reconstitution of Ca
doi: 10.1126/science.1097196
Ge, Y. et al. Two forms of Opa1 cooperate to complete fusion of the mitochondrial inner-membrane. eLife 9, e50973 (2020).
doi: 10.7554/eLife.50973
Bramkamp, M. Bacterial dynamin-like proteins reveal mechanism for membrane fusion. Nat. Commun. 9, 3993 (2018).
doi: 10.1038/s41467-018-06559-6
van de Cauter, L. et al. Optimized cDICE for efficient reconstitution of biological systems in giant unilamellar vesicles. ACS Synth. Biol. 10, 1690–1702 (2021).
doi: 10.1021/acssynbio.1c00068

Auteurs

Nicola De Franceschi (N)

Department of Bionanoscience, Kavli Institute of Nanoscience Delft, Delft University of Technology, Delft, The Netherlands.
IMol Polish Academy of Sciences, Warsaw, Poland.

Roman Barth (R)

Department of Bionanoscience, Kavli Institute of Nanoscience Delft, Delft University of Technology, Delft, The Netherlands.

Sabrina Meindlhumer (S)

Department of Bionanoscience, Kavli Institute of Nanoscience Delft, Delft University of Technology, Delft, The Netherlands.

Alessio Fragasso (A)

Department of Bionanoscience, Kavli Institute of Nanoscience Delft, Delft University of Technology, Delft, The Netherlands.

Cees Dekker (C)

Department of Bionanoscience, Kavli Institute of Nanoscience Delft, Delft University of Technology, Delft, The Netherlands. c.dekker@tudelft.nl.

Classifications MeSH