Engineering Light-Responsive Contractile Actomyosin Networks with DNA Nanotechnology.
DNA nanotechnology
actomyosin networks
bottom-up synthetic biology
symmetry break
water-in-oil droplets
Journal
Advanced biosystems
ISSN: 2366-7478
Titre abrégé: Adv Biosyst
Pays: Germany
ID NLM: 101711718
Informations de publication
Date de publication:
09 2020
09 2020
Historique:
received:
02
04
2020
revised:
26
06
2020
accepted:
30
06
2020
pubmed:
23
7
2020
medline:
21
10
2021
entrez:
23
7
2020
Statut:
ppublish
Résumé
External control and precise manipulation is key for the bottom-up engineering of complex synthetic cells. Minimal actomyosin networks have been reconstituted into synthetic cells; however, their light-triggered symmetry breaking contraction has not yet been demonstrated. Here, light-activated directional contractility of a minimal synthetic actomyosin network inside microfluidic cell-sized compartments is engineered. Actin filaments, heavy-meromyosin-coated beads, and caged ATP are co-encapsulated into water-in-oil droplets. ATP is released upon illumination, leading to a myosin-generated force which results in a motion of the beads along the filaments and hence a contraction of the network. Symmetry breaking is achieved using DNA nanotechnology to establish a link between the network and the compartment periphery. It is demonstrated that the DNA-linked actin filaments contract to one side of the compartment forming actin asters and quantify the dynamics of this process. This work exemplifies that an engineering approach to bottom-up synthetic biology, combining biological and artificial elements, can circumvent challenges related to active multi-component systems and thereby greatly enrich the complexity of synthetic cellular systems.
Identifiants
pubmed: 32696544
doi: 10.1002/adbi.202000102
doi:
Substances chimiques
DNA
9007-49-2
Actomyosin
9013-26-7
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e2000102Informations de copyright
© 2020 The Authors. Published by WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim.
Références
P. Schwille, J. Spatz, K. Landfester, E. Bodenschatz, S. Herminghaus, V. Sourjik, T. J. Erb, P. Bastiaens, R. Lipowsky, A. Hyman, P. Dabrock, J. C. Baret, T. Vidakovic-Koch, P. Bieling, R. Dimova, H. Mutschler, T. Robinson, T. Y. D. Tang, S. Wegner, K. Sundmacher, Angew. Chem., Int. Ed. 2018, 57, 13382.
P. Schwille, Science 2011, 333, 1252.
M. Weiss, J. P. Frohnmayer, L. T. Benk, B. Haller, J. W. Janiesch, T. Heitkamp, M. Börsch, R. B. Lira, R. Dimova, R. Lipowsky, E. Bodenschatz, J. C. Baret, T. Vidakovic-Koch, K. Sundmacher, I. Platzman, J. P. Spatz, Nat. Mater. 2017, 17, 89.
J. P. Frohnmayer, D. Brüggemann, C. Eberhard, S. Neubauer, C. Mollenhauer, H. Boehm, H. Kessler, B. Geiger, J. P. Spatz, Angew. Chem., Int. Ed. 2015, 54, 12472.
R. Maan, E. Loiseau, A. R. Bausch, Biophys. J. 2018, 115, 2395.
K. Y. Lee, S. J. Park, K. A. Lee, S. H. Kim, H. Kim, Y. Meroz, L. Mahadevan, K. H. Jung, T. K. Ahn, K. K. Parker, K. Shin, Nat. Biotechnol. 2018, 36, 530.
T. Pols, H. R. Sikkema, B. F. Gaastra, J. Frallicciardi, W. M. Śmigiel, S. Singh, B. Poolman, Nat. Commun. 2019, 10, 4239.
F. C. Keber, E. Loiseau, T. Sanchez, S. J. DeCamp, L. Giomi, M. J. Bowick, M. C. Marchetti, Z. Dogic, A. R. Bausch, Science 2014, 345, 1135.
S. M. Bartelt, J. Steinkühler, R. Dimova, S. V. Wegner, Nano Lett. 2018, 18, 7268.
O. Siton-Mendelson, A. Bernheim-Groswasser, Cell Adhes. Migr. 2016, 10, 461.
S. Deshpande, Y. Caspi, A. E. C. Meijering, C. Dekker, Nat. Commun. 2016, 7, 10447.
M. P. N. Juniper, M. Weiss, I. Platzman, J. P. Spatz, T. Surrey, Soft Matter 2018, 14, 901.
N. N. Deng, M. Yelleswarapu, L. Zheng, W. T. S. Huck, J. Am. Chem. Soc. 2016, 139, 587.
K. Göpfrich, B. Haller, O. Staufer, Y. Dreher, U. Mersdorf, I. Platzman, J. P. Spatz, ACS Synth. Biol. 2019, 8, 937.
M. Miyazaki, M. Chiba, H. Eguchi, T. Ohki, S. Ishiwata, Nat. Cell Biol. 2015, 17, 480.
E. A. Shah, K. Keren, eLife 2014, 3, e01433.
M. Malik-Garbi, N. Ierushalmi, S. Jansen, E. Abu-Shah, B. L. Goode, A. Mogilner, K. Keren, Nat. Phys. 2019, 15, 509.
K. Dürre, F. C. Keber, P. Bleicher, F. Brauns, C. J. Cyron, J. Faix, A. R. Bausch, Nat. Commun. 2018, 9, 1630.
S. Tanaka, K. Takiguchi, M. Hayashi, Commun. Phys. 2018, 1, 18.
L. L. Pontani, J. van der Gucht, G. Salbreux, J. Heuvingh, J. F. Joanny, C. Sykes, Biophys. J. 2009, 96, 192.
D. Merkle, N. Kahya, P. Schwille, ChemBioChem 2008, 9, 2673.
R. Li, B. Bowerman, Cold Spring Harbor Perspect. Biol. 2009, 2, a003475.
L. Blanchoin, R. Boujemaa-Paterski, C. Sykes, J. Plastino, Physiol. Rev. 2014, 94, 235.
M. Schuppler, F. C. Keber, M. Kröger, A. R. Bausch, Nat. Commun. 2016, 7, 13120.
I. Linsmeier, S. Banerjee, P. W. Oakes, W. Jung, T. Kim, M. P. Murrell, Nat. Commun. 2016, 7, 12615.
Sonal, K. A. Ganzinger, S. K. Vogel, J. Mücksch, P. Blumhardt, P. Schwille, J. Cell Sci. 2018, 132, jcs219899.
K. Takiguchi, J. Biochem. 1991, 109, 520.
F. Backouche, L. Haviv, D. Groswasser, A. Bernheim-Groswasser, Phys. Biol. 2006, 3, 264.
M. P. Murrell, M. L. Gardel, Proc. Natl. Acad. Sci. 2012, 109, 20820.
V. Wollrab, J. M. Belmonte, L. Baldauf, M. Leptin, F. Nédeléc, G. H. Koenderink, J. Cell Sci. 2018, 132, jcs219717.
N. Ierushalmi, M. Malik-Garbi, A. Manhart, E. A. Shah, B. L. Goode, A. Mogilner, K. Keren, eLife 2020, 9, e55368.
K. Göpfrich, I. Platzman, J. P. Spatz, Trends Biotechnol. 2018, 36, 938.
S. M. Douglas, I. Bachelet, G. M. Church, Science 2012, 335, 831.
A. J. M. Wollman, C. Sanchez-Cano, H. M. J. Carstairs, R. A. Cross, A. J. Turberfield, Nat. Nanotechnol. 2013, 9, 44.
K. Jahnke, M. Weiss, C. Frey, S. Antona, J. W. Janiesch, I. Platzman, K. Göpfrich, J. P. Spatz, Adv. Funct. Mater. 2019, 29, 1808647.
M. M. A. E. Claessens, M. Bathe, E. Frey, A. R. Bausch, Nat. Mater. 2006, 5, 748.
Y. Tanaka-Takiguchi, T. Kakei, A. Tanimura, A. Takagi, M. Honda, H. Hotani, K. Takiguchi, J. Mol. Biol. 2004, 341, 467.
S. Köhler, O. Lieleg, A. R. Bausch, PLoS One 2008, 3, e2736.
A. R. Bausch, K. Kroy, Nat. Phys. 2006, 2, 231.
S. Asakura, F. Oosawa, J. Chem. Phys. 1954, 22, 1255.
Y. Lee, P. Famouri, Nano Lett. 2013, 13, 3775.
J. A. McCray, L. Herbette, T. Kihara, D. R. Trentham, Proc. Natl. Acad. Sci. 1980, 77, 7237.
J. Klinth, A. Arner, A. Månsson, J. Muscle Res. Cell Motil. 2003, 24, 15.
A. Dunker, R. R. Rueckert, J. Biol. Chem. 1969, 244, 5074.
Y. Ideses, A. Sonn-Segev, Y. Roichman, A. Bernheim-Groswasser, Soft Matter 2013, 9, 7127.
Y. Ideses, V. Erukhimovitch, R. Brand, D. Jourdain, J. S. Hernandez, U. R. Gabinet, S. A. Safran, K. Kruse, A. Bernheim-Groswasser, Nat. Commun. 2018, 9, 2461.
M. Fritzsche, D. Li, H. Colin-York, V. T. Chang, E. Moeendarbary, J. H. Felce, E. Sezgin, G. Charras, E. Betzig, C. Eggeling, Nat. Commun. 2017, 8, 14347.
B. Geiger, J. P. Spatz, A. D. Bershadsky, Nat. Rev. Mol. Cell Biol. 2009, 10, 21.
J. D. Pardee, J. Aspudich, in Methods in Enzymology, Elsevier, New York 1982, pp. 164-181.
S. J. Kron, Y. Y. Toyoshima, T. Q. Uyeda, J. A. Spudich, in Methods in Enzymology, Elsevier, New York 1991, pp. 399-416.
S. S. Margossian, S. Lowey, in Methods in Enzymology, Elsevier, New York 1982, pp. 55-71.
J. N. Zadeh, C. D. Steenberg, J. S. Bois, B. R. Wolfe, M. B. Pierce, A. R. Khan, R. M. Dirks, N. A. Pierce, J. Comput. Chem. 2010, 32, 170.