Disordered protein-graphene oxide co-assembly and supramolecular biofabrication of functional fluidic devices

Yuanhao Wu; Babatunde O Okesola; Jing Xu; Ivan Korotkin; Alice Berardo; Ilaria Corridori; Francesco Luigi Pellerej di Brocchetti; Janos Kanczler; Jingyu Feng; Weiqi Li; Yejiao Shi; Vladimir Farafonov; Yiqiang Wang; Rebecca F Thompson; Maria-Magdalena Titirici; Dmitry Nerukh; Sergey Karabasov; Richard O C Oreffo; Jose Carlos Rodriguez-Cabello; Giovanni Vozzi; Helena S Azevedo; Nicola M Pugno; Wen Wang; Alvaro Mata

doi:10.1038/s41467-020-14716-z

Disordered protein-graphene oxide co-assembly and supramolecular biofabrication of functional fluidic devices

Yuanhao Wu
, Babatunde O Okesola
, Jing Xu
, Ivan Korotkin
, Alice Berardo
, Ilaria Corridori
, Francesco Luigi Pellerej di Brocchetti
, Janos Kanczler
, Jingyu Feng
, Weiqi Li
, Yejiao Shi
, Vladimir Farafonov
, Yiqiang Wang
, Rebecca F Thompson
, Maria-Magdalena Titirici
, Dmitry Nerukh
, Sergey Karabasov
, Richard O C Oreffo
, Jose Carlos Rodriguez-Cabello
, Giovanni Vozzi

Helena S Azevedo, Nicola M Pugno, Wen Wang, Alvaro Mata

Biodiscovery Institute, University of Nottingham, NG7 2RD, Nottingham, UK.
School of Engineering and Materials Science; Queen Mary University of London, Mile End Road; London, E1 4NS UK
Mathematical Sciences, University of Southampton, Southampton SO17 1BJ, UK.
C3A - Center Agriculture Food Environment, University of Trento/Fondazione Edmund Mach, Via Edmund Mach, 1 - 38010, San Michele all'Adige (TN), Italy.
Laboratory of Bio-inspired, Bionic, Nano, Meta Materials & Mechanics, Università di Trento, via Mesiano, 77, I-38123, Trento, Italy.
Research Center'E. Piaggio' & Dipartimento di Ingegneria dell'Informazione, University of Pisa, Largo Lucio Lazzarino, 256126, Pisa, Italy.
Bone and Joint Research Group, Centre for Human Development, Stem Cells and Regeneration, Institute of Developmental Sciences, University of Southampton, Southampton, SO16 6YD, UK.
Department of Physical Chemistry, V. N. Karazin Kharkiv National University, Svobody Sq. 4, Kharkiv, 61022, Ukraine.
United Kingdom Atomic Energy Authority, Culham Science Centre, Abingdon, OX14 3DB, UK.
The Astbury Biostructure Laboratory, Astbury Centre for Structural Molecular Biology, Faculty of Biological Sciences, University of Leeds, Leeds, UK.
BIOFORGE Group, University of Valladolid, CIBER-BBN, 47011, Valladolid, Spain.
KET Labs, Edoardo Amaldi Foundation, Via del Politecnico snc, 00133, Rome, Italy.
Biodiscovery Institute, University of Nottingham, NG7 2RD, Nottingham, UK. [email protected].

Research output: Contribution to journal › Article › peer-review

60 Citations (Scopus)

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Abstract

Supramolecular chemistry offers an exciting opportunity to assemble materials with molecular precision. However, there remains an unmet need to turn molecular self-assembly into functional materials and devices. Harnessing the inherent properties of both disordered proteins and graphene oxide (GO), we report a disordered protein-GO co-assembling system that through a diffusion-reaction process and disorder-to-order transitions generates hierarchically organized materials that exhibit high stability and access to non-equilibrium on demand. We use experimental approaches and molecular dynamics simulations to describe the underlying molecular mechanism of formation and establish key rules for its design and regulation. Through rapid prototyping techniques, we demonstrate the system's capacity to be controlled with spatio-temporal precision into well-defined capillary-like fluidic microstructures with a high level of biocompatibility and, importantly, the capacity to withstand flow. Our study presents an innovative approach to transform rational supramolecular design into functional engineering with potential widespread use in microfluidic systems and organ-on-a-chip platforms.

Original language	English
Article number	1182
Journal	Nature Communications
Volume	11
Issue number	1
DOIs	https://doi.org/10.1038/s41467-020-14716-z
Publication status	Published - 4 Mar 2020

Bibliographical note

This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

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10.1038/s41467-020-14716-zLicence: CC BY 3.0

Disordered protein-graphene oxide co-assembly and supramolecular
This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
Final published version, 6.46 MBLicence: CC BY 3.0

Cite this

Wu, Y., Okesola, B. O., Xu, J., Korotkin, I., Berardo, A., Corridori, I., di Brocchetti, F. L. P., Kanczler, J., Feng, J., Li, W., Shi, Y., Farafonov, V., Wang, Y., Thompson, R. F., Titirici, M.-M., Nerukh, D., Karabasov, S., Oreffo, R. O. C., Carlos Rodriguez-Cabello, J., ... Mata, A. (2020). Disordered protein-graphene oxide co-assembly and supramolecular biofabrication of functional fluidic devices. Nature Communications, 11(1), Article 1182. https://doi.org/10.1038/s41467-020-14716-z

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abstract = "Supramolecular chemistry offers an exciting opportunity to assemble materials with molecular precision. However, there remains an unmet need to turn molecular self-assembly into functional materials and devices. Harnessing the inherent properties of both disordered proteins and graphene oxide (GO), we report a disordered protein-GO co-assembling system that through a diffusion-reaction process and disorder-to-order transitions generates hierarchically organized materials that exhibit high stability and access to non-equilibrium on demand. We use experimental approaches and molecular dynamics simulations to describe the underlying molecular mechanism of formation and establish key rules for its design and regulation. Through rapid prototyping techniques, we demonstrate the system's capacity to be controlled with spatio-temporal precision into well-defined capillary-like fluidic microstructures with a high level of biocompatibility and, importantly, the capacity to withstand flow. Our study presents an innovative approach to transform rational supramolecular design into functional engineering with potential widespread use in microfluidic systems and organ-on-a-chip platforms.",

author = "Yuanhao Wu and Okesola, \{Babatunde O\} and Jing Xu and Ivan Korotkin and Alice Berardo and Ilaria Corridori and \{di Brocchetti\}, \{Francesco Luigi Pellerej\} and Janos Kanczler and Jingyu Feng and Weiqi Li and Yejiao Shi and Vladimir Farafonov and Yiqiang Wang and Thompson, \{Rebecca F\} and Maria-Magdalena Titirici and Dmitry Nerukh and Sergey Karabasov and Oreffo, \{Richard O C\} and \{Carlos Rodriguez-Cabello\}, Jose and Giovanni Vozzi and Azevedo, \{Helena S\} and Pugno, \{Nicola M\} and Wen Wang and Alvaro Mata",

note = "This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article{\textquoteright}s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article{\textquoteright}s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.",

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Wu, Y, Okesola, BO, Xu, J, Korotkin, I, Berardo, A, Corridori, I, di Brocchetti, FLP, Kanczler, J, Feng, J, Li, W, Shi, Y, Farafonov, V, Wang, Y, Thompson, RF, Titirici, M-M, Nerukh, D, Karabasov, S, Oreffo, ROC, Carlos Rodriguez-Cabello, J, Vozzi, G, Azevedo, HS, Pugno, NM, Wang, W & Mata, A 2020, 'Disordered protein-graphene oxide co-assembly and supramolecular biofabrication of functional fluidic devices', Nature Communications, vol. 11, no. 1, 1182. https://doi.org/10.1038/s41467-020-14716-z

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AU - Wu, Yuanhao

AU - Okesola, Babatunde O

AU - Xu, Jing

AU - Korotkin, Ivan

AU - Berardo, Alice

AU - Corridori, Ilaria

AU - di Brocchetti, Francesco Luigi Pellerej

AU - Kanczler, Janos

AU - Feng, Jingyu

AU - Li, Weiqi

AU - Shi, Yejiao

AU - Farafonov, Vladimir

AU - Wang, Yiqiang

AU - Thompson, Rebecca F

AU - Titirici, Maria-Magdalena

AU - Nerukh, Dmitry

AU - Karabasov, Sergey

AU - Oreffo, Richard O C

AU - Carlos Rodriguez-Cabello, Jose

AU - Vozzi, Giovanni

AU - Azevedo, Helena S

AU - Pugno, Nicola M

AU - Wang, Wen

AU - Mata, Alvaro

N1 - This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

PY - 2020/3/4

Y1 - 2020/3/4

N2 - Supramolecular chemistry offers an exciting opportunity to assemble materials with molecular precision. However, there remains an unmet need to turn molecular self-assembly into functional materials and devices. Harnessing the inherent properties of both disordered proteins and graphene oxide (GO), we report a disordered protein-GO co-assembling system that through a diffusion-reaction process and disorder-to-order transitions generates hierarchically organized materials that exhibit high stability and access to non-equilibrium on demand. We use experimental approaches and molecular dynamics simulations to describe the underlying molecular mechanism of formation and establish key rules for its design and regulation. Through rapid prototyping techniques, we demonstrate the system's capacity to be controlled with spatio-temporal precision into well-defined capillary-like fluidic microstructures with a high level of biocompatibility and, importantly, the capacity to withstand flow. Our study presents an innovative approach to transform rational supramolecular design into functional engineering with potential widespread use in microfluidic systems and organ-on-a-chip platforms.

AB - Supramolecular chemistry offers an exciting opportunity to assemble materials with molecular precision. However, there remains an unmet need to turn molecular self-assembly into functional materials and devices. Harnessing the inherent properties of both disordered proteins and graphene oxide (GO), we report a disordered protein-GO co-assembling system that through a diffusion-reaction process and disorder-to-order transitions generates hierarchically organized materials that exhibit high stability and access to non-equilibrium on demand. We use experimental approaches and molecular dynamics simulations to describe the underlying molecular mechanism of formation and establish key rules for its design and regulation. Through rapid prototyping techniques, we demonstrate the system's capacity to be controlled with spatio-temporal precision into well-defined capillary-like fluidic microstructures with a high level of biocompatibility and, importantly, the capacity to withstand flow. Our study presents an innovative approach to transform rational supramolecular design into functional engineering with potential widespread use in microfluidic systems and organ-on-a-chip platforms.

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Disordered protein-graphene oxide co-assembly and supramolecular biofabrication of functional fluidic devices

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