De Novo design of functional coassembling organic–inorganic hydrogels for hierarchical mineralization and neovascularization
De Novo design of functional coassembling organic–inorganic hydrogels for hierarchical mineralization and neovascularization
Synthetic nanostructured materials incorporating both organic and inorganic components offer a unique, powerful, and versatile class of materials for widespread applications due to the distinct, yet complementary, nature of the intrinsic properties of the different constituents. We report a supramolecular system based on synthetic nanoclay (Laponite, Lap) and peptide amphiphiles (PAs, PAH3) rationally designed to coassemble into nanostructured hydrogels with high structural integrity and a spectrum of bioactivities. Spectroscopic and scattering techniques and molecular dynamic simulation approaches were harnessed to confirm that PAH3 nanofibers electrostatically adsorbed and conformed to the surface of Lap nanodisks. Electron and atomic force microscopies also confirmed an increase in diameter and surface area of PAH3 nanofibers after coassembly with Lap. Dynamic oscillatory rheology revealed that the coassembled PAH3-Lap hydrogels displayed high stiffness and robust self-healing behavior while gas adsorption analysis confirmed a hierarchical and heterogeneous porosity. Furthermore, this distinctive structure within the three-dimensional (3D) matrix provided spatial confinement for the nucleation and hierarchical organization of high-aspect ratio hydroxyapatite nanorods into well-defined spherical clusters within the 3D matrix. Applicability of the organic–inorganic PAH3-Lap hydrogels was assessed in vitro using human bone marrow-derived stromal cells (hBMSCs) and ex vivo using a chick chorioallantoic membrane (CAM) assay. The results demonstrated that the organic–inorganic PAH3-Lap hydrogels promote human skeletal cell proliferation and, upon mineralization, integrate with the CAM, are infiltrated by blood vessels, stimulate extracellular matrix production, and facilitate extensive mineral deposition relative to the controls.
biomineralization, coassembly, laponite, multicomponent biomaterials, nanocomposite hydrogels, peptide amphiphiles, supramolecular
11202–11217
Oreffo, Richard
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Okesola, Babatunde O.
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Mendoza-Martinez, Ana Karen
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Cidonio, Gianluca
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Derkus, Burak
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Boccorh, Delali
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Osuna de la Pena, David
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Elsharkawy, Sherif
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Wu, Yuanhao
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Dawson, Jonathan
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Wark, Alastair
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Knani, Dafna
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Adams, Dave J.
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Mata, Alvaro
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27 July 2021
Oreffo, Richard
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Okesola, Babatunde O.
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Mendoza-Martinez, Ana Karen
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Cidonio, Gianluca
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Derkus, Burak
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Boccorh, Delali
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Osuna de la Pena, David
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Elsharkawy, Sherif
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Wu, Yuanhao
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Dawson, Jonathan
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Wark, Alastair
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Knani, Dafna
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Adams, Dave J.
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Mata, Alvaro
c67ceb11-02c5-429c-a5e6-308c322f176b
Oreffo, Richard, Okesola, Babatunde O., Mendoza-Martinez, Ana Karen, Cidonio, Gianluca, Derkus, Burak, Boccorh, Delali, Osuna de la Pena, David, Elsharkawy, Sherif, Wu, Yuanhao, Dawson, Jonathan, Wark, Alastair, Knani, Dafna, Adams, Dave J. and Mata, Alvaro
(2021)
De Novo design of functional coassembling organic–inorganic hydrogels for hierarchical mineralization and neovascularization.
ACS Nano, 15 (7), .
(doi:10.1021/acsnano.0c09814).
Abstract
Synthetic nanostructured materials incorporating both organic and inorganic components offer a unique, powerful, and versatile class of materials for widespread applications due to the distinct, yet complementary, nature of the intrinsic properties of the different constituents. We report a supramolecular system based on synthetic nanoclay (Laponite, Lap) and peptide amphiphiles (PAs, PAH3) rationally designed to coassemble into nanostructured hydrogels with high structural integrity and a spectrum of bioactivities. Spectroscopic and scattering techniques and molecular dynamic simulation approaches were harnessed to confirm that PAH3 nanofibers electrostatically adsorbed and conformed to the surface of Lap nanodisks. Electron and atomic force microscopies also confirmed an increase in diameter and surface area of PAH3 nanofibers after coassembly with Lap. Dynamic oscillatory rheology revealed that the coassembled PAH3-Lap hydrogels displayed high stiffness and robust self-healing behavior while gas adsorption analysis confirmed a hierarchical and heterogeneous porosity. Furthermore, this distinctive structure within the three-dimensional (3D) matrix provided spatial confinement for the nucleation and hierarchical organization of high-aspect ratio hydroxyapatite nanorods into well-defined spherical clusters within the 3D matrix. Applicability of the organic–inorganic PAH3-Lap hydrogels was assessed in vitro using human bone marrow-derived stromal cells (hBMSCs) and ex vivo using a chick chorioallantoic membrane (CAM) assay. The results demonstrated that the organic–inorganic PAH3-Lap hydrogels promote human skeletal cell proliferation and, upon mineralization, integrate with the CAM, are infiltrated by blood vessels, stimulate extracellular matrix production, and facilitate extensive mineral deposition relative to the controls.
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Accepted manuscript De novo design of functional
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acsnano.0c09814
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Accepted/In Press date: 27 April 2021
e-pub ahead of print date: 28 June 2021
Published date: 27 July 2021
Additional Information:
Funding Information:
The work was supported by the ERC Starting Grant (STROFUNSCAFF), the Medical Research Council (UK Regenerative Medicine Platform Acellular/Smart Materials-3D Architecture, MR/R015651/1) to A.M., J.I.D., and R.O., and the AO Foundation (AOCMF-17-19M). B.O.O. was supported by the Henry Royce Institute for Advanced Materials, funded through Engineering and Physical Sciences Research Council (EPSRC) grants (EP/R00661X/1, EP/ S019367/1, EP/P025021/1, and EP/P025498/1). D.J.A. thanks EPSRC for an award of a fellowship (EP/L021978/2). The experiment at the ISIS Neutron and Muon Source was allocated beam time under experiment number 1810221 (DOI: 10.5286/ISIS.E.90604998 ) and collected on LARMOR. This work benefited from the SasView software, originally developed by the DANSE project under NSF award DMR-0520547. We thank Vicente Araullo-Peters and Giulia Mastroianni at Nanovision and School of Biological and Chemical Sciences (SBCS), QMUL as well as Janos Kanczler, Bone and Joint Research Group, Southampton for technical support. We thank Sarah Rogers, King Stephen, and Adam Washington from ISIS for SANS experiments. We thank Matthew Smith at Henry Royce Institute, Manchester for HRTEM and EDX analyses. We thank Richard Thorogate at London Centre for Nanotechnology for AFM analyses.
Publisher Copyright:
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Keywords:
biomineralization, coassembly, laponite, multicomponent biomaterials, nanocomposite hydrogels, peptide amphiphiles, supramolecular
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Local EPrints ID: 450764
URI: http://eprints.soton.ac.uk/id/eprint/450764
ISSN: 1936-0851
PURE UUID: d8ce0ef7-1e4f-497f-b4e4-3a1dbf9e4df1
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Date deposited: 10 Aug 2021 16:31
Last modified: 06 Jun 2024 04:08
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Contributors
Author:
Babatunde O. Okesola
Author:
Ana Karen Mendoza-Martinez
Author:
Gianluca Cidonio
Author:
Burak Derkus
Author:
Delali Boccorh
Author:
David Osuna de la Pena
Author:
Sherif Elsharkawy
Author:
Yuanhao Wu
Author:
Alastair Wark
Author:
Dafna Knani
Author:
Dave J. Adams
Author:
Alvaro Mata
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