Stimulation of 3D osteogenesis by mesenchymal stem cells using a nanovibrational bioreactor

Penelope M. Tsimbouri; Peter G. Childs; Gabriel D. Pemberton; Jingli Yang; Vineetha Jayawarna; Wich Orapiriyakul; Karl Burgess; Cristina González-García; Gavin Blackburn; Dilip Thomas; Catalina Vallejo-Giraldo; Manus J. P. Biggs; Adam S. G. Curtis; Manuel Salmerón-Sánchez; Stuart Reid; Matthew J. Dalby

doi:10.1038/s41551-017-0127-4

Stimulation of 3D osteogenesis by mesenchymal stem cells using a nanovibrational bioreactor

Penelope M. Tsimbouri, Peter G. Childs, Gabriel D. Pemberton, Jingli Yang, Vineetha Jayawarna, Wich Orapiriyakul, Karl Burgess, Cristina González-García, Gavin Blackburn, Dilip Thomas, Catalina Vallejo-Giraldo, Manus J. P. Biggs, Adam S. G. Curtis, Manuel Salmerón-Sánchez, Stuart Reid^*, Matthew J. Dalby

^*Corresponding author for this work

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

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Abstract

Bone grafts are one of the most commonly transplanted tissues. However, autologous grafts are in short supply, and can be associated with pain and donor-site morbidity. The creation of tissue-engineered bone grafts could help to fulfil clinical demand and provide a crucial resource for drug screening. Here, we show that vibrations of nanoscale amplitude provided by a newly developed bioreactor can differentiate a potential autologous cell source, mesenchymal stem cells (MSCs), into mineralized tissue in 3D. We demonstrate that nanoscale mechanotransduction can stimulate osteogenesis independently of other environmental factors, such as matrix rigidity. We show this by generating mineralized matrix from MSCs seeded in collagen gels with stiffness an order of magnitude below the stiffness of gels needed to induce bone formation in vitro. Our approach is scalable and can be compatible with 3D scaffolds.

Original language	English
Pages (from-to)	758-770
Number of pages	13
Journal	Nature Biomedical Engineering
Volume	1
Issue number	9
DOIs	https://doi.org/10.1038/s41551-017-0127-4
Publication status	Published - 12 Sept 2017

Funding

This work was supported by grants to S.R. and M.J.D. from the BBSRC, BBSRC/SFI and EPSRC (BB/N012690/1, BB/P00220X/1, EP/N013905/1, EP/N012631/1 and EP/P001114/1), along with a Wolfson Merit Award from The Royal Society and a programme grant from Find a Better Way. M.J.P.B. is funded by SFI grant nos. 11/SIRG/B2135 and 13/RC/2073. P.G.C. was funded by an STFC/BBSRC fellowship. We thank J. Hough, H. Nikukar, I. Tifenbrun and K. Robertson for their discussion, C.-A. Smith for technical support, and E. Manson for help with metabolite analysis. We also thank C. Boyle, S. Robertson and P. Campsie for help with the construction of the bioreactor.

Keywords

mesenchymal stem cells
tissue engineering
nanobiotechnology

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10.1038/s41551-017-0127-4

Tsimbouri-etal-NBE-2017-Stimulation-of-3D-osteogenesis-by-mesenchymal-stem-cells-using-a-nanovibrational-bioreactorAccepted author manuscript, 6.51 MB

http://eprints.gla.ac.uk/145039/

Cite this

Tsimbouri, P. M., Childs, P. G., Pemberton, G. D., Yang, J., Jayawarna, V., Orapiriyakul, W., Burgess, K., González-García, C., Blackburn, G., Thomas, D., Vallejo-Giraldo, C., Biggs, M. J. P., Curtis, A. S. G., Salmerón-Sánchez, M., Reid, S., & Dalby, M. J. (2017). Stimulation of 3D osteogenesis by mesenchymal stem cells using a nanovibrational bioreactor. Nature Biomedical Engineering, 1(9), 758-770. https://doi.org/10.1038/s41551-017-0127-4

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abstract = "Bone grafts are one of the most commonly transplanted tissues. However, autologous grafts are in short supply, and can be associated with pain and donor-site morbidity. The creation of tissue-engineered bone grafts could help to fulfil clinical demand and provide a crucial resource for drug screening. Here, we show that vibrations of nanoscale amplitude provided by a newly developed bioreactor can differentiate a potential autologous cell source, mesenchymal stem cells (MSCs), into mineralized tissue in 3D. We demonstrate that nanoscale mechanotransduction can stimulate osteogenesis independently of other environmental factors, such as matrix rigidity. We show this by generating mineralized matrix from MSCs seeded in collagen gels with stiffness an order of magnitude below the stiffness of gels needed to induce bone formation in vitro. Our approach is scalable and can be compatible with 3D scaffolds.",

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Tsimbouri, PM, Childs, PG, Pemberton, GD, Yang, J, Jayawarna, V, Orapiriyakul, W, Burgess, K, González-García, C, Blackburn, G, Thomas, D, Vallejo-Giraldo, C, Biggs, MJP, Curtis, ASG, Salmerón-Sánchez, M, Reid, S & Dalby, MJ 2017, 'Stimulation of 3D osteogenesis by mesenchymal stem cells using a nanovibrational bioreactor', Nature Biomedical Engineering, vol. 1, no. 9, pp. 758-770. https://doi.org/10.1038/s41551-017-0127-4

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AU - Vallejo-Giraldo, Catalina

AU - Biggs, Manus J. P.

AU - Curtis, Adam S. G.

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AB - Bone grafts are one of the most commonly transplanted tissues. However, autologous grafts are in short supply, and can be associated with pain and donor-site morbidity. The creation of tissue-engineered bone grafts could help to fulfil clinical demand and provide a crucial resource for drug screening. Here, we show that vibrations of nanoscale amplitude provided by a newly developed bioreactor can differentiate a potential autologous cell source, mesenchymal stem cells (MSCs), into mineralized tissue in 3D. We demonstrate that nanoscale mechanotransduction can stimulate osteogenesis independently of other environmental factors, such as matrix rigidity. We show this by generating mineralized matrix from MSCs seeded in collagen gels with stiffness an order of magnitude below the stiffness of gels needed to induce bone formation in vitro. Our approach is scalable and can be compatible with 3D scaffolds.

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Stimulation of 3D osteogenesis by mesenchymal stem cells using a nanovibrational bioreactor

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Peter Childs

Stuart Reid

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Stimulation of 3D osteogenesis by mesenchymal stem cells using a nanovibrational bioreactor

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Peter Childs

Stuart Reid

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