Abstract
Leaf photosynthesis, coral mineralization, and trabecular bone growth depend on triply periodic minimal surfaces (TPMSs) with hyperboloidal structure on every surface point with varying Gaussian curvatures. However, translation of this structure into tissue-engineered bone grafts is challenging. This article reports the design and fabrication of high-resolution three-dimensional TPMS scaffolds embodying biomimicking hyperboloidal topography with different Gaussian curvatures, composed of body inherent β-tricalcium phosphate, by stereolithography-based three-dimensional printing and sintering. The TPMS bone scaffolds show high porosity and interconnectivity. Notably, compared with conventional scaffolds, they can reduce stress concentration, leading to increased mechanical strength. They are also found to support the attachment, proliferation, osteogenic differentiation, and angiogenic paracrine function of human mesenchymal stem cells (hMSCs). Through transcriptomic analysis, we theorize that the hyperboloid structure induces cytoskeleton reorganization of hMSCs, expressing elongated morphology on the convex direction and strengthening the cytoskeletal contraction. The clinical therapeutic efficacy of the TPMS scaffolds assessed by rabbit femur defect and mouse subcutaneous implantation models demonstrate that the TPMS scaffolds augment new bone formation and neovascularization. In comparison with conventional scaffolds, our TPMS scaffolds successfully guide the cell fate toward osteogenesis through cell-level directional curvatures and demonstrate drastic yet quantifiable improvements in bone regeneration.
Original language | English |
---|---|
Article number | e2206684119 |
Number of pages | 12 |
Journal | Proceedings of the National Academy of Sciences of the United States of America |
Volume | 119 |
Issue number | 41 |
DOIs | |
Publication status | Published - 11 Oct 2022 |
Keywords
- bone regeneration
- hyperboloidal structure
- mesenchymal stem cells
- TPMS
ASJC Scopus subject areas
- General
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In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 119, No. 41, e2206684119, 11.10.2022.
Research output: Journal article publication › Journal article › Academic research › peer-review
TY - JOUR
T1 - Gaussian curvature-driven direction of cell fate toward osteogenesis with triply periodic minimal surface scaffolds
AU - Yang, Yuhe
AU - Xu, Tianpeng
AU - Bei, Ho Pan
AU - Zhang, Lei
AU - Tang, Chak Yin
AU - Zhang, Ming
AU - Xu, Chenjie
AU - Bian, Liming
AU - Yeung, Kelvin Wai Kwok
AU - Fuh, Jerry Ying Hsi
AU - Zhao, Xin
N1 - Funding Information: Details of the design, fabrication, and characterization of the TPMS scaffolds are described in SI Appendix. The in vitro and in vivo experimental details including cytocompatibility evaluation, effect of TPMS scaffolds on osteogenic differentiation and angiogenic paracrine of hMSCs, and animal experiments are also described in SI Appendix. All animal evaluation was performed with approval from the Ethics Committee of the Hong Kong Polytechnic University (21-22/40-BME-R-CRF). Data, Materials, and Software Availability. All study data are included in the article and/or SI Appendix. Raw data for transcriptomic analysis were deposited under NCBI BioProject PRJNA763989 (54). ACKNOWLEDGMENTS: This work was supported by the Excellent Young Scholars Projects from the National Science Foundation of China (Grant 82122002), the National Key R&D Program of China (Grant 2018YFA0703100), the Collaborative Research Fund (Grant C5044-21GF) from the Research Grants Council of Hong Kong, and the interdepartmental open project from the State Key Laboratory of Ultra-precision Machining Technology (Grant P0033576) and Departmental General Research Fund (G-UAKM, G-UAMY) from Department of Industrial and Systems Engineering from The Hong Kong Polytechnic University and the Strategic Interdisciplinary Research Grant (7020029) from City University of Hong Kong. We also appreciate the support from the University Research Facility in 3D Printing of The Hong Kong Polytechnic University. Author affiliations: aDepartment of Biomedical Engineering, The Hong Kong Polytechnic University, Hung Hom, Hong Kong SAR, China; bDepartment of Mechanical and Aerospace Engineering, Hong Kong University of Science and Technology, Kowloon, Hong Kong SAR, China; cDepartment of Industrial and Systems Engineering, The Hong Kong Polytechnic University, Hung Hom, Kowloon, Hong Kong SAR, China; dDepartment of Biomedical Engineering, City University of Hong Kong, Kowloon, Hong Kong SAR, China; eSchool of Biomedical Sciences and Engineering, South China University of Technology, Guangzhou 510006, China; fNational Engineering Research Center for Tissue Restoration and Reconstruction, South China University of Technology, Guangzhou 510006, China; gDepartment of Orthopaedics & Traumatology, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Pokfulam, Hong Kong SAR, China; and hDepartment of Mechanical Engineering, National University of Singapore, 117575, Singapore 21. S. Ehrig et al., Surface tension determines tissue shape and growth kinetics. Sci. Adv. 5, eaav9394 (2019). 22. Z. Dong, X. Zhao, Application of TPMS structure in bone regeneration. Eng. Regen. 2, 154–162 (2021). 23. H.-T. Jung, S. Y. Lee, E. W. Kaler, B. Coldren, J. A. Zasadzinski, Gaussian curvature and the equilibrium among bilayer cylinders, spheres, and discs. Proc. Natl. Acad. Sci. U.S.A. 99, 15318–15322 (2002). 24. L. Li et al., Early osteointegration evaluation of porous Ti6Al4V scaffolds designed based on triply periodic minimal surface models. J. Orthop. Translat. 19, 94–105 (2019). 25. M. Zhianmanesh, M. Varmazyar, H. Montazerian, Fluid permeability of graded porosity scaffolds architectured with minimal surfaces. ACS Biomater. Sci. Eng. 5, 1228–1237 (2019). 26. X. Li et al., 3D printing of hydroxyapatite/tricalcium phosphate scaffold with hierarchical porous structure for bone regeneration. Biodes. Manuf. 3,15–29 (2020). 27. O. Al-Ketan, R. Rowshan, R. K. A. Al-Rub, Topology-mechanical property relationship of 3D printed strut, skeletal, and sheet based periodic metallic cellular materials. Addit. Manuf. 19, 167–183 (2018). 28. Z. Cai, Z. Liu, X. Hu, H. Kuang, J. Zhai, The effect of porosity on the mechanical properties of 3D-printed triply periodic minimal surface (TPMS) bioscaffold. Biodes. Manuf. 2, 242–255 (2019). 29. S. A. Goldstein, D. L. Wilson, D. A. Sonstegard, L. S. Matthews, The mechanical properties of human tibial trabecular bone as a function of metaphyseal location. J. Biomech. 16, 965–969 (1983). 30. D. Ali, Effect of scaffold architecture on cell seeding efficiency: A discrete phase model CFD analysis. Comput. Biol. Med. 109, 62–69 (2019). 31. F. P. Melchels et al., Effects of the architecture of tissue engineering scaffolds on cell seeding and culturing. Acta Biomater. 6, 4208–4217 (2010). 32. S. Weiss, R. Baumgart, M. Jochum, C. J. Strasburger, M. Bidlingmaier, Systemic regulation of distraction osteogenesis: A cascade of biochemical factors. J. Bone Miner. Res. 17, 1280–1289 (2002). 33. P. Zhuang et al., Nano β-tricalcium phosphate/hydrogel encapsulated scaffolds promote osteogenic differentiation of bone marrow stromal cells through ATP metabolism. Mater. Des. 208, 109881 (2021). 34. A. Klymov et al., Increased acellular and cellular surface mineralization induced by nanogrooves in combination with a calcium-phosphate coating. Acta Biomater. 31, 368–377 (2016). 35. X. Cui et al., Chemokine, vascular and therapeutic effects of combination Simvastatin and BMSC treatment of stroke. Neurobiol. Dis. 36,35–41 (2009). 36. M. R. Kelly-Goss, R. S. Sweat, P. C. Stapor, S. M. Peirce, W. L. Murfee, Targeting pericytes for angiogenic therapies. Microcirculation 21, 345–357 (2014). 37. M. Werner, A. Petersen, N. A. Kurniawan, C. V. C. Bouten, Cell-perceived substrate curvature dynamically coordinates the direction, speed, and persistence of stromal cell migration. Adv. Biosyst. 3, e1900080 (2019). 38. T. Naganuma, The relationship between cell adhesion force activation on nano/micro-topographical surfaces and temporal dependence of cell morphology. Nanoscale 9, 13171–13186 (2017). Downloaded from https://www.pnas.org by Elsevier Science London on October 18, 2022 from IP address 13.228.6.37. 39. J. Liu et al., Talin determines the nanoscale architecture of focal adhesions. Proc. Natl. Acad. Sci. U.S.A. 112, E4864–E4873 (2015). 40. H.-H. Chuang et al., Inhibition of FAK signaling elicits lamin A/C-associated nuclear deformity and cellular senescence. Front. Oncol. 9, 22 (2019). 41. B. M. Baker et al., Cell-mediated fibre recruitment drives extracellular matrix mechanosensing in engineered fibrillar microenvironments. Nat. Mater. 14, 1262–1268 (2015). 42. M. Kovács, J. Tóth, C. Hetényi, A. Málnási-Csizmadia, J. R. Sellers, Mechanism of blebbistatin inhibition of myosin II. J. Biol. Chem. 279, 35557–35563 (2004). 43. P. J. Marie, Targeting integrins to promote bone formation and repair. Nat. Rev. Endocrinol. 9, 288–295 (2013). 44. M.-Y. Shie, S.-J. Ding, Integrin binding and MAPK signal pathways in primary cell responses to surface chemistry of calcium silicate cements. Biomaterials 34, 6589–6606 (2013). 45. S. H. Ranganath, O. Levy, M. S. Inamdar, J. M. Karp, Harnessing the mesenchymal stem cell secretome for the treatment of cardiovascular disease. Cell Stem Cell 10, 244–258 (2012). 46. T.-L. Yew et al., Enhancement of wound healing by human multipotent stromal cell conditioned medium: The paracrine factors and p38 MAPK activation. Cell Transplant. 20, 693–706 (2011). 47. Y. Zhu, C. Goh, A. Shrestha, Biomaterial properties modulating bone regeneration. Macromol. Biosci. 21, e2000365 (2021). 48. Z. Chen et al., Influence of the pore size and porosity of selective laser melted Ti6Al4V ELI porous scaffold on cell proliferation, osteogenesis and bone ingrowth. Mater. Sci. Eng. C 106, 110289 (2020). 49. E. M. Hauge, D. Qvesel, E. F. Eriksen, L. Mosekilde, F. Melsen, Cancellous bone remodeling occurs in specialized compartments lined by cells expressing osteoblastic markers. J. Bone Miner. Res. 16, 1575–1582 (2001). 50. A. A. Vu, D. A. Burke, A. Bandyopadhyay, S. Bose, Effects of surface area and topography on 3D printed tricalcium phosphate scaffolds for bone grafting applications. Addit. Manuf. 39, 101870 (2021). 51. M. Mastrogiacomo et al., Role of scaffold internal structure on in vivo bone formation in macroporous calcium phosphate bioceramics. Biomaterials 27, 3230–3237 (2006). 52. J. Huang et al., Parathyroid hormone derivative with reduced osteoclastic activity promoted bone regeneration via synergistic bone remodeling and angiogenesis. Small 16, e1905876 (2020). 53. K. Bloch, A. Vanichkin, L. G. Damshkaln, V. I. Lozinsky, P. Vardi, Vascularization of wide pore agarose-gelatin cryogel scaffolds implanted subcutaneously in diabetic and non-diabetic mice. Acta Biomater. 6, 1200–1205 (2010). 54. Y. Yang et al., Gaussian curvature–driven direction of cell fate toward osteogenesis with triply periodic minimal surface scaffolds. NCBI: BioProject. https://www.ncbi.nlm.nih.gov/bioproject/ ?term=PRJNA763989. Deposited 16 September 2021. Funding Information: ACKNOWLEDGMENTS. This work was supported by the Excellent Young Scholars Projects from the National Science Foundation of China (Grant 82122002), the National Key R&D Program of China (Grant 2018YFA0703100), the Collaborative Research Fund (Grant C5044-21GF) from the Research Grants Council of Hong Kong, and the interdepartmental open project from the State Key Laboratory of Ultra-precision Machining Technology (Grant P0033576) and Departmental General Research Fund (G-UAKM, G-UAMY) from Department of Industrial and Systems Engineering from The Hong Kong Polytechnic University and the Strategic Interdisciplinary Research Grant (7020029) from City University of Hong Kong. We also appreciate the support from the University Research Facility in 3D Printing of The Hong Kong Polytechnic University. Publisher Copyright: Copyright © 2022 the Author(s). Published by PNAS.
PY - 2022/10/11
Y1 - 2022/10/11
N2 - Leaf photosynthesis, coral mineralization, and trabecular bone growth depend on triply periodic minimal surfaces (TPMSs) with hyperboloidal structure on every surface point with varying Gaussian curvatures. However, translation of this structure into tissue-engineered bone grafts is challenging. This article reports the design and fabrication of high-resolution three-dimensional TPMS scaffolds embodying biomimicking hyperboloidal topography with different Gaussian curvatures, composed of body inherent β-tricalcium phosphate, by stereolithography-based three-dimensional printing and sintering. The TPMS bone scaffolds show high porosity and interconnectivity. Notably, compared with conventional scaffolds, they can reduce stress concentration, leading to increased mechanical strength. They are also found to support the attachment, proliferation, osteogenic differentiation, and angiogenic paracrine function of human mesenchymal stem cells (hMSCs). Through transcriptomic analysis, we theorize that the hyperboloid structure induces cytoskeleton reorganization of hMSCs, expressing elongated morphology on the convex direction and strengthening the cytoskeletal contraction. The clinical therapeutic efficacy of the TPMS scaffolds assessed by rabbit femur defect and mouse subcutaneous implantation models demonstrate that the TPMS scaffolds augment new bone formation and neovascularization. In comparison with conventional scaffolds, our TPMS scaffolds successfully guide the cell fate toward osteogenesis through cell-level directional curvatures and demonstrate drastic yet quantifiable improvements in bone regeneration.
AB - Leaf photosynthesis, coral mineralization, and trabecular bone growth depend on triply periodic minimal surfaces (TPMSs) with hyperboloidal structure on every surface point with varying Gaussian curvatures. However, translation of this structure into tissue-engineered bone grafts is challenging. This article reports the design and fabrication of high-resolution three-dimensional TPMS scaffolds embodying biomimicking hyperboloidal topography with different Gaussian curvatures, composed of body inherent β-tricalcium phosphate, by stereolithography-based three-dimensional printing and sintering. The TPMS bone scaffolds show high porosity and interconnectivity. Notably, compared with conventional scaffolds, they can reduce stress concentration, leading to increased mechanical strength. They are also found to support the attachment, proliferation, osteogenic differentiation, and angiogenic paracrine function of human mesenchymal stem cells (hMSCs). Through transcriptomic analysis, we theorize that the hyperboloid structure induces cytoskeleton reorganization of hMSCs, expressing elongated morphology on the convex direction and strengthening the cytoskeletal contraction. The clinical therapeutic efficacy of the TPMS scaffolds assessed by rabbit femur defect and mouse subcutaneous implantation models demonstrate that the TPMS scaffolds augment new bone formation and neovascularization. In comparison with conventional scaffolds, our TPMS scaffolds successfully guide the cell fate toward osteogenesis through cell-level directional curvatures and demonstrate drastic yet quantifiable improvements in bone regeneration.
KW - bone regeneration
KW - hyperboloidal structure
KW - mesenchymal stem cells
KW - TPMS
UR - http://www.scopus.com/inward/record.url?scp=85139105274&partnerID=8YFLogxK
U2 - 10.1073/pnas.2206684119
DO - 10.1073/pnas.2206684119
M3 - Journal article
C2 - 36191194
AN - SCOPUS:85139105274
SN - 0027-8424
VL - 119
JO - Proceedings of the National Academy of Sciences of the United States of America
JF - Proceedings of the National Academy of Sciences of the United States of America
IS - 41
M1 - e2206684119
ER -