Extracellular matrix decorated polycaprolactone scaffolds for improved mesenchymal stem/stromal cell osteogenesis towards a patient-tailored bone tissue engineering approach.
additive manufacturing
bone tissue engineering
cell-derived extracellular matrix
mesenchymal stem/stromal cells
polycaprolactone scaffolds
Journal
Journal of biomedical materials research. Part B, Applied biomaterials
ISSN: 1552-4981
Titre abrégé: J Biomed Mater Res B Appl Biomater
Pays: United States
ID NLM: 101234238
Informations de publication
Date de publication:
07 2020
07 2020
Historique:
received:
12
12
2018
revised:
05
12
2019
accepted:
20
12
2019
pubmed:
10
1
2020
medline:
6
11
2021
entrez:
10
1
2020
Statut:
ppublish
Résumé
The clinical demand for tissue-engineered bone is growing due to the increase of non-union fractures and delayed healing in an aging population. Herein, we present a method combining additive manufacturing (AM) techniques with cell-derived extracellular matrix (ECM) to generate structurally well-defined bioactive scaffolds for bone tissue engineering (BTE). In this work, highly porous three-dimensional polycaprolactone (PCL) scaffolds with desired size and architecture were fabricated by fused deposition modeling and subsequently decorated with human mesenchymal stem/stromal cell (MSC)-derived ECM produced in situ. The successful deposition of MSC-derived ECM onto PCL scaffolds (PCL-MSC ECM) was confirmed after decellularization using scanning electron microscopy, elemental analysis, and immunofluorescence. The presence of cell-derived ECM within the PCL scaffolds significantly enhanced MSC attachment and proliferation, with and without osteogenic supplementation. Additionally, under osteogenic induction, PCL-MSC ECM scaffolds promoted significantly higher calcium deposition and elevated relative expression of bone-specific genes, particularly the gene encoding osteopontin, when compared to pristine scaffolds. Overall, our results demonstrated the favorable effects of combining MSC-derived ECM and AM-based scaffolds on the osteogenic differentiation of MSC, resulting from a closer mimicry of the native bone niche. This strategy is highly promising for the development of novel personalized BTE approaches enabling the fabrication of patient defect-tailored scaffolds with enhanced biological performance and osteoinductive properties.
Substances chimiques
Biocompatible Materials
0
Polyesters
0
polycaprolactone
24980-41-4
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2153-2166Informations de copyright
© 2020 Wiley Periodicals, Inc.
Références
Badylak, S. F., Freytes, D. O., & Gilbert, T. W. (2009). Extracellular matrix as a biological scaffold material: Structure and function. Acta Biomaterialia, 5, 1-13.
Benders, K. E. M., van Weeren, P. R., Badylak, S. F., Saris, D. B. F., Dhert, W. J. A., & Malda, J. (2013). Extracellular matrix scaffolds for cartilage and bone regeneration. Trends in Biotechnology, 31, 169-176.
Boskey, A. L. (1995). Osteopontin and related phosphorylated Sialoproteins: Effects on mineralization. Annals of the New York Academy of Sciences, 760, 249-256.
Bracaglia, L. G., & Fisher, J. P. (2015). Extracellular matrix-based biohybrid materials for engineering compliant, matrix-dense tissues. Advanced Healthcare Materials, 4, 2475-2487.
Carvalho, M. S., Silva, J. C., Cabral, J. M. S., da Silva, C. L., & Vashishth, D. (2019). Cultured cell-derived extracellular matrices to enhance the osteogenic differentiation and angiogenic properties of human mesenchymal stem/stromal cells. Journal of Tissue Engineering and Regenerative Medicine, 13, 1544-1558.
Carvalho, M. S., Silva, J. C., Udangawa, R. N., Cabral, J. M. S., Ferreira, F. C., da Silva, C. L., … Vashishth, D. (2019). Co-culture cell-derived extracellular matrix loaded electrospun microfibrous scaffolds for bone tissue engineering. Materials Science and Engineering: C, 99, 479-490.
Cheng, C. W., Solorio, L. D., & Alsberg, E. (2014). Decellularized tissue and cell-derived extracellular matrices as scaffolds for orthopaedic tissue engineering. Biotechnology Advances, 32, 462-484.
Chiarello, E., Cadossi, M., Tedesco, G., Capra, P., Calamelli, C., Shehu, A., & Giannini, S. (2013). Autograft, allograft and bone substitutes in reconstructive orthopedic surgery. Aging Clinical and Experimental Research, 25, 101-103.
Choi, Y. C., Choi, J. S., Woo, C. H., & Cho, Y. W. (2014). Stem cell delivery systems inspired by tissue-specific niches. Journal of Controlled Release, 193, 42-50.
Datta, N., Holtorf, H. L., Sikavitsas, V. I., Jansen, J. A., & Mikos, A. G. (2005). Effect of bone extracellular matrix synthesized in vitro on the osteoblastic differentiation of marrow stromal cells. Biomaterials, 26, 971-977.
Datta, N., Pham, Q. P., Sharma, U., Sikavitsas, V. I., Jansen, J. A., & Mikos, A. G. (2006). In vitro generated extracellular matrix and fluid shear stress synergistically enhance 3D osteoblastic differentiation. Proceedings of the National Academy of Sciences, 103, 2488-2493.
Domingos, M., Chiellini, F., Gloria, A., Ambrosio, L., Bartolo, P., & Chiellini, E. (2012). Effect of process parameters on the morphological and mechanical properties of 3D bioextruded poly(ɛ-caprolactone) scaffolds. Rapid Prototyping Journal, 18, 56-67.
Endres, M., Hutmacher, D. W., Salgado, A. J., Kaps, C., Ringe, J., Reis, R. L., … Schantz, J. T. (2003). Osteogenic induction of human bone marrow-derived Mesenchymal progenitor cells in novel synthetic polymer-hydrogel matrices. Tissue Engineering, 9, 689-702.
Eosoly, S., Vrana, N. E., Lohfeld, S., Hindie, M., & Looney, L. (2012). Interaction of cell culture with composition effects on the mechanical properties of polycaprolactone-hydroxyapatite scaffolds fabricated via selective laser sintering (SLS). Materials Science and Engineering C, 32, 2250-2257.
Fernández-Pérez, J., & Ahearne, M. (2019). The impact of decellularization methods on extracellular matrix hydrogels. Scientific Reports, 9, 14993.
Fitzpatrick, L. E., & McDevitt, T. C. (2015). Cell-derived matrices for tissue engineering and regenerative medicine applications. Biomaterials Science, 3, 12-24.
Fu, Y., Liu, L., Cheng, R., & Cui, W. (2018). ECM decorated electrospun nanofiber for improving bone tissue regeneration. Polymers, 10, 272.
Gattazzo, F., Urciuolo, A., & Bonaldo, P. (2014). Extracellular matrix: A dynamic microenvironment for stem cell niche. Biochimica et Biophysica Acta (BBA) - General Subjects, 1840, 2506-2519.
Gericke, A., Qin, C., Spevak, L., Fujimoto, Y., Butler, W. T., Sørensen, E. S., & Boskey, A. L. (2005). Importance of phosphorylation for osteopontin regulation of biomineralization. Calcified Tissue International, 77, 45-54.
Gordeladze, J. O., Haugen, H. J., Lyngstadaas, S. P., & Reseland, J. E. (2017). Bone tissue engineering: State of the art, challenges, and prospects. In Tissue engineering for artificial organs: Regenerative medicine, smart diagnostics and personalized medicine (Vol. 2, pp. 525-551). Chennai, India: Wiley India Private Ltd.
Guler, Z., Silva, J. C., & Sezai Sarac, A. (2017). RGD functionalized poly(ε-caprolactone)/poly(m-anthranilic acid) electrospun nanofibers as high-performing scaffolds for bone tissue engineering RGD functionalized PCL/P3ANA nanofibers. International Journal of Polymeric Materials and Polymeric Biomaterials, 66, 139-148.
Hajiali, F., Tajbakhsh, S., & Shojaei, A. (2018). Fabrication and properties of polycaprolactone composites containing calcium phosphate-based ceramics and bioactive glasses in bone tissue engineering: A review. Polymer Reviews, 58, 164-207.
Harris, G. M., Raitman, I., & Schwarzbauer, J. E. (2018). Cell-derived decellularized matrices. Methods in Cell Biology, 143, 97-114.
Harvestine, J. N., Vollmer, N. L., Ho, S. S., Zikry, C. A., Lee, M. A., & Leach, J. K. (2016). Extracellular matrix-coated composite scaffolds promote Mesenchymal stem cell persistence and Osteogenesis. Biomacromolecules, 17, 3524-3531.
Hasan, A., Byambaa, B., Morshed, M., Cheikh, M. I., Shakoor, R. A., Mustafy, T., & Marei, H. E. (2018). Advances in osteobiologic materials for bone substitutes. Journal of Tissue Engineering and Regenerative Medicine, 12, 1448-1468.
Holmes, D. (2017). Non-union bone fracture: A quicker fix. Nature, 550, S193.
Hoshiba, T., Lu, H., Kawazoe, N., & Chen, G. (2010). Decellularized matrices for tissue engineering. Expert Opinion on Biological Therapy, 10, 1717-1728.
Hutmacher, D. W., Schantz, T., Zein, I., Ng, K. W., Teoh, S. H., & Tan, K. C. (2001). Mechanical properties and cell cultural response of polycaprolactone scaffolds designed and fabricated via fused deposition modeling. Journal of Biomedical Materials Research, 55, 203-216.
Hynes, R. O. (2009). The extracellular matrix: Not just pretty fibrils. Science, 326, 1216-1219.
Kang, Y., Kim, S., Bishop, J., Khademhosseini, A., & Yang, Y. (2012). The osteogenic differentiation of human bone marrow MSCs on HUVEC-derived ECM and β-TCP scaffold. Biomaterials, 33, 6998-7007.
Kang, Y., Kim, S., Khademhosseini, A., & Yang, Y. (2011). Creation of bony microenvironment with CaP and cell-derived ECM to enhance human bone-marrow MSC behavior and delivery of BMP-2. Biomaterials, 32, 6119-6130.
Kim, B., Ventura, R., & Lee, B. T. (2017). Functionalization of porous BCP scaffold by generating cell-derived extracellular matrix from rat bone marrow stem cells culture for bone tissue engineering. Journal of Tissue Engineering and Regenerative Medicine, 12, 1256-1267.
Kim, I. G., Hwang, M. P., Du, P., Ko, J., Ha, C.-W., Do, S. H., & Park, K. (2015). Bioactive cell-derived matrices combined with polymer mesh scaffold for osteogenesis and bone healing. Biomaterials, 50, 75-86.
Kim, J.-Y., Ahn, G., Kim, C., Lee, J.-S., Lee, I.-G., An, S.-H., … Shim, J. H. (2018). Synergistic effects of Beta tri-calcium phosphate and porcine-derived Decellularized bone extracellular matrix in 3D-printed Polycaprolactone scaffold on bone regeneration. Macromolecular Bioscience, 18, 1800025.
Kleinman, H. K., Philp, D., & Hoffman, M. P. (2003). Role of the extracellular matrix in morphogenesis. Current Opinion in Biotechnology, 14, 526-532.
Klontzas, M. E., Vernardis, S. I., Heliotis, M., Tsiridis, E., & Mantalaris, A. (2017). Metabolomics analysis of the osteogenic differentiation of umbilical cord blood mesenchymal stem cells reveals differential sensitivity to osteogenic agents. Stem Cells and Development, 26, 723-733.
Komori, T. (2009). Regulation of osteoblast differentiation by runx2 (pp. 43-49). Boston, MA: Osteoimmunology. Springer.
Ku, Y., Chung, C. P., & Jang, J. H. (2005). The effect of the surface modification of titanium using a recombinant fragment of fibronectin and vitronectin on cell behavior. Biomaterials, 26, 5153-5157.
Kundu, A. K., & Putnam, A. J. (2006). Vitronectin and collagen I differentially regulate osteogenesis in mesenchymal stem cells. Biochemical and Biophysical Research Communications, 347, 347-357.
Lai, Y., Sun, Y., Skinner, C. M., Son, E. L., Lu, Z., Tuan, R. S., … Chen, X.-D. (2010). Reconstitution of marrow-derived extracellular matrix ex vivo: A robust culture system for expanding large-scale highly functional human Mesenchymal stem cells. Stem Cells and Development, 19, 1095-1107.
Low, S. W., Ng, Y. J., Yeo, T. T., & Chou, N. (2009). Use of Osteoplug polycaprolactone implants as novel burr-hole covers. Singapore Medical Journal, 50, 777-780.
Martano, G., Borroni, E. M., Lopci, E., Cattaneo, M. G., Mattioli, M., Bachi, A., … Bifari, F. (2019). Metabolism of stem and progenitor cells: Proper methods to answer specific questions. Frontiers in Molecular Neuroscience, 12, 151.
Matsubara, T., Tsutsumi, S., Pan, H., Hiraoka, H., Oda, R., Nishimura, M., … Kato, Y. (2004). A new technique to expand human mesenchymal stem cells using basement membrane extracellular matrix. Biochemical and Biophysical Research Communications, 313, 503-508.
Melchels, F. P. W., Domingos, M. A. N., Klein, T. J., Malda, J., Bartolo, P. J., & Hutmacher, D. W. (2012). Additive manufacturing of tissues and organs. Progress in Polymer Science, 37, 1079-1104.
Mota, C., Puppi, D., Chiellini, F., & Chiellini, E. (2015). Additive manufacturing techniques for the production of tissue engineering constructs. Journal of Tissue Engineering and Regenerative Medicine, 9, 174-190.
Neves, L. S., Rodrigues, M. T., Reis, R. L., & Gomes, M. E. (2016). Current approaches and future perspectives on strategies for the development of personalized tissue engineering therapies. Expert Review of Precision Medicine and Drug Development, 1, 93-108.
Noh, Y. K., Du, P., Kim, I. G., Ko, J., Kim, S. W., & Park, K. (2016). Polymer mesh scaffold combined with cell-derived ECM for osteogenesis of human mesenchymal stem cells. Biomaterials Research, 20, 6.
Pati, F., Song, T. H., Rijal, G., Jang, J., Kim, S. W., & Cho, D. W. (2015). Ornamenting 3D printed scaffolds with cell-laid extracellular matrix for bone tissue regeneration. Biomaterials, 37, 230-241.
Patrício, T., Domingos, M., Gloria, A., & Bártolo, P. (2014). Fabrication and characterisation of PCL and PCL/PLA scaffolds for tissue engineering. Rapid Prototyping Journal, 20, 145-156.
Poh, P. S. P., Hutmacher, D. W., Holzapfel, B. M., Solanki, A. K., Stevens, M. M., & Woodruff, M. A. (2016). In vitro and in vivo bone formation potential of surface calcium phosphate-coated polycaprolactone and polycaprolactone/bioactive glass composite scaffolds. Acta Biomaterialia, 30, 319-333.
Ragelle, H., Naba, A., Larson, B. L., Zhou, F., Prijić, M., Whittaker, C. A., … Anderson, D. G. (2017). Comprehensive proteomic characterization of stem cell-derived extracellular matrices. Biomaterials, 128, 147-159.
Roseti, L., Parisi, V., Petretta, M., Cavallo, C., Desando, G., Bartolotti, I., & Grigolo, B. (2017). Scaffolds for bone tissue engineering: State of the art and new perspectives. Materials Science and Engineering C, 78, 1246-1262.
Rothrauff, B. B., Yang, G., & Tuan, R. S. (2017). Tissue-specific bioactivity of soluble tendon-derived and cartilage-derived extracellular matrices on adult mesenchymal stem cells. Stem Cell Research & Therapy, 8, 133.
Schantz, J. T., Lim, T. C., Ning, C., Swee, H. T., Kim, C. T., Shih, C. W., & Hutmacher, D. W. (2006). Cranioplasty after trephination using a novel biodegradable burr hole cover: Technical case report. Operative Neurosurgery, 58 ONS-E176. http://www.spartanmedspine.com/files/Cranioplasty-after-Trephination-using-Osteoplug.pdf
Silva, J. C., Moura, C. S., Alves, N., Cabral, J. M. S., & Ferreira, F. C. (2017). Effects of different fibre alignments and bioactive coatings on mesenchymal stem/stromal cell adhesion and proliferation in poly (ɛ-caprolactone) scaffolds towards cartilage repair. Procedia Manufacturing, 12, 132-140.
Solchaga, L. A., Penick, K., Goldberg, V. M., Caplan, A. I., & Welter, J. F. (2010). Fibroblast growth Factor-2 enhances proliferation and delays loss of Chondrogenic potential in human adult bone-marrow-derived Mesenchymal stem cells. Tissue Engineering Part A, 16, 1009-1019.
Thibault, R. A., Scott Baggett, L., Mikos, A. G., & Kasper, F. K. (2010). Osteogenic differentiation of Mesenchymal stem cells on Pregenerated extracellular matrix scaffolds in the absence of Osteogenic cell culture supplements. Tissue Engineering Part A, 16, 431-440.
Tour, G., Wendel, M., & Tcacencu, I. (2011). Cell-derived matrix enhances Osteogenic properties of hydroxyapatite. Tissue Engineering Part A, 17, 127-137.
Won, J.-E., Mateous-Timoneda, M. A., Castano, O., Planell, J. A., Seo, S.-J., Lee, E.-J., … Kim, H.-W. (2015). Fibronectin immobilization on to robotic-dispensed nanobioactive glass/polycaprolactone scaffolds for bone tissue engineering. Biotechnology Letters, 37, 935-942.
Zhang, W., Zhu, Y., Li, J., Guo, Q., Peng, J., Liu, S., … Wang, Y. (2016). Cell-derived extracellular matrix: Basic characteristics and current applications in orthopedic tissue engineering. Tissue Engineering Part B: Reviews, 22, 193-207.
Zurick, K. M., Qin, C., & Bernards, M. T. (2013). Mineralization induction effects of osteopontin, bone sialoprotein, and dentin phosphoprotein on a biomimetic collagen substrate. Journal of Biomedical Materials Research - Part A, 101, 1571-1581.