Functionalized 3D-Printed ST2/Gelatin Methacryloyl/Polcaprolactone Scaffolds for Enhancing Bone Regeneration with Vascularization

Growth factors were often used to improve the bioactivity of biomaterials in order to fabricate biofunctionalized bone grafts for bone defect repair. However, supraphysiological concentrations of growth factors for improving bioactivity could lead to serious side effects, such as ectopic bone formation, radiculitis, swelling of soft tissue in the neck, etc. Therefore, safely and effectively applying growth factors in bone repair biomaterials comes to be an urgent problem that needs to be addressed. In this study, an appropriate concentration (50 ng/mL) of Wnt3a was used to pretreat the 3D-bioprinting gelatin methacryloyl(GelMA)/polycaprolactone(PCL) scaffold loaded with bone marrow stromal cell line ST2 for 24 h. This pretreatment promoted the cell proliferation, osteogenic differentiation, and mineralization of ST2 in the scaffold in vitro, and enhanced angiogenesis and osteogenesis after being implanted in critical-sized mouse calvarial defects. On the contrary, the inhibition of Wnt/β-catenin signaling in ST2 cells reduced the bone repair effect of this scaffold. These results suggested that ST2/GelMA/PCL scaffolds pretreated with an appropriate concentration of Wnt3a in culture medium could effectively enhance the osteogenic and angiogenic activity of bone repair biomaterials both in vitro and in vivo. Moreover, it would avoid the side effects caused by the supraphysiological concentrations of growth factors. This functionalized scaffold with osteogenic and angiogenic activity might be used as an outstanding bone substitute for bone regeneration and repair.

[1]  S. Nandi,et al.  Strategies for Enhancing Vascularization of Biomaterial‐Based Scaffold in Bone Regeneration , 2022, Chemical record.

[2]  Dekun Zhang,et al.  Freestanding vascular scaffolds engineered by direct 3D printing with Gt-Alg-MMT bioinks. , 2022, Materials science & engineering. C, Materials for biological applications.

[3]  A. C. Jayasuriya,et al.  FDA-approved bone grafts and bone graft substitute devices in bone regeneration. , 2021, Materials science & engineering. C, Materials for biological applications.

[4]  L. Meseguer-Olmo,et al.  Modifications in Gene Expression in the Process of Osteoblastic Differentiation of Multipotent Bone Marrow-Derived Human Mesenchymal Stem Cells Induced by a Novel Osteoinductive Porous Medical-Grade 3D-Printed Poly(ε-caprolactone)/β-tricalcium Phosphate Composite , 2021, International journal of molecular sciences.

[5]  Z. Wu,et al.  Biocompatibility evaluation of a 3D-bioprinted alginate-GelMA-bacteria nanocellulose (BNC) scaffold laden with oriented-growth RSC96 cells. , 2021, Materials science & engineering. C, Materials for biological applications.

[6]  Jia Liu,et al.  Photo-crosslinked GelMA/collagen membrane loaded with lysozyme as an antibacterial corneal implant. , 2021, International journal of biological macromolecules.

[7]  A. Aszódi,et al.  A novel in vitro assay to study chondrocyte-to-osteoblast transdifferentiation , 2021, Endocrine.

[8]  S. How,et al.  Fabrication of Hydroxyapatite with Bioglass Nanocomposite for Human Wharton’s-Jelly-Derived Mesenchymal Stem Cell Growing Substrate , 2021, International journal of molecular sciences.

[9]  M. Finšgar,et al.  The Role of Growth Factors in Bioactive Coatings , 2021, Pharmaceutics.

[10]  D. Kaplan,et al.  Functionalized 3D-printed silk-hydroxyapatite scaffolds for enhanced bone regeneration with innervation and vascularization. , 2021, Biomaterials.

[11]  L. Lagneaux,et al.  Cross-Talk Between Mesenchymal Stromal Cells (MSCs) and Endothelial Progenitor Cells (EPCs) in Bone Regeneration , 2021, Frontiers in Cell and Developmental Biology.

[12]  L. Chow,et al.  Strategies to Control or Mimic Growth Factor Activity for Bone, Cartilage, and Osteochondral Tissue Engineering. , 2021, Bioconjugate chemistry.

[13]  R. Lauster,et al.  3D bioprinting of tissue-specific osteoblasts and endothelial cells to model the human jawbone , 2021, Scientific Reports.

[14]  S. Root,et al.  Wnt/β-Catenin Signaling Promotes the Formation of Preodontoblasts In Vitro , 2020, Journal of dental research.

[15]  Liang Gao,et al.  Smurf1-targeting miR-19b-3p-modified BMSCs combined PLLA composite scaffold to enhance osteogenic activity and treat critical-sized bone defects. , 2020, Biomaterials science.

[16]  E. Mazzon,et al.  Functional Relationship between Osteogenesis and Angiogenesis in Tissue Regeneration , 2020, International journal of molecular sciences.

[17]  Lin Deng,et al.  Cyclooxygenase-2 and β-Catenin as Potential Diagnostic and Prognostic Markers in Endometrial Cancer , 2020, Frontiers in Oncology.

[18]  Shaokai Liu,et al.  A biocompatible vascularized graphene oxide (GO)-collagen chamber with osteoinductive and anti-fibrosis effects promotes bone regeneration in vivo , 2020, Theranostics.

[19]  L. Mei,et al.  Estrogen Enhances Osteogenic Differentiation of Human Periodontal Ligament Stem Cells by Activating the Wnt/β-Catenin Signaling Pathway. , 2020, The Journal of craniofacial surgery.

[20]  Mikaël M. Martino,et al.  Growth factors with enhanced syndecan binding generate tonic signalling and promote tissue healing , 2019, Nature Biomedical Engineering.

[21]  J. Fisher,et al.  3D printed HUVECs/MSCs cocultures impact cellular interactions and angiogenesis depending on cell-cell distance. , 2019, Biomaterials.

[22]  Bin Huang,et al.  Orcinol glucoside facilitates the shift of MSC fate to osteoblast and prevents adipogenesis via Wnt/β-catenin signaling pathway , 2019, Drug design, development and therapy.

[23]  R. Vasita,et al.  Dual functional approaches for osteogenesis coupled angiogenesis in bone tissue engineering. , 2019, Materials science & engineering. C, Materials for biological applications.

[24]  H. Yokota,et al.  Wnt3a involved in the mechanical loading on improvement of bone remodeling and angiogenesis in a postmenopausal osteoporosis mouse model , 2019, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[25]  Bin Zhang,et al.  3D cell-based biosensor for cell viability and drug assessment by 3D electric cell/matrigel-substrate impedance sensing. , 2019, Biosensors & bioelectronics.

[26]  Sooyeon Lee,et al.  Wnt signaling and bone regeneration: Can't have one without the other. , 2019, Biomaterials.

[27]  Chia-Che Ho,et al.  3D-Printed Bioactive Calcium Silicate/Poly-ε-Caprolactone Bioscaffolds Modified with Biomimetic Extracellular Matrices for Bone Regeneration , 2019, International journal of molecular sciences.

[28]  M. Ho,et al.  Alpha-5 Integrin Mediates Simvastatin-Induced Osteogenesis of Bone Marrow Mesenchymal Stem Cells , 2019, International journal of molecular sciences.

[29]  M. Leu,et al.  Near-field electrospinning of a polymer/bioactive glass composite to fabricate 3D biomimetic structures , 2018, International journal of bioprinting.

[30]  Liangliang Wang,et al.  Inhibition of protein phosphatase 2A attenuates titanium-particle induced suppression of bone formation. , 2019, International journal of biological macromolecules.

[31]  Niklas Sandler,et al.  Vascularized 3D printed scaffolds for promoting bone regeneration. , 2019, Biomaterials.

[32]  H. Ghanbari,et al.  Comparative study of different polymeric coatings for the next-generation magnesium-based biodegradable stents , 2018, Artificial cells, nanomedicine, and biotechnology.

[33]  Cheng-Ting Shih,et al.  Osteogenic and angiogenic potentials of the cell-laden hydrogel/mussel-inspired calcium silicate complex hierarchical porous scaffold fabricated by 3D bioprinting. , 2018, Materials science & engineering. C, Materials for biological applications.

[34]  T. Best,et al.  Tissue Engineering and Cell-Based Therapies for Fractures and Bone Defects , 2018, Front. Bioeng. Biotechnol..

[35]  Gang Wu,et al.  Tissue-Engineered Bone Immobilized with Human Adipose Stem Cells-Derived Exosomes Promotes Bone Regeneration. , 2018, ACS applied materials & interfaces.

[36]  J. Orbe,et al.  Combined sustained release of BMP2 and MMP10 accelerates bone formation and mineralization of calvaria critical size defect in mice , 2018, Drug delivery.

[37]  Wenmiao Shu,et al.  3D bioactive composite scaffolds for bone tissue engineering , 2017, Bioactive materials.

[38]  Ling Wei,et al.  Intranasally Delivered Wnt3a Improves Functional Recovery after Traumatic Brain Injury by Modulating Autophagic, Apoptotic, and Regenerative Pathways in the Mouse Brain. , 2018, Journal of neurotrauma.

[39]  S. Pluchino,et al.  Wnt3a promotes pro-angiogenic features in macrophages in vitro: Implications for stroke pathology , 2018, Experimental biology and medicine.

[40]  N. Ward,et al.  The Role of Wnt Signalling in Angiogenesis. , 2017, The Clinical biochemist. Reviews.

[41]  E. Badiavas,et al.  Bone Marrow Mesenchymal Stem Cell-Derived CD63+ Exosomes Transport Wnt3a Exteriorly and Enhance Dermal Fibroblast Proliferation, Migration, and Angiogenesis In Vitro. , 2017, Stem cells and development.

[42]  T. Reichert,et al.  WNT3A and the induction of the osteogenic differentiation in adipose tissue derived mesenchymal stem cells. , 2017, Tissue & cell.

[43]  K. Yeung,et al.  Bone grafts and biomaterials substitutes for bone defect repair: A review , 2017, Bioactive materials.

[44]  W. Jiskoot,et al.  Formulation, Delivery and Stability of Bone Morphogenetic Proteins for Effective Bone Regeneration , 2017, Pharmaceutical Research.

[45]  A. Petrie,et al.  Effect of Wnt3a delivery on early healing events during guided bone regeneration , 2017, Clinical oral implants research.

[46]  A. Robling,et al.  Control of Bone Anabolism in Response to Mechanical Loading and PTH by Distinct Mechanisms Downstream of the PTH Receptor , 2017, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[47]  L. Qin,et al.  Angiogenesis Assays for the Evaluation of Angiogenic Properties of Orthopaedic Biomaterials – A General Review , 2017, Advanced healthcare materials.

[48]  S. Dooley,et al.  BMP9 a possible alternative drug for the recently withdrawn BMP7? New perspectives for (re-)implementation by personalized medicine , 2016, Archives of Toxicology.

[49]  F. Fan,et al.  Mesenchymal stem cells stimulate intestinal stem cells to repair radiation-induced intestinal injury , 2016, Cell Death and Disease.

[50]  Ling-ling Wei,et al.  Co-cultured hBMSCs and HUVECs on human bio-derived bone scaffolds provide support for the long-term ex vivo culture of HSC/HPCs. , 2016, Journal of biomedical materials research. Part A.

[51]  James J. Yoo,et al.  A 3D bioprinting system to produce human-scale tissue constructs with structural integrity , 2016, Nature Biotechnology.

[52]  N. Artigas,et al.  Mesenchymal Stem Cells Within Gelatin/CaSO4 Scaffolds Treated Ex Vivo with Low Doses of BMP-2 and Wnt3a Increase Bone Regeneration. , 2016, Tissue engineering. Part A.

[53]  J. Helms,et al.  Reengineering autologous bone grafts with the stem cell activator WNT3A. , 2015, Biomaterials.

[54]  Hui Shi,et al.  Human Umbilical Cord Mesenchymal Stem Cell Exosomes Enhance Angiogenesis Through the Wnt4/β‐Catenin Pathway , 2015, Stem cells translational medicine.

[55]  Y. Zhou,et al.  Bio-inspired hard-to-soft interface for implant integration to bone. , 2015, Nanomedicine : nanotechnology, biology, and medicine.

[56]  D. Burr,et al.  Osteocytes mediate the anabolic actions of canonical Wnt/β-catenin signaling in bone , 2015, Proceedings of the National Academy of Sciences.

[57]  R. Reis,et al.  Controlled release strategies for bone, cartilage, and osteochondral engineering--Part II: challenges on the evolution from single to multiple bioactive factor delivery. , 2013, Tissue engineering. Part B, Reviews.

[58]  R. Nusse,et al.  Translating insights from development into regenerative medicine: the function of Wnts in bone biology. , 2008, Seminars in cell & developmental biology.