Biomaterials Translational ›› 2024, Vol. 5 ›› Issue (1): 69-83.doi: 10.12336/biomatertransl.2024.01.007
• RESEARCH ARTICLES • Previous Articles Next Articles
Jin Yang1,2, Kanwal Fatima1,2, Xiaojun Zhou1,2, Chuanglong He1,2,*(
)
Received:2023-12-06
Revised:2024-02-08
Accepted:2024-02-29
Online:2024-03-28
Published:2024-03-28
Contact:
Chuanglong He, 
Figure 1. Schematic illustration of the construction of PM@GS/PCL composite scaffold and the process of promoting bone regeneration in a rat femoral defect model. 3D: three-dimensional; GelMA: methacrylate gelatin; MSNs: mesoporous silica nanoparticles; PCL: polycaprolactone; PM: PTH@MSNs; PM@GS/PCL: PTH@MSNs/GelMA/SFMA/PCL; PM@GS: PTH@MSNs/GelMA/SFMA; PTH: parathyroid hormone (1–34); PTH@MSNs: PTH-loaded MSNs; SFMA: methacrylated silk fibroin.
Figure 2. Characterisation of MSNs and PMs. (A) TEM images of MSNs at various magnifications. Scale bars: 1 μm (left), 200 nm (middle) and 500 nm (right). (B) SEM images of MSNs at various magnifications. The nanoparticles of MSNs exhibited a homogeneous spherical shape with mesoporous structure. Scale bars: 200 nm (left), 100 nm (middle) and 50 nm (right). (C) The nitrogen absorption-desorption isotherm curves of MSNs and the pore size distribution inside. (D) Size distribution of MSNs and PMs. (E) Zeta potential results of different samples. MSNs: mesoporous silica nanoparticles; P: the equilibrium adsorption pressure of the gas; P0: the saturated vapour pressure of the gas at the adsorption temperature; PM: PTH@MSNs; PTH: parathyroid hormone (1–34); SEM: scanning electron microscope; TEM: transmission electron microscope.
Figure 3. Characterisation of composite scaffolds. (A) SEM images of PCL, GS/PCL and M@GS/PCL at various magnifications and representative photographs of composite scaffolds. Scale bars: 300 μm (upper), 200 μm (middle) and 20 μm (lower). (B) ATR-FTIR spectra of MSNs and different composite scaffolds. (C) Thermogravimetric curves of MSNs, PTH@MSNs and different composite scaffolds. (D) Compressive modulus of PCL and GS/PCL scaffolds. (E) Water contact angle of PCL and GS/PCL scaffolds. (F) The release curves of PTH from PTH@MSNs and PM@GS/PCL in PBS. Data in D-F are presented as the mean ± SD. ATR-FTIR: attenuated total reflectance-Fourier transform infrared; GelMA: methacrylate gelatin; GS: GelMA/SFMA composite hydrogel; M@GS/PCL: MSNs@GelMA/SFMA/PCL; MSNs: mesoporous silica nanoparticles; PBS: phosphate-buffered saline; PCL: polycaprolactone; PM: PTH@MSNs; PM@GS/PCL: PTH@MSNs/GelMA/SFMA/PCL; PTH: parathyroid hormone (1–34); SEM: scanning electron microscope; SFMA: methacrylated silk fibroin.
Figure 4. Impact of composite scaffolds on cell proliferation, migration and angiogenic activities. (A) BMSC proliferation on various scaffolds using a fluorescence microscope on days 1, 3 and 5. Viable cells were stained with Calcein-AM (green), while the dead cells were stained with PI (red). Scale bars: 500 μm. (B) Quantitative analysis of BMSCs proliferation with different scaffolds on days 1, 3 and 5 by CCK-8 assay. (C) Transwell migration assay for HUVECs at 24 hours using crystal violet staining. Scale bars: 500 μm. (D) Tube formation of HUVECs after 6 and 24 hours of incubation. Scale bars: 100 μm. (E–H) Quantitative assessment of angiogenic parameters, including total length, number of junctions, number of meshes, and total mesh area. Data are presented as the mean ± SD. *P < 0.05, **P < 0.01, ***P < 0.001 (one-way analysis of variance followed by Tukey’s post hoc test). BMSC: bone marrow-derived mesenchymal stem cell; CCK-8: cell counting kit-8; GS/PCL: GelMA/SFMA/PCL; GelMA: methacrylate gelatin; HUVEC: human umbilical vein endothelial cell; M@GS/PCL: MSNs@GelMA/SFMA/PCL; MSNs: mesoporous silica nanoparticles; PCL: polycaprolactone; PI: propidium iodide; PM@GS/PCL: PTH@MSNs/GelMA/SFMA/PCL; PTH: parathyroid hormone (1–34); SFMA: methacrylated silk fibroin.
Figure 5. In vitro osteogenic potential of scaffold extracts. (A) Representative images of ALP staining of BMSCs cultured with the conditioned medium from different scaffolds on days 7 and 14. Scale bars: 500 μm. (B) Representative images of ARS staining of BMSCs cultured with extracts from different scaffolds to observe the mineral matrix formation on days 14 and 21. Scale bars: 500 μm. (C) Quantitative result of ALP activity on days 7 and 14. (D) Quantitative result of ARS on days 14 and 21. (E–G) Expression of osteogenesis-related genes in BMSCs after incubation with different scaffold extracts for 7 and 14 days, including Runx2 (E), OCN (F), and OPN (G). Data are presented as the mean ± SD. *P < 0.05, **P < 0.01 (one-way analysis of variance followed by Tukey’s post hoc test). ALP: alkaline phosphatase; ARS: Alizarin red S; BMSC: bone marrow-derived mesenchymal stem cell; GS/PCL: GelMA/SFMA/PCL; GelMA: methacrylate gelatin; M@GS/PCL: MSNs@GelMA/SFMA/PCL; MSNs: mesoporous silica nanoparticles; OCN: osteocalcin; OPN: osteopontin; PCL: polycaprolactone; PM@GS/PCL: PTH@MSNs/GelMA/SFMA/PCL; PTH: parathyroid hormone (1–34); Runx2: runt-related transcription factor 2; SFMA: methacrylated silk fibroin.
Figure 6. Bone regeneration in rat femoral condyle defect model with a diameter of 3 mm. (A) 3D reconstructed micro-CT images after scaffold implantation for 4 and 8 weeks, including overall, cross-section, top view and side view. Black scale bars: 1 mm; white scale bars: 500 μm. (B) BMD, (C) BV/TV and (D) Tb. N analysis of newly formed bone tissues obtained from micro-CT results. Data are presented as the mean ± SD. *P < 0.05 (one-way analysis of variance followed by Tukey’s post hoc test). 3D: three-dimensional; BMD: bone mineral density; BV/TV: ratio of new bone volume to total volume; CT: computed tomography; GS/PCL: GelMA/SFMA/PCL; GelMA: methacrylate gelatin; M@GS/PCL: MSNs@GelMA/SFMA/PCL; MSNs: mesoporous silica nanoparticles; PCL: polycaprolactone; PM@GS/PCL: PTH@MSNs/GelMA/SFMA/PCL; PTH: parathyroid hormone (1–34); SFMA: methacrylated silk fibroin; Tb. N: trabecular number.
Figure 7. Histological analysis of femoral condyle defect at 8 weeks including H&E staining and Masson’s trichrome staining. Red circles indicate the areas of bone defect. Scale bars: 1 mm. GS/PCL: GelMA/SFMA/PCL; GelMA: methacrylate gelatin; H&E: haematoxylin and eosin; M@GS/PCL: MSNs@GelMA/SFMA/PCL; MSNs: mesoporous silica nanoparticles; PCL: polycaprolactone; PM@GS/PCL: PTH@MSNs/GelMA/SFMA/PCL; PTH: parathyroid hormone (1–34); SFMA: methacrylated silk fibroin.
Figure 8. Assessment of osteogenic potential of various scaffolds using immunofluorescence staining. (A) Fluorescence images of OCN (red), OPN (green), and CD31 (red) after implantation for 8 weeks. The nuclei were stained with DAPI (blue). (B–D) Quantification of OCN, OPN and CD31 expression. Data are presented as the mean ± SD (one-way analysis of variance followed by Tukey’s post hoc test). *P < 0.05. CD31: platelet endothelial cell adhesion molecule-1; DAPI: 4′,6-diamidino-2-phenylindole; GS/PCL: GelMA/SFMA/PCL; GelMA: methacrylate gelatin; M@GS/PCL: MSNs@GelMA/SFMA/PCL; MSNs: mesoporous silica nanoparticles; OCN: osteocalcin; OPN: osteopontin; PCL: polycaprolactone; PM@GS/PCL: PTH@MSNs/GelMA/SFMA/PCL; PTH: parathyroid hormone (1–34); SFMA: methacrylated silk fibroin.
Additional Figure 1. Compressive stress-strain curve of PCL and GS/PCL scaffolds. GelMA: methacrylate gelatin; GS/PCL: GelMA/SFMA/PCL; PCL: polycaprolactone; SFMA: methacrylated silk fibroin.
Additional Figure 2. Confocal microscopy images of BMSCs treated with MSNs (A) and fluorescein isothiocyanate-labelled MSNs (green; B) for 48 hours. The cytoskeleton was stained with Alexa Fluor 568 phalloidin (red), and the nucleus was stained with DAPI (blue). Scale bar: 20 μm. BMSCs: bone marrow-derived mesenchymal stem cells; DAPI: 4′,6-diamidino-2-phenylindole; MSNs: mesoporous silica nanoparticles.
Additional Figure 3. Effect of different scaffold extracts on the expression of angiogenesis-related genes in HUVECs at 48 hours. (A) CD31; (B) VEGF. Data are presented as the mean ± SD. **P < 0.01 (one-way analysis of variance followed by Tukey’s post hoc test). CD31: platelet endothelial cell adhesion molecule-1; GelMA: methacrylate gelatin; HUVECs: human umbilical vein endothelial cells; MSNs: mesoporous silica nanoparticles; PCL: polycaprolactone; GS/PCL: GelMA/SFMA/PCL; M@GS/PCL: MSNs/GelMA/SFMA/PCL; PM@GS/PCL: PTH@MSNs/GelMA/SFMA/PCL; PTH: parathyroid hormone (1–34); SFMA: methacrylated silk fibroin; VEGF: vascular endothelial growth factor.
| Gene | Primer sequence |
|---|---|
| BMSCs | |
| Runx2 | Forward: 5′-CAG TAT GAG AGT AGG TGT CCC GC-3′ |
| Reverse: 5′-AAG AGG GGT AAG ACT GGT CAT AGG-3′ | |
| OCN | Forward: 5'-CAA CCC CAA TTG TGA CGA GC-3′ |
| Reverse: 5'-GGC AAC ACA TGC CCT AAA CG-3′ | |
| OPN | Forward: 5′-GTC TTC CCG TTG CTG TCC TGA-3′ |
| Reverse: 5′-TGA GCT GCC AGA ATC AGT CAC T-3′ | |
| GAPDH | Forward: 5′-GAT GAA CAG TAT CCC GAT GCC A-3′ |
| Reverse: 5′-GGT GGA AGA ATG GGA GTT GCT-3′ | |
| HUVECs | |
| CD31 | Forward: 5′-CTG GCC CAG GAG TTT CCA GA-3′ |
| Reverse: 5′-GTT GCC ACT GTG CTC CAC CA-3′ | |
| VEGF | Forward: 5′-ACC GGC TCT GAC CAG GAG TT-3′ |
| Reverse: 5′-CGC CCA GGC TCC TGA ATC TT-3′ | |
| GAPDH | Forward: 5′-CAT GCC ATC ACT GCC ACC CA-3′ |
| Reverse: 5′-TGA CCT TGC CCA CAG CCT TG-3′ |
Additional Table 1. Primers for real-time polymerase chain reaction analysis in BMSCs and HUVECs
| Gene | Primer sequence |
|---|---|
| BMSCs | |
| Runx2 | Forward: 5′-CAG TAT GAG AGT AGG TGT CCC GC-3′ |
| Reverse: 5′-AAG AGG GGT AAG ACT GGT CAT AGG-3′ | |
| OCN | Forward: 5'-CAA CCC CAA TTG TGA CGA GC-3′ |
| Reverse: 5'-GGC AAC ACA TGC CCT AAA CG-3′ | |
| OPN | Forward: 5′-GTC TTC CCG TTG CTG TCC TGA-3′ |
| Reverse: 5′-TGA GCT GCC AGA ATC AGT CAC T-3′ | |
| GAPDH | Forward: 5′-GAT GAA CAG TAT CCC GAT GCC A-3′ |
| Reverse: 5′-GGT GGA AGA ATG GGA GTT GCT-3′ | |
| HUVECs | |
| CD31 | Forward: 5′-CTG GCC CAG GAG TTT CCA GA-3′ |
| Reverse: 5′-GTT GCC ACT GTG CTC CAC CA-3′ | |
| VEGF | Forward: 5′-ACC GGC TCT GAC CAG GAG TT-3′ |
| Reverse: 5′-CGC CCA GGC TCC TGA ATC TT-3′ | |
| GAPDH | Forward: 5′-CAT GCC ATC ACT GCC ACC CA-3′ |
| Reverse: 5′-TGA CCT TGC CCA CAG CCT TG-3′ |
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