Fabrication of magnesium-doped porous polylactic acid microsphere for bone regeneration

doi:10.12336/biomatertransl.2023.04.007

Biomaterials Translational ›› 2023, Vol. 4 ›› Issue (4): 280-290.doi: 10.12336/biomatertransl.2023.04.007

• RESEARCH ARTICLE • Previous Articles Next Articles

Fabrication of magnesium-doped porous polylactic acid microsphere for bone regeneration

Ziwei Tao^1#, Ziyang Yuan^2#, Dong Zhou^3#, Lang Qin¹, Lan Xiao⁴, Shihao Zhang¹, Changsheng Liu¹^,^*(), Jinzhong Zhao²^,^*(), Yulin Li¹^,⁵^,^*()

1 Engineering Research Centre for Biomedical Materials of Ministry of Education, Key Laboratory for Ultrafine Materials of Ministry of Education, School of Materials Science and Engineering, East China University of Science and Technology, Shanghai, China
2 Department of Sports Medicine, Shanghai Sixth People’s Hospital Affiliated to Shanghai Jiao Tong University School of Medicine, Shanghai, China
3 School of Chemistry and Chemical Engineering, Nanchang University, Nanchang, Jiangxi Province, China
4 School of Mechanical, Medical and Process Engineering, Center of Biomedical Technology, Queensland University of Technology, Brisbane, Australia
5 Wenzhou Institute of Shanghai University, Wenzhou, Zhejiang Province, China

Received:2023-10-20 Revised:2023-11-14 Accepted:2023-11-25 Online:2023-12-27 Published:2023-12-28
Contact: Yulin Li, yulinli@ecust.edu.cn;Changsheng Liu, liucs@ecust.edu.cn;Jinzhong Zhao, jzzhao@sjtu.edu.cn.
About author:#Author equally.

Abstract

Abstract:

Biodegradable polymer microspheres that can be used as drug carriers are of great importance in biomedical applications, however, there are still challenges in controllable preparation of microsphere surface morphology and improvement of bioactivity. In this paper, firstly, poly(L-lactic acid) (PLLA) was synthesised by ring-opening polymerisation under anhydrous anaerobic conditions and further combined with the emulsion method, biodegradable PLLA microspheres (PM) with sizes ranging from 60–100 μm and with good sphericity were prepared. In addition, to further improve the surface morphology of PLLA microspheres and enhance their bioactivity, functionalised porous PLLA microspheres loaded with magnesium oxide (MgO)/magnesium carbonate (MgCO₃) (PMg) were also prepared by the emulsion method. The results showed that the loading of MgO/MgCO₃ resulted in the formation of a porous structure on the surface of the microspheres (PMg) and the dissolved Mg²⁺ could be released slowly during the degradation of microspheres. In vitro cellular experiments demonstrated the good biocompatibility of PM and PMg, while the released Mg²⁺ further enhanced the anti-inflammatory effect and osteogenic activity of PMg. Functionalised PMg not only show promise for controlled preparation of drug carriers, but also have translational potential for bone regeneration.

Key words: magnesium ion, osteogenesis, polylactic acid, porous microspheres

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Figures/Tables 8

Figure 1. Schematic preparation of poly(L-lactic acid) microsphere loaded with magnesium oxide (MgO)/magnesium carbonate (MgCO3) microspheres (PMg) and influence of PMg on tendon-derived stem cells (TDSCs). (A) PMg microspheres were obtained in the form of oil in water, dichloromethane (CH2Cl2) is the oil phase, and polyvinyl alcohol (PVA) is the water phase, the oil phase and the water phase are incompatible, so an oil-in-water system is formed, and during stirring, CH2Cl2 gradually evaporates, and poly(L-lactic acid) microsphere (PM) and PMg are formed. (B) PMg microspheres can maintain the continuing release of Mg2+ to promote the TDSC migration, proliferation, osteogenesis. Created with BioRender.com.

Table 1. The primer sequence for polymerase chain reaction

Gene	Primer sequence (5′-3′)
Arg-1	Forward: ATC AAC ACT CCG CTG ACA ACC
	Reverse: ATC TCG CAA GCC GAT GTA CAC
Runx-2	Forward: CGA ACA GAG CAA CAT CTC C
	Reverse: GTC AGT GCC TTC CTT GG
OCN	Forward: ACA AGT CCC ACA CAG CAA C
	Reverse: CCA GGT CAG AGA GGC AGA
GAPDH	Forward: CAA GAA GGT GGT GAA GCA G
	Reverse: CAA AGG TGG AAG AAT GGG

Figure 2. Chemical structure and microstructure analysis of poly(L-lactic acid) (PLLA). (A) Nuclear magnetic resonance spectroscopy, PLLA is a typical structure of polylactide, and the chemical structure of the polymer can be clearly analysed by measuring the chemical shift value of hydrogen. (B) Fourier transformed infrared spectrophotometer, the infrared visible light spectrum can clearly reflect the characteristic functional group structure in the polymer, and the polymer can be detected by the characteristic absorption peak. a.u.: arbitrary unit.

Figure 3. Characterisation of poly(L-lactic acid) microsphere (PM) and poly(L-lactic acid) microsphere loaded with magnesium oxide (MgO)/magnesium carbonate (MgCO3) (PMg). (A, B) Scanning electron micrograph image of PM (A) and PMg (B). (C, D) Particle size distribution of PM (C) and PMg (D). (E) Particle size of PM and PMg. Data are expressed as mean ± SD. (F) Fourier transformed infrared spectrophotometer spectra of PM and PMg. a.u.: arbitrary unit.

Figure 4. Enlarged microscopic images of poly(L-lactic acid) microsphere (PM) and poly(L-lactic acid) microsphere loaded with magnesium oxide (MgO)/magnesium carbonate (MgCO3) (PMg). (A-D) PM surface is smooth and without porous structure, and pores appeared on the surface of PMg, which was attributed to the generation of CO2 from MgCO3. Scale bars: 50 μm (A, C), 10 μm (B, D). (E) The distribution of pore size on the surface of PMg. (F) The contact angle test of PM and PMg. PMg is more hydrophilic and absorbent compared to PM. Data are expressed as mean ± SD.

Figure 5. In vitro degradation behaviours of poly(L-lactic acid) microsphere (PM) and poly(L-lactic acid) microsphere loaded with magnesium oxide (MgO)/magnesium carbonate (MgCO3) (PMg). (A) Accelerated degradation of PMg compared to PM, shows that MgO and MgCO3 accelerate the rate of molecular weight degradation of microspheres. (B) The degradation environment pH of PMg is stable in the neutral range and does not interfere with the body’s typical acidic and alkaline environment. (C) No sudden release of Mg2+ occurred during the 30-day degradation cycle. Data are expressed as mean ± SD, and were analysed by Student’s unpaired t-test. (D) The scanning electron micrograph images of PM before degradation. (E) On the 30th day of degradation, scanning electron micrograph image showed that there was a significant increase in the number of “craters” on the surface of PM. (F) Enlarged scanning electron micrograph images at 30 days of PM degradation (G) The scanning electron micrograph images of PMg before degradation. (H) At 30 days of degradation, the electron micrographs showed that the pores on the surface of PMg were significantly enlarged due to corrosion. (I) Enlarged scanning electron micrograph images at 30 days of PMg degradation. Scale bars: 50 μm (D, E, G, H), 10 μm (F, I).

Figure 6. Cytocompatibility evaluation and live-dead staining of poly(L-lactic acid) microsphere (PM) and poly(L-lactic acid) microsphere loaded with magnesium oxide (MgO)/magnesium carbonate (MgCO3) (PMg). (A) More than 80% of cell viability of tendon-derived stem cells (TDSCs) on PM and PMg, which were normalised by control group. Data are expressed as the mean ± SD (n = 3). *P < 0.05, ***P < 0.001 (one-way analysis of variance followed by Dunnett’s multiple comparisons test). (B) Cytocompatibility of TDSCs on PM and PMg. The live/dead staining assay demonstrated that PM and PMg exhibits no cytotoxicity to cells. TDSCs cultured with osteogenic medium were used as control. Scale bars: 200 μm.

Figure 7. Osteogenic capacity evaluation of poly(L-lactic acid) microsphere (PM) and poly(L-lactic acid) (PLLA) microsphere loaded with magnesium oxide (MgO)/magnesium carbonate (MgCO3) (PMg). (A) The level of alkaline phosphatase (ALP) was more obvious in PMg compared to PM. PMg has more osteogenic properties compared to PM, while PLLA material has some osteogenic properties compared to the control. (B) The expression of anti-inflammatory gene (arginase-1, Arg-1) was more obvious in PMg compared to PM. (C, D) The expression of osteogenic differentiation gene (osteocalcin, Ocn) and (Runx2) was more obvious in PMg compared to PM, while PLLA material can promote osteogenic differentiation of tendon-derived stem cells (TDSCs) compared to the control. RAW264.7 cells were induced with lipopolysaccharides as controls in B and TDSCs cultured with osteogenic medium were as controls in C and D. Data (normalised by control group) are expressed as the mean ± SD (n = 3). *P < 0.05, **P < 0.01 (one-way analysis of variance followed by Dunnett’s multiple comparisons test). GAPDH: glyceraldehyde-3-phosphate dehydrogenase.

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Fabrication of magnesium-doped porous polylactic acid microsphere for bone regeneration

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