Sonodynamic and Enzyme-like Activities of Niobium-based Coatings: Antimicrobial, Cell Proliferation and Cell Differentiation

doi:10.15541/jim20240160

Abstract

Abstract:

Currently, repair of infectious bone defects is still a clinical serious challenge. Here, a heterojunction coating of niobium oxide on pure niobium surface by using microarc oxidation and hydrothermal treatment was prepared. The results showed that the obtained heterogeneous junctions exhibited synchronously enzyme-like and ultrasonic dynamic properties triggered by ultrasound treatment, especially in acidic microenvironment of mimic bacterial infection. Under these key conditions, oxidase-like activity of the heterogeneous junctions was enhanced, generating several reactive oxygen species which can kill bacteria and remove their biofilm, with inhibition and clearance rates were 98.57% and 91.43%, respectively. Under simulated physiological conditions, ultrasound enhanced antioxidant-like enzyme activity of this kind heterogeneous junction, thereby scavenging reactive oxygen species, alleviating oxidative stress, and promoting proliferation and osteogenic differentiation of bone marrow mesenchymal stem cells (rBMSCs). In conclusion, the obtained niobium-based coatings with sonodynamic and enzyme-like activities have profound potential application prospects in infectious bone repair.

Key words: heterojunction, sonodynamic therapy, enzyme-like activity, antibacterial, osteogenic differentiation

CLC Number:

TG174

ZHANG Shumin, XI Xiaowen, SUN Lei, SUN Ping, WANG Deqiang, WEI Jie. Sonodynamic and Enzyme-like Activities of Niobium-based Coatings: Antimicrobial, Cell Proliferation and Cell Differentiation[J]. Journal of Inorganic Materials, 2024, 39(10): 1125-1134.

Figures/Tables 9

Fig. 1 Morphologies of Nb, MN and MN@FS (a) Photographs of Nb, MN and MN@FS; (b-g) SEM images of Nb (b, e), MN (c, f) and MN@FS (d, g); (h) EDS mappings of MN@FS; (i) Particle size distribution of Fe2S3 on the surface of MN@FS (MN: Nb2O5 coatings on pure niobium surfaces prepared by microarc oxidation treatment; FS: Fe2S3)

Fig. 2 XRD patterns (a) and XPS spectra (b-f) of MN and MN@FS (a) XRD patterns of MN and MN@FS; (b) Total XPS spectra of MN@FS; (c, d) High-resolution XPS spectrra of Nb3d (c) and O1s (d) of MN@FS; (e, f) High-resolution XPS spectra of Fe2p (e) and S2p (f) of MN@FS and Fe2S3

Fig. 3 Enzyme-like activity of the samples (a) MB degradation by different samples (pH 5.5); (b) ESR of ·OH production by MN@FS; (c) MB degradation by MN@FS versus pH; (d) Ti2(SO4)3 degradation by different samples (pH 7.4); (e) Oxygen production curves of different samples (pH 7.4, 10 mmol/L H2O2); (f) Mechanism of enzymatic catalytic activity; (g) MB degradation by MN@FS versus US power (pH 5.5, 10 mmol/L H2O2); (h) ESR of·OH production by MN@FS at different conditions (pH 5.5, 10 mmol/L H2O2, 0.5 W/cm2 US); (i) Oxygen production curves of MN@FS versus US power (pH 7.4, 10 mmol/L H2O2)

Fig. 4 Sonodynamic performance of the samples (a, c, d) Degradation of RhB (a), MB (c) and DPBF (d) by MN and MN@FS; (b) Degradation of RhB by MN@FS versus time; (e, f) ESR of ·OH (e) and ·O2- (f) production by MN and MN@FS with US; (g, h) Degradation of RhB (g) and ESR of ·OH production (h) by MN@FS under different conditions. The conditions for all ultrasound stimuli were 1.5 W/cm2, 1 MHz and 5 min, under pH 5.5 and 10 mmol/L H2O2 environment

Fig. 5 Mechanism and electrochemical analysis of the MN@FS heterojunction (a, b) Valence band XPS spectra of Nb2O5 (a) and Fe2S3 (b); (c, d) Tauc plots of Nb2O5 (c) and Fe2S3 (d); (e, f) EIS spectra (e) and transient acoustic-current responses (f) of Fe2S3, MN, and MN@FS; (g) PL spectra of MN and MN@FS; (h) Diagram of the ultrasonic dynamic mechanism of the heterogeneous junction

Fig. 6 Antimicrobial properties of the MN@FS heterojunction (a) Photographs of crystal violet staining; (b) Photographs of colonies; (c) Biofilm residual rate; (d) Antimicrobial rate of S. aureus (****: p < 0.0001, n=3)

Fig. 7 Analysis of the mechanism of sterilization and biofilm clearance by MN@FS (a, b) SEM (a) and ROS fluorescence staining (b) images of S. aureus; (c, d) Protein leakage without US (c) and with US (d) (****: p < 0.0001, n=3)

Fig. 8 Promotion effect of MN@FS on rBMSCs proliferation under oxidative stress conditions (200 μmol/L H2O2) (a, b) SEM (a) and CLSM (b) images of rBMSCs after incubation for different days; (c) Cell proliferation; (d) Cell viability; (e) CLSM images of ROS in cells (*: p < 0.05; ***: p < 0.001; ****: p < 0.0001, n=3)

Fig. 9 Promotion effect of MN@FS on rBMSCs osteogenic differentiation under oxidative stress conditions (200 μmol/L H2O2) (a, b) ALP (a) and alizarin red (b) staining images; (c, d) ALP activity (c) and calcium module formation (d) of rBMSCs at different days after culturing for different days (*: p < 0.05; **: p < 0.01; ***: p < 0.001, n=3)

References 32

[1]	DONG J Y, CHEN F M, YAO Y Y, et al. Bioactive mesoporous silica nanoparticle-functionalized titanium implants with controllable antimicrobial peptide release potentiate the regulation of inflammation and osseointegration. Biomaterials, 2024, 305: 122465.
[2]	ANTONIAC I, MANESCU V, ANTONIAC A, et al. Magnesium- based alloys with adapted interfaces for bone implants and tissue engineering. Regenerative Biomaterials, 2023, 10: rbad095.
[3]	BAI L, CHEN P R, ZHAO Y, et al. A micro/nano-biomimetic coating on titanium orchestrates osteo/angio-genesis and osteoimmunomodulation for advanced osseointegration. Biomaterials, 2021, 278: 121162.
[4]	XU X J, ZUO J H, ZENG H J, et al. Improving osseointegration potential of 3D printed PEEK implants with biomimetic periodontal ligament fiber hydrogel surface modifications. Advanced Functional Materials, 2023, 34: 2308811.
[5]	XIU P, JIA Z J, LV J, et al. Tailored surface treatment of 3D printed porous Ti₆Al₄V by microarc oxidation for enhanced osseointegration via optimized bone in-growth patterns and interlocked bone/implant interface. ACS Applied Materials & Interfaces, 2016, 8(28): 17964.
[6]	CHENG Y J, ZHANG Y F, ZHAO Z, et al. Guanidinium-decorated nanostructure for precision sonodynamic-catalytic therapy of MRSA- infected osteomyelitis. Advanced Materials, 2022, 34(50): 2206646.
[7]	XU P Y, KANKALA R K, WANG S B, et al. Sonodynamic therapy-based nanoplatforms for combating bacterial infections. Ultrasonics Sonochemistry, 2023, 100: 106617.
[8]	FENG X B, LEI J, MA L, et al. Ultrasonic interfacial engineering of MoS₂-modified Zn single-atom catalysts for efficient osteomyelitis sonodynamic ion therapy. Small, 2022, 18(8): 2105775.
[9]	ZHAO Y C, HUANG T, ZHANG X D, et al. Piezotronic and piezo-phototronic effects on sonodynamic disease therapy. Biomedical Engineering Materials, 2023, 1(1): e12006.
[10]	WANG Z R, ZHANG R F, YAN X Y, et al. Structure and activity of nanozymes: inspirations for de novo design of nanozymes. Materials Today, 2020, 41: 81.
[11]	MOU X Z, WU Q Y, ZHANG Z, et al. Nanozymes for regenerative medicine. Small Methods, 2022, 6(11): 2200997.
[12]	XU Z B, ZHU Y F, XIE M K, et al. Mackinawite nanozymes as reactive oxygen species scavengers for acute kidney injury alleviation. Journal of Nanobiotechnology, 2023, 21(1): 281.
[13]	ZHONG C X, LIANG D S, WAN T, et al. Ultrafine-grained Nb-Cu immiscible alloy implants for hard tissue repair: fabrication, characterization, and in vitro and in vivo evaluation. Journal of Materials Science & Technology, 2022, 127: 214.
[14]	SONG Y P, SUN Q, LUO J Q, et al. Cationic and anionic antimicrobial agents Co-templated mesostructured silica nanocomposites with a spiky nanotopology and enhanced biofilm inhibition performance. Nano-Micro Letters, 2022, 14(1): 83.
[15]	SATHASIVAM S, WILLIAMSON B A D, ALTHABAITI S A, et al. Chemical vapor deposition synthesis and optical properties of Nb₂O₅ thin films with hybrid functional theoretical insight into the band structure and band gaps. ACS Applied Materials & Interfaces, 2017, 9(21): 18031.
[16]	CHU Y, WANG P, DING Y H, et al. High-capacity Sb/Fe₂S₃ sodium-ion battery anodes fabricated by a one-step redox reaction, followed by ball milling with graphite. ACS Applied Materials & Interfaces, 2023, 15(20): 24354.
[17]	RAJAN S T, SENTHILNATHAN J, AROCKIARAJAN A. Sputter-coated N-enriched mixed metal oxides (Ta₂O₅-Nb₂O₅-N) composite: a resilient solar driven photocatalyst for water purification. Journal of Hazardous Materials, 2023, 452: 131283.
[18]	TIAN F, WANG S Y, SHI K D, et al. Dual-depletion of intratumoral lactate and ATP with radicals generation for cascade metabolic- chemodynamic therapy. Advanced Science, 2021, 8(24): 2102595.
[19]	ZHANG S X, WANG L R, XU T L, et al. Luminescent MOF- based nanofibers with visual monitoring and antibacterial properties for diabetic wound healing. ACS Applied Materials & Interfaces, 2023, 15(7): 9110.
[20]	WANG X A, LIU T, CHEN M X, et al. An erythrocyte-templated iron single-atom nanozyme for wound healing. Advanced Science, 2024, 11(6): 2307844.
[21]	GAO Z G, LI Y J, ZHANG Y, et al. Biomimetic platinum nanozyme immobilized on 2D metal-organic frameworks for mitochondrion-targeting and oxygen self-supply photodynamic therapy. ACS Applied Materials & Interfaces, 2020, 12(2): 1963.
[22]	WANG Z Q, LI G L, GAO Y, et al. Trienzyme-like iron phosphates- based (FePOs) nanozyme for enhanced anti-tumor efficiency with minimal side effects. Chemical Engineering Journal, 2021, 404: 125574.
[23]	HE D C, WANG W J, FENG N, et al. Defect-modified nano- BaTiO₃ as a sonosensitizer for rapid and high-efficiency sonodynamic sterilization. ACS Applied Materials & Interfaces, 2023, 15(12): 15140.
[24]	LIANG S, XIAO X, BAI L X, et al. Conferring Ti-based MOFs with defects for enhanced sonodynamic cancer therapy. Advanced Materials, 2021, 33(18): 2100333.
[25]	GENG B J, HU J Y, LI Y, et al. Near-infrared phosphorescent carbon dots for sonodynamic precision tumor therapy. Nature Communications, 2022, 13: 5735. DOI PMID
[26]	BOOTLUCK W, CHITTRAKARN T, TECHATO K, et al. S-Scheme α-Fe₂O₃/TiO₂ photocatalyst with Pd cocatalyst for enhanced photocatalytic H₂ production activity and stability. Catalysis Letters, 2022, 152(9): 2590.
[27]	WANG Y W, HU X S, SONG H R, et al. Oxygen vacancies in actiniae-like Nb₂O₅/Nb₂C MXene heterojunction boosting visible light photocatalytic NO removal. Applied Catalysis B-Environmental, 2021, 299: 120677.
[28]	TAYYAB M, LIU Y J, LIU Z G, et al. One-pot in-situ hydrothermal synthesis of ternary In₂S₃/Nb₂O₅/Nb₂C Schottky/ S-scheme integrated heterojunction for efficient photocatalytic hydrogen production. Journal of Colloid and Interface Science, 2022, 628: 500.
[29]	XING F Y, WANG C Z, LIU S Q, et al. Interfacial chemical bond engineering in a direct Z-scheme g-C₃N₄/MoS₂ heterojunction. ACS Applied Materials & Interfaces, 2023, 15(9): 11731.
[30]	YANG L, TIAN B S, XIE Y, et al. Oxygen-vacancy-rich piezoelectric BiO_2-_x nanosheets for augmented piezocatalytic, sonothermal, and enzymatic therapies. Advanced Materials, 2023, 35(29): 2300648.
[31]	DENG R X, ZHOU H, QIN Q X, et al. Palladium-catalyzed hydrogenation of black barium titanate for multienzyme- piezoelectric synergetic tumor therapy. Advanced Materials, 2024, 36: 2307568.
[32]	RONG Q, LI S Y, ZHOU Y, et al. A novel method to improve the osteogenesis capacity of hUCMSCs with dual-directional pre- induction under screened co-culture conditions. Cell Proliferation, 2020, 53(2): e12740.