Ultrasound-driven radical chain reaction and immunoregulation of piezoelectric-based hybrid coating for treating implant infection

Menglin Sun; Jiameng Wang; Xiaobo Huang; Ruiqiang Hang; Peide Han; Jiqiang Guo; Xiaohong Yao; Paul K. Chu; Xiangyu Zhang

doi:10.1016/j.biomaterials.2024.122532

Ultrasound-driven radical chain reaction and immunoregulation of piezoelectric-based hybrid coating for treating implant infection

Menglin Sun, Jiameng Wang, Xiaobo Huang, Ruiqiang Hang, Peide Han, Jiqiang Guo, Xiaohong Yao^*, Paul K. Chu^*, Xiangyu Zhang^*

^*Corresponding author for this work

Research output: Journal Publications and Reviews › RGC 21 - Publication in refereed journal › peer-review

32 Citations (Scopus)

Abstract

The poor efficiency of US-responsive coatings on implants restricts their practical application. Immunotherapy that stimulates immune cells to enhance their antibacterial activity is expected to synergize with sonodynamic therapy for treating implant infection effectively and safely. Herein, US-responsive hybrid coatings composed of the oxygen-deficient BaTiO₃ nanorod arrays and L-arginine (BaTiO_3-x/LA) are designed and prepared on titanium implants for sonocatalytic therapy-cooperated immunotherapy to treat Methicillin-resistant Staphylococcus aureus (MRSA) infection. BaTiO_3-x/LA can generate more oxidizing reactive oxygen species (ROS, hydroxyl radical (·OH)) and reactive nitrogen species (RNS, peroxynitrite anion (ONOO⁻)). The construction of nanorod arrays and oxygen defects balances the piezoelectric properties and sonocatalytic capability during US treatment. The generated piezoelectric electric field provides a sufficient driving force to separate electrons and holes, and the oxygen defects attenuate the electron-hole recombination efficiency, consequently increasing the yield of ROS during the US treatment. Moreover, nitric oxide (NO) released by L-arginine reacts with the superoxide radical (·O₂⁻) to produce ONOO⁻. Since, this radical chain reaction improves the oxidizing ability between bacteria and radicals, the cell membrane (argB, secA2) and DNA (dnaBGXN) are destroyed. The bacterial self-repair mechanism indirectly accelerates bacterial death based on the transcriptome analysis. In addition to participating in the radical chain reaction, NO positively affects macrophage M1 polarization to yield potent phagocytosis to MRSA. As a result, without introducing an extra sonosensitizer, BaTiO_3-x/LA exhibits excellent antibacterial activity against MRSA after the US treatment for 15 min. Furthermore, BaTiO_3-x/LA facilitates macrophage M2 polarization after implantation and improves osteogenic differentiation. The combined effects of sonodynamic therapy and immunoregulation lead to an effective and safe treatment method for implant-associated infections. © 2024 Elsevier Ltd

Original language	English
Article number	122532
Journal	Biomaterials
Volume	307
Online published	14 Mar 2024
DOIs	https://doi.org/10.1016/j.biomaterials.2024.122532
Publication status	Published - Jun 2024

Funding

This work was financially supported by the National Natural Science Foundation of China (52171240), Major Projects in Research and Development of Shanxi (202102130501007), City University of Hong Kong Donation Research Grant (grant number DON-RMG 9229021), Hong Kong PDFS - RGC Postdoctoral Fellowship Scheme (PDFS2122-1S08 and CityU 9061014), and Hong Kong HMRF (Health and Medical Research Fund) (2120972 and CityU 9211320).

Research Keywords

Bacterial infection
Immunoregulation
Piezoelectric nanorod array
Sonodynamic therapy
Titanium implants

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

Access Output

10.1016/j.biomaterials.2024.122532

Other Access Options

Check CityUHK Library

Permanent Link

Right click to copy link

Cite this

@article{5fa5535fe0494d038e0b91cdc69bc7de,

title = "Ultrasound-driven radical chain reaction and immunoregulation of piezoelectric-based hybrid coating for treating implant infection",

abstract = "The poor efficiency of US-responsive coatings on implants restricts their practical application. Immunotherapy that stimulates immune cells to enhance their antibacterial activity is expected to synergize with sonodynamic therapy for treating implant infection effectively and safely. Herein, US-responsive hybrid coatings composed of the oxygen-deficient BaTiO3 nanorod arrays and L-arginine (BaTiO3-x/LA) are designed and prepared on titanium implants for sonocatalytic therapy-cooperated immunotherapy to treat Methicillin-resistant Staphylococcus aureus (MRSA) infection. BaTiO3-x/LA can generate more oxidizing reactive oxygen species (ROS, hydroxyl radical (·OH)) and reactive nitrogen species (RNS, peroxynitrite anion (ONOO−)). The construction of nanorod arrays and oxygen defects balances the piezoelectric properties and sonocatalytic capability during US treatment. The generated piezoelectric electric field provides a sufficient driving force to separate electrons and holes, and the oxygen defects attenuate the electron-hole recombination efficiency, consequently increasing the yield of ROS during the US treatment. Moreover, nitric oxide (NO) released by L-arginine reacts with the superoxide radical (·O2−) to produce ONOO−. Since, this radical chain reaction improves the oxidizing ability between bacteria and radicals, the cell membrane (argB, secA2) and DNA (dnaBGXN) are destroyed. The bacterial self-repair mechanism indirectly accelerates bacterial death based on the transcriptome analysis. In addition to participating in the radical chain reaction, NO positively affects macrophage M1 polarization to yield potent phagocytosis to MRSA. As a result, without introducing an extra sonosensitizer, BaTiO3-x/LA exhibits excellent antibacterial activity against MRSA after the US treatment for 15 min. Furthermore, BaTiO3-x/LA facilitates macrophage M2 polarization after implantation and improves osteogenic differentiation. The combined effects of sonodynamic therapy and immunoregulation lead to an effective and safe treatment method for implant-associated infections. {\textcopyright} 2024 Elsevier Ltd",

keywords = "Bacterial infection, Immunoregulation, Piezoelectric nanorod array, Sonodynamic therapy, Titanium implants",

author = "Menglin Sun and Jiameng Wang and Xiaobo Huang and Ruiqiang Hang and Peide Han and Jiqiang Guo and Xiaohong Yao and Chu, {Paul K.} and Xiangyu Zhang",

year = "2024",

month = jun,

doi = "10.1016/j.biomaterials.2024.122532",

language = "English",

volume = "307",

journal = "Biomaterials",

issn = "0142-9612",

publisher = "Elsevier Ltd.",

}

TY - JOUR

T1 - Ultrasound-driven radical chain reaction and immunoregulation of piezoelectric-based hybrid coating for treating implant infection

AU - Sun, Menglin

AU - Wang, Jiameng

AU - Huang, Xiaobo

AU - Hang, Ruiqiang

AU - Han, Peide

AU - Guo, Jiqiang

AU - Yao, Xiaohong

AU - Chu, Paul K.

AU - Zhang, Xiangyu

PY - 2024/6

Y1 - 2024/6

N2 - The poor efficiency of US-responsive coatings on implants restricts their practical application. Immunotherapy that stimulates immune cells to enhance their antibacterial activity is expected to synergize with sonodynamic therapy for treating implant infection effectively and safely. Herein, US-responsive hybrid coatings composed of the oxygen-deficient BaTiO3 nanorod arrays and L-arginine (BaTiO3-x/LA) are designed and prepared on titanium implants for sonocatalytic therapy-cooperated immunotherapy to treat Methicillin-resistant Staphylococcus aureus (MRSA) infection. BaTiO3-x/LA can generate more oxidizing reactive oxygen species (ROS, hydroxyl radical (·OH)) and reactive nitrogen species (RNS, peroxynitrite anion (ONOO−)). The construction of nanorod arrays and oxygen defects balances the piezoelectric properties and sonocatalytic capability during US treatment. The generated piezoelectric electric field provides a sufficient driving force to separate electrons and holes, and the oxygen defects attenuate the electron-hole recombination efficiency, consequently increasing the yield of ROS during the US treatment. Moreover, nitric oxide (NO) released by L-arginine reacts with the superoxide radical (·O2−) to produce ONOO−. Since, this radical chain reaction improves the oxidizing ability between bacteria and radicals, the cell membrane (argB, secA2) and DNA (dnaBGXN) are destroyed. The bacterial self-repair mechanism indirectly accelerates bacterial death based on the transcriptome analysis. In addition to participating in the radical chain reaction, NO positively affects macrophage M1 polarization to yield potent phagocytosis to MRSA. As a result, without introducing an extra sonosensitizer, BaTiO3-x/LA exhibits excellent antibacterial activity against MRSA after the US treatment for 15 min. Furthermore, BaTiO3-x/LA facilitates macrophage M2 polarization after implantation and improves osteogenic differentiation. The combined effects of sonodynamic therapy and immunoregulation lead to an effective and safe treatment method for implant-associated infections. © 2024 Elsevier Ltd

AB - The poor efficiency of US-responsive coatings on implants restricts their practical application. Immunotherapy that stimulates immune cells to enhance their antibacterial activity is expected to synergize with sonodynamic therapy for treating implant infection effectively and safely. Herein, US-responsive hybrid coatings composed of the oxygen-deficient BaTiO3 nanorod arrays and L-arginine (BaTiO3-x/LA) are designed and prepared on titanium implants for sonocatalytic therapy-cooperated immunotherapy to treat Methicillin-resistant Staphylococcus aureus (MRSA) infection. BaTiO3-x/LA can generate more oxidizing reactive oxygen species (ROS, hydroxyl radical (·OH)) and reactive nitrogen species (RNS, peroxynitrite anion (ONOO−)). The construction of nanorod arrays and oxygen defects balances the piezoelectric properties and sonocatalytic capability during US treatment. The generated piezoelectric electric field provides a sufficient driving force to separate electrons and holes, and the oxygen defects attenuate the electron-hole recombination efficiency, consequently increasing the yield of ROS during the US treatment. Moreover, nitric oxide (NO) released by L-arginine reacts with the superoxide radical (·O2−) to produce ONOO−. Since, this radical chain reaction improves the oxidizing ability between bacteria and radicals, the cell membrane (argB, secA2) and DNA (dnaBGXN) are destroyed. The bacterial self-repair mechanism indirectly accelerates bacterial death based on the transcriptome analysis. In addition to participating in the radical chain reaction, NO positively affects macrophage M1 polarization to yield potent phagocytosis to MRSA. As a result, without introducing an extra sonosensitizer, BaTiO3-x/LA exhibits excellent antibacterial activity against MRSA after the US treatment for 15 min. Furthermore, BaTiO3-x/LA facilitates macrophage M2 polarization after implantation and improves osteogenic differentiation. The combined effects of sonodynamic therapy and immunoregulation lead to an effective and safe treatment method for implant-associated infections. © 2024 Elsevier Ltd

KW - Bacterial infection

KW - Immunoregulation

KW - Piezoelectric nanorod array

KW - Sonodynamic therapy

KW - Titanium implants

UR - http://www.scopus.com/inward/record.url?scp=85187959274&partnerID=8YFLogxK

UR - https://www.scopus.com/record/pubmetrics.uri?eid=2-s2.0-85187959274&origin=recordpage

U2 - 10.1016/j.biomaterials.2024.122532

DO - 10.1016/j.biomaterials.2024.122532

M3 - RGC 21 - Publication in refereed journal

C2 - 38493670

SN - 0142-9612

VL - 307

JO - Biomaterials

JF - Biomaterials

M1 - 122532

ER -

Ultrasound-driven radical chain reaction and immunoregulation of piezoelectric-based hybrid coating for treating implant infection

Abstract

Funding

Research Keywords

UN SDGs

Access Output

Other Access Options

Permanent Link

Other Files and Links

Fingerprint

DON_RMG: Fabrication, Characterization, and Properties of Functional Materials - RMGS

HMRF: Biocompatible Titanium Implants with Antibacterial Capability Arising from the Synergistic Effects of Mechanical and Electrical Interactions and Quantitative Bacteria Sensing Ability Based on Electron Transfer

Cite this