Gold core@CeO2 halfshell Janus nanocomposites catalyze targeted sulfate radical for periodontitis therapy

Sijia Li; Qihang Ding; Lingling Zhang; Fangyu Shi; Chengyu Liu; Tingxuan Li; Yujia Shi; Manlin Qi; Lin Wang; Biao Dong; Shuyan Song; Jiao Sun; Jong Seung Kim; Chunyan Li

doi:10.1016/j.jconrel.2024.05.016

Gold core@CeO₂ halfshell Janus nanocomposites catalyze targeted sulfate radical for periodontitis therapy

J Control Release. 2024 May 14:370:600-613. doi: 10.1016/j.jconrel.2024.05.016. Online ahead of print.

Authors

Sijia Li¹, Qihang Ding², Lingling Zhang³, Fangyu Shi¹, Chengyu Liu¹, Tingxuan Li¹, Yujia Shi¹, Manlin Qi¹, Lin Wang¹, Biao Dong⁴, Shuyan Song⁵, Jiao Sun⁶, Jong Seung Kim⁷, Chunyan Li⁸

Affiliations

¹ Department of Prosthodontics, Jilin Provincial Key Laboratory of Tooth Development and Bone Remodeling, School of Stomatology, Jilin University, Changchun, 130021, PR China.
² Department of Prosthodontics, Jilin Provincial Key Laboratory of Tooth Development and Bone Remodeling, School of Stomatology, Jilin University, Changchun, 130021, PR China; Department of Chemistry, Korea University, Seoul, 02841, Republic of Korea.
³ State Key Laboratory of Rare Earth Resource Utilization, Changchun Institute of Applied Chemistry, Chinese Academy of Sciences, Changchun 130022, PR China.
⁴ State Key Laboratory on Integrated Optoelectronics, College of Electronic Science and Engineering, Jilin University, Changchun 130012, PR China.
⁵ State Key Laboratory of Rare Earth Resource Utilization, Changchun Institute of Applied Chemistry, Chinese Academy of Sciences, Changchun 130022, PR China. Electronic address: songsy@ciac.ac.cn.
⁶ Department of Cell Biology, College of Basic Medical Sciences, Jilin University, Changchun, Jilin 130021, PR China. Electronic address: jiaosun@jlu.edu.cn.
⁷ Department of Chemistry, Korea University, Seoul, 02841, Republic of Korea. Electronic address: jongskim@korea.ac.kr.
⁸ Department of Prosthodontics, Jilin Provincial Key Laboratory of Tooth Development and Bone Remodeling, School of Stomatology, Jilin University, Changchun, 130021, PR China. Electronic address: cyli@jlu.edu.cn.

PMID: 38735394
DOI: 10.1016/j.jconrel.2024.05.016

Abstract

The sulfate radical (SO₄^•-), known for its high reactivity and long lifespan, has emerged as a potent antimicrobial agent. Its exceptional energy allows for the disruption of vital structures and metabolic pathways in bacteria that are usually inaccessible to common radicals. Despite its promising potential, the efficient generation of this radical, particularly through methods involving enzymes and photocatalysis, remains a substantial challenge. Here, we capitalized on the peroxidase (POD)-mimicking activity and photocatalytic properties of cerium oxide (CeO₂) nanozymes, integrating these properties with the enhanced concept of plasma gold nanorod (GNR) to develop a half-encapsulated core@shell GNRs@CeO₂ Janus heterostructure impregnated with persulfate. Under near-infrared irradiation, the GNRs generate hot electrons, thereby boosting the CeO₂'s enzyme-like activity and initiating a potent reactive oxygen species (ROS) storm. This distinct nanoarchitecture facilitates functional specialization, wherein the heterostructure and efficient light absorption ensured continuous hot electron flow, not only enhancing the POD-like activity of CeO₂ for the production of SO₄^•- effectively, but also contributing a significant photothermal effect, disrupting periodontal plaque biofilm and effectively eradicating pathogens. Furthermore, the local temperature elevation synergistically enhances the POD-like activity of CeO₂. Transcriptomics analysis, as well as animal experiments of the periodontitis model, have revealed that pathogens undergo genetic information destruction, metabolic disorders, and pathogenicity changes in the powerful ROS system, and profound therapeutic outcomes in vivo, including anti-inflammation and bone preservation. This study demonstrated that energy transfer to augment nanozyme activity, specifically targeting ROS generation, constitutes a significant advancement in antibacterial treatment.

Keywords: Antibacterial; Nanozyme; Periodontal disease; Photocatalytic antimicrobial therapy; Sulfate radicals.