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Promotion of reactive oxygen species activated by nanosilver surface engineering for resistant bacteria-infected skin tissue therapy

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Abstract

Nanosilver has been regarded as a promising alternative to traditional antibiotics for fighting pathogen-associated infections due to its efficacy toward a broad spectrum of pathogens. However, bacterial resistance to nanosilver has emerged recently. In this contribution, a surface engineering strategy based on N-halamine chemistry to address bacterial resistance to nanosilver was proposed. Using 1,3-dichloro-5,5-dimethylhydantoin (DCDMH) as an N-halamine source, AgCl nanodots were deposited on the surface of Ag nanowires (Ag NWs) via in situ redox reaction to prepare AgCl-on-Ag NWs. After in vitro and in vivo tests, AgCl-on-Ag NWs effectively inactivated two antibiotic-resistant bacteria, ampicillin-resistant Escherichia coli (AREC) and methicillin-resistant Staphylococcus aureus (MRSA) with the minimum bactericidal concentration (MBC) as low as 10 μg·ml−1 and exhibited good biosafety against normal cells. The experimental and theoretical tests demonstrated that AgCl-on-Ag NWs worked on AREC and MASA by generating high level of reactive oxygen species under visible light irradiation, coupled with the sustained Ag+ ion release. Meanwhile, the antibacterial mechanism of AgCl-on-Ag NWs against MRSA was verified at the gene level by transcriptome analysis (RNA sequencing). Moreover, the full-thickness defect model verified that AgCl-on-Ag NWs reduced inflammatory cell infiltration and dramatically accelerated wound healing. This work provides a synergistic mechanism based on nanosilver surface engineering to eradicate the resistant bacteria that can alleviate drug resistance and develop an innovative approach for the treatment of bacterial infections.

摘要

纳米银因其对病原体广谱的抗菌功效而被认为是传统抗生素的可替代物之一，用于对抗与病原体相关的感染。然而，最近研究发现细菌对纳米银也产生了耐药性。本文提出了一种基于N-卤胺化学的表面工程策略，以解决细菌对纳米银的耐药性。使用1,3-二氯-5,5-二甲基海因（DCDMH）作为N-卤素源，通过原位氧化还原反应将AgCl纳米点沉积在Ag纳米线（Ag NWs）的表面，以制备AgCl-on-Ag NWs。通过体外和体内实验验证了AgCl-on-Ag NWs可以有效地灭活两种耐药菌，包括耐氨苄西林钠大肠杆菌（AREC）和耐甲氧西林金黄色葡萄球菌（MRSA），且最小杀菌浓度（MBC）低至10 μg·ml‒1。此外，AgCl-on-Ag NWs对正常细胞表现出良好的生物安全性。通过实验测试和理论计算证明AgCl-on-Ag NWs对AREC和MASA的杀菌机制是可见光照射下产生丰富的活性氧（ROS），以及持续的释放Ag+的协同作用机制。此外，通过转录组分析（RNA测序），AgCl-on-Ag NWs对MRSA的抗菌机制在基因水平得到了验证。最后，通过小鼠表皮创口感染的愈合模型验证了AgCl-on-Ag NWs减少了炎症细胞的浸润，极大地加速了伤口愈合。总之，这项工作提供了一种基于纳米银表面工程的协同机制，以根除耐药菌、避免耐药性，为治疗细菌感染开创了一种新的方法。

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Acknowledgements

This work was financially supported by the National Natural Science Foundation of China (Nos. 22062017 and 22164015), the Inner Mongolia Autonomous Region Program for Key Science and Technology (No. 2020GG0161), the Natural Science Foundation of Inner Mongolia Autonomous Region (No. 2019JQ03), the Ordos City Program for Key Science and Technology (No. 2022YY003), the Open Project of State Key Laboratory of Supramolecular Structure and Materials (No. sklssm2022021), the Program of Higher-Level Talents of Inner Mongolia University (No. 10000-22311201/035) and the Science and Technology Research Projects in Colleges and Universities of Inner Mongolia Autonomous Region (No. NJZZ23091).

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  1. College of Chemistry and Chemical Engineering, Inner Mongolia University, Hohhot, 010021, China

    Pei-Pei Li, Yu Zhang, Chao Wang, Shu-Jie Wang, Wen-Qing Yan, Dou-Xin Xiao, Jing Kang, Hai-Xia Wu & Alideertu Dong

  2. Engineering Research Center of Dairy Quality and Safety Control Technology, Ministry of Education, Inner Mongolia University, Hohhot, 010021, China

    Pei-Pei Li, Yu Zhang, Chao Wang, Shu-Jie Wang, Wen-Qing Yan, Dou-Xin Xiao, Jing Kang, Hai-Xia Wu & Alideertu Dong

  3. International Mongolia Hospital of Inner Mongolia, Hohhot, 010065, China

    De-Zhi Yang

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  1. Pei-Pei Li
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Correspondence to Jing Kang, De-Zhi Yang, Hai-Xia Wu or Alideertu Dong.

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Li, PP., Zhang, Y., Wang, C. et al. Promotion of reactive oxygen species activated by nanosilver surface engineering for resistant bacteria-infected skin tissue therapy. Rare Met. 42, 4167–4183 (2023). https://doi.org/10.1007/s12598-023-02481-z

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  • DOI: https://doi.org/10.1007/s12598-023-02481-z

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