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A versatile Pt-Ce6 nanoplatform as catalase nanozyme and NIR-II photothermal agent for enhanced PDT/PTT tumor therapy

多功能Pt-Ce6纳米平台作为过氧化氢纳米酶和NIR-II光热剂用于增强PDT/PTT肿瘤治疗

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Abstract

The hypoxic nature of solid tumors has severely negative effects on oxygen-based photodynamic therapy. In this study, we used porous Pt nanoparticles as a catalase (CAT) nanozyme, the second near-infrared (NIR-II) region photothermal transition agents (PTAs), and carriers of photosensitizer chlorin e6 (Ce6) to synthesize a composite nanosystem Pt-Ce6. In this system, Pt-Ce6 can continuously and stably decompose H2O2 into oxygen, thereby alleviating tumor hypoxia and improving the effect of photodynamic therapy (PDT). With 650 nm illumination, the reactive oxygen species (ROS) produced by Ce6 will decrease the mitochondrial membrane potential (MMP, ΔΨm) to release cytochrome c (Cyt-c) from the mitochondria into the cytoplasm, eventually leading to mitochondrial-mediated cellular apoptosis during the PDT process. In addition, Pt-Ce6 has good photothermal stability and high photothermal conversion efficiency (52.62%) in the NIR-II region. In U14 tumor-bearing mice, Pt-Ce6 completely suppressed tumor growth and recurrence under laser irradiation. Thus the nanocomposite shows excellent PDT/photothermal therapy (PTT) synergistic performance in vitro and in vivo.

摘要

实体肿瘤的缺氧严重影响着基于氧气的光动力疗法(PDT)的效果. 另外, 单一治疗模式通常难以达到满意的治疗效果. 为此, 我们设计合成了一种多功能纳米复合材料Pt-Ce6用于克服肿瘤乏氧, 实现PDT/PTT协同治疗. 在该体系中, 我们使用多孔Pt纳米粒子作为过氧化氢纳米酶、 近红外二区(NIR-II)光热转换剂和光敏剂二氢卟吩e6 (Ce6)的载体, Pt-Ce6可以持续、 稳定地将H2O2分解成O2, 从而减轻肿瘤缺氧, 增强PDT的效果. 在650 nm激光照射下, Ce6产生的活性氧(ROS)会使线粒体膜电位降低, 促使细胞色素c (Cyt-c)从线粒体释放到细胞质中, 最终导致PDT过程中线粒体介导的细胞凋亡. 此外, Pt-Ce6在NIR-II(1064 nm)具有良好的光热稳定性和较高的光热转换效率(52.62%). 活体实验结果表明该纳米复合材料具有良好的生物相容性和PDT/PTT协同作用, 有效抑制了小鼠肿瘤的生长.

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (51872263 and 31970755), and Zhejiang Provincial Natural Science Foundation (LZ19E020001 and LQ18B010002).

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  1. These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Life and Chemistry, Zhejiang Normal University, Jinhua, 321004, China

    Qing Chen  (陈晴), Su He  (何素), Fangjun Zhang  (张方军), Man Wang  (王曼), Dongmei Wang  (王冬梅), Zhigang Jin  (金志刚) & Chunxia Li  (李春霞)

  2. Institute of Frontier and Interdisciplinarity Science and Institute of Molecular Sciences and Engineering, Shandong University, Qingdao, 266237, China

    Chunxia Li  (李春霞)

  3. Department of Radiology, the Second Hospital of Jilin University, Changchun, 130041, China

    Fengzhi Cui  (崔凤至) & Jianhua Liu  (刘建华)

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  1. Qing Chen  (陈晴)
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  2. Su He  (何素)
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Contributions

Author contributions Li C designed the study and supervised the project; Chen Q conceived the experimental scheme. Chen Q, He S, Zhang F and Wang M performed the experiments; Chen Q, He S and Wang D performed the data analyses; Cui F and Liu J carried out the CT imaging; Chen Q wrote the paper with support from Li C and Jin Z. All authors contributed to the general discussion.

Corresponding authors

Correspondence to Zhigang Jin  (金志刚) or Chunxia Li  (李春霞).

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Conflict of interest The authors declare that they have no conflict of interest.

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Chunxia Li received her PhD degree in 2008 from Changchun Institute of Applied Chemistry, Chinese Academy of Sciences under the guidance of Prof. Jun Lin. After graduation, she became an assistant professor in Prof. Lin’s group and was promoted to associate professor in 2012. She worked at Zhejiang Normal University from 2016 to 2019. Now she is working as a professor at the Institute of Frontier and Interdisciplinarity Science and Institute of Molecular Sciences and Engineering, Shandong University. Her research interests focus on the controllable syntheses of multifuntional inoragnic nanomaterials and their bio-application.

Zhigang Jin received his PhD degree in 2006 from the Institute of Biochemistry and Cell Biology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences under the guidance of Prof. Naihe Jing. After graduation, he became an assistant professor in Prof. Jing’s group. From 2008 to 2017, he worked as post-doc and research associate at Ohio State University and the University of Illinois at Urbana-Champaign, respectively. He has been working as professor in the College of Chemistry and Life Sciences, Zhejiang Normal University since 2017. His research interests focus on molecular mechanism during embryonic development and tumorigenesis.

Qing Chen received her BS degree from Liaocheng University, China, in 2017. She is a postgraduate student under the supervision of Prof. Chunxia Li at Zhejiang Normal University. Her current research focuses on the syntheses and biomedical applications of inorganic nanomaterials.

Su He received her BA degree from Shanxi Medical University, China, in 2017. She is a postgraduate student under the supervision of Prof. Zhigang Jin at Zhejiang Normal University. Her current research interests focus on the virus and stress granules.

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Chen, Q., He, S., Zhang, F. et al. A versatile Pt-Ce6 nanoplatform as catalase nanozyme and NIR-II photothermal agent for enhanced PDT/PTT tumor therapy. Sci. China Mater. 64, 510–530 (2021). https://doi.org/10.1007/s40843-020-1431-5

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