Photonic hyperthermia of malignant peripheral nerve sheath tumors at the third near-infrared biowindow

  1. Yihui Gu
  2. Zhichao Wang
  3. Chengjiang Wei
  4. Yuehua Li
  5. Wei Feng
  6. Wei Wang
  7. Meiqi Chang  Is a corresponding author
  8. Yu Chen  Is a corresponding author
  9. Qingfeng Li  Is a corresponding author
  1. Shanghai Ninth People's Hospital, China
  2. Shanghai Universityy, China
  3. Shanghai Institute of Ceramics, China
  4. Shanghai University, China

Abstract

Malignant peripheral nerve sheath tumors (MPNSTs), as typical aggressive sarcomas, typically carry a dismal prognosis. Given the insensitivity of these tumors to traditional chemotherapy and the absence of effective targeted drugs, new therapeutic strategies for efficient MPNSTs treatment are urgently needed. Recently, photothermal therapy (PTT) has demonstrated significant potential in cancer theranostics due to its minimally invasive nature and excellent therapeutic outcomes. However, the passive utilization of photothermal agents (PTAs) with poor target specificity and biocompatibility substantially hinders the clinical translation and application of this method. A unique near-infrared laser at the third biowindow (NIR-III) was utilized for photonic hyperthermia treatment of MPNSTs without PTAs. The superficial locations and relatively high collagen content of MPNSTs ensure the efficiency of photothermal tumor ablation and make the NIR-III laser a suitable therapeutic option that has potential for use in clinical applications. Using human MPNST cell line and xenograft models, it can be found that although the NIR-III photothermal treatment efficiency varied among individuals, which was possibly influenced by different endoplasmic reticulum stress responses (ERSRs), the expected antineoplastic effect was ultimately achieved after adjustment of the power density and radiation duration. The present study provides an intriguing noninvasive therapy for MPNSTs that accelerates the clinical translation of PTT while avoiding the biocompatibility issues arising from PTAs.

Data availability

The generic database-'Dryad' has been chosen.The unique identifier: doi:10.5061/dryad.3bk3j9km7All data generated or analysed during this study are included in the manuscript and supporting file.

The following data sets were generated

Article and author information

Author details

  1. Yihui Gu

    Department of Plastic and Reconstructive Surgery, Shanghai Ninth People's Hospital, Shanghai, China
    Competing interests
    The authors declare that no competing interests exist.
  2. Zhichao Wang

    Department of Plastic and Reconstructive Surgery, Shanghai Ninth People's Hospital, Shanghai, China
    Competing interests
    The authors declare that no competing interests exist.
  3. Chengjiang Wei

    Department of Plastic and Reconstructive Surgery, Shanghai Ninth People's Hospital, Shanghai, China
    Competing interests
    The authors declare that no competing interests exist.
  4. Yuehua Li

    Department of Plastic and Reconstructive Surgery, Shanghai Ninth People's Hospital, Shanghai, China
    Competing interests
    The authors declare that no competing interests exist.
  5. Wei Feng

    School of Life Sciences, Shanghai Universityy, Shanghai, China
    Competing interests
    The authors declare that no competing interests exist.
  6. Wei Wang

    Department of Plastic and Reconstructive Surgery, Shanghai Ninth People's Hospital, Shanghai, China
    Competing interests
    The authors declare that no competing interests exist.
  7. Meiqi Chang

    State Key Laboratory of High Performance Ceramics and Superfine Microstructure, Shanghai Institute of Ceramics, Shanghai, China
    For correspondence
    changmeiqi@mail.sic.ac.cn
    Competing interests
    The authors declare that no competing interests exist.
  8. Yu Chen

    School of Life Sciences, Shanghai University, Shanghai, China
    For correspondence
    chenyuedu@shu.edu.cn
    Competing interests
    The authors declare that no competing interests exist.
  9. Qingfeng Li

    Department of Plastic and Reconstructive Surgery, Shanghai Ninth People's Hospital, Shanghai, China
    For correspondence
    dr.liqingfeng@shsmu.edu.cn
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7822-618X

Funding

National Natural Science Foundation of China (82102344)

  • Zhichao Wang

National Natural Science Foundation of China (82172228)

  • Qingfeng Li

Shanghai Rising star Program (20QA1405600)

  • Zhichao Wang

Natural Science Foundation of Shanghai (22ZR1422300)

  • Zhichao Wang

Science and Technology Commission of Shanghai Municipality (19JC1413)

  • Qingfeng Li

Shanghai Education Development Foundation (19CG18)

  • Zhichao Wang

Shanghai Municipal Key Clinical Specialty (shslczdzk00901)

  • Qingfeng Li

Innovative research team of high-level local universities in Shanghai (SSMU-ZDCX20180700)

  • Qingfeng Li

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Wei Tao, Harvard University, United States

Ethics

Animal experimentation: All animals received humane care in compliance with the guidelines outlined in the Guide for the Care and Use of Laboratory Animals. All procedures were performed in accordance with the guidelines approved by the Shanghai Medical Experimental Animal Care Commission (IACUC: 2019-0008).

Human subjects: The use of photos and magnetic resonance images of MPNST patients was approved by the Ethics Committee of Shanghai Ninth People's Hospital, Shanghai Jiao Tong University School of Medicine (Reference number: SH9H-2019-T163-2). Informed consent and consent to publish were obtained from patients under institutional review board protocols.

Version history

  1. Received: November 15, 2021
  2. Accepted: August 15, 2022
  3. Accepted Manuscript published: September 16, 2022 (version 1)
  4. Version of Record published: October 11, 2022 (version 2)

Copyright

© 2022, Gu et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Yihui Gu
  2. Zhichao Wang
  3. Chengjiang Wei
  4. Yuehua Li
  5. Wei Feng
  6. Wei Wang
  7. Meiqi Chang
  8. Yu Chen
  9. Qingfeng Li
(2022)
Photonic hyperthermia of malignant peripheral nerve sheath tumors at the third near-infrared biowindow
eLife 11:e75473.
https://doi.org/10.7554/eLife.75473

Share this article

https://doi.org/10.7554/eLife.75473

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