AI Chat Paper
Note: Please note that the following content is generated by AMiner AI. SciOpen does not take any responsibility related to this content.
{{lang === 'zh_CN' ? '文章概述' : 'Summary'}}
{{lang === 'en_US' ? '中' : 'Eng'}}
Chat more with AI
Article Link
Collect
Submit Manuscript
Show Outline
Outline
Show full outline
Hide outline
Outline
Show full outline
Hide outline
Research Article

An oxygen reservoir-irrigated photoimmunotherapy of malignant melanoma

Yao Huang1Tingting Peng2,3( )Yangyan Chen1Fapeng Zhang4Wanshan Hu3XinYi Gao3Hongyu Chen5Ping Tang6Chuanbin Wu3Xin Pan1 ( )
School of Pharmaceutical Sciences, Sun Yat-sen University, Guangzhou 510006, China
International Cooperative Laboratory of Traditional Chinese Medicine Modernization and Innovative Drug Development of Ministry of Education (MOE) of China, Jinan University, Guangzhou 511436, China
College of Pharmacy, Jinan University, Guangzhou 511436, China
Department of Biliary-Pancreatic Surgery, Sun Yat-Sen Memorial Hospital, Sun Yat-Sen University, Guangzhou 510120, China
School of Pharmacy, Shanghai University of Traditional Chinese Medicine, Shanghai 201203, China
Shenzhen University General Hospital, Shenzhen 518055, China
Show Author Information

Graphical Abstract

(a) The anti-tumor efficacy of photodynamic therapy (PDT) is severely limited by hypoxia and dense extracellular matrix (ECM) involved in tumor tissues, and (b) the “full” oxygen reservoir-irrigated PDT allows for stronger and deeper cell-killing effect.

Abstract

Tumor hypoxia is the pivotal factor limiting the therapeutic efficacy of photodynamic therapy (PDT), and can be partly improved by either the oxygen economizing or the oxygen supplementation strategies. Nevertheless, the current studies scarcely integrated the merits of both strategies and neglected the bottleneck of poor oxygen infiltration in deep tumors, resulting in PDT resistance. Herein, we developed an oxygen reservoir-irrigated PDT which integrates oxygen supply, oxygen economizing, and oxygen infiltration altogether. Specifically, mitochondria-targeted mesoporous prussian blue nanoparticles (Ce6@TPB) were fabricated to bridge the gap between oxygen economizing and oxygen supplementation by reducing oxygen output while increasing oxygen input. Hyaluronidase-loaded microneedles were further developed to pave the way for deep PDT with increased infusion of oxygen and photosensitizer by degrading dense extracellular matrix. The modulation of tumor oxygenation and permeability during PDT leads to the complete eradication of primary melanoma and strong immunogenic cell death. Its further combination with checkpoint-blockade inhibitor greatly suppressed the proliferation of distal tumors by reprogramming immune microenvironments, as evidenced by the depletion of M2 macrophage, increased infiltration of anti-tumor immune cells, and elevated excretion of immune cytokines. Therefore, such an oxygen reservoir-irrigated PDT potentiates powerful photoimmunotherapy and provides a favorable prospect for tumor treatment.

Electronic Supplementary Material

Download File(s)
12274_2022_5031_MOESM1_ESM.pdf (1.2 MB)

References

[1]

Dolmans, D. E. J. G. J.; Fukumura, D.; Jain, R. K. Photodynamic therapy for cancer. Nat. Rev. Cancer 2003, 3, 380–387.

[2]

Agostinis, P.; Berg, K.; Cengel, K. A.; Foster, T. H.; Girotti, A. W.; Gollnick, S. O.; Hahn, S. M.; Hamblin, M. R.; Juzeniene, A.; Kessel, D. et al. Photodynamic therapy of cancer: An update. CA Cancer J. Clin. 2011, 61, 250–281.

[3]

Dougherty, T. J.; Gomer, C. J.; Henderson, B. W.; Jori, G.; Kessel, D.; Korbelik, M.; Moan, J.; Peng, Q. Photodynamic therapy. J. Natl. Cancer Inst. 1998, 90, 889–905.

[4]

Kim, S.; Tachikawa, T.; Fujitsuka, M.; Majima, T. Far-red fluorescence probe for monitoring singlet oxygen during photodynamic therapy. J. Am. Chem. Soc. 2014, 136, 11707–11715.

[5]

Song, X. J.; Feng, L. Z.; Liang, C.; Gao, M.; Song, G. S.; Liu, Z. Liposomes co-loaded with metformin and chlorin e6 modulate tumor hypoxia during enhanced photodynamic therapy. Nano Res. 2017, 10, 1200–1212.

[6]

Chen, D. Y.; Suo, M.; Guo, J. C.; Tang, W. X.; Jiang, W.; Liu, Y.; Duo, Y. H. Development of MOF “armor-plated” phycocyanin and synergistic inhibition of cellular respiration for hypoxic photodynamic therapy in patient-derived xenograft models. Adv. Healthc. Mater. 2021, 10, 2001577.

[7]

Fan, Y. T.; Zhou, T. J.; Cui, P. F.; He, Y. J.; Chang, X.; Xing, L.; Jiang, H. L. Modulation of intracellular oxygen pressure by dual-drug nanoparticles to enhance photodynamic therapy. Adv. Funct. Mater. 2019, 29, 1806708.

[8]
Yu, W. Y.; Liu, T.; Zhang, M. K.; Wang, Z. X.; Ye, J. J.; Li, C. X.; Liu, W. L.; Li, R. Q.; Feng, J.; Zhang, X. Z. O2 economizer for inhibiting cell respiration to combat the hypoxia obstacle in tumor treatments. ACS Nano 2019, 13, 1784–1794.
[9]

Xu, T.; Ma, Y. Y.; Yuan, Q. L.; Hu, H. X.; Hu, X. K.; Qian, Z. Y.; Rolle, J. K.; Gu, Y. Q.; Li, S. W. Enhanced ferroptosis by oxygen-boosted phototherapy based on a 2-in-1 nanoplatform of ferrous hemoglobin for tumor synergistic therapy. ACS Nano 2020, 14, 3414–3425.

[10]

Cheng, Y. H.; Cheng, H.; Jiang, C. X.; Qiu, X. F.; Wang, K. K.; Huan, W.; Yuan, A. H.; Wu, J. H.; Hu, Y. Q. Perfluorocarbon nanoparticles enhance reactive oxygen levels and tumour growth inhibition in photodynamic therapy. Nat. Commun. 2015, 6, 8785.

[11]

Zhu, Y.; Jin, D.; Liu, M. M.; Dai, Y.; Li, L.; Zheng, X. W.; Wang, L. L.; Shen, A. Z.; Yu, J. N.; Wu, S. S. et al. Oxygen self-supply engineering-ferritin for the relief of hypoxia in tumors and the enhancement of photodynamic therapy efficacy. Small 2022, 18, 2200116.

[12]

Hong, L.; Li, J. M.; Luo, Y. L.; Guo, T.; Zhang, C. S.; Ou, S.; Long, Y. H.; Hu, Z. Q. Recent advances in strategies for addressing hypoxia in tumor photodynamic therapy. Biomolecules 2022, 12, 81.

[13]

Yang, N.; Xiao, W. Y.; Song, X. J.; Wang, W. J.; Dong, X. C. Recent advances in tumor microenvironment hydrogen peroxide-responsive materials for cancer photodynamic therapy. Nanomicro Lett. 2020, 12, 15.

[14]

Yang, Z. L.; Tian, W.; Wang, Q.; Zhao, Y.; Zhang, Y. L.; Tian, Y.; Tang, Y. X.; Wang, S. J.; Liu, Y.; Ni, Q. Q. et al. Oxygen-evolving mesoporous organosilica coated prussian blue nanoplatform for highly efficient photodynamic therapy of tumors. Adv. Sci. (Weinh.) 2018, 5, 1700847.

[15]

Cheng, L.; Gong, H.; Zhu, W. W.; Liu, J. J.; Wang, X. Y.; Liu, G.; Liu, Z. PEGylated Prussian blue nanocubes as a theranostic agent for simultaneous cancer imaging and photothermal therapy. Biomaterials 2014, 35, 9844–9852.

[16]

Feng, L. S.; Dou, C. R.; Xia, Y. G.; Li, B. H.; Zhao, M. Y.; Yu, P.; Zheng, Y. Y.; El-Toni, A. M.; Atta, N. F.; Galal, A. et al. Neutrophil-like cell-membrane-coated nanozyme therapy for ischemic brain damage and long-term neurological functional recovery. ACS Nano 2021, 15, 2263–2280.

[17]

Wang, S. B.; Chen, Z. X.; Gao, F.; Zhang, C.; Zou, M. Z.; Ye, J. J.; Zeng, X.; Zhang, X. Z. Remodeling extracellular matrix based on functional covalent organic framework to enhance tumor photodynamic therapy. Biomaterials 2020, 234, 119772.

[18]

Salmon, H.; Franciszkiewicz, K.; Damotte, D.; Dieu-Nosjean, M. C.; Validire, P.; Trautmann, A.; Mami-Chouaib, F.; Donnadieu, E. Matrix architecture defines the preferential localization and migration of T cells into the stroma of human lung tumors. J. Clin. Invest. 2012, 122, 899–910.

[19]

Luo, T.; Nocon, A.; Fry, J.; Sherban, A.; Rui, X. L.; Jiang, B. B.; Xu, X. J.; Han, J. Y.; Yan, Y.; Yang, Q. et al. AMPK activation by metformin suppresses abnormal extracellular matrix remodeling in adipose tissue and ameliorates insulin resistance in obesity. Diabetes 2016, 65, 2295–2310.

[20]

Zhang, L.; Wang, Y.; Yang, Y. T.; Liu, Y. Y.; Ruan, S. B.; Zhang, Q. Y.; Tai, X. W.; Chen, J. T.; Xia, T.; Qiu, Y. et al. High tumor penetration of paclitaxel loaded pH sensitive cleavable liposomes by depletion of tumor collagen I in breast cancer. ACS Appl. Mater. Interfaces 2015, 7, 9691–9701.

[21]

Liu, J. J.; Tian, L. L.; Zhang, R.; Dong, Z. L.; Wang, H. R.; Liu, Z. Collagenase-encapsulated pH-responsive nanoscale coordination polymers for tumor microenvironment modulation and enhanced photodynamic nanomedicine. ACS Appl. Mater. Interfaces 2018, 10, 43493–43502.

[22]

Gong, H.; Chao, Y.; Xiang, J.; Han, X.; Song, G. S.; Feng, L. Z.; Liu, J. J.; Yang, G. B.; Chen, Q.; Liu, Z. Hyaluronidase to enhance nanoparticle-based photodynamic tumor therapy. Nano Lett. 2016, 16, 2512–2521.

[23]

Chen, H. P.; Wu, B. Y.; Zhang, M. M.; Yang, P. P.; Yang, B. B.; Qin, W. B.; Wang, Q. Q.; Wen, X. G.; Chen, M. W.; Quan, G. L. et al. A novel scalable fabrication process for the production of dissolving microneedle arrays. Drug Deliv. Transl. Res. 2019, 9, 240–248.

[24]

Lin, S. Q.; Cai, B. Z.; Quan, G. L.; Peng, T. T.; Yao, G. T.; Zhu, C. E.; Wu, Q. L.; Ran, H.; Pan, X.; Wu, C. B. Novel strategy for immunomodulation: Dissolving microneedle array encapsulating thymopentin fabricated by modified two-step molding technology. Eur. J. Pharm. Biopharm. 2018, 122, 104–112.

[25]

Zhang, Q.; Xu, C. C.; Lin, S. Q.; Zhou, H. B.; Yao, G. T.; Liu, H.; Wang, L. L.; Pan, X.; Quan, G. L.; Wu, C. B. Synergistic immunoreaction of acupuncture-like dissolving microneedles containing thymopentin at acupoints in immune-suppressed rats. Acta Pharm. Sin. B 2018, 8, 449–457.

[26]

Ming, H.; Torad, N. L. K.; Chiang, Y. D.; Wu, K. C. W.; Yamauchi, Y. Size- and shape-controlled synthesis of Prussian Blue nanoparticles by a polyvinylpyrrolidone-assisted crystallization process. CrystEngComm 2012, 14, 3387–3396.

[27]

You, Q.; Zhang, K. Y.; Liu, J. Y.; Liu, C. L.; Wang, H. Y.; Wang, M. T.; Ye, S. Y.; Gao, H. Q.; Lv, L. T.; Wang, C. et al. Persistent regulation of tumor hypoxia microenvironment via a bioinspired Pt-based oxygen nanogenerator for multimodal imaging-guided synergistic phototherapy. Adv. Sci. (Weinh.) 2020, 7, 1903341.

[28]

Yang, G. B.; Xu, L. G.; Xu, J.; Zhang, R.; Song, G. S.; Chao, Y.; Feng, L. Z.; Han, F. X.; Dong, Z. L.; Li, B. et al. Smart nanoreactors for pH-responsive tumor homing, mitochondria-targeting, and enhanced photodynamic-immunotherapy of cancer. Nano Lett. 2018, 18, 2475–2484.

[29]

Liew, S. S.; Qin, X. F.; Zhou, J.; Li, L.; Huang, W.; Yao, S. Q. Smart design of nanomaterials for mitochondria-targeted nanotherapeutics. Angewa. Chem., Int. Ed. 2021, 60, 2232–2256.

[30]

Wang, M.; Song, J.; Zhou, F. F.; Hoover, A. R.; Murray, C.; Zhou, B. Q.; Wang, L.; Qu, J. L.; Chen, W. R. NIR-triggered phototherapy and immunotherapy via an antigen-capturing nanoplatform for metastatic cancer treatment. Adv. Sci. (Weinh.) 2019, 6, 1802157.

[31]

Krysko, D. V.; Garg, A. D.; Kaczmarek, A.; Krysko, O.; Agostinis, P.; Vandenabeele, P. Immunogenic cell death and DAMPs in cancer therapy. Nat. Rev. Cancer 2012, 12, 860–875.

[32]

Kroemer, G.; Galluzzi, L.; Kepp, O.; Zitvogel, L. Immunogenic cell death in cancer therapy. Annu. Rev. Immunol. 2013, 31, 51–72.

[33]

Turan, I. S.; Yildiz, D.; Turksoy, A.; Gunaydin, G.; Akkaya, E. U. A bifunctional photosensitizer for enhanced fractional photodynamic therapy: Singlet oxygen generation in the presence and absence of light. Angew. Chem. 2016, 128, 2925–2928.

[34]

Kamata, H.; Honda, S. I.; Maeda, S.; Chang, L. F.; Hirata, H.; Karin, M. Reactive oxygen species promote TNFalpha-induced death and sustained JNK activation by inhibiting MAP kinase phosphatases. Cell 2005, 120, 649–661.

[35]

Shi, C. R.; Liu, T.; Guo, Z. D.; Zhuang, R. Q.; Zhang, X. Z.; Chen, X. Y. Reprogramming tumor-associated macrophages by nanoparticle-based reactive oxygen species photogeneration. Nano Lett. 2018, 18, 7330–7342.

Nano Research
Pages 2875-2884
Cite this article:
Huang Y, Peng T, Chen Y, et al. An oxygen reservoir-irrigated photoimmunotherapy of malignant melanoma. Nano Research, 2023, 16(2): 2875-2884. https://doi.org/10.1007/s12274-022-5031-x
Topics:

715

Views

2

Crossref

2

Web of Science

2

Scopus

0

CSCD

Altmetrics

Received: 11 July 2022
Revised: 01 September 2022
Accepted: 09 September 2022
Published: 24 October 2022
© Tsinghua University Press 2022
Return