Preparation of cuttlefish ink-porphyrin nanoconjugates and its application in photodynamic-photothermal synergistic treatment of tumor cells
Abstract
Biologically derived nanomaterials have gained increasing attention in tumor diagnosis and treatment due to their inherent biocompatibility. In this study, a nanoconjugate of cuttlefish ink (M, extracted from cuttlefish ink sacs) and meso-tetra (4-carboxyphenyl) porphyrin (TCPP), termed M-TCPP, was synthesized. The nanoparticle size of M-TCPP was approximately 120 nm, and it could be activated by a 660 nm light to induce the generation of reactive oxygen species (ROS) via TCPP for photodynamic therapy (PDT) of tumor cells. Additionally, when triggered by an 808 nm light (near-infrared light), the cuttlefish ink component efficiently converted light into heat for photothermal therapy (PTT) of tumor cells. Compared to standalone PDT or PTT, the synergistic combination of PDT-PTT resulted in significantly enhanced tumor cell destruction. Moreover, in vitro experiments demonstrated that M-TCPP exhibited no noticeable toxic side effects. The research offers some inspiration for the development of natural multifunctional biomaterials and their use in tumor therapy.
References
[1]Zhao M, Zhuang H, Li B, et al. In Situ Transformable Nanoplatforms with Supramolecular Cross-Linking Triggered Complementary Function for Enhanced Cancer Photodynamic Therapy. Advanced Materials. 2023; 35(20): e2209944. doi: 10.1002/adma.202209944
[2]Liu Y, Luo Y, Gao Y, et al. Carrier-Free Biomimetic Organic Nanoparticles with Super-High Drug Loading for Targeted NIR-II Excitable Triple-Modal Bioimaging and Phototheranostics. Small. 2024; e2406003. doi: 10.1002/smll.202406003
[3]Gao F, He G, Yin H, et al. Titania-coated 2D gold nanoplates as nanoagents for synergistic photothermal/sonodynamic therapy in the second near-infrared window. Nanoscale. 2019; 11(5): 2374–2384. doi: 10.1039/c8nr07188h
[4]Yu J, Yan H, Zhao F, et al. Intraparticle Electron Transfer for Long-Lasting Tumor Chemodynamic Therapy. Advanced Science. 2024; 11(36): e2403935. doi: 10.1002/advs.202403935
[5]Li C, Pang Y, Xu Y, et al. Near-infrared metal agents assisting precision medicine: From strategic design to bioimaging and therapeutic applications. Chemical Society Reviews. 2023; 52(13): 4392–4442. doi: 10.1039/d3cs00227f
[6]Bindra A, Wang D, Zhao Y. Metal-Organic Frameworks Meet Polymers: From Synthesis Strategies to Healthcare Applications. Advanced Materials. 2023; 35(40): e2300700. doi: 10.1002/adma.202300700
[7]Geng P, Yu N, Macharia D, et al. MOF-derived CuS@Cu-MOF nanocomposites for synergistic photothermal-chemodynamic-chemo therapy. Chemical Engineering Journal. 2022; 441: 135964. doi:10.2139/ssrn.4013479
[8]Zhang M, Liu X, Luo Q, et al. Tumor environment responsive degradable CuS@mSiO2@MnO2/DOX for MRI guided synergistic chemo-photothermal therapy and chemodynamic therapy. Chemical Engineering Journal. 2020; 389: 124450. doi: 10.1016/j.cej.2020.124450
[9]Li B, Wang W, Zhao L, et al. Multifunctional AIE Nanosphere-Based “Nanobomb” for Trimodal Imaging-Guided Photothermal/Photodynamic/Pharmacological Therapy of Drug-Resistant Bacterial Infections. ACS Nano. 2023; 17(5): 4601–4618. doi: 10.1021/acsnano.2c10694
[10]Li L, Li J, Hu R, et al. Tumor Cell Targeting and Responsive Nanoplatform for Multimodal-Imaging Guided Chemodynamic/Photodynamic/Photothermal Therapy toward Triple Negative Breast Cancer. ACS Applied Materials & Interfaces. 2023; 15(23): 27706–27718. doi: 10.1021/acsami.3c04709
[11]Geng P, Xiang G, Zhang W, et al. Hollow copper sulfide loaded protoporphyrin for photothermal⁃sonodynamic therapy of cancer cells. Chinese Journal of Inorganic Chemistry. 2024; 40(10): 1903-1910. doi: 10.11862/CJIC.20240155
[12]Han X, Huang J, Jing X, et al. Oxygen-Deficient Black Titania for Synergistic/Enhanced Sonodynamic and Photoinduced Cancer Therapy at Near Infrared-II Biowindow. ACS Nano. 2018; 12(5): 4545–4555. doi: 10.1021/acsnano.8b00899
[13]Li Y, Wang W, Zhang Y, et al. Design and Synthesis of Nanoscale Zr-Porphyrin IX Framework for Synergistic Photodynamic and Sonodynamic Therapy of Tumors. Acta Chimica Sinica. 2024; 82: 443–448. doi: 10.6023/A24010035
[14]Geng P, Li Y, Macharia Daniel, et al. One Stone, Three Birds: Design and Synthesis of “All-in-One” Nanoscale Mn-Porphyrin Coordination Polymers for Magnetic Resonance Imaging-Guided Synergistic Photodynamic-Sonodynamic Therapy. Journal of Colloid and Interface Science. 2024; 660: 1021–1029. doi: 10.1016/j.jcis.2024.01.157
[15]Chin Y, Yang L, Hsu F, et al. Iron oxide@chlorophyll clustered nanoparticles eliminate bladder cancer by photodynamic immunotherapy-initiated ferroptosis and immunostimulation. Journal of Nanobiotechnology. 2022; 20(1): 373. doi: 10.1186/s12951-022-01575-7
[16]Cheng S, Shi Y, Su C, et al. MnO2 nanosheet-mediated generalist probe: Cancer-targeted dual-microRNAs detection and enhanced CDT/PDT synergistic therapy. Biosensors and Bioelectronics. 2022; 214: 114550. doi: 10.1016/j.bios.2022.114550
[17]Geng P, Yu N, Liu X, et al. GSH-Sensitive Nanoscale Mn3+ -Sealed Coordination Particles as Activatable Drug Delivery Systems for Synergistic Photodynamic-Chemo Therapy. ACS Applied Materials & Interfaces. 2021; 13(27): 31440–31451. doi: 10.1021/acsami.1c06440
[18]Zhang L, Gao Y, Sun S, et al. pH-Responsive metal-organic framework encapsulated gold nanoclusters with modulated release to enhance photodynamic therapy/chemotherapy in breast cancer. Journal of Materials Chemistry B. 2020; 8(8): 1739–1747. doi: 10.1039/c9tb02621e
[19]Wang Y, Chen J, Bo Y, et al. Green synthesis of Au nanoparticles by Scutellaria barbata extract for chemo-photothermal anticancer therapy. Pharmacological Research-Modern Chinese Medicine. 2024; 13: 100536. doi: 10.1016/j.prmcm.2024.100536
[20]Li H, Zhu L, Zhang Y, et al. Biomimetic nanotherapeutics for homotypic-targeting photothermal/chemotherapy of oral cancer. Journal of Controlled Release. 2024; 366: 28–43. doi: 10.1016/j.jconrel.2023.12.039
[21]Liu Y, Zhang J, Zhou X, et al. Dissecting Exciton Dynamics in pH-Activatable Long-Wavelength Photosensitizers for Traceable Photodynamic Therapy. Angewandte Chemie International Edition. 2024; 63(43): e202408064. doi: 10.1002/anie.202408064
[22]Wang H, Xue K, Yang Y, et al. In Situ Hypoxia-Induced Supramolecular Perylene Diimide Radical Anions in Tumors for Photothermal Therapy with Improved Specificity. Journal of the American Chemical Society. 2022; 144(5): 2360–2367. doi: 10.1021/jacs.1c13067
[23]Li W, Yang J, Luo L, et al. Targeting photodynamic and photothermal therapy to the endoplasmic reticulum enhances immunogenic cancer cell death. Nature Communications. 2019; 10(1): 3349. doi: 10.1038/s41467-019-11269-8
[24]Urazaliyeva A, Kanabekova P, Beisenbayev A, et al. All organic nanomedicine for PDT-PTT combination therapy of cancer cells in hypoxia. Scientific Reports. 2024; 14(1): 17507. doi: 10.1038/s41598-024-68077-4
[25]Wan G, Liu Y, Chen B, et al. Recent advances of sonodynamic therapy in cancer treatment. Cancer Biology & Medicine. 2016; 13: 325–338. doi: 10.20892/j.issn.2095-3941.2016.0068
[26]Song X, Zhang Q, Chang M, et al. Nanomedicine-Enabled Sonomechanical, Sonopiezoelectric, Sonodynamic, and Sonothermal Therapy. Advanced Materials. 2023; 35(31): e2212259. doi: 10.1002/adma.202212259
[27]Sheng Y, Ren Q, Tao C, et al. Construction of PEGylated chlorin e6@CuS-Pt theranostic nanoplatforms for nanozymes-enhanced photodynamic-photothermal therapy. Journal of Colloid and Interface Science. 2023; 645: 122–132. doi: 10.1016/j.jcis.2023.04.092
[28]Fernandes N, Rodrigues C, Moreira A, et al. Overview of the application of inorganic nanomaterials in cancer photothermal therapy. Biomaterials Science. 2020; 8(11): 2990–3020. doi: 10.1039/d0bm00222d
[29]Li Y, Huang L, Li X, et al. From biomaterials to biotherapy: cuttlefish ink with protoporphyrin IX nanoconjugates for synergistic sonodynamic-photothermal therapy. Journal of Materials Chemistry B. 2024; 12(7): 1837–1845. doi: 10.1039/d3tb02423g
[30]Tang W, Kang J, Yang L, et al. Thermosensitive nanocomposite components for combined photothermal-photodynamic therapy in liver cancer treatment. Colloids and Surfaces B-Biointerfaces. 2023; 226: 113317. doi: 10.1016/j.colsurfb.2023.113317
[31]Ashkbar A, Rezaei F, Attari F, et al. Treatment of breast cancer in vivo by dual photodynamic and photothermal approaches with the aid of curcumin photosensitizer and magnetic nanoparticles. Scientific Reports. 2020; 10(1): 21206. doi: 10.1038/s41598-020-78241-1
[32]Jin T, Cheng D, Jiang G, et al. Engineering naphthalimide-cyanine integrated near-infrared dye into ROS-responsive nanohybrids for tumor PDT/PTT/chemotherapy. Bioactive Materials. 2021; 14: 42–51. doi: 10.1016/j.bioactmat.2021.12.009
[33]Cai Y, Liang P, Tang Q, et al. Diketopyrrolopyrrole-Triphenylamine Organic Nanoparticles as Multifunctional Reagents for Photoacoustic Imaging-Guided Photodynamic/Photothermal Synergistic Tumor Therapy. ACS Nano. 2017; 11(1): 1054–1063. doi: 10.1021/acsnano.6b07927
[34]Geng P, Yu N, Liu X, et al. One Responsive Stone, Three Birds: Mn (III)-Hemoporfin Frameworks with Glutathione-Enhanced Degradation, MRI, and Sonodynamic Therapy. Advanced Healthcare Materials. 2021; 10(3): 2001463. doi: 10.1002/adhm.202001463
[35]Geng P, Yu N, Liu X, et al. Sub 5 nm Gd3+ -Hemoporfin Framework Nanodots for Augmented Sonodynamic Theranostics and Fast Renal Clearance. Advanced Healthcare Materials. 2021; 10(18): 2100703. doi: 10.1002/adhm.202100703
[36]Qu W, Fan J, Zheng D, et al. Deep-penetration functionalized cuttlefish ink nanoparticles for combating wound infections with synergetic photothermal-immunologic therapy. Biomaterials. 2023; 301: 122231. doi: 10.1016/j.biomaterials.2023.122231
[37]Zhang J, Shi C, Shan F, et al. From biology to biology: Hematoporphyrin-melanin nanoconjugates with synergistic sonodynamic-photothermal effects on malignant tumors. Chemical Engineering Journal. 2021; 408: 127282. doi.org/10.1016/j.cej.2020.127282
[38]Meng X, Wu J, Hu Z, et al. Coordinating effect of ferroptosis and in situ disulfiram toxification for enhanced cancer therapy. Chemical Engineering Journal. 2024; 484: 149313. doi: 10.1016/j.cej.2024.149313
[39]Wang J, Song Z, He M, et al. Light-responsive and ultrapermeable two-dimensional metal-organic framework membrane for efficient ionic energy harvesting. Nature Communication. 2024; 15(1): 2125. doi: 10.1038/s41467-024-46439-w
Copyright (c) 2024 Wei Wang, Yuting Zhang, Yan Li, Yuzi Huang, Shuzhang Xiao, Wenquan Huang, Peng Geng
This work is licensed under a Creative Commons Attribution 4.0 International License.
Authors contributing to this journal agree to publish their articles under the Creative Commons Attribution 4.0 International License, allowing third parties to share their work (copy, distribute, transmit) and to adapt it for any purpose, even commercially, under the condition that the authors are given credit. With this license, authors hold the copyright.