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

Utilizing dual-pathway energy transfer in upconversion nanoconjugates for reinforced photodynamic therapy

Ruohao Zhang1,2Yu Lu1,3Yifei Zhou1,2Kehong Lv1,2Xinyu Fu1,2Jitong Gong1,2Shuang Yao1Xiaozhen Wang4Jing Feng1,2( )Hongjie Zhang1,2,5( )
State Key Laboratory of Rare Earth Resource Utilization, Changchun Institute of Applied Chemistry, Chinese Academy of Sciences, Changchun 130022, China
School of Applied Chemistry and Engineering, University of Science and Technology of China, Hefei 230026, China
College of Chemistry, Jilin University, Changchun 130012, China
Department of Breast Surgery, General Surgery Center, the First Hospital of Jilin University, Changchun 130021, China
Department of Chemistry, Tsinghua University, Beijing 100084, China
Show Author Information

Graphical Abstract

We developed a novel nanoconjugate (UCNP-Ce6/AIEgen) that compensates for insufficient reactive oxygen species (ROS) produced by traditional single-pathway photodynamic therapy (PDT) via dual-pathway energy transfer (direct lanthanide-triplet energy transfer, DTET; Fӧrster resonance energy transfer, FRET) and reinforces PDT effect on 4T1 tumor model in vitro and in vivo.

Abstract

Enhancing the therapeutic effect of existing treatments or developing new non-invasive treatments are important measures to achieve high-efficiency treatment of malignant tumors. Photodynamic therapy (PDT) is an emerging treatment modality, and the key for achieving high-efficiency PDT is to select light with strong tissue penetration depth and enhance the generation of reactive oxygen species (ROS). Although the upconversion nanoparticles (UCNPs) modified with the photosensitizers could achieve PDT with strong penetration depth under near-infrared light irradiation, the ROS generated by traditional single-pathway PDT is still insufficient. Herein, we developed a novel nanoconjugate (UCNP-Ce6/AIEgen) for dual-pathway reinforced PDT, in which the UCNPs were co-modified with chlorin e6 (Ce6) and luminogen with aggregation-induced emission (AIEgen). Due to the presence of AIEgen, UCNP-Ce6/AIEgen could avoid aggregation-caused luminescence quenching in biological water environments and convert upconversion luminescence (UCL) of UCNPs to Ce6-activatable fluorescence. Therefore, under the irradiation of 808 nm laser, UCNP-Ce6/AIEgen can not only undergo direct lanthanide-triplet energy transfer to activate Ce6, but also convert the UCL of UCNPs to the light that can activate Ce6 through Fӧrster resonance energy transfer to generate more ROS, thus promoting tumor cell apoptosis. This work broadens the applications of nanoconjugates of lanthanide-based inorganic materials and organic dyes, and provides a conception for reinforced PDT of tumors.

Electronic Supplementary Material

Download File(s)
12274_2023_6202_MOESM1_ESM.pdf (3.6 MB)

References

[1]

Kuningas, K.; Ukonaho, T.; Päkkilä, H.; Rantanen, T.; Rosenberg, J.; Lövgren, T.; Soukka, T. Upconversion fluorescence resonance energy transfer in a homogeneous immunoassay for estradiol. Anal. Chem. 2006, 78, 4690–4696.

[2]

Fischer, L. H.; Harms, G. S.; Wolfbeis, O. S. Upconverting nanoparticles for nanoscale thermometry. Angew. Chem., Int. Ed. 2011, 50, 4546–4551.

[3]

Bouzigues, C.; Gacoin, T.; Alexandrou, A. Biological applications of rare-earth based nanoparticles. ACS Nano 2011, 5, 8488–8505.

[4]

Li, S. Q.; Huo, H. Q.; Gao, X.; Liu, L. T.; Wang, S. M.; Ye, J. M.; Mu, J.; Song, J. B. Engineering Janus gold nanorod-titania heterostructures with enhanced photocatalytic antibacterial activity against multidrug-resistant bacterial infection. Nano Res. 2023, 16, 2049–2058.

[5]

Zhang, X. G.; Chen, X. M.; Zhang, P.; Li, M. T.; Feng, M.; Zhang, Y. Q.; Cheng, L. L.; Tang, J. J.; Xu, L. T.; Liu, Y. D. et al. A novel two-dimensional nanoheterojunction via facilitating electron-hole pairs separation for synergistic tumor phototherapy and immunotherapy. Nano Res. 2023, 16, 7148–7163.

[6]

Liu, Y. Y.; Meng, X. F.; Bu, W. B. Upconversion-based photodynamic cancer therapy. Coord. Chem. Rev. 2019, 379, 82–98.

[7]

Wang, J.; Qi, J.; Jin, F. Y.; You, Y. C.; Du, Y.; Liu, D.; Xu, X. L.; Chen, M. J.; Shu, G. F.; Zhu, L. W. et al. Spatiotemporally light controlled “drug-free” macromolecules via upconversion-nanoparticle for precise tumor therapy. Nano Today 2022, 42, 101360.

[8]

Dong, H.; Du, S. R.; Zheng, X. Y.; Lyu, G. M.; Sun, L. D.; Li, L. D.; Zhang, P. Z.; Zhang, C.; Yan, C. H. Lanthanide nanoparticles: From design toward bioimaging and therapy. Chem. Rev. 2015, 115, 10725–10815.

[9]

He, Y. L.; Guo, S. W.; Zhang, Y.; Liu, Y.; Ju, H. X. Near-infrared photo-controlled permeability of a biomimetic polymersome with sustained drug release and efficient tumor therapy. ACS Appl. Mater. Interfaces 2021, 13, 14951–14963.

[10]

Jin, J. F.; Xu, Z. H.; Zhang, Y.; Gu, Y. J.; Lam, M. H. W.; Wong, W. T. Upconversion nanoparticles conjugated with Gd3+-DOTA and RGD for targeted dual-modality imaging of brain tumor xenografts. Adv. Healthcare Mater. 2013, 2, 1501–1512.

[11]

Chen, J.; Zhang, D. Y.; Zou, Y.; Wang, Z. J.; Hao, M. C.; Zheng, M.; Xue, X.; Pan, X. X.; Lu, Y. Q.; Wang, J. F. et al. Developing a pH-sensitive Al(OH)3 layer-mediated UCNP@Al(OH)3/Au nanohybrid for photothermal therapy and fluorescence imaging in vivo. J. Mater. Chem. B 2018, 6, 7862–7870.

[12]

Pei, P.; Chen, Y.; Sun, C. X.; Fan, Y.; Yang, Y. M.; Liu, X.; Lu, L. F.; Zhao, M. Y.; Zhang, H. X.; Zhao, D. Y. et al. X-ray-activated persistent luminescence nanomaterials for NIR-II imaging. Nat. Nanotechnol. 2021, 16, 1011–1018.

[13]

Wang, Z.; Qiu, X. E.; Xi, W. S.; Tang, M.; Liu, J. L.; Jiang, H.; Sun, L. N. Tailored upconversion nanomaterial: A hybrid nano fluorescent sensor for evaluating efficacy of lactate dehydrogenase inhibitors as anticancer drugs. Sens. Actuators B Chem. 2021, 345, 130417.

[14]

Jiang, A. Q.; Liu, Y. X.; Ma, L. Y.; Mao, F.; Liu, L. D.; Zhai, X. J.; Zhou, J. Biocompatible heat-shock protein inhibitor-delivered flowerlike short-wave infrared nanoprobe for mild temperature-driven highly efficient tumor ablation. ACS Appl. Mater. Interfaces 2019, 11, 6820–6828.

[15]

Li, L. Y.; Zeng, Z. H.; Chen, Z. X.; Gao, R. Y.; Pan, L. T.; Deng, J. J.; Ye, X. H.; Zhang, J.; Zhang, S. J.; Mei, C. Y. et al. Microenvironment-triggered degradable hydrogel for imaging diagnosis and combined treatment of intraocular choroidal melanoma. ACS Nano 2020, 14, 15403–15416.

[16]

Sun, F. Y.; Shen, H. C.; Yang, Q. H.; Yuan, Z. Y.; Chen, Y. Y.; Guo, W. H.; Wang, Y.; Yang, L.; Bai, Z. T.; Liu, Q. Q. et al. Dual behavior regulation: Tether-free deep-brain stimulation by photothermal and upconversion hybrid nanoparticles. Adv. Mater. 2023, 35, 2210018.

[17]

Wang, C.; Wang, H. M.; Yang, H.; Xu, C.; Wang, Q.; Li, Z.; Zhang, Z. J.; Guan, J. K.; Yu, X. M.; Yang, X. Q. et al. Targeting cancer-associated fibroblasts with hydroxyethyl starch nanomedicine boosts cancer therapy. Nano Res. 2023, 16, 7323–7336.

[18]

Feng, L. L.; He, F.; Liu, B.; Yang, G. X.; Gai, S. L.; Yang, P. P.; Li, C. X.; Dai, Y. L.; Lv, R. C.; Lin, J. g-C3N4 coated upconversion nanoparticles for 808 nm near-infrared light triggered phototherapy and multiple imaging. Chem. Mater 2016, 28, 7935–7946.

[19]

Qi, X. L.; Han, Y. D.; Liu, S. J.; Hu, H. F.; Cheng, Z. Z.; Liu, T. G. NaYF4: Yb/Tm@SiO2-Dox/Cur-CS/OSA nanoparticles with pH and photon responses. Nanotechnology 2021, 32, 255703.

[20]

Chen, Y. X.; Xiang, H. J.; Zhuang, S. W.; Shen, Y. J.; Chen, Y.; Zhang, J. Oxygen-independent photocleavage of radical nanogenerator for near-IR-gated and H2O-mediated free-radical nanotherapy. Adv. Mater. 2021, 33, 2100129.

[21]

Gao, X.; Feng, J.; Song, S. Y.; Liu, K.; Du, K. M.; Zhou, Y. F.; Lv, K. H.; Zhang, H. J. Tumor-targeted biocatalyst with self-accelerated cascade reactions for enhanced synergistic starvation and photodynamic therapy. Nano Today 2022, 43, 101433.

[22]

Soleimany, A.; Khoee, S.; Dias, S.; Sarmento, B. Exploring low-power single-pulsed laser-triggered two-photon photodynamic/photothermal combination therapy using a gold nanostar/graphene quantum dot nanohybrid. ACS Appl. Mater. Interfaces 2023, 15, 20811–20821.

[23]

Zhang, Q.; Sun, S. Q.; Wang, Z.; Li, J. B.; Xie, Y.; Shi, L. Y.; Sun, L. N. Dandelion-inspired hierarchical upconversion nanoplatform for synergistic chemo-photodynamic therapy in vitro. ACS Appl. Bio Mater. 2020, 3, 6015–6024.

[24]

Wang, R.; Wang, X.; Mu, X. L. E.; Feng, W. B.; Lu, Y. X.; Yu, W. S.; Zhou, X. F. Reducing thermal damage to adjacent normal tissue with dual thermo-responsive polymer via thermo-induced phase transition for precise photothermal theranosis. Acta Biomater. 2022, 148, 142–151.

[25]

Ersen, B. C.; Goncu, B.; Dag, A.; Demirel, G. B. GLUT-targeting phototherapeutic nanoparticles for synergistic triple combination cancer therapy. ACS Appl. Mater. Interfaces 2023, 15, 9080–9098.

[26]

Li, H. Y.; Xu, H.; Wang, G. L.; Chen, J. C.; Ji, D. D.; Huang, Y. Y.; Cui, G. Q.; He, H.; Guo, Z. Q. Rational design of mesoporous coordination polymer nanophotosensitizers for photodynamic tumor ablation. ACS Appl. Mater. Interfaces 2023, 15, 21746–21753.

[27]

Lv, K. H.; Yao, L.; Fu, X. Y.; Gao, X.; Wang, H. L.; Zhou, Y. F.; Zhang, R. H.; Lu, Y.; Feng, J.; Zhang, H. J. Indocyanine green-equipped upconversion nanoparticles/CeO2 trigger mutually reinforced dual photodynamic therapy. Nano Today 2023, 52, 101964.

[28]

Wang, Y. W.; Li, Y. M.; Zhang, Z. J.; Wang, L.; Wang, D.; Tang, B. Z. Triple-jump photodynamic theranostics: MnO2 combined upconversion nanoplatforms involving a type-I photosensitizer with aggregation-induced emission characteristics for potent cancer treatment. Adv. Mater. 2021, 33, 2103748.

[29]

Algar, W. R.; Hildebrandt, N.; Vogel, S. S.; Medintz, I. L. FRET as a biomolecular research tool-understanding its potential while avoiding pitfalls. Nat. Methods 2019, 16, 815–829.

[30]

Pini, F.; Francés-Soriano, L.; Andrigo, V.; Natile, M. M.; Hildebrandt, N. Optimizing upconversion nanoparticles for FRET biosensing. ACS Nano 2023, 17, 4971–4984.

[31]

Mei, J.; Hong, Y. N.; Lam, J. W. Y.; Qin, A. J.; Tang, Y. H.; Tang, B. Z. Aggregation-induced emission: The whole is more brilliant than the parts. Adv. Mater. 2014, 26, 5429–5479.

[32]

Siefe, C.; Mehlenbacher, R. D.; Peng, C. S.; Zhang, Y. X.; Fischer, S.; Lay, A.; McLellan, C. A.; Alivisatos, A. P.; Chu, S.; Dionne, J. A. Sub-20 nm core-shell-shell nanoparticles for bright upconversion and enhanced Fӧrster resonant energy transfer. J. Am. Chem. Soc. 2019, 141, 16997–17005.

[33]

Zheng, B. Z.; Zhong, D. N.; Xie, T. T.; Zhou, J.; Li, W. L.; Ilyas, A.; Lu, Y. H.; Zhou, M.; Deng, R. R. Near-infrared photosensitization via direct triplet energy transfer from lanthanide nanoparticles. Chem 2021, 7, 1615–1625.

[34]

Ding, D.; Li, K.; Liu, B.; Tang, B. Z. Bioprobes based on AIE fluorogens. Acc. Chem. Res. 2013, 46, 2441–2453.

[35]

Guan, Y.; Lu, H. G.; Li, W.; Zheng, Y. D.; Jiang, Z.; Zou, J. L.; Gao, H. Near-infrared triggered upconversion polymeric nanoparticles based on aggregation-induced emission and mitochondria targeting for photodynamic cancer therapy. ACS Appl. Mater. Interfaces 2017, 9, 26731–26739.

[36]

Mao, D.; Hu, F.; Yi, Z. G.; Kenry, N.; Xu, S. D.; Yan, S. Q.; Luo, Z. C.; Wu, W. B.; Wang, Z. H.; Kong, D. L. et al. AIEgen-coupled upconversion nanoparticles eradicate solid tumors through dual-mode ROS activation. Sci. Adv. 2020, 6, eabb2712.

[37]

Ding, S. H.; Wu, W. B.; Peng, T. T.; Pang, W.; Jiang, P. F.; Zhan, Q. Q.; Qi, S. H.; Wei, X. B.; Gu, B. B.; Liu, B. Near-infrared light excited photodynamic anticancer therapy based on UCNP@AIEgen nanocomposite. Nanoscale Adv. 2021, 3, 2325–2333.

[38]

Xu, Z. L.; Chen, J.; Li, Y. N.; Hu, T.; Fan, L.; Xi, J. Q.; Han, J.; Guo, R. Yolk-shell Fe3O4@Carbon@Platinum-Chlorin e6 nanozyme for MRI-assisted synergistic catalytic-photodynamic-photothermal tumor therapy. J. Colloid Interface Sci. 2022, 628, 1033–1043.

[39]

Li, X. M.; Shen, D. K.; Yang, J. P.; Yao, C.; Che, R. C.; Zhang, F.; Zhao, D. Y. Successive layer-by-layer strategy for multi-shell epitaxial growth: Shell thickness and doping position dependence in upconverting optical properties. Chem. Mater. 2013, 25, 106–112.

[40]

Xu, Y. Z.; Zhang, H. K.; Zhang, N.; Xu, R. H.; Wang, Z.; Zhou, Y.; Shen, Q. F.; Dang, D. F.; Meng, L. J.; Tang, B. Z. An easily synthesized AIE luminogen for lipid droplet-specific super-resolution imaging and two-photon imaging. Mater. Chem. Front. 2021, 5, 1872–1883.

[41]

Xu, R. H.; Dang, D. F.; Wang, Z.; Zhou, Y.; Xu, Y. Z.; Zhao, Y. Z.; Wang, X. C.; Yang, Z. W.; Meng, L. J. Facilely prepared aggregation-induced emission (AIE) nanocrystals with deep-red emission for super-resolution imaging. Chem. Sci. 2022, 13, 1270–1280.

[42]

Perera, S. S.; Amarasinghe, D. K.; Dissanayake, K. T.; Rabuffetti, F. A. Average and local crystal structure of β-Er:Yb:NaYF4 upconverting nanocrystals probed by X-ray total scattering. Chem. Mater. 2017, 29, 6289–6297.

[43]

Huang, Y. Y.; Mroz, P.; Zhiyentayev, T.; Sharma, S. K.; Balasubramanian, T.; Ruzié, C.; Krayer, M.; Fan, D. Z.; Borbas, K. E.; Yang, E. et al. In vitro photodynamic therapy and quantitative structure-activity relationship studies with stable synthetic near-infrared-absorbing bacteriochlorin photosensitizers. J. Med. Chem. 2010, 53, 4018–4027.

[44]

Aranda, A.; Sequedo, L.; Tolosa, L.; Quintas, G.; Burello, E.; Castell, J. V.; Gombau, L. Dichloro-dihydro-fluorescein diacetate (DCFH-DA) assay: A quantitative method for oxidative stress assessment of nanoparticle-treated cells. Toxicol. in Vitro 2013, 27, 954–963.

Nano Research
Pages 2941-2948
Cite this article:
Zhang R, Lu Y, Zhou Y, et al. Utilizing dual-pathway energy transfer in upconversion nanoconjugates for reinforced photodynamic therapy. Nano Research, 2024, 17(4): 2941-2948. https://doi.org/10.1007/s12274-023-6202-0
Topics:

671

Views

7

Crossref

6

Web of Science

7

Scopus

0

CSCD

Altmetrics

Received: 27 July 2023
Revised: 14 September 2023
Accepted: 14 September 2023
Published: 16 October 2023
© Tsinghua University Press 2023
Return