Construction of a novel fluorescent nanoenzyme based on lanthanides for tumor theranostics

Abstract

Traditional lanthanide fluorides lack therapeutic efficacy against tumors, thus limiting their applications in biomedicine. In this study, we introduce a groundbreaking lanthanide-based nanomaterial known as ligand-free Ba_1.4Mn_0.6LuF₇: Yb³⁺/Er³⁺/Ho³⁺ (abbreviated as BMLF). This innovative material allows for the simultaneous tuning of upconversion luminescence emissions and Fenton-like reactions through the controlled release of Mn ions within the tumor microenvironment. BMLF exhibits dual functionality through integrating ratiometric fluorescence imaging for diagnosis and nanozyme-based catalytic therapy. These capabilities are successfully harnessed for tumor theranostics in vivo. This research presents a novel approach to leveraging lanthanide fluoride nanomaterials, transforming them into fluorescent nanoenzymes with theranostic potential.

Graphical abstract

Keywords

lanthanide fluoride / fluorescent nanoenzyme / tumor theranostics / controllable release

References

[1] Luo Z C, Mao D, Li X C, . Lanthanide-based nanoparticles for cancer phototherapy.Coordination Chemistry Reviews, 2024, 508: 215773

[2] Ferro-Flores G, Ancira-Cortez A, Ocampo-García B, . Molecularly targeted lanthanide nanoparticles for cancer theranostic applications.Nanomaterials, 2024, 14(3): 296

[3] Tong L T, Cao J J, Wang K, . Lanthanide-doped nanomaterials for tumor diagnosis and treatment by second near-infrared fluorescence imaging.Advanced Optical Materials, 2024, 12(4): 2301767

[4] Zhong Y, Wang J, Lu K Q, . NIR-II luminescent nanoparticles based-theranostic platform for drug-induced liver injury diagnoses and ameliorates.Chemical Engineering Journal, 2024, 488: 151058

[5] Zhang L T, Gao F, Liu S Q, . Synthesis of lanthanide-based scintillator@MOF nanocomposites for X-ray-induced photodynamic therapy.Inorganic Chemistry Frontiers, 2024, 11(5): 1607–1615

[6] Feng M, Wang Y Z, Lin B, . Degradable pH-responsive NIR-II imaging probes based on a polymer–lanthanide composite for chemotherapy.Dalton Transactions, 2020, 49(27): 9444–9453

[7] Zheng B Z, Fan J Y, Chen B, . Rare-earth doping in nanostructured inorganic materials.Chemical Reviews, 2022, 122(6): 5519–5603

[8] Yin X M, Xu W, Zhu G, . Towards highly efficient NIR-II response upconversion phosphor enabled by long lifetimes of Er³⁺.Nature Communications, 2022, 13(1): 6549

[9] Jiang M Y, Deng Z M, Zeng S J, . Recent progress on lanthanide scintillators for soft X-ray-triggered bioimaging and deep-tissue theranostics.VIEW, 2021, 2(4): 20200122

[10] Richard C, Viana B . Persistent X-ray-activated phosphors: mechanisms and applications.Light, Science & Applications, 2022, 11(1): 123

[11] Yang Y, Huang J S, Wei W, . Switching the NIR upconversion of nanoparticles for the orthogonal activation of photoacoustic imaging and phototherapy.Nature Communications, 2022, 13(1): 3149

[12] Zhao M Y, Zhuang H J, Zhang H X, . A LRET nanoplatform consisting of lanthanide and amorphous manganese oxide for NIR-II luminescence lifetime imaging of tumor redox status.Angewandte Chemie International Edition, 2022, 61(47): e202209592

[13] Zhang Q, Liu Y, Liu K, . Lanthanide-based microlasers: synthesis, structures, and biomedical applications.Nano Research, 2024, 17(1): 97–111

[14] Luo Z, Yi Z, Liu X . Surface engineering of lanthanide nanoparticles for oncotherapy.Accounts of Chemical Research, 2023, 56(4): 425–439

[15] Karges J . Clinical development of metal complexes as photosensitizers for photodynamic therapy of cancer.Angewandte Chemie International Edition, 2022, 61(5): e202112236

[16] Reddy M L P, Bejoymohandas K S . Luminescent lanthanide-based molecular materials: applications in photodynamic therapy.Dalton Transactions, 2024, 53(5): 1898–1914

[17] Zhao M Y, Sik A, Zhang H X, . Tailored NIR-II lanthanide luminescent nanocrystals for improved biomedical application.Advanced Optical Materials, 2023, 11(11): 2202039

[18] Tessitore G, Mandl G A, Maurizio S L, . The role of lanthanide luminescence in advancing technology.RSC Advances, 2023, 13(26): 17787–17811

[19] Zheng K T, Ma P T . Recent advances in lanthanide-based POMs for photoluminescent applications.Dalton Transactions, 2024, 53(9): 3949–3958

[20] Manikantan V, Varalakshmi G S, Pillai A S, . 5-Fluorouracil-loaded designed praseodymium oxide–poly-β-cyclodextrin nanorods for effectively inhibiting breast cancer cells.Inorganic Chemistry Communications, 2023, 153: 110830

[21] Sabaghi V, Rashidi-Ranjbar P, Davar F, . Development of lanthanide-based “all in one” theranostic nanoplatforms for TME-reinforced T1-weighted MRI/CT bimodal imaging.Journal of Drug Delivery Science and Technology, 2023, 87: 104703

[22] Musib D, Mukherjee M, Roy M . Emerging trends of La(III)-based compounds as the strategic tools for photodynamic therapy.Inorganica Chimica Acta, 2023, 558: 121751

[23] Bi S H, Deng Z M, Huang J Q, . NIR-II responsive upconversion nanoprobe with simultaneously enhanced single-band red luminescence and phase/size control for bioimaging and photodynamic therapy.Advanced Materials, 2023, 35(7): 2207038

[24] Liu W, Sun Y, Zhou B S, . Near-infrared light triggered upconversion nanocomposites with multifunction of enhanced antimicrobial photodynamic therapy and gas therapy for inflammation regulation.Journal of Colloid and Interface Science, 2024, 663: 834–846

[25] He Y, Li X, Guo Y Y, . Upconversion emission and its color modulation of the YVO₄: Er³⁺, Yb³⁺, Cr³⁺ nanoparticles.Optical Engineering, 2024, 63(3): 037106

[26] Liu D, Zeng C, Wang J, . Site preference induced dual-wavelength Mn²⁺ upconversion in K₂NaScF₆: Yb³⁺, Mn²⁺ and its application in temperature sensing.Advanced Optical Materials, 2024, 12(14): 2302819

[27] Su Y, Long Y, Zhao S, . Reduced Fe, Mn-based catalyst with dual reaction sites for rapid decolorization treatment via Fenton-like reactions.Applied Surface Science, 2023, 616: 156522

[28] He Y, Qin H, Wang Z, . Fe–Mn oxycarbide anchored on N-doped carbon for enhanced Fenton-like catalysis: importance of high-valent metal-oxo species and singlet oxygen.Applied Catalysis B: Environmental, 2024, 340: 123204

[29] Liu Y, Wang J . Multivalent metal catalysts in Fenton/Fenton-like oxidation system: a critical review.Chemical Engineering Journal, 2023, 466: 143147

[30] Duan P, Li M, Xu X, . Understanding of interfacial molecular interactions and inner-sphere reaction mechanism in heterogeneous Fenton-like catalysis on Mn-N4 site.Applied Catalysis B: Environmental, 2024, 344: 123619

[31] Xiang L J, Sun Y Q, Wang Y, . Engineered lanthanide-based nanomaterials as a novel bio-probe for in vivo dual-modal imaging.Journal of Luminescence, 2023, 261: 119908

Authors’ contributions

L.J.Xiang: writing-original draft, investigation, and writing –— review & editing; C.Y.Wang, Y.F.Mao, W.J.Li, and Y.Jiang: conceptualization, data curation, formal analysis, and project administration; Z.Huang and Z.F.Hu: project administration and supervision; Y.Wang: supervision, writing — review & editing. All authors have read and agreed to the published version of this manuscript.

Ethical statement

Animal experiments were approved by the Animal Ethics Committee of Anqing Normal University and performed in accordance with the Guidelines for Care and Use of Laboratory Animals of Anqing Normal University.

Declaration of competing interests

The authors declare that they have no competing interests.

Acknowledgements

This work was supported by Key project of the Natural Science Research in Universities of Anhui Province (No. 2023AH050510), Key Laboratory of Micro-nano Energy Materials and Application Technologies, University of Hunan Province (No. 2023HSKFJJ022), 2024 College Student Innovation and Entrepreneurship Training Project (X202410372053), Open Fund Projects of the Province Key Laboratory of the Biodiversity Study and Ecology Conservation in Southwest Anhui (Wsy202202), and 2019 University Excellent Talent Training Project (GXGWFX2019038, Z.H.).

Online appendix

Electronic supplementary material (ESM) can be found in the online version at https://doi.org/10.1007/s11706-024-0698-4 and https://journal.hep.com.cn/foms/EN/10.1007/s11706-024-0698-4 that includes Figs. S1–S6.

RIGHTS & PERMISSIONS

2024 Higher Education Press