An intelligent NIR-IIb-responsive lanthanide@metal–organic framework core–shell nanocatalyst for combined deep-tumor therapy†

Chaoqun Jiang ^a, Yu Chen ^a, Xiaolong Li *^b and Youbin Li *^a
aSchool of Physics and Electronic Sciences, Hunan Provincial Key Laboratory of Flexible Electronic Materials Genome Engineering, Changsha University of Science and Technology, Changsha 410114, People's Republic of China
^bKey Laboratory of Magnetic Molecules and Magnetic Information Materials of Ministry of Education & School of Chemistry and Materials Science of Shanxi Normal University, Taiyuan 030032, China. E-mail: liyoub@csust.edu.cn

First published on 27th August 2024

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Introduction

Colorectal cancer is a type of cancer that affects the rectum, which is responsible for a significant number of cancer-related deaths worldwide.^1–3 Thus, initiating measures to inhibit the progression of lesions is paramount. It is important to note that the clinical treatment methods that are frequently used have some drawbacks. For example, surgical resection often fails to completely remove tumors, leading to tumor retention and recurrence.^4,5 Chemotherapy drugs inevitably cause serious side effects that can result in damage to normal tissues.⁶ Thus, a highly efficient therapeutic modality is needed to prevent the progression of cancer.

As is known, PDT is a highly effective treatment strategy that utilizes photosensitizers (PSs) to convert tissue O₂ into ROS to eliminate tumor cells.^7–12 However, most of the PSs utilized in clinical practice exhibit hydrophobic characteristics and inadequate tumor selectivity and may induce phototoxicity in surrounding normal tissues.^13,14 These drawbacks have impeded the therapy efficacy of PDT, thereby necessitating the development of alternative PSs. Recently, MOFs have been regarded as a highly porous and versatile class of materials, which are synthesized via the coordination-driven assembly of metal ions and organic ligands, thereby allowing high PS loading with minimum self-quenching.¹⁵ However, most MOF-based PDTs typically rely on visible light excitation, thus leading to an undesirable tissue penetration depth. There is an urgent need to develop a MOF-based photosensitizer for effective PDT of deep-seated tumors.

Lanthanide-doped UCNPs are highly promising nanoparticles that can convert near-infrared (NIR) light to UV/visible light, which has attracted considerable attention in multiple biomedical fields.^16–20 UCNPs have recently garnered much attention for their remarkable photoupconversion ability in NIR light-mediated photoregulation of biosensors, biomedicine, etc.^21–26 The resulting UV/visible light can then excite PSs to generate ROS and enable deeper penetrating PDT.^27–33 Chen's group has fabricated a UMOF@Au-based nanocatalyst for cascade-driven PDT under NIR laser irradiation.²⁹ Zhao's group has designed a NIR light-activated UCNP MOF nanocomposite for spatiotemporally controlled protein release.³³ Yan and co-workers presented an upconverting MOF for NIR light-responsive tri-modal therapy of cancer.³¹ However, it is unfortunate that the penetration depth of NIR light irradiation is still limited. Excitingly, evidence suggested that the NIR-IIb window (1400–1600 nm) has enabled deep tissue penetration owing to the reduced light scattering and tissue absorption.^34–36 Therefore, there is an urgent need to develop a NIR-IIb photo-responsive MOF-based nanocomposite for deep tissue PDT.

Meanwhile, the efficacy of a single treatment modality in tumor management is often limited, and the development of a multimodal treatment strategy yet remains a challenge. PTT is a technique that uses nanoagents with photothermal conversion characteristics to generate heat under light irradiation and then kill cancer cells in localized regions.^37–40 Various nanomaterials have been developed as photothermal agents for light-mediated PTT.^37–40 Thereof, ICG is a US Food and Drug Administration-approved fluorescent dye used in clinical practice.^41,42 It can absorb NIR light and convert it into heat energy and singlet oxygen, making it an effective thermal adjuvant therapy nanoagent. Thus, the combination of ICG-based PTT and PDT has proved to be an effective method for treating cancer.

In this work, we have proposed a multifunctional UCNPs@ZrMOF@ICG nanocomposite by in situ coating the ZrMOF on the UCNPs for 1532 nm laser-mediated deep tissue PDT (Scheme 1). The energy transfer from the UCNPs to the porphyrin-based ZrMOF is relatively efficient for burst ROS generation to kill the tumor cells with a high penetration depth. Benefiting from the excellent pore character of the ZrMOF, the ICG molecules were loaded in the ZrMOF for NIR laser-irradiated PTT. We have successfully realized highly efficient cancer treatment by combining PDT with PTT. This research has come up with an innovative synergistic method for enhanced deep tissue antitumor treatments.

Results and discussion

Construction and characterization of the UCNPs@ZrMOF nanocomposite

The NaLuF₄:Er core, NaLuF₄:Er@NaYF₄ core–shell and NaLuF₄:Er@NaYF₄@ZrMOF core–shell–shell nanoparticles were designed using a two-step synthesis method. As shown in Scheme 1, the NaLuF₄:Er core and NaLuF₄:Er@NaYF₄ core–shell nanoparticles were first synthesized using the high-temperature coprecipitation method.³⁶ Then, the OA-NaLuF₄:Er@NaYF₄ core–shell nanoparticles were converted into hydrophilic nanoparticles using the polyacrylic acid (PAA) modification method.³⁶ After this, the Zr ions and the meso-tetra (4-carboxyphenyl) porphine were self-assembled on the PAA-modified NaLuF₄:Er@NaYF₄ core–shell nanoparticles by coordination bonds. The morphology and phase of the nanoparticles were analyzed by transmission electron microscopy (TEM) and X-ray diffraction (XRD). As shown in Fig. 1A, the TEM image of the NaLuF₄:Er core nanoparticles showed a uniform dispersion with an average size of ∼35 nm. The elemental mapping results further proved the formation of the NaLuF₄:Er core nanoparticles (Fig. S1, ESI†). The high-resolution TEM (HRTEM) result (Fig. 1B) indicated the excellent crystallinity nature and the space between the two adjacent lattices was calculated to be 0.301 nm, matching well with the (110) crystal plane of the hexagonal phase NaLuF₄.³⁶ The outer NaYF₄ shell was then coated on the NaLuF₄:Er core nanoparticles to eliminate the surface quenching effect of the NaLuF₄:Er nanoparticles. The resultant core–shell nanoparticles (UCNPs) revealed an average diameter of ∼45 nm (Fig. 1C). The HRTEM images demonstrated the exposure of (100) facets of the hexagonal phase NaYF₄ (Fig. 1D). The elemental mapping results of the nanoparticles further revealed the core–shell structure (Fig. S2, ESI†). The XRD patterns depicted in Fig. 1I provide further evidence of the formation of a hexagonal phase structure (JCPDS: 27-0726).

The structure of the NaLuF₄:Er@NaYF₄@ZrMOF nanoparticles was then analyzed. As shown in Fig. 1E–G, the nanoparticles demonstrated a clear boundary line between the UCNPs and ZrMOF. The surface zeta potentials of the PAA-modified UCNPs and UCNPs@ZrMOF were measured to be −20 and +5 mv, respectively, revealing the electrostatic interaction between the PAA-UCNPs and ZrMOF (Fig. S3, ESI†). HRTEM images revealed that the ZrMOF shell was a non-crystallizable polymer (Fig. 1F). The elemental mapping and EDS line scan results demonstrated the existence of Zr elements in the shell of the nanocomposite (Fig. 1H and Fig. S4, ESI†), proving the successful fabrication of the ZrMOF shell on the core–shell UCNPs. The energy-dispersive X-ray spectrometry result also indicates the existence of Na, F, Lu, Y, Er, and Zr elements (Fig. S5, ESI†). The UC emission of the core and core–shell nanoparticles under 1532 nm laser excitation was then investigated. As shown in Fig. 1J, the UC emission spectra of the core UCNPs display two main emission peaks banded at 550 nm and 670 nm. The present emission peaks can be elucidated by the electronic transitions of Er³⁺ from ²H_11/2/⁴S_3/2 → ⁴F_9/2 (green emission, 550 nm) and ⁴F_9/2 → ⁴I_15/2 (red emission, 670 nm) under 1532 nm excitation (Fig. 1J).³⁵ In order to improve the emission intensity, an inert shell NaYF₄ was coated on the NaLuF₄:Er core nanoparticles to avoid the surface quenching effect (Fig. 1K). In contrast with the UC emission intensities of the NaLuF₄:Er core nanoparticles, those of the NaLuF₄:Er@NaYF₄ core–shell nanoparticles were improved by ∼21 fold, making it more suitable as a light converter (Fig. 1J).

Evaluation of singlet oxygen generation

OA-UCNPs were then modified by PAA according to our previous reports.⁴³ The UC emission of the PAA-UCNPs was then studied. As shown in Fig. S6 (ESI†), the UC emission of PAA-UCNP nanoparticles is decreased by ∼2 times, which can be explained by the quenching effect of OH⁻ groups in water. Then, the ZrMOF shell was in situ grown on the PAA-UCNPs to form the UCNPs@ZrMOF nanocomposite for deep tissue PDT. As shown in Fig. 2A, the UCNPs can emit visible (green and red) emission under 1532 nm laser excitation, and the visible light was absorbed by ZrMOF; thereby, the O₂ was catalyzed by the ZrMOF to generate ROS (¹O₂) for PDT. The UV-vis spectra of the UCNPs@ZrMOF were recorded. As shown in Fig. 2B, the absorbance spectra of the ZrMOF display broadband absorption in the visible region, which highly overlaps with the emission spectra of the UCNPs. The emission spectra of the UCNPs@ZrMOF nanocomposite showed a sharp decrease, further revealing the efficient energy transfer from the UCNPs to the ZrMOF, and the Förster resonance energy transfer (FRET) efficiency was calculated to be ∼85%. The ROS-producing ability of the UCNPs@ZrMOF nanocomposite was further investigated by utilizing the 1,3-diphenylisobenzofuran (DPBF) detection method.⁴⁴ As displayed in Fig. 2C–F, the absorption peaks of DPBF solution at 417 nm remained unchanged after the addition of the UCNPs@ZrMOF nanocomposite without 1532 nm laser excitation. In contrast, the peak intensity of the DPBF solution containing the UCNPs@ZrMOF nanocomposite gradually decreased under 1532 nm laser irradiation for 15 min. The peak intensity at 417 nm decreased by about 35% at low laser power density (0.8 W cm⁻²), proving the high light transfer efficiency of the UCNPs@ZrMOF nanocomposite and high ROS generation ability. Furthermore, the ROS generation ability of the UCNPs@ZrMOF nanocomposite covered with different thicknesses of pork tissue was evaluated. As shown in Fig. S7 (ESI†), slight ROS can still be detected when the thickness of the pork tissue is increased up to 12 mm, revealing the high performance of the UCNPs@ZrMOF nanocomposite for 1532 nm light-triggered deep tissue PDT.

Investigation of photothermal conversion efficiency

Despite the high-performance ROS-producing properties of the UCNPs@ZrMOF nanocomposite for PDT, the use of a single treatment model still hinders the effective treatment of tumors. As is known to all, the ICG molecule is used to treat tumors by converting NIR light into heat energy for PTT. Benefitting from the high biocompatibility of the ICG molecule and the mesoporous nature of the UCNPs@ZrMOF nanocomposite, the ICG molecule was loaded into the UCNPs@ZrMOF nanocomposite for NIR light-mediated PTT. The in vitro photothermal properties of the UCNPs@ZrMOF@ICG nanocomposite were first studied. As shown in Fig. 3A, the UCNPs@ZrMOF@ICG nanocomposite showed strong absorption in the NIR region (∼808 nm). The ICG was encapsulated into the UCNPs@ZrMOF with a high loading capacity of ≈85% (Fig. S8, ESI†). The infrared thermal images of water showed no heating effect, whereas the temperature of the UCNPs@ZrMOF@ICG nanocomposite increased rapidly under 808 nm laser (1 W cm⁻²) irradiation for 6 min (Fig. 3B), demonstrating the high photothermal performance of ICG. The laser power density and concentration-based heating properties of the UCNPs@ZrMOF@ICG nanocomposite were evaluated. As shown in Fig. 3C, the temperature of the UCNPs@ZrMOF@ICG nanocomposite has increased by nearly 55 °C under 808 nm laser irradiation (2 W cm⁻²). The concentration-based temperature profiles were also obtained under 808 nm laser excitation (1.5 W cm⁻²). Inspired by the excellent heating properties, the photothermal conversion efficiency was measured to be ∼28% based on Fig. 3E. The photostability of the UCNPs@ZrMOF@ICG nanocomposite was then studied. As displayed in Fig. 3F, the UCNPs@ZrMOF@ICG nanocomposite showed high photostability after three cycles of turning on/off the 808 nm laser. These results further demonstrate that the UCNPs@ZrMOF@ICG nanocomposite was an ideal photothermal nanoagent for PTT.

In vitro synergistic PDT/PTT assessments

Given the efficient ROS generation ability and high photothermal performance of the UCNPs@ZrMOF@ICG nanocomposite, the in vitro therapeutic effect of the UCNPs@ZrMOF@ICG nanocomposite was investigated (Fig. 4A). The UCNPs@ZrMOF@ICG was first introduced into HCT 116 cells for 4 h incubation, and the HCT 116 cells did not show any noticeable changes in cell viability even after being exposed to UCNPs@ZrMOF@ICG at a concentration of 1000 μg mL⁻¹ (Fig. 4B), indicating the high biocompatibility. Next, we demonstrated the in vitro PDT/PTT of HCT 116 cells under 1532/808 nm laser excitation. As shown in Fig. 4C, the control groups (1–4) could not affect the cell viability. In contrast, both the UCNPs@ZrMOF@ICG plus 1532 nm group and UCNPs@ZrMOF@ICG plus 1532/808 nm group showed efficient therapeutic performance owing to the high ROS generation ability and high photothermal performance. Furthermore, the UCNPs@ZrMOF@ICG plus 1532/808 nm groups showed higher tumor cell kill efficiency (∼63%) than the UCNPs@ZrMOF@ICG plus 1532 group (50%), which was attributed to the synergistic PDT/PTT treatment effect. To visualize the synergistic therapy performance, we performed calcein-acetoxymethyl (AM, live staining) and propidium iodide (PI, dead staining) co-staining tests. The UCNPs@ZrMOF@ICG plus 1532/808 nm group exhibited enhanced tumor therapeutic, which coincided with the result of Fig. 4C (Fig. 4D). The intracellular ROS production ability was then tested by using the 2′,7′-dichlorofluorescein diacetate (DCFH-DA) staining assay. After treatment with UCNPs@ZrMOF@ICG plus 1532/808 nm, the confocal images displayed significantly higher ROS levels than the other groups (Fig. 4E). These results further demonstrated the high synergistic therapy performance of the developed UCNPs@ZrMOF@ICG nanocomposite.

In vivo antitumor therapy

Based on the promising results of synergistic therapy of tumor cells in vitro, we next evaluated the in vivo anti-tumor effectiveness of the UCNPs@ZrMOF@ICG nanocomposite by using the HCT 116 tumor-bearing mice model (Fig. 5A). Prior to executing in vivo therapy, it was imperative to reveal the biodistribution of the UCNPs@ZrMOF@ICG nanocomposite in vivo. The tumor-bearing mice were injected with an identical dosage of the UCNPs@ZrMOF@ICG nanocomposite through the tail vein. The mice were sacrificed after 6, 24, and 48 h of injection and the main organs were collected for inductively coupled plasma mass spectrometry (ICP-MS) detection. As shown in Fig. 5B, the UCNPs@ZrMOF@ICG nanocomposite was mainly excreted from the liver and spleen, and ∼6% of the UCNPs@ZrMOF@ICG nanocomposite was retained in the tumor site after 24 h injection owing to the enhanced permeability and retention effect. We then performed the pharmacokinetic test of the UCNPs@ZrMOF@ICG nanocomposite in vivo after intravenous injection. The pharmacokinetic study was evaluated through detecting the Lu³⁺ contents of blood samples collected at different time points. As shown in Fig. S9 (ESI†), the blood half-time was calculated to be 1.38 h, which allowed for effective tumor retention. Afterwards, the HCT 116 tumor-bearing mice were divided into 5 groups (n = 3) with various treatments: (1) PBS, (2) PBS + 808/1532 nm, (3) UCNPs@ZrMOF@ICG, (4) UCNPs@ZrMOF@ICG + 1532 nm, and (5) UCNPs@ZrMOF@ICG + 1535/808 nm. After intravenous injection for 24 h, a 1532 plus 808 nm laser, an 808 nm laser, and a 1532 plus 808 nm laser was administered with the group (2), (4) and (5) for 10 min every two days, respectively. The drug injections were repeated at 4-day intervals. The body weight and tumor volumes were recorded every two days. As seen in Fig. 5C, the body weight exhibits no obvious changes after different treatments, indicating the high biocompatibility of the UCNPs@ZrMOF@ICG nanocomposite. We then tracked the tumor volumes of mice (Fig. 5D) throughout the treatment period, and the tumors were removed and analyzed after 14 days of treatments (Fig. 5E). In contrast with the control groups (1–3), the UCNPs@ZrMOF@ICG plus 1532 nm laser group (4) exhibit significant inhibition due to the NIR-II light-mediated PDT. Moreover, the UCNPs@ZrMOF@ICG plus 1532/808 nm laser-treated group (5) showed stronger tumor inhibition, proving the enhanced antitumor treatments with the combination of PDT and PTT.

The isolated tumors were further dissected for hematoxylin and eosin (H&E) and terminal deoxynucleotidyl transferase dUTP nick-end labeling (TUNEL) staining tests. As shown in Fig. 5F and G, the UCNPs@ZrMOF@ICG plus 1532/808 nm treated groups displayed severe tissue necrosis when compared with other groups. These results further validated the effectiveness of the proposed synergistic therapy approach for antitumor treatments. Blood biochemistry tests were further conducted. As shown in Fig. S10 (ESI†), no statistical difference was observed after 3 and 7 days of intravenous injection, revealing the negligible toxicities of the UCNPs@ZrMOF@ICG in vivo. The long-term in vivo biosafety of the treatments was also tested. The mice were intravenously injected with UCNPs@ZrMOF@ICG for 15 and 30 days and the control group was monitored without injection. The histopathological test of the main organs (heart, liver, spleen, lungs, and kidneys) displayed no lesion, demonstrating negligible long-term toxicity (Fig. S11, ESI†).

Conclusions

In this work, the UCNPs@ZrMOF nanocomposite was designed by in situ coating the ZrMOF on the UCNPs. The UCNPs were first excited by high tissue penetrating 1532 nm light to generate visible emission, which enables the ZrMOF to absorb the visible light to produce ROS for NIR-IIb light mediated deep tissue PDT. Furthermore, by loading the photothermal nanoagent ICG into the pore of the ZrMOF, the designed UCNPs@ZrMOF@ICG nanocomposite has enabled efficient antitumor treatment through synergistically 1532 nm light-activated PDT and NIR light-mediated PTT. We anticipate that the designed nanoplatform can emerge as a highly effective strategy in combating cancer through the combination of PDT and PTT.

Experimental

All the procedures for the experiments are given in the ESI.†

Author contributions

Chaoqun Jiang: methodology, formal analysis, investigation, data curation, and writing – original draft; Yu Cheng: methodology and investigation; Xiaolong Li: conceptualization, methodology, resources, writing – review and editing, and funding acquisition. Youbin Li: conceptualization, methodology, resources, writing – review and editing, supervision, project administration, and funding acquisition.

Data availability

The data supporting this article have been included as part of the ESI.†

Conflicts of interest

There are no conflicts to declare.

Acknowledgements

This work was supported by the National Natural Science Foundation of China (No. 62205033 and 52003144) and the Hunan Provincial Natural Science Foundation of China (No. 2022JJ40469).

Notes and references

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Footnote

† Electronic supplementary information (ESI) available. See DOI: https://doi.org/10.1039/d4tb01321b

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