A BF₂-bridged J-aggregate on a donor–acceptor conjugated oligomer with NIR-emissive theranostics for efficient bioimaging and cancer therapy

Abstract

The design and synthesis of integrated diagnostic and therapeutic materials are urgently needed to enhance the precise phototherapy (PTT) of tumors. However, there is still an urgent need to develop high-performance organic photothermal agents with suitable theranostic properties, especially those with near-infrared second window (NIR-II) emissive potency. In this study, a BF₂-bridged J-aggregates on the donor–acceptor (D–A) conjugated oligomer CH-1 was designed and synthesized. With the J-aggregate strategy, D–A-type CH-1 in nanoparticles (NPs) achieved enhanced intramolecular charge transfer and thus redshifted the absorption. Under 808 nm laser illumination, the CH-1 NPs achieved a high photothermal conversion efficiency of 66.8% for PTT, resulting in sufficient NIR-II fluorescence emission. In vitro experiments demonstrated that CH-1 NPs could produce enough local heat upon continuous laser illumination, resulting in apoptosis-mediated tumor cell death. In vivo experiments demonstrated the effectiveness of CH-1 NPs in high-resolution NIR-II imaging via whole-body angiography and tumor accumulation beyond 1400 nm. Subsequently, tumor homing and the performance of CH-1 NPs in tumor elimination were further demonstrated in a tumor-bearing mouse model. This study provides a paradigm for the development of NIR J-aggregate nanomedicines, achieving high-performance tumor phototheranostics with good biosafety.

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1. Introduction

Theranostics with imaging-guided therapeutic performance have demonstrated great potential for application in cancer treatment because of their noninvasiveness, spatiotemporal controllability, low toxicity, and ability to be integrated with theranostics.^1,2 Theranostics with photothermal therapy (PTT) performance mainly utilize photothermal agents (PTAs) for absorbing light energy to induce local hyperthermia to eradicate tumors, which is a promising local therapeutic strategy.^3–5 In particular, PTAs that respond in the near-infrared window (NIR, 700–1700 nm) achieve deep tissue penetration and good light safety, thus attracting great attention in recent years.^6–10 To date, various PTAs, such as MXenes,¹¹ gold nanostructures,¹² carbon nanotubes,¹³ and conjugated polymers and molecules,¹⁴ have been widely explored and have undergone many advances in bioimaging and disease therapy. However, the PTT efficiency of recently reported PTAs remains relatively low, especially in the near-infrared (NIR) window. Additionally, the potential toxic hazards of inorganic materials are still a cause for concern.^15–18 Organic PTAs have the advantages of adjustable photophysical and photochemical properties, high reproducibility, good stability and biocompatibility, making them the preferred materials for phototherapeutic applications.^19–22 Thus, high-performance organic PTAs with suitable theranostic properties, especially those with NIR-II emissive potency, should be further developed.^23–25

Organic conjugated materials, including polymeric and oligomeric materials, have been dramatically explored as theranostic agents because of their advantages in terms of good biocompatibility and structure-controllable photoactive performance.^26–30 In recent decades, novel molecules with donor–acceptor (D–A) structures have been gradually developed.^31–35 On the one hand, these molecules can effectively alleviate the toxicity of inorganic nanomaterials; on the other hand, their distorted molecular configurations can significantly inhibit fluorescence quenching and photobleaching caused by π–π stacking.^36–39 In addition, enhanced intramolecular charge transfer (ICT) is conducive to promoting absorption and emission wavelength redshift, increasing the performance of NIR-responsive phototheranostics. In addition to molecular design utilizing the D–A structure, highly ordered J-aggregates constitute an efficient strategy for the development of NIR theranostic agents, especially for enhancing NIR-II fluorescence.^40–44 Researchers have developed several common organic molecules, such as porphyrin derivatives, phycocyanin dyes, BODIPY and perylene imides, that can form J-aggregate arrangements.^45–48 However, at present, the development of organic small-molecule phototheranostic agents still faces enormous challenges, such as the fact that the expansion of the D–A structure mainly relies on the regulation of D–A conjugation.^49,50 More importantly, strategies to incorporate robust NIR-II fluorescence brightness and photothermal performance in a single molecule are lacking.⁵¹

Herein, we developed a J-aggregates nanomedicine (denoted CH-1 NPs) based on the NIR-responsive BF₂-bridged conjugated oligomer CH-1 that can efficiently ablate tumors upon NIR laser illumination for NIR-II fluorescence bioimaging and PTT (Fig. 1). With the J-aggregate strategy, D–A-type CH-1 in the NPs achieved enhanced ICT and thus redshifted the absorption; thus, the PTT effect, with a high photothermal conversion efficiency (PCE) of 66.8%, was activated with 808 nm laser illumination, and sufficient NIR-II fluorescence emission was produced. In vitro experiments demonstrated that CH-1 NPs could produce enough local heat upon continuous laser illumination, resulting in apoptosis-mediated tumor cell death. With NIR-II imaging, the CH-1 NPs provided high-resolution whole-body angiography and demonstrated effectiveness in NIR-II imaging beyond 1400 nm. Subsequently, tumor homing and the performance of CH-1 NPs in tumor elimination were further demonstrated in a tumor-bearing mouse model. This study provides a paradigm for the development of NIR J-aggregate nanomedicines, achieving high-performance tumor theranostics with good biosafety.

Fig. 1 Schematic diagram of the antitumor therapeutic mechanism of CH-1 NPs. Image created with BioRender with permission.

2. Results and discussion

2.1. Nanoparticle preparation and characteristics

A NIR-responsive BF₂-bridged conjugated oligomer CH-1 was designed and synthesized via simple reactions of Suzuki/Knoevenagel condensation (Fig. S1 in the SI). The structure and its intermediates were characterized by nuclear magnetic resonance (NMR), as shown in Fig. S2–S6 in the SI. With a typical D–A-type structure, CH-1 was conjugated with the electron donor methoxy-modified TPA and a strong electron acceptor containing a strong electron-withdrawing BF₂ moiety to enhance ICT and thus redshift the absorption. The highest occupied molecular orbital (HOMO) and the lowest unoccupied molecular orbital (LUMO) of CH-1 were investigated, and the energy gap (E_g) was measured to be approximately 1.57 eV (Fig. S7 in the SI). Due to the strong ICT character, the absorption peak of CH-1 was observed at 810 nm with a molar absorption coefficient of 2.5 × 10⁴ L mol⁻¹ cm⁻¹ in tetrahydrofuran (THF). Hence, the obtained CH-1 has the potential to serve as an NIR photoactive agent. To improve bioavailability, as shown in Fig. 2a, water-soluble NPs based on CH-1 were prepared with 1,2-distearoyl-sn-glycero-3-phosphoethanolamine-N-[methoxy(polyethylene glycol)-2000] (DSPE-PEG₂₀₀₀) via a nanoprecipitation method. As shown in Fig. 2b, compared with those of the free molecules in THF, the absorption spectra of the CH-1 NPs were obviously broader and redshifted from 810 nm to 850 nm due to molecular aggregation. As demonstrated by dynamic light scattering (DLS), the hydrodynamic diameter of the CH-1 NPs was approximately 84 nm, which was confirmed by transmission electron microscopy (TEM) (Fig. 2c). A negative zeta potential (−35.4 mV) was observed for the CH-1 NPs, which also exhibits pretty good stability in various solutions (Fig. S8 and S9 in the SI). The small size of the CH-1 NPs facilitates their tumor targeting and accumulation ability via the enhanced permeability and retention (EPR) effect. Furthermore, the absorption curves remained nearly unchanged before and after irradiation with an 808 nm laser, demonstrating the good photostability of the CH-1 NPs (Fig. S10 in the SI). The CH-1 NPs at various concentrations exhibited obvious fluorescence emission, which agreed with the fluorescence emission spectrum (Fig. 2d and Fig. S11 in the SI). These results indicate that the CH-1 NPs exhibit efficient NIR fluorescence upon 808 nm excitation.

Fig. 2 Preparation and characteristics of CH-1 NPs. (a) Schematic illustration of the preparation of CH-1 NPs. (b) Normalized absorption spectra of the CH-1 molecule and NPs. (c) Size distribution of the CH-1 NPs by DLS and TEM. (d) NIR emission images of CH-1 NPs at different concentrations upon 808 nm light excitation. (e) Temperature profile (black line) of CH-1 NPs under an 808 nm laser (1 W cm⁻²) illumination for 600 s and then cooling, and linear time data against −ln(θ) (red line) during the cooling period. (f) Photothermal curves of CH-1 NPs at different concentrations ranging from 0–100 µg mL⁻¹ under 1 W cm⁻² irradiation with an 808 nm laser. (g) Infrared thermal images. (h) Photothermal stability of the CH-1 NPs during 5 cycles of laser on/off.

To evaluate their therapeutic potential, the PTT properties of the CH-1 NPs were further investigated under 808 nm light excitation. As shown in Fig. 2e, the temperature of the CH-1 NP aqueous solution at a concentration of 100 µg mL⁻¹ increased from 22 to 81 °C under irradiation with an 808 nm laser light, indicating that the CH-1 NPs have good photothermal effects. According to the previously calculated method, the photothermal conversion efficiency (PCE, η) of the CH-1 NPs was determined to be approximately 66.8%, which is comparable to that of recently reported photothermal conversion agents.^52,53 As displayed in Fig. 2f and Fig. S12 in the SI, the photothermal effect of the CH-1 NPs exhibited concentration- and power-dependent behaviors. The thermal imaging results in Fig. 2g further demonstrated the aforementioned concentration-dependent photothermal conversion. Furthermore, the photothermal stability, which is an important indicator of PTT agents, was verified via 5 cycles of consecutive laser on/off examinations (Fig. 2h). Hence, CH-1 NPs are potential candidates for NIR-activated theranostics.

2.2. In vitro anticancer performance

The in vitro biocompatibility and anticancer activity of the CH-1 NPs upon irradiation at 808 nm were explored. First, the cell counting kit-8 (CCK-8) assay was utilized to evaluate the biocompatibility and phototoxicity of the CH-1 NPs. As shown in Fig. 3a, negligible cytotoxicity of CH-1 NPs at a maximum concentration of 30 µg mL⁻¹ was observed in 4T1 cells after 24 h of coincubation without light irradiation. However, the same concentrations of CH-1 NPs exhibited distinct killing effects on 4T1 cells upon light irradiation at 808 nm for 10 min. Notably, less than 20% cell survival was achieved when the concentration of CH-1 NPs was 30 µg mL⁻¹. These results demonstrated that efficient PTT of CH-1 NPs upon exposure to NIR light achieved sufficient antitumor performance. The apoptosis behaviors induced by CH-1 NPs upon irradiation at 808 nm were subsequently confirmed by flow cytometry (Fig. 3b). In addition, live/dead cell staining of tumor cells subjected to various treatments was further investigated. Negligible cell killing was clearly detected in the light irradiation only or CH-1 NPs alone groups, and the CH-1 NPs with 808 nm light irradiation groups caused almost complete tumor cell death (Fig. 3c). These results demonstrated that the CH-1 NPs efficiently promoted tumor cell photoablation upon NIR light irradiation. Furthermore, blood analysis of mice subjected to various treatments, including blood serum and complete blood, was performed after 14 days of treatment. These results indicate that CH-1 NPs have good biochemical safety, providing support for subsequent applications (Fig. 3d). The hemolytic test further demonstrated the good biosafety of the CH-1 NPs (Fig. S13 in the SI).

Fig. 3 In vitro phototherapy performance of CH-1 NPs. (a) Viability of 4T1 cells after treatment with CH-1 NPs and 10 min of irradiation with an 808 nm laser (1.0 W cm⁻²). (b) Flow cytometry plot of the apoptotic state of 4T1 cells after various treatments. (c) Live/dead staining of 4T1 cells treated with calcein-AM (green) and PI (red) after different treatments. (d) Blood serum and complete blood analyses of the treated mice after 14 days of treatment. Statistical analysis was performed via one-way ANOVA. ns: not significant, *P < 0.05, ****P < 0.0001. The data are presented as the mean ± S.D. (n = 3).

2.3. High-resolution NIR-II fluorescence imaging

Imaging-guided phototherapy is considered a powerful means for visualizing therapeutic agent accumulation at the tumor site and monitoring treatment progress. To validate the NIR-II fluorescence imaging performance of the CH-1 NPs, an in vivo NIR-II angiography experiment was conducted via intravenous injection of CH-1 NPs, followed by dynamic visualization via an NIR-II imager with an 808 nm excitation. NIR-II fluorescence signals were recorded after various long-pass (LP) filters were applied in the 1000–1500 nm range (Fig. 4a). Notably, the image of the 1400 nm LP has a higher resolution in whole-body angiography than those of the 1000–1300 nm and 1500 nm LPs. In detail, the yellow-marked blood vessels of the inner thigh were selected to analyse their full width at half maximum (FWHM) and signal-to-noise ratio (SNR) (Fig. 4b). Both the smallest FWHM (0.43 mm) and the largest SNR (3.68) further confirmed the highest resolution in NIR-II imaging with the 1400 nm LP filter. The above results demonstrated the NIR-II fluorescence imaging performance of the CH-1 NPs, especially above 1400 nm. On the basis of these advantages, the in vivo delivery of CH-1 NPs could be clearly visualized via NIR-II imaging.

Fig. 4 High-resolution whole-body NIR-II imaging. In vivo NIR-II angiography of blood vessels labelled with CH-1 NPs after different LP filters (a) and corresponding SNR analysis (b) of yellow-marked vessels. Excitation source: 808 nm laser.

2.4. In vivo theranostics of breast tumors

To evaluate the in vivo phototheranostics of the primary tumor, 4T1 tumor-bearing nude mice were established, and a tumor volume of nearly 80 mm³ was chosen for the next imaging application. To test tumor-targeting performance, the mice were treated with CH-1 NPs (100 µL, 1 mg mL⁻¹) via intravenous injection and then placed in a NIR-II fluorescence imager for real-time observation. As shown in Fig. 5a and Fig. S14 in the SI, the NIR-II fluorescence signal at the tumor sites gradually increased within 24 h postinjection and reached a maximum at 24 h postinjection, suggesting the relatively efficient tumor location of the CH-1 NPs via the EPR effect. Furthermore, although the fluorescence signal intensity decreased gradually at 24 h postinjection, it was still sufficient to support obvious imaging efficiency within 48 h. In addition, NIR-II fluorescence images of the main organs and tumor tissue were further investigated at 24 h postinjection. These results revealed that the fluorescence signals were distributed mainly in the liver, spleen, and tumor tissues, demonstrating the accumulation of CH-1 NPs at the tumor site (Fig. S15 in the SI). Owing to their efficiency in tumor targeting, we further investigated the in vivo PTT performance of CH-1 NPs. After intravenous injection of CH-1 NPs (100 µL, 1 mg mL⁻¹), the treated mice were irradiated with an 808 nm laser at an intensity of 1.0 W cm⁻², and then the temperatures were monitored by an infrared thermal imaging camera. As depicted in Fig. 5b and c, the tumor temperatures of the mice treated with 10 min of irradiation with an 808 nm laser at 1.0 W cm⁻² were increased to 56 °C. In contrast, the tumors in the PBS-treated mice slightly changed in temperature after the same treatment. These results demonstrated the good in vivo photothermal heating performance of CH-1 NPs, which benefitted from sufficient tumor targeting.

Fig. 5 In vivo imaging-guided therapy. (a) NIR-II fluorescence imaging of the tumor targeting ability of CH-1 NPs at different postinjection times. Infrared thermal images (b) and corresponding temperatures (c) of the tumors in the mice treated with 808 nm laser irradiation for 10 min. (d) Digital images of tumors separated from the treated mice at the end of the treatments. (e) Tumor weight analysis of the treated mice after different treatments. (f) Body weight changes of the treated mice within 14 days of treatment. (g) Representative H&E and TUNEL staining of tumor tissue after different treatments. (h) Bcl-2 and Bax staining of tumor tissue after different treatments. Statistical analysis was performed via one-way ANOVA. ns: not significant, ****P < 0.0001. The data are presented as the mean ± S.D. (n = 5).

Taking advantage of the tumor-targeting in vivo photothermal heating performance, in vivo phototherapy of the primary tumor was evaluated in 4T1 tumor-bearing nude mice. The mice with a tumor volume of approximately 80 mm³ were randomly divided into four groups (n = 5 for each group): PBS, PBS with 1.0 W cm⁻² light (PBS + L), CH-1 NPs, and CH-1 NPs with 1.0 W cm⁻² light (CH-1 NPs + L). PBS or CH-1 NPs were intravenously injected into the mice. Additionally, the PBS + L and CH-1 NPs + L groups were treated with 808 nm laser irradiation (1.0 W cm⁻²) for 10 min at 24 h postinjection. As shown in Fig. 5d, the tumors in the PBS + L and CH-1 NPs groups exhibited growth tendencies similar to those in the PBS group. In contrast, the CH-1 NPs + L group exhibited obvious tumor elimination without any recurrence within 14 days of treatment. The tumor weight analysis of the treated mice further confirmed the above results (Fig. 5e). These results indicated that CH-1 NPs completely ablated the breast tumor without any recurrence via the PTT effect.

During the whole period of treatment, there was no obvious difference in mouse weight among the four groups (Fig. 5f). To further demonstrate the effectiveness of CH-1 NPs with 808 nm light irradiation, tumor biopsies, including hematoxylin and eosin (H&E) staining and terminal deoxynucleotidyl transferase dUTP nick end labelling (TUNEL) assays, were performed. As shown in Fig. 5g and Fig. S16 in the SI, efficient apoptosis of tumor cells was achieved in the CH-1 NPs + L group, as evidenced by highly fragmented nuclei and apoptotic brown nuclei, indicating the antitumour efficiency of CH-1 NPs with 808 nm light irradiation. Similarly, Bcl-2 (an antiapoptotic protein) and Bax (a proapoptotic protein) antibody staining is an important method for studying the mechanism of apoptosis. As displayed in Fig. 5h, a lower level of Bcl-2 and higher level of Bax protein expression were observed in the CH-1 NP group than in the other groups, demonstrating the thermal ablation of CH-1 NPs in tumor cells. The preliminary biocompatibility of CH-1 NP treatment and 808 nm light irradiation was further demonstrated via biopsy of H&E-stained tissue from the main organs (Fig. S17 in the SI). These results confirmed the antitumour effectiveness and good biocompatibility of the CH-1 NPs.

3. Conclusions

In summary, J-aggregate nanomedicine CH-1 NPs based on an NIR-responsive BF2-bridged conjugated oligomer were developed, which efficiently eliminated tumors via NIR-II fluorescence imaging-guided PTT upon NIR laser illumination. With the J-aggregate strategy, the D–A-type CH-1 oligomer in the NPs achieved enhanced ICT, which promoted redshifted absorption, further leading to a high PCE of 66.8% for the PTT effect and sufficient NIR-II fluorescence emission with 808 nm laser illumination. In vitro experiments demonstrated that CH-1 NPs could produce enough local heat upon continuous laser illumination, resulting in apoptosis-mediated tumor cell death. Furthermore, the CH-1 NPs provided high-resolution whole-body angiography and demonstrated effectiveness in NIR-II imaging beyond 1400 nm. The performance of CH-1 NPs in tumor elimination was subsequently demonstrated in a tumor-bearing mouse model. This study provides a paradigm for the development of NIR J-aggregate nanomedicine, achieving high-performance tumor phototheranostics with good biosafety. Although the NIR J-aggregate nanomedicine shows many advantages, batch-to-batch reproducibility is another issue that deserves consideration for mass production.

Ethics statement

All animal experiments were performed under the guidelines, evaluated, and approved by the ethics committee of Soochow University, Suzhou, China.

Author contributions

Yuxin Guo and Yujie Ma: methodology, formal analysis, investigation, data curation, and writing of the original draft. Zhenghao Huang: resources and methodology. Huan Chen: resources, methodology and writing, review and editing. Ying Liu and Jing Zhai: investigation, methodology and data curation. Xuejuan Li and Yijian Gao: investigation, resources and data curation. Zebin Chen, Yu Wang and Shengliang Li: conceptualization, writing review and editing, supervision, project administration and funding acquisition.

Conflicts of interest

There are no conflicts to declare.

Data availability

All data supporting this study are available in the article and its supplementary information (SI). The supplementary information includes additional experimental methods and supporting figures. See DOI: https://doi.org/10.1039/d5tb02202a.

Acknowledgements

This work was supported by the National Natural Science Foundation of China (No. 52573172), the Natural Science Foundation of Jiangsu Province (No. BK20231523), Jiangsu Specially Appointed Professorship, Jiangsu Province Health Innovation Team, and the Suzhou Science and Technology Program (No. SKY2022039). This work was also funded by the Guangdong High-level Hospital Construction Fund (No. ynkt2021-zz23) and the 2022 Guangdong Hospital Association Pharmaceutical Research Special Fund for Young Scholars in the Field of Pharmaceutical Research (No. 2022YXKY08). The authors would also like to acknowledge the project funded by the Priority Academic Program Development (PAPD) of Jiangsu Higher Education Institutions and Suzhou International Joint Laboratory for Diagnosis and Treatment of Brain Diseases.

Notes and references

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Footnote

† These authors contributed equally to this work.

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