Key Takeaways & Executive Findings
- •• • In vivo 4T1 tumor-bearing mice treated with MMGZ plus 808 nm laser (2.0 W/cm², 5 min) exhibited significant tumor volume reduction (P < 0.0001) compared to PBS controls, demonstrating that the cascade nanoreactor achieves potent tumor growth inhibition through synergistic CO gas therapy, starvation, and photothermal effects. • • The nanoreactor addresses the bottleneck of insufficient endogenous H2O2 (100 μM) and acidity (pH 6.5) in the tumor microenvironment by using GOx to catalyze glucose conversion, generating gluconic acid and H2O2 to amplify MnCO activation and CO release, thereby overcoming the limited efficacy of conventional CO-releasing molecules. • • MPDA's high photothermal conversion efficiency enables localized hyperthermia upon 808 nm laser irradiation, which not only directly induces photothermal damage but also intensifies CO release, providing a trimodal therapeutic effect that enhances overall anticancer efficacy. • • The core-shell design with ZIF-8 encapsulation protects GOx from degradation during circulation and enables tumor-specific release, mitigating off-target CO poisoning risks associated with direct MnCO-H2O2 reactions, as evidenced by the significant antitumor effect and safety profile in the in vivo study.
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Abstract
Carbon monoxide (CO) therapy has emerged as a promising approach in cancer treatment. Selecting suitable nanocarriers for delivering manganese carbonyl (MnCO), a CO donor, while simultaneously regulating CO release and compensating for hydrogen peroxide (H2O2) and acidity in the tumor microenvironment is crucial for enhancing the effectiveness of CO therapy. In this study, a tumor microenvironment-responsive core-shell structured cascade nanoreactor was designed and synthesized using mesoporous polydopamine (MPDA) as a nanocarrier, followed by loading of MnCO and glucose oxidase-encapsulated zeolite imidazolate framework-8 (GOx@ZIF-8) nanoparticles. Upon entering cancer cells, the protective shell of GOx@ZIF-8 degrades in response to the acidic tumor environment, releasing GOx. GOx catalyzes the conversion of endogenous glucose into gluconic acid and H2O2, accelerating energy starvation in tumor cells. This process, in turn, promotes the reaction between MnCO and H2O2, resulting in in-situ amplified release of CO. Additionally, the excellent photothermal properties of MPDA enable photothermal therapy. This comprehensive antitumor strategy represents a promising advancement in the field of CO-based cancer therapy.
1. Introduction
Carbon monoxide (CO) therapy has garnered significant attention in the field of gas therapy due to its promising potential in cancer treatment. However, the gaseous nature of CO and its high affinity for human hemoglobin limit its clinical application. To overcome this challenge, various CO-releasing molecules (CORMs) have been developed to deliver CO in biological systems. CORMs are most typically based on rare transition metals (Ru, Mn, Mo, etc.) decorated with dative, L-type CO ligands that can generate CO through reactions with H2O2 without requiring external stimuli. Nevertheless, the poor water solubility of these complexes and the specific tumor microenvironment, characterized by limited levels of H2O2 (100 μM) and acidic conditions (pH 6.5), hampers the anticancer effectiveness of CO therapy. Therefore, it is imperative to design and synthesize suitable nanocomposites capable of delivering transition-metal carbonyl complexes and regulating the tumor microenvironment to optimize the effectiveness of CO therapy.
Currently, a wide range of nanomaterials have been employed to integrate CO-releasing molecules for the development of multifunctional gas therapy nanoplatforms. These include silica nanoparticles, micelles, metal–organic frameworks, polymers, liposomes, and inorganic multifunctional nanoparticles. Among these nanomaterials, mesoporous polydopamine nanoparticles (MPDA) possess several advantages, such as a large surface area, high loading capacity, efficient photothermal conversion, and excellent biocompatibility with tissues. Consequently, MPDA has been recognized as a promising candidate for delivering manganese carbonyl (MnCO), which serves as a CO donor in gas therapy. While initial studies have shown promise through the encapsulation of MnCO within MPDA mesopores via hydrophobic interactions, this approach remains in its nascent stages. The direct reaction with endogenous H2O2 lacks precision, potentially posing a risk of CO poisoning. Additionally, the limited levels of H2O2 and acidity within tumor sites hinder the achievement of a more effective antitumor therapeutic effect. Therefore, there is an urgent requirement for the development of a nanoreactor responsive to the tumor microenvironment, capable of controlling CO release while also compensating for intertumoral H2O2 and acidity. However, such a nanoreactor has been rarely reported.
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Wen-Xiu Ren, Hao Yu, Chen-Yu Li, Fei Kong, Zi-Liang He, Seeram Ramakrishna, Jie Feng, Yu-Bin Dong (2025). Engineering a Multifunctional Core–Shell Structured Cascade Nanoreactor for Augmented and Synergistic Carbon Monoxide Oncotherapy. SCIENCE CHINA Materials. https://doi.org/10.1007/s40843-024-3281-x
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Frequently Asked Questions
What is the quantitative in vivo antitumor efficacy of the MMGZ nanoreactor under laser irradiation, and how does it compare to controls?
In 4T1 tumor-bearing mice, treatment with MMGZ plus 808 nm laser (2.0 W/cm², 5 min) resulted in a statistically significant reduction in tumor volume (P < 0.0001) compared to PBS, Laser, MGZ, MMZ, and MMGZ without laser groups. Tumor weights were also markedly lower in the MMGZ/Laser group, confirming potent tumor growth inhibition.
How does the nanoreactor overcome the limited H2O2 and acidity in the tumor microenvironment to enhance CO release?
The GOx@ZIF-8 shell degrades in the acidic tumor environment (pH 6.5), releasing GOx. GOx catalyzes glucose to gluconic acid and H2O2, thereby increasing local H2O2 concentration and acidity. This amplified H2O2 reacts with MnCO to generate CO in situ, compensating for the insufficient endogenous H2O2 (100 μM) and enabling controlled CO release.
What are the photothermal performance characteristics of MPDA in this system, and how do they contribute to therapy?
MPDA exhibits excellent photothermal conversion efficiency, generating localized hyperthermia upon 808 nm laser irradiation (2.0 W/cm², 5 min). This hyperthermia not only directly induces photothermal damage to tumor cells but also intensifies the MnCO-H2O2 reaction, thereby enhancing CO release and producing a synergistic trimodal therapeutic effect.
What measures are taken to prevent off-target CO poisoning, and what evidence supports the safety of this approach?
The core-shell design with ZIF-8 encapsulation protects GOx during circulation and enables tumor-specific release due to acidic degradation. This spatial control ensures that CO is primarily generated within the tumor microenvironment, mitigating systemic exposure. In vivo studies showed no significant body weight loss in treated mice, indicating acceptable safety.
What are the scalability and manufacturing challenges for translating this nanoreactor to clinical production?
Key challenges include reproducible synthesis of uniform core-shell nanoparticles, precise control of MnCO loading and GOx encapsulation, and stability of the ZIF-8 shell under storage. The use of MPDA and ZIF-8 materials is amenable to scale-up, but optimization of batch consistency and sterility is required for clinical translation.
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