ReviewAdvances in smart mesoporous carbon nanoplatforms for photothermal–enhanced synergistic cancer therapy
Introduction
Photothermal therapy (PTT), as a tumor ablation strategy, has received extensive attention in recent years. Compared with traditional treatments, PTT has shown the advantages of high efficiency, low recurrence rate, and short treatment process for solid tumors (lung cancer [1], hepatoma [2], breast cancer [3], prostatic carcinoma [4], and rectal cancer [5]) in clinical practice. Most importantly, PTT is non-invasive or minimally invasive to alleviate the patient’s suffering. The realization of efficient thermal ablation mainly relies on the photothermal conversion effect of photothermal agents. When photothermal agents absorb light, the electrons transition from the ground state to the excited state. With the energy relaxes by nonradiative decay, the surrounding environment is overheated due to the increase of kinetic energy. Apoptosis and necrosis caused by photothermal effect can effectively destroy tumor tissue [6], [7] (Scheme. 2A-B). However, two obstacles faced by PTT greatly hinder the pace of further clinical applications. Firstly, due to the insufficient photothermal conversion efficiency of the existing photothermal agents, the laser power far exceeding the clinical safety requirements is needed to achieve sufficient local ablation. At the same time, the tissues and organs adjacent to the tumors are heated inevitably, causing tissue damage and edema. Secondly, the treatment effect is limited by laser irradiation range and penetration depth. The tumors located in deep tissue or distal end are not adequately treated, which may cause neoplasm residual and thermal tolerance [8], [9]. Therefore, it is urgent and necessary to improve the photothermal conversion efficiency of photothermal agents, enrich the single tumor treatment means of PTT, and impair the thermal tolerance of tumor tissues.
In recent years, mesoporous materials (mesoporous carbon, mesoporous silica, mesoporous polydopamine, etc.) have been widely developed and applied in tumor treatments [10], [11]. Their adjustable pore size and large specific surface area provide convenience for specific drug delivery and surface biofunctionalization. However, most of them have insufficient photothermal conversion efficiency, and thus hard to meet the demands in PTT. MCNs have shown remarkable photothermal conversion efficiency and broad-spectrum absorption in the UV–Vis-NIR region [12]. The progress in long-wavelength PTT makes it possible to achieve effective heating in deep tissues with bearable irradiation power [13]. Additionally, the solid structure guarantees the photothermal stability of MCNs, while it also affects the degradation and elimination of MCNs in vivo. Recently, biodegradable and cleanable composite MCNs have been constructed and obtain instructive results. As important means to improve biosafety, the relevant contents are summarized in Part 4.2. Moreover, compared with other mesoporous materials, MCNs exhibit higher enzyme-like properties. With the light irradiation, the surface of MCNs was activated, and the process of enzyme-like reactions (peroxidases/oxidases, etc.) could be accelerated, which not only directly killed tumors by the generated high-level ROS, but also interfered with redox homeostasis to keep tumors sensitive to anticancer drugs and ROS damage [12], [14] (Scheme 2A).
Based on the remarkable features of MCNs and MCNs-derivates, considerable efforts have been made to explore MCNs-based nanoparticles in combined cancer therapies including chemotherapy-PTT, photodynamic therapy (PDT)-PTT, gene delivery-PTT, carbon nanoenzyme mediated catalytic therapy-PTT, and others (Scheme 1). Local heating by PTT can change the physicochemical properties at the tumor microenvironment (TME) (Scheme 2B-C). With the accelerated molecule thermal movement, the active ingredients can quickly escape from MCNs and be internalized into tumor cells. Moreover, benefit from the light irradiation and thermal effect, chemical/enzymatic reaction could be simultaneously accelerated, especially in dynamic and catalytic therapies [15], [16]. After necrosis and apoptosis, tumor associated antigens were presented to T-cells to activate the local antitumor responses. And the restart of systemic antitumor immune response could specifically identify and remove metastasis malignant tumors [17], [18]. Synergistic treatments can also compensate for the limitations of relying on thermal ablation as the single treatment means of PTT. After most of the tumors are destroyed by PTT, the remaining tumor cells can still be continuously suppressed by the synergistic therapies. In brief, the mature MCNs-based drug delivery systems and local thermal effect can improve the accuracy and therapeutic performance of systemic therapy through multi-ways, producing ‘a whole greater than the sum of the parts’.
MCNs based nanocasting, drug delivery, and therapies were reviewed before [19], [20]. However, important progresses including low-power and high-efficiency PTT, carbon nanoenzymes, degradable composite carbon carriers have been developed recently. Several key considerations should be taken in designing MCNs-based platforms with enhanced PTT and combined therapies. From this point of view, we summarize the recent progress in this field, and divide them into four parts: (1) Characteristics of MCNs used in PTT; (2) PTT combined treatments; (3) Multi-functional MCNs in PTT; (4) Multiple strategies to improve the photothermal effect. For more convenient reference, Table 1 summarizes the PTT combined treatment based on MCNs. Finally, some feasible technologies are prospected to improve the PTT efficiency.
Section snippets
Characteristics of MCNs used in PTT
MCNs are a kind of carbon materials with mesopores of 2–50 nm and particle sizes of tens to hundreds of nanometers. Based on the progress of the nanocasting technology and material science, the composition and nanostructure of MCNs can be accurately adjusted and optimized to achieve specific requirements in terms of improved photothermal conversion efficiency, active ingredient delivery, nanoenzyme catalysis, and bio-imaging. The structural adjustment and physicochemical property manipulation
Chemotherapy with PTT
Chemotherapy is the most widely used treatment for malignant tumors. Classic chemicals have been used in clinic for cancer treatment, such as Dox, paclitaxel, mitoxantrone, and vincristine. Nonetheless, the poor therapeutic effect caused by multidrug resistance (MDR), strong side effects, and low cell uptake rate greatly restricts the clinical application [47]. Hence, the combination and application of PTT and chemotherapy based on MCNs have received extensive attention to enhance the
Multi-functional MCNs in PTT
The combination of PTT and other treatments has shown promising therapeutic effects. Moreover, the excellent biocompatibility, high tumor specificity, and long circulation time of MCNs are also required. In order to acquire better in-vivo performance, various polymers and biofilms have been wrapped on MCNs to prolong the circulation time and increase the drug accumulation at tumor sites. Moreover, the degradable structure of MCNs is of great significance in reducing the potential toxicity. In
Multiple strategies to improve the photothermal effect
Due to the complex tumor environment, the high-risk tumors, deep tissue tumors, and different skin light transmission efficiency must be considered. The absorption of NIR light by skin and tissue fluid greatly hinders the tumor ablation of PTT behind deep tissues. And the high photothermal ablation effect by exerting too powerful laser irradiation in clinics tends to cause unwanted tissue inflammation and edema, making it hard to be applied in the complex tumor environment. Hence, the low power
Conclusion and outlook
In this review, we summarize the breakthrough of functionalized MCNs in PTT combined therapies and enhanced PTT in cancer treatment. Chemotherapy, PDT, tumor catalytic therapy, gene delivery, and immune therapy can be successfully integrated with PTT based on MCNs to promote the therapeutic effect. We also discuss the methods to improve the PTT effect by increasing the efficiency of photothermal conversion and inhibiting the thermal tolerance of tumor cells at the low laser power. However,
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
Grants from National Natural Science Foundation of China (No. 81603058), China Postdoctoral Science Foundation (No. 2021M690483) and Youth Project of Liaoning Provincial Education Department (No. LJKQZ2021030) are greatly acknowledged.
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