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Zhuo, X.; Liu, Z.; Aishajiang, R.; Wang, T.; Yu, D. Copper-Based Nanomaterials in Tumor-Targeted Photothermal Therapy/Photodynamic Therapy. Encyclopedia. Available online: https://encyclopedia.pub/entry/49400 (accessed on 04 August 2024).
Zhuo X, Liu Z, Aishajiang R, Wang T, Yu D. Copper-Based Nanomaterials in Tumor-Targeted Photothermal Therapy/Photodynamic Therapy. Encyclopedia. Available at: https://encyclopedia.pub/entry/49400. Accessed August 04, 2024.
Zhuo, Xiqian, Zhongshan Liu, Reyida Aishajiang, Tiejun Wang, Duo Yu. "Copper-Based Nanomaterials in Tumor-Targeted Photothermal Therapy/Photodynamic Therapy" Encyclopedia, https://encyclopedia.pub/entry/49400 (accessed August 04, 2024).
Zhuo, X., Liu, Z., Aishajiang, R., Wang, T., & Yu, D. (2023, September 20). Copper-Based Nanomaterials in Tumor-Targeted Photothermal Therapy/Photodynamic Therapy. In Encyclopedia. https://encyclopedia.pub/entry/49400
Zhuo, Xiqian, et al. "Copper-Based Nanomaterials in Tumor-Targeted Photothermal Therapy/Photodynamic Therapy." Encyclopedia. Web. 20 September, 2023.
Copper-Based Nanomaterials in Tumor-Targeted Photothermal Therapy/Photodynamic Therapy
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This entry is adapted from the peer-reviewed paper 10.3390/pharmaceutics15092293

Nanotechnology, an emerging and promising therapeutic tool, may improve the effectiveness of phototherapy (PT) in antitumor therapy because of the development of nanomaterials (NMs) with light-absorbing properties. The tumor-targeted PTs, such as photothermal therapy (PTT) and photodynamic therapy (PDT), transform light energy into heat and produce reactive oxygen species (ROS) that accumulate at the tumor site. The increase in ROS levels induces oxidative stress (OS) during carcinogenesis and disease development. Because of the localized surface plasmon resonance (LSPR) feature of copper (Cu), a vital trace element in the human body, Cu-based NMs can exhibit good near-infrared (NIR) absorption and excellent photothermal properties. Compared with other therapeutic modalities, PTT/PDT can precisely target tumor location to kill tumor cells. Moreover, multiple treatment modalities can be combined with PTT/PDT to treat a tumor using Cu-based NMs.

nanomaterials (NMs) photodynamic therapy (PDT) photothermal therapy (PTT) copper (Cu) Cu-based NMs reactive oxygen species (ROS)

1. Introduction

Cancer is a complicated disease characterized by various genetic flaws. The increased incidence of malignant tumors and their predisposition for metastasis are major threats to human health, which lead to higher mortality rates [1][2]. The traditional treatment modalities for tumors, including surgery, radiotherapy, and chemotherapy, can engender various adverse effects, including radioactive damage, toxic side effects of chemotherapeutic drugs, or chemotherapy-induced multidrug resistance, which considerably limits the therapeutic effectiveness of these modalities [3][4][5][6]. The emerging treatment modalities for tumors, such as thermotherapy, immunotherapy, and gene therapy, have provided greater hope for patients [7][8]. However, their prolonged use has been reported to severely impair the immune system, even leading to organ malfunction [9][10]. Discovering a tumor treatment modality with low toxicity to healthy tissues and improved precision presents an imperative and formidable challenge.
Recently, phototherapies (PTs), such as photothermal therapy (PTT) and photodynamic therapy (PDT), are being widely used as effective antitumor therapeutic strategies [10]. In PTT and PDT, photothermal agents (PAs) and photosensitizers (PSs) work as exogenous energy converters or absorbers in the organ affected by the tumor [11]. This has enabled the conversion of visible or laser light energy into thermal energy to induce apoptosis or necrosis of tumor cells at high temperatures, with or without concurrent reactive oxygen species (ROS) generation [12][13][14][15]. PT has specific advantages over other heat-based tumor treatment techniques, including thermotherapy and microwave therapy. Its high precision enables PT to target tumors with the least possible damage to adjacent tissues and organs [16]. Additionally, PT is an excellent method for managing tumors because of its controllability and low toxicity profile. Compared with either PTT or PDT acting alone, the synergistic approach combining PTT and PDT can hasten tumor cell death and increase the therapeutic efficacy [17]. The key components of PTT and PDT are their PAs and PSs, majorly including nanomaterials (NMs) at present, which differ from conventional macromolecules. NMs exhibit excellent characteristics, including high Brunauer–Emmett–Teller (BET), electrical conductivity, spectrum shifts after light absorption, fluorescence properties, and potential for degradation [18]. Therefore, they have been steadily incorporated into cancer research, advancing the field of tumor investigations [19][20][21]. Regarding medical therapeutics, materials of nanoscale dimensions (1–100 nm diameter) have been employed [22]. These NMs have versatile applications in drug transportation, enabling controlled release mechanisms, increasing permeability, traversing biological barriers, and improving overall biocompatibility [23][24][25]. Owing to their unique size and traits, NMs can remarkably change various therapeutic processes and considerably improve treatment efficacy [22]. Metal ion-based NMs, including those of gold (Au), silver (Ag), copper (Cu), and other NMs, exhibit distinctive optical properties, notably the phenomenon of localized surface plasmon resonance (LSPR) [26][27]. LSPR notably strengthens the electric field in the immediate proximity of metal ion-based NMs, based on their capacity to strongly absorb photon energy. Owing to an extensive range of light-induced effects and intermolecular interactions produced, they are used in tumor-targeted PTT/PDT. However, the high cost of Au- or Ag-based NMs and the non-degradability of some PAs/PSs in vivo limits their application in clinical therapy [28]. Cu, a readily available metal, has unique bioactivities that can be used for eliminating tumor cells by regulating various types of cell death [29]. Furthermore, Cu can undergo a Fenton-like reaction to catalyze high ROS content from excess intracellular hydrogen peroxide (H2O2), which can induce bacterial and tumor cell death [30]. The functions and therapeutic involvement of Cu are shown in Figure 1. Al Kayal et al. created electrospun polyurethane membranes covered with Cu nanoparticles (NPs) and ran an antimicrobial test on Escherichia coli and discovered that over half of the bacteria were destroyed, showing its potent bactericidal effects. Additionally, SARS-CoVer-2 was resistant to the antiviral activity by nearly 90% [31]. Cu-based NMs have been widely employed in PTT and PDT in recent years because of their advantageous properties, including strong near-infrared (NIR) absorption and photothermal capabilities [32][33], high BET [34][35], and use in tumor imaging. [36] Furthermore, Cu-based NMs offer considerable advantages in tumor therapy owing to their simple synthesis procedures and relatively high production yields under mild low reaction conditions [37]. Zhao et al. synthesized CCeT NMs (Ce: Chlorin e6, T: TPP-COOH) with Cu2−x Sulfur (S) as the core, which exhibited a photothermal conversion efficiency (PCE) of 10.6% under laser irradiation. At very low concentrations, the temperature increased by 5.3 °C in 10 min and continued to rise with increasing concentration [38], demonstrating the therapeutic advantages of PTT/PDT and that it can be substantially increased using Cu-based NMs.
Pharmaceutics 15 02293 g001
Figure 1. Functions of Cu and therapeutic involvement. CDT: chemodynamic therapy.

2. Application of Copper Oxides in PTT and PDT

Over the past few decades, various Cu-based NMs have emerged as alternative means to amplify the effects of PTT/PDT [39]. Studies indicate that CuO-NPs can hinder pancreatic tumor growth, notably by targeting tumor stem cells [40]. These NPs can induce mitochondrial dysfunction, attributed to the ability of Cu2+ to generate ROS through the Fenton-like reaction and to enhance PCE through electronic transitions between C-2p and Cu-3d [41]. Ma et al. developed CuO@CNSs-DOX (DOX: Doxorubicin) nanoplatforms, elevating the PCE from 6.7% to 10.14%. These platforms achieve anti-tumor effects through the drug action of DOX and the generation of ·OH radicals by Cu2+ [42][43]. The same group synthesized multifunctional MoS2-CuO@BSA/R837 (MCBR, BSA: Bovine Serum Albumin, R837: Imiquimod, a toll-like receptor 7 (TLR7) agonist) nanoflowers. Under 808 nm laser exposure, these nanoflowers exhibited a PCE of 24.6% and a marked increase in ·OH production. Additionally, the inclusion of R837 increased the expression of calreticulin (CRT), triggering immunogenic cell death (ICD), effectively neutralizing primary tumors, and inhibiting metastatic tumors [44]. Taking advantage of Cu2O’s high refractive index above 600 nm, Yu et al. produced core/shell structured Cu@Cu2O@polymer NPs. Under a 660 nm laser exposure and an equivalent Cu concentration, compared to Cu@polymer NPs, the temperature increase for Cu@Cu2O@polymer NPs was about 4.2 °C. This resulted in a temperature rise of at least 23 °C in adjacent tissues, translating to a 7-fold surge in the IC50, relative to prior research [45][46]. These findings underscore that Cu@Cu2O@polymer NPs possess sufficient phototoxicity to exterminate tumor cells. Furthermore, the increased concentration of endogenous H2O2 produced by the LPS endotoxin accelerated the release of Cu ions and ROS, facilitating the eradication of cancer cells [33][45].

3. Application of CuxSy in PTT and PDT

Semiconductor NMs CuxSy have gained attraction in catalysis and sensing sectors due to their optical and electrical properties. Owing to their affordability, minimal cytotoxicity, and high photostability, CuxSy NPs hold promise as Pas [47][48]. Tian et al. synthesized hydrophilic, plate-like Cu9S5 nanocrystals. With a 980 nm laser, the PCE of Cu9S5 reached 25.7%. Interestingly, under identical conditions, this PCE surpassed that of the synthesized Au nanocrystals, which was approximately 23.7%. These nanocrystals eradicated tumor cells in vivo swiftly (in less than 10 min), establishing Cu9S5 nanocrystals as efficient PAs. When hormonal mice underwent subsequent radiation following injection, notable necrosis and shrinkage of tumor cells in the mass region were observed [49][50]. Addressing the challenge that non-targeted ultrasmall metallic NPs face in securing prolonged half-life and satisfactory tumor-site aggregation as PTT agents, Li et al. synthesized CuS NPs and modified them with cetuximab (Ab) to yield CuS-Ab NPs. On exposure to a 1064 nm laser for 10 min, temperatures increase rapidly from 23 °C to 58 °C and are consistently held at 58 °C. Additionally, Ab modification rendered CuS-Ab NPs superior in tumor-targeting and anti-angiogenic capacities, ensuring effective tumor-site accumulation without concomitant damage to other tissues and organs [51]. Cationic polymers, such as PEI, can achieve drug delivery by intensifying the electrostatic adsorption of cations on the cell membrane [52]. Studies have shown that NMs modified with PEI and PSs can be instrumental in the PDT of bladder tumors [53]. Based on this, Mu et al. prepared HRP@CPC@HA NPs (HRP: horseradish peroxidase, CPC: CuS-PEI-Ce6, HA: hyaluronic acid). These particles incorporated HRP within a hollow CuS nanocage [54]. Subjected to 808 nm laser radiation, their PCE was around 34.91%. Concurrently, the surface-bound Ce6 was activated, leading to a large amount of 1O2 generation, the levels of which increased alongside temperature [53]. Additionally, HRP catalyzed the breakdown of intracellular H2O2 to oxygen, addressing the oxygen deficit in tumor cells and facilitating simultaneous multimodal tumor eradication in severely hypoxic TME [55]. Due to the increased concentration of endogenous H2S in tumor cells, Wu et al. synthesize monolocking NPs (MLNPs) [56]. When illuminated with 808 nm radiation, these MLNPs combined with H2S and produced ultra-small CuS nanodots. This interaction elevated tumor temperatures, triggering apoptosis in tumor cells. Mel is released from the NPs which causes the COX-2 enzyme to become inactive, amplifying the PTT action and inhibiting inflammation induced by PTT damage. Notably, these NPs were excreted renally [57]. The development of nanomedicine has witnessed diverse manifestations of CuxSy. Hollow structured CuxSy has particularly piqued interest in oncologic therapy, attributed to its drug-loading ability and high PCE and PAI capability [58][59], yet many extant synthesis methods for CuS-based NMs are intricate, time-consuming, and require special reaction equipment. Consequently, there is an evident need for facile, cost-effective methodologies that employ gentle reaction conditions to fabricate CuxSy NMs.

4. Application of Copper Selenides and Copper Telluride in PTT and PDT

Copper selenides, notably Cu2-XSe NMs, present promising applications in imaging and PTT for cancer treatment, attributed to their biocompatibility, excellent NIR light absorption, and increased PCE [60][61].
Du et al. synthesized CuSe/NC-DOX-DNA NPs (NC: nitrogen-doped carbon) via an environmentally friendly and simple method. Under 808 nm laser exposure, these NPs displayed a PCE of 32.9%, surpassing that of Au nanorods which had a PCE of 22.0% [62]. Moreover, the synergistic action of photocatalysis combined with the Fenton-like reaction of CuSe/NC markedly augmented ROS generation [63]. Concurrently, the encapsulated DOX functioned as a chemotherapeutic agent, realizing a threefold enhanced PTT/CDT/PCT tumor treatment method [64]. It is noteworthy that Cu2-XSe has been identified as an effective PA [61]. In another study, He et al. developed ICG@Cu2-X Se-ZIF-8 (ICG: Indocyanine Green, ZIF-8: a metal-organic framework). After 808 nm laser exposure, this compound exhibited a PCE of 15.5%. In the TME, ZIF-8 breaks down and releases Cu1+ and Cu2+, which leads to a Fenton-like reaction, controls the amount of GSH, and produces ROS [65]. Furthermore, selenium has the ability to regulate selenoprotein, allowing it to prevent the production of osteoclasts and tumor cells, resulting in the synergistic PTT/CDT prevention of malignant bone metastasis [66][67]. Moreover, CuSe is an ideal PS and has been demonstrated to biodegrade. Selenium is released during this process and has been shown to lower the risk of liver cancer, lung cancer, and prostate cancer [68][69]. Pun et al. fabricated COF-CuSe NMs (COF: covalent-organic framework); under 808 nm laser irradiation, the PCE was 26.34% after injection in mice. A large quantity of 1O2 was generated under both 650 nm and 808 nm illumination. Consequently, almost all of the HeLa cells died under laser irradiation. The PTT and PDT anti-tumor treatment strategies showed a synergistic potential [70]. At present, CuSe NMs have been poorly investigated for PTT/PDT and the development of multifunctional CuSe NM is still required to improve anti-tumor therapy for PTT/PDT.
Similar to CuSe, CuTe is considered a novel PAs candidate. Li et al. created CuTe NPs with a plasma peak at 900 nm. Under 830 nm laser irradiation, the mortality of 3T3 embryonic fibroblasts increased [71]. However, it was discovered that some cells were already dead before laser irradiation. It has been demonstrated that CuTe NPs are cytotoxic and PAs. Under 1064 nm laser irradiation, bio Cu2−XTe nanosheets synthesized by Li et al. had a PCE of 48.6%. When Cu1+ and Te are released, the nanosheets can produce ·OH and inhibit the GPx and TrxR enzymes for CDT, significantly inhibiting the proliferation of MCF-7 cells [72]. Shen et al. synthesized CM CTNPs@OVA NMs (CM: melanoma B16-OVA membrane, OVA: ovalbumin) with solid CuTe NPs. Under laser irradiation, there was a significant increase in temperature and production of ROS. In addition, B16-OVA cells produced an abundance of ATP and HMGB-1, which effectively stimulated the immune system and enhanced the anti-tumor treatment [73]. CuTe NPs anti-tumor therapy research in PTT/PDT has received less attention and requires further development and investigation.

5. Application of Cu-Based Nanocomposites in PTT and PDT

Most treatments consisting of a single therapy have a negligible impact on tumor treatment. However, a synergistic combination of multiple therapeutic modalities can improve the efficacy of treating malignant tumors [74]. The same applies to NMs. In cancer treatment, simple Cu-based NMs such as CuS may still be lacking. Therefore, it is necessary to load various materials, drugs, or fluorescents onto Cu-based NMs to create a composite material capable of fluorescence, tumor targeting, and therapy in a single NM.
As a result of the discovery of cuproptosis, Cu-based NMs may induce tumor cell death by modulating the concentration of Cu in tumor cells, offering a novel anti-tumor therapeutic modality [75]. Pan et al. produced GOx@[Cu(tz)] NPs. Under 808 nm laser irradiation, NPs entering tumor cells produced H2O2 and ·OH. In the meantime, under the influence of GSH, GOx hydrolyzed and consumed glucose, generating a large amount of H2O2 and OH that produced a ROS-adding effect [76]. Due to the depletion of glucose and GSH, the NPs bind to lipoylated mitochondrial enzymes, resulting in the aggregation of lipoylated DLAT, which induces cuproptosis and effectively inhibits tumor growth (92.4% inhibition rate) [77]. The synthesis and development of NMs that combine multiple antitumor therapeutic modalities is urgently needed. Xia et al. synthesized metal-organic skeleton nanosheets Cu-TCPP(Al)-Pt-FA (TCPP: Tetrakis (4-carboxyphenyl) porphyrin, FA: folic acid) with surface modification by platinum NPs (Pt NPs) and FA in order to solve the problem of poor oxygenation in tumor tissues. Compared to 25.2% tumor cell survival in vitro without laser irradiation, laser irradiation at 638 nm reduced tumor cell survival to 20.7%. Since Cu2+ can react with GSH via a Fenton-like reaction, it depletes intracellular GSH and increases ROS levels [78]. In the meantime, Pt NPs have catalysis activity comparable to a catalase-like reaction that can continuously convert intracellular H2O2 to O2 in order to alleviate hypoxic TME and enhance the therapeutic effect of PDT [79]. ROS concentration was increased synergistically by these two modalities, which stimulated antigen-presenting cells to activate systemic anti-tumor immune responses and increased the infiltration of cytotoxic T lymphocytes (CTLs) at the tumor site for synergistic immune anti-tumor therapy [80][81]. Xu et al. constructed d-Cu-LDH/ICG NPs (LDH: lactatedehydrogenase) in order to alleviate the tumor hypoxia problem and avoid the poor therapeutic effect caused by tumor hypoxia during PDT treatment [82]. Under 808 nm laser irradiation, the PCE was 88.7% and the production of 1O2 increased as the temperature rose. In the meantime, the rising temperature led to the dissolution of the NMs and the reduction in Cu2+ to Cu1+ by GSH, both of which can consume excessive H2O2 and generate OH in tumor cells via a Fenton-like reaction, resulting in CDT and modulation of the TME [83]. In the meantime, it was demonstrated that hormonal mice had significantly less tumor growth. Hematoxylin and eosin (H&E) staining of major organs revealed no obvious inflammation or damage and demonstrated that the effective anti-tumor agent exhibited no significant systemic toxicity. Yang et al. created NSCuCy NPs containing Cu1+ as the core [84]. Cu1+ undergoes a Fenton-like reaction with O2− to produce ·OH [85]. The fluorescence intensity of the HPF was used to detect the ROS concentration; it was discovered that the fluorescence intensity of the HPF increased rapidly in the presence of NSCuCy NPs under 660 nm irradiation. At pH 5.5, the emission intensity of HPF increased nearly 350-fold after 10 min of irradiation, demonstrating a higher ·OH production efficiency than that at pH 7.4 (180-fold) and targeting accumulation in tumor tissues to achieve complete tumor ablation [86]. Kang et al. developed Au@MSN-Cu/PEG/DSF NPs (Au@MSN: mesoporous silica-coated Au nanorods, DSF: disulfiram). The PCE under 808 nm laser irradiation is 56.32%. With an increase in temperature, the Cu-doped SiO2 framework begins to biodegrade. During the conversion of Cu2+ to Cu1+, releasing DSF can chelate with Cu2+ to produce highly cytotoxic bis (diethyldithiocarbamate) Cu (CuET) [87][88]. Cu1+ binds additionally to mitochondrial protein aggregates during the TCA cycle, inducing cuproptosis in tumor cells [75]. Photothermal therapy′s synergistic effect resulted in an 80.1% tumor inhibition rate, effectively killing tumor cells and inhibiting tumor growth [75][89].
Overall, multifunctional nanocomposite materials that integrate imaging, diagnosis, and therapy have shown significant improvements in tumor treatment compared to single-material therapy. These NMs combine PTT/PDT with drug delivery systems, immunotherapy, and chemotherapy, reducing normal medication dosage and adverse reactions while achieving effective anti-tumor treatment in the short term. However, long-term experimental data on NMs are still needed to verify their long-term toxicity, biosafety, and therapeutic effects to ensure they meet desired goals. Further investigations are required for a comprehensive understanding.

6. Application of Cu-MOF in PTT and PDT

Metal-organic frameworks (MOFs) are a novel type of NMs that combine metal ions or clusters with multisite organic ligands. These MOFs have shown great potential in anti-tumor therapy due to their inherent biodegradability, high porosity, structural diversity, and high drug-loading capacity [90][91][92][93].
For instance, Wu et al. synthesized ultrathin Cu-TCPP MOF nanosheets containing both Cu1+ and Cu2+ which enabled imaging, photothermal conversion, and anti-tumor therapy [36][94]. Under 808 nm laser irradiation, the nanosheets showed a PCE of 36.8% and a significant amount of 1O2 was generated in tumor cells. Cu2+ has unpaired 3d electrons and paramagnetic also allowed the nanosheets to be used for T1-weighted MRI. This multifunctional NMOF design holds promise for tumor PTT [95]. Tang et al. designed two metal-organic materials, MOF-1 and MOF-2, based on this premise. MOF-1 is an aluminum (AL)-MOF that does not contain Cu2+, whereas MOF-2 is an AL-Cu mixed-metal MOF[CuL-[AlOH]2n with Cu2+ at its core. Comparing the two MOFs under 650 nm laser irradiation revealed that MOF-2 has a porous physical structure, which makes the Cu2++ in MOF-2 significantly adsorb intracellular GSH and results in a decrease in GSH and an increase in ROS concentration, which enhances the efficacy of PDT [96]. Similar to the chemotherapeutic drug camptothecin (CPT), MOF-2 was able to eradicate tumor cells in an in vivo experiment. The results of a simultaneous examination of major organ tissue slices revealed little toxicity in vivo [97][98]. This MOF structure, which simultaneously decreases intracellular GSH levels and increases intracellular ROS levels, may provide not only a new strategy for intracellular GSH adsorption but also a new method for enhancing PDT.
Due to the higher cavity structure of emerging Cu-NMOFs, they can be loaded with more PSs or PAs to improve PCE and increase the diffusion range of ROS. Their porous structure also allows for chemotherapeutic drug delivery and synergistic effects with other therapies to enhance anti-tumor efficacy. However, the synthesis process of MOF PSs or PAs can be complex and might exhibit batch-to-batch variations, hindering large-scale NMOF preparation. Moreover, the presence of various metal ions necessitates further investigation into the long-term safety, biocompatibility, pharmacokinetics, and immunoreactivity of NMOFs in mammals through systematic animal studies.

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Subjects: Oncology
Contributors MDPI registered users' name will be linked to their SciProfiles pages. To register with us, please refer to https://encyclopedia.pub/register :
Xiqian Zhuo
,
Zhongshan Liu
,
Reyida Aishajiang
,
Tiejun Wang
,
Duo Yu
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Update Date: 20 Sep 2023
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