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 Table of Contents  
REVIEW ARTICLE
Year : 2012  |  Volume : 8  |  Issue : 3  |  Page : 348-354

Irradiation-mediated carbon nanotubes' use in cancer therapy


1 Key Laboratory of Resources Chemistry of Nonferrous Metals, Ministry of Education, Central South University, Changsha, Hunan, China
2 Key Laboratory of Natural Pharmaceutical and Chemical Biology of Yunnan Province, College of Science, Honghe University, Menzi, Yunnan, China

Date of Web Publication17-Nov-2012

Correspondence Address:
Xiao-Qing Chen
Key Laboratory of Resources Chemistry of Nonferrous Metals, Ministry of Education, Central South University, Changsha, Hunan
China
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Source of Support: Financial supports from the National Natural Science Foundation of China (No. 21201181, 21175155, 21176263), the Research Fund for the Doctoral Program of Higher Education of China (No. 20110162120070), the Planned Science and Technology Project of Hunan Province (No. 2011FJ3175), and the Fundamental Research Funds for the Central Universities (No. 201012200146) are greatly appreciated., Conflict of Interest: None


DOI: 10.4103/0973-1482.103511

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 > Abstract 

Anticancer drugs such as biological therapeutic proteins and peptides are used for treatment of a variety of tumors. However, their wider use has been hindered by their poor bioavailability and the uncontrollable sites of action in vivo. Cancer nano-therapeutics is rapidly progressing, which is being applied for solving some limitations of conventional drug delivery systems. To improve the bio-distribution of anticancer drugs, carbon nanotubes have been used as one of the most effective drug carriers. This review discusses the carbon nanotubes-mediated methods for the delivery of anticancer drugs, with emphasis on the radiation-induced drug-targeted releasing and selective photo-thermal cancer therapy.

Keywords: Cancer therapy, carbon nanotubes, hyperthermia applications, irradiation


How to cite this article:
Yu JG, Jiao FP, Chen XQ, Jiang XY, Peng ZG, Zeng DM, Huang DS. Irradiation-mediated carbon nanotubes' use in cancer therapy. J Can Res Ther 2012;8:348-54

How to cite this URL:
Yu JG, Jiao FP, Chen XQ, Jiang XY, Peng ZG, Zeng DM, Huang DS. Irradiation-mediated carbon nanotubes' use in cancer therapy. J Can Res Ther [serial online] 2012 [cited 2019 Nov 13];8:348-54. Available from: http://www.cancerjournal.net/text.asp?2012/8/3/348/103511


 > Introduction Top


Tumors are usually poorly vascularized. Biological therapeutic protein and peptide drugs are unstable in vivo. To deliver these drugs to the therapeutic target sites would be undoubtedly difficult. [1] Stimulated by an increasing knowledge about the tumor physiology and the distribution of drugs in vivo, targeted drug delivery using bioactive molecules, macromolecules, nanoparticles or other therapeutic moieties has become one of the most important branches in cancer therapies. [2],[3],[4],[5]

Cancer nano-therapeutics literally means cancer treatment performed on a nanoscale. Nano drug carrier is one of the important directions, which is being applied to solve the limitations of conventional drug delivery systems, such as nonspecific biodistribution and targeting, lack of water solubility, etc. [6] With a further surface modification procedure for abovementioned nanosystems, the obtained nano-carriers could overcome the biological barriers in the body. [3] The drug's circulation time, targeted therapy in the bloodstream, and cellular uptake abilities were significantly improved. Nowadays, cancer nano-therapeutics is rapidly progressing. [7]

Since their discovery, [8] carbon nanotubes (CNTs) have won a significant attention continuously. [9],[10],[11] CNT could be imagined as a sheet or more than two sheets of graphite ("graphene sheet") rolled into a tube [Figure 1]. CNT consists exclusively of carbon atoms arranged in a series of condensed benzene rings; thus it belongs to the family of fullerenes, the third allotropic form of carbon along with graphite and diamond. Because of the large surface area, together with the ability to encapsulate small molecules, CNTs have been used as anticancer drug carriers. To improve stacking interaction conjugation between CNTs and drugs, make CNTs more biocompatible, and improve the effects of the cancer treatment, surface modification is needed. [12] Biomedical applications for CNTs are being examined actively, which have become a gripping area for drug delivery in the last decade.
Figure 1: Scheme of graphene sheets (a) and CNTs (b)

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Because of their useful combination of size and physicochemical properties, single-walled CNTs (SWCNTs) could deliver biological molecules, including DNA, siRNA, oligonucleotides, and proteins into cancer cells through cellular membranes by endocytosis. [13],[14],[15] A greater number of multi-walled CNTs (MWCNTs) could also be observed in cellular vacuoles and nuclei with an increasing incubation duration of MWCNTs with cells. [16] Due to their remarkable physicochemical properties, functionalized, water-soluble CNTs would have several potential medical applications in the cancer treatment. [17],[18],[19],[20]

When CNTs were exposed to a radiofrequency (RF) field or other radiations, exceptional thermal destruction could be found. [21],[22],[23],[24] For example, the RF field could induce an efficient heating of aqueous suspension of CNTs, and produce a noninvasive, selective, CNTs concentration-dependent thermal destruction to cancer cell lines in vitro that contained internalized CNTs. [24] Moreover, heat from radiation made blood vessels more permeable to drugs; thus drugs could be transported more effectively into the target tumors. [1] Based on the aforementioned reasons, CNTs allow noninvasive RF field or external radiation treatments to produce targeted lethal thermal injury to the malignant cells [Figure 2].
Figure 2: Scheme of drug-loading and radiation-induced corruption of CNTs to release drugs and produce lethal injury to cancer cell lines

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The purpose of this review is to provide an overview of the CNTs-mediated drug delivery methods, with emphasis on the radiation-induced target drug-releasing systems for cancer therapy. A brief look at the types of functionalized CNTs currently in use as drug delivery for oncotherapy is also included.


 > CNTS-Mediated Oncotherapy Top


Due to their unique physicochemical properties, CNTs have become popular tools in cancer diagnosis and therapy. [25] To study the sensitivity of tumor cells to antitumor drugs, CNTs-based materials were gradually developed. [12],[26],[27] As a convenient means for cancer treatment, CNTs have attracted more and more interests in recent years [Table 1].
Table 1: Schematic representation of the CNTs-mediated cancer therapy

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CNTs as drug cargos for cancer treatment

Nanotechnology is the incorporation of physics, chemistry, and biology at the nano-scale, which is a powerful technology for life science and particularly cancer treatment. Among the vast majority of nano-materials, CNTs offer an extraordinary and challenging opportunity for cancer diagnosis and treatment. In the last less than one decade, CNTs have been further studied and developed for use in novel drug--delivery systems (e.g. anticancer drugs) and made significant advances. To transport and deliver functional biological molecules into various types of mammalian cells, the innate ability of CNTs to breach the cell membrane plays a key role. [25],[46],[47],[48],[49]

To use CNTs as drug delivery, chemical modification of CNTs to improve their solubility or dispersivity and reduce their toxic and side effects is crucial. Noncovalent interaction, formation of complexes, or covalent interaction could do such work. For example, positively charged SWCNTs (SWCNTs + ) reacted with the small interfering RNA (siRNA) to form stable complexes of siRNA: SWCNT + , which could enter into tumor cells and induce antitumor immunity. [31],[32]

Radiation-mediated CNTs in cancer therapy

A noninvasive approach with the potential to treat cancers effectively with minimal or no toxic effects to normal cells would be highly beneficial. Followed by the activation of an agent from light of a specific wavelength, a sequence of photochemical and photo-biologic processes that cause irreversible photo-damage to tumor tissues would be used.

From preclinical and clinical studies over a 40-year period worldwide, photodynamic therapy (PDT) has been established as a useful treatment approach for some cancers. However, tumor-localizing photosensitizing agents are crucially necessary for PDT. [50]

RF ablation (RFA) is clinically used to treat some malignant tumors in practice. However, it is an invasive treatment that requires the insertion of needle electrodes directly into the tumors; thus some unexpected serious drawbacks would be found, [51] e.g. the treatment-induced thermal necrosis in both malignant and normal tissues surrounding the needle electrode without specificity.

It is well known that the tissue penetration by the RF energy field is excellent. If there would be some agents that could convert RF energy into heat, they could be delivered to the malignant cells and produce noninvasive RF treatment of malignant tumors at any site in the body. As research continues, CNT is becoming one of the most efficient drug carriers with special requirements than for general usage [Table 2].
Table 2: Schematic representation of radiation induced the CNTs for selective cancer cell destruction

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Radiofrequency (RF) field

The electron--electron collisions might change the type of the hybridization of the electronic states in the CNTs under electron irradiation. [21] RF field (range, 30-6 GHz) to a single SWCNT rope was studied, [62] and discrete spectral lines originated from the geometrical antenna resonances in the radiation spectra of metallic SWCNT was predicted to exist in both near- and far-field zones. [22] Exposure to a focused external RF field would lead to significant heat released from SWCNTs, allowing them to serve directly as an anticancer therapeutic agent. Combining the RF field-generating system with SWCNTs could efficiently produce thermal cytotoxicity in malignant cells.

Histopathology sections from tumors injected with aqueous sterile Kentera functionalized SWCNTs also revealed complete thermal necrosis of the tumor tissue with a surrounding 2-5 mm zone of thermal injury. So far, no evidence of thermal injury or other abnormalities and toxic irreversible effects was observed for the remaining organs and all other organs that were assayed even at high concentrations of SWCNTs. [24]

Near-infrared (NIR) radiation

Biological systems are highly transparent to NIR light (range, 700--1,100 nm). However, CNTs, including MWCNTs and SWCNTs, could strongly absorb energy from continuous NIR radiation. By an efficient conversion of absorbed energy to heat released, CNTs could be used for localized hyperthermia applications. [63] Experimental results have shown that power levels of 1536 mW would easily achieve hyperthermic temperatures with localized values at 172.7 °C. [64] By targeting CNTs to tumor cells, followed by a noninvasive exposure to NIR light, the generated excessive local heating could cause cell death, which provided an opportunity for optical stimulation of CNTs inside cancer cells to afford selective photothermal cancer therapy. [64],[65],[66],[67],[68],[69],[70],[71],[72],[73],[74]

Oligonucleotides were successfully transported into living cells labeled with folate receptor tumor markers by folate functionalized SWCNTs, and NIR-triggered selective cancer cell destruction was achieved without harming receptor-free normal cells. [52],[54] Hyperthermia could also increase the permeability of tumor vasculature and enhance the delivery of drugs into tumors. Binding of biotinylated polar lipids coupled SWCNTs to human Burkitt's lymphomacells; only the specifically targeted cells were killed after exposure to NIR light in vitro. [75] Cancer cells targeting and killing would be achieved after a brief incubation with monoclonal antibodies (MAbs) coupled SWCNTs and the following NIR radiation. [76]

Although less well studied than SWCNTs, as a consequence of the efficient conversion of NIR irradiation into heat, MWCNTs are potentially of great use for the selective thermal ablation of malignant cells. MWCNTs are composed of concentric SWCNTs and their hydrophobic outer surface must be modified with amphiphilic materials to obtain sufficient aqueous solubility for in vivo applications. MWCNTs also exhibit specific physical properties, which render them ideal candidates in photothermal cancer ablation. With low laser powers (3 W/ cm 2 ) and very short treatment times (a single 30-second treatment), MWCNTs enabled complete ablation of tumors, and an over 3.5-month durable remission in most (about 80%) of treated mice was found. [69] Complete tumor eradication of xenografts was also achieved with a single treatment by the heat released from NIR irradiation of aqueous solutions of DNA encapsulated MWCNTs, no injury or damage to normal tissues in a mouse model of human cancer in vivo was found. [77]

Gamma-ray radiation

Due to the high penetrability of gamma-rays (γ-rays), the micro-environment surrounding drug-loaded nanotubes might be changed after irradiation, which might facilitate the release of drug from its nanotube carrier. Otherwise, the γ-radiation has no effect on the decomposition of drugs while it increases the rate of drug release.

Cancer ancillary drug tea polyphenols (TP) was conjugated to chitosan oligomers (CS, molecule weight: 4000--6000) noncovalently functionalized MWCNTs via hydrogen bonds between CS and TP molecules, the obtained MWCNT composites were used as efficient cargos for drug delivering. Due to the high penetrability of γ-rays, a controlled drug releasing from MWCNT composites was realized by pH variation and gamma radiation, which provided new opportunities for controlled drug releasing and future cancer treatment in vivo. [78]

The toxicology of CNTs

As a cellular transport and delivery system for functional biological cargos, CNTs usually get into cells via endocytosis, which appears to have obvious negative effects on either the transported cargo or the breached cell. [46] However, there were still some reports indicating that CNTs showed toxic and side effects in vivo. [79],[80] For examples, exposure to CNTs was associated with increased incidence of skin diseases, such as carbon fiber dermatitis and hyperkeratosis. [81] However, soluble CNTs alone were nontoxic in vitro, [82] which indicated that chemical modification was very useful for the design of future targeting strategies based on CNTs. [83]

To minimize side effects and improve high efficacy, delivery of chemotherapeutics using magnetic CNTs also paved a new way. [84] Coating bioactive molecules by noncovalent functionalization was another method [Table 3]. We have prepared cystamine-modified MWCNT (MWCNTs- S-S- NH3 + ) composites, whose cytotoxicity on cultured human nasopharyngeal SUNE1 cells in vitro was evaluated. Compared with pristine MWCNTs, the biocompatibility of MWCNTs-S-S-NH3 + was highly improved [Figure 3]. [88]
Figure 3: The cytotoxicity of MWCNTs-S-S-NH3+ in cultured human nasopharyngeal SUNE1 cells

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Table 3: Schematic representation of the CNT toxicology tests

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It has been discovered that CNTs could be metabolized by neutrophil myeloperoxidase. [89] After the main drawback of CNTs, such as their insolubility in aqueous media, was overcome, [19],[90],[91] the possibility of developing CNTs for biomedical applications became a reality. However, the functionalized CNTs (f-CNTs) have less cytoxicity as expected. [92]


 > Conclusion Top


Due to their distinct properties in cell membrane penetration, and loading and release of molecular cargoes, CNTs exhibit potential in biological systems. Although progress has been made to the application of CNTs as drug carriers, there are still some obstacles that block further use of the f-CNTs in cancer chemotherapy. For example, the nonspecific toxicity of anticancer agents to normal cells, and the nontargeted ability of the anticancer agents by f-CNTs are the problems now CNTs face. To discriminate the natural and the cancerous tissues, the targeting ability of the drug carriers based on f-CNTs is extremely essential. To develop the targeting ability of the f-CNTs, conjugation of CNTs with targeted moieties of antibodies, [93] folate, receptors or nanoparticles (NPs) will be urgently crucial. [94],[95]

As one allotropic form of carbon, graphene sheets also showed superior photothermal sensitivity. Due to their better dispersivity, when a suspension of polyvinylpyrrolidone-coated graphene sheets was exposed to NIR radiation (808 nm, 2 W/cm 2 ), more heat was generated than DNA or sodium dodecylbenzenesulfonate solubilized SWCNT under the same conditions. The results indicated that graphene sheets performed significantly better than CNTs in inducing photothermal death of U251 human glioma cells in vitro. [96] Lot of research work should be done to compare CNTs with graphene sheets as drug carriers in the future.

Using CNTs with irradiation (including NIR light, RF field, γ-rays, etc.) might be effective in anticancer therapy. On the long range, it will be more important to investigate the in vivo behavior of the noncovalent and covalent functionalized CNTs rather than CNTs' biodistribution and toxicity in vitro. To achieve their clinical use, such studies should be ongoing in both normal and tumor-bearing experimental animals. Due to the potential superior photothermal of graphene sheets, further studies should also be done to compare the photothermal oncotherapy of CNTs with that of graphene sheets.


 > Acknowledgments Top


The financial supports from the National Natural Science Foundation of China (No. 21201181, 21175155, 21176263), the Research Fund for the Doctoral Program of Higher Education of China (No. 20110162120070), the Planned Science and Technology Project of Hunan Province (No. 2011FJ3175), and the Fundamental Research Funds for the Central Universities (No. 201012200146) are greatly appreciated.

 
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    Figures

  [Figure 1], [Figure 2], [Figure 3]
 
 
    Tables

  [Table 1], [Table 2], [Table 3]


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