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19 May 2023

Carbon Nanomaterials (CNMs) in Cancer Therapy: A Database of CNM-Based Nanocarrier Systems

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School of Chemical Sciences, Dublin City University, Glasnevin, D09 NA55 Dublin, Ireland
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Pharmaceutics2023, 15(5), 1545;https://doi.org/10.3390/pharmaceutics15051545
This article belongs to the Special Issue Carbon-Based Nanomaterials as Multifunctional Nanoplatforms for Cancer Diagnosis and Treatment
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Abstract

Carbon nanomaterials (CNMs) are an incredibly versatile class of materials that can be used as scaffolds to construct anticancer nanocarrier systems. The ease of chemical functionalisation, biocompatibility, and intrinsic therapeutic capabilities of many of these nanoparticles can be leveraged to design effective anticancer systems. This article is the first comprehensive review of CNM-based nanocarrier systems that incorporate approved chemotherapy drugs, and many different types of CNMs and chemotherapy agents are discussed. Almost 200 examples of these nanocarrier systems have been analysed and compiled into a database. The entries are organised by anticancer drug type, and the composition, drug loading/release metrics, and experimental results from these systems have been compiled. Our analysis reveals graphene, and particularly graphene oxide (GO), as the most frequently employed CNM, with carbon nanotubes and carbon dots following in popularity. Moreover, the database encompasses various chemotherapeutic agents, with antimicrotubule agents being the most common payload due to their compatibility with CNM surfaces. The benefits of the identified systems are discussed, and the factors affecting their efficacy are detailed.

1. Introduction

While cancer remains one of the world’s leading causes of death, advances in diagnostics and treatment have seen an overall improvement in detection and mortality rates. However, the current treatment approaches are either highly invasive, in the case of surgical operations, or can cause unwanted toxic side effects, as commonly experienced with chemotherapeutic agents and radiotherapy [1,2]. In particular, the effectiveness of chemotherapeutic agents is often limited by their poor aqueous solubility and nonselective nature, resulting in poor bioavailability and the indiscriminate death of both healthy and cancer cells [3]. To overcome these issues, there has been much research into the use of nanocarriers for the targeted and controlled release of anticancer drugs [4], where carbon nanomaterials (CNMs) have emerged in recent years as very promising candidates for this purpose. CNMs are a distinct class of materials that show altered characteristics to those of bulk carbon materials, such as diamond or graphite. They are classified as 0D, 1D, or 2D, according to the number of dimensions they possess which exist on the nanoscale (<100 nm) [5]. The allotropic nature of carbon means that a variety of these materials exists, some examples of which include graphene [1], carbon nanotubes (CNTs) [6], carbon nano-onions (CNOs) [7], nanodiamonds (NDs) [8], and carbon nanohorns [9]. CNMs have garnered widespread attention for their biomedical applications, such as drug delivery and diagnostics, because of their unique and highly desirable physicochemical and mechanical properties, such as size, biocompatibility, high tensile strength, and ease of chemical functionalisation.
By carefully selecting the production method, the particle sizes of CNMs can be precisely controlled, allowing for the creation of particles comparable in size to biomolecules (<100 nm) [10]. This size control enables CNM-based particles to take advantage of the leaky vasculature surrounding tumour cells through the enhanced permeation and retention (EPR) effect, facilitating the passive targeting of tumour cells [11]. However, passive targeting is generally limited, as not all tumours exhibit the EPR effect, and the random nature of the process makes it difficult to control and can lead to drug resistance [4]. Instead, it is preferable to actively target tumour tissues using targeting moieties that improve drug uptake through mechanisms such as receptor-mediated endocytosis [12]. The advanced surface chemistries provided by CNMs enable the attachment of various targeting ligands (such as folic acid (FA) [13]), imaging agents (such as BODIPY [14]), and anticancer drug molecules (such as cisplatin [15]), facilitating the creation of multifunctional nanocarriers. These nanocarriers can efficiently target, image, and deliver therapeutic agents directly to cancer cells, capitalizing on the unique properties of CNMs. Therefore, CNMs can be used as scaffolds to create theragnostic systems, combining imaging, detection, and treatment modalities in one tiny package to effectively diagnose and treat various illnesses [16].
As mentioned previously, there are many options for functionalising CNMs, with oxidation being one of the most straightforward approaches. This method introduces hydroxyl, carbonyl, and carboxyl groups to the surface of the nanomaterial, allowing for further functionalisation, and significantly increasing the material’s aqueous solubility in the process. Highly soluble CNMs can be utilised to increase the solubility of hydrophobic drugs, an approach taken by Cakmak and Eroglu, who employed graphene oxide (GO) to solubilise tamoxifen [16]. Facilitating the delivery of poorly soluble and/or poorly permeable drugs is a major benefit of the nanocarrier approach, as it does not require extensive modification of the drug molecule itself.
A range of other examples of covalent CNM modification exists, such as amidation, fluorination, and alkylation [17]. Covalent functionalisation methods have their drawbacks, mainly because this type of modification can damage the nanomaterial’s surface [7]. This surface damage can lead to a loss in the CNM’s unique electronic and physical properties, which may be essential to the nanocarrier’s effectiveness.
To circumnavigate issues associated with covalent modification, noncovalent functionalisation methods have been employed to attach components to the CNM. In this case, interactions, such as π–π stacking and hydrophobic interactions, are used to bind a molecule to the CNM surface [18].
A crucial aspect to consider when attaching drug molecules to a CNM is the drug release mechanism, which includes factors such as the release trigger and drug release profile, ensuring controlled and targeted delivery. Noncovalent attachment is particularly suited to reversible drug binding and can be utilised to design pH-responsive [19], redox-responsive [20], and NIR-responsive [21] drug delivery systems. Due to the acidity of tumour microenvironments, pH-sensitive systems are particularly relevant to cancer therapy [22]. This approach can be used to release the bound drug exclusively in the target tumour tissues, reducing unwanted side effects. Covalent strategies, such as drug attachment via hydrolysable ester bonds, have also been used for pH-responsive drug delivery, and often have the benefit of reduced drug leakage at neutral pH [23].
Herein, we present a database of nearly 200 CNM-based nanocarriers that have been utilised as drug delivery systems for clinically approved anticancer drugs. We curated this database through a comprehensive literature analysis, the details of which are provided in the following section. The entries are organised by drug type, and the composition, experimental results, drug loading and release metrics, and biological study models used are detailed. We also provide a critical analysis and discussion of the database and explore possible future research directions in the utilisation of CNM-based nanocarriers for anticancer drug delivery.

2. Methods and Metrics Used to Construct the Database

2.1. Preparation of the Database

This database is an in-depth overview of carbon nanomaterial (CNM)-based anticancer drug delivery systems. To construct the database, CAS SciFindern [24] was utilised as the data source. Combinations of keywords, such as “carbon nanomaterial”, “carbon nanotube”, “chemotherapy drug”, “anticancer drug”, and “doxorubicin”, were used to gather references, and the Boolean operators “AND” and “OR” were used to combine these search terms. Only English research articles that specifically focused on using CNMs to deliver clinically approved anticancer drugs were selected. The following information was extracted from each paper and entered into the database: (1) the anticancer drug used; (2) the composition of the nanocarrier system, including the CNM, and any targeting ligands, fluorophores, dispersants, etc., that were used; (3) the in vitro, in vivo, and ex vivo biological study models that the nanocarrier was tested on, including cell lines and animal breeds; (4) the drug loading and release metrics; these were taken only when explicitly given in the paper and were not calculated in this review; (5) the experimental results and observations, which were typically taken from the Conclusions section of each paper. The references were grouped based on the anticancer drug used, and the database was organised by sorting these drugs alphabetically.

2.2. Drug Loading and Release Metrics

The therapeutic efficacy of a nanocarrier system depends on its ability to absorb and release anticancer drugs; as such, quantitative metrics are needed to measure these systems. Such metrics are used to describe and compare the drug loading and release capabilities of different nanocarrier systems in the database.
The drug loading content (DLC) describes the amount of drug loaded onto the nanocarrier (Equation (1)). It is important to note that whilst most studies use the total mass of the nanocarrier (the CNM base, plus the drug, plus any other components), some studies just use the mass of the CNM itself [25], which leads to artificially higher DLC values.
DLC   wt % = mass   of   drug   bound   to   nanocarrier total   mass   of   nanocarrier × 100
The drug loading efficiency (DLE), sometimes called the encapsulation or entrapment efficiency, is a measure of the effectiveness of the drug loading process and not a quantitative measure of the drug content (Equation (2)).
DLE   wt % = mass   of   drug   bound   to   nanocarrier total   mass   of   drug   added × 100
The drug release efficiency (DRE) quantifies the cumulative release of a therapeutic agent from the nanocarrier (Equation (3)). This is the total amount of bound drug released throughout the experiment.
DRE   wt % = total   mass   of   drug   released mass   of   drug   bound   to   nanocarrier × 100

3. Database of Carbon-Nanomaterial-Based Cancer Therapeutics

Herein, we present a database of CNM-based nanocarrier systems that transport clinically approved anticancer drugs, seen in Table 1 The database includes the composition of the nanocarrier, the in vitro and in vivo biological models the system was tested on, the drug loading and release metrics, and a summary of the experimental results. The database is organized alphabetically by the anticancer drug used in the formulation; an index can be seen in Table 2.
Table 1. Database of CNM-based anticancer nanocarriers.
Table 2. Index of anticancer drug molecules in the CNM nanocarrier database.

4. Discussion

A total of 38 approved anticancer drugs were used in CNM-based nanocarriers in the literature, a breakdown of which can be seen in Figure 1. The anticancer drugs were further classified according to their mechanism of action, and the prevalence of each class is shown in Figure 1. The classes are as follows: (1) Alkylating agents—these work by adding alkyl groups to DNA, which can lead to DNA strand breaks and inhibit DNA replication; (2) Antimetabolites—these interfere with the synthesis of DNA, RNA, and proteins by mimicking essential cellular metabolites; (3) Natural products—this category consists of chemotherapeutic agents derived from natural sources, such as plants, microorganisms, or marine organisms. These agents often target specific aspects of cell division or DNA replication; (4) Hormone therapies—these target hormone-dependent cancers by interfering with the action of specific hormones or hormone receptors; (5) Antimicrotubule agents—these drugs target the microtubules, which play an essential role in cell division. By disrupting the formation or function of microtubules, these agents can inhibit cell division and lead to cancer cell death; (6) Miscellaneous agents—these include chemotherapeutic drugs that do not fit neatly into any of the other categories. The most diverse class of anticancer drugs used were alkylating agents, which is not surprising, as this class includes many Pt-based drugs, which can be easily complexed with oxidized CNMs. The miscellaneous-agent section contained five tyrosine kinase inhibitors, indicating the popularity of this class of drug. Hormone therapies were the least popular class of chemotherapy agents, with only three entries.
Figure 1. Number of anticancer drugs according to class.
For each of the anticancer drugs in the database, several CNM-based nanocarriers have been investigated for their use in drug delivery. A total of 191 examples of CNM-based nanocarrier systems were found in the literature, many of which displayed higher anticancer efficacy with reduced side effects. As discussed in the introduction, the ease of functionalisation of CNM surfaces (graphene and CNT in particular) offers many different approaches to developing nanocarriers. A huge number of ligands were found to be used for drug delivery in the literature. These included polymers, such as PEG, which offer biocompatibility, water solubility, and reduced aggregation in situ [65,96], and biomolecules, such as folic acid, which enable the active targeting of folate receptors on tumour cells [177]. Other commonly used ligands were fluorescent agents, an example of which is Alexa Fluor, which is used for the fluorescent imaging of tumour cells [160], and peptides and proteins, offering improved bioavailability and stability [84]). Many of these approaches combined in the nanocarriers found in the literature show the complexity and breadth of options available to use.
The numerical analysis of the database shown in Figure 2 reveals that graphene (GO in particular) is the most popular class of CNMs to be incorporated into these systems, likely because it is one of the most well-established carbon nanomaterials. Over the years, a catalogue of functionalisation procedures has been developed, allowing for a range of moieties to be attached to the material’s surface [201]. The flat, aromatic surface of graphene lends itself excellently to π–π stacking, which allows for the easy noncovalent stacking of drug molecules. Graphene is also a PTT agent, a property that can be used to bolster the effectiveness of chemotherapy [14]. This is beneficial for the nanocarrier developed in [188], where free TAM is more efficacious than the nanocarrier-bound drug but the PTT potential of rGO makes it an attractive combinatorial therapy. Nonfunctionalised GO and rGO were found to successfully deliver anticancer drugs. GO and rGO showed pH- and NIR-triggered releases in some cases [32,132,148]. This offers a site-specific release of the drug, as the pH in tumour cells is typically lower than that in healthy cells, and NIR offers similar delivery.
Figure 2. A stacked bar chart depicting the number of database entries for each CNM type under each class of anticancer drug.
CNTs came second in terms of popularity, which is surprising, as they are the oldest and most well-studied class of CNMs. This could be due to their tendency to aggregate into bundles in aqueous solutions, which could affect their biocompatibility. CNTs also do not have much in the way of intrinsic therapeutic or imaging properties; however, they do have large surface areas for drug loading. One example of pristine CNTs shows pH-dependent release and PTT [78]. Oxidised MWCNTs were found to be more toxic to healthy cells than cancer cells, which shows a need for further functionalisation [155]. The lack of control of intracellular accumulation also highlights the need for the attachment of targeting ligands to these systems.
Carbon dots, including GQDs, were the third most popular CNM to be used in these systems. The carbon allotropes that make up this new and rising class are tiny, even compared to other CNMs; this allows them to penetrate deep into cells to deliver drug molecules. They are even small enough to cross the blood–brain barrier [202], and their excellent biocompatibility [203] and ease of production in many cases [204] make them excellent nanocarrier scaffolds.
Many types of carbon dots are also water-soluble and have fluorescence imaging capabilities in the pristine form, for dual imaging and drug delivery [175]. Other types of CNMs, such as fullerenes, NDs, CNOs, HMCS, and CNHs, may not be as popular, but they show potential as nanocarriers due to their unique properties. For example, NDs offer improved biocompatibility over other CNMs [114,166], whilst fullerenes and CNOs display ease of functionalisation, narrow PDI, and ease of production [23,59].
In terms of drug moieties, antimicrotubule agents were the most popular payloads for these nanocarriers (Figure 2). This is due to the presence of multiple aromatic rings in these molecules, which facilitate noncovalent attachment to the CNM surface.
Anthracyclines, such as doxorubicin and epirubicin, are particularly popular. Alkylating agents are also quite popular, with platinum-based drugs often being complexed to the surface of the nanomaterial host. This is a particularly popular strategy with highly oxidised materials, such as GO, as the Pt can complex directly with oxygen-containing functional groups. Smaller hydrophilic organic molecules that lack any aromatic rings, such as those in the hormone therapy class, tend to not be so popular in CNM nanocarrier systems due to the lack of noncovalent interactions with the host CNM.
Designing systems that incorporate the intrinsic properties of CNMs allows for additional capabilities without having to chemically modify the material. The fluorescence of CDs and GQDs have proven to be useful for cellular imaging and tracking experiments [36,74,88]. Certain CNMs may also be utilised for killing cancer cells; for example, graphene has been used as a PTT agent, bolstering the effect of traditional chemotherapy [14,148]. Utilising this synergistic approach means that lower amounts of toxic chemotherapy drugs can be given to achieve the same therapeutic effect. The nπ* state of a CNM is essential for its intrinsic photothermal properties, and this state can be modulated by the addition of dopants (such as nitrogen) to the CNM [205]. Strong light absorption is required for a material to display photothermal properties, and a high photothermal conversion efficiency (η) is needed for a nanocarrier to be an effective PTT agent. For example, Forte et al. achieved photothermal-triggered drug release using a carbonised polymer dot-based system with an η value of 67.9% [206].
In general, systems that incorporate combination therapies exhibit some of the strongest anticancer effects due to the synergistic effects of PTT, PDT, single-drug and combination chemotherapy, or immunotherapy [67,129,169,190]. CNMs are the perfect class of nanoparticles for this approach, as they are easy to modify both covalently and noncovalently, with a range of functionalisation approaches available, allowing for the attachment of many different therapeutic agents. This, combined with the intrinsic properties of CNMs, can be leveraged to construct a range of nanocarrier systems.
The DLCs, DLEs, and DREs of nanocarriers are given as the number of entries above and below 50% in Figure 3. This was performed to make the entries more comparable given the differences in the sample sizes. A total of 152 out of 191 nanocarriers found in the literature had DLC, DLE, and/ or DRE data, and where DLC data were given, less than 35% of the nanocarriers were found to display values above 50%. This is similar for all CNMs, and surprisingly, graphene is the lowest, with only 22% of nanocarriers above 50% DLC. A much greater proportion of nanocarriers show DLEs above 50%, with fullerenes showing the lowest percentage of DLE values above 50%, and nanohorns displaying the highest at 100%; however, only one entry was available. This indicates that drug loading is an efficient process. In general, either a DLC or DLE value was given, with the DLE higher than the DLC.
Figure 3. The number of entries that have DLEs, DLCs, or DREs above or below 50%, grouped by CNM class.
The DRE, where given, was found to be quite high, on average, for all CNMs, with NDs displaying the lowest values; however, the sample size for this material was small compared to those for graphene and CNTs. Graphene-based nanocarriers incorporating Fe3O4 showed particularly high loading and release: [47,85,193]. GO-COOH also displayed high loading and release properties [133]. A lot of CNT-based systems with very high loading and release were observed; for example, the FA-PEG-bis-amine MWCNT system displayed 99% DLE and 90% DRE [27], SWCNTs showed 94% DLE and 93% DRE [78], and CNT-PEG displayed 95% DLC and 100% DRE [186].
For carbon dots, the CS-coated Fe3O4–NH2/GQD hybrid displayed 90% DLC + 84% DRE [33], whereas the GQD-HA system showed 98% DLE + 100% DRE [83], and the FA-CD-GOx nanocarrier yielded 82% DLE + 95% DRE [13]. Whilst there were much fewer fullerene systems with high drug loading/release metrics, acylated C60 fullerene displayed 81% DLC and 84% DRE [99]. A single ND system yielded 87% DLE and 80% DRE [166], whereas NHs and NPs do not show high combined loading and release.
The biocompatibility of these formulations must be further investigated, as certain CNMs are known to be toxic [207]. On the one hand, in the case of CNTs, the pristine form is toxic in mice and is dependent on the types of CNTs present [208]. On the other hand, pristine fullerenes such as C60 show no apparent toxicity, whereas some functionalised derivatives are highly toxic [209]. However, as previously discussed, the breadth of functionalisation methods and biocompatible ligands available to modify the surface chemistries of CNMs offers a variety of routes for overcoming this issue. The leakage of a drug at physiological pH is another issue that must be addressed in many systems, as toxic side effects are induced in vivo when the drug is released at neutral pH.

5. Conclusions and Future Directions

Overall, CNMs are incredibly versatile materials that can be used as both the foundation of nanocarrier systems and as therapeutic agents themselves. These systems can be designed to detect, image, and treat a range of tumours, from colorectal, brain, breast, liver, and stomach cancers. CNTs and graphene (GO in particular) were by far the most popular CNMs used in these systems due to their small size, high surface area, and ease of functionalisation. Other CNMs, such as carbon dots, are also growing in popularity due to their unique properties. A huge range of molecules, such as targeting ligands, fluorophores, dispersants, and drugs, can be easily attached to CNM surfaces, allowing for the construction of complex nanosystems.
Extensive in vivo biological work needs to be undertaken to fully understand the toxicity of these systems towards animals, and to overcome the regulatory hurdles needed to move these treatments into clinical trials.
The trend of designing theragnostic systems that incorporate the intrinsic properties of CNMs (such as PTT and fluorescence imaging) will likely be seen more in the future, as it allows for additional capabilities without damaging the CNM itself. Nanocarriers that leverage combinations of different therapies displayed the most potent anticancer effects, and therefore these systems will likely grow in popularity in the coming years.

Author Contributions

H.M. wrote the initial draft of the manuscript and prepared the figures and tables. A.F. assisted in proofreading and editing the document. S.G. supervised the project and assisted in writing and editing the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

The Irish Research Council (IRC) is gratefully acknowledged for providing a Government of Ireland Postgraduate Scholarship (GOIPG) (grant number GOIPG/2021/210) to H.M.

Acknowledgments

The authors wish to thank Michał Bartkowski for the fruitful discussions from the original idea, database planning, and final proofreading of the manuscript.

Conflicts of Interest

The authors declare no conflict of interest.

Abbreviations

5-FU5-FluorouracilHPMCHydroxypropyl methylcellulose
6-MP6-MercaptopurineHSAHuman serum albumin
A1A549-cell-targeting oligonucleotideHYDHydrazone
ADAAdamantaneIMImatinib
ADHAdipic acid dihydrazideiRGDPEGylated RGD peptide
AFAlexa Fluor, AF488/647LALactobionic acid
ALAlendronateLELentinan
Anti-EpCAMEpithelial cell adhesion molecule antibodyLINLinoleic acid
APAAspartic acidMAMannose
AptAptamermAbAnti-VEGF monoclonal antibody
AQ4NBanoxantrone dihydrochloridemCNFMesoporous carbon nanoframe
AsoBcl-2 phosphorothioate antisense deoxyoligonucleotideMETMetformin
ATRAAll-trans retinoic acidMitPMitochondrion-targeting peptide
BSABovine serum albuminMMCMitomycin C
BTBiotinMMTMontmorillonite
CB[7]Cucurbit[7]urilMMT7Macrophage membrane hybridized with T7 peptide
CDCarbon dotMPAMercaptopropionic acid
CDTCyclodextrinMSCDMesoporous silica carbon dot
Ce6Chlorin e6MTXMitoxantrone
CisPCisplatinMETXMethotrexate
CMCCarboxymethyl celluloseMWCNTMultiwalled carbon nanotube
CNPCarbon nanoparticleNCCNanocrystalline cellulose
CNHCarbon nanohornNCNCNitrogen-doped carbon nanotube cup
CNMCarbon nanomaterialNDNanodiamond
CNRCarbon nanoringN-GONitrogen-doped graphene oxide
CNTCarbon nanotubeNGRAspargine–glycine–arginine peptide
COChito oligosaccharideNIRNear-infrared
CPCarboplatinNMCSNitrogen-doped mesoporous carbon sphere
CQDCarbon quantum dotN-prGONitrogen-doped porous reduced graphene oxide
cRGDCyclic RGD motifOPOxaliplatin
CSChitosanPAP-gp monoclonal antibody
CNSCarbon nanospherePAAPoly(acrylic acid)
CURCurcuminPAMAMPoly(amidoamine)
CWKG(KWKG)6H-(-CysTrp-Lys-Gly-)(-Lys-Trp-Lys-Gly-)6-OH peptidePANIPoly(aniline)
CβCDCarboxymethyl β-cyclodextrinPCPhosphatidylcholine
DCA-HPCHSDeoxycholic acid-modified hydroxypropyl chitosanPDAPolydopamine
DESDeep eutectic solventPDTPhotodynamic therapy
DLCDrug loading contentPEGPolyethylene glycol
DLEDrug loading efficiencyPEIPolyethyleneimine
DMPE1,2-dimyristoyl-sn-glycero-3-phosphoethanolaminePF68Pluronic F68
DOA2-(2-(docosyloxy)-2-oxoethoxy)acetic acidPGAPoly(glycolide)
DOXDoxorubicinP-gpP-glycoprotein antibodies
DPPTE1,2-dipalmitoyl-sn-glycero-3-phosphothioethanolPHEAEthanolamine
DREDrug release efficiencyPHEMAPolyhydroxyethyl methacrylate
DSPE1,2-distearoyl-sn-glycero-3-phosphoethanolaminePLAPoly(lactic acid)
DTXDocetaxelPLGAPoly(lactic-co-glycolic acid)
E2β-estradiolPMAAPoly(methacrylic acid)
EGFEpidermal growth factorPNMPoly(N-isopropylacrylamide)
EPIEpirubicinPNVCLPoly(N-vinylcaprolactam)
EtEtoposidePOEGMEAPoly(oligoethylene glycol methyl ether acrylate)
ExoCancer cell exosomesPRMPeptide protamine sulphate
FAFolic acidPTTPhotothermal therapy
FCDbBiotinylated Fe2+-doped carbon dotPTXPaclitaxel
f-CNTsFunctionalised carbon nanotubesPVAPoly(vinyl acetate)
FITCFluorescein isothiocyanatePVPPolyvinylpyrrolidone
FSCNOFucoidan-decorated silica–carbon nano-onionRBCRed blood cell membrane
GAGalactoseRfRiboflavin
GE11EGFR antagonist peptiderGOReduced graphene oxide
GEFGefitinibROSReactive oxygen species
GEMGemcitabineSASodium alginate
GFLGGly-phe-leu-gly enzyme-sensitive peptideSBSB-431542 (TGF-β inhibitor)
GGNGraphene–gold nanocompositesSLP2shRNA plasmid DNA
GlcNGlucosamineSWCNTSingle-walled carbon nanotube
GNRGold nanorodTAMTamoxifen
GOGraphene oxideTATTrans-activating transcriptional activator peptide
GOQDGraphene oxide quantum dotTAUTaurine
GOxGlucose oxidaseTEGTetra(ethylene glycol)
GQDGraphene quantum dotTfTransferrin
GRPGastrin-releasing peptideTMTemozolomide
HAHyaluronic acidTPTumour-targeting peptide (CKQFSALPFNFYT)
HIFAnti-hypoxia-inducible factor 1α antibodyTRTransferrin
HMHM30181A transmembrane P-glycoprotein inhibitorTTTopotecan
HMCSHollow mesoporous carbon sphereUAUrocanic acid
HPMCHydroxypropyl methylcelluloseVEGFVascular endothelial growth factor
HSAHuman serum albuminγPGAγ-polyglutamic acid

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