Polyphenol-Based Nanoparticles: History
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Contributor:
Hicham Wahnou
,
Bertrand Liagre
,
Vincent Sol
,
Hicham El Attar
,
Rukset Attar
,
Mounia Oudghiri
,
Raphaël Emmanuel Duval
,
Youness Limami

Conventional therapies for the treatment of colorectal cancer induce several side effects that impact the effectiveness of current therapies as well as the quality of patients’ life. Natural compounds with anticancer properties have gained attention as potential therapeutic agents for various cancers including colorectal cancer. However, several natural compounds such as polyphenols are facing obstacles for their use as anticancer drugs, such as intrinsic poor solubility, plasmatic instability, ineffective cellular uptake, and biological barriers. Novel approaches in precision medicine and nanomedicine are being developed. In this context, to harness the full potential of natural compounds, researchers have explored the use of nanoparticles as a drug delivery system for targeted and enhanced therapeutic efficacy as well as limited side effects. 

  • colorectal cancer
  • nanomedicine
  • nanoparticles
  • polyphenols
  • natural compounds
  • chemical synthesis
  • drug delivery system
  • signaling pathways
  • cancer

1. Polyphenols-Intrinsic Anticancer Properties

Polyphenols, a diverse class of bioactive compounds, exhibit a distinctive chemical structure characterized by multiple phenolic rings and various functional groups. They can be classified into different subclasses based on their chemical structure and origin (Figure 1) [1]. Flavonoids, which include flavones, flavonols, and flavanones, constitute one major subclass, while phenolic acids such as hydroxybenzoic acids and hydroxycinnamic acids represent another. Additionally, stilbenes, such as resveratrol and other subclasses, contribute to the broad range of polyphenols [1]. Examples of commonly studied polyphenolic compounds in the context of CRC treatment include EGCG found in green tea, curcumin from turmeric, quercetin present in fruits and vegetables, resveratrol obtained from grapes, and genistein found in soybeans. These polyphenols possess unique chemical structures that contribute to their remarkable anticancer activity.
Polyphenolic compounds such as EGCG, quercetin, tannic acid, and resveratrol possess anticancer properties by targeting various cancer hallmarks including inhibition of proliferative signaling, induction of cell death, and modulation of gut microbiota.
Polyphenols can induce cell cycle arrest by targeting various signaling pathways. EGCG, for example, can interact and inhibit receptor tyrosine kinases (RTKs), which are cell surface receptors that play a key role in the activation of the survival PI3K/Akt signaling pathway [2]. Additionally, these compounds can modulate gene expression through epigenetic mechanisms, such as DNA methylation and histone modification, to inhibit tumor growth [3][4][5][6]. Quercetin, on the other hand, can cause S phase arrest by decreasing the protein expression of CDK2, cyclins A and B while upregulating p53 and p57 proteins [7]. Quercetin can also act as a prooxidant molecule causing DNA damage and resulting in cell cycle arrest and/or p53-dependent or independent mitochondrial apoptosis [8]. Similarly, resveratrol can inhibit Akt, STAT3 signaling pathways to block cell in dosage dependent manner [9].
Cell death can also be caused by polyphenolic compounds. EGCG has demonstrated the ability to increase the stability and transcriptional activity of the tumor suppressor p53, leading to apoptosis [10]. Furthermore, EGCG has also been described to induce autophagy through the inactivation of the PI3K/Akt/mTOR signaling pathway [2]. Similarly, quercetin triggers apoptosis in cancer cells by reducing the expression of Bcl-2 through a mitochondria-mediated pathway [11]. Additionally, quercetin treatment has been found to induce protective autophagy by modulating Akt/mTOR signaling and activating HIF-1α signaling, thereby counteracting quercetin-induced apoptotic cell death and affecting its therapeutic effectiveness [12]. Furthermore, resveratrol has also been investigated for its potential to induce cell death such as, apoptosis and autophagy in various cancers, including CRC, by modulating signaling pathways such as caspase-3, caspase-8, Poly (ADP-Ribose) Polymerase (PARP), LC3-I, LC3-II and PI3K/Akt/mTOR [9][13][14]. Necroptosis may also be induced by resveratrol by increasing the levels of p-RIPK3 and p-MLKL [14].
Finally, polyphenols have also been investigated to modulate microbiome polymorphic variability—one of the newly described hallmarks of cancer. Microbiome can influence cancer phenotypes, development, and progression, with specific effects observed in CRC [15]. In fact, the balance between cancer-protective and cancer-promoting microbiomes modulate the incidence and pathogenesis of CRC as well as response to therapy [15]. Polyphenolic compounds have been shown to modulate gut microbiota, affecting the development of CRC [16]. In a model of CRC in mice, supplementation of polyphenols such as isoliquiritigenin, anthocyanin, and EGCG altered the gut microbial composition towards a healthier profile [16]. Additionally, polyphenols can indirectly inhibit tumor growth by influencing the behavior of cells in the tumor microenvironment [17]. For instance, castalagin improves the efficacy of immune therapy by recruiting beneficial gut bacteria [18]. In addition, Musial et al. reported several lines of evidence that support anticancer effects of polyphenols from coffee and green tea extracts towards various cancers including CRC [19].
The efficacy of polyphenols has also been a subject of investigation in clinical trials, highlighting their potential in CRC treatment. By conducting research on clinical trials website to further explore the potential of polyphenols, two completed studies using the keywords “polyphenols” and “colorectal cancer” were found [20]. The first trial, registered as NCT01916239, examined the use of pomegranate extract supplementation in CRC patients as a potential intervention. It aimed to evaluate the impact of pomegranate extract supplementation on biomarkers associated with CRC including metabolic and gene expression profiling. The second trial, registered as NCT01360320, focused on green tea extract and its therapeutic potential. This research aimed to assess the preventive effects of green tea extract on adenomas, which are precursor lesions of CRC. These clinical trials demonstrate the growing interest in investigating the efficacy and safety of polyphenols as promising interventions for CRC treatment, providing valuable insights into their potential benefits. Despite the diverse mechanisms by which polyphenols can destroy CRC cells, the limitations of these compounds present challenges to their extensive utilization in medical research [21][22][23]. Issues such as poor chemical stability, low water solubility, limited bioavailability, rapid elimination from the system, and quick metabolism hinder their broader application [22]. However, significant progress has been made in the field of biological materials and drug delivery strategies, allowing researchers to effectively address these issues [24][25][26][27]. Encapsulation of therapeutic polyphenols within drug delivery systems has emerged as a promising approach to enhance their therapeutic effects (Figure 1).
Cancers 15 03826 g003 550
Figure 1. Overview of the mechanisms of action of some nano-based drug delivery of natural polyphenolic compounds. (A) Polyphenol-based intracellular protein delivery by boronic acid-decorated polymers. The presence of polyphenols increased the affinity between boronic acid-containing polymers and proteins. In acidic environments, the pH-responsive catechol–boronate bonds formed between the boronic acid-conjugated polymers and polyphenols allowed for the release of the RNase that can cause cell death by destroying targeted RNA. (B) DOX−Den complex with the TA−Fe3+ MPN for chemodynamic therapy (CDT). DDTF efficiently transports DOX into cancer cells by evading drug efflux transporters on the plasma membrane. Inside the cells, DOX is delivered to the nuclei through the Fenton reaction-mediated CDT. The excessive production of reactive oxygen species (ROS) induced by the Fenton reaction and DOX ultimately leads to the elimination of drug-resistant cancer cells. (C) MMP-2-sensitive PEGylated EGCG dimer and EGCG dimer facilitated combination immune checkpoint blockade and photodynamic therapy using an αPD-L1/ICG nanocomplex. Once the nanoparticle is activated by MMP-2, it releases αPD-L1/ICG, and the antibody blocks the PLD1 checkpoint, whereas the illumination of the photosensitizer induces various effects including ROS generation and cell death.

2. Polyphenols Properties Enhancement via Nano-Based Delivery Systems

Nano-based delivery strategies enable the simultaneous administration of multiple functional drugs, enhancing the potential of polyphenolic compounds in cancer therapy. Nanocarriers that are commonly utilized to deliver natural polyphenolic compounds in cancer therapy, including in the context of CRC treatment, are micelles, nanogels, liposomes, nanoemulsions, AuNPs, MSNs, and metal–organic frameworks (MOFs) (Figure 2). In this section, researchers will discuss the structure and classification of nanoparticles, their role in enhancing the anticancer properties of polyphenols, and the challenges associated with NP-based delivery systems.
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Figure 2. Classification of nanocarriers that are commonly utilized to deliver polyphenols compounds in cancer therapy. (A) Polymeric NPs, (B) lipid-based NPs, (C) inorganic NPs.

2.1. Micelles

Micelles, as nanocarriers, hold great promise for targeted delivery of polyphenolic compounds in CRC therapy. These self-assembled structures consist of a hydrophilic polymeric shell and a hydrophobic core, offering advantages such as small size and enhanced permeability at lesion sites (Figure 2A) [28]. In CRC treatment, micelles can effectively deliver polyphenolic compounds like resveratrol and curcumin [29][30]. For example, nanomicelles loaded with hypoxia modulator resveratrol and photodynamic reagent chlorin-e6 have shown potential in triggering autophagic cell death and apoptosis of oral squamous cell carcinoma cells [29]. Glutathione (GSH)-sensitive nanomicelles integrated with curcumin have also been designed to target and treat esophageal cancer [30]. Additionally, micelles improve the solubility of polyphenolic compounds, as seen with the nano poly(lactic-co-glycolic acid) (PLGA)-curcumin micelle, which reverses gemcitabine resistance in CRC by suppressing the nuclear factor-κB (NF-κB) signaling pathway [29]. These findings highlight the potential of micelles as effective nanocarriers for delivering polyphenolic compounds in CRC therapy, addressing solubility issues, and enhancing treatment outcomes.

2.2. Nanogels

In addition to micelles and liposomes, nanogels have emerged as another promising type of nanocarrier for targeted delivery of therapeutic agents in CRC therapy. With their porous structures and large, surface-to-volume ratios, nanogels can encapsulate both hydrophilic and hydrophobic therapeutic agents (Figure 2A) [31]. These nanocarriers enhance drug permeability and retention at tumor sites, improving treatment efficacy. For instance, TME-responsive nanogels loaded with resiquimod and EGCG have been developed to alleviate immunosuppression in the tumor microenvironment, leading to an increased ratio of cytotoxic T cells to regulatory T cells and improved immunotherapy outcomes. pH- and thermo-responsive nanogels loaded with DOX and curcumin have also been designed to enhance treatment outcomes in CRC by sensitizing tumor cells to DOX and reducing drug distribution in healthy tissues [32]. Additionally, nanogels can achieve sustained drug release, improving therapeutic effects while minimizing side effects. A curcumin-loaded nanogel demonstrated enhanced tumor growth suppression compared to free curcumin, highlighting the potential of nanogels in optimizing CRC treatment [33].

2.3. Liposomes

On the other hand, liposomes are synthetic vesicles composed of a lipid bilayer that encapsulates aqueous compartments, which have shown promise in CRC therapy (Figure 2B). These spherical nanocarriers, similar to cell membranes, have been FDA-approved for clinical use [34]. Liposomes loaded with tea polyphenols have demonstrated efficacy in treating Helicobacter pylori infection, a major contributor to gastric cancer [35]. Furthermore, the encapsulation of polyphenolic compounds, such as resveratrol and EGCG, in liposomes has improved their stability and anticancer performance in prostate and bladder cancer cells [36][37]. Liposomes can also be tailored for drug delivery in the gastrointestinal environment, providing enhanced stability and bioavailability for therapeutic agents like resveratrol and artemisinin [38]. This approach has shown cytotoxic effects on intestinal adenocarcinoma cells, presenting a potential strategy for treating CRC.

2.4. Nanoemulsions

Nanoemulsion polyphenol is a specialized structure comprising nanoscale droplets suspended within a continuous phase. This unique system involves the combination of two immiscible phases, typically oil and water, which are held together by an emulsifying agent or surfactant. Within the nanoemulsion, polyphenols, such as quercetin, are loaded into the oil phase (Figure 2B). Notably, the use of quercetin nanoemulsion has shown remarkable efficacy in inhibiting the viability of CRC cells in a dose-dependent manner, surpassing the effectiveness of the drug alone [39]. Furthermore, it has been observed that the nanoemulsion significantly enhances cellular toxicity against CRC cell lines, particularly HT-29 and HCT-116, resulting in more efficient cell eradication compared to the free polyphenol agents [39]. Furthermore, in vivo studies have demonstrated that the administration of quercetin emulsion and nanoemulsion can effectively restore the oxidant-antioxidant balance in mice serum samples and reverse the 5-fluorouracil-induced histological damages in intestinal tissue [40]. These findings highlight the significant potential of quercetin nanoemulsion as a promising therapeutic strategy for CRC treatment.

2.5. AuNPs

In the same context, AuNPs have also emerged as promising nanocarriers in the field of CRC treatment due to their advantageous characteristics, including biocompatibility, stability, and the ability to be easily functionalized [41]. These properties make AuNPs an attractive platform for targeted drug delivery [41]. By conjugating polyphenolic compounds onto the surface of AuNPs, a versatile system for delivering therapeutic agents to specific targets is created (Figure 2C) [42]. Numerous studies have demonstrated that polyphenol-coated AuNPs exhibit enhanced cellular uptake and improved bioavailability of therapeutic agents in CRC cells [42]. For instance, the conjugation of EGCG with AuNPs has shown promising anticancer effects in CRC [43]. These effects include induction of cell cycle arrest, promotion of apoptosis, downregulation of NF-κB, and inhibition of tumor growth [43]. The combination of EGCG with AuNPs leads to synergistic therapeutic outcomes, suggesting its potential as an effective strategy for CRC treatment. Moreover, the unique optical properties of AuNPs allow them to serve as photoresponsive agents in photothermal therapy for CRC [41]. By harnessing these properties, AuNPs can selectively destroy tumor cells while sparing healthy tissues.

2.6.  Mesoporous Silica Nanoparticles

MSNs have gained significant attention as drug carriers due to their porous surface, low toxicity, and high drug-loading capacity [44][45]. Different gatekeepers have been utilized to develop controlled release systems based on MSNs [45][46]. However, challenges such as complex preparation processes and premature drug release still exist. To overcome these challenges, polyphenols have emerged as functional coatings on MSNs. Polyphenol-coated MSNs offer tumor targeting and controlled release properties, making them effective and biocompatible nanocarriers for drug delivery (Figure 2C) [47]. For instance, EGCG-modified MSNs have been developed for drug delivery, where the EGCG coating enhances stability, prevents premature drug release, and provides a site for the immobilization of a DNA aptamer for targeted delivery [48]. The polyphenol coatings are physiologically stable and can be degraded under specific conditions, leading to the release of drugs and subsequent cell apoptosis [48]. Other responsive gatekeepers, such as PDA and magnetic particles, have also been employed on MSNs, further expanding their applications in controlled drug delivery and chemotherapy [49][50].

2.7. Metal–Organic Frameworks

MOFs have gained popularity as hybrid porous materials for drug delivery due to their excellent characteristics such as a porous structure, modifiable components, and satisfactory drug loading capacity (Figure 2C) [51]. However, the clinical application of nanoscale MOFs in cancer treatment faces challenges related to protein binding during circulation and low tumor selectivity. To address these issues, modifications are needed to enhance the bio-stability and tumor targeting of MOFs [52].
Polyphenols, particularly PDA, have been extensively studied as coating materials due to their high affinity to surfaces, photothermal conversion effect, and biosafety [53]. For instance, MIL-100, a pH-sensitive degradable MOF, has been coated with HA-PDA to improve the dispersity, biostability, and tumor-targeting capacity of the NPs [54]. Another study utilized zeolitic imidazolate framework-8 (ZIF-8) as a removable template to construct nanocapsules for efficient drug delivery. The ZIF-8 NPs were decorated with an EGCG-Fe(III) coating, resulting in DOX-encapsulated EGCG-Fe(III) nanocapsules. These nanocapsules could be internalized by cancer cells and release drugs in response to the overproduction of ROS in cancer cells [55].

3. Challenges Related to Nano-Based Delivery Systems

The use of various nanocarriers, including micelles, nanogels, liposomes, nanoemulsions, AuNPs, MSNs, and MOFs presents a unique challenge for polyphenol delivery. Indeed, encapsulation and efficient loading of polyphenols within these nanocarriers can be influenced by factors such as polyphenol solubility and compatibility with the carrier system [46]. Achieving controlled release kinetics that match therapeutic needs while preserving polyphenol stability is another hurdle. Biocompatibility and potential toxicity are critical considerations for ensuring the safe use of these nanocarriers in polyphenol delivery [46]. Stability and degradation issues may also arise, impacting the performance and drug release properties of the carriers. Furthermore, scaling up the manufacturing processes while maintaining consistent quality, reproducibility, and control over important parameters poses additional challenges [46]. Overcoming these obstacles through rigorous research and development efforts will advance the field and maximize the potential of nanocarriers for effective polyphenol delivery in biomedical applications.

4. Conclusion

In conclusion, natural polyphenols hold great promise as drug delivery systems for colon cancer treatment. Various nanocarriers have shown effectiveness in delivering these compounds to tumors, improving therapy outcomes. However, challenges such as stability issues and interactions with biological components need addressing. Future prospects include natural polyphenolic mixtures-based formulations, cost-effective isolation methods, and advanced nanocarrier technologies. These advancements could transform colon cancer therapy, enhancing drug delivery efficiency, minimizing side effects, and improving patient outcomes.

This entry is adapted from the peer-reviewed paper 10.3390/cancers15153826

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