Home Physical Sciences Investigating the effect of resveratrol on apoptosis and regulation of gene expression of Caco-2 cells: Unravelling potential implications for colorectal cancer treatment
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Investigating the effect of resveratrol on apoptosis and regulation of gene expression of Caco-2 cells: Unravelling potential implications for colorectal cancer treatment

  • Mohammed Al-Zharani EMAIL logo , Abdullah A. Alkahtane , Norah S. AL-Johani , Bader Almutairi , Nora Alkeraishan , Saud Alarifi , Sahirah M. Alrajeh , Khadijah N. Yaseen , Nada H. Aljarba , Fahd A. Nasr and Saad Alkahtani
Published/Copyright: April 3, 2024
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Open Chemistry
From the journal Open Chemistry Volume 22 Issue 1

Abstract

Colorectal cancer is known for its substantial impact on global morbidity and mortality, with higher prevalence in developed regions. This study delves into the potential treatment advantages of resveratrol (RSV) in addressing colorectal cancer. Apoptosis and gene expression associated with apoptotic factors were explored using Caco-2 cells, a pertinent model for colorectal adenocarcinoma. The effect of RSV on Caco-2 cell viability was investigated using MTT assay and neutral red uptake assay. The level of generated ROS was high in cells exposed to RSV. Likewise, the enzyme superoxide dismutase, responsible for converting ROS into hydrogen peroxide, was concurrently elevated. The effect of RSV on DNA damage was examined through the TUNEL assay. The gene expression analyses for pro-apoptotic elements were studied using qRT-PCR. Furthermore, the impact of RSV on the migration of Caco-2 cells was conducted through a wound-healing assay. Our results reveal RSV’s cytotoxicity on Caco-2 cells, showing dose-dependent inhibition of viability, indicating its promise as a treatment agent. The induction of cell death by apoptosis is substantiated by DNA damage. Notably, the upregulated expression of caspase-3, Bax, and p53 genes suggests RSV’s potential to modulate key apoptosis-related elements. In addition, RSV displayed an inhibitory effect on cellular migration, a significant (p < 0.05 and p < 0.01) in cancer metastasis. These findings underscore RSV’s potential to be a multifaceted therapeutic agent targeting apoptosis and metastatic processes in colorectal cancer.

Keywords: colorectal cancer; Caco-2; resveratrol; apoptosis; antioxidants

1 Introduction

Colorectal carcinoma, a prevalent form of cancer worldwide, ranks among the most frequently diagnosed malignancies, contributing significantly to cancer-related morbidity and mortality. With approximately 1.4 million new colorectal cancer cases reported annually, the global affliction continues to impact public health across the world [1]. Geographical variations in incidence rates have been witnessed, with higher occurrences in developed regions. Several risk factors have been acknowledged to be causal for colorectal carcinoma, including age, family history, lifestyle factors like diet and physical activity, and inflammatory bowel disease [2]. Early detection and intervention play pivotal roles in improving patient outcomes and survival rates. Screening methods such as colonoscopy, fecal occult blood tests, and fecal immunochemical tests have proven effective in identifying precancerous polyps or early-stage cancer, facilitating timely treatment [3]. Furthermore, advances in therapeutic options, including surgery, chemotherapy, targeted therapy, and immunotherapy, provide hope for patients with colorectal carcinoma. Despite these advances, ongoing research efforts are essential to optimize treatment strategies and reduce the impact of this formidable disease on individuals and societies worldwide. Apoptosis, a highly orchestrated form of programmed cell death, is crucial for maintaining tissue homeostasis and eliminating aberrant cells from multicellular organisms. Dysregulation of apoptosis has been implicated in various diseases, including cancer and neurodegenerative disorders, highlighting the significance of understanding the mechanisms that govern this intricate process [4,5]. Hence, there is a budding curiosity in identifying natural compounds that can modulate apoptosis, offering potential therapeutic applications. Resveratrol (RSV, 3,5,4′-trihydroxy-trans-stilbene), a naturally occurring polyphenolic compound abundant in grapes, berries, and other plant sources, has drawn considerable attention for its diverse health benefits [6]. Extensive research has unveiled that RSV possesses a blend of pharmacological activities, including anti-inflammatory, antioxidant, and anti-cancer effects [7]. Of particular interest is its ability to prompt apoptosis in various cancer cell types, rendering it an attractive candidate in cancer management. Of the mechanisms through which RSV promotes apoptosis, one is by activating the p53 tumor suppressor protein [8]. The p53 protein is central for the regulation of cell cycle arrest and induction of apoptosis to cellular stress. RSV has been revealed to enhance the activity of p53 protein, promoting apoptosis in cancer cells [9]. Additionally, RSV can modulate the B-cell lymphoma 2 (Bcl-2) proteins, which play an essential part in regulating the intrinsic apoptotic pathway [10]. By upregulating pro-apoptotic proteins, such as Bax, and downregulating anti-apoptotic proteins, such as Bcl-2, RSV can tip the balance toward apoptosis induction. Several cancers have been studied for their treatment response to RSV. In breast cancer, RSV has been demonstrated to hinder the growth of tumor, induce apoptosis, and sensitize tumor cells to conventional chemotherapeutic agents through p53 activation and Bax upregulation [8]. In prostate cancer, RSV has demonstrated anti-cancer effects by inhibiting cell proliferation and promoting apoptosis, partly via the modulation of p53 post-translational modification by inhibition of Metastasis-associated protein 1 [11]. In light of the apoptotic-inducing properties of RSV observed in numerous cancer cells outlined above, our study focuses on investigating its effects on Caco-2 cells, a well-established model of human colorectal adenocarcinoma. Caco-2 cells exhibit characteristics of intestinal epithelial cells, making them a relevant model to study colorectal cancer and the potential impact of RSV on apoptosis regulation in this context. We employ a comprehensive approach, utilizing cellular and molecular techniques, to assess apoptotic changes in Caco-2 cells following exposure to varying concentrations of RSV. Additionally, we conduct gene expression analyses to elucidate the underlying molecular pathways through which RSV may influence apoptosis-related genes in this specific cancer cell line. By gaining insights into the molecular interactions between RSV and Caco-2 cells, our study aims to further our knowledge of its potential therapeutic benefits for colorectal cancer treatment. Moreover, the findings from this investigation may provide a gateway to develop novel strategies targeting apoptosis-related pathways as a conceivable approach to combat colorectal cancer and other malignancies affecting the gastrointestinal system.

2 Materials and methods

2.1 Cell culture

Caco-2 cells were purchased from American Type Culture Collection (HTB-37 – ATCC, USA), and were cultured in 10% Dulbecco’s modified Eagle’s medium (DMEM) with fetal bovine serum (FBS) and 1% penicillin–streptomycin at 37°Ϲ and 5% CO2. Based on experiments, cells were grown in 6-, 24-, and 96-well plates. The exponentially growing cells were washed with PBS collected by trypsin and spun down at 1,600 rpm for 5 min at 4°Ϲ, and then cells were diluted with the medium at a density of 5 × 105 cells/ml.

2.2 MTT assay

Caco-2 cells were grown in DMEM (Sigma St. Louis, MO, USA) with the addition of 10% FBS and 1% penicillin–streptomycin. The MTT assay was conducted according to a previously documented procedure [12]. In brief, 5 × 104 cells were seeded in each well of 96-well plates and exposed to varying concentrations (10, 25, 50, and 100 μM) of RSV. After incubating for 48 h at 37°C, 10 μl of MTT solution was introduced to each well and further incubated for an additional 3–4 h at a temperature of 37°C. The resultant formazan crystals were then dissolved using isopropanol, and the absorbance was gauged at 540 nm employing a multi-mode Microplate Reader-Gen5TM, BioTek Cytation 5TM, USA. The percentage of cytotoxicity was calculated using the formula

Cell viability ( % ) = Optic density ( OD ) value of experimental samples ÷ OD value of experimental control sample × 100 .

2.3 Neutral red uptake (NRU) assay

The NRU assay kit (PromoCell, Heidelberg, Germany) was used, following a method previously outlined [13]. In 96-well plates, Caco-2 cells (5 × 104 cells/well) were seeded and placed in a 5% CO2 incubator for 48 h at 37°C until they reached 80–85% confluency. Next, cells were subjected to 50 and 70 µM concentrations of RSV for a duration of 48 h. After this exposure, NRU dye (100 µl in DMEM) was introduced and allowed to incubate for a period of 3 h. Following the incubation, the cells were rinsed with fixative and dye extractor solution. The spectrophotometer was utilized to measure the optical density at 540 nm [14]. Cytotoxicity (%) was calculated using the following formula:

Cytotoxicity ( % ) = OD value of experimental control − OD value of experimental sample/ OD value of experimental control × 100 .

2.4 TUNEL assay

The TUNEL assay kit-FITC (Abcam, UK) was utilized for the detection of DNA damage within Caco-2 cells. The cells were placed onto the central area of coverslips in 6-well plates, with a density of 2 × 104 cells/well, and incubated at 37°C for 24 h. Subsequently, the cells were exposed to 50 and 70 µM concentrations of RSV for 48 h. Following this treatment, the cells were rinsed with PBS, fixed using 4% paraformaldehyde for 15 min at 37°C, and then subjected to another PBS wash. Further steps involved adding 1 ml of 70% alcohol to each well, incubating for 10 min in darkness, introducing 51 µl of staining solution, and undergoing a 60 min incubation at 37°C temperature. The cells were then treated with propidium iodide/RNase A solution (10 µl) and left for incubation for 30 min at 37°C. After this, the cells were again suspended using 1 ml of wash buffer and washed with PBS. The coverslips were moved onto microscope slides, and cellular images were taken using a confocal microscope (CRCL’s LSM 780 NLO confocal microscope) [15]

2.5 Reactive oxygen species (ROS)

Cells were seeded and treated, as mentioned earlier. After the completion of the exposure time, cells were washed with PBS. Then, 10 µl of DCFH-DA dye (final concentration of 20 µM) was added and incubated for 30 min at 37°C. Then, the fluorescence intensity was measured using a spectrofluorimeter (Omega Fluostar) at excitation and emission wavelengths of 485 and 530 nm [16], respectively.

2.6 Superoxide dismutase (SOD) assay

For antioxidant enzyme, the scraped cells were incubated in lysis buffer (20 mM Tris-HCl [pH 7.5], 150 mM NaCl, 1 mM Na2 EDTA, 1% Triton, and 2.5 mM sodium pyrophosphate) followed by centrifugation at 15,000 rpm and 4°C for 10 min. SOD as an oxidative stress biomarker was quantified by using the Cayman, USA Kit, and Bradford method [17].

2.7 2.7 qRT-PCR

Cells were exposed to 50 and 70 µM concentrations of RSV for a duration of 48 h. RNA from RSV-exposed Caco-2 cells was extracted by employing the RNeasy Mini Kit (Product Code/Identifier: 74104), followed by reverse transcription into cDNA utilizing the RevertAid First Strand cDNA Synthesis Kit (Thermo Fisher Scientific). The RNA concentration and purity were determined using a Nanodrop 8000 spectrophotometer (Thermo Fisher Scientific). RT-PCR was executed through SYBR Green master mix and the 7,500 Fast RT-PCR System (Applied Biosynthesis, Carlsbad, CA, USA) with gene-specific primers. Subsequently, the quantification of gene expression for pro- and anti-apoptotic marker genes was conducted. The qPCR was carried out in triplicate, and the resulting data were presented as the average of three separate trials. The fold expression of the genes was calculated using the 2⁻DDCT method (where DCT = Ct [target] – Ct [β-actin] and DDCt = DCt [treated] – DCt [untreated]) [16].

2.8 Wound-healing assay

To evaluate the impact of chemical substances on the migration of Caco-2 cells, a wound-healing assay was performed following a method outlined earlier [18]. Cells were placed in 12-well plates at a concentration of 105 cells/well and left to grow until a confluent monolayer was formed at 37°C for 24 h. Following this incubation, a sterile 10 µl pipette tip was used to create a scratch across the cell monolayer. The cells were then washed with PBS to eliminate any detached cells, and renewed media were introduced. Subsequently, the cells were exposed to specific concentrations of RSV, namely 50 and 70 µM, for a duration of 48 h. Imaging was conducted at intervals of 0, 12, 24, 36, and 48 h, utilizing an inverted microscope fitted with a digital MC-170 HD camera (Leica, Germany). The images were analyzed using ImageJ WH_NJ macro software provided [19].

2.9 Mitochondrial membrane potential

The fluorescence dye JC-1 was utilized to assess the potential permeabilization of the mitochondrial membrane in Caco-2 cells triggered by the tested compounds. Cells were grown on cover slips in 6-well and in 96-well black bottom plates at a concentration of 5 × 105 cells in 10% medium, and then incubated in 5% CO2 at 37°C for 24 h. Post-incubation, cells were then subjected to 50 and 70 µM of RSV for 48 h. Next, cells were dyed with JC-1 for 20 min at 37°C in 5% CO2. For the microplate, the monomer dye JC-1 was read at 475 nm excitation and 530 nm emission, but the aggregate JC-1 dye was read at 535 nm excitation and 590 nm emission. To take images, JC-1 was disposed of, cells were rinsed in PBS 3 times, and cover slips were then moved to microscopic slides for fluorescence image capture using CRCL’s LSM780 NLO confocal microscope [20].

2.10 Statistical analysis

Data were analyzed using SPSS software (ver.22; SPSS Inc., Chicago, IL, USA). A comparison between treated cells and control was assessed by one way of variance (ANOVA). The limit of the significance of all analyses was considered significant at a value of p < 0.05.

3 Results

3.1 RSV reduced Caco-2 cell viability

The impact of RSV’s cytotoxicity on Caco-2 cells was evaluated using MTT assay. Caco-2 cells were subjected to different concentrations of RSV, ranging from 10 to 100 µM, over a 48-h period. The results showed that RSV induced a dose-dependent inhibition of the viability of Caco-2 cells with an IC50 of 70 ± 1.5 µM (Figure 1). To select a concentration that will have a high enough cytotoxic effect but not completely kill the cells, two doses (around IC50 value), 50 and 70 µM, were selected for subsequent experiments. To validate the results of the MTT assay, the cytotoxicity of RSV was also investigated by NRU assay at 50 and 70 µM. As observed in NRU assay, both dosages caused significantly increased toxicity of RSV on Caco-2 cells as shown by the increased uptake of NRU in contrast with the untreated control Caco-2 cells, thus confirming the cytotoxicity effect of RSV on cells as shown in MTT assay results (Figure 2).

Figure 1 Antiproliferative effect of RSV as evaluated by MTT assay. Caco-2 cells were treated with 0, 10, 25, 50, and 100 µM of RSV for 48 h. Data are mean ± SE of at least three experiments performed in triplicate. Each value represents mean ± SE (n = 3) (*p < 0.05, ***p < 0.001).
Figure 1

Antiproliferative effect of RSV as evaluated by MTT assay. Caco-2 cells were treated with 0, 10, 25, 50, and 100 µM of RSV for 48 h. Data are mean ± SE of at least three experiments performed in triplicate. Each value represents mean ± SE (n = 3) (*p < 0.05, ***p < 0.001).

Figure 2 Cytotoxic effect of RSV on Caco-2 cells. Cells were treated with 50 and 70 μM) of RSV for 48 h and evaluated by NRU assay. Each value represents the mean ± SE (n = 3) (**p < 0.01).
Figure 2

Cytotoxic effect of RSV on Caco-2 cells. Cells were treated with 50 and 70 μM) of RSV for 48 h and evaluated by NRU assay. Each value represents the mean ± SE (n = 3) (**p < 0.01).

3.2 RSV induced apoptotic cell death in Caco-2 cells

Upon discovering that the decline in cell viability was due to RSV, we proceeded to explore the potential involvement of apoptotic cell death. This investigation encompassed an assessment of potential DNA damage using the Tunel assay. Caco-2 cells were subjected to 50 and 70 µM concentrations of RSV for a 48-h interval. Subsequently, we utilized confocal microscopy to examine potential DNA damage (Figure 3). Notably, it was observed that 50 µM RSV led to significant DNA damage in comparison to the control cells that were not exposed to the compound (p < 0.05). Curiously, the 70 µM concentration did not manifest substantial DNA damage. While the exact reason for this phenomenon remains uncertain, it could potentially be attributed to increased cell death at this dosage or possibly due to the cells being in a later stage of apoptosis.

Figure 3 TUNEL assay results. (a) Fluorescence microphotograph of untreated and treated Caco-2 cells with RVS. Arrows refer to dead cells. (b) The percentage of apoptotic Caco-2 cells after treatment with RVS for 48 h. Each value represents mean ± SE (n = 3) (**p < 0.01).
Figure 3

TUNEL assay results. (a) Fluorescence microphotograph of untreated and treated Caco-2 cells with RVS. Arrows refer to dead cells. (b) The percentage of apoptotic Caco-2 cells after treatment with RVS for 48 h. Each value represents mean ± SE (n = 3) (**p < 0.01).

3.3 RSV induced oxidative activity of SOD

One of the pathways through which DNA damage is triggered involves the generation of ROS within the cell. Evaluation of intracellular ROS production revealed that exposure to 50 µM of RSV led to a substantial increase in intracellular ROS generation after 48 h, in comparison to the control. Interestingly, elevating the dosage to 70 µM resulted in a decline in ROS production (Figure 4). SOD is a critical enzyme that safeguards cells from ROS-induced damage, particularly superoxide radicals [21]. Examining SOD activity subsequent to exposing Caco-2 cells to 50 and 70 µM of RSV revealed a notable surge in SOD activity in cells subjected to 50 µM, in contrast to the control cells (p < 0.05) (Figure 5). However, a reduction in SOD activity was observed in cells exposed to 70 µM. This finding implies an increased ROS generation in cells exposed to 50 µM RSV, a phenomenon not observed at a 70 µM concentration.

Figure 4 Induction of ROS levels in Caco-2 cells after treatment with RVS for 48 h. Each value represents mean ± SE (n = 3) (*p < 0.05).
Figure 4

Induction of ROS levels in Caco-2 cells after treatment with RVS for 48 h. Each value represents mean ± SE (n = 3) (*p < 0.05).

Figure 5 SOD levels in Caco-2 cells after treatment with RVS for 48 h. Data represent mean ± SE (n = 3) (*p < 0.05).
Figure 5

SOD levels in Caco-2 cells after treatment with RVS for 48 h. Data represent mean ± SE (n = 3) (*p < 0.05).

3.4 RSV induced expression of pro-apoptotic genes

Since apoptosis is initiated due to the initiation of pro-apoptotic factors, we investigated the expression of different pro-apoptotic genes in the intrinsic pathway. After a 48-h exposure to RSV at concentrations of 50 and 70 µM, the gene expression of caspase-3, Bax, and p53 was assessed in Caco-2 cells (Figure 6). Our findings demonstrated a noteworthy and proportional elevation in the gene expression of caspase-3, Bax, and p53 following the 48-h RSV exposure. The expression of the caspase gene was 1.1-fold higher in Caco-2 cells exposed to both 50 and 70 µM in comparison to unexposed cells. For Bax, expression levels in cells subjected to 50 and 70 µM were 2.8- and 3.8-fold, respectively. Finally, the p53 gene expression was 1.7- and 2-fold for cells exposed to 50 and 70 µM, respectively, in contrast to unexposed Caco-2 cells.

Figure 6 Fold change in the expression of apoptosis-related genes in Caco-2 cells analyzed qTR-PCR. Cells were exposed to 50 and 70 µM of RVS for 48 h. The quantified genes were P53, Bax, and caspase-3. Data represent mean ± SE (n = 3) (*p < 0.05, **p < 0.01, and ***p < 0.001).
Figure 6

Fold change in the expression of apoptosis-related genes in Caco-2 cells analyzed qTR-PCR. Cells were exposed to 50 and 70 µM of RVS for 48 h. The quantified genes were P53, Bax, and caspase-3. Data represent mean ± SE (n = 3) (*p < 0.05, **p < 0.01, and ***p < 0.001).

3.5 RSV did not induce mitochondrial damage

An outcome of ROS and its triggering of the intrinsic apoptosis pathway involves mitochondrial outer membrane permeabilization (MOMP), leading to the liberation of cytochrome C and eventual apoptosis that is caspase-dependent. To ascertain if RSV-induced apoptosis led to MOMP, the permeability of the mitochondrial outer membrane was examined. The results revealed no notable differences in MOMP between treated cells at both concentrations and untreated Caco-2 cells (Figure 7).

Figure 7 MOMP test of Caco-2 cells treated with RVS for 48 h as evaluated by JC-1. The ratio of aggregate/monomer fluorescence intensity was measured. Data are presented as mean ± SE of three different experiments.
Figure 7

MOMP test of Caco-2 cells treated with RVS for 48 h as evaluated by JC-1. The ratio of aggregate/monomer fluorescence intensity was measured. Data are presented as mean ± SE of three different experiments.

3.6 RSV slowed down cell migration

In our study, we employed the wound healing (scratch) assay to explore the impact of RSV on the migration of Caco-2 cells. These cells were subjected to concentrations of 50 and 70 µM for various time intervals (12, 24, 36, and 48 h). Our findings revealed that both doses of RSV impeded cell migration compared to the control. Upon normalization of the obtained data, untreated control cells exhibited a migration ratio (MR) of 1. When compared to this baseline, both concentrations of RSV induced a time-dependent inhibition of cellular migration. Notably, the data indicated that the 50 µM RSV dose exerted a more pronounced inhibitory effect on cell migration than the 70 µM dose. At 12 and 24 h, both doses displayed similar migration inhibition. However, for the cells exposed to 50 µM RSV, there was no alteration in migration after 36 h (MR of 0.4). Conversely, cells exposed to 70 µM RSV experienced an increase in migration from 0.35 at 24 h to 0.6 after 36 h. Following 48 h of exposure, cells treated with 50 and 70 µM, RSV exhibited MRs of 0.7 and 0.5, respectively, in contrast to the MR of 1 for control cells (Figure 8).

Figure 8 Migration of Caco-2 cells in wound-healing assays. (a) Cells were treated with RVS for 48 h, and images were captured at 0 and 12, 24, 36, and 48 h. (b) The relative migration rate of Caco-2 cells in wound-healing assays. *p < 0.05 and **p < 0.01 vs control.
Figure 8

Migration of Caco-2 cells in wound-healing assays. (a) Cells were treated with RVS for 48 h, and images were captured at 0 and 12, 24, 36, and 48 h. (b) The relative migration rate of Caco-2 cells in wound-healing assays. *p < 0.05 and **p < 0.01 vs control.

4 Discussion

Chemoprevention, a promising approach for managing cancer, involves the use of non-toxic chemical substances to hinder, delay, or reverse the cellular processes associated with carcinogenesis [22]. Numerous naturally occurring compounds have demonstrated protective effects against experimental carcinogenesis, and growing evidence indicates that specific phytochemicals, especially those present in our daily diet, possess significant anti-cancer and cancer chemopreventive properties [23].

Plants have historically proven their effects as a source of therapeutic potential and still produce novel drugs [24]. Medicinal plants contain natural products that show potent antioxidant properties that have been attributed to the presence of biological activities, which in turn exhibit therapeutic effects on human health [25]. Recent focus has been paid to whether naturally occurring compounds can ameliorate the effects of various mutagens and carcinogens or not [26].

RSV is a naturally occurring polyphenolic compound present in diverse plant sources [27]. Within the scope of this research, we explored the impacts of RSV on the initiation of apoptosis in the Caco-2 cell line. This particular cell line holds significance as an invaluable in vitro model for investigating the anti-cancer effects of RSV on colorectal cancer. The evaluation of RSV’s cytotoxic impact on Caco-2 cells, both through MTT and NRU assays, revealed a decline in cell viability following exposure to RSV, with the degree of reduction correlating with the dose. These findings are consistent with prior research that has highlighted RSV’s cytotoxic effects on a range of human tumor cells, spanning myeloid and lymphoid cancer cells, as well as carcinoma cells originating from the breast, cervix, ovary, prostate, liver, pancreas, and thyroid [28,29,30,31,32]. To delve into the operational mechanism of RSV, its impact on DNA damage was investigated, revealing a substantial induction of DNA damage in Caco-2 cells at both tested concentrations. DNA damage holds significant potential to influence the death of cancer cells by initiating a cascade of cellular responses. Among these mechanisms, one of the pivotal pathways is apoptosis, which is set in motion by DNA damage. Previous research has also highlighted RSV’s ability to induce DNA damage in various cancer cell types. For instance, RSV’s interference with ABC transporters and drug-metabolizing enzymes enhances DNA damage, impedes the progression of the cell cycle, triggers apoptosis and autophagy, and consequently thwarts the initiation of the epithelial-to-mesenchymal transition (EMT) [33]. In addition, RSV cotreatment with paclitaxel has been shown to increase cellular cytotoxicity by elevating ROS levels, causing oxidative DNA damage, and ultimately promoting apoptosis in colon cancer cells [34]. This is in support of our finding on ROS generation. We found a high level of ROS generation in cells exposed to RSV (50 µM), which aligns with the findings of other studies [35,36]. Likewise, the enzyme SOD, responsible for converting ROS into hydrogen peroxide, was concurrently elevated. In contrast, a prior investigation has demonstrated that RSV curbs DNA damage by restraining the oxidative production of ROS in bronchial epithelial cells [36]. The divergence between our findings and the outcomes of the aforementioned study could potentially stem from the distinct pathway implicated in bronchial epithelial cells, which represent a normal human cell line. In response to cellular stress, mitochondria release pro-apoptotic molecules, including cytochrome c, into the cytoplasm. Subsequently, cytochrome c sets initiates a sequence of events culminating in the activation of caspases 3 and 7 [37]. Elevated gene and protein expression of specific Bcl-2 family members, like Bax and Bak, along with a corresponding decrease in the gene and protein expressions of anti-apoptotic Bcl-2 protein, fosters MOMP. This, in turn, facilitates the release of pro-apoptotic molecules, including cytochrome c. In essence, a high Bax to Bcl-2 ratio causes induction of caspase-dependent apoptosis [38]. In the present research, an elevation in the gene expression of Bax was noted within the Caco-2 cell line [38,39,40], which would have been expected to induce MOMP. Likewise, a prior investigation revealed an elevated ratio of Bax to Bcl-2 in acute myeloid leukemia patients characterized as poor responders to cytarabine and daunorubicin. Although patients exhibiting remission displayed a lower ratio due to heightened expressions of both Bax and Bcl-2, no significant contrast emerged between the two groups [41]. In support of previous findings, however, we have previously reported a low Bax and Bcl-2 ratio in the Huh-7 cell line in response to cyclophosphamide treatment [42]. The permeability of the mitochondrial membrane was observed to be consistent across all treatment groups in comparison to the control, underscoring the sustained integrity of the mitochondrial membrane. The p53 signaling pathway has been linked to the chemopreventive and anti-cancer attributes of several dietary antioxidants, as substantiated by numerous investigations encompassing both normal and cancerous cell lines, along with animal models [43]. Similarly, RSV has also been shown previously to exhibit chemopreventive properties through the activities of the p53 signaling pathway. A previous study showed that RSV triggered apoptosis and hindered cell transformation induced by tumor promoters in JB6 cells [44]. Additionally, the research demonstrated that RSV triggered the activation of p53 and subsequent apoptosis through a pathway reliant on p53. Likewise, our investigation observed that RSV prompted the dose-dependent enhancement of p53 expression, a phenomenon that could potentially govern survival pathways such as the MAPK pathway, thereby culminating in the observed apoptosis [45]. The migration assay, a key component of our study, sheds light on the potential impact of RSV on the metastatic processes in colorectal cancer, providing insights into the initial phase of metastasis-cell migration [46]. Given the significance of metastasis, understanding how RSV influences cellular migration is crucial for evaluating its potential therapeutic implications. Our findings revealed that RSV exerted a notable effect on inhibiting cellular migration in Caco-2 cells, a representative model of colorectal adenocarcinoma. This inhibitory effect was concentration-dependent, with both 50 and 70 µM doses demonstrating a gradual reduction in cellular migration over time. The observed inhibition of migration by RSV in this research study aligns with outcomes of various other studies that have reported similar findings for RSV in different cancers. Tang et al. [47] demonstrated that 10 µM RSV inhibited IGF-1-induced migration in breast cancer cells. Another study also showed that RSV enhanced the cisplatin antitumor effect by enhancing the inhibitory effects of cisplatin on the human breast cancer MDA-MB-231 cell line [48]. Several mechanisms could underlie RSV’s inhibitory effect on cellular migration. One possible explanation is its ability to modulate signaling pathways involved in cytoskeletal rearrangement, a fundamental process governing cell movement. RSV’s known impact on pathways related to cell adhesion, motility, and cytoskeletal dynamics may contribute to its ability to impede migration. For instance, RSV has been shown to bind several cytoskeletal proteins and inhibit cell migration of A549 cancer cells [49] by proteomic analyses. Moreover, RSV’s role in altering the tumor microenvironment and inhibiting angiogenesis may indirectly influence the migratory behavior of cancer cells [50]. The ability of RSV to impede cellular migration holds clinical importance owing to its capacity to restrain the spread of metastatic disease. The mitigation or deceleration of metastasis plays a vital role in enhancing patient prognosis, given the typically unfavorable outlook and restricted therapeutic avenues associated with advanced metastatic conditions. Our results align with earlier research showcasing RSV’s capacity to counteract metastasis in diverse cancer categories, underscoring its potential as a versatile agent against various forms of cancer. Although our study offers significant understanding regarding the impact of RSV on migration, further research is necessary to unravel the specific molecular mechanisms by which RSV influences this phenomenon in colorectal cancer cells. Additionally, the validation of these findings and the evaluation of their potential therapeutic advantages for patients will require in-depth in vivo studies and clinical trials.

5 Conclusions

In conclusion, our study contributes to the growing body of evidence supporting RSV as a multifunctional compound with potential therapeutic implications for colorectal cancer. While highlighting its chemopreventive, pro-apoptotic, and anti-metastatic effects, we acknowledge that the precise molecular mechanisms underlying these effects require further exploration. The diverse and context-dependent actions of RSV underscore the convolution of its interactions with cellular pathways. Moving forward, further in-depth investigations, including in vivo investigations and clinical trials, are warranted to translate these findings into meaningful therapeutic strategies that can positively impact patients with colorectal cancer.

Acknowledgments

The authors are thankful to the Researchers Supporting Project number (RSP2024R26), King Saud University, Riyadh, Saudi Arabia. Princess Nourah bint Abdulrahman University Researchers Supporting Project number (PNURSP2024R62), Princess Nourah bint Abdulrahman University, Riyadh, Saudi Arabia.

  1. Funding information: This work was funded by Researchers Supporting Project number (RSP2024R26), King Saud University, Riyadh, Saudi Arabia. Princess Nourah bint Abdulrahman University Researchers Supporting Project number (PNURSP2024R62), Princess Nourah bint Abdulrahman University, Riyadh, Saudi Arabia.

  2. Author contributions: Mohammed Al-Zharani and Abdullah A. Alkahtane performed the cytotoxic assays. Saud Alarifi, Sahirah M. Alrajeh, and Khadijah N. Yaseen assessed the generation of iROS. Norah S. AL-Johani and Nora Alkeraishan measured the cell migration. Bader Almutairi and Saad Alkahtani evaluated apoptotic gene expression. Nada H. Aljarba, Saad Alkahtani, and Mohammed Al-Zharani evaluated DNA damage and cell survival. Saud Alarifi, Fahd Nasr and Saad Alkahtani wrote and edited the article. All authors have approved the final article.

  3. Conflict of interest: All authors declare that there is no conflict of interest regarding the publication of this article.

  4. Ethical approval: The conducted research is not related to either human or animal use.

  5. Data availability statement: The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

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Received: 2023-10-31
Revised: 2024-02-24
Accepted: 2024-03-15
Published Online: 2024-04-03

© 2024 the author(s), published by De Gruyter

This work is licensed under the Creative Commons Attribution 4.0 International License.

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https://doi.org/10.1515/chem-2024-0012
Keywords for this article
colorectal cancer; Caco-2; resveratrol; apoptosis; antioxidants
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