Home A novel long noncoding RNA AC125257.1 facilitates colorectal cancer progression by targeting miR-133a-3p/CASC5 axis
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A novel long noncoding RNA AC125257.1 facilitates colorectal cancer progression by targeting miR-133a-3p/CASC5 axis

  • Chuanwen Liao , Zihan Zheng , Junye Liu , Jian Li , Rui Li and Shuqin Hu EMAIL logo
Published/Copyright: March 27, 2023
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Open Medicine
From the journal Open Medicine Volume 18 Issue 1

Abstract

Colorectal cancer (CRC) is a common malignant gastrointestinal tumor. Long noncoding RNAs (lncRNAs) are revealed to be critically involved in CRC progression, providing new direction for exploring the pathogenesis of CRC. This study aimed to explore the biological functions and regulatory mechanisms of lncRNA AC125257.1 in CRC. Western blotting and reverse-transcription quantitative polymerase chain reaction were used for the measurement of gene expression. Cell counting kit-8 assay and flow cytometry analysis were used to explore the effects of AC125257.1 on CRC cell viability and apoptosis. RNA pull-down and immunoprecipitation assays were performed for validating the binding between AC125257.1 and its potential downstream microRNA. Results showed that lncRNA AC125257.1 expression was upregulated in CRC cells and tumor tissues. AC125257.1 enhanced cell viability and suppressed apoptosis of CRC cells. Moreover, the knockdown of AC125257.1 suppressed CRC progression in vitro and inhibited tumor growth in vivo. miR-133a-3p was revealed to bind with AC125257.1 in CRC cells. CASC5 was proved to be targeted by miR-133a-3p. Moreover, rescue assays indicated that the knockdown of AC125257.1 suppressed the pathogenic overexpression of CASC5. To conclude, AC125257.1 aggravates CRC development via miR-873-5p/CASC5 axis. Our findings might suggest a novel perspective that AC125257.1 may become the target for CRC treatment.

Keywords: CRC; AC125257.1; miR-133a-3p; CASC5; cell signaling

1 Introduction

Colorectal cancer (CRC) is known for high fatality rate as commonly diagnosed around the world [1]. Rectum adenocarcinoma (READ) and colon adenocarcinoma (COAD) are two CRC classifications with different anatomical locations and similar molecular mechanisms [2,3]. More than 90% cases of CRC are adenocarcinoma developed from colon and rectum glandular epithelial cells [4]. Although huge breakthroughs have been made on the pathogenesis and treatment of CRC, there still lack efficacious way to prevent and treat CRC. Hence, it is necessary to explore new targets for CRC therapy.

Long noncoding RNAs (lncRNAs) are reported to affect the cancer phenotypes by controlling cellular processes, such as apoptosis, proliferation, migration, and invasion [5]. With over 200 nucleotides in length, lncRNAs regulate expression via multiple ways, including microRNA (miRNA) sponge, epigenetic modifications, and mRNA stabilization [6]. In the competitive endogenous RNA (ceRNA) network, lncRNAs act as miRNA sponges competitively binding to miRNAs to inhibit the suppressive effects of miRNAs on the endogenous targets [7]. For example, lncRNA CASC21 promotes CRC cell proliferation, migration, and invasion and inhibits cell apoptosis by regulating the miR-7-5p/YAP1 axis [8]. lncRNA SNHG10 silencing suppressed the malignant behaviors of CRC cells by interacting with miR-3690 [9]. Recently, the lncRNA AC125257.1 was found to be autophagy related and contributed to poor prognosis in CRC [10]. The bioinformatics analysis also reveals that AC125257.1 is upregulated in CRC tissues compared with normal tissues. Nevertheless, the function and regulatory mechanism of AC125257.1 in CRC progression are largely unclear.

miRNAs are short noncoding transcripts (∼22 nucleotides) critically involved in the development of various diseases, including cancer [11]. Studies have suggested the role of miR-133a-3p as prognostic biomarker in sudden cardiac death, and miR-133a-3p is implicated in the ischemic myocardial injury [12,13]. lncRNA FGD5‑AS1 is indicated to attenuate LPS-caused sepsis by binding to miR-133a-3p to upregulate AQP1 [14]. Substantial evidence has also demonstrated that miR-133a-3p functions as a tumor suppressor in multiple cancers, such as esophageal squamous cell carcinoma, prostate cancer, and gastric cancer [15,16,17]. Moreover, previous studies have revealed that miR-133a-3p is downregulated in CRC tissues and its overexpression inhibits CRC cell proliferation [18]. It is also indicated as a biomarker of CRC [19]. Nevertheless, the findings of the previous study also revealed that SENP1 silencing partially rescued the suppressive effects induced by miR-133a-3p overexpression on CRC cell viability and proliferation, suggesting the existence of other potential mechanisms of miR-133a-3p in CRC, which requires further investigation [18].

Kinetochore scaffold 1 (CASC5, also named KNL1) is reported as an oncogene in lung adenocarcinoma and CRC [20,21]. It inhibits apoptosis and promotes the proliferation of CRC cells [21]. Bioinformatic analysis also reveals that CASC5 is significantly upregulated in the tissues of COAD and rectum adenocarcinoma (READ) patients and CRC patients with high CASC5 expression are predicted with poor overall survival.

In this study, we aimed to investigate the biological functions and regulatory mechanism of AC125257.1 in CRC. We hypothesized that AC125257.1 may affect CRC development via the miR-133a-3p/CASC5 axis. Based on gain- or loss-of-function assays, we explored the effects of AC125257.1 on CRC cell proliferation and apoptosis. The findings of our study may provide new insight into the pathogenesis of CRC.

2 Materials and methods

2.1 Patients and clinical specimens

CRC tissues (n = 36) and adjacent normal tissues (n = 36) were obtained from CRC patients receiving surgery at The First Affiliated Hospital of Nanchang Medical College. Adjacent normal tissues were collected 5 cm away from the cancerous tissues and confirmed by pathological examination. All participants signed the informed consent prior to the study. The information of patients and the correlation between AC125257.1 expression and clinicopathologic characteristics of CRC patients are presented in Table 1.

Table 1

Correlation between AC125257.1 expression and clinicopathologic characteristics of CRC patients

Characteristics Number of patients (n = 36) AC125257.1 expression P value
High (n = 22) Low (n = 14)
Gender 0.419
 Female 15 8 7
 Male 21 14 7
Age (years) 0.592
 <60 11 6 5
 ≥60 25 16 9
Tumor location 0.796
 Colon 20 10 10
 Rectum 16 12 14
Tumor size (cm) 0.755
 <5 14 9 5
 ≥5 22 13 9
TNM stage <0.0001
 I  +  II 16 4 12
 III 20 18 2
Recurrence 0.003
 No 17 6 11
 Yes 19 16 3

  1. Ethics approval and consent to participate: The experiments were approved by the Ethics Committee of The First Affiliated Hospital of Nanchang Medical College. The contents of this study are under full compliance with government policy and the Declaration of Helsinki.

2.2 Bioinformatics analysis

Interactive Analysis of Gene Expression Profiles, abbreviated as GEPIA, was used for RNA expression analysis (http://gepia.cancer-pku.cn/). Meanwhile, it provides customizable options, such as analysis of differential expression between tumor and normal patients, similar gene detection, and survival analysis [22]. The normal/tumor differential analysis and the prognostic value of AC125257.1 referred in our paper were all from GEPIA. Potential miRNAs targeting CASC5 (also named KNL1) were searched on the starBase database (https://starbase.sysu.edu.cn/) under the condition of CLIP-Data ≥ 5, Degradome-Data ≥ 0, pan-Cancer ≥ 10, and programNum ≥ 2. Only miR-133a-3p was screened out and subject to further analysis. lncRNAs possibly bound to miR-133a-3p was predicted on the starBase website under the condition of Degradome-Data ≥ 1.

2.3 Cell culture and transfection

Human colonic epithelial cells (HCoEpiCs, BFN608006386) and four other CRC cell lines from BLUEFBIO (Shanghai, China), including SW480 (BFN60800644), HCT116 (BFN607200665), Caco-2 (BFN60800651), and HCT-8 (BFN60800647), were cultured in flasks coated with Dulbecco’s modified eagle medium [10% (v/v) fetal bovine serum + 1% penicillin–streptomycin solution, Hyclone]. The culture environment was set at 37°C with 5% CO2. For cell transfection, sh-AC125257.1#1/2, sh-NC, miR-133a-3p mimics, NC mimics, and pcDNA3.1/CASC5, were designed by Ribobio Technology (Guangzhou, China). HCT-8 and SW480 were transfected with these vectors using Lipofectamine 2000 (Invitrogen, USA), complied with the product’s protocols.

2.4 Reverse-transcription quantitative polymerase chain reaction (RT-qPCR)

RNAs in CRC cells or tumor tissue were isolated using the RNeasy Mini Kit (Qiagen, Valencia, CA, USA), complied to the product’s protocols. RevertAid First Strand cDNA Synthesis Kit (Thermo Fisher Scientific) was used for reverse transcription. Applied Biosystems™ 7500 Fast Dx Real-Time PCR Instrument was used for qPCR process. The internal controls were U6 and GAPDH. The temperatures for denaturation, annealing, and elongation were set to 95, 60, and 72°C with 40 cycles. The quantitative calculation was performed using 2−ΔΔCT method. Promega (Madison, WI, USA) synthesized all these primer sequences and the primers are shown in Table 2.

Table 2

Primers for RT-qPCR

Primer name Primer sequence
GAPDH forward 5′-TCAAGATCATCAGCAATGCC-3′
GAPDH reverse 5′-CGATACCAAAGTTGTCATGGA-3′
U6 forward 5′-ATACAGAGAAAGTTAGCACGG-3′
U6 reverse 5′-GGAATGCTTCAAAGAGTTGTG-3′
AC125257.1 forward 5′-CGCTCTCCTTCAAGCTCCCG-3′
AC125257.1 reverse 5′-TGGAGAGGCTTCCTGCCCAT-3′
CASC5 forward 5′-ACTATAAAGGTATTCCAGACGG-3′
CASC5 reverse 5′-CAGAAAGCAATGTGTTCATCC-3′
miR-133a-3p forward 5′-TTTGGTCCCCTTCAACCAGCTG-3
miR-133a-3p reverse 5′-GCAGGGTCCGAGGTATTC-3′

2.5 RNA pull-down assay

A total of 1 × 107 cells transfected with biotinylated miR-133a-3p mimic (bio-miR-133a-3p) or bio-NC were lysed. Magnetic RNA-Protein Pull-Down Kit was used for cultivation with magnetic beads. GAPDH was used as a negative control. CASC5 or AC125257.1 expression in precipitated RNA complex was measured by qPCR.

2.6 RNA immunoprecipitation (RIP)

The RIP assay was performed using EZ-Magna RIP™ RNA-Binding Protein Immunoprecipitation Kit (17-701; Millipore), complied with the product’s protocols. A total of 1 × 107 HCT-8 and SW480 cells were lysed and centrifuged at 12,000g for 10 min. Supernatants were then co-incubated with magnetic beads containing anti-IgG (ab172730, 1:100; Abcam) or anti-Ago2 (ab186733, 1:50; Abcam) and then washed with 1,000 μL of RIP wash buffer. The isolated RNA was analyzed by PCR.

2.7 Cell counting kit-8 (CCK-8) assay

HCT-8 and SW480 were cultivated in 96-well plates (4 × 103 cells/well). The corresponding cultivation time was 12, 24, and 48 h at 37°C. The cells were mixed with 10 μL of CCK-8 solution (Dojindo) at 37°C. After 2.5 h, the optical density (OD) value at 450 nm was detected using microplate reader.

2.8 Flow cytometry

The flow cytometry was performed using the Annexin V-FITC/propidium iodide (PI) Apoptosis Detection Kit (Yeasen, Shanghai, China). Cold phosphate-buffered saline (PBS) (Solarbio, Beijing, China) was used for washing. After washing twice with cold PBS buffer, the CRC cells were centrifuged at 4°C and 5 min later and made into 1 × 106 cells/mL suspension with 100 L of 1× binding buffer. After 15 min of complete reaction with 10 μL of PI solution and 5 μL of Annexin V-FITC, the mixture was placed on ice for detection by flow cytometry (BD Biosciences, USA).

2.9 Western blot

The protein of CRC cells was extracted and quantitatively analyzed by the bicinchonininc acid method (Solarbio, Beijing, China). Sodium dodecyl sulfate-polyacrylamide gel electrophoresis (10%) was used for separation. After being transferred to polyvinylidene fluoride membrane (Micropore Company, USA) and sealed with 5% nonfat milk, the mixture was blocked with the tris buffered saline with Tween-20 buffer. After washing with Tween buffer thrice, primary antibodies were added for incubation at 4°C overnight. Then, it was mixed with goat anti-rabbit IgG secondary antibody (1:1,000, ab7090; Abcam, UK) at room temperature. Two hours later, enhanced chemiluminescence reagents (Bio-Rad, Hercules, CA, USA) were used for protein level detection. Primary antibodies were as follows: anti-GAPDH (1:2,500, ab9485), anti-CASC5 (1:1,000, ab70537)), anti-Bcl-2 (1:1,000, ab32124), anti-Bax (1:2,000, ab32503), anti-CDK4 (1:1,000, ab108357), anti-Cyclin A1 (1:1,000, ab270940), and anti-Cyclin D1 (1:1,000, ab16663).

2.10 Animal experiments

BALB/c male nude mice (5 weeks, 20 ± 2 g) were provided by the Vital River (Beijing, China). Mice were randomly divided into the sh-NC and sh-AC125257.1 groups. The cell suspension of HCT116 cells transfected with sh-NC or sh-AC125257.1 (1 × 106 cells/mL) was subcutaneously injected into right axilla of each mouse. Tumor volume growth was monitored weekly by the following formula: volume = width2 × length/2. Mice were sacrificed at day 28, and tumors were obtained and weighed. The animal study has been approved by the Animal Care and Use Committee of The First Affiliated Hospital of Nanchang Medical College.

2.11 Statistics analysis

Data were analyzed using SPSS 19.0 and GraphPad 7.0 and expressed as the mean ± standard deviation. One-way analysis of variance was taken to compare means between three or more groups followed by Dunnett’s post hoc test. Student’s t-test was taken to compare means between two groups. Statistical significance was represented as P < 0.05.

3 Results

3.1 CASC5 was significantly expressed in CRC tissues and cells

From GEPIA database, high expression of CASC5 was found in CRC patients (either with COAD or with rectum adenocarcinoma) (Figure 1a). The overall survival curve showed that patients with high CASC5 level had worse prognosis than those with low level (Figure 1b). RT-qPCR results indicated that the expression of CASC5 was higher in tumor than in adjacent parts (Figure 1c) and higher in CRC cells than in HCoEpiCs (Figure 1d). These results revealed that CASC5 associated with CRC and has bad prognosis.

Figure 1 (a) The distribution of CASC5 in COAD (275 tumor samples and 349 normal samples) and rectum adenocarcinoma (READ, 92 tumor samples and 318 normal samples). Red column represented tumor samples, and gray column represented normal samples. (b) The overall survival curve of patients with low and high CASC5 TPM based on GEPIA database using Log-rank test. (c) Relative CASC5 expression in adjacent and tumor. (d) Relative CASC5 expression in HCoEpiC and four other CRC cell lines. *P < 0.05, **P < 0.01, ***P < 0.001.
Figure 1

(a) The distribution of CASC5 in COAD (275 tumor samples and 349 normal samples) and rectum adenocarcinoma (READ, 92 tumor samples and 318 normal samples). Red column represented tumor samples, and gray column represented normal samples. (b) The overall survival curve of patients with low and high CASC5 TPM based on GEPIA database using Log-rank test. (c) Relative CASC5 expression in adjacent and tumor. (d) Relative CASC5 expression in HCoEpiC and four other CRC cell lines. *P < 0.05, **P < 0.01, ***P < 0.001.

3.2 miR-133a-3p suppressed CASC5 expression through sponging

miRNAs with potential binding site to CASC5 were predicted on the starBase database under the condition of CLIP-Data ≥ 5, Degradome-Data ≥ 0, pan-Cancer ≥ 10, and programNum ≥ 2. The results showed that only miR-133a-3p was screened out. RT-qPCR results showed lowly expressed miR-133a-3p in CRC cells (Figure 2a) and tumor samples (Figure 2b). In SW480 and HCT-8 with miR-133a-3p overexpression, the level of CASC5 expression was significantly downregulated (Figure 2c and d). Western blot results further confirmed this finding (Figure 2e). By using a bio-miR-133a-3p probe, RNA pull-down assay showed that CASC5 has high enrichment in the bio-miR-133a-3p group, demonstrating that CASC5 is targeted by miR-133a-3p (Figure 2f). Moreover, the expression of miR-133a-3p was demonstrated to be negatively correlated with CASC5 expression in CRC patient tissues (Figure 2g).

Figure 2 (a) Relative miR-133a-3p expression in HCoEpiC and four other CRC cell lines. (b) Relative expression of miR-133a-3p in adjacent and tumor. (c) Relative miR-133a-3p expression in SW480 and HCT-8 cell lines transfected with over-miR-133a-3p/miR-NC. (d) Relative CASC5 expression in SW480 and HCT-8 cell lines transfected with over-miR-133a-3p/miR-NC. (e) Western blot results of CASC5 in SW480 and HCT-8 cell lines transfected with over-miR-133a-3p/miR-NC. (f) RNA pull-down results were used to detect the enrichment of CASC5 and GAPDH (negative control) in the complex pulled down by bio-miR-133a-3p or bio-NC. (g) The expression correlation between miR-133a-3p and CASC5 in CRC patient tissues was explored using Pearson correlation analysis. **P < 0.01, ***P < 0.001.
Figure 2

(a) Relative miR-133a-3p expression in HCoEpiC and four other CRC cell lines. (b) Relative expression of miR-133a-3p in adjacent and tumor. (c) Relative miR-133a-3p expression in SW480 and HCT-8 cell lines transfected with over-miR-133a-3p/miR-NC. (d) Relative CASC5 expression in SW480 and HCT-8 cell lines transfected with over-miR-133a-3p/miR-NC. (e) Western blot results of CASC5 in SW480 and HCT-8 cell lines transfected with over-miR-133a-3p/miR-NC. (f) RNA pull-down results were used to detect the enrichment of CASC5 and GAPDH (negative control) in the complex pulled down by bio-miR-133a-3p or bio-NC. (g) The expression correlation between miR-133a-3p and CASC5 in CRC patient tissues was explored using Pearson correlation analysis. **P < 0.01, ***P < 0.001.

3.3 miR-133a-3p reduced CRC cell proliferation and promoted apoptosis while CASC5 partially reversed these effects

By CCK-8 assays, SW480 and HCT-8 transfected with over-miR-133a-3p showed suppressed proliferation, while those transfected with over-miR-133a-3p + CASC5 partially reserved this effect (Figure 3a). As is shown in flow cytometry results, the apoptosis rate of SW480 and HCT-8 transfected with over-miR-133a-3p was remarkably increased, while group transfected with over-miR-133a-3p + CASC5 showed reversed effect (Figure 3b). Further western blot analysis clarified the protein changes (Figure 3c). To be specific, CASC5, BCL2, and CDK4 levels were decreased by overexpressed miR-133a-3p, and BAX level was increased by miR-133a-3p, suggesting the promotive effects of miR-133a-3p on CRC cell apoptosis, further proving the results in Figure 3b. The levels of Cyclin A1 and Cyclin D1 were downregulated, suggesting that overexpressed miR-133a-3p suppressed CRC progression. These effects could all be restored partially by CASC5.

Figure 3 (a) OD value of 450 nm in SW480 and HCT-8 at 0, 12, 24, and 48 h. (b) Flow cytometry results and apoptosis rate of SW480- and HCT-8 transfected with miR-NC, over-miR-133a-3p, and over-miR-133a-3p + CASC5. (c) Western blot results of CASC5, Bcl-2, Bax, CDK4, Cyclin A1, Cyclin D1, and GAPDH in SW480 and HCT-8 transfected with miR-NC, over-miR-133a-3p, and over-miR-133a-3p + CASC5. **P < 0.01, ***P < 0.001 compared with the miR-NC group; ### P < 0.001 compared with the over-miR-133a-3p group.
Figure 3

(a) OD value of 450 nm in SW480 and HCT-8 at 0, 12, 24, and 48 h. (b) Flow cytometry results and apoptosis rate of SW480- and HCT-8 transfected with miR-NC, over-miR-133a-3p, and over-miR-133a-3p + CASC5. (c) Western blot results of CASC5, Bcl-2, Bax, CDK4, Cyclin A1, Cyclin D1, and GAPDH in SW480 and HCT-8 transfected with miR-NC, over-miR-133a-3p, and over-miR-133a-3p + CASC5. **P < 0.01, ***P < 0.001 compared with the miR-NC group; ### P < 0.001 compared with the over-miR-133a-3p group.

3.4 Knockdown of AC125257.1 promoted the expression of miR-133a-3p and suppressed that of CASC5

lncRNAs possibly bound to miR-133a-3p was predicted on the starBase website under the condition of Degradome-Data ≥ 1. Only AC125257.1 was selected under this condition. AC125257.1 showed abundant expression in CRC cells and tumor by RT-qPCR (Figure 4a and b). RNA pull-down assay proved that AC125257.1 was remarkably enriched by the bio-miR-133a-3p probe, indicating that miR-133a-3p is the target miRNA of AC125257.1 (Figure 4c). As shown in Figure 4d–f, the knockdown of AC125257.1 significantly elevated miR-133a-3p expression and suppressed CASC5 expression, which is consistent with the finding in Figure 2c and d. Western blot results further confirmed this finding (Figure 4g). Furthermore, RIP assay validated that compared to the control group (anti-IgG), AC125257.1 and miR-133a-3p were noticeably enriched in microribonucleoproteins with Ago2, suggesting that AC125257.1 acted as the ceRNA for miR-133a-3p and formed an RNA-induced silencing complex in CRC cells (Figure 4h). The expression of CASC5 and AC125257.1 showed positive correlation in CRC patient tissues, while that of miR-133a-3p and AC125257.1 exhibited negative correlation according to Pearson correlation analysis (Figure 4i–g).

Figure 4 (a) Relative AC125257.1 expression in HCoEpiC and four other CRC cell lines. (b) Relative AC125257.1 expression in adjacent and tumor. (c) RNA pull-down results of AC125257.1 using bio-miR-133a-3p or bio-NC. (d) Relative AC125257.1 expression in SW480 and HCT-8 cell lines transfected with sh-NC/sh-AC125257.1. (e) Relative miR-133a-3p expression in SW480 and HCT-8 cell lines transfected with sh-NC/sh-AC125257.1. (f) Relative CASC5 expression in SW480 and HCT-8 cell lines transfected with sh-NC/sh-AC125257.1. (g) Western blot results of CASC5 and GAPDH in SW480 and HCT-8 cell lines transfected with sh-NC/sh-AC125257.1. (h) AC125257.1 and miR-133a-3p levels detected by RIP. (i) Pearson correlation analysis was conducted to examine the expression correlation between CASC5 and AC125257.1. (j) The expression correlation between AC125257.1 and miR-133a-3p in CRC patient tissues. *P < 0.05, **P < 0.01, ***P < 0.001.
Figure 4

(a) Relative AC125257.1 expression in HCoEpiC and four other CRC cell lines. (b) Relative AC125257.1 expression in adjacent and tumor. (c) RNA pull-down results of AC125257.1 using bio-miR-133a-3p or bio-NC. (d) Relative AC125257.1 expression in SW480 and HCT-8 cell lines transfected with sh-NC/sh-AC125257.1. (e) Relative miR-133a-3p expression in SW480 and HCT-8 cell lines transfected with sh-NC/sh-AC125257.1. (f) Relative CASC5 expression in SW480 and HCT-8 cell lines transfected with sh-NC/sh-AC125257.1. (g) Western blot results of CASC5 and GAPDH in SW480 and HCT-8 cell lines transfected with sh-NC/sh-AC125257.1. (h) AC125257.1 and miR-133a-3p levels detected by RIP. (i) Pearson correlation analysis was conducted to examine the expression correlation between CASC5 and AC125257.1. (j) The expression correlation between AC125257.1 and miR-133a-3p in CRC patient tissues. *P < 0.05, **P < 0.01, ***P < 0.001.

3.5 Knockdown of AC125257.1 reduced CRC cell proliferation and promoted apoptosis while CASC5 partially reversed these effects

By CCK-8 assay, SW480 and HCT-8 transfected with sh-AC125257.1 showed suppressed viability, while those transfected with sh-AC125257.1-1/-2 + CASC5 partially reserved this effect (Figure 5a). As is shown in flow cytometry results, the apoptosis rate of SW480 and HCT-8 transfected with sh-AC125257.1 was remarkably increased, while group transfected with sh-AC125257.1-1/-2 + CASC5 showed reversed effect (Figure 5b). Further western blot analysis clarified the protein changes (Figure 5c). To be specific, CASC5, BCL2, and CDK4 levels were decreased by knockdown of AC125257.1, and BAX level was increased by it, suggesting that CRC cell apoptosis was inhibited by AC125257.1. The expression of Cyclin A1 and Cyclin D1 was downregulated, suggesting that the knockdown of AC125257.1 suppressed CRC progression. These effects could all be reversed partially by CASC5.

Figure 5 (a) OD value of 450 nm in SW480- and HCT-8-transfected with sh-NC, sh-AC125257.1, and sh-AC125257.1 + CACS5 at 0, 12, 24, and 48 h. (b) Flow cytometry results and apoptosis rate of SW480 and HCT-8 transfected with sh-NC, sh-AC125257.1, and sh-AC125257.1 + CACS5. (c) WB results of CASC5, Bcl-2, Bax, CDK4, Cyclin A1, Cyclin D1, and GAPDH in SW480- and HCT-8-transfected with sh-NC, sh-AC125257.1, and sh-AC125257.1 + CACS5. **P < 0.01, ***P < 0.001 compared with the sh-NC group; # P < 0.05, ## P < 0.01 compared with the sh-AC125257.1-1/-2 group.
Figure 5

(a) OD value of 450 nm in SW480- and HCT-8-transfected with sh-NC, sh-AC125257.1, and sh-AC125257.1 + CACS5 at 0, 12, 24, and 48 h. (b) Flow cytometry results and apoptosis rate of SW480 and HCT-8 transfected with sh-NC, sh-AC125257.1, and sh-AC125257.1 + CACS5. (c) WB results of CASC5, Bcl-2, Bax, CDK4, Cyclin A1, Cyclin D1, and GAPDH in SW480- and HCT-8-transfected with sh-NC, sh-AC125257.1, and sh-AC125257.1 + CACS5. **P < 0.01, ***P < 0.001 compared with the sh-NC group; # P < 0.05, ## P < 0.01 compared with the sh-AC125257.1-1/-2 group.

3.6 Knockdown of AC125257.1 suppressed CRC tumor growth in vivo

Xenograft tumor-bearing mouse models were established to examine the function of AC125257.1 on CRC tumorigenesis. The results indicated that AC125257.1 knockdown significantly decreased the tumor growth rate, and mouse tumor volume and weight was significantly smaller in the sh-AC125257.1-1 group compared with the control group (Figure 6a and b). Moreover, we examined the expression of miR-133a-3p and CASC5 in mouse tumor tissues. As revealed by RT-qPCR analysis, the expression of miR-133a-3p was significantly increased while the CASC5 levels showed a significant decrease in the sh-AC125257.1-1 group compared with the control group (Figure 6c and d).

Figure 6 (a) Tumor volume in each group was measured on days 7, 14, 21, and 28. (b) Mouse tumor weight in the sh-NC and sh-AC125257.1-1 groups. (c) RT-qPCR was used to detect the expression of miR-133a-3p in mouse tumor tissues in each group. (d) The expression of CASC5 was measured using RT-qPCR mouse tumor tissues in each group. **P < 0.01, ***P < 0.001.
Figure 6

(a) Tumor volume in each group was measured on days 7, 14, 21, and 28. (b) Mouse tumor weight in the sh-NC and sh-AC125257.1-1 groups. (c) RT-qPCR was used to detect the expression of miR-133a-3p in mouse tumor tissues in each group. (d) The expression of CASC5 was measured using RT-qPCR mouse tumor tissues in each group. **P < 0.01, ***P < 0.001.

4 Discussion

In the present study, we found that lncRNA AC125257.1 was upregulated in CRC tissues and cells, and AC125257.1 silencing inhibited the proliferation and promoted the apoptosis of CRC cells by binding with miR-133a-3p to upregulate CASC5. AC125257.1 silencing also showed suppressive effects on CRC tumor growth in vivo. These findings indicated the potential of AC125257.1 as a biomarker and therapeutic target for the treatment of CRC.

Previous study has shown that CASC5 can promote CRC malignancy through m6A methylation [23], suggesting that CASC5 plays an oncogenic role in CRC. Besides CASC5, other potential targets of miR-133a-3p, such as UBA2 and AQP1, are revealed to be implicated in CRC progression. For example, miR-133a has been reported to inhibit the CRC development and metastasis by regulating UBA2 [24]. miR-133a-3p suppresses CRC cell proliferation, migration, and invasion by targeting AQP1 [25]. In this study, we confirmed that CASC5 was abundant in CRC cells and tumor tissues with poor prognosis. Several reports illustrated that miR-133a-3p suppresses CRC development, which is consistent with our findings [25,26,27]. The inner interaction between miR-133a-3p and CASC5 was analyzed by the RNA pull-down assay. We found that CASC5 is targeted by miR-133a-3p. Meanwhile, CASC5 restored the inhibitory effect of miR-133a-3p in CRC cell lines.

As with the data from the TCGA database, we also found that AC125257.1 had high expression in CRC samples (cells and tumor tissues). High expression of AC125257.1 is associated with poor prognosis in CRC patients. lncRNA with multiple cellular functions are closely linked with human cancer progression [28] and has emerged to have the potential as therapeutic target for CRC [29]. The lncRNA-mediated ceRNA regulatory network is an important pathogenic mechanism of CRC [30]. Yu et al. claimed that CXCL12/CXCR4 sponging miR-133a-3p promoted CRC progression [31]. To explore the novel potential ceRNA regulatory network associated with miR-133a-3p, we verified that AC125257.1 can sponge miR-133a-3p by RIP and RNA pull-down experiments. Furthermore, the knockdown of AC125257.1 promoted miR-133a-3p expression and suppressed CASC5 expression, thereby inhibiting CRC cell viability, revealing that AC125257.1 regulates CRC progression by mediating the miR-133a-3p/CASC5 axis. Besides miR-133a-3p, other potential miRNAs binding to AC125257.1, such as miR-944 and miR-133b, are reported to affect CRC development. For example, miR-944 is revealed to suppress the proliferation, migration, and invasion of CRC cells by targeting GATA6 in CRC [32]. miR-133b is reported to reduce the stemness and chemoresistance in colorectal spheroids by regulating DOT1L [33]. The findings of our study may contribute to understanding the regulatory mechanism of CRC.

However, there remained limitations of our study. First, a further expansion of CRC sample size is needed to obtain a more general data. Second, starBase predicted the presence of other miRNA and genes targeted by AC125257.1 and miR-133a-3p, suggesting other pathogenic mechanisms of CRC.

Taken together, these results suggested that knockdown of AC125257.1 inhibits CRC development in vitro and in vivo via miR-133a-3p/CASC5 axis. Our study deepened our understanding of the pathogenesis of CRC. The study also suggested that high levels of CASC5 may be a marker affecting overall survival in CRC patients.

Acknowledgments

We thank technical support from The First Affiliated Hospital of Nanchang Medical College.

  1. Funding information: None.

  2. Author contributions: Chuanwen Liao performed experiments and wrote the draft manuscript. Chuanwen Liao, Zihan Zheng, Junye Liu, Jian Li, and Rui Li performed experiments, analyzed data, and conducted validation. Shuqin Hu supervised this project and revised editing. All the authors have read and approved the article.

  3. Conflict of interest: The authors declare that they have no competing interest.

  4. Data availability statement: Datasets during and/or analyzed during the current study available from the corresponding author on reasonable request.

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Received: 2022-08-18
Revised: 2022-12-05
Accepted: 2022-12-10
Published Online: 2023-03-27

© 2023 the author(s), published by De Gruyter

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

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  217. miR-192 inhibits the activation of hepatic stellate cells by targeting Rictor
  218. Diagnostic and prognostic value of MR-pro ADM, procalcitonin, and copeptin in sepsis
  219. Review Articles
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  237. Liver abscess complicated with multiple organ invasive infection caused by hematogenous disseminated hypervirulent Klebsiella pneumoniae: A case report
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  247. Rapid Communication
  248. Impact of COVID-19 lockdown on glycemic levels during pregnancy: A retrospective analysis
  249. Erratum
  250. Erratum to “Inhibition of miR-21 improves pulmonary vascular responses in bronchopulmonary dysplasia by targeting the DDAH1/ADMA/NO pathway”
  251. Erratum to: “Fer exacerbates renal fibrosis and can be targeted by miR-29c-3p”
  252. Retraction
  253. Retraction of “Study to compare the effect of casirivimab and imdevimab, remdesivir, and favipiravir on progression and multi-organ function of hospitalized COVID-19 patients”
  254. Retraction of “circ_0062491 alleviates periodontitis via the miR-142-5p/IGF1 axis”
  255. Retraction of “miR-223-3p alleviates TGF-β-induced epithelial-mesenchymal transition and extracellular matrix deposition by targeting SP3 in endometrial epithelial cells”
  256. Retraction of “SLCO4A1-AS1 mediates pancreatic cancer development via miR-4673/KIF21B axis”
  257. Retraction of “circRNA_0001679/miR-338-3p/DUSP16 axis aggravates acute lung injury”
  258. Retraction of “lncRNA ACTA2-AS1 inhibits malignant phenotypes of gastric cancer cells”
  259. Special issue Linking Pathobiological Mechanisms to Clinical Application for cardiovascular diseases
  260. Effect of cardiac rehabilitation therapy on depressed patients with cardiac insufficiency after cardiac surgery
  261. Special issue The evolving saga of RNAs from bench to bedside - Part I
  262. FBLIM1 mRNA is a novel prognostic biomarker and is associated with immune infiltrates in glioma
  263. Special Issue Computational Intelligence Methodologies Meets Recurrent Cancers - Part III
  264. Development of a machine learning-based signature utilizing inflammatory response genes for predicting prognosis and immune microenvironment in ovarian cancer
https://doi.org/10.1515/med-2023-0631
Keywords for this article
CRC; AC125257.1; miR-133a-3p; CASC5; cell signaling
Creative Commons
BY 4.0

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  209. Clinical features and management of lymphoepithelial cyst
  210. Serum VEGF, high-sensitivity CRP, and cystatin-C assist in the diagnosis of type 2 diabetic retinopathy complicated with hyperuricemia
  211. ENPP1 ameliorates vascular calcification via inhibiting the osteogenic transformation of VSMCs and generating PPi
  212. Significance of monitoring the levels of thyroid hormone antibodies and glucose and lipid metabolism antibodies in patients suffer from type 2 diabetes
  213. The causal relationship between immune cells and different kidney diseases: A Mendelian randomization study
  214. Interleukin 33, soluble suppression of tumorigenicity 2, interleukin 27, and galectin 3 as predictors for outcome in patients admitted to intensive care units
  215. Identification of diagnostic immune-related gene biomarkers for predicting heart failure after acute myocardial infarction
  216. Long-term administration of probiotics prevents gastrointestinal mucosal barrier dysfunction in septic mice partly by upregulating the 5-HT degradation pathway
  217. miR-192 inhibits the activation of hepatic stellate cells by targeting Rictor
  218. Diagnostic and prognostic value of MR-pro ADM, procalcitonin, and copeptin in sepsis
  219. Review Articles
  220. Prenatal diagnosis of fetal defects and its implications on the delivery mode
  221. Electromagnetic fields exposure on fetal and childhood abnormalities: Systematic review and meta-analysis
  222. Characteristics of antibiotic resistance mechanisms and genes of Klebsiella pneumoniae
  223. Saddle pulmonary embolism in the setting of COVID-19 infection: A systematic review of case reports and case series
  224. Vitamin C and epigenetics: A short physiological overview
  225. Ebselen: A promising therapy protecting cardiomyocytes from excess iron in iron-overloaded thalassemia patients
  226. Aspirin versus LMWH for VTE prophylaxis after orthopedic surgery
  227. Mechanism of rhubarb in the treatment of hyperlipidemia: A recent review
  228. Surgical management and outcomes of traumatic global brachial plexus injury: A concise review and our center approach
  229. The progress of autoimmune hepatitis research and future challenges
  230. METTL16 in human diseases: What should we do next?
  231. New insights into the prevention of ureteral stents encrustation
  232. VISTA as a prospective immune checkpoint in gynecological malignant tumors: A review of the literature
  233. Case Reports
  234. Mycobacterium xenopi infection of the kidney and lymph nodes: A case report
  235. Genetic mutation of SLC6A20 (c.1072T > C) in a family with nephrolithiasis: A case report
  236. Chronic hepatitis B complicated with secondary hemochromatosis was cured clinically: A case report
  237. Liver abscess complicated with multiple organ invasive infection caused by hematogenous disseminated hypervirulent Klebsiella pneumoniae: A case report
  238. Urokinase-based lock solutions for catheter salvage: A case of an upcoming kidney transplant recipient
  239. Two case reports of maturity-onset diabetes of the young type 3 caused by the hepatocyte nuclear factor 1α gene mutation
  240. Immune checkpoint inhibitor-related pancreatitis: What is known and what is not
  241. Does total hip arthroplasty result in intercostal nerve injury? A case report and literature review
  242. Clinicopathological characteristics and diagnosis of hepatic sinusoidal obstruction syndrome caused by Tusanqi – Case report and literature review
  243. Synchronous triple primary gastrointestinal malignant tumors treated with laparoscopic surgery: A case report
  244. CT-guided percutaneous microwave ablation combined with bone cement injection for the treatment of transverse metastases: A case report
  245. Malignant hyperthermia: Report on a successful rescue of a case with the highest temperature of 44.2°C
  246. Anesthetic management of fetal pulmonary valvuloplasty: A case report
  247. Rapid Communication
  248. Impact of COVID-19 lockdown on glycemic levels during pregnancy: A retrospective analysis
  249. Erratum
  250. Erratum to “Inhibition of miR-21 improves pulmonary vascular responses in bronchopulmonary dysplasia by targeting the DDAH1/ADMA/NO pathway”
  251. Erratum to: “Fer exacerbates renal fibrosis and can be targeted by miR-29c-3p”
  252. Retraction
  253. Retraction of “Study to compare the effect of casirivimab and imdevimab, remdesivir, and favipiravir on progression and multi-organ function of hospitalized COVID-19 patients”
  254. Retraction of “circ_0062491 alleviates periodontitis via the miR-142-5p/IGF1 axis”
  255. Retraction of “miR-223-3p alleviates TGF-β-induced epithelial-mesenchymal transition and extracellular matrix deposition by targeting SP3 in endometrial epithelial cells”
  256. Retraction of “SLCO4A1-AS1 mediates pancreatic cancer development via miR-4673/KIF21B axis”
  257. Retraction of “circRNA_0001679/miR-338-3p/DUSP16 axis aggravates acute lung injury”
  258. Retraction of “lncRNA ACTA2-AS1 inhibits malignant phenotypes of gastric cancer cells”
  259. Special issue Linking Pathobiological Mechanisms to Clinical Application for cardiovascular diseases
  260. Effect of cardiac rehabilitation therapy on depressed patients with cardiac insufficiency after cardiac surgery
  261. Special issue The evolving saga of RNAs from bench to bedside - Part I
  262. FBLIM1 mRNA is a novel prognostic biomarker and is associated with immune infiltrates in glioma
  263. Special Issue Computational Intelligence Methodologies Meets Recurrent Cancers - Part III
  264. Development of a machine learning-based signature utilizing inflammatory response genes for predicting prognosis and immune microenvironment in ovarian cancer
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