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Article Open Access

Knockdown of LINC00467 inhibits gastric cancer progression by modulating the sequestration of miR‑141‑3p

  • Authors:
    • Hui Ju
    • Yi Feng
    • Xiaojing Mu
    • Weitai He
    • Guifang He
    • Ben Tian
    • Duo Cai
    • Changchang Liu
    • Yu Song
    • Hao Chen
    • Shihai Liu

  • View Affiliations / Copyright

    Affiliations: Department of Gastroenterology, The Affiliated Hospital of Qingdao University, Qingdao, Shandong 266500, P.R. China, Department of Rehabilitation, The Affiliated Hospital of Qingdao University, Qingdao, Shandong 266500, P.R. China, Department of Healthcare, The Affiliated Hospital of Qingdao University, Qingdao, Shandong 266500, P.R. China, The Key Laboratory of Medicinal Resources and Natural Pharmaceutical Chemistry, The Ministry of Education, College of Life Sciences, Shaanxi Normal University, Xian, Shaanxi 710000, P.R. China, Medical Animal Lab, Medical Research Center, The Affiliated Hospital of Qingdao University, Qingdao, Shandong 266500, P.R. China, Department of Neurosurgery Intensive Medicine, The First Affiliated Hospital of Baotou Medical College, Baotou, Inner Mongolia Autonomous Region 014060, P.R. China, Key Laboratory of Biomedical Information Engineering of Ministry of Education, Biomedical Informatics and Genomics Center, School of Life Science and Technology, Xi'an Jiaotong University, Xi'an, Shaanxi 710049, P.R. China
    Copyright: © Ju et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
  • Article Number: 459
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    Published online on: July 24, 2025
       https://doi.org/10.3892/ol.2025.15205
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Abstract

Gastric cancer (GC) is one of the most common malignancies globally, with notable morbidity and mortality rates. Despite advances in surgical techniques and adjuvant therapies, recurrence and metastasis remain major challenges, highlighting the need for novel biomarkers and therapeutic targets. Long non‑coding RNAs (lncRNAs) have emerged as key regulators in various types of cancer, including GC, which can influence tumor progression through diverse mechanisms. LINC00467, in particular, has been implicated in non‑small cell lung cancer, hepatocellular carcinoma and colorectal cancer, but the role of LINC00467 in GC remains poorly understood. The present study aimed to elucidate the role of LINC00467 in GC progression by investigating its expression patterns, functional impact on cellular behaviors and underlying molecular mechanisms. The expression levels of LINC00467 were evaluated in the GEPIA database of human gastric cancer samples, which demonstrated LINC00467 upregulation in 60 tumor tissue samples from patients with GC compared with that of paired para‑cancerous control tissues. Functionally, LINC00467 promoted glycolysis in GC cells and enhanced their proliferative, migratory and invasive activities. From a mechanistic perspective, LINC00467 was able to bind to microRNA (miR)‑141‑3p in GC cells and a negative correlation between miR‑141‑3p and LINC00467 expression was observed in GC tissue samples. Inhibition of miR‑141‑3p partially reversed the effects of LINC00467 knockdown on GC cell malignancy and LINC00467 was further found to control the expression of the miR‑141‑3p target gene dihydropyriminidase‑like 3 (DPYSL3) in GC cells. Furthermore, lactate accumulation from glycolysis activated the AKT signaling pathway to promote the transcriptional expression of LINC00467 in GC cells and led to persistent glycolysis and GC cell invasion. The present study findings suggested that LINC00467 potentially controls GC progression via regulation of the miR‑141‑3p/DPYSL3 pathway. 
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Figure 1

LINC00467 is upregulated in GC tissues and associates with GC progression. (A) LINC00467 levels in STAD (n=408) and normal tissue samples (n=211) in the GEPIA database. (B) Relative LINC00467 levels in 60 pairs of GC tumor tissue and para-cancerous samples. (C) Patient survival percentage (n=60) was assessed using Kaplan-Meier curves and log-rank tests. Lower LINC00467 expression (n=30) was represented in blue and higher LINC00467 expression (n=30) was represented in red. (D) Analysis of DFS in patients with GC based on relative LINC00467 expression levels. Lower expression (n=30) was represented in blue and higher expression (n=30) was represented in red. (E) Expression levels of LINC00467 across different T stages (T1-T4) and in normal tissues. (F) Relative LINC00467 expression levels were assessed in AGS, HGC27 and MKN45 human GC cells and in GES-1 control cells. *P<0.05; **P<0.01; ***P<0.001. GC, gastric cancer; STAD, stomach adenocarcinoma; GEPIA, Gene Expression Profiling Interactive Analysis; DFS, disease-free survival.

Figure 2

Knockdown of LINC00467 suppresses GC cell proliferation and invasion in vitro and in vivo. HGC27 cells exhibited (A) reduced LINC00467 expression following si-LINC00467 transfection and led to reduced proliferation demonstrated by (B) RTCA and (C) colony formation assays. (D) Si-LINC00467 transfection suppressed EdU uptake by HGC27 cells (scale bar, 100 µm). (E) Transfection of HGC27 cells with si-LINC00467 was associated with reduced migration in a wound healing assay and (F) reduced migration and invasion in Transwell assays compared with si-NC transfection. (G) Tumor volumes were assessed every other day in nude mice injected with HGC27 cells that had been transduced with sh-LINC00467 or sh-NC, demonstrating that LINC00467 knockdown was associated with reduced tumor growth. (H) Quantification of tumor weights (g). (I) Representative images of livers from mice in the two treatment groups (scale bar, 100 µm), with (J) corresponding quantification of the numbers of metastatic nodules. Data are presented as mean ± SD. **P<0.01 vs. si-NC; *P<0.05 vs. sh-NC; ##P<0.01 vs. sh-NC. GC, gastric cancer; RTCA, real-time cell analysis; EdU, 5-Ethynyl-2′-deoxyuridine; NC, negative control; si-NC, small interfering RNA-NC; sh-NC, short hairpin RNA-NC.

Figure 3

LINC00467 promotes glycolysis in GC cells. (A) Changes in relative glucose consumption, (B) ATP levels and (C) lactate production in MKN45 and HGC27 cells after LINC00467 knockdown. Changes in ECAR and OCR levels after LINC00467 knockdown in MKN45 and HGC27 cells. Effects of LINC00467 on glycolysis in (D) MKN45 and (E) HGC27 cells were assessed by ECAR following LINC00467 knockdown. ECAR assay and quantification of (D, right) MKN45 and (E, right) HGC27 cells; OCR assay and quantification of (F) MKN45 and (G) HGC27 cells transfected with LINC00467 knockdown. Quantifications of the OCR results of (F, right) MKN45 and (G, right) HGC27 cells, demonstrated basal respiration, ATP production, maximal respiration and spare capacity. **P<0.01. GC, gastric cancer; ECAR, extracellular acidification rate; OCR, oxygen consumption rate; si-NC, small interfering RNA-negative control; 2-DG, 2-deoxyglucose; FCCP, p-trifluoromethoxy carbonyl cyanide phenylhydrazone; Rot/AA, rotenone and antimycin A.

Figure 4

miR-141-3p is a LINC00467 target in GC cells. (A) Relative LINC00467 expression percentage in nuclear and cytoplasmic compartments was evaluated using U6 and GAPDH as respective nuclear and cytoplasmic normalization controls in AGS and HGC27 cell lines. (B) FISH was used to assess LINC00467 localization in GC cells and ImageJ was used to quantify confocal images (scale bar, 10 mm). (C) Relative miR-141-3p expression levels in control and GC cell lines (AGS, MKN45 and HGC27). (D) Expression levels of LINC00467 and GAPDH mRNA after streptavidin capture were measured in GC cells transfected with biotinylated miR-141-3p-WT or -Mut. (E) MKN45 and (F) HGC27 cells were transfected with miR-141-3p-WT or -Mut. (G) Representative FISH images demonstrated the co-localization of LINC00467 and miR-141-3p (scale bar, 31 µm). (H) Putative miR-141-3p-binding sites within the LINC00467 sequence, with corresponding schematics of the WT and Mut luciferase reporter vectors. (I) Relative miR-141-3p expression was assessed in 60 GC and normal para-cancerous tissue samples. **P<0.01. (J) The relationship between LINC00467 and miR-141-3p was assessed via Spearman correlation analyses in 60 GC samples. r=−0.2951; P<0.05. WT, wild-type; Mut, mutant; AGO2, argonaute 2; miR-141-3p, microRNA-141-3p; FISH, fluorescence in situ hybridization.

Figure 5

LINC00467 and miR-141-3p regulated one another. Relative miR-141-3p expression levels were assessed following transfection with an miR-141-3p mimic or control miR-NC in (A) MKN45 and (B) HGC27 cells. (C) MKN45 cells were co-transfected with WT or Mut LINC00467 vectors along with miR-141-3p mimics or miR-NC, after which luciferase activity was assessed. (D) Knockdown of LINC00467 significantly increased miR-141-3p expression in GC cells. (E) Transfection of HGC27 cells with the miR-141-3p inhibitor resulted in LINC00467 upregulation. (F) Transfection of MKN45 cells with miR-141-3p mimics resulted in LINC00467 downregulation. **P<0.01. miR-141-3p, microRNA-141-3p; miR-NC, microRNA negative control; WT, wild-type; Mut, mutant; GC, gastric cancer.

Figure 6

The impact of LINC00467 knockdown on GC cell malignancy was mediated by miR-141-3p. HGC27 cells were transfected with si-LINC00467 and miR-141-3p inhibitors or corresponding control constructs, after which (A) RTCA and (B) colony formation assays demonstrated that inhibition of miR-141-3p reversed the effects of LINC00467 knockdown on proliferation. (C) Transwell assays demonstrated that miR-141-3p inhibition reversed the effects of LINC00467 knockdown on GC cell migration and invasion. **P<0.01 vs. miR-NC. ns, not significant; miR-141-3p, microRNA-141-3p; RTCA, real-time cell analysis; miR-NC, microRNA negative control; GC, gastric cancer.

Figure 7

DPYSL3, a miR-141-3p target, was indirectly controlled by LINC00467. (A) WT and Mut DPYSL3 3′-UTR sequences. (B) Luciferase reporter assays were used to assess interactions between miR-141-3p interactions with the DPYSL3 3′-UTR, following transfection of MKN45 cells with the miR-141-3p mimics and luciferase reporter vectors containing the WT or Mut DPYSL3 3′-UTR. (C) Relative DPYSL3 mRNA expression levels in HGC27 cells was reduced following LINC00467 knockdown. LINC00467 knockdown in HGC27 cells reduced DPYSL3 protein expression levels (D). Effects of miR-141-3p overexpression and knockdown on DPYSL3 (E) mRNA and (F) protein expression levels, in HGC27 cells. (G) Relationship between DPYSL3 and AKT, Myc and GLUT1 associated with the AKT signaling pathway was explored by Western blotting analysis. **P<0.01, vs. miR-NC. PGK, phosphoglycerate kinase; GLUT1, glucose transporter 1; HK2, hexokinase 2; LDHA/C, lactate dehydrogenase A/C isoforms; WT, wild-type; Mut, mutant; NC, negative control; si-NC, small interfering RNA-NC; miR-141-3p, microRNA-141-3p; DPYSL3, dihydropyriminidase-like 3; miR-NC, microRNA-NC.

Figure 8

LINC00467 suppressed GC cell proliferation, migration and invasion through the LINC00467/miR-141-3p/DPYSL3 axis. Relative mRNA and protein expression levels of DPYSL3 in (A) MKN45 and (B) AGS cells transfected with miR-141-3p mimics and inhibitors, si-NC, si-LINC00467, or LINC00467, using qPCR and Western blotting, respectively. (C) Colony formation assays were used to assess proliferation in MKN45 and AGS cells transfected with miR-141-3p mimics and inhibitors, si-NC, si-LINC00467, or LINC00467. (D) Cell migration and (E) invasion was assessed using Transwell assays in MKN45 and AGS cells, respectively, following transfection with the miR-141-3p mimics and inhibitors, si-NC, si-LINC00467 and OV-LINC00467 (scale bar, 100 µm). Data were indicated as mean ± SD. **P<0.01. GC, gastric cancer; miR-141-3p, microRNA-141-3p; DPYSL3, dihydropyriminidase-like 3; si-NC, small interfering RNA-negative control.

Figure 9

Molecular mechanism associated with the effects of LINC00467 on GC progression via regulation of miR-141-3p and DPYSL3. LINC00467 promoted glycolysis in GC cells and enhanced tumor cell proliferation, migration and invasion. LINC00467 specifically competed with miR-141-3p and downregulation of LINC00467 could upregulate the expression levels of miR-141-3p and downregulate DPYSL3 expression levels, and thus regulate aerobic glycolysis, inhibit proliferation, migration and invasion in GC cells. GC, gastric cancer; miR-141-3p, microRNA-141-3p; DPYSL3, dihydropyriminidase-like 3.
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Copy and paste a formatted citation
Spandidos Publications style
Ju H, Feng Y, Mu X, He W, He G, Tian B, Cai D, Liu C, Song Y, Chen H, Chen H, et al: Knockdown of LINC00467 inhibits gastric cancer progression by modulating the sequestration of miR‑141‑3p. Oncol Lett 30: 459, 2025.
APA
Ju, H., Feng, Y., Mu, X., He, W., He, G., Tian, B. ... Liu, S. (2025). Knockdown of LINC00467 inhibits gastric cancer progression by modulating the sequestration of miR‑141‑3p. Oncology Letters, 30, 459. https://doi.org/10.3892/ol.2025.15205
MLA
Ju, H., Feng, Y., Mu, X., He, W., He, G., Tian, B., Cai, D., Liu, C., Song, Y., Chen, H., Liu, S."Knockdown of LINC00467 inhibits gastric cancer progression by modulating the sequestration of miR‑141‑3p". Oncology Letters 30.4 (2025): 459.
Chicago
Ju, H., Feng, Y., Mu, X., He, W., He, G., Tian, B., Cai, D., Liu, C., Song, Y., Chen, H., Liu, S."Knockdown of LINC00467 inhibits gastric cancer progression by modulating the sequestration of miR‑141‑3p". Oncology Letters 30, no. 4 (2025): 459. https://doi.org/10.3892/ol.2025.15205
Copy and paste a formatted citation
x
Spandidos Publications style
Ju H, Feng Y, Mu X, He W, He G, Tian B, Cai D, Liu C, Song Y, Chen H, Chen H, et al: Knockdown of LINC00467 inhibits gastric cancer progression by modulating the sequestration of miR‑141‑3p. Oncol Lett 30: 459, 2025.
APA
Ju, H., Feng, Y., Mu, X., He, W., He, G., Tian, B. ... Liu, S. (2025). Knockdown of LINC00467 inhibits gastric cancer progression by modulating the sequestration of miR‑141‑3p. Oncology Letters, 30, 459. https://doi.org/10.3892/ol.2025.15205
MLA
Ju, H., Feng, Y., Mu, X., He, W., He, G., Tian, B., Cai, D., Liu, C., Song, Y., Chen, H., Liu, S."Knockdown of LINC00467 inhibits gastric cancer progression by modulating the sequestration of miR‑141‑3p". Oncology Letters 30.4 (2025): 459.
Chicago
Ju, H., Feng, Y., Mu, X., He, W., He, G., Tian, B., Cai, D., Liu, C., Song, Y., Chen, H., Liu, S."Knockdown of LINC00467 inhibits gastric cancer progression by modulating the sequestration of miR‑141‑3p". Oncology Letters 30, no. 4 (2025): 459. https://doi.org/10.3892/ol.2025.15205
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