Eugenol inhibits NEAT1 as a ceRNA in pre-cancerous breast lesions

Objective: Eugenol (EU) from cloves is highly effective against different tumors. The long noncoding ribonucleic acids (lncRNAs), which play a role of competing endogenous RNAs (ceRNAs), suppress microRNAs (miRNAs) involved in post-transcriptional regulatory networks. The present work focused on ana...

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Main Authors: Yusheng Liu, Guijuan Zhang, Yi Ma, Min Ma, Xuefeng Jiang
Format: Article
Language:English
Published: Elsevier 2025-01-01
Series:Heliyon
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Online Access:http://www.sciencedirect.com/science/article/pii/S2405844024173847
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author Yusheng Liu
Guijuan Zhang
Yi Ma
Min Ma
Xuefeng Jiang
author_facet Yusheng Liu
Guijuan Zhang
Yi Ma
Min Ma
Xuefeng Jiang
author_sort Yusheng Liu
collection DOAJ
description Objective: Eugenol (EU) from cloves is highly effective against different tumors. The long noncoding ribonucleic acids (lncRNAs), which play a role of competing endogenous RNAs (ceRNAs), suppress microRNAs (miRNAs) involved in post-transcriptional regulatory networks. The present work focused on analyzing how EU affected pre-cancerous breast lesions (PBL). Methods: Initially, the gene expression profiles of patients (n = 880) in the National Center for Biotechnology Information (NCBI) database were analyzed. Further, we established a lncRNA-miRNA-mRNA ceRNA network through bioinformatics analysis and investigated mechanistic roles of lncRNAs as ceRNAs and the anti-tumor effect of EU using MCF-10AT cells in vitro as well as PBL model rats in vivo. Besides, Nuclear Paraspeckle Assembly Transcript 1 (NEAT1), miR-383-5p, miR-9-5p, matrix metalloproteinase-9 (MMP-9), and vascular endothelial growth factor-A (VEGF-A) expression was examined through quantitative reverse transcription polymerase chain reaction (RT-qPCR), Western blotting, and immunohistochemical staining analyses. Results: There were altogether 1162 mRNAs, 81 miRNAs, and 26 lncRNAs recognized as trend genes in breast cancer (BC) and pre-cancerous BC (pBC), constructing the ceRNA network using 3 lncRNAs, 3 miRNAs, and 38 mRNAs. It was observed that NEAT1, miR-383-5p, miR-9-5p, VEGF-A, and MMP-9 were downregulated in breast tumor cells in accordance with bioinformatics analysis. EU suppressed MCF-10AT cell growth, decreasing the NEAT1, VEGF-A, and MMP-9 levels and increasing miR-383-5p and miR-9-5p expressions in vitro and in vivo. Conclusion: In summary, the EU reduced the VEGF-A and MMP-9 expressions via NEAT1-mediated miR-383-5p and miR-9-5p against PBL, indicating that the EU may be a promising external drug to act against PBL.
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spelling doaj-art-0471f40944f54a149350ca2746795fd22025-01-17T04:51:01ZengElsevierHeliyon2405-84402025-01-01111e41353Eugenol inhibits NEAT1 as a ceRNA in pre-cancerous breast lesionsYusheng Liu0Guijuan Zhang1Yi Ma2Min Ma3Xuefeng Jiang4Department of Traditional Chinese Medicine, Yangjiang People's Hospital, Yangjiang, Guangdong, 529525, China; College of Traditional Chinese Medicine, Jinan University, Guangzhou, Guangdong, 510515, ChinaCollege of Traditional Chinese Medicine, Jinan University, Guangzhou, Guangdong, 510515, ChinaInstitute of Biomedicine and Department of Cellular Biology, Jinan University, Guangzhou, Guangdong, 510515, ChinaCollege of Traditional Chinese Medicine, Jinan University, Guangzhou, Guangdong, 510515, China; Corresponding author. No.42, Dongshan Road, Jiangcheng District, Yangjiang, Guangdong, 529525, China.Department of Traditional Chinese Medicine, Yangjiang People's Hospital, Yangjiang, Guangdong, 529525, China; College of Traditional Chinese Medicine, Jinan University, Guangzhou, Guangdong, 510515, China; Corresponding author. No.42, Dongshan Road, Jiangcheng District, Yangjiang, Guangdong, 529525, China.Objective: Eugenol (EU) from cloves is highly effective against different tumors. The long noncoding ribonucleic acids (lncRNAs), which play a role of competing endogenous RNAs (ceRNAs), suppress microRNAs (miRNAs) involved in post-transcriptional regulatory networks. The present work focused on analyzing how EU affected pre-cancerous breast lesions (PBL). Methods: Initially, the gene expression profiles of patients (n = 880) in the National Center for Biotechnology Information (NCBI) database were analyzed. Further, we established a lncRNA-miRNA-mRNA ceRNA network through bioinformatics analysis and investigated mechanistic roles of lncRNAs as ceRNAs and the anti-tumor effect of EU using MCF-10AT cells in vitro as well as PBL model rats in vivo. Besides, Nuclear Paraspeckle Assembly Transcript 1 (NEAT1), miR-383-5p, miR-9-5p, matrix metalloproteinase-9 (MMP-9), and vascular endothelial growth factor-A (VEGF-A) expression was examined through quantitative reverse transcription polymerase chain reaction (RT-qPCR), Western blotting, and immunohistochemical staining analyses. Results: There were altogether 1162 mRNAs, 81 miRNAs, and 26 lncRNAs recognized as trend genes in breast cancer (BC) and pre-cancerous BC (pBC), constructing the ceRNA network using 3 lncRNAs, 3 miRNAs, and 38 mRNAs. It was observed that NEAT1, miR-383-5p, miR-9-5p, VEGF-A, and MMP-9 were downregulated in breast tumor cells in accordance with bioinformatics analysis. EU suppressed MCF-10AT cell growth, decreasing the NEAT1, VEGF-A, and MMP-9 levels and increasing miR-383-5p and miR-9-5p expressions in vitro and in vivo. Conclusion: In summary, the EU reduced the VEGF-A and MMP-9 expressions via NEAT1-mediated miR-383-5p and miR-9-5p against PBL, indicating that the EU may be a promising external drug to act against PBL.http://www.sciencedirect.com/science/article/pii/S2405844024173847EugenolPre-cancerous breast lesionNEAT1ceRNAmiR-383-5pmiR-9-5p
spellingShingle Yusheng Liu
Guijuan Zhang
Yi Ma
Min Ma
Xuefeng Jiang
Eugenol inhibits NEAT1 as a ceRNA in pre-cancerous breast lesions
Heliyon
Eugenol
Pre-cancerous breast lesion
NEAT1
ceRNA
miR-383-5p
miR-9-5p
title Eugenol inhibits NEAT1 as a ceRNA in pre-cancerous breast lesions
title_full Eugenol inhibits NEAT1 as a ceRNA in pre-cancerous breast lesions
title_fullStr Eugenol inhibits NEAT1 as a ceRNA in pre-cancerous breast lesions
title_full_unstemmed Eugenol inhibits NEAT1 as a ceRNA in pre-cancerous breast lesions
title_short Eugenol inhibits NEAT1 as a ceRNA in pre-cancerous breast lesions
title_sort eugenol inhibits neat1 as a cerna in pre cancerous breast lesions
topic Eugenol
Pre-cancerous breast lesion
NEAT1
ceRNA
miR-383-5p
miR-9-5p
url http://www.sciencedirect.com/science/article/pii/S2405844024173847
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AT minma eugenolinhibitsneat1asacernainprecancerousbreastlesions
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