Clinical and Translational Research
Copyright ©The Author(s) 2022. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Clin Cases. Jun 6, 2022; 10(16): 5165-5184
Published online Jun 6, 2022. doi: 10.12998/wjcc.v10.i16.5165
Circulating miR-627-5p and miR-199a-5p are promising diagnostic biomarkers of colorectal neoplasia
Dong-Yan Zhao, Lei Zhou, Teng-Fei Yin, Yuan-Chen Zhou, Ge-Yu-Jia Zhou, Qian-Qian Wang, Shu-Kun Yao
Dong-Yan Zhao, Ge-Yu-Jia Zhou, Shu-Kun Yao, Graduate school, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing 100730, China
Dong-Yan Zhao, Ge-Yu-Jia Zhou, Shu-Kun Yao, Department of Gastroenterology, China-Japan Friendship Hospital, Beijing 100029, China
Lei Zhou, Department of General Surgery, China-Japan Friendship Hospital, Beijing 100029, China
Teng-Fei Yin, Yuan-Chen Zhou, Qian-Qian Wang, Graduate school, Peking University China-Japan Friendship School of Clinical Medicine, Beijing 100029, China
Author contributions: Zhao DY designed and performed the study, analyzed the data, and drafted the manuscript; Zhou L and Yin TF collected blood samples from subjects, and provided guidance on experimental procedures; Zhou YC, Zhou GYJ, and Wang QQ collected the clinical data and colorectal samples from the subjects; Yao SK designed the study, supervised the study performance, revised the manuscript, and obtained the funding; all authors read and approved the final manuscript.
Supported by National Key Development Plan for Precision Medicine Research, No. 2017YFC0910002.
Institutional review board statement: This study was approved by the Ethics Committee of China-Japan Friendship Hospital (No. 2018-116-K85).
Informed consent statement: All study participants, or their legal guardian, provided informed written consent prior to study enrollment.
Conflict-of-interest statement: There are no conflicts of interest to report.
Data sharing statement: No additional data are available.
Open-Access: This article is an open-access article that was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution NonCommercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: https://creativecommons.org/Licenses/by-nc/4.0/
Corresponding author: Shu-Kun Yao, PhD, Professor, Department of Gastroenterology, China-Japan Friendship Hospital, Graduate school, Chinese Academy of Medical Sciences and Peking Union Medical College, No. 2 Yinghua East Road, Chaoyang District, Beijing 100029, China. shukunyao@126.com
Received: October 22, 2021
Peer-review started: October 22, 2021
First decision: December 27, 2021
Revised: December 29, 2021
Accepted: March 15, 2022
Article in press: March 15, 2022
Published online: June 6, 2022
Processing time: 223 Days and 8 Hours
Abstract
BACKGROUND

Early detection of colorectal neoplasms, including colorectal cancers (CRCs) and advanced colorectal adenomas (AAs), is crucial to improve patient survival. Circulating microRNAs (miRNAs) in peripheral blood are emerging as noninvasive diagnostic markers for multiple cancers, but their potential for screening colorectal neoplasms remains ambiguous.

AIM

To identify candidate circulating cell-free miRNAs as diagnostic biomarkers in patients with colorectal neoplasms.

METHODS

The study was divided into three phases: (1) Candidate miRNAs were selected from three public miRNA datasets using differential gene expression analysis methods; (2) an independent set of serum samples from 60 CRC patients, 60 AA patients and 30 healthy controls (HCs) was included and analyzed by quantitative real-time polymerase chain reaction for miRNAs, and their diagnostic power was detected by receiver operating characteristic (ROC) analysis; and (3) the origin and function of miRNAs in cancer patients were investigated in cancer cell lines and tumor tissues.

RESULTS

Based on bioinformatics analysis, miR-627-5p and miR-199a-5p were differentially expressed in both the serum and tissues of patients with colorectal neoplasms and HCs and were selected for further study. Further validation in an independent cohort revealed that both circulating miR-627-5p and miR-199a-5p were sequentially increased from HCs and AAs to CRCs. The diagnostic power of miR-672-5p yielded an area under the curve (AUC) value of 0.90, and miR-199a-5p had an AUC of 0.83 in discriminating colorectal neoplasms from HCs. A logistic integrated model combining miR-199a-5p and miR-627-5p exhibited a higher diagnostic performance than either miRNA. Additionally, the levels of serum miR-627-5p and miR-199a-5p in CRC patients were significantly lower after surgery than before surgery and the expression of both miRNAs was increased with culture time in the culture media of several CRC cell lines, suggesting that the upregulated serum expression of both miRNAs in CRC might be tumor derived. Furthermore, in vitro experiments revealed that miR-627-5p and miR-199a-5p acted as tumor suppressors in CRC cells.

CONCLUSION

Serum levels of miR-199a-5p and miR-627-5p were markedly increased in patients with colorectal neoplasms and showed strong potential as minimally invasive biomarkers for the early screening of colorectal neoplasms.

Keywords: miR-627-5p; miR-199a-5p; Colorectal neoplasm; Biomarker; Screening; Serum

Core Tip: This report is the first on the diagnostic usefulness of circulating miR-627-5p and miR-199a-5p in patients with colorectal neoplasms. We identified that serum levels of miR-627-5p and miR-199a-5p were markedly elevated in patients with colorectal neoplasia and appeared to be novel biomarkers for the non-invasive screening of colorectal neoplasia. An integrated model combining miR-199a-5p and miR-627-5p obtained a better discriminative capacity than each miRNA alone. Additionally, miR-627-5p and miR-199a-5p had different expression levels in the serum of cancer patients before and after surgery and in vitro gain-of-function experiments demonstrated that both microRNAs played crucial roles in regulating the progression and invasion of colorectal cancer cells.