Soudeh Ghafouri-Fard1
Arian Askari2
Bashdar Mahmud Hussen3,4
Mohammed Fatih Rasul5Sevak Hatamian6
Mohammad Taheri7,8*Arda Kiani9*- 1Department of Medical Genetics, School of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran
- 2Phytochemistry Research Center, Shahid Beheshti University of Medical Sciences, Tehran, Iran
- 3Department of Biomedical Sciences, Cihan University-Erbil, Kurdistan Region, Iraq
- 4Department of Pharmacognosy, College of Pharmacy, Hawler Medical University, Erbil, Iraq
- 5Department of Pharmaceutical Basic Science, Faculty of Pharmacy, Tishk International University, Erbil, Iraq
- 6Department of Anesthesia, Shahid Madani Hospital, School of Medicine, Alborz University of Medical Sciences, Karaj, Iran
- 7Urology and Nephrology Research Center, Shahid Beheshti University of Medical Sciences, Tehran, Iran
- 8Institute of Human Genetics, Jena University Hospital, Jena, Germany
- 9Tracheal Diseases Research Center, National Research Institute of Tuberculosis and Lung Diseases (NRITLD), Shahid Beheshti University of Medical Sciences, Tehran, Iran
miR-671 is encoded by a gene on 7q36.1 and contributes to the pathogenesis of a variety of disorders, including diverse types of cancers, atherosclerosis, ischemic stroke, liver fibrosis, osteoarthritis, Parkinson’s disease, rheumatoid arthritis, acute myocardial infarction and Crohn’s disease. In the context of cancer, different studies have revealed opposite roles for this miRNA. In brief, it has been shown to be down-regulated in pancreatic ductal carcinoma, ovarian cancer, gastric cancer, osteosarcoma, esophageal squamous cell carcinoma and myelodysplastic syndromes. Yet, miR-671 has been up-regulated in glioma, colorectal cancer, prostate cancer and hepatocellular carcinoma. Studies in breast, lung and renal cell carcinoma have reported inconsistent results. The current review aims at summarization of the role of miR-671 in these disorders focusing on its target mRNA in each context and dysregulated signaling pathways. We also provide a summary of the role of this miRNA as a prognostic factor in malignancies.
Introduction
microRNAs (miRNAs) are small-sized non-coding RNAs that partake in the post-transcriptional regulation of gene expression through influencing the stability and translation of transcripts. They are transcribed by RNA polymerase II. The pri-miRNAs produced by this enzyme is capped and polyadenylated. This transcript undergoes a series of cleavage by the Drosha and cytoplasmic Dicer ribonuclease enzymes to produce the stem-loop precursor miRNA and mature miRNA, respectively. The latter is embraced into a RNA-induced silencing complex which can recognize target mRNAs and suppress its translation or destabilize it (Macfarlane and Murphy, 2010). miRNAs participate in the pathoetiology of several disorders through modulation of expression of genes (Hussen et al., 2021), altering signaling pathways (Hussen et al., 2022) or interactions with other types of non-coding RNAs (Ghafouri-Fard et al., 2021a; Taheri et al., 2022).
miR-671 is encoded by a gene on 7q36.1 and involved in the pathogenesis of a range of disorders, including diverse types of cancers, atherosclerosis, ischemic stroke, liver fibrosis, osteoarthritis, Parkinson’s disease, rheumatoid arthritis, acute myocardial infarction and Crohn’s disease. There is not sufficient data about the role of this miRNA in normal physiological processes. However, differential expression of this miRNA in the visceral adipose tissues of patients with non-alcoholic fatty liver disease (Estep et al., 2010) indicates its possible role in metabolic pathways. Moreover, miR-671 has been shown to down-regulate the CDR1 (Cerebellar Degeneration-Related protein 1) gene through an Ago2-slicer-dependent mechanism (Hansen et al., 2011). Moreover, this miRNA has been found to be mainly localized in the nucleus (Hansen et al., 2011). There is no clear evidence about differential expression or functional roles of miR-671-3p versus miR-671-5p. The current review aims at summarization of the role of miR-671 in these disorders focusing on its target mRNA in each context and dysregulated signaling pathways. We also provide a summary of the role of this miRNA as a prognostic factor in malignancies.
miR-671 in cancers
The influence of miR-671 in the carcinogenesis has been valued by a number of studies in cancer cell lines, animal models of cancers and samples obtained from affected individuals. In the succeeding sections, we define the role of miR-671 in the carcinogenesis based on these three lines of evidence.
Cell line studies
Up-regulation of miR-671 in cancer cell lines
Studies in colorectal cancer cell lines have shown down-regulation of circ_PTPRA. Exosomal circ_PTPRA has been shown to induce cell cycle arrest and inhibit proliferation of colorectal cancer cells. In addition, exosomal circ_PTPRA could promote sensitivity of these cells to radiation, resulting in inhibition of colony formation and induction of apoptosis. Mechanistically, circ_PTPRA functions as a sponge for miR-671-5p to increase SMAD4 levels. Taken together, circ_PTPRA inhibits growth and radioresistance of colorectal cancer cells through down-regulation of miR-671-5p levels. Moreover, suppression of miR-671-5p has also blocked growth and radioresistance of these cells through enrichment of expression of SMAD4 (Yang et al., 2022b). Another study in this type of cancer has shown overexpression of a circular RNA, namely circGLIS2. This circRNA is sponged by miR-671. Over-expression of circGLIS2 has led to activation of NF-ƙB pathway and induction of production of pro-inflammatory chemokines leading to stimulation of tumor-associated inflammatory responses via recruitment of leukocytes. Taken together, circGLIS2 activates NF-ƙB signaling and promotes migratory ability of colorectal cancer cells through adsorbing miR-671 (Figure 1) (Chen et al., 2020a). Another functional study in colorectal cancer cells has shown the effect of miR-671-5p up-regulation in enhancement of cell proliferation, migratory capacity, and invasiveness of these cells, whereas its downregulation has led to reverse effects. Therefore, miR-671-5p has been suggested as an oncogenic miRNA in colon cancer which exerts its effects through targeting Tripartite Motif Containing 67 (TRIM67) (Jin et al., 2019), a gene, that is, possibly involved in zinc ion binding activity, regulation of protein localization and negative regulation of Ras protein signal transduction (https://www.genecards.org/cgi-bin/carddisp.pl?gene=TRIM67).
FIGURE 1. The illustration shows signaling pathways underlying the role of miRNA-671 is as a tumor suppressor miRNA in cancers. miRNA-671 inhibits many signaling pathways and carcinogenic mRNAs, resulting in increased apoptosis while lowering proliferation, migration, and invasion of cancer cells.
miR-671-3p has also been shown to exert oncogenic roles in glioma cells through targeting CKAP4 (Lu et al., 2018). Moreover, it has been demonstrated to be sponged by the tumor suppressor circRNA circDLC1 in these cells (Wu et al., 2022a). A single study in lung cancer cells has shown that miR-671-3p enhances progression of lung cancer through blocking expression of FOXP2 expression in lung cancer (Li et al., 2019b), thus referring to an oncogenic role for this miRNA in lung cancer.
Two independent studies in glioblastoma cell lines have revealed that miR-671-5p has transforming roles. Firstly, more than two-fold upregulated levels of miR-671-5p reduced levels of CDR1-AS/VSNL1 in glioblastoma cell lines A172, CAS-1 and DBTRG. This phenomenon is associated with increased migration and proliferation (Barbagallo et al., 2016). In another study it was demonstrated that if upregulated, miR-671-5p has oncogenic roles, but with competing endogenous features of Circular RNA circ_0001946, this miRNA is suppressed and its suppression is in favor of benign properties (Li and Diao, 2019).
Prostate cancer related bioinformatics analysis has shown that miR-671-5p is amongst top differentially expressed miRNAs (Zhu et al., 2020). miR-671-5p has a binding site on the 3′-UTR region of NFIA (Zhu et al., 2020). According to Yang et al., NFIA acts as a tumor suppressor gene in glioma and squamous carcinoma (Yang et al., 2018). Upregulation of miR-671-5p in prostate cancer cell lines reduces NFIA/CRYAB levels and contributes to malignant features like increased proliferation, migration and invasion (Figure 2) (Zhu et al., 2020).
FIGURE 2. The above illustration shows the roles of miRNA-671, which acts as an oncogene and stimulates cancer growth in several types of cancer. MiRNA-671 can target different tumor suppressor mRNAs and, through inhibition of translation, increase proliferation, migration, and invasion of cancer cells.
In kidney cancers category, miR-671-5p has been shown to be overexpressed patterns in clear cell renal cell carcinoma (ccRCC) cell lines (786-O and CAKI-1) (Chi et al., 2020). Its overexpression is regulated by HMGA1, which involves in chromatin remodeling (Chiefari et al., 2018). Upregulated levels of miR-671-5p targets APC (a tumor suppressor gene) and gives rise to invasiveness of ccRCC cells (Chi et al., 2020).
Down-regulation of miR-671 in cancer cell lines
The lncRNA PACERR that sponges miR-671 has been shown to increase the number of M2-polarized cells and enhance proliferation, invasiveness and migration of pancreatic cancer cells. From a mechanistical point of view, PACERR has a role in activation of KLF12/p-AKT/c-myc pathway through sponging miR-671-3p. In fact, this lncRNA is regarded as a regulator of tumor-associated macrophages in pancreatic ductal carcinoma microenvironment (Liu et al., 2022b). Moreover, circ_0092314 has been identified as another non-coding RNA that sponges miR-671 in pancreatic cancer cells, thus increasing expression of S100P and inducing epithelial-mesenchymal transition (EMT) (Shen et al., 2021). These two studies have designated a tumor suppressor effect for miR-671 in pancreatic cancer.
The miR-671-sponging circRNA Circ_0001946 has been shown to be over-expressed in tamoxifen resistant breast cancer cells. This circRNA has been shown to be activated by YY1 in these cells. miR-671-5p mimics could partially reverse the effects of circ_0001946 up-regulation in enhancement of proliferation and invasive properties of drug-resistant breast cancer cells. EGFR has been shown to be the downstream target of miR-671-5p in these cells (Gao et al., 2022). Another study has shown the sponging effect of circSLC8A1 on miR-671 and the impact of this miRNA in the regulation of PTEN/PI3k/AKT pathway (Zhu et al., 2021). Moreover, miR-671-3p has been shown to suppress proliferation and invasiveness of breast cancer cells through modulation of expression of the MTOR-interacting protein DEPTOR (Xia et al., 2020).
Lung cancer cells have also been the subject of functional studies on the role of miR-671. As an example of these studies, Liu et al. (2022a) have shown that the oncogenic role of circRIP2 in this type of cancer is exerted through sequestering miR-671-5p and increasing expression of FOXM1. Moreover, miR-671-5p has been found to inhibit proliferation, migration and invasive aptitude of lung cancer cells through targeting MFAP3L (Ye et al., 2022).
In esophageal squamous cell carcinoma cell lines (including different subtypes of KYSE), elevated levels of FGFR2 activates ERK and AKT signaling pathway and contributes to the malignancy (Li et al., 2019a). Interestingly, miR-671-5p level has shown to be downregulated, hence acting as a tumor suppressor (Li et al., 2019a). Forced expression of this miRNA contributes to diminished levels of FGFR phosphorylation, thus reversing malignant features like proliferation and migration (Li et al., 2019a).
Downregulated levels of miR-671 have also been shown in gastric cancer. In a study conducted by Qiu et al. (2018), reduced level of miR-671-5p has been demonstrated in MKN28 cells compared with normal gastric cells, suggesting an anti-tumor role. Elevating its expression yields decreased ratio of Bcl-2/Bax (increase in BAX), thus promoting apoptosis (Qiu et al., 2018). miR-671-5p targets URGCP and inhibits its expression in MKN28 cells (Qiu et al., 2018). Considering the roles of Up regulator Of Cell Proliferation (URGCP) in the carcinogenesis (Xie et al., 2012; Cai et al., 2015), there is no surprise that targeting it by miR-671-5p has shifted MKN28 cells to normal cell features (Qiu et al., 2018).
Detailed information about the roles of miR-671 in different cancer cell lines is shown in Table 1.
TABLE 1. Function of miR-671 in cancer cell lines (Arrows indicate the effects of changes in the expression of mentioned genes (either endogenous or exogenous). ∆: knockdown or downregulation, MPP+: 1-methyl-4-phenylpyridinium).
Animal studies
Different animal studies have been performed to evaluate the impact of miR-671 dysregulation on the course of tumor formation. Moreover, a number of other studies have focused on circRNAs that act as molecular sponges for miR-671. For instance, up-regulation of circ_00923 in pancreatic cancer cells has led to down-regulation of miR-671 in tissues of affected animals and enhancement of tumor growth (Shen et al., 2021). On the other hand, over-expression of circ_0001946 has resulted in reduction of glioma growth in animal models (Li and Diao, 2019) Similar to cell line studies, studies in xenograft models of cancers have indicated different results regarding the oncogenic versus tumor suppressor effect of miR-671 (Table 2). For instance, in pancreatic cancer models, down-regulation of miR-671 has been associated with enhancement of tumor growth (Shen et al., 2021). Similar results have been obtained in xenograft models of ovarian cancer (Peng et al., 2022). On the other hand, studies in animal models of colorectal cancer have reported opposite results (Yang et al., 2022b). Detailed information about the role of miR-671 in animal models of cancer is presented in Table 2.
TABLE 2. Effect of miR-671 in cancer development based on research in animal models. (∆: knockdown or downregulation).
Studies in human samples
Expression of miR-671-5p has been increased in colon cancer tissues. Notably, up-regulation of miR-671-5p in this type of cancer has been associated with involvement of lymph nodes, TNM stage, and low overall survival time of affected individuals (Jin et al., 2019). In tumor associated macrophages of pancreatic cancer patients, the lncRNA PACERR that sponges miR-7671 has been shown to be over-expressed in association with poor prognosis of patients (Liu et al., 2022b).
Studies in clinical samples of breast cancer have reported different results regarding the expression of miR-671. First, the miR-671-sponging circRNA circ_0001946 has been shown to be over-expressed in breast cancer tissues, leading to down-regulation of miR-671 (Gao et al., 2022). Although two other studies have reported down-regulation of miR-671-3p (Xiong et al., 2018) and miR-671-5p (Tan et al., 2016) in breast cancer samples, another study has demonstrated up-regulation of miR-671 in another cohort of breast cancer patients (Zhu et al., 2021).
Several studies have shown the impact of miR-671 dysregulation on survival of patients with different kinds of cancer, including ovarian, colorectal and lung cancers as well as osteosarcoma (Table 3). However, a single study in breast cancer patients has reported lack of association between expression levels of miR-671 and median survival of patients (Xiong et al., 2018). Moreover, abnormal expression of miR-671 has been associated with tumor size, TNM stage or metastasis in some kind of cancers, such as colorectal cancer (Jin et al., 2019), lung cancer (Ye et al., 2022) and renal cell carcinoma (Chi et al., 2020). In prostate cancer, up-regulation of miR-671-5p has been associated with higher Gleason score, and BCR status and poor prognosis, but not with tumor stage and lymph node metastasis (Zhu et al., 2020).
TABLE 3. Abnormal levels of miR-671 in clinical specimens.
Association between miR-671 variants and risk of soft tissue sarcomas has been assessed in a population of Chinese patients and healthy controls. The results of this study has shown association between miR-671 rs1870238 GC + CC and miR-671 rs2446065 CG + GG genotypes and risk of this type of tumor after adjustment for age and smoking (Zhang et al., 2022a).
Non-malignant conditions
Cell line studies
Experiments in ox-LDL-treated HUVECs have shown down-regulation of miR-671-5p and up-regulation of circPTPRA expression. These two transcripts have been shown to interact with each other. While circPTPRA silencing has reversed ox-LDL-induced decrease in viability of HUVECs, miR-671-5p downregulation could abolish this effect. Cumulatively, circPTPRA silencing can protect against ox-LDL-associated HUVECs damage through enhancing expression of miR-671-5p (Luo and Zhou, 2022).
Another study has shown that the effects of ANRIL silencing in alleviation of neuroinflammatory responses in ischemia is mediated through influencing the miR-671-5p/NF-κB axis (Figure 3) (Deng et al., 2022). Moreover, miR-671-5p could attenuates neuroinflammation through suppression of NF-κB levels (Deng et al., 2021).
FIGURE 3. The illustration represents the main functions of miRNA-671 in non-malignant disorders. The level of miRNA-671 expression influences the development of a wide range of disorders by modulation of several signaling pathways.
miR-671-5p expression has been revealed to be reduced in S1P-induced hepatic stellate cells and TGFβ1-activated hepatic sinusoidal endothelial cells. Moreover, its expression has been negatively correlated with levels of Angpt1 and VWF. Mechanistically, miR-671-5p could target Angpt1 and VWF (Yang et al., 2022b).
miR-671-5p has also been shown to facilitate the effect of lncRNA DLEU1 in the regulation of chondrocytes proliferation, inflammatory responses, and degradation of extracellular matrix (Wu et al., 2022b). Moreover, the sponging effect of circ_0043947 on miR-671-5p is involved in the pathoetiology of IL1β-induced chondrocyte damage and pathogenesis of osteoarthritis (He et al., 2022). Table 4 summarizes the role of miR-671 in the pathogenesis of non-malignant conditions based on the results of cell line studies.
TABLE 4. Cell line studies showing the role of miR-671 in non-malignant conditions.
Animal studies
Expression of miR-671-5p has been down-regulated in the mouse fibrotic liver. Notably, its levels have been negatively correlated with expressions of Angpt1, VWF, sphingosine kinase-1, TGFβ1, HIF1α, HIF2α, and markers of fibrosis. Moreover, expression of miR-671-5p has been lower in hepatic sinusoidal endothelial cells and hepatic stellate cells of CCl4 mice compared with control mice. Administration of miR-671-5p agomir could decrease expressions of Anpgt1 and VWF mRNA and protein levels, and attenuate angiogenesis and fibrosis in the liver of animal models (Yang et al., 2022b). Other investigations in animal models of ischemic stroke, mixed dry eye disease, podocyte injury, acute myocardial infarction and osteoarthritis have verified the role of miR-671 in the pathogenesis of these disorders (Table 5).
TABLE 5. Animal studies on the role of miR-671 in non-malignant conditions (MCAO: middle cerebral artery occlusion-reperfusion).
Studies in human samples
A high throughput sequencing study in pseudoexfoliation syndrome has led to identification of four aberrantly expressed miRNAs among them being miR-671-3p (Tomczyk-Socha et al., 2022). miR-671-5p has also been among miRNAs participating in the pathogenesis of periodontitis through establishment of ceRNA regulatory network regulating autophagy (Bian et al., 2022). miR-671 has also been found to be down-regulated in patients with rheumatoid arthritis (Tang et al., 2019), hand, foot, and mouth disease (Lin et al., 2020), placenta accreta spectrum (Chen et al., 2020b), coronary artery disease (Zhong et al., 2020), Parkinson’s disease (Uwatoko et al., 2019) and Kawasaki disease (Zhang et al., 2018). Table 6 shows the detailed information about the role of this miRNA in human diosrders.
TABLE 6. Human studies on the role of miR-671 in non-malignant conditions.
Expression levels of miR-671 can be used as diagnostic marker in placenta accreta spectrum, osteoarthritis and hand, foot, and mouth disease (Table 7). The best AUC values have been obtained in extremely severe cases of hand, foot, and mouth disease where mir-671 levels could differentiate this condition from healthy status with AUC value of 1.00 (Jia et al., 2014).
TABLE 7. Diagnostic value of miR-671 in diseases (Mild HFMD: MHFMD, extremely severe HFMD: ESHFMD).
Discussion
miR-671 is a miRNA with various roles in human disorders. In the context of cancer, different studies have revealed opposite roles for this miRNA. In brief, it has been shown to be down-regulated in pancreatic ductal carcinoma, ovarian cancer, gastric cancer, osteosarcoma, esophageal squamous cell carcinoma and myelodysplastic syndromes. Yet, miR-671 has been up-regulated in glioma, colorectal cancer, prostate cancer and hepatocellular carcinoma. Studies in breast, lung and renal cell carcinoma have reported inconsistent results which cannot be explained by the differences in the roles of miR-671-3p or miR-671-5p. It is possible that this miRNA exert stage- or grade-specific roles in the carcinogenesis.
miR-671 has functional interactions with circ_PTPRA, circ_0092314, circDLC1, circ_0001946, circSLC8A1, circRIP2, circ_0000620, circPIP5K1A and circCDR1as. In fact, these circRNAs act as molecular sponges for miR-671 to influence expression of miR-671 targets. NF-ƙB, EGFR, PTEN/PI3K/AKT, Wnt, HIF-1α, STAT3 and AKT/ERK/mTOR signaling pathways are among those being influenced by dysregulation of miR-671 in different cancers. Moreover, miR-671 has a role in the regulation of EMT in different tissues. This finding is based on functional studies on the role of this miRNA or circRNAs that sponge this miRNA. Thus, miR-671-targetin therapies might affect progression of cancer, invasiveness and metastatic ability of malignant cells.
miR-671 has also been suggested to predict course of cancers originated from different tissues. This speculation is based on the observed associations between dysregulation of this miRNA and survival of patients as well as correlation between its expression levels and clinicopathological data. However, the role of miR-671 as a diagnostic marker for cancers should be investigated in future. Based on the inconsistencies regarding the exact effects of miR-671 in the development and progression of different cancers, it is not expected that miR-671-targetted therapies enter the clinics in near future. More researches are needed to assign a definite role for this miRNA in each type of cancer.
The impact of miR-671 polymorphisms on risk of cancers has only assessed in sarcoma. Similar studies should be conducted to evaluate the association between these polymorphisms and risk of other cancers.
miR-671 has also a fundamental role in the pathophysiology of non-malignant conditions such as atherosclerosis, ischemic stroke, liver fibrosis, osteoarthritis, Parkinson’s disease, rheumatoid arthritis, acute myocardial infarction and Crohn’s disease. Moreover, it has a potential to be used as a diagnostic marker for placenta accreta spectrum, osteoarthritis and hand, foot, and mouth disease. However, dysregulation of miR-671 in malignant and non-malignant disorders originated from a certain tissue complicates the diagnostic application of this miRNA. Meanwhile, contribution of miR-671 to the pathogenesis of both malignant and non-malignant diseases is best explained by the prominent role of this miRNA in the regulation of activity of signaling pathways the control cell proliferation and apoptosis.
Taken together, miR-671 is a miRNA that can affect several target mRNAs and influence activity of signaling pathways that are involved in a variety of human disorders. However, several questions should be answered in order to propose miR-671-targeted therapies as efficient therapies for human disorders.
Author contributions
SG-F wrote the draft and revised it. MT designed and supervised the study. AA, BH, and AK collected the data and designed the figures and tables. All the authors read the submitted version and approved it.
Funding
This study was financially supported by Shahid Beheshti University of Medical Sciences.
Acknowledgments
The authors would like to thank the clinical research Development Unit (CRDU) of Loghman Hakim Hospital, Shahid Beheshti University of Medical Sciences, Tehran, Iran for their support, cooperation and assistance throughout the period of study.
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Publisher’s note
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Keywords: mir-671, cancer, biomarker, expression, prognostic
Citation: Ghafouri-Fard S, Askari A, Hussen BM, Rasul MF, Hatamian S, Taheri M and Kiani A (2022) A review on the role of miR-671 in human disorders. Front. Mol. Biosci. 9:1077968. doi: 10.3389/fmolb.2022.1077968
Received: 23 October 2022; Accepted: 25 November 2022;
Published: 05 December 2022.
Edited by:
Wei Ye, Guangdong Academy of Science, ChinaReviewed by:
Meredith Tennis, University of Colorado Denver, United StatesGuan Wang, Sichuan University, China
Copyright © 2022 Ghafouri-Fard, Askari, Hussen, Rasul, Hatamian, Taheri and Kiani. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Mohammad Taheri, Mohammad.taheri@uni-jena.de; Arda Kiani, ardakiani@sbmu.ac.ir