https://orcid.org/0000-0001-9958-2220
ABSTRACT
As a self-degradative mechanism, macroautophagy/autophagy has a role in the maintenance of energy homeostasis during critical periods in the development of cells. It also controls cellular damage through the eradication of damaged proteins and organelles. This process is accomplished by tens of ATG (autophagy-related) proteins. Recent studies have shown the involvement of non-coding RNAs in the regulation of autophagy. These transcripts mostly modulate the expression of ATG genes. Both long non-coding RNAs (lncRNAs) and microRNAs (miRNAs) have been shown to modulate the autophagy mechanism. Levels of several lncRNAs and miRNAs are altered in this process. In the present review, we discuss the role of lncRNAs and miRNAs in the regulation of autophagy in diverse contexts such as cancer, deep vein thrombosis, spinal cord injury, diabetes and its complications, acute myocardial infarction, osteoarthritis, pre-eclampsia and epilepsy.
Abbreviations: AMI: acute myocardial infarction; ATG: autophagy-related; lncRNA: long non-coding RNA; miRNA: microRNA.
Introduction
Autophagy is a degradative mechanism that regulates the energy resources at crucial times during development and in periods of nutrient deficiency [Citation1]. This process is also involved in the removal of protein aggregates, elimination of impaired organelles, as well as intracellular pathogens. Autophagy is regarded as a recycling mechanism to enhance energy proficiency through ATP production and governs cellular damage through the eradication of damaged proteins and organelles [Citation1]. Autophagy is accomplished through multiple steps. First, stress-related pathways regulate phagophore formation through modulation of the BECN1/Beclin 1-PIK3C3/VPS34-containing phosphatidylinositol 3-kinase complex at the endoplasmic reticulum. Subsequent multimerization of proteins coded by ATG (autophagy-related) genes and MAP1LC3/LC3 occurs at the phagophore membrane. Then, a number of targets are selected to be degraded and the autophagosome is fused with the lysosome to degrade the trapped molecules through proteolytic reactions [Citation1]. Several ATG proteins participate in autophagy. Notably, many of the corresponding genes are conserved between species [Citation2].
Macroautophagy, microautophagy, and chaperone-mediated autophagy are the principal types of autophagy. All three types lead to proteolytic destruction of cytosolic apparatuses in the cellular lysosomes [Citation3]. Yet, the route of delivery of cytoplasmic elements to the lysosomes differs between these types as in the macroautophagy autophagosome delivers these elements while in the micro-autophagy cytosolic apparatuses are directly delivered to the lysosome. In chaperone-mediated autophagy, targeted proteins are delivered in a complex with chaperone proteins that interact with the lysosomal membrane receptor. This interaction leads to protein unfolding and destruction [Citation3]. Autophagy is regulated by several mechanisms. Among the recently appreciated mechanisms is the involvement of non-coding RNAs (ncRNAs) [Citation4]. It has been revealed that 98% of the genome is transcribed. However, the majority of these transcripts do not encode proteins, thus being described as ncRNAs [Citation5]. Regulatory ncRNAs comprise a significant portion of ncRNAs, with long non-coding RNAs (lncRNAs) and microRNAs (miRNAs) being the most important classes of this group of transcripts. These transcripts can regulate the expression of several genes at the epigenetic, transcriptional, and post-transcriptional levels [Citation5]. Nearly all miRNAs are considered as post-transcriptional suppressors of gene expression. However, lncRNAs can regulate expression of protein-coding genes at both positive and negative directions via different interactions with RNA, protein and chromatin structures [Citation6]. Several lncRNAs have been shown to be evolutionarily conserved [Citation7], albeit to a lesser extent compared with protein-coding genes [Citation8]. It is worth mentioning that the levels of conservation in the promoter areas of lncRNAs are similar to the promoters of several protein-coding genes [Citation6]. Numerous miRNAs have been identified in mammalian genomes, several of them being highly conserved even between remotely related species [Citation9]. While lncRNAs are generated by POLR2 (RNA polymerase II) and POLR3 (RNA polymerase III) [Citation10], miRNAs are transcribed from genomic DNA into primary miRNAs, then being processed into precursor miRNAs and mature miRNAs in a sequential process [Citation10]. Both lncRNAs and miRNAs have been shown to modulate the autophagy mechanism. In the present review, we discuss the role of lncRNAs and miRNAs in the regulation of autophagy in diverse contexts such as cancer, deep vein thrombosis, spinal cord injury, diabetes and its complications, acute myocardial infarction, osteoarthritis, pre-eclampsia and epilepsy. In order to find the relevant literature, we searched PubMed and Google Scholar with the keywords “autophagy” AND “miRNA” or “lncRNA”. Then, we assessed the full texts of the articles to extract data regarding type of disorder, clinical samples, animal models and the molecular pathways being influenced by miRNAs/lncRNAs. Finally, we tabulated the extracted data in order to make the data more comprehensible. It is worth mentioning that the majority of the included studies have assessed the role of miRNA/lncRNAs through functional studies, thus providing enough evidence for contribution of these ncRNAs in the regulation of autophagy.
miRNAs and autophagy
These transcripts have sizes of approximately 22 nucleotides and principally regulate the expression of their target genes at the post-transcriptional level [Citation11]. Several experiments have shown the role of miRNAs in the regulation of autophagy. Dysregulation of miRNAs has been associated with a wide range of disorders, including cancers and nonmalignant disorders.
miRNA and autophagy in cancer
Expression of MIR100 is decreased in renal cell carcinoma cell lines and clinical samples compared with adjacent non-cancerous tissues, while the expression of its target gene, NOX4, is increased in malignant samples. Overexpression of this miRNA or knockdown of its target in the mentioned cell lines has enhanced autophagy while reducing the expression of MTOR (mechanistic target of rapamycin kinase) pathway-associated genes and cancer cell migration and invasion [Citation12]. MIR126 is downregulated in colorectal cancer cells and tissues compared with normal tissues. Forced upregulation of this miRNA compromised viability and growth of these cells and enhanced both autophagy and apoptosis through modulation of expression of the MTOR gene [Citation13]. MIR30A regulates autophagy in hepatocellular carcinoma [Citation14] and gastrointestinal stromal tumor [Citation15]. miRNAs with regulatory roles on the autophagy can also affect epithelial-mesenchymal transition (EMT), thus influencing the metastatic ability of cancer cells [Citation16]. depicts the underlying mechanism of the contribution of two miRNAs in the autophagy and EMT process in the context of gastric cancer.
Figure 1. H. pylori increases MIR543 levels in gastric cancer. This miRNA binds with the 3ʹ UTR of SIRT1 to inhibit its expression. Autophagy has a role in the inhibition of epithelial-mesenchymal transition (EMT) in some situations [Citation16]. Conversely, MIR532-3p levels are decreased in gastric cancer. This miRNA inhibits the expression of RAB3IP. Overexpression of RAB3IP is associated with a decrease in autophagy and enhancement of EMT [Citation79].
![Figure 1. H. pylori increases MIR543 levels in gastric cancer. This miRNA binds with the 3ʹ UTR of SIRT1 to inhibit its expression. Autophagy has a role in the inhibition of epithelial-mesenchymal transition (EMT) in some situations [Citation16]. Conversely, MIR532-3p levels are decreased in gastric cancer. This miRNA inhibits the expression of RAB3IP. Overexpression of RAB3IP is associated with a decrease in autophagy and enhancement of EMT [Citation79].](/cms/asset/20f7516e-dbd1-4e74-87e9-3f07eea80478/kaup_a_1883881_f0001_oc.jpg)
miRNAs and autophagy in cardiac disorders
Overexpression of MIR26B-5p, MIR204-5p, and MIR497-3p reduces IGF1 (insulin like growth factor 1)-induced cardiomyocyte hypertrophy by inhibiting autophagy [Citation17]. Several miRNAs have been identified that regulate autophagy in the context of acute myocardial infarction (AMI). For instance, overexpression of MIR139-5p could prevent cell autophagy induced by hypoxia-reoxygenation injury [Citation18]. Moreover, MIR638 and MIR384 have functional roles in the reduction of cell autophagy by modulating the expression of ATG5 and activation of the phosphoinositide 3-kinase (PI3K)-AKT/protein kinase B pathway, respectively [Citation19,Citation20]. Conversely, the downregulation of MIR30A can prevent autophagy in myocardial cells [Citation21]. Additionally, MIR30A suppresses BECN1-associated autophagy in diabetic cataract [Citation22]. MIR9-5p has a role in increasing migration, invasion, and angiogenesis of endothelial progenitor cells by lessening TRPM7 transcription through induction of PI3K-AKT-related autophagy. Based on the role of endothelial progenitor cells in resolving thrombi, this miRNA has been suggested as a therapeutic target in deep vein thrombosis [Citation23].
miRNAs and autophagy in osteoarthritis
Several miRNAs have been implicated in the pathogenesis of osteoarthritis via different mechanisms. For instance, MIR27A has a role in the down-regulation of PI3K and subsequent increase in autophagy in IL1B/IL-1β-treated chondrocytes [Citation24]. Conversely, MIR128-1 can suppress chondrocyte autophagy by disturbing ATG12 [Citation25]. MIR4262 also has a role in the development of osteoarthritis by modulating cell autophagy [Citation26]. Expression of MIR375 has been increased in cartilage tissues obtained from osteoarthritis cases, while ATG2B expression has been diminished in these samples. MIR375-mediated suppression of ATG2B in the chondrocytes inhibits autophagy and enhances endoplasmic reticulum stress, thus exacerbating osteoarthritis clinical symptoms [Citation27].
miRNA and autophagy in inflammatory bowel diseases
Several miRNAs have been shown to affect autophagy, thus contributing to the pathogenesis of inflammatory bowel disease. For instance, MIR196A and MIR196B can reduce the expression of IRGM and inhibit autophagy by decreasing the accumulation of LC3-II [Citation28]. Besides, the expression of MIR665 has been increased in the intestinal mucosa of patients with inflammatory bowel disease. This miRNA can decrease the expression of XBP1 and ORMDL3 in the course of endoplasmic reticulum stress, enhancing autophagy sensitivity [Citation29]. Finally, the upregulation of MIR221-5p in colitis tissues has been associated with overexpression of SP, implying its role in inflammatory bowel disease autophagy [Citation30].
shows the list of miRNAs that are involved in the process of autophagy.
Table 1. List of autophagy-associated miRNAs
Based on the fundamental roles of autophagy in the development of cancer and its course, expression of autophagy-associated miRNAs can predict cancer patients’ survival. Higher expressions of MIR221, MIR135A1-5p, MIR150, and MIR449A have been associated with unfavorable outcome in patients with colorectal cancer, hepatocellular carcinoma, non-small cell lung carcinoma, and glioma, respectively [Citation31–34]. summarizes the results of studies that assessed the association between expression levels of autophagy-related miRNAs and the survival of cancer patients.
Table 2. Association between the survival of cancer patients and miRNAs that functionally affect autophagy (the expression of miRNAs could be associated with the prognosis independently of autophagy regulation)
LncRNAs and autophagy
LncRNAs are transcripts comprising more than 200 nucleotides, devoid of protein-coding capacity, which are expressed in several tissues and exert regulatory roles on the expression of target genes. Several lncRNAs have been identified that influence the process of autophagy. As autophagy is involved in the pathogenic process of several human disorders, these lncRNAs participate in diverse disorders ranging from cancer to age-related pathologies.
lncRNA and autophagy in cancer
HOTAIR can enhance autophagy through the regulation of ATG3 and ATG7 in hepatocellular carcinoma [Citation35]. Also, MALAT1 can activate autophagy in glioblastoma through the MIR101-3p-STMN1-ATG4D and MIR384-GOLM1 axes [Citation36,Citation37]. NEAT1 has a role in conferring resistance to 5-fluorouracil in colorectal cancer cells through modulation of MIR34A [Citation38]. HULC can modulate cisplatin resistance in gastric cancer through the regulation of FOXM1 expression and suppression of autophagy [Citation39]. This lncRNA enhances the malignant progression of hepatocellular carcinoma cells via reducing expression of MIR15A and increasing expression of SQSTM1/p62. Moreover, the overexpression of HULC enhances LC3 levels and subsequently induces LC3 via SIRT1. HULC also promotes the interaction between LC3 and ATG3. Also, HULC enhances the expression of BECN1. Taken together, HULC increases autophagy through SIRT1-mediated overexpression of LC3-II. HULC also suppresses PTEN expression via autophagy-SQSTM1 and ubiquitin–proteasome mechanisms [Citation40]. shows the mechanism of participation of HULC in the carcinogenesis.
Figure 2. The expression of HULC is increased in hepatocellular carcinoma. This lncRNA inhibits METTL3 binding with pri-MIR15A and decreases methylation of pri-MIR15A. Besides, HULC precludes binding of DGCR8 and DROSHA with this pri-miRNA, leading to a significant reduction in the levels of mature MIR15A. Downregulation of this miRNA results in the upregulation of SQSTM1, which contributes to the formation of autophagosome, suppression of PTEN, and induction of cancer [Citation40]. On the other hand, HULC enhances the binding of METTL3 with pri-MIR675 and increases MIR675 levels. This miRNA binds with 3ʹ UTR of HDAC5 mRNA and decreases its expression. Therefore, SIRT1 levels and the formation of autophagosomes are enhanced. This increases CCND1 synthesis and promotes the proliferation of cancer stem cells [Citation134].
![Figure 2. The expression of HULC is increased in hepatocellular carcinoma. This lncRNA inhibits METTL3 binding with pri-MIR15A and decreases methylation of pri-MIR15A. Besides, HULC precludes binding of DGCR8 and DROSHA with this pri-miRNA, leading to a significant reduction in the levels of mature MIR15A. Downregulation of this miRNA results in the upregulation of SQSTM1, which contributes to the formation of autophagosome, suppression of PTEN, and induction of cancer [Citation40]. On the other hand, HULC enhances the binding of METTL3 with pri-MIR675 and increases MIR675 levels. This miRNA binds with 3ʹ UTR of HDAC5 mRNA and decreases its expression. Therefore, SIRT1 levels and the formation of autophagosomes are enhanced. This increases CCND1 synthesis and promotes the proliferation of cancer stem cells [Citation134].](/cms/asset/51661806-b90f-4a99-91a6-93de6e4a75cf/kaup_a_1883881_f0002_oc.jpg)
lncRNAs and autophagy in nonmalignant conditions
HOTAIR participates in the pathogenesis of intervertebral disc degeneration through modulation of the AMPK-MTOR-ULK1 pathway and enhancement of autophagy, apoptosis, and senescence in the nucleus pulposus cells [Citation41]. In cerebral ischemic stroke, MALAT1 acts as a molecular sponge for MIR26B and MIR200C-3p to upregulate ULK2 and SIRT1, respectively. Both interactions lead to the enhancement of autophagy and the protection of brain microvascular endothelial cells against oxygen-glucose deprivation [Citation42,Citation43]. NEAT1 has a role in the pathogenesis of diverse disorders, including congenital heart disease and Parkinson disease, through enhancement of autophagy via different pathways [Citation44,Citation45]. A number of lncRNAs such as SPAG5-AS1, Gm5524, Gm15645, and SOX2-OT are involved in the regulation of autophagy in the context of diabetic nephropathy [Citation46–48]. Being upregulated in pre-eclampsia, the lncRNA H19 decreases cell viability but enhances invasion and autophagy in trophoblast cells possibly through induction of the PI3K-AKT-MTOR signaling [Citation49].
shows the list and function of autophagy-related lncRNAs.
Table 3. List of autophagy-associated lncRNAs
Vault RNAs (vtRNA) as a group of small ncRNAs being produced by RNA polymerase III can bind with the autophagy receptor SQSTM1 to suppress SQSTM1-dependent autophagy. Mechanistically, vtRNAs binding with SQSTM1 interferes with the oligomerization of SQSTM1 [Citation50]. Notably, the mechanism by which ncRNA may directly regulate protein function in the context of autophagy is implicated in cellular viability [Citation50,Citation51].
Expression levels of autophagy-related lncRNAs can predict the prognosis of patients with diverse cancer types. Most studies in this regard have been performed in patients with hepatocellular carcinoma. HNF1A-AS1, HOTAIR, HAGLROS, SNHG11, and LNCRNA-ATB are among lncRNAs whose upregulation confer unfavorable outcome in this kind of cancer [Citation35,Citation52–55]. summarizes the results of studies that assessed the association between expression levels of autophagy-related lncRNAs and patients’ prognosis. Moreover, few studies have appraised the diagnostic role of these lncRNAs in cancer patients. These studies are also summarized in .
Table 4. Prognostic/diagnostic value of autophagy-related lncRNAs in patients with cancers
Discussion
As a conserved process for the elimination of misfolded proteins and damaged organelles, autophagy is involved in the pathogenesis of several disorders. Autophagy is regulated by both lncRNAs and miRNAs. LncRNAs mostly regulate autophagy through modulation of expression of ATG genes. Their function is exerted through their ceRNA role in which they alter the function of autophagy-related miRNAs [Citation56]. Notably, autophagy itself can regulate the expression of several lncRNAs. An example of this type of regulation is represented by the lncRNA PVT1. The expression of this upregulated lncRNA in diabetic patients is downregulated by autophagy suppression [Citation57]. Globally, the role of autophagy-associated ncRNAs has been mostly assessed in cancers. Autophagy-related ncRNAs have remarkable survival in patients with diverse types of cancers.
The role of miRNAs/lncRNAs in the regulation of autophagy is mostly appraised in the context of cancer. Autophagy is regarded as a “dual sword” in the pathogenesis of cancer. Mostly, it preserves the homeostasis of the cancer milieu by affording nutritional supplements in situations of hypoxia and nutrient shortage. Yet, in certain conditions, autophagy can repress carcinogenesis [Citation58]. This note should be considered in the appraisal of the role of autophagy-related ncRNAs in the carcinogenic process. Moreover, autophagy has a fundamental role in the pathogenesis of several age-related conditions such as intervertebral disc degeneration, ischemia-related disorders such as myocardial infarction and cerebral ischemia, and diabetic-related complications. Thus, miRNAs/lncRNAs that regulate this process are putative therapeutic targets for a wide range of disorders. It is worth mentioning that while autophagy has a protective role against cell injury in cerebral ischemic stroke, in many of the mentioned conditions, it aggravates the pathogenic situation. Therefore, the direction of effects of autophagy in human pathologies should be considered in the design of therapeutic strategies. Moreover, it is possible that autophagy-related lncRNAs/miRNAs modulate specific targets or pathways in each tissue. This is particularly important for miRNAs as they can have several targets with variable levels of complementarity.
In addition to the regulatory role of ncRNAs on autophagy, recent studies indicate that autophagy regulates ncRNA biology. For example, autophagy selectively targets key components of the miRNA machinery to regulate miRNAs stability and function [Citation59,Citation60]. DICER1 and the principal miRNA effector, AGO2, is degraded through the selective autophagy receptor CALCOCO2/NDP52 [Citation60]. Moreover, the autophagy machinery has been reported to regulate intracellular and extracellular transport of RNA-binding proteins and ncRNAs. For instance, the LC3-conjugation system regulates the packaging of RNA-binding proteins into extracellular vesicles [Citation61]. Furthermore, ATG5 has been demonstrated to diminish nuclear transport of MIR126-5p [Citation51]. Finally, the MTORC1 pathway and autophagy control the proper assembly of RNA-induced Silencing complexes (RISCs), therefore affecting miRNA-related functions [Citation62].
According to the complexity of the autophagy process and involvement of several ncRNAs in the regulation of this process, integrative system biology-based methods are the preferred strategies for assessment of expression profile and function of miRNAs and lncRNAs and identification of the functional networks in this process. Each module in this network can be applied as a therapeutic target for disorders that are associated with autophagy. It is worth mentioning that with the constant influx of novel researchers in this field, it is necessary to outline standards for this kind of research. Importantly, investigators should apply these guidelines to ensure appropriate study design [Citation63].
Finally, autophagy-associated lncRNAs and miRNAs can predict patients’ outcomes in diverse cancer types. However, the prognostic role of these transcripts has not been assessed in other pathologic conditions. Thus, future studies should focus on this field to unravel the diagnostic/prognostic role of miRNAs and lncRNAs in these conditions to design personalized approaches for these disorders.
Acknowledgments
This study was financially supported by Shahid Beheshti University of Medical Sciences.
Disclosure statement
The authors declare they have no conflict of interest.
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