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MicroRNAs and Stem Cells

A special issue of International Journal of Molecular Sciences (ISSN 1422-0067). This special issue belongs to the section "Molecular Pathology, Diagnostics, and Therapeutics".

Deadline for manuscript submissions: closed (30 June 2019) | Viewed by 37364

Special Issue Editor

Department of Biochemical Science, University of Sassari, 07100 Sassari, Italy
Interests: stem cells; cell senescence; stem cell differentiation; adipogenesis; osteogenesis; cardiogenesis; conditioned media; nutraceuticals; gene expression; epigenetics; cellular mechanisms; cell-based therapies
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Dear Colleagues,

MicroRNAs are involved in cellular processes such as differentiation, growth, and apoptosis. Stem cells have peculiar properties such as differentiation and self-renewal, which can be strongly influenced by epigenetic changes. In particular, miRNAs are able to fine-tune stem cell behavior by suppressing the translation of many target mRNAs, thus inducing fluctuations in gene expression and protein translation. In particular, two large miRNA families (i.e., the miR-200 and the miR-302 families) are pluripotent activators able to modulate pluripotent genes. These two miRNA families can be down-regulated by the activation of TGF-β, itself being directly modulated by both miR-200 and miR-302 and consequently involved in cell differentiation and reprogramming. Unraveling epigenetic factors and their role in influencing pluripotency and stem cell differentiation capabilities could pave the way for new therapeutic approaches in regenerative medicine. The Special Issue, “MicroRNAs and Stem cells” of the International Journal of Molecular Sciences will include a selection of research papers and reviews about various aspects of the molecular regulation of stem cell behavior and cellular phenotype by miRNA. In addition, clinical studies evaluating miRNA and stem cells in regenerative medicine are suitable.

Assoc. Prof. Margherita Maioli
Guest Editor

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Keywords

  • miRNA
  • Epigenetic
  • Stem cells
  • Pluripotency
  • Stem cell differentiation
  • Gene expression
  • New therapeutic targets

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Published Papers (11 papers)

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Research

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19 pages, 3655 KiB  
Article
microRNAs Regulating Human and Mouse Naïve Pluripotency
by Yuliang Wang, Abdiasis M. Hussein, Logeshwaran Somasundaram, Rithika Sankar, Damien Detraux, Julie Mathieu and Hannele Ruohola-Baker
Int. J. Mol. Sci. 2019, 20(23), 5864; https://doi.org/10.3390/ijms20235864 - 22 Nov 2019
Cited by 13 | Viewed by 3702
Abstract
microRNAs are ~22bp nucleotide non-coding RNAs that play important roles in the post-transcriptional regulation of gene expression. Many studies have established that microRNAs are important for cell fate choices, including the naïve to primed pluripotency state transitions, and their intermediate state, the developmentally [...] Read more.
microRNAs are ~22bp nucleotide non-coding RNAs that play important roles in the post-transcriptional regulation of gene expression. Many studies have established that microRNAs are important for cell fate choices, including the naïve to primed pluripotency state transitions, and their intermediate state, the developmentally suspended diapause state in early development. However, the full extent of microRNAs associated with these stage transitions in human and mouse remain under-explored. By meta-analysis of microRNA-seq, RNA-seq, and metabolomics datasets from human and mouse, we found a set of microRNAs, and importantly, their experimentally validated target genes that show consistent changes in naïve to primed transitions (microRNA up, target genes down, or vice versa). The targets of these microRNAs regulate developmental pathways (e.g., the Hedgehog-pathway), primary cilium, and remodeling of metabolic processes (oxidative phosphorylation, fatty acid metabolism, and amino acid transport) during the transition. Importantly, we identified 115 microRNAs that significantly change in the same direction in naïve to primed transitions in both human and mouse, many of which are novel candidate regulators of pluripotency. Furthermore, we identified 38 microRNAs and 274 target genes that may be involved in diapause, where embryonic development is temporarily suspended prior to implantation to uterus. The upregulated target genes suggest that microRNAs activate stress response in the diapause stage. In conclusion, we provide a comprehensive resource of microRNAs and their target genes involved in naïve to primed transition and in the paused intermediate, the embryonic diapause stage. Full article
(This article belongs to the Special Issue MicroRNAs and Stem Cells)
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14 pages, 1954 KiB  
Article
RNAase III-Type Enzyme Dicer Regulates Mitochondrial Fatty Acid Oxidative Metabolism in Cardiac Mesenchymal Stem Cells
by Xuan Su, Yue Jin, Yan Shen, Il-man Kim, Neal L. Weintraub and Yaoliang Tang
Int. J. Mol. Sci. 2019, 20(22), 5554; https://doi.org/10.3390/ijms20225554 - 07 Nov 2019
Cited by 8 | Viewed by 2657
Abstract
Cardiac mesenchymal stem cells (C-MSC) play a key role in maintaining normal cardiac function under physiological and pathological conditions. Glycolysis and mitochondrial oxidative phosphorylation predominately account for energy production in C-MSC. Dicer, a ribonuclease III endoribonuclease, plays a critical role in the control [...] Read more.
Cardiac mesenchymal stem cells (C-MSC) play a key role in maintaining normal cardiac function under physiological and pathological conditions. Glycolysis and mitochondrial oxidative phosphorylation predominately account for energy production in C-MSC. Dicer, a ribonuclease III endoribonuclease, plays a critical role in the control of microRNA maturation in C-MSC, but its role in regulating C-MSC energy metabolism is largely unknown. In this study, we found that Dicer knockout led to concurrent increase in both cell proliferation and apoptosis in C-MSC compared to Dicer floxed C-MSC. We analyzed mitochondrial oxidative phosphorylation by quantifying cellular oxygen consumption rate (OCR), and glycolysis by quantifying the extracellular acidification rate (ECAR), in C-MSC with/without Dicer gene deletion. Dicer gene deletion significantly reduced mitochondrial oxidative phosphorylation while increasing glycolysis in C-MSC. Additionally, Dicer gene deletion selectively reduced the expression of β-oxidation genes without affecting the expression of genes involved in the tricarboxylic acid (TCA) cycle or electron transport chain (ETC). Finally, Dicer gene deletion reduced the copy number of mitochondrially encoded 1,4-Dihydronicotinamide adenine dinucleotide (NADH): ubiquinone oxidoreductase core subunit 6 (MT-ND6), a mitochondrial-encoded gene, in C-MSC. In conclusion, Dicer gene deletion induced a metabolic shift from oxidative metabolism to aerobic glycolysis in C-MSC, suggesting that Dicer functions as a metabolic switch in C-MSC, which in turn may regulate proliferation and environmental adaptation. Full article
(This article belongs to the Special Issue MicroRNAs and Stem Cells)
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18 pages, 5140 KiB  
Article
Dynamic Regulation of miRNA Expression by Functionally Enhanced Placental Mesenchymal Stem Cells Promotes Hepatic Regeneration in a Rat Model with Bile Duct Ligation
by Jae Yeon Kim, Ji Hye Jun, Soo Young Park, Seong Wook Yang, Si Hyun Bae and Gi Jin Kim
Int. J. Mol. Sci. 2019, 20(21), 5299; https://doi.org/10.3390/ijms20215299 - 24 Oct 2019
Cited by 20 | Viewed by 3156
Abstract
Placenta-derived mesenchymal stem cells (PD-MSCs) were highlighted as therapeutic sources in several degenerative diseases. Recently, microRNAs(miRNAs) were found to mediate one of the therapeutic mechanisms of PD-MSCs in regenerative medicine. To enhance the therapeutic effects of PD-MSCs, we established functionally enhanced PD-MSCs with [...] Read more.
Placenta-derived mesenchymal stem cells (PD-MSCs) were highlighted as therapeutic sources in several degenerative diseases. Recently, microRNAs(miRNAs) were found to mediate one of the therapeutic mechanisms of PD-MSCs in regenerative medicine. To enhance the therapeutic effects of PD-MSCs, we established functionally enhanced PD-MSCs with phosphatase of regenerating liver-1 overexpression (PRL-1(+)). However, the profile and functions of miRNAs induced by PRL-1(+) PD-MSCs in a rat model with hepatic failure prepared by bile duct ligation (BDL) remained unclear. Hence, the objectives of the present study were to analyze the expression of miRNAs and investigate their therapeutic mechanisms for hepatic regeneration via PRL-1(+) in a rat model with BDL. We selected candidate miRNAs based on microarray analysis. Under hypoxic conditions, compared with migrated naïve PD-MSCs, migrated PRL-1(+) PD-MSCs showed improved integrin-dependent migration ability through Ras homolog (RHO) family-targeted miRNA expression (e.g., hsa-miR-30a-5p, 340-5p, and 146a-3p). Moreover, rno-miR-30a-5p and 340-5p regulated engraftment into injured rat liver by transplanted PRL-1(+) PD-MSCs through the integrin family. Additionally, an increase in platelet-derived growth factor receptor A (PDGFRA) by suppressing rno-miR-27a-3p improved vascular structure in rat liver tissues after PRL-1(+) PD-MSC transplantation. Furthermore, decreased rno-miR-122-5p was significantly correlated with increased proliferation of hepatocytes in liver tissues by PRL-1(+) PD-MSCs by activating the interleukin-6 (IL-6) signaling pathway through the repression of rno-miR-21-5p. Taken together, these findings improve the understanding of therapeutic mechanisms based on miRNA-mediated stem-cell therapy in liver diseases. Full article
(This article belongs to the Special Issue MicroRNAs and Stem Cells)
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11 pages, 1583 KiB  
Article
Epigenetics, Stem Cells, and Autophagy: Exploring a Path Involving miRNA
by Francesca Balzano, Ilaria Campesi, Sara Cruciani, Giuseppe Garroni, Emanuela Bellu, Silvia Dei Giudici, Andrea Angius, Annalisa Oggiano, Vincenzo Rallo, Giampiero Capobianco, Salvatore Dessole, Carlo Ventura, Andrea Montella and Margherita Maioli
Int. J. Mol. Sci. 2019, 20(20), 5091; https://doi.org/10.3390/ijms20205091 - 14 Oct 2019
Cited by 11 | Viewed by 3125
Abstract
MiRNAs, a small family of non-coding RNA, are now emerging as regulators of stem cell pluripotency, differentiation, and autophagy, thus controlling stem cell behavior. Stem cells are undifferentiated elements capable to acquire specific phenotype under different kind of stimuli, being a main tool [...] Read more.
MiRNAs, a small family of non-coding RNA, are now emerging as regulators of stem cell pluripotency, differentiation, and autophagy, thus controlling stem cell behavior. Stem cells are undifferentiated elements capable to acquire specific phenotype under different kind of stimuli, being a main tool for regenerative medicine. Within this context, we have previously shown that stem cells isolated from Wharton jelly multipotent stem cells (WJ-MSCs) exhibit gender differences in the expression of the stemness related gene OCT4 and the epigenetic modulator gene DNA-Methyltransferase (DNMT1). Here, we further analyze this gender difference, evaluating adipogenic and osteogenic differentiation potential, autophagic process, and expression of miR-145, miR-148a, and miR-185 in WJ-MSCs derived from males and females. These miRNAs were selected since they are involved in OCT4 and DNMT1 gene expression, and in stem cell differentiation. Our results indicate a difference in the regulatory circuit involving miR-148a/DNMT1/OCT4 autophagy in male WJ-MSCs as compared to female cells. Moreover, no difference was detected in the expression of the two-differentiation regulating miRNA (miR-145 and miR-185). Taken together, our results highlight a different behavior of WJ-MSCs from males and females, disclosing the chance to better understand cellular processes as autophagy and stemness, usable for future clinical applications. Full article
(This article belongs to the Special Issue MicroRNAs and Stem Cells)
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16 pages, 5067 KiB  
Article
The Role of MicroRNAs in Early Chondrogenesis of Human Induced Pluripotent Stem Cells (hiPSCs)
by Ewelina Stelcer, Katarzyna Kulcenty, Marcin Rucinski, Karol Jopek, Magdalena Richter, Tomasz Trzeciak and Wiktoria Maria Suchorska
Int. J. Mol. Sci. 2019, 20(18), 4371; https://doi.org/10.3390/ijms20184371 - 05 Sep 2019
Cited by 18 | Viewed by 3277
Abstract
Human induced pluripotent stem cells (hiPSCs) play an important role in research regarding regenerative medicine. Particularly, chondrocytes differentiated from hiPSCs seems to be a promising solution for patients suffering from osteoarthritis. We decided to perform chondrogenesis in a three-week monolayer culture. Based on [...] Read more.
Human induced pluripotent stem cells (hiPSCs) play an important role in research regarding regenerative medicine. Particularly, chondrocytes differentiated from hiPSCs seems to be a promising solution for patients suffering from osteoarthritis. We decided to perform chondrogenesis in a three-week monolayer culture. Based on transcriptome analysis, hiPSC-derived chondrocytes (ChiPS) demonstrate the gene expression profile of cells from early chondrogenesis. Chondrogenic progenitors obtained by our group are characterized by significantly high expression of Hox genes, strongly upregulated during limb formation and morphogenesis. There are scanty literature data concerning the role of microRNAs in early chondrogenesis, especially in chondrogenic differentiation of hiPSCs. The main aim of this study was to investigate the microRNA expression profile and to select microRNAs (miRNAs) taking part in early chondrogenesis. Our findings allowed for selection crucial miRNAs engaged in both diminishing pluripotency state and chondrogenic process (inter alia hsa-miR-525-5p, hsa-miR-520c-3p, hsa-miR-628-3p, hsa-miR-196b-star, hsa-miR-629-star, hsa-miR-517b, has-miR-187). These miRNAs regulate early chondrogenic genes such as: HOXD10, HOXA11, RARB, SEMA3C. These results were confirmed by RT-qPCR analysis. This work contributes to a better understanding of the role of miRNAs directly involved in chondrogenic differentiation of hiPSCs. These data may result in the establishment of a more efficient protocol of obtaining chondrocyte-like cells from hiPSCs. Full article
(This article belongs to the Special Issue MicroRNAs and Stem Cells)
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14 pages, 2910 KiB  
Article
Functional Dissection of pri-miR-290~295 in Dgcr8 Knockout Mouse Embryonic Stem Cells
by Ming Shi, Jing Hao, Xi-Wen Wang, Le-Qi Liao, Huiqing Cao and Yangming Wang
Int. J. Mol. Sci. 2019, 20(18), 4345; https://doi.org/10.3390/ijms20184345 - 05 Sep 2019
Cited by 3 | Viewed by 2598
Abstract
The DiGeorge syndrome critical region gene 8 (Dgcr8) knockout strategy has been widely used to study the function of canonical microRNAs (miRNAs) in vitro and in vivo. However, primary miRNA (pri-miRNA) transcripts are accumulated in Dgcr8 knockout cells due to interrupted processing. Whether [...] Read more.
The DiGeorge syndrome critical region gene 8 (Dgcr8) knockout strategy has been widely used to study the function of canonical microRNAs (miRNAs) in vitro and in vivo. However, primary miRNA (pri-miRNA) transcripts are accumulated in Dgcr8 knockout cells due to interrupted processing. Whether abnormally accumulated pri-miRNAs have any function is unknown. Here, using clustered regularly interspaced short palindromic repeats system/CRISPR-associated protein 9 (CRISPR/Cas9), we successfully knocked out the primary microRNA-290~295 (pri-miR-290~295) cluster, the most highly expressed miRNA cluster in mouse embryonic stem cells (ESCs), in Dgcr8 knockout background. We found that the major defects associated with Dgcr8 knockout in mouse ESCs, including higher expression of epithelial-to-mesenchymal transition (EMT) markers, slower proliferation, G1 accumulation, and defects in silencing self-renewal, were not affected by the deletion of pri-miR-290~290 cluster. Interestingly, the transcription of neighboring gene nucleotide-binding oligomerization domain, leucine rich repeat and pyrin domain containing 12(Nlrp12) was upregulated upon the deletion of the pri-miR-290~295 cluster. Together, our results suggested that the major defects in Dgcr8 knockout ESCs were not due to the accumulation of pri-miR-290~295, and the deletion of miRNA genes could affect the transcription of neighboring DNA elements. Full article
(This article belongs to the Special Issue MicroRNAs and Stem Cells)
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16 pages, 3028 KiB  
Article
MicroRNA Profiling During Neural Differentiation of Induced Pluripotent Stem Cells
by Katarzyna Kulcenty, Joanna P Wroblewska, Marcin Rucinski, Emilia Kozlowska, Karol Jopek and Wiktoria M Suchorska
Int. J. Mol. Sci. 2019, 20(15), 3651; https://doi.org/10.3390/ijms20153651 - 26 Jul 2019
Cited by 23 | Viewed by 4577
Abstract
MicroRNAs (miRNA) play an essential role in the regulation of gene expression and influence signaling networks responsible for several cellular processes like differentiation of pluripotent stem cells. Despite several studies on the neurogenesis process, no global analysis of microRNA expression during differentiation of [...] Read more.
MicroRNAs (miRNA) play an essential role in the regulation of gene expression and influence signaling networks responsible for several cellular processes like differentiation of pluripotent stem cells. Despite several studies on the neurogenesis process, no global analysis of microRNA expression during differentiation of induced pluripotent stem cells (iPSC) to neuronal stem cells (NSC) has been done. Therefore, we compared the profile of microRNA expression in iPSC lines and in NSC lines derived from them, using microarray-based analysis. Two different protocols for NSC formation were used: Direct and two-step via neural rosette formation. We confirmed the new associations of previously described miRNAs in regulation of NSC differentiation from iPSC. We discovered upregulation of miR-10 family, miR-30 family and miR-9 family and downregulation of miR-302 and miR-515 family expression. Moreover, we showed that miR-10 family play a crucial role in the negative regulation of genes expression belonging to signaling pathways involved in neural differentiation: WNT signaling pathway, focal adhesion, and signaling pathways regulating pluripotency of stem cells. Full article
(This article belongs to the Special Issue MicroRNAs and Stem Cells)
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18 pages, 2366 KiB  
Article
Global MicroRNA Profiling Uncovers miR-206 as a Negative Regulator of Hematopoietic Commitment in Human Pluripotent Stem Cells
by Stéphane Flamant, Jean-Claude Chomel, Christophe Desterke, Olivier Féraud, Emilie Gobbo, Maria-Teresa Mitjavila-Garcia, Adlen Foudi, Frank Griscelli, Ali G. Turhan and Annelise Bennaceur-Griscelli
Int. J. Mol. Sci. 2019, 20(7), 1737; https://doi.org/10.3390/ijms20071737 - 08 Apr 2019
Cited by 1 | Viewed by 2634
Abstract
Although human pluripotent stem cells (hPSCs) can theoretically differentiate into any cell type, their ability to produce hematopoietic cells is highly variable from one cell line to another. The underlying mechanisms of this heterogeneity are not clearly understood. Here, using a whole miRNome [...] Read more.
Although human pluripotent stem cells (hPSCs) can theoretically differentiate into any cell type, their ability to produce hematopoietic cells is highly variable from one cell line to another. The underlying mechanisms of this heterogeneity are not clearly understood. Here, using a whole miRNome analysis approach in hPSCs, we discovered that their hematopoietic competency was associated with the expression of several miRNAs and conversely correlated to that of miR-206 specifically. Lentiviral-based miR-206 ectopic expression in H1 hematopoietic competent embryonic stem (ES) cells markedly impaired their differentiation toward the blood lineage. Integrative bioinformatics identified a potential miR-206 target gene network which included hematopoietic master regulators RUNX1 and TAL1. This work sheds light on the critical role of miR-206 in the generation of blood cells off hPSCs. Our results pave the way for future genetic manipulation of hPSCs aimed at increasing their blood regenerative potential and designing better protocols for the generation of bona fide hPSC-derived hematopoietic stem cells. Full article
(This article belongs to the Special Issue MicroRNAs and Stem Cells)
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Review

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23 pages, 1021 KiB  
Review
MicroRNA Signature in Human Normal and Tumoral Neural Stem Cells
by Andrea Diana, Giuseppe Gaido and Daniela Murtas
Int. J. Mol. Sci. 2019, 20(17), 4123; https://doi.org/10.3390/ijms20174123 - 23 Aug 2019
Cited by 23 | Viewed by 3555
Abstract
MicroRNAs, also called miRNAs or simply miR-, represent a unique class of non-coding RNAs that have gained exponential interest during recent years because of their determinant involvement in regulating the expression of several genes. Despite the increasing number of mature miRNAs recognized in [...] Read more.
MicroRNAs, also called miRNAs or simply miR-, represent a unique class of non-coding RNAs that have gained exponential interest during recent years because of their determinant involvement in regulating the expression of several genes. Despite the increasing number of mature miRNAs recognized in the human species, only a limited proportion is engaged in the ontogeny of the central nervous system (CNS). miRNAs also play a pivotal role during the transition of normal neural stem cells (NSCs) into tumor-forming NSCs. More specifically, extensive studies have identified some shared miRNAs between NSCs and neural cancer stem cells (CSCs), namely miR-7, -124, -125, -181 and miR-9, -10, -130. In the context of NSCs, miRNAs are intercalated from embryonic stages throughout the differentiation pathway in order to achieve mature neuronal lineages. Within CSCs, under a different cellular context, miRNAs perform tumor suppressive or oncogenic functions that govern the homeostasis of brain tumors. This review will draw attention to the most characterizing studies dealing with miRNAs engaged in neurogenesis and in the tumoral neural stem cell context, offering the reader insight into the power of next generation miRNA-targeted therapies against brain malignances. Full article
(This article belongs to the Special Issue MicroRNAs and Stem Cells)
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31 pages, 1856 KiB  
Review
Roles of MicroRNAs in Establishing and Modulating Stem Cell Potential
by Zhenwu Zhang, Lili Zhuang and Chao-Po Lin
Int. J. Mol. Sci. 2019, 20(15), 3643; https://doi.org/10.3390/ijms20153643 - 25 Jul 2019
Cited by 17 | Viewed by 5969 | Correction
Abstract
Early embryonic development in mammals, from fertilization to implantation, can be viewed as a process in which stem cells alternate between self-renewal and differentiation. During this process, the fates of stem cells in embryos are gradually specified, from the totipotent state, through the [...] Read more.
Early embryonic development in mammals, from fertilization to implantation, can be viewed as a process in which stem cells alternate between self-renewal and differentiation. During this process, the fates of stem cells in embryos are gradually specified, from the totipotent state, through the segregation of embryonic and extraembryonic lineages, to the molecular and cellular defined progenitors. Most of those stem cells with different potencies in vivo can be propagated in vitro and recapitulate their differentiation abilities. Complex and coordinated regulations, such as epigenetic reprogramming, maternal RNA clearance, transcriptional and translational landscape changes, as well as the signal transduction, are required for the proper development of early embryos. Accumulated studies suggest that Dicer-dependent noncoding RNAs, including microRNAs (miRNAs) and endogenous small-interfering RNAs (endo-siRNAs), are involved in those regulations and therefore modulate biological properties of stem cells in vitro and in vivo. Elucidating roles of these noncoding RNAs will give us a more comprehensive picture of mammalian embryonic development and enable us to modulate stem cell potencies. In this review, we will discuss roles of miRNAs in regulating the maintenance and cell fate potential of stem cells in/from mouse and human early embryos. Full article
(This article belongs to the Special Issue MicroRNAs and Stem Cells)
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Other

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2 pages, 679 KiB  
Correction
Correction: Zhang, Z.; et al. Roles of MicroRNAs in Establishing and Modulating Stem Cell Potential. Int. J. Mol. Sci. 2019, 20, 3643
by Zhenwu Zhang, Lili Zhuang and Chao-Po Lin
Int. J. Mol. Sci. 2020, 21(11), 3894; https://doi.org/10.3390/ijms21113894 - 29 May 2020
Cited by 2 | Viewed by 1554
Abstract
The authors wish to make the following correction to this paper [...] Full article
(This article belongs to the Special Issue MicroRNAs and Stem Cells)
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