The Expression and Functional Roles of miRNAs in Embryonic and Lineage-Specific Stem Cells

Author(s): Maryam Farzaneh , Masoumeh Alishahi , Zahra Derakhshan , Neda H. Sarani , Farnoosh Attari , Seyed E. Khoshnam* .

Journal Name: Current Stem Cell Research & Therapy

Volume 14 , Issue 3 , 2019

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Abstract:

The discovery of small non-coding RNAs began an interesting era in cellular and molecular biology. To date, miRNAs are the best recognized non-coding RNAs for maintenance and differentiation of pluripotent stem cells including embryonic stem cells (ES), induced pluripotent stem cells (iPSC), and cancer stem cells. ES cells are defined by their ability to self-renew, teratoma formation, and to produce numerous types of differentiated cells. Dual capacity of ES cells for self-renewal and differentiation is controlled by specific interaction with the neighboring cells and intrinsic signaling pathways from the level of transcription to translation. The ES cells have been the suitable model for evaluating the function of non-coding RNAs and in specific miRNAs. So far, the general function of the miRNAs in ES cells has been assessed in mammalian and non-mammalian stem cells. Nowadays, the evolution of sequencing technology led to the discovery of numerous miRNAs in human and mouse ES cells that their expression levels significantly changes during proliferation and differentiation. Several miRNAs have been identified in ectoderm, mesoderm, and endoderm cells, as well. This review would focus on recent knowledge about the expression and functional roles of miRNAs in embryonic and lineage-specific stem cells. It also describes that miRNAs might have essential roles in orchestrating the Waddington's landscape structure during development.

Keywords: Non-coding RNAs, microRNAs, stem cells, embryonic stem cells, lineage-specific stem cells, animal cells.

[1]
Wagers AJ, Weissman IL. Plasticity of adult stem cells. Cell 2004; 116: 639-48.
[2]
Gangaraju VK, Lin H. MicroRNAs: key regulators of stem cells. Nat Rev Mol Cell Biol 2009; 10: 116-25.
[3]
Avgustinova A, Benitah SA. Epigenetic control of adult stem cell function. Nat Rev Mol Cell Biol 2016; 17: 643-58.
[4]
Götz M, Huttner WB. The cell biology of neurogenesis. Nat Rev Mol Cell Biol 2005; 6: 777-88.
[5]
Kelava I, Lancaster MA. Stem cell models of human brain development. Cell Stem Cell 2016; 18: 736-48.
[6]
Leite CF, Almeida TR, Lopes CS, Dias da Silva VJ. Multipotent stem cells of the heart—do they have therapeutic promise? Front Physiol 2015; 6: 123.
[7]
Almada AE, Wagers AJ. Molecular circuitry of stem cell fate in skeletal muscle regeneration, ageing and disease. Nat Rev Mol Cell Biol 2016; 17: 267-79.
[8]
Wang LD, Wagers AJ. Dynamic niches in the origination and differentiation of haematopoietic stem cells. Nat Rev Mol Cell Biol 2011; 12: 643-55.
[9]
Goldman SA. Stem and progenitor cell-based therapy of the central nervous system: hopes, hype, and wishful thinking. Cell Stem Cell 2016; 18: 174-88.
[10]
Ito K, Suda T. Metabolic requirements for the maintenance of self-renewing stem cells. Nat Rev Mol Cell Biol 2014; 15: 243-56.
[11]
Farzaneh M, Attari F, Khoshnam SE. Concise review: LIN28/let-7 signaling, a critical double-negative feedback loop during pluripotency, reprogramming, and Tumorigenicity. Cell Reprogram 2017; 19: 289-93.
[12]
Russo F, Fiscon G, Conte F, Rizzo M, Paci P, Pellegrini M. Interplay between long noncoding RNAs and MicroRNAs in cancer. Methods Mol Biol 2018; 1819: 75-92.
[13]
Khoshnam SE, Winlow W, Farzaneh M. The interplay of MicroRNAs in the inflammatory mechanisms following ischemic stroke. J Neuropathol Exp Neurol 2017; 76: 548-61.
[14]
Kim VN, Han J, Siomi MC. Biogenesis of small RNAs in animals. Nat Rev Mol Cell Biol 2009; 10: 126-39.
[15]
Höck J, Meister G. The Argonaute protein family. Genome Biol 2008; 9: 210.
[16]
Hutvagner G, Simard MJ. Argonaute proteins: key players in RNA silencing. Nat Rev Mol Cell Biol 2008; 9: 22-32.
[17]
Lee Y, Kim M, Han J, et al. MicroRNA genes are transcribed by RNA polymerase II. EMBO J 2004; 23: 4051-60.
[18]
Gunaratne PH. Embryonic stem cell microRNAs: Defining factors in induced pluripotent (iPS) and cancer (CSC) stem cells? Curr Stem Cell Res Ther 2009; 4: 168-77.
[19]
Calvin Li S. T Vu L, Jianying Luo J, F Zhong J, Li Z. A Dethlefs B, G Loudon W, H Kabeer M, Tissue elasticity bridges cancer stem cells to the tumor microenvironment through micrornas: Implications for a “watch-and-wait” approach to cancer. Curr Stem Cell Res Ther 2017; 12: 455-70.
[20]
Meza-Sosa KF, Pedraza-Alva G, Pérez-Martínez L. microRNAs: key triggers of neuronal cell fate. Front Cell Neurosci 2014; 8: 175.
[21]
Vu LT, Keschrumrus V, Zhang X, et al. Tissue elasticity regulated tumor gene expression: implication for diagnostic biomarkers of primitive neuroectodermal tumor. PLoS One 2015; 10: e0120336.
[22]
Iovino N, Cavalli G. Rolling ES cells down the Waddington landscape with Oct4 and Sox2. Cell 2011; 145: 815-7.
[23]
Ferrell JE. Bistability, bifurcations, and Waddington’s epigenetic landscape. Curr Biol 2012; 22: R458-66.
[24]
Klattenhoff C, Theurkauf W. Biogenesis and germline functions of piRNAs. Development 2008; 135: 3-9.
[25]
Fatica A, Bozzoni I. Long non-coding RNAs: new players in cell differentiation and development. Nat Rev Genet 2014; 15: 7-21.
[26]
Khoshnam SE, Winlow W, Farbood Y, Moghaddam HF, Farzaneh M. Emerging roles of microRNAs in ischemic stroke: as possible therapeutic agents. J Stroke 2017; 19: 166.
[27]
Brodersen P, Voinnet O. Revisiting the principles of microRNA target recognition and mode of action. Nat Rev Mol Cell Biol 2009; 10: 141-8.
[28]
Okamura K, Lai EC. Endogenous small interfering RNAs in animals. Nat Rev Mol Cell Biol 2008; 9: 673-8.
[29]
Li Z, Rana TM. Therapeutic targeting of microRNAs: Current status and future challenges. Nat Rev Drug Discov 2014; 13: 622-38.
[30]
Inui M, Martello G, Piccolo S. MicroRNA control of signal transduction. Nat Rev Mol Cell Biol 2010; 11: 252-63.
[31]
Rottiers V, Näär AM. MicroRNAs in metabolism and metabolic disorders. Nat Rev Mol Cell Biol 2012; 13: 239-50.
[32]
Carthew RW, Sontheimer EJ. Origins and mechanisms of miRNAs and siRNAs. Cell 2009; 136: 642-55.
[33]
McManus MT, Sharp PA. Gene silencing in mammals by small interfering RNAs. Nat Rev Genet 2002; 3: 737-47.
[34]
Zhou X, Liao Z, Jia Q, Cheng L, Li F. Identification and characterization of Piwi subfamily in insects. Biochem Biophys Res Commun 2007; 362: 126-31.
[35]
De Wert G, Mummery C. Human embryonic stem cells: research, ethics and policy. Hum Reprod 2003; 18: 672-82.
[36]
Rutnam ZJ, Wight TN, Yang BB. miRNAs regulate expression and function of extracellular matrix molecules. Matrix Biol 2013; 32: 74-85.
[37]
Sakamoto N, Honma R, Sekino Y, et al. Non-coding RNAs are promising targets for stem cell-based cancer therapy. Noncoding RNA Res 2017; 2: 83-7.
[38]
Morin RD, O’Connor MD, Griffith M, et al. Application of massively parallel sequencing to microRNA profiling and discovery in human embryonic stem cells. Genome Res 2008; 18: 610-21.
[39]
Hafner M, Landgraf P, Ludwig J, et al. Identification of microRNAs and other small regulatory RNAs using cDNA library sequencing. Methods 2008; 44: 3-12.
[40]
Bartel DP. MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell 2004; 116: 281-97.
[41]
Bernstein E, Kim SY, Carmell MA, et al. Dicer is essential for mouse development. Nat Genet 2003; 35: 215-7.
[42]
Wang Y, Medvid R, Melton C, Jaenisch R, Blelloch R. DGCR8 is essential for microRNA biogenesis and silencing of embryonic stem cell self-renewal. Nat Genet 2007; 39: 380-5.
[43]
Takeshita F, Patrawala L, Osaki M, et al. Systemic delivery of synthetic microRNA-16 inhibits the growth of metastatic prostate tumors via downregulation of multiple cell-cycle genes. Mol Ther 2010; 18: 181-7.
[44]
Bueno MJ, Malumbres M. MicroRNAs and the cell cycle. BBA-Mol Basis Dis 2011; 1812: 592-601.
[45]
Wang Y, Baskerville S, Shenoy A, Babiarz JE, Baehner L, Blelloch R. Embryonic stem cell–specific microRNAs regulate the G1-S transition and promote rapid proliferation. Nat Genet 2008; 40: 1478-83.
[46]
Suh M-R, Lee Y, Kim JY, et al. Human embryonic stem cells express a unique set of microRNAs. Dev Biol 2004; 270: 488-98.
[47]
Singh SK, Kagalwala MN, Parker-Thornburg J, Adams H, Majumder S. REST maintains self-renewal and pluripotency of embryonic stem cells. Nature 2008; 453: 223-7.
[48]
Xu N, Papagiannakopoulos T, Pan G, Thomson JA, Kosik KS. MicroRNA-145 regulates OCT4, SOX2, and KLF4 and represses pluripotency in human embryonic stem cells. Cell 2009; 137: 647-58.
[49]
Tay Y, Zhang J, Thomson AM, Lim B, Rigoutsos I. MicroRNAs to Nanog, Oct4 and Sox2 coding regions modulate embryonic stem cell differentiation. Nature 2008; 455: 1124-8.
[50]
Viswanathan SR, Daley GQ, Gregory RI. Selective blockade of microRNA processing by Lin28. Science 2008; 320: 97-100.
[51]
Judson RL, Babiarz J, Venere M, Blelloch R. Embryonic stem cell specific microRNAs promote induced pluripotency. Nat Biotechnol 2009; 27: 459.
[52]
Benetti R, Gonzalo S, Jaco I, et al. A mammalian microRNA cluster controls DNA methylation and telomere recombination via Rbl2-dependent regulation of DNA methyltransferases. Nat Struct Mol Biol 2008; 15: 268-79.
[53]
Kaspi H, Chapnik E, Levy M, Beck G, Hornstein E, Soen Y. Brief report: miR‐290–295 regulate embryonic stem cell differentiation propensities by repressing pax6. Stem Cells 2013; 31: 2266-72.
[54]
Goldberg AD, Allis CD, Bernstein E. Epigenetics: A landscape takes shape. Cell 2007; 4: 635-8.
[55]
Tronick E, Hunter RG. Waddington, dynamic systems, and epigenetics. Front Behav Neurosci 2016; 10: 107.
[56]
Gage FH. Mammalian neural stem cells. Science 2000; 287: 1433-8.
[57]
Maiorano NA, Mallamaci A. Promotion of embryonic cortico-cerebral neuronogenesis by miR-124. Neural Dev 2009; 4: 40.
[58]
Tay YMS, Tam WL, Ang YS, et al. MicroRNA‐134 modulates the differentiation of mouse embryonic stem cells, where it causes post‐transcriptional attenuation of Nanog and LRH1. Stem Cells 2008; 26: 17-29.
[59]
Niu CS, Yang Y, Cheng C-D. MiR-134 regulates the proliferation and invasion of glioblastoma cells by reducing Nanog expression. Int J Oncol 2013; 42: 1533-40.
[60]
Zhao C, Sun G, Li S, Shi Y. A feedback regulatory loop involving microRNA-9 and nuclear receptor TLX in neural stem cell fate determination. Nat Struct Mol Biol 2009; 16: 365-71.
[61]
Delaloy C, Liu L, Lee J-A, et al. MicroRNA-9 coordinates proliferation and migration of human embryonic stem cell-derived neural progenitors. Cell Stem Cell 2010; 6: 323-35.
[62]
Bonev B, Pisco A, Papalopulu N. MicroRNA-9 reveals regional diversity of neural progenitors along the anterior-posterior axis. Dev Cell 2011; 20: 19-32.
[63]
Zhao C, Sun G, Li S, et al. MicroRNA let-7b regulates neural stem cell proliferation and differentiation by targeting nuclear receptor TLX signaling. Proc Natl Acad Sci USA 2010; 107: 1876-81.
[64]
Solanas G, Benitah SA. Regenerating the skin: A task for the heterogeneous stem cell pool and surrounding niche. Nat Struct Mol Biol 2013; 14: 737-48.
[65]
Shenoy A, Blelloch RH. Regulation of microRNA function in somatic stem cell proliferation and differentiation. Nat Struct Mol Biol 2014; 15: 565-76.
[66]
Hsu Y-C, Li L, Fuchs E. Emerging interactions between skin stem cells and their niches. Nat Med 2014; 20: 847-56.
[67]
Goodell MA, Nguyen H, Shroyer N. Somatic stem cell heterogeneity: diversity in the blood, skin and intestinal stem cell compartments. Nat Struct Mol Biol 2015; 16: 299-309.
[68]
Vagnozzi AN, Reiter JF, Wong SY. Hair follicle and interfollicular epidermal stem cells make varying contributions to wound regeneration. Cell Cycle 2015; 14: 3408-17.
[69]
Yi R, Poy MN, Stoffel M, Fuchs E. A skin microRNA promotes differentiation by repressing ‘stemness’. Nature 2008; 452: 225-9.
[70]
Yu J, Ryan DG, Getsios S, Oliveira-Fernandes M, Fatima A, Lavker RM. MicroRNA-184 antagonizes microRNA-205 to maintain SHIP2 levels in epithelia. Proc Natl Acad Sci USA 2008; 105: 19300-5.
[71]
Jackson SJ, Zhang Z, Feng D, et al. Rapid and widespread suppression of self-renewal by microRNA-203 during epidermal differentiation. Development 2013; 140: 1882-91.
[72]
Candi E, Amelio I, Agostini M, Melino G. MicroRNAs and p63 in epithelial stemness. Cell Death Differ 2015; 22: 12-21.
[73]
Braun T, Gautel M. Transcriptional mechanisms regulating skeletal muscle differentiation, growth and homeostasis. Nat Struct Mol Biol 2011; 12: 349-61.
[74]
Buckingham M. Myogenic progenitor cells and skeletal myogenesis in vertebrates. Curr Opin Genet Dev 2006; 16: 525-32.
[75]
Ge Y, Chen J. MicroRNAs in skeletal myogenesis. Cell Cycle 2011; 10: 441-8.
[76]
Wang YX, Rudnicki MA. Satellite cells, the engines of muscle repair. Nat Struct Mol Biol 2012; 13: 127-33.
[77]
Purvis N, Bahn A, Katare R. The role of microRNAs in cardiac stem cells. Stem Cells Int 2015; 2015: 194894.
[78]
O’Rourke JR, Georges SA, Seay HR, et al. Essential role for Dicer during skeletal muscle development. Dev Biol 2007; 311: 359-68.
[79]
Chen J-F, Mandel EM, Thomson JM, et al. The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation. Nat Genet 2006; 38: 228-33.
[80]
Ivey KN, Muth A, Arnold J, et al. MicroRNA regulation of cell lineages in mouse and human embryonic stem cells. Cell Stem Cell 2008; 2: 219-29.
[81]
Wang H, Garzon R, Sun H, et al. NF-κB–YY1–miR-29 regulatory circuitry in skeletal myogenesis and rhabdomyosarcoma. Cancer Cell 2008; 14: 369-81.
[82]
Wong CF, Tellam RL. MicroRNA-26a targets the histone methyltransferase Enhancer of Zeste homolog 2 during myogenesis. J Biol Chem 2008; 283: 9836-43.
[83]
Caretti G, Di Padova M, Micales B, Lyons GE, Sartorelli V. The Polycomb Ezh2 methyltransferase regulates muscle gene expression and skeletal muscle differentiation. Genes Dev 2004; 18: 2627-38.
[84]
Rao PK, Kumar RM, Farkhondeh M, Baskerville S, Lodish HF. Myogenic factors that regulate expression of muscle-specific microRNAs. Proc Natl Acad Sci USA 2006; 103: 8721-6.
[85]
Zhao Y, Samal E, Srivastava D. Serum response factor regulates a muscle-specific microRNA that targets Hand2 during cardiogenesis. Nature 2005; 436: 214-20.
[86]
Jang Y-N, Baik EJ. JAK-STAT pathway and myogenic differentiation. JAK-STAT 2013; 2: e23282.
[87]
Liu N, Nelson BR, Bezprozvannaya S, et al. Requirement of MEF2A, C, and D for skeletal muscle regeneration. Proc Natl Acad Sci USA 2014; 111: 4109-14.
[88]
Sun Q, Zhang Y, Yang G, et al. Transforming growth factor-β-regulated miR-24 promotes skeletal muscle differentiation. Nucleic Acids Res 2008; 36: 2690-9.
[89]
Ohgushi H. Osteogenically differentiated mesenchymal stem cells and ceramics for bone tissue engineering. Expert Opin Biol Ther 2014; 14: 197-208.
[90]
Heino TJ, Hentunen TA. Differentiation of osteoblasts and osteocytes from mesenchymal stem cells. Curr Stem Cell Res Ther 2008; 3: 131-45.
[91]
Lian JB, Stein GS, Van Wijnen AJ, et al. MicroRNA control of bone formation and homeostasis. Nat Rev Endocrinol 2012; 8: 212-27.
[92]
Luzi E, Marini F, Sala SC, Tognarini I, Galli G, Brandi ML. Osteogenic differentiation of human adipose tissue‐derived stem cells is modulated by the miR‐26a targeting of the SMAD1 transcription factor. J Bone Miner Res 2008; 23: 287-95.
[93]
Zeng Y, Qu X, Li H, et al. MicroRNA‐100 regulates osteogenic differentiation of human adipose‐derived mesenchymal stem cells by targeting BMPR2. FEBS Lett 2012; 586: 2375-81.
[94]
Kim YJ, Bae SW, Yu SS, Bae YC, Jung JS. miR‐196a regulates proliferation and osteogenic differentiation in mesenchymal stem cells derived from human adipose tissue. J Bone Miner Res 2009; 24: 816-25.
[95]
Zhang J-f, Fu W-m, He M-l, et al. MiRNA-20a promotes osteogenic differentiation of human mesenchymal stem cells by co-regulating BMP signaling. RNA Biol 2011; 8: 829-38.
[96]
Phimphilai M, Zhao Z, Boules H, Roca H, Franceschi RT. BMP signaling is required for RUNX2‐dependent induction of the osteoblast phenotype. J Bone Miner Res 2006; 21: 637-46.
[97]
Zheng L, Tu Q, Meng S, et al. Runx2/dicer/mirna pathway in regulating osteogenesis. J Cell Physiol 2017; 232: 182-91.
[98]
Tiago DM, Marques CL, Roberto VP, Cancela ML, Laizé V. Mir-20a regulates in vitro mineralization and BMP signaling pathway by targeting BMP-2 transcript in fish. Arch Biochem Biophys 2014; 543: 23-30.
[99]
Tu XM, Gu YL, Ren GQ. miR-125a-3p targetedly regulates GIT1 expression to inhibit osteoblastic proliferation and differentiation. Exp Ther Med 2016; 12: 4099-106.
[100]
Eskildsen T, Taipaleenmäki H, Stenvang J, et al. MicroRNA-138 regulates osteogenic differentiation of human stromal (mesenchymal) stem cells in vivo. Proc Natl Acad Sci USA 2011; 108: 6139-44.
[101]
Chung SS, Hu W, Park CY. The role of microRNAs in hematopoietic stem cell and leukemic stem cell function. Ther Adv Hematol 2011; 2: 317-34.
[102]
Hong SH, Kim KS, Oh IH. Concise review: Exploring miRNAs—Toward a better understanding of hematopoiesis. Stem Cells 2015; 33: 1-7.
[103]
Georgantas RW, Hildreth R, Morisot S, et al. CD34+ hematopoietic stem-progenitor cell microRNA expression and function: a circuit diagram of differentiation control. Proc Natl Acad Sci 2007; 104: 2750-5.
[104]
Lechman ER, Gentner B, van Galen P, et al. Attenuation of miR-126 activity expands HSC in vivo without exhaustion. Cell Stem Cell 2012; 11: 799-811.
[105]
Rathjen T, Nicol C, McConkey G, Dalmay T. Analysis of short RNAs in the malaria parasite and its red blood cell host. FEBS Lett 2006; 580: 5185-8.
[106]
Dore LC, Amigo JD, Dos Santos CO, et al. A GATA-1-regulated microRNA locus essential for erythropoiesis. Proc Natl Acad Sci USA 2008; 105: 3333-8.
[107]
Wang Q, Huang Z, Xue H, et al. MicroRNA miR-24 inhibits erythropoiesis by targeting activin type I receptor ALK4. Blood 2008; 111: 588-95.
[108]
Zhao H, Kalota A, Jin S, Gewirtz AM. The c-myb proto-oncogene and microRNA-15a comprise an active autoregulatory feedback loop in human hematopoietic cells. Blood 2009; 113: 505-16.
[109]
Felli N, Pedini F, Romania P, et al. MicroRNA 223-dependent expression of LMO2 regulates normal erythropoiesis. Haematol 2009; 94: 479-86.
[110]
Felli N, Fontana L, Pelosi E, et al. MicroRNAs 221 and 222 inhibit normal erythropoiesis and erythroleukemic cell growth via kit receptor down-modulation. Proc Natl Acad Sci USA 2005; 102: 18081-6.
[111]
Vian L, Di Carlo M, Pelosi E, et al. Transcriptional fine-tuning of microRNA-223 levels directs lineage choice of human hematopoietic progenitors. Cell Death Differ 2014; 21: 290-301.
[112]
Bruchova H, Yoon D, Agarwal AM, Mendell J, Prchal JT. Regulated expression of microRNAs in normal and polycythemia vera erythropoiesis. Exp Hematol 2007; 35: 1657-67.
[113]
Fontana L, Pelosi E, Greco P, et al. MicroRNAs 17-5p–20a–106a control monocytopoiesis through AML1 targeting and M-CSF receptor upregulation. Nat Cell Biol 2007; 9: 775-87.
[114]
Rosa A, Ballarino M, Sorrentino A, et al. The interplay between the master transcription factor PU. 1 and miR-424 regulates human monocyte/macrophage differentiation. Proc Natl Acad Sci 2007; 104: 19849-54.
[115]
Zhou B, Wang S, Mayr C, Bartel DP, Lodish HF. miR-150, a microRNA expressed in mature B and T cells, blocks early B cell development when expressed prematurely. Proc Natl Acad Sci 2007; 104: 7080-5.
[116]
Hinton A, Afrikanova I, Wilson M, et al. A distinct microRNA signature for definitive endoderm derived from human embryonic stem cells. Stem Cells Dev 2009; 19: 797-807.
[117]
Poy MN, Eliasson L, Krutzfeldt J, et al. A pancreatic islet-specific microRNA regulates insulin secretion. Nature 2004; 432: 226-30.
[118]
Fogel GB, Kai ZS, Zargar S, et al. MicroRNA dynamics during human embryonic stem cell differentiation to pancreatic endoderm. Gene 2015; 574: 359-70.
[119]
Vidigal JA, Ventura A. Semin Cancer Biol Elsevier 2012; 428-36.
[120]
Zorn AM, Wells JM. Molecular basis of vertebrate endoderm development. Int Rev Cytol 2007; 259: 49-111.
[121]
Tian Y, Zhang Y, Hurd L, et al. Regulation of lung endoderm progenitor cell behavior by miR302/367. Development 2011; 138: 1235-45.
[122]
Tzur G, Levy A, Meiri E, et al. MicroRNA expression patterns and function in endodermal differentiation of human embryonic stem cells. PLoS One 2008; 3: e3726.
[123]
Esau C, Davis S, Murray SF, et al. miR-122 regulation of lipid metabolism revealed by in vivo antisense targeting. Cell Metab 2006; 3: 87-98.
[124]
McKenna LB, Schug J, Vourekas A, et al. MicroRNAs control intestinal epithelial differentiation, architecture, and barrier function. Gastroenterolo 2010. 139: 1654-1664. e1651.
[125]
Wu W. MicroRNA: Potential targets for the development of novel drugs? Drugs R D 2010; 10: 1-8.
[126]
Kishore R, Verma SK, Mackie AR, et al. Bone marrow progenitor cell therapy-mediated paracrine regulation of cardiac miRNA-155 modulates fibrotic response in diabetic hearts. PLoS One 2013; 8: e60161.
[127]
Garikipati VNS, Krishnamurthy P, Verma SK, et al. Negative Regulation of miR‐375 by Interleukin‐10 Enhances Bone Marrow‐Derived Progenitor Cell‐Mediated Myocardial Repair and Function After Myocardial Infarction. Stem Cells 2015; 33: 3519-29.
[128]
Toba H, Cortez D, Lindsey ML, Chilton RJ. Applications of miRNA technology for atherosclerosis. Curr Atheroscler Rep 2014; 16: 386.
[129]
Harrandah AM, Mora RA, Chan EK. Emerging microRNAs in cancer diagnosis, progression, and immune surveillance. Cancer Lett 2018; 438: 126-32.


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VOLUME: 14
ISSUE: 3
Year: 2019
Page: [278 - 289]
Pages: 12
DOI: 10.2174/1574888X14666190123162402
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