Therapeutic Implications of miRNAs for Muscle-Wasting Conditions

Laura Yedigaryan; Maurilio Sampaolesi

doi:10.3390/cells10113035

journal article Open Access Nov 05, 2021

Therapeutic Implications of miRNAs for Muscle-Wasting Conditions

Laura Yedigaryan

Maurilio Sampaolesi

Cells Vol. 10 No. 11 pp. 3035 · MDPI AG

View at Publisher Save 10.3390/cells10113035

Abstract

MicroRNAs (miRNAs) are small, non-coding RNA molecules that are mainly involved in translational repression by binding to specific messenger RNAs. Recently, miRNAs have emerged as biomarkers, relevant for a multitude of pathophysiological conditions, and cells can selectively sort miRNAs into extracellular vesicles for paracrine and endocrine effects. In the overall context of muscle-wasting conditions, a multitude of miRNAs has been implied as being responsible for the typical dysregulation of anabolic and catabolic pathways. In general, chronic muscle disorders are associated with the main characteristic of a substantial loss in muscle mass. Muscular dystrophies (MDs) are a group of genetic diseases that cause muscle weakness and degeneration. Typically, MDs are caused by mutations in those genes responsible for upholding the integrity of muscle structure and function. Recently, the dysregulation of miRNA levels in such pathological conditions has been reported. This revelation is imperative for both MDs and other muscle-wasting conditions, such as sarcopenia and cancer cachexia. The expression levels of miRNAs have immense potential for use as potential diagnostic, prognostic and therapeutic biomarkers. Understanding the role of miRNAs in muscle-wasting conditions may lead to the development of novel strategies for the improvement of patient management.

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References

158

[1]

Boyer "Myogenic Cell Transplantation in Genetic and Acquired Diseases of Skeletal Muscle" Front. Genet. (2021) 10.3389/fgene.2021.702547

[2]

Cassano "Cellular mechanisms and local progenitor activation to regulate skeletal muscle mass" J. Muscle Res. Cell Motil. (2009) 10.1007/s10974-010-9204-y

[3]

Hamilton "Role of microRNA in muscle regeneration and diseases related to muscle dysfunction in atrophy, cachexia, osteoporosis, and osteoarthritis" Bone Jt. Res. (2020) 10.1302/2046-3758.911.bjr-2020-0178.r1

[4]

Gu "Regulating gene expression in animals through RNA endonucleolytic cleavage" Heliyon (2018) 10.1016/j.heliyon.2018.e00908

[5]

Alles "An estimate of the total number of true human miRNAs" Nucleic Acids Res. (2019) 10.1093/nar/gkz097

[6]

Giarratana "MICAL2 is essential for myogenic lineage commitment" Cell Death Dis. (2020) 10.1038/s41419-020-02886-z

[7]

Ronzoni, F.L., Giarratana, N., Crippa, S., Quattrocelli, M., Cassano, M., Ceccarelli, G., Benedetti, L., Van Herck, J., De Angelis, M.G.C., and Vitale, M. (2021). Guide Cells Support Muscle Regeneration and Affect Neuro-Muscular Junction Organization. Int. J. Mol. Sci., 22. 10.3390/ijms22041939

[8]

Giacomazzi "MicroRNAs promote skeletal muscle differentiation of mesodermal iPSC-derived progenitors" Nat. Commun. (2017) 10.1038/s41467-017-01359-w

[9]

Ronzoni "Met-Activating Genetically Improved Chimeric Factor-1 Promotes Angiogenesis and Hypertrophy in Adult Myogenesis" Curr. Pharm. Biotechnol. (2017) 10.2174/1389201018666170201124602

[10]

Pozzo "Upregulation of miR181a/miR212 Improves Myogenic Commitment in Murine Fusion-Negative Rhabdomyosarcoma" Front. Physiol. (2021) 10.3389/fphys.2021.701354

[11]

Cheung "Maintenance of muscle stem-cell quiescence by microRNA-489" Nature (2012) 10.1038/nature10834

[12]

Georges "Essential role for Dicer during skeletal muscle development" Dev. Biol. (2007) 10.1016/j.ydbio.2007.08.032

[13]

Hill "miRNA interplay: Mechanisms and consequences in cancer" Dis. Model. Mech. (2021) 10.1242/dmm.047662

[14]

Gregory "The Microprocessor complex mediates the genesis of microRNAs" Nature (2004) 10.1038/nature03120

[15]

The nuclear RNase III Drosha initiates microRNA processing

Yoontae Lee, Chiyoung Ahn, Jinju Han et al.

Nature 2003 10.1038/nature01957

[16]

Lund "Nuclear Export of MicroRNA Precursors" Science (2004) 10.1126/science.1090599

[17]

Bernstein "Role for a bidentate ribonuclease in the initiation step of RNA interference" Nature (2001) 10.1038/35053110

[18]

Song "Crystal Structure of Argonaute and Its Implications for RISC Slicer Activity" Science (2004) 10.1126/science.1102514

[19]

Schwarz "Asymmetry in the Assembly of the RNAi Enzyme Complex" Cell (2003) 10.1016/s0092-8674(03)00759-1

[20]

BioRender.com (2021, October 28). microRNA in Cancer. Available online: https://app.biorender.com/biorender-templates.

[21]

Koutsoulidou "Identification of exosomal muscle-specific miRNAs in serum of myotonic dystrophy patients relating to muscle disease progress" Hum. Mol. Genet. (2017) 10.1093/hmg/ddx212

[22]

Arroyo "Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma" Proc. Natl. Acad. Sci. USA (2011) 10.1073/pnas.1019055108

[23]

Turchinovich "Distinct AGO1 and AGO2 associated miRNA profiles in human cells and blood plasma" RNA Biol. (2012) 10.4161/rna.21083

[24]

Turchinovich "Characterization of extracellular circulating microRNA" Nucleic Acids Res. (2011) 10.1093/nar/gkr254

[25]

Vickers "MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins" Nature (2011)

[26]

Wagner "Characterization of Levels and Cellular Transfer of Circulating Lipoprotein-Bound MicroRNAs" Arter. Thromb. Vasc. Biol. (2013) 10.1161/atvbaha.112.300741

[27]

Barone "Skeletal muscle Heat shock protein 60 increases after endurance training and induces peroxisome proliferator-activated receptor gamma coactivator 1 α1 expression" Sci. Rep. (2016) 10.1038/srep19781

[28]

Marceca "MicroRNAs in Skeletal Muscle and Hints on Their Potential Role in Muscle Wasting During Cancer Cachexia" Front. Oncol. (2020) 10.3389/fonc.2020.607196

[29]

McCarthy "MicroRNA-206: The skeletal muscle-specific myomiR" Biochim. Biophys. Acta Bioenerg. (2008) 10.1016/j.bbagrm.2008.03.001

[30]

Sempere "Expression profiling of mammalian microRNAs uncovers a subset of brain-expressed microRNAs with possible roles in murine and human neuronal differentiation" Genome Biol. (2004) 10.1186/gb-2004-5-3-r13

[31]

Small "Regulation of PI3-kinase/Akt signaling by muscle-enriched microRNA-486" Proc. Natl. Acad. Sci. USA (2010) 10.1073/pnas.1000300107

[32]

Quiat "A Family of microRNAs Encoded by Myosin Genes Governs Myosin Expression and Muscle Performance" Dev. Cell (2009) 10.1016/j.devcel.2009.10.013

[33]

Aranega "Identification of regulatory elements directing miR-23a–miR-27a–miR-24-2 transcriptional regulation in response to muscle hypertrophic stimuli" Biochim. Biophys. Acta Bioenerg. (2014) 10.1016/j.bbagrm.2014.07.009

[34]

Perry "Molecular mechanisms regulating myogenic determination and differentiation" Front. Biosci. J. Virtual Libr. (2000) 10.2741/perry

[35]

Rao "Myogenic factors that regulate expression of muscle-specific microRNAs" Proc. Natl. Acad. Sci. USA (2006) 10.1073/pnas.0602831103

[36]

Pais "Regulation of multiple target genes by miR-1/miR-206 is pivotal for C2C12 myoblast differentiation" J. Cell Sci. (2012) 10.1242/jcs.101758

[37]

Yin "ClC-3 is required for LPA-activated Cl− current activity and fibroblast-to-myofibroblast differentiation" Am. J. Physiol. Physiol. (2008) 10.1152/ajpcell.00291.2007

[38]

Habas "Wnt/Frizzled Activation of Rho Regulates Vertebrate Gastrulation and Requires a Novel Formin Homology Protein Daam1" Cell (2001) 10.1016/s0092-8674(01)00614-6

[39]

Kennedy "Retinoic acid enhances skeletal muscle progenitor formation and bypasses inhibition by bone morphogenetic protein 4 but not dominant negative beta-catenin" BMC Biol. (2009) 10.1186/1741-7007-7-67

[40]

Zheng "Identification of Happyhour/MAP4K as Alternative Hpo/Mst-like Kinases in the Hippo Kinase Cascade" Dev. Cell (2015) 10.1016/j.devcel.2015.08.014

[41]

Alteri "Cyclin D1 is a major target of miR-206 in cell differentiation and transformation" J. Cell Biol. (2013)

[42]

Kim "Muscle-specific microRNA miR-206 promotes muscle differentiation" J. Cell Biol. (2006) 10.1083/jcb.200603008

[43]

Li "Downregulation of microRNAs miR-1, -206 and -29 stabilizes PAX3 and CCND2 expression in rhabdomyosarcoma" Lab. Investig. J. Tech. Methods Pathol. (2012) 10.1038/labinvest.2012.10

[44]

Winbanks, C.E., Beyer, C., Hagg, A., Qian, H., Sepulveda, P.V., and Gregorevic, P. (2013). miR-206 Represses Hypertrophy of Myogenic Cells but Not Muscle Fibers via Inhibition of HDAC4. PLoS ONE, 8. 10.1371/journal.pone.0073589

[45]

Koutsoulidou, A., Kyriakides, T.C., Papadimas, G.K., Christou, Y., Kararizou, E., Papanicolaou, E.Z., and Phylactou, L.A. (2015). Elevated Muscle-Specific miRNAs in Serum of Myotonic Dystrophy Patients Relate to Muscle Disease Progress. PLoS ONE, 10. 10.1371/journal.pone.0125341

[46]

Ivey "MicroRNA Regulation of Cell Lineages in Mouse and Human Embryonic Stem Cells" Cell Stem Cell (2008) 10.1016/j.stem.2008.01.016

[47]

Chen "The Role of MicroRNA-1 and MicroRNA-133 in Skeletal Muscle Proliferation and Differentiation" Nat. Genet. (2005) 10.1038/ng1725

[48]

Boutz "MicroRNAs regulate the expression of the alternative splicing factor nPTB during muscle development" Genes Dev. (2007) 10.1101/gad.1500707

[49]

Luo "microRNA133a TargetsFoxl2and Promotes Differentiation of C2C12 into Myogenic Progenitor Cells" DNA Cell Biol. (2015) 10.1089/dna.2014.2522

[50]

Dai "MicroRNA-133b stimulates ovarian estradiol synthesis by targeting Foxl2" FEBS Lett. (2013) 10.1016/j.febslet.2013.06.023

Showing 50 of 158 references

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Details

Published: Nov 05, 2021
Vol/Issue: 10(11)
Pages: 3035
License: View

Authors

L

Laura Yedigaryan

Translational Cardiomyology Laboratory, Stem Cell Biology and Embryology, Department of Development and Regeneration, KU Leuven, 3000 Leuven, Belgium

M

Maurilio Sampaolesi

Translational Cardiomyology Laboratory, Stem Cell Biology and Embryology, Department of Development and Regeneration, KU Leuven, 3000 Leuven, Belgium; Histology and Medical Embryology Unit, Department of Anatomy, Histology, Forensic Medicine and Orthopedics, Sapienza University of Rome, 00185 Rome, Italy

Funding

Research Foundation - Flanders Award: FWO (G0D4517N)

INTERREG – Euregio Meuse-Rhine – Generate your muscle (GYM) Award: 2020-EMR116

C1-KUL 3DMUSYC Award: C14/17/111

Rondoufonds voor Duchenne Onderzoek Award: EQQ-FODUCHO2010

Cite This Article

Laura Yedigaryan, Maurilio Sampaolesi (2021). Therapeutic Implications of miRNAs for Muscle-Wasting Conditions. Cells, 10(11), 3035. https://doi.org/10.3390/cells10113035

Therapeutic Implications of miRNAs for Muscle-Wasting Conditions

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