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Regulation of Skeletal Muscle by microRNAs

Gabriela Placoná Diniz, Da‐Zhi Wang

10.1002/cphy.c150041

Source: Volume 6, Issue 3, July 2016

Published online: June 2016

Full Article on Wiley Online Library



ABSTRACT

MicroRNAs (miRNAs) are a class of small noncoding RNAs highly conserved across species. miRNAs regulate gene expression posttranscriptionally by base pairing to complementary sequences mainly in the 3′‐untranslated region of their target mRNAs to induce mRNA cleavage and translational repression. Thousands of miRNAs have been identified in human and their function has been linked to the regulation of both physiological and pathological processes. The skeletal muscle is the largest human organ responsible for locomotion, posture, and body metabolism. Several conditions such as aging, immobilization, exercise, and diet are associated with alterations in skeletal muscle structure and function. The genetic and molecular pathways that regulate muscle development, function, and regeneration as well as muscular disease have been well established in past decades. In recent years, numerous studies have underlined the importance of miRNAs in the control of skeletal muscle development and function, through its effects on several biological pathways critical for skeletal muscle homeostasis. Furthermore, it has become clear that alteration of the expression of many miRNAs or genetic mutations of miRNA genes is associated with changes on myogenesis and on progression of several skeletal muscle diseases. The present review provides an overview of the current studies and recent progress in elucidating the complex role exerted by miRNAs on skeletal muscle physiology and pathology. © 2016 American Physiological Society. Compr Physiol 6:1279‐1294, 2016.

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Figure 1. Figure 1. Schematic representation of biogenesis of miRNAs and the mechanism of their action. The miRNA gene is transcribed into miRNA primary transcript (Pri miRNA), resulting in a long hairpin structure that contains a 5′ cap and 3′ poly (A) tail. Then, the Pri miRNA is cleaved by Drosha RNase III and cofactors, which releases the pre‐miRNA. The pre‐miRNA is exported into the cytoplasm, and is processed by RNAse III Dicer, into miRNA duplex of ∼20 to 25 nt. Then, the miRNA duplex is separated by action of AGO2, and one miRNA strand is loaded onto an AGO protein to form the RISC. The RISC functions as a guide by base pairing miRNA with its target mRNAs, inducing mRNA cleavage, mRNA deadenylation, and translation repression.
Figure 2. Figure 2. Schematic representation of miRNAs involved in myogenesis. The maintenance of skeletal muscle stem cell quiescence is controlled by miR‐195, miR‐489, and miR‐497 by suppressing Cdc25a, Ccnd2, and Dek, respectively. The entry into the myogenic program is influenced by miR‐1, miR‐27, miR‐133, miR‐206, and miR‐486 by targeting Pax7, Pax3, Mstn, and SRF, respectively. Myoblast differentiation is affected by miR‐1, miR‐125, miR‐155, miR‐186, and miR‐199a by suppressing Hdac4, Igf2, Mef2a, Myog, Fazd4, Jag1, and Wnt2, respectively. MuSCs, skeletal muscle stem cells; Ccnd2, cyclin D2; Cdc25a, cell division cycle 25A; Dek, DEK oncogene; Fzd4, frizzled homolog 4; Hdac4, histone deacetylase 4; Igf2, insulin‐like growth factor 2; Jag1, jagged 1; Mstn, myostatin; Myog, myogenin; Pax3, paired box 3; Pax7, paired box 7; Srf, serum response factor; Wnt2, wingless‐type MMTV integration site family, member 2.
Figure 3. Figure 3. Schematic representation of miRNAs involved in skeletal muscle regeneration. In muscle atrophy, the miR‐30 family miRNA levels were reduced. Muscle atrophy was observed in CryAB knockout (KO) mice. On the other hand, the miR‐128a inhibition was shown to induce myotube hypertrophy. During skeletal muscle regeneration, miR‐26a expression was increased following muscle injury and downregulation of miR‐26a delayed muscle regeneration. The expression of miR‐125b was reduced during muscle regeneration following injury, and overexpression of miR‐125 inhibited muscle regeneration. Genetic deletion of miR‐206 delayed skeletal muscle regeneration in response to injury. miR‐675 miRNA, encoded within H19, exerts a critical function in skeletal muscle regeneration, since H19‐deficient mice show impaired regeneration following injury. MuSCs, skeletal muscle stem cells. Cdc6, cell division cycle 6; Igf2, insulin‐like growth factor 2; Igfbp5, insulin‐like growth factor binding protein 5; Notch3, notch 3; Smad1, SMAD family member 1; Smad4, SMAD family member 4; Smad5, SMAD family member 5.


Figure 1. Schematic representation of biogenesis of miRNAs and the mechanism of their action. The miRNA gene is transcribed into miRNA primary transcript (Pri miRNA), resulting in a long hairpin structure that contains a 5′ cap and 3′ poly (A) tail. Then, the Pri miRNA is cleaved by Drosha RNase III and cofactors, which releases the pre‐miRNA. The pre‐miRNA is exported into the cytoplasm, and is processed by RNAse III Dicer, into miRNA duplex of ∼20 to 25 nt. Then, the miRNA duplex is separated by action of AGO2, and one miRNA strand is loaded onto an AGO protein to form the RISC. The RISC functions as a guide by base pairing miRNA with its target mRNAs, inducing mRNA cleavage, mRNA deadenylation, and translation repression.


Figure 2. Schematic representation of miRNAs involved in myogenesis. The maintenance of skeletal muscle stem cell quiescence is controlled by miR‐195, miR‐489, and miR‐497 by suppressing Cdc25a, Ccnd2, and Dek, respectively. The entry into the myogenic program is influenced by miR‐1, miR‐27, miR‐133, miR‐206, and miR‐486 by targeting Pax7, Pax3, Mstn, and SRF, respectively. Myoblast differentiation is affected by miR‐1, miR‐125, miR‐155, miR‐186, and miR‐199a by suppressing Hdac4, Igf2, Mef2a, Myog, Fazd4, Jag1, and Wnt2, respectively. MuSCs, skeletal muscle stem cells; Ccnd2, cyclin D2; Cdc25a, cell division cycle 25A; Dek, DEK oncogene; Fzd4, frizzled homolog 4; Hdac4, histone deacetylase 4; Igf2, insulin‐like growth factor 2; Jag1, jagged 1; Mstn, myostatin; Myog, myogenin; Pax3, paired box 3; Pax7, paired box 7; Srf, serum response factor; Wnt2, wingless‐type MMTV integration site family, member 2.


Figure 3. Schematic representation of miRNAs involved in skeletal muscle regeneration. In muscle atrophy, the miR‐30 family miRNA levels were reduced. Muscle atrophy was observed in CryAB knockout (KO) mice. On the other hand, the miR‐128a inhibition was shown to induce myotube hypertrophy. During skeletal muscle regeneration, miR‐26a expression was increased following muscle injury and downregulation of miR‐26a delayed muscle regeneration. The expression of miR‐125b was reduced during muscle regeneration following injury, and overexpression of miR‐125 inhibited muscle regeneration. Genetic deletion of miR‐206 delayed skeletal muscle regeneration in response to injury. miR‐675 miRNA, encoded within H19, exerts a critical function in skeletal muscle regeneration, since H19‐deficient mice show impaired regeneration following injury. MuSCs, skeletal muscle stem cells. Cdc6, cell division cycle 6; Igf2, insulin‐like growth factor 2; Igfbp5, insulin‐like growth factor binding protein 5; Notch3, notch 3; Smad1, SMAD family member 1; Smad4, SMAD family member 4; Smad5, SMAD family member 5.
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Article Title: Regulation of Skeletal Muscle by microRNAs
 

How to Cite

Gabriela Placoná Diniz, Da‐Zhi Wang. Regulation of Skeletal Muscle by microRNAs. Compr Physiol 2016, 6: 1279-1294. doi: 10.1002/cphy.c150041