CLC number:
On-line Access: 2024-08-27
Received: 2023-10-17
Revision Accepted: 2024-05-08
Crosschecked: 2023-01-16
Cited: 0
Clicked: 1604
Zhaolu WANG, Jinjin YANG, Xiaohui SUN, Xi SUN, Gongshe YANG, Xin'e SHI. Exosome-mediated regulatory mechanisms in skeletal muscle: a narrative review[J]. Journal of Zhejiang University Science B, 2023, 24(1): 1-14.
@article{title="Exosome-mediated regulatory mechanisms in skeletal muscle: a narrative review",
author="Zhaolu WANG, Jinjin YANG, Xiaohui SUN, Xi SUN, Gongshe YANG, Xin'e SHI",
journal="Journal of Zhejiang University Science B",
volume="24",
number="1",
pages="1-14",
year="2023",
publisher="Zhejiang University Press & Springer",
doi="10.1631/jzus.B2200243"
}
%0 Journal Article
%T Exosome-mediated regulatory mechanisms in skeletal muscle: a narrative review
%A Zhaolu WANG
%A Jinjin YANG
%A Xiaohui SUN
%A Xi SUN
%A Gongshe YANG
%A Xin'e SHI
%J Journal of Zhejiang University SCIENCE B
%V 24
%N 1
%P 1-14
%@ 1673-1581
%D 2023
%I Zhejiang University Press & Springer
%DOI 10.1631/jzus.B2200243
TY - JOUR
T1 - Exosome-mediated regulatory mechanisms in skeletal muscle: a narrative review
A1 - Zhaolu WANG
A1 - Jinjin YANG
A1 - Xiaohui SUN
A1 - Xi SUN
A1 - Gongshe YANG
A1 - Xin'e SHI
J0 - Journal of Zhejiang University Science B
VL - 24
IS - 1
SP - 1
EP - 14
%@ 1673-1581
Y1 - 2023
PB - Zhejiang University Press & Springer
ER -
DOI - 10.1631/jzus.B2200243
Abstract: skeletal muscle plays a paramount role in physical activity, metabolism, and energy balance, while its homeostasis is being challenged by multiple unfavorable factors such as injury, aging, or obesity. exosomes, a subset of extracellular vesicles, are now recognized as essential mediators of intercellular communication, holding great clinical potential in the treatment of skeletal muscle diseases. Herein, we outline the recent research progress in exosomal isolation, characterization, and mechanism of action, and emphatically discuss current advances in exosomes derived from multiple organs and tissues, and engineered exosomes regarding the regulation of physiological and pathological development of skeletal muscle. These remarkable advances expand our understanding of myogenesis and muscle diseases. Meanwhile, the engineered exosome, as an endogenous nanocarrier combined with advanced design methodologies of biomolecules, will help to open up innovative therapeutic perspectives for the treatment of muscle diseases.
[1]AminzadehMA,RogersRG,FournierM,et al.,2018.Exosome-mediated benefits of cell therapy in mouse and human models of Duchenne muscular dystrophy.Stem Cell Rep,10(3):942-955.
[2]ArabT,MallickER,HuangYY,et al.,2021.Characterization of extracellular vesicles and synthetic nanoparticles with four orthogonal single-particle analysis platforms.J Extracell Vesicles,10(6):e12079.
[3]Asare-WereheneM,NakkaK,ReunovA,et al.,2020.The exosome-mediated autocrine and paracrine actions of plasma gelsolin in ovarian cancer chemoresistance.Oncogene,39(7):1600-1616.
[4]BaracosVE,MartinL,KorcM,et al.,2018.Cancer-associated cachexia.Nat Rev Dis Primers,4:17105.
[5]BaroneR,MacalusoF,SangiorgiC,et al.,2016.Skeletal muscle Heat shock protein 60 increases after endurance training and inducesperoxisome proliferator-activated receptor gamma coactivator 1 α1 expression.Sci Rep,6:19781.
[6]BierA,BerensteinP,KronfeldN,et al.,2018.Placenta-derived mesenchymal stromal cells and their exosomes exert therapeutic effects in Duchenne muscular dystrophy.Biomaterials,174:67-78.
[7]BillonN,MonteiroMC,DaniC,2008.Developmental origin of adipocytes: new insights into a pending question.Biol Cell,100(10):563-575.
[8]BuckinghamM,BajardL,ChangT,et al.,2003.The formation of skeletal muscle: from somite to limb.J Anat,202(1):59-68.
[9]ByunSE,SimC,ChungY,et al.,2021.Skeletal muscle regeneration by the exosomes of adipose tissue-derived mesenchymal stem cells.Curr Issues Mol Biol,43(3):1473-1488.
[10]CavallariC,RanghinoA,TapparoM,et al.,2017.Serum-derived extracellular vesicles (EVs) impact on vascular remodeling and prevent muscle damage in acute hind limb ischemia.Sci Rep,7:8180.
[11]ChenCH,ZhengHH,LuoYM,et al.,2021.SUMOylation promotes extracellular vesicle-mediated transmission of lncRNAELNAT1 and lymph node metastasis in bladder cancer.J Clin Invest,131(8):e146431.
[12]ChenW,XieMK,YangB,et al.,2017.Skeletal myogenic differentiation of human urine-derived cells as a potential source for skeletal muscle regeneration.J Tissue Eng Regen Med,11(2):334-341.
[13]ChenYC,ZhuQF,ChengLM,et al.,2021.Exosome detection via the ultrafast-isolation system: EXODUS.Nat Methods,18(2):212-218.
[14]ChoiY,KwonY,KimDK,et al.,2015.Gut microbe-derived extracellular vesicles induce insulin resistance, thereby impairing glucose metabolism in skeletal muscle.Sci Rep,5:15878.
[15]ConceiçãoM,ForcinaL,WiklanderOPB,et al.,2021.Engineered extracellular vesicle decoy receptor-mediated modulation of the IL6 trans-signalling pathway in muscle.Biomaterials,266:120435.
[16]DengZB,MuJY,TsengM,et al.,2015.Enterobacteria-secreted particles induce production of exosome-like S1P-containing particles by intestinal epithelium to drive Th17-mediated tumorigenesis.Nat Commun,6:6956.
[17]DeyBK,GaganJ,YanZ,et al.,2012.miR-26a is required for skeletal muscle differentiation and regeneration in mice.Genes Dev,26(19):2180-2191.
[18]di FeliceV,BaroneR,TrovatoE,et al.,2022.Physiactisome: a new nanovesicle drug containing heat shock protein 60 for treating muscle wasting and cachexia.Cells,11(9):1406
[19]Evguenieva-HackenbergE,HouLL,GlaeserS,et al.,2014.Structure and function of the archaeal exosome.WIREs RNA,5(5):623-635.
[20]FryCS,KirbyTJ,KosmacK,et al.,2017.Myogenic progenitor cells control extracellular matrix production by fibroblasts during skeletal muscle hypertrophy.Cell Stem Cell,20(1):56-69.
[21]FuXR,LiuG,HalimA,et al.,2019.Mesenchymal stem cell migration and tissue repair.Cells,8(8):784.
[22]GaoHH,GaoY,PangWJ,et al.,2018.Iridoviral infection can be reduced by UCHL1-loaded exosomes from the testis of Chinese giant salamanders (Andrias davidianus).Vet Microbiol,224:50-57.
[23]GaoW,LiuHB,YuanJ,et al.,2016.Exosomes derived from mature dendritic cells increase endothelial inflammation and atherosclerosisvia membrane TNF-α mediated NF-κB pathway.J Cell Mol Med,20(12):2318-2327.
[24]GeGQ,ZhangW,NiuLG,et al.,2016.miR-215 functions as a tumor suppressor in epithelial ovarian cancer through regulation of the X-chromosome-linked inhibitor of apoptosis.Oncol Rep,35(3):1816-1822.
[25]GrossJC,ChaudharyV,BartschererK,et al.,2012.Active Wnt proteins are secreted on exosomes.Nat Cell Biol,14(10):1036-1045.
[26]GurunathanS,KangMH,KimJH,2021.A comprehensive review on factors influences biogenesis, functions, therapeutic and clinical implications of exosomes.Int J Nanomedicine,16:1281-1312.
[27]Hassanpour TamrinS,Sanati NezhadA,SenA,2021.Label-free isolation of exosomes using microfluidic technologies.ACS Nano,15(11):17047-17079.
[28]HeY,RodriguesRM,WangXL,et al.,2021.Neutrophil-to-hepatocyte communication via LDLR-dependent miR-223-enriched extracellular vesicle transfer ameliorates nonalcoholic steatohepatitis.J Clin Invest,131(3):e141513.
[29]HuL,KleinJD,HassounahF,et al.,2015.Low-frequency electrical stimulation attenuates muscle atrophy in CKD—a potential treatment strategy.J Am Soc Nephrol,26(3):626-635.
[30]HuWJ,RuZY,ZhouYL,et al.,2019.Lung cancer-derived extracellular vesicles induced myotube atrophy and adipocyte lipolysis via the extracellular IL-6-mediated STAT3 pathway.Biochim Biophys Acta (BBA)-Mol Cell Biol Lipids,1864(8):1091-1102.
[31]HuangY,YuMS,KumaA,et al.,2021.Downregulation of let-7 by electrical acupuncture increases protein synthesis in mice.Front Physiol,12:697139.
[32]IyerSR,ScheiberAL,YarowskyP,et al.,2020.Exosomes isolated from platelet-rich plasma and mesenchymal stem cells promote recovery of function after muscle injury.Am J Sports Med,48(9):2277-2286.
[33]JohnstoneRM,AdamM,HammondJR,et al.,1987.Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes).J Biol Chem,262(19):9412-9420.
[34]KalluriR,LeBleuVS,2020.The biology, function, and biomedical applications of exosomes.Science,367(6478):eaau6977.
[35]KatayamaM,WiklanderOPB,FritzT,et al.,2019.Circulating exosomal miR-20b-5p is elevated in type 2 diabetes and could impair insulin action in human skeletal muscle.Diabetes,68(3):515-526.
[36]KellerMD,ChingKL,LiangFX,et al.,2020.Decoy exosomes provide protection against bacterial toxins.Nature,579(7798):260-264.
[37]KimS,LeeMJ,ChoiJY,et al.,2018.Roles of exosome-like vesicles released from inflammatory C2C12 myotubes: regulation of myocyte differentiation and myokine expression.Cell Physiol Biochem,48(5):1829-1842.
[38]la ShuS,AllenCL,Benjamin-DavalosS,et al.,2021.A rapid exosome isolation using ultrafiltration and size exclusion chromatography (REIUS) method for exosome isolation from melanoma cell lines. In: Hargadon KM (Ed.),Melanoma: Methods and Protocols. Humana,New York, p.289-304.
[39]LarssonL,DegensH,LiMS,et al.,2019.Sarcopenia: aging-related loss of muscle mass and function.Physiol Rev,99(1):427-511.
[40]LeMN,FanZH,2021.Exosome isolation using nanostructures and microfluidic devices.Biomed Mater,16(2):022005.
[41]LengL,DongX,GaoXJ,et al.,2021.Exosome-mediated improvement in membrane integrity and muscle function in dystrophic mice.Mol Ther,29(4):1459-1470.
[42]LiDM,SongHC,ShuoLH,et al.,2020.Gonadal white adipose tissue-derived exosomal MiR-222 promotes obesity-associated insulin resistance.Aging (Albany NY),12(22):22719-22743.
[43]LiK,WongDK,HongKY,et al.,2018.Cushioned-density gradient ultracentrifugation (C-DGUC): a refined and high performance method for the isolation, characterization, and use of exosomes. In: Patel T (Ed.),Extracellular RNA: Methods and Protocols.Humana Press,New York, p.69-83.
[44]LiM,ZeringerE,BartaT,et al.,2014.Analysis of the RNA content of the exosomes derived from blood serum and urine and its potential as biomarkers.Philos Trans Roy Soc B Biol Sci,369(1652):20130502.
[45]LiP,KaslanM,LeeSH,et al.,2017.Progress in exosome isolation techniques.Theranostics,7(3):789-804.
[46]LiXX,WangSH,ZhuRJ,et al.,2016.Lung tumor exosomes induce a pro-inflammatory phenotype in mesenchymal stem cells via NFκB-TLR signaling pathway.J Hematol Oncol,9:42.
[47]LiZY,LiuC,LiSL,et al.,2021.BMSC-derived exosomes inhibit dexamethasone-induced muscle atrophyvia the miR-486-5p/FoxO1 axis.Front Endocrinol (Lausanne),12:681267.
[48]LiuT,SunYC,ChePget aln.,2019.Adipose tissue macrophage-derived exosomal miR-29a regulates obesity-associated insulin resistance.Biochem Biophys Res Commun,515(2):352-358.
[49]ManterolaL,GuruceagaE,Pérez-LarrayaJG,et al.,2014.A small noncoding RNA signature found in exosomes of GBM patient serum as a diagnostic tool.Neuro-Oncology,16(4):520-527.
[50]MiaoCX,ZhangWL,FengLX,et al.,2021.Cancer-derived exosome miRNAs induce skeletal muscle wasting by Bcl-2-mediated apoptosis in colon cancer cachexia.Mol Ther Nucleic Acids,24:923-938.
[51]MinciacchiVR,YouS,SpinelliC,et al.,2015.Large oncosomes contain distinct protein cargo and represent a separate functional class of tumor-derived extracellular vesicles.Oncotarget,6(13):11327-11341.
[52]Monguió-TortajadaM,Morón-FontM,Gámez-ValeroA,et al.,2019.Extracellular-vesicle isolation from different biological fluids by size-exclusion chromatography.Curr Protoc Stem Cell Biol,49:e82.
[53]MytidouC,KoutsoulidouA,KatsioloudiA,et al.,2021.Muscle-derived exosomes encapsulate myomiRs and are involved in local skeletal muscle tissue communication.FASEB J,35(2):e21279.
[54]NairS,JayabalanN,GuanzonD,et al.,2018.Human placental exosomes in gestational diabetes mellitus carry a specific set of miRNAs associated with skeletal muscle insulin sensitivity.Clin Sci (Lond),132(22):2451-2467.
[55]NairVD,GeYC,LiSD,et al.,2020.Sedentary and trained older men have distinct circulating exosomal microRNA profiles at baseline and in response to acute exercise.Front Physiol,11:605.
[56]OliveiraDL,RizzoJ,JoffeLS,et al.,2013.Where do they come from and where do they go: candidates for regulating extracellular vesicle formation in fungi.Int J Mol Sci,14(5):9581-9603.
[57]PanBT,JohnstoneRM,1983.Fate of the transferrin receptor during maturation of sheep reticulocytes in vitro: selective externalization of the receptor.Cell,33(3):967-978.
[58]QiuL,LiuZ,WuCZ,et al.,2020a.C6-ceramide induces salivary adenoid cystic carcinoma cell apoptosis via IP3R-activated UPR and UPR-independent pathways.Biochem Biophys Res Commun,525(4):997-1003.
[59]QiuL,ChenW,WuCZ,et al.,2020b.Exosomes of oral squamous cell carcinoma cells containing miR-181a-3p induce muscle cell atrophy and apoptosis by transmissible endoplasmic reticulum stress signaling.Biochem Biophys Res Commun,533(4):831-837.
[60]RojasEA,CorcheteLA,San-SegundoL,et al.,2017.Amiloride, an old diuretic drug, is a potential therapeutic agent for multiple myeloma.Clin Cancer Res,23(21):6602-6615.
[61]SahuA,ClemensZJ,ShindeSN,et al.,2021.Regulation of aged skeletal muscle regeneration by circulating extracellular vesicles.Nat Aging,1(12):1148-1161.
[62]SamaeekiaR,RabieeB,PutraI,et al.,2018.Effect of human corneal mesenchymal stromal cell-derived exosomes on corneal epithelial wound healing.Invest Ophthalmol Vis Sci,59(12):5194-5200.
[63]SchmidtSF,RohmM,HerzigS,et al.,2018.Cancer cachexia: more than skeletal muscle wasting.Trends Cancer,4(12):849-860.
[64]SchöneichC,DreminaE,GalevaN,et al.,2014.Apoptosis in differentiating C2C12 muscle cells selectively targets Bcl-2-deficient myotubes.Apoptosis,19(1):42-57.
[65]SharmaS,LeClaireM,GimzewskiJK,2018.Ascent of atomic force microscopy as a nanoanalytical tool for exosomes and other extracellular vesicles.Nanotechnology,29(13):132001.
[66]SteinackerJM,Opitz-GressA,BaurS,et al.,2000.Expression of myosin heavy chain isoforms in skeletal muscle of patients with peripheral arterial occlusive disease.J Vasc Surg,31(3):443-449.
[67]SunYX,ShiH,YinSQ,et al.,2018.Human mesenchymal stem cell derived exosomes alleviate type 2 diabetes mellitus by reversing peripheral insulin resistance and relieving β-cell destruction.ACS Nano,12(8):7613-7628.
[68]Tavakoli DarganiZ,SinglaR,JohnsonT,et al.,2018.Exosomes derived from embryonic stem cells inhibit doxorubicin and inflammation-induced pyroptosis in muscle cells.Can J Physiol Pharmacol,96(3):304-307.
[69]ThéryC,WitwerKW,AikawaE,et al.,2018.Minimal information for studies of extracellular vesicles 2018 (MISEV2018): a position statement of the International Society for Extracellular Vesicles and update of the MISEV2014 guidelines.J Extracell Vesicles,7(1):1535750.
[70]TorralbaD,BaixauliF,Villarroya-BeltriC,et al.,2018.Priming of dendritic cells by DNA-containing extracellular vesicles from activated T cells through antigen-driven contacts.Nat Commun,9:2658.
[71]VassilakosG,LeiHQ,YangY,et al.,2019.Deletion of muscle IGF-I transiently impairs growth and progressively disrupts glucose homeostasis in male mice.FASEB J,33(1):181-194.
[72]WangB,ZhangAQ,WangHD,et al.,2019.miR-26a limits muscle wasting and cardiac fibrosis through exosome-mediated microRNA transfer in chronic kidney disease.Theranostics,9(7):1864-1877.
[73]WangCY,SongW,ChenB,et al.,2019.Exosomes isolated from adipose-derived stem cells: a new cell-free approach to prevent the muscle degeneration associated with torn rotator cuffs.Am J Sports Med,47(13):3247-3255.
[74]WangDX,ZhangXH,LiYB,et al.,2022.Exercise-induced browning of white adipose tissue and improving skeletal muscle insulin sensitivity in obese/non-obese growing mice: do not neglect exosomal miR-27a.Front Nutr,9:940673.
[75]WangSW,CescaF,LoersG,et al.,2011.Synapsin I is an oligomannose-carrying glycoprotein, acts as an oligomannose-binding lectin, and promotes neurite outgrowth and neuronal survival when released via glia-derived exosomes.J Neurosci,31(20):7275-7290.
[76]WeiMY,GaoXT,LiuLJ,et al.,2020.Visceral adipose tissue derived exosomes exacerbate colitis severityvia pro-inflammatory miRNAs in high fat diet fed mice.ACS Nano,14(4):5099-5110.
[77]WuCH,SilversCR,MessingEM,et al.,2019.Bladder cancer extracellular vesicles drive tumorigenesis by inducing the unfolded protein response in endoplasmic reticulum of nonmalignant cells.J Biol Chem,294(9):3207-3218.
[78]WuHZ,BallantyneCM,2017.Skeletal muscle inflammation and insulin resistance in obesity.J Clin Invest,127(1):43-54.
[79]WuPP,ZhangB,ShiH,et al.,2018.MSC-exosome: a novel cell-free therapy for cutaneous regeneration.Cytotherapy,20(3):291-301.
[80]WuRY,HuangCS,WuQK,et al.,2019.Exosomes secreted by urine-derived stem cells improve stress urinary incontinence by promoting repair of pubococcygeus muscle injury in rats.Stem Cell Res Ther,10:80.
[81]XuXH,YuanTJ,DadHA,et al.,2021.Plant exosomes as novel nanoplatforms for microRNA transfer stimulate neural differentiation of stem cells in vitro and in vivo.Nano Lett,21(19):8151-8159.
[82]XuYT,ZhangL,OcanseyDKW,et al.,2022.HucMSC-Ex alleviates inflammatory bowel disease via the lnc78583-mediated miR3202/HOXB13 pathway.J Zhejiang Univ-Sci B (Biomed & Biotechnol),23(5):423-431.
[83]YanB,ZhangY,LiangC,et al.,2020.Stem cell-derived exosomes prevent pyroptosis and repair ischemic muscle injury through a novel exosome/circHIPK3/FOXO3a pathway.Theranostics,10(15):6728-6742.
[84]YangDB,ZhangWH,ZhangHY,et al.,2020.Progress, opportunity, and perspective on exosome isolation-efforts for efficient exosome-based theranostics.Theranostics,10(8):3684-3707.
[85]YangXF,XuePP,ChenHR,et al.,2020.Denervation drives skeletal muscle atrophy and induces mitochondrial dysfunction, mitophagy and apoptosis via miR-142a-5p/MFN1 axis.Theranostics,10(3):1415-1432.
[86]YiSL,LiuXJ,ZhongJQ,et al.,2014.Role of caveolin-1 in atrial fibrillation as an anti-fibrotic signaling molecule in human atrial fibroblasts.PLoS ONE,9(1):e85144.
[87]YingW,RiopelM,BandyopadhyayG,et al.,2017.Adipose tissue macrophage-derived exosomal miRNAs can modulate in vivo and in vitro insulin sensitivity.Cell,171(2):372-384.e12.
[88]YingW,GaoH,Dos ReisFCG,et al.,2021.MiR-690, an exosomal-derived miRNA from M2-polarized macrophages, improves insulin sensitivity in obese mice.Cell Metab,33(4):781-790.e5.
[89]YuY,DuHW,WeiSN,et al.,2018.Adipocyte-derived exosomal miR-27a induces insulin resistance in skeletal muscle through repression of PPARγ.Theranostics,8(8):2171-2188.
[90]ZanottiS,GibertiniS,BlasevichF,et al.,2018.Exosomes and exosomal miRNAs from muscle-derived fibroblasts promote skeletal muscle fibrosis.Matrix Biol,74:77-100.
[91]ZeschnigkM,KozianD,KuchC,et al.,1995.Involvement of M-cadherin in terminal differentiation of skeletal muscle cells.J Cell Sci,108(9):2973-2981.
[92]ZhangAQ,WangHD,WangB,et al.,2019.Exogenous miR-26a suppresses muscle wasting and renal fibrosis in obstructive kidney disease.FASEB J,33(12):13590-13601.
[93]ZhangHY,LydenD,2019.Asymmetric-flow field-flow fractionation technology for exomere and small extracellular vesicle separation and characterization.Nat Protoc,14(4):1027-1053.
[94]ZhangHY,FreitasD,KimHS,et al.,2018.Identification of distinct nanoparticles and subsets of extracellular vesicles by asymmetric flow field-flow fractionation.Nat Cell Biol,20(3):332-343.
[95]ZhangWL,SunWK,GuXF,et al.,2022.GDF-15 in tumor-derived exosomes promotes muscle atrophy via Bcl-2/caspase-3 pathway.Cell Death Discov,8:162.
[96]ZhaoL,YuJ,WangJ,et al.,2017.Isolation and identification of miRNAs in exosomes derived from serum of colon cancer patients.J Cancer,8(7):1145-1152.
[97]ZhouL,ZhangT,ShaoW,et al.,2021.Amiloride ameliorates muscle wasting in cancer cachexia through inhibiting tumor-derived exosome release.Skelet Muscle,11:17.
[98]ZhouQ,YangHC,PanHC,et al.,2021.Exosomes isolated from the miR-215-modified bone marrow mesenchymal stem cells protect H2O2-induced rat myoblasts via the miR-215/FABP3 pathway.Exp Mol Pathol,119:104608.
[99]ZhuQW,LiQ,NiuX,et al.,2018.Extracellular vesicles secreted by human urine-derived stem cells promote ischemia repair in a mouse model of hind-limb ischemia.Cell Physiol Biochem,47(3):1181-1192.
Open peer comments: Debate/Discuss/Question/Opinion
<1>