Abstract
Skeletal muscle may be injured upon physical activity, or due to myofiber frailty caused by degenerative disorders. As a metabolic tissue, skeletal muscle has the innate ability of regeneration. Skeletal muscle regeneration may be endowed to the action of quiescent satellite cells, the resident muscle stem cells, and other interstitial and inflammatory cells that directly and indirectly contribute to adult myogenesis. However, the process of muscle regeneration greatly relies on intercellular communication through signaling factors such as proteins, microRNAs (miRNAs), inflammatory cytokines, and membrane lipids that must be tightly coordinated. It is becoming more evident that the release and transmission of these factors involve extracellular vesicles (EVs) liberated by myofibers and other cells in the milieu of the injured muscle. The cargo of EVs is responsible for altering the state of their target cells by delivering purposeful molecules such as messenger RNAs, miRNAs, lipids, and proteins or by aiming at the alteration of gene expression. These changes activate downstream pathways involved in tissue repair. Due to the heterogeneity of EVs with regard to their cargo, location, size, as well as timing of formation and release, the repair and regeneration of skeletal muscle may subsequently be impacted. This chapter focuses on the impact of EVs as biological cues directing stem cell differentiation and modulating the overall process of skeletal muscle regeneration.
Abbreviations
- ADMSC:
-
Adipose-derived mesenchymal stem cell
- Ago:
-
Argonaute
- Akt:
-
Protein kinase B
- ASCT2:
-
Alanine-serine-cysteine transporter 2
- ASM:
-
Acid sphingomyelinase
- BMD:
-
Becker muscular dystrophy
- CCL2:
-
C-C motif chemokine ligand 2
- CDK2:
-
Cyclin-dependent kinase 2
- circRNA:
-
Circular RNA
- CXCL1:
-
C-X-C motif chemokine ligand 1
- CXCL1:
-
Fractalkine
- DMD:
-
Duchenne muscular dystrophy
- ECM:
-
Extracellular matrix
- ESCRT:
-
Endosomal sorting complexes required for transport
- EV:
-
Extracellular vesicle
- FAP:
-
Fibro-adipogenic progenitor
- GJA1:
-
Connexin 43
- HGF:
-
Hepatocyte growth factor
- IGF-1:
-
Insulin-like growth factor-1
- IL-4:
-
Interleukin 4
- ILV:
-
Intraluminal vesicle
- iPSC:
-
Induced pluripotent stem cell
- lncRNA:
-
Long noncoding RNA
- MAB:
-
Mesoangioblast
- MDC/CCL22:
-
Macrophage-derived chemokine
- miRNA:
-
microRNA
- MSC:
-
Mesenchymal stem cell
- MVB:
-
Multivesicular body
- myomiRs:
-
Muscle microRNA
- NO:
-
Nitric oxide
- Nox1:
-
NADPH oxidase 1
- NRG1:
-
Neuregulin 1 protein
- p120:
-
Catenin delta-1
- PDGF-α:
-
Platelet-derived growth factor-α
- PIC:
-
Twist2s and PW1+ interstitial cell
- piRNA:
-
PIWI-interacting RNA
- PSC:
-
Pluripotent stem cell
- RISC:
-
RNA-induced silencing complex
- rRNA:
-
Ribosomal RNA
- S1P:
-
Sphingosine-1-phosphate
- SC:
-
Satellite cell
- scaRNA:
-
Small Cajal body-specific RNA
- snoRNA:
-
Small nucleolar RNA
- snRNA:
-
Small nuclear RNA
- TGF-β:
-
Transforming growth factor-β
- TLR:
-
Toll-like receptor
- tRNA:
-
Transfer RNA
- UTR:
-
Untranslated region
- VEGF:
-
Vascular endothelial growth factor
References
Alvarez-Erviti L, Seow Y, Yin H et al (2011) Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes. Nat Biotechnol 29:341–345. https://doi.org/10.1038/nbt.1807
Amato AA, Griggs RC (2011) Overview of the muscular dystrophies. Handb Clin Neurol Muscul Dystrophies 101:1–9. https://doi.org/10.1016/b978-0-08-045031-5.00001-3
Andrews NW, Almeida PE, Corrotte M (2014) Damage control: cellular mechanisms of plasma membrane repair. Trends Cell Biol 24:734–742. https://doi.org/10.1016/j.tcb.2014.07.008
Angelis LD, Berghella L, Coletta M et al (1999) Skeletal myogenic progenitors originating from embryonic dorsal aorta Coexpress endothelial and myogenic markers and contribute to postnatal muscle growth and regeneration. J Cell Biol 147:869–878. https://doi.org/10.1083/jcb.147.4.869
Armulik A, Genové G, Betsholtz C (2011) Pericytes: developmental, physiological, and pathological perspectives, problems, and promises. Dev Cell 21:193–215. https://doi.org/10.1016/j.devcel.2011.07.001
Babiychuk EB, Draeger A (2000) Annexins in cell membrane dynamics. J Cell Biol 150:1113–1124. https://doi.org/10.1083/jcb.150.5.1113
Baghdadi MB, Tajbakhsh S (2018) Regulation and phylogeny of skeletal muscle regeneration. Dev Biol 433:200–209. https://doi.org/10.1016/j.ydbio.2017.07.026
Barreca MM, Cancemi P, Geraci F (2020) Mesenchymal and induced pluripotent stem cells-derived extracellular vesicles: the new frontier for regenerative medicine? Cell 9:1163. https://doi.org/10.3390/cells9051163
Bartel DP (2004) MicroRNAs. Cell 116:281–297. https://doi.org/10.1016/s0092-8674(04)00045-5
Bianco P, Robey PG (2000) Marrow stromal stem cells. J Clin Investig 105:1663–1668. https://doi.org/10.1172/jci10413
Bihan MCL, Bigot A, Jensen SS et al (2012) In-depth analysis of the secretome identifies three major independent secretory pathways in differentiating human myoblasts. J Proteome 77:344–356. https://doi.org/10.1016/j.jprot.2012.09.008
Bittel DC, Jaiswal JK (2019) Contribution of extracellular vesicles in rebuilding injured muscles. Front Physiol 10:828. https://doi.org/10.3389/fphys.2019.00828
Bjornson CR, Cheung TH, Liu L et al (2012) Notch signaling is necessary to maintain quiescence in adult muscle stem cells. Stem Cells 30:232–242. https://doi.org/10.1002/stem.773
Boldrin L, Muntoni F, Morgan JE (2010) Are human and mouse satellite cells really the same? J Histochem Cytochem 58:941–955. https://doi.org/10.1369/jhc.2010.956201
Bouter A, Gounou C, Bérat R et al (2011) Annexin-A5 assembled into two-dimensional arrays promotes cell membrane repair. Nat Commun 2(1):270. https://doi.org/10.1038/ncomms1270
Boye TL, Maeda K, Pezeshkian W et al (2017) Annexin A4 and A6 induce membrane curvature and constriction during cell membrane repair. Nat Commun 8(1). https://doi.org/10.1038/s41467-017-01743-6
Braun T, Gautel M (2011) Transcriptional mechanisms regulating skeletal muscle differentiation, growth and homeostasis. Nat Rev Mol Cell Biol 12:349–361. https://doi.org/10.1038/nrm3118
Buckingham M (2007) Skeletal muscle progenitor cells and the role of Pax genes. C R Biol 330:530–533. https://doi.org/10.1016/j.crvi.2007.03.015
Cacchiarelli D, Martone J, Girardi E et al (2010) MicroRNAs involved in molecular circuitries relevant for the Duchenne muscular dystrophy pathogenesis are controlled by the dystrophin/nNOS pathway. Cell Metab 12:341–351. https://doi.org/10.1016/j.cmet.2010.07.008
Callis TE, Deng Z, Chen JF, Wang DZ (2008) Muscling through the microRNA world. Exp Biol Med 233:131–138. https://doi.org/10.3181/0709-mr-237
Campanella C, Bavisotto CC, Logozzi M et al (2019) On the choice of the extracellular vesicles for therapeutic purposes. Int J Mol Sci 20:236. https://doi.org/10.3390/ijms20020236
Cazzella V, Martone J, Pinnarò C et al (2012) Exon 45 skipping through U1-snRNA antisense molecules recovers the Dys-nNOS pathway and muscle differentiation in human DMD myoblasts. Mol Ther 20:2134–2142. https://doi.org/10.1038/mt.2012.178
Cezar CA, Mooney DJ (2015) Biomaterial-based delivery for skeletal muscle repair. Adv Drug Deliv Rev 84:188–197. https://doi.org/10.1016/j.addr.2014.09.008
Chakrabarti S, Kobayashi KS, Flavell RA et al (2003) Impaired membrane resealing and autoimmune myositis in synaptotagmin VII–deficient mice. J Cell Biol 162:543–549. https://doi.org/10.1083/jcb.200305131
Chang NC, Sincennes M-C, Chevalier FP et al (2018) The dystrophin glycoprotein complex regulates the epigenetic activation of muscle stem cell commitment. Cell Stem Cell 22(5):755. https://doi.org/10.1016/j.stem.2018.03.022
Chazaud B (2015) Inflammation during skeletal muscle regeneration and tissue remodeling: application to exercise-induced muscle damage management. Immunol Cell Biol 94:140–145. https://doi.org/10.1038/icb.2015.97
Chen JF, Callis TE, Wang D-Z (2008) microRNAs and muscle disorders. J Cell Sci 122:13–20. https://doi.org/10.1242/jcs.041723
Chen JF, Mandel EM, Thomson JM et al (2005) The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation. Nat Genet 38:228–233. https://doi.org/10.1038/ng1725
Choi DS, Kim DK, Kim YK, Gho YS (2013) Proteomics, transcriptomics and lipidomics of exosomes and ectosomes. Proteomics 13:1554–1571. https://doi.org/10.1002/pmic.201200329
Choi JS, Yoon HI, Lee KS et al (2016) Exosomes from differentiating human skeletal muscle cells trigger myogenesis of stem cells and provide biochemical cues for skeletal muscle regeneration. J Control Release 222:107–115. https://doi.org/10.1016/j.jconrel.2015.12.018
Cocucci E, Meldolesi J (2015) Ectosomes and exosomes: shedding the confusion between extracellular vesicles. Trends Cell Biol 25:364–372. https://doi.org/10.1016/j.tcb.2015.01.004
Coenen-Stass AM, Betts CA, Lee YF et al (2016) Selective release of muscle-specific, extracellular microRNAs during myogenic differentiation. Hum Mol Genet 25:3960–3974. https://doi.org/10.1093/hmg/ddw237
Corrotte M, Almeida PE, Tam C et al (2013) Caveolae internalization repairs wounded cells and muscle fibers. elife 2:e00926. https://doi.org/10.7554/elife.00926
Crescitelli R, Lässer C, Szabó TG et al (2013) Distinct RNA profiles in subpopulations of extracellular vesicles: apoptotic bodies, microvesicles and exosomes. J Extracell Vesicles 2:20677. https://doi.org/10.3402/jev.v2i0.20677
Creuzet S, Lescaudron L, Li Z, Fontaine-Pérus J (1998) MyoD, Myogenin, and Desmin-nls-lacZ transgene emphasize the distinct patterns of satellite cell activation in growth and regeneration. Exp Cell Res 243:241–253. https://doi.org/10.1006/excr.1998.4100
D’Souza RF, Woodhead JST, Zeng N et al (2018) Circulatory exosomal miRNA following intense exercise is unrelated to muscle and plasma miRNA abundances. Am J Physiol-Endocrinol Metab 315(4). https://doi.org/10.1152/ajpendo.00138.2018
Darabi R, Arpke RW, Irion S et al (2012) Human ES- and iPS-derived myogenic progenitors restore DYSTROPHIN and improve contractility upon transplantation in dystrophic mice. Cell Stem Cell 10:610–619. https://doi.org/10.1016/j.stem.2012.02.015
Darabi R, Santos FNC, Filareto A et al (2011) Assessment of the myogenic stem cell compartment following transplantation ofPax3/Pax7-induced embryonic stem cell-derived progenitors. Stem Cells 29:777–790. https://doi.org/10.1002/stem.625
Day K, Shefer G, Richardson JB et al (2007) Nestin-GFP reporter expression defines the quiescent state of skeletal muscle satellite cells. Dev Biol 304:246–259. https://doi.org/10.1016/j.ydbio.2006.12.026
Defour A, Meulen JHVD, Bhat R et al (2014) Dysferlin regulates cell membrane repair by facilitating injury-triggered acid sphingomyelinase secretion. Cell Death Dis 5(6):e1306. https://doi.org/10.1038/cddis.2014.272
Demonbreun AR, Mcnally EM (2017) Muscle cell communication in development and repair. Curr Opin Pharmacol 34:7–14. https://doi.org/10.1016/j.coph.2017.03.008
Draeger A, Babiychuk EB (2013) Ceramide in plasma membrane repair. Sphingolipids in disease. Handb Exp Pharmacol 216:341–353. https://doi.org/10.1007/978-3-7091-1511-4_17
Duelen R, Sampaolesi M (2017) Stem cell technology in cardiac regeneration: a pluripotent stem cell promise. EBioMedicine 16:30–40. https://doi.org/10.1016/j.ebiom.2017.01.029
Figliolini F, Ranghino A, Grange C et al (2020) Extracellular vesicles from adipose stem cells prevent muscle damage and inflammation in a mouse model of hind limb ischemia. Arterioscler Thromb Vasc Biol 40:239–254. https://doi.org/10.1161/atvbaha.119.313506
Forcina L, Cosentino M, Musarò A (2020) Mechanisms regulating muscle regeneration: insights into the interrelated and time-dependent phases of tissue healing. Cell 9:1297. https://doi.org/10.3390/cells9051297
Forterre A, Jalabert A, Chikh K et al (2013) Myotube-derived exosomal miRNAs downregulate Sirtuin1 in myoblasts during muscle cell differentiation. Cell Cycle 13:78–89. https://doi.org/10.4161/cc.26808
Fry CS, Kirby TJ, Kosmac K et al (2017) Myogenic progenitor cells control extracellular matrix production by fibroblasts during skeletal muscle hypertrophy. Cell Stem Cell 20:56–69. https://doi.org/10.1016/j.stem.2016.09.010
Garcia-Martin R, Wang G, Brandão BB et al (2021) MicroRNA sequence codes for small extracellular vesicle release and cellular retention. Nature 601:446–451. https://doi.org/10.1038/s41586-021-04234-3
Gasperi RD, Hamidi S, Harlow LM et al (2017) Denervation-related alterations and biological activity of miRNAs contained in exosomes released by skeletal muscle fibers. Sci Rep 7(1). https://doi.org/10.1038/s41598-017-13105-9
Gasser O, Hess C, Miot S et al (2003) Characterisation and properties of ectosomes released by human polymorphonuclear neutrophils. Exp Cell Res 285:243–257. https://doi.org/10.1016/s0014-4827(03)00055-7
Guescini M, Maggio S, Ceccaroli P et al (2017) Extracellular vesicles released by Oxidatively injured or intact C2C12 Myotubes promote distinct responses converging toward Myogenesis. Int J Mol Sci 18:2488. https://doi.org/10.3390/ijms18112488
György B, Hung ME, Breakefield XO, Leonard JN (2015) Therapeutic applications of extracellular vesicles: clinical promise and open questions. Annu Rev Pharmacol Toxicol 55:439–464. https://doi.org/10.1146/annurev-pharmtox-010814-124630
Hamrick MW (2012) The skeletal muscle secretome: an emerging player in muscle–bone crosstalk. BoneKEy Rep 1(60). https://doi.org/10.1038/bonekey.2012.60
Hemler ME (2003) Tetraspanin proteins mediate cellular penetration, invasion, and fusion events and define a novel type of membrane microdomain. Annu Rev Cell Dev Biol 19:397–422. https://doi.org/10.1146/annurev.cellbio.19.111301.153609
Hindi SM, Kumar A (2016) Toll-like receptor signalling in regenerative myogenesis: friend and foe. J Pathol 239:125–128. https://doi.org/10.1002/path.4714
Hoffman EP, Fischbeck KH, Brown RH et al (1988) Characterization of dystrophin in muscle-biopsy specimens from patients with Duchenne’s or Becker’s muscular dystrophy. N Engl J Med 318:1363–1368. https://doi.org/10.1056/nejm198805263182104
Horn A, Meulen JHVD, Defour A et al (2017) Mitochondrial redox signaling enables repair of injured skeletal muscle cells. Sci Signal 10(495). https://doi.org/10.1126/scisignal.aaj1978
Huang CC, Narayanan R, Alapati S, Ravindran S (2016) Exosomes as biomimetic tools for stem cell differentiation: applications in dental pulp tissue regeneration. Biomaterials 111:103–115. https://doi.org/10.1016/j.biomaterials.2016.09.029
Ieronimakis N, Pantoja M, Hays AL et al (2013) Increased sphingosine-1-phosphate improves muscle regeneration in acutely injured mdx mice. Skelet Muscle 3:20. https://doi.org/10.1186/2044-5040-3-20
Ishii K, Sakurai H, Suzuki N et al (2018) Recapitulation of extracellular LAMININ environment maintains Stemness of satellite cells in vitro. Stem Cell Rep 10:568–582. https://doi.org/10.1016/j.stemcr.2017.12.013
Jaiswal JK, Chakrabarti S, Andrews NW, Simon SM (2004) Synaptotagmin VII restricts fusion pore expansion during lysosomal exocytosis. PLoS Biol. https://doi.org/10.1371/journal.pbio.0020233
Jaiswal JK, Lauritzen SP, Scheffer L et al (2014) S100A11 is required for efficient plasma membrane repair and survival of invasive cancer cells. Nat Commun 5:3795. https://doi.org/10.1038/ncomms4795
Janas T, Janas MM, Sapoń K, Janas T (2015) Mechanisms of RNA loading into exosomes. FEBS Lett 589:1391–1398. https://doi.org/10.1016/j.febslet.2015.04.036
Jeppesen DK, Fenix AM, Franklin JL et al (2019) Reassessment of exosome composition. Cell 177(2):428–445. https://doi.org/10.1016/j.cell.2019.02.029
Jeske R, Bejoy J, Marzano M, Li Y (2020) Human pluripotent stem cell-derived extracellular vesicles: characteristics and applications. Tissue Eng Part B Rev 26:129–144. https://doi.org/10.1089/ten.teb.2019.0252
Jiang B, Yan L, Wang X et al (2019) Concise review: mesenchymal stem cells derived from human pluripotent cells, an unlimited and quality-controllable source for therapeutic applications. Stem Cells 37:572–581. https://doi.org/10.1002/stem.2964
Jimenez AJ, Maiuri P, Lafaurie-Janvore J et al (2014) ESCRT machinery is required for plasma membrane repair. Science 343:1247136–1247136. https://doi.org/10.1126/science.1247136
Joe AWB, Yi L, Natarajan A et al (2010) Muscle injury activates resident fibro/adipogenic progenitors that facilitate myogenesis. Nat Cell Biol 12:153–163. https://doi.org/10.1038/ncb2015
Judson RN, Rossi FMV (2020) Towards stem cell therapies for skeletal muscle repair. npj Regenerative Med. https://doi.org/10.1038/s41536-020-0094-3
Kajimoto T, Mohamed NNI, Badawy SMM et al (2017) Involvement of Gβγ subunits of Giprotein coupled with S1P receptor on multivesicular endosomes in F-actin formation and cargo sorting into exosomes. J Biol Chem 293:245–253. https://doi.org/10.1074/jbc.m117.808733
Kajimoto T, Okada T, Miya S et al (2013) Ongoing activation of sphingosine 1-phosphate receptors mediates maturation of exosomal multivesicular endosomes. Nat Commun 293:245–253. https://doi.org/10.1038/ncomms3712
Kalluri R, Lebleu VS (2016) Discovery of double-stranded genomic DNA in circulating exosomes. Cold Spring Harb Symp Quant Biol 81:275–280. https://doi.org/10.1101/sqb.2016.81.030932
Karpati G, Pouliot Y, Carpenter S (1988) Expression of immunoreactive major histocompatibility complex products in human skeletal muscles. Ann Neurol 23:64–72. https://doi.org/10.1002/ana.410230111
Kawiak J, Brzóska E, Grabowska I et al (2006) Contribution of stem cells to skeletal muscle regeneration. Folia Histochem Cytobiol 44:75–79. https://doi.org/10.5603/4570
Kim HS, Choi DY, Yun SJ et al (2011) Proteomic analysis of microvesicles derived from human mesenchymal stem cells. J Proteome Res 11:839–849. https://doi.org/10.1021/pr200682z
Kim S, Kim TM (2019) Generation of mesenchymal stem-like cells for producing extracellular vesicles. World J Stem Cells 11:270–280. https://doi.org/10.4252/wjsc.v11.i5.270
Kim S, Lee MJ, Choi JY et al (2018) Roles of exosome-like vesicles released from inflammatory C2C12 Myotubes: regulation of myocyte differentiation and Myokine expression. Cell Physiol Biochem 48:1829–1842. https://doi.org/10.1159/000492505
Klimczak A, Kozlowska U, Kurpisz M (2018) Muscle stem/progenitor cells and mesenchymal stem cells of bone marrow origin for skeletal muscle regeneration in muscular dystrophies. Arch Immunol Ther Exp 66:341–354. https://doi.org/10.1007/s00005-018-0509-7
Kostallari E, Baba-Amer Y, Alonso-Martin S et al (2015) Pericytes in the myovascular niche promote post-natal myofiber growth and satellite cell quiescence. Development 142:1242–1253. https://doi.org/10.1242/dev.115386
Kowal J, Arras G, Colombo M et al (2016) Proteomic comparison defines novel markers to characterize heterogeneous populations of extracellular vesicle subtypes. Proc Natl Acad Sci (8):113, 8. https://doi.org/10.1073/pnas.1521230113
Kurosaka M, Machida S (2013) Interleukin-6-induced satellite cell proliferation is regulated by induction of the JAK2/STAT3 signalling pathway through cyclin D1 targeting. Cell Prolif 46:365–373. https://doi.org/10.1111/cpr.12045
Lai RC, Tan SS, Teh BJ et al (2012) Proteolytic potential of the MSC exosome proteome: implications for an exosome-mediated delivery of therapeutic proteasome. Int J Proteomics 2012:1–14. https://doi.org/10.1155/2012/971907
Lemos DR, Babaeijandaghi F, Low M et al (2015) Nilotinib reduces muscle fibrosis in chronic muscle injury by promoting TNF-mediated apoptosis of fibro/adipogenic progenitors. Nat Med 21:786–794. https://doi.org/10.1038/nm.3869
Leoni G, Alam A, Neumann PA et al (2012) Annexin A1, formyl peptide receptor, and NOX1 orchestrate epithelial repair. J Clin Investig 123:443–454. https://doi.org/10.1172/jci65831
Leoni G, Neumann PA, Kamaly N et al (2015) Annexin A1–containing extracellular vesicles and polymeric nanoparticles promote epithelial wound repair. J Clin Investig 125:1215–1227. https://doi.org/10.1172/jci76693
Li M, Zeringer E, Barta T et al (2014) Analysis of the RNA content of the exosomes derived from blood serum and urine and its potential as biomarkers. Philos Trans R Soc B: Biol Sci 369:20130502. https://doi.org/10.1098/rstb.2013.0502
Linzbach AJ (1976) Hypertrophy, hyperplasia and structural dilatation of the human heart. Physical activity and coronary heart disease. Adv Cardiol 18:1–14. https://doi.org/10.1159/000399507
Liu N, Garry GA, Li S et al (2017) A Twist2-dependent progenitor cell contributes to adult skeletal muscle. Nat Cell Biol 19:202–213. https://doi.org/10.1038/ncb3477
Maeda Y, Yonemochi Y, Nakajyo Y et al (2017) CXCL12 and osteopontin from bone marrow-derived mesenchymal stromal cells improve muscle regeneration. Sci Rep 7(1):3305. https://doi.org/10.1038/s41598-017-02928-1
Maffioletti SM, Noviello M, English K, Tedesco FS (2014) Stem cell transplantation for muscular dystrophy: the challenge of immune response. Biomed Res Int 2014:1–12. https://doi.org/10.1155/2014/964010
Manček-Keber M, Frank-Bertoncelj M, Hafner-Bratkovič I et al (2015) Toll-like receptor 4 senses oxidative stress mediated by the oxidation of phospholipids in extracellular vesicles. Sci Signal 8(381):ra60. https://doi.org/10.1126/scisignal.2005860
Mantovani A, Sica A, Locati M (2007) New vistas on macrophage differentiation and activation. Eur J Immunol 37:14–16. https://doi.org/10.1002/eji.200636910
Matsuzaka Y, Kishi S, Aoki Y et al (2014) Three novel serum biomarkers, miR-1, miR-133a, and miR-206 for limb-girdle muscular dystrophy, Facioscapulohumeral muscular dystrophy, and Becker muscular dystrophy. Environ Health Prev Med 19:452–458. https://doi.org/10.1007/s12199-014-0405-7
Matsuzaka Y, Tanihata J, Komaki H et al (2016) Characterization and functional analysis of extracellular vesicles and muscle-abundant miRNAs (miR-1, miR-133a, and miR-206) in C2C12 myocytes and mdx mice. PLoS One 11(12):e0167811. https://doi.org/10.1371/journal.pone.0167811
Mauro A (1961) Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol 9:493–495. https://doi.org/10.1083/jcb.9.2.493
Meldolesi J (2018) Exosomes and ectosomes in intercellular communication. Curr Biol 28(8):R435–R444. https://doi.org/10.1016/j.cub.2018.01.059
Mellows B, Mitchell R, Antonioli M et al (2017) Protein and molecular characterization of a clinically compliant amniotic fluid stem cell-derived extracellular vesicle fraction capable of accelerating muscle regeneration through enhancement of angiogenesis. Stem Cells Dev 26:1316–1333. https://doi.org/10.1089/scd.2017.0089
Minasi MM, Riminucci M, De Angelis L et al (2002) The meso-angioblast: a multipotent, self-renewing cell that originates from the dorsal aorta and differentiates into most mesodermal tissues. Dev Dis 129:2773–2783
Mitchell R, Mellows B, Sheard J et al (2019) Secretome of adipose-derived mesenchymal stem cells promotes skeletal muscle regeneration through synergistic action of extracellular vesicle cargo and soluble proteins. Stem Cell Res Ther 10(1):116. https://doi.org/10.1186/s13287-019-1213-1
Miyanishi M, Tada K, Koike M et al (2007) Identification of Tim4 as a phosphatidylserine receptor. Nature 450:435–439. https://doi.org/10.1038/nature06307
Moss FP, Leblond CP (1970) Nature of dividing nuclei in skeletal muscle of growing rats. J Cell Biol 44:459–461. https://doi.org/10.1083/jcb.44.2.459
Mourikis P, Sambasivan R, Castel D et al (2012) A critical requirement for notch signaling in maintenance of the quiescent skeletal muscle stem cell state. Stem Cells 30:243–252. https://doi.org/10.1002/stem.775
Mulcahy LA, Pink RC, Carter DRF (2014) Routes and mechanisms of extracellular vesicle uptake. J Extracell Vesicles 3:24641. https://doi.org/10.3402/jev.v3.24641
Murphy C, Withrow J, Hunter M et al (2018) Emerging role of extracellular vesicles in musculoskeletal diseases. Mol Asp Med 60:123–128. https://doi.org/10.1016/j.mam.2017.09.006
Musarò A (2014) The basis of muscle regeneration. Adv Biol 2014:1–16. https://doi.org/10.1155/2014/612471
Nagata Y, Kobayashi H, Umeda M et al (2006) Sphingomyelin levels in the plasma membrane correlate with the activation state of muscle satellite cells. J Histochem Cytochem 54:375–384. https://doi.org/10.1369/jhc.5a6675.2006
Naguibneva I, Ameyar-Zazoua M, Polesskaya A et al (2006) The microRNA miR-181 targets the homeobox protein Hox-A11 during mammalian myoblast differentiation. Nat Cell Biol 8:278–284. https://doi.org/10.1038/ncb1373
Nakamura TY, Iwata Y, Sampaolesi M et al (2001) Stretch-activated cation channels in skeletal muscle myotubes from sarcoglycan-deficient hamsters. Am J Phys Cell Phys 281(2). https://doi.org/10.1152/ajpcell.2001.281.2.c690
Nakamura Y, Miyaki S, Ishitobi H et al (2015) Mesenchymal-stem-cell-derived exosomes accelerate skeletal muscle regeneration. FEBS Lett 589:1257–1265. https://doi.org/10.1016/j.febslet.2015.03.031
Pascual-Gil S, Garbayo E, Díaz-Herráez P et al (2015) Heart regeneration after myocardial infarction using synthetic biomaterials. J Control Release 203:23–38. https://doi.org/10.1016/j.jconrel.2015.02.009
Pelosi L, Berardinelli MG, Forcina L et al (2015) Increased levels of interleukin-6 exacerbate the dystrophic phenotype in mdx mice. Hum Mol Genet 24:6041–6053. https://doi.org/10.1093/hmg/ddv323
Pelosi M, Rossi MD, Barberi L, Musarò A (2014) IL-6 impairs myogenic differentiation by downmodulation of p90RSK/eEF2 and mTOR/p70S6K axes, without affecting AKT activity. Biomed Res Int 2014:1–12. https://doi.org/10.1155/2014/206026
Phinney DG, Giuseppe MD, Njah J et al (2015) Mesenchymal stem cells use extracellular vesicles to outsource mitophagy and shuttle microRNAs. Nat Commun 6:8472. https://doi.org/10.1038/ncomms9472
Pierre BAS, Tidball JG (1994) Differential response of macrophage subpopulations to soleus muscle reloading after rat hindlimb suspension. J Appl Physiol 77:290–297. https://doi.org/10.1152/jappl.1994.77.1.290
Quattrocelli M, Cassano M, Crippa S et al (2010) Cell therapy strategies and improvements for muscular dystrophy. Cell Death Differ 17:1222–1229. https://doi.org/10.1038/cdd.2009.160
Quattrocelli M, Sampaolesi M (2015) The mesmiRizing complexity of microRNAs for striated muscle tissue engineering. Adv Drug Deliv Rev 88:37–52. https://doi.org/10.1016/j.addr.2015.04.011
Querejeta R, López B, González A et al (2004) Increased collagen type I synthesis in patients with heart failure of hypertensive origin. Circulation 110:1263–1268. https://doi.org/10.1161/01.cir.0000140973.60992.9a
Rejman J, Oberle V, Zuhorn IS, Hoekstra D (2004) Size-dependent internalization of particles via the pathways of clathrin- and caveolae-mediated endocytosis. Biochem J 377:159–169. https://doi.org/10.1042/bj20031253
Relaix F, Montarras D, Stéphane Z et al (2005) Pax3 and Pax7 have distinct and overlapping functions in adult muscle progenitor cells. J Cell Biol 172:91–102. https://doi.org/10.1083/jcb.200508044
Relaix F, Zammit PS (2012) Satellite cells are essential for skeletal muscle regeneration: the cell on the edge returns Centre stage. Development 139:2845–2856. https://doi.org/10.1242/dev.069088
Reznik M (1969) Thymidine-3H uptake by satellite cells of regenerating skeletal muscle. J Cell Biol 40:568–571. https://doi.org/10.1083/jcb.40.2.568
Riazifar M, Pone EJ, Lötvall J, Zhao W (2017) Stem cell extracellular vesicles: extended messages of regeneration. Annu Rev Pharmacol Toxicol 57:125–154. https://doi.org/10.1146/annurev-pharmtox-061616-030146
Roberts TC, Blomberg KEM, Mcclorey G et al (2012) Expression analysis in multiple muscle groups and serum reveals complexity in the MicroRNA transcriptome of the mdx mouse with implications for therapy. Mol Ther Nucleic Acids 1(8):e39. https://doi.org/10.1038/mtna.2012.26
Romancino DP, Paterniti G, Campos Y et al (2013) Identification and characterization of the nano-sized vesicles released by muscle cells. FEBS Lett 587:1379–1384. https://doi.org/10.1016/j.febslet.2013.03.012
Romero M, Keyel M, Shi G et al (2017) Intrinsic repair protects cells from pore-forming toxins by microvesicle shedding. Cell Death Differ 24:798–808. https://doi.org/10.1038/cdd.2017.11
Rondon-Berrios H, Wang Y, Mitch WE (2014) Can muscle-kidney crosstalk slow progression of CKD? J Am Soc Nephrol 25:2681–2683. https://doi.org/10.1681/asn.2014060566
Rumman M, Dhawan J, Kassem M (2015) Concise review: quiescence in adult stem cells: biological significance and relevance to tissue regeneration. Stem Cells 33:2903–2912. https://doi.org/10.1002/stem.2056
Sahoo S, Losordo DW (2014) Exosomes and cardiac repair after myocardial infarction. Circ Res 114:333–344. https://doi.org/10.1161/circresaha.114.300639
Sakuma K, Yamaguchi A (2012) Molecular and cellular mechanism of muscle regeneration. Skeletal Muscle – From Myogenesis to Clinical Relations https://doi.org/10.5772/48229
Sansone P, Savini C, Kurelac I et al (2017) Packaging and transfer of mitochondrial DNA via exosomes regulate escape from dormancy in hormonal therapy-resistant breast cancer. Proc Natl Acad Sci. https://doi.org/10.1073/pnas.1704862114
Santoni de Sio FRS, Gritti A, Cascio P et al (2008) Lentiviral vector gene transfer is limited by the proteasome at Postentry steps in various types of stem cells. Stem Cells 26:2142–2152. https://doi.org/10.1634/stemcells.2007-0705
Scharner J, Zammit PS (2011) The muscle satellite cell at 50: the formative years. Skelet Muscle 1:28. https://doi.org/10.1186/2044-5040-1-28
Scheffer LL, Sreetama SC, Sharma N et al (2014) Mechanism of Ca2+−triggered ESCRT assembly and regulation of cell membrane repair. Nat Commun 5:5646. https://doi.org/10.1038/ncomms6646
Schiaffino S, Dyar KA, Ciciliot S et al (2013) Mechanisms regulating skeletal muscle growth and atrophy. FEBS J 280:4294–4314. https://doi.org/10.1111/febs.12253
Schneider DJ, Speth JM, Penke LR et al (2017) Mechanisms and modulation of microvesicle uptake in a model of alveolar cell communication. J Biol Chem 292:20897–20910. https://doi.org/10.1074/jbc.m117.792416
Schultz E, Gibson MC, Champion T (1978) Satellite cells are mitotically quiescent in mature mouse muscle: an EM and radioautographic study. J Exp Zool 206:451–456. https://doi.org/10.1002/jez.1402060314
Siracusa J, Koulmann N, Bourdon S et al (2016) Circulating miRNAs as biomarkers of acute muscle damage in rats. Am J Pathol 186:1313–1327. https://doi.org/10.1016/j.ajpath.2016.01.007
Snow MH (1977) Myogenic cell formation in regenerating rat skeletal muscle injured by mincing II. An autoradiographic study. Anat Rec 188:201–217. https://doi.org/10.1002/ar.1091880206
Sreetama SC, Takano T, Nedergaard M et al (2015) Injured astrocytes are repaired by Synaptotagmin XI-regulated lysosome exocytosis. Cell Death Differ 23:596–607. https://doi.org/10.1038/cdd.2015.124
Steens J, Klein D (2018) Current strategies to generate human mesenchymal stem cells in vitro. Stem Cells Int 2018:1–10. https://doi.org/10.1155/2018/6726185
Svensson KJ, Christianson HC, Wittrup A et al (2013) Exosome uptake depends on ERK1/2-heat shock protein 27 signaling and lipid raft-mediated endocytosis negatively regulated by Caveolin-1. J Biol Chem 288:17713–17724. https://doi.org/10.1074/jbc.m112.445403
Takahashi K, Yamanaka S (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126:663–676. https://doi.org/10.1016/j.cell.2006.07.024
Tam C, Idone V, Devlin C et al (2010) Exocytosis of acid sphingomyelinase by wounded cells promotes endocytosis and plasma membrane repair. J Cell Biol 189:1027–1038. https://doi.org/10.1083/jcb.201003053
Taverna S, Pucci M, Alessandro R (2017) Extracellular vesicles: small bricks for tissue repair/regeneration. Ann Transl Med 5:83–83. https://doi.org/10.21037/atm.2017.01.53
Tedesco FS, Gerli MFM, Perani L et al (2012) Transplantation of genetically corrected human iPSC-derived progenitors in mice with limb-girdle muscular dystrophy. Sci Transl Med 4(140):140ra89. https://doi.org/10.1126/scitranslmed.3003541
Tidball JG (2017) Regulation of muscle growth and regeneration by the immune system. Nat Rev Immunol 17:165–178. https://doi.org/10.1038/nri.2016.150
Tsiapalis D, O’Driscoll L (2020) Mesenchymal stem cell derived extracellular vesicles for tissue engineering and regenerative medicine applications. Cell 9:991. https://doi.org/10.3390/cells9040991
Uezumi A, Fukada SI, Yamamoto N et al (2010) Mesenchymal progenitors distinct from satellite cells contribute to ectopic fat cell formation in skeletal muscle. Nat Cell Biol 12:143–152. https://doi.org/10.1038/ncb2014
van Balkom BWM, Eisele AS, Pegtel DM et al (2015) Quantitative and qualitative analysis of small RNAs in human endothelial cells and exosomes provides insights into localized RNA processing, degradation and sorting. J Extracell Vesicles 4:26760. https://doi.org/10.3402/jev.v4.26760
van Rooij E, Liu N, Olson EN (2008) MicroRNAs flex their muscles. Trends Genet 24:159–166. https://doi.org/10.1016/j.tig.2008.01.007
Vechetti IJ Jr (2019) Emerging role of extracellular vesicles in the regulation of skeletal muscle adaptation. J Appl Physiol 127:645–653. https://doi.org/10.1152/japplphysiol.00914.2018
Verdera HC, Gitz-Francois JJ, Schiffelers RM, Vader P (2017) Cellular uptake of extracellular vesicles is mediated by clathrin-independent endocytosis and macropinocytosis. J Control Release 266:100–108. https://doi.org/10.1016/j.jconrel.2017.09.019
Villarroya-Beltri C, Gutiérrez-Vázquez C, Sánchez-Cabo F et al (2013) Sumoylated hnRNPA2B1 controls the sorting of miRNAs into exosomes through binding to specific motifs. Nat Commun 4:2980. https://doi.org/10.1038/ncomms3980
Wang C, Song W, Chen B 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 47:3247–3255. https://doi.org/10.1177/0363546519876323
Whitham M, Parker BL, Friedrichsen M et al (2018) Extracellular vesicles provide a means for tissue crosstalk during exercise. Cell Metab 27(1):237–251.e4. https://doi.org/10.1016/j.cmet.2017.12.001
Wiendl H, Lautwein A, Mitsdörffer M et al (2003) Antigen processing and presentation in human muscle: cathepsin S is critical for MHC class II expression and upregulated in inflammatory myopathies. J Neuroimmunol 138:132–143. https://doi.org/10.1016/s0165-5728(03)00093-6
Wosczyna MN, Rando TA (2018) A muscle stem cell support group: coordinated cellular responses in muscle regeneration. Dev Cell 46:135–143. https://doi.org/10.1016/j.devcel.2018.06.018
Wu R, Huang C, Wu Q 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. https://doi.org/10.1186/s13287-019-1182-4
Wu R, Li H, Zhai L et al (2015) MicroRNA-431 accelerates muscle regeneration and ameliorates muscular dystrophy by targeting Pax7 in mice. Nat Commun 6. https://doi.org/10.1038/ncomms8713
Xiang C, Yang K, Liang Z et al (2018) Sphingosine-1-phosphate mediates the therapeutic effects of bone marrow mesenchymal stem cell-derived microvesicles on articular cartilage defect. Transl Res 193:42–53. https://doi.org/10.1016/j.trsl.2017.12.003
Xu K, Lin J, Zandi R et al (2016) MicroRNA-mediated target mRNA cleavage and 3′-uridylation in human cells. Sci Rep 6:30242. https://doi.org/10.1038/srep30242
Yablonka-Reuveni Z, Rivera AJ (1994) Temporal expression of regulatory and structural muscle proteins during myogenesis of satellite cells on isolated adult rat fibers. Dev Biol 164:588–603. https://doi.org/10.1006/dbio.1994.1226
Young CS, Hicks MR, Ermolova NV et al (2016) A single CRISPR-Cas9 deletion strategy that targets the majority of DMD patients restores dystrophin function in hiPSC-derived muscle cells. Cell Stem Cell 18:533–540. https://doi.org/10.1016/j.stem.2016.01.021
Yuan J, Liu H, Gao W et al (2018) MicroRNA-378 suppresses myocardial fibrosis through a paracrine mechanism at the early stage of cardiac hypertrophy following mechanical stress. Theranostics 8:2565–2582. https://doi.org/10.7150/thno.22878
Zakharova L, Svetlova M, Fomina AF (2007) T cell exosomes induce cholesterol accumulation in human monocytes via phosphatidylserine receptor. J Cell Physiol 212:174–181. https://doi.org/10.1002/jcp.21013
Zanotti S, Gibertini S, Blasevich F et al (2018) Exosomes and exosomal miRNAs from muscle-derived fibroblasts promote skeletal muscle fibrosis. Matrix Biol 74:77–100. https://doi.org/10.1016/j.matbio.2018.07.003
Zhu Y, Wang Y, Zhao B et al (2017) Comparison of exosomes secreted by induced pluripotent stem cell-derived mesenchymal stem cells and synovial membrane-derived mesenchymal stem cells for the treatment of osteoarthritis. Stem Cell Res Ther 8:64. https://doi.org/10.1186/s13287-017-0510-9
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Section Editor information
Rights and permissions
Copyright information
© 2022 Springer Nature Singapore Pte Ltd.
About this entry
Cite this entry
Yedigaryan, L., Sampaolesi, M. (2022). Skeletal Muscle–Extricated Extracellular Vesicles: Facilitators of Repair and Regeneration. In: Haider, K.H. (eds) Handbook of Stem Cell Therapy. Springer, Singapore. https://doi.org/10.1007/978-981-16-6016-0_49-1
Download citation
DOI: https://doi.org/10.1007/978-981-16-6016-0_49-1
Received:
Accepted:
Published:
Publisher Name: Springer, Singapore
Print ISBN: 978-981-16-6016-0
Online ISBN: 978-981-16-6016-0
eBook Packages: Springer Reference Biomedicine and Life SciencesReference Module Biomedical and Life Sciences