Review Article

Cellular Players in Skeletal Muscle Regeneration

Table 1

Phenotypic synopsis of the cells found in skeletal muscle interstitium.

Cell typesMarkersNegative markersReferenceSecreted moleculesReference

Stem cellsResidentSatellite cells*#Pax7, Pax3, Myf5, Barx2, M-cadherin, CD206, CCL2/CCR2, CTRs, CXCR4, c-Met, CD34, p75NTR, Tie-2, α7-intergin, β1-integrin, VECAM-1, syndecan-3 and syndecan-4, NCAM/CD56, caveolin-1, Nestin, SM/C-2.6, PW1, HMGB1
CD45, Sca-1, desmin, MyHC[15, 2041]
Nonspecified locationMuscle-derived side population cells (MSP cells)*
Abcg2, Sca-1, CD11, Gr-1, CD5c-kit, CD43, CD45, CD34.[8, 42, 43]
PICs PW1, Sca-1, CD34, vimentinPDGFRα[43, 44]
Slow-adhering stem cells (SASCs)*Notch1, STAT3, Msx1, Pax3, MMP2[45]
Sk-34 myoendothelial progenitors CD34, Sca-1, c-MetCD45, CD14, CD31, CD49, CD144 Flk1, MyoD, myf-5, myf-6, myogenin, M-cadherin, Pax-3, Pax-7.[46]
Vessel-associatedMesoangioblasts (vessel-associated stem cells)*E-selectin, β7, integrin, AlCAM, CD44, cav1, FGFR1, CXCR-4, TNF-R, TNFR 1a, IL-10R, IL-4R, RAGE, TLR4 (HMGB1 rec), CD13CD34, CD45, CD117 CD31[4749]HMGB1, VEGF, CXCL12/SDF1, CCL2, VEGF B, bFGF, FGF7, PDGF AA, HDGF[49, 50]
Myogenic endothelial cells (MECs) CD56, CD34, Pax7, von Willebrand factor, VE-cadherin/CD144, UEA-1 receptorCD45[51, 52]
Pericytes*#CCR2, Abcg2, Alkaline phosphatase, αSMA, desmin, NG2, aminopeptidase A/B, RGS5, CD146, PDGFRα and β, NG2vWF, CD31, CD34, CD144, CD45, CD56, Pax7
[5260]Ang 1[29]
Adventitial cells (ACs) CD34, Sca-1, Flk1, CD140bc-kit, CD31, CD146, CD45[61, 62]
Blood-derivedAC133+ cellsCD133, CD34, CD90, CD45[63]
Bone marrow-derived SP cellsc-kit, CD43, CD45, Sca-1B220, Mac-1, Gr-1, CD4, CD5, CD8, CD34[42]

Interstitial cellsVascular cellsEndothelial cellsvon Willebrand factor, CD146, CD31, CD34, CD144, CD105, Abcg2, Tie-2CCR2[52, 54, 56, 6466]MCP-1, TNFα, VEGF, IGF-1, FGF-2, PDGF-BB, HGF, IL-6, IL-8, TNFα[29, 33, 6769]
Smooth muscle cells
SMA, CCR2, α-actin, caldesmon, calponin
[59, 70, 71] Ang 1[29]
Nerve cellsSchwann cellsNCAM/CD56, nestin
S-100, GFAP, Krox24
cytokeratin[7277]CTNF, IGF-1, NGF[78]
Perineurial cellsEpithelial membrane antigen (EMA)
GLUT-1, claudin-1, ZO-1, connexins, occludin, vinculin, talin, desmin, titin, spectrin, CD34, VE-cadherin, AQP-1, tenascin-C
cytokeratin
S-100, CD57, neurofilaments
[74, 79, 80]
Neurons (axon)Nf200, βIII tubulin[76]Neuregulin, calcitonin gene related peptide (CGRP)[76]
Resident cells in muscle connective tissue sheathsFibroblastsCCR2, vimentin, procollagen, ET-TR, FSP-1, SMA[60, 8185]
PDGF AA, MCP-1, TNFα, Ang-1[29, 50, 67, 69]
Tcf4+ fibroblasts Tcf4, PDGFRαPax7, MyoD, F4/80[86, 87]
SDF-1+ muscle-derived fibroblasts*SDF-1[24]
MPs
 FAPs*#Sca-1, PDGFRα, CD34 CD45, CD31, α7 integrin
[10, 56, 83, 88]IL6[83]
 PDGFRα+*#PDGFRα, vimentinNG2, SMA, Pax7, M-cadherin
[10]
 Tie2+ skeletogenic  progenitors*#Tie2, Sca-1, PDFGRα, CD29, CD34CD31, CD45, CD11b, CXCR4, c-kit, NG2[89]
Telocytes (TCs)*#c-kit, CD34, vimentin, PDGFRα/β[90, 91] VEGF
[91]
Blood-derived connective tissue cellsMacrophages M1CD68, CD86, CD40, CD14, MHC I/II, CCR2[49, 71]TNFα, IL1β, TNFα, IL-6, TNF-α, IL- 1β, IL-12, IFN-γ, NO, VEGF, HMGB1, CCL2, MCP-1
[49, 67]
Macrophages M2CD163, CD36, CD163, CD206, MHC I/II, CD14, αV-integrin, αVβ3I, VCAM-1, membrane-bound CX3CL1, ICAM-1 PECAM-1[49, 92]IGF1, IL10, MMP-9, IL10 and Low: IL-6, TNF-α, IL- 1β, IFN-γ
[49]
Mast cellsc-kit, mast cell triptase[93, 94]TNFα, histamine, chymase, tryptase, IL-1, IL-6
[67, 93, 95]
PolimorphonuclearCXCR2, CD11b, CD45[96]MPO[97]

MyoblastsMyogenin, Pax3 (cycling myoblasts), α-actin, myosin heavy chain, CCR1 and CCR5, CCR2. gp130 and LIFR, NCAM/CD56, VLA-4, CX3CR1, LFA-1 and PECAM-1, Sca-1, Tie-2, p75NTR, desmin, Myf5, HMGB1, TLR4, nestinPax7, CCR2[28, 29, 34, 39, 73, 78, 88, 92, 98103]TNFα, INFγ, VEGF, Ang-1
G-CSF/G-CSFR
[104, 105]

Myocytes/MyotubesMyogenin, MRF4, CNTFR, NCAM/CD56, nestin, RAGE[34, 73, 78, 102, 103]TNFα[104]

In vitro, in situ.