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Satellite Cells and Skeletal Muscle Regeneration

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ABSTRACT

Skeletal muscles are essential for vital functions such as movement, postural support, breathing, and thermogenesis. Muscle tissue is largely composed of long, postmitotic multinucleated fibers. The life‐long maintenance of muscle tissue is mediated by satellite cells, lying in close proximity to the muscle fibers. Muscle satellite cells are a heterogeneous population with a small subset of muscle stem cells, termed satellite stem cells. Under homeostatic conditions all satellite cells are poised for activation by stimuli such as physical trauma or growth signals. After activation, satellite stem cells undergo symmetric divisions to expand their number or asymmetric divisions to give rise to cohorts of committed satellite cells and thus progenitors. Myogenic progenitors proliferate, and eventually differentiate through fusion with each other or to damaged fibers to reconstitute fiber integrity and function. In the recent years, research has begun to unravel the intrinsic and extrinsic mechanisms controlling satellite cell behavior. Nonetheless, an understanding of the complex cellular and molecular interactions of satellite cells with their dynamic microenvironment remains a major challenge, especially in pathological conditions. The goal of this review is to comprehensively summarize the current knowledge on satellite cell characteristics, functions, and behavior in muscle regeneration and in pathological conditions. © 2015 American Physiological Society. Compr Physiol 5:1027‐1059, 2015.

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Figure 1. Figure 1. Skeletal muscle anatomy. Schematic illustrating the structure of skeletal muscle. Skeletal muscles are divided into bundles containing numerous myofibers. Myofibers are multinucleated cylindrical cells that are surrounded by a vast network of blood vessels and nerves. Satellite cells are small mononuclear cells located between the plasmalemma of the myofibers and the basal membrane.
Figure 2. Figure 2. Satellite cell markers. Images of single extensor digitorium longus (EDL) myofiber labeled for different markers of satellite cells. The left image shows a multinucleated myofiber with two satellite cells stained by Pax7 antibody (red) and a nuclear dye (DAPI, blue). The right picture displays a satellite cell stained with M‐cadherin (red) on the apical side and α7‐integrin (white) on the basal side.
Figure 3. Figure 3. The satellite cell niche. Cross‐section of a tibialis anterior (TA) muscle immunostained with laminin (white), M‐cadherin (green), Pax7 (red), and a nuclear dye (DAPI, blue). All muscle fibers are surrounded by laminin. The insert in the top right corner shows a magnification of a satellite cell (Pax7‐positive) in its niche.
Figure 4. Figure 4. Embryonic muscle development. The image shows a mouse embryo transgenic for a fluorescent expression reporter (TdTomato) of the myogenic transcription factor Myf5 at 10.5 days after fertilization. At this developmental stage Myf5 is highly expressed in the somites. Somites develop antero‐posteriorly, with the anterior somites being the most mature ones and the posterior somites the least developed.
Figure 5. Figure 5. Genetic programme regulating skeletal muscle stem cell fate. Hierarchical network of the transcription factors controlling embryonic progenitor cell fate during limb and trunk muscle development. Pax3 and Pax7 control the myogenic specification of embryonic progenitors. Pax3/7 can directly target Myf5 and MyoD expression and thus myogenic determination. Myf5 also acts partially upstream of MyoD and can trigger its expression. Upregulation of myogenin and MRF4 induces myogenic differentiation. A population of Pax3/7+ progenitor cells does not express MRFs and gives rise to satellite stem cells during late fetal myogenesis.
Figure 6. Figure 6. Skeletal muscle regeneration. H&E staining (nuclei stained in dark blue and cytosolic proteins stained in red) illustrating the different stages of muscle regeneration following cardiotoxin injury. Two days following injury, myofiber structure is severely impaired and a multitude of mononuclear cells (myoblasts, inflammatory cells, fibroblasts, etc.) are present in the damaged area. At five days postinjury, there is the formation of small new myofibers with centralized nuclei and many cells remain in the exudate. Two months after the injury, muscle architecture is similar to uninjured muscle.
Figure 7. Figure 7. Myogenic lineage progression. Following muscle injury quiescent satellite cells (Pax7+ and Myf5+/−) are activated and differentiate to myoblasts (Pax7+, Myf5+, and MyoD+). After several rounds of proliferation, myoblasts exit the cell cycle and become myocytes (Pax7−, MyoD+, myogenin+, and MRF4+). Myocytes can undergo a fusion process to form multinucleated myotubes (myogenin+, MRF4+, and MyHC+) that eventually mature into myofibers. The satellite stem cell subpopulation (Pax7+ and Myf5−) can also self‐renew to replenish the satellite cell pool.
Figure 8. Figure 8. Myogenic regulatory factors in proliferating myoblasts. Images from single EDL myofibers cultured ex vivo for 60 h (dashed line delineates the myofiber membrane). Staining for Pax7 (green) and MyoD (red) shows that at this stage cells express either only Pax7 (arrowhead), only MyoD, or both (arrow).
Figure 9. Figure 9. Myogenic regulatory factors in differentiating myoblasts. Pictures from EDL isolated myofibers cultured ex vivo for 72 h (dashed line delineates the myofiber membrane). Staining for Pax7 (green) and myogenin (red) shows that cells that acquire the differentiation marker myogenin lose expression of Pax7.
Figure 10. Figure 10. Asymmetric and stochastic self‐renewal. Satellite cells can be divided in two subpopulations: committed satellite cells and satellite stem cells. Satellite stem cells can perform asymmetric division in an apical‐basal orientation or symmetric division in a planar orientation (relative to the myofiber). Asymmetric division allows for the formation of one committed daughter cell that will participate in myogenesis, and for the maintenance of the original satellite stem cell. Symmetric division of satellite stem cells produces two daughter stem cells and favors satellite stem cell expansion. Committed satellite cells can divide to form two committed daughter cells that participate in the myogenesis process.
Figure 11. Figure 11. Symmetric versus asymmetric divisions. Images show myofibers isolated from EDL muscles of Myf5‐cre R26R‐YFP stained with Pax7 (red), YFP (for Myf5, green), and a nuclear dye (DAPI, blue). The myofiber membrane is outlined by a dashed line. In these mice, expression of Myf5 leads to permanent yellow‐fluorescent protein (YFP) staining. Most of the satellite cells express Myf5 (YFP+) during development, but a subpopulation of satellite stem cells never expressed Myf5 (YFP−). YFP− satellite stem cells can perform asymmetric division (A) and give rise to a committed progenitor (YFP+), or perform symmetric division (B) and produce two satellite stem cells (YFP−). Asymmetric divisions occur mostly in an apical‐basal orientation (A), while symmetric divisions occur with planar orientation (B and C).
Figure 12. Figure 12. Wnt7a‐activated pathways in myogenic cells. In myogenic cells, Wnt7a binds to Fzd7 and induces various responses depending on the myogenic stage. In satellite stem cells, Wnt7a forms a complex with the Fzd7 receptor, Scd4 coreceptor and fibronectin to activate the planar cell polarity pathway. This noncanonical pathway leads to the symmetric stem cell division. In myogenic progenitors, Wnt7a leads to rearrangements of the cytoskeleton and increases directional cell migration. Lastly, in muscle fibers, Wnt7a activates the Akt/mTOR pathway, in an IGF‐1‐independent manner, and promotes myofiber hypertrophy.
Figure 13. Figure 13. Satellite cell migration. Schematic representing a migrating satellite cell. Satellite cells receive many guidance cues from their microenvironment that promote chemotaxis toward the damaged area (ex: HGF) or repulse the cell away from uninjured region (ex: Ephrins).
Figure 14. Figure 14. Myotube formation. Pictures from primary myoblasts cultured in vitro in differentiation medium (low‐serum medium). Cells are stained with a nuclear dye (DAPI, blue) and myosin heavy chain (MyHC, in green). Almost no myoblasts express MyHC before the addition of differentiation medium. After 1 day in differentiation medium, the cells start to express MyHC. At three days, myoblasts fuse to form small multinucleated myotubes (few myonuclei per myotube). After 5 days of differentiation, myotubes become larger and contain more nuclei.
Figure 15. Figure 15. Epigenetic control of stemness and lineage determination genes during myogenic differentiation. In undifferentiated satellite cells and myoblasts, lineage determination gene regulatory regions such as the myogenin promoter are repressed through a combination of epigenetic mechanisms. MyoD is repressed by its association with SIRT1 and HDACs. MEF2 also recruits HDACs as well as SUV39H1, the histone methyltransferase responsible for H3K9 methylation. The Polycomb Repressive complex 2 (PRC2) containing the histone methyltransferase EZH2 is also recruited on the myogenin promoter by the transcription factor YY1. Together, these protein complexes are responsible to establish heterochromatin formation that is repressive for transcription. In undifferentiated satellite cells and myoblasts, stemness genes like Pax7 are active and are thus occupied by histone acetyltransferases (HAT) as well as the SWI/SNF chromatin remodeling complex and the MLL/Trithorax complex, responsible for H3K4me3 deposition. These proteins promote the formation of euchromatin, which is permissive for transcription. When cells receive differentiation cues, these epigenetic complexes are relocalized to different regulatory regions. Repressive complexes leave the promoters of lineage determination genes, which become active, and could be recruited to the promoters of stemness genes that need to be silenced. In contrast, proteins involved in active chromatin configuration leave the promoters of stemness genes and are relocalized at muscle specific promoters (myogenin). The myogenin promoter is thus occupied by the MLL/Trithorax complex, by HATs, by the SWI/SNF complex as well as by the demethylase UTX.
Figure 16. Figure 16. The satellite cell microenvironment. The satellite cell niche is composed of various ECM proteins and cell types. Cell types such as inflammatory cells and stromal cells can physically interact with satellite cells or release various cytokines, growth factors and ECM components that will influence satellite cell behavior.
Figure 17. Figure 17. Inflammation and myogenesis. Inflammation is characterized by the activation of mast cells (MC), followed by the early recruitment of granulocytes (polymorphonuclear cells, PMN), and the accumulation of monocytes/macrophages. Macrophage accumulation is classically composed of an initial proinflammatory phase (M1 macrophages) followed by an anti‐inflammatory phase (M2 macrophages). These different leukocytes secrete factors that directly influence the function of myogenic cells. Initial burst of leukocytes has been shown to stimulate satellite cell activation and proliferation. M1 macrophages promote myoblast proliferation and repress early differentiation, while M2 macrophages stimulate differentiation and myofiber growth.
Figure 18. Figure 18. Degeneration of dystrophic muscles. Images from dystrophic tibialis anterior muscles. H&E staining showing centronucleated fibers that indicate muscle regeneration. Sirius red (fibrotic tissue in red) and trichrome masson (fibrotic tissue in blue) illustrate the massive fibrosis response in the dystrophic muscles.
Figure 19. Figure 19. Satellite cell therapy. Schematic illustrating the different steps of cell therapy. Healthy satellite cells are isolated from donor muscle tissue and are cultured in vitro or directly transplanted into diseased host muscle. Healthy satellite cells will then fuse to host myofibers to form hybrid fibers. Addition of new healthy nuclei to host myofibers can partially correct genetic disorders such as muscular dystrophies. However, this therapeutic avenue has major technical limitations such as short‐term engraftment, limited availability of donor cells, and poor cell migration and survival.


Figure 1. Skeletal muscle anatomy. Schematic illustrating the structure of skeletal muscle. Skeletal muscles are divided into bundles containing numerous myofibers. Myofibers are multinucleated cylindrical cells that are surrounded by a vast network of blood vessels and nerves. Satellite cells are small mononuclear cells located between the plasmalemma of the myofibers and the basal membrane.


Figure 2. Satellite cell markers. Images of single extensor digitorium longus (EDL) myofiber labeled for different markers of satellite cells. The left image shows a multinucleated myofiber with two satellite cells stained by Pax7 antibody (red) and a nuclear dye (DAPI, blue). The right picture displays a satellite cell stained with M‐cadherin (red) on the apical side and α7‐integrin (white) on the basal side.


Figure 3. The satellite cell niche. Cross‐section of a tibialis anterior (TA) muscle immunostained with laminin (white), M‐cadherin (green), Pax7 (red), and a nuclear dye (DAPI, blue). All muscle fibers are surrounded by laminin. The insert in the top right corner shows a magnification of a satellite cell (Pax7‐positive) in its niche.


Figure 4. Embryonic muscle development. The image shows a mouse embryo transgenic for a fluorescent expression reporter (TdTomato) of the myogenic transcription factor Myf5 at 10.5 days after fertilization. At this developmental stage Myf5 is highly expressed in the somites. Somites develop antero‐posteriorly, with the anterior somites being the most mature ones and the posterior somites the least developed.


Figure 5. Genetic programme regulating skeletal muscle stem cell fate. Hierarchical network of the transcription factors controlling embryonic progenitor cell fate during limb and trunk muscle development. Pax3 and Pax7 control the myogenic specification of embryonic progenitors. Pax3/7 can directly target Myf5 and MyoD expression and thus myogenic determination. Myf5 also acts partially upstream of MyoD and can trigger its expression. Upregulation of myogenin and MRF4 induces myogenic differentiation. A population of Pax3/7+ progenitor cells does not express MRFs and gives rise to satellite stem cells during late fetal myogenesis.


Figure 6. Skeletal muscle regeneration. H&E staining (nuclei stained in dark blue and cytosolic proteins stained in red) illustrating the different stages of muscle regeneration following cardiotoxin injury. Two days following injury, myofiber structure is severely impaired and a multitude of mononuclear cells (myoblasts, inflammatory cells, fibroblasts, etc.) are present in the damaged area. At five days postinjury, there is the formation of small new myofibers with centralized nuclei and many cells remain in the exudate. Two months after the injury, muscle architecture is similar to uninjured muscle.


Figure 7. Myogenic lineage progression. Following muscle injury quiescent satellite cells (Pax7+ and Myf5+/−) are activated and differentiate to myoblasts (Pax7+, Myf5+, and MyoD+). After several rounds of proliferation, myoblasts exit the cell cycle and become myocytes (Pax7−, MyoD+, myogenin+, and MRF4+). Myocytes can undergo a fusion process to form multinucleated myotubes (myogenin+, MRF4+, and MyHC+) that eventually mature into myofibers. The satellite stem cell subpopulation (Pax7+ and Myf5−) can also self‐renew to replenish the satellite cell pool.


Figure 8. Myogenic regulatory factors in proliferating myoblasts. Images from single EDL myofibers cultured ex vivo for 60 h (dashed line delineates the myofiber membrane). Staining for Pax7 (green) and MyoD (red) shows that at this stage cells express either only Pax7 (arrowhead), only MyoD, or both (arrow).


Figure 9. Myogenic regulatory factors in differentiating myoblasts. Pictures from EDL isolated myofibers cultured ex vivo for 72 h (dashed line delineates the myofiber membrane). Staining for Pax7 (green) and myogenin (red) shows that cells that acquire the differentiation marker myogenin lose expression of Pax7.


Figure 10. Asymmetric and stochastic self‐renewal. Satellite cells can be divided in two subpopulations: committed satellite cells and satellite stem cells. Satellite stem cells can perform asymmetric division in an apical‐basal orientation or symmetric division in a planar orientation (relative to the myofiber). Asymmetric division allows for the formation of one committed daughter cell that will participate in myogenesis, and for the maintenance of the original satellite stem cell. Symmetric division of satellite stem cells produces two daughter stem cells and favors satellite stem cell expansion. Committed satellite cells can divide to form two committed daughter cells that participate in the myogenesis process.


Figure 11. Symmetric versus asymmetric divisions. Images show myofibers isolated from EDL muscles of Myf5‐cre R26R‐YFP stained with Pax7 (red), YFP (for Myf5, green), and a nuclear dye (DAPI, blue). The myofiber membrane is outlined by a dashed line. In these mice, expression of Myf5 leads to permanent yellow‐fluorescent protein (YFP) staining. Most of the satellite cells express Myf5 (YFP+) during development, but a subpopulation of satellite stem cells never expressed Myf5 (YFP−). YFP− satellite stem cells can perform asymmetric division (A) and give rise to a committed progenitor (YFP+), or perform symmetric division (B) and produce two satellite stem cells (YFP−). Asymmetric divisions occur mostly in an apical‐basal orientation (A), while symmetric divisions occur with planar orientation (B and C).


Figure 12. Wnt7a‐activated pathways in myogenic cells. In myogenic cells, Wnt7a binds to Fzd7 and induces various responses depending on the myogenic stage. In satellite stem cells, Wnt7a forms a complex with the Fzd7 receptor, Scd4 coreceptor and fibronectin to activate the planar cell polarity pathway. This noncanonical pathway leads to the symmetric stem cell division. In myogenic progenitors, Wnt7a leads to rearrangements of the cytoskeleton and increases directional cell migration. Lastly, in muscle fibers, Wnt7a activates the Akt/mTOR pathway, in an IGF‐1‐independent manner, and promotes myofiber hypertrophy.


Figure 13. Satellite cell migration. Schematic representing a migrating satellite cell. Satellite cells receive many guidance cues from their microenvironment that promote chemotaxis toward the damaged area (ex: HGF) or repulse the cell away from uninjured region (ex: Ephrins).


Figure 14. Myotube formation. Pictures from primary myoblasts cultured in vitro in differentiation medium (low‐serum medium). Cells are stained with a nuclear dye (DAPI, blue) and myosin heavy chain (MyHC, in green). Almost no myoblasts express MyHC before the addition of differentiation medium. After 1 day in differentiation medium, the cells start to express MyHC. At three days, myoblasts fuse to form small multinucleated myotubes (few myonuclei per myotube). After 5 days of differentiation, myotubes become larger and contain more nuclei.


Figure 15. Epigenetic control of stemness and lineage determination genes during myogenic differentiation. In undifferentiated satellite cells and myoblasts, lineage determination gene regulatory regions such as the myogenin promoter are repressed through a combination of epigenetic mechanisms. MyoD is repressed by its association with SIRT1 and HDACs. MEF2 also recruits HDACs as well as SUV39H1, the histone methyltransferase responsible for H3K9 methylation. The Polycomb Repressive complex 2 (PRC2) containing the histone methyltransferase EZH2 is also recruited on the myogenin promoter by the transcription factor YY1. Together, these protein complexes are responsible to establish heterochromatin formation that is repressive for transcription. In undifferentiated satellite cells and myoblasts, stemness genes like Pax7 are active and are thus occupied by histone acetyltransferases (HAT) as well as the SWI/SNF chromatin remodeling complex and the MLL/Trithorax complex, responsible for H3K4me3 deposition. These proteins promote the formation of euchromatin, which is permissive for transcription. When cells receive differentiation cues, these epigenetic complexes are relocalized to different regulatory regions. Repressive complexes leave the promoters of lineage determination genes, which become active, and could be recruited to the promoters of stemness genes that need to be silenced. In contrast, proteins involved in active chromatin configuration leave the promoters of stemness genes and are relocalized at muscle specific promoters (myogenin). The myogenin promoter is thus occupied by the MLL/Trithorax complex, by HATs, by the SWI/SNF complex as well as by the demethylase UTX.


Figure 16. The satellite cell microenvironment. The satellite cell niche is composed of various ECM proteins and cell types. Cell types such as inflammatory cells and stromal cells can physically interact with satellite cells or release various cytokines, growth factors and ECM components that will influence satellite cell behavior.


Figure 17. Inflammation and myogenesis. Inflammation is characterized by the activation of mast cells (MC), followed by the early recruitment of granulocytes (polymorphonuclear cells, PMN), and the accumulation of monocytes/macrophages. Macrophage accumulation is classically composed of an initial proinflammatory phase (M1 macrophages) followed by an anti‐inflammatory phase (M2 macrophages). These different leukocytes secrete factors that directly influence the function of myogenic cells. Initial burst of leukocytes has been shown to stimulate satellite cell activation and proliferation. M1 macrophages promote myoblast proliferation and repress early differentiation, while M2 macrophages stimulate differentiation and myofiber growth.


Figure 18. Degeneration of dystrophic muscles. Images from dystrophic tibialis anterior muscles. H&E staining showing centronucleated fibers that indicate muscle regeneration. Sirius red (fibrotic tissue in red) and trichrome masson (fibrotic tissue in blue) illustrate the massive fibrosis response in the dystrophic muscles.


Figure 19. Satellite cell therapy. Schematic illustrating the different steps of cell therapy. Healthy satellite cells are isolated from donor muscle tissue and are cultured in vitro or directly transplanted into diseased host muscle. Healthy satellite cells will then fuse to host myofibers to form hybrid fibers. Addition of new healthy nuclei to host myofibers can partially correct genetic disorders such as muscular dystrophies. However, this therapeutic avenue has major technical limitations such as short‐term engraftment, limited availability of donor cells, and poor cell migration and survival.
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Nicolas A. Dumont, C. Florian Bentzinger, Marie‐Claude Sincennes, Michael A. Rudnicki. Satellite Cells and Skeletal Muscle Regeneration. Compr Physiol 2015, 5: 1027-1059. doi: 10.1002/cphy.c140068