Platelet releasate promotes skeletal myogenesis by increasing muscle stem cell commitment to differentiation and accelerates muscle regeneration following acute injury

Scully, David; Sfyri, Peggy; Verpoorten, Sandrine; Papadopoulos, Petros; Muñoz-Turrillas, María Carmen; Mitchell, Robert D.; Aburima, Ahmed; Patel, Ketan; Gutiérrez, Laura; Naseem, Khalid M.; Matsakas, Antonios

doi:10.1111/apha.13207

Cited by 19 publications

(54 citation statements)

References 87 publications

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“…Importantly, in slow proliferating cell types such as cardiomyocytes and chondrocytes, optimised platelet releasate may be used to enhance regeneration (Hargrave, Varghese, Barabutis, Catravas, & Zemlin, ; Ishibashi, Hikita, Fujihara, Takato, & Hoshi, ; Senyo, Lee, & Kuhn, ). Previously, we have found a strong correlation between the platelet concentration used to make platelet releasate and proliferation of skeletal myoblasts (Scully et al, ).…”

Section: Introductionmentioning

confidence: 84%

Optimising platelet secretomes to deliver robust tissue‐specific regeneration

Scully

Sfyri

Wilkinson

et al. 2019

J Tissue Eng Regen Med

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Promoting cell proliferation is the cornerstone of most tissue regeneration therapies.As platelet-based applications promote cell division and can be customised for tissuespecific efficacy, this makes them strong candidates for developing novel regenerative therapies. Therefore, the aim of this study was to determine if platelet releasate could be optimised to promote cellular proliferation and differentiation of specific tissues. Growth factors in platelet releasate were profiled for physiological and supraphysiological platelet concentrations. We analysed the effect of physiological and supraphysiological releasate on C2C12 skeletal myoblasts, H9C2 rat cardiomyocytes, human dermal fibroblasts (HDF), HaCaT keratinocytes, and chondrocytes. Cellular proliferation and differentiation were assessed through proliferation assays, mRNA, and protein expression. We show that supraphysiological releasate is not simply a concentrated version of physiological releasate. Physiological releasate promoted C2C12, HDF, and chondrocyte proliferation with no effect on H9C2 or HaCaT cells. Supraphysiological releasate induced stronger proliferation in C2C12 and HDF cells compared with physiological releasate. Importantly, supraphysiological releasate induced proliferation of H9C2 cells. The proliferative effects of skeletal and cardiac muscle cells were in part driven by vascular endothelial growth factor alpha. Furthermore, supraphysiological releasate induced differentiation of H9C2 and C2C12, HDF, and keratinocytes. This study provides insights into the ability of releasate to promote muscle, heart, skin, and cartilage cell proliferation and differentiation and highlights the importance of optimising releasate composition for tissue-specific regeneration.

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Section: Introductionmentioning

confidence: 84%

Optimising platelet secretomes to deliver robust tissue‐specific regeneration

Scully

Sfyri

Wilkinson

et al. 2019

J Tissue Eng Regen Med

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“…Isolated satellite cells were seeded at a density of 10 000 cells per well in 8‐well XF plates pre‐coated with matrigel as described previously . In brief, cells were pre‐incubated in growth medium (DMEM, 10% horse serum, 0.5% chicken embryo extract, 1% Penicillin/Streptomycin) for 24 hours and switched to differentiation medium (DM, 2% horse serum) for 5 subsequent days.…”

Section: Methodsmentioning

confidence: 99%

“…Tibialis anterior (TA) muscle injury was induced as previously described . Briefly, mice were injected with a total of 30 µL, 50 µmol/L Naja pallida CTX (Latoxan) into the TA muscle.…”

Section: Methodsmentioning

confidence: 99%

“…Isolated satellite cells were seeded at a density of 10 000 cells per well in 8-well XF plates pre-coated with matrigel as described previously. 89 In brief, cells were pre-incubated in growth medium (DMEM, 10% horse serum, 0.5% chicken embryo extract, 1% Penicillin/Streptomycin) for 24 hours and switched to differentiation medium (DM, 2% horse serum) for 5 subsequent days. Prior to the experiment, sensor cartridges were hydrated with XF calibrate solution (pH 7.4), as recommended by the manufacturer's instructions and incubated at 37°C in a non-CO 2 environment for 24 hours.…”

Section: Seahorse Xfp Extracellular Flux Measurementmentioning

confidence: 99%

“…Tibialis anterior (TA) muscle injury was induced as previously described. 89 Briefly, mice were injected with a total of 30 µL, 50 µmol/L Naja pallida CTX (Latoxan) into the TA muscle. Mice were humanely killed 5-and 10-days post-injury and the TA muscles were collected for subsequent immunohistochemistry.…”

Section: Cardiotoxin (Ctx) Induced Muscle Injury In Vivomentioning

confidence: 99%

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Loss of CD36 protects against diet‐induced obesity but results in impaired muscle stem cell function, delayed muscle regeneration and hepatic steatosis

et al. 2019

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Aim The prevalence of obesity is a major risk factor for cardiovascular and metabolic diseases including impaired skeletal muscle regeneration. Since skeletal muscle regenerative capacity is regulated by satellite cells, we aimed to investigate whether a high‐fat diet impairs satellite cell function and whether this is linked to fatty acid uptake via CD36. We also aimed to determine whether loss of CD36 impacts on muscle redox homeostasis and skeletal muscle regenerative capacity. Methods We studied the impact of a high‐fat diet and CD36 deficiency on murine skeletal muscle morphology, redox homeostasis, satellite cell function, bioenergetics and lipid accumulation in the liver. We also determined the effect of CD36 deficiency on skeletal muscle regeneration. Results High‐fat diet increased body weight, intramuscular lipid accumulation and oxidative stress in wild‐type mice that were significantly mitigated in CD36‐deficient mice. High‐fat diet and CD36 deficiency independently attenuated satellite cell function on single fibres and myogenic capacity on primary satellite cells. CD36 deficiency resulted in delayed skeletal muscle regeneration following acute injury with cardiotoxin. CD36‐deficient and wild‐type primary satellite cells had distinct bioenergetic profiles in response to palmitate. High‐fat diet induced hepatic steatosis in both genotypes that was more pronounced in the CD36‐deficient mice. Conclusion This study demonstrates that CD36 deficiency protects against diet‐induced obesity, intramuscular lipid deposition and oxidative stress but results in impaired muscle satellite cell function, delayed muscle regeneration and hepatic steatosis. CD36 is a key mediator of fatty acid uptake in skeletal muscle, linking obesity with satellite cell function and muscle regeneration.

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Signaling roles of platelets in skeletal muscle regeneration

Graca,

Minden‐Birkenmaier,

Stephan

et al. 2023

BioEssays

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Platelets have important hemostatic functions in repairing blood vessels upon tissue injury. Cytokines, growth factors, and metabolites stored in platelet α‐granules and dense granules are released upon platelet activation and clotting. Emerging evidence indicates that such platelet‐derived signaling factors are instrumental in guiding tissue regeneration. Here, we discuss the important roles of platelet‐secreted signaling factors in skeletal muscle regeneration. Chemokines secreted by platelets in the early phase after injury are needed to recruit neutrophils to injured muscles, and impeding this early step of muscle regeneration exacerbates inflammation at later stages, compromises neo‐angiogenesis and the growth of newly formed myofibers, and reduces post‐injury muscle force production. Platelets also contribute to the recruitment of pro‐regenerative stromal cells from the adipose tissue, and the platelet releasate may also regulate the metabolism and proliferation of muscle satellite cells, which sustain myogenesis. Therefore, harnessing the signaling functions of platelets and the platelet secretome may provide new avenues for promoting skeletal muscle regeneration in health and disease.

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Platelet releasate promotes skeletal myogenesis by increasing muscle stem cell commitment to differentiation and accelerates muscle regeneration following acute injury

Cited by 19 publications

References 87 publications

Optimising platelet secretomes to deliver robust tissue‐specific regeneration

Optimising platelet secretomes to deliver robust tissue‐specific regeneration

Loss of CD36 protects against diet‐induced obesity but results in impaired muscle stem cell function, delayed muscle regeneration and hepatic steatosis

Signaling roles of platelets in skeletal muscle regeneration

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