Thermal stress and selection for growth affect myogenic satellite cell lipid accumulation and adipogenic gene expression through mechanistic target of rapamycin pathway

Lay Summary Turkey breast muscle growth and development are sensitive to temperatures immediately after hatch due to an immature thermoregulatory system. Meat yield or quality problems may arise from external thermal stress during this period. Modern commercial turkeys are selected for increased growth and breast muscle yield. However, with excessive enlargement of muscle fibers, there are increased incidences of muscle damage and fat deposition in the breast muscle. The breast meat can be downgraded due to the meat quality problems. Satellite cells (SCs) are the only source of cells responsible for post-hatch muscle growth in poultry, and they are sensitive to temperature. This study identifies the cellular mechanisms in regulating thermal stress-induced fat synthesis in turkey breast muscle SCs. The results of the current study provide insight into how thermal stress and selection for rapid growth affect the fat content in SCs. These results have potential application in the development of temperature manipulation strategies to control fat production by SCs, which will impact poultry breast meat quality. Satellite cells (SCs) are multipotential stem cells having the plasticity to convert to an adipogenic lineage in response to thermal stress during the period of peak mitotic activity (the first week after hatch in poultry). The mechanistic target of rapamycin (mTOR) pathway, which regulates cellular function and fate of SCs, is greatly altered by thermal stress in turkey pectoralis major muscle SCs. The objective of the present study was to determine the effects of thermal stress, selection for growth, and the role of the mTOR pathway on SC intracellular lipid accumulation and expression of adipogenic regulatory genes. These effects were analyzed using SCs isolated from the pectoralis major muscle of 1-wk-old modern faster-growing commercial turkey line (NC) selected for increased growth and breast muscle yield as compared with SCs of a historic slower-growing Randombred Control Line 2 (RBC2) turkey. Heat stress (43 degrees C) of SCs during proliferation increased intracellular lipid accumulation (P < 0.001), whereas cold stress (33 degrees C) showed an inhibitory effect (P < 0.001) in both lines. Knockdown of mTOR reduced the intracellular lipid accumulation (P < 0.001) and suppressed the expression of several adipogenic regulatory genes: peroxisome proliferator-activated receptor-gamma (PPAR gamma; P < 0.001), CCAAT/enhancer-binding protein-beta (C/EBP beta; P < 0.001), and neuropeptide-Y (NPY; P < 0.001) during both proliferation and differentiation. The NC line SCs showed fewer reductions in lipid accumulation compared with the RBC2 line independent of temperature. Both intracellular lipid accumulation (P < 0.001) and PPAR gamma expression (P < 0.001) were greater at 72 h of proliferation than at 48 h of differentiation in both the RBC2 and NC lines independent of temperature. Thus, hot and cold thermal stress affected intracellular lipid accumulation in the pectoralis major muscle SCs, in part, through the mTOR pathway in wea growth-dependent manner. Altered intracellular lipid accumulation could eventually affect intramuscular fat deposition, resulting in a long-lasting effect on the structure and protein to fat ratio of the poultry pectoralis major muscle. The results of the current study provide valuable information on the development of temperature manipulation strategies to reduce the fat content in breast muscle satellite cells, which may decrease the incidence of structural defects and improve the breast meat quality of modern commercial poultry.

Automated summary

The growth and development of turkey breast muscle are highly sensitive to temperature, which highlights the importance of temperature management immediately after hatch. Excessive enlargement of muscle fibers can lead to muscle damage and fat deposition in the breast meat, impacting meat quality. This study investigates the cellular mechanisms involved in thermal stress-induced fat synthesis in turkey breast muscle satellite cells, providing valuable insights for the development of temperature manipulation strategies to control fat production and improve poultry meat quality.