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. 2021 Jun 1:12:667814.
doi: 10.3389/fphys.2021.667814. eCollection 2021.

Effect of Temperature and Selection for Growth on Intracellular Lipid Accumulation and Adipogenic Gene Expression in Turkey Pectoralis Major Muscle Satellite Cells

Jiahui Xu  1 , Gale M Strasburg  2 , Kent M Reed  3 , Sandra G Velleman  1
Affiliations

Effect of Temperature and Selection for Growth on Intracellular Lipid Accumulation and Adipogenic Gene Expression in Turkey Pectoralis Major Muscle Satellite Cells

Jiahui Xu et al. Front Physiol. .

Abstract

As multipotential stem cells, satellite cells (SCs) have the potential to express adipogenic genes resulting in lipid synthesis with thermal stress. The present study determined the effect of temperature on intracellular lipid synthesis and adipogenic gene expression in SCs isolated from the pectoralis major (p. major) muscle of 7-day-old fast-growing modern commercial (NC) turkeys compared to SCs from unselected slower-growing turkeys [Randombred Control Line 2 (RBC2)]. Since proliferating and differentiating SCs have different responses to thermal stress, three incubation strategies were used: (1) SCs proliferated at the control temperature of 38°C and differentiated at 43° or 33°C; (2) SCs proliferated at 43° or 33°C and differentiated at 38°C; or (3) SCs both proliferated and differentiated at 43°, 38°, or 33°C. During proliferation, lipid accumulation increased at 43°C and decreased at 33°C with the NC line showing greater variation than the RBC2 line. During proliferation at 43°C, peroxisome proliferator-activated receptor-γ (PPARγ) and neuropeptide-Y (NPY) expression was reduced to a greater extent in the NC line than the RBC2 line. At 33°C, expression of PPARγ, NPY, and CCAAT/enhancer-binding protein-β (C/EBPβ) was upregulated, but only in the RBC2 line. During differentiation, both lines showed greater changes in lipid accumulation and in C/EBPβ and NPY expression if the thermal challenge was initiated during proliferation. These data suggest that adipogenic gene expression is more responsive to thermal challenge in proliferating SCs than in differentiating SCs, and that growth-selection has increased temperature sensitivity of SCs, which may significantly affect breast muscle structure and composition.

Keywords: adipogenic potential; muscle; satellite cell; selection for growth; temperature.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

FIGURE 1
FIGURE 1
Expression of peroxisome proliferator-activated receptor gamma (PPARγ) at 72 h of proliferation (72 hP) and 48 h of differentiation (48 hD) in satellite cells isolated from the pectoralis major (p. major) muscle of 7-day-old Randombred Control Line 2 (RBC2) and 7-day-old Nicholas Commercial (NC) turkeys. (A) Satellite cell proliferation at 38° or 43°C for 72 h. (B) Satellite cell proliferation at 38° or 33°C for 72 h. (C) Satellite cell proliferation for 72 h and differentiation for 48 h, both at 38°C (38°→38°C); proliferation at 38°C for 72 h and differentiation at 43°C for 48 h (38°→43°C); proliferation at 43°C for 72 h and differentiation at 38°C for 48 h (43°→38°C); or proliferation for 72 h and differentiation for 48 h, both at 43°C (43°→43°C). (D) Satellite cell proliferation for 72 h and differentiation for 48 h, both at 38°C (38°→38°C); proliferation at 38°C for 72 h and differentiation at 33°C for 48 h (38°→33°C); proliferation at 33°C for 72 h and differentiation at 38°C for 48 h (33°→38°C); or proliferation for 72 h and differentiation for 48 h, both at 33°C (33°→33°C). Each graph bar represents a mean arbitrary unit, and each error bar represents a standard error of the mean. Mean values without a same letter were significantly different (P ≤ 0.05).
FIGURE 2
FIGURE 2
Expression of CCAAT/enhancer-binding protein beta (C/EBPβ) at 72 h of proliferation (72 hP) and 48 h of differentiation (48 hD) in satellite cells isolated from the pectoralis major (p. major) muscle of 7-day-old Randombred Control Line 2 (RBC2) and 7-day-old Nicholas Commercial (NC) turkeys. (A) Satellite cell proliferation at 38° or 43°C for 72 h. (B) Satellite cell proliferation at 38° or 33°C for 72 h. (C) Satellite cell proliferation for 72 h and differentiation for 48 h, both at 38°C (38°→38°C); proliferation at 38°C for 72 h and differentiation at 43°C for 48 h (38°→43°C); proliferation at 43°C for 72 h and differentiation at 38°C for 48 h (43°→38°C); or proliferation for 72 h and differentiation for 48 h, both at 43°C (43°→43°C). (D) Satellite cell proliferation for 72 h and differentiation for 48 h, both at 38°C (38°→38°C); proliferation at 38°C for 72 h and differentiation at 33°C for 48 h (38°→33°C); proliferation at 33°C for 72 h and differentiation at 38°C for 48 h (33°→38°C); or proliferation for 72 h and differentiation for 48 h, both at 33°C (33°→33°C). Each graph bar represents a mean arbitrary unit, and each error bar represents a standard error of the mean. Mean values without a same letter were significantly different (P ≤ 0.05).
FIGURE 3
FIGURE 3
Expression of neuropeptide Y (NPY) at 72 h of proliferation (72 hP) and 48 h of differentiation (48 hD) in satellite cells isolated from the pectoralis major (p. major) muscle of 7-day-old Randombred Control Line 2 (RBC2) and 7-day-old Nicholas Commercial (NC) turkeys. (A) Satellite cell proliferation at 38° or 43°C for 72 h. (B) Satellite cell proliferation at 38° or 33°C for 72 h. (C) Satellite cell proliferation for 72 h and differentiation for 48 h, both at 38°C (38°→38°C); proliferation at 38°C for 72 h and differentiation at 43°C for 48 h (38°→43°C); proliferation at 43°C for 72 h and differentiation at 38°C for 48 h (43°→38°C); or proliferation for 72 h and differentiation for 48 h, both at 43°C (43°→43°C). (D) Satellite cell proliferation for 72 h and differentiation for 48 h, both at 38°C (38°→38°C); proliferation at 38°C for 72 h and differentiation at 33°C for 48 h (38°→33°C); proliferation at 33°C for 72 h and differentiation at 38°C for 48 h (33°→38°C); or proliferation for 72 h and differentiation for 48 h, both at 33°C (33°→33°C). Each graph bar represents a mean arbitrary unit, and each error bar represents a standard error of the mean. Mean values without a same letter were significantly different (P ≤ 0.05).
FIGURE 4
FIGURE 4
Expression of kruppel like factor 1 (KLF1) at 72 h of proliferation (72 hP) and 48 h of differentiation (48 hD) in satellite cells isolated from the pectoralis major (p. major) muscle of 7-day-old Randombred Control Line 2 (RBC2) and 7-day-old Nicholas Commercial (NC) turkeys. (A) Satellite cell proliferation at 38° or 43°C for 72 h. (B) Satellite cell proliferation at 38° or 33°C for 72 h. (C) Satellite cell proliferation for 72 h and differentiation for 48 h, both at 38°C (38°→38°C); proliferation at 38°C for 72 h and differentiation at 43°C for 48 h (38°→43°C); proliferation at 43°C for 72 h and differentiation at 38°C for 48 h (43°→38°C); or proliferation for 72 h and differentiation for 48 h, both at 43°C (43°→43°C). (D) Satellite cell proliferation for 72 h and differentiation for 48 h, both at 38°C (38°→38°C); proliferation at 38°C for 72 h and differentiation at 33°C for 48 h (38°→33°C); proliferation at 33°C for 72 h and differentiation at 38°C for 48 h (33°→38°C); or proliferation for 72 h and differentiation for 48 h, both at 33°C (33°→33°C). Each graph bar represents a mean arbitrary unit, and each error bar represents a standard error of the mean. Mean values without a same letter were significantly different (P ≤ 0.05).
FIGURE 5
FIGURE 5
Expression of kruppel like factor 7 (KLF7) at 72 h of proliferation (72 hP) and 48 h of differentiation (48 hD) in satellite cells isolated from the pectoralis major (p. major) muscle of 7-day-old Randombred Control Line 2 (RBC2) and 7-day-old Nicholas Commercial (NC) turkeys. (A) Satellite cell proliferation at 38° or 43°C for 72 h. (B) Satellite cell proliferation at 38° or 33°C for 72 h. (C) Satellite cell proliferation for 72 h and differentiation for 48 h, both at 38°C (38°→38°C); proliferation at 38°C for 72 h and differentiation at 43°C for 48 h (38°→43°C); proliferation at 43°C for 72 h and differentiation at 38°C for 48 h (43°→38°C); or proliferation for 72 h and differentiation for 48 h, both at 43°C (43°→43°C). (D) Satellite cell proliferation for 72 h and differentiation for 48 h, both at 38°C (38°→38°C); proliferation at 38°C for 72 h and differentiation at 33°C for 48 h (38°→33°C); proliferation at 33°C for 72 h and differentiation at 38°C for 48 h (33°→38°C); or proliferation for 72 h and differentiation for 48 h, both at 33°C (33°→33°C). Each graph bar represents a mean arbitrary unit, and each error bar represents a standard error of the mean. Mean values without a same letter were significantly different (P ≤ 0.05).
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