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. 2023 Jan 3:101:skad343.
doi: 10.1093/jas/skad343.

Temperature Fluctuations Modulate Molecular Mechanisms in Skeletal Muscle and Influence Growth Potential in Beef Steers

Zachary K Smith  1 , Erika Eckhardt  2 , Won Seob Kim  2 , Ana Clara Baio Menezes  1 , Warren C Rusche  1 , Jongkyoo Kim  3
Affiliations

Temperature Fluctuations Modulate Molecular Mechanisms in Skeletal Muscle and Influence Growth Potential in Beef Steers

Zachary K Smith et al. J Anim Sci. .

Abstract

Our investigation elucidated the effects of severe temperature fluctuations on cellular and physiological responses in beef cattle. Eighteen Red Angus beef steers with an average body weight of 351 ± 24.5 kg were divided into three treatment groups: 1) Control (CON), exposed to a temperature-humidity index (THI) of 42 for 6 h without any temperature changes; 2) Transport (TP), subjected to a one-mile trailer trip with a THI of 42 for 6 h; and 3) Temperature swing (TS), exposed to a one-mile trailer trip with a THI shift from 42 to 72-75 for 3 h. Our findings indicate that TS can induce thermal stress in cattle, regardless of whether the overall temperature level is excessively high or not. Behavioral indications of extreme heat stress in the cattle were observed, including extended tongue protrusion, reduced appetite, excessive salivation, and increased respiratory rate. Furthermore, we observed a pronounced overexpression (P < 0.05) of heat shock proteins (HSPs) 20, 27, and 90 in response to the TS treatment in the longissimus muscle (LM). Alterations in signaling pathways associated with skeletal muscle growth were noted, including the upregulation (P < 0.01) of Pax7, Myf5, and myosin heavy chain (MHC) isoforms. In addition, an increase (P < 0.05) in transcription factors associated with adipogenesis was detected (P < 0.05), such as PPARγ, C/EBPα, FAS, and SCD in the TS group, suggesting the potential for adipose tissue accumulation due to temperature fluctuations. Our data illustrated the potential impacts of these temperature fluctuations on the growth of skeletal muscle and adipose tissue in beef cattle.

Keywords: adipose tissue; beef cattle; skeletal muscle; thermal stress.

Plain language summary

In this study, we investigated the effects of severe temperature fluctuations on beef cattle and their cellular and physiological responses. Our findings demonstrate that even moderate temperature swings can cause thermal stress in cattle, leading to observable behavioral signs such as extended tongue protrusion, reduced appetite, excessive salivation, and increased respiratory rate. We also observed a significant increase in the expression of heat shock proteins (HSPs), which protect cells from stress, indicating their importance as early responders to temperature fluctuations. Furthermore, we examined the signaling pathways involved in skeletal muscle growth and found that severe temperature fluctuations can stimulate the upregulation of myogenic regulatory factors and myosin heavy chains. These changes suggest an increased demand for muscle contractile properties and hyperplasia during temperature challenges. In addition, our study revealed alterations in transcription factors associated with adipogenesis, such as PPARγ and C/EBPα, indicating the potential for adipose tissue accumulation in response to temperature fluctuations.

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Conflict of interest statement

All authors declare that there is no conflict of interest with this study.

Figures

Figure 1.
Figure 1.
(A) Respiratory rate measured in cattle in the Temperature Swing (TS) group. (B) Rectal temperature measured 3 h after trial initiated. (C) Serum cortisol levels in steers: baseline levels measured in the morning before the trial started. Blood samples from the Control (CON), Temperature Swing (TS), and Transportation (TP) groups were taken after 3 h of treatment.
Figure 2.
Figure 2.
mRNA expression and protein abundance levels of heat shock protein (HSP) 20, 27, 70, and 90 in beef steers under temperature swing and transport conditions. (A) HSP20, 27, 70, and 90 mRNA levels in CON, TS, and TP groups. (B) Western blots (top) and quantification of protein levels (bottom) of HSP20, HSP27, HSP70, and HSP90 in CON, TS, and TP groups. Error bars indicate the standard error. The P-values are determined by one-way ANOVA (*P < 0.05, **P < 0.01).
Figure 3.
Figure 3.
mRNA expression and protein abundance levels of myogenic regulatory factors (MRFs) (MyoD, MyoG, Myf5), Pax7, IGF-1, and P70S6K in beef steers under temperature swing and transport conditions. (A) MRFs (MyoD, MyoG, Myf5), Pax7, IGF-1, and P70S6K mRNA levels in CON, TS, and TP groups. (B) Western blots (top) and quantification of protein levels (bottom) of Pax7, Myf5, and IGF-1 in CON, TS, and TP groups. Error bars indicate the standard error. The P-values are determined by one-way ANOVA (*P < 0.05, **P < 0.01).
Figure 4.
Figure 4.
mRNA expression of myosin heavy chain (MHC) I, IIA, and IIX in beef steers under temperature swing and transport conditions. Error bars indicate the standard error. The P-values are determined by one-way ANOVA (*P < 0.05, **P < 0.01).
Figure 5.
Figure 5.
The protein levels of Akt, mTOR, and P70S6K in LD muscle of beef steers under temperature swing and transport conditions. Error bars indicate the standard error. The P-values are determined by one-way ANOVA (*P < 0.05, **P < 0.01).
Figure 6.
Figure 6.
mRNA expression and protein abundance levels of adipogenesis markers (PPARγ, C/EBPα, FAS, and SCD) in beef steers under temperature swing and transport conditions. (A) PPARγ, C/EBPα, FAS, and SCD mRNA levels in CON, TS, and TP groups. (B) Western blots (top) and quantification of protein levels (bottom) of PPARγ, C/EBPα, SCD, and FAS in CON, TS, and TP groups. Error bars indicate the standard error. The P-values are determined by one-way ANOVA (*P < 0.05, **P < 0.01).
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