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      Acute exercise in a hot environment increases heat shock protein 70 and peroxisome proliferator-activated receptor γ coactivator 1α mRNA in Thoroughbred horse skeletal muscle

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          Abstract

          Heat acclimatization or acclimation training in horses is practiced to reduce physiological strain and improve exercise performance in the heat, which can involve metabolic improvement in skeletal muscle. However, there is limited information concerning the acute signaling responses of equine skeletal muscle after exercise in a hot environment. The purpose of this study was to investigate the hypothesis that exercise in hot conditions induces greater changes in heat shock proteins and mitochondrial-related signaling in equine skeletal muscle compared with exercise in cool conditions. Fifteen trained Thoroughbred horses [4.6 ± 0.4 (mean ± SE) years old; 503 ± 14 kg] were assigned to perform a treadmill exercise test in cool conditions [ COOL; Wet Bulb Globe Temperature (WBGT), 12.5°C; n = 8] or hot conditions ( HOT; WBGT, 29.5°C; n = 7) consisting of walking at 1.7 m/s for 1 min, trotting at 4 m/s for 5 min, and cantering at 7 m/s for 2 min and at 90% of VO 2max for 2 min, followed by walking at 1.7 m/s for 20 min. Heart rate during exercise and plasma lactate concentration immediately after exercise were measured. Biopsy samples were obtained from the middle gluteal muscle before and at 4 h after exercise, and relative quantitative analysis of mRNA expression using real-time RT-PCR was performed. Data were analyzed with using mixed models. There were no significant differences between the two groups in peak heart rate ( COOL, 213 ± 3 bpm; HOT, 214 ± 4 bpm; p = 0.782) and plasma lactate concentration ( COOL, 13.1 ± 1.4 mmoL/L; HOT, 17.5 ± 1.7 mmoL/L; p = 0.060), while HSP-70 ( COOL, 1.9-fold, p = 0.207; HOT, 2.4-fold, p = 0.045), PGC-1α ( COOL, 3.8-fold, p = 0.424; HOT, 8.4-fold, p = 0.010), HIF-1α ( COOL, 1.6-fold, p = 0.315; HOT, 2.2-fold, p = 0.018) and PDK4 ( COOL, 7.6-fold, p = 0.412; HOT, 14.1-fold, p = 0.047) mRNA increased significantly only in HOT at 4 h after exercise. These data indicate that acute exercise in a hot environment facilitates protective response to heat stress (HSP-70), mitochondrial biogenesis (PGC-1α and HIF-1α) and fatty acid oxidation (PDK4).

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          Heat shock proteins: modifying factors in physiological stress responses and acquired thermotolerance.

          Cells from virtually all organisms respond to a variety of stresses by the rapid synthesis of a highly conserved set of polypeptides termed heat shock proteins (HSPs). The precise functions of HSPs are unknown, but there is considerable evidence that these stress proteins are essential for survival at both normal and elevated temperatures. HSPs also appear to play a critical role in the development of thermotolerance and protection from cellular damage associated with stresses such as ischemia, cytokines, and energy depletion. These observations suggest that HSPs play an important role in both normal cellular homeostasis and the stress response. This mini-review examines recent evidence and hypotheses suggesting that the HSPs may be important modifying factors in cellular responses to a variety of physiologically relevant conditions such as hyperthermia, exercise, oxidative stress, metabolic challenge, and aging.
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            Heat acclimation improves exercise performance.

            This study examined the impact of heat acclimation on improving exercise performance in cool and hot environments. Twelve trained cyclists performed tests of maximal aerobic power (VO2max), time-trial performance, and lactate threshold, in both cool [13°C, 30% relative humidity (RH)] and hot (38°C, 30% RH) environments before and after a 10-day heat acclimation (∼50% VO2max in 40°C) program. The hot and cool condition VO2max and lactate threshold tests were both preceded by either warm (41°C) water or thermoneutral (34°C) water immersion to induce hyperthermia (0.8-1.0°C) or sustain normothermia, respectively. Eight matched control subjects completed the same exercise tests in the same environments before and after 10 days of identical exercise in a cool (13°C) environment. Heat acclimation increased VO2max by 5% in cool (66.8 ± 2.1 vs. 70.2 ± 2.3 ml·kg(-1)·min(-1), P = 0.004) and by 8% in hot (55.1 ± 2.5 vs. 59.6 ± 2.0 ml·kg(-1)·min(-1), P = 0.007) conditions. Heat acclimation improved time-trial performance by 6% in cool (879.8 ± 48.5 vs. 934.7 ± 50.9 kJ, P = 0.005) and by 8% in hot (718.7 ± 42.3 vs. 776.2 ± 50.9 kJ, P = 0.014) conditions. Heat acclimation increased power output at lactate threshold by 5% in cool (3.88 ± 0.82 vs. 4.09 ± 0.76 W/kg, P = 0.002) and by 5% in hot (3.45 ± 0.80 vs. 3.60 ± 0.79 W/kg, P < 0.001) conditions. Heat acclimation increased plasma volume (6.5 ± 1.5%) and maximal cardiac output in cool and hot conditions (9.1 ± 3.4% and 4.5 ± 4.6%, respectively). The control group had no changes in VO2max, time-trial performance, lactate threshold, or any physiological parameters. These data demonstrate that heat acclimation improves aerobic exercise performance in temperate-cool conditions and provide the scientific basis for employing heat acclimation to augment physical training programs.
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              Exercise intensity-dependent regulation of peroxisome proliferator-activated receptor coactivator-1 mRNA abundance is associated with differential activation of upstream signalling kinases in human skeletal muscle.

              Skeletal muscle contraction increases intracellular ATP turnover, calcium flux, and mechanical stress, initiating signal transduction pathways that modulate peroxisome proliferator-activated receptor gamma coactivator-1alpha (PGC-1alpha)-dependent transcriptional programmes. The purpose of this study was to determine if the intensity of exercise regulates PGC-1alpha expression in human skeletal muscle, coincident with activation of signalling cascades known to regulate PGC-1alpha transcription. Eight sedentary males expended 400 kcal (1674 kj) during a single bout of cycle ergometer exercise on two separate occasions at either 40% (LO) or 80% (HI) of . Skeletal muscle biopsies from the m. vastus lateralis were taken at rest and at +0, +3 and +19 h after exercise. Energy expenditure during exercise was similar between trials, but the high intensity bout was shorter in duration (LO, 69.9 +/- 4.0 min; HI, 36.0 +/- 2.2 min, P < 0.05) and had a higher rate of glycogen utilization (P < 0.05). PGC-1alpha mRNA abundance increased in an intensity-dependent manner +3 h after exercise (LO, 3.8-fold; HI, 10.2-fold, P < 0.05). AMP-activated protein kinase (AMPK) (2.8-fold, P < 0.05) and calcium/calmodulin-dependent protein kinase II (CaMKII) phosphorylation (84%, P < 0.05) increased immediately after HI but not LO. p38 mitogen-activated protein kinase (MAPK) phosphorylation increased after both trials (2.0-fold, P < 0.05), but phosphorylation of the downstream transcription factor, activating transcription factor-2 (ATF-2), increased only after HI (2.4-fold, P < 0.05). Cyclic-AMP response element binding protein (CREB) phosphorylation was elevated at +3 h after both trials (80%, P < 0.05) and class IIa histone deacetylase (HDAC) phosphorylation increased only after HI (2.0-fold, P < 0.05). In conclusion, exercise intensity regulates PGC-1alpha mRNA abundance in human skeletal muscle in response to a single bout of exercise. This effect is mediated by differential activation of multiple signalling pathways, with ATF-2 and HDAC phosphorylation proposed as key intensity-dependent mediators.
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                Author and article information

                Contributors
                Journal
                Front Vet Sci
                Front Vet Sci
                Front. Vet. Sci.
                Frontiers in Veterinary Science
                Frontiers Media S.A.
                2297-1769
                21 August 2023
                2023
                : 10
                : 1230212
                Affiliations
                [1] 1Sports Science Division, Equine Research Institute, Japan Racing Association , Shimotsuke, Japan
                [2] 2Department of Biological Sciences, Graduate School of Sciences and Technology for Innovation, Yamaguchi University , Yamaguchi, Japan
                [3] 3Department of Veterinary Pathophysiology and Animal Health, Graduate School of Agricultural and Life Sciences, The University of Tokyo , Bunkyo, Japan
                [4] 4Racehorse Hospital, Miho Training Center , Inashiki, Japan
                Author notes

                Edited by: Morteza Hosseini-Ghaffari, University of Bonn, Germany

                Reviewed by: Cesar Rosales-Nieto, Texas State University, United States; Ali Razzaghi, Ferdowsi University of Mashhad, Iran

                *Correspondence: Yusaku Ebisuda, ebisuda@ 123456equinst.go.jp
                Article
                10.3389/fvets.2023.1230212
                10475567
                37671280
                9bae100b-c3a9-4449-9e78-a9b0dbdadf39
                Copyright © 2023 Ebisuda, Mukai, Takahashi, Yoshida, Kawano, Matsuhashi, Miyata, Kuwahara and Ohmura.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 28 May 2023
                : 08 August 2023
                Page count
                Figures: 5, Tables: 2, Equations: 0, References: 63, Pages: 9, Words: 6833
                Categories
                Veterinary Science
                Original Research
                Custom metadata
                Livestock Genomics

                heat stress,exercise,thoroughbred horses,messenger rna,skeletal muscle

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