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    A Review of Effects of Heat Stress on Substance and Energy Metabolism in Muscle

    2015-12-16 01:48:26ShiyongWUZhiFANGBoXUELongzhouLIUYeYANG
    Agricultural Science & Technology 2015年5期
    關(guān)鍵詞:油雞雞飼料西北農(nóng)林科技大學(xué)

    Shiyong WU,Zhi FANG,Bo XUE,Longzhou LIU,Ye YANG*

    1.College of Animal Science,Yangtze University,Jingzhou 434025,China;

    2.Jingzhou Haida Feed Co.,Ltd.,Jingzhou 434025,China

    A Review of Effects of Heat Stress on Substance and Energy Metabolism in Muscle

    Shiyong WU1,2,Zhi FANG1,Bo XUE1,Longzhou LIU1,Ye YANG1*

    1.College of Animal Science,Yangtze University,Jingzhou 434025,China;

    2.Jingzhou Haida Feed Co.,Ltd.,Jingzhou 434025,China

    Environmental temperature is a major factor affecting animal performance in South China.With global warming,heat stress will become more and more serious.This paper reviewed the effects of heat stress on metabolism of proteins,glucose,fat and energy in skeletal muscle and related mechanisms so as to provide theoretical guidance for alleviating heat stress and improving production performance of animal suffering from heat stress.

    Heat stress;Muscle;Substance metabolism;Energy metabolism

    H eat stress is currently a major environmental factor affecting production performance and economic efficiency of livestock and poultry.When the ambient temperature is higher than the optimum temperature for the growth of livestock and poultry,the absorption and metabolism of substance and energy is changed from the production status (i.e.growth)to the maintaining status. This kind of change will greatly reduce the animal performance in terms of nutrients distribution,and the body weight gain and body composition will be also affected,resulting in great economic losses[1].Due to rising global temperatures,these negative effects will become increasingly apparent in the future.Muscle tissue is a major constitutent of the body,and it is also the most active organization for metabolism activities.Currently,more and more studies clarify that heat stress can reduce or prevent the deposition of muscle tissue and reduce the performance of skeletal muscle, such as changed endocrine mode,increased catabolism and reduced anabolism[2].However,there are rare researches on the changes in metabolism and biochemistry in muscle tissue of animal suffering from heat stress.This paper described the mechanism of changed substance and energy metabolism caused by heat stress,providing a basis for the preparation of measures to improve the production performance of heat-stressed animals.

    Effect of Heat Stress on Substance Metabolism

    Proteins

    Heat stress affects the metabolism of protein after the digestion and absorption,especially the protein content in the carcass lean tissue.Generally,constant heat stress is considered to reduce significantly the synthesis rates of proteins,RNA and DNA,reducing the deposition of proteins.In different animals,the degrees of changes in protein metabo-lism are different.Skeletal muscle is the main source of energy for animal body. During heat stress,skeletal muscle will be degraded.There are many indexes for evaluating the degradation of skeletal muscle,such as plasma urea nitrogen,3-methyl-histidine and creatine.In the heat-stressed pigs,the concentration of plasma urea nitrogen will be increased.Plasma urea nitrogen mainly comes from two parts: synthesized microbial protein in rumen (ruminants)and deaminized amino acids in liver(monogastric animals). But the amino acids are derived from the degradation of feed or skeletal muscle.So the plasma urea nitrogen is not a very scientific index for evaluating the degradation of skeletal muscle. Instead,the indexes of 3-methyl-histidine and creatine are better.In the heat-stressed poultry and pigs,the concentrations of 3-methyl-histidine and creatine will all be increased[3-4]. Other studies also show that heat stress reduces the protein level,especially the casein content,in milk.However,it is still unclear whether the reduced protein content is caused by the increased catabolism or the increased protein cleavage after muscle damage.In the heat-stressed animals,the plasma insulin level is increased,but the main function of insulin is to prevent muscle catabolism.

    The effect of heat stress on digestibility of amino acid is still controversial,which may be related to the differences in experimental animal,diet type and research method.Zhong et al.[5]studied the effects of environmental temperature on metabolism of 28-dold broilers.The results showed that the high temperature treatment(32℃) had no significant effects on the true digestibilities of amino acids,except that of glycine.On one hand,heat stress reduced the activity of proteinase in the upper gastrointestine, reducing the digestibilities of proteins and amino acids in the upper digestive tract.On the other hand,heat stress reduced the emptying rate of feed, making the nutrients more fully ab-sorbed,thereby increasing the digestibilities of proteins and amino acids.Both the two kinds of effects cancelled each other out,so the digestibilities of amino acids were maintained unchanged[6].

    Carbohydrates

    Skeletal muscle and liver are the main places for animals to utilize glucose.Heat stress enhances the utilization of glucose by skeletal muscle. Particularly,the degree of glycolysis is increased.So the lactic acid content in muscle is also increased.Lactate dehydrogenase(LDH)is a key enzyme in glycolysis.Studies have shown that during the heat stress,the activity of LDH is significantly increased.The liver plays an important role in the distribution and metabolism of nutrients in body.During the heat stress,the hepatic glucose production is increased[7], which is caused by enhanced glycogenolysis and gluconeogenesis. Studies have also shown that the expression of liver pyruvate carboxylase gene is also increased during the heat stress.The pyruvate carboxylase is a major rate-limiting enzyme regulating lactic acid and alanine entering gluconeogenesis[8].Although the liver glucose content is significantly reduced after the digestion of carbohydrates, the exogenous glucose has no effect on the heat stress-induced hepatic glucose production.All the studies mentioned above indicate that the heat stress increases the dependence of peripheral tissues(muscle and fat)on glycolysis.

    The enhanced glycolysis during the heat stress is a result of long-term evolutionary selection of cells.It is a protective mechanism of cells.Under heat stress,the expression level of pyruvate dehydrogenase kinase 4 (PDK4)is increased in skeletal muscle.The PDK4 inhibits the activity of pyruvate dehydrogenase(PDH)complex.It also regulates glucose’s entering tricarboxylic acid cycle(TCA).The PDK4 is also responsible for the conversion of pyruvate to acetyl-COA. The PDH complex is not inactivated under the action of PDK4,but it is activated under the action of pyruvate dehydrogenase phosphatase[9].At the transcriptional level,the activities of PDK4 and pyruvate dehydrogenase phosphatase are regulated by cellular energy state,metabolic intermediates (acetyl-COA,NADH),transcription factors and hormones(i.e.cortisol and insulin)[10].Under heat stress,the gastrointestine is damaged,so the lipopolysaccharide content is increased in blood.The lipopolysaccharide inhibits PDH activity through the TNF-α and NF-KB pathways in muscle[11].Further studies show that the heat stress enhances glycolysis and reduces the liquidity of TCA cycle.It indicates that the conversion rate of lactic acid to pyruvate is increased,increasing lactic acid production in muscle.During the heat stress,the decreased glucose oxidation and metabolism and increased glycolysis may be a protective mechanism of cells.Mitochondrial oxidative metabolism is the major source of reactive oxygen species(ROS),but the overproduction of ROS can damage proteins,DNA and lipids and decrease cell functions.Thus,the increased transcriptional level of PDK4 and induced inactivity of PDH may be a mechanism of reducing the oxidation of substrates and the generation of ROS in mitochondrias,preventing cell injury[12].

    Fats

    Heat stress changes carcass fat content,blood lipid pattern and fat decomposability.In the heat-stressed pigs and chickens,the deposition of fat is increased.In particularly,the effect of heat stress on abdominal fat of chickens is greatest.Ain Baziz et al.[13]found that at the temperature of 21-29℃,the body fat and abdominal fat of chickens were increased by 0.8%and 1.6%respectively when the temperature is increased by 1℃.Wang et al.[14]found that the high-temperature environment increased the abdominal fat rate by 52%under the condition of free feed,and the high-temperature treatment increased the abdominal fat weight by 49%under the condition of same feed intake.It indicates that the basal metabolism and exercise of broilers are reduced under high temperature,and this part of extra energy is stored in the form of abdominal fat. The study of Kouba et al.showed that the subcutaneous fat and abdominal fat contents of heat-stressed(31℃) growing pigs,in weight of 20 kg,were increased significantly,and at the same time,the body fat content was also increased.In the heat-stressed animals,the increased body fat is mainly caused by the reduced degradation of fat.Heat stress also increases insulin sensitivity and basal insulin concentration.Insulin is a hormone that promotes lipogenesis and inhibits lipolysis.Studies have shown that heat stress can reduce plasma free fatty acid(NEFA)concentration in sheep and cattle.NEFA is a product of lipolysis and fat mobilization.The study results show that heat stress can reduce the lipolysis rate and fat degradation enzyme activity[15].

    Effect of Heat Stress on Energy Metabolism in Cells

    The changed energy metabolism caused by heat stress is the result of long-term evolutionary selection.This kind of adaptive change in metabolism is probably to increase the survival rate.The cellular energy metabolism of animals mainly refers to mitochondrial oxidative phosphorylation.The effects of heat stress on cellular energy metabolism are mainly achieved through the changes in mitochondrial metabolism.AMPK,Sirt1 and mTOR are all receptors for caloric restriction[16].Under condition of heat stress,the limitation of energy and nutrients supply will increase the AMP/ ATP ratio.Once AMPK senses the changes in AMP/ATP ratio,it is activated.The phosphorylated AMPK will further activate PGC-1α.The AMPK and PGC-1α together initiate the transcription of mitochondrial genes and regulate mitochondrial energy metabolism[17].

    Under heat stress,the caloric restriction also increases cellular NAD+ concentration.The Sirt1 is activated under the action of NAD+.The activated Sirt1 further activate PGC-1α by deacetylation,promoting mitochondrial biosynthesis[17].On the contrary,under the condition of energy excess,the GCN5-mediated acetylation reduces the PGC-1α activity.Sirt 3 is a mitochondrial protein related to caloric restriction and antioxidant defense.It activates the mitochondrial superoxide dismutase SOD through deacetylation,so Sirt3 has a very important role in anti-oxidation function.Sirt3 is the target of PGC-1α.The nutrients limitation will activate Sirt3,and further activate PGC-1α.In contrast,the nutrients excess will increase the mitochondrial Sirt3 content[18].Sirt3,instead of SOD, has effects on many key enzymes for mitochondrial metabolism.The Sirt1-PGC-1α-Sirt3 axis describes the beneficial effects of caloric restriction on extending life through regulating mitochondrial functions at the transcriptional and post-translational levels.

    The mTOR can also feel the energy and nutrients deficiency,and regulate the expression and activity of PGC-1α[19].The mTOR is a important regulator for cell growth and metabolism.Under the conditions of energy restriction,the mTOR signal is inhibited by the phosphorylation of AMPK subunit.The effects of mTOR on mitochondrial biosynthesis are achieved through different signaling pathways:the inhibited mTOR activity increases the expression of oxidative phosphorylation proteins,and the increased fatty acid oxidation-related proteins decreases the translation of proteins;mTOR’s activating mitochondrial activity is not related to the synthesis of regulatory proteins,but instead,it directly affects the transcription through PGC-1α complex.Therefore,animal bodies can be adapted to caloric restriction through PGC-1α’s regulating the adaptability of mitochondrial energy metabolism in skeletal muscle.

    Responsible editor:Tingting XU

    [1]THORNTON P,HERRERO M,FREEMAN A,et al.Vulnerability,climate change and livestock research opportunities and challenges for poverty alleviation[J].J Semi-Arid Trop Agric Res, 2007,4:1-23.

    [2]BEEDE DK,COLLIER RJ.Potential nutritional strategies for intensively managed cattle during thermal stress[J]. Journal of Animal Science,1986,62: 543-554.

    [3]YUNIANTO VD,HAYASHIT K,KAIWDA S,et al.Effect of environmental temperature on muscle protein turnover and heat production in tube-fed broiler chickens[J].British Journal of Nutrition, 1997,77:897-909.

    [4]PEARCE SC,HARRIS AJ,GABLER NK,et al.Effects of heat stress on Na/K+ATPase activity in growing pigs [J].Journal of Animal Science,2011,89 (E-Suppl.1):596(Abstract).

    [5]ZHONG J(仲菊),YANG QM(楊全明), WANG BP(王本平),et al.The effects of ambient temperatures on feed true amino acid availability in broilers(環(huán)境溫度對雞飼料氨基酸真消化率的影響) [J].Chinese Journal of Animal Nutrition (動物營養(yǎng)學(xué)報(bào)),2003,5(1):54-60.

    [6]WOLFENSON D,SKLAN D,GRABER Y,et al.Absorption of protein,fatty acids and minerals in young turkeys under heat and cold stress[J].British Poultry Science,1987,28(4):739-742.

    [7]FEBBRAIO MA.Alterations in energy metabolism during exercise and heat stress[J].Sports Medicine,2001,31:47-59.

    [8]RHOADS RP,BAUMGARD LH,SUAGEE JK.2011 AND 2012 EARLY CAREERS ACHIEVEMENT AWARDS: Metabolic priorities during heat stress with an emphasis on skeletal muscle [J].Journal of Animal Science,2013, 91:2492-2503.

    [9]HARRIS RA,BOWKER-KINLEY MM, HUANG B,et al.Regulation of the activity of the pyruvate dehydrogenase complex[J].Advances in Enzyme Regulation,2002,42:249-259.

    [10]SUGDEN MC,HOLNESS MJ.Mechanisms underlying regulation of the expression and activities of the mammalian pyruvate dehydrogenase kinases[J].Archives of Physiology and Biochemistry,2006,112:139-149.

    [11]ALAMDARI ND,CONSTANTIN-TEODOSIU A,MURTON S,et al.Temporal changes in the involvement of pyruvate dehydrogenase complex in muscle lactate accumulation during lipopolysaccharide infusion in rats[J]. Journal of Physiology,2008,586: 1767-1775.

    [12]RHOADS RP,LA NOCE AJ,WHEELOCK JB,et al.Short communication: Alterations in expression of gluconeogenic genes during heat stress and exogenous bovine somatotropin administration[J].Journal of Dairy Science,2011,94:1917-1921.

    [13]AIN BAZIN H,GAERAERT PA,PADILHA JC,et al.Chronic heat exposure enchance fat deposition and modifies muscle and fat partition in broiler carcasses[J].Poultry Science,1996,75: 505-513.

    [14]WANG QJ(王啟軍).Effect of high temperature environment on body fat deposition and lipid metabolism at different growth stages of Beijing Fatty Chicken(高溫環(huán)境對不同生長階段北京油雞脂肪沉積及脂質(zhì)代謝的影響) [D].Yangling:Northwest Agriculture& Forestry University(楊凌:西北農(nóng)林科技大學(xué)),2006.

    [15]TORLINSKA T,BANACH R,PALUSZAK J,et al.Hyperthermia effect on lipolytic processes in rat blood and adipose tissue[J].Acta Physioca Polonica,1987,38:361-366.

    [16]WENZ T.Regulation of mitochondrial biogenesis and PGC-1α under cellular stress[J].Mitochondrion,2013,13: 134-142.

    [17]CANTO C,AUWERX J.PGC-1alpha, SIRT1 and AMPK,an energy sensing network that controls energy expenditure[J].Current Opinion in Lipidology, 2009,20:98-105.

    [18]SEBASTIAN C,MOSTOSLAVSKY R. SIRT3 in calorie restriction:can you hear me now[J].Cell,2010,143:667-668.

    [19]DOGAN S,JOHANNSEN AC,GRANDE JP,et al.Effects of intermittent and chronic calorie restriction on mammalian target of rapamycin(mTOR) and IGF-I signaling pathways in mammary fat pad tissues and mammary tumors[J].Nutrition and Cancer,2011, 63:389-401.

    Responsible proofreader:Xiaoyan WU

    Supported by Key Project of Natural Science Foundation of Hubei Province (2013CFA100);National Natural Science Foundation of China(31472117).

    *Corresponding author.E-mail:yangyecaas@sina.com

    Received:April 1,2015 Accepted:May 6,2015

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