Volume 13 Issue 1
Mar.  2022
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Ruiping Xu, Canwen Yu, Liyao Mao, Mengchen Jiang, Luyao Gao, Ming Li, Jinsong Liu. 2022: Antioxidant defense mechanisms and fatty acid catabolism in Red-billed Leiothrix (Leiothrix lutea) exposed to high temperatures. Avian Research, 13(1): 100013. doi: 10.1016/j.avrs.2022.100013
Citation: Ruiping Xu, Canwen Yu, Liyao Mao, Mengchen Jiang, Luyao Gao, Ming Li, Jinsong Liu. 2022: Antioxidant defense mechanisms and fatty acid catabolism in Red-billed Leiothrix (Leiothrix lutea) exposed to high temperatures. Avian Research, 13(1): 100013. doi: 10.1016/j.avrs.2022.100013

Antioxidant defense mechanisms and fatty acid catabolism in Red-billed Leiothrix (Leiothrix lutea) exposed to high temperatures

doi: 10.1016/j.avrs.2022.100013
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  • Corresponding author: E-mail address: 20190035@wzu.edu.cn (M. Li); E-mail address: ljs@wzu.edu.cn (J. Liu)
  • Received Date: 26 Jun 2021
  • Accepted Date: 06 Dec 2021
  • Publish Date: 24 Feb 2022
  • Extreme hot weather is occurring more frequently due to global warming, posing a significant threat to species survival. Birds in particular are more likely to overheat in hot weather because they have a higher body temperature. This study used a heat stress model to investigate the antioxidant defense mechanisms and changes in fatty acid catabolism in Red-billed Leiothrix (Leiothrix lutea) to gain an understanding of how birds adapt to high temperatures. The birds were divided into five groups: a control group (30 ℃ for 0 days), 1 D group (40 ℃ for 1 day), 3 D group (40 ℃ for 3 days), 14 D group (40 ℃ for 14 days) and recovery group (40 ℃ for 14 days, then 30 ℃ for 14 days). Our results indicated that when Red-billed Leiothrix are subjected to heat stress, malondialdehyde (MDA) content in the liver significantly increased, as did the enzyme activities of catalase (CAT), glutathione–SH–peroxidase (GSH-PX) and total antioxidant capacity (T-AOC) in the liver. Furthermore, there was a significant increase in heat shock protein 70 (HSP70) expression in the liver, while avian uncoupling protein (avUCP) expression in muscle was significantly reduced. Additionally, there was a significant reduction in fatty acid catabolism enzyme activity such as 3-hydroxyacyl-CoAdehydrogenase (HOAD) activity in the heart, and carnitine palmitoyl transferase 1 (CPT-1) and citrate synthase (CS) activity in the heart and liver. Furthermore, fatty acid translocase (FAT/CD36) in the heart, heart-type fatty acid binding protein (H-FABP) and fatty acid binding protein (FABP-pm) in the liver and heart were also significantly decreased. These changes reverted after treatment, but not to the same level as the control group. Our results indicated that when Red-billed Leiothrix are exposed to heat stress their internal antioxidant defense system is activated to counteract the damage caused by high temperatures. However, even with high antioxidant levels, prolonged high temperature exposure still caused some degree of oxidative damage possibly requiring a longer recovery time. Additionally, Red-billed Leiothrix may be able to resist heat stress by reducing fatty acid transport and catabolism.

     

  • 1 Ruiping Xu and Canwen Yu contributed equally to this work.
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  • Akbarian A, Michiels J, Degroote J. Association between heat stress and oxidative stress in poultry; mitochondrial dysfunction and dietary interventions with phytochemicals. Anim Biotechnol. 2016;7:37 doi: 10.1186/s40104-016-0097-5
    Azad MA, Kikusato M, Maekawa T. Metabolic characteristics and oxidative damage to skeletal muscle in broiler chickens exposed to chronic heat stress. Comp Biochem Physiol A. 2010;155:401-6 doi: 10.1016/j.cbpa.2009.12.011
    Banerjee, S., Chaturvedi, C.M., 2016. Migratory preparation associated alterations in pectoralis muscle biochemistry and proteome in Palearctic-Indian emberizid migratory finch, red-headed bunting, Emberiza bruniceps. Comp. Biochem. Physiol. D 17, 9–25
    Beckman K, Ames B. The free radical theory of aging matures. Physiol Rev. 1998;78:547-81 doi: 10.1152/physrev.1998.78.2.547
    Belhadj SI, Najar T, Ghram A. Heat stress effects on livestock: molecular, cellular and metabolic aspects. J Anim Physiol Anim Nutr. 2016;100:401-12 doi: 10.1111/jpn.12379
    Berry BJ, Trewin AJ, Amitrano AM. Use the protonmotive force: mitochondrial uncoupling and reactive oxygen species. J Mol Biol. 2018;430:3873-91 doi: 10.1016/j.jmb.2018.03.025
    Castiglione GM, Xu ZH, Zhou LL. Adaptation of the master antioxidant response connects metabolism, lifespan and feather development pathways in birds. Nat Commun. 2020;11:2476 doi: 10.1038/s41467-020-16129-4
    Chen KX, Wang CM, Wang GY. Energy budget, oxidative stress and antioxidant in striped hamster acclimated to moderate cold and warm temperatures. J Therm Biol. 2014;44:35-40 doi: 10.1016/j.jtherbio.2014.06.005
    Coburn CT, Knapp FF, Febbraio M. Defective uptake and utilization of long chain fatty acids in muscle and adipose tissues of CD36 knockout mice. J Biol Chem. 2000;275:32523-9 doi: 10.1074/jbc.M003826200
    Cooper CE, Hurley LL, Deviche P. Physiological responses of wild zebra finches (Taeniopygia guttata) to heatwaves. J Exp Biol. 2020;223:1-20
    Coort SLM, Hasselbaink DM, Koonen DPY. Enhanced sarcolemmal FAT/CD36 content and triacylglycerol storage in cardiac myocytes from obese zucker rats. Diabetes. 2004;53:1655-63 doi: 10.2337/diabetes.53.7.1655
    Cui DQ, Wang N, Ge JR. The role of temperature as a driver of metabolic flexibility in the Red-billed Leiothrix (Leiothrix lutea). Avian Res. 2019;10:46 doi: 10.1186/s40657-019-0184-3
    Del Vesco AP, Gasparino E. Production of reactive oxygen species, gene expression, and enzymatic activity in quail subjected to acute heat stress. J Anim Sci. 2013;91:582-7 doi: 10.2527/jas.2012-5498
    Diffenbaugh NS, Field CB. Changes in ecologically critical terrestrial climate conditions. Science. 2013;341:486-92 doi: 10.1126/science.1237123
    El Golli-Bennour E, Bacha H. HSP70 expression as biomarkers of oxidative stress: mycotoxins’ exploration. Toxicology. 2011;287:1-7 doi: 10.1016/j.tox.2011.06.002
    Fang XL, Zhu XT, Chen SF. Differential gene expression pattern in hypothalamus of chickens during fasting-induced metabolic reprogramming: functions of glucose and lipid metabolism in the feed intake of chickens. J Poult sci. 2014;93:2841-54 doi: 10.3382/ps.2014-04047
    Farag MR, Alagawany M. Physiological alterations of poultry to the high environmental temperature. J Therm Biol. 2018;76:101-6 doi: 10.1016/j.jtherbio.2018.07.012
    Feder ME, Hofmann GE. Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol. 1999;61:243-82
    Freeman MT, Czenze ZJ, Schoeman K. Extreme hyperthermia tolerance in the world’s most abundant wild bird. Sci Rep. 2020;10:13098 doi: 10.1038/s41598-020-69997-7
    Gibb AA, Hill BG. Metabolic coordination of physiological and pathological cardiac remodeling. Circulation. 2018;123:107-28 doi: 10.1161/circresaha.118.312017
    Guglielmo CG. Move that fatty acid: fuel selection and transport in migratory birds and bats. Integr Comp Biol. 2010;50:336-45 doi: 10.1093/icb/icq097
    Heather LC, Cole MA, Lygate CA. Fatty acid transporter levels and palmitate oxidation rate correlate with ejection fraction in the infarcted rat heart. Cardiovasc Res. 2006;72:430-7 doi: 10.1016/j.cardiores.2006.08.020
    Heather LC, Howell NJ, Emmanuel Y. Changes in cardiac substrate transporters and metabolic proteins mirror the metabolic shift in patients with aortic stenosis. PloS One. 2011;6:e26326 doi: 10.1371/journal.pone.0026326
    Hu RZ, He YJ, Arowolo MA. Polyphenols as potential attenuators of heat stress in poultry production. Antioxidants. 2019;8:11 doi: 10.3390/antiox8010011
    Hulbert AJ, Pamplona R, Buffenstein R. Life and death: metabolic rate, membrane composition, and life span of animals. Physiol Rev. 2007;87:1175-213 doi: 10.1152/physrev.00047.2006
    Hutter JJ, Mestril R, Tam EK. Overexpression of heat shock protein 72 in transgenic mice decreases infarct size in vivo. Circulation. 1996;94:1408-11 doi: 10.1161/01.CIR.94.6.1408
    Ismail IB, Al-Busadah KA, El-Bahr SM. Oxidative stress biomarkers and biochemical profile in broilers chicken fed zinc bacitracin and ascorbic acid under hot climate. Am J Biochem Mol Biol. 2013;3:202-14 doi: 10.3923/ajbmb.2013.202.214
    Jimenez AG, O’connor ES, Tobin KJ. Does cellular metabolism from primary fibroblasts and oxidative stress in blood differ between mammals and birds? The (lack-thereof) scaling of oxidative stress. Integr Comp Biol. 2019;59:953-69 doi: 10.1093/icb/icz017
    Joergensen LB, Overgaard J, Hunter-Manseau F. Dramatic changes in mitochondrial substrate use at critically high temperatures: a comparative study using. J Exp Biol. 2021;224:240960 doi: 10.1242/jeb.240960
    Li M, Wang XS, Xu FP. The change in heat shock protein expression in avermectin induced neurotoxicity of the pigeon (Columba livia) both in vivo and in vitro. Ecotoxicol Environ Saf. 2014;110:95-102 doi: 10.1016/j.ecoenv.2014.08.015
    Li M, Zhou S, Wang X. Effects of in vitro and in vivo avermectin exposure on alpha synuclein expression and proteasomal activity in pigeons. Ecotoxicol Environ Saf. 2017;135:24-31 doi: 10.1016/j.ecoenv.2016.09.014
    Liu M, Wang XL, Yuan SB. Study on heat stress and anti-stress effect of chitosan on the Red-billed Leiothrixs (Leiothrix lutea). J China West Norm U (Nat Sci Ed). 2015;36:1-6
    Lu Z, He XF, Ma BB. Chronic heat stress impairs the quality of breast-muscle meat in broilers by affecting redox status and energy-substance metabolism. J Agric Food Chem. 2017;65:11251-8 doi: 10.1021/acs.jafc.7b04428
    Mates JM, Perez-Gomez C, Nunez DC. Antioxidant enzymes and human diseases. Clin Biochem. 1999;32:595-603 doi: 10.1016/S0009-9120(99)00075-2
    Mayer MP, Gierasch LM. Recent advances in the structural and mechanistic aspects of HSP70 molecular chaperones. J Biol Chem. 2019;294:2085-97 doi: 10.1074/jbc.rev118.002810
    Mcfarlan JT, Bonen A, Guglielmo CG. Seasonal upregulation of fatty acid transporters in flight muscles of migratory white-throated sparrows (Zonotrichia albicollis). J Exp Biol. 2009;212:2934-40 doi: 10.1242/jeb.031682
    Mckechnie AE, Hockey PaR, Wolf BO. Feeling the heat: Australian landbirds and climate change. Emu. 2012;112:1-7 doi: 10.12929/jls.05.2.01
    Mihara M, Uchiyama M. Determination of malonaldehyde precursor in tissues by thiobarbituric acid test. Anal Biochem. 1978;86:271-8 doi: 10.1016/0003-2697(78)90342-1
    Mujahid A, Akiba Y, Toyomizu M. Acute heat stress induces oxidative stress and decreases adaptation in young white leghorn cockerels by downregulation of avian uncoupling protein. Poultly Sci. 2007;86:364-71 doi: 10.1093/ps/86.2.364
    Mujahid A, Sato K, Akiba Y. Acute heat stress stimulates mitochondrial superoxide production in broiler skeletal muscle, possibly via downregulation of uncoupling protein content. Poultly Sci. 2006;85:1259-65 doi: 10.1093/ps/85.7.1259
    Musatov A, Carroll CA, Liu YC. Identification of bovine heart cytochrome c oxidase subunits modified by the lipid peroxidation product 4-hydroxy-2-nonenal. Biochemistry. 2002;41:8212-20 doi: 10.1021/bi025896u
    Nawab A, Ibtisham F, Li G. Heat stress in poultry production: mitigation strategies to overcome the future challenges facing the global poultry industry. J Therm Biol. 2018;78:131-9 doi: 10.1016/j.jtherbio.2018.08.010
    Negre-Salvayre A, Hirtz C, Carrera G. A role for uncoupling protein-2 as a regulator of mitochondrial hydrogen peroxide generation. FASEB. 1997;11:809-15 doi: 10.1096/fasebj.11.10.9271366
    Osakabe M, Imamura T, Nakano R. Combination of restriction endonuclease digestion with the ΔΔCt method in real-time PCR to monitor etoxazole resistance allele frequency in the two-spotted spider mite. Pestic Biochem Physiol. 2017;139:1-8 doi: 10.1016/j.pestbp.2017.04.003
    Palmieri F. Mitochondrial carrier proteins. FEBS. 1994;346:48-54 doi: 10.1016/0014-5793(94)00329-7
    Pamplona R, Costantini D. Molecular and structural antioxidant defenses against oxidative stress in animals. Am J Physiol-REG. 2011;301:R843-63 doi: 10.1152/ajpregu.00034.2011
    Pearce SC, Gabler NK, Ross JW. The effects of heat stress and plane of nutrition on metabolism in growing pigs. J Anim Sci. 2013;91:2108-18 doi: 10.2527/jas.2012-5738
    Price ER, Mcfarlan JT, Guglielmo CG. Preparing for migration? The effects of photoperiod and exercise on muscle oxidative enzymes, lipid transporters, and phospholipids in white-crowned sparrows. Physiol Biochem Zool. 2010;83:252-62 doi: 10.1086/605394
    Putri M, Syamsunarno MR, Iso T. CD36 is indispensable for thermogenesis under conditions of fasting and cold stress. Biochem Biophys Res Commun. 2015;457:520-5 doi: 10.1016/j.bbrc.2014.12.124
    Rehaman Z-U, Chand N, Khan S. Evaluating the immune response and antioxidant potential in four broiler strains under chronic high ambient temperature. Pak J Zool. 2017;49:2087-91
    Riddell EA, Iknayan KJ, Hargrove L. Exposure to climate change drives stability or collapse of desert mammal and bird communities. Science. 2021;371:633-6 doi: 10.1126/science.abd4605
    Sanders SR, Cole LC, Flann KL. Effects of acute heat stress on skeletal muscle gene expression associated with energy metabolism in rats. FASEB. 2009;23:589
    Shan Q, Ma FT, Wei JY. Physiological functions of heat shock proteins. Curr Protein Pept Sci. 2020;21:751-60 doi: 10.2174/1389203720666191111113726
    Sheafor BA. Metabolic enzyme activities across an altitudinal gradient: an examination of pikas (genus Ochotona). J Exp biol. 2003;206:1241-9 doi: 10.1242/jeb.00226
    Shwartz G, Rhoads ML, Vanbaale MJ. Effects of a supplemental yeast culture on heat-stressed lactating holstein cows. J Dairy Sci. 2009;92:935-42 doi: 10.3168/jds.2008-1496
    Sotome R, Hirasawa A, Kikusato M. In vivo emergence of beige-like fat in chickens as physiological adaptation to cold environments. Amino Acids. 2021;53:381-93 doi: 10.1007/s00726-021-02953-5
    Stillman JH. Heat waves, the new normal: summertime temperature extremes will impact animals, ecosystems, and human communities. Physiology. 2019;34:86-100 doi: 10.1152/physiol.00040.2018
    Surai PF, Kochish II, Fisinin VI. Antioxidant defence systems and oxidative stress in poultry biology: an update. Antioxidants. 2019;8:235 doi: 10.3390/antiox8070235
    Stager M, Swanson DL, Cheviron ZA. Regulatory mechanisms of metabolic flexibility in the dark-eyed junco (Junco hyemalis). J Exp Biol. 2015;218:767-77 doi: 10.1242/jeb.113472
    Tan S, Wen J, Shi LL. The increase in fat content in the warm-acclimated striped hamsters is associated with the down-regulated metabolic thermogenesis. Comp Biochem Physiol A. 2016;201:162-72 doi: 10.1016/j.cbpa.2016.07.013
    Tran DH, Wang ZV. Glucose metabolism in cardiac hypertrophy and heart failure. J Am Heart Assoc. 2019;8:e012673 doi: 10.1161/JAHA.119.012673
    Vandana G, Sejian V, Lees A. Heat stress and poultry production: impact and amelioration. Int J Biometeorol. 2021;65:163-79 doi: 10.1007/s00484-020-02023-7
    Warren R, Price J, Graham E. The projected effect on insects, vertebrates, and plants of limiting global warming to 1.5 ℃ rather than 2 ℃. Science. 2018;360:791-5 doi: 10.1126/science.aar3646
    Yu JM, Bao ED, Yan JY. Expression and localization of HSPs in the heart and blood vessel of heat-stressed broilers. Cell Stress Chaperones. 2008;13:327-35 doi: 10.1007/s12192-008-0031-7
    Zeng T, Li JJ, Wang DQ. Effects of heat stress on antioxidant defense system, inflammatory injury, and heat shock proteins of Muscovy and Pekin ducks: evidence for differential thermal sensitivities. Cell Stress Chaperones. 2014;19:895-901 doi: 10.1007/s12192-014-0514-7
    Zheng WH, Li M, Liu JS. Seasonal acclimatization of metabolism in Eurasian tree sparrows (Passer montanus). Comp Biochem Physiol. 2008;151:519-25 doi: 10.1016/j.cbpa.2008.07.009
    Zhou SS, Cao LL, Xu WD. Effect of temperature on oxidative stress, antioxidant levels and uncoupling protein expression in striped hamsters. Comp Biochem Physiol. 2015;189:84-90 doi: 10.1016/j.cbpa.2015.07.017
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