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Glutathione peroxidases in poultry biology: Part 1. Classification and mechanisms of action

Published online by Cambridge University Press:  21 March 2018

P.F. SURAI*
Affiliation:
Trakia University, Stara Zagora, Bulgaria Moscow State Academy of Veterinary Medicine and Biotechnologynamed after K.I. Skryabin, Moscow, Russia Szent Istvan University, Godollo, Hungary Sumy National Agrarian University, Sumy, Ukraine Odessa National Academy of Food Technologies, Ukraine
I.I. KOCHISH
Affiliation:
Moscow State Academy of Veterinary Medicine and Biotechnologynamed after K.I. Skryabin, Moscow, Russia
V.I. FISININ
Affiliation:
All Russian Institute of Poultry Husbandry, Sergiev Posad, Russia
*
Corresponding author: [email protected]
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Abstract

Glutathione peroxidase (GSH-Px) was described as a selenoprotein in 1973 and, since then, a great body of information has been accumulated to validate its important role in the antioxidant defence network in all animals, including poultry. The GSH-Px family includes at least eight members, and four of them (GSH-Px1, GSH-Px2, GSH-Px3 and GSH-Px4) are shown to be selenoproteins in animals. They are characterised by species- and tissue-specificity in their expression and activity. An optimal Se status in tissues/body is key for maximum expression of GSH-Px and therefore, in avian research GSH-Px activity is widely used as a biomarker for determining Se status and requirements. On the other hand, GSH-Px is an inducible enzyme and its activity depends on the level of stress and can be used as an index of antioxidant defences. In poultry production two forms of Se-dependent GSH-Px (GSH-Px1 and GSH-Px4) have received most attention. The aim of this paper is to review GSH-Px properties and functions in relation to poultry biology with special emphasis to its role in chicken adaptation to various stress conditions. Recent advances in selenoprotein identification and characterisation in relation to poultry Se status, dietary sources of Se and stress conditions can shed light on the roles of GSH-Px in avian biology.

Type
Review
Copyright
Copyright © World's Poultry Science Association 2018 

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References

ARAI, T., SUGAWARA, M., SAKO, T., MOTOYOSHI, S., SHIMURA, T., TSUTSUI, N. and KONNO, T. (1994) Glutathione peroxidase activity in tissues of chickens supplemented with dietary selenium. Comparative Biochemistry and Physiology 107A: 245-248.Google Scholar
BANNING, A., DEUBEL, S., KLUTH, D., ZHOU, Z. and BRIGELIUS-FLOHÉ, R. (2005) The GI-GPx gene is a target for Nrf2. Molecular and Cell Biology 25: 4914-4923.CrossRefGoogle ScholarPubMed
BERTELSMANN, H., KUEHBACHER, M., WESELOH, G., KYRIAKOPOULOS, A. and BEHNE, D. (2007) Sperm nuclei glutathione peroxidases and their occurrence in animal species with cysteine-containing protamines. Biochimica et Biophysica Acta 1770: 1459-1467.CrossRefGoogle ScholarPubMed
BREQUE, C., SURAI, P. and BRILLARD, J.P. (2006) Antioxidant status of the lower oviduct in the chicken varies with age and dietary vitamin E supplementation. Molecular Reproduction and Development 73: 1045-1051.CrossRefGoogle ScholarPubMed
BRIGELIUS-FLOHÉ, R. and MAIORINO, M. (2013) Glutathione peroxidases. Biochimica et Biophysica Acta 1830: 3289-3303.CrossRefGoogle ScholarPubMed
BUNK, M.J. and COMBS, G.F. (Jr) (1980) Effect of selenium on appetite in the selenium-deficient chick. Journal of Nutrition 110: 743-749.Google Scholar
CHADIO, S.E., PAPPAS, A.C., PAPANASTASATOS, A., PANTELIA, D., DARDAMANI, A., FEGEROS, K. and ZERVAS, G. (2015) Effects of high selenium and fat supplementation on growth performance and thyroid hormones concentration of broilers. Journal of Trace Elements in Medicine and Biology 29: 202-207.Google Scholar
CHANCE, B., SIES, H. and BOVERIES, A. (1979) Hydroperoxide metabolism in mammalian organs. Physiological Reviews 59: 527-605.CrossRefGoogle ScholarPubMed
CHU, F.F., DOROSHOW, J.H. and ESWORTHY, R.S. (1993) Expression, Characterization, and Tissue Distribution of a New Cellular Selenium-dependent Glutathione Peroxidase, GSHPx-GI. The Journal of Biological Chemistry 268: 2571-2576.CrossRefGoogle ScholarPubMed
COHEN, H.J. and AVISSAR, N. (1993) Molecular and biochemical aspects of selenium metabolism and deficiency. Progress in Clinical and Biological Research 380: 191-202.Google Scholar
COWAN, D.B., WEISEL, R.D., WILLIAMS, W.G. and MICKLE, D.A. (1993) Identification of oxygen responsive elements in the 5'-flanking region of the human glutathione peroxidase gene. Journal of Biological Chemistry 268: 26904-26910.CrossRefGoogle ScholarPubMed
CRACK, P.J., TAYLOR, J.M., ALI, U., MANSELL, A. and HERTZOG, P.J. (2006) Potential contribution of NF-kappaB in neuronal cell death in the glutathione peroxidase-1 knockout mouse in response to ischemia-reperfusion injury. Stroke 37: 1533-1538.CrossRefGoogle ScholarPubMed
DAUN, C. and AKESSON, B. (2004) Glutathione peroxidase activity, and content of total and soluble selenium in five bovine and porcine organs used in meat production. Meat Science 66: 801-807.CrossRefGoogle ScholarPubMed
DE HAAN, J.B., CRACK, P.J., FLENTJAR, N., IANNELLO, R.C., HERTZOG, P.J. and KOLA, I. (2003) An imbalance in antioxidant defense affects cellular function: the pathophysiological consequences of a reduction in antioxidant defense in the glutathione peroxidase-1 (Gpx1) knockout mouse. Redox Report 8: 69-79.Google Scholar
ENGBERG, R.M., LAURIDSEN, C., JENSEN, S.K. and JAKOBSEN, K. (1996) Inclusion of oxidized vegetable oil in broiler diets. Its influence on nutrient balance and on the antioxidative status of broilers. Poultry Science 75: 1003-1011.Google Scholar
ESWORTHY, R.S., SWIDEREK, K.M., HO, Y.S. and CHU, F.F. (1998) Selenium-dependent glutathione peroxidase-GI is a major glutathione peroxidase activity in the mucosal epithelium of rodent intestine . Biochimica et Biophysica Acta 1381: 213-226.CrossRefGoogle Scholar
FLOHE, L. and BRIGELIUS-FLOHE, R. (2016) Basics and news on glutathione peroxidases, in: HATFIELD, D.L., SCHWEIZER, U., TSUI, P.A. & GLADYSHEV, V.N. (Eds) Selenium. Its molecular biology and role in human health, pp.211-222 (Fourth Edition, Springer, New York).Google Scholar
GAO, Y., ZHANG, J., HUANG, X. and ZHANG, G. (2017) Glutathione Peroxidase 1, Selenoprotein K, and Selenoprotein H May Play Important Roles in Chicken Testes in Response to Selenium Deficiency. Biological Trace Element Research 179: 271-276.CrossRefGoogle ScholarPubMed
GHEISARI, H.R. and MOTAMEDI, H. (2010) Chloride salt type/ionic strength and refrigeration effects on antioxidant enzymes and lipid oxidation in cattle, camel and chicken meat. Meat Science 86: 377-383.Google Scholar
HANDY, D.E., LUBOS, E., YANG, Y., GALBRAITH, J.D., KELLY, N., ZHANG, Y.Y., LEOPOLD, J.A. and LOSCALZO, J. (2009) Glutathione peroxidase-1 regulates mitochondrial function to modulate redox-dependent cellular responses. Journal of Biological Chemistry 284: 11913-11921.CrossRefGoogle ScholarPubMed
HOAC, T., DAUN, C., TRAFIKOWSKA, U., ZACKRISSON, J. and ÅKESSON, B. (2006) Influence of heat treatment on lipid oxidation and glutathione peroxidase activity in chicken and duck meat. Innovative Food Science and Emerging Technologies 7: 88-93.Google Scholar
IMAI, H. and NAKAGAWA, Y. (2003) Biological significance of phospholipid hydroperoxide glutathione peroxidase (PHGPx, GPx4) in mammalian cells. Free Radical Biology & Medicine 34: 145-169.Google Scholar
IMAI, H., SUMI, D., HANAMOTO, A., ARAI, M. and SUGIYAMA, A. (1995) Molecular cloning and functional expression of a cDNA for rat phospholipid hydroperoxide glutathione peroxidase: 3'-untranslated region of the gene is necessary for functional expression. Journal of Biochemistry(Tokyo) 118: 1061-1067.CrossRefGoogle ScholarPubMed
JIANG, X.Q., CAO, C.Y., LI, Z.Y., LI, W., ZHANG, C., LIN, J., LI, X.N. and LI, J.L. (2017) Delineating hierarchy of selenotranscriptome expression and their response to selenium status in chicken central nervous system. Journal of Inorganic Biochemistry 169: 13-22.CrossRefGoogle ScholarPubMed
JIN, X., KENNEDY, S.W., DI MUCCIO, T. and MOON, T.W. (2001) Role of oxidative stress and antioxidant defense in 3,3',4,4',5-pentachlorobiphenyl-induced toxicity and species-differential sensitivity in chicken and duck embryos. Toxicology and Applied Pharmacology 172: 241-248.Google Scholar
KIM, Y.S. and COMBS, G.F. (1993) Effect of dietary selenium and vitamin E on glutathione concentrations and glutathione S-transferase activities in chick liver and plasma. Nutrition Research 13: 455-463.Google Scholar
KONG, B.W., KIM, H. and FOSTER, D.N. (2003) Cloning and expression analysis of chicken phospholipid-hydroperoxide glutathione peroxidase. Animal Biotechnology 14: 19-29.CrossRefGoogle ScholarPubMed
LI, J.L. and SUNDE, R.A. (2016) Selenoprotein Transcript Level and Enzyme Activity as Biomarkers for Selenium Status and Selenium Requirements of Chickens (Gallus gallus). PLoS One 11 (4): e0152392.Google Scholar
LUAN, Y., ZHAO, J., YAO, H., ZHAO, X., FAN, R., ZHAO, W., ZHANG, Z. and XU, S. (2016) Selenium Deficiency Influences the mRNA Expression of Selenoproteins and Cytokines in Chicken Erythrocytes. Biological Trace Element Research 171: 427-436.CrossRefGoogle ScholarPubMed
LUBOS, E., LOSCALZO, J. and HANDY, D.E. (2011) Glutathione peroxidase-1 in health and disease: from molecular mechanisms to therapeutic opportunities. Antioxidants & Redox Signaling 15: 1957-1997.Google Scholar
MADDIPATI, K.R. and MARNETT, L.J. (1987) Characterization of the Major Hydroperoxide-Reducing Activity of Human Plasma. Purification and Properties of a Selenium-Dependent Glutathione Peroxidase. The Journal of Biological Chemistry 262: 17398-17403.Google Scholar
MANN, K. and MANN, M. (2008) The chicken egg yolk plasma and granule proteomes. Proteomics 8: 178-191.CrossRefGoogle ScholarPubMed
MIYAZAKI, S. (1991) Effect of chemicals on glutathione peroxidase of chick liver. Research in Veterinary Science 51: 120-122.Google Scholar
MIYAZAKI, S. and MOTOI, Y. (1992) Tissue distribution of monomeric glutathione peroxidase in broiler chicks. Research in Veterinary Science 53: 47-51.Google Scholar
MIYAZAKI, S. and MOTOI, Y. (1996) Purification and characterisation of chicken liver monomeric glutathione peroxidase. British Poultry Science 37: 651-660.Google Scholar
MORK, H., LEX, B., SCHEURLEN, M., DREHER, I., SCHUTZE, N., KOHRLE, J. and JAKOB, F. (1998) Expression pattern of gastrointestinal selenoproteins - targets for selenium supplementation. Nutrition and Cancer 32: 64-70.CrossRefGoogle ScholarPubMed
MUGESH, G. and SINGH, H.B. (2000) Synthetic organoselenium compounds as antioxidants: glutathione peroxidase activity. Chemical Society Reviews 29: 347-357.Google Scholar
NAM, S.Y., BAEK, I.J., LEE, B.J., IN, C.H., JUNG, E.Y., YON, J.M., AHN, B., KANG, J.K., YU, W.J. and YUN, Y.W. (2003) Effects of 17beta-estradiol and tamoxifen on the selenoprotein phospholipid hydroperoxide glutathione peroxidase (PHGPx) mRNA expression in male reproductive organs of rats. The Journal of Reproduction and Development 49: 389-396.Google Scholar
NAYERNIA, K., DIACONU, M., AUMULLER, G., WENNEMUTH, G., SCHWANDT, I., KLEENE, K., KUEHN, H. and ENGEL, W. (2004) Phospholipid hydroperoxide glutathione peroxidase: expression pattern during testicular development in mouse and evolutionary conservation in spermatozoa. Molecular Reproduction and Development 67: 458-464.CrossRefGoogle ScholarPubMed
OMAYE, S.T. and TAPPEL, A.L. (1974) Effect of dietary selenium on glutathione peroxidase in the chick. Journal of Nutrition 104: 747-753.Google Scholar
PANNALA, V.R., BAZIL, J.N., CAMARA, A.K. and DASH, R.K. (2014) A mechanistic mathematical model for the catalytic action of glutathione peroxidase. Free Radical Research 48: 487-502.CrossRefGoogle ScholarPubMed
PARTYKA, A., LUKASZEWICZ, E. and NIŻAŃSKI, W. (2012) Lipid peroxidation and antioxidant enzymes activity in avian semen. Animal Reproduction Science 134: 184-190.CrossRefGoogle ScholarPubMed
PARTYKA, A., ŁUKASZEWICZ, E. and NIŻAŃSKI, W. (2012a) Effect of cryopreservation on sperm parameters, lipid peroxidation and antioxidant enzymes activity in fowl semen. Theriogenology 77: 1497-1504.Google Scholar
ROTRUCK, J.T., POPE, A.L., GANTHER, H.E., SWANSON, A.B., HAFEMAN, D.G. and HOEKSTRA, W.G. (1973) Selenium: biochemical role as a component of glutathione peroxidase. Science 179: 588-590.Google Scholar
ROVERI, A., MAIORINO, M., NISII, C. and URSINI, F. (1994) Purification and characterization of phospholipid hydroperoxide glutathione peroxidase from rat testis mitochondrial membranes. Biochimica et Biophysica Acta 1208: 211-221.CrossRefGoogle ScholarPubMed
SAVASKAN, N.E., UFER, C., KÜHN, H. and BORCHERT, A. (2007) Molecular biology of glutathione peroxidase 4: from genomic structure to developmental expression and neural function. Biological Chemistry 388: 1007-1017.Google Scholar
SHARMA, A., YUEN, D., HUET, O., PICKERING, R., STEFANOVIC, N., BERNATCHEZ, P. and DE HAAN, J.B. (2016) Lack of glutathione peroxidase-1 facilitates a pro-inflammatory and activated vascular endothelium. Vascular Pharmacology 79: 32-42.Google Scholar
SINGH, A., RANGASAMY, T., THIMMULAPPA, R.K., LEE, H., OSBURN, W.O., BRIGELIUS-FLOHÉ, R., KENSLER, T.W., YAMAMOTO, M. and BISWAL, S. (2006) Glutathione peroxidase 2, the major cigarette smoke-inducible isoform of GPX in lungs, is regulated by Nrf2. American Journal of Respiratory Cell and Molecular Biology 35: 639-650.CrossRefGoogle ScholarPubMed
STARRS, A.P., ORGEIG, S., DANIELS, C.B., DAVIES, M. and LOPATKO, O.V. (2001) Antioxidant enzymes in the developing lungs of egg-laying and metamorphosing vertebrates. Journal of Experimental Biology 204: 3973-3981.Google Scholar
SUNDE, R.A. (1993) Intracellular glutathione peroxidases - structure, regulation, and function, in: BURK, RF. (Ed.) Selenium in Biology and Human Health, pp.45-77 (Springer-Verlag New-York).Google Scholar
SUNDE, R.A. and HADLEY, K.B. (2010) Phospholipid hydroperoxide glutathione peroxidase (Gpx4) is highly regulated in male turkey poults and can be used to determine dietary selenium requirements. Experimental Biology and Medicine 235: 23-31.CrossRefGoogle ScholarPubMed
SUNDE, R.A., SUNDE, G.R., SUNDE, C.M., SUNDE, M.L. and EVENSON, J.K. (2015) Cloning, Sequencing, and Expression of Selenoprotein Transcripts in the Turkey (Meleagris gallopavo). PLoS One 10 (6): e0129801.Google Scholar
SURAI, P.F. (1999) Tissue-specific changes in the activities of antioxidant enzymes during the development of the chicken embryo. British Poultry Science 40: 397-405.Google Scholar
SURAI, P.F. (2006) Selenium in Nutrition and Health. Nottingham University Press, Nottingham, UK.Google Scholar
SURAI, P.F. (2015) Carnitine Enigma: From Antioxidant Action to Vitagene Regulation. Part 2. Transcription Factors and Practical Applications. Journal of Veterinary Science and Medicine 3 (2): 17.Google Scholar
SURAI, P.F., BLESBOIS, E., GRASSEAU, I., GHALAH, T., BRILLARD, J-P., WISHART, G., CEROLINI, S. and SPARKS, N.H.C. (1998a) Fatty acid composition, glutathione peroxidase and superoxide dismutase activity and total antioxidant activity of avian semen. Comparative Biochemistry and Physiology 120B: 527-533.Google Scholar
SURAI, P.F., BRILLARD, J-P., SPEAKE, B.K., BLESBOIS, E., SEIGNEURIN, F. and SPARKS, N.H.C. (2000) Phospholipid fatty acid composition, vitamin E content and susceptibility to lipid peroxidation of duck spermatozoa. Theriogenology 53: 1025-1039.CrossRefGoogle ScholarPubMed
SURAI, P.F., CEROLINI, S., WISHART, G.J., SPEAKE, B.K., NOBLE, R.C. and SPARKS, N.H.C. (1998b) Lipid and antioxidant composition of chicken semen and its susceptibility to peroxidation. Poultry and Avian Biology Reviews 9: 11-23.Google Scholar
SURAI, P.F. and FISININ, V.I. (2016a) Vitagenes in poultry production. Part 1. Environmental and technological stresses. World's Poultry Science Journal 72: 721-734.Google Scholar
SURAI, P.F. and FISININ, V.I. (2016b) Vitagenes in poultry production. Part 1. Nutritional and Internal stresses. World's Poultry Science Journal 72: 761-772.Google Scholar
SURAI, P.F., KOSTJUK, I.A., WISHART, G., MACPHERSON, A., SPEAKE, B., NOBLE, R.C., IONOV, I.A. and KUTZ, E. (1998c) Effect of vitamin E and selenium of cockerel diets on glutathione peroxidase activity and lipid peroxidation susceptibility in sperm, testes and liver. Biological Trace Element Research 64: 119-132.Google Scholar
SURAI, P.F., SPEAKE, B.K., NOBLE, R.C. and SPARKS, N.H.C. (1999) Tissue-specific antioxidant profiles and susceptibility to lipid peroxidation of the newly hatched chick. Biological Trace Element Research 68: 63-78.Google Scholar
TAKAHASHI, K., AVISSAR, N., WHITIN, J. and COHEN, H. (1987) Purification and characterization of human plasma glutathione peroxidase: a selenoglycoprotein distinct from the known cellular enzyme. Archives of Biochemistry and Biophysics 256: 677-686.CrossRefGoogle ScholarPubMed
TAPPEL, M.E., CHAUDIERE, J. and TAPPEL, A.L. (1982) Glutathione peroxidase activities of animal tissues. Comparative Biochemistry and Physiology B. 73: 945-949.Google Scholar
TAYLOR, R.M. and SUNDE, R.A. (2016) Selenoprotein Transcript Level and Enzyme Activity as Biomarkers for Selenium Status and Selenium Requirements in the Turkey (Meleagris gallopavo). PLoS One 11 (3): e0151665.Google Scholar
URSINI, F., MAIORINO, M. and GREGOLIN, C. (1985) The selenoenzyme phospholipid hydroperoxide glutathione peroxidase. Biochimica et Biophysica Acta 839: 62-70.Google Scholar
URSINI, F., HEIM, S., KIESS, M., MAIORINO, M., ROVERI, A., WISSING, J. and FLOHÉ, L. (1999) Dual function of the selenoprotein PHGPx during sperm maturation. Science 285: 1393-1396.Google Scholar
VENDITTI, P., DANIELE, C.M., BALESTRIERI, M. and DI MEO, S. (1999) Protection against oxidative stress in liver of four different vertebrates. Journal of Experimental Zoology 284: 610-616.3.0.CO;2-I>CrossRefGoogle ScholarPubMed
YAO, H., ZHAO, W., ZHAO, X., FAN, R., KHOSO, P.A., ZHANG, Z., LIU, W. and XU, S. (2014) Selenium deficiency mainly influences the gene expressions of antioxidative selenoproteins in chicken muscles. Biological Trace Element Research 161: 318-327.Google Scholar
ZENTENO-SAVIN, T., ST LEGER, J. and PONGANIS, P.J. (2010) Hypoxemic and ischemic tolerance in emperor penguins. Comparative Biochemistry and Physiology C. Toxicology and Pharmacology 152: 18-23.Google Scholar
ZHANG, J.L., XU, B., HUANG, X.D., GAO, Y.H., CHEN, Y. and SHAN, A.S. (2016) Selenium Deficiency Affects the mRNA Expression of Inflammatory Factors and Selenoprotein Genes in the Kidneys of Broiler Chicks. Biological Trace Element Research 171: 201-207.CrossRefGoogle ScholarPubMed
ZOIDIS, E., PAPPAS, A.C., GEORGIOU, C.A., KOMAITIS, E. and FEGGEROS, K. (2010) Selenium affects the expression of GPx4 and catalase in the liver of chicken. Comparative Biochemistry and Physiology. B Biochemistry and Molecular Biology 155: 294-300.CrossRefGoogle ScholarPubMed