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Molecular targets of dietary phytochemicals for the alleviation of heat stress in poultry

Published online by Cambridge University Press:  25 February 2013

K. SAHIN*
Affiliation:
Department of Animal Nutrition, Faculty of Veterinary Science, Firat University, Elazig, Turkey
C. ORHAN
Affiliation:
Department of Animal Nutrition, Faculty of Veterinary Science, Firat University, Elazig, Turkey
M.O. SMITH
Affiliation:
Department of Animal Science, The University of Tennessee, TN, USA
N. SAHIN
Affiliation:
Department of Animal Nutrition, Faculty of Veterinary Science, Firat University, Elazig, Turkey
*
Corresponding author: nsahinkm@yahoo.com
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Abstract

Heat stress compromises performance and productivity through reducing feed intake, while decreasing nutrient utilisation, growth rate, egg production, egg quality and feed efficiency, leading to economic losses in poultry. High temperatures can lead to oxidative stress associated with a reduced antioxidant status in the bird in vivo, as reflected by increased oxidative damage and lowered plasma concentrations of antioxidants. Several strategies are currently available to alleviate the negative effects of high environmental temperature on the performance of poultry. However, as it is expensive to cool buildings in which animals are housed, many efforts are focused on dietary manipulation. In terms of reducing the negative effects of environmental stress, antioxidants are used in poultry feed because of the reported benefits of these supplements, including their anti-stress effects. In this review, the mode of action of these supplements is investigated, and evidence is presented showing that phytochemicals can alter several cell signalling pathways. The agents include epigallocatechin-3-gallate (EGCG; green tea), lycopene (tomato) and resveratrol (red grapes, peanuts and berries). The cell-signalling pathways inhibited by EGCG include transcription factors (nuclear factor kappa-light-chain-enhancer of activated B cells (NF-κB)) and nuclear factors (erythroid-derived 2-like 2 (Nrf2)) and activator protein-1 (AP-1) that regulate cyclooxygenase-2 (COX-2). This review will also address some of the mechanisms proposed for the heat stress preventive activity of EGCG, lycopene and resveratrol focusing on the induction of antioxidant enzymes (phase II enzymes) through the activation of the antioxidant response element (ARE) transcription system.

Type
Reviews
Copyright
Copyright © World's Poultry Science Association 2013

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References

AGGARWAL, B.B. and SHISHODIA, S. (2006) Molecular targets of dietary agents for prevention and therapy of cancer. Biochemical Pharmacology 71: 1397-1421.CrossRefGoogle ScholarPubMed
ALI, S. and MANN, D.A. (2004) Signal transduction via the NF-kappaB pathway: a targeted treatment modality for infection, inflammation and repair. Cell Biochemistry and Function 22: 67-79.CrossRefGoogle ScholarPubMed
ANDO, M., KATAGIRI, K., YAMAMOTO, S., WAKAMATSU, K., KAWAHARA, I., ASANUMA, S., USUDA, M. and SASAKI, K. (1997) Age-related effects of heat stress on protective enzymes for peroxides and microsomal monooxygenase in rat liver. Environmental Health Perspectives 105: 726-733.Google ScholarPubMed
BEN-DOR, A., STEINER, M., GHEBER, L., DANILENKO, M., DUBI, N., LINNEWIEL, K., ZICK, A., SHARONI, Y. and LEVY, J. (2005) Carotenoids activate the antioxidant response element transcription system. Molecular Cancer Therapeutics 4: 177-186.CrossRefGoogle ScholarPubMed
BOGIN, E., AVIDAR, Y., PECH-WAFFENSCHMIDT, V., DORON, Y., ISRAELI, B.A. and KEVHAYEV, E. (1996) The relationship between heat stress, survivability and blood composition of the domestic chicken. European Journal of Clinical Chemistry and Clinical Biochemistry 34: 463-469.Google Scholar
DINKOVA-KOSTOVA, A.T., HOLTZCLAW, W.D., COLE, R.N., ITOH, K., WAKABAYASHI, N., KATOH, Y., YAMAMOTO, M. and TALALAY, P. (2002) Direct evidence that sulfhydryl groups of Keap1 are the sensors regulating induction of phase 2 enzymes that protect against carcinogens and oxidants. Proceedings of the National Academy of Sciences of the United States of America 99: 11908-11913.CrossRefGoogle ScholarPubMed
ETCHES, R., JOHN, J.M. and GIBBINS, A.M.V. (2008) Behavioural, physiological, neuroendocrine and molecular responses to heat stress, in: DAGHIR, N.J. (Ed.) Poultry Production in Hot Climates, Second Edition, pp. 48-79 (CAB International, Wallingford, UK).Google Scholar
GARG, R. and MARU, G. (2009) Dietary curcumin enhances benzo(a)pyrene-induced apoptosis resulting in a decrease in BPDE-DNA adducts in mice. Journal of Environmental Pathology, Toxicology and Oncology 28: 121-131.Google Scholar
GILMORE, T.D. (2006) Introduction to NF-kappaB: players, pathways, perspectives. Oncogene 25: 6680-6684.Google Scholar
GUPTA, S.C., SUNDARAM, C., REUTER, S. and AGGARWAL, B.B. (2010) Inhibiting NF-κB activation by small molecules as a therapeutic strategy. Biochimica et Biophysica Acta 1799: 775-787.Google Scholar
GUPTA, A., KUMAR, A. and KULKARNI, S.K. (2011) Targeting oxidative stress, mitochondrial dysfunction and neuroinflammatory signalling by selective cyclooxygenase (COX)-2 inhibitors mitigates MPTP-induced neurotoxicity in mice. Progress in Neuro-Psychopharmacology and Biological Psychiatry 35: 974-981.CrossRefGoogle ScholarPubMed
HARGREAVES, M., DILLO, P., ANGUS, D. and FEBBRAIO, M. (1996) Effect of fluid ingestion on muscle metabolism during prolonged exercise. Journal of Applied Physiology 80: 363-366.Google Scholar
ITOH, K., WAKABAYASHI, N., KATOH, Y., ISHII, T., IGARASHI, K., ENGEL, J.D. and YAMAMOTO, M. (1999) Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain. Genes and Development 13: 76-86.CrossRefGoogle Scholar
IWAGAMI, Y. (1996) Changes in the ultrastructure of human cells related to certain biological responses under hyperthermic culture conditions. Human Cell 9: 353-366.Google Scholar
KELLOFF, G.J., CROWELL, J.A., STEELE, V.E., LUBET, R.A., MALONE, W.A., BOONE, C.W., KOPELOVICH, L., HAWK, E.T., LIEBERMAN, R., LAWRENCE, J.A., ALI, I., VINER, J.L. and SIGMAN, C.C. (2000) Progress in cancer chemoprevention: development of diet-derived chemopreventive agents. Journal of Nutrition 130: 467-471.Google Scholar
KOBAYASHI, A., KANG, M.I., WATAI, Y., TONG, K.I., SHIBATA, T., UCHIDA, K. and YAMAMOTO, M. (2006) Oxidative and electrophilic stresses activate Nrf2 through inhibition of ubiquitination activity of Keap1. Molecular and Cellular Biology 26: 221-229.CrossRefGoogle ScholarPubMed
LI, H.Y., ZHONG, Y.F., WU, S.Y. and SHI, N. (2007) NF-E2 related factor 2 activation and heme oxygenase-1 induction by tert-butylhydroquinone protect against deltamethrin-mediated oxidative stress in PC12 cells. Chemical Research in Toxicology 20: 1242-1251.Google Scholar
LIAN, F. and WANG, X.D. (2008) Enzymatic metabolites of lycopene induce Nrf2-mediated expression of phase II detoxifying/antioxidant enzymes in human bronchial epithelial cells. International Journal of Cancer 123: 1262-1268.CrossRefGoogle ScholarPubMed
MAGER, W.H. and De KRUIJFF, A.J. (1995) Stress-induced transcriptional activation. Microbiological Reviews 59: 506-531.CrossRefGoogle ScholarPubMed
MANNA, S.K., MUKHOPADHYAY, A. and AGGARWAL, B.B. (2000) Resveratrol suppresses TNF-induced activation of nuclear transcription factors NF-kappa B, activator protein-1, and apoptosis: potential role of reactive oxygen intermediates and lipid peroxidation. The Journal of Immunology 164: 6509-6519.Google Scholar
MASHALY, M.M., HENDRICKS, G.L., KALAMA, M.A., GEHAD, A.E., ABBAS, A.O. and PATTERSON, P.H. (2004) Effect of heat stress on production parameters and immune responses of commercial laying hens. Poultry Science 83: 889-894.Google Scholar
MUJAHID, A., YOSHIKI, Y., AKIBA, Y. and TOYOMIZU, M. (2005) Superoxide radical production in chicken skeletal muscle induced by acute heat stress. Poultry Science 84: 307-314.Google Scholar
MUKHTAR, H. and AHMAD, N. (2000) Tea polyphenols: prevention of cancer and optimizing health. The American Journal of Clinical Nutrition 71: 1698-1704.Google Scholar
NA, H.K. and SURH, Y.J. (2008) Modulation of Nrf2-mediated antioxidant and detoxifying enzyme induction by the green tea polyphenol EGCG. Food and Chemical Toxicology 46: 1271-1278.Google Scholar
NAIR, S., BARVE, A., KHOR, T.O., SHEN, G.X., LIN, W., CHAN, J.Y., CAI, L. and KONG, A.N. (2010) Regulation of Nrf2- and AP-1-mediated gene expression by epigallocatechin-3-gallate and sulforaphane in prostate of Nrf2-knockout or C57BL/6J mice and PC-3 AP-1 human prostate cancer cells. Acta Pharmacologica Sinica 31: 1223-1240.Google Scholar
NAIR, S., LI, W. and KONG, A.N. (2007) Natural dietary anti-cancer chemopreventive compounds: redox-mediated differential signalling mechanisms in cytoprotection of normal cells versus cytotoxicity in tumour cells. Acta Pharmacologica Sinica 28: 459-472.Google Scholar
NELSON, D.E., IHEKWABA, A.E., ELLIOTT, M., JOHNSON, J.R., GIBNEY, C.A., FOREMAN, B.E., NELSON, G., SEE, V., HORTON, C.A., SPILLER, D.G., EDWARDS, S.W., MCDOWELL, HP., UNITT, J.F., SULLIVAN, E., GRIMLEY, R., BENSON, N., BROOMHEAD, D., KELL, D.B. and WHITE, M.R. (2004) Oscillations in NF-kappaB signalling control the dynamics of gene expression. Science 306: 704-708.Google Scholar
NGUYEN, T., NIOI, P. and PICKETT, C.B. (2009) The Nrf2-antioxidant response element signalling pathway and its activation by oxidative stress. The Journal of Biological Chemistry 284: 13291-13295.CrossRefGoogle ScholarPubMed
ORHAN, C., TUZCU, M., GENCOGLU, H., SAHIN, N. and SAHIN, K. (2012) Epigallocatechin-3-gallate inhibits activation of AP-1, COX-2 and heat shock proteins in liver of quail reared under heat stress (Unpublished).Google Scholar
SAHIN, K., ORHAN, C., AKDEMIR, F., TUZCU, M., IBEN, C. and SAHIN, N. (2012) Resveratrol protects quail hepatocytes against heat stress: modulation of the Nrf2 transcription factor and heat shock proteins. Journal of Animal Physiology and Animal Nutrition 96: 66-74.Google Scholar
SAHIN, K., ORHAN, C., TUZCU, M., ALI, S., SAHIN, N. and HAYIRLI, A. (2010) Epigallocatechin-3-gallate prevents lipid peroxidation and enhances antioxidant defense system via modulating hepatic nuclear transcription factors in heat-stressed quails. Poultry Science 89: 2251-2258.CrossRefGoogle ScholarPubMed
SAHIN, K., SAHIN, N., KUCUK, O., HAYIRLI, A. and PRASAD, A.S. (2009a) Role of dietary zinc in heat-stressed poultry: a review. Poultry Science 88: 2176-2183.Google Scholar
SAHIN, N., ORHAN, C., TUZCU, M., SAHIN, K. and KUCUK, O. (2008) The effects of tomato powder supplementation on performance and lipid peroxidation in quail. Poultry Science 87: 276-283.CrossRefGoogle ScholarPubMed
SAHIN, N., TUZCU, M., ORHAN, C., ONDERCI, M., EROKSUZ, Y. and SAHIN, K. (2009b) The effects of vitamin C and E supplementation on heat shock protein 70 response of ovary and brain in heat-stressed quail. British Poultry Science 50: 259-265.CrossRefGoogle Scholar
SAHIN, K. and KUCUK, O. (2003) Heat stress and dietary vitamin supplementation of poultry diets. Nutrition Abstracts and Reviews. Series B: Livestock Feeds and Feeding 73: 41-50.Google Scholar
SAHIN, K., ORHAN, C., AKDEMIR, F., TUZCU, T., ALI, S. and SAHIN, N. (2011) Tomato powder supplementation activates Nrf-2 via ERK/Akt signalling pathway and attenuates heat stress-related responses in quails. Animal Feed Science and Technology 65: 230-237.Google Scholar
SANDERCOCK, D.A., HUNTER, R.R., NUTE, G.R., MITCHELL, M.A. and HOCKING, P.M. (2001) Acute heat stress-induced alterations in blood acid-base status and skeletal muscle membrane integrity in broiler chickens at two ages: implications for meat quality. Poultry Science 80: 418-425.CrossRefGoogle ScholarPubMed
SEN, R. and BALTIMORE, D. (1986) Inducibility of kappa immunoglobulin enhancer-binding protein Nf-kappa B by a posttranslational mechanism. Cell 47: 921-928.Google Scholar
SHAULIAN, E. and KARIN, M. (2002) AP-1 as a regulator of cell life and death. Nature Cell Biology 4: 131-136.Google Scholar
SHEN, G., XU, C., HU, R., JAIN, M.R., GOPALKRISHNAN, A., NAIR, S., HUANG, M.T., CHAN, J.Y. and KONG, A.N. (2006) Modulation of nuclear factor E2-related factor 2-mediated gene expression in mice liver and small intestine by cancer chemopreventive agent curcumin. Molecular Cancer Therapeutics 5: 39-51.Google Scholar
SIEGEL, H.S. (1995) Stress, Strains and Resistance. British Poultry Science 36: 3-22.CrossRefGoogle ScholarPubMed
SINGH, S. and AGGARWAL, B.B. (1995) Activation of transcription factor NF-kappa B is suppressed by curcumin (diferuloylmethane) [corrected]. The Journal of Biological Chemistry 270: 24995-25000.CrossRefGoogle ScholarPubMed
SMITH, A.J. (1974) Changes in the average weight and shell thickness of eggs produced by hens exposed to high environmental temperatures. A review. Tropical Animal Health and Production 6: 237-244.Google Scholar
SUBBARAMAIAH, K., CHUNG, W.J., MICHALUART, P., TELANG, N., TANABE, T., INOUE, H., JANG, M., PEZZUTO, J.M. and DANNENBERG, A.J. (1998) Resveratrol inhibits cyclooxygenase-2 transcription and activity in phorbol ester-treated human mammary epithelial cells. The Journal of Biological Chemistry 273: 21875-21882.CrossRefGoogle ScholarPubMed
SURH, Y.J. and NA, H.K. (2008) NF-kappaB and Nrf2 as prime molecular targets for chemoprevention and cytoprotection with anti-inflammatory and antioxidant phytochemicals. Genes and Nutrition 2: 313-317.Google Scholar
THAXTON, P. and SIEGEL, H.S. (1970) Immunodepression in young chickens by high environmental temperature. Poultry Science 49: 202-205.Google Scholar
TREVISANATO, S.I. and KIM, Y.I. (2000) Tea and health. Nutrition Reviews 58: 1-10.Google Scholar
TUZCU, M., SAHIN, N., KARATEPE, M., CIKIM, G., KILINC, U. and SAHIN, K. (2008) Epigallocatechin-3-gallate supplementation can improve antioxidant status in stressed quail. British Poultry Science 49: 643-648.CrossRefGoogle ScholarPubMed
WILLIAMS, C.S., MANN, M. and DUBOIS, R.N. (1999) The role of cyclooxygenases in inflammation, cancer, and development. Oncogene 18: 7908-7916.Google Scholar
WOLFENSON, D., FERI, Y.F., SNAPIR, N. and BERMAN, A. (1979) Effect of diurnal or nocturnal heat stress on egg formation. British Poultry Science 20: 167-174.Google Scholar
YALCIN, S., OZKAN, , S, , TURKMUT, L. and SIEGEL, P.B. (2001) Responses to heat stress in commercial and local broiler stocks. 1. Performance traits. British Poultry Science 42: 149-152.Google Scholar
YAMAMOTO, T., SUZUKI, T., KOBAYASHI, A., WAKABAYASHI, J., MAHER, J., MOTOHASHI, H. and YAMAMOTO, M. (2008) Physiological significance of reactive cysteine residues of Keap1 in determining Nrf2 activity. Molecular and Cellular Biology 28: 2758-2770.CrossRefGoogle ScholarPubMed
YANG, F., OZ, H.S., BARVE, S., DE VILLIERS, W.J., MCCLAIN, C.J. and VARILEK, G.W. (2001) The green tea polyphenol ( )-epigallocatechin-3-gallate blocks nuclear factor-kappa B activation by inhibiting I kappa B kinase activity in the intestinal epithelial cell line IEC-6. Molecular Pharmacology 60: 528-533.Google Scholar
YU, R., CHEN, C., MO, Y.Y., HEBBAR, V., OWUOR, E.D., TAN, T.H. and KONG, A.N. (2000) Activation of mitogen-activated protein kinase pathways induces antioxidant response element-mediated gene expression via a Nrf2-dependent mechanism. The Journal of Biological Chemistry 275: 39907-39913.Google Scholar