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Modulation of NF-κB and Nrf2 pathways by lycopene supplementation in heat-stressed poultry

Published online by Cambridge University Press:  03 June 2015

K. SAHIN
K. SAHIN*
Affiliation:
Department of Animal Nutrition, Faculty of Veterinary Science, Firat University, Elazig, Turkey
*
Corresponding author: [email protected]
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Abstract

Heat stress is characterised by reduced antioxidant status, and is one of the physiological alterations in response to exposure to higher temperatures in birds, which results in increased oxidative stress and immune suppression. The transcription entity nuclear factor-kappa light chain enhancer of B cells (NF-κB) controls the expression of genes involved in a number of physiological responses, including immune inflammatory responses, acute-phase inflammatory responses, oxidative stress responses, cell adhesion, differentiation, and apoptosis. The nuclear factor-2 erythroid related factor-2 (Nrf2), the redox-sensitive transcription factor, plays a key role in regulating induction of phase II detoxifying or antioxidant enzymes. Thus, activation of Nrf2 is considered to be an important molecular target of many anti-stressor agents. However, during heat stress conditions this regulation is disturbed offering an opportunity for therapeutic intervention. Heat stress is a condition in which the expression pattern of NF-κB and Nrf2 changes. To reduce the negative effects of heat, antioxidants are used in poultry diets for their anti-stress effects, associated with improved nutrient utilisation. For instance, lycopene, a powerful antioxidant, is particularly important because of its ability to quench reactive oxygen. This review focuses on the role of the NF-κB and Nrf2 in heat stress condition and summarises the therapeutic outcomes of lycopene in feed, targeted at the NF-κB and Nrf2 pathways in heat-stressed poultry.

Keywords

heat stresslycopeneNF-κBNrf2poultry
Type
Reviews
Information
World's Poultry Science Journal , Volume 71 , Issue 2 , June 2015 , pp. 271 - 284
Copyright
Copyright © World's Poultry Science Association 2015 

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References

AGGARWAL, B.B. (2004) Nuclear factor-kappaB: the enemy within. Cancer Cell 6: 203-208.CrossRefGoogle Scholar
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
AGARWAL, S. and RAO, A.V. (2000) Carotenoids and chronic diseases. Drug Metabolism and Drug Interactions 17: 189-210.CrossRefGoogle ScholarPubMed
AKDEMIR, F., ORHAN, C., SAHIN, N., SAHIN, K. and HAYIRLI, A. (2012) Tomato powder in laying hen diets: effects on concentrations of yolk carotenoids and lipid peroxidation. British Poultry Science 53: 675-680.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
CHEN, X.L., DODD, G., THOMAS, S., ZHANG, X., WASSERMAN, M.A., ROVIN, B.H. and KUNSCH, C. (2006) Activation of Nrf2/ARE pathway protects endothelial cells from oxidant injury and inhibits inflammatory gene expression. American Journal of Physiology-Heart and Circulatory Physiology 290: H1862-H1870 DOI: 10.1152/ajpheart.00651.CrossRefGoogle Scholar
CHEN, L., FISCHLE, W., VERDIN, E. and GREENE, W.C. (2001) Duration of nuclear NF-kappaB action regulated by reversible acetylation. Science 293: 1653-1657.CrossRefGoogle Scholar
DEJARDIN, E. (2006) The alternative NF-kappaB pathway from biochemistry to biology: pitfalls and promises for future drug development. Biochemical Pharmacology 6: 1161-1179.CrossRefGoogle Scholar
DI MASCIO, P., KAISER, S. and SIES, H. (1989) Lycopene as the most efficient biological carotenoid singlet oxygen quencher. Archives of Biochemistry and Biophysics 274: 532-538.CrossRefGoogle ScholarPubMed
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
ENGLMAIEROVÁ, M., BUBANCOVÁ, I., VÍT, T. and SKŘIVAN, M. (2011) The effect of lycopene and vitamin E on growth performance, quality and oxidative stability of chicken leg meat. Czech Journal of Animal Science 56: 536-543.CrossRefGoogle Scholar
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
GESSNER, D.K., FIESEL, A., MOST, E., DINGES, J., WEN, G., RINGSEIS, R. and EDER, K. (2013) Supplementation of a grape seed and grape marc meal extract decreases activities of the oxidative stress-responsive transcription factors NF-κB and Nrf2 in the duodenal mucosa of pigs. Acta Veterinaria Scandinavica. 55: 18. doi: 10.1186/1751-0147-55-18.CrossRefGoogle Scholar
GILMORE, T.D. (2006) Introduction to NF-kappaB: players, pathways, perspectives. Oncogene 25: 6680-6684.CrossRefGoogle Scholar
GIOVANNUCCI, E. (2002) A review of epidemiologic studies of tomatoes, lycopene, and prostate cancer. Experimental Biology and Medicine (Maywood) 227: 852-859.CrossRefGoogle ScholarPubMed
GHOSH, S. and KARIN, M. (2002) Missing pieces in the NF-kappaB puzzle. Cell 109 (Suppl): S81-S96.CrossRefGoogle ScholarPubMed
GORALCZYK, R. and SILER, U. (2003) The role of lycopene in health and disease, in: FENWICK, R. (Ed) Phytochemicals in health and disease, pp. 285-309 (Dekker, New York, NY).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.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.CrossRefGoogle ScholarPubMed
HEBER, D. and LU, Q.Y. (2002) Overview of mechanisms of action of lycopene. Experimental Biology and Medicine (Maywood) 227: 920-923.CrossRefGoogle ScholarPubMed
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 ScholarPubMed
KARIN, M., YAMAMOTO, Y. and WANG, Q.M. (2004) The IKK NF-kappa B system: a treasure trove for drug development. Nature Reviews Drug Discovery 3: 17-26.CrossRefGoogle ScholarPubMed
KHACHIK, F., BEECHER, G.R. and SMITH, J.C. Jr (1995) Lutein, lycopene, and their oxidative metabolites in chemoprevention of cancer. Journal of Cellular Biochemistry- Supplement 22: 236-246.CrossRefGoogle ScholarPubMed
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
LATCHMAN, D.S. (1997) Transcription factors: an overview. The International Journal of Biochemistry & Cell Biology 29: 1305-1312.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.CrossRefGoogle ScholarPubMed
LI, W., KHOR, T.O., XU, C., SHEN, G., JEONG, W.S., YU, S. and KONG, A.N. (2008) Activation of Nrf2-antioxidant signalling attenuates NF-kappaB-inflammatory response and elicits apoptosis, Biochemical Pharmacology 76: 1485-1489.CrossRefGoogle Scholar
LIU, G.H., QU, J. and SHEN, X. (2008) NF-kappaB/p65 antagonizes Nrf2-ARE pathway by depriving CBP from Nrf2 and facilitating recruitment of HDAC3 to MafK. Biochimica Biophysica Acta 1783: 713-727.CrossRefGoogle ScholarPubMed
LIU, L.L., HE, J.H., XIE, H.B., YANG, Y.S., LI, J.C. and ZOU, Y. (2014) Resveratrol induces antioxidant and heat shock protein mRNA expression in response to heat stress in black-boned chickens. Poultry Science 93: 54-62.CrossRefGoogle ScholarPubMed
LU, R., DAN, H., WU, R., MENG, W., LIU, N., JIN, X., ZHOU, M., ZENG, X., ZHOU, G. and CHEN, Q. (2011) Lycopene: features and potential significance in the oral cancer and precancerous lesions. Journal of Oral Pathology & Medicine 40: 361-368.CrossRefGoogle ScholarPubMed
MAGER, W.H. and DE KRUIJFF, A.J. (1995) Stress-induced transcriptional activation. Microbiological Reviews 59: 506-531.CrossRefGoogle ScholarPubMed
MANGELS, A.R., HOLDEN, J.M., BEECHER, G.R., FORMAN, M.R. and LANZA, E. (1993) Carotenoid contents of fruits and vegetables: an evaluation of analytical data. Journal of the American Dietetic Association 93: 284-296.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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 tumor cells. Acta Pharmacologica Sinica 28: 459-472.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
OLSON, J.A. and KRINSKY, N.I. (1995) Introduction: the colorful, fascinating world of the carotenoids: important physiologic modulators. FASEB Journal 9: 1547-1550.CrossRefGoogle ScholarPubMed
ORHAN, C., TUZCU, M., GENCOGLU, H., SAHIN, N., HAYIRLI, A. and SAHIN, K. (2013) Epigallocatechin-3-gallate exerts protective effects against heat stress through modulating stress-responsive transcription factors in poultry. British Poultry Science 54: 447-53.CrossRefGoogle ScholarPubMed
PAHL, H.L. (1999) Activators and target genes of Rel/NF-kappaB transcription factors. Oncogene, 18: 6853-6866.CrossRefGoogle ScholarPubMed
PALOZZA, P., CATALANO, A., SIMONE, R.E., MELE, M.C. and CITTADINI, A. (2012) Effect of lycopene and tomato products on cholesterol metabolism. Annals of Nutrition & Metabolism 61: 126-34.CrossRefGoogle ScholarPubMed
RAO, A.V. and AGARWAL, S. (1999) Role of lycopene as antioxidant carotenoid in the prevention of chronic diseases: A review. Nutrition Research 19: 305-323.CrossRefGoogle Scholar
SAHIN, K., ORHAN, C., SMITH, M.O. and SAHIN, K. (2013a) Molecular targets of dietary phytochemicals for the alleviation of heat stress in poultry World's Poultry Science Journal 69: 113-123.CrossRefGoogle Scholar
SAHIN, K., ORHAN, C., TUZCU, M. and SAHIN, N. (2013b) The Effects of lycopene on the meat lycopene levels, antioxidant enzymes and Nrf2 pathway in broiler chickens. 2nd International Poultry Meat Congress. 24-28 April 2013 Antalya, Turkey.Google Scholar
SAHIN, K., ORHAN, C., TUZCU, Z., TUZCU, M. and SAHIN, N. (2012a) Curcumin ameloriates heat stress via inhibition of oxidative stress and modulation of Nrf2/HO-1 pathway in quail. Food Chemical Toxicology 50: 4035-4041.CrossRefGoogle ScholarPubMed
SAHIN, K., ORHAN, C., AKDEMIR, F., TUZCU, M., IBEN, C. and SAHIN, N. (2012b) 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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle 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. (2009) Role of dietary zinc in heat-stressed poultry: a review. Poultry Science 88: 2176-2183.CrossRefGoogle ScholarPubMed
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, K., ONDERCI, M., SAHIN, N., GURSU, M.F. and KUCUK, O. (2006) Effects of lycopene supplementation on antioxidant status, oxidative stress, performance and carcass characteristics in heat-stressed Japanese quail. Journal of Thermal Biology 31: 307-312.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
ŠEVČÍKOVÁ, S., SKŘIVAN, M. and DLOUHÁ, G. (2008) The effect of lycopene supplementation on lipid profile and meat quality of broiler chickens. Czech Journal Animal Science 53: 431-440.CrossRefGoogle Scholar
SEN, R. and BALTIMORE, D. (1986) Inducibility of kappa immunoglobulin enhancer-binding protein Nf-kappa B by a posttranslational mechanism. Cell 47: 921-928.CrossRefGoogle ScholarPubMed
SETHI, G., SUNG, B. and AGGARWAL, B.B. (2008) Nuclear factor-kappaB activation: from bench to bedside. Experimental Biology Medicine (Maywood) 233: 21-31.CrossRefGoogle ScholarPubMed
SOARES, M.P., SELDON, M.P., GREGOIRE, I.P., VASSILEVSKAIA, T., BERBERAT, P.O., YU, J., TSUI, T.Y. and BACH, F.H. (2004) Haemoxygenase-1modulates the expression of adhesion molecules associated with endothelial cell activation, Journal of Immunology 172: 3553-3563.CrossRefGoogle ScholarPubMed
TANAKA, T., SHINIMIZU, M. and MORIWAKI, H. (2012) Cancer chemoprevention by carotenoids. Molecules 17: 3202-3242.CrossRefGoogle ScholarPubMed
WANG, D., WESTERHEIDE, S.D., HANSON, J.L. and BALDWIN, A.S. Jr (2000) Tumor necrosis factor alpha-induced phosphorylation of RelA/p65 on Ser529 is controlled by casein kinase II. Journal of Biological Chemistry 275: 32592-32597.CrossRefGoogle ScholarPubMed
VAN BREEMEN, R.B. and PAJKOVIC, N. (2008) Multitargeted therapy of cancer by lycopene. Cancer Letter 269: 339-351.CrossRefGoogle ScholarPubMed
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, J., FAN, G.H., WADZINSKI, B.E., SAKURAI, H. and RICHMOND, A. (2001) Protein phosphatase 2A interacts with and directly dephosphorylates RelA. Journal of Biological Chemistry 276: 47828-47833.CrossRefGoogle ScholarPubMed
YANG, X.D., HUANG, B., LI, M., LAMB, A., KELLEHER, N.L. and CHEN, L.F. (2009) Negative regulation of NF-kappaB action by Set9-mediated lysine methylation of the RelA subunit. EMBO Journal 28: 1055-1066.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
YU, M., LI, H., LIU, Q., LIU, F., TANG, L., LI, C., YUAN, Y., ZHAN, Y. XU, , W., LI, W., CHEN, H., GE, C., WANG, J. and YANG, X. (2011) Nuclear factor p65 interacts with Keap1 to repress the Nrf2-ARE pathway. Cell Signaling 23: 883-892.CrossRefGoogle ScholarPubMed