Browse > Article
http://dx.doi.org/10.5713/ajas.18.0538

Potential crosstalk of oxidative stress and immune response in poultry through phytochemicals - A review  

Lee, M.T. (Department of Animal Science, National Chung Hsing University)
Lin, W.C. (Department of Animal Science, National Chung Hsing University)
Lee, T.T. (Department of Animal Science, National Chung Hsing University)
Publication Information
Asian-Australasian Journal of Animal Sciences / v.32, no.3, 2019 , pp. 309-319 More about this Journal
Abstract
Phytochemicals which exist in various plants and fungi are non-nutritive compounds that exert numerous beneficial bioactive actions for animals. In recent years following the restriction of antibiotics, phytochemicals have been regarded as a primal selection when dealing with the challenges during the producing process in the poultry industry. The selected fast-growing broiler breed was more fragile when confronting the stressors in their growing environments. The disruption of oxidative balance that impairs the production performance in birds may somehow be linked to the immune system since oxidative stress and inflammatory damage are multi-stage processes. This review firstly discusses the individual influence of oxidative stress and inflammation on the poultry industry. Next, studies related to the application of phytochemicals or botanical compounds with the significance of their antioxidant and immunomodulatory abilities are reviewed. Furthermore, we bring up nuclear factor (erythroid-derived 2)-like 2 (Nrf2) and nuclear factor kappa B ($NF-{\kappa}B$) for they are respectively the key transcription factors involved in oxidative stress and inflammation for elucidating the underlying signal transduction pathways. Finally, by the discussion about several reports using phytochemicals to regulate these transcription factors leading to the improvement of oxidative status, heme oxygenase-1 gene is found crucial for Nrf2-mediated $NF-{\kappa}B$ inhibition.
Keywords
Phytochemicals; Oxidative Stress; Immune Response; Poultry;
Citations & Related Records
Times Cited By KSCI : 4  (Citation Analysis)
연도 인용수 순위
1 Kamboh AA, Khan MA, Kaka U, et al. Effect of dietary supplementation of phytochemicals on immunity and haematology of growing broiler chickens. Ital J Anim Sci 2018;17:1038-43.   DOI
2 Lee MT, Lin WC, Yu B, Lee TT. Antioxidant capacity of phytochemicals and their potential effects on oxidative status in animals - A review. Asian-Australas J Anim Sci 2017;30:299-308.   DOI
3 Unekwu HR, Audu JA, Makun MH, Chidi EE. Phytochemical screening and antioxidant activity of methanolic extract of selected wild edible Nigerian mushrooms. Asian Pac J Trop Dis 2014;4(Suppl 1):S153-S7.   DOI
4 Jiang Z, Schatzmayr G, Mohnl M, Applegate TJ. Net effect of an acute phase response-Partial alleviation with probiotic supplementation. Poult Sci 2010;89:28-33.   DOI
5 Aziza A, Awadin W. Impact of dietary supplementation of whole flaxseed and flaxseed meal to infected broiler chickens with Eimeria tenella. Asian J Anim Vet Adv 2018;13:166-74.   DOI
6 Humphrey BD, Klasing KC. Modulation of nutrient metabolism and homeostasis by the immune system. World's Poult Sci J 2004;60:90-100.   DOI
7 Ahmed SM, Luo L, Namani A, Wang XJ, Tang X. Nrf2 signaling pathway: pivotal roles in inflammation. Biochim Biophys Acta Mol Basis Dis 2017;1863:585-97.   DOI
8 Ebrahimzadeh SK, Navidshad B, Farhoomandl P, Mirzaei Aghjehgheshlagh F. Effects of grape pomace and vitamin E on performance, antioxidant status, immune response, gut morphology and histopathological responses in broiler chickens. S Afr J Anim Sci 2018;48:324-36.   DOI
9 Cheng G, Zhao Y, Li Y, et al. Forsythiaside attenuates lipopolysaccharide- induced inflammatory responses in the bursa of Fabricius of chickens by downregulating the $NF-{\kappa}B$ signaling pathway. Exp Ther Med 2014;7:179-84.   DOI
10 Fontana AR, Antoniolli A, Bottini R. Grape pomace as a sustainable source of bioactive compounds: extraction, characterization, and biotechnological applications of phenolics. J Agric Food Chem 2013;61:8987-9003.   DOI
11 Iqbal Z, Kamran Z, Sultan JI, et al. Replacement effect of vitamin E with grape polyphenols on antioxidant status, immune, and organs histopathological responses in broilers from 1- to 35-d age. J Appl Poult Res 2015;24:127-34.   DOI
12 Brenes A, Viveros A, Goni I, et al. Effect of grape pomace concentrate and vitamin E on digestibility of polyphenols and antioxidant activity in chickens. Poult Sci 2008;87:307-16.   DOI
13 Valenzuela-Grijalva NV, Pinelli-Saavedra A, Muhlia-Almazan A, Dominguez-Diaz D, Gonzalez-Rios H. Dietary inclusion effects of phytochemicals as growth promoters in animal production. J Anim Sci Technol 2017;59:8.   DOI
14 Wandati TW, Kenji GM, Onguso JM. Phytochemicals in edible wild mushrooms from selected areas in Kenya. J Food Res 2013;2:137-44.   DOI
15 Barbieri R, Coppo E, Marchese A, et al. Phytochemicals for human disease: An update on plant-derived compounds antibacterial activity. Microbiol Res 2017;196:44-68.   DOI
16 Sahin K, Orhan C, Smith MO, Sahin N. Molecular targets of dietary phytochemicals for the alleviation of heat stress in poultry. Worlds Poult Sci J 2013;69:113-24.   DOI
17 Broom LJ, Kogut MH. Inflammation: friend or foe for animal production? Poult Sci 2018;97:510-4.   DOI
18 Surai PF. Antioxidant systems in poultry biology: superoxide dismutase. J Anim Res Nutr 2015;1:8.
19 Gessner DK, Ringseis R, Eder K. Potential of plant polyphenols to combat oxidative stress and inflammatory processes in farm animals. J Anim Physiol Anim Nutr 2017;101:605-28.   DOI
20 Huang CM, Lee TT. Immunomodulatory effects of phytogenics in chickens and pigs - a review. Asian-Australas J Anim Sci 2018;31:617-27.   DOI
21 Castellani P, Balza E, Rubartelli A. Inflammation, DAMPs, tumor development, and progression: a vicious circle orchestrated by redox signaling. Antioxid Redox Signal 2014;20:1086-97.   DOI
22 Rajput N, Naeem M, Ali S, et al. The effect of dietary supplementation with the natural carotenoids curcumin and lutein on broiler pigmentation and immunity. Poult Sci 2013;92:1177-85.   DOI
23 Li J, Lan T, Zhang C, et al. Reciprocal activation between IL-6/STAT3 and NOX4/Akt signalings promotes proliferation and survival of non-small cell lung cancer cells. Oncotarget 2015;6:1031-48.   DOI
24 Mittal M, Siddiqui MR, Tran K, Reddy SP, Malik AB. Reactive oxygen species in inflammation and tissue injury. Antioxid Redox Signal 2014;20:1126-67.   DOI
25 Yarru LP, Settivari RS, Gowda NK, et al. Effects of turmeric (Curcuma longa) on the expression of hepatic genes associated with biotransformation, antioxidant, and immune systems in broiler chicks fed aflatoxin. Poult Sci 2009;88:2620-7.   DOI
26 Gowda NKS, Ledoux DR, Rottinghaus GE, Bermudez AJ, Chen YC. Antioxidant efficacy of curcuminoids from turmeric (Curcuma longa L.) powder in broiler chickens fed diets containing aflatoxin B1. Br J Nutr 2009;102:1629-34.   DOI
27 Gowda NKS, Ledoux DR, Rottinghaus GE, Bermudez AJ, Chen YC. Efficacy of Turmeric (Curcuma longa), containing a known level of curcumin, and a hydrated sodium calcium aluminosilicate to ameliorate the adverse effects of aflatoxin in broiler chicks. Poult Sci 2008;87:1125-30.   DOI
28 Ribeiro B, Valentao P, Baptista P, Seabra RM, Andrade PB. Phenolic compounds, organic acids profiles and antioxidative properties of beefsteak fungus (Fistulina hepatica). Food Chem Toxicol 2007;45:1805-13.   DOI
29 Kozarski M, Klaus A, Jakovljevic D, et al. Antioxidants of edible mushrooms. Molecules 2015;20:19489-525.   DOI
30 Yang JH, Lin HC, Mau JL. Antioxidant properties of several commercial mushrooms. Food Chem 2002;77:229-35.   DOI
31 Valentao, P, Lopes G, Valente M, et al. Quantitation of nine organic acids in wild mushrooms. J Agric Food Chem 2005;53:3626-30.   DOI
32 Yildiz O, Can Z, Laghari AQ, Sahin H, Malkoc M. Wild edible mushrooms as a natural source of phenolics and antioxidants. J Food Chem 2015;39:148-54.
33 Haddad JJ. Science review: Redox and oxygen-sensitive transcription factors in the regulation of oxidant-mediated lung injury: role for nuclear $factor-{\kappa}B$. Crit Care 2002;6:481-90.   DOI
34 Aggarwal BB, Shishodia S. Molecular targets of dietary agents for prevention and therapy of cancer. Biochem Pharmacol 2006;71:1397-421.   DOI
35 Gupta SC, Sundaram C, Reuter S, Aggarwal BB. Inhibiting $NF-{\kappa}B$ activation by small molecules as a therapeutic strategy. Biochim Biophys Acta 2010;1799:775-87.   DOI
36 Wu Y, Lu J, Antony S, et al. Activation of TLR4 is required for the synergistic induction of dual oxidase 2 and dual oxidase A2 by IFN-${\gamma}$ and lipopolysaccharide in human pancreatic cancer cell lines. J Immunol 2013;190:1859-72.   DOI
37 Calabrese V, Cornelius C, Mancuso C, et al. Cellular stress response: A novel target for chemoprevention and nutritional neuroprotection in aging, neurodegenerative disorders and longevity. Neurochem Res 2008;33:2444-71.   DOI
38 Latchman DS. Transcription factors: an overview. Int J Biochem Cell Biol 1997;29:1305-12.   DOI
39 Lee MT, Lin WC, Wang SY, et al. Evaluation of potential antioxidant and anti-inflammatory effects of Antrodia cinnamomea powder and the underlying molecular mechanisms via Nrf2-and $NF-{\kappa}B$-dominated pathways in broiler chickens. Poult Sci 2018;97:2419-34.   DOI
40 Selye H. A syndrome produced by diverse nocuous agents. Nature 1936;138:32.   DOI
41 Li Y, Ma QG, Zhao LH, et al. Protective efficacy of ${\alpha}$-lipoic acid against aflatoxinB1-induced oxidative damage in the liver. Asian-Australas J Anim Sci 2014;27:907-15.   DOI
42 Sahin K, Orhan C, Akdemir F, et al. Resveratrol protects quail hepatocytes against heat stress: modulation of the Nrf2 transcription factor and heat shock proteins. J Anim Physiol Anim Nutr 2012;96:66-74.   DOI
43 Sahin K, Orhan C, Tuzcu Z, Tuzcu M, Sahin N. Curcumin ameloriates heat stress via inhibition of oxidative stress and modulation of Nrf2/HO-1 pathway in quail. Food Chem Toxicol 2012;50:4035-41.   DOI
44 Fialkow L, Wang Y, Downey GP. Reactive oxygen and nitrogen species as signaling molecules regulating neutrophil function. Free Radic Biol Med 2007;42:153-64.   DOI
45 Ali S, Mann DA. Signal transduction via the NF-kappaB pathway: a targeted treatment modality for infection, inflammation and repair. Cell Biochem Funct 2004;22:67-79.   DOI
46 Sahin N, Tuzcu M, Orhan C, et al. The effects of vitamin C and E supplementation on heat shock protein 70 response of ovary and brain in heat-stressed quail. Br Poult Sci 2009;50:259-65.   DOI
47 Sahin K, Orhan C, Akdemir F, et al. Tomato powder supplementation activates Nrf-2 via ERK/Akt signaling pathway and attenuates heat stress-related responses in quails. Anim Feed Sci Technol 2011;165:230-7.   DOI
48 Mruk DD, Silvestrini B, Mo MY, Cheng CY. Antioxidant superoxide dismutase - a review: its function, regulation in the testis, and role in male fertility. Contraception 2002;65:305-11.   DOI
49 Koolhaas JM, Bartolomucci A, Buwalda B, et al. Stress revisited: A critical evaluation of the stress concept. Neurosci Biobehav Rev 2011;35:1291-301.   DOI
50 Surai PF, Fisinin VI. Vitagenes in poultry production: Part 3. Vitagene concept development. World's Poult Sci J 2016;72:793-804.   DOI
51 Vargas-Sancheza RD, Torrescano-Urrutiab GR, Ibarra-Ariasc FJ, et al. Effect of dietary supplementation with Pleurotus ostreatus on growth performance and meat quality of Japanese quail. Livest Sci 2018;207:117-25.   DOI
52 Lee TT, Ciou JY, Chiang CJ, Chao YP, Yu B. Effect of Pleurotus eryngii stalk residue on the oxidative status and meat quality of broiler chickens. J Agric Food Chem 2012;60:11157-63.   DOI
53 Li S, Shah NP. Effects of various heat treatments on phenolic profiles and antioxidant activities of Pleurotus eryngii extracts. J Food Sci 2013;78:1122-9.   DOI
54 Zhang A, Li X, Xing C, Yang J, Sun P. Antioxidant activity of polysaccharide extracted from Pleurotus eryngii using response surface methodology. Int J Biol Macromol 2014;65:28-32.   DOI
55 Chen J, Mao D, Yong Y, et al. Hepatoprotective and hypolipidemic effects of water-soluble polysaccharidic extract of Pleurotus eryngii. Food Chem 2012;130:687-94.   DOI
56 Jeong YT, Jeong SC, Gu YA, Islam R, Song CH. Antitumor and immunomodulating activities of endo-biopolymers otained from a submerged culture of Pleurotus eryngii. Food Sci Biotechnol 2010;19:399-404.   DOI
57 Guo FC, Kwakkel RP, Williams BA, et al. Effects of mushroom and herb polysaccharides on cellular and humoral immune responses of Eimeria tenella infected chickens. Poult Sci 2004;83:1124-32.   DOI
58 Piao XL, Jang MH, Cui J, Piao X. Lignans from the fruits of Forsythia suspensa. Bioorg Med Chem Lett 2008;18:1980-4.   DOI
59 Li X, Jiao LL, Zhang X, et al. Anti-tumor and immunomodulating activities of proteoglycans from mycelium of Phellinus nigricans and culture medium. Int Immunopharmacol 2008;8:909-15.   DOI
60 Ullah MI, Akhtar M, Iqbal Z, Muhammad F. Immunotherapeutic activities of mushroom derived polysaccharides in chicken. Int J Agric Biol 2014;16:269-76.
61 Zhang HY, Piao XS, Zhang Q, et al. The effects of Forsythia suspensa extract and berberine on growth performance, immunity, antioxidant activities, and intestinal microbiota in broilers under high stocking density. Poult Sci 2013;92:1981-8.   DOI
62 Zhang ZW, Wang QH, Zhang JL, et al. Effects of oxidative stress on immunosuppresion induced by selenium deficiency in chickens. Biol Trace Elem Res 2012;149:352-61.   DOI
63 Ben-Dor A, Steiner M, Gheber L, et al. Carotenoids activate the antioxidant response element transcription system. Mol Cancer Ther 2005;4:177-86.
64 Deeb N, Cahaner A. Genotype-by-environment interaction with broiler genotypes differing in growth rate. 3. Growth rate and water consumption of broiler progeny from weight-selected versus nonselected parents under normal and high ambient temperatures. Poult Sci 2002;81:293-301.   DOI
65 Lara LJ, Rostagno MH. Impact of heat stress on poultry production. Animals (Basel) 2013;3:356-69.   DOI
66 Yahav S, Straschnow A, Luger D, et al. Ventilation, sensible heat loss, broiler energy, and water balance under harsh environmental conditions. Poult Sci 2004;83:253-8.   DOI
67 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
68 Nguyen T, Nioi P, Pickett CB. The Nrf2-antioxidant response element signaling pathway and its activation by oxidative stress. J Biol Chem 2009;284:13291-5.   DOI
69 Cheng G, Zhao Y, Li H, et al. Forsythiaside attenuates lipopolysaccharide-induced inflammatory responses in the bursa of Fabricius of chickens by downregulating the $NF-{\kappa}B$ signaling pathway. Exp Ther Med 2014;7:179-84.   DOI
70 Lee JM, Johnson JA. An important role of Nrf2-ARE pathway in the cellular defense mechanism. J Biochem Mol Biol 2004;37:139-43.
71 Cardozo LF, Pedruzzi LM, Stenvinkel P, et al. Nutritional strategies to modulate inflammation and oxidative stress pathways via activation of the master antioxidant switch Nrf2. Biochimie 2013;95:1525-33.   DOI
72 Jin W, Wang H, Yan W, et al. Disruption of Nrf2 enhances upregulation of nuclear factor-kappaB activity, proinflammatory cytokines, and intercellular adhesion molecule-1 in the brain after traumatic brain injury. Mediators Inflamm 2008;2008:725174.   DOI
73 Jung KA, Kwak MK. The Nrf2 system as a potential target for the development of indirect antioxidants. Molecules 2010;15:7266-91.   DOI
74 Oeckinghaus A, Hayden MS, Ghosh S. Crosstalk in $NF-{\kappa}B$ signaling pathways. Nat Immunol 2011;12:695-708.   DOI
75 Gilmore TD. Introduction to NF-kappaB: players, pathways, perspectives. Oncogene 2006;25:6680-4.   DOI
76 Grigorieva MA, Belichko OA, Shabaldin SV, Fisinin VI, Surai PF. Vitagene regulation as a new strategy to fight stresses in poultry production. Agric Biol 2017;52:716-30.
77 Farombi EO, YShrotriya S, Na HK, Kim SH, Surh YJ. Curcumin attenuates dimethylnitrosamine-induced liver injury in rats through Nrf2-mediated induction of heme oxygenase-1. Food Chem Toxicol 2008;46:1279-87.   DOI
78 Rubiolo JA, Mithieux G, Vega FV. Resveratrol protects primary rat hepatocytes against oxidative stress damage: activation of the Nrf2 transcription factor and augmented activities of antioxidant enzymes. Eur J Pharmacol 2008;591:66-72.   DOI
79 Sankar P, Telang AG, Manimaran A. Protective effect of curcumin on cypermethrin-induced oxidative stress in Wistar rats. Exp Toxicol Pathol 2012;64:487-93.   DOI
80 Wardyn JD, Ponsford AH, Sanderson CM. Dissecting molecular cross-talk between Nrf2 and $NF-{\kappa}B$ response pathways. Biochem Soc Trans 2015;43:621-6.   DOI
81 de Jonge J, van Trijp HC. The impact of broiler production system practices on consumer perceptions of animal welfare. Poult Sci 2013;92:3080-95.   DOI
82 Lee Y, Lee S, Gadde UD, Oh S, Lillehoj HS. Relievable effect of dietary Allium hookeri on LPS induced intestinal inflammation response in young broiler chickens. J Immunol 2017;198:(1 Supplement)226.3.
83 Nie CX, Zhang WJ, Wang YG, et al. Tissue lipid metabolism and hepatic metabolomic profiling in response to supplementation of fermented cottonseed meal in the diets of broiler chickens. J Zhejiang Univ Sci B 2015;16:447-55.   DOI
84 Sihvo HK, Immonen K, Puolanne E. Myodegeneration with fibrosis and regeneration in the pectoralis major muscle of broilers. Vet Pathol 2014;51:619-23.   DOI
85 Hou DX, Luo D, Tanigawa S, et al. Prodelphinidin B-4 3'-Ogallate, a tea polyphenol, is involved in the inhibition of COX-2 and iNOS via the downregulation of TAK1-$NF-{\kappa}B$ pathway. Biochem Pharmacol 2007;74:742-51.   DOI
86 Zhang B, Yan L, Li Q, et al. Dynamic succession of substrateassociated bacterial composition and function during Ganoderma lucidum growth. Peer J 2018;6:e4975.   DOI
87 Fard SH, Toghyani M, Tabeidian SA. Effect of oyster mushroom wastes on performance, immune responses and intestinal morphology of broiler chickens. Int J Recycl Org Waste Agric 2014;3:141-6.   DOI
88 Gill BS, Navgeet, Kumar S. Ganoderma lucidum targeting lung cancer signaling: a review. Tumor Biol 2017;39:1010428317707437.
89 Huang S, Mao J, Ding K, et al. Polysaccharides from Ganoderma lucidum promote cognitive function and neutral progenitor proliferation in mouse model of Alzheimer's disease. Stem Cell Reports 2017;8:84-94.   DOI
90 Liu T, Ma Q, Zhao L, et al. Protective effects of sporoderm-broken spores of Ganderma lucidum on growth performance, antioxidant capacity and immune function of broiler chickens exposed to low level of Aflatoxin B1. Toxins (Basel) 2016;8:278.   DOI
91 Pan L, Zhao PF, Ma XK, et al. Forsythia suspensa extract protects broilers against breast muscle oxidative injury induced by corticosterone mimicked pre-slaughter acute stress. Poult Sci 2018;97:2095-105.   DOI
92 AL-Zuhariy MTB, Hassan WH. Hepatoprotective and immunostimulatory effect of Ganoderma, Andrographolide and Turmeric against Aflatoxicosis in broiler chickens. Int J Poult Sci 2017;16:281-7.   DOI
93 Wang L, Piao XL, Kim SW, et al. Effects of Forsythia suspensa extract on growth performance, nutrient digestibility, and antioxidant activities in broiler chickens under high ambient temperature. Poult Sci 2008;87:1287-94.   DOI
94 Zeng ZK, Li QY, Piao XS, et al. Forsythia suspensa extract attenuates corticosterone-induced growth inhibition, oxidative injury, and immune depression in broilers. Poult Sci 2014;93:1774-81.   DOI