Hostname: page-component-8448b6f56d-m8qmq Total loading time: 0 Render date: 2024-04-19T05:15:21.725Z Has data issue: false hasContentIssue false
  • English
  • Français

Dietary supplementation of pyrroloquinoline quinone disodium protects against oxidative stress and liver damage in laying hens fed an oxidized sunflower oil-added diet

Published online by Cambridge University Press:  03 February 2016

J. Wang ,
H. J. Zhang ,
L. Xu ,
C. Long ,
K. G. Samuel ,
H. Y. Yue ,
L. L. Sun ,
S. G. Wu  and
G. H. Qi
J. Wang
Affiliation:
Key Laboratory of Feed Biotechnology of Ministry of Agriculture, Feed Research Institute, Chinese Academy of Agricultural Sciences, Beijing 100081, China
H. J. Zhang
Affiliation:
Key Laboratory of Feed Biotechnology of Ministry of Agriculture, Feed Research Institute, Chinese Academy of Agricultural Sciences, Beijing 100081, China
L. Xu
Affiliation:
Key Laboratory of Feed Biotechnology of Ministry of Agriculture, Feed Research Institute, Chinese Academy of Agricultural Sciences, Beijing 100081, China
C. Long
Affiliation:
Key Laboratory of Feed Biotechnology of Ministry of Agriculture, Feed Research Institute, Chinese Academy of Agricultural Sciences, Beijing 100081, China
K. G. Samuel
Affiliation:
Key Laboratory of Feed Biotechnology of Ministry of Agriculture, Feed Research Institute, Chinese Academy of Agricultural Sciences, Beijing 100081, China
H. Y. Yue
Affiliation:
Key Laboratory of Feed Biotechnology of Ministry of Agriculture, Feed Research Institute, Chinese Academy of Agricultural Sciences, Beijing 100081, China
L. L. Sun
Affiliation:
Shanghai Medical Life Science Research Center Co. Ltd., Shanghai 200032, China
S. G. Wu*
Affiliation:
Key Laboratory of Feed Biotechnology of Ministry of Agriculture, Feed Research Institute, Chinese Academy of Agricultural Sciences, Beijing 100081, China
G. H. Qi*
Affiliation:
Key Laboratory of Feed Biotechnology of Ministry of Agriculture, Feed Research Institute, Chinese Academy of Agricultural Sciences, Beijing 100081, China
*
†E-mail: wushugeng@caas.cn or qiguanghai@caas.cn
†E-mail: wushugeng@caas.cn or qiguanghai@caas.cn
Get access

Abstract

The protective effects of dietary pyrroloquinoline quinone disodium (PQQ.Na2) supplementation against oxidized sunflower oil-induced oxidative stress and liver injury in laying hens were examined. Three hundred and sixty 53-week-old Hy-Line Gray laying hens were randomly allocated into one of the five dietary treatments. The treatments included: (1) a diet containing 2% fresh sunflower oil; (2) a diet containing 2% thermally oxidized sunflower oil; (3) an oxidized sunflower oil diet with 100 mg/kg of added vitamin E; (4) an oxidized sunflower oil diet with 0.08 mg/kg of PQQ.Na2; and (5) an oxidized sunflower oil diet with 0.12 mg/kg of PQQ.Na2. Birds fed the oxidized sunflower oil diet showed a lower feed intake compared to birds fed the fresh oil diet or oxidized oil diet supplemented with vitamin E (P=0.009). Exposure to oxidized sunflower oil increased plasma malondialdehyde (P<0.001), hepatic reactive oxygen species (P<0.05) and carbonyl group levels (P<0.001), but decreased plasma glutathione levels (P=0.006) in laying hens. These unfavorable changes induced by the oxidized sunflower oil diet were modulated by dietary vitamin E or PQQ.Na2 supplementation to levels comparable to the fresh oil group. Dietary supplementation with PQQ.Na2 or vitamin E increased the activities of total superoxide dismutase and glutathione peroxidase in plasma and the liver, when compared with the oxidized sunflower oil group (P<0.05). PQQ.Na2 or vitamin E diminished the oxidized sunflower oil diet induced elevation of liver weight (P=0.026), liver to BW ratio (P=0.001) and plasma activities of alanine aminotransferase (P=0.001) and aspartate aminotransferase (P<0.001) and maintained these indices at the similar levels to the fresh oil diet. Furthermore, oxidized sunflower oil increased hepatic DNA tail length (P<0.05) and tail moment (P<0.05) compared with the fresh oil group. Dietary supplementation of PQQ.Na2 or vitamin E decreased the oxidized oil diet induced DNA tail length and tail moment to the basal levels in fresh oil diet. These results indicate that PQQ.Na2 is a potential antioxidant and is as effective against oxidized oil-related liver injury in laying hens as vitamin E. The protective effects of PQQ.Na2 against liver damage induced by oxidized oil may be partially due to its role in the scavenging of free radicals, inhibiting of lipid peroxidation and enhancing of antioxidant defense systems.

Keywords

pyrroloquinoline quinone disodiumoxidized sunflower oiloxidative stressliver damagelaying hen
Type
Research Article
Information
animal , Volume 10 , Issue 7 , July 2016 , pp. 1129 - 1136
Copyright
© The Animal Consortium 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

a

These authors contributed equally to this study.

References

Bajpayee, M, Pandey, AK, Parmar, D, Mathur, N, Seth, PK and Dhawan, A 2005. Comet assay responses in human lymphocytes are not influenced by the menstrual cycle: a study in healthy Indian females. Mutation Research 565, 163–172.CrossRefGoogle Scholar
Bishop, A, Gallop, PM and Karnovsky, ML 1998. Pyrroloquinoline quinone: a novel vitamin? Nutrition Reviews 56, 287–293.Google Scholar
Chao, PM, Chao, CY, Lin, FJ and Huang, CJ 2001. Oxidized frying oil up-regulates hepatic acyl-CoA oxidase and cytochrome P450 4 A1 genes in rats and activates PPARα . The Journal of Nutrition 131, 3166–3174.CrossRefGoogle ScholarPubMed
Eder, K and Ringseis, H 2010. Health aspects of oxidized dietary fats. In Oxidation in foods and beverages and antioxidant applications (ed. E Decker, R Elias and DJ McClements), pp. 143–166. Woodhead Publishing Limited, Philadelphia, PA, USA.CrossRefGoogle Scholar
Engberg, RM, Lauridsen, C, Jensen, SK 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
Esterbauer, H 1993. Cytotoxicity and genotoxicity of lipid-oxidation products. The American Journal of Clinical Nutrition 57, 779S–785S.CrossRefGoogle ScholarPubMed
Fontagné-Dicharry, S, Lataillade, E, Surget, A, Larroquet, L, Cluzeaud, M and Kaushik, S 2014. Antioxidant defense system is altered by dietary oxidized lipid in first-feeding rainbow trout (Oncorhynchus mykiss). Aquaculture 424–425, 220–227.Google Scholar
ISO 1996. Animal and vegetable fats and oils-Determination of iodine value (ISO 3961:1996 (IDT.). International Organization for Standardization, Geneva, Switzerland.Google Scholar
ISO 2007. Animal and vegetable fats and oils-Determination of peroxide value-Iodometric (visual) endpoint determination (ISO 3960:2007 (IDT.). International Organization for Standarization, Geneva, Switzerland.Google Scholar
ISO 2009. Animal and vegetable fats and oils-Determination of acid value and acidity (ISO 660:2009 (IDT.). International Organization for Standardization, Geneva, Switzerland.Google Scholar
Hy-Line International 2011. Hy-Line International Online Management Guide: Management Guide for All Hy-Line Varieties of Laying Hens. Retrieved Feburary 22, 2012, from http://www.hyline.com/Redbook/New.html.Google Scholar
Końca, K, Lankoff, A, Banasik, A, Lisowska, H, Kuszewski, T, Góźdź, S, Koza, Z and Wojcik, A 2003. A cross-platform public domain PC image-analysis program for the comet assay. Mutation Research 534, 15–20.Google Scholar
Liu, P, Chen, C, Kerr, BJ, Weber, TE, Johnston, LJ and Shurson, GC 2014. Influence of thermally-oxidized vegetable oils and animal fats on growth performance, liver gene expression, and liver and serum cholesterol and triglycerides in young pigs. Journal of Animal Science 92, 2960–2970.CrossRefGoogle ScholarPubMed
López-Varela, S, Sánchez-Muniz, FJ and Cuesta, C 1995. Decreased food efficiency ratio, growth retardation and changes in liver fatty acid composition in rats consuming thermally oxidized and polymerized sunflower oil used for frying. Food and Chemical Toxicology 33, 181–189.CrossRefGoogle ScholarPubMed
Lu, T, Harper, AF, Zhao, J, Corl, BA, LeRoith, T and Dalloul, RA 2014a. Effects of a dietary antioxidant blend and vitamin E on fatty acid profile, liver function, and inflammatory response in broiler chickens fed a diet high in oxidants. Poultry Science 93, 1–9.Google ScholarPubMed
Lu, T, Harper, AF, Dibner, JJ, Scheffler, JM, Corl, BA, Estienne, MJ, Zhao, J and Dalloul, RA 2014b. Supplementing antioxidants to pigs fed diets high in oxidants: II. Effects on carcass characteristics, meat quality, and fatty acid profile. Journal of Animal Science 92, 5464–5475.Google Scholar
Misra, HS, Khairnar, NP, Barik, A, Priyadarsini, KI, Mohan, H and Apte, SK 2004. Pyrroloquinoline-quinone: a reactive oxygen species scavenger in bacteria. FEBS Letters 578, 26–30.Google Scholar
Ng, CY, Leong, XF, Masbah, N, Adam, SK, Kamisah, Y and Jaarin, K 2014. Heated vegetable oils and cardiovascular disease risk factors. Vascular Pharmacology 61, 1–9.Google Scholar
Noji, N, Nakamura, T, Kitahata, N, Taguchi, K, Kudo, T, Yoshida, S, Tsujimoto, M, Sugiyama, T and Asami, T 2007. Simple and sensitive method for pyrroloquinoline quinone (PQQ) analysis in various foods using liquid chromatography/electrospray-ionization tandem mass spectrometry. Journal of Agricultural and Food Chemistry 55, 7258–7263.Google Scholar
NRC 1994. Nutrient requirements of poultry, 9th revised edition. National Academy Press, Washington, DC, USA.Google Scholar
Rosero, DS, Odle, J, Moeser, AJ, Boyd, RD and van Heugten, E 2015. Peroxidised dietary lipids impair intestinal function and morphology of the small intestine villi of nursery pigs in a dose-dependent manner. British Journal of Nutrition 114, 1985–1992.Google Scholar
Rucker, R, Chowanadisai, W and Nakano, M 2009. Potential physiological importance of pyrroloquinoline quinone. Alternative Medicine Review 14, 268–277.Google ScholarPubMed
Samuel, KG, Zhang, HJ, Wang, J, Wu, SG, Yue, HY, Sun, LL and Qi, GH 2015. Effects of dietary pyrroloquinoline quinone disodium on growth performance, carcass yield and antioxidant status of broiler chicks. Animal 9, 409–416.CrossRefGoogle ScholarPubMed
Sheehy, PJA, Morrissey, PA and Flynn, A 1994. Consumption of thermally-oxidized sunflower oil by chicks reduces α-tocopherol status and increases susceptibility of tissues to lipid oxidation. British Journal of Nutrition 71, 53–65.Google Scholar
Smith, SA, King, RE and Min, DB 2007. Oxidative and thermal stabilities of genetically modified high oleic sunflower oil. Food Chemistry 102, 1208–1213.Google Scholar
Staprans, I, Rapp, JH, Pan, XM, Kim, KY and Feingold, KR 1994. Oxidized lipids in the diet are a source of oxidized lipid in chylomicrons of human serum. Arteriosclerosis, Thrombosis, and Vascular Biology 14, 1900–1905.Google Scholar
Takabayashi, F, Tahara, S, Kaneko, T and Harada, N 2004. Effect of green tea catechins on oxidative DNA damage of hamster pancreas and liver induced by N-nitrosobis (2-oxopropyl) amine and/or oxidized soybean oil. BioFactors 21, 335–337.Google Scholar
Tchaparian, E, Marshal, L, Cutler, G, Bauerly, K, Chowanadisai, W, Satre, M, Harris, C and Rucker, RB 2010. Identification of transcriptional networks responding to pyrroloquinoline quinone dietary supplementation and their influence on thioredoxin expression, and the JAK/STAT and MAPK pathways. Biochemical Journal 429, 515–526.Google Scholar
Tsuchida, T, Yasuyama, T, Higuchi, K, Watanabe, A, Urakami, T, Akaike, T, Sato, K and Maeda, H 1993. The protective effect of pyrroloquinoline quinone and its derivatives against carbon tetrachloride-induced liver injury of rats. Journal of Gastroenterology and Hepatology 8, 342–347.Google Scholar
Wang, J, Zhang, HJ, Samuel, KG, Long, C, Wu, SG, Yue, HY, Sun, LL and Qi, GH 2015. Effects of dietary pyrroloquinoline quinone disodium on growth, carcass characteristics, redox status, and mitochondria metabolism in broilers. Poultry Science 94, 215–225.Google Scholar
Xu, L 2011. Effects of dietary pyrroloquinoline quinone supplementation on performance and anti-oxidant ability of laying hens. MSc thesis, Chinese Academy of Agricultural Sciences, Beijing, China.Google Scholar
Yuan, Y, Chen, YJ, Liu, YJ, Yang, HJ, Liang, GY and Tian, LX 2014. Dietary high level of vitamin premix can eliminate oxidized fish oil-induced oxidative damage and loss of reducing capacity in juvenile largemouth bass (Micropterus salmoides). Aquaculture Nutrition 20, 109–117.Google Scholar
Yue, HY, Wang, J, Qi, XL, Ji, F, Liu, MF, Wu, SG, Zhang, HJ and Qi, GH 2011. Effects of dietary oxidized oil on laying performance, lipid metabolism, and apolipoprotein gene expression in laying hens. Poultry Science 90, 1728–1736.Google Scholar
Zhang, L, Yue, HY, Wu, SG, Xu, L, Zhang, HJ, Yan, HJ, Cao, YL, Gong, YS and Qi, GH 2010. Transport stress in broilers: ll. Superoxide production, adenosine phosphate concentrations, and mRNA levels of avian uncoupling protein, avian adenine nucleotide translocator, and avian peroxisome proliferator-activated receptor-γ coactivator-1α in skeletal muscles. Poultry Science 89, 393–400.Google Scholar
Zhang, P, Xu, YP, Sun, JX, Li, XY, Wang, LH and Jin, LJ 2009. Protection of pyrroloquinoline quinone against methylmercury-induced neurotoxicity via reducing oxidative stress. Free Radical Research 43, 224–233.Google Scholar
Zhang, Q, Ding, M, Cao, Z, Zhang, JJ, Ding, F and Ke, KF 2013. Pyrroloquinoline quinine protects rat brain cortex against acute glutamate-induced neurotoxicity. Neurochemical Research 38, 1661–1671.Google Scholar
Zhang, W, Xiao, S, Lee, EJ and Ahn, DU 2010. Consumption of oxidized oil increases oxidative stress in broilers and affects the quality of breast meat. Journal of Agricultural and Food Chemistry 59, 969–974.Google Scholar