Dietary lycopene alters the expression of antioxidant enzymes and modulates the blood lipid profile of pigs
Marcelise Regina Fachinello A B , Eliane Gasparino A , André Vinicius Sturzenegger Partyka A , Angélica de Souza Khatlab A , Leandro Dalcin Castilha A , Laura Marcela Diaz Huepa A , Leonardo Felipe Malavazi Ferreira A and Paulo Cesar Pozza AA Department of Animal Science, Universidade Estadual de Maringá – UEM, Maringá, Paraná 87020-900, Brazil.
B Corresponding author. Email: lise_faqui@hotmail.com
Animal Production Science 60(6) 806-814 https://doi.org/10.1071/AN18456
Submitted: 23 July 2018 Accepted: 30 June 2019 Published: 18 March 2020
Abstract
Lycopene has the highest antioxidant activity among carotenoids due to its high number of conjugated double bonds; thus, it can be used in pig diets to look for improvements in growth performance and health status, eliminating or preventing the formation of free radicals. Therefore, the aim of the present study was to investigate the effects of dietary lycopene on the growth performance, the gene expression of antioxidant enzymes and blood lipid profile of finishing pigs. In total, 40 barrows and 40 gilts (Piétrain × Landrace × Large White) were used, averaging 75.04 ± 1.6 kg of initial bodyweight. Pigs were distributed in a 2 × 5 factorial arrangement, consisting of two genders (male and female) and five dietary levels of lycopene (0, 12.5, 25.0, 37.5 and 50.0 mg/kg of diet) supplemented for 28 days. It was observed that gilts presented with average daily feed intake (P = 0.001) being lower and the gain : feed ratio (P = 0.001) higher than for barrows. Increasing dietary lycopene concentration provided a linear decrease in the gene expression of the enzymes superoxide dismutase (SOD1; P = 0.018) and catalase (P = 0.001) in the liver of gilts. The gilts showed a lower gene expression than did barrows for SOD1 gene (P = 0.001) receiving 50.0 mg lycopene/kg of diet and for catalase gene (P = 0.001) receiving of 0, 12.5 and 50.0 mg lycopene/kg of diet. Glutathione peroxidase showed a lower expression (P = 0.001) for gilts than for barrows. Total cholesterol, low-density lipoprotein (LDL) and LDL : high-density lipoprotein (HDL) ratio decreased (P = 0.001) as lycopene concentration increased in the diet. Increasing dietary lycopene in pig diets improved the lipid profile of the blood plasma, providing an increase in the concentration of high-density lipoprotein (HDL; P = 0.001). Gilts had greater plasma concentrations of urea (P = 0.001) and triglycerides (P = 0.001) and lower concentrations of HDL (P = 0.001), LDL (P = 0.001) and a lower LDL : HDL ratio (P = 0.004) than did barrows. Dietary lycopene up to 50 mg/kg does not affect the growth performance of pigs, acting as a potent modulator of the lipid profile and also reducing the plasma concentrations of total cholesterol and low-density lipoproteins, while increasing the high-density lipoproteins. In addition, lycopene also reduces the gene expression of superoxide dismutase and catalase enzymes in the liver of gilts.
Additional keywords: antioxidant, carotenoids, enzymes.
References
Agarwal NB, Argwal NK, Mediratta PK, Sharma KK (2011) Effect of lamotrigine, oxcarbazepine and topiramate on cognitive functions and oxidative stress in PTZ-kindled mice. Seizure 20, 257–262.| Effect of lamotrigine, oxcarbazepine and topiramate on cognitive functions and oxidative stress in PTZ-kindled mice.Crossref | GoogleScholarGoogle Scholar | 21247777PubMed |
Aguilera-Soto JI, Méndez-Llorente F, López-Carlos MA, Ramírez RG, Carrillo-Muro O, Escareño-Sánchez LM, Medina-Flores CA (2014) Effect of fermentable liquid diet based on tomato Silage on the performance of growing finishing pigs. Interciencia 39, 428–431.
Arab L, Steck S (2000) Lycopene and cardiovascular disease. American Journal of Clinical Nutrition 71, 1691S–1695S.
| Lycopene and cardiovascular disease.Crossref | GoogleScholarGoogle Scholar | 10837319PubMed |
Borras C, Sastre J, Garcia-Sala D, Lloret A, Pallardo FV, Vina J (2003) Mitochondria from females exhibit higher antioxidant gene expression and lower oxidative damage than males. Free Radical Biology & Medicine 34, 546–552.
| Mitochondria from females exhibit higher antioxidant gene expression and lower oxidative damage than males.Crossref | GoogleScholarGoogle Scholar |
Brown MS, Goldstein JL (1986) A receptor-mediated pathway for cholesterol homeostasis Science 232, 34–47.
| A receptor-mediated pathway for cholesterol homeostasisCrossref | GoogleScholarGoogle Scholar | 3513311PubMed |
Chung SH, Son AR, Le SA, Kim BG (2014) Effects of dietary tomato processing byproducts on pork nutrient composition and loin quality of pig. Asian Journal of Animal and Veterinary Advances 9, 775–781.
| Effects of dietary tomato processing byproducts on pork nutrient composition and loin quality of pig.Crossref | GoogleScholarGoogle Scholar |
Coble DJ, Redmond SB, Hale B, Lamont SJ (2011) Distinct lines of chickens express different splenic cytokine profiles in response to Salmonella enteritidis challenge. Poultry Science 90, 1659–1663.
| Distinct lines of chickens express different splenic cytokine profiles in response to Salmonella enteritidis challenge.Crossref | GoogleScholarGoogle Scholar | 21753200PubMed |
Correia CS, Alfaia CM, Madeira MS, Lopes PA, Matos TJ, Cunha LF, Prates JA, Freire JP (2017) Dietary inclusion of tomato pomace improves meat oxidative stability of young pigs. Journal of Animal Physiology and Animal Nutrition 101, 1215–1226.
Da Costa LA, Badawi A, El-Sohemy A (2012) Nutrigenetics and modulation of oxidative stress. Annals of Nutrition & Metabolism 60, 27–36.
Fuhrman B, Elis A, Aviram M (1997) Hypocholesterolemic effect of lycopene and beta-carotene is related to suppression of cholesterol synthesis and augmentation of LDL receptor activity in macrophages. Biochemical and Biophysical Research Communications 233, 658–662.
| Hypocholesterolemic effect of lycopene and beta-carotene is related to suppression of cholesterol synthesis and augmentation of LDL receptor activity in macrophages.Crossref | GoogleScholarGoogle Scholar | 9168909PubMed |
Gessner DK, Fiesel A, Most E, Dinges J, Wen G, Ringseis R, Eder K (2013) Supplementation of a grape seed and grape marc meal extract decreases activities of the oxidative stress-responsive transcription factors NF-kappaB and Nrf2 in the duodenal mucosa of pigs. Acta Veterinaria Scandinavica 55, 18
| Supplementation of a grape seed and grape marc meal extract decreases activities of the oxidative stress-responsive transcription factors NF-kappaB and Nrf2 in the duodenal mucosa of pigs.Crossref | GoogleScholarGoogle Scholar | 23453040PubMed |
Girao MP, Silva EMP, Melo MP (2012) Dietary lycopene supplementation on Nile tilapia (Oreochromis niloticus) juveniles submitted to confinement: effects on cortisol level and antioxidant response. Aquaculture Research 43, 789–798.
| Dietary lycopene supplementation on Nile tilapia (Oreochromis niloticus) juveniles submitted to confinement: effects on cortisol level and antioxidant response.Crossref | GoogleScholarGoogle Scholar |
Halliwell B, Gutteridge JMC (2015) ‘Free radicals in biology and medicine.’ 5th edn. (Oxford University Press: New York, NY, USA)
Hassan HA, Edrees GM (2004) Therapeutic effect of Lycopene-rich tomato juice on cardiac disorder in rats fed on fried food in oxidized frying oil. Resultados da pesquisa. Egyptian Journal of Hospital Medicine 14, 115–126.
Hu R, Saw CL, Yu R, Kong AN (2010) Regulation of Nrf2 signaling for cancer chemoprevention: antioxidant coupled with anti-inflammatory. Antioxidants & Redox Signalling 13, 1679–1698.
| Regulation of Nrf2 signaling for cancer chemoprevention: antioxidant coupled with anti-inflammatory.Crossref | GoogleScholarGoogle Scholar |
Huber PC, Almeida WP, Fátima A (2008) Glutationa e enzimas relacionadas: papel biológico e importância em processos patológicos. Quimica Nova 31, 1170–1179.
| Glutationa e enzimas relacionadas: papel biológico e importância em processos patológicos.Crossref | GoogleScholarGoogle Scholar |
Ivanov NI, Cowel SP, Brownb P, Renniea PS, Gunsa ES, Cox ME (2007) Lycopene differentially induces quiescence and apoptosis in androgenresponsive and independent prostate cancer cell line. Clinical Nutrition 26, 252–263.
| Lycopene differentially induces quiescence and apoptosis in androgenresponsive and independent prostate cancer cell line.Crossref | GoogleScholarGoogle Scholar | 17337101PubMed |
Kander MC, Cui Y, Liu Z (2017) Gender difference in oxidative stress: a new look at the mechanisms for cardiovascular diseases. Journal of Cellular and Molecular Medicine 21, 1024–1032.
| Gender difference in oxidative stress: a new look at the mechanisms for cardiovascular diseases.Crossref | GoogleScholarGoogle Scholar | 27957792PubMed |
Kobayashi M, Yamamoto M (2006) Nrf2–Keap1 regulation of cellular defense mechanisms against electrophiles and reactive oxygen species. Advances in Enzyme Regulation 46, 113–140.
| Nrf2–Keap1 regulation of cellular defense mechanisms against electrophiles and reactive oxygen species.Crossref | GoogleScholarGoogle Scholar | 16887173PubMed |
Kujawska M, Ewertowska M, Adamska T, Sadowski C, Ignatowicz E, Jodynis-Liebert J (2014) Antioxidant effect of lycopene-enriched tomato paste on N-nitrosodiethylamine-induced oxidative stress in rats. Journal of Physiology and Biochemistry 70, 981–990.
| Antioxidant effect of lycopene-enriched tomato paste on N-nitrosodiethylamine-induced oxidative stress in rats.Crossref | GoogleScholarGoogle Scholar | 25387411PubMed |
Lobo GP, Hessel S, Eichinger A, Noy N, Moise AR, Wyss A, Palczewski K, Von Lintig J (2010) ISX is a retinoic acid-sensitive gatekeeper that controls intestinal beta,beta-carotene absorption and vitamin A production. Federation of American Societies for Experimental Biology 24, 1656–1666.
| ISX is a retinoic acid-sensitive gatekeeper that controls intestinal beta,beta-carotene absorption and vitamin A production.Crossref | GoogleScholarGoogle Scholar |
Luo C, Wu XG (2011) Lycopene enhances antioxidant enzyme activities and immunity function in N-methyl-N′-nitro-N-nitrosoguanidine-induced gastric cancer rats. International Journal of Molecular Sciences 12, 3340–3351.
| Lycopene enhances antioxidant enzyme activities and immunity function in N-methyl-N′-nitro-N-nitrosoguanidine-induced gastric cancer rats.Crossref | GoogleScholarGoogle Scholar | 21686188PubMed |
Lykkesfeldt J, Svendsen O (2007) Oxidants and antioxidants in disease: oxidative stress in farm animals. Veterinary Journal 173, 502–511.
| Oxidants and antioxidants in disease: oxidative stress in farm animals.Crossref | GoogleScholarGoogle Scholar |
Millán J, Pintó X, Muñoz A, Zúñiga M, Rubiés-Prat J, Pallardo LF, Masana L, Mangas A, Hernández-Mijares A, González-Santos P, Ascaso JF, Pedro-Botet J (2009) Lipoprotein ratios: physiological significance and clinical usefulness in cardiovascular prevention. Vascular Health and Risk Management 5, 757–765.
Moreira EA, Fagundes RL, Filho DW, Neves D, Sell F, Bellisle F, Kupek E (2005) Effects of diet energy level and tomato powder consumption on antioxidant status in rats. Clinical Nutrition 24, 1038–1046.
| Effects of diet energy level and tomato powder consumption on antioxidant status in rats.Crossref | GoogleScholarGoogle Scholar | 16183173PubMed |
Moreno FS, Rossielo MR, Manjeshwar S, Nath R, Rao PM, Rajalakshimi S, Sarma DSR (1995) Effect of b-carotene on the expression of 3- hydroxi-3-methylglutaryl coenzyme A redutase in rat liver. Cancer Letters 96, 201–208.
| Effect of b-carotene on the expression of 3- hydroxi-3-methylglutaryl coenzyme A redutase in rat liver.Crossref | GoogleScholarGoogle Scholar | 7585458PubMed |
Mulkalwar SA, Munjal NS, More UK, More B, Chaudhari AB, Dewda PR (2012) Effect of purified lycopene on lipid profile, antioxidant enzyme and blood glucose in hyperlipidemic rabbits. American journal of PharmTech Research 2, 461–470.
National Research Council (NRC) (2012) ‘Nutrient requirements of swine.’ 11th edn. (National Academies Press: Washington, DC, USA)
Oliveira GCD, Moreira I, Furlan AC, Bastos AO, Fraga AL (2004) Efeito das dietas de baixo teor de proteína bruta, suplementadas com aminoácidos, para leitões machos castrados (15 a 30 kg). Revista Brasileira de Zootecnia 33, 1747–1757.
| Efeito das dietas de baixo teor de proteína bruta, suplementadas com aminoácidos, para leitões machos castrados (15 a 30 kg).Crossref | GoogleScholarGoogle Scholar |
Orok EJ, Bowland JP (1975) Rapeseed, peanut and soybean meals as protein supplements: plasma urea concentrations of pigs on different feed intakes as indices of dietary protein quality Canadian Journal of Animal Science 55, 347–351.
Pajk T, Rezar V, Levart A, Salobir J (2006) Efficiency of apples, strawberries, and tomatoes for reduction of oxidative stress in pigs as a model for humans. Nutrition 22, 376–384.
Palozza P, Catalano A, Simone RE, Mele MC, Cittadini A (2012) Effect of lycopene and tomato products on cholesterol metabolism. Annals of Nutrition & Metabolism 61, 126–134.
| Effect of lycopene and tomato products on cholesterol metabolism.Crossref | GoogleScholarGoogle Scholar |
Pandir D, Unal B, Bas H (2016) Lycopene protects the diabetic rat kidney against oxidative stress-mediated oxidative damage induced by furan. Brazilian Archives of Biology and Technology 59, 16150794
| Lycopene protects the diabetic rat kidney against oxidative stress-mediated oxidative damage induced by furan.Crossref | GoogleScholarGoogle Scholar |
Prakash A, Kumar A (2013) Lycopene protects against memory impairment and mito-oxidative damage induced by colchicine in rats: an evidence of nitric oxide signaling. European Journal of Pharmacology 721, 373–381.
| Lycopene protects against memory impairment and mito-oxidative damage induced by colchicine in rats: an evidence of nitric oxide signaling.Crossref | GoogleScholarGoogle Scholar | 24075937PubMed |
Riso P, Brusamolino A, Contino D, Martini D, Vendrame S, Bo CD, Porrin M (2010) Lycopene absorption in humans after the intake of two different single-dose lycopene formulations. Pharmacological Research 62, 318–321.
| Lycopene absorption in humans after the intake of two different single-dose lycopene formulations.Crossref | GoogleScholarGoogle Scholar | 20558293PubMed |
Rissanen T (2006) Lycopene and cardiovascular disease. In ‘Tomatoes lycopene and human health’. (Ed. AV Rao) pp. 141–152. (Caledonian Science Press: Stranraer, Scotland, UK)
Sahin K, Onderci MC, Sahin N (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.
| Effects of lycopene supplementation on antioxidant status,oxidative stress, performance and carcass characteristics in heat-stressed Japanese quail.Crossref | GoogleScholarGoogle Scholar |
Simone RE, Russo M, Catalano A, Monego G, Froehlich K, Boehm V, Palozza P (2011) Lycopene inhibits NF-kB-mediated IL-8 expression and changes redox and PPARγ signalling in cigarette smoke-stimulated macrophages. PLoS One 6, e19652
| Lycopene inhibits NF-kB-mediated IL-8 expression and changes redox and PPARγ signalling in cigarette smoke-stimulated macrophages.Crossref | GoogleScholarGoogle Scholar | 21625550PubMed |
Singh K, Bal BS, Chopra S, Singh S, Malhotra N (2012) Ameliorative effect of lycopene on lipid peroxidation and certain antioxidant enzymes in diabetic patients. Journal of Diabetes & Metabolism 3, 1000202
| Ameliorative effect of lycopene on lipid peroxidation and certain antioxidant enzymes in diabetic patients.Crossref | GoogleScholarGoogle Scholar |
Soucek P, Zuber R, Anzenbacherová E, Anzenbacher P, Guengreich FP (2001) Minipig cytochrome P450 3A, 2A and 2C enzymes have similar properties to human analogs. BMC Pharmacology 1, 11
| Minipig cytochrome P450 3A, 2A and 2C enzymes have similar properties to human analogs.Crossref | GoogleScholarGoogle Scholar | 11737866PubMed |
Taranu I, Habeanu M, Gras MA, Pistol GC, Lefter N, Palade M, Ropota M, Chedea VS, Marin DE (2017) Effect of xenobiotic compounds from grape waste on liver function and oxidattus in pigs. Archiva Zootechnica 20(2), 5–24.
Teoh-Fitzgerald ML, Domann FE (2012) Superoxide dismutase and cancer therapy. In ‘Oxidative stress in cancer. Biology and therapy’. (Eds DR Spitz, KJ Dornfeld, K Krishnan, D Gius) pp. 59–84. (Humana Press: New York, NY, USA)
Tiidus PM (2000) Estrogen and gender effects on muscle damage, inflammation, and oxidative stress. Canadian Journal of Applied Physiology 25, 274–287.
| Estrogen and gender effects on muscle damage, inflammation, and oxidative stress.Crossref | GoogleScholarGoogle Scholar | 10953066PubMed |
Upaganlawa AB, Balaraman R (2012) Cardioprotective effect of vitamin E in combination with lycopene on lipid profile lipid metabolizing enzymes and infarction size in myocardial infarction induced by isoproterenol. Pharmacologia 3, 215–220.
| Cardioprotective effect of vitamin E in combination with lycopene on lipid profile lipid metabolizing enzymes and infarction size in myocardial infarction induced by isoproterenol.Crossref | GoogleScholarGoogle Scholar |
van Breemen RB, Pajkovic N (2008) Multitargeted therapy of cancer by lycopene. Cancer Letters 269, 339–351.
| Multitargeted therapy of cancer by lycopene.Crossref | GoogleScholarGoogle Scholar | 18585855PubMed |
Verghese M, Richardson JE, Boateng J, Shackelford LA, Howard C, Walker LT, Chawan CB (2008) Dietary lycopene has a protective effect on cardiovascular disease in New Zealand male rabbits. Journal of Biological Sciences 8, 268–277.
| Dietary lycopene has a protective effect on cardiovascular disease in New Zealand male rabbits.Crossref | GoogleScholarGoogle Scholar |
Wang XD (2012) Lycopene metabolism and its biological significance. American Journal of Clinical Nutrition 96, 1214S–1222S.
| Lycopene metabolism and its biological significance.Crossref | GoogleScholarGoogle Scholar | 23053559PubMed |
Wang X, Sato R, Brown MS, Hua X, Goldsteinm JL (1994) SREBP-1, a membrane-bound transcription factor released by sterol-regulated proteolysis. Journal Cell 77, 53–62.
| SREBP-1, a membrane-bound transcription factor released by sterol-regulated proteolysis.Crossref | GoogleScholarGoogle Scholar | 8156598PubMed |
Wang X, Magkos F, Mittendorfer B (2011) Sex differences in lipid and lipoprotein metabolism: it’s not just about sex hormones. Journal of Clinical Endocrinology and Metabolism 96, 885–893.
| Sex differences in lipid and lipoprotein metabolism: it’s not just about sex hormones.Crossref | GoogleScholarGoogle Scholar | 21474685PubMed |