Hostname: page-component-cd9895bd7-8ctnn Total loading time: 0 Render date: 2024-12-26T13:43:55.741Z Has data issue: false hasContentIssue false
  • English
  • Français

Effects of curcumin on performance, antioxidation, intestinal barrier and mitochondrial function in ducks fed corn contaminated with ochratoxin A

Published online by Cambridge University Press:  12 April 2018

D. Ruan ,
W. C. Wang ,
C. X. Lin ,
A. M. Fouad ,
W. Chen ,
W. G. Xia ,
S. Wang ,
X. Luo ,
W. H. Zhang  and
S. J. Yan
...Show all authors
D. Ruan
Affiliation:
College of Animal Science, South China Agricultural University, Guangzhou 510642, China Institute of Animal Science, Guangdong Academy of Agricultural Sciences, Guangzhou 510640, China
W. C. Wang
Affiliation:
College of Animal Science, South China Agricultural University, Guangzhou 510642, China
C. X. Lin
Affiliation:
Institute of Animal Science, Guangdong Academy of Agricultural Sciences, Guangzhou 510640, China
A. M. Fouad
Affiliation:
Institute of Animal Science, Guangdong Academy of Agricultural Sciences, Guangzhou 510640, China Department of Animal Production, Faculty of Agriculture, Cairo University, Giza 12613, Egypt
W. Chen
Affiliation:
Institute of Animal Science, Guangdong Academy of Agricultural Sciences, Guangzhou 510640, China
W. G. Xia
Affiliation:
Institute of Animal Science, Guangdong Academy of Agricultural Sciences, Guangzhou 510640, China
S. Wang
Affiliation:
Institute of Animal Science, Guangdong Academy of Agricultural Sciences, Guangzhou 510640, China
X. Luo
Affiliation:
Institute of Animal Science, Guangdong Academy of Agricultural Sciences, Guangzhou 510640, China
W. H. Zhang
Affiliation:
Agro-biological Gene Research Center, Guangdong Academy of Agricultural Sciences, Guangzhou 510640, China
S. J. Yan
Affiliation:
Agro-biological Gene Research Center, Guangdong Academy of Agricultural Sciences, Guangzhou 510640, China
C. T. Zheng
Affiliation:
Institute of Animal Science, Guangdong Academy of Agricultural Sciences, Guangzhou 510640, China
L. Yang*
Affiliation:
College of Animal Science, South China Agricultural University, Guangzhou 510642, China
*
†E-mail: [email protected]
Get access

Abstract

Curcumin has been attributed with antioxidant, anti-inflammatory, antibacterial activities, and has shown highly protective effects against enteropathogenic bacteria and mycotoxins. Ochratoxin A (OTA) is one of the major intestinal pathogenic mycotoxins. The possible effect of curcumin on the alleviation of enterotoxicity induced by OTA is unknown. The effects of dietary curcumin supplementation on OTA-induced oxidative stress, intestinal barrier and mitochondrial dysfunctions were examined in young ducks. A total of 540 mixed-sex 1-day-old White Pekin ducklings with initial BW (43.4±0.1 g) were randomly assigned into controls (fed only the basal diet), a group fed an OTA-contaminated diet (2 mg/kg feed), and a group fed the same OTA-contaminated feed plus 400 mg/kg of curcumin. Each treatment consisted of six replicates, each containing 30 ducklings and treatment lasted for 21 days. There was a significant decrease in average daily gain (ADG) and increased feed : gain caused by OTA (P<0.05); curcumin co-treatment prevented the decrease in BW and ADG compared with the OTA group (P<0.05). Histopathological and ultrastructural examination showed clear signs of enterotoxicity caused by OTA, but these changes were largely prevented by curcumin supplementation. Curcumin decreased the concentrations of interleukin-1β, tumor necrosis factor-α and malondialdehyde, and increased the activity of glutathione peroxidase induced by OTA in the jejunal mucosa of ducks (P<0.05). Additionally, curcumin increased jejunal mucosa occludin and tight junction protein 1 mRNA and protein levels, and decreased those of ρ-associated protein kinase 1 (P<0.05). Notably, curcumin inhibited the increased expression of apoptosis-related genes, and downregulated mitochondrial transcription factors A, B1 and B2 caused by OTA without any effects on RNA polymerase mitochondrial (P<0.05). These results indicated that curcumin could protect ducks from OTA-induced impairment of intestinal barrier function and mitochondrial integrity.

Keywords

curcuminochratoxin Aenterotoxicityintestinal functionducks
Type
Research Article
Information
animal , Volume 13 , Issue 1 , January 2019 , pp. 42 - 52
Copyright
© The Animal Consortium 2018 

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

Present address: Institute of Animal Science, Guangdong Academy of Agricultural Sciences, No.1 Dafeng First Street, Wushan Road, Tianhe District, Guangzhou 510640, China.

References

Al-Anati, L, Essid, E, Stenius, U, Beuerlein, K, Schuh, K and Petzinger, E 2010. Differential cell sensitivity between OTA and LPS upon releasing TNF-α . Toxins 2, 1279–1299.Google Scholar
Asin-Cayuela, J and Gustafsson, CM 2007. Mitochondrial transcription and its regulation in mammalian cells. Trends in Biochemical Sciences 32, 111–117.Google Scholar
Bradford, MM 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.Google Scholar
Chung, HL, Hwang, JB, Park, JJ and Kim, SG 2002. Expression of transforming growth factor beta1, transforming growth factor type I and II receptors, and TNF-alpha in the mucosa of the small intestine in infants with food protein-induced enterocolitis syndrome. Journal of Allergy and Clinical Immunology 109, 150–154.Google Scholar
Dorta, DJ, Pigoso, AA, Mingatto, FE, Rodrigues, T, Prado, IMR, Helena, AFC, Uyemura, SA, Santos, AC and Curti, C 2005. The interaction of flavonoids with mitochondria: effects on energetic processes. Chemicro-Biological Interactions 152, 67–78.Google Scholar
Du, LJ, Kim, JJ, Shen, JH and Dai, N 2016. Crosstalk between inflammation and ROCK/MLCK signaling pathways in gastrointestinal disorders with intestinal hyperpermeability. Gastroenterology Research and Practice 2016, 7374197.Google Scholar
Gowda, NKS, Ledoux, DR, Rottinghaus, GE, Bermudez, AJ and Chen, YC 2009. Antioxidant efficacy of curcuminoids from turmeric (Curcuma longa L.) powder in broiler chickens fed diets containing aflatoxin B1 . British Journal of Nutrition 102, 1629–1634.Google Scholar
Grenier, B and Applegate, TJ 2013. Modulation of intestinal functions following mycotoxin ingestion: meta-analysis of published experiments in animals. Toxins 5, 396–430.Google Scholar
Hoehler, D and Marquardt, RR 1996. Influence of vitamins E and C on the toxic effects of ochratoxin A and T-2 toxin in chicks. Poultry Science 75, 1508–1515.Google Scholar
Ikeda, M, Ide, T, Fujino, T, Arai, S, Saku, K, Kakino, T, Tyynismaa, H, Yamasaki, T, Yamada, K, Kang, D, Suomalainen, A and Sunagawa, K 2015. Overexpression of TFAM or twinkle increases mtDNA copy number and facilitates cardioprotection associated with limited mitochondrial oxidative stress. PLoS ONE 10, 0119687.Google Scholar
Kang, D, Kim, SH and Hamasaki, N 2007. Mitochondrial transcription factor A (TFAM): roles in maintenance of mtDNA and cellular functions. Mitochondrion 7, 39–44.Google Scholar
Kanki, T, Nakayama, H, Sasaki, N, Takio, K, Alam, TI, Hamasaki, N and Kang, D 2004. Mitochondrial nucleoid and transcription factor A. Annals of the New York Academy of Sciences 1011, 61–68.Google Scholar
Kőszegi, T and Poór, M 2016. Ochratoxin A: molecular interactions, mechanisms of toxicity and prevention at the molecular level. Toxins 8, 111.Google Scholar
Li, JY, Yu, Y, Hao, J, Jin, H and Xu, HJ 1996. Determination of diamine oxidase activity in intestinal tissue and blood using spectrophotometry. Amino Acids & Biotic Resources 18, 28–30.Google Scholar
Maresca, M, Mahfound, R, Pfohl-Leszkowicz, A and Fantini, J 2001. The mycotoxin ochratoxin A alters intestinal barrier and absorption functions but has no effect on chloride secretion. Toxicology and Applied Pharmacology 176, 54–63.Google Scholar
McLaughlin, J, Padfield, PJ, Burt, JPH and O’Neill, CA 2004. Ochratoxin A increases permeability through tight junctions by removal of specific claudin isoforms. American Journal of Physiology Cell Physiology 287, 1412–1417.Google Scholar
Moghadamtousi, SZ, Kadir, HA, Hassandarvish, P, Tajik, H, Abubakar, S and Zandi, K 2014. A review on antibacterial, antiviral, and antifungal activity of curcumin. BioMed Research International 2014, 186864.Google Scholar
Muhammad, I, Sun, XQ, Wang, H, Li, W, Wang, XH, Cheng, P, Li, SH, Zhang, XY and Hamid, S 2017. Curcumin successfully inhibited the computationally identified CYP2A6 enzyme-mediated bioactivation of aflatoxin B1 in Arbor Acres broiler. Frontiers in Pharmacology 8, 143.Google Scholar
National Research Council (NRC) 1994. Nutrient requirements of Poultry, 9th revised edition. National Academy Press, Washington, DC, USA.Google Scholar
Poór, M, Veres, B, Jakus, PB, Antus, C, Montskó, G, Zrínyi, Z, Vladimir-Knežević, S, Petrik, J and Kőszegi, T 2014. Flavonoid diosmetin increases ATP levels in kidney cells and relieves ATP depleting effect of ochratoxin A. Journal of Photochemistry and Photobiology B: Biology 132, 1–9.Google Scholar
Prior, MG, Oneil, JB and Sisodia, CS 1980. Effects of ochratoxin A on growth response and residues in broilers. Poultry Science 59, 1254–1257.Google Scholar
Rainey, NE, Moustapha, A, Parker, R and Petit, PX 2017. Curcumin a multifaceted compound with hormetic behavior that mediates an intricate crosstalk between mitochondrial biogenesis, mitophagy, mitophagic death and apoptosis. Preprints 2017, 2017010039.Google Scholar
Rajput, N, Muhammad, N, Yan, R, Zhong, X and Wang, T 2013. Effect of dietary supplementation of curcumin on growth performance, intestinal morphology and nutrients utilization of broiler chicks. The Journal of Poultry Science 50, 44–52.Google Scholar
Ranaldi, G, Mancini, E, Ferruzza, S, Sambuy, Y and Perozzi, G 2007. Effects of red wine on ochratoxin A toxicity in intestinal Caco-2/TC7 cells. Toxicology in Vitro 21, 204–210.Google Scholar
Rao, VK, Ramana, MV, Girisham, S and Reddy, SM 2013. Culture media and factors influencing ochratoxin A production by two species of Penicillium isolated from poultry feeds. National Academy Science Letters 36, 101–110.Google Scholar
Ringot, D, Chango, A, Schneider, Y and Larondelle, Y 2006. Toxicokinetics and toxicodynamics of ochratoxin A, an update. Chem-Biological Interactions 159, 18–46.Google Scholar
Shen, G, Xu, C, Hu, R, Jain, MR, Gopalkrishnan, A, Nair, S, Huang, MT, Chan, JY and Kong, AN 2006. Modulation of nuclear factor E2-related 2-mediated gene expression in mice liver and small intestine by cancer chemopreventive agent curcumin. Molecular Cancer Therapeutics 5, 39–51.Google Scholar
Śliżewska, K and Piotrowska, M 2014. Reduction of ochratoxin A in chicken feed using probiotic. Annals of Agricultural and Environmental Medicine 21, 676–680.Google Scholar
Solcan, C, Pavel, G, Floristean, VC, Chiriac, ISB, Şlencu, BG and Solcan, G 2015. Effect of ochratoxin A on the intestinal mucosa and mucosa-associated lymphoid tissues in broiler chickens. Acta Veterinaria Hungarica 63, 30–48.Google Scholar
Stoev, SD 2016. Food security and foodborne mycotoxicoses, risk assessment, preventive measures, and underestimated hazard of masked mycotoxins or joint mycotoxin interaction. Food Toxicology 9, 169–199.Google Scholar
Suliman, HB, Carraway, MS, Welty-Wolf, KE, Whorton, AR and Piantadosi, CA 2003. Lipopolysaccharide stimulates mitochondrial biogenesis via activation of nuclear respiratory factor-1. Journal of Biological Chemistry 278, 41510–41518.Google Scholar
Taha, R, Seidman, E, Mailhot, G, Boudreau, F, Gendron, F, Beaulieu, J, Menard, D, Delvin, E, Amre, D and Levy, E 2010. Oxidative stress and mitochondrial functions in the intestinal Caco-2/15 cell line. PLoS ONE 5, 11817.Google Scholar
Turner, JR 2009. Intestinal mucosal barrier function in health and disease. Nature Reviews Immunology 9, 799–809.Google Scholar
Venditti, P, Stefano, LD and Meo, SD 2013. Mitochondrial metabolism of reactive oxygen species. Mitochondrion 13, 71–82.Google Scholar
Wang, N, Wang, G, Hao, JX, Ma, JJ, Wang, Y, Jiang, XY and Jiang, HQ 2012. Curcumin ameliorates hydrogen peroxide-induced epithelial barrier disruption by upregulating heme oxygenase-1 expression in human intestinal epithelial cells. Digestive Diseases and Sciences 57, 1792–1801.Google Scholar
Wei, YH, Lu, TN and Wei, RD 1985. Effect of ochratoxin A on rat liver mitochondrial respiration and oxidative phosphorylation. Toxicology 36, 119–123.Google Scholar
Zhong, L 2008. Effects of moldy feed by Aspergillus ochraceus on Cherry Valley male duck. Master thesis, South China Agricultural University, Guangzhou, China.Google Scholar
Supplementary material: File

Ruan et al. supplementary material 1

Supplementary Figure

Download Ruan et al. supplementary material 1(File)
File 246.3 KB