Hostname: page-component-586b7cd67f-t7fkt Total loading time: 0 Render date: 2024-11-25T20:14:03.977Z Has data issue: false hasContentIssue false
  • English
  • Français

Effects of maternal methyl donor on the pork characteristics of offspring pigs with prenatal exposure to bisphenol A

Published online by Cambridge University Press:  25 October 2017

Y. Zhuo ,
J. Wang ,
H. Liu ,
D. Mou ,
T. Adebowale ,
L. Che ,
Z. Fang ,
S. Xu ,
G. Liu  and
Y. Lin
...Show all authors
Y. Zhuo
Affiliation:
Institute of Animal Nutrition, Sichuan Agricultural University, Chengdu, Sichuan 611130, People’s Republic of China
J. Wang
Affiliation:
Institute of Animal Nutrition, Sichuan Agricultural University, Chengdu, Sichuan 611130, People’s Republic of China
H. Liu
Affiliation:
Institute of Animal Nutrition, Sichuan Agricultural University, Chengdu, Sichuan 611130, People’s Republic of China
D. Mou
Affiliation:
Institute of Animal Nutrition, Sichuan Agricultural University, Chengdu, Sichuan 611130, People’s Republic of China
T. Adebowale
Affiliation:
Key Laboratory of Agro-ecological Processes in Subtropical Region, Institute of Subtropical Agriculture, Chinese Academy of Sciences, Hunan 410125, People’s Republic of China
L. Che
Affiliation:
Institute of Animal Nutrition, Sichuan Agricultural University, Chengdu, Sichuan 611130, People’s Republic of China
Z. Fang
Affiliation:
Institute of Animal Nutrition, Sichuan Agricultural University, Chengdu, Sichuan 611130, People’s Republic of China
S. Xu
Affiliation:
Institute of Animal Nutrition, Sichuan Agricultural University, Chengdu, Sichuan 611130, People’s Republic of China
G. Liu
Affiliation:
Key Laboratory of Agro-ecological Processes in Subtropical Region, Institute of Subtropical Agriculture, Chinese Academy of Sciences, Hunan 410125, People’s Republic of China
Y. Lin
Affiliation:
Institute of Animal Nutrition, Sichuan Agricultural University, Chengdu, Sichuan 611130, People’s Republic of China
B. Feng
Affiliation:
Institute of Animal Nutrition, Sichuan Agricultural University, Chengdu, Sichuan 611130, People’s Republic of China
N. Abdullah Al-Dhabi
Affiliation:
Department of Botany and Microbiology, Addiriyah Chair for Environmental Studies, College of Science, King Saud University, Riyadh 11451, Saudi Arabia
J. Li
Affiliation:
Institute of Animal Nutrition, Sichuan Agricultural University, Chengdu, Sichuan 611130, People’s Republic of China
V. Duraipandiyan
Affiliation:
Department of Botany and Microbiology, Addiriyah Chair for Environmental Studies, College of Science, King Saud University, Riyadh 11451, Saudi Arabia
D. Wu*
Affiliation:
Institute of Animal Nutrition, Sichuan Agricultural University, Chengdu, Sichuan 611130, People’s Republic of China
*
†E-mail: [email protected]; [email protected]
Get access

Abstract

To explore the effects of maternal nutrition on offspring muscle characteristics, a total of 56 sows were assigned to one of the four dietary groups during gestation: control (CON), or control diets supplemented with methyl donor (MET), bisphenol A (BPA), and combined BPA and MET (BPA+MET). Compared with CON offspring, MET offspring showed a higher meat redness value, but lower glycogen content in the longissimus thoracis (LT). Moreover, compared with CON offspring, MET offspring showed lower LT glycogen synthase (GS) mRNA levels at birth and the finishing stage, and increased methylation at the GS promoter. Prenatal BPA exposure reduced the pH and redness value of meat, but increased the lightness value, lactate content, glycolytic potential and lactate dehydrogenase (LDH) enzyme activity in the LT muscle. Prenatal BPA exposure increased LDH mRNA levels in the LT muscle at birth and the finishing stage, and reduced methylation at the LDH promoter. Thus, maternal MET affects muscle GS and LDH expression via DNA methylation, thereby resulting in persistent effects on pork quality.

Keywords

methyl donorbisphenol Asowsmeat qualitymethylation
Type
Research Article
Information
animal , Volume 12 , Issue 6 , June 2018 , pp. 1306 - 1315
Copyright
© The Animal Consortium 2017 

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

Yong Zhuo and Jun Wang contributed equally to this work.

References

Anderson, OS, Sant, KE and Dolinoy, DC 2012. Nutrition and epigenetics: an interplay of dietary methyl donors, one-carbon metabolism and DNA methylation. The Journal of Nutritional Biochemistry 23, 853–859.Google Scholar
Berkes, CA and Tapscott, SJ 2005. MyoD and the transcriptional control of myogenesis. Seminars in Cell & Developmental Biology 16, 585–595.Google Scholar
Bertol, T, Braña, D, Ellis, M, Ritter, M, Peterson, B, Mendoza, O and McKeith, F 2011. Effect of feed withdrawal and dietary energy source on muscle glycolytic potential and blood acid-base responses to handling in slaughter-weight pigs. Journal of Animal Science 89, 1561–1573.Google Scholar
Brenet, F, Moh, M, Funk, P, Feierstein, E, Viale, AJ, Socci, ND and Scandura, JM 2011. DNA methylation of the first exon is tightly linked to transcriptional silencing. PloS One 6, e14524.Google Scholar
Brewer, M, Zhu, L, Bidner, B, Meisinger, D and McKeith, F 2001. Measuring pork color: effects of bloom time, muscle, pH and relationship to instrumental parameters. Meat Science 57, 169–176.Google Scholar
Bowker, BC 2013. Meat Science And Muscle Biology Symposium: in utero factors that influence postnatal muscle growth, carcass composition, and meat quality. Journal of Animal Science 91, 1417–1418.Google Scholar
Calvisi, DF, Simile, MM, Ladu, S, Pellegrino, R, De Murtas, V, Pinna, F, Tomasi, ML, Frau, M, Virdis, P and De Miglio, MR 2007. Altered methionine metabolism and global DNA methylation in liver cancer: relationship with genomic instability and prognosis. International Journal of Cancer 121, 2410–2420.Google Scholar
Chao, HH, Zhang, XF, Chen, B, Pan, B, Zhang, LJ, Li, L, Sun, XF, Shi, QH and Shen, W 2012. Bisphenol A exposure modifies methylation of imprinted genes in mouse oocytes via the estrogen receptor signaling pathway. Histochemistry and Cell Biology 137, 249–259.Google Scholar
Dolinoy, DC, Huang, D and Jirtle, RL 2007. Maternal nutrient supplementation counteracts bisphenol A-induced DNA hypomethylation in early development. Proceedings of the National Academy of Sciences 104, 13056–13061.Google Scholar
Guay, F, Matte, JJ, Girard, CL, Palin, MF, Giguère, A and Laforest, JP 2002. Effects of folic acid and vitamin B 12 supplements on folate and homocysteine metabolism in pigs during early pregnancy. British Journal of Nutrition 88, 253–263.Google Scholar
Hamilton, D, Miller, K, Ellis, M, McKeith, F and Wilson, E 2003. Relationships between longissimus glycolytic potential and swine growth performance, carcass traits, and pork quality. Journal of Animal Science 81, 2206–2212.Google Scholar
Jones, PA 2012. Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nature Reviews Genetics 13, 484–492.Google Scholar
Kruszynska, YT, Ciaraldi, TP and Henry, RR 2011. Regulation of glucose metabolism in skeletal muscle. In Comprehensive physiology. Handbook of physiology, the endocrine system, the endocrine pancreas and regulation of metabolism (ed. D M Pollock), pp. 579–607. The American Physiological Society, Bethesda, Maryland, USA.Google Scholar
Laing, L, Viana, J, Dempster, E, Trznadel, M, Trunkfield, L, Webster, TU, van Aerle, R, Paull, G, Wilson, R and Mill, J 2016. Bisphenol A causes reproductive toxicity, decreases dnmt1 transcription, and reduces global DNA methylation in breeding zebrafish (Danio rerio). Epigenetics 11, 526–538.CrossRefGoogle ScholarPubMed
Law, JA and Jacobsen, SE 2010. Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nature Reviews Genetics 11, 204–220.Google Scholar
Lebret, B, Meunier-Salaun, MC, Foury, A, Mormede, P, Dransfield, E and Dourmad, JY 2006. Influence of rearing conditions on performance, behavioral, and physiological responses of pigs to preslaughter handling, carcass traits, and meat quality. Journal of Animal Science 84, 2436–2447.CrossRefGoogle ScholarPubMed
Leheska, J, Wulf, D and Maddock, R 2002. Effects of fasting and transportation on pork quality development and extent of postmortem metabolism. Journal of Animal Science 80, 3194–3202.Google Scholar
Lillycrop, KA and Burdge, GC 2012. Epigenetic mechanisms linking early nutrition to long term health. Best Practice & Research Clinical Endocrinology & Metabolism 26, 667–676.CrossRefGoogle ScholarPubMed
Liu, J, Lam, JB, Chow, KH, Xu, A, Lam, KS, Moon, RT and Wang, Y 2008. Adiponectin stimulates Wnt inhibitory factor-1 expression through epigenetic regulations involving the transcription factor specificity protein 1. Carcinogenesis 29, 2195–2202.CrossRefGoogle ScholarPubMed
Ma, Y, Xia, W, Wang, D, Wan, Y, Xu, B, Chen, X, Li, Y and Xu, S 2013. Hepatic DNA methylation modifications in early development of rats resulting from perinatal BPA exposure contribute to insulin resistance in adulthood. Diabetologia 56, 2059–2067.CrossRefGoogle ScholarPubMed
Mancini, R and Hunt, M 2005. Current research in meat color. Meat Science 71, 100–121.Google Scholar
Matte, J, Guay, F and Girard, C 2006. Folic acid and vitamin B12 in reproducing sows: new concepts. Canadian Journal of Animal Science 86, 197–205.Google Scholar
Monin, G and Sellier, P 1985. Pork of low technological quality with a normal rate of muscle pH fall in the immediate post-mortem period: the case of the Hampshire breed. Meat Science 13, 49–63.Google Scholar
Mou, D, Wang, J, Liu, H, Chen, Y, Che, L, Fang, Z, Xu, S, Lin, Y, Feng, B, Li, J and Wu, D 2017. Maternal methyl donor supplementation during gestation counteracts bisphenol A- induced oxidative stress in sows and offspring. Nutrition 45, 76–84.CrossRefGoogle ScholarPubMed
National Research Council (NRC) 2012. Nutrient requirements of swine, 11th revised edition. National Academy Press, Washington, DC, USA.Google Scholar
Oberdoerffer, S 2012. A conserved role for intragenic DNA methylation in alternative pre-mRNA splicing. Transcription 3, 106–109.Google Scholar
Pederson, BA, Schroeder, JM, Parker, GE, Smith, MW, DePaoli-Roach, AA and Roach, PJ 2005. Glucose metabolism in mice lacking muscle glycogen synthase. Diabetes 54, 3466–3473.Google Scholar
Rubin, BS 2011. Bisphenol A: an endocrine disruptor with widespread exposure and multiple effects. The Journal of steroid biochemistry and molecular biology 127, 27–34.CrossRefGoogle ScholarPubMed
Schübeler, D 2015. Function and information content of DNA methylation. Nature 517, 321–326.Google Scholar
Scheffler, T and Gerrard, D 2007. Mechanisms controlling pork quality development: The biochemistry controlling postmortem energy metabolism. Meat Science 77, 7–16.Google Scholar
Stockland, W and Blaylock, L 1974. Choline requirement of pregnant sows and gilts under restricted feeding conditions. Journal of Animal Science 39, 1113–1116.Google Scholar
Suman, SP and Joseph, P 2013. Myoglobin chemistry and meat color. Annual review of food science and technology 4, 79–99.Google Scholar
van Wettere, W, Smits, R and Hughes, P 2013. Methyl donor supplementation of gestating sow diets improves pregnancy outcomes and litter size. Animal Production Science 53, 1–7.Google Scholar
Wang, J, Wu, Z, Li, D, Li, N, Dindot, SV, Satterfield, MC, Bazer, FW and Wu, G 2012. Nutrition, epigenetics, and metabolic syndrome. Antioxidants & Redox Signaling 17, 282–301.Google Scholar
Zhang, C, Luo, J, Yu, B, Zheng, P, Huang, Z, Mao, X, He, J, Yu, J, Chen, J and Chen, D 2015. Dietary resveratrol supplementation improves meat quality of finishing pigs through changing muscle fiber characteristics and antioxidative status. Meat Science 102, 15–21.Google Scholar
Supplementary material: PDF

Zhuo et al supplementary material 1

Zhuo et al supplementary material

Download Zhuo et al supplementary material 1(PDF)
PDF 397 KB