Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-27T08:06:54.209Z Has data issue: false hasContentIssue false

Effects of maternal vitamin D3 during pregnancy on FASN and LIPE mRNA expression in offspring pigs

Published online by Cambridge University Press:  27 March 2020

Liping Guo
Affiliation:
Sumy National Agrarian University, Sumy, Ukraine School of Food Science and Technology, Henan Institute of Science and Technology, Xinxiang, Henan, 453003, P. R. China
Zhiguo Miao*
Affiliation:
College of Animal Science and Veterinary Medicine, Henan Institute of Science and Technology, Xinxiang, Henan, 453003, P. R. China
Hanjun Ma
Affiliation:
School of Food Science and Technology, Henan Institute of Science and Technology, Xinxiang, Henan, 453003, P. R. China
Sergiy Melnychuk
Affiliation:
Sumy National Agrarian University, Sumy, Ukraine
*
Author for correspondence: Zhiguo Miao, E-mail: miaozhiguo1998@126.com

Abstract

In this study, sows were fed 200 (LD), 800 (ND) and 3200 (HD) IU of vitamin D3/kg basal diet during pregnancy (from 41 d to birth), respectively. All their offspring pigs were fed the same vitamin D3 replete die. At 150 days of age, a total of 18 offspring pigs (six offspring pigs per maternal diet group, sex balance) were weighed and slaughtered to investigate effects of maternal vitamin D3 during pregnancy on fatty acids synthase (FASN) and hormone-sensitive lipase (LIPE) expression in offspring pigs. The results showed that LD offspring pigs had higher FASN mRNA expression and the ratio of FASN/LIPE mRNA expression in subcutaneous adipose tissue, as well as higher LIPE mRNA expression of longissimus dorsal muscle, whereas, had lower the ratio of FASN/LIPE mRNA expression in longissimus dorsal muscle compared with ND or HD offspring pigs, respectively. Meanwhile, LD offspring pigs had higher carcass fat, average backfat thickness (ABFT), serum insulin and leptin levels, lower intramuscular fat (IMF), serum free fatty acid and triglycerol levels compared with ND or HD offspring pigs. In addition, the ratio of FASN/LIPE mRNA expression was negatively correlated with IMF content, and positively correlated to carcass fat content and ABFT in offspring pigs. Meanwhile, FASN mRNA expression was positively correlated with carcass fat content, while negatively correlated with ABFT in offspring pigs. These results suggested that maternal vitamin D3 affected fat accumulation and meat quality by regulating FASN and LIPE mRNA expression in offspring pigs.

Type
Animal Research Paper
Copyright
Copyright © Cambridge University Press 2020

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

*

These two authors contributed equally to this work.

References

AOAC (Association of the Official Analytical Chemists) (1990) Official Methods of Analysis, 15th Edn. Gaithersburg, MD, USA: AOAC.Google Scholar
Barber, MC, Ward, RJ, Richards, SE, Salter, AM, Buttery, PJ, Vernon, RG and Travers, MT (2000) Ovine adipose tissue monounsaturated fat content is correlated to depot-specific expression of the stearoyl-CoA desaturase gene. Journal of Animal Science 78, 6268.CrossRefGoogle ScholarPubMed
Beckman, LM, Earthman, CP, Thomas, W, Compher, CW, Muniz, J, Horst, RL, Ikramuddin, S, Kellogg, TA and Sibley, SD (2013) Serum 25(OH) vitamin D concentration changes after Roux-en-Y gastric bypass surgery. Obesity 21, E599E606.CrossRefGoogle ScholarPubMed
Belenchia, AM, Jones, KL, Will, M, Beversdorf, DQ, Vieira-Potter, V, Rosenfeld, CS and Peterson, CA (2018) Maternal vitamin D deficiency during pregnancy affects expression of adipogenic-regulating genes peroxisome proliferator-activated receptor gamma (PPARγ) and vitamin D receptor (VDR) in lean male mice offspring. European Journal of Nutrition 57, 723730.CrossRefGoogle ScholarPubMed
Bhat, M, Noolu, B, Qadri, SS and Ismail, A (2014) Vitamin D deficiency decreases adiposity in rats and causes altered expression of uncoupling proteins and steroid receptor coactivator3. The Journal of Steroid Biochemistry and Molecular Biology 144, 304312.CrossRefGoogle ScholarPubMed
Boon, N, Hul, GB, Sicard, A, Kole, E, Van Den Berg, ER, Viguerie, N, Langin, D and Saris, WH (2006) The effects of increasing serum calcitriol on energy and fat metabolism and gene expression. Obesity 14, 17391746.CrossRefGoogle ScholarPubMed
Buettner, C and Camacho, RC (2008) Hypothalamic control of hepatic glucose production and its potential role in insulin resistance. Endocrinology Metabolism Clinics North America 37, 825840.CrossRefGoogle ScholarPubMed
Caron-Jobin, M, Morisset, AS, Tremblay, A, Huot, C, Légaré, D and Tchernof, A (2011) Elevated serum 25(OH)D concentrations, vitamin D, and calcium intakes are associated with reduced adipocyte size in women. Obesity 19, 13351341.CrossRefGoogle ScholarPubMed
Carrelli, A, Bucovsky, M, Horst, R, Cremers, S, Zhang, C, Bessler, M, Schrope, B, Evanko, J, Blanco, J, Silverberg, SJ and Stein, EM (2017) Vitamin D storage in adipose tissue of obese and normal weight women. Journal of Bone and Mineral Research 32, 237242.CrossRefGoogle ScholarPubMed
Chango, A and Pogribny, IP (2015) Considering maternal dietary modulators for epigenetic regulation and programming of the fetal epigenome. Nutrients 7, 27482770.CrossRefGoogle ScholarPubMed
Chen, J, Yang, X-J, Tong, H, Chen, J and Zhao, R-Q (2004) Expressions of FAS and HSL mRNA in longissimus dorsi muscle and their relation to intramuscular fat contents in pig. Journal of Agricultural Biotechnology 12, 422426.Google Scholar
Dix, CF, Barcley, JL and Wright, ORL (2018) The role of vitamin D in adipogenesis. Nutrition Reviews 76, 4759.CrossRefGoogle ScholarPubMed
Du, M, Tong, J, Zhao, J, Underwood, KR, Zhu, M, Ford, SP and Nathanielsz, PW (2010) Fetal programming of skeletal muscle development in ruminant animals. Journal of Animal Science 88, E51E60.CrossRefGoogle ScholarPubMed
Du, M, Wang, B, Fu, X, Yang, Q and Zhu, MJ (2015) Fetal programming in meat production. Meat Science 109, 4047.CrossRefGoogle ScholarPubMed
Fish, E, Beverstein, G, Olson, D, Reinhardt, S, Garren, M and Gould, J (2010) Vitamin D status of morbidly obese bariatric surgery patients. Journal of Surgical Research 164, 198202.CrossRefGoogle ScholarPubMed
Flohr, JR, Tokach, MD, Dritz, SS, DeRouchey, JM, Goodband, RD, Nelssen, JL and Bergstrom, JR (2014) An evaluation of the effects of added vitamin D3 in maternal diets on sow and pig performance. Journal of Animal Science 92, 594603.CrossRefGoogle ScholarPubMed
Flohr, JR, Woodworth, JC, Bergstrom, JR, Tokach, MD, Dritz, SS, Goodband, RD and DeRouchey, JM (2016) Evaluating the impact of maternal vitamin D supplementation on sow performance: II. Subsequent growth performance and carcass characteristics of growing pigs. Journal of Animal Science 94, 46434653.CrossRefGoogle ScholarPubMed
Gangloff, A, Bergeron, J, Lemieux, I, Tremblay, A, Poirier, P, Alméras, N and Després, JP (2020) Relationships between circulating 25(OH) vitamin D, leptin levels and visceral adipose tissue volume: results from a 1-year lifestyle intervention program in men with visceral obesity. International Journal of Obesity (Lond) 44, 280288.CrossRefGoogle ScholarPubMed
Haemmerle, G, Zimmermann, R and Zechner, R (2003) Letting lipids go: hormone-sensitive lipase. Current Opinion in Lipidology 14, 289297.CrossRefGoogle ScholarPubMed
Huang, QC, Xu, ZR, Han, XY and Li, WF (2008) Effect of dietary betaine supplementation on lipogenic enzyme activities and fatty acid synthase mRNA expression in finishing pigs. Animal Feed Science and Technology 140, 365375.CrossRefGoogle Scholar
Ishida, Y, Taniguchi, H and Baba, S (1988) Possible involvement of 1-alpha,25-dihydroxyvitamin D3 in proliferation and differentiation of 3T3-L1 cells. Biochemical and Biophysical Research Communications 151, 11221127.CrossRefGoogle ScholarPubMed
Jakobsen, J, Maribo, H, Bysted, A, Sommer, HM and Hels, O (2007) 25-hydroxyvitamin D3 affects vitamin D status similar to vitamin D3 in pigs – but the meat produced has a lower content of vitamin D. British Journal of Nutrition 98, 908913.CrossRefGoogle Scholar
Ji, S, Doumit, ME and Hill, RA (2015) Correction: regulation of adipogenesis and Key adipogenic gene expression by 1,25-dihydroxyvitamin D in 3T3-L1 cells. PLoS One 10, e0134199.CrossRefGoogle ScholarPubMed
Kong, J and Li, YC (2006) Molecular mechanism of 1,25-dihydroxyvitamin D3 inhibition of adipogenesis in 3T3-L1 cells. American Journal of Physiology Endocrinology and Metabolism 290, E916E924.CrossRefGoogle ScholarPubMed
Lee, YH, Petkova, AP, Mottillo, EP and Granneman, JG (2012) In vivo identification of bipotential adipocyte progenitors recruited by β3-adrenoceptor activation and high-fat feeding. Cell Metabolism 15, 480491.CrossRefGoogle ScholarPubMed
Leung, PS (2016) The potential protective action of vitamin D in hepatic insulin resistance and pancreatic islet dysfunction in type 2 diabetes mellitus. Nutrients 8, 147.CrossRefGoogle ScholarPubMed
Mahajan, A and Stahl, CH (2009) Dihydroxy-cholecalciferol stimulates adipocytic differentiation of porcine mesenchymal stem cells. Journal of Nutritional Biochemistry 20, 512520.CrossRefGoogle ScholarPubMed
Marcotorchino, J, Tournaiaire, F and Landrier, J-F (2013) Vitamin D, adipose tissue, and obesity. Hormone Molecular Biology and Clinical Investigation 15, 123128.CrossRefGoogle ScholarPubMed
Miao, ZG, Wang, LJ, Xu, ZR, Huang, JF and Wang, YR (2008) Developmental patterns in hormone and lipid metabolism of growing Jinhua and Landrace gilts. Canadian Journal of Animal Science 88, 601607.CrossRefGoogle Scholar
Miao, ZG, Wang, LJ, Xu, ZR, Huang, JF and Wang, YR (2009) Developmental changes of carcass composition, meat quality and organs in the Jinhua pig and Landrace. Animal: An International Journal of Animal Bioscience 3, 468473.CrossRefGoogle ScholarPubMed
Miao, Z, Zhu, F, Zhang, H, Chang, X, Xie, H, Zhang, J and Xu, Z (2010) Developmental patterns of FASN and LIPE mRNA expression in adipose tissue of growing Jinhua and Landrace gilts. Czech Journal of Animal Science 55, 557564.CrossRefGoogle Scholar
NRC (National Research Council) (2012) Nutrient Requirements of Swine, 7th Revised Edn, Washington, DC, USA: National Academies Press.Google Scholar
Qiao, Y, Huang, Z, Li, Q, Liu, Z, Hao, C, Shi, G, Dai, R and Xie, Z (2007) Developmental changes of the FAS and HSL mRNA expression and their effects on the content of intramuscular fat in Kazak and Xinjiang sheep. Journal of Genetics and Genomics 34, 909917.CrossRefGoogle ScholarPubMed
Scherer, T, O'Hare, J, Diggs-Andrews, K, Schweiger, M, Cheng, B, Lindtner, C, Zielinski, E, Vempati, P, Su, K, Dighe, S, Milsom, T, Puchowicz, M, Scheja, L, Zechner, R, Fisher, SJ, Previs, SF and Buettner, C (2011) Brain insulin controls adipose tissue lipolysis and lipogenesis. Cell Metablism 13, 183194.CrossRefGoogle ScholarPubMed
Semenkovich, CF (1997) Regulation of fatty acid synthase (FAS). Progress in Lipid Research 36, 4353.CrossRefGoogle Scholar
Sinclair, KD, Allegrucci, C, Singh, R, Gardner, DS, Sebastian, S, Bispham, J, Thurston, A, Huntley, JF, Rees, WD, Maloney, CA, Lea, RG, Craigon, J, McEvoy, TG and Young, LE (2007) DNA Methylation, insulin resistance, and blood pressure in offspring determined by maternal periconceptional B vitamin and methionine status. Proceedings of the National Academy of Sciences of the United States of America 104, 1935119356.CrossRefGoogle ScholarPubMed
Smith, S, Witkowski, A and Joshi, AK (2003) Structural and functional organization of the animal fatty acid synthase. Progress in Lipid Research 42, 289317.CrossRefGoogle ScholarPubMed
Suzuki, K, Inomata, K, Katoh, K, Kadowaki, H and Shibata, T (2009) Genetic correlations among carcass cross-sectional fat area ratios, production traits, intramuscular fat, and serum leptin concentration in Duroc pigs. Journal of Animal Science 87, 22092215.CrossRefGoogle ScholarPubMed
Tong, J, Zhu, MJ, Underwood, KR, Hess, BW, Ford, SP and Du, M (2008) AMP-activated protein kinase and adipogenesis in sheep fetal skeletal muscle and 3T3-L1 cells. Journal of Animal Science 86, 12961305.CrossRefGoogle ScholarPubMed
Wallace, AM, Gibson, S, De La Hunty, A, Lamberg-Allardt, C and Ashwell, M (2010) Measurement of 25-hydroxyvitamin D in the clinical laboratory: current procedures, performance characteristics and limitations. Steroids 75, 477488.CrossRefGoogle ScholarPubMed
Wang, B, Yang, Q, Harris, CL, Nelson, ML, Busboom, JR, Zhu, MJ and Du, M (2016) Nutrigenomic regulation of adipose tissue development – role of retinoic acid: a review. Meat Science 120, 100106.CrossRefGoogle ScholarPubMed
Wang, B, Fu, X, Liang, X, Wang, Z, Yang, Q, Zou, T, Nie, W, Zhao, J, Gao, P, Zhu, MJ, De Avila, JM, Maricelli, J, Rodgers, BD and Du, M (2017) Maternal retinoids increase PDGFRα + progenitor population and beige adipogenesis in progeny by stimulating vascular development. EBioMedicine 18, 288299.CrossRefGoogle ScholarPubMed
Wen, J, Hong, Q, Wang, X, Zhu, L, Wu, T, Xu, P, Fu, Z, You, L, Wang, X, Ji, C and Guo, X (2018) The effect of maternal vitamin D deficiency during pregnancy on body fat and adipogenesis in rat offspring. Scientific Reports 8, 365.CrossRefGoogle ScholarPubMed
Yang, QY, Liang, JF, Rogers, CJ, Zhao, JX, Zhu, MJ and Du, M (2013) Maternal obesity induces epigenetic modifications to facilitate Zfp423 expression and enhance adipogenic differentiation in fetal mice. Diabetes 62, 37273735.CrossRefGoogle ScholarPubMed
Yao, Y, Zhu, L, He, L, Duan, Y, Liang, W, Nie, Z, Jin, Y, Wu, X and Fang, Y (2015) A meta-analysis of the relationship between vitamin D deficiency and obesity. International Journal of Clinical and Experimental Medicine 8, 1497714984.Google ScholarPubMed
Zhou, H, Chen, Y, Lv, G, Zhuo, Y, Lin, Y, Feng, B, Fang, Z, Che, L, Li, J, Xu, S and Wu, D (2016) Improving maternal vitamin D status promotes prenatal and postnatal skeletal muscle development of pig offspring. Nutrition (Burbank, Los Angeles County, Calif.) 32, 11441152.CrossRefGoogle ScholarPubMed
Zhu, MJ, Ford, SP, Means, WJ, Hess, BW, Nathanielsz, PW and Du, M (2006) Maternal nutrient restriction affects properties of skeletal muscle in offspring. Journal of Physiology 575, 241250.CrossRefGoogle ScholarPubMed
Zhuang, H, Lin, Y and Yang, G (2007) Effects of 1,25-dihydroxyvitamin D3 on proliferation and differentiation of porcine preadipocyte in vitro. Chemico-Biological Interactions 170, 114123.CrossRefGoogle ScholarPubMed
Supplementary material: File

Guo et al. supplementary material

Tables S1-S2

Download Guo et al. supplementary material(File)
File 15.6 KB