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Recent advances of vitamin D in immune, reproduction, performance for pig: a review

Published online by Cambridge University Press:  02 June 2021

Pan Yang  and
Yongxi Ma Open the ORCID record for Yongxi Ma [Opens in a new window]
Pan Yang
Affiliation:
Department of Animal Nutrition and Feed Science, State Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural University, Beijing100193, People's Republic of China
Yongxi Ma*
Affiliation:
Department of Animal Nutrition and Feed Science, State Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural University, Beijing100193, People's Republic of China
*
Author for correspondence: Yongxi Ma, Department of Animal Nutrition and Feed Science, State Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural University, Beijing100193, People's Republic of China. E-mail: mayongxi2005@163.com
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Abstract

Vitamin D (VD) has been reported to play multiple and significant roles in improving pig health via modulating calcium and phosphorus homeostasis, skeletal muscle development and the immune system. Apart from food, photochemical action of 7-dehydrocholesterol in the skin is the main source of this molecule for pigs. The VD from dietary intake or photosynthesized via skin can be absorbed into the liver for hydroxylation, and further hydroxylated into the hormone form of VD (1,25-dihydroxyvitamin D3 or 1,25(OH)2D3) in the kidney. As a sterol hormone, 1,25(OH)2D3 is able to bind with the VD receptor (VDR), and this ligand-receptor complex (VDR/retinoic X receptor) translocates from the cytoplasm into the nucleus to regulate gene expression, thus modulating metabolism. In this review, we summarized the recent studies regarding the non-skeletal health benefits of VD for pigs, and focused on the recent advances in the cellular and molecular mechanisms of VD that affects the immune system and reproductive health. This review provides a reference for future research and application of VD in pigs.

Keywords

Immunepigreproductive healthserum 25(OH)D3vitamin D
Type
Review Article
Information
Animal Health Research Reviews , Volume 22 , Issue 1 , June 2021 , pp. 85 - 95
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Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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References

Amundson, LA, Hernandez, LL and Crenshaw, TD (2017) Serum and tissue 25-OH vitamin D3 concentrations do not predict bone abnormalities and molecular markers of vitamin D metabolism in the hypovitaminosis D kyphotic pig model. British Journal of Nutrition 118, 30–40.CrossRefGoogle Scholar
Arnold, J, Madson, DM, Acvp, D, Ensley, SM, Goff, JP, Stevenson, GW, Acvp, D, Crenshaw, T, Wang, C and Horst, RL (2015) Survey of serum vitamin D status across stages of swine production and evaluation of supplemental bulk vitamin D premixes used in swine diets. Journal of Swine Health and Production 23, 28–34.Google Scholar
Baeke, F, Gysemans, C, Korf, H and Mathieu, C (2010) Vitamin D insufficiency: implications for the immune system. Pediatric Nephrology 25, 1597–1606.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, 723–730.CrossRefGoogle ScholarPubMed
Chishimba, L, Thickett, DR, Stockley, RA and Wood, AM (2010) The vitamin D axis in the lung: a key role for vitamin D-binding protein. Thorax 65, 456–462.CrossRefGoogle ScholarPubMed
Chun, RF, Lauridsen, AL, Suon, L, Zella, LA, Pike, JW, Modlin, RL, Martineau, AR, Wilkinson, RJ, Adams, J and Hewison, M (2010) Vitamin D-binding protein directs monocyte responses to 25-hydroxy- and 125-dihydroxyvitamin D. The Journal of Clinical Endocrinology & Metabolism 95, 3368–3376.CrossRefGoogle Scholar
Cippitelli, M and Santoni, A (1998) Vitamin D3: a transcriptional modulator of the interferon-γ gene. European Journal of Immunology 28, 3017–3030.3.0.CO;2-6>CrossRefGoogle ScholarPubMed
Coffey, JD, Hines, EA, Starkey, JD, Starkey, CW and Chung, TK (2012) Feeding 25-hydroxycholecalciferol improves gilt reproductive performance and fetal vitamin D status. Journal of Animal Science 90, 3783–3788.CrossRefGoogle ScholarPubMed
Del Pinto, R, Ferri, C and Cominelli, F (2017) Vitamin D axis in inflammatory bowel diseases: role, current uses and future perspectives. International Journal of Molecular Sciences 18, 2360.CrossRefGoogle ScholarPubMed
Dicken, CL, Israel, DD, Davis, JB, Sun, Y, Shu, J, Hardin, J and Neal-Perry, G (2012) Peripubertal vitamin D3 deficiency delays puberty and disrupts the estrous cycle in adult female mice. Biology of Reproduction 51, 1–12.Google Scholar
Du, H, Daftary, GS, Lalwani, SI and Taylor, HS (2005) Direct regulation of HOXA10 by 1, 25–(OH)2D3 in human myelomonocytic cells and human endometrial stromal cells. Molecular Endocrinology 19, 2222–2233.CrossRefGoogle ScholarPubMed
Duffy, SK, Kelly, AK, Rajauria, G, Clarke, LC, Gath, V, Monahan, FJ and O'Doherty, JV (2018a) The effect of 25-hydroxyvitamin D3 and phytase inclusion on pig performance bone parameters and pork quality in finisher pigs. Journal of Animal Physiology and Animal Nutrition 102, 1296–1305.CrossRefGoogle Scholar
Duffy, SK, Kelly, AK, Rajauria, G, Jakobsen, J, Clarke, LC, Monahan, FJ, Dowling, KG, Hull, G, Galvin, K, Cashman, KD, Hayes, A and O'Doherty, JV (2018b) The use of synthetic and natural vitamin D sources in pig diets to improve meat quality and vitamin D content. Meat Science 143, 60–68.CrossRefGoogle Scholar
Feldman, D, Krishnan, AV, Swami, S, Giovannucci, E and Feldman, BJ (2014) The role of vitamin D in reducing cancer risk and progression. Nature Reviews Cancer 14, 342–357.CrossRefGoogle ScholarPubMed
Ferreira, GB, Vanherwegen, AS, Eelen, G, Gutiérrez, ACF, VanLommel, L, Marchal, K, Verlinden, L, Verstuyf, A, Nogueira, T, Georgiadou, M, Schuit, F, Eizirik, DL, Gysemans, C, Carmeliet, P, Overbergh, L and Mathieu, C (2015) Vitamin D3 induces tolerance in human dendritic cells by activation of intracellular metabolic pathways. Cell Reports 10, 711–725.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, 594–603.CrossRefGoogle ScholarPubMed
Flohr, JR, Woodworth, JC, Bergstrom, JR, Tokach, MD, Dritz, SS, Goodband, RD and DeRouchey, JM (2016a) Evaluating the impact of maternal vitamin D supplementation: I, sow performance serum vitamin metabolites and neonatal muscle characteristics. Journal of Animal Science 94, 4629–4642.CrossRefGoogle Scholar
Flohr, JR, Woodworth, JC, Bergstrom, JR, Tokach, MD, Dritz, SS, Goodband, RD and DeRouchey, JM (2016b) 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, 4643–4653.CrossRefGoogle Scholar
Holick, MF (2007) Vitamin D deficiency. New England Journal of Medicine 357, 266–281.CrossRefGoogle ScholarPubMed
Holick, MF, Binkley, NC, Bischoff-Ferrari, HA, Gordon, CM, Hanley, DA, Heaney, RP, Murad, MH and Weaver, CM (2011) Evaluation, treatment, and prevention of vitamin D deficiency: an Endocrine Society clinical practice guideline. Journal of Clinical Endocrinology and Metabolism 96, 1911–1930.CrossRefGoogle ScholarPubMed
Jang, YD, Ma, J, Lu, N, Lim, J, Monegue, HJ, Stuart, RL and Lindemann, MD (2018) Administration of vitamin D3 by injection or drinking water alters serum 25-hydroxycholecalciferol concentrations of nursery pigs. Asian-Australasian Journal of Animal Science 31, 278–286.CrossRefGoogle Scholar
Jeffery, LE, Burke, F, Mura, M, Zheng, Y, Qureshi, OS, Hewison, M, Walker, LSK, Lammas, DA, Raza, K and Sansom, DM (2009) 1, 25-Dihydroxyvitamin D3 and IL-2 combine to inhibit T cell production of inflammatory cytokines and promote development of regulatory T cells expressing CTLA-4 and FoxP3. The Journal of Immunology 183, 5458–5467.CrossRefGoogle ScholarPubMed
Jones, G, Prosser, DE and Kaufmann, M (2012) 25-Hydroxyvitamin D-24-hydroxylase (CYP24A1): its important role in the degradation of vitamin D. Archives of Biochemistry and Biophysics 523, 9–18.CrossRefGoogle ScholarPubMed
Kinuta, K, Tanaka, H, Moriwake, T, Aya, K, Kato, S and Seino, Y (2000) Vitamin D is an important factor in estrogen biosynthesis of both female and male gonads. Endocrinology 141, 1317–1324.CrossRefGoogle ScholarPubMed
Konowalchuk, JD, Rieger, AM, Kiemele, MD, Ayres, DC and Barreda, DR (2013) Modulation of weanling pig cellular immunity in response to diet supplementation with 25-hydroxyvitamin D3. Veterinary Immunology and Immunopathology 155, 57–66.CrossRefGoogle Scholar
Lauridsen, C (2014) Triennial growth symposium-establishment of the 2012 vitamin D requirements in swine with focus on dietary forms and levels of vitamin D. Journal of Animal Science 92, 910–916.CrossRefGoogle ScholarPubMed
Lauridsen, C, Halekoh, U, Larsen, T and Jensen, SK (2010) Reproductive performance and bone status markers of gilts and lactating sows supplemented with two different forms of vitamin D. Journal of Animal Science 88, 202–213.CrossRefGoogle ScholarPubMed
Lee, KN, Kang, HS, Jeon, JH, Kim, EM, Yoon, SR, Song, H, Lyu, CY, Piao, ZH, Kim, SU, Han, YH, Song, SS, Lee, YH, Song, KS, Kim, YM, Yu, DY and Choi, I (2005) VDUP1 is required for the development of natural killer cells. Immunity 22, 195–208.CrossRefGoogle ScholarPubMed
Lewis, AJ and Southern, LL (2000) Swine Nutrition. Florida: CRC press. Copyright, p. 1032.CrossRefGoogle Scholar
Liao, B, Zhang, K, Ding, X, Xu, Z and Bai, S (2011) Effects of dietary supplementation with 25-OH-D3 on antibody and cytokine levels in serum and intestinal contents of weanling pigs with or without rotavirus challenge. Chinese Journal of Animal Nutrition 23, 34–42.Google Scholar
Lin, Y, Lv, G, Dong, HJ, Wu, D, Tao, ZY, Xu, SY, Che, LQ, Fang, ZF, Bai, SP, Feng, B, Li, J and Xu, XY (2017) Effects of the different levels of dietary vitamin D on boar performance and semen quality. Livestock Science 203, 63–68.CrossRefGoogle Scholar
Mahon, BD, Wittke, A, Weaver, V and Cantorna, MT (2003) The targets of vitamin D depend on the differentiation and activation status of CD4 positive T cells. Journal of Cellular Biochemistry 89, 922–932.CrossRefGoogle ScholarPubMed
Meuter, A, Thoby, JM, Lichou, JY and Renouf, B (2016a) Modulation role of dietary 25-hydroxycholecalciferol on immune response of weanling piglets. Journées de la Recherche Porcine en France 48, 347–348.Google Scholar
Meuter, A, Thoby, JM, Lichou, JY and Renouf, B (2016b) Effect of dietary 25-hydroxycholecalciferol on performance of gestating and lactating sows and their litters. Journées de la Recherche Porcine en France 48, 153–154.Google Scholar
Mizwicki, MT and Norman, AW (2009) The vitamin D sterol-vitamin D receptor ensemble model offers unique insights into both genomic and rapid-response signaling. Science Signaling 2, 1–15.CrossRefGoogle ScholarPubMed
Molnár, F, Sigüeiro, R, Sato, Y, Araujo, C, Schuster, I, Antony, P, Peluso, J, Muller, C, Mouriño, A, Moras, D and Rochel, N (2011) 1α25(OH)2-3-epi-vitamin D3 a natural physiological metabolite of vitamin D3: its synthesis biological activity and crystal structure with its receptor. PLoS ONE 6, 2–3.CrossRefGoogle Scholar
NRC (1998) Nutrient Requirements of Swine. Washington: National Academies Press, Copyright, p. 211.Google Scholar
NRC (2012) Nutrient Requirements of Swine. Washington: National Academies Press, Copyright, p. 424.Google Scholar
O'Brien, MA and Jackson, MW (2012) Vitamin D and the immune system: beyond rickets. Veterinary Journal 194, 27–33.CrossRefGoogle ScholarPubMed
Palmer, MT, Lee, YK, Maynard, CL, Oliver, JR, Bikle, DD, Jetten, AM and Weaver, CT (2011) Lineage-specific effects of 125-dihydroxyvitamin D3 on the development of effector CD4 T cells. Journal of Biological Chemistry 286, 997–1004.CrossRefGoogle Scholar
Raimundo, FV, Lang, MAB, Scopel, L, Marcondes, NA, Araújo, MGA, Faulhaber, GAM and Furlanetto, TW (2015) Effect of fat on serum 25-hydroxyvitamin D levels after a single oral dose of vitamin D in young healthy adults: a double-blind randomized placebo-controlled study. European Journal of Nutrition 54, 391–396.CrossRefGoogle ScholarPubMed
Regassa, A, Adhikari, R, Nyachoti, CM and Kim, WK (2015) Effects of 25-(OH)D3 on fecal Ca and P excretion bone mineralization Ca and P transporter mRNA expression and performance in growing female pigs. Journal of Environmental Science and Health 50, 293–299.CrossRefGoogle ScholarPubMed
Sadarangani, SP, Whitaker, JA and Poland, GA (2015) ‘Let there be light’: the role of vitamin D in the immune response to vaccines. Expert Review of Vaccines 14, 1427–1440.CrossRefGoogle Scholar
Saddoris, KL, Fleet, JC and Radcliffe, JS (2019) The effect of dietary vitamin D supplementation on sodium-dependent phosphate uptake and expression of NaPi-IIb in the small intestine of weanling pigs. Journal of Animal Science. doi: 10.1093/jas/skz106, Epub ahead of print.CrossRefGoogle ScholarPubMed
Shahrokhi, SZ, Ghaffari, F and Kazerouni, F (2016) Role of vitamin D in female reproduction. Clinica Chimica Acta 455, 33–38.CrossRefGoogle ScholarPubMed
Sherman, MH, Yu, RT, Engle, DD, Ding, N, Atkins, AR, Tiriac, H, Collisson, EA, Connor, F, Van Dyke, T, Kozlov, S, Martin, P, Tseng, TW, Dawson, DW, Donahue, TR, Masamune, A, Shimosegawa, T, Apte, MV, Wilson, JS, Ng, B, Lau, SL, Gunton, JE, Wahl, GM, Hunter, T, Drebin, JA, O'Dwyer, PJ, Liddle, C, Tuveson, DA, Downes, M and Evans, RM (2014) Vitamin D receptor-mediated stromal reprogramming suppresses pancreatitis and enhances pancreatic cancer therapy. Cell 159, 80–93.CrossRefGoogle ScholarPubMed
Sugiyama, T, Kusuhara, S, Chung, TK, Yonekura, H, Azem, E and Hayakawa, T (2013) Effects of 25-hydroxy-cholecalciferol on the development of osteochondrosis in swine. Animal Science Journal 84, 341–349.CrossRefGoogle ScholarPubMed
Thayer, MT, Nelssen, JL, Langemeier, AJ, Morton, J, Gonzales, JM, Kruger, SR, Ou, Z, Makowski, AJ and Bergstrom, JR (2018) The effects of maternal dietary supplementation of cholecalciferol (vitamin D3) and 25(OH)D3 on sow and progeny performance. Translational Animal Science 3, 692–708.CrossRefGoogle Scholar
Tian, G, Liang, X, Chen, D, Mao, X, Yu, J, Zheng, P, He, J, Huang, Z and Yu, B (2016) Vitamin D3 supplementation alleviates rotavirus infection in pigs and IPEC-J2 cells via regulating the autophagy signaling pathway. The Journal of Steroid Biochemistry and Molecular Biology 163, 157–163.CrossRefGoogle ScholarPubMed
von Rosenberg, SJ, Weber, GM, Erhardt, A, Höller, U, Wehr, UA and Rambeck, WA (2016) Tolerance evaluation of overdosed dietary levels of 25-hydroxyvitamin D3 in growing piglets. Journal of Animal Physiology and Animal Nutrition 100, 371–380.CrossRefGoogle ScholarPubMed
Waterhouse, M, Hope, B, Krause, L, Morrison, M, Protani, MM, Zakrzewski, M and Neale, RE (2018) Vitamin D and the gut microbiome: a systematic review of in vivo studies. European Journal of Nutrition 58, 2895–2910.CrossRefGoogle ScholarPubMed
Weber, GM, Witschi, AKM, Wenk, C and Martens, H (2014) Triennial growth symposium-effects of dietary 25-hydroxycholecalciferol and cholecalciferol on blood vitamin D and mineral status bone turnover milk composition and reproductive performance of sows. Journal of Animal Science 92, 899–909.CrossRefGoogle ScholarPubMed
Wei, D, Dong, H, Lyu, G, Wu, D, Xu, S, Fang, Z, Che, L, Feng, B, Li, J and Lin, Y (2017) Effect of dietary vitamin D forms on reproductive performance of boars. Chinese Journal of Animal Nutrition 29, 4323–4333.Google Scholar
Wei, Z, Yoshihara, E, He, N, Hah, N, Fan, W, Pinto, AFM, Huddy, T, Wang, Y, Ross, B, Estepa, G, Dai, Y, Ding, N, Sherman, MH, Fang, S, Zhao, X, Liddle, C, Atkins, AR, Yu, RT, Downes, M and Evans, RM (2018) Vitamin D switches BAF complexes to protect β cells. Cell 173, 1–15.CrossRefGoogle ScholarPubMed
Wilborn, BS, Kerth, CR, Owsley, WF, Jones, WR and Frobish, LT (2004) Improving pork quality by feeding supranutritional concentrations of vitamin D3. Journal of Animal Science 82, 218–224.CrossRefGoogle ScholarPubMed
Witschi, AKM, Liesegang, A, Gebert, S, Weber, GM and Wenk, C (2011) Effect of source and quantity of dietary vitamin D in maternal and creep diets on bone metabolism and growth in piglets. Journal of Animal Science 89, 1844–1852.CrossRefGoogle Scholar
Wu, S, Zhang, YG, Lu, R, Xia, Y, Zhou, D, Petrof, EO, Claud, EC, Chen, D, Chang, EB, Carmeliet, G and Sun, J (2015) Intestinal epithelial vitamin D receptor deletion leads to defective autophagy in colitis. Gut 64, 1082–1094.CrossRefGoogle ScholarPubMed
Yang, J, Tian, G, Chen, D, Zheng, P, Yu, J, Mao, X, He, J, Luo, Y, Luo, J, Huang, Z and Yu, B (2019) Effects of dietary 25-hydroxyvitamin D3 supplementation on growth performance immune function and antioxidative capacity in weaned piglets. Archives of Animal Nutrition 73, 44–51.CrossRefGoogle ScholarPubMed
Yang, P, Wang, HK, Li, LX and Ma, YX (2020) The strategies for the supplementation of vitamins and trace minerals in pig production: surveying major producers in China. Asian-Australasian Journal of Animal Science. doi: 10.5713/ajas.20.0521, Epub ahead of print.Google ScholarPubMed
Zhang, JY, Bae, JE, Jeong, YJ and Kim, IH (2017) Impact of 25-hydroxyvitamin D3 on productive performance of gestating sows. Korean Journal of Agricultural Science 44, 254–260.Google Scholar
Zhao, Y, Yu, B, Mao, X, He, J, Huang, Z, Zheng, P, Yu, J, Han, G, Liang, X and Chen, D (2014) Dietary vitamin D supplementation attenuates immune responses of pigs challenged with rotavirus potentially through the retinoic acid-inducible gene I signalling pathway. British Journal of Nutrition 112, 381–389.CrossRefGoogle ScholarPubMed
Zhao, Y, Yu, B, Mao, X, He, J, Huang, Z, Zheng, P, Yu, J, Han, G, Liang, X and Chen, D (2015) Effect of 25-hydroxyvitamin D3 on rotavirus replication and gene expressions of RIG-I signalling molecule in porcine rotavirus–infected IPEC-J2 cells. Archives of Animal Nutrition 69, 227–235.CrossRefGoogle ScholarPubMed
Zhou, H, Chen, Y, Lv, G, Zhuo, Y, Lin, Y, Feng, B, Fang, Z, Che, L, Li, J, Xu, S and Wu, D (2016a) Improving maternal vitamin D status promotes prenatal and postnatal skeletal muscle development of pig offspring. Nutrition (Burbank, Los Angeles County, Calif.) 32, 1144–1152.CrossRefGoogle Scholar
Zhou, H, Chen, Y, Zhuo, Y, Lv, G, Lin, Y, Feng, B, Fang, Z, Che, L, Li, J, Xu, S and Wu, D (2016b) Effects of 25-hydroxycholecalciferol supplementation in maternal diets on milk quality and serum bone status markers of sows and bone quality of piglets. Animal Science Journal 88, 476–483.CrossRefGoogle Scholar
Zhu, J and Deluca, HF (2012) Vitamin D 25-hydroxylase–four decades of searching, are we there yet? Archives of Biochemistry and Biophysics 523, 30–36.CrossRefGoogle ScholarPubMed
Zhu, JG, Ochalek, JT, Kaufmann, M, Jones, G and DeLuca, HF (2013) CYP2R1 is a major but not exclusive contributor to 25-hydroxyvitamin D production in vivo. Proceedings of the National Academy of Sciences USA 110, 15650–15655.CrossRefGoogle Scholar
Zimmermann, P and Curtis, N (2019) Factors that influence the immune response to vaccination. Clinical Microbiology Reviews 32, 1–50.CrossRefGoogle ScholarPubMed