Dietary N-carbamylglutamate and rumen-protected l-arginine supplementation during intrauterine growth restriction in undernourished ewes improve fetal thymus development and immune function
Hao Zhang A B E , Fangfang Zhao A B , Haitao Nie C , Tiewei Ma C , Ziyu Wang C , Feng Wang C and Juan J. Loor D
+ Author Affiliations
- Author Affiliations
A Laboratory of Metabolic Manipulation of Herbivorous Animal Nutrition, College of Animal Science and Technology, Yangzhou University, #48, Weihui Road,Yangzhou 225009, P.R. China.
B Joint International Research Laboratory of Agriculture and Agri-product Safety, Yangzhou University, #48, Weihui Road, Yangzhou 225009, P.R. China.
C Jiangsu Engineering Technology Research Center of Mutton Sheep and Goat Industry, Nanjing Agricultural University, #1, Tongwei Road, Nanjing 210095, P.R. China.
D Department of Animal Sciences and Division of Nutritional Sciences, University of Illinois, Urbana, IL, USA.
E Corresponding author. Email: zhanghao_850220@126.com
Reproduction, Fertility and Development 30(11) 1522-1531 https://doi.org/10.1071/RD18047
Submitted: 8 February 2018 Accepted: 23 April 2018 Published: 13 July 2018
Abstract
The aims of the present study were to determine whether dietary supplementation with N-carbamylglutamate (NCG) and rumen-protected l-arginine (RP-Arg) to underfed Hu sheep would improve fetal thymus development and immune function. From Day 35 to Day 110 of gestation, 32 Hu ewes carrying twin fetuses were randomly allocated to one of four groups (n = 8 per group): 100% National Research Council (NRC)-recommended nutrient requirements (CON), 50% NRC recommendations (RES), 50% NRC recommendations supplemented with 20 g day−1 RP-Arg (RES+ARG), and 50% NRC recommendations supplemented with 5 g day−1 NCG (RES+NCG). Medullary thickness was increased (P < 0.05) in RES compared with CON ewes, but was reduced (P < 0.05) in both RES+ARG and RES+NCG ewes compared with RES ewes. There were no differences in superoxide dismutase and glutathione peroxidase activity or malondialdehyde levels in the RES+ARG and RES+NCG groups compared with the CON group (P > 0.05). Concentrations of IgA, interleukin (IL)-1β and IL-10 in fetal umbilical cord blood were reduced (P < 0.05) in RES compared with CON ewes, but were increased (P < 0.05) in both RES+ARG and RES+NCG ewes. Expression of Bax, Fas and p53 mRNA was increased (P < 0.05) in RES compared with CON ewes, but were reduced (P > 0.05) in both RES+ARG and RES+NCG ewes. These results indicate that dietary supplementation with NCG and RP-Arg could help alleviate the negative effects of intrauterine growth restriction on fetal thymus development and immune function.
Additional keywords: immune function, sheep.
References
Al-Gubory, K. H., Fowler, P. A., and Garrel, C. (2010). The roles of cellular reactive oxygen species, oxidative stress and antioxidants in pregnancy outcomes. Int. J. Biochem. Cell Biol. 42, 1634–1650.| The roles of cellular reactive oxygen species, oxidative stress and antioxidants in pregnancy outcomes.Crossref | GoogleScholarGoogle Scholar |
Assaily, W., Rubinger, D. A., Wheaton, K., Lin, Y., Ma, W., Xuan, W., Brown-Endres, L., Tsuchihara, K., Mak, T. W., and Benchimol, S. (2011). ROS-mediated p53 induction of Lpin1 regulates fatty acid oxidation in response to nutritional stress. Mol. Cell 44, 491–501.
| ROS-mediated p53 induction of Lpin1 regulates fatty acid oxidation in response to nutritional stress.Crossref | GoogleScholarGoogle Scholar |
Batistel, F., Arroyo, J. M., Garces, C. I. M., Trevisi, E., Parys, C., Ballou, M. A., and Loor, J. J. (2018). Ethyl-cellulose rumen-protected methionine alleviates inflammation and oxidative stress and improves neutrophil function during the periparturient period and early lactation in Holstein dairy cows. J. Dairy Sci. 101, 480–490.
| Ethyl-cellulose rumen-protected methionine alleviates inflammation and oxidative stress and improves neutrophil function during the periparturient period and early lactation in Holstein dairy cows.Crossref | GoogleScholarGoogle Scholar |
Bensaad, K., and Vousden, K. H. (2005). Savior and slayer: the two faces of p53. Nat. Med. 11, 1278–1279.
| Savior and slayer: the two faces of p53.Crossref | GoogleScholarGoogle Scholar |
Boehm, T., Scheu, S., Pfeffer, K., and Bleul, C. C. (2003). Thymic medullary epithelial cell differentiation, thymocyte emigration, and the control of autoimmunity require lympho-epithelial cross talk via LTbetaR. J. Exp. Med. 198, 757–769.
| Thymic medullary epithelial cell differentiation, thymocyte emigration, and the control of autoimmunity require lympho-epithelial cross talk via LTbetaR.Crossref | GoogleScholarGoogle Scholar |
Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248–254.
| A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.Crossref | GoogleScholarGoogle Scholar |
Briana, D. D., Liosi, S., Gourgiotis, D., Boutsikou, M., Marmarinos, A., Baka, S., Hassiakos, D., and Malamitsi-Puchner, A. (2012). Fetal concentrations of the growth factors TGF-alpha and TGF-beta1 in relation to normal and restricted fetal growth at term. Cytokine 60, 157–161.
| Fetal concentrations of the growth factors TGF-alpha and TGF-beta1 in relation to normal and restricted fetal growth at term.Crossref | GoogleScholarGoogle Scholar |
Chacher, B., Wang, D. M., Liu, H. Y., and Liu, J. X. (2012). Degradation of l-arginine and N-carbamoyl glutamate and their effect on rumen fermentation in vitro. Ital. J. Anim. Sci. 11, e68.
| Degradation of l-arginine and N-carbamoyl glutamate and their effect on rumen fermentation in vitro.Crossref | GoogleScholarGoogle Scholar |
Chacher, B., Zhu, W., Ye, J. A., Wang, D. M., and Liu, J. X. (2014). Effect of dietary N-carbamoylglutamate on milk production and nitrogen utilization in high-yielding dairy cows. J. Dairy Sci. 97, 2338–2345.
| Effect of dietary N-carbamoylglutamate on milk production and nitrogen utilization in high-yielding dairy cows.Crossref | GoogleScholarGoogle Scholar |
Coleman, J. W. (2001). Nitric oxide in immunity and inflammation. Int. Immunopharmacol. 1, 1397–1406.
| Nitric oxide in immunity and inflammation.Crossref | GoogleScholarGoogle Scholar |
Contreras, Y. M., Yu, X., Hale, M. A., Callaway, C. W., Bareyan, D., McKnight, R. A., Joss-Moore, L. A., Enioutina, E. Y., and Lane, R. H. (2011). Intrauterine growth restriction alters T-lymphocyte cell number and dual specificity phosphatase 1 levels in the thymus of newborn and juvenile rats. Pediatr. Res. 70, 123–129.
| Intrauterine growth restriction alters T-lymphocyte cell number and dual specificity phosphatase 1 levels in the thymus of newborn and juvenile rats.Crossref | GoogleScholarGoogle Scholar |
Eldem, T., Speiser, P., and Hincal, A. (1991). Optimization of spray-dried and -congealed lipid micropellets and characterization of their surface morphology by scanning electron microscopy. Pharm. Res. 8, 47–54.
| Optimization of spray-dried and -congealed lipid micropellets and characterization of their surface morphology by scanning electron microscopy.Crossref | GoogleScholarGoogle Scholar |
Gao, F., Liu, Y., Zhang, C., Zhang, Z., and Song, S. (2013). Effect of intrauterine growth restriction during late pregnancy on the growth performance, blood components, immunity and anti-oxidation capability of ovine fetus. Livest. Sci. 155, 435–441.
| Effect of intrauterine growth restriction during late pregnancy on the growth performance, blood components, immunity and anti-oxidation capability of ovine fetus.Crossref | GoogleScholarGoogle Scholar |
Gluckman, P. D., and Hanson, M. A. (2006). The consequences of being born small – an adaptive perspective. Horm. Res. 65, 5–14.
Gybina, A. A., and Prohaska, J. R. (2003). Increased rat brain cytochrome c correlates with degree of perinatal copper deficiency rather than apoptosis. J. Nutr. 133, 3361–3368.
| Increased rat brain cytochrome c correlates with degree of perinatal copper deficiency rather than apoptosis.Crossref | GoogleScholarGoogle Scholar |
He, Q., Ren, P. P., Kong, X. F., Xu, W. X., Tang, H. R., Yin, Y. L., and Wang, Y. L. (2011). Intrauterine growth restriction alters the metabonome of the serum and jejunum in piglets. Mol. Biosyst. 7, 2147–2155.
| Intrauterine growth restriction alters the metabonome of the serum and jejunum in piglets.Crossref | GoogleScholarGoogle Scholar |
Hervás, G., Frutos, P., Serrano, E., Mantecón, A. R., and Giráldez, F. J. (2000). Effect of tannic acid on rumen degradation and intestinal digestion of treated soya bean meals in sheep. J. Agric. Sci. 135, 305–310.
| Effect of tannic acid on rumen degradation and intestinal digestion of treated soya bean meals in sheep.Crossref | GoogleScholarGoogle Scholar |
Hu, L., Peng, X., Chen, H., Yan, C., Liu, Y., Xu, Q., Fang, Z., Lin, Y., Xu, S., Feng, B., Li, J., Wu, , and Che, L. (2017). Effects of intrauterine growth retardation and Bacillus subtilis PB6 supplementation on growth performance, intestinal development and immune function of piglets during the suckling period. Eur. J. Nutr. 56, 1753–1765.
| Effects of intrauterine growth retardation and Bacillus subtilis PB6 supplementation on growth performance, intestinal development and immune function of piglets during the suckling period.Crossref | GoogleScholarGoogle Scholar |
Johnson, M. L., Redmer, D. A., and Reynolds, L. P. (1997). Uterine growth, cell proliferation, and c-fos proto-oncogene expression throughout the estrous cycle in ewes. Biol. Reprod. 56, 393–401.
| Uterine growth, cell proliferation, and c-fos proto-oncogene expression throughout the estrous cycle in ewes.Crossref | GoogleScholarGoogle Scholar |
Lassala, A., Bazer, F. W., Cudd, T. A., Datta, S., Keisler, D. H., Satterfield, M. C., Spencer, T. E., and Wu, G. (2010). Parenteral administration of l-arginine prevents fetal growth restriction in undernourished ewes. J. Nutr. 140, 1242–1248.
| Parenteral administration of l-arginine prevents fetal growth restriction in undernourished ewes.Crossref | GoogleScholarGoogle Scholar |
Li, P., Yin, Y. L., Li, D. F., Kim, W. S., and Wu, G. Y. (2007). Amino acids and immune function. Br. J. Nutr. 98, 237–252.
| Amino acids and immune function.Crossref | GoogleScholarGoogle Scholar |
Liu, X. D., Wu, X., Yin, Y. L., Liu, Y. Q., Geng, M. M., Yang, H. S., Blachier, F., and Wu, G. Y. (2012). Effects of dietary l-arginine or N-carbamylglutamate supplementation during late gestation of sows on the miR-15b/16, miR-221/222, VEGFA and eNOS expression in umbilical vein. Amino Acids 42, 2111–2119.
| Effects of dietary l-arginine or N-carbamylglutamate supplementation during late gestation of sows on the miR-15b/16, miR-221/222, VEGFA and eNOS expression in umbilical vein.Crossref | GoogleScholarGoogle Scholar |
Liu, Y., He, S., Zhang, Y., Xia, W., Li, M., Zhang, C., and Gao, F. (2015). Effects of intrauterine growth restriction during late pregnancy on the development of the ovine fetal thymus and the T-lymphocyte subpopulation. Am. J. Reprod. Immunol. 74, 26–37.
| Effects of intrauterine growth restriction during late pregnancy on the development of the ovine fetal thymus and the T-lymphocyte subpopulation.Crossref | GoogleScholarGoogle Scholar |
Lomada, D., Liu, B., Coghlan, L., Hu, Y., and Richie, E. R. (2007). Thymus medulla formation and central tolerance are restored in IKKalpha−/− mice that express an IKKalpha transgene in keratin 5+ thymic epithelial cells. J. Immunol. 178, 829–837.
| Thymus medulla formation and central tolerance are restored in IKKalpha−/− mice that express an IKKalpha transgene in keratin 5+ thymic epithelial cells.Crossref | GoogleScholarGoogle Scholar |
Longley, D. B., Allen, W. L., McDermott, U., Wilson, T. R., Latif, T., Boyer, J., Lynch, M., and Johnston, P. G. (2004). The roles of thymidylate synthase and p53 in regulating Fas-mediated apoptosis in response to antimetabolites. Clin. Cancer Res. 10, 3562–3571.
| The roles of thymidylate synthase and p53 in regulating Fas-mediated apoptosis in response to antimetabolites.Crossref | GoogleScholarGoogle Scholar |
Lu, J., Moochhala, S., Kaur, C., and Ling, E. (2000). Changes in apoptosis-related protein (p53, Bax, Bcl-2 and Fos) expression with DNA fragmentation in the central nervous system in rats after closed head injury. Neurosci. Lett. 290, 89–92.
| Changes in apoptosis-related protein (p53, Bax, Bcl-2 and Fos) expression with DNA fragmentation in the central nervous system in rats after closed head injury.Crossref | GoogleScholarGoogle Scholar |
Maddocks, O. D. K., and Vousden, K. H. (2011). Metabolic regulation by p53. J. Mol. Med. 89, 237–245.
| Metabolic regulation by p53.Crossref | GoogleScholarGoogle Scholar |
Manley, N. R. (2000). Thymus organogenesis and molecular mechanisms of thymic epithelial cell differentiation. Semin. Immunol. 12, 421–428.
| Thymus organogenesis and molecular mechanisms of thymic epithelial cell differentiation.Crossref | GoogleScholarGoogle Scholar |
Martinou, J. C., and Green, D. R. (2001). Breaking the mitochondrial barrier. Nat. Rev. Mol. Cell Biol. 2, 63–67.
| Breaking the mitochondrial barrier.Crossref | GoogleScholarGoogle Scholar |
Mitsumori, K., Takegawa, K., Shimo, T., Onodera, H., Yasuhara, K., and Takahashi, M. (1996). Morphometric and immunohistochemical studies on atrophic changes in lympho-hematopoietic organs of rats treated with piperonyl butoxide or subjected to dietary restriction. Arch. Toxicol. 70, 809–814.
| Morphometric and immunohistochemical studies on atrophic changes in lympho-hematopoietic organs of rats treated with piperonyl butoxide or subjected to dietary restriction.Crossref | GoogleScholarGoogle Scholar |
Moura, C. S., Lollo, P. C. B., Morato, P. N., Risso, E. M., and Amaya-Farfan, J. (2017). Modulatory effects of arginine, glutamine and branched-chain amino acids on heat shock proteins, immunity and antioxidant response in exercised rats. Food Funct. 8, 3228–3238.
| Modulatory effects of arginine, glutamine and branched-chain amino acids on heat shock proteins, immunity and antioxidant response in exercised rats.Crossref | GoogleScholarGoogle Scholar |
National Research Council (NRC) (1985). ‘Nutrient Requirements of Sheep.’ 6th edn. (National Academy Press: Washington, DC.)
Osgerby, J. C., Wathes, D. C., Howard, D., and Gadd, T. S. (2002). The effect of maternal undernutrition on ovine fetal growth. J. Endocrinol 173, 131–141.
Osorio, J. S., Trevisi, E., Ji, P., Drackley, J. K., Luchini, D., Bertoni, G., and Loor, J. J. (2014). Biomarkers of inflammation, metabolism, and oxidative stress in blood, liver, and milk reveal a better immunometabolic status in peripartal cows supplemented with Smartamine M or MetaSmart. J. Dairy Sci. 97, 7437–7450.
| Biomarkers of inflammation, metabolism, and oxidative stress in blood, liver, and milk reveal a better immunometabolic status in peripartal cows supplemented with Smartamine M or MetaSmart.Crossref | GoogleScholarGoogle Scholar |
Paglia, D. E., and Valentine, W. N. (1967). Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J. Lab. Clin. Med. 70, 158–169.
Panchenko, L. F., Brusov, O. S., Gerasimov, A. M., and Loktaeva, T. D. (1975). Intramitochondrial localization and release of rat liver superoxide dismutase. FEBS Lett. 55, 84–87.
| Intramitochondrial localization and release of rat liver superoxide dismutase.Crossref | GoogleScholarGoogle Scholar |
Placer, Z. A., Cushman, L. L., and Johnson, B. C. (1966). Estimation of product of lipid peroxidation (malonyl dialdehyde) in biochemical systems. Anal. Biochem. 16, 359–364.
| Estimation of product of lipid peroxidation (malonyl dialdehyde) in biochemical systems.Crossref | GoogleScholarGoogle Scholar |
Russel, A. J. F., Doney, J. M., and Gunn, R. G. (1969). Subjective assessment of body fat in live sheep. J. Agric. Sci. 72, 451–454.
| Subjective assessment of body fat in live sheep.Crossref | GoogleScholarGoogle Scholar |
Satterfield, M. C., Dunlap, K. A., Keisler, D. H., Bazer, F. W., and Wu, G. (2013). Arginine nutrition and fetal brown adipose tissue development in nutrient-restricted sheep. Amino Acids 45, 489–499.
| Arginine nutrition and fetal brown adipose tissue development in nutrient-restricted sheep.Crossref | GoogleScholarGoogle Scholar |
Savino, W., and Dardenne, M. (2010). Nutritional imbalances and infections affect the thymus: consequences on T-cell-mediated immune responses. Proc. Nutr. Soc. 69, 636–643.
| Nutritional imbalances and infections affect the thymus: consequences on T-cell-mediated immune responses.Crossref | GoogleScholarGoogle Scholar |
Savino, W., Mendes-Da-Cruz, D. A., Smaniotto, S., Silva-Monteiro, E., and Villa-Verde, D. M. (2004). Molecular mechanisms governing thymocyte migration: combined role of chemokines and extracellular matrix. J. Leukoc. Biol. 75, 951–961.
| Molecular mechanisms governing thymocyte migration: combined role of chemokines and extracellular matrix.Crossref | GoogleScholarGoogle Scholar |
Scheaffer, A. N., Caton, J. S., Redmer, D. A., Arnold, D. R., and Reynolds, L. P. (2004). Effect of dietary restriction, pregnancy, and fetal type on intestinal cellularity and vascularity in Columbia and Romanov ewes. J. Anim. Sci. 82, 3024–3033.
| Effect of dietary restriction, pregnancy, and fetal type on intestinal cellularity and vascularity in Columbia and Romanov ewes.Crossref | GoogleScholarGoogle Scholar |
Seitan, V. C., Hao, B., Tachibana-Konwalski, K., Lavagnolli, T., Mira-Bontenbal, H., Brown, K. E., Teng, G., Carroll, T., Terry, A., Horan, K., Marks, H., Adams, D. J., Schatz, D. G., Aragon, L., Fisher, A. G., Krangel, M. S., Nasmyth, K., and Merkenschlager, M. (2011). A role for cohesin in T-cell-receptor rearrangement and thymocyte differentiation. Nature 476, 467–471.
| A role for cohesin in T-cell-receptor rearrangement and thymocyte differentiation.Crossref | GoogleScholarGoogle Scholar |
Tan, B., Yin, Y., Liu, Z., Tang, W., Xu, H., Kong, X., Li, X., Yao, K., Gu, W., Smith, S. B., and Wu, G. (2011). Dietary l-arginine supplementation differentially regulates expression of lipid-metabolic genes in porcine adipose tissue and skeletal muscle. J. Nutr. Biochem. 22, 441–445.
| Dietary l-arginine supplementation differentially regulates expression of lipid-metabolic genes in porcine adipose tissue and skeletal muscle.Crossref | GoogleScholarGoogle Scholar |
Van Loo, G., Saelens, X., van Gurp, M., MacFarlane, M., Martin, S. J., and Vandenabeele, P. (2002). The role of mitochondrial factors in apoptosis: a Russian roulette with more than one bullet. Cell Death Differ. 9, 1031–1042.
| The role of mitochondrial factors in apoptosis: a Russian roulette with more than one bullet.Crossref | GoogleScholarGoogle Scholar |
Vousden, K. H., and Prives, C. (2009). Blinded by the light: the growing complexity of p53. Cell 137, 413–431.
| Blinded by the light: the growing complexity of p53.Crossref | GoogleScholarGoogle Scholar |
Wu, G., Knabe, D. A., and Kim, S. W. (2004). Arginine nutrition in neonatal pigs. J. Nutr. 134, 2783S–S790S.
| Arginine nutrition in neonatal pigs.Crossref | GoogleScholarGoogle Scholar |
Wu, G., Bazer, F. W., Wallace, J. M., and Spencer, T. E. (2006). Board-invited review: intrauterine growth retardation: implications for the animal sciences. J. Anim. Sci. 84, 2316–2337.
| Board-invited review: intrauterine growth retardation: implications for the animal sciences.Crossref | GoogleScholarGoogle Scholar |
Wu, X., Yin, Y. L., Liu, Y. Q., Liu, X. D., Liu, Z. Q., Li, T. J., Huang, R. L., Ruan, Z., and Deng, Z. Y. (2012a). Effect of dietary arginine and N-carbamoylglutamate supplementation on reproduction and gene expression of eNOS, VEGFA and PlGF1 in placenta in late pregnancy of sows. Anim. Reprod. Sci. 132, 187–192.
| Effect of dietary arginine and N-carbamoylglutamate supplementation on reproduction and gene expression of eNOS, VEGFA and PlGF1 in placenta in late pregnancy of sows.Crossref | GoogleScholarGoogle Scholar |
Wu, X., Zhang, Y., Liu, Z., Li, T. J., and Yin, Y. L. (2012b). Effects of oral supplementation with glutamate or combination of glutamate and N-carbamylglutamate on intestinal mucosa morphology and epithelium cell proliferation in weanling piglets. J. Anim. Sci. 90, 337–339.
| Effects of oral supplementation with glutamate or combination of glutamate and N-carbamylglutamate on intestinal mucosa morphology and epithelium cell proliferation in weanling piglets.Crossref | GoogleScholarGoogle Scholar |
Xu, Y. Q., Guo, Y. W., Shi, B. L., Yan, S. M., and Guo, X. Y. (2018). Dietary arginine supplementation enhances the growth performance and immune status of broiler chickens. Livest. Sci. 209, 8–13.
| Dietary arginine supplementation enhances the growth performance and immune status of broiler chickens.Crossref | GoogleScholarGoogle Scholar |
Yin, J., Ren, W. K., Liu, G., Duan, J. L., Yang, G., Wu, L., Li, T. J., and Yin, Y. L. (2013a). Birth oxidative stress and the development of an antioxidant system in newborn piglets. Free Radic. Res. 47, 1027–1035.
| Birth oxidative stress and the development of an antioxidant system in newborn piglets.Crossref | GoogleScholarGoogle Scholar |
Yin, J., Ren, W. K., Wu, X. S., Yang, G., Wang, J., Li, T. J., and Su, D. D. (2013b). Oxidative stress-mediated signaling pathways: a review. J. Food Agric. Environ. 11, 132–139.
Yin, J., Wu, M. M., Xiao, H., Ren, W. K., Duan, J. L., Yang, G., Li, T. J., and Yin, Y. L. (2014). Development of an antioxidant system after early weaning in piglets. J. Anim. Sci. 92, 612–619.
| Development of an antioxidant system after early weaning in piglets.Crossref | GoogleScholarGoogle Scholar |
Yin, J., Duan, J. L., Cui, Z. J., Ren, W. K., Li, T. J., and Yin, Y. L. (2015a). Hydrogen peroxide-induced oxidative stress activates NF-κB and Nrf2/Keap1 signals and triggers autophagy in piglets. RSC Advances 5, 15479–15486.
| Hydrogen peroxide-induced oxidative stress activates NF-κB and Nrf2/Keap1 signals and triggers autophagy in piglets.Crossref | GoogleScholarGoogle Scholar |
Yin, J., Liu, M. F., Ren, W. K., Duan, J. L., Yang, G., Zhao, Y. R., Fang, R. J., Chen, L. X., Li, T. J., and Yin, Y. L. (2015b). Effects of dietary supplementation with glutamate and aspartate on diquat-induced oxidative stress in piglets. PLoS One 10, e0122893.
| Effects of dietary supplementation with glutamate and aspartate on diquat-induced oxidative stress in piglets.Crossref | GoogleScholarGoogle Scholar |
Zeng, X., Huang, Z., Mao, X., Wang, J., Wu, G., and Qiao, S. (2012). N-Carbamylglutamate enhances pregnancy outcome in rats through activation of the PI3K/PKB/mTOR signaling pathway. PLoS One 7, e41192.
| N-Carbamylglutamate enhances pregnancy outcome in rats through activation of the PI3K/PKB/mTOR signaling pathway.Crossref | GoogleScholarGoogle Scholar |
Zhan, X. A., Min, W., Zhao, R. Q., Lia, W. F., and Xua, Z. R. (2007). Effects of different selenium source on selenium distribution, loin quality and antioxidant status in finishing pigs. Anim. Feed Sci. Technol. 132, 202–211.
| Effects of different selenium source on selenium distribution, loin quality and antioxidant status in finishing pigs.Crossref | GoogleScholarGoogle Scholar |
Zhang, F., Zeng, X., Yang, F., Huang, Z., Liu, H., Ma, X., and Qiao, S. (2013). Dietary N-carbamylglutamate supplementation boosts intestinal mucosal immunity in Escherichia coli challenged piglets. PLoS One 8, e66280.
| Dietary N-carbamylglutamate supplementation boosts intestinal mucosal immunity in Escherichia coli challenged piglets.Crossref | GoogleScholarGoogle Scholar |
Zhang, H., Nie, H. T., Wang, Q., Wang, Z. Y., Zhang, Y. L., Guo, R. H., and Wang, F. (2015). Trace element concentrations and distributions in the main body tissues and the net requirements for maintenance and growth of Dorper × Hu lambs. J. Anim. Sci. 93, 2471–2481.
| Trace element concentrations and distributions in the main body tissues and the net requirements for maintenance and growth of Dorper × Hu lambs.Crossref | GoogleScholarGoogle Scholar |
Zhang, H., Sun, L., Wang, Z., Deng, M., Nie, H., Zhang, G., Ma, T., and Wang, F. (2016a). N-Carbamylglutamate and l-arginine improved maternal and placental development in underfed ewes. Reproduction 151, 623–635.
| N-Carbamylglutamate and l-arginine improved maternal and placental development in underfed ewes.Crossref | GoogleScholarGoogle Scholar |
Zhang, H., Sun, L. W., Wang, Z. Y., Deng, M. T., Zhang, G. M., Guo, R. H., Ma, T. W., and Wang, F. (2016b). Dietary-carbamylglutamate and rumen-protected-arginine supplementation ameliorate fetal growth restriction in undernourished ewes. J. Anim. Sci. 94, 2072–2085.
| Dietary-carbamylglutamate and rumen-protected-arginine supplementation ameliorate fetal growth restriction in undernourished ewes.Crossref | GoogleScholarGoogle Scholar |
Zhang, H., Dong, L., Wang, M., Yu, L., and Wang, H. (2018). Effects of dietary l-arginine and N-carbamylglutamate supplementation on intestinal integrity, immune function and oxidative status in intrauterine growth retarded suckling lambs. J. Agric. Food Chem. , .
| Effects of dietary l-arginine and N-carbamylglutamate supplementation on intestinal integrity, immune function and oxidative status in intrauterine growth retarded suckling lambs.Crossref | GoogleScholarGoogle Scholar |
Zhang, H., Nie, H., Wang, Z., and Wang, F. (2018a). The net iron, manganese, copper, and zinc requirements for maintenance and growth of Dorper × Hu ewe lambs. Ital. J. Anim. Sci. 1, 1–9.
Zhang, H., Sun, L. W., Wang, Z. Y., Ma, T. W., Deng, M. T., Wang, F., and Zhang, Y. L. (2018b). Energy and protein requirements for maintenance of Hu sheep during pregnancy. J. Integr. Agric. 17, 173–183.
| Energy and protein requirements for maintenance of Hu sheep during pregnancy.Crossref | GoogleScholarGoogle Scholar |
Zhou, Z., Garrow, T. A., Dong, X., Luchini, D. N., and Loor, J. J. (2017). Hepatic activity and transcription of betaine-homocysteine methyltransferase, methionine synthase, and cystathionine synthase in periparturient dairy cows are altered to different extents by supply of methionine and choline-3. J. Nutr. 147, 11–19.
| Hepatic activity and transcription of betaine-homocysteine methyltransferase, methionine synthase, and cystathionine synthase in periparturient dairy cows are altered to different extents by supply of methionine and choline-3.Crossref | GoogleScholarGoogle Scholar |
