No CrossRef data available.
Article contents
The amino acid sensor methionyl-tRNA synthetase is required for methionine-induced milk protein synthesis in a domestic pigeon model
Published online by Cambridge University Press: 03 June 2024
Abstract
This study was conducted to investigate whether methionyl-tRNA synthetase (MetRS) is a mediator of methionine (Met)-induced crop milk protein synthesis via the janus kinase 2 (JAK2)/signal transducer and activator of transcription 5 (STAT5) signalling pathway in breeding pigeons. In Experiment 1, a total of 216 pairs of breeding pigeons were divided into three groups (control, Met-deficient, and Met-rescue groups). In Experiments 2 and 3, forty pairs of breeding pigeons from each experiment were allocated into four groups. The second experiment included a control group and three MetRS inhibitor (REP8839) groups. The third experiment included a Met-deficient group, Met-sufficient group, REP8839 + Met-deficient group and REP8839 + Met-sufficient group. Experiment 1 showed that Met supplementation increased crop development, crop milk protein synthesis, the protein expression of MetRS and JAK2/STAT5 signalling pathway, and improved squab growth. Experiment 2 showed that crop development, crop milk protein synthesis and the protein expression of MetRS and the JAK2/STAT5 signalling pathway were decreased, and squab growth was inhibited by the injection of 1·0 mg/kg body weight REP8839, which was the selected dose for the third experiment. Experiment 3 showed that Met supplementation increased crop development, crop milk protein synthesis and the expression of MetRS and JAK2/STAT5 signalling pathway and rescued squab growth after the injection of REP8839. Moreover, the co-immunoprecipitation results showed that there was an interaction between MetRS and JAK2. Taken together, these findings indicate that MetRS mediates Met-induced crop milk protein synthesis via the JAK2/STAT5 signalling pathway, resulting in improved squab growth in breeding pigeons.
- Type
- Research Article
- Information
- Copyright
- © The Author(s), 2024. Published by Cambridge University Press on behalf of The Nutrition Society
References
Sales, J & Janssens, G (2003) Nutrition of the domestic pigeon (Columba livia domestica). World’s Poult Sci J 59, 221–232.Google Scholar
Xie, W, Fu, Z, Pan, N, et al. (2019) Leucine promotes the growth of squabs by increasing crop milk protein synthesis through the TOR signaling pathway in the domestic pigeon (Columba livia). Poult Sci 98, 5514–5524.Google Scholar
Hu, XC, Gao, CQ, Wang, XH, et al. (2016) Crop milk protein is synthesized following activation of the IRS1/Akt/TOR signaling pathway in the domestic pigeon (Columba livia). Br Poult Sci 2016, 855–862.Google Scholar
Oftedal, OT (2012) The evolution of milk secretion and its ancient origins. Animal 6, 355–368.Google Scholar
Luo, C, Zhao, S, Zhang, M, et al. (2018) SESN2 negatively regulates cell proliferation and casein synthesis by inhibition the amino acid-mediated mTORC1 pathway in cow mammary epithelial cells. Sci Rep 8, 3912.Google Scholar
Dai, W, White, R, Liu, J, et al. (2018) Seryl-tRNA synthetase-mediated essential amino acids regulate β-casein synthesis via cell proliferation and mammalian target of rapamycin (mTOR) signaling pathway in bovine mammary epithelial cells. J Dairy Sci 101, 10456–10468.Google Scholar
Bionaz, M & Loor, JJ (2011) Gene networks driving bovine mammary protein synthesis during the lactation cycle. Bioinform. Bio. Insights 5, 83–98.Google Scholar
Yang, JX, Wang, CH, Xu, QB, et al. (2015) Methionyl-Methionine promotes α-s1 casein synthesis in bovine mammary gland explants by enhancing intracellular substrate availability and activating JAK2-STAT5 and mTOR-mediated signaling pathways. J Nutr 145, 1748–1753.Google Scholar
Brosnan, JT, Brosnan, ME, Bertolo, RF, et al. (2007) Methionine: a metabolically unique amino acid. Livest Sci 11, 2–7.Google Scholar
Wang, C, Liu, H, Wang, Y, et al. (2010) Effects of dietary supplementation of methionine and lysine on milk production and nitrogen utilization in dairy cows. J Dairy Sci 93, 3661–3670.Google Scholar
Kim, JE & Lee, HG (2021) Amino acids supplementation for the milk and milk protein production of dairy cows. Animals 11, 2118.Google Scholar
McFadden, J, Girard, C, Tao, S, et al. (2020) Symposium review: one-carbon metabolism and methyl donor nutrition in the dairy cow. J Dairy Sci 103, 5668–5683.Google Scholar
Zhong, C, Zhang, Y, Pan, N, et al. (2022) Dietary DL-methionine replacement by a novel DL-methionyl-DL-methionine dipeptide increases milk protein synthesis in breeding pigeons and improves the growth performance of squabs. Anim Feed Sci Tech 292, 115420.Google Scholar
Nan, X, Bu, D, Li, X, et al. (2014) Ratio of lysine to methionine alters expression of genes involved in milk protein transcription and translation and mTOR phosphorylation in bovine mammary cells. Physiol Genomics 46, 268–275.Google Scholar
Hou, X, Jiang, M, Zhou, J, et al. (2020) Examination of methionine stimulation of gene expression in dairy cow mammary epithelial cells using RNA-sequencing. J Dairy Res 87, 226–231.Google Scholar
Chen, M, Pan, N, Wang, X, et al. (2020) Methionine promotes crop milk protein synthesis through the JAK2-STAT5 signaling during lactation of domestic pigeons (Columba livia). Food Funct 11, 10786–10798.Google Scholar
Yao, P & Fox, PL (2020) Aminoacyl-tRNA synthetases in cell signaling. In The Enzymes, pp. 243–275 [Pouplana, LR and Kaguni, LS, editors]. Cambridge: Academic Press.Google Scholar
Yu, YC, Han, JM & Kim, S (2021) Aminoacyl-tRNA synthetases and amino acid signaling. Biochim Biophys Acta Mol Cell Res 1868, 118889.Google Scholar
Luo, C, Qi, H, Huang, X, et al. (2019) GlyRS is a new mediator of amino acid-induced milk synthesis in bovine mammary epithelial cells. J Cell Physiol 234, 2973–2983.Google Scholar
Dai, W, Zhao, F, Liu, J, et al. (2020) Seryl-tRNA synthetase is involved in methionine stimulation of β-casein synthesis in bovine mammary epithelial cells. Br J Nutr 123, 489–498.Google Scholar
Lin, X, Li, S, Zou, Y, et al. (2018) Lysine stimulates protein synthesis by promoting the expression of ATB0,+ and activating the mTOR pathway in bovine mammary epithelial cells. J Nutr 148, 1426–1433.Google Scholar
Zhang, Y, Li, F, Lu, Z, et al. (2023) L-Malic acid facilitates stem cell-driven intestinal epithelial renewal through the amplification of β-catenin signaling by targeting Frizzled7 in chicks. J Agric Food Chem 71, 13079–13091.Google Scholar
Zhong, C, Tong, D, Zhang, Y, et al. (2022) DL-methionine and DL-methionyl-DL-methionine increase intestinal development and activate Wnt/β-catenin signaling activity in domestic pigeons (Columba livia). Poult Sci 101, 101644.Google Scholar
Jariyahatthakij, P, Chomtee, B, Poeikhampha, T, et al. (2018) Effects of adding methionine in low-protein diet and subsequently fed low-energy diet on productive performance, blood chemical profile, and lipid metabolism-related gene expression of broiler chickens. Poult Sci 97, 2021–2033.Google Scholar
Liu, Y, Wang, D, Zhao, L, et al. (2022) Effect of methionine deficiency on the growth performance, serum amino acids concentrations, gut microbiota and subsequent laying performance of layer chicks. Front Vet Sci 9, 878107.Google Scholar
Wu, Y, Tang, J, Cao, J, et al. (2021) Effect of dietary L-methionine supplementation on growth performance, carcass traits, and plasma parameters of starter pekin ducks at different dietary energy levels. Animals 11, 144.Google Scholar
Fagundes, NS, Milfort, MC, Williams, SM, et al. (2020) Dietary methionine level alters growth, digestibility, and gene expression of amino acid transporters in meat-type chickens. Poult Sci 99, 67–75.Google Scholar
Wathes, D, Fenwick, M, Cheng, Z, et al. (2007) Influence of negative energy balance on cyclicity and fertility in the high producing dairy cow. Theriogenology 68, S232–41.Google Scholar
Reda, FM, Swelum, AA, Hussein, EO, et al. (2020) Effects of varying dietary DL-methionine levels on productive and reproductive performance, egg quality, and blood biochemical parameters of quail breeders. Animals 10, 1839.Google Scholar
Gauthier, R, Largouët, C, Gaillard, C, et al. (2019) Dynamic modeling of nutrient use and individual requirements of lactating sows. J Anim Sci 97, 2822–2836.Google Scholar
Guan, X, Pettigrew, J, Ku, P, et al. (2004) Dietary protein concentration affects plasma arteriovenous difference of amino acids across the porcine mammary gland. J Anim Sci 82, 2953–2963.Google Scholar
Moll, R, Divo, M & Langbein, L (2008) The human keratins: biology and pathology. Histochem Cell Biol 129, 705–733.Google Scholar
Li, X, Dong, X, Xue, Y, et al. (2014) Increased expression levels of E-cadherin, cytokeratin 18 and 19 observed in preeclampsia were not correlated with disease severity. Placenta 35, 625–631.Google Scholar
Boutinaud, M, Guinard-Flament, J & Jammes, H (2004) The number and activity of mammary epithelial cells, determining factors for milk production. Reprod Nutr Dev 44, 499–508.Google Scholar
Zhu, J, Xie, P, Zheng, M, et al. (2023) Dynamic changes in protein concentrations of keratins in crop milk and related gene expression in pigeon crops during different incubation and chick rearing stages. Br Poult Sci 64, 100–109.Google Scholar
Yang, J, Xiong, L, Wang, R, et al. (2015)
In vitro expression of cytokeratin 18, 19 and tube formation of adipose-derived stem cells induced by the breast epithelial cell line HBL-100. J Cell Mol Med 19, 2827–2831.Google Scholar
Gillespie, MJ, Haring, VR, McColl, KA, et al. (2011) Histological and global gene expression analysis of the ‘lactating’ pigeon crop. BMC Genom 12, 452.Google Scholar
Bhat, MY, Dar, TA & Singh, LR (2016) Casein proteins: structural and functional aspects. In Milk Proteins-From Structure to Biological Properties and Health Aspects, pp. 64187 Gigli, I, editor. Rijeka: InTech.Google Scholar
Jin, C, He, Y, Jiang, S, et al. (2023) Chemical composition of pigeon crop milk and factors affecting its production: a review. Poult Sci 102, 102681.Google Scholar
Tian, M, Qi, Y, Zhang, X, et al. (2020) Regulation of the JAK2-STAT5 pathway by signaling molecules in the mammary gland. Front Cell Dev Biol 8, 604896.Google Scholar
Zhang, M, Zhao, S, Wang, S, et al. (2018) D-Glucose and amino acid deficiency inhibits casein synthesis through JAK2/STAT5 and AMPK/mTOR signaling pathways in mammary epithelial cells of dairy cows. J Dairy Sci 101, 1737–1746.Google Scholar
Kim, WS, Kim, MJ, Kim, DO, et al. (2017) Suppressor of cytokine signaling 2 negatively regulates NK cell differentiation by inhibiting JAK2 activity. Sci Rep 7, 46153.Google Scholar
Huang, YL, Zhao, F, Luo, CC, et al. (2013) SOCS3-mediated blockade reveals major contribution of JAK2/STAT5 signaling pathway to lactation and proliferation of dairy cow mammary epithelial cells in vitro. Molecules 18, 12987–13002.Google Scholar
Chen, Q, Zhao, F, Ren, Y, et al. (2020) Parenterally delivered methionyl-methionine dipeptide during pregnancy enhances mammogenesis and lactation performance over free methionine by activating PI3K-AKT signaling in methionine-deficient mice. J Nutr 150, 1186–1195.Google Scholar
Zhou, J, Yue, S, Xue, B, et al. (2021) Enhanced supply of methionine regulates protein synthesis in bovine mammary epithelial cells under hyperthermia condition. J Anim Sci Technol 63, 1126–1141.Google Scholar
Ochsner, UA, Sun, X, Jarvis, T, et al. (2007) Aminoacyl-tRNA synthetases: essential and still promising targets for new anti-infective agents. Expert opin Invest Drugs 16, 573–593.Google Scholar
Ochsner, UA, Young, CL, Stone, KC, et al. (2005) Mode of action and biochemical characterization of REP8839, a novel inhibitor of methionyl-tRNA synthetase. Antimicrob Agents Chemother 49, 4253–4262.Google Scholar
Green, LS, Bullard, JM, Ribble, W, et al. (2009) Inhibition of methionyl-tRNA synthetase by REP8839 and effects of resistance mutations on enzyme activity. Antimicrob Agents Chemother 53, 86–94.Google Scholar
Wang, L, Lin, Y, Bian, Y, et al. (2014) Leucyl-tRNA synthetase regulates lactation and cell proliferation via mTOR signaling in dairy cow mammary epithelial cells. Int J Mol Sci 15, 5952–5969.Google Scholar
Lu et al. supplementary material
Lu et al. supplementary material
File
22.8 KB