70
Views
0
CrossRef citations to date
0
Altmetric
Ruminants Nutrition and Feeding

Maternal N-carbamylglutamate and L-arginine supplementations improve foetal jejunal oxidation resistance, integrity and immune function in malnutrition sheep during pregnancy

, , , , , , , & show all
Pages 989-1001 | Received 23 Jan 2024, Accepted 25 Jun 2024, Published online: 04 Jul 2024

References

  • Baumgarten HD, Wright CM, Rossidis AC, Lawrence KM, Kim AG, Mejaddam AY, McGovern PE, Orr MN, Coons BE, Butt Z, et al. 2020. The extrauterine environment for neonatal development supports normal intestinal maturation and development. Cell Mol Gastroenterol Hepatol. 10(3):623–637. doi: 10.1016/j.jcmgh.2020.05.006.
  • Bayne JE, Edmondson MA. 2021. Diseases of the gastrointestinal system. In: Pugh DG, editor. Sheep, goat, and cervid medicine. Amsterdam: Elsevier; p. 63–96.
  • Berlinguer F, Porcu C, Molle G, Cabiddu A, Dattena M, Gallus M, Pasciu V, Succu S, Sotgiu FD, Paliogiannis P, et al. 2019. Circulating concentrations of key regulators of nitric oxide production in undernourished sheep carrying single and multiple fetuses. Animals. 10(1):65. doi: 10.3390/ani10010065.
  • Bodis J, Farkas B, Nagy B, Kovacs K, Sulyok E. 2022. The role of L-arginine-NO system in female reproduction: a narrative review. Int J Mol Sci. 23(23):14908. doi: 10.3390/ijms232314908.
  • Caleb I, Erlitz L, Telek V, Vecsernyés M, Sétáló G, Hardi P, Takács I, Jancsó G, Nagy T. 2021. Characterizing autophagy in the cold ischemic injury of small bowel grafts: evidence from rat jejunum. Metabolites. 11(6):396. doi: 10.3390/metabo11060396.
  • Cappelli K, Ferlisi F, Mecocci S, Maranesi M, Trabalza-Marinucci M, Zerani M, Dal BA, Acuti G. 2021. Dietary supplementation of olive mill waste water polyphenols in rabbits: evaluation of the potential effects on hepatic apoptosis, inflammation and metabolism through RT-qPCR approach. Animals. 11(10):2932. doi: 10.3390/ani11102932.
  • Castro-Rodríguez DC, Rodríguez-González GL, Menjivar M, Zambrano E. 2020. Maternal interventions to prevent adverse fetal programming outcomes due to maternal malnutrition: evidence in animal models. Placenta. 102:49–54. doi: 10.1016/j.placenta.2020.04.002.
  • Celik E, Taysi S, Sucu S, Ulusal H, Sevincler E, Celik A. 2019. Urotensin 2 and oxidative stress levels in maternal serum in pregnancies complicated by intrauterine growth restriction. Medicina. 55(7):328. doi: 10.3390/medicina55070328.
  • Chacher B, Wang D, Liu H, Liu J. 2012. Degradation of L-arginine and N-carbamoyl glutamate and their effect on rumen fermentation in vitro. Ital J Anim Sci. 11(4):e68. doi: 10.4081/ijas.2012.e68.
  • Chacher B, Zhu W, Ye J, Wang D, Liu J. 2014. Effect of dietary N-carbamoylglutamate on milk production and nitrogen utilization in high-yielding dairy cows. J Dairy Sci. 97(4):2338–2345. doi: 10.3168/jds.2013-7330.
  • Choksi YA, Reddy VK, Singh K, Barrett CW, Short SP, Parang B, Keating CE, Thompson JJ, Verriere TG, Brown RE, et al. 2018. BVES is required for maintenance of colonic epithelial integrity in experimental colitis by modifying intestinal permeability. Mucosal Immunol. 11(5):1363–1374. doi: 10.1038/s41385-018-0043-2.
  • Corzo C, Fuchsbichler A, Savencu I, Afonso Urich J, Zimmer A, Lochmann D, Reyer S, Salar-Behzadi S. 2021. Lipid-microparticles for pulmonary delivery of active pharmaceutical ingredients: impact of lipid crystallization on spray-drying processability. Int J Pharm. 610:121259. doi: 10.1016/j.ijpharm.2021.121259.
  • Crawford CK, Lopez Cervantes V, Quilici ML, Armién AG, Questa M, Matloob MS, Huynh LD, Beltran A, Karchemskiy SJ, Crakes KR, et al. 2022. Inflammatory cytokines directly disrupt the bovine intestinal epithelial barrier. Sci Rep. 12(1):14578. doi: 10.1038/s41598-022-18771-y.
  • Gu F, Zhu S, Hou J, Tang Y, Liu JX, Xu Q, Sun HZ. 2023. The hindgut microbiome contributes to host oxidative stress in postpartum dairy cows by affecting glutathione synthesis process. Microbiome. 11(1):87. doi: 10.1186/s40168-023-01535-9.
  • Hoffman ML, Reed SA, Pillai SM, Jones AK, McFadden KK, Zinn SA, Govoni KE. 2017. Physiology and endocrinology symposium: the effects of poor maternal nutrition during gestation on offspring postnatal growth and metabolism. J Anim Sci. 95(5):2222–2232. doi: 10.2527/jas.2016.1229.
  • Hu S, Han M, Rezaei A, Li D, Wu G, Ma X. 2017. L-arginine modulates glucose and lipid metabolism in obesity and diabetes. Curr Protein Pept Sci. 18(6):599–608. doi: 10.2174/1389203717666160627074017.
  • Kolic J, Sun WG, Johnson JD, Guess N. 2023. Amino acid-stimulated insulin secretion: a path forward in type 2 diabetes. Amino Acids. 55(12):1857–1866. doi: 10.1007/s00726-023-03352-8.
  • Kumar S, Ahmad A, Kushwaha N, Shokeen N, Negi S, Gautam K, Singh A, Tiwari P, Garg R, Agarwal R, et al. 2022. Selection of ideal reference genes for gene expression analysis in COVID-19 and mucormycosis. Microbiol Spectr. 10(6):e01656–e01622. doi: 10.1128/spectrum.01656-22.
  • Liu C, Feng X, Li Q, Wang Y, Li Q, Hua M. 2016. Adiponectin, TNF-α and inflammatory cytokines and risk of type 2 diabetes: a systematic review and meta-analysis. Cytokine. 86:100–109. doi: 10.1016/j.cyto.2016.06.028.
  • López-Sánchez LM, Aranda E, Rodríguez-Ariza A. 2020. Nitric oxide and tumor metabolic reprogramming. Biochem Pharmacol. 176:113769. doi: 10.1016/j.bcp.2019.113769.
  • Madsen JG, Pardo C, Kreuzer M, Bee G. 2017. Impact of dietary l-arginine supply during early gestation on myofiber development in newborn pigs exposed to intra-uterine crowding. J Anim Sci Biotechno. 8:1–12.
  • Martini S, Austin T, Aceti A, Faldella G, Corvaglia L. 2020. Free radicals and neonatal encephalopathy: mechanisms of injury, biomarkers, and antioxidant treatment perspectives. Pediatr Res. 87(5):823–833. doi: 10.1038/s41390-019-0639-6.
  • Meyer AM, Caton JS. 2016. Role of the small intestine in developmental programming: impact of maternal nutrition on the dam and offspring. Adv Nutr. 7(1):169–178. doi: 10.3945/an.115.010405.
  • National Research Council. 2007. Nutrient requirements of small ruminants: sheep, goats, cervids and new world camelids. Washington, DC: National Academies Press.
  • Nüse B, Holland T, Rauh M, Gerlach RG, Mattner J. 2023. L-arginine metabolism as pivotal interface of mutual host–microbe interactions in the gut. Gut Microbes. 15(1):2222961. doi: 10.1080/19490976.2023.2222961.
  • Pillai-Kastoori L, Schutz-Geschwender AR, Harford JA. 2020. A systematic approach to quantitative Western blot analysis. Anal Biochem. 593:113608. doi: 10.1016/j.ab.2020.113608.
  • Purdy PH, Spiller SF, McGuire E, McGuire K, Koepke K, Lake S, Blackburn HD. 2020. Critical factors for non-surgical artificial insemination in sheep. Small Ruminant Res. 191:106179. doi: 10.1016/j.smallrumres.2020.106179.
  • Rahman MS, Hossain KS, Das S, Kundu S, Adegoke EO, Rahman MA, Hannan MA, Uddin MJ, Pang MG. 2021. Role of insulin in health and disease: an update. Int J Mol Sci. 22(12):6403. doi: 10.3390/ijms22126403.
  • Russel A, Doney J, Gunn R. 1969. Subjective assessment of body fat in live sheep. J Agric Sci. 72(3):451–454. doi: 10.1017/S0021859600024874.
  • Sakuma C, Nakagawa M, Tomioka Y, Maruyama T, Entzminger K, Fleming JK, Shibata T, Kurosawa Y, Okumura CJ, Arakawa T, et al. 2022. Western blotting of native proteins from agarose gels. Biotechniques. 72(5):207–218. doi: 10.2144/btn-2022-0012.
  • Satterfield MC, Edwards AK, Bazer FW, Dunlap KA, Steinhauser CB, Wu G. 2021. Placental adaptation to maternal malnutrition. Reproduction. 162(4):R73–R83. doi: 10.1530/REP-21-0179.
  • Su W, Zhang H, Ying Z, Li Y, Zhou L, Wang F, Zhang L, Wang T. 2018. Effects of dietary L-methionine supplementation on intestinal integrity and oxidative status in intrauterine growth-retarded weanling piglets. Eur J Nutr. 57(8):2735–2745. doi: 10.1007/s00394-017-1539-3.
  • Suzuki T, Yamamoto M. 2015. Molecular basis of the Keap1–Nrf2 system. Free Radic Biol Med. 88(Pt B):93–100. doi: 10.1016/j.freeradbiomed.2015.06.006.
  • Tokuda S, Yu ASL. 2019. Regulation of epithelial cell functions by the osmolality and hydrostatic pressure gradients: a possible role of the tight junction as a sensor. Int J Mol Sci. 20(14):3513. doi: 10.3390/ijms20143513.
  • Weckman AM, McDonald CR, Baxter JAB, Fawzi WW, Conroy AL, Kain KC. 2019. Perspective: l -arginine and L-citrulline supplementation in pregnancy: a potential strategy to improve birth outcomes in low-resource settings. Adv Nutr. 10(5):765–777. doi: 10.1093/advances/nmz015.
  • Wittmeier P, Hummel S. 2022. Agarose gel electrophoresis to assess PCR product yield: comparison with spectrophotometry, fluorometry and qPCR. Biotechniques. 72(4):155–158. doi: 10.2144/btn-2021-0094.
  • Wu G, Bazer FW, Satterfield MC, Gilbreath KR, Posey EA, Sun Y. 2022. L-Arginine nutrition and metabolism in ruminants. In: Cole DA, Haresign W, editors. Recent advances in animal nutrition and metabolism. London: Butterworths; p. 177–206.
  • Xie S, Jiang L, Wang M, Sun W, Yu S, Turner JR, Yu Q. 2020. Cadmium ingestion exacerbates Salmonella infection, with a loss of goblet cells through activation of Notch signaling pathways by ROS in the intestine. J Hazard Mater. 391:122262. doi: 10.1016/j.jhazmat.2020.122262.
  • Xue Y, Guo C, Hu F, Zhu W, Mao S. 2019. Maternal undernutrition induces fetal hepatic lipid metabolism disorder and affects the development of fetal liver in a sheep model. Faseb J. 33(9):9990–10004. doi: 10.1096/fj.201900406R.
  • Ye C, Zeng X, Zhu J, Liu Y, Ye Q, Qiao S, Zeng X. 2017. Dietary N-carbamylglutamate supplementation in a reduced protein diet affects carcass traits and the profile of muscle amino acids and fatty acids in finishing pigs. J Agric Food Chem. 65(28):5751–5758. doi: 10.1021/acs.jafc.7b02301.
  • Yuan S, Wang Q, Li J, Xue J-C, Li Y, Meng H, Hou X-T, Nan J-X, Zhang Q-G. 2022. Inflammatory bowel disease: an overview of Chinese herbal medicine formula-based treatment. Chin Med. 17(1):74. doi: 10.1186/s13020-022-00633-4.
  • Zeng X, Huang Z, Mao X, Wang J, Wu G, Qiao S. 2012. N-carbamylglutamate enhances pregnancy outcome in rats through activation of the PI3K/PKB/mTOR signaling pathway. PLoS One. 7(7):e41192. doi: 10.1371/journal.pone.0041192.
  • Zhang H, Peng A, Guo S, Wang M, Loor JJ, Wang H. 2019a. Dietary N-carbamylglutamate and L-arginine supplementation improve intestinal energy status in intrauterine-growth-retarded suckling lambs. Food Funct. 10(4):1903–1914. doi: 10.1039/c8fo01618f.
  • Zhang H, Peng A, Yu Y, Guo S, Wang M, Wang H. 2019c. L-arginine protects ovine intestinal epithelial cells from lipopolysaccharide-induced apoptosis through alleviating oxidative stress. J Agric Food Chem. 67(6):1683–1690. doi: 10.1021/acs.jafc.8b06739.
  • Zhang H, Sun H, Peng A, Guo S, Wang M, Loor J, Wang H. 2019b. N-carbamylglutamate and L-arginine promote intestinal function in suckling lambs with intrauterine growth restriction by regulating antioxidant capacity via a nitric oxide–dependent pathway. Food Funct. 10(10):6374–6384. doi: 10.1039/c9fo01752f.
  • Zhang H, Sun L, Wang Z, Deng M, Zhang G, Guo R, Ma T, Wang F. 2016. Dietary N-carbamylglutamate and rumen-protected L-arginine supplementation ameliorate fetal growth restriction in undernourished ewes. J Anim Sci. 94(5):2072–2085. doi: 10.2527/jas.2015-9587.
  • Zhang H, Zheng Y, Zha X, Ma Y, Liu X, Elsabagh M, Wang H, Wang M. 2022. Dietary L-arginine or N-Carbamylglutamate alleviates colonic barrier injury, oxidative stress, and inflammation by modulation of intestinal microbiota in intrauterine growth-retarded suckling lambs. Antioxidants. 11(11):2251. doi: 10.3390/antiox11112251.
  • Zhu L, Luo F, Hu W, Han Y, Wang Y, Zheng H, Guo X, Qin J. 2018. Bacterial communities in the womb during healthy pregnancy. Front Microbiol. 9:2163. doi: 10.3389/fmicb.2018.02163.
  • Zihni C, Mills C, Matter K, Balda MS. 2016. Tight junctions: from simple barriers to multifunctional molecular gates. Nat Rev Mol Cell Biol. 17(9):564–580. doi: 10.1038/nrm.2016.80.