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Stage-specific feed intake restriction differentially regulates placental traits and proteome of goats

  • Qiongxian Yan (a1) (a2), Juanzhi Xu (a1) (a3), Xiaosong Wu (a3) (a4), Dingding Su (a3) and Zhiliang Tan (a1) (a4)...
Abstract

A total of twenty-four healthy twin-bearing Liuyang black goats were allocated to two trials. In Trial 1, twelve goats received either the control diet (CG, n 6, 100 % feed) or restricted diet (RG, n 6, 60 % feed of CG) from gestation days 26 to 65 after synchronisation. In Trial 2, the remaining goats were randomly and equally divided into two treatments: CG and RG from days 95 to 125 of gestation. Placental traits, fetal weight, serum parameters, nitric oxide (NO), angiogenesis gene expression and cotyledon proteome were measured at the end of each trial. In early pregnancy, the total and relative weights of placenta, uterine caruncle and cotyledon, as well as fetus, were increased (P<0·05) in RG. The NO content in maternal serum was also increased (P<0·05) in RG. In all, fifty differentially expressed proteins were identified in cotyledon. The up-regulated proteins are related to proliferation and fission of trophoblast cell and the placenta angiogenesis. During the late pregnancy trial, placental weight was increased (P<0·05) in RG, but weight of the fetus was decreased (P<0·05). The capillary density in the cotyledon was also decreased (P<0·01). A total of fifty-eight proteins were differentially expressed in cotyledon. The up-regulated proteins in RG are related to placenta formation, blood flow regulation and embryonic development. These results indicated that feed intake restriction during gestation influenced the placental and fetal development in a stage-dependent manner. These findings have important implications for developing novel nutrient management strategies in goat production.

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Corresponding author
* Corresponding authors: Z. Tan, email zltan@isa.ac.cn; X. Wu, email wuxiaosong529@126.com
References
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1. Bell, AW & Ehrhardt, RA (2002) Regulation of placental nutrient transport and implications for fetal growth. Nutr Res Rev 15, 211230.
2. Barry, JS & Anthony, RV (2008) The pregnant sheep as a model for human pregnancy. Theriogenology 69, 5567.
3. Fowden, AL, Ward, JW, Wooding, FPB, et al. (2006) Programming placental nutrient transport capacity. J Physiol 572, 515.
4. Ward, JW, Forhead, AJ, Wooding, FBP, et al. (2006) Functional significance and cortisol dependence of the gross morphology of ovine placentomes during late gestation. Biol Reprod 74, 137145.
5. Sibley, CP, Brownbill, P, Dilworth, M, et al. (2010) Adaptation in placental nutrient supply to meet fetal growth demand: implications for programming. Placenta 31, S70S74.
6. Wooding, FB (1992) Current topic: the synepitheliochorial placenta of ruminants: binucleate cell fusions and hormone production. Placenta 13, 101113.
7. Igwebuike, UM & Ezeasor, DN (2013) The morphology of placentomes and formation of chorionic vinous trees in West African Dwarf goats (Capra hircus). Vet Arhiv 83, 313321.
8. Igwebuike, UM & Ezeasor, DN (2014) Morphological adaptations for histotrophic nutrition in the placenta of West African Dwarf goats. Slov Vet Res 51, 1119.
9. Igwebuike, UM & Ezeasor, DN (2012) Morphological assessment of placentomal trophoblastic epithelium in the placenta of West African Dwarf goats: a light and electron microscopic study. Anim Reprod Sci 136, 6168.
10. Meuris, S, Nagy, AM, Delognedesnoeck, J, et al. (1995) Temporal relationship between the human chorionic-gonadotropin peak and the establishment of intervillous blood-flow in early-pregnancy. Hum Reprod 10, 947950.
11. Babu, GJJ, Radhakrishna, KV, Ramalakshmi, BA, et al. (2008) Maternal nutrition in early pregnancy effects placental development. Placenta 29, A55A55.
12. Jauniaux, E, Jurkovic, D, Gulbis, B, et al. (1994) Investigation of the acid-base-balance of celomic and amniotic fluids in early human-pregnancy. Am J Obstet Gynecol 170, 13651369.
13. Genbacev, O, Joslin, R, Damsky, CH, et al. (1996) Hypoxia alters early gestation human cytotrophoblast differentiation/invasion in vitro and models the placental defects that occur in preeclampsia. J Clin Invest 97, 540550.
14. Rodesch, F, Simon, P, Donner, C, et al. (1992) Oxygen measurements in endometrial and trophoblastic tissues during early-pregnancy. Obstet Gynecol 80, 283285.
15. Burton, GJ & Fowden, AL (2012) Review: The placenta and developmental programming: balancing fetal nutrient demands with maternal resource allocation. Placenta 33, Suppl., S23S27.
16. LangleyEvans, SC, Phillips, GJ, Benediktsson, R, et al. (1996) Protein intake in pregnancy, placental glucocorticoid metabolism and the programming of hypertension in the rat. Placenta 17, 169172.
17. Spencer, NJ, Dickson, EJ, Hennig, GW, et al. (2006) Sensory elements within the circular muscle are essential for mechanotransduction of ongoing peristaltic reflex activity in guinea-pig distal colon. J Physiol 576, 519531.
18. Dwyer, CM, Calvert, SK, Farish, M, et al. (2005) Breed, litter and parity effects on placental weight and placentome number, and consequences for the neonatal behaviour of the lamb. Theriogenology 63, 10921110.
19. Konyali, A, Tolu, C, Das, G, et al. (2007) Factors affecting placental traits and relationships of placental traits with neonatal behaviour in goat. Anim Reprod Sci 97, 394401.
20. Gao, H, Yallampalli, U & Yallampalli, C (2013) Gestational protein restriction affects trophoblast differentiation. Front Biosci (Elite Ed) 5, 591601.
21. Rebelato, HJ, Esquisatto, MA, de Sousa Righi, EF, et al. (2016) Gestational protein restriction alters cell proliferation in rat placenta. J Mol Histol 47, 203211.
22. Rutland, CS, Latunde-Dada, AO, Thorpe, A, et al. (2007) Effect of gestational nutrition on vascular integrity in the murine placenta. Placenta 28, 734742.
23. Daniel, Z, Swali, A, Emes, R, et al. (2016) The effect of maternal undernutrition on the rat placental transcriptome: protein restriction up-regulates cholesterol transport. Genes Nutr 11, 27.
24. Perry, VE, Norman, ST, Owen, JA, et al. (1999) Low dietary protein during early pregnancy alters bovine placental development. Anim Reprod Sci 55, 1321.
25. Heasman, L, Clarke, L, Firth, K, et al. (1998) Influence of restricted maternal nutrition in early to mid gestation on placental and fetal development at term in sheep. Pediatr Res 44, 546551.
26. Osgerby, JC, Wathes, DC, Howard, D, et al. (2004) The effect of maternal undernutrition on the placental growth trajectory and the uterine insulin-like growth factor axis in the pregnant ewe. J Endocrinol 182, 89103.
27. Steyn, C, Hawkins, P, Saito, T, et al. (2001) Undernutrition during the first half of gestation increases the predominance of fetal tissue in late-gestation ovine placentomes. Eur J Obstet Gynecol Reprod Biol 98, 165170.
28. Redmer, DA, Luther, JS, Milne, JS, et al. (2009) Fetoplacental growth and vascular development in overnourished adolescent sheep at day 50, 90 and 130 of gestation. Reproduction 137, 749757.
29. Ehrhardt, RA & Bell, AW (1995) Growth and metabolism of the ovine placenta during mid-gestation. Placenta 16, 727741.
30. Wallace, JM, Bourke, DA & Aitken, RP (1999) Nutrition and fetal growth: paradoxical effects in the overnourished adolescent sheep. J Reprod Fertil Suppl 54, 385399.
31. Weidner, N, Folkman, J, Pozza, F, et al. (1992) Tumor angiogenesis: a new significant and independent prognostic indicator in early-stage breast carcinoma. J Natl Cancer Inst 84, 18751887.
32. Li, C, Tong, H, Yan, Q, et al. (2016) L-Theanine improves immunity by altering TH2/TH1 cytokine balance, brain neurotransmitters, and expression of phospholipase C in rat hearts. Med Sci Monit 22, 662669.
33. Livak, KJ & Schmittgen, TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25, 402408.
34. Zhang, T, Guo, Y, Guo, X, et al. (2013) Comparative proteomics analysis of placenta from pregnant women with intrahepatic cholestasis of pregnancy. PLOS ONE 8, e83281.
35. Redmer, DA, Milne, JS, Aitken, RP, et al. (2012) Decreasing maternal nutrient intake during the final third of pregnancy in previously overnourished adolescent sheep: Effects on maternal nutrient partitioning and feto-placental development. Placenta 33, 114121.
36. Morteza, A, Abdollahi, A & Bandarian, M (2012) Serum nitric oxide syntheses and lipid profile of the mothers with IUGR pregnancies uncomplicated with preeclampsia. Does insulin resistance matter? Gynecol Endocrinol 28, 139142.
37. Gouge, RC, Marshburn, P, Gordan, BE, et al. (1998) Nitric oxide as a regulator of embryonic development. Biol Reprod 58, 875879.
38. Dubey, PK, Tripathi, V, Singh, RP, et al. (2012) Expression of nitric oxide synthase isoforms in different stages of buffalo (Bubalus bubalis) ovarian follicles: effect of nitric oxide on in vitro development of preantral follicle. Theriogenology 77, 280291.
39. Maul, H, Longo, M, Saade, GR, et al. (2003) Nitric oxide and its role during pregnancy: from ovulation to delivery. Curr Pharm Des 9, 359380.
40. Sagar, P, Prasad, JK, Prasad, S, et al. (2012) Effect of L-arginine methyl ester (L-NAME) on hormonal profile and estrous cycle length in buffaloes (Bubalus bubalis). Trop Anim Health Prod 44, 16971702.
41. Madore, E, Harvey, N, Parent, J, et al. (2003) An aldose reductase with 20 alpha-hydroxysteroid dehydrogenase activity is most likely the enzyme responsible for the production of prostaglandin f2 alpha in the bovine endometrium. J Biol Chem 278, 1120511212.
42. Lacroix Pepin, N, Chapdelaine, P & Fortier, MA (2013) Evaluation of the prostaglandin F synthase activity of human and bovine aldo-keto reductases: AKR1A1s complement AKR1B1s as potent PGF synthases. Prostaglandins Other Lipid Mediat 106, 124132.
43. Rukosuev, VS (1992) Immunofluorescent localization of collagen type-I, type-Iii, type-Iv, type-V, fibronectin, laminin, entactin, and heparan-sulfate proteoglycan in human immature placenta. Experientia 48, 285287.
44. Saarela, J, Ylikarppa, R, Rehn, M, et al. (1998) Complete primary structure of two variant forms of human type XVIII collagen and tissue-specific differences in the expression of the corresponding transcripts. Matrix Biol 16, 319328.
45. Kitroser, E, Pomeranz, M, Shochet, GE, et al. (2012) The involvement of eukaryotic translation initiation factor 4E in extravillous trophoblast cell function. Placenta 33, 717724.
46. Ozmen, A, Unek, G, Kipmen-Korgun, D, et al. (2011) The expression of Akt and ERK1/2 proteins decreased in dexamethasone-induced intrauterine growth restricted rat placental development. J Mol Histol 42, 237249.
47. Wu, M, Komori, N, Qin, C, et al. (2008) Extracellular signal-regulated kinase (ERK) and protein kinase B (AKT) pathways involved in spinal cord stimulation (SCS)-induced vasodilation. Brain Res 1207, 7383.
48. Zheng, J, Wen, Y, Song, Y, et al. (2008) Activation of multiple signaling pathways is critical for fibroblast growth factor 2- and vascular endothelial growth factor-stimulated ovine fetoplacental endothelial cell proliferation. Biol Reprod 78, 143150.
49. Rout, UK & Dhossche, JM (2010) Liquid-diet with alcohol alters maternal, fetal and placental weights and the expression of molecules involved in integrin signaling in the fetal cerebral cortex. Int J Environ Res Public Health 7, 40234036.
50. Epple, H, Cremasco, V, Zhang, K, et al. (2008) Phospholipase Cgamma2 modulates integrin signaling in the osteoclast by affecting the localization and activation of Src kinase. Mol Cell Biol 28, 36103622.
51. Han, J, Li, L, Hu, J, et al. (2010) Epidermal growth factor stimulates human trophoblast cell migration through Rho A and Rho C activation. Endocrinology 151, 17321742.
52. Lin, JC & Tarn, WY (2009) RNA-binding motif protein 4 translocates to cytoplasmic granules and suppresses translation via argonaute2 during muscle cell differentiation. J Biol Chem 284, 3465834665.
53. Oh, SY, Hwang, JR, Lee, Y, et al. (2016) Isolation of basal membrane proteins from BeWo cells and their expression in placentas from fetal growth-restricted pregnancies. Placenta 39, 2432.
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British Journal of Nutrition
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