Abstract
The neonate with low birth weight (LBW) resulted from intrauterine growth retardation (IUGR) exists a substantial risk of postpartum death. Placental insufficiency is responsible for inadequate fetal growth; however, the pathological mechanisms of placental dysfunction-induced IUGR in pigs remain unclear. In this study, the characteristics of placental morphology, placental transcriptome, and cord serum metabolome were explored between the Kele piglets with LBW and the ones with normal birth weight (NBW). Results showed that LBW was a common occurrence in Kele piglets. The LBW placentas showed inferior villus development and lower villi density compared to NBW placentas. There were 1024 differentially expressed genes (DEGs) identified by transcriptome analysis between the LBW and NBW placentas, of which 218 and 806 genes were up- and down-regulated in the LBW placentas, respectively. PPI network analysis showed that ITGB2, CD4, IL6, ITGB3, LCK, RAC2, CD8A, JAK3, TYROBP, and CXCR4 were hub genes in all DEGs. From GO and KEGG enrichment analysis, DEGs were primarily enriched in immunological response, cell adhesion, immune response, cytokine-cytokine receptor interaction, and PI3K-Akt signaling pathway. By using metabolomic analysis, a total of 115 differential metabolites in the cord serum of LBW and NBW piglets were found, mostly linked to amino acid metabolism and sphingolipid metabolism. In comparison to NBW piglets, LBW piglets had lower levels of arginine, isoleucine, and aspartic acid in the cord. Taken together, these data revealed dysplasia of the placental villus, insufficient supply of nutrients, and abnormal immune function of the placenta may be associated with the occurrence and development of LBW in Kele pigs.
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References
Ao, Z., Liu, D., Zhao, C., Yue, Z., Shi, J., Zhou, R., Cai, G., Zheng, E., Li, Z., and Wu, Z., 2017. Birth weight, umbilical and placental traits in relation to neonatal loss in cloned pigs. Placenta, 57, 94-101. https://doi.org/10.1016/j.placenta.2017.06.010
Ao, Z., Wu, Z., Zhao, H., Wu, Z., and Li, Z., 2021. Associations of cord metabolome and biochemical parameters with the neonatal deaths of cloned pigs. Reproduction in Domestic Animals, 56(12), 1519-1528. https://doi.org/10.1111/rda.14014
Bao, Y.S., Zhang, P., Xie, R.J., Wang, M., Wang, Z.Y., Zhou, Z., Zhai, W.J., Feng, S.Z., and Han, M.Z., 2011. The regulation of CD4+ T cell immune responses toward Th2 cell development by prostaglandin E2. International Immunopharmacology, 11(10), 1599-1605. https://doi.org/10.1016/j.intimp.2011.05.021
Barapatre, N., Kampfer, C., Henschen, S., Schmitz, C., Edler von Koch, F., and Frank, H.G., 2021. Growth restricted placentas show severely reduced volume of villous components with perivascular myofibroblasts. Placenta, 109, 19-27. https://doi.org/10.1016/j.placenta.2021.04.006
Barcia Durán, J.G., Lu, T., Houghton, S., Geng, F., Schreiner, R., Xiang, J., Rafii, S., Redmond, D., and Lis, R., 2021. Endothelial Jak3 expression enhances pro-hematopoietic angiocrine function in mice. Communications Biology, 4(1), 406. https://doi.org/10.1038/s42003-021-01846-3
Cetin, I., Marconi, A.M., Corbetta, C., Lanfranchi, A., Baggiani, A.M., Battaglia, F.C., and Pardi, G., 1992. Fetal amino acids in normal pregnancies and in pregnancies complicated by intrauterine growth retardation. Early Human Development, 29(1-3), 183-186. https://doi.org/10.1016/0378-3782(92)90136-5
Chao de la Barca, J.M., Chabrun, F., Lefebvre, T., Roche, O., Huetz, N., Blanchet, O., Legendre, G., Simard, G., Reynier, P., and Gascoin, G., 2022. A Metabolomic Profiling of Intra-Uterine Growth Restriction in Placenta and Cord Blood Points to an Impairment of Lipid and Energetic Metabolism. Biomedicines, 10(6), 1411. https://doi.org/10.3390/biomedicines10061411
Chauvin, S., Yinon, Y., Xu, J., Ermini, L., Sallais, J., Tagliaferro, A., Todros, T., Post, M., and Caniggia, I., 2015. Aberrant TGFβ Signalling Contributes to Dysregulation of Sphingolipid Metabolism in Intrauterine Growth Restriction. Journal of Clinical Endocrinology & Metabolism, 100(7), E986-996. https://doi.org/10.1210/jc.2015-1288
Chen, F., Wang, T., Feng, C., Lin, G., Zhu, Y., Wu, G., Johnson, G., and Wang, J., 2015. Proteome Differences in Placenta and Endometrium between Normal and Intrauterine Growth Restricted Pig Fetuses. Plos One, 10(11), e0142396. https://doi.org/10.1371/journal.pone.0142396
Cindrova-Davies, T., and Sferruzzi-Perri, A.N., 2022. Human placental development and function. Seminars in Cell & Developmental Biology, 131, 66-77. https://doi.org/10.1016/j.semcdb.2022.03.039
Cox, B., Leavey, K., Nosi, U., Wong, F., and Kingdom, J., 2015. Placental transcriptome in development and pathology: expression, function, and methods of analysis. American Journal of Obstetrics And Gynecology, 213(4 Suppl), S138-151. https://doi.org/10.1016/j.ajog.2015.07.046
Daoud, G., Rassart, E., Masse, A., and Lafond, J., 2006. Src family kinases play multiple roles in differentiation of trophoblasts from human term placenta. Journal of Physiology-london, 571(Pt 3), 537-553. https://doi.org/10.1113/jphysiol.2005.102285
Davenport, B.N., Wilson, R.L., and Jones, H.N., 2022. Interventions for placental insufficiency and fetal growth restriction. Placenta, 125, 4-9. https://doi.org/10.1016/j.placenta.2022.03.127
Deng, D., Tan, X., Han, K., Ren, R., Cao, J., and Yu, M., 2020. Transcriptomic and ChIP-seq Integrative Analysis Reveals Important Roles of Epigenetically Regulated lncRNAs in Placental Development in Meishan Pigs. Genes (Basel), 11(4), 397. https://doi.org/10.3390/genes11040397
Diaz-Cueto, L., Dominguez-Lopez, P., Paniagua, L., Martinez-Quezada, R., and Arechavaleta-Velasco, F., 2021. Cadmium exposure reduces invasion of the human trophoblast-derived HTR-8/SVneo cells by inhibiting cell adhesion and matrix metalloproteinase-9 secretion. Reproductive Toxicology, 100, 68-73. https://doi.org/10.1016/j.reprotox.2021.01.001
Dumolt, J.H., Powell, T.L., and Jansson, T., 2021. Placental Function and the Development of Fetal Overgrowth and Fetal Growth Restriction. Obstetrics And Gynecology Clinics of North America, 48(2), 247-266. https://doi.org/10.1016/j.ogc.2021.02.001
Dunk, C.E., Roggensack, A.M., Cox, B., Perkins, J.E., Åsenius, F., Keating, S., Weksberg, R., Kingdom, J.C., and Adamson, S.L., 2012. A distinct microvascular endothelial gene expression profile in severe IUGR placentas. Placenta, 33(4), 285-293. https://doi.org/10.1016/j.placenta.2011.12.020
Egbor, M., Ansari, T., Morris, N., Green, C.J., and Sibbons, P.D., 2006. Morphometric placental villous and vascular abnormalities in early- and late-onset pre-eclampsia with and without fetal growth restriction. Bjog-an International Journal of Obstetrics And Gynaecology, 113(5), 580-589. https://doi.org/10.1111/j.1471-0528.2006.00882.x
Fakhr, Y., Brindley, D.N., and Hemmings, D.G., 2021. Physiological and pathological functions of sphingolipids in pregnancy. Cellular Signalling, 85, 110041. https://doi.org/10.1016/j.cellsig.2021.110041
Faquini, S., Guerra, G., Galindo, M.W.S., Gusmão, I.M.B., Vilela, L.S., and Souza, A.S., 2022. Prognostic factors and perinatal outcomes in early-onset intrauterine growth restriction due to placental insufficiency. Journal of Maternal-fetal & Neonatal Medicine, 35(25), 7119-7125. https://doi.org/10.1080/14767058.2021.1944092
Favretto, D., Cosmi, E., Ragazzi, E., Visentin, S., Tucci, M., Fais, P., Cecchetto, G., Zanardo, V., Viel, G., and Ferrara, S.D., 2012. Cord blood metabolomic profiling in intrauterine growth restriction. Analytical And Bioanalytical Chemistry, 402(3), 1109-1121. https://doi.org/10.1007/s00216-011-5540-z
Frank, J.W., Steinhauser, C.B., Wang, X., Burghardt, R.C., Bazer, F.W., and Johnson, G.A., 2021. Loss of ITGB3 in ovine conceptuses decreases conceptus expression of NOS3 and SPP1: implications for the developing placental vasculature†. Biology of Reproduction, 104(3), 657-668. https://doi.org/10.1093/biolre/ioaa212
Gu, C., Mao, X., Chen, D., Yu, B., and Yang, Q., 2019. Isoleucine Plays an Important Role for Maintaining Immune Function. Current Protein & Peptide Science, 20(7), 644-651. https://doi.org/10.2174/1389203720666190305163135
Hales, J., Moustsen, V.A., Nielsen, M.B., and Hansen, C.F., 2013. Individual physical characteristics of neonatal piglets affect preweaning survival of piglets born in a noncrated system. Journal of Animal Science 91(10), 4991-5003. https://doi.org/10.2527/jas.2012-5740
Hannun, Y.A., and Obeid, L.M., 2008. Principles of bioactive lipid signalling: lessons from sphingolipids. Nature Reviews Molecular Cell Biology, 9(2), 139-150. https://doi.org/10.1038/nrm2329
Hauguel-de Mouzon, S., and Guerre-Millo, M., 2006. The placenta cytokine network and inflammatory signals. Placenta, 27(8), 794-798. https://doi.org/10.1016/j.placenta.2005.08.009
Hu, C., Yang, Y., Deng, M., Yang, L., Shu, G., Jiang, Q., Zhang, S., Li, X., Yin, Y., Tan, C., and Wu, G., 2020. Placentae for Low Birth Weight Piglets Are Vulnerable to Oxidative Stress, Mitochondrial Dysfunction, and Impaired Angiogenesis. Oxidative Medicine And Cellular Longevity, 2020, 8715412. https://doi.org/10.1155/2020/8715412
Irtegun, S., Akcora-Yıldız, D., Pektanc, G., and Karabulut, C., 2017. Deregulation of c-Src tyrosine kinase and its downstream targets in pre-eclamptic placenta. Journal of Obstetrics And Gynaecology Research, 43(8), 1278-1284. https://doi.org/10.1111/jog.13350
Kim, J., Erikson, D.W., Burghardt, R.C., Spencer, T.E., Wu, G., Bayless, K.J., Johnson, G.A., and Bazer, F.W., 2010. Secreted phosphoprotein 1 binds integrins to initiate multiple cell signaling pathways, including FRAP1/mTOR, to support attachment and force-generated migration of trophectoderm cells. Matrix Biology, 29(5), 369-382. https://doi.org/10.1016/j.matbio.2010.04.001
Limesand, S.W., Rozance, P.J., Smith, D., and Hay, W.W., Jr., 2007. Increased insulin sensitivity and maintenance of glucose utilization rates in fetal sheep with placental insufficiency and intrauterine growth restriction. American Journal of Physiology-endocrinology And Metabolism, 293(6), E1716-1725. https://doi.org/10.1152/ajpendo.00459.2007
Lin, G., Liu, C., Feng, C., Fan, Z., Dai, Z., Lai, C., Li, Z., Wu, G., and Wang, J., 2012. Metabolomic analysis reveals differences in umbilical vein plasma metabolites between normal and growth-restricted fetal pigs during late gestation. Journal of Nutrition, 142(6), 990-998. https://doi.org/10.3945/jn.111.153411
Lin, G., Wang, X., Wu, G., Feng, C., Zhou, H., Li, D., and Wang, J., 2014. Improving amino acid nutrition to prevent intrauterine growth restriction in mammals. Amino Acids, 46(7), 1605-1623. https://doi.org/10.1007/s00726-014-1725-z
Liu, J.J., Ran, X.Q., Li, S., Feng, Y., and Wang, J.F., 2009. Polymorphism in the first intron of follicle stimulating hormone beta gene in three Chinese pig breeds and two European pig breeds. Animal Reproduction Science, 111(2-4), 369-375. https://doi.org/10.1016/j.anireprosci.2008.03.004
Liu, J., Chen, X.X., Li, X.W., Fu, W., and Zhang, W.Q., 2016. Metabolomic Research on Newborn Infants With Intrauterine Growth Restriction. Medicine (Baltimore), 95(17), e3564. https://doi.org/10.1097/md.0000000000003564
Majewska, M., Lipka, A., Paukszto, L., Jastrzebski, J.P., Szeszko, K., Gowkielewicz, M., Lepiarczyk, E., Jozwik, M., and Majewski, M.K., 2019. Placenta Transcriptome Profiling in Intrauterine Growth Restriction (IUGR). International Journal of Molecular Sciences, 20(6), 1510. https://doi.org/10.3390/ijms20061510
McIntosh, S.Z., Maestas, M.M., Dobson, J.R., Quinn, K.E., Runyan, C.L., and Ashley, R.L., 2021. CXCR4 signaling at the fetal-maternal interface may drive inflammation and syncytia formation during ovine pregnancy†. Biology of Reproduction, 104(2), 468-478. https://doi.org/10.1093/biolre/ioaa203
Moros, G., Boutsikou, T., Fotakis, C., Iliodromiti, Z., Sokou, R., Katsila, T., Xanthos, T., Iacovidou, N., and Zoumpoulakis, P., 2021. Insights into intrauterine growth restriction based on maternal and umbilical cord blood metabolomics. Scientific Reports, 11(1), 7824. https://doi.org/10.1038/s41598-021-87323-7
Mussap, M., Antonucci, R., Noto, A., and Fanos, V., 2013. The role of metabolomics in neonatal and pediatric laboratory medicine. Clinica Chimica Acta, 426, 127-138. https://doi.org/10.1016/j.cca.2013.08.020
Narang, K., Cheek, E.H., Enninga, E.A.L., and Theiler, R.N., 2021. Placental Immune Responses to Viruses: Molecular and Histo-Pathologic Perspectives. International Journal of Molecular Sciences, 22(6), 2921. https://doi.org/10.3390/ijms22062921
Nardozza, L.M., Caetano, A.C., Zamarian, A.C., Mazzola, J.B., Silva, C.P., Marçal, V.M., Lobo, T.F., Peixoto, A.B., and Araujo Júnior, E., 2017. Fetal growth restriction: current knowledge. Archives of Gynecology And Obstetrics, 295(5), 1061-1077. https://doi.org/10.1007/s00404-017-4341-9
Ness, R.B., and Sibai, B.M., 2006. Shared and disparate components of the pathophysiologies of fetal growth restriction and preeclampsia. American Journal of Obstetrics And Gynecology, 195(1), 40-49. https://doi.org/10.1016/j.ajog.2005.07.049
Obinata, H., and Hla, T., 2019. Sphingosine 1-phosphate and inflammation. International Immunology, 31(9), 617-625. https://doi.org/10.1093/intimm/dxz037
Pantham, P., Rosario, F.J., Weintraub, S.T., Nathanielsz, P.W., Powell, T.L., Li, C., and Jansson, T., 2016. Down-Regulation of Placental Transport of Amino Acids Precedes the Development of Intrauterine Growth Restriction in Maternal Nutrient Restricted Baboons. Biology of Reproduction, 95(5), 98. https://doi.org/10.1095/biolreprod.116.141085
Raghupathy, R., Al-Azemi, M., and Azizieh, F., 2012. Intrauterine growth restriction: cytokine profiles of trophoblast antigen-stimulated maternal lymphocytes. Clinical & Developmental Immunology, 2012, 734865. https://doi.org/10.1155/2012/734865
Redline, R.W., 2008. Placental pathology: a systematic approach with clinical correlations. Placenta, 29 Suppl A, S86–91. https://doi.org/10.1016/j.placenta.2007.09.003
Roberts, A.W., Kim, C., Zhen, L., Lowe, J.B., Kapur, R., Petryniak, B., Spaetti, A., Pollock, J.D., Borneo, J.B., Bradford, G.B., Atkinson, S.J., Dinauer, M.C., and Williams, D.A., 1999. Deficiency of the hematopoietic cell-specific Rho family GTPase Rac2 is characterized by abnormalities in neutrophil function and host defense. Immunity, 10(2), 183-196. https://doi.org/10.1016/s1074-7613(00)80019-9
Rosario, F.J., Kanai, Y., Powell, T.L., and Jansson, T., 2013. Mammalian target of rapamycin signalling modulates amino acid uptake by regulating transporter cell surface abundance in primary human trophoblast cells. Journal of Physiology-london, 591(3), 609-625. https://doi.org/10.1113/jphysiol.2012.238014
Sales, F., Pacheco, D., Blair, H., Kenyon, P., and McCoard, S., 2013. Muscle free amino acid profiles are related to differences in skeletal muscle growth between single and twin ovine fetuses near term. Springerplus, 2, 483. https://doi.org/10.1186/2193-1801-2-483
Sitras, V., Paulssen, R., Leirvik, J., Vårtun, A., and Acharya, G., 2009. Placental gene expression profile in intrauterine growth restriction due to placental insufficiency. Reproductive Sciences, 16(7), 701-711. https://doi.org/10.1177/1933719109334256
Solevåg, A.L., Zykova, S.N., Thorsby, P.M., and Schmölzer, G.M., 2021. Metabolomics to Diagnose Oxidative Stress in Perinatal Asphyxia: Towards a Non-Invasive Approach. Antioxidants, 10(11), 1753. https://doi.org/10.3390/antiox10111753
Street, M.E., Seghini, P., Fieni, S., Ziveri, M.A., Volta, C., Martorana, D., Viani, I., Gramellini, D., and Bernasconi, S., 2006. Changes in interleukin-6 and IGF system and their relationships in placenta and cord blood in newborns with fetal growth restriction compared with controls. European Journal of Endocrinology, 155(4), 567-574. https://doi.org/10.1530/eje.1.02251
Struwe, E., Berzl, G., Schild, R., Blessing, H., Drexel, L., Hauck, B., Tzschoppe, A., Weidinger, M., Sachs, M., Scheler, C., Schleussner, E., and Dötsch, J., 2010. Microarray analysis of placental tissue in intrauterine growth restriction. Clinical Endocrinology, 72(2), 241-247. https://doi.org/10.1111/j.1365-2265.2009.03659.x
Tan, C., Huang, Z., Xiong, W., Ye, H., Deng, J., and Yin, Y., 2022. A review of the amino acid metabolism in placental function response to fetal loss and low birth weight in pigs. Journal of Animal Science And Biotechnology, 13(1), 28. https://doi.org/10.1186/s40104-022-00676-5
Tanaka, T., Narazaki, M., and Kishimoto, T., 2014. IL-6 in inflammation, immunity, and disease. Cold Spring Harbor Perspectives in Biology, 6(10), a016295. https://doi.org/10.1101/cshperspect.a016295
Tang, Y., Li, M., Wang, J., Pan, Y., and Wu, F.X., 2015. CytoNCA: a cytoscape plugin for centrality analysis and evaluation of protein interaction networks. Biosystems, 127, 67-72. https://doi.org/10.1016/j.biosystems.2014.11.005
Tanner, A.R., Lynch, C.S., Kennedy, V.C., Ali, A., Winger, Q.A., Rozance, P.J., and Anthony, R.V., 2021. CSH RNA Interference Reduces Global Nutrient Uptake and Umbilical Blood Flow Resulting in Intrauterine Growth Restriction. International Journal of Molecular Sciences, 22(15), 8150. https://doi.org/10.3390/ijms22158150
Tomasello, E., and Vivier, E., 2005. KARAP/DAP12/TYROBP: three names and a multiplicity of biological functions. European Journal of Immunology, 35(6), 1670-1677. https://doi.org/10.1002/eji.200425932
Wang, T., Liu, C., Feng, C., Wang, X., Lin, G., Zhu, Y., Yin, J., Li, D., and Wang, J., 2013. IUGR alters muscle fiber development and proteome in fetal pigs. Frontiers in Bioscience-landmark, 18(2), 598-607. https://doi.org/10.2741/4123
Wang, J., Feng, C., Liu, T., Shi, M., Wu, G., and Bazer, F.W., 2017. Physiological alterations associated with intrauterine growth restriction in fetal pigs: Causes and insights for nutritional optimization. Molecular Reproduction And Development, 84(9), 897-904. https://doi.org/10.1002/mrd.22842
Wixey, J.A., Chand, K.K., Colditz, P.B., and Bjorkman, S.T., 2017. Review: Neuroinflammation in intrauterine growth restriction. Placenta, 54, 117-124. https://doi.org/10.1016/j.placenta.2016.11.012
Wu, G., Bazer, F.W., Wallace, J.M., and Spencer, T.E., 2006. Board-invited review: intrauterine growth retardation: implications for the animal sciences. Journal of Animal Science, 84(9), 2316-2337. https://doi.org/10.2527/jas.2006-156
Wu, G., Bazer, F.W., Johnson, G.A., Herring, C., Seo, H., Dai, Z., Wang, J., Wu, Z., and Wang, X., 2017. Functional amino acids in the development of the pig placenta. Molecular Reproduction And Development, 9(84), 870-882. https://doi.org/10.1002/mrd.22809
Wu, G., Li, X., Seo, H., McLendon, B.A., Kramer, A.C., Bazer, F.W., and Johnson, G.A., 2022. Osteopontin (OPN)/Secreted Phosphoprotein 1 (SPP1) Binds Integrins to Activate Transport of Ions Across the Porcine Placenta. Frontiers in Bioscience-landmark, 27(4), 117. https://doi.org/10.31083/j.fbl2704117
Yee, N.K., and Hamerman, J.A., 2013. β(2) integrins inhibit TLR responses by regulating NF-κB pathway and p38 MAPK activation. European Journal of Immunology, 43(3), 779-792. https://doi.org/10.1002/eji.201242550
Yoshino, O., Yamada-Nomoto, K., Kano, K., Ono, Y., Kobayashi, M., Ito, M., Yoneda, S., Nakashima, A., Shima, T., Onda, T., Osuga, Y., Aoki, J., and Saito, S., 2019. Sphingosine 1 Phosphate (S1P) Increased IL-6 Expression and Cell Growth in Endometriotic Cells. Reproductive Sciences, 26(11), 1460-1467. https://doi.org/10.1177/1933719119828112
Zhu, Y., Li, T., Huang, S., Wang, W., Dai, Z., Feng, C., Wu, G., and Wang, J., 2018. Maternal L-glutamine supplementation during late gestation alleviates intrauterine growth restriction-induced intestinal dysfunction in piglets. Amino Acids, 50(9), 1289-1299. https://doi.org/10.1007/s00726-018-2608-5
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This study was supported by the Youth Science and Technology Talent Development Project of the Education Department of Guizhou Province, China (No. QJHKYZ[2021]081), two grants received from the Department of Science and Technology of Guizhou Province, China (No. QKHJC-ZK[2021]YB166 and No. QKHZC[2021]YB147), the China Scholarship Council (No. LJM [2021]109), the Guizhou Province swine industry development project (QCN[2021]157), and the Guizhou Outstanding Young Scientific and technological Talents Training Program (No. QKHPTRC[2021]5630).
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Zheng Ao, Caizai Zhang, and Zhimin Wu conceived and designed the study. Zhimin Wu acquired the data. Caizai Zhang analyzed and interpreted the data. Guangling Hu and Yiyu Zhang contributed to contributed materials; Zheng Ao and Caizai Zhang wrote and revised the paper.
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Zhang, C., Wu, Z., Hu, G. et al. Exploring characteristics of placental transcriptome and cord serum metabolome associated with low birth weight in Kele pigs. Trop Anim Health Prod 55, 340 (2023). https://doi.org/10.1007/s11250-023-03733-x
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DOI: https://doi.org/10.1007/s11250-023-03733-x