465
Views
3
CrossRef citations to date
0
Altmetric
ORIGINAL RESEARCH

Gestational Diabetes Mellitus Impedes Fetal Lung Development Through Exosome-Dependent Crosstalk Between Trophoblasts and Lung Epithelial Cells

, ORCID Icon, , , , , , , & show all
Pages 641-657 | Received 12 Nov 2022, Accepted 02 Feb 2023, Published online: 08 Feb 2023

References

  • Hod M, Kapur A, Sacks DA, et al. The International Federation of Gynecology and Obstetrics (FIGO) Initiative on gestational diabetes mellitus: a pragmatic guide for diagnosis, management, and care. Int J Gynaecol Obstet. 2015;131(Suppl 3):S173–211. doi:10.1016/S0020-7292(15)30007-2
  • McIntyre HD, Zhang C, Desoye G, et al. Gestational diabetes mellitus. Nat Rev Dis Primers. 2019;5:47. doi:10.1038/s41572-019-0098-8
  • Group, H. S. C. R. The Hyperglycemia and Adverse Pregnancy Outcome (HAPO) Study. Int J Gynaecol Obstet. 2002;78:69–77. doi:10.1016/s0020-7292(02)00092-9
  • Aboughalia H, Pathak P, Basavalingu D, et al. Imaging review of obstetric sequelae of maternal diabetes mellitus. Radiographics. 2022;42:302–319. doi:10.1148/rg.210164
  • Ejdesjo A, Wentzel P, Eriksson UJ. Influence of maternal metabolism and parental genetics on fetal maldevelopment in diabetic rat pregnancy. Am J Physiol Endocrinol Metab. 2012;302:E1198–1209. doi:10.1152/ajpendo.00661.2011
  • Gheorman L, Iliescu D, Ceausu I, et al. Importance of early complex evaluation in high-risk pregnancy associated to diabetes mellitus. Case presentation and review of the literature. Rom J Morphol Embryol. 2011;52:1127–1132.
  • Fung GP, Chan LM, Ho YC, et al. Does gestational diabetes mellitus affect respiratory outcome in late-preterm infants? Early Hum Dev. 2014;90:527–530. doi:10.1016/j.earlhumdev.2014.04.006
  • Abu-Heija AT, Al-Bash M, Mathew M. Gestational and pregestational diabetes mellitus in Omani women: comparison of obstetric and perinatal outcomes. Sultan Qaboos Univ Med J. 2015;15:e496–500. doi:10.18295/squmj.2015.15.04.009
  • Becquet O, Khabbaz F, Alberti C, et al. Insulin treatment of maternal diabetes mellitus and respiratory outcome in late-preterm and term singletons. BMJ Open. 2015;5:e008192. doi:10.1136/bmjopen-2015-008192
  • Delaney C, Cornfield DN. Risk factors for persistent pulmonary hypertension of the newborn. Pulm Circ. 2012;2:15–20. doi:10.4103/2045-8932.94818
  • Yildiz Atar H, Baatz JE, Ryan RM. Molecular mechanisms of maternal diabetes effects on fetal and neonatal surfactant. Children. 2021;8. doi:10.3390/children8040281
  • Raikkonen K, Gissler M, Kajantie E. Associations between maternal antenatal corticosteroid treatment and mental and behavioral disorders in children. JAMA. 2020;323:1924–1933. doi:10.1001/jama.2020.3937
  • Raikkonen K, Gissler M, Tapiainen T, Kajantie E. Associations between maternal antenatal corticosteroid treatment and psychological developmental and neurosensory disorders in children. JAMA Netw Open. 2022;5:e2228518. doi:10.1001/jamanetworkopen.2022.28518
  • Olmos-Ortiz A, Flores-Espinosa P, Díaz L, et al. Immunoendocrine dysregulation during gestational diabetes mellitus: the central role of the placenta. Int J Mol Sci. 2021;22. doi:10.3390/ijms22158087
  • Radaelli T, Varastehpour A, Catalano P, Hauguel-de Mouzon S. Gestational diabetes induces placental genes for chronic stress and inflammatory pathways. Diabetes. 2003;52:2951–2958. doi:10.2337/diabetes.52.12.2951
  • Taglauer E, Abman SH, Keller RL. Recent advances in antenatal factors predisposing to bronchopulmonary dysplasia. Semin Perinatol. 2018;42:413–424. doi:10.1053/j.semperi.2018.09.002
  • Parsons A, Netsanet A, Seedorf GJ, Abman SH, Taglauer ES. Understanding the role of placental pathophysiology in the development of bronchopulmonary dysplasia (BPD). Am J Physiol Lung Cell Mol Physiol. 2022. doi:10.1152/ajplung.00204.2022
  • Chiarello DI, Salsoso R, Toledo F, et al. Foetoplacental communication via extracellular vesicles in normal pregnancy and preeclampsia. Mol Aspects Med. 2018;60:69–80. doi:10.1016/j.mam.2017.12.002
  • Zhang Y, Liu Y, Liu H, Tang WH. Exosomes: biogenesis, biologic function and clinical potential. Cell Biosci. 2019;9:19. doi:10.1186/s13578-019-0282-2
  • Salomon C, Scholz-Romero K, Sarker S, et al. Gestational diabetes mellitus is associated with changes in the concentration and bioactivity of placenta-derived exosomes in maternal circulation across gestation. Diabetes. 2016;65:598–609. doi:10.2337/db15-0966
  • Rice GE, Scholz-Romero K, Sweeney E, et al. The effect of glucose on the release and bioactivity of exosomes from first trimester trophoblast cells. J Clin Endocrinol Metab. 2015;100:E1280–1288. doi:10.1210/jc.2015-2270
  • Salomon C, Torres MJ, Kobayashi M, et al. A gestational profile of placental exosomes in maternal plasma and their effects on endothelial cell migration. PLoS One. 2014;9:e98667. doi:10.1371/journal.pone.0098667
  • Nair S, Jayabalan N, Guanzon D, et al. Human placental exosomes in gestational diabetes mellitus carry a specific set of miRNAs associated with skeletal muscle insulin sensitivity. Clin Sci (Lond). 2018;132:2451–2467. doi:10.1042/CS20180487
  • Valadi H, Ekstrom K, Bossios A, et al. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol. 2007;9:654–659. doi:10.1038/ncb1596
  • Chen X, Liang H, Zhang J, Zen K, Zhang CY. Secreted microRNAs: a new form of intercellular communication. Trends Cell Biol. 2012;22:125–132. doi:10.1016/j.tcb.2011.12.001
  • Metzger B. International association of diabetes and pregnancy study groups recommendations on the diagnosis and classification of hyperglycemia in pregnancy. Diabetes Care. 2010;33:676–682. doi:10.2337/dc09-1848
  • Shen L, Li Y, Li R, et al. Placenta‑associated serum exosomal miR‑155 derived from patients with preeclampsia inhibits eNOS expression in human umbilical vein endothelial cells. Int J Mol Med. 2018;41:1731–1739. doi:10.3892/ijmm.2018.3367
  • Zhu J, Liu B, Wang Z, et al. Exosomes from nicotine-stimulated macrophages accelerate atherosclerosis through miR-21-3p/PTEN-mediated VSMC migration and proliferation. Theranostics. 2019;9:6901–6919. doi:10.7150/thno.37357
  • Nair S, Jayabalan N, Guanzon D, et al. Human placental exosomes in gestational diabetes mellitus carry a specific set of miRNAs associated with skeletal muscle insulin sensitivity. Clin sci. 2018;132:2451–2467. doi:10.1042/cs20180487
  • Del Moral PM, Warburton D. Explant culture of mouse embryonic whole lung, isolated epithelium, or mesenchyme under chemically defined conditions as a system to evaluate the molecular mechanism of branching morphogenesis and cellular differentiation. Methods Mol Biol. 2010;633:71–79. doi:10.1007/978-1-59745-019-5_5
  • Khoshgoo N, Kholdebarin R, Pereira-Terra P, et al. Prenatal microRNA miR-200b Therapy Improves Nitrofen-induced Pulmonary Hypoplasia Associated With Congenital Diaphragmatic Hernia. Ann Surg. 2019;269:979–987. doi:10.1097/SLA.0000000000002595
  • Barker DJ. Fetal nutrition and cardiovascular disease in adult life. Lancet. 1993;341:938–941. doi:10.1016/0140-6736(93)91224-a
  • Mestan KK, Steinhorn RH. Fetal origins of neonatal lung disease: understanding the pathogenesis of bronchopulmonary dysplasia. Am J Physiol Lung Cell Mol Physiol. 2011;301:L858–859. doi:10.1152/ajplung.00314.2011
  • Xita N, Tsatsoulis A. Fetal origins of the metabolic syndrome. Ann N Y Acad Sci. 2010;1205:148–155. doi:10.1111/j.1749-6632.2010.05658.x
  • Zou K, Ding G, Huang H. Advances in research into gamete and embryo-fetal origins of adult diseases. Sci China Life Sci. 2019;62:360–368. doi:10.1007/s11427-018-9427-4
  • Azad MB, Moyce BL, Guillemette L, et al. Diabetes in pregnancy and lung health in offspring: developmental origins of respiratory disease. Paediatr Respir Rev. 2017;21:19–26. doi:10.1016/j.prrv.2016.08.007
  • Burton GJ, Fowden AL, Thornburg KL. Placental origins of chronic disease. Physiol Rev. 2016;96:1509–1565. doi:10.1152/physrev.00029.2015
  • Cleal JK, Poore KR, Lewis RM. The placental exposome, placental epigenetic adaptations and lifelong cardio-metabolic health. Mol Aspects Med. 2022;87:101095. doi:10.1016/j.mam.2022.101095
  • Nguyen-Ngo C, Jayabalan N, Salomon C, Lappas M. Molecular pathways disrupted by gestational diabetes mellitus. J Mol Endocrinol. 2019;63:R51–R72. doi:10.1530/JME-18-0274
  • Lappas M, Hiden U, Desoye G, et al. The role of oxidative stress in the pathophysiology of gestational diabetes mellitus. Antioxid Redox Signal. 2011;15:3061–3100. doi:10.1089/ars.2010.3765
  • Hebert JF, Myatt L. Placental mitochondrial dysfunction with metabolic diseases: therapeutic approaches. Biochim Biophys Acta Mol Basis Dis. 2021;1867:165967. doi:10.1016/j.bbadis.2020.165967
  • Sobrevia L, Valero P, Grismaldo A, et al. Mitochondrial dysfunction in the fetoplacental unit in gestational diabetes mellitus. Biochim Biophys Acta Mol Basis Dis. 2020;1866:165948. doi:10.1016/j.bbadis.2020.165948
  • Bedell S, Hutson J, de Vrijer B, Eastabrook G. Effects of maternal obesity and gestational diabetes mellitus on the placenta: current knowledge and targets for therapeutic interventions. Curr Vasc Pharmacol. 2021;19:176–192. doi:10.2174/1570161118666200616144512
  • American College of Obstetricians and Gynecologists. ACOG Practice Bulletin No. 190: gestational Diabetes Mellitus. Obstet Gynecol. 2018;131:e49–e64. doi:10.1097/AOG.0000000000002501
  • Mayor RS, Finch KE, Zehr J, et al. Maternal high-fat diet is associated with impaired fetal lung development. Am J Physiol Lung Cell Mol Physiol. 2015;309:L360–368. doi:10.1152/ajplung.00105.2015
  • Mitchell MD, Peiris HN, Kobayashi M, et al. Placental exosomes in normal and complicated pregnancy. Am J Obstet Gynecol. 2015;213:S173–181. doi:10.1016/j.ajog.2015.07.001
  • Sarker S, Scholz-Romero K, Perez A, et al. Placenta-derived exosomes continuously increase in maternal circulation over the first trimester of pregnancy. J Transl Med. 2014;12:204. doi:10.1186/1479-5876-12-204
  • Kam W, Clauser E, Kim YS, Kan YW, Rutter WJ. Cloning, sequencing, and chromosomal localization of human term placental alkaline phosphatase cDNA. Proc Natl Acad Sci U S A. 1985;82:8715–8719. doi:10.1073/pnas.82.24.8715
  • Mincheva-Nilsson L, Nagaeva O, Chen T, et al. Placenta-derived soluble MHC class I chain-related molecules down-regulate NKG2D receptor on peripheral blood mononuclear cells during human pregnancy: a possible novel immune escape mechanism for fetal survival. J Immunol. 2006;176:3585–3592. doi:10.4049/jimmunol.176.6.3585
  • Bai K, Liu X, Li J, et al. Human placental exosomes induce maternal systemic immune tolerance by reprogramming circulating monocytes. J Nanobiotechnology. 2022;20:86. doi:10.1186/s12951-022-01283-2
  • Shen L, Vanhara P, Koutna I, et al. Placenta associated serum exosomal miR155 derived from patients with preeclampsia inhibits eNOS expression in human umbilical vein endothelial cells. Int J Mol Med. 2018;41:1731–1739. doi:10.3892/ijmm.2018.3367
  • Guarino E, Poggi C, Grieco GE, et al. Circulating MicroRNAs as biomarkers of gestational diabetes mellitus: updates and perspectives. Int J Endocrinol. 2018;2018:6380463. doi:10.1155/2018/6380463
  • Cooper JR, Abdullatif MB, Burnett E, et al. Long term culture of the A549 cancer cell line promotes multilamellar body formation and differentiation towards an alveolar Type II pneumocyte phenotype. PLoS One. 2016;11:e0164438. doi:10.1371/journal.pone.0164438
  • Rucka Z, Vanhara P, Koutna I, et al. Differential effects of insulin and dexamethasone on pulmonary surfactant-associated genes and proteins in A549 and H441 cells and lung tissue. Int J Mol Med. 2013;32:211–218. doi:10.3892/ijmm.2013.1363
  • Foster KA, Oster CG, Mayer MM, Avery ML, Audus KL. Characterization of the A549 cell line as a type II pulmonary epithelial cell model for drug metabolism. Exp Cell Res. 1998;243:359–366. doi:10.1006/excr.1998.4172
  • Schittny JC. Development of the lung. Cell Tissue Res. 2017;367:427–444. doi:10.1007/s00441-016-2545-0
  • Danopoulos S, Alonso I, Thornton ME, et al. Human lung branching morphogenesis is orchestrated by the spatiotemporal distribution of ACTA2, SOX2, and SOX9. Am J Physiol Lung Cell Mol Physiol. 2018;314:L144–L149. doi:10.1152/ajplung.00379.2017
  • Kimura J, Deutsch GH. Key mechanisms of early lung development. Pediatr Dev Pathol. 2007;10:335–347. doi:10.2350/07-06-0290.1
  • Del Riccio V, van Tuyl M, Post M. Apoptosis in lung development and neonatal lung injury. Pediatr Res. 2004;55:183–189. doi:10.1203/01.PDR.0000103930.93849.B2
  • May M, Marx A, Seidenspinner S, Speer CP. Apoptosis and proliferation in lungs of human fetuses exposed to chorioamnionitis. Histopathology. 2004;45:283–290. doi:10.1111/j.1365-2559.2004.01936.x
  • He MY, Wang G, Han SS, et al. Negative impact of hyperglycaemia on mouse alveolar development. Cell Cycle. 2018;17:80–91. doi:10.1080/15384101.2017.1403683
  • Metzger RJ, Klein OD, Martin GR, Krasnow MA. The branching programme of mouse lung development. Nature. 2008;453:745–750. doi:10.1038/nature07005
  • Rockich BE, Hrycaj SM, Shih H, et al. Sox9 plays multiple roles in the lung epithelium during branching morphogenesis. Proc Natl Acad Sci U S A. 2013;110:E4456–4464. doi:10.1073/pnas.1311847110
  • Park WY, Miranda B, Lebeche D, Hashimoto G. FGF-10 is a chemotactic factor for distal epithelial buds during lung development. Dev Biol. 1998;201:125–134. doi:10.1006/dbio.1998.8994
  • Veldhuizen EJ, Haagsman HP. Role of pulmonary surfactant components in surface film formation and dynamics. Biochim Biophys Acta. 2000;1467:255–270. doi:10.1016/s0005-2736(00)00256-x
  • Guttentag SH, Phelps DS, Stenzel W, Warshaw JB, Floros J. Surfactant protein A expression is delayed in fetuses of streptozotocin-treated rats. Am J Physiol. 1992;262:L489–494. doi:10.1152/ajplung.1992.262.4.L489
  • Guttentag SH, Phelps DS, Warshaw JB, Floros J. Delayed hydrophobic surfactant protein (SP-B, SP-C) expression in fetuses of streptozotocin-treated rats. Am J Respir Cell Mol Biol. 1992;7:190–197. doi:10.1165/ajrcmb/7.2.190
  • Miakotina OL, Dekowski SA, Snyder JM. Insulin inhibits surfactant protein A and B gene expression in the H441 cell line. Biochim Biophys Acta. 1998;1442:60–70. doi:10.1016/s0167-4781(98)00121-3
  • Rayani HH, Gewolb IH, Floros J. Glucose decreases steady state mRNA content of hydrophobic surfactant proteins B and C in fetal rat lung explants. Exp Lung Res. 1999;25:69–79. doi:10.1080/019021499270439
  • Zhu Y, Zhang T, Sun D, et al. Profiling maternal plasma microRNA expression in early pregnancy to predict gestational diabetes mellitus. Int J Gynaecol Obstet. 2015;130:49–53. doi:10.1016/j.ijgo.2015.01.010
  • Trajkovski M, Hausser J, Soutschek J, et al. MicroRNAs 103 and 107 regulate insulin sensitivity. Nature. 2011;474:649–653. doi:10.1038/nature10112
  • Zhang L, Zhang T, Sun D, et al. Diagnostic value of dysregulated microribonucleic acids in the placenta and circulating exosomes in gestational diabetes mellitus. J Diabetes Investig. 2021;12:1490–1500. doi:10.1111/jdi.13493