Placental Compartmentalization of Lipid Metabolism: Implications for Singleton and Twin Pregnancies

Overview

Journal Reprod Sci

Publisher Springer

Specialty Reproductive Medicine

Date 2020 Nov 10

PMID 33171514

Citations 4

Authors

Alejandra Abascal-Saiz

Eva Fuente-Luelmo

Maria Haro

Maria de la Calle

Maria P Ramos-Alvarez

German Perdomo

Jose L Bartha

Affiliations

Soon will be listed here.

Abstract

The study of placental lipid metabolism in uncomplicated pregnancies has not been developed in the literature to date. Its importance lies in expanding the knowledge of placental function to enable comparison with pathological pregnancies in future research. The aim of the present study was to compare the lipid metabolic activity and storage of the maternal and fetal sides of the placenta in healthy pregnancies. Moreover, we compare singleton vs. twin pregnancies to determine if placental metabolic needs differ. We analyzed placental explants from uncomplicated pregnancies, 20 from singleton and 8 from bichorial-biamniotic twin pregnancies (n = 28). Six cotyledon fragments were collected from each placenta at different distances from the umbilical cord, three close to the chorionic plate (hereinafter, we will refer to them as "fetal side") and another three close to the anchoring villi into the decidua basalis (referred to as "maternal side"). The samples were analyzed for quantitative assay placental fatty acid oxidation (FAO) and esterification (FAE) activities and triglyceride levels. The location of lipid storage in the chorionic villi was assessed by Oil red-O staining. Placental fatty acid oxidation did not show differences when comparing the maternal and fetal sides of the placenta or between single and twin pregnancies. When comparing placental sides, FAE was increased twofold in the maternal side compared to the fetal side of the placenta (P = 0.013). The tendency for lipogenesis in the placenta was exemplified by the FAE/FAO ratio, which was a 37.1% higher on the maternal side (P = 0.019). Despite this, triglyceride levels were five times higher in the fetal side than in the maternal one (P = 0.024). When analyzing singleton vs. twins, FAE was superior in the fetal side in multiple pregnancies (× 2.6, P = 0.007) and the FAE/FAO ratio was significantly higher in twins than in singleton pregnancies, on both sides of the placenta. Despite this finding, triglyceride levels were similar in twin and singleton pregnancies. Comparing the placentas of twins in the same pregnancy, there were no differences in lipid metabolism (FAO or FAE) or placental triglyceride levels between the two co-twins. Using Oil red-O staining, lipid storage in chorionic villi was found to be located on the syncytiotrophoblast cells and not in the connecting axis. The maternal side of the placenta is more active in the esterification of fatty acids, while the storage of neutral lipids concentrates on the fetal side. Moreover, multiple gestations have increased esterification without changes in the concentration of placental triglycerides, probably due to a higher transfer to the fetal circulation in response to the greater energy demand from twin fetuses.

Citing Articles

Decreased Fatty Acid Oxidation Gene Expression in Pre-Eclampsia According to the Onset and Presence of Intrauterine Growth Restriction.

Abascal-Saiz A, Fuente-Luelmo E, Haro M, Fioravantti V, Antolin E, Ramos-Alvarez M Nutrients. 2023; 15(18).

PMID: 37764661 PMC: 10536348. DOI: 10.3390/nu15183877.

Maternal preconception thyroid autoimmunity is associated with neonatal birth weight conceived by PCOS women undergoing their first in vitro fertilization/intracytoplasmic sperm injection.

Jiang H, Chen L, Huang N, Shi H, Chi H, Yang R J Ovarian Res. 2023; 16(1):140.

PMID: 37452360 PMC: 10347740. DOI: 10.1186/s13048-023-01208-z.

Maternal Preconception Glucose Homeostasis and Insulin Resistance Are Associated with Singleton and Twin Birthweight of Neonates Conceived by PCOS Women Undergoing IVF/ICSI Cycles.

Jiang H, Guo Y, Chen L, Shi H, Huang N, Chi H J Clin Med. 2023; 12(11).

PMID: 37298057 PMC: 10254064. DOI: 10.3390/jcm12113863.

The Relationship between Angiogenic Factors and Energy Metabolism in Preeclampsia.

Abascal-Saiz A, Duque-Alcorta M, Fioravantti V, Antolin E, Fuente-Luelmo E, Haro M Nutrients. 2022; 14(10).

PMID: 35631313 PMC: 9145768. DOI: 10.3390/nu14102172.

References

Santana D, Surita F, Cecatti J . Multiple Pregnancy: Epidemiology and Association with Maternal and Perinatal Morbidity. Rev Bras Ginecol Obstet. 2018; 40(9):554-562. PMC: 10316907. DOI: 10.1055/s-0038-1668117. View

Santana D, Silveira C, Costa M, Souza R, Surita F, Souza J . Perinatal outcomes in twin pregnancies complicated by maternal morbidity: evidence from the WHO Multicountry Survey on Maternal and Newborn Health. BMC Pregnancy Childbirth. 2018; 18(1):449. PMC: 6245698. DOI: 10.1186/s12884-018-2082-9. View

Rakheja D, Bennett M, FOSTER B, Domiati-Saad R, Rogers B . Evidence for fatty acid oxidation in human placenta, and the relationship of fatty acid oxidation enzyme activities with gestational age. Placenta. 2002; 23(5):447-50. DOI: 10.1053/plac.2002.0808. View

Shekhawat P, Bennett M, Sadovsky Y, Nelson D, Rakheja D, Strauss A . Human placenta metabolizes fatty acids: implications for fetal fatty acid oxidation disorders and maternal liver diseases. Am J Physiol Endocrinol Metab. 2003; 284(6):E1098-105. DOI: 10.1152/ajpendo.00481.2002. View

Kolahi K, Louey S, Varlamov O, Thornburg K . Real-Time Tracking of BODIPY-C12 Long-Chain Fatty Acid in Human Term Placenta Reveals Unique Lipid Dynamics in Cytotrophoblast Cells. PLoS One. 2016; 11(4):e0153522. PMC: 4849650. DOI: 10.1371/journal.pone.0153522. View

Gude N, Roberts C, Kalionis B, King R . Growth and function of the normal human placenta. Thromb Res. 2004; 114(5-6):397-407. DOI: 10.1016/j.thromres.2004.06.038. View

Kolahi K, Valent A, Thornburg K . Real-time microscopic assessment of fatty acid uptake kinetics in the human term placenta. Placenta. 2018; 72-73:1-9. PMC: 7597898. DOI: 10.1016/j.placenta.2018.07.014. View

Okita J, Johnston J, MACDONALD P . Source of prostaglandin precursor in human fetal membranes: arachidonic acid content of amnion and chorion laeve in diamnionic-dichorionic twin placentas. Am J Obstet Gynecol. 1983; 147(5):477-82. DOI: 10.1016/0002-9378(83)90001-7. View

Bartha J, Visiedo F, Fernandez-Deudero A, Bugatto F, Perdomo G . Decreased mitochondrial fatty acid oxidation in placentas from women with preeclampsia. Placenta. 2011; 33(2):132-4. DOI: 10.1016/j.placenta.2011.11.027. View

10.

Visiedo F, Bugatto F, Sanchez V, Cozar-Castellano I, Bartha J, Perdomo G . High glucose levels reduce fatty acid oxidation and increase triglyceride accumulation in human placenta. Am J Physiol Endocrinol Metab. 2013; 305(2):E205-12. DOI: 10.1152/ajpendo.00032.2013. View

11.

Perdomo G, Commerford S, Richard A, Adams S, Corkey B, ODoherty R . Increased beta-oxidation in muscle cells enhances insulin-stimulated glucose metabolism and protects against fatty acid-induced insulin resistance despite intramyocellular lipid accumulation. J Biol Chem. 2004; 279(26):27177-86. DOI: 10.1074/jbc.M403566200. View

12.

Brown N, Stefanovic-Racic M, Sipula I, Perdomo G . The mammalian target of rapamycin regulates lipid metabolism in primary cultures of rat hepatocytes. Metabolism. 2007; 56(11):1500-7. DOI: 10.1016/j.metabol.2007.06.016. View

13.

Perdomo G, Kim D, Zhang T, Qu S, Thomas E, Toledo F . A role of apolipoprotein D in triglyceride metabolism. J Lipid Res. 2010; 51(6):1298-311. PMC: 3035493. DOI: 10.1194/jlr.M001206. View

14.

Lindsay K, Hellmuth C, Uhl O, Buss C, Wadhwa P, Koletzko B . Longitudinal Metabolomic Profiling of Amino Acids and Lipids across Healthy Pregnancy. PLoS One. 2015; 10(12):e0145794. PMC: 4699222. DOI: 10.1371/journal.pone.0145794. View

15.

Herrera E, Amusquivar E, Lopez-Soldado I, Ortega H . Maternal lipid metabolism and placental lipid transfer. Horm Res. 2006; 65 Suppl 3:59-64. DOI: 10.1159/000091507. View

16.

Bartha J, Bugatto F, Fernandez-Deudero A, Fernandez-Macias R, Perdomo G . Tissue specific expression of human fatty acid oxidation enzyme genes in late pregnancy. Lipids Health Dis. 2016; 15(1):200. PMC: 5117526. DOI: 10.1186/s12944-016-0373-6. View

17.

Perazzolo S, Hirschmugl B, Wadsack C, Desoye G, Lewis R, Sengers B . The influence of placental metabolism on fatty acid transfer to the fetus. J Lipid Res. 2016; 58(2):443-454. PMC: 5282960. DOI: 10.1194/jlr.P072355. View

18.

Chavan-Gautam P, Rani A, Freeman D . Distribution of Fatty Acids and Lipids During Pregnancy. Adv Clin Chem. 2018; 84:209-239. DOI: 10.1016/bs.acc.2017.12.006. View

19.

Hummel L, Zimmermann T, Schirrmeister W, Wagner H . Synthesis, turnover and compartment analysis of the free fatty acids in the placenta of rats. Acta Biol Med Ger. 1976; 35(10):1311-6. View

20.

Rebholz S, Burke K, Yang Q, Tso P, Woollett L . Dietary fat impacts fetal growth and metabolism: uptake of chylomicron remnant core lipids by the placenta. Am J Physiol Endocrinol Metab. 2011; 301(2):E416-25. PMC: 3154537. DOI: 10.1152/ajpendo.00619.2010. View