Advertisement

Amino Acids

, Volume 50, Issue 9, pp 1205–1214 | Cite as

Placental release of taurine to both the maternal and fetal circulations in human term pregnancies

  • Maia Blomhoff HolmEmail author
  • Oddrun Kristiansen
  • Ane Moe Holme
  • Nasser Ezzatkhah Bastani
  • Hildegunn Horne
  • Rune Blomhoff
  • Guttorm Haugen
  • Tore Henriksen
  • Trond Melbye Michelsen
Original Article

Abstract

Taurine is regarded as an essential amino acid in utero, and fetal taurine supply is believed to rely solely on placental transfer from maternal plasma. Despite its potential role in intrauterine growth restriction and other developmental disturbances, human in vivo studies of taurine transfer between the maternal, placental, and fetal compartments are scarce. We studied placental transfer of taurine in uncomplicated human term pregnancies in vivo in a cross-sectional study of 179 mother-fetus pairs. During cesarean section, we obtained placental tissue and plasma from incoming and outgoing vessels on the maternal and fetal sides of the placenta. Taurine was measured by liquid chromatography–tandem mass spectrometry. We calculated paired arteriovenous differences, and measured placental expression of the taurine biosynthetic enzyme cysteine sulfinic acid decarboxylase (CSAD) with quantitative real-time polymerase chain reaction and western blot. We observed a fetal uptake (p < 0.001), an uteroplacental release (p < 0.001), and a negative placental consumption of taurine (p = 0.001), demonstrating a bilateral placental release to the maternal and fetal compartments. Increasing umbilical vein concentrations and fetal uptake was associated with the uteroplacental release to the maternal circulation (rs = − 0.19, p = 0.01/rs = − 0.24, p = 0.003), but not with taurine concentrations in placental tissue. CSAD-mRNA was expressed in placental tissue, suggesting a potential for placental taurine synthesis. Our observations show that the placenta has the capacity to a bilateral taurine release, indicating a fundamental role of taurine in the human placental homeostasis beyond the supply to the fetus.

Keywords

Taurine Placenta Fetus Transfer Arteriovenous differences CSAD 

Notes

Acknowledgements

First, we would like to thank the participating women for contributing to our study. We would also like to acknowledge the anesthesiologists, specialist nurses, obstetricians, and midwives at Oslo University Hospital for offering their time and skills to help us with the sampling procedure. We further thank Trine M. Reine and Anne Randi Enget at the Department of Nutrition at the University of Oslo who performed the qRT-PCR analysis, and Jan Haavik at the Department of Biomedicine at the University of Bergen who generously provided the CSAD antibody for western blot analysis.

Funding

This study was funded by grants from the South-Eastern Norway Regional Health Authority, the Throne Holst foundation, the Norwegian National Advisory Unit on Women’s Health, Oslo University Hospital, and the Department of Obstetrics, Oslo University Hospital.

Compliance with ethical standards

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. The study was approved by the data protection officials at Oslo University Hospital and the Regional Committee for Medical and Health Research Ethics, Southern Norway 2419/2011.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Conflict of interest

Rune Blomhoff is a chair holder in AS Vitas. Otherwise, the authors declare that they have no conflict of interest.

Supplementary material

726_2018_2576_MOESM1_ESM.pdf (115 kb)
Supplementary material 1 (PDF 114 kb)
726_2018_2576_MOESM2_ESM.pdf (137 kb)
Supplementary material 2 (PDF 137 kb)

References

  1. Alterman MA, Hunziker P (2011) Amino acid analysis: methods and protocols. Humana Press, USAGoogle Scholar
  2. Boujendar S, Reusens B, Merezak S, Ahn MT, Arany E, Hill D, Remacle C (2002) Taurine supplementation to a low protein diet during foetal and early postnatal life restores a normal proliferation and apoptosis of rat pancreatic islets. Diabetologia 45(6):856–866.  https://doi.org/10.1007/s00125-002-0833-6 CrossRefPubMedGoogle Scholar
  3. Cetin I, Marconi AM, Bozzetti P, Sereni LP, Corbetta C, Pardi G, Battaglia FC (1988) Umbilical amino acid concentrations in appropriate and small for gestational age infants: a biochemical difference present in utero. Am J Obstet Gynecol 158(1):120–126CrossRefPubMedGoogle Scholar
  4. Cetin I, Corbetta C, Sereni LP, Marconi AM, Bozzetti P, Pardi G, Battaglia FC (1990) Umbilical amino acid concentrations in normal and growth-retarded fetuses sampled in utero by cordocentesis. Am J Obstet Gynecol 162(1):253–261CrossRefPubMedGoogle Scholar
  5. Cetin I, Ronzoni S, Marconi AM, Perugino G, Corbetta C, Battaglia FC, Pardi G (1996) Maternal concentrations and fetal-maternal concentration differences of plasma amino acids in normal and intrauterine growth-restricted pregnancies. Am J Obstet Gynecol 174(5):1575–1583CrossRefPubMedGoogle Scholar
  6. Cetin I, de Santis MS, Taricco E, Radaelli T, Teng C, Ronzoni S, Spada E, Milani S, Pardi G (2005) Maternal and fetal amino acid concentrations in normal pregnancies and in pregnancies with gestational diabetes mellitus. Am J Obstet Gynecol 192(2):610–617.  https://doi.org/10.1016/j.ajog.2004.08.011 CrossRefPubMedGoogle Scholar
  7. Desforges M, Parsons L, Westwood M, Sibley CP, Greenwood SL (2013) Taurine transport in human placental trophoblast is important for regulation of cell differentiation and survival. Cell Death Dis 4:e559.  https://doi.org/10.1038/cddis.2013.81 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Desforges M, Whittaker H, Farmer E, Sibley CP, Greenwood SL (2015) Effects of taurine depletion on human placental syncytiotrophoblast renewal and susceptibility to oxidative stress. Adv Exp Med Biol 803:63–73.  https://doi.org/10.1007/978-3-319-15126-7_6 CrossRefPubMedPubMedCentralGoogle Scholar
  9. Ditchfield AM, Desforges M, Mills TA, Glazier JD, Wareing M, Mynett K, Sibley CP, Greenwood SL (2015) Maternal obesity is associated with a reduction in placental taurine transporter activity. Int J Obes (Lond) 39(4):557–564.  https://doi.org/10.1038/ijo.2014.212 CrossRefPubMedCentralGoogle Scholar
  10. Gaull G, Sturman JA, Raiha NC (1972) Development of mammalian sulfur metabolism: absence of cystathionase in human fetal tissues. Pediatr Res 6(6):538–547.  https://doi.org/10.1203/00006450-197206000-00002 CrossRefPubMedGoogle Scholar
  11. Haugen G, Kiserud T, Godfrey K, Crozier S, Hanson M (2004) Portal and umbilical venous blood supply to the liver in the human fetus near term. Ultrasound Obstet Gynecol 24(6):599–605.  https://doi.org/10.1002/uog.1744 CrossRefPubMedGoogle Scholar
  12. Hayashi S, Sanada K, Sagawa N, Yamada N, Kido K (1978) Umbilical vein-artery differences of plasma amino acids in the last trimester of human pregnancy. Biol Neonate 34(1–2):11–18CrossRefPubMedGoogle Scholar
  13. Hayes KC, Sturman JA (1981) Taurine in metabolism. Annu Rev Nutr 1:401–425.  https://doi.org/10.1146/annurev.nu.01.070181.002153 CrossRefPubMedGoogle Scholar
  14. Hibbard JU, Pridjian G, Whitington PF, Moawad AH (1990) Taurine transport in the in vitro perfused human placenta. Pediatr Res 27(1):80–84.  https://doi.org/10.1203/00006450-199001000-00021 CrossRefPubMedGoogle Scholar
  15. Holm MB, Bastani NE, Holme AM, Zucknick M, Jansson T, Refsum H, Morkrid L, Blomhoff R, Henriksen T, Michelsen TM (2017) Uptake and release of amino acids in the fetal-placental unit in human pregnancies. PLoS One 12(10):e0185760.  https://doi.org/10.1371/journal.pone.0185760 CrossRefPubMedPubMedCentralGoogle Scholar
  16. Holme AM, Holm M, Roland MC, Horne H, Michelsen TM, Haugen G, Henriksen T (2017) The 4-vessel sampling approach to integrative studies of human placental physiology in vivo. J Vis Exp (126).  https://doi.org/10.3791/55847
  17. Hultman K, Alexanderson C, Manneras L, Sandberg M, Holmang A, Jansson T (2007) Maternal taurine supplementation in the late pregnant rat stimulates postnatal growth and induces obesity and insulin resistance in adult offspring. J Physiol 579(Pt 3):823–833.  https://doi.org/10.1113/jphysiol.2006.124610 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Jozwik M, Teng C, Battaglia FC, Meschia G (1999) Fetal supply of amino acids and amino nitrogen after maternal infusion of amino acids in pregnant sheep. Am J Obstet Gynecol 180(2 Pt 1):447–453CrossRefPubMedGoogle Scholar
  19. Karl PI, Fisher SE (1990) Taurine transport by microvillous membrane vesicles and the perfused cotyledon of the human placenta. Am J Physiol 258(3 Pt 1):C443–C451CrossRefPubMedGoogle Scholar
  20. Korneeva KL, Rodriguez RR, Ralchenko SV, Martunovska OV, Frolova AO, Martsenyuk OP, Manzhula LV, Melnyk VT, Shkoropad OY, Obolenska MY (2016) Expression of genes, encoding the enzymes of cysteine metabolism in human placenta in the first and third trimesters of uncomplicated pregnancy. Ukrain Biochem J 88(1):88–98.  https://doi.org/10.15407/ubj88.01.088 CrossRefGoogle Scholar
  21. Liu J, Liu L, Chen H (2011) Antenatal taurine supplementation for improving brain ultrastructure in fetal rats with intrauterine growth restriction. Neuroscience 181:265–270.  https://doi.org/10.1016/j.neuroscience.2011.02.056 CrossRefPubMedGoogle Scholar
  22. Miyamoto Y, Balkovetz DF, Leibach FH, Mahesh VB, Ganapathy V (1988) Na+ + Cl−-gradient-driven, high-affinity, uphill transport of taurine in human placental brush-border membrane vesicles. FEBS Lett 231(1):263–267CrossRefPubMedGoogle Scholar
  23. Norberg S, Powell TL, Jansson T (1998) Intrauterine growth restriction is associated with a reduced activity of placental taurine transporters. Pediatr Res.  https://doi.org/10.1203/00006450-199808000-00016 PubMedCrossRefGoogle Scholar
  24. Park E, Park SY, Cho IS, Kim BS, Schuller-Levis G (2017) A novel cysteine sulfinic acid decarboxylase knock-out mouse: taurine distribution in various tissues with and without taurine supplementation. Adv Exp Med Biol 975:461–474.  https://doi.org/10.1007/978-94-024-1079-2_37 CrossRefPubMedGoogle Scholar
  25. Philipps AF, Holzman IR, Teng C, Battaglia FC (1978) Tissue concentrations of free amino acids in term human placentas. Am J Obstet Gynecol 131(8):881–887CrossRefPubMedGoogle Scholar
  26. Prenton MA, Young M (1969) Umbilical vein-artery and uterine arterio-venous plasma amino acid differences (in the human subject). J Obstet Gynaecol Br Commonw 76(5):404–411CrossRefPubMedGoogle Scholar
  27. Rigano S, Ferrazzi E, Boito S, Pennati G, Padoan A, Galan H (2010) Blood flow volume of uterine arteries in human pregnancies determined using 3D and bi-dimensional imaging, angio-Doppler, and fluid-dynamic modeling. Placenta 31(1):37–43.  https://doi.org/10.1016/j.placenta.2009.10.010 CrossRefPubMedGoogle Scholar
  28. Ripps H, Shen W (2012) Review: taurine: a “very essential” amino acid. Mol Vis 18:2673–2686PubMedPubMedCentralGoogle Scholar
  29. Roos S, Powell TL, Jansson T (2004) Human placental taurine transporter in uncomplicated and IUGR pregnancies: cellular localization, protein expression, and regulation. Am J Physiol Regul Integr Comp Physiol 287(4):R886–R893.  https://doi.org/10.1152/ajpregu.00232.2004 CrossRefPubMedGoogle Scholar
  30. Steingrimsdottir T, Ronquist G, Ulmsten U (1993) Balance of amino acids in the pregnant human uterus at term. Eur J Obstet Gynecol Reprod Biol 50(3):197–202CrossRefPubMedGoogle Scholar
  31. Stipanuk MH, Dominy JE Jr, Lee JI, Coloso RM (2006) Mammalian cysteine metabolism: new insights into regulation of cysteine metabolism. J Nutr 136(6 Suppl):1652s–1659sCrossRefPubMedGoogle Scholar
  32. Sturman JA, Rassin DK, Gaull GE (1970) Distribution of transsulphuration enzymes in various organs and species. Int J Biochem 1(2):251–253.  https://doi.org/10.1016/0020-711X(70)90102-3 CrossRefGoogle Scholar
  33. Tappaz ML (2004) Taurine biosynthetic enzymes and taurine transporter: molecular identification and regulations. Neurochem Res 29(1):83–96CrossRefPubMedGoogle Scholar
  34. Tsuchiya H, Matsui K, Muramatsu T, Ando T, Endo F (2009) Differences between the amino acid concentrations of umbilical venous and arterial blood. Arch Dis Child Fetal Neonatal Ed 94(2):F155–F156.  https://doi.org/10.1136/adc.2008.147256 CrossRefPubMedGoogle Scholar
  35. Vallejos C, Riquelme G (2007) The maxi-chloride channel in human syncytiotrophoblast: a pathway for taurine efflux in placental volume regulation? Placenta 28(11–12):1182–1191.  https://doi.org/10.1016/j.placenta.2007.06.005 CrossRefPubMedGoogle Scholar
  36. Velazquez A, Rosado A, Bernal A, Noriega L, Arevalo N (1976) Amino acid pools in the feto-maternal system. Biol Neonate 29(1–2):28–40CrossRefPubMedGoogle Scholar
  37. Winge I, Teigen K, Fossbakk A, Mahootchi E, Kleppe R, Sköldberg F, Kämpe O, Haavik J (2015) Mammalian CSAD and GADL1 have distinct biochemical properties and patterns of brain expression. Neurochem Int 90:173–184.  https://doi.org/10.1016/j.neuint.2015.08.013 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2018

Authors and Affiliations

  • Maia Blomhoff Holm
    • 1
    • 2
    Email author
  • Oddrun Kristiansen
    • 1
    • 2
  • Ane Moe Holme
    • 1
    • 2
  • Nasser Ezzatkhah Bastani
    • 3
  • Hildegunn Horne
    • 1
    • 2
  • Rune Blomhoff
    • 3
    • 4
  • Guttorm Haugen
    • 2
    • 5
  • Tore Henriksen
    • 1
    • 2
  • Trond Melbye Michelsen
    • 1
    • 6
  1. 1.Division of Obstetrics and Gynecology, Department of ObstetricsOslo University HospitalOsloNorway
  2. 2.Institute of Clinical MedicineUniversity of OsloOsloNorway
  3. 3.Department of Nutrition, Institute of Basic Medical SciencesUniversity of OsloOsloNorway
  4. 4.Division of Cancer Medicine, Department of Clinical ServiceOslo University HospitalOsloNorway
  5. 5.Division of Obstetrics and Gynecology, Department of Fetal MedicineOslo University HospitalOsloNorway
  6. 6.Norwegian Advisory Unit on Women’s HealthOslo University HospitalOsloNorway

Personalised recommendations