Placenta
Volume 31, Issue 4 , Pages 289-294 , April 2010

Aldosterone and Cortisol Acutely Stimulate Na+/H+ Exchanger Activity in the Syncytiotrophoblast of the Human Placenta: Effect of Fetal Sex

,Accepted 23 December 2009.

References 

  1. Burckhardt G, Di Sole F, Helmle-Kolb C. The Na+/H+ exchanger gene family. J Nephrol. 2002;15:S3–S21
  2. Nakamura N, Tanaka S, Teko Y, Mitsui K, Kanazawa H. Four Na+/H+ exchanger isoforms are distributed to golgi and post-golgi compartments and are involved in organelle pH regulation. J Biol Chem. 2005;280:1561–1572
  3. Hughes JL, Doughty IM, Glazier JD, Powell TL, Jansson T, D'Souza SW, et al. Activity and expression of the Na+/H+ exchanger in the microvillous plasma membrane of the syncytiotrophoblast in relation to gestation and small for gestational age birth. Pediatr Res. 2000;48:652–659
  4. Pepe GJ, Burch MG, Sibley CP, Davis WA, Albrecht ED. Expression of the messenger ribonucleic acids and proteins for the Na+/H+ exchangers and their regulatory factors in baboon and human placental syncytiotrophoblast. Endocrinology. 2001;142:3685–3692
  5. Johansson M, Glazier JD, Sibley CP, Jansson T, Powell TL. Activity and protein expression of the Na+/H+ exchanger is reduced in syncytiotrophoblast microvillous plasma membranes isolated from preterm intrauterine growth restriction pregnancies. J Clin Endocrinol Metab. 2002;87:5686–5694
  6. Speake PF, Mynett KJ, Glazier JD, Greenwood SL, Sibley CP. Activity and expression of Na+/H+ exchanger isoforms in the syncytiotrophoblast of the human placenta. Pflugers Arch. 2005;450:123–130
  7. Cowley E, Sellers M, Illsley N. Intracellular pH homeostasis in cultured human placental syncytiotrophoblast cells: recovery from acidification. Am J Physiol Cell Physiol. 2005;288:C891–C898
  8. Powell TL, Illsley NP. A novel technique for studying cellular function in human placenta: gestational changes in intracellular pH regulation. Placenta. 1996;17:661–668
  9. Harvey BJ, Alzamora R, Healy V, Renard C, Doolan CM. Rapid responses to steroid hormones: from frog skin to human colon. A homage to Hans Ussing. Biochim Biophys Acta. 2002;1566:116–128
  10. Edwards CR, Stewart PM, Burt D, Brett L, McIntyre MA, Sutanto WS, et al. Localisation of 11-β-hydroxysteroid dehydrogenase–tissue specific protector of the mineralocorticoid receptor. Lancet. 1988;2:986–989
  11. Alzamora R, Michea L, Marusic ET. Role of 11-β-hydroxysteroid dehydrogenase in nongenomic aldosterone effects in human arteries. Hypertension. 2000;35:1099–1104
  12. Verriere VA, Hynes D, Faherty S, Devaney J, Bousquet J, Harvey BJ, et al. Rapid effects of dexamethasone on intracellular pH and Na+/H+ exchanger activity in human bronchial epithelial cells. J Biol Chem. 2005;280:35807–35814
  13. Markos F, Healy V, Harvey BJ. Aldosterone rapidly activates Na+/H+ exchange in M-1 cortical collecting duct cells via a PKC-MAPK pathway. Nephron Physiol. 2005;99:p1–9
  14. Funder JW, Pearce PT, Smith R, Smith AI. Mineralocorticoid action: target tissue specificity is enzyme, not receptor, mediated. Science. 1988;242:583–585
  15. Pezzi V, Mathis JM, Rainey WE, Carr BR. Profiling transcript levels for steroidogenic enzymes in fetal tissues. J Steroid Biochem Mol Biol. 2003;87:181–189
  16. Condon J, Gosden C, Gardener D, Nickson P, Hewison M, Howie AJ, et al. Expression of type 2 11-β-hydroxysteroid dehydrogenase and corticosteroid hormone receptors in early human fetal life. J Clin Endocrinol Metab. 1998;83:4490–4497
  17. Hirasawa G, Takeyama J, Sasano H, Fukushima K, Suzuki T, Muramatu Y, et al. 11-β -hydroxysteroid dehydrogenase type II and mineralocorticoid receptor in human placenta. J Clin Endocrinol Metab. 2000;85:1306–1309
  18. Driver P, Kilby M, Bujalska I, Walker E, Hewison M, Stewart P. Expression of 11 -β-hydroxysteroid dehydrogenase isozymes and corticosteroid hormone receptors in primary cultures of human trophoblast and placental bed biopsies. Mol Hum Reprod. 2001;7:357–363
  19. Pepe GJ, Burch MG, Albrecht ED. Localization and developmental regulation of 11beta-hydroxysteroid dehydrogenase-1 and -2 in the baboon syncytiotrophoblast. Endocrinology. 2001;142:68–80
  20. Johnstone JF, Bocking AD, Unlugedik E, Challis JR. The effects of chorioamnionitis and betamethasone on 11-β-hydroxysteroid dehydrogenase types 1 and 2 and the glucocorticoid receptor in preterm human placenta. J Soc Gynecol Investig. 2005;12:238–245
  21. Murphy VE, Zakar T, Smith R, Giles WB, Gibson PG, Clifton VL. Reduced 11-β -hydroxysteroid dehydrogenase type 2 activity is associated with decreased birth weight centile in pregnancies complicated by asthma. J Clin Endocrinol Metab. 2002;87:1660–1668
  22. Clifton V, Murphy V. Maternal asthma as a model for examining fetal sex-specific effects on maternal physiology and placental mechanisms that regulate human fetal growth. Placenta. 2004;25:S45–S52
  23. Sooranna SR, Oteng-Ntim E, Meah R, Ryder TA, Bajoria R. Characterization of human placental explants: morphological, biochemical and physiological studies using first and third trimester placenta. Hum Reprod. 1999;14:536–541
  24. Thomas JA, Buchsbaum RN, Zimniak A, Racker E. Intracellular pH measurements in Ehrlich ascites tumor cells utilizing spectroscopic probes generated in situ. Biochemistry. 1979;18:2210–2218
  25. Brown RW, Chapman KE, Kotelevtsev Y, Yau JL, Lindsay RS, Brett L, et al. Cloning and production of antisera to human placental 11-β-hydroxysteroid dehydrogenase type 2. Biochem J. 1996;313:1007–1017
  26. Jung-Testas I, Baulieu EE. Inhibition of glucocorticosteroid action in cultured L-929 mouse fibroblasts by RU 486, a new anti-glucocorticosteroid of high affinity for the glucocorticosteroid receptor. Exp Cell Res. 1983;147:177–182
  27. Sakauye C, Feldman D. Agonist and antimineralocorticoid activities of spirolactones. Am J Physiol. 1976;231:93–97
  28. Mahnensmith RL, Aronson PS. Interrelationships among quinidine, amiloride and lithium as inhibitors of the renal Na+/H+ exchanger. J Biol Chem. 1985;260:12586–12592
  29. Bonvalet JP, Doignon I, Blot-Chabaud M, Pradelles P, Farman N. Distribution of 11-β-hydroxysteroid dehydrogenase along the rabbit nephron. J Clin Invest. 1990;86:832–837
  30. Grossmann C, Benesic A, Krug AW, Freudinger R, Mildenberger S, Gassner B, et al. Human mineralocorticoid receptor expression renders cells responsive for nongenotropic aldosterone actions. Mol Endocrinol. 2005;19:1697–1710
  31. Chrousos GP, Kino T. Intracellular glucocorticoid signaling: a formerly simple system turns stochastic. Sci STKE. 2005;10.1126/stke.3042005pe3042048
  32. Lu NZ, Cidlowski JA. Translational regulatory mechanisms generate N-terminal glucocorticoid receptor isoforms with unique transcriptional target genes. Mol Cell. 2005;18:331–342
  33. Kino T, Tiulpakov A, Ichijo T, Chheng L, Kozasa T, Chrousos GP. G protein beta interacts with the glucocorticoid receptor and suppresses its transcriptional activity in the nucleus. J Cell Biol. 2005;169:885–896
  34. Murphy VE, Gibson PG, Giles WB, Zakar T, Smith R, Bisits AM, et al. Maternal asthma is associated with reduced female fetal growth. Am J Respir Crit Care Med. 2003;168:1317–1323
  35. Morris ME, Lee HJ, Predko LM. Gender differences in the membrane transport of endogenous and exogenous compounds. Pharmacol Rev. 2003;55:229–240
  36. Mazor M, Chaim W, Hershkowitz R, Levy J, Leiberman JR, Glezerman M. Association between preterm birth and increased maternal plasma cortisol concentrations. Obstet Gynecol. 1994;84:521–524
  37. Beitins IZ, Bayard F, Levitsky L, Ances IG, Kowarski A, Migeon CJ. Plasma aldosterone concentration at delivery and during the newborn period. J Clin Invest. 1972;51:386–394
  38. Yehuda R, Mulherin Engel S, Brand SR, Seckl J, Marcus SM, Berkowitz GS. Transgenerational effects of posttraumatic stress disorder in babies of mothers exposed to the World Trade Center attacks during pregnancy. J Clin Endocrinol Metab. 2005;90:4115–4118
  39. Dalziel S, Walker N, Parag V, Mantell C, Rea H, Rodgers A, et al. Cardiovascular risk factors after antenatal exposure to betamethasone: 30-year follow-up of a randomised controlled trial. Lancet. 2005;365:1856–1862
  40. Seckl JR, Meaney MJ. Glucocorticoid programming. Ann N Y Acad Sci. 2004;1032:63–84
  41. Murphy BE, Diez d'Aux RC. Steroid levels in the human fetus: cortisol and cortisone. J Clin Endocrinol Metab. 1972;35:678–683
  42. Seckl JR. Glucocorticoid programming of the fetus; adult phenotypes and molecular mechanisms. Mol Cell Endocrinol. 2001;185:61–71
  43. Clarke K, Ward J, Forhead A, Giussani D, Fowden A. Regulation of 11-β-hydroxysteroid dehydrogenase type 2 activity in ovine placenta by fetal cortisol. J Endocrinol. 2002;172:527–534
  44. Fowden A, Forhead A. Endocrine mechanisms of intrauterine programming. Reproduction. 2004;127:515–526
  45. Benson CA, Wintour EM. The effect of bilateral fetal adrenalectomy on fluid balance in the ovine fetus. J Physiol. 1995;489:235–241
  46. Audette MC, Greenwood SL, Sibley CP, Challis JRG, Jones RL. Dexamethasone treatment stimulates amino acid transport via System A in human term placenta. Placenta. 2008;29:A66
  47. Jones HN, Ashworth CJ, Page KR, McArdle HJ. Cortisol stimulates System A amino acid transport and SNAT2 expression in a human placental cell line (BeWo). Am J Physiol Endocrinol Metab. 2006;291:E596–E603
  48. Wyrwoll CS, Seckl JR, Holmes MC. Altered placental function of 11-β-hydroxysteroid dehydrogenase 2 knockout mice. Endocrinology. 2009;150:1287–1293
  49. Sibley CP, Turner MA, Cetin I, Ayuk P, Boyd CA, D'Souza SW, et al. Placental phenotypes of intrauterine growth. Pediatr Res. 2005;58:827–832
  50. Shotwell MA, Jayme DW, Kilberg MS, Oxender DL. Neutral amino acid transport systems in Chinese hamster ovary cells. J Biol Chem. 1981;256:5422–5427
  51. Glazier J, O'Donnell A, Sibley C. The effect of pH on the placental microvillous membrane system A amino acid transporter. Placenta. 1996;17:A16

PII: S0143-4004(10)00003-2

doi: 10.1016/j.placenta.2009.12.025

Placenta
Volume 31, Issue 4 , Pages 289-294 , April 2010