Chronic glucocorticoid exposure potentiates placental chorionic plate artery constriction: Implications for aberrant fetoplacental vascular resistance in fetal growth restriction

Endocrinology

Volumn 154, Issue 2, 2013, Pages 876-887

  Nugent, J L ^a   Wareing, M ^a   Palin, V ^a   Sibley, C P ^a   Baker, P N ^b   Ray, D W ^a   Farrow, S N ^a   Jones, Rebecca Lee ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF AUCKLAND   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

11BETA HYDROXYSTEROID DEHYDROGENASE 1; 11BETA HYDROXYSTEROID DEHYDROGENASE 2; 15 HYDROXY 11ALPHA,9ALPHA EPOXYMETHANOPROSTA 5,13 DIENOIC ACID; BRADYKININ RECEPTOR; CYCLOOXYGENASE 2; ENDOCRINE GLAND DERIVED VASCULAR ENDOTHELIAL GROWTH FACTOR; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GLUCOCORTICOID; GLUCOCORTICOID RECEPTOR; MIFEPRISTONE; THROMBOXANE RECEPTOR;

ARTERY; ARTERY CONSTRICTION; ARTICLE; BLOOD FLOW; BLOOD VESSEL REACTIVITY; CHORIONIC PLATE ARTERY; DOSE RESPONSE; DRUG EXPOSURE; HUMAN; IMMUNOREACTIVITY; INTRAUTERINE GROWTH RETARDATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; VASCULAR RESISTANCE; VASOCONSTRICTION; VASODILATATION;

11-BETA-HYDROXYSTEROID DEHYDROGENASES; 15-HYDROXY-11 ALPHA,9 ALPHA-(EPOXYMETHANO)PROSTA-5,13-DIENOIC ACID; ARTERIES; CARBENOXOLONE; CHORION; DEXAMETHASONE; FEMALE; FETAL GROWTH RETARDATION; GLUCOCORTICOIDS; HUMANS; HYDROCORTISONE; MIFEPRISTONE; PLACENTA; PLACENTAL CIRCULATION; PREGNANCY; VASOCONSTRICTION; VASODILATION;

EID: 84872691717     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2012-1927     Document Type: Article

References (50)

1. Perinatal and Maternal Mortality Review Committee. Fifth Annual Report of the Perinatal and Maternal Mortality Review Committee: Reporting Mortality 2009. Health Quality and Safety Commission New Zealand, New Zealand; 2011.
2. Bukowski R. Stillbirth and fetal growth restriction. Clin Obstet Gynecol. 53:673-680.
3. Rinaudo P, Wang E. Fetal programming and metabolic syndrome. Annu Rev Physiol. 2012;74:107-130.
4. Langley-Evans SC, McMullen S. Developmental origins of adult disease. Med Princ Pract. 2010;19:87-98.
5. Erskine RL, Ritchie JW. Umbilical artery blood flow characteristics in normal and growth-retarded fetuses. Br J Obstet Gynaecol. 1985;92:605-610. (Pubitemid 15062615)
6. Trudinger BJ, Giles WB, Cook CM, Bombardieri J, Collins L. Fetal umbilical artery flow velocity waveforms and placental resistance: clinical significance. Br J Obstet Gynaecol. 1985;92:23-30. (Pubitemid 15195843)
7. Kingdom JC, Burrell SJ, Kaufmann P. Pathology and clinical implications of abnormal umbilical artery Doppler waveforms. Ultrasound Obstet Gynecol. 1997;9:271-286. (Pubitemid 27254191)
8. Poston L, McCarthy AL, Ritter JM. Control of vascular resistance in the maternal and feto-placental arterial beds. Pharmacol Ther. 1995;65:215-239.
9. Wareing M, Crocker IP, Warren AY, Taggart MJ, Baker PN. Characterization of small arteries isolated from the human placental chorionic plate. Placenta. 2002;23:400-409. (Pubitemid 41110504)
10. Mills TA, Wareing M, Bugg GJ, Greenwood SL, Baker PN. Chorionic plate artery function and Doppler indices in normal pregnancy and intrauterine growth restriction. Eur J Clin Invest. 2005;35:758-764. (Pubitemid 41783593)
11. Yang S, Zhang L. Glucocorticoids and vascular reactivity. Curr Vasc Pharmacol. 2004;2:1-12. (Pubitemid 38855010)
12. Inoue H, Umesono K, Nishimori T, Hirata Y, Tanabe T. Glucocorticoid- mediated suppression of the promoter activity of the cyclooxygenase-2 gene is modulated by expression of its receptor in vascular endothelial cells. Biochem Biophys Res Commun. 1999;254:292-298. (Pubitemid 29290393)
13. Scott BA, Lawrence B, Nguyen HH, Meyer WJ 3rd. Aldosterone and dexamethasone binding inhumanarterial smooth muscle cells. J Hypertens. 1987;5:739-744. (Pubitemid 18029957)
14. Christy C, Hadoke PW, Paterson JM, Mullins JJ, Seckl JR, Walker BR. 11β-Hydroxysteroid dehydrogenase type 2 in mouse aorta: localization and influence on response to glucocorticoids. Hypertension. 2003;42:580-587. (Pubitemid 37237357)
15. Benediktsson R, Calder AA, Edwards CR, Seckl JR. Placental 11β-hydroxysteroid dehydrogenase: a key regulator of fetal glucocorticoid exposure. Clin Endocrinol (Oxf). 1997;46:161-166. (Pubitemid 27122161)
16. Shams M, Kilby MD, Somerset DA, et al. 11β-Hydroxysteroid dehydrogenase type 2 in human pregnancy and reduced expression in intrauterine growth restriction. Hum Reprod. 1998;13:799-804. (Pubitemid 28239177)
17. Ain R, Canham LN, Soares MJ. Dexamethasone-induced intrauterine growth restriction impacts the placental prolactin family, insulin-like growth factor-II and the Akt signaling pathway. J Endocrinol. 2005;185:253-263. (Pubitemid 40691792)
18. Braun T, Li S, Moss TJ, et al. Maternal betamethasone administration reduces binucleate cell number and placental lactogen in sheep. J Endocrinol. 2007;194:337-347. (Pubitemid 47249672)
19. Newnham JP, Evans SF, Godfrey M, Huang W, Ikegami M, Jobe A. Maternal, but not fetal, administration of corticosteroids restricts fetal growth. J Matern Fetal Med. 1999;8:81-87. (Pubitemid 29218463)
20. Waddell BJ, Hisheh S, Dharmarajan AM, Burton PJ. Apoptosis in rat placenta is zone-dependent and stimulated by glucocorticoids. Biol Reprod. 2000;63:1913-1917.
21. Clifton VL, Wallace EM, Smith R. Short-term effects of glucocorticoids in the human fetal-placental circulation in vitro. J Clin Endocrinol Metab. 2002;87:2838-2842. (Pubitemid 34655352)
22. Potter SM, Dennedy MC, Morrison JJ. Corticosteroids and fetal vasculature: effects of hydrocortisone, dexamethasone and betamethasone on human umbilical artery. BJOG. 2002;109:1126-1131. (Pubitemid 35287082)
23. Tower CL, Lui S, Charlesworth NR, Smith SD, Aplin JD, Jones RL. Differential expression of angiotensin II type 1 and type 2 receptors at the maternal-fetal interface: potential roles in early placental development. Reproduction. 2010;140(6):931-942.
24. Lee MJ, Wang Z, Yee H, et al. Expression and regulation of glucocorticoid receptor in human placental villous fibroblasts. Endocrinology. 2005;146:4619-4626. (Pubitemid 41446599)
25. Nelson DM, Walsh SW. Thromboxane and prostacyclin production by different compartments of the human placental villus. J Clin Endocrinol Metab. 1989;68:676-683. (Pubitemid 19081446)
26. Hafezi-Moghadam A, Simoncini T, Yang Z, et al. Acute cardiovascular protective effects of corticosteroids are mediated by non-transcriptional activation of endothelial nitric oxide synthase. Nat Med. 2002;8:473-479. (Pubitemid 34546749)
27. Wallace EM, Baker LS. Effect of antenatal betamethasone administration on placental vascular resistance. Lancet. 1999;353:1404-1407. (Pubitemid 29192413)
28. Edwards A, Baker LS, Wallace EM. Changes in fetoplacental vessel flow velocity waveforms following maternal administration of betamethasone. Ultrasound Obstet Gynecol. 2002;20:240-244.
29. McCarthy AL, Woolfson RG, Evans BJ, Davies DR, Raju SK, Poston L. Functional characteristics of small placental arteries. Am J Obstet Gynecol. 1994;170:945-951. (Pubitemid 24224727)
30. Schulz M, Eggert M, Baniahmad A, Dostert A, Heinzel T, Renkawitz R. RU486-induced glucocorticoid receptor agonism is controlled by the receptor N terminus and by corepressor binding. J Biol Chem. 2002;277:26238-26243. (Pubitemid 34967112)
31. Zhang S, Jonklaas J, Danielsen M. The glucocorticoid agonist activities of mifepristone (RU486) and progesterone are dependent on glucocorticoid receptor levels but not on EC50 values. Steroids. 2007;72:600-608. (Pubitemid 46764797)
32. Omar HA, Ramirez R, Gibson M. Properties of a progesterone-induced relaxation in human placental arteries and veins. J Clin Endocrinol Metab. 1995;80:370-373.
33. Cudeville C, Mondon F, Robert B, Rebourcet R, Mignot TM, Benassayag C, Ferre F. Evidence for progesterone receptors in the human fetoplacental vascular tree. Biol Reprod. 2000;62:759-765. (Pubitemid 30118320)
34. Lewis GD, Campbell WB, Johnson AR. Inhibition of prostaglandin synthesis by glucocorticoids in human endothelial cells. Endocrinology. 1986;119:62-69. (Pubitemid 16100708)
35. Wallerath T, Witte K, Schafer SC, et al. Down-regulation of the expression of endothelial NO synthase is likely to contribute to glucocorticoid-mediated hypertension. Proc Natl Acad Sci USA. 1999;96:13357-13362.
36. Sakaue M, Hoffman BB. Glucocorticoids induce transcription and expression of the α1B adrenergic receptor gene in DTT1 MF-2 smooth muscle cells. J Clin Invest. 1991;88:385-389.
37. Ullian ME, Walsh LG, Morinelli TA. Potentiation of angiotensin II action by corticosteroids in vascular tissue. Cardiovasc Res. 1996;32:266-273. (Pubitemid 26246872)
38. Li M, Bullock CM, Knauer DJ, Ehlert FJ, Zhou QY. Identification of two prokineticin cDNAs: recombinant proteins potently contract gastrointestinal smooth muscle. Mol Pharmacol. 2001;59:692-698. (Pubitemid 32273997)
39. Nusing RM, Hirata M, Kakizuka A, Eki T, Ozawa K, Narumiya S. Characterization and chromosomal mapping of the human thromboxane A2 receptor gene. J Biol Chem. 1993;268:25253-25259. (Pubitemid 23335553)
40. Rocca B, Loeb AL, Strauss JF 3rd, Vezza R, Habib A, Li H, FitzGerald GA. Directed vascular expression of the thromboxane A2 receptor results in intrauterine growth retardation. Nat Med. 2000;6:219-221. (Pubitemid 30082370)
41. Rogers KM, Bonar CA, Estrella JL, Yang S. Inhibitory effect of glucocorticoid on coronary artery endothelial function. Am J Physiol Heart Circ Physiol. 2002;283:H1922-H1928. (Pubitemid 35217026)
42. Wareing M, Greenwood SL, Baker PN. Reactivity of human placental chorionic plate vessels is modified by level of oxygenation: differences between arteries and veins. Placenta. 2006;27:42-48. (Pubitemid 41662878)
43. Wang X, Athayde N, Trudinger B. Microvascular endothelial cell activation is present in the umbilical placental microcirculation in fetal placental vascular disease. Am J Obstet Gynecol. 2004;190:596-601. (Pubitemid 38406765)
44. Brem AS, Bina RB, King TC, Morris DJ. Localization of 2 11β-OH steroid dehydrogenase isoforms in aortic endothelial cells. Hypertension. 1998;31:459-462.
45. Sun K, Yang K, Challis JR. Differential expression of 11β-hydroxysteroid dehydrogenase types 1 and 2 in human placenta and fetal membranes. J Clin Endocrinol Metab. 1997;82:300-305. (Pubitemid 27021315)
46. Nacharaju VL, Divald A, McCalla CO, Yang L, Muneyyirci-Delale O. 11β-Hydroxysteroid dehydrogenase inhibitor carbenoxolone stimulates chorionic gonadotropin secretion from human term cytotrophoblast cells differentiated in vitro. Am J Reprod Immunol. 2004;52:133-138. (Pubitemid 39149317)
47. Sun K, Adamson SL, Yang K, Challis JR. Interconversion of cortisol and cortisone by 11β-hydroxysteroid dehydrogenases type 1 and 2 in the perfused human placenta. Placenta. 1999;20:13-19. (Pubitemid 29039246)
48. Chrousos GP. Adrenocorticoids and adrenocortical antagonists. In: Katzung BG, Masters SB, Trevor AJ, eds. Basic and Clinical Pharmacology. 10th ed. Columbus, OH: McGraw-Hill Medical; 2006:635-652.
49. Kenny LC, Baker PN, Kendall DA, Randall MD, Dunn WR. The role of gap junctions in mediating endothelium-dependent responses to bradykinin in myometrial small arteries isolated from pregnant women. Br J Pharmacol. 2002;136:1085-1088. (Pubitemid 34970058)
50. Edwards G, Feletou M, Gardener MJ, Thollon C, Vanhoutte PM, Weston AH. Role of gap junctions in the responses to EDHF in rat and guinea-pig small arteries. Br J Pharmacol. 1999;128:1788-1794. (Pubitemid 30011893)