Early dexamethasone treatment induces placental apoptosis in sheep

Reproductive Sciences

Volumn 22, Issue 1, 2015, Pages 47-59

  Braun, Thorsten ^a   Meng, Wenbin ^a,b   Shang, Hongkai ^a,c   Li, Shaofu ^d   Sloboda, Deborah M ^e   Ehrlich, Loreen ^a   Lange, Karolin ^a   Xu, Huaisheng ^a,f   Henrich, Wolfgang ^a   Dudenhausen, Joachim W ^a   Plagemann, Andreas ^a   Newnham, John P ^d   Challis, John R G ^d,g,h  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b AFFILIATED HOSPITAL OF INNER MONGOLIA MEDICAL UNIVERSITY   (China)

^c HANGZHOU FIRST PEOPLE'S HOSPITAL   (China)

^d UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^e MCMASTER UNIVERSITY   (Canada)

^f LINYI PEOPLE'S HOSPITAL   (China)

^g UNIVERSITY OF TORONTO   (Canada)

^h SIMON FRASER UNIVERSITY   (Canada)

Author keywords

apoptopic markers; binucleate cell; glucocorticoid; placenta; placental lactogen

Indexed keywords

CYCLINE; DEXAMETHASONE; PLACENTA LACTOGEN; PROTEIN BAX; PROTEIN P53; SODIUM CHLORIDE; GLUCOCORTICOID;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DRUG EFFECT; EWE; FEMALE; FETUS; FETUS DEVELOPMENT; FETUS GROWTH; FIRST TRIMESTER PREGNANCY; GESTATION PERIOD; GESTATIONAL AGE; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PLACENTA; PLACENTAL APOPTOSIS; ANIMAL; CELL PROLIFERATION; CHEMICALLY INDUCED; COMPARATIVE STUDY; DRUG EFFECTS; FETUS WEIGHT; INTRAUTERINE GROWTH RETARDATION; METABOLISM; PATHOLOGY; PREGNANCY; SEX DIFFERENCE; SHEEP; TIME FACTOR;

ANIMALS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; CELL PROLIFERATION; DEXAMETHASONE; FEMALE; FETAL GROWTH RETARDATION; FETAL WEIGHT; GESTATIONAL AGE; GLUCOCORTICOIDS; MALE; PLACENTA; PREGNANCY; PROLIFERATING CELL NUCLEAR ANTIGEN; SEX FACTORS; SHEEP; TIME FACTORS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84919684048     PISSN: 19337191     EISSN: 19337205     Source Type: Journal    
DOI: 10.1177/1933719114542028     Document Type: Article

References (85)

1. Liggins GC, Howie RN. A controlled trial of antepartum glucocorticoid treatment for prevention of the respiratory distress syndrome in premature infants. Pediatrics. 1972 ; 50 ((4)). 515-525
2. NIH Consensus Development Panel on the Effect of Corticosteroids for Fetal Maturation on Perinatal Outcomes. JAMA. 1995 ; 273 ((5)). 413-418
3. Roberts D, Dalziel S. Antenatal corticosteroids for accelerating fetal lung maturation for women at risk of preterm birth. Cochrane Database Syst Rev. 2006 ; (3). CD004454
4. Forest MG. Recent advances in the diagnosis and management of congenital adrenal hyperplasia due to 21-hydroxylase deficiency. Hum Reprod Update. 2004 ; 10 ((6)). 469-485
5. Lajic S, Nordenstrom A, Hirvikoski T. Long-term outcome of prenatal treatment of congenital adrenal hyperplasia. Endocr Dev. 2008 ; 13: 82-98
6. David M, Forest MG. Prenatal treatment of congenital adrenal hyperplasia resulting from 21-hydroxylase deficiency. J Pediatr. 1984 ; 105 ((5)). 799-803
7. Pang SY, Pollack MS, Marshall RN, Immken L. Prenatal treatment of congenital adrenal hyperplasia due to 21-hydroxylase deficiency. N Engl J Med. 1990 ; 322 ((2)). 111-115
8. Dorr HG, Sippell WG. Prenatal dexamethasone treatment in pregnancies at risk for congenital adrenal hyperplasia due to 21-hydroxylase deficiency: effect on midgestational amniotic fluid steroid levels. J Clin Endocrinol Metab. 1993 ; 76 ((1)). 117-120
9. Hirvikoski T, Nordenstrom A, Lindholm T, et al. Cognitive functions in children at risk for congenital adrenal hyperplasia treated prenatally with dexamethasone. J Clin Endocrinol Metab. 2007 ; 92 ((2)). 542-548
10. Hirvikoski T, Nordenstrom A, Lindholm T, Lindblad F, Ritzen EM, Lajic S. Long-term follow-up of prenatally treated children at risk for congenital adrenal hyperplasia: does dexamethasone cause behavioural problems?. Eur J Endocrinol. 2008 ; 159 ((3)). 309-316
11. Lajic S, Wedell A, Bui TH, Ritzen EM, Holst M. Long-term somatic follow-up of prenatally treated children with congenital adrenal hyperplasia. J Clin Endocrinol Metab. 1998 ; 83 ((11)). 3872-3880
12. Trautman PD, Meyer-Bahlburg HF, Postelnek J, New MI. Effects of early prenatal dexamethasone on the cognitive and behavioral development of young children: results of a pilot study. Psychoneuroendocrinology. 1995 ; 20 ((4)). 439-449
13. Dodic M, Hantzis V, Duncan J, et al. Programming effects of short prenatal exposure to cortisol. FASEB J. 2002 ; 16 ((9)). 1017-1026
14. Roghair RD, Segar JL, Sharma RV, et al. Newborn lamb coronary artery reactivity is programmed by early gestation dexamethasone before the onset of systemic hypertension. Am J Physiol Regul Integr Comp Physiol. 2005 ; 289 ((4)). R1169 - R1176
15. Dodic M, McAlinden AT, Jefferies AJ, et al. Differential effects of prenatal exposure to dexamethasone or cortisol on circulatory control mechanisms mediated by angiotensin II in the central nervous system of adult sheep. J Physiol. 2006 ; 571 ((pt 3)). 651-660
16. De Blasio MJ, Dodic M, Jefferies AJ, Moritz KM, Wintour EM, Owens JA. Maternal exposure to dexamethasone or cortisol in early pregnancy differentially alters insulin secretion and glucose homeostasis in adult male sheep offspring. Am J Physiol Endocrinol Metab. 2007 ; 293 ((1)). E75 - E82
17. Dodic M, Abouantoun T, O'Connor A, Wintour EM, Moritz KM. Programming effects of short prenatal exposure to dexamethasone in sheep. Hypertension. 2002 ; 40 ((5)). 729-734
18. Braun T, Li S, Sloboda DM, et al. Effects of maternal dexamethasone treatment in early pregnancy on pituitary-adrenal axis in fetal sheep. Endocrinology. 2009 ; 150 ((12)). 5466-5477
19. Li S, Sloboda DM, Moss TJ, et al. Effects of glucocorticoid treatment given in early or late gestation on growth and development in sheep. JDOHaD. 2013 ; 4 ((2)). 146-156
20. Cox DB. The effect of maternal dexamethasone during early pregnancy on fetal growth, development and the control of glucose homeostasis. J Soc Gynecol Invest. 1999 ; 6 ((suppl 1)). 251
21. Li S, Nitsos I, Polglase GR, et al. The effects of dexamethasone treatment in early gestation on hypothalamic-pituitary-adrenal responses and gene expression at 7 months of postnatal age in sheep. Reprod Sci. 2012 ; 19 ((3)). 260-270
22. Challis JR, Sloboda D, Matthews SG, et al. The fetal placental hypothalamic-pituitary-adrenal (HPA) axis, parturition and post natal health. Mol Cell Endocrinol. 2001 ; 185 ((1-2)). 135-144
23. Braun T, Challis JR, Newnham JP, Sloboda DM. Early-life glucocorticoid exposure: the hypothalamic-pituitary-adrenal axis, placental function, and long-term disease risk. Endocr Rev. 2013 ; 34 ((6)). 885-916
24. Ehrhardt RA, Bell AW. Growth and metabolism of the ovine placenta during mid-gestation. Placenta. 1995 ; 16 ((8)). 727-741
25. Audette MC, Connor KL, Braun T, et al. Maternal glucocorticoid administartion in early pregnancy and the relationship between 11ßHSD2 mRNA in ovine placenta and fetal weight across gestation. Reprod Sci (Suppl). 2008 ; 15 (S2). 273A
26. Braun T, Li S, Moss TJ, et al. Maternal betamethasone administration reduces binucleate cell number and placental lactogen in sheep. J Endocrinol. 2007 ; 194 ((2)). 337-347
27. Braun T, Li S, Moss TJ, et al. Differential appearance of placentomes and expression of prostaglandin H synthase type 2 in placentome subtypes after betamethasone treatment of sheep late in gestation. Placenta. 2011 ; 32 ((4)). 295-303
28. Clarke KA, Ward JW, Forhead AJ, Giussani DA, Fowden AL. Regulation of 11 beta-hydroxysteroid dehydrogenase type 2 activity in ovine placenta by fetal cortisol. J Endocrinol. 2002 ; 172 ((3)). 527-534
29. Clifton VL, Rennie N, Murphy VE. Effect of inhaled glucocorticoid treatment on placental 11beta-hydroxysteroid dehydrogenase type 2 activity and neonatal birthweight in pregnancies complicated by asthma. Aust N Z J Obstet Gynaecol. 2006 ; 46 ((2)). 136-140
30. Cottrell EC, Seckl JR. Prenatal stress, glucocorticoids and the programming of adult disease. Front Behav Neurosci. 2009 ; 3: 19
31. Gatford KL, Owens JA, Li S, et al. Repeated betamethasone treatment of pregnant sheep programs persistent reductions in circulating IGF-I and IGF-binding proteins in progeny. Am J Physiol Endocrinol Metab. 2008 ; 295 ((1)). E170 - E178
32. Hahn T, Barth S, Graf R, et al. Placental glucose transporter expression is regulated by glucocorticoids. J Clin Endocrinol Metab. 1999 ; 84 ((4)). 1445-1452
33. Seckl JR, Holmes MC. Mechanisms of disease: glucocorticoids, their placental metabolism and fetal 'programming' of adult pathophysiology. Nat Clin Pract Endocrinol Metab. 2007 ; 3 ((6)). 479-488
34. Handwerger S, Maurer WF, Crenshaw C, Hurley T, Barrett J, Fellows RE. Development of the sheep as an animal model to study placental lactogen physiology. J Pediatr. 1975 ; 87 ((6 pt 2)). 1139-1143
35. Vatnick I, Schoknecht PA, Darrigrand R, Bell AW. Growth and metabolism of the placenta after unilateral fetectomy in twin pregnant ewes. J Dev Physiol. 1991 ; 15 ((6)). 351-356
36. Handwerger S, Freemark M. The roles of placental growth hormone and placental lactogen in the regulation of human fetal growth and development. J Pediatr Endocrinol Metab. 2000 ; 13 ((4)). 343-356
37. Oliver MH, Harding JE, Breier BH, Evans PC, Gluckman PD. The nutritional regulation of circulating placental lactogen in fetal sheep. Pediatr Res. 1992 ; 31 ((5)). 520-523
38. Schoknecht PA, McGuire MA, Cohick WS, Currie WB, Bell AW. Effect of chronic infusion of placental lactogen on ovine fetal growth in late gestation. Domest Anim Endocrinol. 1996 ; 13 ((6)). 519-528
39. Kappes SM, Warren WC, Pratt SL, Liang R, Anthony RV. Quantification and cellular localization of ovine placental lactogen messenger ribonucleic acid expression during mid- and late gestation. Endocrinology. 1992 ; 131 ((6)). 2829-2838
40. Wooding FB. The role of the binucleate cell in ruminant placental structure. J Reprod Fertil Suppl. 1982 ; 31: 31-39
41. Wooding FB, Morgan G, Monaghan S, Hamon M, Heap RB. Functional specialization in the ruminant placenta: evidence for two populations of fetal binucleate cells of different selective synthetic capacity. Placenta. 1996 ; 17 ((1)). 75-86
42. Ward JW, Wooding FB, Fowden AL. The effects of cortisol on the binucleate cell population in the ovine placenta during late gestation. Placenta. 2002 ; 23 ((6)). 451-458
43. Ashwell JD, Lu FW, Vacchio MS. Glucocorticoids in T cell development and function. Annu Rev Immunol. 2000 ; 18: 309-345
44. Gaynon PS, Carrel AL. Glucocorticosteroid therapy in childhood acute lymphoblastic leukemia. Adv Exp Med Biol. 1999 ; 457: 593-605
45. Elmore S. Apoptosis: a review of programmed cell death. Toxicol Pathol. 2007 ; 35 ((4)). 495-516
46. Salvetti NR, Ortega HH, Veiga-Lopez A, Padmanabhan V. Developmental programming: impact of prenatal testosterone excess on ovarian cell proliferation and apoptotic factors in sheep. Biol Reprod. 2012 ; 87 (1). 22, 1-10
47. Lyahyai J, Goldammer T, Beattie AE, Zaragoza P, Martin-Burriel I. Positional and functional characterisation of apoptosis related genes belonging to the BCL2 family in sheep. Cytogenet Genome Res. 2005 ; 109 ((4)). 519-526
48. Cox DB, Fraser M, Challis JRG. Placental development following maternal dexamethasone treatment during early pregnancy. J Soc Gynecol Invest. 1999 ; 6 ((suppl 1)). 120
49. Gluckman PD, Kaplan SL, Rudolph AM, Grumbach MM. Hormone ontogeny in the ovine fetus. II. Ovine chorionic somatomammotropin in mid- and late gestation in the fetal and maternal circulations. Endocrinology. 1979 ; 104 ((6)). 1828-1833
50. Gentili S, Morrison JL, McMillen IC. Intrauterine growth restriction and differential patterns of hepatic growth and expression of IGF1, PCK2, and HSDL1 mRNA in the sheep fetus in late gestation. Biol Reprod. 2009 ; 80 ((6)). 1121-1127
51. Passmore M, Nataatmadja M, Fraser JF. Selection of reference genes for normalisation of real-time RT-PCR in brain-stem death injury in Ovis aries. BMC Mol Biol. 2009 ; 10 ((1)). 72
52. Hyatt MA, Gopalakrishnan GS, Bispham J, et al. Maternal nutrient restriction in early pregnancy programs hepatic mRNA expression of growth-related genes and liver size in adult male sheep. J Endocrinol. 2007 ; 192 ((1)). 87-97
53. Garcia J, Simon MA, Duran M, Canceller J, Aneiros FJ. Differential efficacy of a cognitive-behavioral intervention versus pharmacological treatment in the management of fibromyalgic syndrome. Psychol Health Med. 2006 ; 11 ((4)). 498-506
54. Vandesompele J, De Preter K, Pattyn F, et al. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 2002 ; 3 ( 7 ):
55. Li S, Nitsos I, Polglase GR, Newnham JP, Challis JR, Moss TJ. Effects of tail docking and castration on stress responses in lambs and the influence of prenatal glucocorticoid treatment. Reprod Fertil Dev. 2013 ; 25 ((7)). 1020-1025
56. Bell AW, Hay WW, Ehrhardt RA. Placental transport of nutrients and its implications for fetal growth. J Reprod Fertil Suppl. 1999 ; 54: 401-410
57. Braun T, Sloboda DM, Li S, Moss TJ, Newnham JP, Challis JRG. Early prenatal glucocorticoid exposure on placental anthropometry in sheep differs from late gestation exposure. J Dev Origins Health Dis. 2009 ; 1: 195
58. Penninga L, Longo LD. Ovine placentome morphology: effect of high altitude, long-term hypoxia. Placenta. 1998 ; 19 ((2-3)). 187-193
59. Vatnick I, Ignotz G, McBride BW, Bell AW. Effect of heat stress on ovine placental growth in early pregnancy. J Dev Physiol. 1991 ; 16 ((3)). 163-166
60. Steyn C, Hawkins P, Saito T, Noakes DE, Kingdom JC, Hanson MA. Undernutrition during the first half of gestation increases the predominance of fetal tissue in late-gestation ovine placentomes. Eur J Obstet Gynecol Reprod Biol. 2001 ; 98 ((2)). 165-170
61. Gardner DS, Ward JW, Giussani DA, Fowden AL. The effect of a reversible period of adverse intrauterine conditions during late gestation on fetal and placental weight and placentome distribution in sheep. Placenta. 2002 ; 23 ((6)). 459-466
62. Alexander G. Studies on the placenta of the sheep (Ovis aries L.). Placental size. J Reprod Fertil. 1964 ; 7: 289-305
63. Wintour EM, Alcorn D, McFarlane A, Moritz K, Potocnik SJ, Tangalakis K. Effect of maternal glucocorticoid treatment on fetal fluids in sheep at 0.4 gestation. Am J Physiol. 1994 ; 266 ((4 pt 2)). R1174 - R1181
64. Ward JW, Forhead AJ, Wooding FB, Fowden AL. Functional significance and cortisol dependence of the gross morphology of ovine placentomes during late gestation. Biol Reprod. 2006 ; 74 ((1)). 137-145
65. Ward JW, Wooding FB, Fowden AL. Ovine feto-placental metabolism. J Physiol. 2004 ; 554 ((pt 2)). 529-541
66. Lacroix MC, Bolifraud P, Durieux D, Pauloin A, Vidaud M, Kann G. Placental growth hormone and lactogen production by perifused ovine placental explants: regulation by growth hormone-releasing hormone and glucose. Biol Reprod. 2002 ; 66 ((3)). 555-561
67. Wooding P, Burton G Comparative Placentation. Wooding P Burton G, ed. Berlin, Germany: Springer-Verlag Berlin Heidelberg ; 2008: 133-167.
68. Wooding FB, Hobbs T, Morgan G, Heap RB, Flint AP. Cellular dynamics of growth in sheep and goat synepitheliochorial placentomes: an autoradiographic study. J Reprod Fertil. 1993 ; 98 ((1)). 275-283
69. Wooding FB. Current topic: the synepitheliochorial placenta of ruminants: binucleate cell fusions and hormone production. Placenta. 1992 ; 13 ((2)). 101-113
70. Fowden AL, Ward JW, Wooding FP, Forhead AJ, Constancia M. Programming placental nutrient transport capacity. J Physiol. 2006 ; 572 ((pt 1)). 5-15
71. Byatt JC, Welply JK, Leimgruber RM, Collier RJ. Characterization of glycosylated bovine placental lactogen and the effect of enzymatic deglycosylation on receptor binding and biological activity. Endocrinology. 1990 ; 127 ((3)). 1041-1049
72. Owen D, Matthews SG. Glucocorticoids and sex-dependent development of brain glucocorticoid and mineralocorticoid receptors. Endocrinology. 2003 ; 144 ((7)). 2775-2784
73. Reznikov AG, Nosenko ND, Tarasenko LV. Prenatal stress and glucocorticoid effects on the developing gender-related brain. J Steroid Biochem Mol Biol. 1999 ; 69 ((1-6)). 109-115
74. O'Regan D, Kenyon CJ, Seckl JR, Holmes MC. Glucocorticoid exposure in late gestation in the rat permanently programs gender-specific differences in adult cardiovascular and metabolic physiology. Am J Physiol Endocrinol Metab. 2004 ; 287: E863 - E870
75. Eriksson JG, Kajantie E, Osmond C, Thornburg K, Barker DJ. Boys live dangerously in the womb. Am J Hum Biol. 2009 ; 22 ((3)). 330-335
76. Osei-Kumah A, Smith R, Jurisica I, Caniggia I, Clifton VL. Sex-specific differences in placental global gene expression in pregnancies complicated by asthma. Placenta. 2011 ; 32 ((8)). 570-578
77. Roberge S, Lacasse Y, Tapp S, et al. Role of fetal sex in the outcome of antenatal glucocorticoid treatment to prevent respiratory distress syndrome: systematic review and meta-analysis. J Obstet Gynaecol Can. 2011 ; 33 ((3)). 216-226
78. Ballard PL, Ballard RA, Granberg JP, et al. Fetal sex and prenatal betamethasone therapy. J Pediatr. 1980 ; 97 ((3)). 451-454
79. Spinillo A, Capuzzo E, Ometto A, Stronati M, Baltaro F, Iasci A. Value of antenatal corticosteroid therapy in preterm birth. Early Hum Dev. 1995 ; 42 ((1)). 37-47
80. Challis J, Newnham J, Petraglia F, Yeganegi M, Bocking A. Fetal sex and preterm birth. Placenta. 2013 ; 34 ((2)). 95-99
81. Clifton VL. Review: sex and the human placenta: mediating differential strategies of fetal growth and survival. Placenta. 2010 ; (31 suppl). S33 - S39
82. Li S, Moss TJ, Nitsos I, et al. The impact of maternal synthetic glucocorticoid administration in late pregnancy on fetal and early neonatal hypothalamic-pituitary-adrenal axis regulatory genes is dependent upon dose and gestational age at exposure. JDOHaD. 2013 ; 4 ((1)). 77-89
83. Dickinson H, O'Connell B, Walker D, Moritz K Glucocorticoids - New Recognition of Our Familiar Friend. Qian X, ed. Rijeka, Croatia: InTech ; 2012: 391-406.
84. Murphy VE, Gibson PG, Giles WB, et al. Maternal asthma is associated with reduced female fetal growth. Am J Respir Crit Care Med. 2003 ; 168 ((11)). 1317-1323
85. Connor KL, Challis JR, van Zijl P, et al. Do alterations in placental 11beta-hydroxysteroid dehydrogenase (11betaHSD) activities explain differences in fetal hypothalamic-pituitary-adrenal (HPA) function following periconceptional undernutrition or twinning in sheep?. Reprod Sci. 2009 ; 16 ((12)). 1201-1212