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RESEARCH ARTICLE

Loss of the pregnancy-induced rise in cortisol concentrations in the ewe impairs the fetal insulin-like growth factor axis

Ellen C. Jensen A F , Laura Bennet A , Charles Wood B , Mark Vickers C , Bernhard Breier D , Alistair J. Gunn A and Maureen Keller-Wood E
+ Author Affiliations
- Author Affiliations

A Department of Physiology, Faculty of Medical and Health Sciences, The University of Auckland, Private Bag 92019, Auckland 1023, New Zealand.

B The Department of Physiology and Functional Genomics, University of Florida, Gainesville, FL 32611, USA.

C The Liggins Institute, The University of Auckland, Private Bag 92019, Auckland 1023, New Zealand.

D Institute of Food, Nutrition and Human Health, Massey University, Albany Campus, Auckland 0745, New Zealand.

E The Department of Pharmacodynamics, University of Florida, Gainesville, FL 32610-0274, USA.

F Corresponding author. Email: e.knapp@auckland.ac.nz

Reproduction, Fertility and Development 23(5) 665-672 https://doi.org/10.1071/RD10317
Submitted: 25 November 2010  Accepted: 22 December 2010   Published: 5 May 2011

Abstract

Maternal cortisol levels increase during pregnancy. Although this change is important for optimal fetal growth, the mechanisms of the changes in growth remain unclear. The hypothesis examined was that alterations in maternal plasma cortisol concentrations are associated with changes in the fetal insulin-like growth factor (IGF) axis. Pregnant ewes in late gestation (115 ± 0.4 days) were studied: six control animals, five ewes given 1 mg kg–1 day–1 cortisol (high cortisol) and five adrenalectomised ewes given 0.5–0.6 mg kg–1 day–1 cortisol (low cortisol). Blood samples were taken throughout the experiment and at necropsy (130 ± 0.2 days) and fetal liver was frozen for mRNA analysis. Fetal IGF-I and insulin plasma concentrations were lower and insulin-like growth factor-binding protein-1 (IGFBP-1) concentrations were higher in the low cortisol group compared with those in the control group (P < 0.05). Fetal liver IGF-II and IGFBP-3 mRNA were decreased in low cortisol animals compared with controls (P < 0.05). There were no significant changes in these parameters in the high cortisol group, and there were no changes in fetal liver IGF-I, growth hormone receptor, IGF-I receptor, IGF-II receptor, IGFBP-1 or IGFBP-2 mRNA levels between the groups. These data suggest that reduced fetal IGF availability contributes to reduced fetal growth when maternal cortisol secretion is impaired, but not during exposure to moderate increases in cortisol.

Additional keywords: glucocorticoids, maternal stress.


References

Ahmad, I., Beharry, K. D., Valencia, A. M., Cho, S., Guajardo, L., Nageotte, M. P., and Modanlou, H. D. (2006). Influence of a single course of antenatal betamethasone on the maternal–fetal insulin–IGF–GH axis in singleton pregnancies. Growth Horm. IGF Res. 16, 267–275.
Influence of a single course of antenatal betamethasone on the maternal–fetal insulin–IGF–GH axis in singleton pregnancies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XptFCntLw%3D&md5=2d49ab63753cd2b7a243d707248986f8CAS | 16920374PubMed |

Bassett, J. M., and Thorburn, G. D. (1971). The regulation of insulin secretion by the ovine foetus in utero. J. Endocrinol. 50, 59–74.
The regulation of insulin secretion by the ovine foetus in utero.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3MXhtlOlu74%3D&md5=32c79a48440f02e66e0fd3de10469813CAS | 4325619PubMed |

Bell, M. E., Wood, C. E., and Keller-Wood, M. (1991). Influence of reproductive state on pituitary–adrenal activity in the ewe. Domest. Anim. Endocrinol. 8, 245–254.
Influence of reproductive state on pituitary–adrenal activity in the ewe.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3MzgtVygsw%3D%3D&md5=89506fbabb0312250850e720dddbea78CAS | 1649030PubMed |

Bennet, L., Oliver, M. H., Gunn, A. J., Hennies, M., and Breier, B. (2001). Differential changes in insulin-like growth factors and their binding proteins following asphyxia in the preterm fetal sheep. J. Physiol. 531, 835–841.
Differential changes in insulin-like growth factors and their binding proteins following asphyxia in the preterm fetal sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXivVaksL0%3D&md5=8ff8f409696fd0d4127af230bea587f0CAS | 11251062PubMed |

Blache, D., Tellam, R. L., Chagas, L. M., Blackberry, M. A., Vercoe, P. E., and Martin, G. B. (2000). Level of nutrition affects leptin concentrations in plasma and cerebrospinal fluid in sheep. J. Endocrinol. 165, 625–637.
Level of nutrition affects leptin concentrations in plasma and cerebrospinal fluid in sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXktl2qtrw%3D&md5=65a9bd32d510ab663ce03fc99243e561CAS | 10828846PubMed |

Bland, J. M., and Altman, D. G. (1995). Calculating correlation coefficients with repeated observations: Part 1– correlation within subjects. BMJ 310, 446..
| 7873953PubMed |

Bloomfield, F. H., van Zijl, P. L., Bauer, M. K., Phua, H. H., and Harding, J. E. (2006). Effect of pulsatile growth hormone administration to the growth-restricted fetal sheep on somatotrophic axis gene expression in fetal and placental tissues. Am. J. Physiol. Endocrinol. Metab. 291, E333–E339.
Effect of pulsatile growth hormone administration to the growth-restricted fetal sheep on somatotrophic axis gene expression in fetal and placental tissues.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XovVWgt7g%3D&md5=2499f423fd94f06902dee768ff7bb87bCAS | 16507606PubMed |

Blum, W. F., and Breier, B. H. (1994). Radioimmunoassays for IGFs and IGFBPs. Growth Regul. 4, 11–19.
| 1:CAS:528:DyaK2cXktVWit7w%3D&md5=a21e6e6498f9656c9110f4db39115012CAS | 7515738PubMed |

Breier, B. H., Gallaher, B. W., and Gluckman, P. D. (1991). Radioimmunoassay for insulin-like growth factor-I: solutions to some potential problems and pitfalls. J. Endocrinol. 128, 347–357.
Radioimmunoassay for insulin-like growth factor-I: solutions to some potential problems and pitfalls.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXhtFGiur8%3D&md5=3d2078f48615e930aa00417e7b308047CAS | 1707433PubMed |

Buescher, M. A., McClamrock, H. D., and Adashi, E. Y. (1992). Cushing syndrome in pregnancy. Obstet. Gynecol. 79, 130–137.
| 1:STN:280:DyaK38%2Fos1aktA%3D%3D&md5=dda37b8cf6009c6bb39af65a20dcaa8aCAS | 1727571PubMed |

Carr, B. R., Parker, C. R., Madden, J. D., MacDonald, P. C., and Porter, J. C. (1981). Maternal plasma adrenocorticotropin and cortisol relationships throughout human pregnancy. Am. J. Obstet. Gynecol. 139, 416–422.
| 1:CAS:528:DyaL3MXkslOrtbc%3D&md5=0763603bf9948d43872cb6135deba40fCAS | 6258436PubMed |

Carr, J. M., Owens, J. A., Grant, P. A., Walton, P. E., Owens, P. C., and Wallace, J. C. (1995). Circulating insulin-like growth factors (IGFs), IGF-binding proteins (IGFBPs) and tissue mRNA levels of IGFBP-2 and IGFBP-4 in the ovine fetus. J. Endocrinol. 145, 545–557.
Circulating insulin-like growth factors (IGFs), IGF-binding proteins (IGFBPs) and tissue mRNA levels of IGFBP-2 and IGFBP-4 in the ovine fetus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXmtV2gtr0%3D&md5=203ad711839f656a87d302f935580427CAS | 7543554PubMed |

Conover, C. A. (1990). Regulation of insulin-like growth factor (IGF)-binding protein synthesis by insulin and IGF-I in cultured bovine fibroblasts. Endocrinology 126, 3139–3145.
Regulation of insulin-like growth factor (IGF)-binding protein synthesis by insulin and IGF-I in cultured bovine fibroblasts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXitVSgsbo%3D&md5=be66e6a49d67a2e6ef357e076b4e94f0CAS | 1693568PubMed |

de Weerth, C., and Buitelaar, J. K. (2005). Physiological stress reactivity in human pregnancy – a review. Neurosci. Biobehav. Rev. 29, 295–312.
Physiological stress reactivity in human pregnancy – a review.Crossref | GoogleScholarGoogle Scholar | 15811500PubMed |

Delhanty, P. J., and Han, V. K. (1993). The expression of insulin-like growth factor (IGF)-binding protein-2 and IGF-II genes in the tissues of the developing ovine fetus. Endocrinology 132, 41–52.
The expression of insulin-like growth factor (IGF)-binding protein-2 and IGF-II genes in the tissues of the developing ovine fetus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXpsFSrsA%3D%3D&md5=8c05012d8ed505286a3ec44c0b5978e8CAS | 7678219PubMed |

Florini, J. R., Ewton, D. Z., and Coolican, S. A. (1996). Growth hormone and the insulin-like growth factor system in myogenesis. Endocr. Rev. 17, 481–517.
| 1:CAS:528:DyaK28XmvF2hs7k%3D&md5=ba75f0411da770bc27ded4cc7e2e1248CAS | 8897022PubMed |

Fowden, A. L. (1995). Endocrine regulation of fetal growth. Reprod. Fertil. Dev. 7, 351–363.
Endocrine regulation of fetal growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXpvVShtr4%3D&md5=009f12800e6b1aff1b5d95bf01aa095cCAS | 8606944PubMed |

Fowden, A. L., and Forhead, A. J. (2009). Endocrine regulation of feto-placental growth. Horm. Res. 72, 257–265.
Endocrine regulation of feto-placental growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXht12hurjJ&md5=b923135dd418ad9987001725fcc5752eCAS | 19844111PubMed |

Gatford, K. L., Owens, J. A., Li, S., Moss, T. J., Newnham, J. P., Challis, J. R., and Sloboda, D. M. (2008). Repeated betamethasone treatment of pregnant sheep programs persistent reductions in circulating IGF-I and IGF-binding proteins in progeny. Am. J. Physiol. Endocrinol. Metab. 295, E170–E178.
Repeated betamethasone treatment of pregnant sheep programs persistent reductions in circulating IGF-I and IGF-binding proteins in progeny.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXoslyhurY%3D&md5=872a15391e9195f6c1fcde3c63f6af20CAS | 18492775PubMed |

Giudice, L. C., de Zegher, F., Gargosky, S. E., Dsupin, B. A., de las Fuentes, L., Crystal, R. A., Hintz, R. L., and Rosenfeld, R. G. (1995). Insulin-like growth factors and their binding proteins in the term and preterm human fetus and neonate with normal and extremes of intrauterine growth. J. Clin. Endocrinol. Metab. 80, 1548–1555.
Insulin-like growth factors and their binding proteins in the term and preterm human fetus and neonate with normal and extremes of intrauterine growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXlsV2rsL0%3D&md5=88ac6b3916bb37e4c88bd62493d09b63CAS | 7538146PubMed |

Hyatt, M. A., Walker, D. A., Stephenson, T., and Symonds, M. E. (2004). Ontogeny and nutritional manipulation of the hepatic prolactin–growth hormone–insulin-like growth factor axis in the ovine fetus and in neonate and juvenile sheep. Proc. Nutr. Soc. 63, 127–135.
Ontogeny and nutritional manipulation of the hepatic prolactin–growth hormone–insulin-like growth factor axis in the ovine fetus and in neonate and juvenile sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXktFGlu70%3D&md5=fbb520c8c140198935bd46d522782c8dCAS | 15070443PubMed |

Iwamoto, H. S., Murray, M. A., and Chernausek, S. D. (1992). Effects of acute hypoxemia on insulin-like growth factors and their binding proteins in fetal sheep. Am. J. Physiol. 263, E1151–E1156.
| 1:CAS:528:DyaK3sXnsl2rsQ%3D%3D&md5=95ddc1cf2fdd85cb182273ce74eb4676CAS | 1282302PubMed |

Jensen, E. C., Gallaher, B. W., Breier, B. H., and Harding, J. E. (2002a). The effect of a chronic maternal cortisol infusion on the late-gestation fetal sheep. J. Endocrinol. 174, 27–36.
The effect of a chronic maternal cortisol infusion on the late-gestation fetal sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XlvFeqtb4%3D&md5=0e89a09d9a2d6220de099bfe00e6c7b6CAS | 12098660PubMed |

Jensen, E., Wood, C., and Keller-Wood, M. (2002b). The normal increase in adrenal secretion during pregnancy contributes to maternal volume expansion and fetal homeostasis. J. Soc. Gynecol. Investig. 9, 362–371.
The normal increase in adrenal secretion during pregnancy contributes to maternal volume expansion and fetal homeostasis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XoslGhtLk%3D&md5=2435898ecbb844e7182088228028db91CAS | 12445601PubMed |

Jensen, E., Wood, C. E., and Keller-Wood, M. (2003). Alterations in maternal corticosteroid levels influence fetal urine and lung liquid production. J. Soc. Gynecol. Investig. 10, 480–489.
Alterations in maternal corticosteroid levels influence fetal urine and lung liquid production.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXps1OltrY%3D&md5=d8e7f7cb531263ba94971215a12f0714CAS | 14662161PubMed |

Jensen, E., Wood, C. E., and Keller-Wood, M. (2005). Chronic alterations in ovine maternal corticosteroid influence uterine blood flow and placental and fetal growth. Am. J. Physiol. Regul. Integr. Comp. Physiol. 288, R54–R61.
Chronic alterations in ovine maternal corticosteroid influence uterine blood flow and placental and fetal growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVCqur8%3D&md5=6801c8352301cf13e332058f50316328CAS | 15231491PubMed |

Jensen, E. C., Rochette, M., Bennet, L., Wood, C. E., Gunn, A. J., and Keller-Wood, M. (2010). Physiological changes in maternal cortisol do not alter expression of growth-related genes in the ovine placenta. Placenta 31, 1064–1069.
Physiological changes in maternal cortisol do not alter expression of growth-related genes in the ovine placenta.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsVyhsLvP&md5=9397abb9858809ea0bf4349bb5de602dCAS | 20951429PubMed |

Jones, J. I., and Clemmons, D. R. (1995). Insulin-like growth factors and their binding proteins: biological actions. Endocr. Rev. 16, 3–34.
| 1:CAS:528:DyaK2MXltlKhu7g%3D&md5=c16b44063956cf7380d44828f96ff56fCAS | 7758431PubMed |

Kajantie, E., Hytinantti, T., Koistinen, R., Risteli, J., Rutanen, E. M., Seppala, M., and Andersson, S. (2001). Markers of type I and type III collagen turnover, insulin-like growth factors and their binding proteins in cord plasma of small premature infants: relationships with fetal growth, gestational age, preeclampsia and antenatal glucocorticoid treatment. Pediatr. Res. 49, 481–489.
Markers of type I and type III collagen turnover, insulin-like growth factors and their binding proteins in cord plasma of small premature infants: relationships with fetal growth, gestational age, preeclampsia and antenatal glucocorticoid treatment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjtVyitb0%3D&md5=62133f0811c1806448ff796247fe2a5aCAS | 11264430PubMed |

Keller-Wood, M., Cudd, T. A., Norman, W., Caldwell, S. M., and Wood, C. E. (1998). Sheep model for study of maternal adrenal gland function during pregnancy. Lab. Anim. Sci. 48, 507–512.
| 1:STN:280:DyaK1M7ovF2gtA%3D%3D&md5=3eadd60b3b18762370d7345f4d2257dfCAS | 10090066PubMed |

Keller-Wood, M., Wood, C. E., Hua, Y., and Zhang, D. (2005). Mineralocorticoid receptor expression in late-gestation ovine fetal lung. J. Soc. Gynecol. Investig. 12, 84–91.
Mineralocorticoid receptor expression in late-gestation ovine fetal lung.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVyis7s%3D&md5=bbedb43d032db7484211202a96ddbb30CAS | 15695102PubMed |

Keller-Wood, M., von Reitzenstein, M., and McCartney, J. (2009). Is the fetal lung a mineralocorticoid receptor target organ? Induction of cortisol-regulated genes in the ovine fetal lung, kidney and small intestine. Neonatology 95, 47–60.
Is the fetal lung a mineralocorticoid receptor target organ? Induction of cortisol-regulated genes in the ovine fetal lung, kidney and small intestine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsV2ku7bL&md5=84d4a6320d824a1df9a4999b40cada0aCAS | 18787337PubMed |

Li, J., Forhead, A. J., Dauncey, M. J., Gilmour, R. S., and Fowden, A. L. (2002). Control of growth hormone receptor and insulin-like growth factor-I expression by cortisol in ovine fetal skeletal muscle. J. Physiol. 541, 581–589.
Control of growth hormone receptor and insulin-like growth factor-I expression by cortisol in ovine fetal skeletal muscle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XlsVWjur8%3D&md5=e74a81140a4a0500d2a8e893124aef52CAS | 12042362PubMed |

Livak, K. J., and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(–Delta Delta C(T)) Method. Methods 25, 402–408.
Analysis of relative gene expression data using real-time quantitative PCR and the 2(–Delta Delta C(T)) Method.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhtFelt7s%3D&md5=e0ea026c02920b4196beca401ea8984bCAS | 11846609PubMed |

McIntyre, H. D., Serek, R., Crane, D. I., Veveris-Lowe, T., Parry, A., Johnson, S., Leung, K. C., Ho, K. K., Bougoussa, M., Hennen, G., Igout, A., Chan, F. Y., Cowley, D., Cotterill, A., and Barnard, R. (2000). Placental growth hormone (GH), GH-binding protein, and insulin-like growth factor axis in normal, growth-retarded and diabetic pregnancies: correlations with fetal growth. J. Clin. Endocrinol. Metab. 85, 1143–1150.
Placental growth hormone (GH), GH-binding protein, and insulin-like growth factor axis in normal, growth-retarded and diabetic pregnancies: correlations with fetal growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXisFOqsro%3D&md5=9f32cf2c9d41305f4b82c1a1e0db71dbCAS | 10720053PubMed |

McLellan, K. C., Hooper, S. B., Bocking, A. D., Delhanty, P. J., Phillips, I. D., Hill, D. J., and Han, V. K. (1992). Prolonged hypoxia induced by the reduction of maternal uterine blood flow alters insulin-like growth factor-binding protein-1 (IGFBP-1) and IGFBP-2 gene expression in the ovine fetus. Endocrinology 131, 1619–1628.
Prolonged hypoxia induced by the reduction of maternal uterine blood flow alters insulin-like growth factor-binding protein-1 (IGFBP-1) and IGFBP-2 gene expression in the ovine fetus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XmsV2muro%3D&md5=32ae70ce580dfbfb447b89bee3e484c3CAS | 1382958PubMed |

Meinel, L., Zoidis, E., Zapf, J., Hassa, P., Hottiger, M. O., Auer, J. A., Schneider, R., Gander, B., Luginbuehl, V., Bettschart-Wolfisberger, R., Illi, O. E., Merkle, H. P., and von Rechenberg, B. (2003). Localized insulin-like growth factor I delivery to enhance new bone formation. Bone 33, 660–672.
Localized insulin-like growth factor I delivery to enhance new bone formation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXnvVersLw%3D&md5=15516a44ecea813453efd9879cdbd9e9CAS | 14555272PubMed |

Mellor, D. J., and Murray, L. (1982). Effects on the rate of increase in fetal girth of re-feeding ewes after short periods of severe undernutrition during late pregnancy. Res. Vet. Sci. 32, 377–382.
| 1:STN:280:DyaL383kvFWksw%3D%3D&md5=f7339973cc0b45548b3c9d458d093ab8CAS | 7100656PubMed |

O’Shaughnessy, R. W., and Hackett, K. J. (1984). Maternal Addison’s disease and fetal growth retardation. A case report. J. Reprod. Med. 29, 752–756.
| 1:STN:280:DyaL2M%2Fot1ymuw%3D%3D&md5=35508e05c46f018dca6a64683deb95dcCAS | 6512785PubMed |

Oliver, M. H., Harding, J. E., Breier, B. H., Evans, P. C., and Gluckman, P. D. (1993). Glucose but not a mixed amino acid infusion regulates plasma insulin-like growth factor-I concentrations in fetal sheep. Pediatr. Res. 34, 62–65.
Glucose but not a mixed amino acid infusion regulates plasma insulin-like growth factor-I concentrations in fetal sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXltlahurw%3D&md5=8ec0abd724c68b57b332055dcb438f14CAS | 8356021PubMed |

Ooi, G. T., Orlowski, C. C., Brown, A. L., Becker, R. E., Unterman, T. G., and Rechler, M. M. (1990). Different tissue distribution and hormonal regulation of messenger RNAs encoding rat insulin-like growth factor-binding proteins-1 and -2. Mol. Endocrinol. 4, 321–328.
Different tissue distribution and hormonal regulation of messenger RNAs encoding rat insulin-like growth factor-binding proteins-1 and -2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXhslejsr4%3D&md5=43c99eee31ca699eebf082ccadb4f339CAS | 1691819PubMed |

Osler, M. (1962). Addison’s disease and pregnancy. Acta Endocrinol. (Copenh.) 41, 67–78.
| 1:STN:280:DyaF38%2FosVSlsQ%3D%3D&md5=b952f72b20baab7f7597da3f277980f2CAS | 14482540PubMed |

Price, W. A., Stiles, A. D., Moats-Staats, B. M., and D’Ercole, A. J. (1992). Gene expression of insulin-like growth factors (IGFs), the type 1 IGF receptor and IGF-binding proteins in dexamethasone-induced fetal growth retardation. Endocrinology 130, 1424–1432.
Gene expression of insulin-like growth factors (IGFs), the type 1 IGF receptor and IGF-binding proteins in dexamethasone-induced fetal growth retardation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XhvVyhsLw%3D&md5=671770227f80e95c22b4a64ef0fff52cCAS | 1371449PubMed |

Quaedackers, J. S., Roelfsema, V., Fraser, M., Gunn, A. J., and Bennet, L. (2005). Cardiovascular and endocrine effects of a single course of maternal dexamethasone treatment in preterm fetal sheep. BJOG 112, 182–191.
Cardiovascular and endocrine effects of a single course of maternal dexamethasone treatment in preterm fetal sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhvVClsb4%3D&md5=b7db287aac5fae365a95860a78bbd4acCAS | 15663582PubMed |

Reini, S. A., Wood, C. E., Jensen, E., and Keller-Wood, M. (2006). Increased maternal cortisol in late-gestation ewes decreases fetal cardiac expression of 11{beta}-HSD2 mRNA and the ratio of AT1 to AT2 receptor mRNA. Am. J. Physiol. Regul. Integr. Comp. Physiol. 291, R1708–R1716.
Increased maternal cortisol in late-gestation ewes decreases fetal cardiac expression of 11{beta}-HSD2 mRNA and the ratio of AT1 to AT2 receptor mRNA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXktVGl&md5=d27f198a39aa1119101919fe87dc78c9CAS | 16902187PubMed |

Schwartz, J., and Morrison, J. L. (2005). Impact and mechanisms of fetal physiological programming. Am. J. Physiol. Regul. Integr. Comp. Physiol. 288, R11–R15.
Impact and mechanisms of fetal physiological programming.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVCqtbs%3D&md5=0004417348c4278ddfc5122d3642ed0eCAS | 15590991PubMed |

Seckl, J. R., and Meaney, M. J. (2004). Glucocorticoid programming. Ann. N. Y. Acad. Sci. 1032, 63–84.
Glucocorticoid programming.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXislWitLY%3D&md5=18b11ab03be095d7ec5b4f2d95299883CAS | 15677396PubMed |

Shaikh, S., Bloomfield, F. H., Bauer, M. K., Phua, H. H., Gilmour, R. S., and Harding, J. E. (2005). Amniotic IGF-I supplementation of growth-restricted fetal sheep alters IGF-I and IGF receptor type 1 mRNA and protein levels in placental and fetal tissues. J. Endocrinol. 186, 145–155.
Amniotic IGF-I supplementation of growth-restricted fetal sheep alters IGF-I and IGF receptor type 1 mRNA and protein levels in placental and fetal tissues.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmvV2ht78%3D&md5=e2915f97ac300aa89c50cb21a006d601CAS | 16002544PubMed |

Shen, W., Wisniowski, P., Ahmed, L., Boyle, D. W., Denne, S. C., and Liechty, E. A. (2003). Protein anabolic effects of insulin and IGF-I in the ovine fetus. Am. J. Physiol. Endocrinol. Metab. 284, E748–E756.
| 1:CAS:528:DC%2BD3sXjtlykurs%3D&md5=80672c3f45a59381d0cee9afa6abbde2CAS | 12488244PubMed |

Sipes, S. L., and Malee, M. P. (1992). Endocrine disorders in pregnancy. Obstet. Gynecol. Clin. North Am. 19, 655–677.
| 1:STN:280:DyaK3s7jtlGhsw%3D%3D&md5=e06115bb1b25bb99a2fbce24065686acCAS | 1484653PubMed |

Straus, D. S., Ooi, G. T., Orlowski, C. C., and Rechler, M. M. (1991). Expression of the genes for insulin-like growth factor-I (IGF-I), IGF-II and IGF-binding proteins-1 and -2 in fetal rat under conditions of intrauterine growth retardation caused by maternal fasting. Endocrinology 128, 518–525.
Expression of the genes for insulin-like growth factor-I (IGF-I), IGF-II and IGF-binding proteins-1 and -2 in fetal rat under conditions of intrauterine growth retardation caused by maternal fasting.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXpsFOnsw%3D%3D&md5=873109ec021d9dbee0da094cb14cf010CAS | 1846108PubMed |

Tönshoff, B., and Mehls, O. (1996). Interaction between glucocorticoids and the somatotrophic axis. Acta Paediatr. Suppl. 85, 72–75.
Interaction between glucocorticoids and the somatotrophic axis.Crossref | GoogleScholarGoogle Scholar |

Unterman, T., Lascon, R., Gotway, M. B., Oehler, D., Gounis, A., Simmons, R. A., and Ogata, E. S. (1990). Circulating levels of insulin-like growth factor-binding protein-1 (IGFBP-1) and hepatic mRNA are increased in the small-for-gestational age (SGA) fetal rat. Endocrinology 127, 2035–2037.
Circulating levels of insulin-like growth factor-binding protein-1 (IGFBP-1) and hepatic mRNA are increased in the small-for-gestational age (SGA) fetal rat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXmtV2gsbk%3D&md5=8da8a636ea027770daaff998ced172e2CAS | 1698152PubMed |

Wood, C. E. (1988). Are fetal adrenocorticotropic hormone and renin secretion suppressed by maternal cortisol secretion? Am. J. Physiol. 255, R412–R417.
| 1:CAS:528:DyaL1cXls1eksLw%3D&md5=57e57f019ccf59179375aac85244ffc4CAS | 2843058PubMed |

Wood, C. E., and Rudolph, A. M. (1984). Can maternal stress alter fetal adrenocorticotropin secretion? Endocrinology 115, 298–301.
Can maternal stress alter fetal adrenocorticotropin secretion?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXks1Kgu7Y%3D&md5=4f0843e795025c9705be447051063137CAS | 6329652PubMed |

Wood, C. E., Cudd, T. A., Kane, C., and Engelke, K. (1993). Fetal ACTH and blood pressure responses to thromboxane mimetic U-46619. Am. J. Physiol. 265, R858–R862.
| 1:CAS:528:DyaK2cXisVaitw%3D%3D&md5=8774fa21ce94a3a38c831af431416eeaCAS | 8238457PubMed |