Foetal and placental 11β-HSD2: A hub for developmental programming

Acta Physiologica

Volumn 210, Issue 2, 2014, Pages 288-295

  Cottrell, E C ^a   Seckl, J R ^b   Holmes, M C ^b   Wyrwoll, C S ^c  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

11 hydroxysteroid dehydrogenase type 2; Anxiety; Developmental programming; Glucocorticoids; Hypothalamic pituitary adrenal axis

Indexed keywords

11BETA HYDROXYSTEROID DEHYDROGENASE 2; GLUCOCORTICOID;

ANIMAL BEHAVIOR; BEHAVIOR DISORDER; DISEASE ASSOCIATION; EXPOSURE; FETUS DEVELOPMENT; HEART DISEASE; MENTAL DISEASE; METABOLIC DISORDER; NERVE CELL DIFFERENTIATION; NEUROLOGIC DISEASE; NONHUMAN; PLACENTA DEVELOPMENT; PLACENTA FUNCTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; ANIMAL; EMBRYOLOGY; FEMALE; FETAL GROWTH RETARDATION; FETUS; METABOLIC SYNDROME X; METABOLISM; MOUSE; PHYSIOLOGY; PLACENTA; PREGNANCY;

11-BETA-HYDROXYSTEROID DEHYDROGENASE TYPE 2; ANIMALS; FEMALE; FETAL DEVELOPMENT; FETAL GROWTH RETARDATION; FETUS; GLUCOCORTICOIDS; METABOLIC SYNDROME X; MICE; PLACENTA; PREGNANCY;

EID: 84892421699     PISSN: 17481708     EISSN: 17481716     Source Type: Journal    
DOI: 10.1111/apha.12187     Document Type: Review

References (56)

1. Aiken, C.E. & Ozanne, S.E. 2013. Sex differences in developmental programming models. Reproduction 145, R1-R13.
2. Barker, D.J., Winter, P.D., Osmond, C., Margetts, B. & Simmonds, S.J. 1989. Weight in infancy and death from ischaemic heart disease. Lancet 2, 577-580.
3. Benassayag, C., Souski, I., Mignot, T.M., Robert, B., Hassid, J., Duc-Goiran, P., Mondon, F., Rebourcet, R., Dehennin, L., Nunez, E.A. & Ferre, F. 2001. Corticosteroid-binding globulin status at the fetomaternal interface during human term pregnancy. Biol Reprod 64, 812-821.
4. Benediktsson, R., Lindsay, R.S., Noble, J., Seckl, J.R. & Edwards, C.R. 1993. Glucocorticoid exposure in utero: new model for adult hypertension. Lancet 341, 339-341.
5. Bernstein, I.M., Horbar, J.D., Badger, G.J., Ohlsson, A. & Golan, A. 2000. Morbidity and mortality among very-low-birth-weight neonates with intrauterine growth restriction. The Vermont Oxford Network. Am J Obstet Gynecol 182, 198-206.
6. Blasco, M.J., Lopez Bernal, A. & Turnbull, A.C. 1986. 11 Beta-hydroxysteroid dehydrogenase activity of the human placenta during pregnancy. Horm Metab Res 18, 638-641.
7. Bloomfield, F.H., Oliver, M.H., Giannoulias, C.D., Gluckman, P.D., Harding, J.E. & Challis, J.R. 2003. Brief undernutrition in late-gestation sheep programs the hypothalamic-pituitary-adrenal axis in adult offspring. Endocrinology 144, 2933-2940.
8. Bolten, M.I., Wurmser, H., Buske-Kirschbaum, A., Papousek, M., Pirke, K.M. & Hellhammer, D. 2011. Cortisol levels in pregnancy as a psychobiological predictor for birth weight. Arch Womens Ment Health 14, 33-41.
9. Brown, R.W., Diaz, R., Robson, A.C., Kotelevtsev, Y.V., Mullins, J.J., Kaufman, M.H. & Seckl, J.R. 1996. The ontogeny of 11beta-hydroxysteroid dehydrogenase type 2 and mineralocorticoid receptor gene expression reveal intricate control of glucocorticoid action in development. Endocrinology 137, 794-797.
10. Buss, C., Davis, E.P., Muftuler, L.T., Head, K. & Sandman, C.A. 2010. High pregnancy anxiety during mid-gestation is associated with decreased gray matter density in 6-9-year-old children. Psychoneuroendocrinology 35, 141-153.
11. Challis, J.R., Berdusco, E.T., Jeffray, T.M., Yang, K. & Hammond, G.L. 1995. Corticosteroid-binding globulin (CBG) in fetal development. J Steroid Biochem Mol Biol 53, 523-527.
12. Challis, J.R., Sloboda, D., Matthews, S.G., Holloway, A., Alfaidy, N., Patel, F.A., Whittle, W., Fraser, M., Moss, T.J. & Newnham, J. 2001. The fetal placental hypothalamic-pituitary-adrenal (HPA) axis, parturition and post natal health. Mol Cell Endocrinol 185, 135-144.
13. Clifton, V.L. 2005. Sexually dimorphic effects of maternal asthma during pregnancy on placental glucocorticoid metabolism and fetal growth. Cell Tissue Res 322, 63-71.
14. Cottrell, E.C. & Seckl, J.R. 2009. Prenatal stress, glucocorticoids and the programming of adult disease. Front Behav Neurosci 3, 19.
15. Cottrell, E.C., Holmes, M.C., Livingstone, D.E., Kenyon, C.J. & Seckl, J.R. 2012. Reconciling the nutritional and glucocorticoid hypotheses of fetal programming. FASEB J 26, 1866-1874.
16. Cuffe, J.S., Dickinson, H., Simmons, D.G. & Moritz, K.M. 2011. Sex specific changes in placental growth and MAPK following short term maternal dexamethasone exposure in the mouse. Placenta 32, 981-989.
17. Dave-Sharma, S., Wilson, R.C., Harbison, M.D., Newfield, R., Azar, M.R., Krozowski, Z.S., Funder, J.W., Shackleton, C.H., Bradlow, H.L., Wei, J.Q. et al. 1998. Examination of genotype and phenotype relationships in 14 patients with apparent mineralocorticoid excess. J Clin Endocrinol Metab 83, 2244-2254.
18. Diaz, R., Brown, R.W. & Seckl, J.R. 1998. Distinct ontogeny of glucocorticoid and mineralocorticoid receptor and 11beta-hydroxysteroid dehydrogenase types I and II mRNAs in the fetal rat brain suggest a complex control of glucocorticoid actions. J Neurosci 18, 2570-2580.
19. Draper, N. & Stewart, P.M. 2005. 11beta-hydroxysteroid dehydrogenase and the pre-receptor regulation of corticosteroid hormone action. J Endocrinol 186, 251-271.
20. Edwards, C.R., Benediktsson, R., Lindsay, R.S. & Seckl, J.R. 1993. Dysfunction of placental glucocorticoid barrier: link between fetal environment and adult hypertension? Lancet 341, 355-357.
21. Godfrey, K.M. & Barker, D.J. 2001. Fetal programming and adult health. Public Health Nutr 4, 611-624.
22. Goedhart, G., Vrijkotte, T.G., Roseboom, T.J., van der Wal, M.F., Cuijpers, P. & Bonsel, G.J. 2010. Maternal cortisol and offspring birthweight: results from a large prospective cohort study. Psychoneuroendocrinology 35, 644-652.
23. Goland, R.S., Jozak, S., Warren, W.B., Conwell, I.M., Stark, R.I. & Tropper, P.J. 1993. Elevated levels of umbilical cord plasma corticotropin-releasing hormone in growth-retarded fetuses. J Clin Endocrinol Metab 77, 1174-1179.
24. Holmes, M.C. & Seckl, J.R. 2006. The role of 11beta-hydroxysteroid dehydrogenases in the brain. Mol Cell Endocrinol 248, 9-14.
25. Holmes, M.C., Abrahamsen, C.T., French, K.L., Paterson, J.M., Mullins, J.J. & Seckl, J.R. 2006a. The mother or the fetus? 11beta-hydroxysteroid dehydrogenase type 2 null mice provide evidence for direct fetal programming of behavior by endogenous glucocorticoids. J Neurosci 26, 3840-3844.
26. Holmes, M.C., Sangra, M., French, K.L., Whittle, I.R., Paterson, J., Mullins, J.J. & Seckl, J.R. 2006b. 11Beta-hydroxysteroid dehydrogenase type 2 protects the neonatal cerebellum from deleterious effects of glucocorticoids. Neuroscience 137, 865-873.
27. Jung, C., Ho, J.T., Torpy, D.J., Rogers, A., Doogue, M., Lewis, J.G., Czajko, R.J. & Inder, W.J. 2011. A longitudinal study of plasma and urinary cortisol in pregnancy and postpartum. J Clin Endocrinol Metab 96, 1533-1540.
28. Kotelevtsev, Y., Brown, R.W., Fleming, S., Kenyon, C., Edwards, C.R., Seckl, J.R. & Mullins, J.J. 1999. Hypertension in mice lacking 11beta-hydroxysteroid dehydrogenase type 2. J Clin Invest 103, 683-689.
29. Langley-Evans, S.C., Phillips, G.J., Benediktsson, R., Gardner, D.S., Edwards, C.R., Jackson, A.A. & Seckl, J.R. 1996. Protein intake in pregnancy, placental glucocorticoid metabolism and the programming of hypertension in the rat. Placenta 17, 169-172.
30. Laplante, D.P., Brunet, A., Schmitz, N., Ciampi, A. & King, S. 2008. Project Ice Storm: prenatal maternal stress affects cognitive and linguistic functioning in 5 1/2-year-old children. J Am Acad Child Adolesc Psychiatry 47, 1063-1072.
31. Lindsay, R.S., Lindsay, R.M., Edwards, C.R. & Seckl, J.R. 1996. Inhibition of 11-beta-hydroxysteroid dehydrogenase in pregnant rats and the programming of blood pressure in the offspring. Hypertension 27, 1200-1204.
32. Mairesse, J., Lesage, J., Breton, C., Breant, B., Hahn, T., Darnaudery, M., Dickson, S.L., Seckl, J., Blondeau, B., Vieau, D., Maccari, S. & Viltart, O. 2007. Maternal stress alters endocrine function of the feto-placental unit in rats. Am J Physiol Endocrinol Metab 292, E1526-E1533.
33. McTernan, C.L., Draper, N., Nicholson, H., Chalder, S.M., Driver, P., Hewison, M., Kilby, M.D. & Stewart, P.M. 2001. Reduced placental 11beta-hydroxysteroid dehydrogenase type 2 mRNA levels in human pregnancies complicated by intrauterine growth restriction: an analysis of possible mechanisms. J Clin Endocrinol Metab 86, 4979-4983.
34. Murphy, B.E., Clark, S.J., Donald, I.R., Pinsky, M. & Vedady, D. 1974. Conversion of maternal cortisol to cortisone during placental transfer to the human fetus. Am J Obstet Gynecol 118, 538-541.
35. Newsome, C.A., Shiell, A.W., Fall, C.H., Phillips, D.I., Shier, R. & Law, C.M. 2003. Is birth weight related to later glucose and insulin metabolism? - a systematic review. Diabet Med 20, 339-348.
36. Nyirenda, M.J., Lindsay, R.S., Kenyon, C.J., Burchell, A. & Seckl, J.R. 1998. Glucocorticoid exposure in late gestation permanently programs rat hepatic phosphoenolpyruvate carboxykinase and glucocorticoid receptor expression and causes glucose intolerance in adult offspring. J Clin Invest 101, 2174-2181.
37. O'Connor, T.G., Ben-Shlomo, Y., Heron, J., Golding, J., Adams, D. & Glover, V. 2005. Prenatal anxiety predicts individual differences in cortisol in pre-adolescent children. Biol Psychiatry 58, 211-217.
38. O'Donnell, K.J., Bugge Jensen, A., Freeman, L., Khalife, N., O'Connor, T.G. & Glover, V. 2012. Maternal prenatal anxiety and downregulation of placental 11beta-HSD2. Psychoneuroendocrinology 37, 818-826.
39. Phillips, D.I., Barker, D.J., Fall, C.H., Seckl, J.R., Whorwood, C.B., Wood, P.J. & Walker, B.R. 1998. Elevated plasma cortisol concentrations: a link between low birth weight and the insulin resistance syndrome? J Clin Endocrinol Metab 83, 757-760.
40. Phillips, D.I., Walker, B.R., Reynolds, R.M., Flanagan, D.E., Wood, P.J., Osmond, C., Barker, D.J. & Whorwood, C.B. 2000. Low birth weight predicts elevated plasma cortisol concentrations in adults from 3 populations. Hypertension 35, 1301-1306.
41. Raikkonen, K., Pesonen, A.K., Heinonen, K., Lahti, J., Komsi, N., Eriksson, J.G., Seckl, J.R., Jarvenpaa, A.L. & Strandberg, T.E. 2009. Maternal licorice consumption and detrimental cognitive and psychiatric outcomes in children. Am J Epidemiol 170, 1137-1146.
42. Raikkonen, K., Seckl, J.R., Heinonen, K., Pyhala, R., Feldt, K., Jones, A., Pesonen, A.K., Phillips, D.I., Lahti, J., Jarvenpaa, A.L., Eriksson, J.G., Matthews, K.A., Strandberg, T.E. & Kajantie, E. 2010. Maternal prenatal licorice consumption alters hypothalamic-pituitary-adrenocortical axis function in children. Psychoneuroendocrinology 35, 1587-1593.
43. Reynolds, R.M. 2013. Glucocorticoid excess and the developmental origins of disease: two decades of testing the hypothesis-2012 Curt Richter Award Winner. Psychoneuroendocrinology 38, 1-11.
44. Shams, M., Kilby, M.D., Somerset, D.A., Howie, A.J., Gupta, A., Wood, P.J., Afnan, M. & Stewart, P.M. 1998. 11Beta-hydroxysteroid dehydrogenase type 2 in human pregnancy and reduced expression in intrauterine growth restriction. Hum Reprod 13, 799-804.
45. Stewart, P.M., Murry, B.A. & Mason, J.I. 1994. Type 2 11 beta-hydroxysteroid dehydrogenase in human fetal tissues. J Clin Endocrinol Metab 78, 1529-1532.
46. Stewart, P.M., Rogerson, F.M. & Mason, J.I. 1995. Type 2 11 beta-hydroxysteroid dehydrogenase messenger ribonucleic acid and activity in human placenta and fetal membranes: its relationship to birth weight and putative role in fetal adrenal steroidogenesis. J Clin Endocrinol Metab 80, 885-890.
47. Strandberg, T.E., Jarvenpaa, A.L., Vanhanen, H. & McKeigue, P.M. 2001. Birth outcome in relation to licorice consumption during pregnancy. Am J Epidemiol 153, 1085-1088.
48. Tang, J.I., Kenyon, C.J., Seckl, J.R. & Nyirenda, M.J. 2011. Prenatal overexposure to glucocorticoids programs renal 11beta-hydroxysteroid dehydrogenase type 2 expression and salt-sensitive hypertension in the rat. J Hypertens 29, 282-289.
49. Vieau, D., Sebaai, N., Leonhardt, M., Dutriez-Casteloot, I., Molendi-Coste, O., Laborie, C., Breton, C., Deloof, S. & Lesage, J. 2007. HPA axis programming by maternal undernutrition in the male rat offspring. Psychoneuroendocrinology 32(Suppl 1), S16-S20.
50. Welberg, L.A., Seckl, J.R. & Holmes, M.C. 2000. Inhibition of 11beta-hydroxysteroid dehydrogenase, the foeto-placental barrier to maternal glucocorticoids, permanently programs amygdala GR mRNA expression and anxiety-like behaviour in the offspring. Eur J Neurosci 12, 1047-1054.
51. Whincup, P.H., Kaye, S.J., Owen, C.G., Huxley, R., Cook, D.G., Anazawa, S., Barrett-Connor, E., Bhargava, S.K., Birgisdottir, B.E., Carlsson, S. et al. 2008. Birth weight and risk of type 2 diabetes: a systematic review. JAMA 300, 2886-2897.
52. Wyrwoll, C.S. & Holmes, M.C. 2011. Prenatal excess glucocorticoid exposure and adult affective disorders: a role for serotonergic and catecholamine pathways. Neuroendocrinology 95, 47-55.
53. Wyrwoll, C.S., Seckl, J.R. & Holmes, M.C. 2009. Altered placental function of 11beta-hydroxysteroid dehydrogenase 2 knockout mice. Endocrinology 150, 1287-1293.
54. Wyrwoll, C.S., Holmes, M.C. & Seckl, J.R. 2011. 11beta-hydroxysteroid dehydrogenases and the brain: from zero to hero, a decade of progress. Front Neuroendocrinol 32, 265-286.
55. Yehuda, R. & Seckl, J. 2011. Minireview: stress-related psychiatric disorders with low cortisol levels: a metabolic hypothesis. Endocrinology 152, 4496-4503.
56. Yehuda, R., Engel, S.M., Brand, S.R., Seckl, J., Marcus, S.M. & Berkowitz, G.S. 2005. Transgenerational effects of posttraumatic stress disorder in babies of mothers exposed to the World Trade Center attacks during pregnancy. J Clin Endocrinol Metab 90, 4115-4118.