Fetal brain 11β-hydroxysteroid dehydrogenase type 2 selectively determines programming of adult depressive-like behaviors and cognitive function, but not anxiety behaviors in male mice

Psychoneuroendocrinology

Volumn 59, Issue , 2015, Pages 59-70

  Wyrwoll, Caitlin ^a,c   Keith, Marianne ^a   Noble, June ^a   Stevenson, Paula L ^a   Bombail, Vincent ^a   Crombie, Sandra ^a   Evans, Louise C ^a   Bailey, Matthew A ^a   Wood, Emma ^b   Seckl, Jonathan R ^a   Holmes, Megan C ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

Affective behaviors; Brain 11 HSD2; Developmental programming; Glucocorticoids

Indexed keywords

11BETA HYDROXYSTEROID DEHYDROGENASE; CORTICOSTERONE; GLUCOCORTICOID; NEUROTRANSMITTER; 11BETA HYDROXYSTEROID DEHYDROGENASE 2;

ADULT; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; BRAIN FUNCTION; CATALYSIS; COGNITION; COGNITIVE DEFECT; CONTROLLED STUDY; DEPRESSION; ENZYME DEFICIENCY; FETUS CIRCULATION; FETUS DEVELOPMENT; FETUS GROWTH; HIPPOCAMPUS; MALE; MOUSE; NONHUMAN; PATHOGENESIS; PLACENTA; PLACENTA DEVELOPMENT; PREGNANCY; PRIORITY JOURNAL; WILD TYPE; ANIMAL; ANXIETY DISORDER; BLOOD; BRAIN; DISEASE MODEL; EMBRYOLOGY; ENZYMOLOGY; FEMALE; FETOMATERNAL TRANSFUSION; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY; RISK FACTOR;

11-BETA-HYDROXYSTEROID DEHYDROGENASE TYPE 2; ANIMALS; ANXIETY DISORDERS; BRAIN; DEPRESSIVE DISORDER; DISEASE MODELS, ANIMAL; FEMALE; FETAL DEVELOPMENT; GLUCOCORTICOIDS; MALE; MATERNAL-FETAL EXCHANGE; MICE; MICE, KNOCKOUT; PLACENTA; PREGNANCY; RISK FACTORS; STRESS, PHYSIOLOGICAL;

EID: 84937408145     PISSN: 03064530     EISSN: 18733360     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2015.05.003     Document Type: Article

References (60)

1. Barker G.R., Bird F., Alexander V., Warburton E.C. Recognition memory for objects, place, and temporal order: a disconnection analysis of the role of the medial prefrontal cortex and perirhinal cortex. J. Neurosci. 2007, 27:2948-2957.
2. Barker G.R., Warburton E.C. When is the hippocampus involved in recognition memory?. J. Neurosci. 2011, 31:10721-10731.
3. Benediktsson R., Calder A.A., Edwards C.R., Seckl J.R. Placental 11 beta-hydroxysteroid dehydrogenase: a key regulator of fetal glucocorticoid exposure. Clin. Endocrinol. (Oxf.) 1997, 46:161-166.
4. Bhagwagar Z., Rabiner E.A., Sargent P.A., Grasby P.M., Cowen P.J. Persistent reduction in brain serotonin1A receptor binding in recovered depressed men measured by positron emission tomography with [11C]WAY-100635. Mol. Psychiatry 2004, 9:386-392.
5. Blier P., Ward N.M. Is there a role for 5-HT1A agonists in the treatment of depression?. Biol. Psychiatry 2003, 53:193-203.
6. Brown R.W., Chapman K.E., Edwards C.R., Seckl J.R. Human placental 11 beta-hydroxysteroid dehydrogenase: evidence for and partial purification of a distinct NAD-dependent isoform. Endocrinology 1993, 132:2614-2621.
7. Brown R.W., Diaz R., Robson A.C., Kotelevtsev Y.V., Mullins J.J., Kaufman M.H., Seckl J.R. The ontogeny of 11 beta-hydroxysteroid dehydrogenase type 2 and mineralocorticoid receptor gene expression reveal intricate control of glucocorticoid action in development. Endocrinology 1996, 137:794-797.
8. Brown R.W., Kotolevtsev Y., Leckie C., Lindsay R.S., Lyons V., Murad P., Mullins J.J., Chapman K.E., Edwards C.R.W., Seckl J.R. Isolation and cloning of human placental 11β-hydroxysteroid dehydrogenase-2 cDNA. Biochem. J 1996, 313:1007-1017.
9. Burton P.J., Smith R.E., Krozowski Z.S., Waddell B.J. Zonal distribution of 11 beta-hydroxysteroid dehydrogenase types 1 and 2 messenger ribonucleic acid expression in the rat placenta and decidua during late pregnancy. Biol. Reprod. 1996, 55:1023-1028.
10. Cannizzaro C., Plescia F., Martire M., Gagliano M., Cannizzaro G., Mantia G., Cannizzaro E. Single, intense prenatal stress decreases emotionality and enhances learning performance in the adolescent rat offspring: interaction with a brief, daily maternal separation. Behav. Brain Res. 2006, 169:128-136.
11. Constancia M., Angiolini E., Sandovici I., Smith P., Smith R., Kelsey G., Dean W., Ferguson-Smith A., Sibley C.P., Reik W., Fowden A. Adaptation of nutrient supply to fetal demand in the mouse involves interaction between the Igf2 gene and placental transporter systems. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:19219-19224.
12. Cost K.T., Lobell T.D., Williams-Yee Z.N., Henderson S., Dohanich G. The effects of pregnancy, lactation, and primiparity on object-in-place memory of female rats. Horm. Behav. 2014, 65:32-39.
13. Cottrell E.C., Holmes M.C., Livingstone D.E., Kenyon C.J., Seckl J.R. Reconciling the nutritional and glucocorticoid hypotheses of fetal programming. FASEB J. 2012, 26:1866-1874.
14. Cottrell E.C., Seckl J.R. Prenatal stress, glucocorticoids and the programming of adult disease. Front. Behav. Neurosci. 2009, 3:19.
15. Cottrell E.C., Seckl J.R., Holmes M.C., Wyrwoll C.S. Foetal and placental 11beta-HSD2: a hub for developmental programming. Acta Physiol. (Oxf) 2014, 210:288-295.
16. Diaz R., Brown R.W., Seckl J.R. 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. 1998, 18:2570-2580.
17. Franklin T.B., Linder N., Russig H., Thony B., Mansuy I.M. Influence of early stress on social abilities and serotonergic functions across generations in mice. PLoS ONE 2011, 6:e21842.
18. Gartside S.E., Johnson D.A., Leitch M.M., Troakes C., Ingram C.D. Early life adversity programs changes in central 5-HT neuronal function in adulthood. Eur. J. Neurosci. 2003, 17:2401-2408.
19. Goodfellow N.M., Benekareddy M., Vaidya V.A., Lambe E.K. Layer II/III of the prefrontal cortex: inhibition by the serotonin 5-HT1A receptor in development and stress. J. Neurosci. 2009, 29:10094-10103.
20. Harris A., Seckl J. Glucocorticoids, prenatal stress and the programming of disease. Horm. Behav. 2011, 59:279-289.
21. Harris H.J., Kotelevtsev Y., Mullins J.J., Seckl J.R., Holmes M.C. Intracellular regeneration of glucocorticoids by 11beta-hydroxysteroid dehydrogenase (11beta-HSD)-1 plays a key role in regulation of the hypothalamic-pituitary-adrenal axis: analysis of 11beta-HSD-1-deficient mice. Endocrinology 2001, 142:114-120.
22. Hewitt D.P., Mark P.J., Waddell B.J. Glucocorticoids prevent the normal increase in placental vascular endothelial growth factor expression and placental vascularity during late pregnancy in the rat. Endocrinology 2006, 147:5568-5574.
23. Holmes M.C., Abrahamsen C.T., French K.L., Paterson J.M., Mullins J.J., Seckl J.R. 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. 2006, 26:3840-3844.
24. Holmes M.C., French K.L., Seckl J.R. Dysregulation of diurnal rhythms of serotonin 5-HT2C and corticosteroid receptor gene expression in the hippocampus with food restriction and glucocorticoids. J. Neurosci. 1997, 17:4056-4065.
25. Holmes M.C., Sangra M., French K.L., Whittle I.R., Paterson J., Mullins J.J., Seckl J.R. 11β-Hydroxysteroid dehydrogenase type 2 protects the neonatal cerebellum from deleterious effects of glucocorticoids. Neuroscience 2006, 137:865-873.
26. Hunter R.W., Craigie E., Homer N.Z., Mullins J.J., Bailey M.A. Acute inhibition of NCC does not activate distal electrogenic Na+ reabsorption or kaliuresis. Am. J. Physiol. Renal Physiol. 2014, 306:F457-F467.
27. Jensen Pena C., Monk C., Champagne F.A. Epigenetic effects of prenatal stress on 11beta-hydroxysteroid dehydrogenase-2 in the placenta and fetal brain. PLoS ONE 2012, 7:e39791.
28. Kamphuis P.J., Gardoni F., Kamal A., Croiset G., Bakker J.M., Cattabeni F., Gispen W.H., van Bel F., Di Luca M., Wiegant V.M. Long-lasting effects of neonatal dexamethasone treatment on spatial learning and hippocampal synaptic plasticity. Involvement of the NMDA receptor complex. FASEB J. 2003, 17:911-913.
29. Kanitz E., Otten W., Tuchscherer M., Grabner M., Brussow K.P., Rehfeldt C., Metges C.C. High and low protein ratio carbohydrate dietary ratios during gestation alter maternal-fetal cortisol regulation in pigs. PLoS ONE 2012, 7:e52748.
30. Karten Y.J., Nair S.M., van Essen L., Sibug R., Joels M. Long-term exposure to high corticosterone levels attenuates serotonin responses in rat hippocampal CA1 neurons. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:13456-13461.
31. Khashan A.S., McNamee R., Henriksen T.B., Pedersen M.G., Kenny L.C., Abel K.M., Mortensen P.B. Risk of affective disorders following prenatal exposure to severe life events: a Danish population-based cohort study. J. Psychiatr. Res. 2011, 45:879-885.
32. Krugers H.J., Lucassen P.J., Karst H., Joels M. Chronic stress effects on hippocampal structure and synaptic function: relevance for depression and normalization by anti-glucocorticoid treatment. Front. Synaptic Neurosci. 2010, 2:24.
33. Langley-Evans S.C., Phillips G.J., Benediktsson R., Gardner D.S., Edwards C.R., Jackson A.A., Seckl J.R. Protein intake in pregnancy, placental glucocorticoid metabolism and the programming of hypertension in the rat. Placenta 1996, 17:169-172.
34. Lemaire V., Koehl M., Le Moal M., Abrous D.N. Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:11032-11037.
35. Lucassen P.J., Bosch O.J., Jousma E., Kromer S.A., Andrew R., Seckl J.R., Neumann I.D. Prenatal stress reduces postnatal neurogenesis in rats selectively bred for high, but not low, anxiety: possible key role of placental 11beta-hydroxysteroid dehydrogenase type 2. Eur. J. Neurosci. 2009, 29:97-103.
36. 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. Maternal stress alters endocrine function of the feto-placental unit in rats. Am. J. Physiol. Endocrinol. Metab. 2007, 292:E1526-E1533.
37. Marrocco J., Reynaert M.L., Gatta E., Gabriel C., Mocaer E., Di Prisco S., Merega E., Pittaluga A., Nicoletti F., Maccari S., Morley-Fletcher S., Mairesse J. The effects of antidepressant treatment in prenatally stressed rats support the glutamatergic hypothesis of stress-related disorders. J. Neurosci. 2014, 34:2015-2024.
38. Miyagawa K., Tsuji M., Fujimori K., Saito Y., Takeda H. Prenatal stress induces anxiety-like behavior together with the disruption of central serotonin neurons in mice. Neurosci. Res. 2011, 70:111-117.
39. Mombereau C., Gur T.L., Onksen J., Blendy J.A. Differential effects of acute and repeated citalopram in mouse models of anxiety and depression. Int. J. Neuropsychopharmacol. 2010, 13:321-334.
40. Mueller B.R., Bale T.L. Sex-specific programming of offspring emotionality after stress early in pregnancy. J. Neurosci. 2008, 28:9055-9065.
41. Muneoka K., Mikuni M., Ogawa T., Kitera K., Kamei K., Takigawa M., Takahashi K. Prenatal dexamethasone exposure alters brain monoamine metabolism and adrenocortical response in rat offspring. Am. J. Physiol. 1997, 273:R1669-R1675.
42. O'Donnell K.J., Bugge Jensen A., Freeman L., Khalife N., O'Connor T.G., Glover V. Maternal prenatal anxiety and downregulation of placental 11beta-HSD2. Psychoneuroendocrinology 2012, 37:818-826.
43. Pesonen A.K., Raikkonen K., Lano A., Peltoniemi O., Hallman M., Kari M.A. Antenatal betamethasone and fetal growth in prematurely born children: implications for temperament traits at the age of 2 years. Pediatrics 2009, 123:e31-e37.
44. Pryce C.R., Aubert Y., Maier C., Pearce P.C., Fuchs E. The developmental impact of prenatal stress, prenatal dexamethasone and postnatal social stress on physiology, behaviour and neuroanatomy of primate offspring: studies in rhesus macaque and common marmoset. Psychopharmacology (Berl) 2011, 214:33-53.
45. Raikkonen K., Pesonen A.K., Heinonen K., Lahti J., Komsi N., Eriksson J.G., Seckl J.R., Jarvenpaa A.L., Strandberg T.E. Maternal licorice consumption and detrimental cognitive and psychiatric outcomes in children. Am. J. Epidemiol. 2009, 170:1137-1146.
46. 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. Maternal prenatal licorice consumption alters hypothalamic-pituitary-adrenocortical axis function in children. Psychoneuroendocrinology 2010, 35:1587-1593.
47. Rasmuson S., Olsson T., Henriksson B.G., Kelly P.A., Holmes M.C., Seckl J.R., Mohammed A.H. Environmental enrichment selectively increases 5-HT1A receptor mRNA expression and binding in the rat hippocampus. Brain Res. Mol. Brain Res. 1998, 53:285-290.
48. Sargent P.A., Kjaer K.H., Bench C.J., Rabiner E.A., Messa C., Meyer J., Gunn R.N., Grasby P.M., Cowen P.J. Brain serotonin1A receptor binding measured by positron emission tomography with [11C]WAY-100635: effects of depression and antidepressant treatment. Arch. Gen. Psychiatry 2000, 57:174-180.
49. Steru L., Chermat R., Thierry B., Simon P. The tail suspension test: a new method for screening antidepressants in mice. Psychopharmacology (Berl) 1985, 85:367-370.
50. Trautman P.D., Meyer-Bahlburg H.F.L., Postelnek J., New M.I. Effects of early prenatal dexamethasone on the cognitive and behavioral development of young children: results of a pilot study. Psychoneuroendocrinology 1995, 20:439-449.
51. Tronche F., Kellendonk C., Kretz O., Gass P., Anlag K., Orban P.C., Bock R., Klein R., Schütz G. Disruption of the glucocorticoid receptor gene in the nervous system results in reduced anxiety. Nat. Genet. 1999, 23:99-103.
52. Van den Hove D.L., Lauder J.M., Scheepens A., Prickaerts J., Blanco C.E., Steinbusch H.W. Prenatal stress in the rat alters 5-HT1A receptor binding in the ventral hippocampus. Brain Res. 2006, 1090:29-34.
53. van Riel E., Meijer O.C., Steenbergen P.J., Joels M. Chronic unpredictable stress causes attenuation of serotonin responses in cornu ammonis 1 pyramidal neurons. Neuroscience 2003, 120:649-658.
54. Weinstock M. The long-term behavioural consequences of prenatal stress. Neurosci. Biobehav. Rev. 2008, 32:1073-1086.
55. Welberg L.A., Seckl J.R., Holmes M.C. 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. 2000, 12:1047-1054.
56. Wyrwoll C.S., Holmes M.C. Prenatal excess glucocorticoid exposure and adult affective disorders: a role for serotonergic and catecholamine pathways. Neuroendocrinology 2012, 95:47-55.
57. Wyrwoll C.S., Seckl J.R., Holmes M.C. Altered placental function of 11beta-hydroxysteroid dehydrogenase 2 knockout mice. Endocrinology 2009, 150:1287-1293.
58. Yaka R., Salomon S., Matzner H., Weinstock M. Effect of varied gestational stress on acquisition of spatial memory, hippocampal LTP and synaptic proteins in juvenile male rats. Behav. Brain Res. 2007, 179:126-132.
59. Yau J.L., Noble J., Kenyon C.J., Hibberd C., Kotelevtsev Y., Mullins J.J., Seckl J.R. Lack of tissue glucocorticoid reactivation in 11beta -hydroxysteroid dehydrogenase type 1 knockout mice ameliorates age-related learning impairments. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:4716-4721.
60. Yeh T., Lin Y., Lin H., Huang C., Hsieh W., Lin C., Tsai C. Outcomes at school age after postnatal dexamethasone therapy for lung disease of prematurity. N. Engl. J. Med. 2004, 350:1304-1313.