Prenatal arsenic exposure alters the programming of the glucocorticoid signaling system during embryonic development

Neurotoxicology and Teratology

Volumn 47, Issue , 2015, Pages 66-79

  Caldwell, Katharine E ^a   Labrecque, Matthew T ^a   Solomon, Benjamin R ^a   Ali, Abdulmehdi ^b   Allan, Andrea M ^a  

^a UNIVERSITY OF NEW MEXICO SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NEW MEXICO   (United States)

Author keywords

11 hydroxysteroid dehydrogenase isozymes; Arsenic; Brain; Fetal; Glucocorticoid; Placenta

Indexed keywords

11BETA HYDROXYSTEROID DEHYDROGENASE 1; 11BETA HYDROXYSTEROID DEHYDROGENASE 2; ARSENIC; BRAIN PROTEIN; CORTICOTROPIN RELEASING FACTOR; GLUCOCORTICOID; GLUCOCORTICOID RECEPTOR; MESSENGER RNA; MINERALOCORTICOID RECEPTOR; FK 506 BINDING PROTEIN; TACROLIMUS BINDING PROTEIN 5;

ADULTHOOD; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN LEVEL; CONTROLLED STUDY; CORTICOSTEROID METABOLISM; CORTICOSTERONE BLOOD LEVEL; CROWN RUMP LENGTH; EMBRYO DEVELOPMENT; FEMALE; FETUS; FETUS DEVELOPMENT; GENE EXPRESSION; GESTATIONAL AGE; IMMUNOBLOTTING; MALE; MOUSE; NEGATIVE FEEDBACK; NONHUMAN; PLACENTA; PLACENTA WEIGHT; PRENATAL EXPOSURE; PROTEIN ANALYSIS; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; AGE; ANIMAL; ANIMAL EMBRYO; BLOOD; BRAIN; C57BL MOUSE; CHEMICALLY INDUCED; DOSE RESPONSE; DRUG EFFECTS; EMBRYOLOGY; GENE EXPRESSION REGULATION; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PREGNANCY; SEXUAL DEVELOPMENT;

AGE FACTORS; ANIMALS; ARSENIC; BRAIN; DOSE-RESPONSE RELATIONSHIP, DRUG; EMBRYO, MAMMALIAN; EMBRYONIC DEVELOPMENT; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLUCOCORTICOIDS; MALE; MICE; MICE, INBRED C57BL; PLACENTA; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RNA, MESSENGER; SEX CHARACTERISTICS; SIGNAL TRANSDUCTION; TACROLIMUS BINDING PROTEINS;

EID: 84912126343     PISSN: 08920362     EISSN: 18729738     Source Type: Journal    
DOI: 10.1016/j.ntt.2014.11.006     Document Type: Article

References (117)

1. Abou-Seif C., Shipman K.L., Allars M., Norris M.H., Chen Y.X., Smith R., et al. Tissue specific epigenetic differences in CRH gene expression. Front Biosci 2012, 17:713-725.
2. Ahir B.K., Sanders A.P., Rager J.E., Fry R.C. Systems biology and birth defects prevention: blockade of the glucocorticoid receptor prevents arsenic-induced birth defects. Environ Health Perspect 2013, 121:332-338.
3. Arnett M.G., Kolber B.J., Boyle M.P., Muglia L.J. Behavioral insights from mouse models of forebrain-and amygdala-specific glucocorticoid receptor genetic disruption. Mol Cell Endocrinol 2011, 336:2-5.
4. Barlow S.M., McElhatton P.R., Sullivan F.M. The relation between maternal restraint and food deprivation, plasma corticosterone, and induction of cleft palate in the offspring of mice. Teratology 1975, 12:97-103.
5. Barr F.D., Krohmer L.J., Hamilton J.W., Sheldon L.A. Disruption of histone modification and CARM1 recruitment by arsenic represses transcription at glucocorticoid receptor-regulated promoters. PLoS ONE 2009, 4:e6766.
6. Bellavance M.A., Rivest S. The HPA - immune axis and the immunomodulatory actions of glucocorticoids in the brain. Front Immunol 2014, 5:136.
7. Bodwell J.E., Kingsley L.A., Hamilton J.W. Arsenic at very low concentrations alters glucocorticoid receptor (GR)-mediated gene activation but not GR-mediated gene repression: complex dose-response effects are closely correlated with levels of activated GR and require a functional GR DNA binding domain. Chem Res Toxicol 2004, 17:1064-1076.
8. Bolten M., Nast I., Skrundz M., Stadler C., Hellhammer D.H., Meinlschmidt G. Prenatal programming of emotion regulation: neonatal reactivity as a differential susceptibility factor moderating the outcome of prenatal cortisol levels. J Psychosom Res 2013, 75:351-357.
9. Brown R.W., Diaz R., Robson A.C., Kotelevtsev Y.V., Mullins J.J., Kaufman M.H., et al. 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.
10. Brunton P.J., Russell J.A. Neuroendocrine control of maternal stress responses and fetal programming by stress in pregnancy. Prog Neuropsychopharmacol Biol Psychiatry 2011, 35:1178-1191.
11. Buckley C.T., Caldwell K.K. Two-layer antibody capture of enzymes on the surface of microtiter plates: application to the study of the regulation of phospholipase C-gamma1 catalytic activity. Anal Biochem 2003, 320:193-198.
12. Burnstein K.L., Bellingham D.L., Jewell C.M., Powell-Oliver F.E., Cidlowski J.A. Autoregulation of glucocorticoid receptor gene expression. Steroids 1991, 56:52-58.
13. Caldwell K.K., Sheema S., Paz R.D., Samudio-Ruiz S.L., Laughlin M.H., Spence N.E., et al. Fetal alcohol spectrum disorder-associated depression: evidence for reductions in the levels of brain-derived neurotrophic factor in a mouse model. Pharmacol Biochem Behav 2008, 90:614-624.
14. Caldwell K.K., Goggin S.L., Tyler C.R., Allan A.M. Prenatal alcohol exposure is associated with altered subcellular distribution of glucocorticoid and mineralocorticoid receptors in the adolescent mouse hippocampal formation. Alcohol Clin Exp Res 2014, 38:392-400.
15. Carter R.N., Paterson J.M., Tworowska U., Stenvers D.J., Mullins J.J., Seckl J.R., et al. Hypothalamic-pituitary-adrenal axis abnormalities in response to deletion of 11beta-HSD1 is strain-dependent. J Neuroendocrinol 2009, 21:879-887.
16. Caumette G., Ouypornkochagorn S., Scrimgeour C.M., Raab A., Feldmann J. Monitoring the arsenic and iodine exposure of seaweed-eating North Ronaldsay sheep from the gestational and suckling periods to adulthood by using horns as a dietary archive. Environ Sci Technol 2007, 41:2673-2679.
17. Chapman K., Holmes M., Seckl J. 11Beta-hydroxysteroid dehydrogenases: intracellular gate-keepers of tissue glucocorticoid action. Physiol Rev 2013, 93:1139-1206.
18. Chen Y., Parvez F., Gamble M., Islam T., Ahmed A., Argos M., et al. Arsenic exposure at low-to-moderate levels and skin lesions, arsenic metabolism, neurological functions, and biomarkers for respiratory and cardiovascular diseases: review of recent findings from the Health Effects of Arsenic Longitudinal Study (HEALS) in Bangladesh. Toxicol Appl Pharmacol 2009, 239:184-192.
19. Conradt E., Lester B.M., Appleton A.A., Armstrong D.A., Marsit C.J. The roles of DNA methylation of NR3C1 and 11beta-HSD2 and exposure to maternal mood disorder in utero on newborn neurobehavior. Epigenetics 2013, 8:1321-1329.
20. Davey J.C., Bodwell J.E., Gosse J.A., Hamilton J.W. Arsenic as an endocrine disruptor: effects of arsenic on estrogen receptor-mediated gene expression in vivo and in cell culture. Toxicol Sci 2007, 98:75-86.
21. de Kloet E.R., Karst H., Joels M. Corticosteroid hormones in the central stress response: quick-and-slow. Front Neuroendocrinol 2008, 29:268-272.
22. Dean F., Matthews S.G. Maternal dexamethasone treatment in late gestation alters glucocorticoid and mineralocorticoid receptor mRNA in the fetal guinea pig brain. Brain Res 1999, 846:253-259.
23. Douglas A.J., Brunton P.J., Bosch O.J., Russell J.A., Neumann I.D. Neuroendocrine responses to stress in mice: hyporesponsiveness in pregnancy and parturition. Endocrinology 2003, 144:5268-5276.
24. Erdeljan P., MacDonald J.F., Matthews S.G. Glucocorticoids and serotonin alter glucocorticoid receptor (GR) but not mineralocorticoid receptor (MR) mRNA levels in fetal mouse hippocampal neurons, in vitro. Brain Res 2001, 896:130-136.
25. Fei D.L., Koestler D.C., Li Z., Giambelli C., Sanchez-Mejias A., Gosse J.A., et al. Association between in utero arsenic exposure, placental gene expression, and infant birth weight: a US birth cohort study. Environ Health 2013, 12:58.
26. Ferreccio C., Smith A.H., Duran V., Barlaro T., Benitez H., Valdes R., et al. Case-control study of arsenic in drinking water and kidney cancer in uniquely exposed Northern Chile. Am J Epidemiol 2013, 178:813-818.
27. Gennari-Moser C., Khankin E.V., Schuller S., Escher G., Frey B.M., Portmann C.B., et al. Regulation of placental growth by aldosterone and cortisol. Endocrinology 2011, 152:263-271.
28. Gilsbach R., Kouta M., Bonisch H., Bruss M. Comparison of in vitro and in vivo reference genes for internal standardization of real-time PCR data. Biotechniques 2006, 40:173-177.
29. Gluckman P.D., Hanson M.A., Beedle A.S. Early life events and their consequences for later disease: a life history and evolutionary perspective. Am J Hum Biol 2007, 19:1-19.
30. Goggin S.L., Labrecque M.T., Allan A.M. Perinatal exposure to 50ppb sodium arsenate induces hypothalamic-pituitary-adrenal axis dysregulation in male C57BL/6 mice. Neurotoxicology 2012, 33:1338-1345.
31. Goldstein J.M., Handa R.J., Tobet S.A. Disruption of fetal hormonal programming (prenatal stress) implicates shared risk for sex differences in depression and cardiovascular disease. Front Neuroendocrinol 2014, 35:140-158.
32. Gosse J.A., Taylor V.F., Jackson B.P., Hamilton J.W., Bodwell J.E. Monomethylated trivalent arsenic species disrupt steroid receptor interactions with their DNA response elements at non-cytotoxic cellular concentrations. J Appl Toxicol 2014, 34:498-505.
33. Govindan M.V., Pothier F., Leclerc S., Palaniswami R., Xie B. Human glucocorticoid receptor gene promotor-homologous down regulation. J Steroid Biochem Mol Biol 1991, 40:317-323.
34. Grino M., Young W.S., Burgunder J.M. Ontogeny of expression of the corticotropin-releasing factor gene in the hypothalamic paraventricular nucleus and of the proopiomelanocortin gene in rat pituitary. Endocrinology 1989, 124:60-68.
35. Hamilton J.W., Kaltreider R.C., Bajenova O.V., Ihnat M.A., McCaffrey J., Turpie B.W., et al. Molecular basis for effects of carcinogenic heavy metals on inducible gene expression. Environ Health Perspect 1998, 106(Suppl. 4):1005-1015.
36. Harris A., Seckl J. Glucocorticoids, prenatal stress and the programming of disease. Horm Behav 2011, 59:279-289.
37. 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.
38. Harris A.P., Holmes M.C., de Kloet E.R., Chapman K.E., Seckl J.R. Mineralocorticoid and glucocorticoid receptor balance in control of HPA axis and behaviour. Psychoneuroendocrinology 2013, 38:648-658.
39. He W., Greenwell R.J., Brooks D.M., Calderon-Garciduenas L., Beall H.D., Coffin J.D. Arsenic exposure in pregnant mice disrupts placental vasculogenesis and causes spontaneous abortion. Toxicol Sci 2007, 99:244-253.
40. Herman J.P., Patel P.D., Akil H., Watson S.J. Localization and regulation of glucocorticoid and mineralocorticoid receptor messenger RNAs in the hippocampal formation of the rat. Mol Endocrinol 1989, 3:1886-1894.
41. Herman J.P., McKlveen J.M., Solomon M.B., Carvalho-Netto E., Myers B. Neural regulation of the stress response: glucocorticoid feedback mechanisms. Braz J Med Biol Res 2012, 45:292-298. (et al.).
42. Holmes M.C., Seckl J.R. The role of 11beta-hydroxysteroid dehydrogenases in the brain. Mol Cell Endocrinol 2006, 248:9-14.
43. Huang C.C., Shih M.C., Hsu N.C., Chien Y., Chung B.C. Fetal glucocorticoid synthesis is required for development of fetal adrenal medulla and hypothalamus feedback suppression. Endocrinology 2012, 153:4749-4756.
44. Hughes M.F., Kenyon E.M., Edwards B.C., Mitchell C.T., Razo L.M., Thomas D.J. Accumulation and metabolism of arsenic in mice after repeated oral administration of arsenate. Toxicol Appl Pharmacol 2003, 191:202-210.
45. Jamieson P.M., Fuchs E., Flugge G., Seckl J.R. Attenuation of hippocampal 11beta-hydroxysteroid dehydrogenase type 1 by chronic psychosocial stress in the tree shrew. Stress 1997, 2:123-132.
46. Jaskoll T., Choy H.A., Chen H., Melnick M. Developmental expression and CORT-regulation of TGF-beta and EGF receptor mRNA during mouse palatal morphogenesis: correlation between CORT-induced cleft palate and TGF-beta 2 mRNA expression. Teratology 1996, 54:34-44.
47. Jin Y., Wang G., Zhao F., Liao Y., Sun D., Zhong Y., et al. Distribution of speciated arsenicals in mice exposed to arsenite at the early life. Ecotoxicol Environ Saf 2010, 73:1323-1326.
48. Joels M., Sarabdjitsingh R.A., Karst H. Unraveling the time domains of corticosteroid hormone influences on brain activity: rapid, slow, and chronic modes. Pharmacol Rev 2012, 64:901-938.
49. Joshi S.K., Shrestha S. Diabetes mellitus: a review of its associations with different environmental factors. Kathmandu Univ Med J 2010, 8:109-115.
50. Kalinyak J.E., Dorin R.I., Hoffman A.R., Perlman A.J. Tissue-specific regulation of glucocorticoid receptor mRNA by dexamethasone. J Biol Chem 1987, 262:10441-10444.
51. Kaltreider R.C., Davis A.M., Lariviere J.P., Hamilton J.W. Arsenic alters the function of the glucocorticoid receptor as a transcription factor. Environ Health Perspect 2001, 109:245-251.
52. Keegan C.E., Karolyi I.J., Knapp L.T., Bourbonais F.J., Camper S.A., Seasholtz A.F. Expression of corticotropin-releasing hormone transgenes in neurons of adult and developing mice. Mol Cell Neurosci 1994, 5:505-514.
53. Khalife N., Glover V., Taanila A., Ebeling H., Jarvelin M.R., Rodriguez A. Prenatal glucocorticoid treatment and later mental health in children and adolescents. PLoS ONE 2013, 8:e81394.
54. Khulan B., Drake A.J. Glucocorticoids as mediators of developmental programming effects. Best Pract Res Clin Endocrinol Metab 2012, 26:689-700.
55. Kitchin K.T., Wallace K. The role of protein binding of trivalent arsenicals in arsenic carcinogenesis and toxicity. J Inorg Biochem 2008, 102:532-539.
56. Kitchin K.T., Del Razo L.M., Brown J.L., Anderson W.L., Kenyon E.M. An integrated pharmacokinetic and pharmacodynamic study of arsenite action. 1. Heme oxygenase induction in rats. Teratog Carcinog Mutagen 1999, 19:385-402.
57. Li X., Li B., Xi S., Zheng Q., Lv X., Sun G. Prolonged environmental exposure of arsenic through drinking water on the risk of hypertension and type 2 diabetes. Environ Sci Pollut Res Int 2013, 20:8151-8161.
58. Lu K., Abo R.P., Schlieper K.A., Graffam M.E., Levine S., Wishnok J.S., et al. Arsenic exposure perturbs the gut microbiome and its metabolic profile in mice: an integrated metagenomics and metabolomics analysis. Environ Health Perspect 2014, 122:284-291.
59. Lukaszewski M.A., Butruille L., Moitrot E., Montel V., Dickes-Coopman A., Lesage J., et al. The hypothalamic POMC mRNA expression is upregulated in prenatally undernourished male rat offspring under high-fat diet. Peptides 2013, 43:146-154.
60. Luo H., Deng Z., Liu L., Shen L., Kou H., He Z., et al. Prenatal caffeine ingestion induces transgenerational neuroendocrine metabolic programming alteration in second generation rats. Toxicol Appl Pharmacol 2014, 274:383-392.
61. Martinez E.J., Kolb B.L., Bell A., Savage D.D., Allan A.M. Moderate perinatal arsenic exposure alters neuroendocrine markers associated with depression and increases depressive-like behaviors in adult mouse offspring. Neurotoxicology 2008, 29:647-655.
62. Martinez-Finley E.J., Ali A.M., Allan A.M. Learning deficits in C57BL/6J mice following perinatal arsenic exposure: consequence of lower corticosterone receptor levels?. Pharmacol Biochem Behav 2009, 94:271-277.
63. Martinez-Finley E.J., Goggin S.L., Labrecque M.T., Allan A.M. Reduced expression of MAPK/ERK genes in perinatal arsenic-exposed offspring induced by glucocorticoid receptor deficits. Neurotoxicol Teratol 2011, 33:530-537.
64. McClintock T.R., Chen Y., Parvez F., Makarov D.V., Ge W., Islam T., et al. Association between arsenic exposure from drinking water and hematuria: results from the Health Effects of Arsenic Longitudinal Study. Toxicol Appl Pharmacol 2014, 276:21-27.
65. McMullen S., Mostyn A. Animal models for the study of the developmental origins of health and disease. Proc Nutr Soc 2009, 68:306-320.
66. Merlot E., Couret D., Otten W. Prenatal stress, fetal imprinting and immunity. Brain Behav Immun 2008, 22:42-51.
67. Milford D.V., Shackleton C.H., Stewart P.M. Mineralocorticoid hypertension and congenital deficiency of 11 beta-hydroxysteroid dehydrogenase in a family with the syndrome of 'apparent' mineralocorticoid excess. Clin Endocrinol (Oxf) 1995, 43:241-246.
68. Moon K., Guallar E., Navas-Acien A. Arsenic exposure and cardiovascular disease: an updated systematic review. Curr Atheroscler Rep 2012, 14:542-555.
69. Mostafa M.G., Cherry N. Arsenic in drinking water and renal cancers in rural Bangladesh. Occup Environ Med 2013, 70:768-773.
70. Muglia L.J., Jenkins N.A., Gilbert D.J., Copeland N.G., Majzoub J.A. Expression of the mouse corticotropin-releasing hormone gene in vivo and targeted inactivation in embryonic stem cells. J Clin Invest 1994, 93:2066-2072.
71. Pavlides C., McEwen B.S. Effects of mineralocorticoid and glucocorticoid receptors on long-term potentiation in the CA3 hippocampal field. Brain Res 1999, 851:204-214.
72. Perrone-Bizzozero N.I., Sower A.C., Bird E.D., Benowitz L.I., Ivins K.J., Neve R.L. Levels of the growth-associated protein GAP-43 are selectively increased in association cortices in schizophrenia. Proc Natl Acad Sci U S A 1996, 93:14182-14187.
73. Reichardt H.M., Schutz G. Feedback control of glucocorticoid production is established during fetal development. Mol Med 1996, 2:735-744.
74. Reynolds R.M. Glucocorticoid excess and the developmental origins of disease: two decades of testing the hypothesis-2012 Curt Richter Award Winner. Psychoneuroendocrinology 2013, 38:1-11.
75. Rodriguez J.S., Zurcher N.R., Keenan K.E., Bartlett T.Q., Nathanielsz P.W., Nijland M.J. Prenatal betamethasone exposure has sex specific effects in reversal learning and attention in juvenile baboons. Am J Obstet Gynecol 2011, 204:545.e1-545.e10.
76. Rodriguez-Barranco M., Lacasana M., Aguilar-Garduno C., Alguacil J., Gil F., Gonzalez-Alzaga B., et al. Association of arsenic, cadmium and manganese exposure with neurodevelopment and behavioural disorders in children: a systematic review and meta-analysis. Sci Total Environ 2013, 454-455:562-577.
77. Rosado J.L., Ronquillo D., Kordas K., Rojas O., Alatorre J., Lopez P., et al. Arsenic exposure and cognitive performance in Mexican schoolchildren. Environ Health Perspect 2007, 115:1371-1375.
78. Rosewicz S., McDonald A.R., Maddux B.A., Goldfine I.D., Miesfeld R.L., Logsdon C.D. Mechanism of glucocorticoid receptor down-regulation by glucocorticoids. J Biol Chem 1988, 263:2581-2584.
79. Santos M.S., Joles J.A. Early determinants of cardiovascular disease. Best Pract Res Clin Endocrinol Metab 2012, 26:581-597.
80. Sapolsky R.M., Krey L.C., McEwen B.S. Glucocorticoid-sensitive hippocampal neurons are involved in terminating the adrenocortical stress response. Proc Natl Acad Sci U S A 1984, 81:6174-6177.
81. Sapolsky R.M., Zola-Morgan S., Squire L.R. Inhibition of glucocorticoid secretion by the hippocampal formation in the primate. J Neurosci 1991, 11:3695-3704.
82. Sarkar P., Bergman K., O'Connor T.G., Glover V. Maternal antenatal anxiety and amniotic fluid cortisol and testosterone: possible implications for foetal programming. J Neuroendocrinol 2008, 20:489-496.
83. Sarr O., Yang K., Regnault T.R. In utero programming of later adiposity: the role of fetal growth restriction. J Pregnancy 2012, 2012:134758.
84. Sase S., Meyer K., Lubec G., Korz V. Different expression of membrane-bound and cytosolic hippocampal steroid receptor complexes during spatial training in young male rats. Eur Neuropsychopharmacol 2014, (pii: S0924-977X(14)00254-5).
85. Schmidt M.V., Oitzl M.S., Muller M.B., Ohl F., Wurst W., Holsboer F., et al. Regulation of the developing hypothalamic-pituitary-adrenal axis in corticotropin releasing hormone receptor 1-deficient mice. Neuroscience 2003, 119:589-595.
86. Schmitz R., Heinig J., Klockenbusch W., Kiesel L., Steinhard J. Antenatal diagnosis of a giant fetal hepatic hemangioma and treatment with maternal corticosteroid. Ultraschall Med 2009, 30:223-226.
87. Shaw J.R., Gabor K., Hand E., Lankowski A., Durant L., Thibodeau R., et al. Role of glucocorticoid receptor in acclimation of killifish (Fundulus heteroclitus) to seawater and effects of arsenic. Am J Physiol Regul Integr Comp Physiol 2007, 292:R1052-R1060.
88. Simons S.S., Chakraborti P.K., Cavanaugh A.H. Arsenite and cadmium(II) as probes of glucocorticoid receptor structure and function. J Biol Chem 1990, 265:1938-1945.
89. Sloboda D.M., Moss T.J., Li S., Matthews S.G., Challis J.R., Newnham J.P. Expression of glucocorticoid receptor, mineralocorticoid receptor, and 11beta-hydroxysteroid dehydrogenase 1 and 2 in the fetal and postnatal ovine hippocampus: ontogeny and effects of prenatal glucocorticoid exposure. J Endocrinol 2008, 197:213-220.
90. Sooy K., Webster S.P., Noble J., Binnie M., Walker B.R., Seckl J.R., et al. Partial deficiency or short-term inhibition of 11beta-hydroxysteroid dehydrogenase type 1 improves cognitive function in aging mice. J Neurosci 2010, 30:13867-13872.
91. Spandidos A., Wang X., Wang H., Dragnev S., Thurber T., Seed B. A comprehensive collection of experimentally validated primers for polymerase chain reaction quantitation of murine transcript abundance. BMC Genomics 2008, 9:633.
92. Spandidos A., Wang X., Wang H., Seed B. PrimerBank: a resource of human and mouse PCR primer pairs for gene expression detection and quantification. Nucleic Acids Res 2010, 38:D792-D799.
93. Speirs H.J., Seckl J.R., Brown R.W. Ontogeny of glucocorticoid receptor and 11beta-hydroxysteroid dehydrogenase type-1 gene expression identifies potential critical periods of glucocorticoid susceptibility during development. J Endocrinol 2004, 181:105-116.
94. Spencer S.J. Early life programming of obesity: the impact of the perinatal environment on the development of obesity and metabolic dysfunction in the offspring. Curr Diabetes Rev 2012, 8:55-68.
95. Stancato L.F., Hutchison K.A., Chakraborti P.K., Simons S.S., Pratt W.B. Differential effects of the reversible thiol-reactive agents arsenite and methyl methanethiosulfonate on steroid binding by the glucocorticoid receptor. Biochemistry 1993, 32:3729-3736.
96. Stranahan A.M., Arumugam T.V., Lee K., Mattson M.P. Mineralocorticoid receptor activation restores medial perforant path LTP in diabetic rats. Synapse 2010, 64:528-532.
97. Styblo M., Delnomdedieu M., Hughes M.F., Thomas D.J. Identification of methylated metabolites of inorganic arsenic by thin-layer chromatography. J Chromatogr B Biomed Appl 1995, 668:21-29.
98. Thompson A., Han V.K., Yang K. Spatial and temporal patterns of expression of 11beta-hydroxysteroid dehydrogenase types 1 and 2 messenger RNA and glucocorticoid receptor protein in the murine placenta and uterus during late pregnancy. Biol Reprod 2002, 67:1708-1718.
99. Tyler C.R., Allan A.M. Adult hippocampal neurogenesis and mRNA expression are altered by perinatal arsenic exposure in mice and restored by brief exposure to enrichment. PLoS ONE 2013, 8:e73720.
100. Tyler C.R., Solomon B.R., Ulibarri A.L., Allan A.M. Fluoxetine treatment ameliorates depression induced by perinatal arsenic exposure via a neurogenic mechanism. Neurotoxicology 2014, 44C:98-109.
101. Vahter M. Effects of arsenic on maternal and fetal health. Annu Rev Nutr 2009, 29:381-399.
102. Vaughan O.R., Sferruzzi-Perri A.N., Fowden A.L. Maternal corticosterone regulates nutrient allocation to fetal growth in mice. J Physiol 2012, 590:5529-5540.
103. Venihaki M., Carrigan A., Dikkes P., Majzoub J.A. Circadian rise in maternal glucocorticoid prevents pulmonary dysplasia in fetal mice with adrenal insufficiency. Proc Natl Acad Sci U S A 2000, 97:7336-7341.
104. von Ehrenstein O.S., Poddar S., Yuan Y., Mazumder D.G., Eskenazi B., Basu A., et al. Children's intellectual function in relation to arsenic exposure. Epidemiology 2007, 18:44-51.
105. Wadhwa P.D., Buss C., Entringer S., Swanson J.M. Developmental origins of health and disease: brief history of the approach and current focus on epigenetic mechanisms. Semin Reprod Med 2009, 27:358-368.
106. Wang X., Seed B. Selection of oligonucleotide probes for protein coding sequences. Bioinformatics 2003, 19:796-802.
107. Wang Z., Frederick J., Garabedian M.J. Deciphering the phosphorylation "code" of the glucocorticoid receptor in vivo. J Biol Chem 2002, 277:26573-26580.
108. Wasserman G.A., Liu X., Parvez F., Ahsan H., Factor-Litvak P., van Geen A., et al. Water arsenic exposure and children's intellectual function in Araihazar, Bangladesh. Environ Health Perspect 2004, 112:1329-1333.
109. Wong S.T., Chan H.L., Teo S.K. The spectrum of cutaneous and internal malignancies in chronic arsenic toxicity. Singapore Med J 1998, 39:171-173.
110. Wu F., Molinaro P., Chen Y. Arsenic exposure and subclinical endpoints of cardiovascular diseases. Curr Environ Health Rep 2014, 1:148-162.
111. Wyrwoll C.S., Seckl J.R., Holmes M.C. Altered placental function of 11beta-hydroxysteroid dehydrogenase 2 knockout mice. Endocrinology 2009, 150:1287-1293.
112. Xi S., Jin Y., Lv X., Sun G. Distribution and speciation of arsenic by transplacental and early life exposure to inorganic arsenic in offspring rats. Biol Trace Elem Res 2010, 134:84-97.
113. Xie H., Huang S., Martin S., Wise J.P. Arsenic is cytotoxic and genotoxic to primary human lung cells. Mutat Res Genet Toxicol Environ Mutagen 2014, 760:33-41.
114. Xu D., Chen M., Pan X.L., Xia L.P., Wang H. Dexamethasone induces fetal developmental toxicity through affecting the placental glucocorticoid barrier and depressing fetal adrenal function. Environ Toxicol Pharmacol 2011, 32:356-363.
115. Yau J.L., Seckl J.R. Local amplification of glucocorticoids in the aging brain and impaired spatial memory. Front Aging Neurosci 2012, 4:24.
116. Yau J.L., Noble J., Seckl J.R. 11beta-hydroxysteroid dehydrogenase type 1 deficiency prevents memory deficits with aging by switching from glucocorticoid receptor to mineralocorticoid receptor-mediated cognitive control. J Neurosci 2011, 31:4188-4193.
117. Zhang X., Clark A.F., Yorio T. FK506-binding protein 51 regulates nuclear transport of the glucocorticoid receptor beta and glucocorticoid responsiveness. Invest Ophthalmol Vis Sci 2008, 49:1037-1047.