Steroid profiling reveals widespread local regulation of glucocorticoid levels during mouse development

Endocrinology (United States)

Volumn 156, Issue 2, 2015, Pages 511-522

  Taves, Matthew D ^a   Plumb, Adam W ^a   Sandkam, Benjamin A ^a   Ma, Chunqi ^a,c   Van Der Gugten, Jessica Grace ^a,c   Holmes, Daniel T ^a   Close, David A ^a   Abraham, Ninan ^b   Soma, Kiran K ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b SIMON FRASER UNIVERSITY   (Canada)

^c ST PAUL S HOSPITAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ALDOSTERONE SYNTHASE; CHOLESTEROL MONOOXYGENASE (SIDE CHAIN CLEAVING); CORTICOSTERONE; CORTODOXONE; CYTOCHROME P450 2A1; DEOXYCORTICOSTERONE; GLUCOCORTICOID; HYDROCORTISONE; PROGESTERONE; STEROID;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE MARROW; BRAIN LEVEL; CONTROLLED STUDY; CORTICOSTEROID BLOOD LEVEL; CORTICOSTERONE BLOOD LEVEL; EMBRYO; FEMALE; GENE EXPRESSION; HEART DEVELOPMENT; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HYDROCORTISONE BLOOD LEVEL; HYDROCORTISONE RELEASE; IMMUNOASSAY; IN VIVO STUDY; LIVER LEVEL; MALE; METABOLIC REGULATION; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROGESTERONE BLOOD LEVEL; REAL TIME POLYMERASE CHAIN REACTION; SOLID PHASE EXTRACTION; SPLEEN; STEROID ANALYSIS; STEROID BLOOD LEVEL; STEROIDOGENESIS; TANDEM MASS SPECTROMETRY; THYMUS; TISSUE LEVEL; ANIMAL; BIOSYNTHESIS; BLOOD; BRAIN; C57BL MOUSE; GENE EXPRESSION REGULATION; GROWTH, DEVELOPMENT AND AGING; HEART MUSCLE; LIVER; MASS SPECTROMETRY; METABOLISM;

ANIMALS; BONE MARROW; BRAIN; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GROWTH AND DEVELOPMENT; LIVER; MALE; MASS SPECTROMETRY; MICE, INBRED C57BL; MYOCARDIUM; SPLEEN; STEROIDS; THYMUS GLAND;

EID: 84921671296     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2013-1606     Document Type: Article

References (67)

1. Norris DO. Vertebrate Endocrinology, 4th ed. Burlington, VT: Elsevier; 2007
2. Guyton AC, Hall JE. Textbook of Medical Physiology, 11th ed. PhilaDelphia, PA: Elsevier; 2006
3. Taves MD, Gomez-Sanchez CE, Soma KK. Extra-Adrenal glucocorticoids and mineralocorticoids: eviDence for local synthesis, regulation, and function.AmJ Physiol Endocrinol Metab. 2011;301:E11-E24
4. Seckl JR, Holmes MC.Mechanisms of disease: glucocorticoids, their placental metabolism and fetal programming of adult pathophysiology. Nat Clin Pract Endocrinol Metab. 2007;3:479-488
5. Breuner CW, Orchinik M. Plasma binding proteins as mediators of corticosteroid action in vertebrates. J Endocrinol. 2002;175:99-112
6. Sapolsky RM, Romero LM, Munck AU. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr Rev. 2000;21:55-89
7. Wada H. Glucocorticoids: mediators of vertebrate ontogenetic transitions. Gen Comp Endocrinol. 2008;156:441-453
8. McEwen BS, Wingfield JC. The concept of allostasis in biology and biomedicine. Horm Behav. 2003;43:2-15
9. Walker BR. Glucocorticoids and cardiovascular disease. Eur J Endocrinol. 2007;157:545-559
10. Vegiopoulos A, Herzig S. Glucocorticoids, metabolism and metabolic diseases. Mol Cell Endocrinol. 2007;275:43-61
11. Demas GE, Nelson RJ. Ecoimmunology. New York, NY: Oxford; 2012
12. Makin HLJ, Gower DB. Steroid Analysis. New York, NY: Springer; 2010
13. Vacchio MS, Papadopoulos V, Ashwell JD. Steroid production in the thymus: implications for thymocyte selection. J Exp Med. 1994; 179:1835-1846
14. Lechner O, Wiegers GJ, Oliveira-dos-Santos AJ, et al. Glucocorticoid production in the murine thymus. Eur J Immunol. 2000;30: 337-346
15. Lechner O, Dietrich H, Wiegers GJ, Vacchio M, Wick G. Glucocorticoid production in the chicken bursa and thymus. Int Immunol. 2001;13:769-776
16. Schmidt KL, Soma KK. Cortisol and corticosterone in the songbird immune and nervous systems: local vs. systemic levels during Development. Am J Physiol Regul Integr Comp Physiol. 2008;295: R103-R110
17. Vinson GP. The mislabelling of Deoxycorticosterone: making sense of corticosteroid structure and function. J Endocrinol. 2011;211: 3-16
18. Close DA, Yun SS, McCormick SD, Wildbill AJ, Li W. 11-Deoxycortisol is a corticosteroid hormone in the lamprey. Proc Natl Acad Sci USA. 2010;107:13942-13947
19. Duval D, Durant S, Homo-Delarche F. Effect of antiglucocorticoids on Dexamethasone-induced inhibition of uridine incorporation and cell lysis in isolated mouse thymocytes. J Steroid Biochem. 1984; 20:283-287
20. Gomez-Sanchez E, Gomez-Sanchez CE. The multifaceted mineralocorticoid receptor. Compr Physiol. 2014;4:965-994
21. Meaney MJ, Sapolsky RM, McEwen BS. The Development of the glucocorticoid receptor system in the rat limbic brain. I. Ontogeny and autoregulation. Brain Res. 1985;18:159-164
22. Lupien SJ, McEwen BS, Gunnar MR, Heim C. Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat Rev Neurosci. 2009;10:434-445
23. Mittelstadt PR, Monteiro JP, Ashwell JD. Thymocyte responsiveness to endogenous glucocorticoids is required for immunological fitness. J Clin Invest. 2012;122:2384-2394
24. Rog-Zielinska EA, Thomson A, Kenyon CJ, et al. Glucocorticoid receptor is required for foetal heart maturation. Hum Mol Genet. 2013;22:3269-3282
25. Liggins GC. The role of cortisol in preparing the fetus for birth. Reprod Fertil Dev. 1994;6:141-150
26. Schmidt MV, Schmidt M, Enthoven L, Van Der Mark M, Levine S, De Kloet ER, Oitzl MS. The postnatal Development of the hypothalamic-pituitary-Adrenal axis in the mouse. Int J Dev Neurosci. 2003; 21:125-132
27. Clapcote SJ, RoDer JC. Simplex PCR assay for sex Determination in mice. BioTechniques. 2005;38:702-706
28. Newman AE, Chin EH, Schmidt KL, Bond L, Wynne-Edwards KE, Soma KK. Analysis of steroids in songbird plasma and brain by coupling solid phase extraction to radioimmunoassay. Gen Comp Endocrinol. 2008;155:503-510
29. Taves MD, Schmidt KL, Ruhr IM, Kapusta K, Prior NH, Soma KK. Steroid concentrations in plasma, whole blood and brain: effects of saline perfusion to remove blood contamination from brain. PLoS One. 2010;5:e15727
30. Taves MD, Ma C, Heimovics SA, Saldanha CJ, Soma KK. Measurement of steroid concentrations in brain tissue: methodological consiDerations. Front Endocrinol (Lausanne). 2011;2:39
31. Qiao S, Chen L, Okret S, Jondal M. Age-related synthesis of glucocorticoids in thymocytes. Exp Cell Res. 2008;314:3027-3035
32. De Jonge HJ, Fehrmann RS, De Bont ES, et al. EviDence based selection of housekeeping genes. PLoS One. 2007;2:e898
33. PaziranDeh A, Xue Y, Rafter I, Sjvall J, Jondal M, Okret S. Paracrine glucocorticoid activity produced by mouse thymic epithelial cells. FASEB J. 1999;13:893-901
34. Hiramatsu R, Nisula BC. Erythrocyte-Associated cortisol: measurement, kinetics of dissociation, and potential physiological significance. J Clin Endocrinol Metab. 1987;64:1224-1232
35. Van WeerDen WM, Bierings HG, Van Steenbrugge GJ, De Jong FH, SchrDer FH. Adrenal glands of mouse and rat do not synthesize androgens. Life Sci. 1992;50:857-861
36. Touitou Y, Auzeby A, Bogdan A. Cortisol and cortisone production in rat and mouse adrenal incubations. J Steroid Biochem Mol Biol. 1990;37:279-284
37. Holmes MC, Carter RN, Noble J, et al. 11-Hydroxysteroid Dehydrogenase type 1 expression is increased in the aged mouse hippocampus and parietal cortex and causes memory impairments. J Neurosci. 2010;30:6916-6920
38. Sheppard KE, Autelitano DJ. 11-Hydroxysteroid Dehydrogenase 1 transforms 11-Dehydrocorticosterone into transcriptionally active glucocorticoid in neonatal rat heart. Endocrinology. 2002;143: 198-204
39. Sivukhina E, Helbling JC, Minni AM, et al. Intrinsic expression of transcortin in neural cells of the mouse brain: a histochemical and molecular study. J Exp Biol. 2013;216:245-252
40. Homma H, Listowsky I. IDentification of Yb-glutathione-S-transferase as a major rat liver protein labeled with Dexamethasone 21-methanesulfonate. Proc Natl Acad Sci USA. 1985;82:7165-7169
41. Rowe JD, Nieves E, Listowsky I. Subunit diversity and tissue distribution of human glutathione S-transferases: interpretations based on electrospray ionization-MS and peptiDe sequence-specific antisera. Biochem J. 1997;325:481-486
42. Silvestre JS, Robert V, Heymes C, et al. Myocardial production of aldosterone and corticosterone in the rat. Physiological regulation. J Biol Chem. 1998;273:4883-4891
43. Gomez-Sanchez CE, ZhouMY,Cozza EN, Morita H, Foecking MF, Gomez-Sanchez EP. Aldosterone biosynthesis in the rat brain. Endocrinology. 1997;138:3369-3373
44. Keeney DS, Jenkins CM, Waterman MR. Developmentally regulated expression of adrenal 17-hydroxylase cytochrome P450 in the mouse embryo. Endocrinology. 1995;136:4872-4879
45. Varon HH, Touchstone JC. 17-Hydroxycorticoids in mouse adrenal incubates. Acta Endocrinol. 1964;46:65-70
46. Gillis S, Crabtree GR, Smith KA. Glucocorticoid-induced inhibition of T cell growth factor production. I. The effect on mitogen-induced lymphocyte proliferation. J Immunol. 1979;123:1624-1631
47. Iwata M, Hanaoka S, Sato K. Rescue of thymocytes and T cell hybridomas from glucocorticoid-induced apoptosis by stimulation via the T cell receptor/CD3 complex: a possible in vitro moDel for positive selection of the T cell repertoire. Eur J Immunol. 1991;21:643-648
48. Hughes GC, Clark EA, Wong AH. The intracellular progesterone receptor regulates CD4 T cells and T cell-DepenDent antibody responses. J Leukoc Biol. 2013;93:369-375
49. Lee JH, Lydon JP, Kim CH. Progesterone suppresses the mTOR pathway and promotes generation of induced regulatoryTcells with increased stability. Eur J Immunol. 2012;42:2683-2696
50. Tibbetts TA, DeMayo F, Rich S, Conneely OM, OMalley BW. Progesterone receptors in the thymus are required for thymic involution during pregnancy and for normal fertility. Proc Natl Acad Sci USA. 1999;96:12021-12026
51. Orkin SH, Zon LI. Hematopoiesis: an evolving paradigm for stem cell biology. Cell. 2008;132:631-644
52. Gruver-Yates AL, Quinn MA, Cidlowski JA. Analysis of glucocorticoid receptors and their apoptotic response to Dexamethasone in male murine B cells during Development. Endocrinology. 2014;155: 463-474
53. Garvy BA, Telford WG, King LE, Fraker PJ. Glucocorticoids and irradiation-induced apoptosis in normal murine bone marrow Blineage lymphocytes as Determined by flow cytometry. Immunology. 1993;79:270-277
54. Schmidt KL, Malisch JL, Breuner CW, Soma KK. Corticosterone and cortisol binding sites in plasma, immune organs and brain of Developing zebra finches: Intracellular and membrane-Associated receptors. Brain Behav Immun. 2010;24:908-918
55. Bartholome B, Spies CM, Gaber T, et al. Membrane glucocorticoid receptors (mGCR) are expressed in normal human peripheral blood mononuclear cells and up-regulated after in vitro stimulation and in patients with rheumatoid arthritis. FASEB J. 2004;18:70-80
56. Trottier MD, Newsted MM, King LE, Fraker PJ. Natural glucocorticoids induce expansion of all Developmental stages of murine bone marrow granulocytes without inhibiting function. Proc Natl Acad Sci USA. 2008;105:2028-2033
57. Bauer A, Tronche F, Wessely O, et al. The glucocorticoid receptor is required for stress erythropoiesis. Genes Dev. 1999;13:2996-3002
58. Pitt B, Zannad F, Remme WJ, et al. The effect of spironolactone on morbidity and mortality in patients with severe heart failure. Randomized Aldactone Evaluation Study Investigators. N Engl J Med. 1999;341:709-717
59. Young MJ, Clyne CD, Cole TJ, FunDer JW. Cardiac steroidogenesis in the normal and failing heart. J Clin Endocrinol Metab. 2001;86: 5121-5126
60. Kayes-Wandover KM, White PC. Steroidogenic enzyme gene expression in the human heart. J Clin Endocrinol Metab. 2000;85: 2519-2525
61. Ye P, Kenyon CJ, MacKenzie SM, et al. The aldosterone synthase (CYP11B2) and 11-hydroxylase (CYP11B1) genes are not expressed in the rat heart. Endocrinology. 2005;146:5287-5293
62. Gomez-Sanchez EP, Ahmad N, Romero DG, Gomez-Sanchez CE. Origin of aldosterone in the rat heart. Endocrinology. 2004;145: 4796-4802
63. Jamieson PM, Chapman KE, Edwards CR, Seckl JR. 11-Hydroxysteroid Dehydrogenase is an exclusive 11-reductase in primary cultures of rat hepatocytes: effect of physicochemical and hormonal manipulations. Endocrinology. 1995;136:4754-4761
64. Hattangadi SM, Wong P, Zhang L, Flygare J, Lodish HF. From stem cell to red cell: regulation of erythropoiesis at multiple levels by multiple proteins, RNAs, and chromatin modifications. Blood. 2011;118:6258-6268
65. Schaer DJ, Boretti FS, Schoedon G, Schaffner A. Induction of the CD163-DepenDent haemoglobin uptake by macrophages as a novel anti-inflammatory action of glucocorticoids. Br J Haematol. 2002; 119:239-243
66. Higo S, Hojo Y, Ishii H, et al. Endogenous synthesis of corticosteroids in the hippocampus. PLoS One. 2011;6:e21631
67. Schmidt KL, Pradhan DS, Shah AH, Charlier TD, Chin EH, Soma KK. Neurosteroids, immunosteroids, and the Balkanization of endocrinology. Gen Comp Endocrinol. 2008;157:266-274.