Reverse effect of mammalian hypocalcemic cortisol in fish: Cortisol stimulates Ca 2+ uptake via glucocorticoid receptor-mediated vitamin D 3 metabolism

PLoS ONE

Volumn 6, Issue 8, 2011, Pages

  Lin, Chia Hao ^a,b   Tsai, I Lun ^c   Su, Che Hsien ^d   Tseng, Deng Yu ^e   Hwang, Pung Pung ^a,b,d  

^a NATIONAL DEFENSE MEDICAL CENTER   (Taiwan)

^b INSTITUTE OF CELLULAR AND ORGANISMIC BIOLOGY   (Taiwan)

^c NATIONAL PINGTUNG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Taiwan)

^d NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^e NATIONAL UNIVERSITY OF TAINAN   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CHANNEL; CALCIUM ION; CHOLESTANETRIOL 26 MONOOXYGENASE; CHOLESTANETRIOL 26 MONOOXYGENASE LIKE; COLECALCIFEROL; EPITHELIAL CALCIUM CHANNEL; FRESH WATER; GLUCOCORTICOID RECEPTOR; HYDROCORTISONE; HYDROXYSTEROID 11 BETA DEHYDROGENASE 2; MINERALOCORTICOID RECEPTOR; OXYGENASE; STEROID 11BETA MONOOXYGENASE; UNCLASSIFIED DRUG; CALCITRIOL RECEPTOR; CALCIUM; ECAC PROTEIN, ZEBRAFISH; VANILLOID RECEPTOR; ZEBRAFISH PROTEIN;

ACCLIMATIZATION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALCIUM TRANSPORT; CONTROLLED STUDY; EMBRYO; FISH; GENE SILENCING; HYPOCALCEMIA; MAMMAL; NONHUMAN; PROTEIN EXPRESSION; REGULATORY MECHANISM; VITAMIN D METABOLISM; ZEBRA FISH; ANIMAL; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY;

DANIO RERIO; MAMMALIA; TELEOST FISH; VERTEBRATA;

ANIMALS; CALCIUM; CYTOCHROME P-450 CYP27A1; GENE EXPRESSION REGULATION; HYDROCORTISONE; RECEPTORS, CALCITRIOL; RECEPTORS, GLUCOCORTICOID; TRPV CATION CHANNELS; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 80051971314     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0023689     Document Type: Article

References (61)

1. Charmandari E, Tsigos C, Chrousos G, (2005) Endocrinology of the stress response. Ann Rev Physiol 67: 259-284.
2. McLaughlin F, Mackintosh J, Hayes BP, McLaren A, Uings IJ, et al. (2002) Glucocorticoid-induced osteopenia in the mouse as assessed by histomorphometry, microcomputed tomography, and biochemical markers. Bone 30: 924-930.
3. Patschan D, Loddenkemper K, Buttgereit F, (2001) Molecular mechanisms of glucocorticoid-induced osteoporosis. Bone 29: 498-505.
4. Lukert BP, Raisz LG, (1990) Glucocorticoid-induced osteoporosis: pathogenesis and management. Ann Intern Med 112: 352-364.
5. Huybers S, Naber TH, Bindels RJ, Hoenderop JG, (2007) Prednisolone-induced Ca2+ malabsorption is caused by diminished expression of the epithelial Ca2+ channel TRPV6. Am J Physiol Gastrointest Liver Physiol 292 (1): G92-97.
6. Kim MH, Lee GS, Jung EM, Choi KC, Oh GT, et al. (2009) Dexamethasone differentially regulates renal and duodenal calcium-processing genes in calbindin-D9k and-D28k knockout mice. Exp Physiol 94 (1): 138-151.
7. Bury NR, Sturm A, (2007) Evolution of the corticosteroid receptor signalling pathway in fish. Gen Comp Endocrinol 153 (1-3): 47-56.
8. Mommsen TP, Vijayan MM, Moon TW, (1999) Cortisol in teleosts: dynamics, mechanisms of action, and metabolic regulation. Rev Fish Biol Fish 9: 211-268.
9. Trapp T, Holsboer F, (1996) Heterodimerization between mineralocorticoid and glucocorticoid receptors increases the functional diversity of corticosteroid action. Trends Pharmacol Sci 17: 145-149.
10. Baker ME, (2003) Evolution of Glucocorticoid and Mineralocorticoid Responses: Go Fish. Endocrinology 144: 4223-4225.
11. Nelson DR, (2003) Comparison of P450s from human and fugu: 420 million years of vertebrate P450 evolution. Arch Biochem Biophys 409: 18-24.
12. Colombe L, Fostier A, Bury N, Pakdel F, Guigen Y, et al. (2000) A mineralocorticoid-like receptor in the rainbow trout, Oncorhynchus mykiss: cloning and characterization of its steroid binding domain. Steroids 65: 319-328.
13. Bury NR, Sturm A, Le Rouzic P, Lethimonier C, Ducouret B, et al. (2003) Evidence for two distinct functional glucocorticoid receptors in teleost fish. J Mol Endocrinol 31: 141-156.
14. Greenwood AK, Butler PC, White RB, DeMarco U, Pearce D, et al. (2003) Multiple corticosteroid receptors in a teleost fish: distinct sequences, expression patterns, and transcriptional activities. Endocrinology 144: 4226-4236.
15. Sturm A, Bury NR, Dengreville L, Fagart J, Flouriot G, et al. (2005) 11-Deoxycorticosterone is a potentagonist of the rainbow trout (Oncorhynchus mykiss) mineralocorticoid receptor. Endocrinology 146: 47-55.
16. Kiilerich P, Kristiansen K, Madsen SS, (2007) Cortisol regulation of ion transporter mRNA in Atlantic salmon gill and the effect of salinity on the signaling pathway. J Endocrinol 194 (2): 417-427.
17. DeLuca HF, (1988) The vitamin D story: a collaborative effort of basic science and clinical medicine. FASEB Journal 2: 224-236.
18. Haussler MR, Whitfield GK, Haussler CA, Hsieh JC, Thompson PD, et al. (1998) The nuclear vitamin D receptor: biological and molecular regulatory properties revealed. Bone Miner Res 13: 325-349.
19. Holick MF, (2007) Vitamin D Deficiency. N Engl J Med 357: 266-281.
20. Swarup K, Das VK, Norman AW, (1991) Dose-dependent vitamin D3 and 1,25-dihydroxyvitamin D3-induced hypercalcemia and hyperphosphatemia in male cyprinoid Cyprinus carpio. Comp Biochem Physiol A Physiol 100 (2): 445-447.
21. Sundell K, Norman AW, Björnsson BT, (1993) 1,25(OH)2 vitamin D3 increases ionized plasma calcium concentrations in the immature Atlantic cod Gadus morhua. Gen Comp Endocrinol 91 (3): 344-351.
22. Abbink W, Hang XM, Guerreiro PM, Spanings FA, Ross HA, et al. (2007) Parathyroid hormone-related protein and calcium regulation in vitamin D-deficient sea bream (Sparus auratus). J Endocrinol 193: 473-480.
23. Lock EJ, Ornsrud R, Aksnes L, Spanings FA, Waagbo R, et al. (2007) The vitamin D receptor and its ligand 1alpha,25-dihydroxyvitamin D3 in Atlantic salmon (Salmo salar). J Endocrinol 193: 459-471.
24. Chesney RW, Mazess RB, Hamstra AJ, DeLuca HF, O'Reagan S, et al. (1978) Reduction of serum-1, 25-dihydroxyvitamin-D3 in children receiving glucocorticoids. Lancet 312 (8100): 1123-1125.
25. Seeman E, Kumar R, Hunder GG, Scott M, Heath H 3rd, et al. (1980) Production, degradation, and circulating levels of 1,25-dihydroxyvitamin D3 in health and in chronic glucocorticoid excess. J Clin Invest 66 (4): 664-669.
26. Morris HA, Need AG, O'Loughlin PD, Horowitz M, Bridges A, et al. (1990) Malabsorption of calcium in corticosteroid-induced osteoporosis. Calcif Tissue Int 46 (5): 305-308.
27. Prummel MF, Wiersinga WM, Lips P, Sanders GT, Sauerwein HP, et al. (1991) The course of biochemical parameters of bone turnover during treatment with corticosteroids. J Clin Endocrinol Metab 72 (2): 382-386.
28. Bikle DD, Halloran B, Fong L, Steinbach L, Shellito J, et al. (1993) Elevated 1,25-dihydroxyvitamin D3 levels in patients with chronic obstructive pulmonary disease treated with prednisone. J Clin Endocrinol Metab 76 (2): 456-461.
29. Cosman F, Nieves J, Herbert J, Shen V, Lindsay R, et al. (1994) High-dose glucocorticoids in multiple sclerosis patients exert direct effects on the kidney and skeleton. J Bone Miner Res 9 (7): 1097-1105.
30. Evans DH, Piermarini PM, Choe KP, (2005) The multifunctional fish gill: Dominant site of gas exchange, osmoregulation, acid-base regulation, and excretion of nitrogenous waste. Physiol Rev 85: 97-177.
31. McCormick SD, Bradshaw D, (2006) Hormonal control of salt and water balance in vertebrates. Gen Comp Endocrinol 147 (1): 3-8.
32. Hwang PP, Perry SF, (2010) Ionic and acid-base regulation. In: Pery SF, Ekker M, Farrell AP, Brauner CJ, editors. Zebrafish: A Fish Physiology, 1st ed. vol. 29 pp. 311-344 Academic Press, New York, NY, USA.
33. Hwang PP, Lee TH, Lin LY, (2011) Ion Regulation in Fish Gills: Recent Progress in the Cellular and Molecular Mechanisms. Am J Physiol Regul Integr Comp Physiol 301: R28-R47.
34. Hwang PP, Lee TH, (2007) New insights into fish ion regulation and mitochondrion-rich cells. Comp Biochem Physiol A Mol Integr Physiol 148 (3): 479-97.
35. Hoenderop JG, Nilius B, Bindels RJ, (2005) Calcium absorption across epithelia. Physiol Rev 85: 373-422.
36. Flik G, Perry SF, (1989) Cortisol stimulates whole body calcium uptake and the branchial calcium pump in freshwater rainbow trout. J Endocrinol 120: 75-82.
37. Shahsavarani A, Perry SF, (2006) Hormonal and environmental regulation of epithelial calcium channel in gill of rainbow trout. Am J Physiol Regul Integr Comp Physiol 291: R1490-R1498.
38. Kelly SP, Wood CM, (2008) Cortisol stimulates calcium transport across cultured gill epithelia from freshwater rainbow trout. In Vitro Cell Dev Biol Anim 44 (3-4): 96-104.
39. Hwang PP, (2009) Ion uptake and acid secretion in zebrafish (Danio rerio). J Exp Biol 212 (11): 1745-1752.
40. Pan TC, Liao BK, Huang CJ, Lin LY, Hwang PP, et al. (2005) Epithelial Ca2+ channel expression and Ca2+ uptake in developing zebrafish. Am J Physiol Regul Integr Comp Physiol 289 (4): R1202-1211.
41. Liao BK, Deng AN, Chen SC, Chou MY, Hwang PP, et al. (2007) Expression and water calcium dependence of calcium transporter isoforms in zebrafish gill mitochondrion-rich cells. BMC Genomics 8: 354.
42. Tseng DY, Chou MY, Tseng YC, Hsiao CD, Huang CJ, et al. (2009) Effects of stanniocalcin 1 on calcium uptake in zebrafish (Danio rerio) embryo. Am J Physiol Regul Integr Comp Physiol 296 (3): R549-557.
43. Lin GR, Weng CF, Wang JI, Hwang PP, (1999) Effects of cortisol on ion regulation in developing tilapia (Oreochromis mossambicus) larvae on seawater adaptation. Physiol Biochem Zool 72 (4): 397-404.
44. Chen YY, Lu FI, Hwang PP, (2003) Comparisons of calcium regulation in fish larvae. J Exp Zool 295: 127-135.
45. Mathew LK, Sengupta S, Kawakami A, Andreasen EA, Löhr CV, et al. (2007) Unraveling tissue regeneration pathways using chemical genetics. J Biol Chem 282 (48): 35202-35210.
46. Perry SF, Goss GG, Fenwick JC, (1992) Interrelationships between gill chloride cell morphology and calcium uptake in freshwater teleosts. Fish Physiol Biochem 10: 327-337.
47. Vennekens R, Hoenderop JG, Prenen J, Stuiver M, Willems PH, et al. (2000) Permeation and gating properties of the novel epithelial Ca2+ channel. J Biol Chem 275: 3963-3969.
48. Funder JW, (2005) Mineralocorticoid receptors: distribution and activation. Heart Fail Rev 10: 15-22.
49. Jiang JQ, Wang DS, Senthilkumaran B, Kobayashi T, Kobayashi HK, et al. (2003) Isolation, characterization and expression of 11beta-hydroxysteroid dehydrogenase type 2 cDNAs from the testes of Japanese eel (Anguilla japonica) and Nile tilapia (Oreochromis niloticus). J Mol Endocrinol 31 (2): 305-315.
50. Kusakabe M, Nakamura I, Young G, (2003) 11beta-hydroxysteroid dehydrogenase complementary deoxyribonucleic acid in rainbow trout: cloning, sites of expression, and seasonal changes in gonads. Endocrinology 144 (6): 2534-2545.
51. Cole MA, Kim PJ, Kalman BA, Spencer RL, (2000) Dexamethasone suppression of corticosteroid secretion: evaluation of the site of action by receptor measures and functional studies. Psychoneuroendocrinology 25: 151-167.
52. McGowan JE, Sysyn G, Petersson KH, Sadowska GB, Mishra OP, et al. (2000) Effect of dexamethasone treatment on maturational changes in the NMDA receptor in sheep brain. J Neurosci 20 (19): 7424-9.
53. Maule AG, Schreck CB, (1991) Stress and cortisol treatment changed affinity and number of glucocorticoid receptors in leukocytes and gill of coho salmon. Gen Comp Endocrinol 84 (1): 83-93.
54. Pottinger TG, Pickering AD, (1990) The effect of cortisol administration on hepatic and plasma estradiol-binding capacity in immature female rainbow trout (Oncorhynchus mykiss). Gen Comp Endocrinol 80 (2): 264-273.
55. Shrimpton JM, Randall DJ, (1994) Downregulation of corticosteroid receptors in gills of coho salmon due to stress and cortisol treatment. Am J Physiol 267: R432-438.
56. Takahashi H, Sakamoto T, Hyodo S, Shepherd BS, Kaneko T, et al. (2006) Expression of glucocorticoid receptor in the intestine of a euryhaline teleost, the Mozambique tilapia (Oreochromis mossambicus): effect of seawater exposure and cortisol treatment. Life Sci 78 (20): 2329-2335.
57. Weisbart M, Chakraborti PK, Gallivan G, Eales JG, (1987) Dynamics of cortisol receptor activity in the gills of the brook trout, Salvelinus fontinalis, during seawater adaptation. Gen Comp Endocrinol 68 (3): 440-448.
58. Shultz TD, Bollman S, Kumar R, (1982) Decreased intestinal calcium absorption in vivo and normal brush border membrane vesicle calcium uptake in cortisol-treated chickens: evidence for dissociation of calcium absorption from brush border vesicle uptake. Proc Natl Acad Sci U S A 79 (11): 3542-3546.
59. Schaaf MJ, Champagne D, van Laanen IH, van Wijk DC, Meijer AH, et al. (2008) Discovery of a functional glucocorticoid receptor beta-isoform in zebrafish. Endocrinology 149 (4): 1591-1599.
60. Qiu A, Hogstrand C, (2004) Functional characterisation and genomic analysis of an epithelial calcium channel (ECaC) from pufferfish, Fugu rubripes. Gene 342 (1): 113-123.
61. Howarth DL, Law SH, Barnes B, Hall JM, Hinton DE, et al. (2008) Paralogous vitamin D receptors in teleosts: transition of nuclear receptor function. Endocrinology 149 (5): 2411-2422.