Cortisol regulates Na+ uptake in zebrafish, Danio rerio, larvae via the glucocorticoid receptor

Molecular and Cellular Endocrinology

Volumn 364, Issue 1-2, 2012, Pages 113-125

  Kumai, Yusuke ^a   Nesan, Dinushan ^b   Vijayan, Mathilakath M ^b   Perry, Steve F ^a  

^a UNIVERSITY OF OTTAWA   (Canada)

^b UNIVERSITY OF WATERLOO   (Canada)

Author keywords

Cortisol; Glucocorticoid receptor; Low pH; Na+ H+ exchanger 3b; Rhcg1; Zebrafish

Indexed keywords

ACID; ALDOSTERONE; DEXAMETHASONE; GLUCOCORTICOID RECEPTOR; HYDROCORTISONE; MIFEPRISTONE; PROTEIN RHCG1; SODIUM PROTON EXCHANGE PROTEIN 3; SODIUM PROTON EXCHANGE PROTEIN 3B; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BODY COMPOSITION; CELL TYPE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EMBRYO; GENETIC TRANSCRIPTION AND TRANSLATION; HORMONAL REGULATION; IMMUNOHISTOCHEMISTRY; INCUBATION TIME; IONOCYTE; LARVA; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN FUNCTION; SODIUM TRANSPORT; ZEBRA FISH;

ACCLIMATIZATION; ALDOSTERONE; AMMONIA; ANIMALS; ANTI-INFLAMMATORY AGENTS; CATION TRANSPORT PROTEINS; DEXAMETHASONE; HORMONE ANTAGONISTS; HYDROCORTISONE; HYDROGEN-ION CONCENTRATION; ION TRANSPORT; LARVA; MIFEPRISTONE; RECEPTORS, GLUCOCORTICOID; RECEPTORS, MINERALOCORTICOID; RNA, SMALL INTERFERING; SODIUM; SODIUM-HYDROGEN ANTIPORTER; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84867501273     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2012.08.017     Document Type: Article

References (77)

1. Alderman S.L., Bernier N.J. Ontogeny of the corticotropin-releasing factor system in zebrafish. General and Comparative Endocrinology 2009, 164:61-69.
2. Alsop D., Vijayan M.M. Development of the corticosteroid stress axis and receptor expression in zebrafish. American Journal of Physiology - Regulatory, Integrative and Comparative Physiology 2008, 294:R711-R719.
3. Andersen D.E., Reid S., Moon T.W., Perry S.F. Metabolic effects associated with chronically elevated cortisool in rainbow trout Oncorhynchus mykiss. Canadian Journal of Fisheries and Aquatic Sciences 1991, 48:1811-1817.
4. Bindon S., Gilmour K., Fenwick J., Perry S. The effects of branchial chloride cell proliferation on respiratory function in the rainbow trout, Oncorhynchus mykiss. Journal of Experimental Biology 1994, 197:47-63.
5. Bindon S.D., Fenwick J.C., Perry S.F. Branchial chloride cell proliferation in the rainbow trout, Oncorhynchus mykiss: implications for gas transfer. Canadian Journal of Zoology 1994, 72:1395-1402.
6. + exchanger-3 (NHE3) by activation of NHE3 exocytosis. American Journal of Physiology - Renal Physiology 2005, 289:F685-F691.
7. Boisen A.M.Z., Amstrup J., Novak I., Grosell M. Sodium and chloride transport in soft water and hard water acclimated zebrafish (Danio rerio). Biochimica et Biophysica Acta (BBA) - Biomembranes 2003, 1618:207-218.
8. Braun M.H., Steele S.L., Ekker M., Perry S.F. Nitrogen excretion in developing zebrafish (Danio rerio): a role for Rh proteins and urea transporters. American Journal of Physiology - Renal Physiology 2009, 296:F994-F1005.
9. Bui P., Bagherie-Lachidan M., Kelly S.P. Cortisol differentially alters claudin isoforms in cultured puffer fish gill epithelia. Molecular and Cellular Endocrinology 2010, 317:120-126.
10. Bury N.R., Sturm A. Evolution of the corticosteroid receptor signalling pathway in fish. General and Comparative Endocrinology 2007, 153:47-56.
11. +-ATPase-rich cells in zebrafish (Danio rerio). American Journal of Physiology - Regulatory, Integrative and Comparative Physiology 2009, 296:R1192-R1201.
12. Chasiotis H., Wood C.M., Kelly S.P. Cortisol reduces paracellular permeability and increases occludin abundance in cultured trout gill epithelia. Molecular and Cellular Endocrinology 2010, 323:232-238.
13. Colombe L., Fostier A., Bury N., Pakdel F., Guiguen Y. A mineralocorticoid-like receptor in the rainbow trout, Oncorhynchus mykiss: cloning and characterization of its steroid binding domain. Steroids 2000, 65:319-328.
14. Colombo L., Bern H.A., Pieprzyk J., Johnson D.W. Corticosteroidogenesis in vitro by the head kidney of tilapia mossambica (Cichlidae, Teleostei). Endocrinology 1972, 91:450-462.
15. Dickmeis T., Lahiri K., Nica G., Vallone D., Santoriello C., Neumann C.J., Hammerschmidt M., Foulkes N.S. Glucocorticoids play a key role in circadian cell cycle rhythms. PLoS Biology 2007, 5:e78.
16. Donowitz M., Mohan S., Zhu C.X., Chen T.-E., Lin R., Cha B., Zachos N.C., Murtazina R., Sarker R., Li X. NHE3 regulatory complexes. Journal of Experimental Biology 2009, 212:1638-1646.
17. Engeszer R.E., Patterson L.B., Rao A.A., Parichy D.M. Zebrafish in the wild: a review of natural history and new notes from the field. Zebrafish 2007, 4:21-40.
18. + uptake in mitochondria-rich cells whose differentiation is dependent on foxi3a. American Journal of Physiology Regulatory Integrative and Comparative Physiology 2007, 292:R470-R480.
19. Evans D.H., Piermarini P.M., Choe K.P. The multifunctional fish gill: dominant site of gas exchange, osmoregulation, acid-base regulation, and excretion of nitrogenous waste. Physiological Reviews 2005, 85:97-177.
20. Flik G., Perry S.F. Cortisol stimulates whole body calcium uptake and the branchial calcium pump in freshwater rainbow trout. Journal of Endocrinology 1989, 120:75-82.
21. Gilmour K., Collier C., Dey C., Perry S. Roles of cortisol and carbonic anhydrase in acid-base compensation in rainbow trout, Oncorhynchus mykiss. Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology 2011, 181:501-515.
22. Gonzalez R.J., Wilson R.W., Wood C.M. Ionoregulation in tropical fishes from ion poor, acidic blackwaters. Fish Physiology 2005, 397-442. Academic Press, New York, NY. A.L. Val (Ed.).
23. Hirata T., Kaneko T., Ono T., Nakazato T., Furukawa N., Hasegawa S., Wakabayashi S., Shigekawa M., Chang M.-H., Romero M.F., Hirose S. Mechanism of acid adaptation of a fish living in a pH 3.5 lake. American Journal of Physiology - Regulatory, Integrative and Comparative Physiology 2003, 284:R1199-R1212.
24. Horng J.-L., Lin L.-Y., Huang C.-J., Katoh F., Kaneko T., Hwang P.-P. Knockdown of V-ATPase subunit A (atp6v1a) impairs acid secretion and ion balance in zebrafish (Danio rerio). American Journal of Physiology - Regulatory, Integrative and Comparative Physiology 2007, 292:R2068-R2076.
25. +-ATPase-rich cells in zebrafish embryos acclimated to an acidic environment. American Journal of Physiology - Cell Physiology 2009, 296:C682-C692.
26. Hwang P.-P. Ion uptake and acid secretion in zebrafish (Danio rerio). Journal of Experimental Biology 2009, 212:1745-1752.
27. Hwang P.-P., Lee T.-H., Lin L.-Y. Ion regulation in fish gills: recent progress in the cellular and molecular mechanisms. American Journal of Physiology - Regulatory, Integrative and Comparative Physiology 2011, 301:R28-R47.
28. Hwang P.P., Wu S.M. Role of cortisol in hypoosmoregulation in larvae of the tilapia (Oreochromis mossambicus). General and Comparative Endocrinology 1993, 92:318-324.
29. Hwang P.-P., Lee T.-H. New insights into fish ion regulation and mitochondrion-rich cells. Comparative Biochemistry and Physiology - Part A: Molecular & Integrative Physiology 2007, 148:479-497.
30. Hwang P.-P., Perry S.F. Ionic and acid-base regulation. Fish Physiology 2010, 311-344. Academic Press. S.F. Perry, M. Ekker, A.P. Farrell, C.J. Brauner (Eds.).
31. Inoue D., Wittbrodt J. One for all-a highly efficient and versatile method for fluorescent immunostaining in fish embryos. PLoS ONE 2011, 6(5):e19713.
32. Ivanis G., Braun M., Perry S.F. Renal expression and localization of SLC9A3 sodium/hydrogen exchanger and its possible role in acid-base regulation in freshwater rainbow trout (Oncorhynchus mykiss). American Journal of Physiology - Regulatory, Integrative and Comparative Physiology 2008, 295:R971-R978.
33. Ivanis G., Esbaugh A.J., Perry S.F. Branchial expression and localization of SLC9A2 and SLC9A3 sodium/hydrogen exchangers and their possible role in acid-base regulation in freshwater rainbow trout (Oncorhynchus mykiss). Journal of Experimental Biology 2008, 211:2467-2477.
34. Kelly S.P., Chasiotis H. Glucocorticoid and mineralocorticoid receptors regulate paracellular permeability in a primary cultured gill epithelium. Journal of Experimental Biology 2011, 214:2308-2318.
35. Kiilerich P., Kristiansen K., Madsen S.S. Cortisol regulation of ion transporter mRNA in Atlantic salmon gill and the effect of salinity on the signaling pathway. Journal of Endocrinology 2007, 194:417-427.
36. Kiilerich P., Tipsmark C.K., Borski R.J., Madsen S.S. Differential effects of cortisol and 11-deoxycorticosterone on ion transport protein mRNA levels in gills of two euryhaline teleosts, Mozambique tilapia (Oreochromis mossambicus) and striped bass (Morone saxatilis). Journal of Endocrinology 2011, 209:115-126.
37. + exchange activity in renal brush border membrane vesicles in response to metabolic acidosis: the role of glucocorticoids. Proceedings of the National Academy of Sciences 1984, 81:630-634.
38. + balance in zebrafish (Danio rerio) during prolonged exposure to acidic water. Comparative Biochemistry and Physiology - Part A: Molecular and Integrative Physiology 2011, 160:52-62.
39. + uptake in larval zebrafish, Danio rerio, in acidic water. American Journal of Physiology - Regulatory, Integrative and Comparative Physiology 2011, 301:R1517-R1528.
40. Laurent P., Perry S.F. Effects of cortisol on gill chloride cell morphology and ionic uptake in the freshwater trout, Salmo gairdneri. Cell and Tissue Research 1990, 259:429-442.
41. 3 metabolism. PLoS ONE 2011, 6:e23689.
42. +-ATPase activity in crude homogenates of fish gill tissue: inhibitor sensitivity and environmental and hormonal regulation. Journal of Experimental Biology 1993, 180:163-174.
43. Lin L.Y., Horng J.L., Kunkel J.G., Hwang P.P. Proton pump-rich cell secretes acid in skin of zebrafish larvae. Americal Journal of Physiology Cell Physiology 2006, 290:C371-C378.
44. McCormick S.D. Endocrine control of osmoregulation in teleost fish. American Zoologist 2001, 41:781-794.
45. McCormick S.D., Bradshaw D. Hormonal control of salt and water balance in vertebrates. General and Comparative Endocrinology 2006, 147:3-8.
46. +-ATPase activity and isoform mRNA levels in Atlantic salmon. General and Comparative Endocrinology 2008, 157:35-40.
47. McCurley A., Callard G. Characterization of housekeeping genes in zebrafish: male-female differences and effects of tissue type, developmental stage and chemical treatment. BMC Molecular Biology 2008, 9:102.
48. Mommsen T.P., Vijayan M.M., Moon T.W. Cortisol in teleosts: dynamics, mechanisms of action, and metabolic regulation. Reviews in Fish Biology and Fisheries 1999, 9:211-268.
49. Nesan, D., Kamkar, M., Burrows, J., Scott, I.C., Marsden, M., Vijayan, M.M., 2012. Glucocorticoid Receptor Signaling Is Essential for Mesoderm Formation and Muscle Development in Zebrafish. Endocrinology, 153, 1288-1300.
50. 2+ uptake in developing zebrafish. American Journal of Physiolology - Regulatory Integrative Compative Physiology 2005, 289:R1202-R1211.
51. Perry S.F. The chloride cell: structure and function in the gills of freshwater fishes. Annual Review of Physiology 1997, 59:325-347.
52. Perry S.F., Goss G.G., Fenwick J.C. Interrelationships between gill chloride cell morphology and calcium uptake in freshwater teleosts. Fish Physiology and Biochemistry 1992, 10:327-337.
53. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001, 29:e45.
54. Pippal J.B., Cheung C.M.I., Yao Y.-Z., Brennan F.E., Fuller P.J. Characterization of the zebrafish (Danio rerio) mineralocorticoid receptor. Molecular and Cellular Endocrinology 2010, 332:58-66.
55. - transport in two species of freshwater fish. Physiological and Biochemical Zoology 2005, 78:259-272.
56. Prunet P., Sturm A., Milla S. Multiple corticosteroid receptors in fish: from old ideas to new concepts. General and Comparative Endocrinology 2006, 147:17-23.
57. Rodela T.M., Esbaugh A.J., McDonald M.D., Gilmour K.M., Walsh P.J. Evidence for transcriptional regulation of the urea transporter in the gill of the Gulf toadfish, Opsanus beta. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 2011, 160:72-80.
58. Rodela T.M., McDonald M.D., Walsh P.J., Gilmour K.M. Interactions between cortisol and Rhesus glycoprotein expression in ureogenic toadfish, Opsanus beta. Journal of Experimental Biology 2012, 215:314-323.
59. Scott G., Keir K., Schulte P. Effects of spironolactone and RU486 on gene expression and cell proliferation after freshwater transfer in the euryhaline killifish. Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology 2005, 175:499-510.
60. Shahsavarani A., Perry S.F. Hormonal and environmental regulation of epithelial calcium channel in gill of rainbow trout (Oncorhynchus mykiss). American Journal of Physiology - Regulatory, Integrative and Comparative Physiology 2006, 291:R1490-R1498.
61. Shih T.-H., Horng J.-L., Hwang P.-P., Lin L.-Y. Ammonia excretion by the skin of zebrafish (Danio rerio) larvae. American Journal of Physiology - Cell Physiology 2008, 295:C1625-C1632.
62. Shih T.-H., Horng J.-L., Liu S.-T., Hwang P.-P., Lin L.-Y. Rhcg1 and NHE3b are involved in ammonium-dependent sodium uptake by zebrafish larvae acclimated to low-sodium water. American Journal of Physiology - Regulatory, Integrative and Comparative Physiology 2012, 302:R84-R93.
63. Shono T., Kurokawa D., Miyake T., Okabe M. Acquisition of glial cells missing 2 enhancers contributes to a diversity of ionocytes in zebrafish. PLoS ONE 2011, 6:e23746.
64. Sloman K.A., Desforges P.R., Gilmour K.M. Evidence for a mineralocorticoid-like receptor linked to branchial chloride cell proliferation in freshwater rainbow trout. Journal of Experimental Biology 2001, 204:3953-3961.
65. Sturm A., Bury N., Dengreville L., Fagart J., Flouriot G., Rafestin-Oblin M.E., Prunet P. 11-Deoxycorticosterone is a potent agonist of the rainbow trout (Oncorhynchus mykiss) mineralocorticoid receptor. Endocrinology 2005, 146:47-55.
66. Tipsmark C.K., Jã̧rgensen C., Brande-Lavridsen N., Engelund M., Olesen J.H., Madsen S.S. Effects of cortisol, growth hormone and prolactin on gill claudin expression in Atlantic salmon. General and Comparative Endocrinology 2009, 163:270-277.
67. + exchange complex. Journal of Experimental Biology 2009, 212:878-892.
68. Verdouw H., Van Echteld C.J.A., Dekkers E.M.J. Ammonia determination based on indophenol formation with sodium salicylate. Water Research 1978, 12:399-402.
69. Wendelaar Bonga S.E. The stress response in fish. Physiological Reviews 1997, 77:591-625.
70. Weihrauch D., Wilkie M.P., Walsh P.J. Ammonia and urea transporters in gills of fish and aquatic crustaceans. Journal of Experimental Biology 2009, 212:1716-1730.
71. Westerfield M. The Zebrafish Book. A Guide for The Laboratory Use Of Zebrafish (Danio rerio) 2000, Univ. of Oregon Press, Eugene, OR.
72. Wood C.M., Kelly S.P., Zhou B., Fletcher M., O'Donnell M., Eletti B., Pärt P. Cultured gill epithelia as models for the freshwater fish gill. Biochimica et Biophysica Acta (BBA) - Biomembranes 2002, 1566:72-83.
73. Wood C.M., Matsuo A.Y.O., Gonzalez R.J., Wilson R.W., Patrick M.L., Val A.L. Mechanisms of ion transport in Potamotrygon, a stenohaline freshwater elasmobranch native to the ion-poor blackwaters of the Rio Negro. Journal of Experimental Biology 2002, 205:3039-3054.
74. Wright P.A., Wood C.M. A new paradigm for ammonia excretion in aquatic animals: role of Rhesus (Rh) glycoproteins. Journal of Experimental Biology 2009, 212:2303-2312.
75. Wu S.-C., Horng J.-L., Liu S.-T., Hwang P.-P., Wen Z.-H., Lin C.-S., Lin L.-Y. Ammonium-dependent sodium uptake in mitochondrion-rich cells of medaka (Oryzias latipes) larvae. American Journal of Physiology - Cell Physiology 2010, 298:C237-C250.
76. Yao M., Hu F., Denver R.J. Distribution and corticosteroid regulation of glucocorticoid receptor in the brain of Xenopus laevis. Journal of Comparative Neurology 2008, 508:967-982.
77. Yan J.J., Chou M.Y., Kaneko T., Hwang P.P. Gene expression of Na+/H+ exchanger in zebrafish H+-ATPase-rich cells during acclimation to low-Na+ and acidic environments. American Journal of Physiology Cell Physiology 2007, 293:C1814-C1823.