The neuroretina is a novel mineralocorticoid target: Aldosterone up-regulates ion and water channels in Müller glial cells

FASEB Journal

Volumn 24, Issue 9, 2010, Pages 3405-3415

  Zhao, Min ^a   Valamanesh, Fatemeh ^a,b   Celerier, Isabelle ^d   Savoldelli, Michele ^c   Jonet, Laurent ^a   Jeanny, Jean Claude ^a   Jaisser, Frederic ^d   Farman, Nicolette ^d   Behar Cohen, Francine ^a  

^a INSERM   (France)

^b FONDATION OPHTALMOLOGIQUE ADOLPHE DE ROTHSCHILD   (France)

^c HÔTEL DIEU   (France)

^d CENTRE DE RECHERCHE DES CORDELIERS   (France)

Author keywords

Aquaporin 4; ENaC sodium channel; Glucocorticoids; Kir 4.1 potassium channel; Mineralocorticoid receptor

Indexed keywords

11BETA HYDROXYSTEROID DEHYDROGENASE 2; ALDOSTERONE; AQUAPORIN 4; BETA ACTIN; GLUCOCORTICOID RECEPTOR; ION CHANNEL; MINERALOCORTICOID; MINERALOCORTICOID RECEPTOR; POTASSIUM CHANNEL; SODIUM CHANNEL;

ANIMAL CELL; AQP4 GENE; ARTICLE; CONTROLLED STUDY; DIABETIC MACULAR EDEMA; ENAC ALPHA GENE; EXPLANT; GENE; GENE LOCATION; GLIA CELL; HOMEOSTASIS; HUMAN; HUMAN CELL; HYDRATION; IMMUNOFLUORESCENCE; KIR4.1 GENE; LEWIS RAT; MICROVILLUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION; RECEPTOR OCCUPANCY; RECEPTOR UPREGULATION; REGULATORY MECHANISM; RETINA; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ALDOSTERONE; ANIMALS; AQUAPORIN 4; BLOTTING, WESTERN; CELL LINE; CELLS, CULTURED; DEXAMETHASONE; EPITHELIAL SODIUM CHANNEL; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION; HUMANS; IMMUNOHISTOCHEMISTRY; POLYMERASE CHAIN REACTION; POTASSIUM CHANNELS, INWARDLY RECTIFYING; RATS; RATS, INBRED LEW; RECEPTORS, GLUCOCORTICOID; RECEPTORS, MINERALOCORTICOID; RETINA;

RATTUS;

EID: 77956628297     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.09-154344     Document Type: Article

References (43)

1. Bringmann, A., Pannicke, T., Grosche, J., Francke, M., Wiedemann, P., Skatchkov, S. N., Osborne, N. N., and Reichenbach, A. (2006) Muller cells in the healthy and diseased retina. Prog. Retin. Eye Res. 25, 397-424
2. Verkman, A. S., Ruiz-Ederra, J., and Levin, M. H. (2008) Functions of aquaporins in the eye. Prog. Retin. Eye Res. 27, 420-433
3. Baath, J., Ells, A. L., Crichton, A., Kherani, A., and Williams, R. G. (2007) Safety profile of intravitreal triamcinolone acetonide. J. Ocul. Pharmacol. Ther. 23, 304-310
4. Jonas, J. B., Kreissig, I., and Degenring, R. (2005) Intravitreal triamcinolone acetonide for treatment of intraocular proliferative, exudative, and neovascular diseases. Prog. Retin. Eye Res. 24, 587-611 (Pubitemid 40949559)
5. Massin, P., Audren, F., Haouchine, B., Erginay, A., Bergmann, J. F., Benosman, R., Caulin, C., and Gaudric, A. (2004) Intravitreal triamcinolone acetonide for diabetic diffuse macular edema: preliminary results of a prospective controlled trial. Ophthalmology 111, 218-224 (Pubitemid 38183217)
6. Valamanesh, F., Torriglia, A., Savoldelli, M., Gandolphe, C., Jeanny, J. C., BenEzra, D., and Behar-Cohen, F. (2007) Glucocorticoids induce retinal toxicity through mechanisms mainly associated with paraptosis. Mol. Vis. 13, 1746-1757 (Pubitemid 47499927)
7. Farman, N., and Rafestin-Oblin, M. E. (2001) Multiple aspects of mineralocorticoid selectivity. Am. J. Physiol. Renal Physiol. 280, F181-F192
8. Viengchareun, S., Le Menuet, D., Martinerie, L., Munier, M., Pascual-Le Tallec, L., and Lombes, M. (2007) The mineralocorticoid receptor: insights into its molecular and (patho)physiological biology. Nucl. Recept. Signal. 5, e012
9. Pippal, J. B., and Fuller, P. J. (2008) Structure-function relationships in the mineralocorticoid receptor. J. Mol. Endocrinol. 41, 405-413
10. Revollo, J. R., and Cidlowski, J. A. (2009) Mechanisms generating diversity in glucocorticoid receptor signaling. Ann. N. Y. Acad. Sci. 1179, 167-178
11. Bhalla, V., Soundararajan, R., Pao, A. C., Li, H., and Pearce, D. (2006) Disinhibitory pathways for control of sodium transport: regulation of ENaC by SGK1 and GILZ. Am. J. Physiol. Renal Physiol. 291, F714-F721
12. Yoo, D., Kim, B. Y., Campo, C., Nance, L., King, A., Maouyo, D., and Welling, P. A. (2003) Cell surface expression of the ROMK (Kir 1.1) channel is regulated by the aldosterone-induced kinase, SGK-1, and protein kinase A. J. Biol. Chem. 278, 23066-23075
13. Farman, N., Maubec, E., Poeggeler, B., Klatte, J. E., Jaisser, F., and Paus, R. (2010) The mineralocorticoid receptor as a novel player in skin biology: beyond the renal horizon? Exp. Dermatol. 19, 100-107.
14. Zennaro, M. C., Caprio, M., and Feve, B. (2009) Mineralocorticoid receptors in the metabolic syndrome. Trends Endocrinol. Metab. 20, 444-451
15. Joels, M., Karst, H., DeRijk, R., and de Kloet, E. R. (2008) The coming out of the brain mineralocorticoid receptor. Trends Neurosci. 31, 1-7
16. Derijk, R. H., and de Kloet, E. R. (2008) Corticosteroid receptor polymorphisms: determinants of vulnerability and resilience. Eur. J. Pharmacol. 583, 303-311
17. Rickard, A. J., and Young, M. J. (2009) Corticosteroid receptors, macrophages and cardiovascular disease. J. Mol. Endocrinol. 42, 449-459
18. Fiebeler, A., Muller, D. N., Shagdarsuren, E., and Luft, F. C. (2007) Aldosterone, mineralocorticoid receptors, and vascular inflammation. Curr. Opin. Nephrol. Hypertens. 16, 134-142
19. Funder, J. W. (2007) The role of aldosterone and mineralocorticoid receptors in cardiovascular disease. Am. J. Cardiovasc. Drugs 7, 151-157 (Pubitemid 47047985)
20. Wilkinson-Berka, J. L., Tan, G., Jaworski, K., and Miller, A. G. (2009) Identification of a retinal aldosterone system and the protective effects of mineralocorticoid receptor antagonism on retinal vascular pathology. Circ. Res. 104, 124-133
21. Mirshahi, M., Nicolas, C., Mirshahi, A., Hecquet, C., d'Hermies, F., Faure, J. P., and Agarwal, M. K. (1996) The mineralocorticoid hormone receptor and action in the eye. Biochem. Biophys. Res. Commun. 219, 150-156
22. Limb, G. A., Salt, T. E., Munro, P. M., Moss, S. E., and Khaw, P. T. (2002) In vitro characterization of a spontaneously immortalized human Muller cell line (MIO-M1). Invest. Ophthalmol. Vis. Sci. 43, 864-869
23. De Kozak, Y., Naud, M. C., Bellot, J., Faure, J. P., and Hicks, D. (1994) Differential tumor necrosis factor expression by resident retinal cells from experimental uveitis-susceptible and -resistant rat strains. J. Neuroimmunol 55, 1-9 (Pubitemid 24356801)
24. Ouvrard-Pascaud, A., Sainte-Marie, Y., Benitah, J. P., Perrier, R., Soukaseum, C., Cat, A. N., Royer, A., Le Quang, K., Charpentier, F., Demolombe, S., Mechta-Grigoriou, F., Beggah, A. T., Maison- Blanche, P., Oblin, M. E., Delcayre, C., Fishman, G. I., Farman, N., Escoubet, B., and Jaisser, F. (2005) Conditional mineralocorticoid receptor expression in the heart leads to life-threatening arrhythmias. Circulation 111, 3025-3033
25. Duc, C., Farman, N., Canessa, C. M., Bonvalet, J. P., and Rossier, B. C. (1994) Cell-specific expression of epithelial sodium channel alpha, beta, and gamma subunits in aldosterone-responsive epithelia from the rat: localization by in situ hybridization and immunocytochemistry. J. Cell Biol. 127, 1907-1921
26. Bringmann, A., Iandiev, I., Pannicke, T., Wurm, A., Hollborn, M., Wiedemann, P., Osborne, N. N., and Reichenbach, A. (2009) Cellular signaling and factors involved in Muller cell gliosis: neuroprotective and detrimental effects. Prog. Retin. Eye Res. 28, 423-451
27. Goodyear, M. J., Crewther, S. G., and Junghans, B. M. (2009) A role for aquaporin-4 in fluid regulation in the inner retina. Vis. Neurosci. 26, 159-165
28. Pitt, B., Zannad, F., Remme, W. J., Cody, R., Castaigne, A., Perez, A., Palensky, J., and Wittes, J. (1999) The effect of spironolactone on morbidity and mortality in patients with severe heart failure. Randomized Aldactone Evaluation Study Investigators. N. Engl. J. Med. 341, 709-717
29. Rozeboom, A. M., Akil, H., and Seasholtz, A. F. (2007) Mineralocorticoid receptor overexpression in forebrain decreases anxiety-like behavior and alters the stress response in mice. Proc. Natl. Acad. Sci. U. S. A. 104, 4688-4693
30. Pascual-Le Tallec, L., and Lombes, M. (2005) The mineralocorticoid receptor: a journey exploring its diversity and specificity of action. Mol. Endocrinol. 19, 2211-2221
31. Moscona, A. A., and Piddington, R. (1967) Enzyme induction by corticosteroids in embryonic cells: steroid structure and inductive effect. Science 158, 496-497
32. Golestaneh, N., De Kozak, Y., Klein, C., and Mirshahi, M. (2001) Epithelial sodium channel and the mineralocorticoid receptor in cultured rat Muller glial cells. Glia 33, 160-168 (Pubitemid 32160979)
33. Brockway, L. M., Zhou, Z. H., Bubien, J. K., Jovov, B., Benos, D. J., and Keyser, K. T. (2002) Rabbit retinal neurons and glia express a variety of ENaC/DEG subunits. Am. J. Physiol. Cell. Physiol. 283, C126-C134
34. Kofuji, P., Ceelen, P., Zahs, K. R., Surbeck, L. W., Lester, H. A., and Newman, E. A. (2000) Genetic inactivation of an inwardly rectifying potassium channel (Kir4.1 subunit) in mice: phenotypic impact in retina. J. Neurosci. 20, 5733-5740
35. Iandiev, I., Pannicke, T., Hollborn, M., Wiedemann, P., Reichenbach, A., Grimm, C., Reme, C. E., and Bringmann, A. (2008) Localization of glial aquaporin-4 and Kir4.1 in the light-injured murine retina. Neurosci. Lett. 434, 317-321
36. Ruiz-Ederra, J., Zhang, H., and Verkman, A. S. (2007) Evidence against functional interaction between aquaporin-4 water channels and Kir4.1 potassium channels in retinal Muller cells. J. Biol. Chem. 282, 21866-21872 (Pubitemid 47195767)
37. Boulkroun, S., Fay, M., Zennaro, M. C., Escoubet, B., Jaisser, F., Blot-Chabaud, M., Farman, N., and Courtois-Coutry, N. (2002) Characterization of rat NDRG2 (N-Myc downstream regulated gene 2), a novel early mineralocorticoid-specific induced gene. J. Biol. Chem. 277, 31506-31515 (Pubitemid 34968952)
38. Gaeggeler, H. P., Gonzalez-Rodriguez, E., Jaeger, N. F., Loffing-Cueni, D., Norregaard, R., Loffing, J., Horisberger, J. D., and Rossier, B. C. (2005) Mineralocorticoid versus glucocorticoid receptor occupancy mediating aldosterone-stimulated sodium transport in a novel renal cell line. J. Am. Soc. Nephrol. 16, 878-891
39. Leopold, J. A., Dam, A., Maron, B. A., Scribner, A. W., Liao, R., Handy, D. E., Stanton, R. C., Pitt, B., and Loscalzo, J. (2007) Aldosterone impairs vascular reactivity by decreasing glucose-6-phosphate dehydrogenase activity. Nat. Med. 13, 189-197 (Pubitemid 46245770)
40. Berger, S., Bleich, M., Schmid, W., Cole, T. J., Peters, J., Watanabe, H., Kriz, W., Warth, R., Greger, R., and Schutz, G. (1998) Mineralocorticoid receptor knockout mice: pathophysiology of Na+ metabolism. Proc. Natl. Acad. Sci. U. S. A. 95, 9424-9429
41. Cole, T. J., Blendy, J. A., Monaghan, A. P., Krieglstein, K., Schmid, W., Aguzzi, A., Fantuzzi, G., Hummler, E., Unsicker, K., and Schutz, G. (1995) Targeted disruption of the glucocorticoid receptor gene blocks adrenergic chromaffin cell development and severely retards lung maturation. Genes Dev. 9, 1608-1621
42. Kaur, C., Sivakumar, V., Yong, Z., Lu, J., Foulds, W. S., and Ling, E. A. (2007) Blood-retinal barrier disruption and ultrastructural changes in the hypoxic retina in adult rats: the beneficial effect of melatonin administration. J. Pathol. 212, 429-439
43. Guo, C., Martinez-Vasquez, D., Mendez, G. P., Toniolo, M. F., Yao, T. M., Oestreicher, E. M., Kikuchi, T., Lapointe, N., Pojoga, L., Williams, G. H., Ricchiuti, V., and Adler, G. K. (2006) Mineralocorticoid receptor antagonist reduces renal injury in rodent models of types 1 and 2 diabetes mellitus. Endocrinology 147, 5363-5373