Failure to downregulate the epithelial sodium channel causes salt sensitivity in hsd11b2 heterozygote mice

Hypertension

Volumn 60, Issue 3, 2012, Pages 684-690

  Craigie, Eilidh ^a   Evans, Louise C ^a   Mullins, John J ^a   Bailey, Matthew A ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

glucocorticoid receptor; renin angiotensin system; RU486; spironolactone

Indexed keywords

11BETA HYDROXYSTEROID DEHYDROGENASE 2; ALDOSTERONE; AMILORIDE; BENZAMIL; CORTICOSTERONE; EPITHELIAL SODIUM CHANNEL; MESSENGER RNA; MIFEPRISTONE; SERUM AND GLUCOCORTICOID REGULATED KINASE 1; SPIRONOLACTONE;

ANIMAL EXPERIMENT; ARTICLE; BLOOD PRESSURE; CONTROLLED STUDY; CORRELATION ANALYSIS; CORTICOSTERONE BLOOD LEVEL; DOWN REGULATION; GENOTYPE; GLOMERULUS FILTRATION RATE; HETEROZYGOTE; HIGH SODIUM INTAKE; HYPERTENSION; KIDNEY BLOOD FLOW; KIDNEY VASCULAR RESISTANCE; MOUSE; NONHUMAN; PHENOTYPE; PHYSICAL SENSITIVITY; POTASSIUM EXCRETION; PRIORITY JOURNAL; SALT SENSITIVITY; SODIUM ABSORPTION; SODIUM EXCRETION; SODIUM INTAKE; SODIUM RESTRICTION;

11-BETA-HYDROXYSTEROID DEHYDROGENASE TYPE 2; ANIMALS; BLOOD PRESSURE; CORTICOSTERONE; DOWN-REGULATION; EPITHELIAL SODIUM CHANNELS; GENOTYPE; HETEROZYGOTE; KIDNEY; MICE; MICE, INBRED STRAINS; MODELS, ANIMAL; PHENOTYPE; RECEPTORS, GLUCOCORTICOID; REGIONAL BLOOD FLOW; SALT-TOLERANCE; SODIUM, DIETARY; VASCULAR RESISTANCE;

EID: 84865511140     PISSN: 0194911X     EISSN: 15244563     Source Type: Journal    
DOI: 10.1161/HYPERTENSIONAHA.112.196410     Document Type: Article

References (46)

1. Couser WG, Riella MC. Cardiovascular disease: World Kidney Day 2011-protect your kidneys, save your heart. Nat Rev Nephrol. 2011;7: 130-132.
2. Haddy FJ. Role of dietary salt in hypertension. Life Sci. 2006;79: 1585-1592.
3. Weinberger MH, Fineberg NS, Fineberg SE, Weinberger M. Salt sensitivity, pulse pressure, and death in normal and hypertensive humans. Hypertension. 2001;37:429-432.
4. Sanders PW. Vascular consequences of dietary salt intake. Am J Physiol Renal Physiol. 2009;297:F237-F243.
5. Waanders F, de Vries LV, van Goor H, Hillebrands JL, Laverman GD, Bakker SJ, Navis G. Aldosterone, from (patho)physiology to treatment in cardiovascular and renal damage. Curr Vasc Pharmacol. 2011;9: 594-605.
6. Nishiyama A, Yao L, Nagai Y, Miyata K, Yoshizumi M, Kagami S, Kondo S, Kiyomoto H, Shokoji T, Kimura S, Kohno M, Abe Y. Possible contributions of reactive oxygen species and mitogen-activated protein kinase to renal injury in aldosterone/salt-induced hypertensive rats. Hypertension. 2004;43:841-848.
7. Usukura M, Zhu A, Yoneda T, Karashima S, Yagi K, Yamagishi M, Takeda Y. Effects of a high-salt diet on adipocyte glucocorticoid receptor and 11β-hydroxysteroid dehydrogenase 1 in salt-sensitive hypertensive rats. Steroids. 2009;74:978-982.
8. Bailey MA, Mullins JJ, Kenyon CJ. Mineralocorticoid and glucocorticoid receptors stimulate epithelial sodium channel activity in a mouse model of Cushing syndrome. Hypertension. 2009;54:890-896.
9. Shibata S, Mu S, Kawarazaki H, Muraoka K, Ishizawa K, Yoshida S, Kawarazaki W, Takeuchi M, Ayuzawa N, Miyoshi J, Takai Y, Ishikawa A, Shimosawa T, Ando K, Nagase M, Fujita T. Rac1 GTPase in rodent kidneys is essential for salt-sensitive hypertension via a mineralocorticoid receptor-dependent pathway. J Clin Invest. 2011;12:3233-3243.
10. Funder JW, Pearce PT, Smith R, Smith AI. Mineralocorticoid action: target tissue specificity is enzyme, not receptor, mediated. Science. 1988; 242:583-585.
11. Funder JW. Aldosterone and mineralocorticoid receptors in the cardiovascular system. Prog Cardiovasc Dis. 2010;52:393-400.
12. Kotelevtsev Y, Brown RW, Fleming S, Kenyon C, Edwards CR, Seckl JR, Mullins JJ. Hypertension in mice lacking 11β-hydroxysteroid dehydrogenase type 2. J Clin Invest. 1999;103:683-689.
13. Bailey MA, Paterson JM, Hadoke PW, Wrobel N, Bellamy CO, Brownstein DG, Seckl JR, Mullins JJ. A switch in the mechanism of hypertension in the syndrome of apparent mineralocorticoid excess. J Am Soc Nephrol. 2008;19:47-58.
14. Dave-Sharma S, Wilson RC, Harbison MD, Newfield R, Azar MR, Krozowski ZS, Funder JW, Shackleton CH, Bradlow HL, Wei JQ, Hertecant J, Moran A, Neiberger RE, Balfe JW, Fattah A, Daneman D, Akkurt HI, De Santis C, New MI. Examination of genotype and phenotype relationships in 14 patients with apparent mineralocorticoid excess. J Clin Endo Metab. 1998;83:2244-2254.
15. Ulick S, Tedde R, Mantero F. Pathogenesis of the type 2 variant of the syndrome of apparent mineralocorticoid excess. J Clin Endo Metab. 1990;70:200-206.
16. Agarwal AK, Giacchetti G, Lavery G, Nikkila H, Palermo M, Ricketts M, McTernan C, Bianchi G, Manunta P, Strazzullo P, Mantero F, White PC, Stewart PM. CA-Repeat polymorphism in intron 1 of HSD11B2: effects on gene expression and salt sensitivity. Hypertension. 2000;36:187-194.
17. Alikhani-Koupaei R, Fouladkou F, Fustier P, Cenni B, Sharma AM, Deter HC, Frey BM, Frey FJ. Identification of polymorphisms in the human 11β-hydroxysteroid dehydrogenase type 2 gene promoter: functional characterization and relevance for salt sensitivity. FASEB J. 2007;21: 3618-3628.
18. Bocchi B, Kenouch S, Lamarre-Cliche M, Muffat-Joly M, Capron MH, Fiet J, Morineau G, Azizi M, Bonvalet JP, Farman N. Impaired 11β-hydroxysteroid dehydrogenase type 2 activity in sweat gland ducts in human essential hypertension. Hypertension. 2004;43:803-808.
19. Poch E, Gonzalez D, Giner V, Bragulat E, Coca A, de La Sierra A. Molecular basis of salt sensitivity in human hypertension: evaluation of renin-angiotensin-aldosterone system gene polymorphisms. Hypertension. 2001;38:1204-1209.
20. Kerstens MN, Navis G, Dullaart RP. Salt sensitivity and 11β-hydroxysteroid dehydrogenase type 2 activity. Am J Hypertens. 2004;17: 283-284.
21. Melander O, Frandsen E, Groop L, Hulthen UL. No evidence of a relation between 11β-hydroxysteroid dehydrogenase type 2 activity and salt sensitivity. Am J Hypertens. 2003;16:729-733.
22. Bailey MA, Craigie E, Livingstone DE, Kotelevtsev YV, Al-Dujaili EA, Kenyon CJ, Mullins JJ. Hsd11b2 haploinsufficiency in mice causes salt sensitivity of blood pressure. Hypertension. 2011;57:515-520.
23. Mullins LJ, Bailey MA, Mullins JJ. Hypertension, kidney, and transgenics: a fresh perspective. Physiol Rev. 2006;86:709-746.
24. Soundararajan R, Pearce D, Ziera T. The role of the ENaC-regulatory complex in aldosterone-mediated sodium transport. Mol Cell Endocrinol. 2012;350:242-247.
25. + exchanger gene family: structure and function studies. Am J Physiol. 1995;269:G1-G11.
26. Kleyman TR, Cragoe EJ Jr. The mechanism of action of amiloride. Semin Nephrol. 1988;8:242-248.
27. Morineau G, Sulmont V, Salomon R, Fiquet-Kempf B, Jeunemaitre X, Nicod J, Ferrari P. Apparent mineralocorticoid excess: report of six new cases and extensive personal experience. J Am Soc Nephrol. 2006;17: 3176-3184.
28. Quinkler M, Stewart PM. Hypertension and the cortisol-cortisone shuttle. J Clin Endo Metab. 2003;88:2384-2392.
29. Gaeggeler HP, Gonzalez-Rodriguez E, Jaeger NF, Loffing-Cueni D, Norregaard R, Loffing J, Horisberger JD, Rossier BC. Mineralocorticoid versus glucocorticoid receptor occupancy mediating aldosteronestimulated sodium transport in a novel renal cell line. J Am Soc Nephrol. 2005;16:878-891.
30. Naray-Fejes-Toth A, Fejes-Toth G. Glucocorticoid receptors mediate mineralocorticoid-like effects in cultured collecting duct cells. Am J Physiol. 1990;259:F672-F678.
31. + . J Am Soc Nephrol. 2003;14:1107-1115.
32. Ackermann D, Gresko N, Carrel M, Loffing-Cueni D, Habermehl D, Gomez-Sanchez C, Rossier BC, Loffing J. In vivo nuclear translocation of mineralocorticoid and glucocorticoid receptors in rat kidney: differential effect of corticosteroids along the distal tubule. Am J Physiol Renal Physiol. 2010;299:F1473-F1485.
33. + channels by adrenal steroids: Mineralocorticoid and glucocorticoid effects. Am J Physiol Renal Physiol. 2012;302:F20-F26.
34. + channel in vitro and in vivo. Proc Natl Acad Sci. 2007;104:4020-4024.
35. O'Reilly M, Marshall E, Macgillivray T, Mittal M, Xue W, Kenyon CJ, Brown RW. Dietary electrolyte-driven responses in the renal WNK kinase pathway in vivo. J Am Soc Nephrol. 2006;17:2402-2413.
36. Li C, Li Y, Liu H, Sun Z, Lu J, Zhao Y. Glucocorticoid repression of human with-no-lysine (K) kinase-4 gene expression is mediated by the negative response elements in the promoter. J Mol Endocrinol. 2008; 40:3-12.
37. Mu S, Shimosawa T, Ogura S, Wang H, Uetake Y, Kawakami-Mori F, Marumo T, Yatomi Y, Geller DS, Tanaka H, Fujita T. Epigenetic modulation of the renal β-adrenergic-WNK4 pathway in salt-sensitive hypertension. Nat Med. 2011;17:573-580.
38. Goodwin JE, Zhang J, Velazquez H, Geller DS. The glucocorticoid receptor in the distal nephron is not necessary for the development or maintenance of dexamethasone-induced hypertension. Biochem Biophys Res Commun. 2010;394:266-271.
39. Hatakeyama H, Inaba S, Takeda R, Miyamori I. 11β-Hydroxysteroid dehydrogenase in human vascular cells. Kidney Int. 2000;57:1352-1357.
40. Gong R, Morris DJ, Brem AS. Variable expression of 11β hydroxysteroid dehydrogenase isoforms in vascular endothelial cells. Steroids. 2008;73: 1187-1196.
41. Hadoke PW, Christy C, Kotelevtsev YV, Williams BC, Kenyon CJ, Seckl JR, Mullins JJ, Walker BR. Endothelial cell dysfunction in mice after transgenic knockout of type 2, but not type 1, 11β-hydroxysteroid dehydrogenase. Circulation. 2001;104:2832-2837.
42. Kusche-Vihrog K, Sobczak K, Bangel N, Wilhelmi M, Nechyporuk-Zloy V, Schwab A, Schillers H, Oberleithner H. Aldosterone and amiloride alter ENaC abundance in vascular endothelium. Pflugers Arch. 2008;455: 849-857.
43. Oberleithner H, Riethmuller C, Schillers H, MacGregor GA, de Wardener HE, Hausberg M. Plasma sodium stiffens vascular endothelium and reduces nitric oxide release. Proc Natl Acad Sci. 2007;104:16281-16286.
44. Weber CS, Thayer JF, Rudat M, Sharma AM, Perschel FH, Buchholz K, Deter HC. Salt-sensitive men show reduced heart rate variability, lower norepinephrine and enhanced cortisol during mental stress. J Hum Hypertens. 2008;22:423-431.
45. Kerstens MN, van der Kleij FG, Boonstra AH, Sluiter WJ, Koerts J, Navis G, Dullaart RP. Salt loading affects cortisol metabolism in normotensive subjects: relationships with salt sensitivity. J Clin Endo Metab. 2003;88: 4180-4185.
46. Geerling JC, Loewy AD. Aldosterone-sensitive neurons in the nucleus of the solitary tract: efferent projections. J Comp Neurol. 2006;497: 223-250.