Mineralocorticoid receptor antagonism attenuates glomerular filtration barrier remodeling in the transgenic Ren2 rat

American Journal of Physiology - Renal Physiology

Volumn 296, Issue 5, 2009, Pages

  Whaley Connell, Adam ^a,d   Habibi, Javad ^a,d   Wei, Yongzhong ^a,d   Gutweiler, Alex ^a,d   Jellison, Jessica ^a   Wiedmeyer, Charles E ^b   Ferrario, Carlos M ^c   Sowers, James R ^a,d  

^a University of Missouri   (United States)

^b UNIVERSITY OF MISSOURI   (United States)

^c WAKE FOREST UNIVERSITY   (United States)

^d WJB Dorn VA Medical Center   (United States)

Author keywords

Oxidative stress; Podocyte; Reduced nicotinamide adenine dinucleotide phosphate oxidase; Renal mineralocorticoid receptor

Indexed keywords

ALDOSTERONE; INSULIN; INSULIN RECEPTOR SUBSTRATE 1; MINERALOCORTICOID RECEPTOR; PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; RHO KINASE; SPIRONOLACTONE;

ALBUMINURIA; ALDOSTERONE BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG ANTAGONISM; GENE OVEREXPRESSION; GLOMERULUS FILTRATION; LOW DRUG DOSE; NONHUMAN; OXIDATIVE STRESS; PARACRINE SIGNALING; PODOCYTE; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; RAT; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; TISSUE REPAIR; TRANSGENIC RAT;

EID: 66049141708     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.90646.2008     Document Type: Article

References (43)

1. 307. J Biol Chem 275: 9047-9054, 2000.
2. Brown NJ, Nakamura S, Ma L, Nakamura I, Donnert E, Freeman M, Vaughan DE, Fogo AB. Aldosterone modulates plasminogen activator inhibitor-1 and glomerulosclerosis in vivo. Kidney Int 58: 1219-1227, 2000. (Pubitemid 30429870)
3. Calle C, Campión J, García-Arencibia M, Maestro B, Dávila N. Transcriptional inhibition of the human insulin receptor gene by aldosterone. J Steroid Biochem Mol Biol 84: 543-553, 2003. (Pubitemid 36588808)
4. Campbell DJ, Rong P, Kladis A, Rees B, Ganten D, Skinner SL. Angiotensin and bradykinin peptides in the TGR(mRen-2)27 rat. Hypertension 25: 1014-1020, 1995.
5. Connell JMC, Davies E. The new biology of aldosterone. J Endocrinol 186: 1-20, 2005. (Pubitemid 41015660)
6. Cooper SA, Whaley-Connell A, Habibi J, Wei Y, Lastra G, Manrique C, Stas S, Sowers JR. Renin-angiotensin-aldosterone system and oxidative stress in cardiovascular insulin resistance. Am J Physiol Heart Circ Physiol 293: H2009-H2023, 2007. (Pubitemid 47605846)
7. Diah S, Zhang GX, Nagai Y, Zhang W, Gang L, Kimura S, Hamid MR, Tamiya T, Nishiyama A, Hitomi H. Aldosterone induces myofibroblastic transdifferentiation and collagen gene expression through the Rho-kinase dependent signaling pathway in rat mesangial cells. Exp Cell Res 314: 3654-3662, 2008.
8. Fujisawa G, Okada K, Muto S, Fujita N, Itabashi N, Kusano E, Ishibashi S. Spironolactone prevents early renal injury in streptozotocin-induced diabetic rats. Kidney Int 66: 1493-1502, 2004. (Pubitemid 39298382)
9. Funder JW. The nongenomic actions of aldosterone. Endocr Rev 26: 313-321, 2005.
10. Gojo A, Utsunomiya K, Taniguchi K, Yokota T, Ishizawa S, Kanazawa Y, Kurata H, Tajima N. The Rho-kinase inhibitor, fasudil, attenuates diabetic nephropathy in streptozotocin-induced diabetic rats. Eur J Pharmacol 568: 242-247, 2007. (Pubitemid 46976901)
11. Hayashi K, Wakino S, Kanda T, Homma K, Sugano N, Saruta T. Molecular mechanisms and therapeutic strategies of chronic renal injury: role of rho-kinase in the development of renal injury. J Pharmacol Sci 100: 29-33, 2006. (Pubitemid 43161611)
12. Hitomi H, Kiyomoto H, Nishiyama A, Hara T, Moriwaki K, Kaifu K, Ihara G, Fujita Y, Ugawa T, Kohno M. Aldosterone suppresses insulin signaling via the downregulation of insulin receptor substrate-1 in vascular smooth muscle cells. Hypertension 50: 750-755, 2007. (Pubitemid 47442741)
13. Jessup JA, Trask AJ, Chappell MC, Nagata S, Kato J, Kitamura K, Ferrario CM. Localization of the novel angiotensin peptide, angiotensin-(1-12), in heart and kidney of hypertensive and normotensive rats. Am J Physiol Heart Circ Physiol 294: H2614-H2618, 2008.
14. Johar S, Cave AC, Narayanapanicker A, Grieve DJ, Shah AM. Aldosterone mediates angiotensin II-induced interstitial cardiac fibrosis via a Nox2-containing NADPH oxidase. FASEB J 20: 1546-1548, 2006.
15. Kikuchi Y, Yamada M, Imakiire T, Kushiyama T, Higashi K, Hyodo N, Yamamoto K, Oda T, Suzuki S, Miura S. A Rho-kinase inhibitor, fasudil, prevents development of diabetes and nephropathy in insulin-resistant diabetic rats. J Endocrinol 192: 595-603, 2007. (Pubitemid 46455962)
16. Kolavennu V, Zeng L, Peng H, Wang Y, Danesh FR. Targeting of RhoA/ROCK signaling ameliorates progression of diabetic nephropathy independent of glucose control. Diabetes 57: 714-723, 2008.
17. Koshikawa S, Nishikimi T, Inaba C, Akimoto K, Matsuoka H. Fasudil, a Rho-kinase inhibitor, reverses L-NAME exacerbated severe nephrosclerosis in spontaneously hypertensive rats. J Hypertens 26: 1837-1848, 2008.
18. Lastra G, Whaley-Connell A, Manrique C, Habibi J, Gutweiler AA, Appesh L, Hayden MR, Wei Y, Ferrario C, Sowers JR. Low-dose spironolactone reduces reactive oxygen species generation and improves insulin-stimulated glucose transport in skeletal muscle in the TG(mRen2)27 rat. Am J Physiol Endocrinol Metab 295: E110-E116, 2008.
19. Lee JK, Tsai SY. Multiple hormone response elements can confer glucocorticoid regulation on the human insulin receptor gene. Mol Endocrinol 8: 625-634, 1994.
20. Lehtonen S. Connecting the interpodocyte slit diaphragm and actin dynamics: emerging role for the nephrin signaling complex. Kidney Int 73: 903-905, 2008.
21. Mazak I, Fiebeler A, Muller DN, Park JK, Shagdarsuren E, Lindschau C, Dechend R, Viedt C, Pilz B, Haller H, Luft FC. Aldosterone potentiates angiotensin II-induced signaling in vascular smooth muscle cells. Circulation 109: 2792-2800, 2004. (Pubitemid 38737927)
22. Miyata K, Rahman M, Shokoji T, Nagai Y, Zhang GX, Sun GP, Kimura S, Yukimura T, Kiyomoto H, Kohno M, Abe Y, Nishiyama A. Aldosterone stimulates reactive oxygen species production through activation of NADPH oxidase in rat mesangial cells. J Am Soc Nephrol 16: 2906-2912, 2005.
23. Montezano AC, Callera GE, Yogi A, He Y, Tostes RC, He G, Schiffrin EL, Touyz RM. Aldosterone and angiotensin II synergistically stimulate migration in vascular smooth muscle cells through c-Src-regulated redox-sensitive RhoA pathways. Arterioscler Thromb Vasc Biol 28: 1511-1518, 2008.
24. Morris EM, Whaley-Connell A, Thyfault JP, Britton SL, Lock LG, Wei Y, Ibdah JI, Sowers JR. Low aerobic capacity and high fat diet contributes to oxidative stress and IRS-1 degradation in the kidney. Am J Nephrol 30: 112-119, 2008.
25. Nagase M, Yoshida S, Shibata S, Nagase T, Gotoda T, Ando K, Fujita T. Enhanced aldosterone signaling in the early nephropathy of rats with metabolic syndrome: possible contribution of fat-derived factors. J Am Soc Nephrol 17: 3438-3446, 2006.
26. Nagata S, Kato J, Sasaki K, Minamino N, Eto T, Kitamura K. Isolation and identification of pro-angiotensin-12, a possible component of the renin-angiotensin system. Biochem Biophys Res Commun 350: 1026-1031, 2006. (Pubitemid 44596223)
27. Nakano S, Kobayashi N, Yoshida K, Ohno T, Matsuoka H. Cardioprotective mechanisms of spironolactone associated with the angiotensin-converting enzyme/epidermal growth factor receptor/extracellular signal-regulated kinases, NAD(P)H oxidase/lectin-like oxidized low-density lipoprotein receptor-1, and Rho-kinase pathways in aldosterone/salt-induced hypertensive rats. Hypertens Res 28: 925-936, 2005. (Pubitemid 43173963)
28. Onozato ML, Tojo A, Kobayashi N, Goto A, Matsuoka H, Fujita T. Dual blockade of aldosterone and angiotensin II additively suppresses TGF-beta and NADPH oxidase in the hypertensive kidney. Nephrol Dial Transplant 22: 1314-1322, 2007. (Pubitemid 47072218)
29. Peng F, Wu D, Gao B, Ingram AJ, Zhang B, Chorneyko K, McKenzie R, Krepinsky JC. RhoA/Rho-kinase contribute to the pathogenesis of diabetic renal disease. Diabetes 57: 1683-1692, 2008.
30. Pitt B, Zannad F, Remme WJ, Cody R, Castaigne A, Perez A, Palensky J, Wittes J, Eplerenone Post-Acute Myocardial Infarction Heart Failure Efficacy and Survival Study Investigators. Eplerenone, a selective aldosterone blocker, in patients with left ventricular dysfunction after myocardial infarction. N Engl J Med 348: 1309-1321, 2003. (Pubitemid 36384098)
31. Sander M, Bader M, Djavidani B, Maser-Gluth C, Vecsei P, Mullins J, Ganten D, Peters J. The role of the adrenal gland in hypertensive transgenic rat TGR(mREN2)27. Endocrinology 131: 807-814, 1992.
32. Schiffrin EL. Effects of aldosterone on the vasculature. Hypertension 47: 312-1218, 2006.
33. Sharma K, Ramachandrarao S, Qiu G, Usui HK, Zhu Y, Dunn SR, Ouedraogo R, Hough K, McCue P, Chan L, Falkner B, Goldstein BJ. Adiponectin regulates albuminuria and podocyte function in mice. J Clin Invest 118: 1645-1656, 2008.
34. Stas S, Whaley-Connell A, Habibi J, Appesh L, Hayden MR, Karuparthi PR, Qazi M, Morris EM, Cooper SA, Link CD, Stump C, Hay M, Ferrario C, Sowers JR. Mineralocorticoid receptor blockade attenuates chronic overexpression of the renin-angiotensin-aldosterone system stimulation of reduced nicotinamide adenine dinucleotide phosphate oxidase and cardiac remodeling. Endocrinology 148: 3773-3780, 2007.
35. Sun GP, Kohno M, Guo P, Nagai Y, Miyata K, Fan YY, Kimura S, Kiyomoto H, Ohmori K, Li DT, Abe Y, Nishiyama A. Involvements of Rho-kinase and TGF-beta pathways in aldosterone-induced renal injury. J Am Soc Nephrol 17: 2193-2201, 2006. (Pubitemid 44141909)
36. Tejada T, Catanuto P, Ijaz A, Santos JV, Xia X, Sanchez P, Sanabria N, Lenz O, Elliot SJ, Fornoni A. Failure to phosphorylate AKT in podocytes from mice with early diabetic nephropathy promotes cell death. Kidney Int 73: 1385-1393, 2008.
37. Wei Y, Whaley-Connell AT, Rehmer J, Habibi J, Young J, Rehmer N, Patel K, Hayden MR, DeMarco VG, Ferrario CM, Ibdah JI, Sowers JR. Mineralocorticoid receptor blockade attenuates vascular apoptosis and injury. Hypertension 53: 158-165, 2009.
38. Whaley-Connell A, Govindarajan G, Habibi J, Hayden MR, Cooper SA, Wei Y, Ma L, Qazi M, Link D, Karuparthi PR, Stump C, Ferrario C, Sowers JR. Angiotensin II-mediated oxidative stress promotes myocardial tissue remodeling in the transgenic (mRen2)27 Ren2 rat. Am J Physiol Endocrinol Metab 293: E355-E363, 2007.
39. Whaley-Connell A, Habibi J, Nistala R, Cooper SA, Karuparthi PR, Hayden MR, Rehmer N, DeMarco VG, Andresen BT, Wei Y, Ferrario C, Sowers JR. Attenuation of angiotensin II-mediated NADPH oxidase activation and glomerular filtration barrier remodeling with statin treatment. Hypertension 51: 474-480, 2008.
40. Whaley-Connell AT, Chowdhury NA, Hayden MR, Stump CS, Habibi J, Wiedmeyer CE, Gallagher PE, Tallant EA, Cooper SA, Link CD, Ferrario C, Sowers JR. Oxidative stress and glomerular filtration barrier injury: role of the renin-angiotensin system in the Ren2 transgenic rat. Am J Physiol Renal Physiol 291: F1308-F1314, 2006.
41. Wolfrum S, Dendorfer A, Rikitake Y, Stalker TJ, Gong Y, Scalia R, Dominiak P, Liao JK. Inhibition of Rho-kinase leads to rapid phosphatidylinositol 3-kinase/protein kinase Akt and cardiovascular protection. Arterioscler Thromb Vasc Biol 24: 1842-1847, 2004.
42. Xue C, Siragy HM. Local renal aldosterone system and its regulation by salt, diabetes, and angiotensin II type 1 receptor. Hypertension 46: 584-590, 2005. (Pubitemid 41379384)
43. Zhao W, Ahokas RA, Weber KT, Sun Y. ANG II-induced cardiac molecular and cellular events: role of aldosterone. Am J Physiol Heart Circ Physiol 291: H336-H343, 2006.