DOI QR코드

DOI QR Code

Aldosterone Up-regulates Production of Plasminogen Activator Inhibitor-1 by Renal Mesangial Cells

  • Yuan, Jun (Department of nephrology, Renmin Hospital of Wuhan University) ;
  • Jia, Ruhan (Department of nephrology, Renmin Hospital of Wuhan University) ;
  • Bao, Yan (Department of nephrology, Renmin Hospital of Wuhan University)
  • 발행 : 2007.03.31

초록

In vivo studies have demonstrated that aldosterone is an independent contributor to glomerulosclerosis. In the present study, we have investigated whether aldosterone itself mediated glomerulosclerosis, as angiotensin II (Ang II) did, by inducing cultured renal mesangial cells to produce plasminogen activator inhibitor-1 (PAI-1), and whether these effects were mediated by aldosterone-induced increase in transforming growth factor $\beta_1$ (TGF-$\beta_1$) expression and cellular reactive oxygen species (ROS) activity. Quiescent rat mesangial cells were treated by aldosterone alone or by combination of aldosterone and spironolactone, Ang II, neutralizing antibody to TGF-$\beta_1$ or antioxidant Nacetylcysteme (NAC). This study indicate that aldosterone can increase PAI-1 mRNA and protein expression by cultured mesangial cells alone, which is independent of aldosterone-induced increases in TGF-$\beta_1$ expression and cellular ROS. The effects on PAI-1, TGF-$\beta_1$ and ROS generation were markedly attenuated by spironolactone, a mineralocorticoid receptor antagonist, which demonstrate that mineralocorticoid receptor (MR) may play a role in mediating these effects of aldosterone.

키워드

참고문헌

  1. Aldigier, J. C., Kanjanbuch, T., Ma, L. J., Brown, N. J. and Fogo A. B. (2005) Regression of existing glomerulosclerosis by inhibition of aldosterone. J. Am. Soc. Nephrol. 16, 3306-3314. https://doi.org/10.1681/ASN.2004090804
  2. Baricos, W. H., Cortez, S. L., Deboisblanc, M. and Xin, S. (1999) Transforming growth factor-beta is a potent inhibitor of extracellular matrix degradation by cultured human mesangial cells. J. Am. Soc. Nephrol. 10, 790-795.
  3. Booth, R. E., Johnson, J. P. and Stockand, J. D. (2002) Aldosterone. Adv. Physiol. Educ. 26, 8-20. https://doi.org/10.1152/advan.00051.2001
  4. Brown, N. J., Agirbasli, M. A., Williams, G. H., Litchfield, W. R. and Vaughan, D. E. (1998) Effect of activation and inhibition of the renin-angiotensin system on plasma PAI-1. Hypertension 32, 965-971. https://doi.org/10.1161/01.HYP.32.6.965
  5. Brown, N. J., Kim, K. S., Chen, Y. Q., Blevins, L. S., Nadeau, J. H., Meranze, S. G. and Vaughan, D. E. (2000) Synergistic effect of adrenal steroids and angiotensin II on plasminogen activator inhibitor-1 production. J. Clin. Endocrinol. Metab. 85, 336-344. https://doi.org/10.1210/jc.85.1.336
  6. Brown, N. J., Nakamura, S., Ma, L., Nakamura, I., Donnert, E., Freeman, M., Vaughan, D. E. and Fogo, A. B. (2000) Aldosterone modulates plasminogen activator inhibitor-1 and glomerulosclerosis in vivo. Kidney Int. 58, 1219-1227. https://doi.org/10.1046/j.1523-1755.2000.00277.x
  7. Cheng, J. J., Chao, Y. J., Wung, B. S. and Wang, D. L. (1996) Cyclic strain-induced plasminogen activator inhibitor-1 (PAI-1) release from endothelial cells involves reactive oxygen species. Biochem. Biophys. Res. Commun. 225, 100-105. https://doi.org/10.1006/bbrc.1996.1136
  8. Dennler, S., Itoh, S., Vivien, D., ten Dijke, P., Huet, S. and Gauthier, J. M. (1998) Direct binding of Smad3 and Smad4 to critical TGF beta-inducible elements in the promoter of human plasminogen activator inhibitor-type 1 gene. EMBO J. 17, 3091-3100. https://doi.org/10.1093/emboj/17.11.3091
  9. Du, X. L., Edelstein, D., Rossetti, L., Fantus, I. G., Goldberg, H., Ziyadeh, F., Wu, J. and Brownlee, M. (2000) Hyperglycemiainduced mitochondrial superoxide overproduction activates the hexosamine pathway and induces plasminogen activator inhibitor-1 expression by increasing Sp1 glycosylation. Proc. Natl. Acad. Sci. USA 97, 12222-12226. https://doi.org/10.1073/pnas.97.22.12222
  10. Eddy, A. A. (2000) Molecular basis of renal fibrosis. Pediatr Nephrol. 15, 290-301. https://doi.org/10.1007/s004670000461
  11. Eddy, A. A. (2002) Plasminogen activator inhibitor-1 and the kidney. Am. J. Physiol. Renal. Physiol. 283, 209-220. https://doi.org/10.1152/ajprenal.00032.2002
  12. Feria, I., Pichardo, I., Juarez, P., Ramirez, V., Gonzalez, M. A., Uribe, N., Garcia-Torres, R., Lopez-Casillas, F., Gamba, G. and Bobadilla, N. A. (2003) Therapeutic benefit of spironolactone in experimental chronic cyclosporine A nephrotoxicity. Kidney Int. 63, 43-52.
  13. Fiebeler, A. and Luft, F. C. (2005) The mineralocorticoid receptor and oxidative stress. Heart Fail Rev. 10, 47-52. https://doi.org/10.1007/s10741-005-2348-y
  14. Fogari, R. and Zoppi, A. (2005) Is the effect of antihypertensive drugs on platelet aggregability and fibrinolysis clinically relevant?. Am. J. Cardiovasc. Drugs 5, 211-223. https://doi.org/10.2165/00129784-200505040-00001
  15. Fujisawa, G., Okada, K., Muto, S., Fujita, N., Itabashi, N., Kusano, E. and Ishibashi, S. (2004) Spironolactone prevents early renal injury in streptozotocin-induced diabetic rats. Kidney Int. 66, 1493-1502. https://doi.org/10.1111/j.1523-1755.2004.00913.x
  16. Ha, H. and Lee, H. B. (2005) Reactive oxygen species amplify glucose signalling in renal cells cultured under high glucose and in diabetic kidney. Nephrology (Carlton) 10, 7-10. https://doi.org/10.1111/j.1440-1797.2005.00365.x
  17. Hollenberg, N. K. (2004) Aldosterone in the development and progression of renal injury. Kidney Int. 66, 1-9. https://doi.org/10.1111/j.1523-1755.2004.00701.x
  18. Jiang, Z., Seo, J. Y., Ha, H., Lee, E. A., Kim, Y. S., Han, D. C., Uh, S. T., Park, C. S. and Lee, H. B. (2003) Reactive oxygen species mediate TGF-beta1-induced plasminogen activator inhibitor-1 upregulation in mesangial cells. Biochem. Biophys. Res. Commun. 309, 961-966. https://doi.org/10.1016/j.bbrc.2003.08.102
  19. Juknevicius, I., Segal, Y., Kren, S., Lee, R. and Hostetter, T. H. (2004) Effect of aldosterone on renal transforming growth factor-beta. Am. J. Physiol. Renal. Physiol. 286, 1059-1062. https://doi.org/10.1152/ajprenal.00202.2003
  20. Kagami, S., Kuhara, T., Okada, K., Kuroda, Y., Border, W. A. and Noble, N. A. (1997) Dual effects of angiotensin II on the plasminogen/plasmin system in rat mesangial cells. Kidney Int. 51, 664-671. https://doi.org/10.1038/ki.1997.96
  21. Krag, S., Danielsen, C. C., Carmeliet, P., Nyengaard, J. and Wogensen, L. (2005) Plasminogen activator inhibitor-1 gene deficiency attenuates TGF-beta1-induced kidney disease. Kidney Int. 68, 2651-2666. https://doi.org/10.1111/j.1523-1755.2005.00737.x
  22. Krug, A. W., Schuster, C., Gassner, B., Freudinger, R., Mildenberger, S., Troppmair, J. and Gekle, M. (2002) Human epidermal growth factor receptor-1 expression renders Chinese hamster ovary cells sensitive to alternative aldosterone signaling. J. Biol. Chem. 277, 45892-45897. https://doi.org/10.1074/jbc.M208851200
  23. Kuriyama, S., Otsuka, Y., Iida, R., Matsumoto, K., Tokudome, G. and Hosoya, T. (2005) Morning blood pressure predicts hypertensive organ damage in patients with renal diseases: effect of intensive antihypertensive therapy in patients with diabetic nephropathy. Intern. Med. 44, 1239-1246. https://doi.org/10.2169/internalmedicine.44.1239
  24. Lai, L. Y., Gu, Y., Chen, J., Yu, S. Q., Ma, J., Yang, H. C. and Lin, S. Y. (2003) Production of aldosterone by rat mesangial cell and the accumulation of extracellular matrix induced by aldosterone. Zhonghua Yi Xue Za Zhi. 83, 1900-1905.
  25. Lee, E. A., Seo, J. Y., Jiang, Z., Yu, M. R., Kwon, M. K., Ha, H. and Lee, H. B. (2005) Reactive oxygen species mediate high glucose-induced plasminogen activator inhibitor-1 up-regulation in mesangial cells and in diabetic kidney. Kidney Int. 67, 1762- 1771. https://doi.org/10.1111/j.1523-1755.2005.00274.x
  26. Lee, H. B., Yu, M. R., Yang, Y., Jiang, Z. and Ha, H. (2003) Reactive oxygen species-regulated signaling pathways in diabetic nephropathy. J. Am. Soc. Nephrol. 14, 241-245. https://doi.org/10.1097/01.ASN.0000077410.66390.0F
  27. Ma, L. J., Yang, H., Gaspert, A., Carlesso, G., Barty, M. M., Davidson, J. M., Sheppard, D. and Fogo, A. B. (2003) Transforming growth factor-beta-dependent and -independent pathways of induction of tubulointerstitial fibrosis in beta6(-/-) mice. Am. J. Pathol. 163, 1261-1273. https://doi.org/10.1016/S0002-9440(10)63486-4
  28. Mignatti, P. (1995) Extracellular matrix remodeling by metalloproteinases and plasminogen activators. Kidney Int. Suppl. 49, 12-14.
  29. Miric, G., Dallemagne, C., Endre, Z., Margolin, S., Taylor, S. M. and Brown, L. (2001) Reversal of cardiac and renal fibrosis by pirfenidone and spironolactone in streptozotocin-diabetic rats. Br. J. Pharmacol. 133, 687-694. https://doi.org/10.1038/sj.bjp.0704131
  30. Miyata, K., Rahman, M., Shokoji, T., Nagai, Y., Zhang, G. X., Sun, G. P., Kimura, S., Yukimura, T., Kiyomoto, H., Kohno, M., Abe, Y. and Nishiyama, A. (2005) Aldosterone stimulates reactive oxygen species production through activation of NADPH oxidase in rat mesangial cells. J. Am. Soc. Nephrol. 16, 2906-2912. https://doi.org/10.1681/ASN.2005040390
  31. Motojima, M., Ando, T. and Yoshioka, T. (2000) Sp1-like activity mediates angiotensin-II-induced plasminogen-activator inhibitor type-1 (PAI-1) gene expression in mesangial cells. Biochem. J. 349, 435-441. https://doi.org/10.1042/0264-6021:3490435
  32. Nishiyama, A. and Abe, Y. (2004) Aldosterone and renal injury. Nippon Yakurigaku Zasshi. 124, 101-109. https://doi.org/10.1254/fpj.124.101
  33. Nishiyama, A. and Abe, Y. (2006) Molecular mechanisms and therapeutic strategies of chronic renal injury: renoprotective effects of aldosterone blockade. J. Pharmacol. Sci. 100, 9-16. https://doi.org/10.1254/jphs.FMJ05003X3
  34. Nishiyama, A., Yao, L., Fan, Y., Kyaw, M., Kataoka, N., Hashimoto, K., Nagai, Y., Nakamura, E., Yoshizumi, M., Shokoji, T., Kimura, S., Kiyomoto, H., Tsujioka, K., Kohno, M., Tamaki, T., Kajiya, F. and Abe, Y. (2005) Involvement of aldosterone and mineralocorticoid receptors in rat mesangial cell proliferation and deformability. Hypertension 45, 710-716. https://doi.org/10.1161/01.HYP.0000154681.38944.9a
  35. Peters, H., Border, W. A. and Noble, N. A. (1999) Targeting TGFbeta overexpression: maximizing the antifibrotic actions of angiotensin II blockade in anti-Thy1 glomerulonephritis. Nephrol. Dial. Transplant. 14, 22-23.
  36. Rerolle, J. P., Hertig, A., Nguyen, G., Sraer, J. D. and Rondeau, E. P. (2000) Plasminogen activator inhibitor type 1 is a potential target in renal fibrogenesis. Kidney Int. 58, 1841-1850. https://doi.org/10.1111/j.1523-1755.2000.00355.x
  37. Rodrigo, R. and Bosco, C. (2006) Oxidative stress and protective effects of polyphenols: Comparative studies in human and rodent kidney. A review. Comp. Biochem. Physiol. C. Toxicol. Pharmacol. 142, 317-327. https://doi.org/10.1016/j.cbpc.2005.11.002
  38. Sato, A., Hayashi, K., Naruse, M. and Saruta, T. (2003) Effectiveness of aldosterone blockade in patients with diabetic nephropathy. Hypertension 41, 64-68. https://doi.org/10.1161/01.HYP.0000044937.95080.E9
  39. Schnaper, H. W. (1995) Balance between matrix synthesis and degradation: a determinant of glomerulosclerosis. Pediatr. Nephrol. 9, 104-111. https://doi.org/10.1007/BF00858986
  40. Stetler-Stevenson, W. G. (1996) Dynamics of matrix turnover during pathologic remodeling of the extracellular matrix. Am. J. Pathol. 148, 1345-1350.
  41. Tomooka, S., Border, W. A., Marshall, B. C. and Noble, N. A. (1992) Glomerular matrix accumulation is linked to inhibition of the plasmin protease system. Kidney Int. 42, 1462-1469. https://doi.org/10.1038/ki.1992.442
  42. Vassalli, J. D., Sappino, A. P. and Belin, D. (1991) The plasminogen activator/plasmin system. J. Clin. Invest. 88, 1067-1072. https://doi.org/10.1172/JCI115405
  43. Vaughan, D. E. (2001) Angiotensin, fibrinolysis, and vascular homeostasis. Am. J. Cardiol. 87, 18-24. https://doi.org/10.1016/S0002-9149(01)01509-0
  44. Wilson, H. M., Reid, F. J., Brown, P. A., Power, D. A., Haites, N. E. and Booth, N. A. (1993) Effect of transforming growth factor-beta 1 on plasminogen activators and plasminogen activator inhibitor-1 in renal glomerular cells. Exp. Nephrol. 1, 343-350.
  45. Zhao, W., Spitz, D. R., Oberley, L. W. and Robbins, M. E. (2001) Redox modulation of the pro-fibrogenic mediator plasminogen activator inhibitor-1 following ionizing radiation. Cancer Res. 61, 5537-5543.
  46. Ziyadeh, F. N., Han, D. C., Cohen, J. A., Guo, J. and Cohen, M. P. (1998) Glycated albumin stimulates fibronectin gene expression in glomerular mesangial cells: involvement of the transforming growth factor-beta system. Kidney Int. 53, 631- 638. https://doi.org/10.1046/j.1523-1755.1998.00815.x

피인용 문헌

  1. Blockade of T-type voltage-dependent Ca2+ channels by benidipine, a dihydropyridine calcium channel blocker, inhibits aldosterone production in human adrenocortical cell line NCI-H295R vol.584, pp.2-3, 2008, https://doi.org/10.1016/j.ejphar.2008.02.001
  2. Aldosterone: effects on the kidney and cardiovascular system vol.6, pp.5, 2010, https://doi.org/10.1038/nrneph.2010.30
  3. Aldosterone and inflammation vol.17, pp.3, 2010, https://doi.org/10.1097/MED.0b013e3283391989
  4. Aldosterone and diabetic kidney disease vol.9, pp.6, 2009, https://doi.org/10.1007/s11892-009-0074-x
  5. Contribution of aldosterone to cardiovascular and renal inflammation and fibrosis vol.9, pp.8, 2013, https://doi.org/10.1038/nrneph.2013.110
  6. Role of transforming growth factor-β superfamily signaling pathways in human disease vol.1782, pp.4, 2008, https://doi.org/10.1016/j.bbadis.2008.01.006
  7. Effect of eplerenone, enalapril and their combination treatment on diabetic nephropathy in type II diabetic rats vol.24, pp.1, 2008, https://doi.org/10.1093/ndt/gfn448