Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2014, Article ID 124902, 14 pages
http://dx.doi.org/10.1155/2014/124902
Research Article

Effect of Angiotensin II and Small GTPase Ras Signaling Pathway Inhibition on Early Renal Changes in a Murine Model of Obstructive Nephropathy

1Unidad de Fisiopatología Renal y Cardiovascular, Instituto “Reina Sofía” de Investigación Nefrológica, Fundación Renal Iñigo Alvarez de Toledo, Departamento de Fisiología y Farmacología, Universidad de Salamanca, Edificio Departamental, Campus Miguel de Unamuno, 37007 Salamanca, Spain
2Centro de Investigación del Cáncer (CSIC), Universidad de Salamanca, 37007 Salamanca, Spain
3Diabetes Complications Research Centre, Conway Institute of Biomolecular and Biomedical Research, University College Dublin, Belfield, Dublin 4, Ireland
4Instituto de Investigaciones Biomédicas de Salamanca (IBSAL), 37007 Salamanca, Spain
5Departamento de Anatomía e Histología Humanas, Universidad de Salamanca, 37007 Salamanca, Spain
6Universidad Francisco de Vitoria, 28223 Madrid, Spain

Received 27 February 2014; Revised 12 May 2014; Accepted 6 June 2014; Published 3 July 2014

Academic Editor: Akito Maeshima

Copyright © 2014 Ana B. Rodríguez-Peña et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. A. C. Ucero, A. Benito-Martin, M. C. Izquierdo et al., “Unilateral ureteral obstruction: beyond obstruction,” International Urology and Nephrology, vol. 46, no. 4, pp. 765–776, 2014. View at Publisher · View at Google Scholar
  2. J. Bascands and J. P. Schanstra, “Obstructive nephropathy: insights from genetically engineered animals,” Kidney International, vol. 68, no. 3, pp. 925–937, 2005. View at Publisher · View at Google Scholar · View at Scopus
  3. S. Klahr, S. Ishidoya, and J. Morrissey, “Role of angiotensin II in the tubulointerstitial fibrosis of obstructive nephropathy,” American Journal of Kidney Diseases, vol. 26, no. 1, pp. 141–146, 1995. View at Publisher · View at Google Scholar · View at Scopus
  4. J. L. Pimentel Jr., A. Montero, S. Wang, I. Yosipiv, S. El-Dahr, and M. Martinez-Maldonado, “Sequential changes in renal expression of renin-angiotensin system genes in acute unilateral ureteral obstruction,” Kidney International, vol. 48, no. 4, pp. 1247–1253, 1995. View at Publisher · View at Google Scholar · View at Scopus
  5. J. L. Pimentel Jr., C. L. Sundell, S. Wang, J. B. Kopp, Á. Montero, and M. Martínez-Maldonado, “Role of angiotensin II in the expression and regulation of transforming growth factor-β in obstructive nephropathy,” Kidney International, vol. 48, no. 4, pp. 1233–1246, 1995. View at Publisher · View at Google Scholar · View at Scopus
  6. V. Esteban, O. Lorenzo, M. Rupérez et al., “Angiotensin II, via AT1 and AT2 receptors and NF-κB pathway, regulates the inflammatory response in unilateral ureteral obstruction,” Journal of the American Society of Nephrology, vol. 15, no. 6, pp. 1514–1529, 2004. View at Publisher · View at Google Scholar · View at Scopus
  7. M. El Chaar, J. Chen, S. V. Seshan et al., “Effect of combination therapy with enalapril and the TGF-β antagonist 1D11 in unilateral ureteral obstruction,” The American Journal of Physiology—Renal Physiology, vol. 292, no. 4, pp. F1291–F1301, 2007. View at Publisher · View at Google Scholar · View at Scopus
  8. D. Kellner, J. Chen, I. Richardson et al., “Angiotensin receptor blockade decreases fibrosis and fibroblast expression in a rat model of unilateral ureteral obstruction,” The Journal of Urology, vol. 176, no. 2, pp. 806–812, 2006. View at Publisher · View at Google Scholar · View at Scopus
  9. S. Klahr and J. Morrissey, “Comparative effects of ACE inhibition and angiotensin II receptor blockade in the prevention of renal damage,” Kidney International, Supplements, vol. 62, no. 82, pp. S23–S26, 2002. View at Google Scholar · View at Scopus
  10. C. O. Chen, M. H. Park, M. S. Forbes et al., “Angiotensin-converting enzyme inhibition aggravates renal interstitial injury resulting from partial unilateral ureteral obstruction in the neonatal rat,” American Journal of Physiology: Renal Physiology, vol. 292, no. 3, pp. F946–F955, 2007. View at Publisher · View at Google Scholar · View at Scopus
  11. C. M. Coleman, J. J. Minor, L. E. Burt, B. A. Thornhill, M. S. Forbes, and R. L. Chevalier, “Angiotensin AT1-receptor inhibition exacerbates renal injury resulting from partial unilateral ureteral obstruction in the neonatal rat,” The American Journal of Physiology—Renal Physiology, vol. 293, no. 1, pp. F262–F268, 2007. View at Publisher · View at Google Scholar · View at Scopus
  12. B. J. Stoneking, T. E. Hunley, H. Nishimura et al., “Renal angiotensin converting enzyme promotes renal damage during ureteral obstruction,” The Journal of Urology, vol. 160, no. 3, pp. 1070–1074, 1998. View at Publisher · View at Google Scholar · View at Scopus
  13. M. Aplin, G. L. Christensen, and J. L. Hansen, “Pharmacologic perspectives of functional selectivity by the angiotensin II type 1 receptor,” Trends in Cardiovascular Medicine, vol. 18, no. 8, pp. 305–312, 2008. View at Publisher · View at Google Scholar · View at Scopus
  14. G. Yin, C. Yan, and B. C. Berk, “Angiotensin II signaling pathways mediated by tyrosine kinases,” International Journal of Biochemistry and Cell Biology, vol. 35, no. 6, pp. 780–783, 2003. View at Publisher · View at Google Scholar · View at Scopus
  15. R. L. Chevalier, M. S. Forbes, and B. A. Thornhill, “Ureteral obstruction as a model of renal interstitial fibrosis and obstructive nephropathy,” Kidney International, vol. 75, no. 11, pp. 1145–1152, 2009. View at Publisher · View at Google Scholar · View at Scopus
  16. M. T. Grande and J. M. López-Novoa, “Fibroblast activation and myofibroblast generation in obstructive nephropathy,” Nature Reviews Nephrology, vol. 5, no. 6, pp. 319–328, 2009. View at Publisher · View at Google Scholar · View at Scopus
  17. J. M. Rojas and E. Santos, “Ras genes and human cancer: different implications and different roles,” Current Genomics, vol. 3, no. 4, pp. 295–311, 2002. View at Publisher · View at Google Scholar · View at Scopus
  18. M. M. Muthalif, N. A. Karzoun, L. Gaber et al., “Angiotensin II-induced hypertension contribution of Ras GTPase/mitogen-activated protein kinase and cytochrome P450 metabolites,” Hypertension, vol. 36, no. 4, pp. 604–609, 2000. View at Publisher · View at Google Scholar · View at Scopus
  19. B. Schieffer, W. G. Paxton, Q. Chai, M. B. Marrero, and K. E. Bernstein, “Angiotensin II controls p21ras activity via pp60c-src,” Journal of Biological Chemistry, vol. 271, no. 17, pp. 10329–10333, 1996. View at Publisher · View at Google Scholar · View at Scopus
  20. M. T. Grande and J. M. López-Novoa, “Therapeutical relevance of MAP-kinase inhibitors in renal diseases: current knowledge and future clinical perspectives,” Current Medicinal Chemistry, vol. 15, no. 20, pp. 2054–2070, 2008. View at Publisher · View at Google Scholar · View at Scopus
  21. C. Martínez-Salgado, A. B. Rodríguez-Peña, and J. M. López-Novoa, “Involvement of small Ras GTPases and their effectors in chronic renal disease,” Cellular and Molecular Life Sciences, vol. 65, no. 3, pp. 477–492, 2008. View at Publisher · View at Google Scholar · View at Scopus
  22. M. T. Grande, M. Arévalo, A. Núñez, J. B. Cannata-Andía, E. Santos, and J. M. López-Novoa, “Targeted genomic disruption of H-ras and N-ras has no effect on early renal changes after unilateral ureteral ligation,” World Journal of Urology, vol. 27, no. 6, pp. 787–797, 2009. View at Publisher · View at Google Scholar · View at Scopus
  23. A. B. Rodríguez-Peña, M. T. Grande, N. Eleno et al., “Activation of Erk1/2 and Akt following unilateral ureteral obstruction,” Kidney International, vol. 74, no. 2, pp. 196–209, 2008. View at Publisher · View at Google Scholar · View at Scopus
  24. I. Fuentes-Calvo, A. M. Blázquez-Medela, N. Eleno, E. Santos, J. M. López-Novoa, and C. Martínez-Salgado, “H-Ras isoform modulates extracellular matrix synthesis, proliferation, and migration in fibroblasts,” American Journal of Physiology: Cell Physiology, vol. 302, no. 4, pp. C686–C697, 2012. View at Publisher · View at Google Scholar · View at Scopus
  25. I. Fuentes-Calvo, P. Crespo, E. Santos, J. M. López-Novoa, and C. Martínez-Salgado, “The small GTPase N-Ras regulates extracellular matrix synthesis, proliferation and migration in fibroblasts,” Biochimica et Biophysica Acta, vol. 1833, no. 12, pp. 2734–2744, 2013. View at Publisher · View at Google Scholar · View at Scopus
  26. C. Martínez-Salgado, I. Fuentes-Calvo, B. García-Cenador, E. Santos, and J. M. López-Novoa, “Involvement of H-and N-Ras isoforms in transforming growth factor-β1-induced proliferation and in collagen and fibronectin synthesis,” Experimental Cell Research, vol. 312, no. 11, pp. 2093–2106, 2006. View at Publisher · View at Google Scholar · View at Scopus
  27. M. T. Grande, I. Fuentes-Calvo, M. Arevalo et al., “Deletion of H-Ras decreases renal fibrosis and myofibroblast activation following ureteral obstruction in mice,” Kidney International, vol. 77, no. 6, pp. 509–518, 2010. View at Publisher · View at Google Scholar · View at Scopus
  28. C. C. Sharpe, M. E. C. Dockrell, R. Scott et al., “Evidence of a role for Ki-RAS in the stimulated proliferation of renal fibroblasts,” Journal of the American Society of Nephrology, vol. 10, no. 6, pp. 1186–1192, 1999. View at Google Scholar · View at Scopus
  29. J. Wang, L. J. Newbury, A. S. Knisely, B. Monia, B. M. Hendry, and C. C. Sharpe, “Antisense knockdown of Kras inhibits fibrosis in a rat model of unilateral ureteric obstruction,” The American Journal of Pathology, vol. 180, no. 1, pp. 82–90, 2012. View at Publisher · View at Google Scholar · View at Scopus
  30. J. F. Hancock and R. G. Parton, “Ras plasma membrane signalling platforms,” The Biochemical Journal, vol. 389, no. 1, pp. 1–11, 2005. View at Publisher · View at Google Scholar · View at Scopus
  31. R. Masterson, K. Kelynack, T. Hewitson, and G. Becker, “Effect of inhibition of farnesylation and geranylgeranylation on renal fibrogenesis in vitro,” Nephron—Experimental Nephrology, vol. 102, no. 1, pp. e19–e29, 2006. View at Publisher · View at Google Scholar · View at Scopus
  32. M. Buemi, M. Senatore, F. Corica et al., “Statins and progressive renal disease,” Medicinal Research Reviews, vol. 22, no. 1, pp. 76–84, 2002. View at Publisher · View at Google Scholar · View at Scopus
  33. M. Jakobisiak and J. Golab, “Potential antitumor effects of statins (Review),” International Journal of Oncology, vol. 23, no. 4, pp. 1055–1069, 2003. View at Google Scholar · View at Scopus
  34. M. Crul, G. J. De Klerk, J. H. Beijnen, and J. H. M. S. Schellens, “Ras biochemistry and farnesyl transferase inhibitors: a literature survey,” Anti-Cancer Drugs, vol. 12, no. 3, pp. 163–184, 2001. View at Publisher · View at Google Scholar · View at Scopus
  35. A. Ruocco, M. Santillo, M. Cicale et al., “Farnesyl transferase inhibitors induce neuroprotection by inhibiting Ha-Ras signalling pathway,” The European Journal of Neuroscience, vol. 26, no. 11, pp. 3261–3266, 2007. View at Publisher · View at Google Scholar · View at Scopus
  36. Y. Qian, S. M. Sebti, and A. D. Hamilton, “Farnesyltransferase as a target for anticancer drug design,” Biopolymers, vol. 43, no. 1, pp. 25–41, 1997. View at Publisher · View at Google Scholar · View at Scopus
  37. A. B. Rodríguez-Peña, E. Santos, M. Arévalo, and J. M. López-Novoa, “Activation of small GTPase Ras and renal fibrosis,” Journal of Nephrology, vol. 18, no. 3, pp. 341–349, 2005. View at Google Scholar · View at Scopus
  38. M. Gharaee-Kermani, R. Wiggins, F. Wolber, M. Goyal, and S. H. Phan, “Fibronectin is the major fibroblast chemoattractant in rabbit anti-glomerular basement membrane disease,” The American Journal of Pathology, vol. 148, no. 3, pp. 961–967, 1996. View at Google Scholar · View at Scopus
  39. G. Serini, M. Bochaton-Piallat, P. Ropraz et al., “The fibronectin domain ED-A is crucial for myofibroblastic phenotype induction by transforming growth factor-β1,” The Journal of Cell Biology, vol. 142, no. 3, pp. 873–881, 1998. View at Publisher · View at Google Scholar · View at Scopus
  40. T. Masaki, R. Foti, P. A. Hill, Y. Ikezumi, R. C. Atkins, and D. J. Nikolic-Paterson, “Activation of the ERK pathway precedes tubular proliferation in the obstructed rat kidney,” Kidney International, vol. 63, no. 4, pp. 1256–1264, 2003. View at Publisher · View at Google Scholar · View at Scopus
  41. B. Pat, T. Yang, C. Kong, D. Watters, D. W. Johnson, and G. Gobe, “Activation of ERK in renal fibrosis after unilateral ureteral obstruction: modulation by antioxidants,” Kidney International, vol. 67, no. 3, pp. 931–943, 2005. View at Publisher · View at Google Scholar · View at Scopus
  42. T. Moriyama, N. Kawada, K. Nagatoya et al., “Fluvastatin suppresses oxidative stress and fibrosis in the interstitium of mouse kidneys with unilateral ureteral obstruction,” Kidney International, vol. 59, no. 6, pp. 2095–2103, 2001. View at Publisher · View at Google Scholar · View at Scopus
  43. Y. Mizuguchi, A. Miyajima, T. Kosaka, T. Asano, and M. Hayakawa, “Atorvastatin ameliorates renal tissue damage in unilateral ureteral obstruction,” The Journal of Urology, vol. 172, no. 6 I, pp. 2456–2459, 2004. View at Publisher · View at Google Scholar · View at Scopus
  44. J. M. Vieira Jr., E. Mantovani, L. Tavares Rodrigues et al., “Simvastatin attenuates renal inflammation, tubular transdifferentiation and interstitial fibrosis in rats with unilateral ureteral obstruction,” Nephrology Dialysis Transplantation—European Renal Association, vol. 20, no. 8, pp. 1582–1591, 2005. View at Publisher · View at Google Scholar · View at Scopus
  45. C. Kamdar, S. Y. Chou, U. M. M. Mooppan, H. Kim, and F. A. Gulmi, “Atorvastatin protects renal function in the rat with acute unilateral ureteral obstruction,” Urology, vol. 75, no. 4, pp. 853–857, 2010. View at Publisher · View at Google Scholar · View at Scopus
  46. L. J. Mazzei, I. M. García, L. Altamirano, N. G. Docherty, and W. Manucha, “Rosuvastatin preserves renal structure following unilateral ureteric obstruction in the neonatal rat,” American Journal of Nephrology, vol. 35, no. 2, pp. 103–113, 2012. View at Publisher · View at Google Scholar · View at Scopus
  47. A. F. Safina, A. E. Varga, A. Bianchi et al., “Ras alters epithelial-mesenchymal transition in response to TGFβ by reducing actin fibers and cell-matrix adhesion,” Cell Cycle, vol. 8, no. 2, pp. 284–298, 2009. View at Publisher · View at Google Scholar · View at Scopus
  48. M. Jordà, A. Vinyals, A. Marazuela et al., “Id-1 is induced in MDCK epithelial cells by activated Erk/MAPK pathway in response to expression of the Snail and E47 transcription factors,” Experimental Cell Research, vol. 313, no. 11, pp. 2389–2403, 2007. View at Publisher · View at Google Scholar · View at Scopus
  49. X. Wei, X. Wang, Y. Xia et al., “Kindlin-2 regulates renal tubular cell plasticity by activation of Ras and its downstream signaling,” American Journal of Physiology—Renal Physiology, vol. 306, no. 2, pp. F271–F278, 2014. View at Google Scholar
  50. H. Peinado, M. Quintanilla, and A. Cano, “Transforming growth factor β-1 induces Snail transcription factor in epithelial cell lines. Mechanisms for epithelial mesenchymal transitions,” The Journal of Biological Chemistry, vol. 278, no. 23, pp. 21113–21123, 2003. View at Publisher · View at Google Scholar · View at Scopus
  51. M. Sabbatini, M. Santillo, A. Pisani et al., “Inhibition of Ras/ERK1/2 signaling protects against postischemic renal injury,” The American Journal of Physiology: Renal Physiology, vol. 290, no. 6, pp. F1408–F1415, 2006. View at Publisher · View at Google Scholar · View at Scopus