Table of Contents Author Guidelines Submit a Manuscript
Journal of Diabetes Research
Volume 2015, Article ID 310645, 10 pages
http://dx.doi.org/10.1155/2015/310645
Research Article

Renal Kallikrein Activation and Renoprotection after Dual Blockade of Renin-Angiotensin System in Diet-Induced Diabetic Nephropathy

1Center for Diabetic Systems Medicine, Guangxi Key Laboratory of Excellence, Guilin Medical University, Guilin 541004, China
2Molecular Endocrinology and Toxicology Laboratory, Department of Biology, Hong Kong Baptist University, Kowloon 999077, Hong Kong
3Department of Endocrinology, Guangdong Hospital of Traditional Chinese Medicine, Guangzhou 510120, China

Received 22 October 2014; Revised 19 January 2015; Accepted 9 March 2015

Academic Editor: Konstantinos Kantartzis

Copyright © 2015 Xia Zou 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. P. J. Held, F. K. Port, R. L. Webb et al., “The United States Renal Data System's 1991 annual data report: an introduction,” American Journal of Kidney Diseases, vol. 18, no. 5, supplement 2, pp. 1–16, 1991. View at Google Scholar
  2. W. Yang, J. Lu, J. Weng et al., “Prevalence of diabetes among men and women in China,” The New England Journal of Medicine, vol. 362, no. 12, pp. 1090–1101, 2010. View at Publisher · View at Google Scholar · View at Scopus
  3. Y. Xu, L. Wang, J. He et al., “Prevalence and control of diabetes in Chinese adults,” The Journal of the American Medical Association, vol. 310, no. 9, pp. 948–959, 2013. View at Publisher · View at Google Scholar
  4. L. Zhang, F. Wang, L. Wang et al., “Prevalence of chronic kidney disease in China: a cross-sectional survey,” The Lancet, vol. 379, no. 9818, pp. 815–822, 2012. View at Publisher · View at Google Scholar · View at Scopus
  5. C. Y. Pan, L. T. Ho, S. Soegondo et al., “Prevalence of albuminuria and cardiovascular risk profile in a referred cohort of patients with type 2 diabetes: an Asian perspective,” Diabetes Technology and Therapeutics, vol. 10, no. 5, pp. 397–403, 2008. View at Publisher · View at Google Scholar · View at Scopus
  6. E. Ritz, I. Rychlik, F. Locatelli, and S. Halimi, “End-stage renal failure in type 2 diabetes: a medical catastrophe of worldwide dimensions,” American Journal of Kidney Diseases, vol. 34, no. 5, pp. 795–808, 1999. View at Publisher · View at Google Scholar · View at Scopus
  7. R. E. Schmieder, G. Bakris, and M. R. Weir, “Telmisartan in incipient and overt diabetic renal disease,” Journal of Nephrology, vol. 24, no. 3, pp. 263–273, 2011. View at Publisher · View at Google Scholar · View at Scopus
  8. S. Anderson and R. Komers, “Inhibition of the renin-angiotensin system: is more better?” Kidney International, vol. 75, no. 1, pp. 12–14, 2009. View at Publisher · View at Google Scholar · View at Scopus
  9. J. L. Finch, E. B. Suarez, K. Husain et al., “Effect of combining an ACE inhibitor and a VDR activator on glomerulosclerosis, proteinuria, and renal oxidative stress in uremic rats,” American Journal of Physiology—Renal Physiology, vol. 302, no. 1, pp. 141–149, 2012. View at Publisher · View at Google Scholar · View at Scopus
  10. J. Allard, M. Buléon, E. Cellier et al., “ACE inhibitor reduces growth factor receptor expression and signaling but also albuminuria through B2-kinin glomerular receptor activation in diabetic rats,” The American Journal of Physiology: Renal Physiology, vol. 293, no. 4, pp. F1083–F1092, 2007. View at Publisher · View at Google Scholar · View at Scopus
  11. B. M. Brenner, M. E. Cooper, D. de Zeeuw et al., “Effects of losartan on renal and cardiovascular outcomes in patients with type 2 diabetes and nephropathy,” The New England Journal of Medicine, vol. 345, no. 12, pp. 861–869, 2001. View at Publisher · View at Google Scholar · View at Scopus
  12. H.-H. Parving, H. Lehnert, J. Brochner-Mortensen, R. Gomis, S. Andersen, and P. Arner, “The effect of irbesartan on the development of diabetic nephropathy in patients with type 2 diabetes,” The New England Journal of Medicine, vol. 345, no. 12, pp. 870–878, 2001. View at Publisher · View at Google Scholar · View at Scopus
  13. M. Ruiz-Ortega, O. Lorenzo, M. Rupérez, V. Esteban, S. Mezzano, and J. Egido, “Renin-angiotensin system and renal damage: emerging data on angiotensin II as a proinflammatory mediator,” Contributions to Nephrology, vol. 29, no. 135, pp. 123–137, 2001. View at Publisher · View at Google Scholar · View at Scopus
  14. G. T. McInnes, K. P. J. O'Kane, H. Istad, S. Keinänen-Kiukaanniemi, and H. F. C. M. van Mierlo, “Comparison of the AT1-receptor blocker, candesartan cilexetil, and the ACE inhibitor, lisinopril, in fixed combination with low dose hydrochlorothiazide in hypertensive patients,” Journal of Human Hypertension, vol. 14, no. 4, pp. 263–269, 2000. View at Publisher · View at Google Scholar · View at Scopus
  15. S. M. Nauli, “An ACE inhibitor improves vascular outcomes in a PKD model,” The American Journal of Physiology—Renal Physiology, vol. 301, no. 5, p. F958, 2011. View at Publisher · View at Google Scholar · View at Scopus
  16. L. Tylicki, M. Renke, P. Rutkowski et al., “Dual blockade of the renin-angiotensin-aldosterone system with high-dose angiotensin-converting enzyme inhibitor for nephroprotection: an open, controlled, randomized study,” Scandinavian Journal of Urology and Nephrology, vol. 42, no. 4, pp. 381–388, 2008. View at Publisher · View at Google Scholar · View at Scopus
  17. T. Shiraishi, Y. Tamura, K. Taniguchi et al., “Combination of ACE inhibitor with nicorandil provides further protection in chronic kidney disease,” The American Journal of Physiology—Renal Physiology, vol. 307, no. 12, pp. 1313–1322, 2014. View at Google Scholar
  18. M. Kakoki and O. Smithies, “The kallikrein–kinin system in health and in diseases of the kidney,” Kidney International, vol. 75, no. 10, pp. 1019–1030, 2009. View at Publisher · View at Google Scholar · View at Scopus
  19. G. Spinetti, O. Fortunato, D. Cordella et al., “Tissue Kallikrein is essential for invasive capacity of circulating proangiogenic cells,” Circulation Research, vol. 108, no. 3, pp. 284–293, 2011. View at Publisher · View at Google Scholar · View at Scopus
  20. U. Nöthlings, H. Boeing, G. Maskarinec et al., “Food intake of individuals with and without diabetes across different countries and ethnic groups,” European Journal of Clinical Nutrition, vol. 65, no. 5, pp. 635–641, 2011. View at Publisher · View at Google Scholar · View at Scopus
  21. E. Ritz and S. R. Orth, “Nephropathy in patients with type 2 diabetes mellitus,” The New England Journal of Medicine, vol. 341, no. 15, pp. 1127–1133, 1999. View at Publisher · View at Google Scholar · View at Scopus
  22. H.-L. Zhao, Y. Sui, J. Guan et al., “Fat redistribution and adipocyte transformation in uninephrectomized rats,” Kidney International, vol. 74, no. 4, pp. 467–477, 2008. View at Publisher · View at Google Scholar · View at Scopus
  23. H.-L. Zhao, P. C. Y. Tong, F. M. M. Lai, B. Tomlinson, and J. C. N. Chan, “Association of glomerulopathy with the 5′-end polymorphism of the aldose reductase gene and renal insufficiency in type 2 diabetic patients,” Diabetes, vol. 53, no. 11, pp. 2984–2991, 2004. View at Publisher · View at Google Scholar · View at Scopus
  24. H.-L. Zhao, F. M. M. Lai, P. C. Y. Tong, B. Tomlinson, and J. C. N. Chan, “Clinicopathologic characteristics of nodular glomerulosclerosis in Chinese patients with type 2 diabetes,” American Journal of Kidney Diseases, vol. 44, no. 6, pp. 1039–1049, 2004. View at Publisher · View at Google Scholar · View at Scopus
  25. B. A. Perkins, L. P. Aiello, and A. S. Krolewski, “Diabetes complications and the renin-angiotensin system,” The New England Journal of Medicine, vol. 361, no. 1, pp. 83–85, 2009. View at Publisher · View at Google Scholar · View at Scopus
  26. S. C. W. Tang, J. C. K. Leung, and K. N. Lai, “The kallikrein-kinin system,” Contributions to Nephrology, vol. 170, no. 3, pp. 145–155, 2011. View at Publisher · View at Google Scholar · View at Scopus
  27. A. Manto, P. Cotroneo, G. Porcelli et al., “Urinary kallikrein excretion in type 1 (insulin-dependent) diabetes mellitus,” Diabetologia, vol. 36, no. 5, pp. 423–427, 1993. View at Publisher · View at Google Scholar · View at Scopus
  28. T. Baba, S. Murabayashi, T. Ishizaki, Y. Idol, K. Aoyagi, and K. Takebe, “Renal kallikrein in diabetic patients with hypertension accompanied by nephropathy,” Diabetologia, vol. 29, no. 3, pp. 162–167, 1986. View at Publisher · View at Google Scholar · View at Scopus
  29. S. Bodin, C. Chollet, N. Goncalves-Mendes et al., “Kallikrein protects against microalbuminuria in experimental type I diabetes,” Kidney International, vol. 76, no. 4, pp. 395–403, 2009. View at Publisher · View at Google Scholar · View at Scopus
  30. J. N. Harvey, A. A. Jaffa, H. S. Margolius, and R. K. Mayfield, “Renal kallikrein and hemodynamic abnormalities of diabetic kidney,” Diabetes, vol. 39, no. 3, pp. 299–304, 1990. View at Publisher · View at Google Scholar · View at Scopus
  31. C. Tschöpe, A. Reinecke, U. Seidl et al., “Functional, biochemical, and molecular investigations of renal kallikrein-kinin system in diabetic rats,” The American Journal of Physiology—Heart and Circulatory Physiology, vol. 277, no. 6, pp. H2333–H2340, 1999. View at Google Scholar · View at Scopus
  32. S.-J. Kwak, J. Paeng, D. H. Kim et al., “Local kallikrein-kinin system is involved in podocyte apoptosis under diabetic conditions,” Apoptosis, vol. 16, no. 5, pp. 478–490, 2011. View at Publisher · View at Google Scholar · View at Scopus
  33. C. Zhao, P. Wang, X. Xiao et al., “Gene therapy with human tissue kallikrein reduces hypertension and hyperinsulinemia in fructose-induced hypertensive rats,” Hypertension, vol. 42, no. 5, pp. 1026–1033, 2003. View at Publisher · View at Google Scholar · View at Scopus
  34. G. Yuan, J. Deng, T. Wang et al., “Tissue kallikrein reverses insulin resistance and attenuates nephropathy in diabetic rats by activation of phosphatidylinositol 3-kinase/protein kinase B and adenosine 5′-monophosphate-activated protein kinase signaling pathways,” Endocrinology, vol. 148, no. 5, pp. 2016–2026, 2007. View at Publisher · View at Google Scholar · View at Scopus
  35. A. Riad, J. L. Zhuo, H. P. Schultheiss, and C. Tschöpe, “The role of the renal kallikrein-kinin system in diabetic nephropathy,” Current Opinion in Nephrology and Hypertension, vol. 16, no. 1, pp. 22–26, 2007. View at Publisher · View at Google Scholar · View at Scopus
  36. F. J. P. Blanco, M. J. C. López, C. F. García, R. S. Sánchez, and A. R. Cuartero, “Renal kallikrein in diabetic nephropathy,” Revista Clínica Española, vol. 188, no. 3, pp. 123–126, 1991. View at Google Scholar · View at Scopus
  37. S. B. Lall, S. Kunchaparty, H. H. Siddiqui, and J. S. Bajaj, “Plasma renin activity and urinary kallikrein excretion in response to intravenous furosemide in diabetic patients,” Acta Diabetologica Latina, vol. 27, no. 4, pp. 337–342, 1990. View at Publisher · View at Google Scholar · View at Scopus
  38. T. Ando, K. Shimamoto, N. Ura et al., “The renal Kallikrein-Kinin system in renoparenchymal hypertension,” Advances in Experimental Medicine and Biology, vol. 247, no. 21, pp. 127–132, 1989. View at Google Scholar · View at Scopus
  39. J. Damas, N. Garbacki, and P. J. Lefebvre, “The kallikrein-kinin system, angiotensin converting enzyme inhibitors and insulin sensitivity,” Diabetes/Metabolism Research and Reviews, vol. 20, no. 4, pp. 288–297, 2004. View at Publisher · View at Google Scholar · View at Scopus
  40. O. B. Holland, J. M. Chud, and H. Braunstein, “Urinary kallikrein excretion in essential and mineralocorticoid hypertension,” Journal of Clinical Investigation, vol. 65, no. 2, pp. 347–356, 1980. View at Publisher · View at Google Scholar · View at Scopus
  41. W. H. Yiu, D. W. L. Wong, L. Y. Y. Chan, and et al, “Tissue kallikrein mediates pro-inflammatory pathways and activation of protease-activated receptor-4 in proximal tubular epithelial cells,” PLoS ONE, vol. 9, no. 2, Article ID e88894, 2014. View at Publisher · View at Google Scholar
  42. R. A. S. Santos, A. J. Ferreira, and A. C. Simões E Silva, “Recent advances in the angiotensin-converting enzyme 2-angiotensin(1-7)-Mas axis,” Experimental Physiology, vol. 93, no. 5, pp. 519–527, 2008. View at Publisher · View at Google Scholar · View at Scopus
  43. C. M. Ferrario and J. Varagic, “The ANG-(1-7)/ACE2/mas axis in the regulation of nephron function,” American Journal of Physiology—Renal Physiology, vol. 298, no. 6, pp. F1297–F1305, 2010. View at Publisher · View at Google Scholar · View at Scopus
  44. C. M. Ferrario, J. Jessup, M. C. Chappell et al., “Effect of angiotensin-converting enzyme inhibition and angiotensin II receptor blockers on cardiac angiotensin-converting enzyme 2,” Circulation, vol. 111, no. 20, pp. 2605–2610, 2005. View at Publisher · View at Google Scholar · View at Scopus
  45. C. M. Ferrario, J. Jessup, P. E. Gallagher et al., “Effects of renin-angiotensin system blockade on renal angiotensin-(1-7) forming enzymes and receptors,” Kidney International, vol. 68, no. 5, pp. 2189–2196, 2005. View at Publisher · View at Google Scholar · View at Scopus
  46. X. Cao, F.-Y. Yang, Z. Xin, R.-R. Xie, and J.-K. Yang, “The ACE2/Ang-(1–7)/Mas axis can inhibit hepatic insulin resistance,” Molecular and Cellular Endocrinology, vol. 393, no. 1-2, pp. 30–38, 2014. View at Publisher · View at Google Scholar
  47. Z. Su, J. Zimpelmann, and K. D. Burns, “Angiotensin-(1-7) inhibits angiotensin II-stimulated phosphorylation of MAP kinases in proximal tubular cells,” Kidney International, vol. 69, no. 12, pp. 2212–2218, 2006. View at Publisher · View at Google Scholar · View at Scopus
  48. M. Iwai and M. Horiuchi, “Devil and angel in the renin-angiotensin system: ACE-angiotensin II-AT1 receptor axis vs. ACE2-angiotensin-(1–7)-Mas receptor axis,” Hypertension Research, vol. 32, no. 7, pp. 533–536, 2009. View at Publisher · View at Google Scholar · View at Scopus
  49. L. F. Fried, N. Emanuele, J. H. Zhang et al., “Combined angiotensin inhibition for the treatment of diabetic nephropathy,” The New England Journal of Medicine, vol. 369, no. 20, pp. 1892–1903, 2013. View at Publisher · View at Google Scholar · View at Scopus
  50. J. A. Phipps and E. P. Feener, “The kallikrein-kinin system in diabetic retinopathy: lessons for the kidney,” Kidney International, vol. 73, no. 10, pp. 1114–1119, 2008. View at Publisher · View at Google Scholar · View at Scopus
  51. D. de Zeeuw, “The end of dual therapy with renin-angiotensin-aldosterone system blockade?” The New England Journal of Medicine, vol. 369, no. 20, pp. 1960–1962, 2013. View at Publisher · View at Google Scholar · View at Scopus