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Journal of Diabetes Research
Volume 2017, Article ID 4989847, 10 pages
https://doi.org/10.1155/2017/4989847
Research Article

Sulodexide Protects Renal Tubular Epithelial Cells from Oxidative Stress-Induced Injury via Upregulating Klotho Expression at an Early Stage of Diabetic Kidney Disease

1Key Laboratory of Chinese Internal Medicine of Ministry of Education and Beijing and Renal Research Institution of Beijing University of Chinese Medicine, Dongzhimen Hospital Affiliated to Beijing University of Chinese Medicine, Beijing 100700, China
2Institute of Nephrology, Zhanjiang Key Laboratory of Prevention and Management of Chronic Kidney Disease, Guangdong Medical University, Zhanjiang, Guangdong 524001, China
3The First Affiliated Hospital of Zhengzhou University, Zhengzhou, China
4Chonbuk National University, Jeonju, Republic of Korea

Correspondence should be addressed to Yaoxian Wang; nc.ude.mcub@9422a and Wei Jing Liu; moc.liamtoh@7791-gnijiewuil

Received 23 December 2016; Accepted 6 April 2017; Published 27 August 2017

Academic Editor: Hiroshi Okamoto

Copyright © 2017 Yu Ning Liu 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. V. Soetikno, W. Arozal, and M. Louisa, “New insight into the molecular drug target of diabetic nephropathy,” International Journal of Endocrinology, vol. 2014, Article ID 968681, 9 pages, 2014. View at Publisher · View at Google Scholar · View at Scopus
  2. G. Tonolo and S. Cherchi, “Tubulointerstitial disease in diabetic nephropathy,” International Journal of Nephrology and Renovascular, vol. 7, pp. 107–115, 2014. View at Publisher · View at Google Scholar · View at Scopus
  3. H. B. Lee, M. R. Yu, Y. Yang, Z. Jiang, and H. Ha, “Reactive oxygen species-regulated signaling pathways in diabetic nephropathy,” Journals of the American Society of Nephrology, vol. 14, Supplement 3, no. 8, pp. S241–S245, 2003. View at Google Scholar
  4. D. Verzola, M. T. Gandolfo, G. Gaetani et al., “Accelerated senescence in the kidneys of patients with type 2 diabetic nephropathy,” American Journal of Physiology-Renal Physiology, vol. 295, no. 5, pp. F1563–F1573, 2008. View at Publisher · View at Google Scholar · View at Scopus
  5. O. Asai, K. Nakatani, T. Tanaka et al., “Decreased renal α-klotho expression in early diabetic nephropathy in humans and mice and its possible role in urinary calcium excretion,” Kidney International, vol. 81, no. 6, pp. 539–547, 2012. View at Publisher · View at Google Scholar · View at Scopus
  6. M. F. Cheng, L. J. Chen, and J. T. Cheng, “Decrease of klotho in the kidney of streptozotocin-induced diabetic rats,” Journal of Biomedicine & Biotechnology, vol. 2010, Article ID 513853, 7 pages, 2010. View at Publisher · View at Google Scholar · View at Scopus
  7. M. C. Hu, M. Kuro-o, and O. W. Moe, “Klotho and kidney disease,” Journal of Nephrology, vol. 23, Supplement 16, pp. S136–S144, 2010. View at Google Scholar
  8. S. Zununi Vahed, P. Nikasa, and M. Ardalan, “Klotho and renal fibrosis,” Nephro-urology Monthly, vol. 5, no. 5, pp. 946–948, 2013. View at Publisher · View at Google Scholar · View at Scopus
  9. J. S. Huang, C. T. Chuang, M. H. Liu, S. H. Lin, J. Y. Guh, and L. Y. Chuang, “Klotho attenuates high glucose-induced fibronectin and cell hypertrophy via the ERK1/2-p38 kinase signaling pathway in renal interstitial fibroblasts,” Molecular and Cellular Endocrinology, vol. 390, no. 1-2, pp. 45–53, 2014. View at Publisher · View at Google Scholar · View at Scopus
  10. A. V. Gaddi, A. F. Cicero, and G. Gambaro, “Nephroprotective action of glycosaminoglycans: why the pharmacological properties of sulodexide might be reconsidered,” International Journal of Nephrology and Renovascular Disease, vol. 3, pp. 99–105, 2010. View at Google Scholar
  11. A. F. Cicero and S. Ertek, “Preclinical and clinical evidence of nephro- and cardiovascular protective effects of glycosaminoglycans,” Archives of Medical Science, vol. 6, no. 4, pp. 469–477, 2010. View at Publisher · View at Google Scholar · View at Scopus
  12. A. A. House and M. A. Weir, “Sulodexide for diabetic nephropathy: another one bites the dust,” American Journal of Kidney Diseases, vol. 58, no. 5, pp. 692–694, 2011. View at Publisher · View at Google Scholar · View at Scopus
  13. K. Suminska-Jasinska, A. Polubinska, M. Ciszewicz, A. Mikstacki, A. Antoniewicz, and A. Breborowicz, “Sulodexide reduces senescence-related changes in human endothelial cells17,” Medical Science Monitor, no. 4, pp. Cr222–Cr226, 2011. View at Google Scholar
  14. H. Y. Jin, K. A. Lee, S. K. Song et al., “Sulodexide prevents peripheral nerve damage in streptozotocin induced diabetic rats,” European Journal of Pharmacology, vol. 674, no. 2-3, pp. 217–226, 2012. View at Publisher · View at Google Scholar · View at Scopus
  15. W. J. Liu, S. H. Xie, Y. N. Liu et al., “Dipeptidyl peptidase IV inhibitor attenuates kidney injury in streptozotocin-induced diabetic rats,” The Journal of Pharmacology and Experimental Therapeutics, vol. 340, no. 2, pp. 248–255, 2012. View at Publisher · View at Google Scholar · View at Scopus
  16. A. Kuhad and K. Chopra, “Attenuation of diabetic nephropathy by tocotrienol: involvement of NFkB signaling pathway,” Life Sciences, vol. 84, no. 9-10, pp. 296–301, 2009. View at Publisher · View at Google Scholar · View at Scopus
  17. Y. Kato, E. Arakawa, S. Kinoshita et al., “Establishment of the anti-klotho monoclonal antibodies and detection of klotho protein in kidneys,” Biochemical and Biophysical Research Communications, vol. 267, no. 2, pp. 597–602, 2000. View at Publisher · View at Google Scholar · View at Scopus
  18. F. L. Jepsen and P. B. Mortensen, “Interstitial fibrosis of the renal cortex in minimal change lesion and its correlation with renal function. A quantitative study,” Virchows Archiv A, Pathological Anatomy and Histology, vol. 383, no. 3, pp. 265–270, 1979. View at Google Scholar
  19. E. J. Lewis, L. G. Hunsicker, W. R. Clarke et al., “Renoprotective effect of the angiotensin-receptor antagonist irbesartan in patients with nephropathy due to type 2 diabetes,” The New England Journal of Medicine, vol. 345, no. 12, pp. 851–860, 2001. View at Publisher · View at Google Scholar · View at Scopus
  20. 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
  21. A. Solini, A. Carraro, I. Barzon, and G. Crepaldi, “Therapy with glycosaminoglycans lower albumin excretion rate in non-insulin dependent diabetic patients,” Diabetes, Nutrition & Metabolism, vol. 7, no. 7, pp. 304–307, 1994. View at Google Scholar
  22. C. Abaterusso and G. Gambaro, “The role of glycosaminoglycans and sulodexide in the treatment of diabetic nephropathy,” Treatments in Endocrinology, vol. 5, no. 4, pp. 211–222, 2006. View at Google Scholar
  23. G. Gambaro, I. Kinalska, A. Oksa et al., “Oral sulodexide reduces albuminuria in microalbuminuric and macroalbuminuric type 1 and type 2 diabetic patients: the Di.N.A.S. randomized trial,” Journal of the American Society of Nephrology, vol. 13, no. 6, pp. 1615–1625, 2002. View at Google Scholar
  24. E. J. Lewis, J. B. Lewis, T. Greene et al., “Sulodexide for kidney protection in type 2 diabetes patients with microalbuminuria: a randomized controlled trial,” American Journal of Kidney Diseases, vol. 58, no. 5, pp. 729–736, 2011. View at Publisher · View at Google Scholar · View at Scopus
  25. D. K. Packham, R. Wolfe, A. T. Reutens et al., “Sulodexide fails to demonstrate renoprotection in overt type 2 diabetic nephropathy,” Journal of the American Society of Nephrology, vol. 23, no. 1, pp. 123–130, 2012. View at Publisher · View at Google Scholar · View at Scopus
  26. M. Rossini, T. Naito, H. Yang et al., “Sulodexide ameliorates early but not late kidney disease in models of radiation nephropathy and diabetic nephropathy,” Nephrology, Dialysis, Transplantation, vol. 25, no. 6, pp. 1803–1810, 2010. View at Publisher · View at Google Scholar · View at Scopus
  27. Y. Lin, M. Kuro-o, and Z. Sun, “Genetic deficiency of anti-aging gene klotho exacerbates early nephropathy in STZ-induced diabetes in male mice,” Endocrinology, vol. 154, no. 10, pp. 3855–3863, 2013. View at Publisher · View at Google Scholar · View at Scopus
  28. I. M. Kacso, C. I. Bondor, and G. Kacso, “Soluble serum klotho in diabetic nephropathy: relationship to VEGF-A,” Clinical Biochemistry, vol. 45, no. 16-17, pp. 1415–1420, 2012. View at Publisher · View at Google Scholar · View at Scopus
  29. S. Banerjee, Y. Zhao, P. S. Sarkar, K. P. Rosenblatt, R. G. Tilton, and S. Choudhary, “Klotho ameliorates chemically induced endoplasmic reticulum (ER) stress signaling,” Cellular Physiology and Biochemistry, vol. 31, no. 4-5, pp. 659–672, 2013. View at Publisher · View at Google Scholar · View at Scopus
  30. U. Benck, S. Haeckel, J. H. Clorius, and F. J. van der Woude, “Proteinuria-lowering effect of heparin therapy in diabetic nephropathy without affecting the renin-angiotensin-aldosterone system,” Clinical Journal of the American Society of Nephrology, vol. 2, no. 1, pp. 58–67, 2007. View at Publisher · View at Google Scholar · View at Scopus
  31. X. Zhou, K. Chen, H. Lei, and Z. Sun, “Klotho gene deficiency causes salt-sensitive hypertension via monocyte chemotactic protein-1/CC chemokine receptor 2-mediated inflammation,” Journal of the American Society of Nephrology, vol. 26, no. 1, pp. 121–132, 2015. View at Publisher · View at Google Scholar · View at Scopus
  32. C. Zanchi, M. Locatelli, A. Benigni et al., “Renal expression of FGF23 in progressive renal disease of diabetes and the effect of ACE inhibitor,” PLoS One, vol. 8, no. 8, article e70775, 2013. View at Publisher · View at Google Scholar · View at Scopus
  33. J. Karalliedde, G. Maltese, B. Hill, G. Viberti, and L. Gnudi, “Effect of renin-angiotensin system blockade on soluble klotho in patients with type 2 diabetes, systolic hypertension, and albuminuria,” Clinical Journal of the American Society of Nephrology, vol. 8, no. 11, pp. 1899–1905, 2013. View at Publisher · View at Google Scholar · View at Scopus
  34. A. Nakamura, K. Shikata, T. Nakatou et al., “Combination therapy with an angiotensin-converting-enzyme inhibitor and an angiotensin II receptor antagonist ameliorates microinflammation and oxidative stress in patients with diabetic nephropathy,” Journal of Diabetes Investigation, vol. 4, no. 2, pp. 195–201, 2013. View at Publisher · View at Google Scholar · View at Scopus