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BioMed Research International
Volume 2014, Article ID 782625, 10 pages
http://dx.doi.org/10.1155/2014/782625
Research Article

High Glucose Induces Sumoylation of Smad4 via SUMO2/3 in Mesangial Cells

1Department of Endocrinology, Affiliated Hospital of Luzhou Medical College, Luzhou, Sichuan 646000, China
2Department of Endocrinology, The Central Hospital of Bazhong City, Sichuan 636000, China

Received 27 February 2014; Accepted 1 May 2014; Published 27 May 2014

Academic Editor: Keizo Kanasaki

Copyright © 2014 Xueqin Zhou 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. F. P. Schena and L. Gesualdo, “Pathogenetic mechanisms of diabetic nephropathy,” Journal of the American Society of Nephrology, vol. 16, supplement 3, pp. S30–S33, 2005. View at Publisher · View at Google Scholar · View at Scopus
  2. B. Najafian, C. E. Alpers, and A. B. Fogo, “Pathology of human diabetic nephropathy,” Contributions to Nephrology, vol. 170, pp. 36–47, 2011. View at Publisher · View at Google Scholar · View at Scopus
  3. F. C. Brosius III, “New insights into the mechanisms of fibrosis and sclerosis in diabetic nephropathy,” Reviews in Endocrine and Metabolic Disorders, vol. 9, no. 4, pp. 245–254, 2008. View at Publisher · View at Google Scholar · View at Scopus
  4. D. Pohlers, J. Brenmoehl, I. Löffler et al., “TGF-β and fibrosis in different organs-molecular pathway imprints,” Biochimica et Biophysica Acta, vol. 1792, no. 8, pp. 746–756, 2009. View at Publisher · View at Google Scholar · View at Scopus
  5. H. Y. Lan, “Transforming growth factor-β/Smad signalling in diabetic nephropathy,” Clinical and Experimental Pharmacology and Physiology, vol. 39, no. 8, pp. 731–738, 2012. View at Publisher · View at Google Scholar · View at Scopus
  6. S. Yamagishi, Y. Inagaki, T. Okamoto, S. Amano, K. Koga, and M. Takeuchi, “Advanced glycation end products inhibit de novo protein synthesis and induce TGF-β overexpression in proximal tubular cells,” Kidney International, vol. 63, no. 2, pp. 464–473, 2003. View at Publisher · View at Google Scholar · View at Scopus
  7. Y. Inoue and T. Imamura, “Regulation of TGF-β family signaling by E3 ubiquitin ligases,” Cancer Science, vol. 99, no. 11, pp. 2107–2112, 2008. View at Publisher · View at Google Scholar · View at Scopus
  8. M. L. Burch, W. Zheng, and P. J. Little, “Smad linker region phosphorylation in the regulation of extracellular matrix synthesis,” Cellular and Molecular Life Sciences, vol. 68, no. 1, pp. 97–107, 2011. View at Publisher · View at Google Scholar · View at Scopus
  9. C. Gao, G. Chen, L. Liu et al., “Impact of high glucose and proteasome inhibitor MG132 on histone H2A and H2B ubiquitination in rat glomerular mesangial cells,” Journal of Diabetes Research, vol. 2013, Article ID 589474, 10 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  10. J. S. Kang, E. F. Saunier, R. J. Akhurst, and R. Derynck, “The type I TGF-β receptor is covalently modified and regulated by sumoylation,” Nature Cell Biology, vol. 10, no. 6, pp. 654–664, 2008. View at Publisher · View at Google Scholar · View at Scopus
  11. P. S. Lee, C. Chang, D. Liu, and R. Derynck, “Sumoylation of Smad4, the common Smad mediator of transforming growth factor-β family signaling,” Journal of Biological Chemistry, vol. 278, no. 30, pp. 27853–27863, 2003. View at Publisher · View at Google Scholar · View at Scopus
  12. Z. Hannoun, S. Greenhough, E. Jaffray, R. T. Hay, and D. C. Hay, “Post-translational modification by SUMO,” Toxicology, vol. 278, no. 3, pp. 288–293, 2010. View at Publisher · View at Google Scholar · View at Scopus
  13. K. I. Kim and S. H. Baek, “Chapter 7 small ubiquitin-like modifiers in cellular malignancy and metastasis,” International Review of Cell and Molecular Biology C, vol. 273, pp. 265–311, 2009. View at Publisher · View at Google Scholar · View at Scopus
  14. K. A. Wilkinson and J. M. Henley, “Mechanisms, regulation and consequences of protein SUMOylation,” Biochemical Journal, vol. 428, no. 2, pp. 133–145, 2010. View at Publisher · View at Google Scholar · View at Scopus
  15. Y. E. Wang, O. Pernet, and B. Lee, “Regulation of the nucleocytoplasmic trafficking of viral and cellular proteins by ubiquitin and small ubiquitin-related modifiers,” Biology of the Cell, vol. 104, no. 3, pp. 121–138, 2012. View at Publisher · View at Google Scholar · View at Scopus
  16. J. Wang, “Cardiac function and disease: emerging role of small ubiquitin-related modifier,” Wiley Interdisciplinary Reviews: Systems Biology and Medicine, vol. 3, no. 4, pp. 446–457, 2011. View at Publisher · View at Google Scholar · View at Scopus
  17. K. Miyazono, Y. Kamiya, and K. Miyazawa, “SUMO amplifies TGF-β signalling,” Nature Cell Biology, vol. 10, no. 6, pp. 635–637, 2008. View at Publisher · View at Google Scholar · View at Scopus
  18. P. Teekakirikul, S. Eminaga, O. Toka et al., “Cardiac fibrosis in mice with hypertrophic cardiomyopathy is mediated by non-myocyte proliferation and requires Tgf-β,” Journal of Clinical Investigation, vol. 120, no. 10, pp. 3520–3529, 2010. View at Publisher · View at Google Scholar · View at Scopus
  19. T. Nakamura, R. Sakata, T. Ueno, M. Sata, and H. Ueno, “Inhibition of transforming growth factor β prevents progression of liver fibrosis and enhances hepatocyte regeneration in dimethylnitrosamine- treated rats,” Hepatology, vol. 32, no. 2, pp. 247–255, 2000. View at Google Scholar · View at Scopus
  20. A. Biernacka, M. Dobaczewski, and N. G. Frangogiannis, “TGF-β signaling in fibrosis,” Growth Factors, vol. 29, no. 5, pp. 196–202, 2011. View at Publisher · View at Google Scholar · View at Scopus
  21. C. H. Heldin and A. Moustakas, “Role of Smads in TGFβ signaling,” Cell and Tissue Research, vol. 347, no. 1, pp. 21–36, 2012. View at Publisher · View at Google Scholar · View at Scopus
  22. Y. S. Kanwar, J. Wada, L. Sun et al., “Diabetic nephropathy: mechanisms of renal disease progression,” Experimental Biology and Medicine, vol. 233, no. 1, pp. 4–11, 2008. View at Publisher · View at Google Scholar · View at Scopus
  23. H. Y. Lan and A. C. Chung, “Transforming growth factor-beta and Smads,” Contributions to Nephrology, vol. 170, no. 1, pp. 75–82, 2011. View at Publisher · View at Google Scholar
  24. M. Kanauchi, H. Nishioka, and K. Dohi, “Diagnostic significance of urinary fibronectin in diabetic nephropathy,” Nihon Jinzo Gakkai Shi, vol. 37, no. 1, pp. 127–133, 1995. View at Google Scholar
  25. Y. Furuse, N. Hashimoto, M. Maekawa et al., “Activation of the Smad pathway in glomeruli from a spontaneously diabetic rat model, OLETF rats,” Nephron-Experimental Nephrology, vol. 98, no. 3, pp. e100–e108, 2004. View at Publisher · View at Google Scholar · View at Scopus
  26. K. Inazaki, Y. Kanamaru, Y. Kojima et al., “Smad3 deficiency attenuates renal fibrosis, inflammation, and apoptosis after unilateral ureteral obstruction,” Kidney International, vol. 66, no. 2, pp. 597–604, 2004. View at Publisher · View at Google Scholar · View at Scopus
  27. X. M. Meng, X. R. Huang, J. Xiao et al., “Disruption of Smad4 impairs TGF-Β/Smad3 and Smad7 transcriptional regulation during renal inflammation and fibrosis in vivo and in vitro,” Kidney International, vol. 81, no. 3, pp. 266–279, 2012. View at Publisher · View at Google Scholar · View at Scopus
  28. T. Sakairi, K. Hiromura, S. Takahashi et al., “Effects of proteasome inhibitors on rat renal fibrosis in vitro and in vivo,” Nephrology, vol. 16, no. 1, pp. 76–86, 2011. View at Publisher · View at Google Scholar · View at Scopus
  29. Y. Takiyama, T. Harumi, J. Watanabe et al., “Tubular injury in a rat model of type 2 diabetes is prevented by metformin: a possible role of HIF-1α expression and oxygen metabolism,” Diabetes, vol. 60, no. 3, pp. 981–992, 2011. View at Publisher · View at Google Scholar · View at Scopus
  30. I. Paddibhatla, M. J. Lee, M. E. Kalamarz, R. Ferrarese, and S. Govind, “Role for sumoylation in systemic inflammation and immune homeostasis in Drosophila larvae,” PLoS Pathogens, vol. 6, no. 12, Article ID e1001234, 2010. View at Publisher · View at Google Scholar · View at Scopus
  31. K. Bettermann, M. Benesch, S. Weis, and J. Haybaeck, “SUMOylation in carcinogenesis,” Cancer Letters, vol. 316, no. 2, pp. 113–125, 2012. View at Publisher · View at Google Scholar · View at Scopus
  32. J. Wang and R. J. Schwartz, “Sumoylation and regulation of cardiac gene expression,” Circulation Research, vol. 107, no. 1, pp. 19–29, 2010. View at Publisher · View at Google Scholar · View at Scopus
  33. J. S. Steffan, N. Agrawal, J. Pallos et al., “SUMO modification of Huntingtin and Huntington's disease pathology,” Science, vol. 304, no. 5667, pp. 100–104, 2004. View at Publisher · View at Google Scholar · View at Scopus
  34. E. Meulmeester and F. Melchior, “Cell biology: SUMO,” Nature, vol. 452, no. 7188, pp. 709–711, 2008. View at Publisher · View at Google Scholar · View at Scopus
  35. D. Guo, M. Li, Y. Zhang et al., “A functional variant of SUMO4, a new I kappa B alpha modifier, is associated with type 1 diabetes,” Nature Genetics, vol. 36, no. 8, pp. 837–841, 2004. View at Publisher · View at Google Scholar
  36. J. Zhao, “Sumoylation regulates diverse biological processes,” Cellular and Molecular Life Sciences, vol. 64, no. 23, pp. 3017–3033, 2007. View at Publisher · View at Google Scholar · View at Scopus
  37. H. Lomelí and M. Vázquez, “Emerging roles of the SUMO pathway in development,” Cellular and Molecular Life Sciences, vol. 68, no. 24, pp. 4045–4064, 2011. View at Publisher · View at Google Scholar · View at Scopus
  38. S. Imoto, K. Sugiyama, R. Muromoto, N. Sato, T. Yamamoto, and T. Matsuda, “Regulation of transforming growth factor-β signaling by protein inhibitor of activated STAT, PIASy through Smad3,” Journal of Biological Chemistry, vol. 278, no. 36, pp. 34253–34258, 2003. View at Publisher · View at Google Scholar · View at Scopus
  39. X. Lin, M. Liang, Y. Liang, F. C. Brunicardi, F. Melchior, and X. Feng, “Activation of transforming growth factor-β signaling by SUMO-1 modification of tumor suppressor Smad4/DPC4,” Journal of Biological Chemistry, vol. 278, no. 21, pp. 18714–18719, 2003. View at Publisher · View at Google Scholar · View at Scopus
  40. M. Liang, F. Melchior, X. Feng, and X. Lin, “Regulation of Smad4 sumoylation and transforming growth factor-β signaling by protein inhibitor of activated STAT1,” Journal of Biological Chemistry, vol. 279, no. 22, pp. 22857–22865, 2004. View at Publisher · View at Google Scholar · View at Scopus
  41. X. Lin, M. Liang, Y. Liang, F. C. Brunicardi, and X. Feng, “SUMO-1/Ubc9 promotes nuclear accumulation and metabolic stability of tumor suppressor Smad4,” Journal of Biological Chemistry, vol. 278, no. 33, pp. 31043–31048, 2003. View at Publisher · View at Google Scholar · View at Scopus
  42. J. Long, G. Wang, H. E. Dongming, and F. Liu, “Repression of Smad4 transcriptional activity by SUMO modification,” Biochemical Journal, vol. 379, no. 1, pp. 23–29, 2004. View at Publisher · View at Google Scholar · View at Scopus
  43. A. Khodzhigorova, A. Distler, V. Lang et al., “Inhibition of sumoylation prevents experimental fibrosis,” Annals of the Rheumatic Diseases, vol. 71, no. 11, pp. 1904–1908, 2012. View at Publisher · View at Google Scholar · View at Scopus
  44. S. J. Netherton and S. Bonni, “Suppression of TGFβ-induced epithelial-mesenchymal transition like phenotype by a PIAS1 regulated sumoylation pathway in NMuMG epithelial cells,” PLoS ONE, vol. 5, no. 11, Article ID e13971, 2010. View at Publisher · View at Google Scholar · View at Scopus
  45. K. Torikoshi, H. Abe, T. Matsubara et al., “Protein inhibitor of activated stat, piasy regulates α-smooth muscle actin expression by interacting with e12 in mesangial cells,” PLoS ONE, vol. 7, no. 7, Article ID e41186, 2012. View at Publisher · View at Google Scholar · View at Scopus