Table of Contents Author Guidelines Submit a Manuscript
Erratum

An erratum for this article has been published. To view the erratum, please click here.

Journal of Diabetes Research
Volume 2015 (2015), Article ID 504761, 12 pages
http://dx.doi.org/10.1155/2015/504761
Research Article

NADPH Oxidase-Induced NALP3 Inflammasome Activation Is Driven by Thioredoxin-Interacting Protein Which Contributes to Podocyte Injury in Hyperglycemia

1Department of Nephrology, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430022, China
2Department of Neurobiology, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430030, China

Received 14 November 2014; Revised 15 February 2015; Accepted 18 February 2015

Academic Editor: Daisuke Koya

Copyright © 2015 Pan Gao 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. M. Brownlee, “Biochemistry and molecular cell biology of diabetic complications,” Nature, vol. 414, no. 6865, pp. 813–820, 2001. View at Publisher · View at Google Scholar · View at Scopus
  2. U. Sen, P. Basu, O. A. Abe et al., “Hydrogen sulfide ameliorates hyperhomocysteinemia-associated chronic renal failure,” The American Journal of Physiology—Renal Physiology, vol. 297, no. 2, pp. F410–F419, 2009. View at Publisher · View at Google Scholar · View at Scopus
  3. F.-F. He, C. Zhang, S. Chen et al., “Role of CD2-associated protein in albumin overload-induced apoptosis in podocytes,” Cell Biology International, vol. 35, no. 8, pp. 827–834, 2011. View at Publisher · View at Google Scholar · View at Scopus
  4. K. Susztak, A. C. Raff, M. Schiffer, and E. P. Böttinger, “Glucose-induced reactive oxygen species cause apoptosis of podocytes and podocyte depletion at the onset of diabetic nephropathy,” Diabetes, vol. 55, no. 1, pp. 225–233, 2006. View at Publisher · View at Google Scholar · View at Scopus
  5. M. W. Steffes, D. Schmidt, R. McCrery et al., “Glomerular cell number in normal subjects and in type 1 diabetic patients,” Kidney International, vol. 59, no. 6, pp. 2104–2113, 2001. View at Publisher · View at Google Scholar · View at Scopus
  6. G. Ren, C. Huynh, K. Bijian, and A. V. Cybulsky, “Role of apoptosis signal-regulating kinase 1 in complement-mediated glomerular epithelial cell injury,” Molecular Immunology, vol. 45, no. 8, pp. 2236–2246, 2008. View at Publisher · View at Google Scholar · View at Scopus
  7. F. Yi, M. Xia, N. Li, C. Zhang, L. Tang, and P.-L. Li, “Contribution of guanine nucleotide exchange factor Vav2 to hyperhomocysteinemic glomerulosclerosis in rats,” Hypertension, vol. 53, no. 1, pp. 90–96, 2009. View at Publisher · View at Google Scholar · View at Scopus
  8. C. Zhang, J.-J. Hu, M. Xia, K. M. Boini, C. Brimson, and P.-L. Li, “Redox signaling via lipid raft clustering in homocysteine-induced injury of podocytes,” Biochimica et Biophysica Acta, vol. 1803, no. 4, pp. 482–491, 2010. View at Publisher · View at Google Scholar · View at Scopus
  9. C. Zhang, J. J. Hu, M. Xia et al., “Protection of podocytes from hyperhomocysteinemia-induced injury by deletion of the gp91phox gene,” Free Radical Biology and Medicine, vol. 48, no. 8, pp. 1109–1117, 2010. View at Publisher · View at Google Scholar · View at Scopus
  10. S. C. Eisenbarth, O. R. Colegio, W. O'Connor Jr., F. S. Sutterwala, and R. A. Flavell, “Crucial role for the Nalp3 inflammasome in the immunostimulatory properties of aluminium adjuvants,” Nature, vol. 453, no. 7198, pp. 1122–1126, 2008. View at Publisher · View at Google Scholar · View at Scopus
  11. J. M. Kahlenberg and G. R. Dubyak, “Differing caspase-1 activation states in monocyte versus macrophage models of IL-1β processing and release,” Journal of Leukocyte Biology, vol. 76, no. 3, pp. 676–684, 2004. View at Publisher · View at Google Scholar · View at Scopus
  12. S. L. Cassel, S. C. Eisenbarth, S. S. Iyer et al., “The Nalp3 inflammasome is essential for the development of silicosis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 26, pp. 9035–9040, 2008. View at Publisher · View at Google Scholar · View at Scopus
  13. C. Zhang, K. M. Boini, M. Xia et al., “Activation of Nod-like receptor protein 3 inflammasomes turns on podocyte injury and glomerular sclerosis in hyperhomocysteinemia,” Hypertension, vol. 60, no. 1, pp. 154–162, 2012. View at Publisher · View at Google Scholar · View at Scopus
  14. S. Mariathasan, D. S. Weiss, K. Newton et al., “Cryopyrin activates the inflammasome in response to toxins and ATP,” Nature, vol. 440, no. 7081, pp. 228–232, 2006. View at Publisher · View at Google Scholar · View at Scopus
  15. S. Malozowski and J. T. Sahlroot, “Interleukin-1-receptor antagonist in type 2 diabetes mellitus,” The New England Journal of Medicine, vol. 357, no. 3, pp. 302–303, 2007. View at Publisher · View at Google Scholar · View at Scopus
  16. R. Zhou, A. Tardivel, B. Thorens, I. Choi, and J. Tschopp, “Thioredoxin-interacting protein links oxidative stress to inflammasome activation,” Nature Immunology, vol. 11, no. 2, pp. 136–140, 2010. View at Publisher · View at Google Scholar · View at Scopus
  17. F. Meissner, K. Molawi, and A. Zychlinsky, “Superoxide dismutase 1 regulates caspase-1 and endotoxic shock,” Nature Immunology, vol. 9, no. 8, pp. 866–872, 2008. View at Publisher · View at Google Scholar · View at Scopus
  18. S. L. Demento, S. C. Eisenbarth, H. G. Foellmer et al., “Inflammasome-activating nanoparticles as modular systems for optimizing vaccine efficacy,” Vaccine, vol. 27, no. 23, pp. 3013–3021, 2009. View at Publisher · View at Google Scholar · View at Scopus
  19. J. M. Abais, C. Zhang, M. Xia et al., “NADPH oxidase-mediated triggering of inflammasome activation in mouse podocytes and glomeruli during hyperhomocysteinemia,” Antioxidants and Redox Signaling, vol. 18, no. 13, pp. 1537–1548, 2013. View at Publisher · View at Google Scholar · View at Scopus
  20. R. Zhou, A. S. Yazdi, P. Menu, and J. Tschopp, “A role for mitochondria in NLRP3 inflammasome activation,” Nature, vol. 469, no. 7329, pp. 221–225, 2011. View at Publisher · View at Google Scholar · View at Scopus
  21. J. B. Johnston, J. W. Barrett, S. H. Nazarian et al., “A poxvirus-encoded pyrin domain protein interacts with ASC-1 to inhibit host inflammatory and apoptotic responses to infection,” Immunity, vol. 23, no. 6, pp. 587–598, 2005. View at Publisher · View at Google Scholar · View at Scopus
  22. C. M. Oslowski, T. Hara, B. O'Sullivan-Murphy et al., “Thioredoxin-interacting protein mediates ER stress-induced β cell death through initiation of the inflammasome,” Cell Metabolism, vol. 16, no. 2, pp. 265–273, 2012. View at Publisher · View at Google Scholar · View at Scopus
  23. L. Franchi, T. Eigenbrod, and G. Núñez, “Cutting edge: TNF-α mediates sensitization to ATP and silica via the NLRP3 inflammasome in the absence of microbial stimulation,” Journal of Immunology, vol. 183, no. 2, pp. 792–796, 2009. View at Publisher · View at Google Scholar · View at Scopus
  24. A. M. Kaimul, H. Nakamura, H. Masutani, and J. Yodoi, “Thioredoxin and thioredoxin-binding protein-2 in cancer and metabolic syndrome,” Free Radical Biology and Medicine, vol. 43, no. 6, pp. 861–868, 2007. View at Publisher · View at Google Scholar · View at Scopus
  25. K. Schroder, R. Zhou, and J. Tschopp, “The NLRP3 inflammasome: a sensor for metabolic danger?” Science, vol. 327, no. 5963, pp. 296–300, 2010. View at Publisher · View at Google Scholar · View at Scopus
  26. B.-C. Liu, X. Song, X.-Y. Lu et al., “High glucose induces podocyte apoptosis by stimulating TRPC6 via elevation of reactive oxygen species,” Biochimica et Biophysica Acta, vol. 1833, no. 6, pp. 1434–1442, 2013. View at Publisher · View at Google Scholar · View at Scopus
  27. P. Gao, X. F. Meng, H. Su et al., “Thioredoxin-interacting protein mediates NALP3 inflammasome activation in podocytes during diabetic nephropathy,” Biochimica et Biophysica Acta—Molecular Cell Research, vol. 1843, no. 11, pp. 2448–2460, 2014. View at Publisher · View at Google Scholar
  28. S. Faubel, D. Ljubanovic, L. Reznikov, H. Somerset, C. A. Dinarello, and C. L. Edelstein, “Caspase-1-deficient mice are protected against cisplatin-induced apoptosis and acute tubular necrosis,” Kidney International, vol. 66, no. 6, pp. 2202–2213, 2004. View at Publisher · View at Google Scholar · View at Scopus
  29. A. Vilaysane, J. Chun, M. E. Seamone et al., “The NLRP3 inflammasome promotes renal inflammation and contributes to CKD,” Journal of the American Society of Nephrology, vol. 21, no. 10, pp. 1732–1744, 2010. View at Publisher · View at Google Scholar · View at Scopus
  30. J. Zhao, H. Wang, C. Dai et al., “P2X7 blockade attenuates murine lupus nephritis by inhibiting activation of the NLRP3/ASC/Caspase 1 pathway,” Arthritis and Rheumatism, vol. 65, no. 12, pp. 3176–3185, 2013. View at Publisher · View at Google Scholar · View at Scopus
  31. K.-F. Hua, S.-M. Yang, T.-Y. Kao et al., “Osthole mitigates progressive IgA nephropathy by inhibiting reactive oxygen species generation and NF-kappaB/NLRP3 pathway,” PLoS ONE, vol. 8, no. 10, Article ID e77794, 2013. View at Publisher · View at Google Scholar · View at Scopus
  32. R. Scarpioni, D. Rigante, L. Cantarini et al., “Renal involvement in secondary amyloidosis of Muckle-Wells syndrome: marked improvement of renal function and reduction of proteinuria after therapy with human anti-interleukin-1β monoclonal antibody canakinumab,” Clinical Rheumatology, 2014. View at Publisher · View at Google Scholar · View at Scopus
  33. J. Tschopp and K. Schroder, “NLRP3 inflammasome activation: the convergence of multiple signalling pathways on ROS production?” Nature Reviews Immunology, vol. 10, no. 3, pp. 210–215, 2010. View at Publisher · View at Google Scholar · View at Scopus
  34. F. Giacco and M. Brownlee, “Oxidative stress and diabetic complications,” Circulation Research, vol. 107, no. 9, pp. 1058–1070, 2010. View at Publisher · View at Google Scholar · View at Scopus
  35. J. M. Forbes, M. T. Coughlan, and M. E. Cooper, “Oxidative stress as a major culprit in kidney disease in diabetes,” Diabetes, vol. 57, no. 6, pp. 1446–1454, 2008. View at Publisher · View at Google Scholar · View at Scopus
  36. Y. Gorin, K. Block, J. Hernandez et al., “Nox4 NAD(P)H oxidase mediates hypertrophy and fibronectin expression in the diabetic kidney,” The Journal of Biological Chemistry, vol. 280, no. 47, pp. 39616–39626, 2005. View at Publisher · View at Google Scholar · View at Scopus
  37. S. Yamagishi, “Comment on: Thallas-Bonke et al. (2008) ‘Inhibition of NADPH oxidase prevents advanced glycation end product-mediated damage in diabetic nephropathy through a protein kinase C-alpha-dependent pathway’, Diabetes, vol. 57, pp. 460–469, 2008,” Diabetes, vol. 57, no. 6, pp. e13–e14, 2008. View at Google Scholar
  38. S. Ruiz, P. E. Pergola, R. A. Zager, and N. D. Vaziri, “Targeting the transcription factor Nrf2 to ameliorate oxidative stress and inflammation in chronic kidney disease,” Kidney International, vol. 83, no. 6, pp. 1029–1041, 2013. View at Publisher · View at Google Scholar · View at Scopus
  39. S. S. Gill and N. Tuteja, “Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants,” Plant Physiology and Biochemistry, vol. 48, no. 12, pp. 909–930, 2010. View at Publisher · View at Google Scholar · View at Scopus
  40. Y. Meyer, B. B. Buchanan, F. Vignols, and J.-P. Reichheld, “Thioredoxins and glutaredoxins: unifying elements in redox biology,” Annual Review of Genetics, vol. 43, pp. 335–367, 2009. View at Publisher · View at Google Scholar · View at Scopus
  41. D. F. D. Mahmood, A. Abderrazak, K. El Hadri, T. Simmet, and M. Rouis, “The thioredoxin system as a therapeutic target in human health and disease,” Antioxidants and Redox Signaling, vol. 19, no. 11, pp. 1266–1303, 2013. View at Publisher · View at Google Scholar · View at Scopus
  42. K.-S. Chen and H. F. DeLuca, “Isolation and characterization of a novel cDNA from HL-60 cells treated with 1,25-dihydroxyvitamin D-3,” Biochimica et Biophysica Acta, vol. 1219, no. 1, pp. 26–32, 1994. View at Publisher · View at Google Scholar · View at Scopus
  43. E. Junn, S. H. Han, J. Y. Im et al., “Vitamin D3 up-regulated protein 1 mediates oxidative stress via suppressing the thioredoxin function,” Journal of Immunology, vol. 164, no. 12, pp. 6287–6295, 2000. View at Publisher · View at Google Scholar · View at Scopus
  44. J. W. Chung, J.-H. Jeon, S.-R. Yoon, and I. Choi, “Vitamin D3 upregulated protein 1 (VDUP1) is a regulator for redox signaling and stress-mediated diseases,” The Journal of Dermatology, vol. 33, no. 10, pp. 662–669, 2006. View at Publisher · View at Google Scholar · View at Scopus
  45. P. C. Schulze, J. Yoshioka, T. Takahashi, Z. He, G. L. King, and R. T. Lee, “Hyperglycemia promotes oxidative stress through inhibition of thioredoxin function by thioredoxin-interacting protein,” The Journal of Biological Chemistry, vol. 279, no. 29, pp. 30369–30374, 2004. View at Publisher · View at Google Scholar · View at Scopus
  46. X. Li, Y. Rong, M. Zhang et al., “Up-regulation of thioredoxin interacting protein (Txnip) by p38 MAPK and FOXO1 contributes to the impaired thioredoxin activity and increased ROS in glucose-treated endothelial cells,” Biochemical and Biophysical Research Communications, vol. 381, no. 4, pp. 660–665, 2009. View at Publisher · View at Google Scholar · View at Scopus
  47. A. Advani, R. E. Gilbert, K. Thai et al., “Expression, localization, and function of the thioredoxin system in diabetic nephropathy,” Journal of the American Society of Nephrology, vol. 20, no. 4, pp. 730–741, 2009. View at Publisher · View at Google Scholar
  48. Y. Hamada and M. Fukagawa, “A possible role of thioredoxin interacting protein in the pathogenesis of streptozotocin-induced diabetic nephropathy,” Kobe Journal of Medical Sciences, vol. 53, no. 1-2, pp. 53–61, 2007. View at Google Scholar · View at Scopus
  49. T. Kobayashi, S. Uehara, T. Ikeda, H. Itadani, and H. Kotani, “Vitamin D3 up-regulated protein-1 regulates collagen expression in mesangial cells,” Kidney International, vol. 64, no. 5, pp. 1632–1642, 2003. View at Publisher · View at Google Scholar · View at Scopus