Involvement of Nrf2-GSH signaling in TGFβ1-stimulated epithelial-to-mesenchymal transition changes in rat renal tubular cells

Archives of Pharmacal Research

Volumn 38, Issue 2, 2015, Pages 272-281

  Ryoo, In Geun ^a   Shin, Dong Ha ^b   Kang, Kyung Shin ^c   Kwak, Mi Kyoung ^a  

^a The Catholic University of Korea   (South Korea)

^b Yeungnam University   (South Korea)

^c Daewon Foreign Language High School   (South Korea)

Author keywords

Epithelial to mesenchymal transition; GSH; Nrf2; Renal tubular cell; TGF 1

Indexed keywords

GLUTATHIONE; NFE2L2 PROTEIN, RAT; RECOMBINANT PROTEIN; TRANSCRIPTION FACTOR NRF2; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL; CELL LINE; CYTOLOGY; DRUG EFFECTS; EPITHELIAL MESENCHYMAL TRANSITION; EPITHELIUM CELL; GENE EXPRESSION; GENE SILENCING; GENETICS; KIDNEY PROXIMAL TUBULE; METABOLISM; RAT; SIGNAL TRANSDUCTION;

ANIMALS; CELL LINE; EPITHELIAL CELLS; EPITHELIAL-MESENCHYMAL TRANSITION; GENE EXPRESSION; GENE KNOCKDOWN TECHNIQUES; GLUTATHIONE; KIDNEY TUBULES, PROXIMAL; NF-E2-RELATED FACTOR 2; RATS; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA1;

EID: 84936933414     PISSN: 02536269     EISSN: 19763786     Source Type: Journal    
DOI: 10.1007/s12272-014-0380-y     Document Type: Article

References (49)

1. Artaud-Macari, E., D. Goven, S. Brayer, A. Hamimi, V. Besnard, J. Marchal-Somme, Z.E. Ali, B. Crestani, S. Kerdine-Romer, A. Boutten, and M. Bonay. 2013. Nuclear factor erythroid 2-related factor 2 nuclear translocation induces myofibroblastic dedifferentiation in idiopathic pulmonary fibrosis. Antioxidants and Redox Signaling 18: 66-79.
2. Bakin, A.V., N.V. Stourman, K.R. Sekhar, C. Rinehart, X. Yan, M.J. Meredith, C.L. Arteaga, and M.L. Freeman. 2005. Smad3-ATF3 signaling mediates TGF-beta suppression of genes encoding Phase II detoxifying proteins. Free Radical Biology and Medicine 38: 375-387.
3. Biernacka, A., M. Dobaczewski, and N.G. Frangogiannis. 2011. TGF-beta signaling in fibrosis. Growth Factors 29: 196-202.
4. Bondi, C.D., N. Manickam, D.Y. Lee, K. Block, Y. Gorin, H.E. Abboud, and J.L. Barnes. 2010. NAD(P)H oxidase mediates TGF-beta1-induced activation of kidney myofibroblasts. Journal of the American Society of Nephrology 21: 93-102.
5. Brown, S.L., K.R. Sekhar, G. Rachakonda, S. Sasi, and M.L. Freeman. 2008. Activating transcription factor 3 is a novel repressor of the nuclear factor erythroid-derived 2-related factor 2 (Nrf2)-regulated stress pathway. Cancer Research 68: 364-368.
6. Choi, H.K., Pokharel, Y.R., Lim, S.C., Han, H.K., Ryu, C.S., Kim, S.K., Kwak, M.K., and Kang, K.W. 2009. Inhibition of liver fibrosis by solubilized coenzyme Q10: Role of Nrf2 activation in inhibiting transforming growth factor-beta1 expression. Toxicology and Applied Pharmacology.
7. Derynck, R., and Y.E. Zhang. 2003. Smad-dependent and Smad-independent pathways in TGF-beta family signalling. Nature 425: 577-584.
8. Fragiadaki, M., and R.M. Mason. 2011. Epithelial-mesenchymal transition in renal fibrosis: Evidence for and against. International Journal of Experimental Pathology 92: 143-150.
9. Franklin, C.C., M.E. Rosenfeld-Franklin, C. White, T.J. Kavanagh, and N. Fausto. 2003. TGFbeta1-induced suppression of glutathione antioxidant defenses in hepatocytes: caspase-dependent post-translational and caspase-independent transcriptional regulatory mechanisms. Faseb J 17: 1535-1537.
10. Hackett, T.L., S.M. Warner, D. Stefanowicz, F. Shaheen, D.V. Pechkovsky, L.A. Murray, R. Argentieri, A. Kicic, S.M. Stick, T.R. Bai, and D.A. Knight. 2009. Induction of epithelial-mesenchymal transition in primary airway epithelial cells from patients with asthma by transforming growth factor-beta1. American Journal of Respiratory and Critical Care Medicine 180: 122-133.
11. Hertig, A., J. Verine, B. Mougenot, C. Jouanneau, N. Ouali, P. Sebe, D. Glotz, P.Y. Ancel, E. Rondeau, and Y.C. Xu-Dubois. 2006. Risk factors for early epithelial to mesenchymal transition in renal grafts. American Journal of Transplantation 6: 2937-2946.
12. Hwang, M., H.J. Kim, H.J. Noh, Y.C. Chang, Y.M. Chae, K.H. Kim, J.P. Jeon, T.S. Lee, H.K. Oh, Y.S. Lee, and K.K. Park. 2006. TGF-beta1 siRNA suppresses the tubulointerstitial fibrosis in the kidney of ureteral obstruction. Experimental and Molecular Pathology 81: 48-54.
13. Itoh, K., N. Wakabayashi, Y. Katoh, T. Ishii, K. Igarashi, J.D. Engel, and M. Yamamoto. 1999. Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain. Genes and Development 13: 76-86.
14. Iwano, M., D. Plieth, T.M. Danoff, C. Xue, H. Okada, and E.G. Neilson. 2002. Evidence that fibroblasts derive from epithelium during tissue fibrosis. Journal of Clinical Investigation 110: 341-350.
15. Jiang, T., Z. Huang, Y. Lin, Z. Zhang, D. Fang, and D.D. Zhang. 2010. The protective role of Nrf2 in streptozotocin-induced diabetic nephropathy. Diabetes 59: 850-860.
16. Jiang, Y.S., T. Jiang, B. Huang, P.S. Chen, and J. Ouyang. 2013. Epithelial-mesenchymal transition of renal tubules: Divergent processes of repairing in acute or chronic injury? Medical Hypotheses 81: 73-75.
17. Kalluri, R., and R.A. Weinberg. 2009. The basics of epithelial-mesenchymal transition. Journal of Clinical Investigation 119: 1420-1428.
18. Kasai, H., J.T. Allen, R.M. Mason, T. Kamimura, and Z. Zhang. 2005. TGF-beta1 induces human alveolar epithelial to mesenchymal cell transition (EMT). Respiratory Research 6: 56.
19. Kashihara, N., Y. Haruna, V.K. Kondeti, and Y.S. Kanwar. 2010. Oxidative stress in diabetic nephropathy. Current Medicinal Chemistry 17: 4256-4269.
20. Kobayashi, A., M.I. Kang, H. Okawa, M. Ohtsuji, Y. Zenke, T. Chiba, K. Igarashi, and M. Yamamoto. 2004. Oxidative stress sensor Keap1 functions as an adaptor for Cul3-based E3 ligase to regulate proteasomal degradation of Nrf2. Molecular and Cellular Biology 24: 7130-7139.
21. Kobayashi, M., and M. Yamamoto. 2005. Molecular mechanisms activating the Nrf2-Keap1 pathway of antioxidant gene regulation. Antioxidants and Redox Signaling 7: 385-394.
22. Kwak, M.K., and T.W. Kensler. 2010. Targeting NRF2 signaling for cancer chemoprevention. Toxicology and Applied Pharmacology 244: 66-76.
23. Kwak, M.K., N. Wakabayashi, K. Itoh, H. Motohashi, M. Yamamoto, and T.W. Kensler. 2003. Modulation of gene expression by cancer chemopreventive dithiolethiones through the Keap1-Nrf2 pathway: Identification of novel gene clusters for cell survival. Journal of Biological Chemistry 278: 8135-8145.
24. Lee, J.M., S. Dedhar, R. Kalluri, and E.W. Thompson. 2006. The epithelial-mesenchymal transition: new insights in signaling, development, and disease. Journal of Cell Biology 172: 973-981.
25. Lewerenz, J., and P. Maher. 2011. Control of redox state and redox signaling by neural antioxidant systems. Antioxidants and Redox Signaling 14: 1449-1465.
26. Li, W., and A.N. Kong. 2009. Molecular mechanisms of Nrf2-mediated antioxidant response. Molecular Carcinogenesis 48: 91-104.
27. Liu, R.M., and K.A. Gaston Pravia. 2010. Oxidative stress and glutathione in TGF-beta-mediated fibrogenesis. Free Radical Biology and Medicine 48: 1-15.
28. Liu, R.M., P.K. Vayalil, C. Ballinger, D.A. Dickinson, W.T. Huang, S. Wang, T.J. Kavanagh, Q.L. Matthews, and E.M. Postlethwait. 2012. Transforming growth factor beta suppresses glutamate-cysteine ligase gene expression and induces oxidative stress in a lung fibrosis model. Free Radical Biology and Medicine 53: 554-563.
29. Liu, Y. 2004. Epithelial to mesenchymal transition in renal fibrogenesis: pathologic significance, molecular mechanism, and therapeutic intervention. Journal of the American Society of Nephrology 15: 1-12.
30. Margetts, P.J., P. Bonniaud, L. Liu, C.M. Hoff, C.J. Holmes, J.A. West-Mays, and M.M. Kelly. 2005. Transient overexpression of TGF-β1 induces epithelial mesenchymal transition in the rodent peritoneum. Journal of the American Society of Nephrology 16: 425-436.
31. Nakamura, T., M. Matsushima, Y. Hayashi, M. Shibasaki, K. Imaizumi, N. Hashimoto, K. Shimokata, Y. Hasegawa, and T. Kawabe. 2011. Attenuation of transforming growth factor-beta-stimulated collagen production in fibroblasts by quercetin-induced heme oxygenase-1. American Journal of Respiratory Cell and Molecular Biology 44: 614-620.
32. Oh, C.J., J.Y. Kim, A.K. Min, K.G. Park, R.A. Harris, H.J. Kim, and I.K. Lee. 2012. Sulforaphane attenuates hepatic fibrosis via NF-E2-related factor 2-mediated inhibition of transforming growth factor-beta/Smad signaling. Free Radical Biology and Medicine 52: 671-682.
33. Paine, A., B. Eiz-Vesper, R. Blasczyk, and S. Immenschuh. 2010. Signaling to heme oxygenase-1 and its anti-inflammatory therapeutic potential. Biochemical Pharmacology 80: 1895-1903.
34. Pat, B., T. Yang, C. Kong, D. Watters, D.W. Johnson, and G. Gobe. 2005. Activation of ERK in renal fibrosis after unilateral ureteral obstruction: modulation by antioxidants. Kidney International 67: 931-943.
35. Pohlers, D., J. Brenmoehl, I. Loffler, C.K. Muller, C. Leipner, S. Schultze-Mosgau, A. Stallmach, R.W. Kinne, and G. Wolf. 2009. TGF-beta and fibrosis in different organs - molecular pathway imprints. Biochimica et Biophysica Acta 1792: 746-756.
36. Rastaldi, M.P., F. Ferrario, L. Giardino, G. Dell'antonio, C. Grillo, P. Grillo, F. Strutz, G.A. Muller, G. Colasanti, and G. D'amico. 2002. Epithelial-mesenchymal transition of tubular epithelial cells in human renal biopsies. Kidney International 62: 137-146.
37. Rhyu, D.Y., Y. Yang, H. Ha, G.T. Lee, J.S. Song, S.T. Uh, and H.B. Lee. 2005. Role of reactive oxygen species in TGF-beta1-induced mitogen-activated protein kinase activation and epithelial-mesenchymal transition in renal tubular epithelial cells. Journal of the American Society of Nephrology 16: 667-675.
38. Sato, M., Y. Muragaki, S. Saika, A.B. Roberts, and A. Ooshima. 2003. Targeted disruption of TGF-beta1/Smad3 signaling protects against renal tubulointerstitial fibrosis induced by unilateral ureteral obstruction. Journal of Clinical Investigation 112: 1486-1494.
39. Shin, D.H., H.M. Park, K.A. Jung, H.G. Choi, J.A. Kim, D.D. Kim, S.G. Kim, K.W. Kang, S.K. Ku, T.W. Kensler, and M.K. Kwak. 2010. The NRF2-heme oxygenase-1 system modulates cyclosporin A-induced epithelial-mesenchymal transition and renal fibrosis. Free Radical Biology and Medicine 48: 1051-1063.
40. Simonson, M.S. 2007. Phenotypic transitions and fibrosis in diabetic nephropathy. Kidney International 71: 846-854.
41. Soetikno, V., F.R. Sari, A.P. Lakshmanan, S. Arumugam, M. Harima, K. Suzuki, H. Kawachi, and K. Watanabe. 2013. Curcumin alleviates oxidative stress, inflammation, and renal fibrosis in remnant kidney through the Nrf2-keap1 pathway. Molecular Nutrition and Food Research 57: 1649-1659.
42. Wakabayashi, N., A.T. Dinkova-Kostova, W.D. Holtzclaw, M.L. Kang, A. Kobayashi, M. Yamamoto, T.W. Kensler, and P. Talalay. 2004. Protection against electrophile and oxidant stress by induction of the phase 2 response: Fate of cysteines of the Keap1 sensor modified by inducers. Proceedings of the National Academy of Sciences of the United States of America 101: 2040-2045.
43. Willis, B.C., J.M. Liebler, K. Luby-Phelps, A.G. Nicholson, E.D. Crandall, R.M. Du Bois, and Z. Borok. 2005. Induction of epithelial-mesenchymal transition in alveolar epithelial cells by transforming growth factor-beta1: Potential role in idiopathic pulmonary fibrosis. American Journal of Pathology 166: 1321-1332.
44. Wynn, T.A. 2008. Cellular and molecular mechanisms of fibrosis. Journal of Pathology 214: 199-210.
45. Yamamoto, T., T. Suzuki, A. Kobayashi, J. Wakabayashi, J. Maher, H. Motohashi, and M. Yamamoto. 2008. Physiological significance of reactive cysteine residues of Keap1 in determining Nrf2 activity. Molecular and Cellular Biology 28: 2758-2770.
46. Zarjou, A., and A. Agarwal. 2012. Heme oxygenase-1 as a target for TGF-beta in kidney disease. Seminars in Nephrology 32: 277-286.
47. Zavadil, J., and E.P. Bottinger. 2005. TGF-beta and epithelial-to-mesenchymal transitions. Oncogene 24: 5764-5774.
48. Zhang, D.D., S.C. Lo, J.V. Cross, D.J. Templeton, and M. Hannink. 2004. Keap1 is a redox-regulated substrate adaptor protein for a Cul3-dependent ubiquitin ligase complex. Molecular and Cellular Biology 24: 10941-10953.
49. Zhang, M., Z. Zhang, H.Y. Pan, D.X. Wang, Z.T. Deng, and X.L. Ye. 2009. TGF-beta1 induces human bronchial epithelial cell-to-mesenchymal transition in vitro. Lung 187: 187-194.