Bone morphogenetic protein-7 inhibits proximal tubular epithelial cell Smad3 signaling via increased SnoN expression

American Journal of Pathology

Volumn 176, Issue 3, 2010, Pages 1139-1147

  Luo, Dong Dong ^a   Phillips, Aled ^a   Fraser, Donald ^a  

^a CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; OSTEOGENIC PROTEIN 1; PROTEIN SNON; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; KIDNEY EPITHELIUM; KIDNEY PROXIMAL TUBULE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROXIMAL TUBULE EPITHELIAL CELL;

EID: 77749279452     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.2353/ajpath.2010.090459     Document Type: Article

References (45)

1. Wynn T: Cellular and molecular mechanisms of fibrosis. J Pathol 2008, 214:199-210
2. Massague J: How cells read TGF-β signals. Nat Rev Mol Cell Biol 2000, 1:169-178
3. Morrissey J, Hruska K, Guo G, Wang S, Chen Q, Klahr S: Bone morphogenetic protein-7 improves renal fibrosis and accelerates the return of renal function, J Am Soc Nephrol 2002, 13(Suppl 1): S14-S21
4. Zeisberg M, Hanai J, Sugimoto H, Mammoto T, Charytan D, Strutz F, Kalluri R: BMP-7 counteracts TGF-β1-induced epithelial-to-mesenchymal transition and reverses chronic renal injury. Nat Med 2003, 9:964-968
5. Zeisberg M, Bottiglio C, Kumar N, Maeshima Y, Strutz F, Muller GA, Kalluri R: Bone morphogenic protein-7 inhibits progression of chronic renal fibrosis associated with two genetic mouse models. Am J Physiol Renal Physiol 2003, 285:F1060-F1067
6. Sugimoto H, Grahovac G, Zeisberg M, Kalluri R: Renal fibrosis and glomerulosclerosis in a new mouse model of diabetic nephropathy and its regression by bone morphogenic protein-7 and advanced glycation end product inhibitors. Diabetes 2007, 56:1825-1833
7. Wang S, Hirschberg R: Bone morphogenetic protein-7 signals opposing transforming growth factor β in mesangial cells. J Biol Chem 2004, 279:23200-23206
8. Selbi W, de la Motte C, Hascall V, Phillips A: BMP-7 modulates hyaluronan-mediated proximal tubular cell-monocyte interaction. J Am Soc Nephrol 2004, 15:1199-1211
9. Zhang XL, Selbi W, de la Motte C, Hascall V, Phillips AO: Bone morphogenic protein-7 inhibits monocyte-stimulated TGF-β1 generation in renal proximal tubular epithelial cells. J Am Soc Nephrol 2005, 16:79-89
10. Valcourt U, Kowanetz M, Niimi H, Heldin CH, Moustakas A: TGF-β and the Smad signaling pathway support transcriptomic reprogramming during epithelial-mesenchymal cell transition. Mol Biol Cell 2005, 16(4):1987-2002
11. Ross S, Hill CS: How the Smads regulate transcription. Int J Biochem Cell Biol 2008, 40:383-408
12. Fraser D, Brunskill N, Ito T, Phillips A: Long-term exposure of proximal tubular epithelial cells to glucose induces transforming growth factor-β1 synthesis via an autocrine PDGF loop. Am J Pathol 2003, 163:2565-2574
13. Zhang M, Fraser D, Phillips A: ERK, p38, and Smad signaling pathways differentially regulate transforming growth factor-β1 autoinduction in proximal tubular epithelial cells. Am J Pathol 2006, 169:1282-1293
14. Piek E, Moustakas A, Kurisaki A, Heldin CH, ten Dijke P: TGF-β type I receptor/ALK-5 and Smad proteins mediate epithelial to mesenchymal transdifferentiation in NMuMG breast epithelial cells. J Cell Sci 1999, 112:4557-4568
15. Felici A, Wurthner JU, Parks WT, Giam LR-y, Reiss M, Karpova TS, McNally JG, Roberts AB: TLP, a novel modulator of TGF-β signaling, has opposite effects on Smad2- and Smad3-dependent signaling. EMBO J 2003, 22:4465-4477
16. McLoughlin RM, Witowski J, Robson RL, Wilkinson TS, Hurst SM, Williams AS, Williams JD, Rose-John S, Jones SA, Topley N: Interplay between IFN-γ and IL-6 signaling governs neutrophil trafficking and apoptosis during acute inflammation. J Clin Invest 2003, 112: 598-607
17. Kim BC, Song CY, Hong HK, Lee HS: Role of CAGA boxes in the plasminogen activator inhibitor-1 promoter in mediating oxidized lowdensity lipoprotein-induced transcriptional activation in mesangial cells. Transl Res 2007, 150:180-188
18. Roberts AB, Tian F, Byfield SD, Stuelten C, Ooshima A, Saika S, Flanders KC: Smad3 is key to TGF-β-mediated epithelial-to-mesenchymal transition, fibrosis, tumor suppression and metastasis. Cytokine Growth Factor Rev 2006, 17:19-27
19. Eddy AA, Fogo AB: Plasminogen activator inhibitor-1 in chronic kidney disease: evidence and mechanisms of action. J Am Soc Nephrol 2006, 17:2999-3012
20. Stroschein SL, Wang W, Luo K: Cooperative binding of Smad proteins to two adjacent DNA elements in the plasminogen activator inhibitor-1 promoter mediates transforming growth factor β-induced smad-dependent transcriptional activation. J Biol Chem 1999, 274:9431-9441
21. Daly AC, Randall RA, Hill CS: Transforming growth factor β-induced Smad1/5 phosphorylation in epithelial cells is mediated by novel receptor complexes and is essential for anchorage-independent growth. Mol Cell Biol 2008, 28:6889-6902
22. Shi Y, Massague J: Mechanisms of TGF-β signaling from cell membrane to the nucleus. Cell 2003, 113:685-700
23. Poncelet A-C, Schnaper HW, Tan R, Liu Y, Runyan CE: Cell phenotype-specific down-regulation of Smad3 involves decreased gene activation as well as protein degradation. J Biol Chem 2007, 282:15534-15540
24. Li W, Chen F, Nagarajan RP, Liu X, Chen Y: Characterization of the DNA-binding property of Smad5. Biochem Biophys Res Commun 2001, 286:1163-1169
25. Luo K: Ski and SnoN: negative regulators of TGF-β signaling. Curr Opin Genet Dev 2004, 14:65-70
26. Levy L, Howell M, Das D, Harkin S, Episkopou V, Hill CS: Arkadia activates Smad3/Smad4-dependent transcription by triggering signal-induced SnoN degradation. Mol Cell Biol 2007, 27:6068-6083
27. Stroschein SL, Bonni S, Wrana JL, Luo K: Smad3 recruits the anaphase-promoting complex for ubiquitination and degradation of SnoN. Genes Dev 2001, 15:2822-2836
28. Godin RE, Robertson EJ, Dudley AT: Role of BMP family members during kidney development. Int J Dev Biol 1999, 43:405-411
29. Kazama I, Mahoney Z, Miner JH, Graf D, Economides AN, Kreidberg JA: Podocyte-derived BMP7 is critical for nephron development. J Am Soc Nephrol 2008, 19:2181-2191
30. Wang SN, Lapage J, Hirschberg R: Loss of tubular bone morphogenetic protein-7 in diabetic nephropathy. J Am Soc Nephrol 2001, 12:2392-2399
31. Gould SE, Day M, Jones SS, Dorai H: BMP-7 regulates chemokine, cytokine, and hemodynamic gene expression in proximal tubule cells. Kidney Int 2002, 61:51-60
32. Zeisberg EM, Tarnavski O, Zeisberg M, Dorfman AL, McMullen JR, Gustafsson E, Chandraker A, Yuan X, Pu WT, Roberts AB, Neilson EG, Sayegh MH, Izumo S, Kalluri R: Endothelial-to-mesenchymal transition contributes to cardiac fibrosis. Nat Med 2007, 13:952-961
33. Border WA, Noble NA: Transforming growth factor β in tissue fibrosis. N Engl J Med 1994, 331:1286-1292
34. Coimbra T, Wiggins R, Noh JW, Merritt S, Phan SH: Transforming growth factor-β production in anti-glomerular basement membrane disease in the rabbit. Am J Pathol 1991, 138:223-234
35. Nakamura T, Miller D, Ruoslahti E, Border WA: Production of extracellular matrix by glomerular epithelial cells is regulated by transforming growth factor-β1. Kidney Int 1992, 41:1213-1221
36. Border WA, Okuda S, Languino LR, Sporn MB, Ruoslahti E: Suppression of experimental glomerulonephritis by antiserum against transforming growth factor β1. Nature 1990, 346:371-374
37. Sharma K, Jin Y, Guo J, Ziyadeh FN: Neutralization of TGF-β by anti-TGF-β antibody attenuates kidney hypertrophy and the enhanced extracellular matrix gene expression in STZ-induced diabetic mice. Diabetes 1996, 45:522-530
38. Liu Y: Renal fibrosis: new insights into the pathogenesis and therapeutics. Kidney Int 2006, 69:213-217
39. II110. Oncogene 1998, 17:2505-2513
40. Stroschein SL, Wang W, Zhou S, Zhou Q, Luo K: Negative feedback regulation of TGF-β signaling by the SnoN oncoprotein. Science 1999, 286:771-774
41. Yang J, Zhang X, Li Y, Liu Y: Downregulation of Smad transcriptional corepressors SnoN and Ski in the fibrotic kidney: an amplification mechanism for TGF-β1 signaling. J Am Soc Nephrol 2003, 14:3167-3177
42. Tan R, Zhang J, Tan X, Zhang X, Yang J, Liu Y: Downregulation of SnoN expression in obstructive nephropathy is mediated by an enhanced ubiquitin-dependent degradation. J Am Soc Nephrol 2006, 17:2781-2791
43. Fukasawa H, Yamamoto T, Togawa A, Ohashi N, Fujigaki Y, Oda T, Uchida C, Kitagawa K, Hattori T, Suzuki S, Kitagawa M, Hishida A: Ubiquitin-dependent degradation of SnoN and Ski is increased in renal fibrosis induced by obstructive injury. Kidney Int 2006, 69:1733-1740
44. Yang J, Dai C, Liu Y: A novel mechanism by which hepatocyte growth factor blocks tubular epithelial to mesenchymal transition. J Am Soc Nephrol 2005, 16:68-78
45. Tan R, Zhang X, Yang J, Li Y, Liu Y: Molecular basis for the cell type specific induction of SnoN expression by hepatocyte growth factor. J Am Soc Nephrol 2007, 18:2340-2349