Recapitulation of embryological programmes in renal fibrosis - The importance of epithelial cell plasticity and developmental genes

Nephron - Physiology

Volumn 103, Issue 3, 2006, Pages

  Roxburgh, Sarah A ^a,b   Murphy, Madeline ^a   Pollock, Carol A ^c   Brazil, Derek P ^a,b  

^a UNIVERSITY COLLEGE DUBLIN   (Ireland)

^b MATER MISERICORDIAE UNIVERSITY HOSPITAL   (Ireland)

^c UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Bone morphogenic proteins; Diabetic nephropathy; Epithelial mesenchymal transition; Gremlin; Transforming growth factor ; Tubulointerstitial fibrosis

Indexed keywords

ADVANCED GLYCATION END PRODUCT; ADVANCED GLYCATION END PRODUCT RECEPTOR; ALPHA SMOOTH MUSCLE ACTIN; BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 4; CHORDIN; CONNECTIVE TISSUE GROWTH FACTOR; CYSTEINE; GENE PRODUCT; GREMLIN; OSTEOGENIC PROTEIN 1; SMAD PROTEIN; TISSUE PLASMINOGEN ACTIVATOR; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG;

DEVELOPMENTAL GENETICS; DIABETES MELLITUS; DIABETIC NEPHROPATHY; DISEASE COURSE; INTERSTITIAL NEPHRITIS; KIDNEY DEVELOPMENT; KIDNEY EPITHELIUM; KIDNEY FAILURE; KIDNEY FIBROSIS; KIDNEY SCAR; MESENCHYME; MYOFIBROBLAST; NONHUMAN; PRIORITY JOURNAL; SHORT SURVEY;

ANIMALS; EMBRYONIC DEVELOPMENT; EPITHELIAL CELLS; GENES, DEVELOPMENTAL; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; KIDNEY; KIDNEY DISEASES; MESODERM;

EID: 33745435247     PISSN: 16602137     EISSN: None     Source Type: Journal    
DOI: 10.1159/000092453     Document Type: Short Survey

References (70)

1. Schena F: Epidemiology of end stage renal disease: international comparisons of renal replacement therapy. Kidney Int 2000;57(suppl 74):S39-S45.
2. US Renal Data System, USRDS 2004 Annual Data Report: Atlas of End-Stage Renal Disease in the United States. www.usrds.org/adr_2004. htm.
3. Nath KA: The tubulointerstitium in progressive renal disease. Kidney Int 1998;54:992-994.
4. Liu Y: Epithelial to mesenchymal transition in renal fibrogenesis: pathologic significance, molecular mechanism, and therapeutic intervention. J Am Soc Nephrol 2004;15:1-12.
5. Zeisberg M, Kalluri R: The role of epithelial-to-mesenchymal transition in renal fibrosis. J Mol Med 2004;82:175-181.
6. Okada H, Inoue T, Suzuki H, Strutz F, Neilson EG: Epithelial-mesenchymal transformation of renal tubular epithelial cells in vitro and in vivo. Nephrol Dial Transplant 2000;15(suppl 6):44-46.
7. Fogo AB: Diabetic nephropathy: it's in the numbers. Kidney Int 2002;61:2274-2275.
8. Pedagogos E, Hewitson T, Fraser I, Nicholls K, Becker G: Myofibroblasts and arteriolar sclerosis in human diabetic nephropathy. Am J Kidney Dis 1997;29:912-918.
9. Strutz F, Okada H, Lo CW, Danoff T, Carone RL, Tomaszewski JE, Neilson EG: Identification and characterization of a fibroblast marker: FSP-1. J Cell Biol 1995;130:393-405.
10. Horster MF, Braun GS, Huber SM: Embryonic renal epithelia: induction, nephrogenesis, and cell differentiation. Physiol Rev 1999;79:1157-1191.
11. Valdes F, Alvarez AM, Locascio A, Vega S, Herrera B, Fernandez M, Benito M, Nieto MA, Fabregat I: The epithelial mesenchymal transition confers resistance to the apoptotic effects of transforming growth factor-beta in fetal rat hepatocytes. Mol Cancer Res 2002;1:68-78.
12. Zeisberg M, Hanai J, Sugimoto H, Mammoto T, Charytan D, Strutz F, Kalluri R: BMP-7 counteracts TGF-beta1-induced epithelial-to-mesenchymal transition and reverses chronic renal injury. Nat Med 2003;9:964-968.
13. Ng YY, Fan JM, Mu W, Nikolic-Paterson DJ, Yang WC, Huang TP, Atkins RC, Lan HY: Glomerular epithelial-myofibroblast transdifferentiation in the evolution of glomerular crescent formation. Nephrol Dial Transplant 1999;14:2860-2872.
14. Yang J, Liu Y: Blockage of tubular epithelial to myofibroblast transition by hepatocyte growth factor prevents renal interstitial fibrosis. J Am Soc Nephrol 2002;13:96-107.
15. Okada H, Danoff TM, Kalluri R, Neilson EG: Early role of FSP-1 in epithelial-mesenchymal transformation. Am J Physiol 1997;273:F563-F574.
16. Okada H, Ban S, Nagao S, Takahashi H, Suzuki H, Neilson EG: Progressive renal fibrosis in murine polycystic kidney disease: an immunohistochemical observation. Kidney Int 2000;58:587-597.
17. Okada H, Inoue T, Kanno Y, Kobayashi T, Ban S, Kalluri R, Suzuki H: Renal fibroblast-like cells in Goodpasture syndrome rats. Kidney Int 2001;60:597-606.
18. Ng YY, Huang TP, Yang WC, Chen ZP, Yang AH, Mu W, Nikolic-Paterson DJ, Atkins RC, Lan HY: Tubular epithelial-myofibroblast transdifferentiation in progressive tubulointerstitial fibrosis in 5/6 nephrectomized rats. Kidney Int 1998;54:864-876.
19. Rastaldi MP, Ferrario F, Giardino L, Dell'Antonio G, Grillo C, Grillo P, Strutz F, Muller GA, Colasanti G, D'Amico G: Epithelial-mesenchymal transition of tubular epithelial cells in human renal biopsies. Kidney Int 2002;62:137-146.
20. Oldfield MD, Bach LA, Forbes JM, Nikolic-Paterson D, McRobert A, Thallas V, Atkins RC, Osicka T, Jerums G, Cooper ME: Advanced glycation end products cause epithelial-myofibroblast transdifferentiation via the receptor for advanced glycation end products (RAGE). J Clin Invest 2001;108:1853-1863.
21. Iwano M, Plieth D, Danoff TM, Xue C, Okada H, Neilson EG: Evidence that fibroblasts derive from epithelium during tissue fibrosis. J Clin Invest 2002;110:341-350.
22. Yang J, Shultz RW, Mars WM, Wegner RE, Li Y, Dai C, Nejak K, Liu Y: Disruption of tissue-type plasminogen activator gene in mice reduces renal interstitial fibrosis in obstructive nephropathy. J Clin Invest 2002;110:1525-1538.
23. Yang J, Liu Y: Dissection of key events in tubular epithelial to myofibroblast transition and its implications in renal interstitial fibrosis. Am J Pathol 2001;159:1465-1475.
24. Fan JM, Ng YY, Hill PA, Nikolic-Paterson DJ, Mu W, Atkins RC, Lan HY: Transforming growth factor-beta regulates tubular epithelial-myofibroblast transdifferentiation in vitro. Kidney Int 1999;56:1455-1467.
25. Gore-Hyer E, Shegogue D, Markiewicz M, Lo S, Hazen-Martin D, Greene EL, Grotendorst G, Trojanowska M: TGF-beta and CTGF have overlapping and distinct fibrogenic effects on human renal cells. Am J Physiol Renal Physiol 2002;283:F707-F716.
26. Strutz F, Zeisberg M, Ziyadeh FN, Yang CQ, Kalluri R, Muller GA, Neilson EG: Role of basic fibroblast growth factor-2 in epithelial-mesenchymal transformation. Kidney Int 2002;61:1714-1728.
27. Yang J, Dai C, Liu Y: Hepatocyte growth factor gene therapy and angiotensin II blockade synergistically attenuate renal interstitial fibrosis in mice. J Am Soc Nephrol 2002;13:2464-2477.
28. Fan JM, Huang XR, Ng YY, Nikolic-Paterson DJ, Mu W, Atkins RC, Lan HY: Interleukin-1 induces tubular epithelial-myofibroblast transdifferentiation through a transforming growth factor-beta1-dependent mechanism in vitro. Am J Kidney Dis 2001;37:820-831.
29. Cheng S, Lovett DH: Gelatinase A (MMP-2) is necessary and sufficient for renal tubular cell epithelial-mesenchymal transformation. Am J Pathol 2003;162:1937-1949.
30. Bhowmick NA, Zent R, Ghiassi M, McDonnell M, Moses HL: Integrin-beta1 signaling is necessary for transforming growth factor-beta activation of p38MAPK and epithelial plasticity. J Biol Chem 2001;276:46707-46713.
31. Bhowmick NA, Ghiassi M, Bakin A, Aakre M, Lundquist CA, Engel ME, Arteaga CL, Moses HL: Transforming growth factor-beta1 mediates epithelial to mesenchymal transdifferentiation through a RhoA-dependent mechanism. Mol Biol Cell 2001;12:27-36.
32. Hartsough MT, Mulder KM: Transforming growth factor beta activation of p44MAPK in proliferating cultures of epithelial cells. J Biol Chem 1995;270:7117-7124.
33. Zavadil J, Bitzer M, Liang D, Yang YC, Massimi A, Kneitz S, Piek E, Bottinger EP: Genetic programs of epithelial cell plasticity directed by transforming growth factor-beta. Proc Natl Acad Sci USA 2001;98:6686-6691.
34. Hocevar BA, Brown TL, Howe PH: TGF-beta induces fibronectin synthesis through a c-Jun N-terminal kinase-dependent, Smad4-independent pathway. Embo J 1999;18:1345-1356.
35. Rhyu DY, Yang Y, Ha H, Lee GT, Song JS, Uh ST, Lee HB: Role of reactive oxygen species in TGF-beta1-induced mitogen-activated protein kinase activation and epithelial-mesenchymal transition in renal tubular epithelial cells. J Am Soc Nephrol 2005;16:667-675.
36. Sadlier DM, Connolly SB, Kieran NE, Roxburgh S, Brazil DP, Kairaitis L, Wang Y, Harris DC, Doran P, Brady HR: Sequential extracellular matrix-focused and baited-global cluster analysis of serial transcriptomic profiles identifies candidate modulators of renal tubulointerstitial fibrosis in murine adriamycin-induced nephropathy. J Biol Chem 2004;279:29670-29680.
37. Dudley AT, Lyons KM, Robertson EJ: A requirement for bone morphogenetic protein-7 during development of the mammalian kidney and eye. Genes Dev 1995;9:2795-2807.
38. Miyazaki Y, Oshima K, Fogo A, Hogan BL, Ichikawa I: Bone morphogenetic protein-4 regulates the budding site and elongation of the mouse ureter. J Clin Invest 2000;105:863-873.
39. Piscione TD, Yager TD, Gupta IR, Grinfeld B, Pei Y, Attisano L, Wrana JL, Rosenblum ND: BMP-2 and OP-1 exert direct and opposite effects on renal branching morphogenesis. Am J Physiol 1997;273:F961-F975.
40. Simon M, Maresh JG, Harris SE, Hernandez JD, Arar M, Olson MS, Abboud HE: Expression of bone morphogenetic protein-7 mRNA in normal and ischemic adult rat kidney. Am J Physiol 1999;276:F382-F389.
41. Wang SN, Lapage J, Hirschberg R: Loss of tubular bone morphogenetic protein-7 in diabetic nephropathy. J Am Soc Nephrol 2001;12:2392-2399.
42. 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.
43. Wang S, Chen Q, Simon TC, Strebeck F, Chaudhary L, Morrissey J, Liapis H, Klahr S, Hruska KA: Bone morphogenic protein-7 (BMP-7), a novel therapy for diabetic nephropathy. Kidney Int 2003;63:2037-2049.
44. 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.
45. 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.
46. Wang S, Hirschberg R: BMP-7 antagonizes TGF-beta-dependent fibrogenesis in mesangial cells. Am J Physiol Renal Physiol 2003;284:F1006-F1013.
47. Zeisberg M, Shah AA, Kalluri R: Bone morphogenic protein-7 induces mesenchymal to epithelial transition in adult renal fibroblasts and facilitates regeneration of injured kidney. J Biol Chem 2005;280:8094-8100.
48. Zeisberg M, Muller GA, Kalluri R: Are there endogenous molecules that protect kidneys from injury? The case for bone morphogenic protein-7 (BMP-7). Nephrol Dial Transplant 2004;19:759-761.
49. Topol LZ, Bardot B, Zhang Q, Resau J, Huillard E, Marx M, Calothy G, Blair DG: Biosynthesis, post-translation modification, and functional characterization of Drm/Gremlin. J Biol Chem 2000;275:8785-8793.
50. Lappin DW, McMahon R, Murphy M, Brady HR: Gremlin: an example of the re-emergence of developmental programmes in diabetic nephropathy. Nephrol Dial Transplant 2002;17(suppl 9):65-67.
51. Merino R, Rodriguez-Leon J, Macias D, Ganan Y, Economides AN, Hurle JM: The BMP antagonist Gremlin regulates outgrowth, chondrogenesis and programmed cell death in the developing limb. Development 1999;126:5515-5522.
52. Hsu DR, Economides AN, Wang X, Eimon PM, Harland RM: The Xenopus dorsalizing factor Gremlin identifies a novel family of secreted proteins that antagonize BMP activities. Mol Cell 1998;1:673-683.
53. Topol LZ, Marx M, Laugier D, Bogdanova NN, Boubnov NV, Clausen PA, Calothy G, Blair DG: Identification of drm, a novel gene whose expression is suppressed in transformed cells and which can inhibit growth of normal but not transformed cells in culture. Mol Cell Biol 1997;17:4801-4810.
54. Khokha MK, Hsu D, Brunet LJ, Dionne MS, Harland RM: Gremlin is the BMP antagonist required for maintenance of Shh and Fgf signals during limb patterning. Nat Genet 2003;34:303-307.
55. Michos O, Panman L, Vintersten K, Beier K, Zeller R, Zuniga A: Gremlin-mediated BMP antagonism induces the epithelial-mesenchymal feedback signaling controlling metanephric kidney and limb organogenesis. Development 2004;131:3401-3410.
56. Murphy M, Godson C, Cannon S, Kato S, Mackenzie HS, Martin F, Brady HR: Suppression subtractive hybridization identifies high glucose levels as a stimulus for expression of connective tissue growth factor and other genes in human mesangial cells. J Biol Chem 1999;274:5830-5834.
57. McMahon R, Murphy M, Clarkson M, Taal M, Mackenzie HS, Godson C, Martin F, Brady HR: IHG-2, a mesangial cell gene induced by high glucose, is human gremlin. Regulation by extracellular glucose concentration, cyclic mechanical strain, and transforming growth factor-beta1. J Biol Chem 2000;275:9901-9904.
58. Kattla J, Harno E, Dorman A, Brady H, Godson C, Brazil D: Identification of Connective Tissue Growth Factor as a potential early marker of Diabetic Nephropathy in the Goto-Kakizaki rat model of type 2 diabetes (abstract). J Am Soc Nephrol 2004;15:264A.
59. Murphy M, McMahon R, Clarkson M, Gupta S, Brady HR: Induction of gremlin expression in the remnant kidney in vivo and during TGF-beta-induced epithelial-mesenchymal transformation in vitro (abstract). J Am Soc Nephrol 2000;11:625A.
60. Dolan V, Murphy M, Sadlier D, Lappin D, Doran P, Godson C, Martin F, O'Meara Y, Schmid H, Henger A, Kretzler M, Droguett A, Mezzano S, Brady HR: Expression of gremlin, a bone morphogenetic protein antagonist, in human diabetic nephropathy. Am J Kidney Dis 2005;45:1034-1039.
61. Neilson EG: Setting a trap for tissue fibrosis. Nat Med 2005;11:373-374.
62. Abreu JG, Ketpura NI, Reversade B, De Robertis EM: Connective-tissue growth factor (CTGF) modulates cell signalling by BMP and TGF-beta. Nat Cell Biol 2002;4:599-604.
63. Roxburgh S, Kattla J, Sadlier D, O'Meara Y, Pollock C, Brazil D: Differential expression of actin cytoskeletal genes during epithelial-to- mesenchymal transition (abstract). Nephrology 2005;10:A396.
64. Lin J, Patel SR, Cheng X, Cho EA, Levitan I, Ullenbruch M, Phan SH, Park JM, Dressler GR: Kielin/chordin-like protein, a novel enhancer of BMP signaling, attenuates renal fibrotic disease. Nat Med 2005;11:387-393.
65. Wu C, Dedhar S: Integrin-linked kinase (ILK) and its interactors: a new paradigm for the coupling of extracellular matrix to actin cytoskeleton and signaling complexes. J Cell Biol 2001;155:505-510.
66. Ozdamar B, Bose R, Barrios-Rodiles M, Wang HR, Zhang Y, Wrana JL: Regulation of the polarity protein Par-6 by TGF-beta receptors controls epithelial cell plasticity. Science 2005;307:1603-1609.
67. Nagatoya K, Moriyama T, Kawada N, Takeji M, Oseto S, Murozono T, Ando A, Imai E, Hori M: Y-27632 prevents tubulointerstitial fibrosis in mouse kidneys with unilateral ureteral obstruction. Kidney Int 2002;61:1684-1695.
68. Li JH, Wang W, Huang XR, Oldfield M, Schmidt AM, Cooper ME, Lan HY: Advanced glycation end products induce tubular epithelial-myofibroblast transition through the RAGE-ERK1/2 MAP kinase signaling pathway. Am J Pathol 2004;164:1389-1397.
69. Strutz F, Heeg M, Kochsiek T, Siemers G, Zeisberg M, Muller GA: Effects of pentoxifylline, pentifylline and gamma-interferon on proliferation, differentiation, and matrix synthesis of human renal fibroblasts. Nephrol Dial Transplant 2000;15:1535-1546.
70. Liu Y, Rajur K, Tolbert E, Dworkin LD: Endogenous hepatocyte growth factor ameliorates chronic renal injury by activating matrix degradation pathways. Kidney Int 2000;58:2028-2043.