Heterozygous disruption of activin receptor-like kinase 1 is associated with increased renal fibrosis in a mouse model of obstructive nephropathy

Kidney International

Volumn 85, Issue 2, 2014, Pages 319-332

  Muñoz Félix, José M ^a,b   López Novoa, José M ^a,b   Martínez Salgado, Carlos ^a,b,c  

^a UNIVERSITY OF SALAMANCA   (Spain)

^b INSTITUTO DE INVESTIGACIÓN BIOMÉDICA DE SALAMANCA IBSAL   (Spain)

^c HOSPITAL UNIVERSITARIO DE SALAMANCA   (Spain)

Author keywords

ALK1; extracellular matrix; fibroblasts; fibrosis; obstructive nephropathy

Indexed keywords

ACTIVIN RECEPTOR LIKE KINASE 1; ALPHA SMOOTH MUSCLE ACTIN; CALVASCULIN; COLLAGEN TYPE 1; ENDOGLIN; FIBRONECTIN; SCLEROPROTEIN; SMAD PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL PROLIFERATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DISEASE ASSOCIATION; FIBROBLAST; GENE DISRUPTION; GENOTYPE; HAPLOINSUFFICIENCY; HETEROZYGOSITY; INTERSTITIAL NEPHRITIS; KIDNEY CELL CULTURE; KIDNEY FIBROSIS; MOUSE; MYOFIBROBLAST; NONHUMAN; OBSTRUCTIVE NEPHROPATHY; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; UNILATERAL URETERAL OBSTRUCTION;

ACTINS; ACTIVIN RECEPTORS, TYPE I; ANIMALS; BIOLOGICAL MARKERS; CELL PROLIFERATION; CELLS, CULTURED; COLLAGEN TYPE I; DISEASE MODELS, ANIMAL; EXTRACELLULAR MATRIX; FIBRONECTINS; FIBROSIS; HAPLOINSUFFICIENCY; HETEROZYGOTE; KIDNEY; KIDNEY DISEASES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYOFIBROBLASTS; S100 PROTEINS; SIGNAL TRANSDUCTION; SMAD PROTEINS; TIME FACTORS; TRANSFORMING GROWTH FACTOR BETA; URETERAL OBSTRUCTION;

EID: 84895905722     PISSN: 00852538     EISSN: 15231755     Source Type: Journal    
DOI: 10.1038/ki.2013.292     Document Type: Article

References (46)

1. Zeisberg M, Neilson EG. Mechanisms of tubulointerstitial fibrosis. J Am Soc Nephrol 2010; 21: 1819-1834
2. Grande MT, Lopez-Novoa JM. Fibroblast activation and myofibroblast generation in obstructive nephropathy. Nat Rev 2009; 5: 319-328
3. Strutz F, Zeisberg M. Renal fibroblasts and myofibroblasts in chronic kidney disease. J Am Soc Nephrol 2006; 17: 2992-2998
4. Border WA, Noble NA. TGF-beta in kidney fibrosis: A target for gene therapy. Kidney Int 1997; 51: 1388-1396
5. Lopez-Hernandez FJ, Lopez-Novoa JM. Role of TGF-beta in chronic kidney disease: An integration of tubular, glomerular and vascular effects. Cell Tissue Res 2012; 347: 141-154
6. Eddy AA. Interstitial inflammation and fibrosis in rats with diet-induced hypercholesterolemia. Kidney Int 1996; 50: 1139-1149
7. Garcia-Sanchez O, Lopez-Hernandez FJ, Lopez-Novoa JM. An integrative view on the role of TGF-beta in the progressive tubular deletion associated with chronic kidney disease. Kidney Int 2010; 77: 950-955
8. Massague J. How cells read TGF-beta signals. Nat Rev Mol Cell Biol 2000; 1: 169-178
9. Laping NJ. ALK5 inhibition in renal disease. Curr Opin Pharmacol 2003; 3: 204-208
10. Goumans MJ, Valdimarsdottir G, Itoh S et al. Balancing the activation state of the endothelium via two distinct TGF-beta type I receptors. EMBO J 2002; 21: 1743-1753
11. Lebrin F, Deckers M, Bertolino P et al. TGF-beta receptor function in the endothelium. Cardiovasc Res 2005; 65: 599-608
12. Bertolino P, Deckers M, Lebrin F et al. Transforming growth factor-beta signal transduction in angiogenesis and vascular disorders. Chest 2005; 128: 585S-590S
13. Goumans MJ, Valdimarsdottir G, Itoh S et al. Activin receptor-like kinase (ALK)1 is an antagonistic mediator of lateral TGFbeta/ALK5 signaling. Mol Cell 2003; 12: 817-828
14. Massague J, Attisano L, Wrana JL. The TGF-beta family and its composite receptors. Trends Cell Biol 1994; 4: 172-178
15. Rodriguez-Barbero A, Obreo J, Eleno N et al. Endoglin expression in human and rat mesangial cells and its upregulation by TGF-beta1. Biochem Biophys Res Commun 2001; 282: 142-147
16. Rodriguez-Pena A, Prieto M, Duwel A et al. Up-regulation of endoglin, a TGF-beta-binding protein, in rats with experimental renal fibrosis induced by renal mass reduction. Nephrol Dial Transplant 2001; 16(Suppl 1): 34-39
17. Rodriguez-Pena A, Eleno N, Duwell A et al. Endoglin upregulation during experimental renal interstitial fibrosis in mice. Hypertension 2002; 40: 713-720
18. Wang W, Koka V, Lan HY. Transforming growth factor-beta and Smad signalling in kidney diseases. Nephrology (Carlton, Vic 2005; 10: 48-56
19. Sato M, Muragaki Y, Saika S et al. Targeted disruption of TGF-beta1/Smad3 signaling protects against renal tubulointerstitial fibrosis induced by unilateral ureteral obstruction. J Clin Invest 2003; 112: 1486-1494
20. Meng XM, Huang XR, Chung AC et al. Smad2 protects against TGF-beta/Smad3-mediated renal fibrosis. J Am Soc Nephrol 2010; 21: 1477-1487
21. Wiercinska E, Wickert L, Denecke B et al. Id1 is a critical mediator in TGFbeta-induced transdifferentiation of rat hepatic stellate cells. Hepatology 2006; 43: 1032-1041
22. Pannu J, Nakerakanti S, Smith E et al. Transforming growth factor-beta receptor type I-dependent fibrogenic gene program is mediated via activation of Smad1 and ERK1/2 pathways. J Biol Chem 2007; 282: 10405-10413
23. Scharpfenecker M, Floot B, Korlaar R et al. ALK1 heterozygosity delays development of late normal tissue damage in the irradiated mouse kidney. Radiother Oncol 2011; 99: 349-355
24. Chevalier RL, Forbes MS, Thornhill BA. Ureteral obstruction as a model of renal interstitial fibrosis and obstructive nephropathy. Kidney Int 2009; 75: 1145-1152
25. Oh SP, Seki T, Goss KA et al. Activin receptor-like kinase 1 modulates transforming growth factor-beta 1 signaling in the regulation of angiogenesis. Proc Natl Acad Sci USA 2000; 97: 2626-2631
26. Truong LD, Sheikh-Hamad D, Chakraborty S et al. Cell apoptosis and proliferation in obstructive uropathy. Semin Nephrol 1998; 18: 641-651
27. Sharma AK, Mauer SM, Kim Y et al. Interstitial fibrosis in obstructive nephropathy. Kidney Int 1993; 44: 774-788
28. Wright EJ, McCaffrey TA, Robertson AP et al. Chronic unilateral ureteral obstruction is associated with interstitial fibrosis and tubular expression of transforming growth factor-beta. Lab Invest 1996; 74: 528-537
29. Sutaria PM, Ohebshalom M, McCaffrey TA et al. Transforming growth factor-beta receptor types I and II are expressed in renal tubules and are increased after chronic unilateral ureteral obstruction. Life Sci 1998; 62: 1965-1972
30. Finnson KW, Parker WL, ten Dijke P et al. ALK1 opposes ALK5/Smad3 signaling and expression of extracellular matrix components in human chondrocytes. J Bone Miner Res 2008; 23: 896-906
31. Blaney Davidson EN, Remst DF, Vitters EL et al. Increase in ALK1/ALK5 ratio as a cause for elevated MMP-13 expression in osteoarthritis in humans and mice. J Immunol 2009; 182: 7937-7945
32. Moon JA, Kim HT, Cho IS et al. IN-1130, a novel transforming growth factor-beta type I receptor kinase (ALK5) inhibitor, suppresses renal fibrosis in obstructive nephropathy. Kidney Int 2006; 70: 1234-1243
33. ten Dijke P, Hill CS. New insights into TGF-beta-Smad signalling. Trends Biochem Sci 2004; 29: 265-273
34. Massague J, Seoane J, Wotton D. Smad transcription factors. Genes Dev 2005; 19: 2783-2810
35. Lan HY. Diverse roles of TGF-beta/Smads in renal ibrosis and inflammation. Int J Biol Sci 2011; 7: 1056-1067
36. Datto MB, Frederick JP, Pan L et al. Targeted disruption of Smad3 reveals an essential role in transforming growth factor beta-mediated signal transduction. Mol Cell Biol 1999; 19: 2495-2504
37. Manson SR, Niederhoff RA, Hruska KA et al. The BMP-7-Smad1/5/8 pathway promotes kidney repair after obstruction induced renal injury. J Urol 2011; 185: 2523-2530
38. Zeisberg M, Hanai J, Sugimoto H et al. BMP-7 counteracts TGF-beta1-induced epithelial-To-mesenchymal transition and reverses chronic renal injury. Nat Med 2003; 9: 964-968
39. Morris E, Chrobak I, Bujor A et al. Endoglin promotes TGF-beta/Smad1 signaling in scleroderma fibroblasts. J Cell Physiol 2011; 226: 3340-3348
40. Laping NJ, Grygielko E, Mathur A et al. Inhibition of transforming growth factor (TGF)-beta1-induced extracellular matrix with a novel inhibitor of the TGF-beta type I receptor kinase activity: SB-431542. Mol Pharmacol 2002; 62: 58-64
41. Scherner O, Meurer SK, Tihaa L et al. Endoglin differentially modulates antagonistic transforming growth factor-beta1 and BMP-7 signaling. J Biol Chem 2007; 282: 13934-13943
42. Rodriguez-Pena AB, Grande MT, Eleno N et al. Activation of Erk1/2 and Akt following unilateral ureteral obstruction. Kidney Int 2008; 74: 196-209
43. Muller GA, Markovic-Lipkovski J, Frank J et al. The role of interstitial cells in the progression of renal diseases. J Am Soc Nephrol 1992; 2: S198-S205
44. Nagatoya K, Moriyama T, Kawada N et al. Y-27632 prevents tubulointerstitial fibrosis in mouse kidneys with unilateral ureteral obstruction. Kidney Int 2002; 61: 1684-1695
45. Sharpe CC, Dockrell ME, Noor MI et al. Role of Ras isoforms in the stimulated proliferation of human renal fibroblasts in primary culture. J Am Soc Nephrol 2000; 11: 1600-1606
46. Grande MT, Fuentes-Calvo I, Arevalo M et al. Deletion of H-Ras decreases renal fibrosis and myofibroblast activation following ureteral obstruction in mice. Kidney Int 2010; 77: 509-518