Thrombospondin-1 plays a profibrotic and pro-inflammatory role during ureteric obstruction

Kidney International

Volumn 81, Issue 12, 2012, Pages 1226-1238

  Bige, Nake ^a,b   Shweke, Nasim ^a,b   Benhassine, Safa ^a,b   Jouanneau, Chantal ^a,b   Vandermeersch, Sophie ^a,b   Dussaule, Jean Claude ^a,b,c   Chatziantoniou, Christos ^a,b   Ronco, Pierre ^a,b,d   Boffa, Jean Jacques ^a,b,d  

^a INSERM   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c HÔPITAL SAINT ANTOINE   (France)

^d HÔPITAL TENON   (France)

Author keywords

Renal fibrosis; renal progression; TGF

Indexed keywords

COLLAGEN TYPE 3; MONOCYTE CHEMOTACTIC PROTEIN 1; THROMBOSPONDIN 1; TRANSFORMING GROWTH FACTOR BETA; VASCULOTROPIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; ATROPHY; CELL PROLIFERATION; CHRONIC KIDNEY DISEASE; CONTROLLED STUDY; DOWN REGULATION; GENE; GENE EXPRESSION; GLOMERULUS CAPILLARY; KIDNEY DISEASE; KIDNEY FIBROSIS; KIDNEY FUNCTION; KIDNEY PARENCHYMA; KIDNEY STRUCTURE; KIDNEY TUBULE CELL; KNOCKOUT GENE; LYMPHOCYTE ACTIVATION; MALE; NEPHRITIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; TH17 CELL; TSP 1 GENE; URETER OBSTRUCTION; WILD TYPE;

EID: 84861702734     PISSN: 00852538     EISSN: 15231755     Source Type: Journal    
DOI: 10.1038/ki.2012.21     Document Type: Article

References (51)

1. Ikoma M, Kawamura T, Kakinuma Y et al. Cause of variable therapeutic efficiency of angiotensin converting enzyme inhibitor on glomerular lesions. Kidney Int 1991; 40: 195-202.
2. Flamant M, Placier S, Rodenas A et al. Discoidin domain receptor 1 null mice are protected against hypertension-induced renal disease. J Am Soc Nephrol 2006; 17: 3374-3381. (Pubitemid 44865280)
3. Shweke N, Boulos N, Jouanneau C et al. Tissue transglutaminase contributes to interstitial renal fibrosis by favoring accumulation of fibrillar collagen through TGF-beta activation and cell infiltration. Am J Pathol 2008; 173: 631-642.
4. Flamant M, Placier S, Dubroca C et al. Role of matrix metalloproteinases in early hypertensive vascular remodeling. Hypertension 2007; 50: 212-218. (Pubitemid 46986043)
5. Chatziantoniou C, Boffa JJ, Ardaillou R et al. Nitric oxide inhibition induces early activation of type I collagen gene in renal resistance vessels and glomeruli in transgenic mice. Role of endothelin. J Clin Invest 1998; 101: 2780-2789. (Pubitemid 28294587)
6. Helle F, Jouzel C, Chadjichristos C et al. Improvement of renal hemodynamics during hypertension-induced chronic renal disease: role of EGF receptor antagonism. Am J Physiol Renal Physiol 2009; 297: F191-F199.
7. Boffa JJ, Lu Y, Placier S et al. Regression of renal vascular and glomerular fibrosis: role of angiotensin II receptor antagonism and matrix metalloproteinases. J Am Soc Nephrol 2003; 14: 1132-1144. (Pubitemid 36514656)
8. Huby AC, Rastaldi MP, Caron K et al. Restoration of podocyte structure and improvement of chronic renal disease in transgenic mice overexpressing renin. PLoS One 2009; 4: e6721.
9. Adamczak M, Gross ML, Krtil J et al. Reversal of glomerulosclerosis after high-dose enalapril treatment in subtotally nephrectomized rats. J Am Soc Nephrol 2003; 14: 2833-2842. (Pubitemid 37305646)
10. Piecha G, Koleganova N, Gross ML et al. Regression of glomerulosclerosis in subtotally nephrectomized rats: effects of monotherapy with losartan, spironolactone, and their combination. Am J Physiol Renal Physiol 2008; 295: F137-F144.
11. Ohtake T, Oka M, Maesato K et al. Pathological regression by angiotensin II type 1 receptor blockade in patients with mesangial proliferative glomerulonephritis. Hypertens Res 2008; 31: 387-394. (Pubitemid 351597490)
12. Lazzeri E, Mazzinghi B, Romagnani P. Regeneration and the kidney. Curr Opin Nephrol Hypertens 2010; 19: 248-253.
13. Menke J, Iwata Y, Rabacal WA et al. CSF-1 signals directly to renal tubular epithelial cells to mediate repair in mice. J Clin Invest 2009; 119: 2330-2334.
14. Chevalier RL, Forbes MS, Thornhill BA. Ureteral obstruction as a model of renal interstitial fibrosis and obstructive nephropathy. Kidney Int 2009; 75: 1145-1152.
15. Ito K, Chen J, El Chaar M et al. Renal damage progresses despite improvement of renal function after relief of unilateral ureteral obstruction in adult rats. Am J Physiol Renal Physiol 2004; 287: F1283-F1293. (Pubitemid 39507237)
16. Chevalier RL, Thornhill BA, Chang AY et al. Recovery from release of ureteral obstruction in the rat: relationship to nephrogenesis. Kidney Int 2002; 61: 2033-2043. (Pubitemid 34539321)
17. Koo JW, Kim Y, Rozen S et al. Enalapril accelerates remodeling of the renal interstitium after release of unilateral ureteral obstruction in rats. J Nephrol 2003; 16: 203-209. (Pubitemid 37304076)
18. Cochrane AL, Kett MM, Samuel CS et al. Renal structural and functional repair in a mouse model of reversal of ureteral obstruction. J Am Soc Nephrol 2005; 16: 3623-3623.
19. Crawford SE, Stellmach V, Murphy-Ullrich JE et al. Thrombospondin-1 is a major activator of TGF-beta1 in vivo. Cell 1998; 93: 1159-1170. (Pubitemid 28307421)
20. Isenberg JS, Martin-Manso G, Maxhimer JB et al. Regulation of nitric oxide signalling by thrombospondin 1: implications for anti-angiogenic therapies. Nat Rev Cancer 2009; 9: 182-194.
21. Carlson CB, Lawler J, Mosher DF. Structures of thrombospondins. Cell Mol Life Sci 2008; 65: 672-686.
22. Kalluri R, Neilson EG. Epithelial-mesenchymal transition and its implications for fibrosis. J Clin Invest 2003; 112: 1776-1784. (Pubitemid 38063698)
23. Tapmeier TT, Brown KL, Tang Z et al. Reimplantation of the ureter after unilateral ureteral obstruction provides a model that allows functional evaluation. Kidney Int 2008; 73: 885-889. (Pubitemid 351398288)
24. Puri TS, Shakaib MI, Chang A et al. Chronic kidney disease induced in mice by reversible unilateral ureteral obstruction is dependent on genetic background. Am J Physiol Renal Physiol 2010; 298: F1024-F1032.
25. Wada T, Furuichi K, Sakai N et al. Gene therapy via blockade of monocyte chemoattractant protein-1 for renal fibrosis. J Am Soc Nephrol 2004; 15: 940-948. (Pubitemid 38375313)
26. Nishida M, Hamaoka K. Macrophage phenotype and renal fibrosis in obstructive nephropathy. Nephron Exp Nephrol 2008; 110: e31-e36.
27. Ricardo SD, van Goor H, Eddy AA. Macrophage diversity in renal injury and repair. J Clin Invest 2008; 118: 3522-3530.
28. Lin SL, Li B, Rao S et al. Macrophage Wnt7b is critical for kidney repair and regeneration. Proc Natl Acad Sci USA 2010; 107: 4194-4199.
29. 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. (Pubitemid 38056275)
30. Pepper MS. Transforming growth factor-beta: vasculogenesis, angiogenesis, and vessel wall integrity. Cytokine Growth Factor Rev 1997; 8: 21-43. (Pubitemid 27214687)
31. Nunes I, Gleizes PE, Metz CN et al. Latent transforming growth factor-beta binding protein domains involved in activation and transglutaminasedependent cross-linking of latent transforming growth factor-beta. J Cell Biol 1997; 136: 1151-1163. (Pubitemid 27131745)
32. Ma LJ, Yang H, Gaspert A et al. Transforming growth factor-betadependent and-independent pathways of induction of tubulointerstitial fibrosis in beta6(-/-) mice. Am J Pathol 2003; 163: 1261-1273. (Pubitemid 37175076)
33. Kang DH, Joly AH, Oh SW et al. Impaired angiogenesis in the remnant kidney model: I. Potential role of vascular endothelial growth factor and thrombospondin-1. J Am Soc Nephrol 2001; 12: 1434-1447. (Pubitemid 32666326)
34. Daniel C, Schaub K, Amann K et al. Thrombospondin-1 is an endogenous activator of TGF-beta in experimental diabetic nephropathy in vivo. Diabetes 2007; 56: 2982-2989. (Pubitemid 350223633)
35. Hohenstein B, Daniel C, Hausknecht B et al. Correlation of enhanced thrombospondin-1 expression, TGF-beta signalling and proteinuria in human type-2 diabetic nephropathy. Nephrol Dial Transplant 2008; 23: 3880-3887.
36. Zhang X, Lawler J. Thrombospondin-based antiangiogenic therapy. Microvasc Res 2007; 74: 90-99. (Pubitemid 350064284)
37. Ogata Y, Ishidoya S, Fukuzaki A et al. Upregulated expression of transforming growth factor-beta, type IV collagen, and plasminogen activator inhibitor-1 mRNA are decreased after release of unilateral ureteral obstruction. Tohoku J Exp Med 2002; 197: 159-168. (Pubitemid 35378739)
38. Lawler J, Sunday M, Thibert V et al. Thrombospondin-1 is required for normal murine pulmonary homeostasis and its absence causes pneumonia. J Clin Invest 1998; 101: 982-992. (Pubitemid 28125276)
39. Kang DH, Anderson S, Kim YG et al. Impaired angiogenesis in the aging kidney: vascular endothelial growth factor and thrombospondin-1 in renal disease. Am J Kidney Dis 2001; 37: 601-611. (Pubitemid 32195301)
40. Daniel C, Wiede J, Krutzsch HC et al. Thrombospondin-1 is a major activator of TGF-beta in fibrotic renal disease in the rat in vivo. Kidney Int 2004; 65: 459-468. (Pubitemid 38130640)
41. Daniel C, Takabatake Y, Mizui M et al. Antisense oligonucleotides against thrombospondin-1 inhibit activation of tgf-beta in fibrotic renal disease in the rat in vivo. Am J Pathol 2003; 163: 1185-1192. (Pubitemid 37040154)
42. Hochegger K, Knight S, Hugo C et al. Role of thrombospondin-1 in the autologous phase of an accelerated model of anti-glomerular basement membrane glomerulonephritis. Nephron Exp Nephrol 2004; 96: e31-e38.
43. Thakar CV, Zahedi K, Revelo MP et al. Identification of thrombospondin 1 (TSP-1) as a novel mediator of cell injury in kidney ischemia. J Clin Invest 2005; 115: 3451-3459. (Pubitemid 43121833)
44. Grimbert P, Bouguermouh S, Baba N et al. Thrombospondin/CD47 interaction: a pathway to generate regulatory T cells from human CD4+ CD25T cells in response to inflammation. J Immunol 2006; 177: 3534-3541. (Pubitemid 44359884)
45. Miossec P, Korn T, Kuchroo VK. Interleukin-17 and type 17 helper T cells. N Engl J Med 2009; 361: 888-898.
46. Agah A, Kyriakides TR, Lawler J et al. The lack of thrombospondin-1 (TSP1) dictates the course of wound healing in double-TSP1/TSP2-null mice. Am J Pathol 2002; 161: 831-839. (Pubitemid 34988370)
47. Paust HJ, Turner JE, Steinmetz OM et al. The IL-23/Th17 axis contributes to renal injury in experimental glomerulonephritis. J Am Soc Nephrol 2009; 20: 969-979.
48. Yang K, Vega JL, Hadzipasic M et al. Deficiency of thrombospondin-1 reduces Th17 differentiation and attenuates experimental autoimmune encephalomyelitis. J Autoimmun 2009; 32: 94-103.
49. Lanz TV, Ding Z, Ho PP et al. Angiotensin II sustains brain inflammation in mice via TGF-beta. J Clin Invest 2010; 120: 2782-2794.
50. Shetty S, Kaushik S, Mojamdar M et al. Viability testing of homograft valves using methyl thiazol tetrazolium assay. J Postgrad Med 1996; 42: 72-75. (Pubitemid 126730142)
51. Bonheur JA, Albadawi H, Patton GM et al. A noninvasive murine model of hind limb ischemia-reperfusion injury. J Surg Res 2004; 116: 55-63. (Pubitemid 38083285)