Thrombospondin 2 functions as an endogenous regulator of angiogenesis and inflammation in experimental glomerulonephritis in mice

Journal of the American Society of Nephrology

Volumn 18, Issue 3, 2007, Pages 788-798

  Daniel, Christoph ^a   Amann, Kerstin ^a   Hohenstein, Bernd ^a   Bornstein, Paul ^b   Hugo, Christian ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; CD4 ANTIGEN; CD8ALPHA ANTIGEN; COLLAGEN TYPE 1; COLLAGEN TYPE 4; FIBRIN; GELATINASE A; GLOMERULUS BASEMENT MEMBRANE ANTIBODY; SMAD2 PROTEIN; SMAD3 PROTEIN; THROMBOSPONDIN 1; THROMBOSPONDIN 2; TRANSFORMING GROWTH FACTOR BETA;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CAPILLARY; CELL DEATH; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVITY; EXTRACELLULAR MATRIX; GLOMERULONEPHRITIS; IMMUNE RESPONSE; INFLAMMATION; INFLAMMATORY CELL; KIDNEY CORTEX; KIDNEY FUNCTION; KIDNEY INJURY; KIDNEY INTERSTITIUM; KIDNEY TUBULE; MACROPHAGE; MONOCYTE; MOUSE; NEPHRITIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; STAINING; UPREGULATION; WILD TYPE;

EID: 33947275633     PISSN: 10466673     EISSN: None     Source Type: Journal    
DOI: 10.1681/ASN.2006080873     Document Type: Article

References (36)

1. Bornstein P: Thrombospondins as matricellular modulators of cell function. J Clin Invest 107: 929-934, 2001
2. Yang Z, Strickland DK, Bornstein P: Extracellular matrix metalloproteinase 2 levels are regulated by the low density lipoprotein-related scavenger receptor and thrombospondin 2. J Biol Chem 276: 8403-8408, 2001
3. Iruela-Arispe ML, Liska DJ, Sage EH, Bornstein P: Differential expression of thrombospondin 1, 2, and 3 during murine development. Dev Dyn 197: 40-56, 1993
4. Kyriakides TR, Zhu YH, Smith LT, Bain SD, Yang Z, Lin MT, Danielson KG, Iozzo RV, LaMarca M, McKinney CE, Ginns EI, Bornstein P: Mice that lack thrombospondin 2 display connective tissue abnormalities that are associated with disordered collagen fibrillogenesis, an increased vascular density, and a bleeding diathesis. J Cell Biol 140: 419-430, 1998
5. Kyriakides TR, Zhu YH, Yang Z, Huynh G, Bornstein P: Altered extracellular matrix remodeling and angiogenesis in sponge granulomas of thrombospondin 2-null mice. Am J Pathol 159: 1255-1262, 2001
6. Lange-Asschenfeldt B, Weninger W, Velasco P, Kyriakides TR, von Andrian UH, Bornstein P, Detmar M: Increased and prolonged inflammation and angiogenesis in delayed-type hypersensitivity reactions elicited in the skin of thrombospondin-2-deficient mice. Blood 99: 538-545, 2002
7. Kyriakides TR, Tam JW, Bornstein P: Accelerated wound healing in mice with a disruption of the thrombospondin 2 gene. J Invest Dermatol 113: 782-787, 1999
8. Streit M, Riccardi L, Velasco P, Brown LF, Hawighorst T, Bornstein P, Detmar M: Thrombospondin-2: A potent endogenous inhibitor of tumor growth and angiogenesis. Proc Natl Acad Sci U S A 96: 14888-14893, 1999
9. Park YW, Kang YM, Butterfield J, Detmar M, Goronzy JJ, Weyand CM: Thrombospondin 2 functions as an endogenous regulator of angiogenesis and inflammation in rheumatoid arthritis. Am J Pathol 165: 2087-2098, 2004
10. Daniel C, Takabatake Y, Mizui M, Isaka Y, Kawashi H, Rupprecht H, Imai E, Hugo C: Antisense oligonucleotides against thrombospondin-1 inhibit activation of TGF-beta in fibrotic renal disease in the rat in vivo. Am J Pathol 163: 1185-1192, 2003
11. Daniel C, Wiede J, Krutzsch HC, Ribeiro SM, Roberts DD, Murphy-Ullrich JE, Hugo C: Thrombospondin-1 is a major activator of TGF-beta in fibrotic renal disease in the rat in vivo. Kidney Int 65: 459-468, 2004
12. Schultz-Cherry S, Chen H, Mosher DF, Misenheimer TM, Krutzsch HC, Roberts DD, Murphy-Ullrich JE: Regulation of transforming growth factor-beta activation by discrete sequences of thrombospondin 1. J Biol Chem 270: 7304-7310, 1995
13. Kang DH, Kanellis J, Hugo C, Truong L, Anderson S, Kerjaschki D, Schreiner GF, Johnson RJ: Role of the microvascular endothelium in progressive renal disease. J Am Soc Nephrol 13: 806-816, 2002
14. Iruela-Arispe L, Gordon K, Hugo C, Duijvestijn AM, Claffey KP, Reilly M, Couser WG, Alpers CE, Johnson RJ: Participation of glomerular endothelial cells in the capillary repair of glomerulonephritis. Am J Pathol 147: 1715-1727, 1995
15. Kim YG, Suga SI, Kang DH, Jefferson JA, Mazzali M, Gordon KL, Matsui K, Breiteneder-Geleff S, Shankland SJ, Hughes J, Kerjaschki D, Schreiner GF, Johnson RJ: Vascular endothelial growth factor accelerates renal recovery in experimental thrombotic microangiopathy. Kidney Int 58: 2390-2399, 2000
16. Masuda Y, Shimizu A, Mori T, Ishiwata T, Kitamura H, Ohashi R, Ishizaki M, Asano G, Sugisaki Y, Yamanaka N: Vascular endothelial growth factor enhances glomerular capillary repair and accelerates resolution of experimentally induced glomerulonephritis. Am J Pathol 159: 599-608, 2001
17. Ostendorf T, Kunter U, Eitner F, Loos A, Regele H, Kerjaschki D, Henninger DD, Janjic N, Floege J: VEGF(165) mediates glomerular endothelial repair. J Clin Invest 104: 913-923, 1999
18. Hohenstein B, Kasperek L, Kobelt DJ, Daniel C, Gambaryan S, Renne T, Walter U, Amann KU, Hugo CP: Vasodilator-stimulated phosphoprotein-deficient mice demonstrate increased platelet activation but improved renal endothelial preservation and regeneration in passive nephrotoxic nephritis. J Am Soc Nephrol 16: 986-996, 2005
19. Reinders ME, Rabelink TJ, Briscoe DM: Angiogenesis and endothelial cell repair in renal disease and allograft rejection. J Am Soc Nephrol 17: 932-942, 2006
20. Ophascharoensuk V, Fero ML, Hughes J, Roberts JM, Shankland SJ: The cyclin-dependent kinase inhibitor p27Kip1 safeguards against inflammatory injury. Nat Med 4: 575-580, 1998
21. Hugo C, Shankland SJ, Bowen-Pope DF, Couser WG, Johnson RJ: Extraglomerular origin of the mesangial cell after injury. A new role of the juxtaglomerular apparatus. J Clin Invest 100: 786-794, 1997
22. Mihatsch MJ, Bremer J: Acid fuchsin orange G-stain (AFOG) for glomerular protein deposits. Clin Nephrol 9: 259, 1978
23. Kyriakides TR, Zhu YH, Yang Z, Bornstein P: The distribution of the matricellular protein thrombospondin 2 in tissues of embryonic and adult mice. J Histochem Cytochem 46: 1007-1015, 1998
24. Shih W, Hines WH, Neilson EG: Effects of cyclosporin A on the development of immune-mediated interstitial nephritis. Kidney Int 33: 1113-1118, 1988
25. Hughes J, Johnson RJ, Mooney A, Hugo C, Gordon K, Savill J: Neutrophil fate in experimental glomerular capillary injury in the rat. Emigration exceeds in situ clearance by apoptosis. Am J Pathol 150: 223-234, 1997
26. Bornstein P, Agah A, Kyriakides TR: The role of thrombospondins 1 and 2 in the regulation of cell-matrix interactions, collagen fibril formation, and the response to injury. Int J Biochem Cell Biol 36: 1115-1125, 2004
27. Armstrong LC, Bjorkblom B, Hankenson KD, Siadak AW, Stiles CE, Bornstein P: Thrombospondin 2 inhibits microvascular endothelial cell proliferation by a caspase-independent mechanism. Mol Biol Cell 13: 1893-1905, 2002
28. Ohashi R, Kitamura H, Yamanaka N: Peritubular capillary injury during the progression of experimental glomerulonephritis in rats. J Am Soc Nephrol 11: 47-56, 2000
29. Kang DH, Anderson S, Kim YG, Mazzalli M, Suga S, Jefferson JA, Gordon KL, Oyama TT, Hughes J, Hugo C, Kerjaschki D, Schreiner GF, Johnson RJ: Impaired angiogenesis in the aging kidney: Vascular endothelial growth factor and thrombospondin-1 in renal disease. Am J Kidney Dis 37: 601-611, 2001
30. Kang DH, Joly AH, Oh SW, Hugo C, Kerjaschki D, Gordon KL, Mazzali M, Jefferson JA, Hughes J, Madsen KM, Schreiner GF, Johnson RJ: Impaired angiogenesis in the remnant kidney model: I. Potential role of vascular endothelial growth factor and thrombospondin-1. J Am Soc Nephrol 12: 1434-1447, 2001
31. Thomas SE, Anderson S, Gordon KL, Oyama TT, Shankland SJ, Johnson RJ: Tubulointerstitial disease in aging: Evidence for underlying peritubular capillary damage, a potential role for renal ischemia. J Am Soc Nephrol 9: 231-242, 1998
32. Kang DH, Hughes J, Mazzali M, Schreiner GF, Johnson RJ: Impaired angiogenesis in the remnant kidney model: II. Vascular endothelial growth factor administration reduces renal fibrosis and stabilizes renal function. J Am Soc Nephrol 12: 1448-1457, 2001
33. Armstrong LC, Bornstein P: Thrombospondins 1 and 2 function as inhibitors of angiogenesis. Matrix Biol 22: 63-71, 2003
34. Cheng S, Pollock AS, Mahimkar R, Olson JL, Lovett DH: Matrix metalloproteinase 2 and basement membrane integrity: A unifying mechanism for progressive renal injury. FASEB J 20: 1898-1900, 2006
35. Cheng S, Lovett DH: Gelatinase A (MMP-2) is necessary and sufficient for renal tubular cell epithelial-mesenchymal transformation. Am J Pathol 162: 1937-1949, 2003
36. Schroen B, Heymans S, Sharma U, Blankesteijn WM, Pokharel S, Cleutjens JP, Porter JG, Evelo CT, Duisters R, van Leeuwen RE, Janssen BJ, Debets JJ, Smits JF, Daemen MJ, Crijns HJ, Bornstein P, Pinto YM: Thrombospondin-2 is essential for myocardial matrix integrity: Increased expression identifies failure-prone cardiac hypertrophy. Circ Res 95: 515-522, 2004