Selective stimulation of VEGFR2 accelerates progressive renal disease

American Journal of Pathology

Volumn 179, Issue 1, 2011, Pages 155-166

  Sato, Waichi ^a   Tanabe, Katsuyuki ^c   Kosugi, Tomoki ^a,c   Hudkins, Kelly ^d   Lanaspa, Miguel A ^a   Zhang, Li ^a   Campbell Thompson, Martha ^a   Li, Qiuhong ^b   Long, David A ^e   Alpers, Charles E ^d   Nakagawa, Takahiko ^a,c  

^a UNIVERSITY OF FLORIDA   (United States)

^b UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF COLORADO   (United States)

^d UNIVERSITY OF WASHINGTON   (United States)

^e UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; ALPHA SMOOTH MUSCLE ACTIN; ENDOTHELIAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE; PLATELET DERIVED GROWTH FACTOR; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; VASCULOTROPIN A; VASCULOTROPIN RECEPTOR 2;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD PRESSURE REGULATION; CELL DAMAGE; CELL PROLIFERATION; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE COURSE; HUMAN; HUMAN CELL; KIDNEY DISEASE; KIDNEY INJURY; MALE; MESANGIUM CELL; MOUSE; MYOFIBROBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; UNINEPHRECTOMY;

ANIMALS; BLOTTING, WESTERN; CELLS, CULTURED; DEPENDOVIRUS; HUMANS; IMMUNOENZYME TECHNIQUES; KIDNEY DISEASES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYOFIBROBLASTS; NEOVASCULARIZATION, PATHOLOGIC; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 80052475033     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2011.03.024     Document Type: Article

References (106)

1. D.H. Kang, S. Anderson, Y.G. Kim, M. Mazzalli, S. Suga, J.A. Jefferson, K.L. Gordon, T.T. Oyama, J. Hughes, C. Hugo, D. Kerjaschki, G.F. Schreiner, and R.J. Johnson Impaired angiogenesis in the aging kidney: vascular endothelial growth factor and thrombospondin-1 in renal disease Am J Kidney Dis 37 2001 601 611
2. D.H. Kang, A.H. Joly, S.W. Oh, C. Hugo, D. Kerjaschki, K.L. Gordon, M. Mazzali, J.A. Jefferson, J. Hughes, K.M. Madsen, G.F. Schreiner, and R.J. Johnson Impaired angiogenesis in the remnant kidney model: I Potential role of vascular endothelial growth factor and thrombospondin-1 J Am Soc Nephrol 12 2001 1434 1447
3. S. Suga, Y.G. Kim, A. Joly, E. Puchacz, D.H. Kang, J.A. Jefferson, J.A. Abraham, J. Hughes, R.J. Johnson, and G.F. Schreiner Vascular endothelial growth factor (VEGF121) protects rats from renal infarction in thrombotic microangiopathy Kidney Int 60 2001 1297 1308
4. D.H. Kang, J. Hughes, M. Mazzali, G.F. Schreiner, and R.J. Johnson 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 2001 1448 1457
5. H.T. Yuan, X.Z. Li, J.E. Pitera, D.A. Long, and A.S. Woolf Peritubular capillary loss after mouse acute nephrotoxicity correlates with down-regulation of vascular endothelial growth factor-A and hypoxia-inducible factor-1 alpha Am J Pathol 163 2003 2289 2301
6. Y.G. Kim, S.I. Suga, D.H. Kang, J.A. Jefferson, M. Mazzali, K.L. Gordon, K. Matsui, S. Breiteneder-Geleff, S.J. Shankland, J. Hughes, D. Kerjaschki, G.F. Schreiner, and R.J. Johnson Vascular endothelial growth factor accelerates renal recovery in experimental thrombotic microangiopathy Kidney Int 58 2000 2390 2399
7. A. Shimizu, Y. Masuda, T. Mori, H. Kitamura, M. Ishizaki, Y. Sugisaki, and Y. Fukuda Vascular endothelial growth factor165 resolves glomerular inflammation and accelerates glomerular capillary repair in rat anti-glomerular basement membrane glomerulonephritis J Am Soc Nephrol 15 2004 2655 2665
8. A.S. de Vriese, R.G. Tilton, M. Elger, C.C. Stephan, W. Kriz, and N.H. Lameire Antibodies against vascular endothelial growth factor improve early renal dysfunction in experimental diabetes J Am Soc Nephrol 12 2001 993 1000
9. A. Flyvbjerg, F. Dagnaes-Hansen, A.S. De Vriese, B.F. Schrijvers, R.G. Tilton, and R. Rasch Amelioration of long-term renal changes in obese type 2 diabetic mice by a neutralizing vascular endothelial growth factor antibody Diabetes 51 2002 3090 3094
10. T. Nakagawa, W. Sato, Y.Y. Sautin, O. Glushakova, B. Croker, M.A. Atkinson, C.C. Tisher, and R.J. Johnson Uncoupling of vascular endothelial growth factor with nitric oxide as a mechanism for diabetic vasculopathy J Am Soc Nephrol 17 2006 736 745
11. W. Sato, T. Kosugi, L. Zhang, C.A. Roncal, M. Heinig, M. Campbell-Thompson, Y. Yuzawa, M.A. Atkinson, M.B. Grant, B.P. Croker, and T. Nakagawa The pivotal role of VEGF on glomerular macrophage infiltration in advanced diabetic nephropathy Lab Invest 88 2008 949 961
12. B. Barleon, S. Sozzani, D. Zhou, H.A. Weich, A. Mantovani, and D. Marmé Migration of human monocytes in response to vascular endothelial growth factor (VEGF) is mediated via the VEGF receptor flt-1 Blood 87 1996 3336 3343
13. S.C. Shih, M. Ju, N. Liu, and L.E. Smith Selective stimulation of VEGFR-1 prevents oxygen-induced retinal vascular degeneration in retinopathy of prematurity J Clin Invest 112 2003 50 57
14. G.H. Fong, J. Rossant, M. Gertsenstein, and M.L. Breitman Role of the Flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothelium Nature 376 1995 66 70
15. A. Kiba, H. Sagara, T. Hara, and M. Shibuya VEGFR-2-specific ligand VEGF-E induces non-edematous hyper-vascularization in mice Biochem Biophys Res Commun 301 2003 371 377
16. B. Li, A.K. Ogasawara, R. Yang, W. Wei, G.W. He, T.F. Zioncheck, S. Bunting, A.M. de Vos, and H. Jin KDR (VEGF receptor 2) is the major mediator for the hypotensive effect of VEGF Hypertension 39 2002 1095 1100
17. M.E. Cooper, D. Vranes, S. Youssef, S.A. Stacker, A.J. Cox, B. Rizkalla, D.J. Casley, L.A. Bach, D.J. Kelly, and R.E. Gilbert Increased renal expression of vascular endothelial growth factor (VEGF) and its receptor VEGFR-2 in experimental diabetes Diabetes 48 1999 2229 2239
18. T. Nakagawa Uncoupling of the VEGF-endothelial nitric oxide axis in diabetic nephropathy: an explanation for the paradoxical effects of VEGF in renal disease Am J Physiol Renal Physiol 292 2007 F1665 F1672
19. T. Nakagawa, T. Kosugi, M. Haneda, C.J. Rivard, and D.A. Long Abnormal angiogenesis in diabetic nephropathy Diabetes 58 2009 1471 1478
20. B. Li, G. Fuh, G. Meng, X. Xin, M.E. Gerritsen, B. Cunningham, and A.M. de Vos Receptor-selective variants of human vascular endothelial growth factor Generation and characterization J Biol Chem 275 2000 29823 29828
21. H.P. Gerber, A. McMurtrey, J. Kowalski, M. Yan, B.A. Keyt, V. Dixit, and N. Ferrara Vascular endothelial growth factor regulates endothelial cell survival through the phosphatidylinositol 3′-kinase/Akt signal transduction pathway Requirement for Flk-1/KDR activation J Biol Chem 273 1998 30336 30343
22. H. Gille, J. Kowalski, B. Li, J. LeCouter, B. Moffat, T.F. Zioncheck, N. Pelletier, and N. Ferrara Analysis of biological effects and signaling properties of Flt-1 (VEGFR-1) and KDR (VEGFR-2) A reassessment using novel receptor-specific vascular endothelial growth factor mutants J Biol Chem 276 2001 3222 3230
23. W. Mu, D.A. Long, X. Ouyang, A. Agarwal, P.E. Cruz, C.A. Roncal, T. Nakagawa, X. Yu, W.W. Hauswirth, and R.J. Johnson Angiostatin overexpression is associated with an improvement in chronic kidney injury by an anti-inflammatory mechanism Am J Physiol Renal Physiol 296 2009 F145 F152
24. T. Nakagawa, W. Sato, O. Glushakova, M. Heinig, T. Clarke, M. Campbell-Thompson, Y. Yuzawa, M. Atkinson, R.J. Johnson, and B. Croker Diabetic eNOS knockout mice develop advanced diabetic nephropathy J Am Soc Nephrol 18 2007 539 550
25. T. Masaki, F. Chow, D.J. Nikolic-Paterson, R.C. Atkins, and G.H. Tesch Heterogeneity of antigen expression explains controversy over glomerular macrophage accumulation in mouse glomerulonephritis Nephrol Dial Transplant 18 2003 178 181
26. Y. Yuzawa, J.R. Brentjens, J. Brett, P.R. Caldwell, C. Esposito, A. Fukatsu, G. Godman, D. Stern, and G. Andres Antibody-mediated redistribution and shedding of endothelial antigens in the rabbit J Immunol 150 1993 5633 5646
27. Working Group of the International IgA Nephropathy Network and the Renal Pathology Society I.S. Roberts, H.T. Cook, S. Troyanov, C.E. Alpers, A. Amore, and J. Barratt The Oxford classification of IgA nephropathy: pathology definitions, correlations, and reproducibility Kidney Int 76 2009 546 556
28. T. Nakayama, W. Sato, A. Yoshimura, L. Zhang, T. Kosugi, M. Campbell-Thompson, H. Kojima, B.P. Croker, and T. Nakagawa Endothelial von Willebrand factor release due to eNOS deficiency predisposes to thrombotic microangiopathy in mouse aging kidney Am J Pathol 176 2010 2198 2208
29. L.W. Wu, L.D. Mayo, J.D. Dunbar, K.M. Kessler, M.R. Baerwald, E.A. Jaffe, D. Wang, R.S. Warren, and D.B. Donner Utilization of distinct signaling pathways by receptors for vascular endothelial cell growth factor and other mitogens in the induction of endothelial cell proliferation J Biol Chem 275 2000 5096 5103
30. A. Flyvbjerg, B.F. Schrijvers, A.S. De Vriese, R.G. Tilton, and R. Rasch Compensatory glomerular growth after unilateral nephrectomy is VEGF dependent Am J Physiol Endocrinol Metab 283 2002 E362 E366
31. D. Senthil, G.G. Choudhury, C. McLaurin, and B.S. Kasinath Vascular endothelial growth factor induces protein synthesis in renal epithelial cells: a potential role in diabetic nephropathy Kidney Int 64 2003 468 479
32. C.S. Facemire, A.B. Nixon, R. Griffiths, H. Hurwitz, and T.M. Coffman Vascular endothelial growth factor receptor 2 controls blood pressure by regulating nitric oxide synthase expression Hypertension 54 2009 652 658
33. M.J. Iatropoulos, and G.M. Williams Proliferation markers Exp Toxicol Pathol 48 1996 175 181
34. R. Ohashi, A. Shimizu, Y. Masuda, H. Kitamura, M. Ishizaki, Y. Sugisaki, and N. Yamanaka Peritubular capillary regression during the progression of experimental obstructive nephropathy J Am Soc Nephrol 13 2002 1795 1805
35. J. Floege, F. Eitner, and C.E. Alpers A new look at platelet-derived growth factor in renal disease J Am Soc Nephrol 19 2008 12 23
36. V. Eremina, S. Cui, H. Gerber, N. Ferrara, J. Haigh, A. Nagy, M. Ema, J. Rossant, S. Jothy, J.H. Miner, and S.E. Quaggin Vascular endothelial growth factor a signaling in the podocyte-endothelial compartment is required for mesangial cell migration and survival J Am Soc Nephrol 17 2006 724 735
37. S. Thomas, J. Vanuystel, G. Gruden, V. Rodriguez, D. Burt, L. Gnudi, B. Hartley, and G. Viberti Vascular endothelial growth factor receptors in human mesangium in vitro and in glomerular disease J Am Soc Nephrol 11 2000 1236 1243
38. A. Pettersson, J.A. Nagy, L.F. Brown, C. Sundberg, E. Morgan, S. Jungles, R. Carter, J.E. Krieger, E.J. Manseau, V.S. Harvey, I.A. Eckelhoefer, D. Feng, A.M. Dvorak, R.C. Mulligan, and H.F. Dvorak Heterogeneity of the angiogenic response induced in different normal adult tissues by vascular permeability factor/vascular endothelial growth factor Lab Invest 80 2000 99 115
39. C. Kremer, G. Breier, W. Risau, and K.H. Plate Up-regulation of flk-1/vascular endothelial growth factor receptor 2 by its ligand in a cerebral slice culture system Cancer Res 57 1997 3852 3859
40. K.L. Hudkins, D.G. Gilbertson, M. Carling, S. Taneda, S.D. Hughes, M.S. Holdren, T.E. Palmer, S. Topouzis, A.C. Haran, A.L. Feldhaus, and C.E. Alpers Exogenous PDGF-D is a potent mesangial cell mitogen and causes a severe mesangial proliferative glomerulopathy J Am Soc Nephrol 15 2004 286 298
41. S. Hakroush, M.J. Moeller, F. Theilig, B. Kaissling, T.P. Sijmonsma, M. Jugold, A.L. Akeson, M. Traykova-Brauch, H. Hosser, B. Hhnel, H.J. Gröne, R. Koesters, and W. Kriz Effects of increased renal tubular vascular endothelial growth factor (VEGF) on fibrosis, cyst formation, and glomerular disease Am J Pathol 175 2009 1883 1895
42. S.G. Ball, C.A. Shuttleworth, and C.M. Kielty Vascular endothelial growth factor can signal through platelet-derived growth factor receptors J Cell Biol 177 2007 489 500
43. D. Veron, K.J. Reidy, C. Bertuccio, J. Teichman, G. Villegas, J. Jimenez, W. Shen, J.B. Kopp, D.B. Thomas, and A. Tufro Overexpression of VEGF-A in podocytes of adult mice causes glomerular disease Kidney Int 77 2010 989 999
44. K. Sison, V. Eremina, H. Baelde, W. Min, M. Hirashima, I.G. Fantus, and S.E. Quaggin Glomerular structure and function require paracrine, not autocrine, VEGF-VEGFR-2 signaling J Am Soc Nephrol 21 2010 1691 1701
45. M.J. Vitalone, P.J. O'Connell, E. Jimenez-Vera, A. Yuksel, M. Wavamunno, C.L. Fung, J.R. Chapman, and B.J. Nankivell Epithelial-to-mesenchymal transition in early transplant tubulointerstitial damage J Am Soc Nephrol 19 2008 1571 1583
46. J.F. Mann, R.E. Schmieder, M. McQueen, L. Dyal, H. Schumacher, J. Pogue, X. Wang, A. Maggioni, A. Budaj, S. Chaithiraphan, K. Dickstein, M. Keltai, K. Metsarinne, A. Oto, A. Parkhomenko, L.S. Piegas, T.L. Svendsen, K.K. Teo, S. Yusuf ONTARGET investigators Renal outcomes with telmisartan, ramipril, or both, in people at high vascular risk (the ONTARGET study): a multicentre, randomised, double-blind, controlled trial Lancet 372 2008 547 553
47. R.P. Brandes, F.H. Schmitz-Winnenthal, M. Félétou, A. Gödecke, P.L. Huang, P.M. Vanhoutte, I. Fleming, and R. Busse An endothelium-derived hyperpolarizing factor distinct from NO and prostacyclin is a major endothelium-dependent vasodilator in resistance vessels of wild-type and endothelial NO synthase knockout mice Proc Natl Acad Sci USA 97 2000 9747 9752
48. Y. Iwakiri, G. Cadelina, W.C. Sessa, and R.J. Groszmann Mice with targeted deletion of eNOS develop hyperdynamic circulation associated with portal hypertension Am J Physiol Gastrointest Liver Physiol 283 2002 G1074 G1081
49. S. Yang, S. Wei, A. Pozzi, and J.H. Capdevila The arachidonic acid epoxygenase is a component of the signaling mechanisms responsible for VEGF-stimulated angiogenesis Arch Biochem Biophys 489 2009 82 91
50. A.C. Webler, U.R. Michaelis, R. Popp, E. Barbosa-Sicard, A. Murugan, J.R. Falck, B. Fisslthaler, and I. Fleming Epoxyeicosatrienoic acids are part of the VEGF-activated signaling cascade leading to angiogenesis Am J Physiol Cell Physiol 295 2008 C1292 C1301
51. S. Nishimura, I. Manabe, M. Nagasaki, Y. Hosoya, H. Yamashita, H. Fujita, M. Ohsugi, K. Tobe, T. Kadowaki, R. Nagai, and S. Sugiura Adipogenesis in obesity requires close interplay between differentiating adipocytes, stromal cells, and blood vessels Diabetes 56 2007 1517 1526
52. J. Tam, D.G. Duda, J.Y. Perentes, R.S. Quadri, D. Fukumura, and R.K. Jain Blockade of VEGFR2 and not VEGFR1 can limit diet-induced fat tissue expansion: role of local versus bone marrow-derived endothelial cells PLoS One 4 2009 e4974
53. A. Pruna, N. Peyri, M. Berard, and M.C. Boffa Thrombomodulin is synthesized by human mesangial cells Kidney Int 51 1997 687 693
54. D.H. Kang, S. Anderson, Y.G. Kim, M. Mazzalli, S. Suga, J.A. Jefferson, K.L. Gordon, T.T. Oyama, J. Hughes, C. Hugo, D. Kerjaschki, G.F. Schreiner, and R.J. Johnson Impaired angiogenesis in the aging kidney: vascular endothelial growth factor and thrombospondin-1 in renal disease Am J Kidney Dis 37 2001 601 611 (Pubitemid 32195301)
55. D.H. Kang, A.H. Joly, S.W. Oh, C. Hugo, D. Kerjaschki, K.L. Gordon, M. Mazzali, J.A. Jefferson, J. Hughes, K.M. Madsen, G.F. Schreiner, and R.J. Johnson Impaired angiogenesis in the remnant kidney model: I Potential role of vascular endothelial growth factor and thrombospondin-1 J Am Soc Nephrol 12 2001 1434 1447 (Pubitemid 32666326)
56. S. Suga, Y.G. Kim, A. Joly, E. Puchacz, D.H. Kang, J.A. Jefferson, J.A. Abraham, J. Hughes, R.J. Johnson, and G.F. Schreiner Vascular endothelial growth factor (VEGF121) protects rats from renal infarction in thrombotic microangiopathy Kidney Int 60 2001 1297 1308 (Pubitemid 32960025)
57. D.H. Kang, J. Hughes, M. Mazzali, G.F. Schreiner, and R.J. Johnson 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 2001 1448 1457 (Pubitemid 32666327)
58. H.T. Yuan, X.Z. Li, J.E. Pitera, D.A. Long, and A.S. Woolf Peritubular capillary loss after mouse acute nephrotoxicity correlates with down-regulation of vascular endothelial growth factor-A and hypoxia-inducible factor-1 alpha Am J Pathol 163 2003 2289 2301 (Pubitemid 37466473)
59. Y.G. Kim, S.I. Suga, D.H. Kang, J.A. Jefferson, M. Mazzali, K.L. Gordon, K. Matsui, S. Breiteneder-Geleff, S.J. Shankland, J. Hughes, D. Kerjaschki, G.F. Schreiner, and R.J. Johnson Vascular endothelial growth factor accelerates renal recovery in experimental thrombotic microangiopathy Kidney Int 58 2000 2390 2399
60. A. Shimizu, Y. Masuda, T. Mori, H. Kitamura, M. Ishizaki, Y. Sugisaki, and Y. Fukuda Vascular endothelial growth factor165 resolves glomerular inflammation and accelerates glomerular capillary repair in rat anti-glomerular basement membrane glomerulonephritis J Am Soc Nephrol 15 2004 2655 2665 (Pubitemid 41103372)
61. A.S. de Vriese, R.G. Tilton, M. Elger, C.C. Stephan, W. Kriz, and N.H. Lameire Antibodies against vascular endothelial growth factor improve early renal dysfunction in experimental diabetes J Am Soc Nephrol 12 2001 993 1000 (Pubitemid 32378340)
62. A. Flyvbjerg, F. Dagnaes-Hansen, A.S. De Vriese, B.F. Schrijvers, R.G. Tilton, and R. Rasch Amelioration of long-term renal changes in obese type 2 diabetic mice by a neutralizing vascular endothelial growth factor antibody Diabetes 51 2002 3090 3094
63. T. Nakagawa, W. Sato, Y.Y. Sautin, O. Glushakova, B. Croker, M.A. Atkinson, C.C. Tisher, and R.J. Johnson Uncoupling of vascular endothelial growth factor with nitric oxide as a mechanism for diabetic vasculopathy J Am Soc Nephrol 17 2006 736 745
64. W. Sato, T. Kosugi, L. Zhang, C.A. Roncal, M. Heinig, M. Campbell-Thompson, Y. Yuzawa, M.A. Atkinson, M.B. Grant, B.P. Croker, and T. Nakagawa The pivotal role of VEGF on glomerular macrophage infiltration in advanced diabetic nephropathy Lab Invest 88 2008 949 961
65. B. Barleon, S. Sozzani, D. Zhou, H.A. Weich, A. Mantovani, and D. Marmé Migration of human monocytes in response to vascular endothelial growth factor (VEGF) is mediated via the VEGF receptor flt-1 Blood 87 1996 3336 3343 (Pubitemid 26115364)
66. S.C. Shih, M. Ju, N. Liu, and L.E. Smith Selective stimulation of VEGFR-1 prevents oxygen-induced retinal vascular degeneration in retinopathy of prematurity J Clin Invest 112 2003 50 57 (Pubitemid 38056375)
67. G.H. Fong, J. Rossant, M. Gertsenstein, and M.L. Breitman Role of the Flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothelium Nature 376 1995 66 70
68. A. Kiba, H. Sagara, T. Hara, and M. Shibuya VEGFR-2-specific ligand VEGF-E induces non-edematous hyper-vascularization in mice Biochem Biophys Res Commun 301 2003 371 377 (Pubitemid 36279248)
69. B. Li, A.K. Ogasawara, R. Yang, W. Wei, G.W. He, T.F. Zioncheck, S. Bunting, A.M. de Vos, and H. Jin KDR (VEGF receptor 2) is the major mediator for the hypotensive effect of VEGF Hypertension 39 2002 1095 1100 (Pubitemid 34620130)
70. M.E. Cooper, D. Vranes, S. Youssef, S.A. Stacker, A.J. Cox, B. Rizkalla, D.J. Casley, L.A. Bach, D.J. Kelly, and R.E. Gilbert Increased renal expression of vascular endothelial growth factor (VEGF) and its receptor VEGFR-2 in experimental diabetes Diabetes 48 1999 2229 2239 (Pubitemid 29521855)
71. T. Nakagawa Uncoupling of the VEGF-endothelial nitric oxide axis in diabetic nephropathy: an explanation for the paradoxical effects of VEGF in renal disease Am J Physiol Renal Physiol 292 2007 F1665 F1672 (Pubitemid 47105355)
72. T. Nakagawa, T. Kosugi, M. Haneda, C.J. Rivard, and D.A. Long Abnormal angiogenesis in diabetic nephropathy Diabetes 58 2009 1471 1478
73. B. Li, G. Fuh, G. Meng, X. Xin, M.E. Gerritsen, B. Cunningham, and A.M. de Vos Receptor-selective variants of human vascular endothelial growth factor Generation and characterization J Biol Chem 275 2000 29823 29828 (Pubitemid 32043867)
74. H.P. Gerber, A. McMurtrey, J. Kowalski, M. Yan, B.A. Keyt, V. Dixit, and N. Ferrara Vascular endothelial growth factor regulates endothelial cell survival through the phosphatidylinositol 3′-kinase/Akt signal transduction pathway Requirement for Flk-1/KDR activation J Biol Chem 273 1998 30336 30343 (Pubitemid 28545503)
75. H. Gille, J. Kowalski, B. Li, J. LeCouter, B. Moffat, T.F. Zioncheck, N. Pelletier, and N. Ferrara Analysis of biological effects and signaling properties of Flt-1 (VEGFR-1) and KDR (VEGFR-2) A reassessment using novel receptor-specific vascular endothelial growth factor mutants J Biol Chem 276 2001 3222 3230
76. W. Mu, D.A. Long, X. Ouyang, A. Agarwal, P.E. Cruz, C.A. Roncal, T. Nakagawa, X. Yu, W.W. Hauswirth, and R.J. Johnson Angiostatin overexpression is associated with an improvement in chronic kidney injury by an anti-inflammatory mechanism Am J Physiol Renal Physiol 296 2009 F145 F152
77. T. Nakagawa, W. Sato, O. Glushakova, M. Heinig, T. Clarke, M. Campbell-Thompson, Y. Yuzawa, M. Atkinson, R.J. Johnson, and B. Croker Diabetic eNOS knockout mice develop advanced diabetic nephropathy J Am Soc Nephrol 18 2007 539 550 (Pubitemid 46193319)
78. T. Masaki, F. Chow, D.J. Nikolic-Paterson, R.C. Atkins, and G.H. Tesch Heterogeneity of antigen expression explains controversy over glomerular macrophage accumulation in mouse glomerulonephritis Nephrol Dial Transplant 18 2003 178 181 (Pubitemid 36104496)
79. Y. Yuzawa, J.R. Brentjens, J. Brett, P.R. Caldwell, C. Esposito, A. Fukatsu, G. Godman, D. Stern, and G. Andres Antibody-mediated redistribution and shedding of endothelial antigens in the rabbit J Immunol 150 1993 5633 5646 (Pubitemid 23180678)
80. Working Group of the International IgA Nephropathy Network and the Renal Pathology Society I.S. Roberts, H.T. Cook, S. Troyanov, C.E. Alpers, A. Amore, and J. Barratt The Oxford classification of IgA nephropathy: pathology definitions, correlations, and reproducibility Kidney Int 76 2009 546 556
81. T. Nakayama, W. Sato, A. Yoshimura, L. Zhang, T. Kosugi, M. Campbell-Thompson, H. Kojima, B.P. Croker, and T. Nakagawa Endothelial von Willebrand factor release due to eNOS deficiency predisposes to thrombotic microangiopathy in mouse aging kidney Am J Pathol 176 2010 2198 2208
82. L.W. Wu, L.D. Mayo, J.D. Dunbar, K.M. Kessler, M.R. Baerwald, E.A. Jaffe, D. Wang, R.S. Warren, and D.B. Donner Utilization of distinct signaling pathways by receptors for vascular endothelial cell growth factor and other mitogens in the induction of endothelial cell proliferation J Biol Chem 275 2000 5096 5103 (Pubitemid 30108910)
83. A. Flyvbjerg, B.F. Schrijvers, A.S. De Vriese, R.G. Tilton, and R. Rasch Compensatory glomerular growth after unilateral nephrectomy is VEGF dependent Am J Physiol Endocrinol Metab 283 2002 E362 E366 (Pubitemid 34827453)
84. D. Senthil, G.G. Choudhury, C. McLaurin, and B.S. Kasinath Vascular endothelial growth factor induces protein synthesis in renal epithelial cells: a potential role in diabetic nephropathy Kidney Int 64 2003 468 479 (Pubitemid 36871918)
85. C.S. Facemire, A.B. Nixon, R. Griffiths, H. Hurwitz, and T.M. Coffman Vascular endothelial growth factor receptor 2 controls blood pressure by regulating nitric oxide synthase expression Hypertension 54 2009 652 658
86. M.J. Iatropoulos, and G.M. Williams Proliferation markers Exp Toxicol Pathol 48 1996 175 181 (Pubitemid 26078643)
87. R. Ohashi, A. Shimizu, Y. Masuda, H. Kitamura, M. Ishizaki, Y. Sugisaki, and N. Yamanaka Peritubular capillary regression during the progression of experimental obstructive nephropathy J Am Soc Nephrol 13 2002 1795 1805 (Pubitemid 34700604)
88. J. Floege, F. Eitner, and C.E. Alpers A new look at platelet-derived growth factor in renal disease J Am Soc Nephrol 19 2008 12 23
89. V. Eremina, S. Cui, H. Gerber, N. Ferrara, J. Haigh, A. Nagy, M. Ema, J. Rossant, S. Jothy, J.H. Miner, and S.E. Quaggin Vascular endothelial growth factor a signaling in the podocyte-endothelial compartment is required for mesangial cell migration and survival J Am Soc Nephrol 17 2006 724 735
90. S. Thomas, J. Vanuystel, G. Gruden, V. Rodriguez, D. Burt, L. Gnudi, B. Hartley, and G. Viberti Vascular endothelial growth factor receptors in human mesangium in vitro and in glomerular disease J Am Soc Nephrol 11 2000 1236 1243 (Pubitemid 30416219)
91. A. Pettersson, J.A. Nagy, L.F. Brown, C. Sundberg, E. Morgan, S. Jungles, R. Carter, J.E. Krieger, E.J. Manseau, V.S. Harvey, I.A. Eckelhoefer, D. Feng, A.M. Dvorak, R.C. Mulligan, and H.F. Dvorak Heterogeneity of the angiogenic response induced in different normal adult tissues by vascular permeability factor/vascular endothelial growth factor Lab Invest 80 2000 99 115 (Pubitemid 30067385)
92. C. Kremer, G. Breier, W. Risau, and K.H. Plate Up-regulation of flk-1/vascular endothelial growth factor receptor 2 by its ligand in a cerebral slice culture system Cancer Res 57 1997 3852 3859 (Pubitemid 27381235)
93. K.L. Hudkins, D.G. Gilbertson, M. Carling, S. Taneda, S.D. Hughes, M.S. Holdren, T.E. Palmer, S. Topouzis, A.C. Haran, A.L. Feldhaus, and C.E. Alpers Exogenous PDGF-D is a potent mesangial cell mitogen and causes a severe mesangial proliferative glomerulopathy J Am Soc Nephrol 15 2004 286 298 (Pubitemid 38140769)
94. S. Hakroush, M.J. Moeller, F. Theilig, B. Kaissling, T.P. Sijmonsma, M. Jugold, A.L. Akeson, M. Traykova-Brauch, H. Hosser, B. Hhnel, H.J. Gröne, R. Koesters, and W. Kriz Effects of increased renal tubular vascular endothelial growth factor (VEGF) on fibrosis, cyst formation, and glomerular disease Am J Pathol 175 2009 1883 1895
95. S.G. Ball, C.A. Shuttleworth, and C.M. Kielty Vascular endothelial growth factor can signal through platelet-derived growth factor receptors J Cell Biol 177 2007 489 500 (Pubitemid 46718277)
96. D. Veron, K.J. Reidy, C. Bertuccio, J. Teichman, G. Villegas, J. Jimenez, W. Shen, J.B. Kopp, D.B. Thomas, and A. Tufro Overexpression of VEGF-A in podocytes of adult mice causes glomerular disease Kidney Int 77 2010 989 999
97. K. Sison, V. Eremina, H. Baelde, W. Min, M. Hirashima, I.G. Fantus, and S.E. Quaggin Glomerular structure and function require paracrine, not autocrine, VEGF-VEGFR-2 signaling J Am Soc Nephrol 21 2010 1691 1701
98. M.J. Vitalone, P.J. O'Connell, E. Jimenez-Vera, A. Yuksel, M. Wavamunno, C.L. Fung, J.R. Chapman, and B.J. Nankivell Epithelial-to-mesenchymal transition in early transplant tubulointerstitial damage J Am Soc Nephrol 19 2008 1571 1583
99. J.F. Mann, R.E. Schmieder, M. McQueen, L. Dyal, H. Schumacher, J. Pogue, X. Wang, A. Maggioni, A. Budaj, S. Chaithiraphan, K. Dickstein, M. Keltai, K. Metsarinne, A. Oto, A. Parkhomenko, L.S. Piegas, T.L. Svendsen, K.K. Teo, S. Yusuf ONTARGET investigators Renal outcomes with telmisartan, ramipril, or both, in people at high vascular risk (the ONTARGET study): a multicentre, randomised, double-blind, controlled trial Lancet 372 2008 547 553
100. R.P. Brandes, F.H. Schmitz-Winnenthal, M. Félétou, A. Gödecke, P.L. Huang, P.M. Vanhoutte, I. Fleming, and R. Busse An endothelium-derived hyperpolarizing factor distinct from NO and prostacyclin is a major endothelium-dependent vasodilator in resistance vessels of wild-type and endothelial NO synthase knockout mice Proc Natl Acad Sci USA 97 2000 9747 9752 (Pubitemid 30650847)
101. Y. Iwakiri, G. Cadelina, W.C. Sessa, and R.J. Groszmann Mice with targeted deletion of eNOS develop hyperdynamic circulation associated with portal hypertension Am J Physiol Gastrointest Liver Physiol 283 2002 G1074 G1081 (Pubitemid 35192843)
102. S. Yang, S. Wei, A. Pozzi, and J.H. Capdevila The arachidonic acid epoxygenase is a component of the signaling mechanisms responsible for VEGF-stimulated angiogenesis Arch Biochem Biophys 489 2009 82 91
103. A.C. Webler, U.R. Michaelis, R. Popp, E. Barbosa-Sicard, A. Murugan, J.R. Falck, B. Fisslthaler, and I. Fleming Epoxyeicosatrienoic acids are part of the VEGF-activated signaling cascade leading to angiogenesis Am J Physiol Cell Physiol 295 2008 C1292 C1301 (Pubitemid 352790340)
104. S. Nishimura, I. Manabe, M. Nagasaki, Y. Hosoya, H. Yamashita, H. Fujita, M. Ohsugi, K. Tobe, T. Kadowaki, R. Nagai, and S. Sugiura Adipogenesis in obesity requires close interplay between differentiating adipocytes, stromal cells, and blood vessels Diabetes 56 2007 1517 1526 (Pubitemid 46842598)
105. J. Tam, D.G. Duda, J.Y. Perentes, R.S. Quadri, D. Fukumura, and R.K. Jain Blockade of VEGFR2 and not VEGFR1 can limit diet-induced fat tissue expansion: role of local versus bone marrow-derived endothelial cells PLoS One 4 2009 e4974
106. A. Pruna, N. Peyri, M. Berard, and M.C. Boffa Thrombomodulin is synthesized by human mesangial cells Kidney Int 51 1997 687 693 (Pubitemid 27157952)