Vascular endothelial growth factor (VEGF) and its role in diabetic nephropathy

Epitheorese Klinikes Farmakologias kai Farmakokinetikes

Volumn 27, Issue 3, 2009, Pages 275-282

  Tomos, C ^a   Mironidou Tzouveleki, Maria ^a  

^a ARISTOTLE UNIVERSITY OF THESSALONIKI   (Greece)

Author keywords

Diabetic nephropathy; Vascular endothelial growth factor (VEGF)

Indexed keywords

VASCULOTROPIN;

ANGIOGENESIS; DIABETES MELLITUS; DIABETIC NEPHROPATHY; GLOMERULUS FILTRATION; HUMAN; NONHUMAN; PODOCYTE; PROTEIN EXPRESSION; PROTEINURIA; REVIEW;

EID: 74049116313     PISSN: 10116575     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (82)

1. Held P.J., Port F.K., Webb R.L., Wolfe R.A., Garcia J.R., Blagg C.R., Agodoa L.Y.: The United States Renal Data System's 1991 annual data report: an introduction. Am. J. Kidney Dis. 18: 1-16 (1991)
2. Futrakul N., Sridama V., Futrakul P.: Microalbuminuria - a biomarker of renal microvascular disease. Ren. Fail. 31: 140-143 (2009)
3. Dronavalli S., Duka I., Bakris G.L.: The pathogenesis of diabetic nephropathy. Nat. Clin. Pract. Endocrinol. Metab. 4: 444-452 (2008)
4. Mauer S.M., Steffes M.W., Ellis E.N., Sutherland D.E., Brown D.M., Goetz F.C.: Structural-functional relationships in diabetic nephropathy. J. Clin. Invest. 74: 1143-1155 (1984)
5. Osterby R., Gall M.A., Schmitz A., Nielsen F.S., Nyberg G., Parving H.H.: Glomerular structure and function in proteinuric type 2 (non-insulin-dependent) diabetic patients. Diabetologia 36: 1064-1070 (1993)
6. White K.E., Bilous R.W.: Type 2 diabetic patients with nephropathy show structural-functional relationships that are similar to type 1 disease. J. Am. Soc. Nephrol. 11: 1667-1673 (2000)
7. Salmon A.H., Neal C.R., Harper S.J.: New aspects of glomerular filtration barrier structure and function: five layers (at least) not three. Curr. Opin. Nephrol. Hypertens. 18: 197-205 (2009)
8. Satchell S.C., Tooke J.E.: What is the mechanism of microalbuminuria in diabetes: a role for the glomerular endothelium? Diabetologia 51: 714-725 (2008)
9. Houck K.A., Ferrara N., Winer J., Cachianes G., Li B., Leung D.W.: The vascular endothelial growth factor family: identification of a fourth molecular species and characterization of alternative splicing of RNA. Mol. Endocrinol. 5: 1806-1814 (1991)
10. Neufeld G., Cohen T., Gengrinovitch S., Poltorak Z.: Vascular endothelial growth factor (VEGF) and its receptors. FASEB J. 13: 9-22 (1999)
11. Carmeliet P.: Angiogenesis in health and disease. Nat. Med. 9: 653-660 (2003)
12. Ferrara N., Gerber H.P.: The role of vascular endothelial growth factor in angiogenesis. Acta Haematol. 106: 148-156 (2001)
13. Bates D.O., Cui T.G., Doughty J.M., Winkler M., Sugiono M., Shields J.D., Peat D., Gillatt D., Harper S.J.: VEGF165b, an inhibitory splice variant of vascular endothelial growth factor, is down-regulated in renal cell carcinoma. Cancer Res. 62: 4123-4131 (2002)
14. Perrin R.M., Konopatskaya O., Qiu Y., Harper S., Bates D.O., Churchill A.J.: Diabetic retinopathy is associated with a switch in splicing from anti- to pro-angiogenic isoforms of vascular endothelial growth factor. Diabetologie 48: 2422-2427 (2005)
15. Neufeld G., Cohen T., Gitay-Goren H., Poltorak Z., Tessler S., Sharon R., Gengrinovitch S., Levi B.Z.: Similarities and differences between the vascular endothelial growth factor (VEGF) splice variants. Cancer Metastasis Rev. 15: 153-158 (1996)
16. Ferrara N., Gerber H.P., LeCouter J.: The biology of VEGF and its receptors. Nat. Med. 9: 669-676 (2003)
17. Bates D.O., MacMillan P.P., Manjaly J.G., Qiu Y., Hudson S.J., Bevan H.S., Hunter A.J., Soothill P.W., Read M., Donaldson L.F., Harper S.J.: The endogenous anti-angiogenic family of splice variants of VEGF, VEGFxxxb, are down-regulated in pre-eclamptic placentae at term. Clin Sci (Lond) 110: 575-585 (2006)
18. Varey A.H., Rennel E.S., Qiu Y., Bevan H.S., Perrin R.M., Raffy S., Dixon A.R., Paraskeva C., Zaccheo O., Hassan A.B., Harper S.J., Bates D.O.: VEGF 165 b, an antiangiogenic VEGF-A isoform, binds and inhibits bevacizumab treatment in experimental colorectal carcinoma: balance of pro- and antiangiogenic VEGF-A isoforms has implications for therapy. Br. J. Cancer 98: 1366-1379 (2008)
19. Bevan H.S., van den Akker N.M., Qiu Y., Polman J.A., Foster R.R., Yem J., Nishikawa A., Satchell S.C., Harper S.J., Gittenberger-de Groot A.C., Bates D.O.: The alternatively spliced anti-angiogenic family of VEGF isoforms VEGFxxxb in human kidney development. Nephron Physiol. 110: p57-67 (2008)
20. Takahashi H., Shibuya M.: The vascular endothelial growth factor (VEGF)/VEGF receptor system and its role under physiological and pathological conditions. Clin Sci (Lond) 109: 227-241 (2005)
21. Petrova T.V., Makinen T., Alitalo K.: Signaling via vascular endothelial growth factor receptors. Exp. Cell Res. 253: 117-130 (1999)
22. Gospodarowicz D., Abraham J.A., Schilling J.: Isolation and characterization of a vascular endothelial cell mitogen produced by pituitary-derived folliculo stellate cells. Proc. Natl. Acad. Sci. U. S. A. 86: 7311-7315 (1989)
23. Kendall R.L., Thomas K.A.: Inhibition of vascular endothelial cell growth factor activity by an endogenously encoded soluble receptor. Proc. Natl. Acad. Sci. U. S. A. 90: 10705-10709 (1993)
24. Roeckl W., Hecht D., Sztajer H., Waltenberger J., Yayon A., Weich H.A.: Differential binding characteristics and cellular inhibition by soluble VEGF receptors 1 and 2. Exp. Cell Res. 241: 161-170 (1998)
25. Shweiki D., Itin A., Softer D., Keshet E.: Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis. Nature 359: 843-845 (1992)
26. Levy A.P., Levy N.S., Wegner S., Goldberg M.A.: Transcriptional regulation of the rat vascular endothelial growth factor gene by hypoxia. J. Biol. Chem. 270: 13333-13340 (1995)
27. Liu Y., Cox S.R., Morita T., Kourembanas S.: Hypoxia regulates vascular endothelial growth factor gene expression in endothelial cells. Identification of a 5′ enhancer. Circ. Res. 77: 638-643 (1995)
28. Biscetti F., Gaetani E., Flex A., Aprahamian T., Hopkins T., Straface G., Pecorini G., Stigliano E., Smith R.C., Angelini F., Castellot J.J., Jr., Pola R.: Selective activation of peroxisome proliferator-activated receptor (PPAR)alpha and PPAR gamma induces neoangiogenesis through a vascular endothelial growth factor-dependent mechanism. Diabetes 57: 1394-1404 (2008)
29. Hoshi S., Nomoto K., Kuromitsu J., Tomari S., Nagata M.: High glucose induced VEGF expression via PKC and ERK in glomerular podocytes. Biochem. Biophys. Res. Commun. 290: 177-184 (2002)
30. Feliers D., Duraisamy S., Barnes J.L., Ghosh-Choudhury G., Kasinath B.S.: Translational regulation of vascular endothelial growth factor expression in renal epithelial cells by angiotensin II. Am. J. Physiol. Renal Physiol. 288: F521-529 (2005)
31. Simon M., Rockl W., Hornig C., Grone E.F., Theis H., Weich H.A., Fuchs E., Yayon A., Grone H.J.: Receptors of vascular endothelial growth factor/vascular permeability factor (VEGF/VPF) in fetal and adult human kidney: localization and [125I]VEGF binding sites. J. Am. Soc. Nephrol. 9: 1032-1044 (1998)
32. Schrijvers B.F., Flyvbjerg A., De Vriese A.S.: The role of vascular endothelial growth factor (VEGF) in renal pathophysiology. Kidney Int. 65: 2003-2017 (2004)
33. Robert B., Zhao X., Abrahamson D.R.: Coexpression of neuropilin-1, Flk1, and VEGF(164) in developing and mature mouse kidney glomeruli. Am. J. Physiol. Renal Physiol. 279: F275-282 (2000)
34. Harper S.J., Xing C.Y., Whittle C., Parry R., Gillatt D., Peat D., Mathieson P.W.: Expression of neuropilin-1 by human glomerular epithelial cells in vitro and in vivo. Clin Sci (Lond) 101: 439-446 (2001)
35. Chen S., Kasama Y., Lee J.S., Jim B., Marin M., Ziyadeh F.N.: Podocyte-derived vascular endothelial growth factor mediates the stimulation of alpha3(IV) collagen production by transforming growth factor-beta1 in mouse podocytes. Diabetes 53: 2939-2949 (2004)
36. Ohlson M., Sorensson J., Lindstrom K., Blom A.M., Fries E., Haraldsson B.: Effects of filtration rate on the glomerular barrier and clearance of four differently shaped molecules. Am. J. Physiol. Renal Physiol. 281: F103-113 (2001)
37. Eremina V., Quaggin S.E.: The role of VEGF-A in glomerular development and function. Curr. Opin. Nephrol. Hypertens. 13: 9-15 (2004)
38. Foster R.R., Hole R., Anderson K., Satchell S.C., Coward R.J., Mathieson P.W., Gillatt D.A., Saleem M.A., Bates D.O., Harper S.J.: Functional evidence that vascular endothelial growth factor may act as an autocrine factor on human podocytes. Am. J. Physiol. Renal Physiol. 284: F1263-1273 (2003)
39. Peng H., Wang C., Ye Z.C., Chen Y.R., Zhang J., Chen Z.J., Yu X.Q., Lou T.Q.: How increased VEGF induces glomerular hyperpermeability: a potential signaling pathway of Rac1 activation. Acta Diabetol.: (2009)
40. Harhaj N.S., Antonetti O.A.: Regulation of tight junctions and loss of barrier function in pathophysiology. Int. J. Biochem. Cell Biol. 36: 1206-1237 (2004)
41. Eremina V., Cui S., Gerber H., Ferrara N., Haigh J., Nagy A., Ema M., Rossant J., Jothy S., Miner J.H., Quaggin S.E.: Vascular endothelial growth factor a signaling in the podocyte-endothelial compartment is required for mesangial cell migration and survival. J. Am. Soc. Nephrol. 17: 724-735 (2006)
42. Kitamoto Y., Tokunaga H., Tomita K.: Vascular endothelial growth factor is an essential molecule for mouse kidney development: glomerulogenesis and nephrogenesis. J. Clin. Invest. 99: 2351-2357 (1997)
43. Eremina V., Sood M., Haigh J., Nagy A., Lajoie G., Ferrara N., Gerber H.P., Kikkawa Y., Miner J.H., Quaggin S.E.: Glomerular-specific alterations of VEGF-A expression lead to distinct congenital and acquired renal diseases. J. Clin. Invest. 111: 707-716 (2003)
44. Sugimoto H., Hamano Y., Charytan D., Cosgrove D., Kieran M., Sudhakar A., Kalluri R.: Neutralization of circulating vascular endothelial growth factor (VEGF) by anti-VEGF antibodies and soluble VEGF receptor 1 (sFlt-1) induces proteinuria. J. Biol. Chem. 278: 12605-12608 (2003)
45. Maynard S.E., Min J.Y., Merchan J., Lim K.H., Li J., Mondai S., Libermann T.A., Morgan J.P., Sellke F.W., Stillman I.E., Epstein F.H., Sukhatme V.P., Karumanchi S.A.: Excess placental soluble fms-like tyrosine kinase 1 (sFlt1) may contribute to endothelial dysfunction, hypertension, and proteinuria in preeclampsia. J. Clin. Invest. 111: 649-658 (2003)
46. Greek source
47. Eremina V., Jefferson J.A., Kowalewska J., Hochster H., Haas M., Weisstuch J., Richardson C., Kopp J.B., Kabir M.G., Backx P.H., Gerber H.P., Ferrara N., Barisoni L., Alpers C.E., Quaggin S.E.: VEGF inhibition and renal thrombotic microangiopathy. N. Engl. J. Med. 358: 1129-1136 (2008)
48. Zhu X., Wu S., Dahut W.L., Parikh C.R.: Risks of proteinuria and hypertension with bevacizumab, an antibody against vascular endothelial growth factor: systematic review and meta-analysis. Am. J. Kidney Dis. 49: 186-193 (2007)
49. Ostendorf T., Kunter U., Eitner F., Loos A., Regele H., Kerjaschki D., Henninger D.D., Janjic N., Floege J.: VEGF(165) mediates glomerular endothelial repair. J. Clin. Invest. 104: 913-923 (1999)
50. Liu E., Morimoto M., Kitajima S., Koike T., Yu Y., Shiiki H., Nagata M., Watanabe T., Fan J.: Increased expression of vascular endothelial growth factor in kidney leads to progressive impairment of glomerular functions. J. Am. Soc. Nephrol. 18: 2094-2104 (2007)
51. Schumacher V.A., Jeruschke S., Eitner F., Becker J.U., Pitschke G., Ince Y., Miner J.H., Leuschner I., Engers R., Everding A.S., Bulla M., Royer-Pokora B.: Impaired glomerular maturation and lack of VEGF165b in Denys-Drash syndrome. J. Am. Soc. Nephrol. 18: 719-729 (2007)
52. Cooper M.E., Vranes D., Youssef S., Stacker S.A., Cox A.J., Rizkalla B., Casley D.J., Bach L.A., Kelly D.J., Gilbert R.E.: Increased renal expression of vascular endothelial growth factor (VEGF) and its receptor VEGFR-2 in experimental diabetes. Diabetes 48: 2229-2239 (1999)
53. Chou E., Suzuma I., Way K.J., Opland D., Clermont A.C., Naruse K., Suzuma K., Bowling N.L., Vlahos C.J., Aiello L.P., King G.L.: Decreased cardiac expression of vascular endothelial growth factor and its receptors in insulin-resistant and diabetic States: a possible explanation for impaired collateral formation in cardiac tissue. Circulation 105: 373-379 (2002)
54. de Vriese A.S., Tilton R.G., Elger M., Stephan C.C., Kriz W., Lameire N.H.: Antibodies against vascular endothelial growth factor improve early renal dysfunction in experimental diabetes. J. Am. Soc. Nephrol. 12: 993-1000 (2001)
55. Ku C.H., White K.E., Dei Cas A., Hayward A., Webster Z., Bilous R., Marshall S., Viberti G., Gnudi L.: Inducible overexpression of sFlt-1 in podocytes ameliorates glomerulopathy in diabetic mice. Diabetes 57: 2824-2833 (2008)
56. Chiarelli F., Spagnoli A., Basciani F., Tumini S., Mezzetti A., Cipollone F., Cuccurullo F., Morgese G., Verrotti A.: Vascular endothelial growth factor (VEGF) in children, adolescents and young adults with Type 1 diabetes mellitus: relation to glycaemic control and microvascular complications. Diabet. Med. 17: 650-656 (2000)
57. Hovind P., Tarnow L., Oestergaard P.B., Parving H.H.: Elevated vascular endothelial growth factor in type 1 diabetic patients with diabetic nephropathy. Kidney Int. Suppl. 75: S56-61 (2000)
58. Diamant M., Hanemaaijer R., Verheijen J.H., Smit J.W., Radder J.K., Lemkes H.H.: Elevated matrix metalloproteinase-2 and -9 in urine, but not in serum, are markers of type 1 diabetic nephropathy. Diabet. Med. 18: 423-424 (2001)
59. Malamitsi-Puchner A., Sarandakou A., Tziotis J., Dafogianni C., Bartsocas C.S.: Serum levels of basic fibroblast growth factor and vascular endothelial growth factor in children and adolescents with type 1 diabetes mellitus. Pediatr. Res. 44: 873-875 (1998)
60. Bailey E., Bottomley M.J., Westwell S., Pringle J.H., Furness P.N., Feehally J., Brenchley P.E., Harper S.J.: Vascular endothelial growth factor mRNA expression in minimal change, membranous, and diabetic nephropathy demonstrated by non-isotopic in situ hybridisation. J. Clin. Pathol. 52: 735-738 (1999)
61. Grone H.J., Simon M., Grone E.F.: Expression of vascular endothelial growth factor in renal vascular disease and renal allografts. J. Pathol. 177: 259-267 (1995)
62. Ziyadeh F.N., Hoffman B.B., Han D.C., Iglesias-De La Cruz M.C., Hong S.W., Isono M., Chen S., McGowan T.A., Sharma K.: Long-term prevention of renal insufficiency, excess matrix gene expression, and glomerular mesangial matrix expansion by treatment with monoclonal antitransforming growth factor-beta antibody in db/db diabetic mice. Proc. Natl. Acad. Sci. U. S. A. 97: 8015-8020 (2000)
63. Tsuchida K., Makita Z., Yamagishi S., Atsumi T., Miyoshi H., Obara S., Ishida M., Ishikawa S., Yasumura K., Koike T.: Suppression of transforming growth factor beta and vascular endothelial growth factor in diabetic nephropathy in rats by a novel advanced glycation end product inhibitor, OPB-9195. Diabetologia 42: 579-588 (1999)
64. Hoshi S., Shu Y., Yoshida F., Inagaki T., Sonoda J., Watanabe T., Nomoto K., Nagata M.: Podocyte injury promotes progressive nephropathy in zucker diabetic fatty rats. Lab. Invest. 82: 25-35 (2002)
65. Flyvbjerg A., Dagnaes-Hansen F., De Vriese A.S., Schrijvers B.F., Tilton R.G., Rasch R.: Amelioration of long-term renal changes in obese type 2 diabetic mice by a neutralizing vascular endothelial growth factor antibody. Diabetes 51: 3090-3094 (2002)
66. Schrijvers B.F., Flyvbjerg A., Tilton R.G., Lameire N.H., De Vriese A.S.: A neutralizing VEGF antibody prevents glomerular hypertrophy in a model of obese type 2 diabetes, the Zucker diabetic fatty rat. Nephrol. Dial. Transplant. 21: 324-329 (2006)
67. Sung S.H., Ziyadeh F.N., Wang A., Pyagay P.E., Kanwar Y.S., Chen S.: Blockade of vascular endothelial growth factor signaling ameliorates diabetic albuminuria in mice. J. Am. Soc. Nephrol. 17: 3093-3104 (2006)
68. Schrijvers B.F., De Vriese A.S., Tilton R.G., Van de Voorde J., Denner L., Lameire N.H., Flyvbjerg A.: Inhibition of vascular endothelial growth factor (VEGF) does not affect early renal changes in a rat model of lean type 2 diabetes. Horm. Metab. Res. 37: 21-25 (2005)
69. Wasada T., Kawahara R., Katsumori K., Naruse M., Omori Y.: Plasma concentration of immunoreactive vascular endothelial growth factor and its relation to smoking. Metabolism. 47: 27-30 (1998)
70. Kubisz P., Chudy P., Stasko J., Galajda P., Holly P., Vysehradsky R., Mokan M.: Circulating vascular endothelial growth factor in the normo- and/or microalbuminuric patients with type 2 diabetes mellitus. Acta Diabetol.: (2009)
71. Kim N.H., Kim K.B., Kim D.L., Kim S.G., Choi K.M., Baik S.H., Choi D.S., Kang Y.S., Han S.Y., Han K.H., Ji Y.H., Cha D.R.: Plasma and urinary vascular endothelial growth factor and diabetic nephropathy in Type 2 diabetes mellitus. Diabet. Med. 21: 545-551 (2004)
72. Kim N.H., Oh J.H., Seo J.A., Lee K.W., Kim S.G., Choi K.M., Baik S.H., Choi D.S., Kang Y.S., Han S.Y., Han K.H., Ji Y.H., Cha D.R.: Vascular endothelial growth factor (VEGF) and soluble VEGF receptor FLT-1 in diabetic nephropathy. Kidney Int. 67: 167-177 (2005)
73. Cha D.R., Kim N.H., Yoon J.W., Jo S.K., Cho W.Y., Kim H.K., Won N.H.: Role of vascular endothelial growth factor in diabetic nephropathy. Kidney Int. Suppl. 77: S104-112 (2000)
74. Hohenstein B., Hausknecht B., Boehmer K., Riess R., Brekken R.A., Hugo C.P.: Local VEGF activity but not VEGF expression is tightly regulated during diabetic nephropathy in man. Kidney Int. 69: 1654-1661 (2006)
75. Bortoloso E., Del Prete D., Dalla Vestra M., Gambaro G., Saller A., Antonucci F., Baggio B., Anglani F., Fioretto P.: Quantitave and qualitative changes in vascular endothelial growth factor gene expression in glomeruli of patients with type 2 diabetes. Eur. J. Endocrinol. 150: 799-807 (2004)
76. Lindenmeyer M.T., Kretzler M., Boucherot A., Berra S., Yasuda Y., Henger A., Eichinger F., Gaiser S., Schmid H., Rastaldi M.P., Schrier R.W., Schlondorff D., Cohen C.D.: Interstitial vascular rarefaction and reduced VEGF-A expression in human diabetic nephropathy. J. Am. Soc. Nephrol., 18: 1765-1776 (2007)
77. Baelde H.J., Eikmans M., Lappin D.W., Doran P.P., Hohenadel D., Brinkkoetter P.T., van der Woude F.J., Waldherr R., Rabelink T.J., de Heer E., Bruijn J.A.: Reduction of VEGF-A and CTGF expression in diabetic nephropathy is associated with podocyte loss. Kidney Int. 71: 637-645 (2007)
78. Breyer M.D., Bottinger E., Brosius F.C., 3rd, Coffman T.M., Harris R.C., Heilig C.W., Sharma K.: Mouse models of diabetic nephropathy. J. Am. Soc. Nephrol. 16: 27-45 (2005)
79. Banks R.E., Forbes M.A., Kinsey S.E., Stanley A., Ingham E., Walters C., Selby P.J.: Release of the angiogenic cytokine vascular endothelial growth factor (VEGF) from platelets: significance for VEGF measurements and cancer biology. Br. J. Cancer 77: 956-964 (1998)
80. Nielsen H.J., Werther K., Mynster T., Brunner N.: Soluble vascular endothelial growth factor in various blood transfusion components. Transfusion (Paris) 39: 1078-1083 (1999)
81. Woolard J., Wang W.Y., Bevan H.S., Qiu Y., Morbidelli L., Pritchard-Jones R.O., Cui T.G., Sugiono M., Waine E., Perrin R., Foster R., Digby-Bell J., Shields J.D., Whittles C.E., Mushens R.E., Gillatt D.A., Ziche M., Harper S.J., Bates D.O.: VEGF165b, an inhibitory vascular endothelial growth factor splice variant: mechanism of action, in vivo effect on angiogenesis and endogenous protein expression. Cancer Res. 64: 7822-7835 (2004)
82. Wolf G., Chen S., Ziyadeh F.N.: From the periphery of the glomerular capillary wall toward the center of disease: podocyte injury comes of age in diabetic nephropathy. Diabetes 54: 1626-1634 (2005)