Role of the eNOS-NO system in regulating the antiproteinuric effects of VEGF receptor 2 inhibition in diabetes

BioMed Research International

Volumn 2013, Issue , 2013, Pages

  Advani, Andrew ^a   Connelly, Kim A ^a   Advani, Suzanne L ^a   Thai, Kerri ^a   Zhang, Yuan ^b   Kelly, Darren J ^b   Gilbert, Richard E ^a  

^a ST MICHAEL'S HOSPITAL   (Canada)

^b ST VINCENT S HOSPITAL   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ENDOTHELIAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE; VANDETANIB; VASCULOTROPIN INHIBITOR; VASCULOTROPIN RECEPTOR 2; N (4 BROMO 2 FLUOROPHENYL) 6 METHOXY 7 ((1 METHYLPIPERIDIN 4 YL)METHOXY)QUINAZOLIN 4 AMINE; N-(4-BROMO-2-FLUOROPHENYL)-6-METHOXY-7-((1-METHYLPIPERIDIN-4-YL)METHOXY)QUINAZOLIN-4-AMINE; PIPERIDINE DERIVATIVE; QUINAZOLINE DERIVATIVE; VASCULOTROPIN RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIABETES MELLITUS; ENZYME ACTIVITY; GENE EXPRESSION; GLOMERULOSCLEROSIS; HYPERTENSION; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; KIDNEY INJURY; MALE; NONHUMAN; PHARMACOLOGICAL BLOCKING; PROTEIN URINE LEVEL; PROTEINURIA; RAT; SYSTOLIC BLOOD PRESSURE; URINARY EXCRETION; ANIMAL; BLOOD PRESSURE; DRUG ANTAGONISM; DRUG EFFECT; ENZYMOLOGY; EXPERIMENTAL DIABETES MELLITUS; KIDNEY; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; SYSTOLE; URINE; ANTAGONISTS AND INHIBITORS; COMPLICATION; DRUG EFFECTS;

ANIMALS; BLOOD PRESSURE; DIABETES MELLITUS, EXPERIMENTAL; HYPERTENSION; KIDNEY; MALE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; PIPERIDINES; PROTEINURIA; QUINAZOLINES; RATS; RECEPTORS, VASCULAR ENDOTHELIAL GROWTH FACTOR; SYSTOLE;

EID: 84884272553     PISSN: 23146133     EISSN: 23146141     Source Type: Journal    
DOI: 10.1155/2013/201475     Document Type: Article

References (37)

1. 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 1999 48 11 2229 2239 2-s2.0-0032712434 10.2337/diabetes.48.11.2229
2. 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. The Journal of Clinical Investigation 2003 111 5 707 716 2-s2.0-0037370325 10.1172/JCI200317423
3. 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. The New England Journal of Medicine 2008 358 11 1129 1136 2-s2.0-40849130173 10.1056/NEJMoa0707330
4. Advani A., Kelly D. J., Advani S. L., Cox A. J., Thai K., Zhang Y., White K. E., Gow R. M., Marshall S. M., Steer B. M., Marsden P. A., Rakoczy P. E., Gilbert R. E., Role of VEGF in maintaining renal structure and function under normotensive and hypertensive conditions. Proceedings of the National Academy of Sciences of the United States of America 2007 104 36 14448 14453 2-s2.0-35448963479 10.1073/pnas.0703577104
5. Izzedine H., Rixe O., Billemont B., Baumelou A., Deray G., Angiogenesis inhibitor therapies: focus on kidney toxicity and hypertension. American Journal of Kidney Diseases 2007 50 2 203 218 2-s2.0-34447635695 10.1053/j.ajkd.2007.04. 025
6. 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. Journal of the American Society of Nephrology 2006 17 11 3093 3104 2-s2.0-33750713086 10.1681/ASN.2006010064
7. Ku C.-H., White K. E., Cas A. D., 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 2008 57 10 2824 2833 2-s2.0-58149343883 10.2337/db08-0647
8. Flyvbjerg A., Dagnæs-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 2002 51 10 3090 3094 2-s2.0-0036789207
9. 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. Journal of the American Society of Nephrology 2001 12 5 993 1000 2-s2.0-0035034655
10. Oltean S., Neal C. R., Mavrou A., VEGF165b overexpression restores normal glomerular water permeability in VEGF164-overexpressing adult mice. American Journal of Physiology 2012 303 7 F1026 F1036 10.1152/ajprenal.00410.2011
11. Lin S.-L., Chang F.-C., Schrimpf C., Chen Y.-T., Wu C.-F., Wu V.-C., Chiang W.-C., Kuhnert F., Kuo C. J., Chen Y.-M., Wu K.-D., Tsai T.-J., Duffield J. S., Targeting endothelium-pericyte cross talk by inhibiting VEGF receptor signaling attenuates kidney microvascular rarefaction and fibrosis. American Journal of Pathology 2011 178 2 911 923 2-s2.0-79951816985 10.1016/j.ajpath. 2010.10.012
12. Sivaskandarajah G. A., Jeansson M., Maezawa Y., Eremina V., Baelde H. J., Quaggin S. E., Vegfa protects the glomerular microvasculature in diabetes. Diabetes 2012 61 11 2958 2966 10.2337/DB11-1655
13. Yuen D. A., Stead B. E., Zhang Y., eNOS deficiency predisposes podocytes to injury in diabetes. Journal of the American Society of Nephrology 2012 23 11 1810 1823 10.1681/ASN.2011121170
14. Facemire C. S., Nixon A. B., Griffiths R., Hurwitz H., Coffman T. M., Vascular endothelial growth factor receptor 2 controls blood pressure by regulating nitric oxide synthase expression. Hypertension 2009 54 3 652 658 2-s2.0-70349249625 10.1161/HYPERTENSIONAHA.109.129973
15. Hennequin L. F., Stokes E. S. E., Thomas A. P., Johnstone C., Plé P. A., Ogilvie D. J., Dukes M., Wedge S. R., Kendrew J., Curwen J. O., Novel 4-anilinoquinazolines with C-7 basic side chains: design and structure activity relationship of a series of potent, orally active, VEGF receptor tyrosine kinase inhibitors. Journal of Medicinal Chemistry 2002 45 6 1300 1312 2-s2.0-0037075812 10.1021/jm011022e
16. Buñag R. D., Validation in awake rats of a tail-cuff method for measuring systolic pressure. Journal of Applied Physiology 1973 34 2 279 282 2-s2.0-0015576365
17. Advani A., Huang Q., Thai K., Advani S. L., White K. E., Kelly D. J., Yuen D. A., Connelly K. A., Marsden P. A., Gilbert R. E., Long-term administration of the histone deacetylase inhibitor vorinostat attenuates renal injury in experimental diabetes through an endothelial nitric oxide synthase-dependent mechanism. American Journal of Pathology 2011 178 5 2205 2214 2-s2.0-79959209876 10.1016/j.ajpath.2011.01.044
18. Advani A., Gilbert R. E., Thai K., Gow R. M., Langham R. G., Cox A. J., Connelly K. A., Zhang Y., Herzenberg A. M., Christensen P. K., Pollock C. A., Qi W., Tan S. M., Parving H.-H., Kelly D. J., Expression, localization, and function of the thioredoxin system in diabetic nephropathy. Journal of the American Society of Nephrology 2009 20 4 730 741 2-s2.0-65249094807 10.1681/ASN.2008020142
19. +-atpase in the kidney. Hypertension 2009 54 2 261 269 2-s2.0-68549111147 10.1161/HYPERTENSIONAHA.109. 128645
20. Wu K. K., Regulation of endothelial nitric oxide synthase activity and gene expression. Annals of the New York Academy of Sciences 2002 962 122 130 2-s2.0-0036276672
21. Uy A. L., Simper N. B., Champeaux A. L., Perkins R. M., Progressive bevacizumab-associated renal thrombotic microangiopathy. NDT Plus 2009 2 1 36 39 2-s2.0-58449132320 10.1093/ndtplus/sfn168
22. Sison K., Eremina V., Baelde B., Min M., Hirashima H., Fantus F., Quaggin Q., Glomerular structure and function require paracrine, not autocrine, VEGF-VEGFR-2 signaling. Journal of the American Society of Nephrology 2010 21 10 1691 1701 10.1681/ASN.2010030295 2-s2.0-79960136604
23. Senger D. R., Galli S. J., Dvorak A. M., Perruzzi C. A., Harvey V. S., Dvorak H. F., Tumor cells secrete a vascular permeability factor that promotes accumulation of ascites fluid. Science 1983 219 4587 983 985 2-s2.0-0021111648
24. Kennedy C. R. J., What type of VEGF do you need? Journal of the American Society of Nephrology 2010 21 9 1410 1412 2-s2.0-77956507917 10.1681/ASN.2010070767
25. Kim H. W., Lim J. H., Kim M. Y., Chung S., Shin S. J., Chung H. W., Choi B. S., Kim Y.-S., Chang Y. S., Park C. W., Long-term blockade of vascular endothelial growth factor receptor-2 aggravates the diabetic renal dysfunction associated with inactivation of the Akt/eNOS-NO axis. Nephrology Dialysis Transplantation 2011 26 4 1173 1188 2-s2.0-79953862219 10.1093/ndt/gfq610
26. Komers R., Anderson S., Paradoxes of nitric oxide in the diabetic kidney. American Journal of Physiology 2003 284 6 F1121 F1137 2-s2.0-0037609623
27. Nakagawa T., Sato W., Glushakova O., Heinig M., Clarke T., Campbell-Thompson M., Yuzawa Y., Atkinson M. A., Johnson R. J., Croker B., Diabetic endothelial nitric oxide synthase knockout mice develop advanced diabetic nephropathy. Journal of the American Society of Nephrology 2007 18 2 539 550 2-s2.0-33846701668 10.1681/ASN.2006050459
28. Mohan S., Reddick R. L., Musi N., Horn D. A., Yan B., Prihoda T. J., Natarajan M., Abboud-Werner S. L., Diabetic eNOS knockout mice develop distinct macro- and microvascular complications. Laboratory Investigation 2008 88 5 515 528 2-s2.0-42549103718 10.1038/labinvest.2008.23
29. Kanetsuna Y., Takahashi K., Nagata M., Gannon M. A., Breyer M. D., Harris R. C., Takahashi T., Deficiency of endothelial nitric-oxide synthase confers susceptibility to diabetic nephropathy in nephropathy-resistant inbred mice. American Journal of Pathology 2007 170 5 1473 1484 2-s2.0-34250816918 10.2353/ajpath.2007.060481
30. Zhao H. J., Wang S., Cheng H., Zhang M.-Z., Takahashi T., Fogo A. B., Breyer M. D., Harris R. C., Endothelial nitric oxide synthase deficiency produces accelerated nephropathy in diabetic mice. Journal of the American Society of Nephrology 2006 17 10 2664 2669 2-s2.0-33749236623 10.1681/ASN.2006070798
31. Kosugi T., Nakayama T., Li Q., Chiodo V. A., Zhang L., Campbell-Thompson M., Grant M., Croker B. P., Nakagawa T., Soluble Flt-1 gene therapy ameliorates albuminuria but accelerates tubulointerstitial injury in diabetic mice. American Journal of Physiology 2010 298 3 F609 F616 2-s2.0-77649096732 10.1152/ajprenal.00377.2009
32. Ziehe M., Morbidelli L., Choudhuri R., Zhang H.-T., Donnini S., Granger H. J., Bicknell R., Nitric oxide synthase lies downstream from vascular endothelial growth factor-induced but not basic fibroblast growth factor-induced angiogenesis. The Journal of Clinical Investigation 1997 99 11 2625 2634 2-s2.0-0031008458
33. Morbidelli L., Chang C.-H. O., Douglas J. G., Granger H. J., Ledda F., Ziche M., Nitric oxide mediates mitogenic effect of VEGF on coronary venular endothelium. American Journal of Physiology 1996 270 1 H411 H415 2-s2.0-0030042761
34. Parenti A., Morbidelli L., Cui X.-L., Douglas J. G., Hood J. D., Granger H. J., Ledda F., Ziche M., Nitric oxide is an upstream signal of vascular endothelial growth factor-induced extracellular signal-regulated kinase 1/2 activation in postcapillary endothelium. Journal of Biological Chemistry 1998 273 7 4220 4226 2-s2.0-0032512822 10.1074/jbc.273.7.4220
35. Foster R. R., The importance of cellular VEGF bioactivity in the development of glomerular disease. Nephron 2009 113 1 e8 e15 2-s2.0-67649884485 10.1159/000228078
36. Nakagawa T., Uncoupling of the VEGF-endothelial nitric oxide axis in diabetic nephropathy: an explanation for the paradoxical effects of VEGF in renal disease. American Journal of Physiology 2007 292 6 F1665 F1672 2-s2.0-34447625374 10.1152/ajprenal.00495.2006
37. Advani A., Gilbert R. E., The endothelium in diabetic nephropathy. Seminars in Nephrology 2012 32 2 199 207 10.1016/j.semnephrol.2012.02.006