Angiotensin II contributes to diabetic renal dysfunction in rodents and humans via notch1/snail pathway

American Journal of Pathology

Volumn 183, Issue 1, 2013, Pages 119-130

  Gagliardini, Elena ^a   Perico, Norberto ^a   Rizzo, Paola ^a   Buelli, Simona ^a   Longaretti, Lorena ^a   Perico, Luca ^a   Tomasoni, Susanna ^a   Zoja, Carla ^a   Macconi, Daniela ^a   Morigi, Marina ^a   Remuzzi, Giuseppe ^a,b   Benigni, Ariela ^a  

^a MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

^b Azienda Ospedaliera Papa Giovanni XXIII   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOTENSIN II; NEPHRIN; NOTCH1 RECEPTOR; RAMIPRIL; TRANSCRIPTION FACTOR HES 1; TRANSCRIPTION FACTOR SNAIL;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL CULTURE; CLINICAL ARTICLE; CONTROLLED STUDY; DIABETIC NEPHROPATHY; DOWN REGULATION; DRUG DOSE TITRATION; ENZYME INHIBITION; FEMALE; GENE TRANSLOCATION; GLOMERULUS FILTRATION; HUMAN; HUMAN TISSUE; HYPERTENSION; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; KIDNEY BIOPSY; KIDNEY PERFUSION; KIDNEY STRUCTURE; MALE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PODOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEINURIA; RAT; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM;

AGED; ANGIOTENSIN II; ANIMALS; CASE-CONTROL STUDIES; CELLS, CULTURED; DIABETES MELLITUS, TYPE 2; DIABETIC NEPHROPATHIES; DOWN-REGULATION; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; KIDNEY; LINEAR MODELS; MALE; MEMBRANE PROTEINS; MICROSCOPY, ELECTRON, TRANSMISSION; MIDDLE AGED; RATS; RATS, SPRAGUE-DAWLEY; RATS, ZUCKER; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTOR, NOTCH1; TRANSCRIPTION FACTORS;

EID: 84879393432     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2013.03.025     Document Type: Article

References (42)

1. S. Wild, G. Roglic, A. Green, R. Sicree, and H. King Global prevalence of diabetes: estimates for the year 2000 and projections for 2030 Diabetes Care 27 2004 1047 1053
2. M.A. Gall, K. Borch-Johnsen, P. Hougaard, F.S. Nielsen, and H.H. Parving Albuminuria and poor glycemic control predict mortality in NIDDM Diabetes 44 1995 1303 1309
3. G. Remuzzi, A. Schieppati, and P. Ruggenenti Clinical practice: nephropathy in patients with type 2 diabetes N Engl J Med 346 2002 1145 1151
4. R. Zatz, B.R. Dunn, T.W. Meyer, S. Anderson, H.G. Rennke, and B.M. Brenner Prevention of diabetic glomerulopathy by pharmacological amelioration of glomerular capillary hypertension J Clin Invest 77 1986 1925 1930
5. E. Gagliardini, S. Conti, A. Benigni, G. Remuzzi, and A. Remuzzi Imaging of the porous ultrastructure of the glomerular epithelial filtration slit J Am Soc Nephrol 21 2010 2081 2089
6. A. Remuzzi, N. Perico, C.S. Amuchastegui, B. Malanchini, M. Mazerska, C. Battaglia, T. Bertani, and G. Remuzzi Short- and long-term effect of angiotensin II receptor blockade in rats with experimental diabetes J Am Soc Nephrol 4 1993 40 49
7. R.V. Durvasula, A.T. Petermann, K. Hiromura, M. Blonski, J. Pippin, P. Mundel, R. Pichler, S. Griffin, W.G. Couser, and S.J. Shankland Activation of a local tissue angiotensin system in podocytes by mechanical strain Kidney Int 65 2004 30 39
8. W. Kriz, N. Gretz, and K.V. Lemley Progression of glomerular diseases: is the podocyte the culprit? Kidney Int 54 1998 687 697
9. H. Pavenstadt, W. Kriz, and M. Kretzler Cell biology of the glomerular podocyte Physiol Rev 83 2003 253 307
10. A. Benigni, E. Gagliardini, and G. Remuzzi Changes in glomerular perm-selectivity induced by angiotensin II imply podocyte dysfunction and slit diaphragm protein rearrangement Semin Nephrol 24 2004 131 140
11. S. Doublier, G. Salvidio, E. Lupia, V. Ruotsalainen, D. Verzola, G. Deferrari, and G. Camussi Nephrin expression is reduced in human diabetic nephropathy: evidence for a distinct role for glycated albumin and angiotensin II Diabetes 52 2003 1023 1030
12. G.I. Welsh, and M.A. Saleem The podocyte cytoskeleton: key to a functioning glomerulus in health and disease Nat Rev Nephrol 8 2012 14 21
13. E. Gagliardini, D. Corna, C. Zoja, F. Sangalli, F. Carrara, M. Rossi, S. Conti, D. Rottoli, L. Longaretti, A. Remuzzi, G. Remuzzi, and A. Benigni Unlike each drug alone, lisinopril if combined with avosentan promotes regression of renal lesions in experimental diabetes Am J Physiol Renal Physiol 297 2009 F1448 F1456
14. A. Fukuda, L.T. Wickman, M.P. Venkatareddy, Y. Sato, M.A. Chowdhury, S.Q. Wang, K.A. Shedden, R.C. Dysko, J.E. Wiggins, and R.C. Wiggins Angiotensin II-dependent persistent podocyte loss from destabilized glomeruli causes progression of end stage kidney disease Kidney Int 81 2012 40 55
15. M.X. Ilagan, and R. Kopan SnapShot: notch signaling pathway Cell 128 2007 1246
16. M. Murea, J.K. Park, S. Sharma, H. Kato, A. Gruenwald, T. Niranjan, H. Si, D.B. Thomas, J.M. Pullman, M.L. Melamed, and K. Susztak Expression of Notch pathway proteins correlates with albuminuria, glomerulosclerosis, and renal function Kidney Int 78 2010 514 522
17. T. Niranjan, B. Bielesz, A. Gruenwald, M.P. Ponda, J.B. Kopp, D.B. Thomas, and K. Susztak The Notch pathway in podocytes plays a role in the development of glomerular disease Nat Med 14 2008 290 298
18. C. Sahlgren, M.V. Gustafsson, S. Jin, L. Poellinger, and U. Lendahl Notch signaling mediates hypoxia-induced tumor cell migration and invasion Proc Natl Acad Sci U S A 105 2008 6392 6397
19. I. Matsui, T. Ito, H. Kurihara, E. Imai, T. Ogihara, and M. Hori Snail, a transcriptional regulator, represses nephrin expression in glomerular epithelial cells of nephrotic rats Lab Invest 87 2007 273 283
20. M.A. Saleem, M.J. O'Hare, J. Reiser, R.J. Coward, C.D. Inward, T. Farren, C.Y. Xing, L. Ni, P.W. Mathieson, and P. Mundel A conditionally immortalized human podocyte cell line demonstrating nephrin and podocin expression J Am Soc Nephrol 13 2002 630 638
21. R. Lapinski, N. Perico, A. Remuzzi, F. Sangalli, A. Benigni, and G. Remuzzi Angiotensin II modulates glomerular capillary permselectivity in rat isolated perfused kidney J Am Soc Nephrol 7 1996 653 660
22. D. Macconi, M. Abbate, M. Morigi, S. Angioletti, M. Mister, S. Buelli, M. Bonomelli, P. Mundel, K. Endlich, A. Remuzzi, and G. Remuzzi Permselective dysfunction of podocyte-podocyte contact upon angiotensin II unravels the molecular target for renoprotective intervention Am J Pathol 168 2006 1073 1085
23. P. Ruggenenti, P. Cravedi, M.C. Sghirlanzoni, E. Gagliardini, S. Conti, F. Gaspari, G. Marchetti, M. Abbate, and G. Remuzzi Effects of rituximab on morphofunctional abnormalities of membranous glomerulopathy Clin J Am Soc Nephrol 3 2008 1652 1659
24. E.R. Weibel Practical Methods for Biological Morphometry 1979 Academic Press Inc. London pp 40-116
25. D. Macconi, F. Sangalli, M. Bonomelli, S. Conti, L. Condorelli, E. Gagliardini, G. Remuzzi, and A. Remuzzi Podocyte repopulation contributes to regression of glomerular injury induced by ACE inhibition Am J Pathol 174 2009 797 807
26. K. Miyata, N. Ohashi, Y. Suzaki, A. Katsurada, and H. Kobori Sequential activation of the reactive oxygen species/angiotensinogen/renin-angiotensin system axis in renal injury of type 2 diabetic rats Clin Exp Pharmacol Physiol 35 2008 922 927
27. C. Zoja, S. Cattaneo, F. Fiordaliso, V. Lionetti, V. Zambelli, M. Salio, D. Corna, C. Pagani, D. Rottoli, C. Bisighini, G. Remuzzi, and A. Benigni Distinct cardiac and renal effects of ETA receptor antagonist and ACE inhibitor in experimental type 2 diabetes Am J Physiol Renal Physiol 301 2011 F1114 F1123
28. G.I. Welsh, and M.A. Saleem Nephrin-signature molecule of the glomerular podocyte? J Pathol 220 2010 328 337
29. M. Vooijs, C.T. Ong, B. Hadland, S. Huppert, Z. Liu, J. Korving, M. van den Born, T. Stappenbeck, Y. Wu, H. Clevers, and R. Kopan Mapping the consequence of Notch1 proteolysis in vivo with NIP-CRE Development 134 2007 535 544
30. B. Purow Notch inhibitors as a new tool in the war on cancer: a pathway to watch Curr Pharm Biotechnol 10 2009 154 160
31. T. Balla, P. Varnai, Y. Tian, and R.D. Smith Signaling events activated by angiotensin II receptors: what goes before and after the calcium signals Endocr Res 24 1998 335 344
32. L. Saward, and P. Zahradka Angiotensin II activates phosphatidylinositol 3-kinase in vascular smooth muscle cells Circ Res 81 1997 249 257
33. X.C. Liu, B.C. Liu, X.L. Zhang, M.X. Li, and J.D. Zhang Role of ERK1/2 and PI3-K in the regulation of CTGF-induced ILK expression in HK-2 cells Clin Chim Acta 382 2007 89 94
34. C.J. Molloy, D.S. Taylor, and H. Weber Angiotensin II stimulation of rapid protein tyrosine phosphorylation and protein kinase activation in rat aortic smooth muscle cells J Biol Chem 268 1993 7338 7345
35. J. Sadoshima, Z. Qiu, J.P. Morgan, and S. Izumo Angiotensin II and other hypertrophic stimuli mediated by G protein-coupled receptors activate tyrosine kinase, mitogen-activated protein kinase, and 90-kD S6 kinase in cardiac myocytes: the critical role of Ca(2+)-dependent signaling Circ Res 76 1995 1 15
36. Y.H. Jin, H. Kim, M. Oh, H. Ki, and K. Kim Regulation of Notch1/NICD and Hes1 expressions by GSK-3alpha/beta Mol Cells 27 2009 15 19
37. N. Perico, S.C. Amuchastegui, V. Colosio, G. Sonzogni, T. Bertani, and G. Remuzzi Evidence that an angiotensin-converting enzyme inhibitor has a different effect on glomerular injury according to the different phase of the disease at which the treatment is started J Am Soc Nephrol 5 1994 1139 1146
38. H.H. Parving, H. Lehnert, J. Brochner-Mortensen, R. Gomis, S. Andersen, and P. Arner The effect of irbesartan on the development of diabetic nephropathy in patients with type 2 diabetes N Engl J Med 345 2001 870 878
39. B.M. Brenner, M.E. Cooper, D. de Zeeuw, W.F. Keane, W.E. Mitch, H.H. Parving, G. Remuzzi, S.M. Snapinn, Z. Zhang, and S. Shahinfar Effects of losartan on renal and cardiovascular outcomes in patients with type 2 diabetes and nephropathy N Engl J Med 345 2001 861 869
40. P. Ruggenenti, A. Fassi, A.P. Ilieva, I.P. Iliev, C. Chiurchiu, N. Rubis, G. Gherardi, B. Ene-Iordache, F. Gaspari, A. Perna, P. Cravedi, A. Bossi, R. Trevisan, N. Motterlini, and G. Remuzzi Effects of verapamil added-on trandolapril therapy in hypertensive type 2 diabetes patients with microalbuminuria: the BENEDICT-B randomized trial J Hypertens 29 2011 207 216
41. P. Ruggenenti, A. Fassi, A.P. Ilieva, S. Bruno, I.P. Iliev, V. Brusegan, N. Rubis, G. Gherardi, F. Arnoldi, M. Ganeva, B. Ene-Iordache, F. Gaspari, A. Perna, A. Bossi, R. Trevisan, A.R. Dodesini, and G. Remuzzi Preventing microalbuminuria in type 2 diabetes N Engl J Med 351 2004 1941 1951
42. P. Ruggenenti, E. Perticucci, P. Cravedi, V. Gambara, M. Costantini, S.K. Sharma, A. Perna, and G. Remuzzi Role of remission clinics in the longitudinal treatment of CKD J Am Soc Nephrol 19 2008 1213 1224