Targeting the renin angiotensin system for remission/regression of chronic kidney disease

Histology and Histopathology

Volumn 25, Issue 5, 2010, Pages 655-668

  Macconi, Daniela ^a  

^a MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

Author keywords

Angiotensin II; Chronic kidney disease; RAS blockade; Regression; Remission

Indexed keywords

ANGIOTENSIN 1 RECEPTOR ANTAGONIST; ANGIOTENSIN II; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR;

ANIMAL; BIOLOGICAL MODEL; CHRONIC KIDNEY FAILURE; DIABETIC NEPHROPATHY; DRUG ANTAGONISM; DRUG COMBINATION; DRUG EFFECT; FOCAL GLOMERULOSCLEROSIS; HUMAN; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; PROTEINURIA; REMISSION; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; RENOVASCULAR HYPERTENSION; REVIEW;

ANGIOTENSIN II; ANGIOTENSIN II TYPE 1 RECEPTOR BLOCKERS; ANGIOTENSIN-CONVERTING ENZYME INHIBITORS; ANIMALS; DIABETIC NEPHROPATHIES; DRUG THERAPY, COMBINATION; GLOMERULOSCLEROSIS, FOCAL SEGMENTAL; HUMANS; HYPERTENSION, RENAL; MODELS, BIOLOGICAL; PROTEINURIA; REMISSION INDUCTION; RENAL INSUFFICIENCY, CHRONIC; RENIN-ANGIOTENSIN SYSTEM;

EID: 77953043650     PISSN: 02133911     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (133)

1. Abbate M., Zoja C., Rottoli D., Corna D., Perico N., Bertani T. and Remuzzi G. (1999). Antiproteinuric therapy while preventing the abnormal protein traffic in proximal tubule abrogates protein- and complement-dependent interstitial inflammation in experimental renal disease. J. Am. Soc. Nephrol. 10, 804-813.
2. Abbate M., Zoja C., Morigi M., Rottoli D., Angioletti S., Tomasoni S., Zanchi C., Longaretti L., Donadelli R. and Remuzzi G. (2002). Transforming growth factor-beta1 is up-regulated by podocytes in response to excess intraglomerular passage of proteins: a central pathway in progressive glomerulosclerosis. Am. J. Pathol. 161, 2179-2193.
3. Abbate M., Zoja C. and Remuzzi G. (2006). How does proteinuria cause progressive renal damage? J. Am. Soc. Nephrol. 17, 2974-2984.
4. Adamczak M., Gross M.L., Amann K. and Ritz E. (2004). Reversal of glomerular lesions involves coordinated restructuring of glomerular microvasculature. J. Am. Soc. Nephrol. 15, 3063-3072.
5. Adamczak M., Gross M.L., Krtil J., Koch A., Tyralla K., Amann K. and Ritz E. (2003). Reversal of glomerulosclerosis after high-dose enalapril treatment in subtotally nephrectomized rats. J. Am. Soc. Nephrol. 14, 2833-2842.
6. Agarwal R. (2001). Add-on angiotensin receptor blockade with maximized ACE inhibition. Kidney Int. 59, 2282-2289.
7. Anderson P.W., Do Y.S. and Hsueh W.A. (1993). Angiotensin II causes mesangial cell hypertrophy. Hypertension 21, 29-35.
8. Appel D., Kershaw D.B., Smeets B., Yuan G., Fuss A., Frye B., Elger M., Kriz W., Floege J. and Moeller M.J. (2009). Recruitment of podocytes from glomerular parietal epithelial cells. J. Am. Soc. Nephrol. 20, 333-343.
9. Bariety J., Mandet C., Hill G.S. and Bruneval P. (2006). Parietal podocytes in normal human glomeruli. J. Am. Soc. Nephrol. 17, 2770-2780.
10. Benigni A., Gagliardini E., Remuzzi A., Corna D. and Remuzzi G. (2001a). Angiotensin-converting enzyme inhibition prevents glomerular-tubule disconnection and atrophy in passive Heymann nephritis, an effect not observed with a calcium antagonist. Am. J. Pathol. 159, 1743-1750.
11. Benigni A., Tomasoni S., Gagliardini E., Zoja C., Grunkemeyer J.A., Kalluri R. and Remuzzi G. (2001b). Blocking angiotensin II synthesis/activity preserves glomerular nephrin in rats with severe nephrosis. J. Am. Soc. Nephrol. 12, 941-948.
12. Benigni A., Corna D., Zoja C., Longaretti L., Gagliardini E., Perico N., Coffman T.M. and Remuzzi G. (2004). Targeted deletion of angiotensin II type 1A receptor does not protect mice from progressive nephropathy of overload proteinuria. J. Am. Soc. Nephrol. 15, 2666-2674.
13. Bjorck S., Mulec H., Johnsen S.A., Norden G. and Aurell M. (1992). Renal protective effect of enalapril in diabetic nephropathy. BMJ 304, 339-343.
14. Boffa J.J., Lu Y., Placier S., Stefanski A., Dussaule J.C. and Chatziantoniou C. (2003). Regression of renal vascular and glomerular fibrosis: role of angiotensin II receptor antagonism and matrix metalloproteinases. J. Am. Soc. Nephrol. 14, 1132-1144.
15. Bonnet F., Cooper M.E., Kawachi H., Allen T.J., Boner G. and Cao Z. (2001). Irbesartan normalises the deficiency in glomerular nephrin expression in a model of diabetes and hypertension. Diabetologia 44, 874-877.
16. Brenner B.M., Meyer T.W. and Hostetter T.H. (1982). Dietary protein intake and the progressive nature of kidney disease: the role of hemodynamically mediated glomerular injury in the pathogenesis of progressive glomerular sclerosis in aging, renal ablation, and intrinsic renal disease. N. Engl. J. Med. 307, 652-659.
17. Breyer J.A., Bain R.P., Evans J.K., Nahman N.S. Jr, Lewis E.J., Cooper M., McGill J. and Berl T. (1996). Predictors of the progression of renal insufficiency in patients with insulin-dependent diabetes and overt diabetic nephropathy. The Collaborative Study Group. Kidney Int. 50, 1651-1658.
18. Caruso-Neves C., Pinheiro A.A., Cai H., Souza-Menezes J. and Guggino W.B. (2006). PKB and megalin determine the survival or death of renal proximal tubule cells. Proc. Natl. Acad. Sci. USA 103, 18810-18815.
19. Catapano F., Chiodini P., De Nicola L., Minutolo R., Zamboli P., Gallo C. and Conte G. (2008). Antiproteinuric response to dual blockade of the renin-angiotensin system in primary glomerulonephritis: meta-analysis and metaregression. Am. J. Kidney Dis. 52, 475-485.
20. 1R blockade. Kidney Int. 74, 1128-1138.
21. Dalla Vestra M., Masiero A., Roiter A.M., Saller A., Crepaldi G. and Fioretto P. (2003). Is podocyte injury relevant in diabetic nephropathy? Studies in patients with type 2 diabetes. Diabetes 52, 1031-1035.
22. Dandapani S.V., Sugimoto H., Matthews B.D., Kolb R.J., Sinha S., Gerszten R.E., Zhou J., Ingber D.E., Kalluri R. and Pollak M.R. (2007). Alpha-actinin-4 is required for normal podocyte adhesion. J. Biol. Chem. 282, 467-477.
23. De Craemer D., Lobe E., Pauwels M., Verbeelen D. and Van den Branden C. (2001). Angiotensin II administration causes enhanced expression of glomerulosclerosis-related markers and decreased renal antioxidant enzyme activities in rats. Exp. Nephrol. 9, 125-132.
24. Deen W.M., Bridges C.R., Brenner B.M. and Myers B.D. (1985). Heteroporous model of glomerular size selectivity: application to normal and nephrotic humans. Am. J. Physiol. 249, F374-389.
25. Dessapt C., Baradez M.O., Hayward A., Cas A.D., Thomas S.M., Viberti G. and Gnudi L. (2009). Mechanical forces and TGF{beta}1 reduce podocyte adhesion through {alpha}3{beta}1 integrin downregulation. Nephrol. Dial. Transplant. 24, 2645-2655.
26. Dirks J.H., de Zeeuw D., Agarwal S.K., Atkins R.C., Correa-Rotter R., D'Amico G., Bennett P.H., El Nahas M., Valdes R.H., Kaseje D., Katz I.J., Naicker S., Rodriguez-Iturbe B., Schieppati A., Shaheen F., Sitthi-Amorn C., Solez K., Viberti G., Remuzzi G. and Weening J.J. International Society of Nephrology Commission for the Global Advancement of Nephrology Study Group 2004. (2005). Prevention of chronic kidney and vascular disease: toward global health equity-the Bellagio 2004 Declaration. Kidney Int. Suppl. S1-6.
27. Doublier S., Salvidio G., Lupia E., Ruotsalainen V., Verzola D., Deferrari G. and Camussi G. (2003). Nephrin expression is reduced in human diabetic nephropathy: evidence for a distinct role for glycated albumin and angiotensin II. Diabetes 52, 1023-1030.
28. Durvasula R.V., Petermann A.T., Hiromura K., Blonski M., Pippin J., Mundel P., Pichler R., Griffin S., Couser W.G. and Shankland S.J. (2004). Activation of a local tissue angiotensin system in podocytes by mechanical strain. Kidney Int. 65, 30-39.
29. Endlich N., Kress K.R., Reiser J., Uttenweiler D., Kriz W., Mundel P. and Endlich K. (2001). Podocytes respond to mechanical stress in vitro. J. Am. Soc. Nephrol. 12, 413-422.
30. Fintha A., Sebe A., Masszi A., Terebessy T., Huszar T., Rosivall L. and Mucsi I. (2007). Angiotensin II activates plasminogen activator inhibitor-I promoter in renal tubular epithelial cells via the AT1 receptor. Acta Physiol. Hung. 94, 19-30.
31. Fioretto P., Steffes M.W., Sutherland D.E., Goetz F.C. and Mauer M. (1998). Reversal of lesions of diabetic nephropathy after pancreas transplantation. N. Engl. J. Med. 339, 69-75. (Pubitemid 28304880)
32. Fogo A.B. (2005). New capillary growth: a contributor to regression of sclerosis? Curr. Opin. Nephrol. Hypertens. 14, 201-203.
33. Fujihara C.K., Velho M., Malheiros D.M. and Zatz R. (2005). An extremely high dose of losartan affords superior renoprotection in the remnant model. Kidney Int. 67, 1913-1924.
34. Gibson I.W., Downie I., Downie T.T., Han S.W., More I.A. and Lindop G.B. (1992). The parietal podocyte: a study of the vascular pole of the human glomerulus. Kidney Int. 41, 211-214.
35. Gisen Group (1997). Randomized placebo-controlled trial of effect of ramipril on decline in glomerular filtration rate and risk of terminal renal failure in proteinuric, non-diabetic nephropathy. Lancet 349, 1857-1863.
36. Gloy J., Henger A., Fischer K.G., Nitschke R., Mundel P., Bleich M., Schollmeyer P., Greger R. and Pavenstadt H. (1997). Angiotensin II depolarizes podocytes in the intact glomerulus of the Rat. J. Clin. Invest. 99, 2772-2781. (Pubitemid 27259825)
37. Goncalves A.R., Fujihara C.K., Mattar A.L., Malheiros D.M., Noronha Ide L., de Nucci G. and Zatz R. (2004). Renal expression of COX-2, ANG II, and AT1 receptor in remnant kidney: strong renoprotection by therapy with losartan and a nonsteroidal anti-inflammatory. Am. J. Physiol. Renal Physiol. 286, F945-954.
38. Gross M.L., El-Shakmak A., Szabo A., Koch A., Kuhlmann A., Munter K., Ritz E. and Amann K. (2003a). ACE-inhibitors but not endothelin receptor blockers prevent podocyte loss in early diabetic nephropathy. Diabetologia 46, 856-868.
39. Gross M.L., Ritz E., Schoof A., Helmke B., Parkman A., Tulp O., Munter K. and Amann K. (2003b). Renal damage in the SHR/N-cp type 2 diabetes model: comparison of an angiotensin-converting enzyme inhibitor and endothelin receptor blocker. Lab. Invest. 83, 1267-1277.
40. Hannken T., Schroeder R., Stahl R.A. and Wolf G. (1998). Angiotensin II-mediated expression of p27Kip1 and induction of cellular hypertrophy in renal tubular cells depend on the generation of oxygen radicals. Kidney Int. 54, 1923-1933.
41. Haugen E.N., Croatt A.J. and Nath K.A. (2000). Angiotensin II induces renal oxidant stress in vivo and heme oxygenase-1 in vivo and in vitro. Kidney Int. 58, 144-152.
42. Hoffmann S., Podlich D., Hahnel B., Kriz W. and Gretz N. (2004). Angiotensin II type 1 receptor overexpression in podocytes induces glomerulosclerosis in transgenic rats. J. Am. Soc. Nephrol. 15, 1475-1487.
43. Hollenberg N.K., Parving H.H., Viberti G., Remuzzi G., Ritter S., Zelenkofske S., Kandra A., Daley W.L. and Rocha R. (2007). Albuminuria response to very high-dose valsartan in type 2 diabetes mellitus. J. Hypertens. 25, 1921-1926.
44. Hostetter T.H., Olson J.L., Rennke H.G., Venkatachalam M.A. and Brenner B.M. (1981). Hyperfiltration in remnant nephrons: a potentially adverse response to renal ablation. Am. J. Physiol. 241, F85-93.
45. Hou F.F., Xie D., Zhang X., Chen P.Y., Zhang W.R., Liang M., Guo Z.J. and Jiang J.P. (2007). Renoprotection of Optimal Antiproteinuric Doses (ROAD) Study: a randomized controlled study of benazepril and losartan in chronic renal insufficiency. J. Am. Soc. Nephrol. 18, 1889-1898.
46. Hsu H.H., Hoffmann S., Endlich N., Velic A., Schwab A., Weide T., Schlatter E. and Pavenstadt H. (2008). Mechanisms of angiotensin II signaling on cytoskeleton of podocytes. J. Mol. Med. 86, 1379-1394.
47. Ikoma M., Kawamura T., Kakinuma Y., Fogo A. and Ichikawa I. (1991). Cause of variable therapeutic efficiency of angiotensin converting enzyme inhibitor on glomerular lesions. Kidney Int. 40, 195-202.
48. Ingram A.J., Ly H., Thai K., Kang M. and Scholey J.W. (1999). Activation of mesangial cell signaling cascades in response to mechanical strain. Kidney Int. 55, 476-485. (Pubitemid 29082874)
49. Iseki K., Ikemiya Y., Iseki C. and Takishita S. (2003). Proteinuria and the risk of developing end-stage renal disease. Kidney Int. 63, 1468-1474. (Pubitemid 36350012)
50. Jafar T.H., Stark P.C., Schmid C.H., Landa M., Maschio G., Marcantoni C., de Jong P.E., de Zeeuw D., Shahinfar S., Ruggenenti P., Remuzzi G. and Levey A.S. (2001). Proteinuria as a modifiable risk factor for the progression of non-diabetic renal disease. Kidney Int. 60, 1131-1140.
51. Jaimes E.A., Galceran J.M. and Raij L. (1998). Angiotensin II induces superoxide anion production by mesangial cells. Kidney Int. 54, 775-784.
52. John R. and Nelson P.J. (2007). Dendritic cells in the kidney. J. Am. Soc. Nephrol. 18, 2628-2635.
53. Joles J.A., Braam B. and Verhaar M.C. (2006). ACE inhibition and glomerular repair: restructuring or regeneration? Kidney Int. 69, 1105-1107.
54. Kagami S., Border W.A., Miller D.E. and Noble N.A. (1994). Angiotensin II stimulates extracellular matrix protein synthesis through induction of transforming growth factor-beta expression in rat glomerular mesangial cells. J. Clin. Invest. 93, 2431-2437.
55. Kanno Y., Takenaka T., Nakamura T. and Suzuki H. (2006). Add-on angiotensin receptor blocker in patients who have proteinuric chronic kidney diseases and are treated with angiotensin-converting enzyme inhibitors. Clin. J. Am. Soc. Nephrol. 1, 730-737.
56. Kaplan J.M., Kim S.H., North K.N., Rennke H., Correia L.A., Tong H.Q., Mathis B.J., Rodriguez-Perez J.C., Allen P.G., Beggs A.H. and Pollak M.R. (2000). Mutations in ACTN4, encoding alpha-actinin-4, cause familial focal segmental glomerulosclerosis. Nat. Genet. 24, 251-256.
57. Kelly D.J., Aaltonen P., Cox A.J., Rumble J.R., Langham R., Panagiotopoulos S., Jerums G., Holthofer H. and Gilbert R.E. (2002). Expression of the slit-diaphragm protein, nephrin, in experimental diabetic nephropathy: differing effects of anti-proteinuric therapies. Nephrol. Dial. Transplant. 17, 1327-1332.
58. Kim Y.H., Goyal M., Kurnit D., Wharram B., Wiggins J., Holzman L., Kershaw D. and Wiggins R. (2001). Podocyte depletion and glomerulosclerosis have a direct relationship in the PAN-treated rat. Kidney Int. 60, 957-968.
59. Kos C.H., Le T.C., Sinha S., Henderson J.M., Kim S.H., Sugimoto H., Kalluri R., Gerszten R.E. and Pollak M.R. (2003). Mice deficient in alpha-actinin-4 have severe glomerular disease. J. Clin. Invest. 111, 1683-1690.
60. Kuhlmann A., Haas C.S., Gross M.L., Reulbach U., Holzinger M., Schwarz U., Ritz E. and Amann K. (2004). 1,25-Dihydroxyvitamin D3 decreases podocyte loss and podocyte hypertrophy in the subtotally nephrectomized rat. Am. J. Physiol. Renal Physiol. 286, F526-533.
61. Kunz R., Friedrich C., Wolbers M. and Mann J.F. (2008). Meta-analysis: effect of monotherapy and combination therapy with inhibitors of the renin angiotensin system on proteinuria in renal disease. Ann. Intern. Med. 148, 30-48.
62. Lemley K.V., Lafayette R.A., Safai M., Derby G., Blouch K., Squarer A. and Myers B.D. (2002). Podocytopenia and disease severity in IgA nephropathy. Kidney Int. 61, 1475-1485.
63. Lewis E.J., Hunsicker L.G., Bain R.P. and Rohde R.D. (1993). The effect of angiotensin-converting-enzyme inhibition on diabetic nephropathy. The Collaborative Study Group. N. Engl. J. Med. 329, 1456-1462.
64. Li Y., Kang Y.S., Dai C., Kiss L.P., Wen X. and Liu Y. (2008). Epithelial-to-mesenchymal transition is a potential pathway leading to podocyte dysfunction and proteinuria. Am. J. Pathol. 172, 299-308.
65. Liang X.B., Ma L.J., Naito T., Wang Y., Madaio M., Zent R., Pozzi A. and Fogo A.B. (2006). Angiotensin type 1 receptor blocker restores podocyte potential to promote glomerular endothelial cell growth. J. Am. Soc. Nephrol. 17, 1886-1895.
66. Ma L.J., Nakamura S., Aldigier J.C., Rossini M., Yang H., Liang X., Nakamura I., Marcantoni C. and Fogo A.B. (2005). Regression of glomerulosclerosis with high-dose angiotensin inhibition is linked to decreased plasminogen activator inhibitor-1. J. Am. Soc. Nephrol. 16, 966-976.
67. Ma L.J., Nakamura S., Whitsitt J.S., Marcantoni C., Davidson J.M. and Fogo A.B. (2000). Regression of sclerosis in aging by an angiotensin inhibition-induced decrease in PAI-1. Kidney Int. 58, 2425-2436.
68. Macconi D., Ghilardi M., Bonassi M.E., Mohamed E.I., Abbate M., Colombi F., Remuzzi G. and Remuzzi A. (2000). Effect of angiotensin-converting enzyme inhibition on glomerular basement membrane permeability and distribution of zonula occludens-1 in MWF rats. J. Am. Soc. Nephrol. 11, 477-489.
69. Macconi D., Abbate M., Morigi M., Angioletti S., Mister M., Buelli S., Bonomelli M., Mundel P., Endlich K., Remuzzi A. and Remuzzi G. (2006a). Permselective dysfunction of podocyte-podocyte contact upon angiotensin II unravels the molecular target for renoprotective intervention. Am. J. Pathol. 168, 1073-1085.
70. Macconi D., Bonomelli M., Benigni A., Plati T., Sangalli F., Longaretti L., Conti S., Kawachi H., Hill P., Remuzzi G. and Remuzzi A. (2006b). Pathophysiologic implications of reduced podocyte number in a rat model of progressive glomerular injury. Am. J. Pathol. 168, 42-54.
71. Macconi D., Chiabrando C., Schiarea S., Aiello S., Cassis L., Gagliardini E., Noris M., Buelli S., Zoja C., Corna D., Mele C., Fanelli R., Remuzzi G. and Benigni A. (2009a). Proteasomal processing of albumin by renal dendritic cells generates antigenic peptides. J. Am. Soc. Nephrol. 20, 123-130.
72. Macconi D., Sangalli F., Bonomelli M., Conti S., Condorelli L., Gagliardini E., Remuzzi G. and Remuzzi A. (2009b). Podocyte Repopulation Contributes to Regression of Glomerular Injury Induced by Ace Inhibition. Am. J. Pathol. 174, 797-807.
73. Mann J.F., Schmieder R.E., McQueen M., Dyal L., Schumacher H., Pogue J., Wang X., Maggioni A., Budaj A., Chaithiraphan S., Dickstein K., Keltai M., Metsarinne K., Oto A., Parkhomenko A., Piegas L.S., Svendsen T.L., Teo K.K. and Yusuf S. (2008). 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, 547-553.
74. Mauer S.M., Steffes M.W., Sutherland D.E., Najarian S., Michael A.F. and Brown D.M. (1975). Studies of the rate of regression of the glomerular lesions in diabetic rats treated with pancreatic islet transplantation. Diabetes 24, 280-285.
75. Meyer T.W., Bennett P.H. and Nelson R.G. (1999). Podocyte number predicts long-term urinary albumin excretion in Pima Indians with Type II diabetes and microalbuminuria. Diabetologia 42, 1341-1344.
76. Morelli E., Loon N., Meyer T., Peters W. and Myers B.D. (1990). Effects of converting-enzyme inhibition on barrier function in diabetic glomerulopathy. Diabetes 39, 76-82.
77. Nakajima H., Takenaka M., Kaimori J.Y., Nagasawa Y., Kosugi A., Kawamoto S., Imai E., Hori M. and Okubo K. (2002). Gene expression profile of renal proximal tubules regulated by proteinuria. Kidney Int. 61, 1577-1587.
78. Nakamura S., Nakamura I., Ma L., Vaughan D.E. and Fogo A.B. (2000). Plasminogen activator inhibitor-1 expression is regulated by the angiotensin type 1 receptor in vivo. Kidney Int. 58, 251-259.
79. Nakamura T., Ushiyama C., Suzuki S., Hara M., Shimada N., Ebihara I. and Koide H. (2000a). The urinary podocyte as a marker for the differential diagnosis of idiopathic focal glomerulosclerosis and minimal-change nephrotic syndrome. Am. J. Nephrol. 20, 175-179.
80. Nakamura T., Ushiyama C., Suzuki S., Hara M., Shimada N., Ebihara I. and Koide H. (2000b). Urinary excretion of podocytes in patients with diabetic nephropathy. Nephrol. Dial. Transplant. 15, 1379-1383.
81. Nakamura T., Ushiyama C., Suzuki S., Hara M., Shimada N., Sekizuka K., Ebihara I. and Koide H. (2000c). Effects of angiotensin-converting enzyme inhibitor, angiotensin II receptor antagonist and calcium antagonist on urinary podocytes in patients with IgA nephropathy. Am. J. Nephrol. 20, 373-379.
82. Niranjan T., Bielesz B., Gruenwald A., Ponda M.P., Kopp J.B., Thomas D.B. and Susztak K. (2008). The Notch pathway in podocytes plays a role in the development of glomerular disease. Nat. Med. 14, 290-298.
83. Nitschke R., Henger A., Ricken S., Gloy J., Muller V., Greger R. and Pavenstadt H. (2000). Angiotensin II increases the intracellular calcium activity in podocytes of the intact glomerulus. Kidney Int. 57, 41-49.
84. Pagtalunan M.E., Miller P.L., Jumping-Eagle S., Nelson R.G., Myers B.D., Rennke H.G., Coplon N.S., Sun L. and Meyer T.W. (1997). Podocyte loss and progressive glomerular injury in type II diabetes. J. Clin. Invest. 99, 342-348.
85. Parving H.H., Andersen A.R., Smidt U.M., Hommel E., Mathiesen E.R. and Svendsen P.A. (1987). Effect of antihypertensive treatment on kidney function in diabetic nephropathy. Br. Med. J. (Clin. Res. Ed.) 294, 1443-1447.
86. Parving H.H., Hommel E. and Smidt U.M. (1988). Protection of kidney function and decrease in albuminuria by captopril in insulin dependent diabetics with nephropathy. BMJ 297, 1086-1091.
87. Perico N., Benigni A. and Remuzzi G. (2008). Present and future drug treatments for chronic kidney diseases: evolving targets in renoprotection. Nat. Rev. Drug Discov. 7, 936-953.
88. Perico N., Codreanu I., Schieppati A. and Remuzzi G. (2005). The scientific care for prevention: an overview. Kidney Int. Suppl. S8-13.
89. Petermann A.T., Krofft R., Blonski M., Hiromura K., Vaughn M., Pichler R., Griffin S., Wada T., Pippin J., Durvasula R. and Shankland S.J. (2003). Podocytes that detach in experimental membranous nephropathy are viable. Kidney Int. 64, 1222-1231.
90. Petermann A.T., Pippin J., Durvasula R., Pichler R., Hiromura K., Monkawa T., Couser W.G. and Shankland S.J. (2005). Mechanical stretch induces podocyte hypertrophy in vitro. Kidney Int. 67, 157-166.
91. Peterson J.C., Adler S., Burkart J.M., Greene T., Hebert L.A., Hunsicker L.G., King A.J., Klahr S., Massry S.G. and Seifter J.L. (1995). Blood pressure control, proteinuria, and the progression of renal disease. The Modification of Diet in Renal Disease Study. Ann. Intern. Med. 123, 754-762.
92. Remuzzi A., Puntorieri S., Battaglia C., Bertani T. and Remuzzi G. (1990). Angiotensin converting enzyme inhibition ameliorates glomerular filtration of macromolecules and water and lessens glomerular injury in the rat. J. Clin. Invest. 85, 541-549.
93. Remuzzi A., Perticucci E., Ruggenenti P., Mosconi L., Limonta M. and Remuzzi G. (1991). Angiotensin converting enzyme inhibition improves glomerular size-selectivity in IgA nephropathy. Kidney Int. 39, 1267-1273.
94. Remuzzi A., Perico N., Amuchastegui C.S., Malanchini B., Mazerska M., Battaglia C., Bertani T. and Remuzzi G. (1993). Short- and long-term effect of angiotensin II receptor blockade in rats with experimental diabetes. J. Am. Soc. Nephrol. 4, 40-49.
95. Remuzzi A., Imberti O., Puntorieri S., Malanchini B., Macconi D., Magrini L., Bertani T. and Remuzzi G. (1994). Dissociation between antiproteinuric and antihypertensive effect of angiotensin converting enzyme inhibitors in rats. Am. J. Physiol. 267, F1034-1044.
96. Remuzzi A., Benigni A., Malanchini B., Bruzzi I., Foglieni C. and Remuzzi G. (1995). ACE inhibition prevents renal failure and death in uninephrectomized MWF/Ztm rats. Kidney Int. 47, 1319-1326.
97. Remuzzi A., Fassi A., Bertani T., Perico N. and Remuzzi G. (1999). ACE inhibition induces regression of proteinuria and halts progression of renal damage in a genetic model of progressive nephropathy. Am. J. Kidney Dis. 34, 626-632.
98. Remuzzi A., Gagliardini E., Donadoni C., Fassi A., Sangalli F., Lepre M.S., Remuzzi G. and Benigni A. (2002). Effect of angiotensin II antagonism on the regression of kidney disease in the rat. Kidney Int. 62, 885-894.
99. Remuzzi A., Gagliardini E., Sangalli F., Bonomelli M., Piccinelli M., Benigni A. and Remuzzi G. (2006). ACE inhibition reduces glomerulosclerosis and regenerates glomerular tissue in a model of progressive renal disease. Kidney Int. 69, 1124-1130.
100. Ronconi E., Sagrinati C., Angelotti M.L., Lazzeri E., Mazzinghi B., Ballerini L., Parente E., Becherucci F., Gacci M., Carini M., Maggi E., Serio M., Vannelli G.B., Lasagni L., Romagnani S. and Romagnani P. (2009). Regeneration of glomerular podocytes by human renal progenitors. J. Am. Soc. Nephrol. 20, 322-332.
101. Rossing K., Christensen P.K., Hovind P. and Parving H.H. (2005). Remission of nephrotic-range albuminuria reduces risk of end-stage renal disease and improves survival in type 2 diabetic patients. Diabetologia 48, 2241-2247.
102. Rudnicki M., Eder S., Perco P., Enrich J., Scheiber K., Koppelstatter C., Schratzberger G., Mayer B., Oberbauer R., Meyer T.W. and Mayer G. (2007). Gene expression profiles of human proximal tubular epithelial cells in proteinuric nephropathies. Kidney Int. 71, 325-335.
103. Ruggenenti P. and Remuzzi G. (2009). Is the ONTARGET renal substudy actually out of target? Nat. Rev. Nephrol. 5, 436-437.
104. Ruggenenti P., Perna A., Gherardi G., Gaspari F., Benini R. and Remuzzi G. (1998a). Renal function and requirement for dialysis in chronic nephropathy patients on long-term ramipril: REIN follow-up trial. Gruppo Italiano di Studi Epidemiologici in Nefrologia (GISEN). Ramipril Efficacy in Nephropathy. Lancet 352, 1252-1256.
105. Ruggenenti P., Perna A., Mosconi L., Pisoni R. and Remuzzi G. (1998b). Urinary protein excretion rate is the best independent predictor of ESRF in non-diabetic proteinuric chronic nephropathies. "Gruppo Italiano di Studi Epidemiologici in Nefrologia" (GISEN). Kidney Int. 53, 1209-1216.
106. Ruggenenti P., Perna A., Benini R., Bertani T., Zoccali C., Maggiore Q., Salvadori M. and Remuzzi G. (1999). In chronic nephropathies prolonged ACE inhibition can induce remission: dynamics of time-dependent changes in GFR. Investigators of the GISEN Group. Gruppo Italiano Studi Epidemiologici in Nefrologia. J. Am. Soc. Nephrol. 10, 997-1006.
107. Ruggenenti P., Mosconi L., Vendramin G., Moriggi M., Remuzzi A., Sangalli F. and Remuzzi G. (2000). ACE inhibition improves glomerular size selectivity in patients with idiopathic membranous nephropathy and persistent nephrotic syndrome. Am. J. Kidney Dis. 35, 381-391.
108. Ruggenenti P., Brenner B.M. and Remuzzi G. (2001a). Remission achieved in chronic nephropathy by a multidrug approach targeted at urinary protein excretion. Nephron 88, 254-259.
109. Ruggenenti P., Schieppati A. and Remuzzi G. (2001b). Progression, remission, regression of chronic renal diseases. Lancet 357, 1601-1608.
110. Ruggenenti P., Perna A. and Remuzzi G. (2003). Retarding progression of chronic renal disease: the neglected issue of residual proteinuria. Kidney Int. 63, 2254-2261.
111. Ruggenenti P., Perticucci E., Cravedi P., Gambara V., Costantini M., Sharma S.K., Perna A. and Remuzzi G. (2008). Role of remission clinics in the longitudinal treatment of CKD. J. Am. Soc. Nephrol. 19, 1213-1224.
112. Ruiz-Ortega M., Bustos C., Hernandez-Presa M.A., Lorenzo O., Plaza J.J. and Egido J. (1998). Angiotensin II participates in mononuclear cell recruitment in experimental immune complex nephritis through nuclear factor-kappa B activation and monocyte chemoattractant protein-1 synthesis. J. Immunol. 161, 430-439.
113. Sagrinati C., Netti G.S., Mazzinghi B., Lazzeri E., Liotta F., Frosali F., Ronconi E., Meini C., Gacci M., Squecco R., Carini M., Gesualdo L., Francini F., Maggi E., Annunziato F., Lasagni L., Serio M., Romagnani S. and Romagnani P. (2006). Isolation and characterization of multipotent progenitor cells from the Bowman's capsule of adult human kidneys. J. Am. Soc. Nephrol. 17, 2443-2456.
114. Schiffer M., Bitzer M., Roberts I.S., Kopp J.B., ten Dijke P., Mundel P. and Bottinger E.P. (2001). Apoptosis in podocytes induced by TGF-beta and Smad7. J. Clin. Invest. 108, 807-816.
115. Schmieder R.E., Klingbeil A.U., Fleischmann E.H., Veelken R. and Delles C. (2005). Additional antiproteinuric effect of ultrahigh dose candesartan: a double-blind, randomized, prospective study. J. Am. Soc. Nephrol. 16, 3038-3045.
116. Scruggs B., Donnert E., Ma L.-J., Bertram J. and Fogo A.B. (2005). Capillary branching contributes to regression of sclerosis by angiotensin receptor blocker (ARB). J. Am. Soc. Nephrol. 674A.
117. Shankland S.J. (2006). The podocyte's response to injury: role in proteinuria and glomerulosclerosis. Kidney Int. 69, 2131-2147.
118. Steffes M.W., Schmidt D., McCrery R. and Basgen J.M. (2001). Glomerular cell number in normal subjects and in type 1 diabetic patients. Kidney Int. 59, 2104-2113.
119. Strutz F.M. (2009). EMT and proteinuria as progression factors. Kidney Int. 75, 475-481.
120. Tarver-Carr M.E., Brancati F.L., Eberhardt M.S. and Powe N.R. (2000). Proteinuria and the risk of chronic kidney disease (CKD) in the United States. J. Am. Soc. Nephrol. 11, 168A.
121. Teles F., Machado F.G., Ventura B.H., Malheiros D.M., Fujihara C.K., Silva L.F. and Zatz R. (2009). Regression of glomerular injury by losartan in experimental diabetic nephropathy. Kidney Int. 75, 72-79.
122. Vogelmann S.U., Nelson W.J., Myers B.D. and Lemley K.V. (2003). Urinary excretion of viable podocytes in health and renal disease. Am. J. Physiol. Renal Physiol. 285, F40-48.
123. Wharram B.L., Goyal M., Wiggins J.E., Sanden S.K., Hussain S., Filipiak W.E., Saunders T.L., Dysko R.C., Kohno K., Holzman L.B. and Wiggins R.C. (2005). Podocyte depletion causes glomerulosclerosis: diphtheria toxin-induced podocyte depletion in rats expressing human diphtheria toxin receptor transgene. J. Am. Soc. Nephrol. 16, 2941-2952.
124. White K.E., Bilous R.W., Marshall S.M., El Nahas M., Remuzzi G., Piras G., De Cosmo S. and Viberti G. (2002). Podocyte number in normotensive type 1 diabetic patients with albuminuria. Diabetes 51, 3083-3089.
125. Wiggins J.E., Goyal M., Sanden S.K., Wharram B.L., Shedden K.A., Misek D.E., Kuick R.D. and Wiggins R.C. (2005). Podocyte hypertrophy, "adaptation," and "decompensation" associated with glomerular enlargement and glomerulosclerosis in the aging rat: prevention by calorie restriction. J. Am. Soc. Nephrol. 16, 2953-2966.
126. Wiggins R.C. (2007). The spectrum of podocytopathies: a unifying view of glomerular diseases. Kidney Int. 71, 1205-1214.
127. Wilmer W.A., Hebert L.A., Lewis E.J., Rohde R.D., Whittier F., Cattran D., Levey A.S., Lewis J.B., Spitalewitz S., Blumenthal S. and Bain R.P. (1999). Remission of nephrotic syndrome in type 1 diabetes: long-term follow-up of patients in the Captopril Study. Am. J. Kidney Dis. 34, 308-314.
128. Wilson H.M., Haites N.E. and Booth N.A. (1997). Effect of angiotensin II on plasminogen activator inhibitor-1 production by cultured human mesangial cells. Nephron 77, 197-204.
129. Wolf G., Ziyadeh F.N., Thaiss F., Tomaszewski J., Caron R.J., Wenzel U., Zahner G., Helmchen U. and Stahl R.A. (1997). Angiotensin II stimulates expression of the chemokine RANTES in rat glomerular endothelial cells. Role of the angiotensin type 2 receptor. J. Clin. Invest. 100, 1047-1058.
130. Xue J.L., Ma J.Z., Louis T.A. and Collins A.J. (2001). Forecast of the number of patients with end-stage renal disease in the United States to the year 2010. J. Am. Soc. Nephrol. 12, 2753-2758.
131. Yoshioka T., Rennke H.G., Salant D.J., Deen W.M. and Ichikawa I. (1987). Role of abnormally high transmural pressure in the permselectivity defect of glomerular capillary wall: a study in early passive Heymann nephritis. Circ. Res. 61, 531-538.
132. Yu D., Petermann A., Kunter U., Rong S., Shankland S.J. and Floege J. (2005). Urinary podocyte loss is a more specific marker of ongoing glomerular damage than proteinuria. J. Am. Soc. Nephrol. 16, 1733-1741.
133. Zoja C., Corna D., Camozzi D., Cattaneo D., Rottoli D., Batani C., Zanchi C., Abbate M. and Remuzzi G. (2002). How to fully protect the kidney in a severe model of progressive nephropathy: a multidrug approach. J. Am. Soc. Nephrol. 13, 2898-2908.