Seminars in Nephrology
Volume 24, Issue 2 , Pages 158-167 , March 2004

Angiotensin-converting enzyme inhibition and angiotensin II antagonism in nondiabetic chronic nephropathies

  • Piero Ruggenenti

      Affiliations

    • Department of Medicine and Transplantation, Ospedali Riuniti, Bergamo-Mario Negri Institute for Pharmacological Research, Bergamo, Italy
    • Department of Renal Medicine, Clinical Research Center for Rare Diseases “Aldo e Cele Daccò,” Mario Negri Institute for Pharmacological Research, Bergamo, Italy
    • Corresponding Author InformationAddress reprint requests to Piero Ruggenenti, MD, Mario Negri Institute for Pharmacological Research, Via Gavazzeni, 11, 24125 Bergamo, Italy

References 

  1. Aros C, Remuzzi G. The renin-angiotensin system in progression, remission and regression of chronic nephropathies. J Hypertens. 2002;20(suppl):S45–S53
  2. Yoshioka T, Rennke HG, Salant DJ, et al.  Role of abnormally high transmural pressure in the permselectivity defect of glomerular capillary wall (A study in early passive Heymann nephritis). Circ Res. 1987;61:531–538
  3. Bohrer MP, Deen WM, Robertson CR, Brenner BM. Mechanism of angiotensin II-induced proteinuria in the rat. Am J Physiol. 1977;233:F13–F21
  4. Lapinski R, Perico N, Remuzzi A, et al.  A II modulates glomerular capillary permselectivity in rat isolated perfused kidney. J Am Soc Nephrol. 1996;7:653–660
  5. Kritz W, Hackenthal E, Nobiling R, et al.  A role for podocytes to counteract capillary wall distension. Kidney Int. 1994;45:369–376
  6. Shake JG, Brandt RC, Daniels BS. A II induces actin polymerization within the glomerular filtration barrier (Possible role in the local regulation of ultrafiltration). J Am Soc Nephrol. 1992;3:568; (abstract)
  7. Gloy J, Henger A, Fischer K-G, et al.  A II depolarizes podocytes in the intact glomerulus of the rat. J Clin Invest. 1997;99:2772–2781
  8. Remuzzi G, Bertani T. Pathophysiology of progressive nephropathies. N Engl J Med. 1998;339:1448–1456
  9. Abbate M, Zoja C, Morigi M, et al.  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. 2002;161:2179–2199
  10. Bertani T, Zoja C, Abbate M, et al.  Age-related nephropathy and proteinuria in rats with intact kidneys exposed to diets with different protein content. Lab Invest. 1989;60:196–204
  11. Bertani T, Cutillo F, Zoja C, et al.  Tubulointerstitial lesions mediate renal damage in adriamycin glomerulopathy. Kidney Int. 1986;30:488–496
  12. Zoja C, Morigi M, Remuzzi G. Proteinuria and phenotypic change of proximal tubular cells. J Am Soc Nephrol. 2003;14:S36–S41
  13. Barnes PJ, Karin M. Nuclear factor-kB—A pivotal transcription factor in chronic inflammatory diseases. N Engl J Med. 1997;336:1066–1071
  14. Baldwin AS. The transcription factor NF-kB and human disease. J Clin Invest. 2001;107:3–11
  15. Zoja C, Donadelli R, Colleoni S, et al.  Protein overload stimulates RANTES production by proximal tubular cells depending on NF-kB activation. Kidney Int. 1998;53:1608–1615
  16. Morigi M, Macconi D, Zoja C, et al.  Protein overload-induced NF-kB activation in proximal tubular cells requires H202 through a PKC-dependent pathway. J Am Soc Nephrol. 2002;13:1179–1189
  17. Mezzano SA, Barria M, Droguett MA, et al.  Tubular NF-kB and AP-1 activation in human proteinuric renal disease. Kidney Int. 2001;60:1366–1377
  18. Eddy AA. Role of cellular infiltrates in response to proteinuria. Am J Kidney Dis. 2001;37(Suppl 2):S25–S29
  19. Johnson DW, Saunders HJ, Baxter RC, et al.  Paracrine stimulation of human renal fibroblasts by proximal tubule cells. Kidney Int. 1998;54:747–757
  20. Zoja C, Benigni A, Remuzzi G. Cellular responses to protein overload (Key event in renal disease). Curr Opin Nephrol Hypertens. 2004;13:31–37
  21. Hsu SI-H, Couser WG. Chronic progression of tubulointerstitial damage in proteinuric renal disease is mediated by complement activation (A therapeutic role for complement inhibitors?). J Am Soc Nephrol. 2003;14:S186–S191
  22. Wolf G. A II as a mediator of tubulointerstitial injury. Nephrol Dial Transplant. 2000;15(suppl):61–63
  23. Wolf G, Ziyadeh F. Renal tubular hypertrophy induced by A II. Semin Nephrol. 1997;17:448–454
  24. Wolf G, Kalluri R, Ziyadeh F, et al.  A II induces alpha3 (IV) collagen expression in cultured urine proximal tubular cells. Proc Assoc Am Physic. 1999;11:357–364
  25. Strutz F, Muller GA. Interstitial pathomechanisms underlying progressive tubulointerstitial damage. Kidney Blood Press Res. 1999;22:71–80
  26. Baricos WH, Cortez SL, el-Dahr SS, et al.  ECM degradation by cultured human mesangial cells is mediated by a PA/plasmin/MMP-2 cascade. Kidney Int. 1995;47:1039–1047
  27. Keane WF, Raij L. Relationship among altered glomerular barrier permselectivity. A II, and mesangial uptake of macromolecules. Lab Invest. 1985;52:599–604
  28. Egido J. Vasoactive hormones and renal sclerosis. Kidney Int. 1996;49:578–597
  29. Okada H, Danoff T, Kalluri R, et al.  Early role of Fsp 1 in epithelial-mesenchymal transformation. Am J Physiol. 1997;273:F563–F574
  30. Benigni A, Corna D, Zoja C, et al.  Targeted deletion of Angiotensin II type 1 receptor does not protect mice from progressive nephropathy of overload proteinuria. J Am Soc Nephrol. 2002;13:341; (abstract)
  31. Zatz R, Dunn BR, Meyer TW, et al.  Prevention of diabetic glomerulopathy by pharmacological amelioration of glomerular capillary hypertension. J Clin Invest. 1986;77:1925–1930
  32. Remuzzi A, Puntorieri S, Battaglia C, et al.  Angiotensin converting enzyme inhibition ameliorates glomerular filtration of macromolecules and water and lessens glomerular injury in the rat. J Clin Invest. 1990;85:541–549
  33. Donadelli R, Abbate M, Zanchi C, et al.  Protein traffic activates NF-kB gene signaling and promotes MCP-1-dependent interstitial inflammation. Am J Kidney Dis. 2000;36:1226–1241
  34. Taal MW, Brenner BM. Renoprotective benefits of RAS inhibitionFro ACEi to angiotensin II antagonists. Kidney Int. 2000;57:1803–1817
  35. Maschio G, Alberti D, Janin G, et al.  Effect of the angiotensin-converting-enzyme inhibitor benazepril on the progression of chronic renal insufficiency. The Angiotensin-Converting-Enzyme Inhibition in Progressive Renal I Study Group. N Engl J Med. 1996;334:939–945
  36. The GISEN Group (Gruppo Italiano di Studi Epidemiologici in Nefrologia) . Randomised 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. 1997;349:1857–1863
  37. Ruggenenti P, Perna A, Gherardi G, et al.  Gruppo Italiano di Studi Epidemiologici in Nefrologia (GISEN)   Renal function and requirement for dialysis in chronic nephropathy patients on long-term ramipril (REIN follow-up trial). Lancet. 1998;352:1252–1256
  38. Ruggenenti P, Perna A, Gherardi G, et al.  Renoprotective properties of ACE-inhibition in non-diabetic nephropathies with non-nephrotic proteinuria. Lancet. 1999;354:359–364
  39. Ruggenenti P, Perna A, Remuzzi G  Investigators of the GISEN Group . Retarding progression of chronic renal disease (The neglected issue of residual proteinuria). Kidney Int. 2003;63:2254–2261
  40. Ruggenenti P, Perna A, Remuzzi G. ACE inhibitors to prevent end-stage renal disease: When to start and why possibly never to stop: A post hoc analysis of the REIN trial result. Ramipril Eficacy in Nephropathy. J Am Soc Nephrol. 2001;12:2832–2837
  41. Kam-Tao P, Chow K-M, Wong TY-H, Leung C-B, Szeto C-C. Effects of an angiotensin converting enzyme inhibitor on residual renal function in patients receiving peritoneal dialysis. Ann Intern Med. 2003;139:105–112
  42. Agodoa LY, Appel L, Bakris GL, et al.  African American Study of Kidney Disease and Hypertension (AASK) Study Group: Effect of ramipril vs amlodipine on renal outcomes in hypertensive nephrosclerosis: A randomized controlled trial. JAMA. 2001;285:2719–2728
  43. Wright JT, Bakris G, Green T, et al.  African American Study of Kidney Disease and Hypertension (AASK) Study Group   Effect of blood pressure lowering and antihypertensive drug class on progression of hypertensive kidney disease (Results from the AASK trial). JAMA. 2002;288:2421–2431
  44. Ruggenenti P, Perna A, Benini R, et al.  In chronic nephropathies prolonged ACE inhibition can induce remission (Dynamics of time-dependent changes in GFR). J Am Soc Nephrol. 1999;10:997–1006
  45. Remuzzi A, Fassi A, Bertani T, et al.  ACE inhibition induces regression of proteinuria and halts progression of renal damage in a genetic model of progressive nephropathy. Am J Kidney Dis. 1999;34:626–632
  46. Ikoma M, Kawamura T, Kakinuma Y, et al.  Cause of variable therapeutic efficiency of angiotensin converting enzyme inhibitor on glomerular lesions. Kidney Int. 1991;40:195–202
  47. Ma L-J, Nakamura S, Whitsitt JS, et al.  Regression of sclerosis in aging by an angiotensin inhibition-induced decrease in PAI-1. Kidney Int. 2000;58:2425–2436
  48. Ruggenenti P, Mise N, Pisoni R, et al.  Diverse effects of increasing Lisinopril doses on lipid abnormalities in chronic nephropathies. Circulation. 2003;107:586–592
  49. Taal MW, Brenner BM. Combination ACEi and ARB therapy (Additional benefit in renoprotection?). Curr Opin Nephrol Hypertens. 2002;11:377–381
  50. Ruggenenti P, Remuzzi G. Is therapy with combined ACE inhibitor and angiotensin receptor antagonist the new “gold standard” of treatment for non-diabetic chronic proteinuric nephropathies? Nephrology (in press)
  51. Remuzzi A, Gagliardini E, Donadoni A, et al.  Effect of A II antagonism on the regression of kidney disease in the rat. Kidney Int. 2002;62:885–894
  52. Zoja C, Corna D, Camozzi D, et al.  How to fully protect the kidney in a severe model of progressive nephropathy (A multidrug approach). J Am Soc Nephrol. 2002;13:2898–2908
  53. Campbell R, Sangalli F, Perticucci E, et al.  Effects of combined ACE inhibitor and angiotensin II antagonist treatment in human chronic nephropathies. Kidney Int. 2003;63:1094–1103
  54. Nakao N, Yoshimura A, Morita H, et al.  Combination treatment of angiotensin II receptor blocker and angiotensin converting enzyme inhibitor in non diabetic renal disease (COOPERATE) (A randomized controlled trial). Lancet. 2003;361:117–124
  55. Zoja C, Corna D, Rottoli D, et al.  Effect of combining ACE inhibitor and statin in severe experimental nephropathy. Kidney Int. 2002;61:1635–1645
  56. Yang J, Shultz RW, Mars WM, et al.  Disruption of tissue-type plasminogen activator gene in mice reduces renal interstitial fibrosis in obstructive nephropathy. J Clin Invest. 2002;110:1525–1538
  57. Ziyadeh FN, Hoffman BB, Cheol Han D, et al.  Long-term prevention of renal insufficiency, excess matrix gene expression, and glomerular mesangial matrix expansion by treatment with monoclonal antitransforming growth factor-β antibody in db/db diabetic mice. Proc Natl Acad Sci USA. 2000;97:8015–8020
  58. Taal MW, Nenov VD, Wong W, et al.  Vasopeptidase inhibition affords greater renoprotection than angiotensin-converting enzyme inhibition alone. J Am Soc Nephrol. 2001;12:2051–2059
  59. Remuzzi G, Zoja C, Gagliardini E, et al.  Combining an antiproteinuric approach with micophenolate mofetil fully suppresses progressive nephropathy of experimental animals. J Am Soc Nephrol. 1999;10:1542–1549
  60. Nangaku M, Pippin J, Couser WG. C6 mediates chronic progression of tubulointerstitial damage in rats with remnant kidneys. J Am Soc Nephrol. 2002;13:928–936
  61. Muller DN, Shagdarsuren E, Park J-K, et al.  Immunosuppressive treatment protects against A II-induced renal damage. Am J Pathol. 2002;161:1679–1693
  62. Ruggenenti P, Schieppati A, Remuzzi G. Progression, remission, regression of chronic renal diseases. Lancet. 2001;357:1601–1608
  63. Ruggenenti P, Brenner BM, Remuzzi G. Remission achieved in chronic nephropathy by a multidrug approach targeted at urinary protein excretion. Nephron. 2001;88:254–259
  64. Fioretto P, Steffes MW, Sutherland DE, et al.  Reversal of lesions of diabetic nephropathy after pancreas transplantation. N Engl J Med. 1998;339:69–75
  65. Perico N, Amuchastegui CS, Colosio V, et al.  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. 1994;5:1139–1146
  66. Trivedi HS, Pang MMH, Campbell A, et al.  Slowing the progression of chronic renal failure (Economic benefits and patients’ perspectives). Am J Kidney Dis. 2002;39:721–729
  67. Hall WD. Abnormalities of kidney function as a cause and a consequence of cardiovascular disease. Am J Med Sci. 1999;317:176–182
  68. Parfrey PS, Foley RN. The clinical epidemiology of cardiac disease in chronic renal failure. J Am Soc Nephrol. 1999;10:1606–1615
  69. Mann JFE, Gestein HC, Pogue J, et al.  Renal insufficiency as a predictor of cardiovascular outcomes and the impact of Ramipril (The HOPE randomized trial). Ann Intern Med. 2001;134:629–636
  70. Baigent C, Burbury K, Wheeler D. Premature cardiovascular disease in chronic renal failure. Lancet. 2000;356:147–152
  71. Sdevanski A, Schmidt KG, Waldherr R, et al.  Early increase in blood pressure and diastolic left ventricular malfunction in patients with glomerulonephritis. Kidney Int. 1996;50:1321–1326
  72. Kronenberg F, Kuen E, Ritz E, et al.  Apolipoprotein A-IV serum concentrations are elevated in patients with mild and moderate renal failure. J Am Soc Nephrol. 2000;11:105–115
  73. Jungers P, Joly D, Massy Z, et al.  Sustained reduction of hyperhomocysteinaemia with folic acid supplementation in predialysis patients. Nephrol Dial Transplant. 1999;14:2903–2906
  74. Fliser D, Pacini G, Engelleiter R, et al.  Insulin resistance and hyperinsulinemia are already present in patients with incipient renal disease. Kidney Int. 1998;53:1343–1347
  75. Gall M-A, Borch-Johnsen K, Hougaard P, Nielsen FS, Parving H-H. Albuminuria and poor glycemic control predict mortality in NIDD?. Diabetes. 1995;44:1303–1309
  76. Yusuf S, Ionn E. Anti-ischemic effects of ACE-inhibitors (Review of current clinical evidence and ongoing trials). Eur Heart J. 1998;19:J36–J44
  77. Hoy WE, Wang Z, Baker PRA, Kelly AM. Secondary prevention of renal and cardiovascular disease (Results of a renal and cardiovascular treatment program in an Australian Aboriginal community). J Am Soc Nephrol. 2003;14:S178–S185
  78. The Heart Outcomes Prevention Evaluation Study Investigators . Effects of angiotensin converting enzyme inhibitor, ramipril, on cardiovascular events in high-risk patients. N Engl J Med. 2000;342:145–153
  79. Shlipak MG. Pharmacotherapy for heart failure in patients with renal insufficiency. Ann Intern Med. 2003;138:917–924

PII: S0270-9295(03)00192-X

doi: 10.1016/j.semnephrol.2003.11.002

Seminars in Nephrology
Volume 24, Issue 2 , Pages 158-167 , March 2004