Multiorgan-protective actions of blockers of the renin-angiotensin system, statins and erythropoietin: Common pleiotropic effects in reno-, cardio- and neuroprotection

Acta Clinica Belgica

Volumn 63, Issue 3, 2008, Pages 152-169

  Gluhovschi, Gheorghe ^a   Gluhovschi, C ^a   Bob, F ^a   Velciov, S ^a   Trandafirescu, V ^a   Petrica, L ^a   Bozdog, G ^a  

^a VICTOR BABES UNIVERSITY OF MEDICINE AND PHARMACY   (Romania)

Author keywords

ACE inhibition; Erythropoietin; Multi organ protection; Pleiotropic effects; Statins

Indexed keywords

ANGIOTENSIN RECEPTOR ANTAGONIST; ATORVASTATIN; CANDESARTAN; CAPTOPRIL; CERIVASTATIN; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; ENALAPRIL; EPOSARTAN; ERYTHROPOIETIN; EZETIMIBE; FLUINDOSTATIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; IRBESARTAN; LISINOPRIL; LOSARTAN; MEVINOLIN; NIFEDIPINE; PERINDOPRIL; PRAVASTATIN; RAMIPRIL; ROSUVASTATIN; SIMVASTATIN; TELMISARTAN; TRANDOLAPRIL; VALSARTAN;

ADD ON THERAPY; ARTERIAL STIFFNESS; ATHEROSCLEROSIS; CHRONIC KIDNEY DISEASE; CLINICAL PRACTICE; CLINICAL TRIAL; DIABETIC NEPHROPATHY; DRUG ACTIVITY; DRUG EFFECT; DRUG MECHANISM; DYSLIPIDEMIA; GLOMERULOPATHY; HEART INFARCTION; HEART PROTECTION; HEYMANN NEPHRITIS; HUMAN; HYPERCHOLESTEROLEMIA; HYPERTENSION; INSULIN DEPENDENT DIABETES MELLITUS; KIDNEY FAILURE; NEUROPROTECTION; NONHUMAN; PLEIOTROPY; RENAL PROTECTION; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; REVIEW; STROKE;

EID: 47949084299     PISSN: 00015512     EISSN: None     Source Type: Journal    
DOI: 10.1179/acb.2008.026     Document Type: Review

References (141)

1. Gluhovschi Gh, Bozdog Gh, Petrica L, et al. Multi-organ protection and the kidney. From nephroprotection, cardioprotection, neuroprotection to multi-organ protection. Nefrologia (Madrid, Spain) 2004; Vol XXIV, 519-35.
2. Brenner BM. The history and future of nephroprotection. Kidney Int 2003, 64 (4): 1163.
3. Remuzzi G, Bertani T. Pathophysiology of progressive nephropathies. N Engl J Med 1998; 339 (20): 1448-56.
4. Schieppati A, Remuzzi G. The future of renoprotection: frustration and promises. Kidney Int 2003; 64(6): 1947-55.
5. Bernadet-Monrozies P, Rostaing L, Kamar N, Durand D. The effect of angiotensin-converting enzyme inhibitors on the progression of chronic renal failure. Presse Med 2002; 31,36, 1714-20
6. Thone- Reineke C, Steckelings UM, Unger T. Angiotensin receptor blockers and cerebral protection in stroke. J Hypertens Suppl 2006; 24:115-21.
7. Holmer SR, Riegger GA. Role of cardiac renin-angiotensin system in hypertensive heart disease. Herz 1995; 20: 322-9.
8. Dzau V. The cardiovascular continuum and renin-angiotensin-aldosterone system blockade. J Hypertens Suppl 2005; 23(1): S9-17.
9. Culman J, Blume A, Gohlke P, Unger T. The renin-angiotensin system in the brain: possible therapeutic implications for AT(1)-receptor blockers. J Hum Hypertens 2002;16 Suppl 3: S64-70.
10. Codreanu I, Perico N, Remuzzi G. Dual blockade of the reninangiotensin system: the ultimate treatment for renal protection? J Am Soc Nephrol 2005;16 Suppl 1:S34-8.
11. Weir MR, Henrich WL. Theoretical basis and clinical evidence for differential effects of angiotensin-converting enzyme inhibitors and angiotensin II receptor subtype 1 blockers. Curr Opin Nephrol Hypertens 2000 Jul;9(4):403-11.
12. Ferrari P. Prescribing angiotensin-converting enzyme inhibitors and angiotensin receptor blockers in chronic kidney disease. Nephrology (Carlton) 2007; 12: 81-9.
13. Montalescot G, Collet JP. Preserving cardiac function in the hypertensive patient why renal parameters hold the key. Eur heart J 2005; 26: 2616-22.
14. Carr AA, Kowey PR, Devereux RB, et al. Hospitalizations for new heart failure among subjects with diabetes mellitus in the RENAAL and LIFE studies. Am J Cardiol 2005 Dec 1; 96(11): 1530-6.
15. Zanella MT, Ribeiro AB. The role of angiotensin II antagonist in type 2 diabetes mellitus: a review of renoprotection tudy. Clin Ther 2002; 24: 1019-34.
16. Petrica L, Petrica M, Bob F, et al. Renal-, cardiac- and cerebroprotective effects of Perindopril in patients with primary chronic glomerulonephritis. Nefrologia 2003; 8: 71.
17. Richer C, Fornes P, Vacher E, et al. Trandolaprils protective effects in stroke-prone spontaneously hypertensive rats persist long after treatment withdrawal. Am J Cardiol 1994 Apr 7;73(10):26C-35C.
18. Vacher E, Fornes P, Domergue V, et al. Quinapril prevents stroke both during and after the treatment period in stroke-prone spontaneously hypertensive rats. Am J Hypertens 1993 Nov;6(11 Pt 1):951-9.
19. Chen HC, Guh JY, Chang JM, Hsieh MC, Shin SJ, Lai YH. Role of lipid control in diabetic nephropathy. Kidney Int Suppl 2005; 94: S60-S2.
20. Danesh FR, Kanwar YS. Modulatory effects of HMG-CoA reductase inhibitors in diabetic microangiopathy. FASEB J 2004;18(7):805-15.
21. Mason JC, Ahmed Z, Mankoff R, et al. Statin-induced expression of decay-accelerating factor protects vascular endothelium against complement-mediated injury. Cir Res 2002; 91: 696-703.
22. Laufs U, Custodis F, Bohm M. HMG-CoA reductase inhibitors in chronic heart failure: potential mechanisms of benefit and risk. Drugs 2006;66(2):145-54.
23. Gueler F, Park JK, Rong S, et al. Statins attenuate ischemia reperfusion injury by inducing hemo oxygenase-1 in infiltrating macrophages. Am J Pathol 2007; 170: 1192-9.
24. Skaletz-Rorowski A, Walsh K. Statin therapy and angiogenesis. Curr Opin Lipidol 2003; 14(6):599-603.
25. D'Amico G. Statins and renal diseases: from primary prevention to renal replacement therapy. J Am Soc Nephrol 2006; 17(Suppl2) S148-S52.
26. Rosenson RS. Low high-density lipoprotein cholesterol and cardiovascular disease: risk reduction with statin therapy. Am Heart J 2006;151(3):556-63.
27. Chen J, Zhang C, Jiang H, et al. Atorvastatin induction on VEGF and BDNF promotes brain plasticity after stroke in mice. J Cereb Blood Flow Metab 2005; 25: 281-90.
28. Takahashi HK, Weitz-Schmidt G, Iwagaki H, et al. Hypothesis: the antitunor activities of statins may be mediated by IL-18. J Leukoc Biol 2006; 80: 215-6.
29. Campese VM, Park J. HMG-CoA reductase inhibitors and the kidney. Kidney Int 2007; 71:1215-22.
30. Verma A, Ranganna KM, Reddy RS, Verma M, Gordon N. Effect of xxxx on C-reactive protein and renal function in patients with chronic kidney disease. J Am Cardiol 2005; 96: 1290-2.
31. Steffens S, Mach F. Drug insight: immunomodulatory effects of statins- potential benefits for renal patients. Nat Clin Pract Nephrol 2006, 2: 378-87.
32. Kasiske BL, Heim-Duthoy KL, Singer GG, et al. The effects of lipid-lowering agents on acute renal allograft rejection. Transplantation 2001; 12: 223-7.
33. Campbell MJ, Esserman LJ, Zhou Y, et al. Breast cancer growth prevention by statins. Cancer Res 2006; 66: 8707-14.
34. Sivaprasad U, Abbas T, Dutta A. Differential efficacy of 3-hydroxy-3-methylglutaryl CoA reductase inhibitors on the cell cycle of prostate cancer cells. Mol Cancer Ther 2006, 5: 2310-6.
35. Palinski W, Tsimikas S. Immunomodulatory effects of statins: mechanisms and potential impact on arteriosclerosis. J Am Soc Nephrol 2002; 13: 1673-81.
36. Heusinger-Ribeiro J, Fischer B, Goppelt-Strube M, et al. Differential effects of simvastatin on mesangial cells. Kidney Int 2004; 66: 187-95.
37. Buemi M, Nostra L, Crasci E, et al. Statins in nephrotic syndrome: a new weapon against tissue injury. Med Res Rev 2005;25(6):587-609.
38. Tonelly M, Moye L, Sacks FM, Cole T, Curhan GC. Cholesterol and recurrent events trial investigators. Effect of pravastatin on loss of renal function in people with moderate chronic renal insufficiency and cardiovascular disease. J Am Soc Nephrol 2003; 14: 1605-13.
39. Nakamura T, Ushiyama C, Hirokawa K, et al. Effect of cerivastatin on proteinuria and urinary podocytes in patients with chronic glomerulonephritis. Nephrol Dial Transplant 2002; 17: 798-802.
40. Weiner DE, Sarank MJ. Managing dyslipidemia in chronic kidney disease. J Gen Intern Med 2004; 19: 1045-52.
41. Tonelly M, Moye L, Sacks FM, Cole T, Curhan GC. Effect of pravastatin on loss of renal function in people with moderate chronic renal insufficiency and cardiovascular disease. J Am Soc Nephrol 2003; 14: 1605-13.
42. Agrawal R. Statin induced proteinuria: renal injury or renoprotection?. J Am Soc Nephrol 2004; 15: 2502.
43. Chen JC, Huang KC, Lin WW. HMG-CoA reductase inhibitors upregulate heme oxygenase-1 expression in murine RAW264.7 macrophages via ERK, p38 MAPK and protein kinase G pathways. Cell Signal 2006;18(1):32-9.
44. Yoshimura A, Nemoto T, Segenoya Y, et al. Effect of simvastatin on proliferative nephritis and cell-cycle protein expression. Kidney Int 1999 (Suppl 7); S84-S7.
45. Vrtovsnik F, Couette S, Prie D, Lallemand D, Friedlander G. Lovastatin-induced inhibition of renal epithelial tubular cell proliferation involves a p21ras activated AP-1 dependent pathway. Kidney Int 1997; 52: 1016-27.
46. Bussolati B, Deregibus MC, Fonsato V, et al. Statins prevent oxidized LDL-induced injury of glomerular podocytes by activating the phosphatidylinositol 3-kinase/AKT-signaling pathway. J Am Soc Nephrol 2005; 16: 1936-47.
47. Schindler R. Causes and therapy of microinflammation in renal failure. Nephrol Dial. Transplant 2004, 19 (suppl 5): v34-v40.
48. Elisaf M, Mikhailidis DP. Statins and renal function. Angiology 2002; 53(5):493-502.
49. Yasuda H, Yuen PS, Hu X, Zhou H, Star RA. Simvastatin improves sepsis-induced mortality and acute kidney injury via renal vascular effects. Kidney Int 2006; 69: 1535-42.
50. Christensen M, Su AW, Snyder RW, et al. Simvastatin protection against acute immune-mediated glomerulonephritis in mice. Kidney Int 2006, 69:457-63.
51. GuL, Ni Z, Qian J, Tomino Y. Pravastatin inhibits carboxymethyllysine- induced monocyte chemoattractant protein 1 expression in podocytes via prevention of signalling events. Nephron. Exp Nephrol 2007; 106: 1-10.
52. Massy ZA, Andrejak M. The interest of statins in nephrology. Presse Med 2004 9;33(17):1207-12.
53. Kim SI, Han DC, Lee HB. Lovastatin inhibits TGF-beta1 expression in diabetic rat glomeruli and cultured rat mesangial cels. J Am Soc Nephrol 2000; 11:80-7.
54. Holdaas H, Fellstrom B, Jardine AG; on behalf of the ALERT study group. Clinical practice guidelines for managing dyslipidemias in kidney transplant patients: lessons to be learnt from the assessment of Lescol in renal transplantation (ALERT) trial. Am J Transplant 2005;5(6):1574-5.
55. Panichi V, Paoletti S, Mantuano E, et al. In vitro and in vivo effects of simvastatin on inflammatory markers in pre-dialysis patients. Nephrol Dial Transplant 2006; 21:337-44.
56. Sandhu S, Wiebe N, Fried LF, Tonelly M. Statins for improving renal outcomes: a meta-analysis J Am Soc Nephrol 2006; 17: 2006-16.
57. Levi M. Do statins have a beneficial effect on the kidney. Nat Clin Practice Nephrology 2006; 2: 666-7.
58. Ozsoy RC, van der Steeg WA, Kastelein JJP, Arisz L, Koopman MG. Dyslipidaemia as predictor of progressive renal failure and the impact of treatment with atorvastatin. Nephrol Dial Transplant 2007; 22:1578-86.
59. Liao JK. Clinical implications for statin pleiotropy. Curr Opin Lipidol 2005;16(6):624-9.
60. Chen HC, Guh JY, Shin SJ, Lai YH. Pravastatin suppress superoxide and fibronectin production of glomerular mesangial cells induced by oxidized-LDL and high glucose. Atherosclerosis 2002; 160: 141-6.
61. Endres M. Statins and stroke. J Cereb Blood Flow Metab. 2005 Sep;25(9):1093-110.
62. Sacco RL, Liao JK. Drugs insight: statins and stroke. Nat Clin Pract Cardiovasc Med 2005; 2:576-84.
63. Zhou B, Teramukai S, Fukushima M. Prevention and treatment of dementia or Alzheimer's disease by statins: a meta-analysis. Dement Geriatr Cogn Disord 2007;23(3):194-201.
64. Sieff CA. Regulation of erythropoiesis. Up to Date 2006, 14.1.
65. Maxwell PH, Osmond MK, Pugh CW, et al. Identification of the renal erythropoietin- producing cells using transgenic mice. Kidney Int 1993; 44: 1149.
66. Loya F, Yang Y, Lin H, et al. Transgenic mice carrying the erythropoietin gene promoter linked to lacZ express the reporter in proximal convoluted tubule cells after hypoxia. Blood 1994; 84: 1831.
67. Sasaki P. Pleiotropic functions of erythropoietin. Intern Med 2003; 42:142-9.
68. Mulcahy L. The erythopoietin receptor. Semin Oncol 2001; 28(Suppl8): 19-23.
69. Yoshimura A, Arai K. Physician Education: The Erythtopoietin receptor and signal transduction. Oncologic 1996; 1: 337-9.
70. Sawyer ST, Jacobs-Helber SM. Unraveling distinct intracellular signals that promote survival and proliferation: study of erythropoietin, stem cell factor, and constitutive signaling in leukemic cells. J Hematother Stem Cell Res 2000;9(1):21-9.
71. van der Meer P, Voors AA, Lipsic E, et al. Erythropoietin in cardiovascular diseases. Eur Heart J 2004; 25(4):285-91.
72. Beleslin-Cokic BB, Cokic VP, Yu X, et al. Erythropoietin and hypoxia stimulate erythropoietin receptor and nitric oxide production by endothelial cells. Blood 2004;104(7):2073-80.
73. Jelkmann W., Wagner K. Beneficial and ominous aspects of the pleiotropic action of erythropoietin. Ann Hematol 2004; 83: 673-86.
74. Lappin TR, Maxwell P, Johnston PG. Epo's alter ego: erythropoietin has multiple actions. Stem Cells 2002; 20: 485-92.
75. Baker JE. Erythropoietin mimics ischemic preconditioning. Vascul Pharmacol 2005; 42(5-6):233-41.
76. Silverberg DS, Wexler D, Iaina A, et al. The interaction between heart failure and other heart diseases, renal failure and anemia. Semin Nephrol 2006; 26:296-306.
77. Peterson TE, Katusic ZS. EPO tecting the endothelium. Br J Pharmacol 2007; 150:823-5.
78. Ribatti D, Presta M, Vacca A, et al. Human erythropoietin induces a proangiogenic phenotype in cultured endothelial cells and stimulates neovascularisation in vivo. Blood 1999, 93: 2627-36.
79. Carlini RG, Reyes AA, Rothstein M. Recombinant human erythropoietin stimulates angiogenesis in vitro. Kidney Int 1995; 47: 740-5.
80. Nagai T, Akizawa T, Nakashima Y, et al. Effects of rHuEpo on cellular proliferation and endothelin-1 production in cultured endothelial cells. Nephrol Dial Transplant 1995; 10: 1814-9.
81. Carlini RG, Dusso AS, Obialo CI, et al. Recombinant human erythropoietin (rHuEpo) increases endothelin-1 release by endothelial cells. Kidney Int 1993; 43: 1010-4.
82. D'Uscio LV, Smith LA, Santham AV, et al. Essential role of endothelial nitric oxide synthase in vascular effects of erythropoietin. Hypertension 2007; 49: 1142-8.
83. Le Minh K, Klemm K, Abshagen K, et al. Attenuation of inflammation and apoptosis by pre- and post treatment of darbepoetin alpha in acute liver failure of mice. Am J Pathol 2007; 170:1954-63.
84. Katavetin P, Inaqi R, Miyata T, et al. Erythropoietin induces heme oxygenase expression and attenuates oxidative stress. Biochem Biophys Res Commun 2007; 359: 928-34.
85. Siren AL, Ehrenreich H. Erythropoietin- a novel concept for neuroprotection. Eur Arch Psychiatry Clin Neurosci 2001; 251: 179-84.
86. Maiese K, Li F, Chong Z. New avenues of exploration for erythropoietin. JAMA 2005; 293: 90-5.
87. Katz O, Gil L, Lifshitz L, et al. Erythropoietin enhances immune response in mice. Eur J Immunol 2007; 37: 1584-93.
88. Fiordaliso F, Chimenti S, Staszewsky L, et al. A nonerythropoietic derivative of erythropoietin protects the myocardium from ischemia-reperfusion injury. Proc Natl Acad Sci U S A 2005;102(6):2046-51.
89. Boogaerts M. Pleiotropic effects of erythropoietin in neuronal and vascular systems. Curr Med Res Opin 2006; 22 (Suppl 4):15-22.
90. Wright GL, Hanlon P, Amin K, et al. Erythropoietin receptor expression in adult rat cardiomyocytes is associated with an acute cardioprotective effect for recombinant erythropoietin during ischemia-reperfusion injury. FASEB J 2004;18(9):1031-3.
91. Prunier F, Pfister O, Hadri L, et al. Delayed erythropoietin therapy reduces post-MI cardiac remodeling only at a dose that mobilizes endothelial progenitor cells. Am J Physiol. Heart Circ Physiol 2007; 292(1):H522-9.
92. Namiuchi S, Kagoya Y, Ohta Y, et al. High serum erythropoietin level is associated with smaller infarct size in patients with acute myocardial infarction who undergo successful primary percutaneous coronary intervention. J Am Coll Cardiol 2005; 45: 1406-12.
93. Roger SD, McMahon LP, Clarkson A, et al. Effects of early and late intervention with epoetin alpha on left ventricular mass among patients with chronic kidney disease (stage 3 or 4): results of a randomized clinical trial. J Am Soc Nephrol 2004;15(1):148-56.
94. Macdougall IC, Temple RM, Kwan JT. Is early treatment of anaemia with epoetin-alpha beneficial to pre-dialysis chronic kidney disease patients? Results of a multicentre, open-label, prospective, randomized, comparative group trial. Nephrol Dial Transplant 2007;22(3):784-93.
95. Nagai A, Nakagawa E, Choi HB, et al. Erythropoietin and erythropoietin receptors in human CNS neurons, astrocytes, microglia, and oligodendrocytes grown in culture. J Neuropathol Exp Neurol 2001;60(4):386-92.
96. Bahlmann FH, de Groot K, Haller H, Fliser D. Erythropoietin: is it more than correcting anaemia? Nephrol Dial Transplant 2004; 19: 20-2.
97. Ehrenreich H, Hasselblatt M, Dembowski C, et al. Erythropoietin therapy for acute stroke is both safe and beneficial. Mol Med 2002; 8(8):495-505.
98. Noguchi CT, Asavaritikai P, Teng R, Jia Y. Role of erythropoietin in the brain. Crit Rev Oncol Hematol 2007 [Epub ahead of print].
99. Viviani B, Bartesaghi S, Corsini E, et al. Erythropoietin protects primary hippocampal neurons increasing the expression of brain-derived neurotrophic factor. J Neurochem 2005;93(2):412-21.
100. Buemi M, Cavallaro E, Floccari F, et al. The pleiotropic effects of erythropoietin in central nervous system. J Neuropathol Exp Neurol 2003; 62: 228-36.
101. Gorio A, Gokman N, Erbayraktar S, et al. Recombinant human erythropoietin counteracts secondary injury and markedly enhances neurological recovery from experimental spinal cord trauma. Proc Natl Acad Sci USA 2002; 99: 9450-5.
102. Springborg JB, Ma X, Rochart P, et al. A single subcutaneous bolus of erythropoietin nromalizaed cerbral blood floww autoregulation after subarachnoid haemorrhage in rats. Br J Pharmacol 2002; 135: 823-9.
103. Hasselblatt M, Ehrenreich H, Siren AL. The brain erythropoietin system and its potential for therapeutic exploitation in brain disease. J Neurosurg Anesthesiol 2006; 18: 132-8.
104. Leist M, Ghezzi P, Grasso G, et al. Derivaties of erythropoietin that are tissue protective but not erythropoietic. Science 2004; 305:239-42.
105. Ehrenreich H, Hasselblatt M, Dembovski C, et al. Erythropoietin therapy for acute stroke is both safe and beneficial. Mol Med 2002; 8: 495-505.
106. Meyers CA. Neurocognitive dysfunction in cancer patients. Oncology (Huntington) 2000; 14: 75-9.
107. Westenfelder C. Unexpected renal actions of erythropoietin. Exp Nephrol 2002;10(5-6):294-8.
108. Spandou E, Tsouchnikas I, Karkavelas G, et al. Erythropoietin attenuates renal injury in experimental acute renal failure ischaemic/ reperfusion model. Nephrol Dial Transplant, 2006; 21:330-6.
109. Johnson DW, Pat B, Vesey DA, et al. Delayed administration of darbepoetin or erythropoietin protects against ischemic acute renal injury and failure. Kidney Int 2006; 69:1806-13.
110. Vesey DA, Cheung C, Pat B, et al. Erythropoietin protects against ischaemic acute renal injury. Nephrol Dial Transplant 2004;19(2):348-55.
111. Lee SH, Li C, Lim SW, et al. Attenuation of interstitial inflammation and fibrosis by recombinant human erythropoietin in chronic cyclosporine nephropathy. Am J Nephrol 2005; 25(1):64-76.
112. Logar CM, Brinkkoetter PT, Krofft RD et al. Darbepoetin alfa protects podocytes from apoptosis in vitro and in vivo. Kidney Int 2007 [Epub ahead of print].
113. Park J, Gage BF, Vijayan A. Use of EPO in critically ill patients with acute renal failure requiring renal replacement therapy. Am J Kidney Dis 2005; 46(5): 791-8.
114. Strippoli GF, Craig JC, Manno C, Schena FP. Hemoglobin targets for the anemia of chronic kidney disease: a meta- analysis of randomized controlled trials. J Am Soc Nephrol 2004; 15: 3154.
115. Jones CH, Ridley L, Richardson D. Which EPO dose per week? Nephrol Dial Transplant 2002;17(10):1855.
116. Evans RW. Recombinant human erythropoietin and the quality of life of end-stage renal disease patients: a comparative analysis. Am J Kidney Dis 1991;18(4 Suppl 1):62-70.
117. Fink J, Blahut S, Reddy M, Light P. Use of erythropoietin before the initiation of dialysis and its impact on mortality. Am J Kidney Dis 2001 Feb;37(2):348-55.
118. Carrera F, Disney A, Molina M. Extended dosing intervals with erythropoiesis-stimulating agents in chronic kidney disease: a review of clinical data. Nephrol Dial Transplant 2007; 22 Suppl4: iv19-iv30.
119. Iaina A, Silverberg DS, Wexley D. Therapy insight: copngestive heart failure, chronic kidney disease and anemia, the cardioanemia renal syndrome. Natl Clin Parct Cardiovasc Med 2005; 2: 95-100.
120. Silverberg DS, Wexley D, Iaina A, et al. Anemia, chronic renal disease and congestive heart failure- the cardiorenal anemia syndrome: the need for cooperation between cardiologist and nephrologist. Int Urol Nephrol 2006; 38: 295-310.
121. Jie KE, Verhaar MC, Cramer MJ, et al. Erythropoietin and the cardiorenal syndrome: cellular mechanisms on the cardiorenal connectors. Am J Physiol Renal Physiol 2006; 291(5): F932-F44.
122. Faggiotto A, Paoletti R. Statins and blockers of the renin-angiotensin system. Vascular protection beyond their primary mode of action. Hypertension 1999; 34: 987-96.
123. Zoja C, Corna D, Camozzi D, et al. How to fully protect the kidney in a severe model of progressive nephropathy: multidrug approach. J Am Soc Nephrol 2002; 13: 2898-2908.
124. Gryglewski RJ, Uracz W, Swies J, et al. Comparison of endothelial pleiotropic actions of angiotensin converting enzyme inhibitors and statins. Am NY Acad Sci 2001; 947: 229-45.
125. Delbosc S, Cristol JP, Descomps B, Mimran A, Jover B. Simvastatin prevents angiotensin II-induced cardiac alteration and oxidative stress. Hypertension 2002; 40: 142-7.
126. Koh KK, Son JW, Ahn JY, et al. Simvastatin combined with ramipril treatment in hypercholesterolemic patients. Hypertension 2004; 44: 180-5.
127. Koh KK, Quon MJ, Han SH, et al. Additive beneficial effects of losartan combined with simvastatin in the treatment of hypercolesterolemic , hypertensive patients. Circulation 2004; 110(24):3687-92.
128. Zoja C, Corna D, Rottoli D, et al. Effect of combining ACE inhibitor and statin in severe experimental nephropathy. Kidney Int 2002; 61: 1635-45.
129. Lee SK, Jin SY, Han DC, Hwang SD, Lee HB. Effects of delayed treatment with enalapril and/or lovastatin on the progression of glomerulosclerosis in 5/6 nephrectomized rats. Nephrol Dial Transplant 1993;8(12):1338-43.
130. Saijonmaa O, Nyman T, Fyhrquist T. Atorvastatin inhibits angiotensin- converting enzyme induction in differentiating human macrophages. Am J Physiol Heart Circ Physiol 2007; 292: 1917-21.
131. Albitar S, Genin R, Fen-Chong M, Serveaux MO, Bourgeon B. High dose enalapril impairs the response to erythropoietin treatment in haemodialysis patients. Nephrol Dial Transplant 1998; 13: 1206-10.
132. Walter J. Does captopril decrease the effect of human recombinant erythropoietin in haemodialysis patients? Nephrol DialTransplant 1994; 8: 1428-31.
133. Hesse E, Sperschneider H, Stein G. Do ACE inhibitors influence the dose of human recombinant erythropoietin in dialysis patients? Nephrol Dial Transplant 1996; 11: 749-51.
134. Conlon PJ, Albers F, Butterly D, Schwab SJ. ACE inhibitors do not affect erythropoetin efficacy in haemodialysis patients. Nephrol DialTransplant 1994; 9: 1358.
135. Abu-.Alfa AK, Cruz DN, Perazella MA, Mahnensmith RL, Simon D, Bisa MJ. ACE inhibitors do not induce recombinat human erythropoietin resistance in haemodialysis patients. Am J Kidney Dis 2000; 35: 1076-82.
136. Chew CG, Weise MD, Disney APS. The effect of angiotensin II receptor antagonist on the exogenous erythropoietin requirment of haemodialysis patients. Nephrol Dial Transplant 1999; 14: 2047-9.
137. Piccoli A, Pastori G, Pierobon E, et al. Anti-renin-angiotensin-system drugs and development of anemia in chronic kidney disease. J Nephrol 2005; 18: 585-91.
138. Sanchez JA. ACE inhibitors do not decrease rHuEPO response in patients with end - stage renal failure. Nephrol Dial Transplant 1995; 10: 1476-7.
139. Schiff H, Lang SM. Angiotensin- converting enzyme inhibitors but not Angiotensin II AT1 receptors antagonist affect erythropoiesis in patients with anemia of end - stage renal disease. Nephron 1999;81:106-8.
140. Chlopicki S, Gryglewski R. Angiotensin converting enzyme (ACE) and hydroxy methyl glutaryl- Coa (HMG-CoA) reductase inhibitors in the forefront of pharmacology of endothelium. Pharmacological Reports 2006; 57: Suppl 86-96.
141. Boucher K, Siegel CS, Sharma P, et al. HMG-CoA reductase inhibitors induce apoptosis in pericytes. Microvasc Res 2006; 71: 91-102.