Oxidative stress as a common pathway to chronic tubulointerstitial injury in kidney allografts

American Journal of Physiology - Renal Physiology

Volumn 293, Issue 2, 2007, Pages

  Djamali, Arjang ^a,b  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Apoptosis; Blood oxygen leveldependent magnetic resonance imaging; Chronic allograft nephropathy; Epithelial to mesenchymal transition; Heat shock proteins; Hypoxia; Inflammation; Transplantation

Indexed keywords

ANTIOXIDANT; CYCLOSPORIN; IMMUNOSUPPRESSIVE AGENT; ISOPROSTANE; MYCOPHENOLIC ACID; RAPAMYCIN;

ANEMIA; APOPTOSIS; CHRONIC DISEASE; DIABETES MELLITUS; DYSLIPIDEMIA; HUMAN; HYPERTENSION; HYPOXEMIA; HYPOXIA; INFLAMMATION; INTERSTITIAL NEPHRITIS; INTERSTITIUM; KIDNEY ALLOGRAFT; KIDNEY TRANSPLANTATION; LIPID PEROXIDATION; MACROPHAGE; MONKEY; MYOFIBROBLAST; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PRIORITY JOURNAL; PROTEINURIA; REVIEW; TISSUE OXYGENATION;

EID: 34548419397     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00037.2007     Document Type: Review

References (112)

1. Anonymous. Routine vitamin supplementation to prevent cancer and cardiovascular disease: recommendations and rationale. Ann Intern Med 139: 51-55, 2003.
2. Abe M, O'Connor P, Kaldunski ML, Liang M, Roman RJ, Cowley AW Jr. Effect of sodium delivery on superoxide and nitric oxide in the medullary thick ascending limb. Am J Physiol Renal Physiol 291: F350-F357, 2006.
3. Adler S, Huang H, Wolin MS, Kaminski PM. Oxidant stress leads to impaired regulation of renal cortical oxygen consumption by nitric oxide in the aging kidney. J Am Soc Nephrol 15: 52-60, 2004.
4. Albrecht EW, Stegeman CA, Tiebosch AT, Tegzess AM, van Goor H. Expression of inducible and endothelial nitric oxide synthases, formation of peroxynitrite and reactive oxygen species in human chronic renal transplant failure. Am J Transplant 2: 448-453, 2002.
5. Albrecht EW, van Goor H, Smit-van Oosten A, Stegeman CA. Long-term dietary L-arginine supplementation attenuates proteinuria and focal glomerulosclerosis in experimental chronic renal transplant failure. Nitric Oxide 8: 53-58, 2003.
6. Allen DA, Harwood S, Varagunam M, Raftery MJ, Yaqoob MM. High glucose-induced oxidative stress causes apoptosis in proximal tubular epithelial cells and is mediated by multiple caspases. FASEB J 17: 908-910, 2003.
7. Arrigo AP, Firdaus WJ, Mellier G, Moulin M, Paul C, Diaz-Latoud C, Kretz-Remy C. Cytotoxic effects induced by oxidative stress in cultured mammalian cells and protection provided by Hsp27 expression. Methods 35: 126-138, 2005.
8. Arrigo AP, Virot S, Chaufour S, Firdaus W, Kretz-Remy C, Diaz-Latoud C. Hsp27 consolidates intracellular redox homeostasis by upholding glutathione in its reduced form and by decreasing iron intracellular levels. Antioxid Redox Signal 7: 414-422, 2005.
9. Azuma H, Nadeau KC, Ishibashi M, Tilney NL. Prevention of functional, structural, and molecular changes of chronic rejection of rat renal allografts by a specific macrophage inhibitor. Transplantation 60: 1577-1582, 1995.
10. Basnakian AG, Kaushal GP, Shah SV. Apoptotic pathways of oxidative damage to renal tubular epithelial cells. Antioxid Redox Signal 4: 915-924, 2002.
11. Beckman KB, Ames BN. The free radical theory of aging matures. Physiol Rev 78: 547-581, 1998.
12. Brezis M, Rosen S. Hypoxia of the renal medulla - its implications for disease. N Engl J Med 332: 647-655, 1995.
13. Brune B, Zhou J, von Knethen A. Nitric oxide, oxidative stress, and apoptosis. Kidney Int Suppl: S22-S24, 2003.
14. Burns WC, Twigg SM, Forbes JM, Pete J, Tikellis C, Thallas-Bonke V, Thomas MC, Cooper ME, Kantharidis P. Connective tissue growth factor plays an important role in advanced glycation end product-induced tubular epithelial-to-mesenchymal transition: implications for diabetic renal disease. J Am Soc Nephrol 17: 2484-2494, 2006.
15. Campise M, Bamonti F, Novembrino C, Ippolito S, Tarantino A, Cornelli U, Lonati S, Cesana BM, Ponticelli C. Oxidative stress in kidney transplant patients. Transplantation 76: 1474-1478, 2003.
16. Chabrashvili T, Tojo A, Onozato ML, Kitiyakara C, Quinn MT, Fujita T, Welch WJ, Wilcox CS. Expression and cellular localization of classic NADPH oxidase subunits in the spontaneously hypertensive rat kidney. Hypertension 39: 269-274, 2002.
17. Chade AR, Bentley MD, Zhu X, Rodriguez-Porcel M, Niemeyer S, mores-Arriaga B, Napoli C, Ritman EL, Lerman A, Lerman LO. Antioxidant intervention prevents renal neovascularization in hypercholesterolemic pigs. J Am Soc Nephrol 15: 1816-1825, 2004.
18. Chen CF, Tsai SY, Ma MC, Wu MS. Hypoxic preconditioning enhances renal superoxide dismutase levels in rats. J Physiol 552: 561-569, 2003.
19. Cho M, Hunt TK, Hussain MZ. Hydrogen peroxide stimulates macrophage vascular endothelial growth factor release. Am J Physiol Heart Circ Physiol 280: H2357-H2363, 2001.
20. Cochrane AL, Ricardo SD. Oxidant stress and regulation of chemokines in the development of renal interstitial fibrosis. Contrib Nephrol 139: 102-119, 2003.
21. Colvin RB. Chronic allograft nephropathy. N Engl J Med 349: 2288-2290, 2003.
22. Cornell LD, Colvin RB. Chronic allograft nephropathy. Curr Opin Nephrol Hypertens 14: 229-234, 2005.
23. Cristol JP, Vela C, Maggi MF, Descomps B, Mourad G. Oxidative stress and lipid abnormalities in renal transplant recipients with or without chronic rejection. Transplantation 65: 1322-1328, 1998.
24. Djamali A, Reese S, Oberley T, Hullett D, Becker B. Heat shock protein 27 in chronic allograft nephropathy: a local stress response. Transplantation 79: 1645-1657, 2005.
25. Djamali A, Reese S, Yracheta J, Oberley T, Hullett D, Becker B. Epithelial-to-mesenchymal transition and oxidative stress in chronic allograft nephropathy. Am J Transplant 5: 500-509, 2005.
26. Djamali A, Sadowski E, Muehrer R, Reese S, Smavatkul C, Vidyasagar A, Fain S, Lipscomb RC, Hullett DA, Samaniego-Picota M, Grist T, Becker B. BOLD-MRI assessment of intrarenal oxygenation and oxidative stress in patients with chronic kidney allograft dysfunction. Am J Physiol Renal Physiol 292: F513-F522, 2007.
27. Djamali A, Sadowski EA, Samaniego-Picota M, Fain SB, Muehrer RJ, Alford SK, Grist TM, Becker BN. Noninvasive assessment of early kidney allograft dysfunction by blood oxygen level-dependent magnetic resonance imaging. Transplantation 82: 621-628, 2006.
28. Djamali A, Samaniego M, Muth B, Muehrer R, Hofmann RM, Pirsch J, Howard A, Mourad G, Becker BN. Medical care of kidney transplant recipients after the first posttransplant year. Clin J Am Soc Nephrol 1: 623-640, 2006.
29. Eidelman RS, Hollar D, Hebert PR, Lamas GA, Hennekens CH. Randomized trials of vitamin E in the treatment and prevention of cardiovascular disease. Arch Intern Med 164: 1552-1556, 2004.
30. Epstein FH. Oxygen and renal metabolism. Kidney Int 51: 381-385, 1997.
31. Essawy M, Soylemezoglu O, Muchaneta-Kubara EC, Shortland J, Brown CB, el Nahas AM. Myofibroblasts and the progression of diabetic nephropathy. Nephrol Dial Transplant 12: 43-50, 1997.
32. Finkel T, Holbrook NJ. Oxidants, oxidative stress and the biology of ageing. Nature 408: 239-247, 2000.
33. Galletti P, Di Gennaro CI, Migliardi V, Indaco S, Della RF, Manna C, Chiodini P, Capasso G, Zappia V. Diverse effects of natural antioxidants on cyclosporin cytotoxicity in rat renal tubular cells. Nephrol Dial Transplant 20: 1551-1558, 2005.
34. Gottmann U, Oltersdorf J, Schaub M, Knoll T, Back WE, van der Woude FJ, Braun C. Oxidative stress in chronic renal allograft nephropathy in rats: effects of long-term treatment with carvedilol, BM 91.0228, or α-tocopherol. J Cardiovasc Pharmacol 42: 442-450, 2003.
35. Greenberg ER. Vitamin E supplements: good in theory, but is the theory good? Ann Intern Med 142: 75-76, 2005.
36. Griendling KK, Sorescu D, Ushio-Fukai M. NAD(P)H oxidase: role in cardiovascular biology and disease. Circ Res 86: 494-501, 2000.
37. Gutierrez J, Ballinger SW, Darley-Usmar VM, Landar A. Free radicals, mitochondria, and oxidized lipids: the emerging role in signal transduction in vascular cells. Circ Res 99: 924-932, 2006.
38. Ha H, Lee HB. Reactive oxygen species and matrix remodeling in diabetic kidney. J Am Soc Nephrol 14: S246-S249, 2003.
39. Haidara MA, Yassin HZ, Rateb M, Ammar H, Zorkani MA. Role of oxidative stress in development of cardiovascular complications in diabetes mellitus. Curr Vasc Pharmacol 4: 215-227, 2006.
40. Halloran PF, Melk A, Barth C. Rethinking chronic allograft nephropathy: the concept of accelerated senescence. J Am Soc Nephrol 10: 167-181, 1999.
41. Hertig A, Verine J, Mougenot B, Jouanneau C, Ouali N, Sebe P, Glotz D, Ancel PY, Rondeau E, Xu-Dubois YC. Risk factors for early epithelial to mesenchymal transition in renal grafts. Am J Transplant 6: 2937-2946, 2006.
42. Hildeman DA, Mitchell T, Kappler J, Marrack P. T cell apoptosis and reactive oxygen species. J Clin Invest 111: 575-581, 2003.
43. Himmelfarb J, McMonagle E. Albumin is the major plasma protein target of oxidant stress in uremia. Kidney Int 60: 358-363, 2001.
44. Himmelfarb J, McMonagle E, McMenamin E. Plasma protein thiol oxidation and carbonyl formation in chronic renal failure. Kidney Int 58: 2571-2578, 2000.
45. Himmelfarb J, Stenvinkel P, Ikizler TA, Hakim RM. The elephant in uremia: oxidant stress as a unifying concept of cardiovascular disease in uremia. Kidney Int 62: 1524-1538, 2002.
46. Ishii Y, Sawada T, Kubota K, Fuchinoue S, Teraoka S, Shimizu A. Injury and progressive loss of peritubular capillaries in the development of chronic allograft nephropathy. Kidney Int 67: 321-332, 2005.
47. Iwano M, Plieth D, Danoff TM, Xue C, Okada H, Neilson EG. Evidence that fibroblasts derive from epithelium during tissue fibrosis. J Clin Invest 110: 341-350, 2002.
48. Jay D, Hitomi H, Griendling KK. Oxidative stress and diabetic cardiovascular complications. Free Radic Biol Med 40: 183-192, 2006.
49. Kalluri R, Neilson EG. Epithelial-mesenchymal transition and its implications for fibrosis. J Clin Invest 112: 1776-1784, 2003.
50. Kaplan B, Meier-Kriesche HU. Death after graft loss: an important late study endpoint in kidney transplantation. Am J Transplant 2: 970-974, 2002.
51. Kitiyakara C, Chabrashvili T, Chen Y, Blau J, Karber A, Aslam S, Welch WJ, Wilcox CS. Salt intake, oxidative stress, and renal expression of NADPH oxidase and superoxide dismutase. J Am Soc Nephrol 14: 2775-2782, 2003.
52. Klaunig JE, Kamendulis LM. The role of oxidative stress in carcino-genesis. Annu Rev Pharmacol Toxicol 44: 239-267, 2004.
53. Land W, Schneeberger H, Schleibner S, Illner WD, Abendroth D, Rutili G, Arfors KE, Messmer K. The beneficial effect of human recombinant superoxide dismutase on acute and chronic rejection events in recipients of cadaveric renal transplants. Transplantation 57: 211-217, 1994.
54. Le HM, Hegyi I, Cueni-Loffing D, Loffing J, Kaissling B. Characterization of renal interstitial fibroblast-specific protein 1/S100A4-positive cells in healthy and inflamed rodent kidneys. Histochem Cell Biol 123: 335-346, 2005.
55. Lee HB, Yu MR, Yang Y, Jiang Z, Ha H. Reactive oxygen species-regulated signaling pathways in diabetic nephropathy. J Am Soc Nephrol 14: S241-S245, 2003.
56. Lehoux G, Le GC, Stankova J, Rola-Pleszczynski M. Upregulation of expression of the chemokine receptor CCR5 by hydrogen peroxide in human monocytes. Mediators Inflamm 12: 29-35, 2003.
57. Liu Y. Epithelial to mesenchymal transition in renal fibrogenesis: pathologic significance, molecular mechanism, and therapeutic intervention. J Am Soc Nephrol 15: 1-12, 2004.
58. Lloberas N, Torras J, Herrero-Fresneda I, Cruzado JM, Riera M, Hurtado I, Grinyo JM. Postischemic renal oxidative stress induces inflammatory response through PAF and oxidized phospholipids. Prevention by antioxidant treatment. FASEB J 16: 908-910, 2002.
59. MacMicking J, Xie QW, Nathan C. Nitric oxide and macrophage function. Annu Rev Immunol 15: 323-350, 1997.
60. MacMillan-Crow LA, Crow JP, Kerby JD, Beckman JS, Thompson JA. Nitration and inactivation of manganese superoxide dismutase in chronic rejection of human renal allografts. Proc Natl Acad Sci USA 93: 11853-11858, 1996.
61. MacMillan-Crow LA, Cruthirds DL, Ahki KM, Sanders PW, Thompson JA. Mitochondrial tyrosine nitration precedes chronic allograft nephropathy. Free Radic Biol Med 31: 1603-1608, 2001.
62. Meier-Kriesche HU, Baliga R, Kaplan B. Decreased renal function is a strong risk factor for cardiovascular death after renal transplantation. Transplantation 75: 1291-1295, 2003.
63. Meng S, Roberts LJ, Cason GW, Curry TS, Manning RD Jr. Superoxide dismutase and oxidative stress in Dahl salt-sensitive and -resistant rats. Am J Physiol Regul Integr Comp Physiol 283: R732-R738, 2002.
64. Miller ER III, Pastor-Barriuso R, Dalal D, Riemersma RA, Appel LJ, Guallar E. Meta-analysis: high-dosage vitamin E supplementation may increase all-cause mortality. Ann Intern Med 142: 37-46, 2004.
65. Minuz P, Patrignani P, Gaino S, Degan M, Menapace L, Tommasoli R, Seta F, Capone ML, Tacconelli S, Palatresi S, Bencini C, Del VC, Mansueto G, Arosio E, Santonastaso CL, Lechi A, Morganti A, Patrono C. Increased oxidative stress and platelet activation in patients with hypertension and renovascular disease. Circulation 106: 2800-2805, 2002.
66. Nadeau KC, Azuma H, Tilney NL. Sequential cytokine dynamics in chronic rejection of rat renal allografts: roles for cytokines RANTES and MCP-1. Proc Natl Acad Sci USA 92: 8729-8733, 1995.
67. Nakanishi K, Tajima F, Nakamura A, Yagura S, Ookawara T, Yamashita H, Suzuki K, Taniguchi N, Ohno H. Effects of hypobaric hypoxia on antioxidant enzymes in rats. J Physiol 489: 869-876, 1995.
68. Nangaku M. Chronic hypoxia and tubulointerstitial injury: a final common pathway to end-stage renal failure. J Am Soc Nephrol 17: 17-25, 2006.
69. Nankivell BJ, Borrows RJ, Fung CL, O'Connell PJ, Allen RD, Chapman JR. The natural history of chronic allograft nephropathy. N Engl J Med 349: 2326-2333, 2003.
70. Nankivell BJ, Chapman JR. Chronic allograft nephropathy: current concepts and future directions. Transplantation 81: 643-654, 2006.
71. Neuhofer W, Muller E, Burger-Kentischer A, Fraek ML, Thurau K, Beck FX. Inhibition of NaCl-induced heat shock protein 72 expression renders MDCK cells susceptible to high urea concentrations. Pflügers Arch 437: 611-616, 1999.
72. Nickenig G, Harrison DG. The AT1-type angiotensin receptor in oxidative stress and atherogenesis. Part I: oxidative stress and atherogenesis. Circulation 105: 393-396, 2002.
73. Oberg BP, McMenamin E, Lucas FL, McMonagle E, Morrow J, Ikizler TA, Himmelfarb J. Increased prevalence of oxidant stress and inflammation in patients with moderate to severe chronic kidney disease. Kidney Int 65: 1009-1016, 2004.
74. Oldfield MD, Bach LA, Forbes JM, Nikolic-Paterson D, McRobert A, Thallas V, Atkins RC, Osicka T, Jerums G, Cooper ME. Advanced glycation end products cause epithelial-myofibroblast transdifferentiation via the receptor for advanced glycation end products (RAGE). J Clin Invest 108: 1853-1863, 2001.
75. Pallone TL. Is oxidative stress differentially regulated in the renal cortex and medulla? Nat Clin Pract Nephrol 2: 118-119, 2006.
76. Park J, Ha H, Seo J, Kim MS, Kim HJ, Huh KH, Park K, Kim YS. Mycophenolic acid inhibits platelet-derived growth factor-induced reactive oxygen species and mitogen-activated protein kinase activation in rat vascular smooth muscle cells. Am J Transplant 4: 1982-1990, 2004.
77. Pascual M, Theruvath T, Kawai T, Tolkoff-Rubin N, Cosimi AB. Strategies to improve long-term outcomes after renal transplantation. N Engl J Med 346: 580-590, 2002.
78. Pat B, Yang T, Kong C, Watters D, Johnson DW, Gobe G. Activation of ERK in renal fibrosis after unilateral ureteral obstruction: modulation by antioxidants. Kidney Int 67: 931-943, 2005.
79. Qi W, Chen X, Poronnik P, Pollock CA. The renal cortical fibroblast in renal tubulointerstitial fibrosis. Int J Biochem Cell Biol 38: 1-5, 2006.
80. Racusen LC, Solez K, Colvin RB, Bonsib SM, Castro MC, Cavallo T, Croker BP, Demetris AJ, Drachenberg CB, Fogo AB, Furness P, Gaber LW, Gibson IW, Glotz D, Goldberg JC, Grande J, Halloran PF, Hansen HE, Hartley B, Hayry PJ, Hill CM, Hoffman EO, Hunsicker LG, Lindblad AS, Yamaguchi Y. The Banff 97 working classification of renal allograft pathology. Kidney Int 55: 713-723, 1999.
81. Raj DS, Lim G, Levi M, Qualls C, Jain SK. Advanced glycation end products and oxidative stress are increased in chronic allograft nephropathy. Am J Kidney Dis 43: 154-160, 2004.
82. Ramachandiran S, Huang Q, Dong J, Lau SS, Monks TJ. Mitogen-activated protein kinases contribute to reactive oxygen species-induced cell death in renal proximal tubule epithelial cells. Chem Res Toxicol 15: 1635-1642, 2002.
83. Ramzy D, Rao V, Tumiati LC, Xu N, Miriuka S, Delgado D, Ross HJ. Role of endothelin-1 and nitric oxide bioavailability in transplant-related vascular injury: comparative effects of rapamycin and cyclosporine. Circulation 114: I214-I219, 2006.
84. Rhyu DY, Yang Y, Ha H, Lee GT, Song JS, Uh ST, Lee HB. Role of reactive oxygen species in TGF-β1-induced mitogen-activated protein kinase activation and epithelial-mesenchymal transition in renal tubular epithelial cells. J Am Soc Nephrol 16: 667-675, 2005.
85. Robertson H, Ali S, McDonnell BJ, Burt AD, Kirby JA. Chronic renal allograft dysfunction: the role of T cell-mediated tubular epithelial to mesenchymal cell transition. J Am Soc Nephrol 15: 390-397, 2004.
86. Rodriguez-Iturbe B, Vaziri ND, Herrera-Acosta J, Johnson RJ. Oxidative stress, renal infiltration of immune cells, and salt-sensitive hypertension: all for one and one for all. Am J Physiol Renal Physiol 286: F606-F616, 2004.
87. Romero F, Rodriguez-Iturbe B, Parra G, Gonzalez L, Herrera-Acosta J, Tapia E. Mycophenolate mofetil prevents the progressive renal failure induced by 5/6 renal ablation in rats. Kidney Int 55: 945-955, 1999.
88. Rosenberger C, Pratschke J, Rudolph B, Heyman SN, Schindler R, Babel N, Eckardt KU, Frei U, Rosen S, Reinke P. Immunohistochemical detection of hypoxia-inducible factor-1α in human renal allograft biopsies. J Am Soc Nephrol 18: 343-351, 2007.
89. Sakai M, Tsukada T, Harris RC. Oxidant stress activates AP-1 and heparin-binding epidermal growth factor-like growth factor transcription in renal epithelial cells. Exp Nephrol 9: 28-39, 2001.
90. Shihabi A, Li WG, Miller FJ Jr, Weintraub NL. Antioxidant therapy for atherosclerotic vascular disease: the promise and the pitfalls. Am J Physiol Heart Circ Physiol 282: H797-H802, 2002.
91. Simic-Ogrizovic S, Simic T, Reljic Z, Markovic S, Blagojevic R, Radivojevic D, Lezaic V, Djukanovic L, Mimic-Oka J. Markers of oxidative stress after renal transplantation. Transpl Int 11, Suppl1: S125-S129, 1998.
92. Simmons EM, Langone A, Sezer MT, Vella JP, Recupero P, Morrow JD, Ikizler TA, Himmelfarb J. Effect of renal transplantation on biomarkers of inflammation and oxidative stress in end-stage renal disease patients. Transplantation 79: 914-919, 2005.
93. Stanner SA, Hughes J, Kelly CN, Buttriss J. A review of the epidemiological evidence for the 'antioxidant hypothesis'. Public Health Nutr 7: 407-422, 2004.
94. Sugimoto H, Mundel TM, Kieran MW, Kalluri R. Identification of fibroblast heterogeneity in the tumor microenvironment. Cancer Biol Ther 5: 2006.
95. Tariq M, Morais C, Sobki S, Al SM, Al KA. N-acetylcysteine attenuates cyclosporin-induced nephrotoxicity in rats. Nephrol Dial Transplant 14: 923-929, 1999.
96. + T regulatory cell infiltrates. J Immunol 172: 5753-5764, 2004.
97. Trevisan R, Dodesini AR, Lepore G. Lipids and renal disease. J Am Soc Nephrol 17: S145-S147, 2006.
98. Ueda S, Masutani H, Nakamura H, Tanaka T, Ueno M, Yodoi J. Redox control of cell death. Antioxid Redox Signal 4: 405-414, 2002.
99. Vaziri ND, Dicus M, Ho ND, Boroujerdi-Rad L, Sindhu RK. Oxidative stress and dysregulation of superoxide dismutase and NADPH oxidase in renal insufficiency. Kidney Int 63: 179-185, 2003.
100. Vaziri ND, Rodriguez-Iturbe B. Mechanisms of disease: oxidative stress and inflammation in the pathogenesis of hypertension. Nat Clin Pract Nephrol 2: 582-593, 2006.
101. Verzola D, Bertolotto MB, Villaggio B, Ottonello L, Dallegri F, Salvatore F, Berruti V, Gandolfo MT, Garibotto G, Deferrari G. Oxidative stress mediates apoptotic changes induced by hyperglycemia in human tubular kidney cells. J Am Soc Nephrol 15, Suppl1: S85-S87, 2004.
102. Vongwiwatana A, Tasanarong A, Rayner DC, Melk A, Halloran PF. Epithelial to mesenchymal transition during late deterioration of human kidney transplants: the role of tubular cells in fibrogenesis. Am J Transplant 5: 1367-1374, 2005.
103. Vos IH, Joles JA, Rabelink TJ. The role of nitric oxide in renal transplantation. Semin Nephrol 24: 379-388, 2004.
104. Wolfe RA, Ashby VB, Milford EL, Ojo AO, Ettenger RE, Agodoa LY, Held PJ, Port FK. Comparison of mortality in all patients on dialysis, patients on dialysis awaiting transplantation, and recipients of a first cadaveric transplant. N Engl J Med 341: 1725-1730, 1999.
105. Yusuf S, Sleight P, Pogue J, Bosch J, Davies R, Dagenais G. Effects of an angiotensin-converting-enzyme inhibitor, ramipril, on cardiovascular events in high-risk patients. The Heart Outcomes Prevention Evaluation Study Investigators. N Engl J Med 342: 145-153, 2000.
106. Zandi-Nejad K, Eddy AA, Glassock RJ, Brenner BM. Why is proteinuria an ominous biomarker of progressive kidney disease? Kidney Int Suppl: S76-S89, 2004.
107. Zavadil J, Bottinger EP. TGF-β and epithelial-to-mesenchymal transitions. Oncogene 24: 5764-5774, 2005.
108. Zhan CD, Sindhu RK, Pang J, Ehdaie A, Vaziri ND. Superoxide dismutase, catalase and glutathione peroxidase in the spontaneously hypertensive rat kidney: effect of antioxidant-rich diet. J Hypertens 22: 2025-2033, 2004.
109. Zhan CD, Sindhu RK, Vaziri ND. Up-regulation of kidney NAD(P)H oxidase and calcineurin in SHR: reversal by lifelong antioxidant supplementation. Kidney Int 65: 219-227, 2004.
110. Zhang Y, Huang L, Zhang J, Moskophidis D, Mivechi NF. Targeted disruption of hsf1 leads to lack of thermotolerance and defines tissue-specific regulation for stress-inducible Hsp molecular chaperones. J Cell Biochem 86: 376-393, 2002.
111. Zhu JW, Yu BM, Ji YB, Zheng MH, Li DH. Upregulation of vascular endothelial growth factor by hydrogen peroxide in human colon cancer. World J Gastroenterol 8: 153-157, 2002.
112. Zoja C, Morigi M, Remuzzi G. Proteinuria and phenotypic change of proximal tubular cells. J Am Soc Nephrol 14, Suppl1: S36-S41, 2003.