Journal of Molecular Medicine

, Volume 82, Issue 2, pp 91–101

Leukocyte recruitment and acute renal failure



Despite advances in medical technology, acute renal failure (ARF) still represents a major challenge in clinical medicine, as morbidity and mortality have remained unchanged over the past two decades. The pathophysiology of ARF is highly complex and only poorly understood; new insights into the pathophysiology of ARF are therefore of utmost importance to develop better understanding and therapies. Acute tubular necrosis (ATN) is the predominant cause of ARF and often arises as a consequence of septic, toxic, or ischemic insults. The recruitment of leukocytes into the kidney has recently emerged as a key event in the development of experimental ischemic and septic ARF. A few descriptive clinical studies support this idea. However, the clinical relevance of various animal models remains unclear, as does the importance of different leukocyte subsets, and even methodological aspects as how to quantify renal leukocyte recruitment. This review summarizes and critically evaluates experimental findings that provide insight into the role of leukocytes and their recruitment during ARF. We aim to provide a valid description of ARF, illustrate animal models of ARF, review qualitative and quantitative methods to assess renal leukocyte recruitment, and discuss the components of the leukocyte recruitment cascade and their role in ARF.


Kidney failure, acute Leukocytes Neutrophils 



Acute renal failure


Acute tubular necrosis


Intercellular adhesion molecule








Melanocyte-stimulating hormone


Platelet-activating factor




  1. 1.
    Singri N, Ahya SN, Levin ML (2003) Acute renal failure. JAMA 289:747–751PubMedGoogle Scholar
  2. 2.
    Nash K, Hafeez A, Hou S (2002) Hospital-acquired renal insufficiency. Am J Kidney Dis 39:930–936PubMedGoogle Scholar
  3. 3.
    Liano F, Junco E, Pascual J, Madero R, Verde E, the Madrid Acute Renal Failure Study Group (1998) The spectrum of acute renal failure in the intensive care unit compared with that seen in other settings. Kidney Int S66:S16–S24Google Scholar
  4. 4.
    Sheridan AM, Bonventre JV (2001) Pathophysiology of ischemic acute renal failure. Contrib Nephrol 7–21Google Scholar
  5. 5.
    Okusa MD (2002) The inflammatory cascade in acute ischemic renal failure. Nephron 90:133–138CrossRefPubMedGoogle Scholar
  6. 6.
    Solez K, Kramer EC, Fox JA, Heptinstall RH (1974) Medullary plasma flow and intravascular leukocyte accumulation in acute renal failure. Kidney Int 6:24–37PubMedGoogle Scholar
  7. 7.
    Solez K, Morel-Maroger L, Sraer JD (1979) The morphology of “acute tubular necrosis” in man: analysis of 57 renal biopsies and a comparison with the glycerol model. Medicine (Baltimore) 58:362–376Google Scholar
  8. 8.
    Koo DD, Welsh KI, McLaren AJ, Roake JA, Morris PJ, Fuggle SV (1999) Cadaver versus living donor kidneys: impact of donor factors on antigen induction before transplantation. Kidney Int 56:1551–1559PubMedGoogle Scholar
  9. 9.
    Koo DD, Welsh KI, Roake JA, Morris PJ, Fuggle SV (1998) Ischemia/reperfusion injury in human kidney transplantation: an immunohistochemical analysis of changes after reperfusion. Am J Pathol 153:557–566PubMedGoogle Scholar
  10. 10.
    Singbartl K, Ley K (2000) Protection from ischemia-reperfusion induced severe acute renal failure by blocking E-selectin. Crit Care Med 28:2507–2514PubMedGoogle Scholar
  11. 11.
    Singbartl K, Green SA, Ley K (2000) Blocking P-selectin protects from ischemia/reperfusion-induced acute renal failure. FASEB J 14:48–54PubMedGoogle Scholar
  12. 12.
    Chiao H, Kohda Y, Mcleroy P, Craig L, Housini I, Star RA (1997) Alpha-melanocyte-stimulating hormone protects against renal injury after ischemia in mice and rats. J Clin Invest 99:1165–1172PubMedGoogle Scholar
  13. 13.
    Okusa MD, Linden J, Huang L, Rieger JM, Macdonald TL, Huynh LP (2000) A (2A) adenosine receptor-mediated inhibition of renal injury and neutrophil adhesion. Am J Physiol 279:F809–F818Google Scholar
  14. 14.
    Lindner JR, Song J, Xu F, Klibanov AL, Singbartl K, Ley K, Kaul S (2000) Noninvasive ultrasound imaging of inflammation using microbubbles targeted to activated leukocytes. Circulation 102:2745–2750PubMedGoogle Scholar
  15. 15.
    Singbartl K, Forlow SB, Ley K (2001) Platelet, but not endothelial, P-selectin is critical for neutrophil-mediated acute postischemic renal failure. FASEB J 15:2337–2344PubMedGoogle Scholar
  16. 16.
    Willinger CC, Schramek H, Pfaller K, Pfaller W (1992) Tissue distribution of neutrophils in postischemic acute renal failure. Virchows Arch B 62:237–243PubMedGoogle Scholar
  17. 17.
    Takada M, Nadeau KC, Shaw GD, Marquette KA, Tilney NL (1997) The cytokine-adhesion molecule cascade in ischemia/reperfusion injury of the rat kidney. Inhibition by a soluble P-selectin ligand. J Clin Invest 99:2682–2690PubMedGoogle Scholar
  18. 18.
    Hayashi H, Imanishi N, Ohnishi M, Tojo SJ (2001) Sialyl Lewis X and anti-P-selectin antibody attenuate lipopolysaccharide-induced acute renal failure in rabbits. Nephron 87:352–360PubMedGoogle Scholar
  19. 19.
    Cunningham PN, Dyanov HM, Park P, Wang J, Newell KA, Quigg RJ (2002) Acute renal failure in endotoxemia Is caused by TNF acting directly on TNF receptor-1 in kidney. J Immunol 168:5817–5823PubMedGoogle Scholar
  20. 20.
    Khan RZ, Badr KF (1999) Endotoxin and renal function: perspectives to the understanding of septic acute renal failure and toxic shock. Nephrol Dial Transplant 14:814–818PubMedGoogle Scholar
  21. 21.
    De Vriese AS (2003) Prevention and treatment of acute renal failure in sepsis. J Am Soc Nephrol 14:792–805Google Scholar
  22. 22.
    Hollenberg SM, Dumasius A, Easington C, Colilla SA, Neumann A, Parrillo JE (2001) Characterization of a hyperdynamic murine model of resuscitated sepsis using echocardiography. Am J Respir Crit Care Med 164:891–895Google Scholar
  23. 23.
    Cartmell T, Mitchell D, Lamond FJ, Laburn HP (2002) Route of administration differentially affects fevers induced by Gram-negative and Gram-positive pyrogens in rabbits. Exp Physiol 87:391–399PubMedGoogle Scholar
  24. 24.
    Deitch EA (1998) Animal models of sepsis and shock: a review and lessons learned. Shock 9:1–11Google Scholar
  25. 25.
    Maier S, Emmanuilidis K, Entleutner M, Zantl N, Werner M, Pfeffer K, Heidecke CD (2000) Massive chemokine transcription in acute renal failure due to polymicrobial sepsis. Shock 14:187–192PubMedGoogle Scholar
  26. 26.
    Burne-Taney MJ, Kofler J, Yokota N, Weisfeldt M, Traystman RJ, Rabb H (2003) Acute renal failure after whole body ischemia is characterized by inflammation and T cell-mediated injury. Am J Physiol 285:F87–F94Google Scholar
  27. 27.
    Bishop MJ, Kowalski TF, Guidotti SM, Harlan JM (1992) Antibody against neutrophil adhesion improves reperfusion and limits alveolar infiltrate following unilateral pulmonary artery occlusion. J Surg Res 52:199–204PubMedGoogle Scholar
  28. 28.
    Paller MS (1989) Effect of neutrophil depletion on ischemic renal injury in the rat. J Lab Clin Med 113:379–386PubMedGoogle Scholar
  29. 29.
    Thornton MA, Winn R, Alpers CE, Zager RA (1989) An evaluation of the neutrophil as a mediator of in vivo renal ischemic-reperfusion injury. Am J Pathol 135:509–515PubMedGoogle Scholar
  30. 30.
    Chaudhuri A, Nielsen S, Elkjaer ML, Zbrzezna V, Fang F, Pogo AO (1997) Detection of Duffy antigen in the plasma membranes and caveolae of vascular endothelial and epithelial cells of nonerythroid organs. Blood 89:701–712PubMedGoogle Scholar
  31. 31.
    Ysebaert DK, De Greef KE, Vercauteren SR, Ghielli M, Verpooten GA, Eyskens EJ, De Broe ME (2000) Identification and kinetics of leukocytes after severe ischaemia/reperfusion renal injury. Nephrol Dial Transplant 15:1562–1574PubMedGoogle Scholar
  32. 32.
    Kelly KJ, Williams WW. J, Colvin RB, Meehan SM, Springer TA, Gutierrez-Ramos JC, Bonventre JV (1996) Intercellular adhesion molecule-1-deficient mice are protected against ischemic renal injury. J Clin Invest 97:1056–1063PubMedGoogle Scholar
  33. 33.
    Bradley PP, Priebat DA, Christensen RD, Rothstein G (1982) Measurement of cutaneous inflammation: estimation of neutrophil content with an enzyme marker. J Invest Dermatol 78:206–209PubMedGoogle Scholar
  34. 34.
    Bos A, Wever R, Roos D (1978) Characterization and quantification of the peroxidase in human monocytes. Biochim Biophys Acta 525:37–44PubMedGoogle Scholar
  35. 35.
    Barone FC, Hillegass LM, Tzimas MN, Schmidt DB, Foley JJ, White RF, Price WJ, Feuerstein GZ, Clark RK, Griswold DE, (1995) Time-related changes in myeloperoxidase activity and leukotriene B4 receptor binding reflect leukocyte influx in cerebral focal stroke. Mol Chem Neuropathol 24:13–30PubMedGoogle Scholar
  36. 36.
    Hillegass LM, Griswold DE, Brickson B, Albrightson-Winslow C (1990) Assessment of myeloperoxidase activity in whole rat kidney. J Pharmacol Methods 24:285–295PubMedGoogle Scholar
  37. 37.
    Ormrod DJ, Harrison GL, Miller TE (1987) Inhibition of neutrophil myeloperoxidase activity by selected tissues. J Pharmacol Methods 18:137–142PubMedGoogle Scholar
  38. 38.
    Grisham MB, Benoit JN, Granger DN (1990) Assessment of leukocyte involvement during ischemia and reperfusion of intestine. Methods Enzymol 186:729–742PubMedGoogle Scholar
  39. 39.
    Schierwagen C, Bylund-Fellenius AC, Lundberg C (1990) Improved method for quantification of tissue PMN accumulation measured by myeloperoxidase activity. J Pharmacol Methods 23:179–186PubMedGoogle Scholar
  40. 40.
    Goor H van, Fidler V, Weening JJ, Grond J (1991) Determinants of focal and segmental glomerulosclerosis in the rat after renal ablation. Evidence for involvement of macrophages and lipids. Lab Invest 64:754–765PubMedGoogle Scholar
  41. 41.
    Lemay S, Rabb H, Postler G, Singh AK (2000) Prominent and sustained up-regulation of gp130-signaling cytokines and the chemokine MIP-2 in murine renal ischemia-reperfusion injury. Transplantation 69:959–963PubMedGoogle Scholar
  42. 42.
    Zwacka RM, Zhang Y, Halldorson J, Schlossberg H, Dudus L, Engelhardt JF (1997) CD4 (+) T-lymphocytes mediate ischemia/reperfusion-induced inflammatory responses in mouse liver. J Clin Invest 100:279–289PubMedGoogle Scholar
  43. 43.
    Burne MJ, Daniels F, El Ghandour A, Mauiyyedi S, Colvin RB, O’Donnell MP, Rabb H (2001) Identification of the CD4 (+) T cell as a major pathogenic factor in ischemic acute renal failure. J Clin Invest 108:1283–1290PubMedGoogle Scholar
  44. 44.
    Rabb H, Daniels F, O’Donnell M, Haq M, Saba SR, Keane W, Tang WW (2000) Pathophysiological role of T lymphocytes in renal ischemia-reperfusion injury in mice. Am J Physiol 279:F525–F531Google Scholar
  45. 45.
    Park P, Haas M, Cunningham PN, Bao L, Alexander JJ, Quigg RJ (2002) Injury in renal ischemia-reperfusion is independent from immunoglobulins and T lymphocytes. Am J Physiol 282:F352Google Scholar
  46. 46.
    Shultz LD, Lang PA, Christianson SW, Gott B, Lyons B, Umeda S, Leiter E, Hesselton R, Wagar EJ, Leif JH, Kollet O, Lapidot T, Greiner DL (2000) NOD/LtSz-Rag1null mice: an immunodeficient and radioresistant model for engraftment of human hematolymphoid cells, HIV infection, and adoptive transfer of NOD mouse diabetogenic T cells. J Immunol 164:2496–2507PubMedGoogle Scholar
  47. 47.
    Asakura A, Rudnicki MA (2002) Side population cells from diverse adult tissues are capable of in vitro hematopoietic differentiation. Exp Hematol 30:1339–1345PubMedGoogle Scholar
  48. 48.
    Lindner JR, Coggins MP, Kaul S, Klibanov AL, Brandenburger GH, Ley K (2000) Microbubble persistence in the microcirculation during ischemia/reperfusion and inflammation is caused by integrin- and complement-mediated adherence to activated leukocytes. Circulation 101:668–675PubMedGoogle Scholar
  49. 49.
    Lindner JR (2001) Assessment of inflammation with contrast ultrasound. Prog Cardiovasc Dis 44:111–120PubMedGoogle Scholar
  50. 50.
    Butcher EC (1991) Leukocyte-endothelial cell recognition: three (or more) steps to specificity and diversity. Cell 67:1033–1036PubMedGoogle Scholar
  51. 51.
    Springer TA (1995) Traffic signals on endothelium for lymphocyte recirculation and leukocyte emigration. Annu Rev Physiol 57:827–872PubMedGoogle Scholar
  52. 52.
    Kubes P (2002) The complexities of leukocyte recruitment. Semin Immunol 14:65–72PubMedGoogle Scholar
  53. 53.
    Patel KD, Cuvelier SL, Wiehler S (2002) Selectins: critical mediators of leukocyte recruitment. Semin Immunol 14:73–81PubMedGoogle Scholar
  54. 54.
    Yang J, Hirata T, Croce K, Merrill-Skoloff G, Tchernychev B, Williams E, Flaumenhaft R, Furie BC, Furie B (1999) Targeted gene disruption demonstrates that P-selectin glycoprotein ligand 1 (PSGL-1) is required for P-selectin-mediated but not E-selectin-mediated neutrophil rolling and migration. J Exp Med 190:1769–1782PubMedGoogle Scholar
  55. 55.
    Hicks AE. R, Nolan SL, Ridger VC, Hellewell PG, Norman KE (2003) Recombinant P-selectin glycoprotein ligand-1 directly inhibits leukocyte rolling by all 3 selectins in vivo: complete inhibition of rolling is not required for anti-inflammatory effect. Blood 101:3249–3256PubMedGoogle Scholar
  56. 56.
    Sperandio M, Smith ML, Forlow SB, Olson TS, Xia L, Mcever RP, Ley K (2003) P-selectin glycoprotein ligand-1 mediates L-selectin-dependent leukocyte rolling in venules. J Exp Med 197:1355PubMedGoogle Scholar
  57. 57.
    Rossi D, Zlotnik A (2000) The biology of chemokines and their receptors. Annu Rev Immunol 18:217–242PubMedGoogle Scholar
  58. 58.
    Luster AD (1998) Chemokines—chemotactic cytokines that mediate inflammation. N Engl J Med 338:436–445PubMedGoogle Scholar
  59. 59.
    Olson TS, Ley K (2002) Chemokines and chemokine receptors in leukocyte trafficking. Am J Physiol 283:R7–R28Google Scholar
  60. 60.
    Ginsberg MH, Du X, Plow EF (1992) Inside-out integrin signalling. Curr Opin Cell Biol 4:766–771Google Scholar
  61. 61.
    Diamond MS, Springer TA (1994) The dynamic regulation of integrin adhesiveness. Curr Biol 4:506–517PubMedGoogle Scholar
  62. 62.
    Forlow SB, Foley PL, Ley K (2002) Severely reduced neutrophil adhesion and impaired host defense against fecal and commensal bacteria in CD18−/−P-selectin−/− double null mice. FASEB J 16:1488–1496PubMedGoogle Scholar
  63. 63.
    Forlow SB, White EJ, Barlow SC, Feldman SH, Lu H, Bagby GJ, Beaudet AL, Bullard DC, Ley K (2000) Severe inflammatory defect and reduced viability in CD18 and E-selectin double-mutant mice. J Clin Invest 106:1457–1466PubMedGoogle Scholar
  64. 64.
    Vestweber D (2002) Regulation of endothelial cell contacts during leukocyte extravasation. Curr Opin Cell Biol 14:587–593CrossRefPubMedGoogle Scholar
  65. 65.
    Muller WA (2003) Leukocyte-endothelial-cell interactions in leukocyte transmigration and the inflammatory response. Trends Immunol 24:327–334PubMedGoogle Scholar
  66. 66.
    Bianchi E, Bender JR, Blasi F, Pardi R (1997) Through and beyond the wall: late steps in leukocyte transendothelial migration. Immunol Today 18:586–591CrossRefPubMedGoogle Scholar
  67. 67.
    Burns AR, Walker DC, Brown ES, Thurmon LT, Bowden RA, Keese CR, Simon SI, Entman ML, Smith CW (1997) Neutrophil transendothelial migration is independent of tight junctions and occurs preferentially at tricellular corners. J Immunol 159:2893–2903PubMedGoogle Scholar
  68. 68.
    Allport JR, Muller WA, Luscinskas FW (2000) Monocytes induce reversible focal changes in vascular endothelial cadherin complex during transendothelial migration under flow. J Cell Biol 148:203–216CrossRefPubMedGoogle Scholar
  69. 69.
    Werr J, Johansson J, Eriksson EE, Hedqvist P, Ruoslahti E, Lindbom L (2000) Integrin alpha (2) beta (1) (VLA-2) is a principal receptor used by neutrophils for locomotion in extravascular tissue. Blood 95:1804–1809PubMedGoogle Scholar
  70. 70.
    Werr J, Xie X, Hedqvist P, Ruoslahti E, Lindbom L (1998) beta1 integrins are critically involved in neutrophil locomotion in extravascular tissue In vivo. J Exp Med 187:2091–2096PubMedGoogle Scholar
  71. 71.
    Muller WA, Weigl SA, Deng X, Phillips DM (1993) PECAM-1 is required for transendothelial migration of leukocytes. J Exp Med 178:449–460PubMedGoogle Scholar
  72. 72.
    Muller WA, Randolph GJ (1999) Migration of leukocytes across endothelium and beyond: molecules involved in the transmigration and fate of monocytes. J Leukoc Biol 66:698–704PubMedGoogle Scholar
  73. 73.
    Williams LA, Martin-Padura I, Dejana E, Hogg N, Simmons DL (1999) Identification and characterisation of human junctional adhesion molecule (JAM). Mol Immunol 36:1175–1188CrossRefPubMedGoogle Scholar
  74. 74.
    Martin-Padura I, Lostaglio S, Schneemann M, Williams L, Romano M, Fruscella P, Panzeri C, Stoppacciaro A, Ruco L, Villa A, Simmons D, Dejana E (1998) Junctional adhesion molecule, a novel member of the immunoglobulin superfamily that distributes at intercellular junctions and modulates monocyte transmigration. J Cell Biol 142:117–127PubMedGoogle Scholar
  75. 75.
    Schenkel AR, Mamdouh Z, Chen X, Liebman RM, Muller WA (2002) CD99 plays a major role in the migration of monocytes through endothelial junctions. Nat Immunol 3:143–150CrossRefGoogle Scholar
  76. 76.
    Jung U, Norman KE, Scharffetter-Kochanek K, Beaudet AL, Ley KTransit time of leukocytes rolling through venules controls cytokine-induced inflammatory cell recruitment in vivo. J Clin Invest 102:1526–1533Google Scholar
  77. 77.
    Yeo EL, Sheppard JA, Feuerstein IA (1994) Role of P-selectin and leukocyte activation in polymorphonuclear cell adhesion to surface adherent activated platelets under physiologic shear conditions (an injury vessel wall model). Blood 83:2498–2507PubMedGoogle Scholar
  78. 78.
    Merhi Y, Provost P, Chauvet P, Theoret JF, Phillips ML, Latour JG (1999) Selectin blockade reduces neutrophil interaction with platelets at the site of deep arterial injury by angioplasty in pigs. Arterioscler Thromb Vasc Biol 19:372–377PubMedGoogle Scholar
  79. 79.
    Merhi Y, Provost P, Guidoin R, Latour JG (1997) Importance of platelets in neutrophil adhesion and vasoconstriction after deep carotid arterial injury by angioplasty in pigs. Arterioscler Thromb Vasc Biol 17:1185–1191PubMedGoogle Scholar
  80. 80.
    Merhi Y, Lacoste LL, Lam JY (1994) Neutrophil implications in platelet deposition and vasoconstriction after deep arterial injury by angioplasty in pigs. Circulation 90:997–1002PubMedGoogle Scholar
  81. 81.
    Huo Y, Schober A, Forlow SB, Smith DF, Hyman MC, Jung S, Littman DR, Weber C, Ley K (2003) Circulating activated platelets exacerbate atherosclerosis in mice deficient in apolipoprotein E. Nat Med 9:61–67PubMedGoogle Scholar
  82. 82.
    Massberg S, Enders G, Leiderer R, Eisenmenger S, Vestweber D, Krombach F, Messmer K (1998) Platelet-endothelial cell interactions during ischemia/reperfusion: the role of P-selectin. Blood 92:507–515PubMedGoogle Scholar
  83. 83.
    Rabb H, Ramirez G, Saba SR, Reynolds D, Xu J, Flavell R, Antonia S (1996) Renal ischemic-reperfusion injury in L-selectin-deficient mice. Am J Physiol 271:F408–F413PubMedGoogle Scholar
  84. 84.
    Nemoto T, Burne MJ, Daniels F, O’Donnell MP, Crosson J, Berens K, Issekutz A, Kasiske BL, Keane WF, Rabb H (2001) Small molecule selectin ligand inhibition improves outcome in ischemic acute renal failure. Kidney Int 60:2205–2214PubMedGoogle Scholar
  85. 85.
    Burne MJ, Rabb H (2002) Pathophysiological contributions of fucosyltransferases in renal ischemia reperfusion injury. J Immunol 169:2648–2652PubMedGoogle Scholar
  86. 86.
    Matsukawa A, Lukacs NW, Hogaboam CM, Knibbs RN, Bullard DC, Kunkel SL, Stoolman LM (2002) Mice genetically lacking endothelial selectins are resistant to the lethality in septic peritonitis. Exp Mol Pathol 72:68–76PubMedGoogle Scholar
  87. 87.
    Kelly KJ, Tolkoff-Rubin NE, Rubin RH, Williams WW Jr, Meehan SM, Meschter CL, Christenson JG, Bonventre JV (1996) An oral platelet-activating factor antagonist, Ro-24-4736, protects the rat kidney from ischemic injury. Am J Physiol 271:F1061–F1067PubMedGoogle Scholar
  88. 88.
    Miura M, Fu X, Zhang QW, Remick DG, Fairchild RL (2001) Neutralization of Gro alpha and macrophage inflammatory protein-2 attenuates renal ischemia/reperfusion injury. Am J Pathol 159:2137–2145PubMedGoogle Scholar
  89. 89.
    Leonard MO, Hannan K, Burne MJ, Lappin DW, Doran P, Coleman P, Stenson C, Taylor CT, Daniels F, Godson C, Petasis NA, Rabb H, Brady HR (2002) 15-Epi-16-(para-fluorophenoxy)-lipoxin A (4)-methyl ester, a synthetic analogue of 15-epi-lipoxin A (4), is protective in experimental ischemic acute renal failure. J Am Soc Nephrol 13:1657–1662Google Scholar
  90. 90.
    Rabb H, Mendiola CC, Dietz J, Saba SR, Issekutz TB, Abanilla F, Bonventre JV, Ramirez G (1994) Role of CD11a and CD11b in ischemic acute renal failure in rats. Am J Physiol 267:F1052–F1058PubMedGoogle Scholar
  91. 91.
    Rabb H, Mendiola CC, Saba SR, Dietz JR, Smith CW, Bonventre JV, Ramirez G (1995) Antibodies to ICAM-1 protect kidneys in severe ischemic reperfusion injury. Biochem Biophys Res Commun 211:67–73PubMedGoogle Scholar
  92. 92.
    Kelly KJ, Williams WW. J, Colvin RB, Bonventre JV (1994) Antibody to intercellular adhesion molecule 1 protects the kidney against ischemic injury. Proc Natl Acad Sci USA 91:812–816PubMedGoogle Scholar
  93. 93.
    Haller H, Dragun D, Miethke A, Park JK, Weis A, Lippoldt A, Gross V, Luft FC (1996) Antisense oligonucleotides for ICAM-1 attenuate reperfusion injury and renal failure in the rat. Kidney Int 50:473–480PubMedGoogle Scholar
  94. 94.
    Chiao H, Kohda Y, Mcleroy P, Craig L, Linas S, Star RA (1998) Alpha-melanocyte-stimulating hormone inhibits renal injury in the absence of neutrophils. Kidney Int 54:765–774PubMedGoogle Scholar
  95. 95.
    Jo SK, Yun SY, Chang KH, Cha DR, Cho WY, Kim HK, Won NH (2001) Alpha-MSH decreases apoptosis in ischaemic acute renal failure in rats: possible mechanism of this beneficial effect. Nephrol Dial Transplant 16:1583–1591PubMedGoogle Scholar
  96. 96.
    Okusa MD, Linden J, Macdonald T, Huang L (1999) Selective A2A adenosine receptor activation reduces ischemia-reperfusion injury in rat kidney. Am J Physiol 277:F404–F412PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  1. 1.Klinik und Poliklinik für Anästhesiologie und operative IntensivmedizinUniversitätsklinikum MünsterMünsterGermany
  2. 2.Cardiovascular Research CenterUniversity of VirginiaCharlottesvilleUSA

Personalised recommendations