Improving the outcome of kidney transplantation by ameliorating renal ischemia reperfusion injury: Lost in translation?

Journal of Translational Medicine

Volumn 14, Issue 1, 2016, Pages

  Saat, T C ^a   van den Akker, E K ^a   IJzermans, J N M ^a   Dor, F J M F ^a   de Bruin, R W F ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

Ischemia reperfusion injury; Kidney transplantation; Translation; Treatment

Indexed keywords

MICRORNA; MICRORNA 146A; MICRORNA 187; MICRORNA 192; MICRORNA 194; MICRORNA 199A 3P; MICRORNA 20A; MICRORNA 21; MICRORNA 214; MICRORNA 805; RECOMBINANT ERYTHROPOIETIN; SUPEROXIDE DISMUTASE; UNCLASSIFIED DRUG;

APOPTOSIS; CALORIC RESTRICTION; CLINICAL EFFECTIVENESS; COLD ISCHEMIA; DELAYED GRAFT FUNCTION; GRAFT SURVIVAL; HUMAN; INCIDENCE; KIDNEY ISCHEMIA; KIDNEY PRESERVATION; KIDNEY TRANSPLANTATION; MESENCHYMAL STEM CELL TRANSPLANTATION; NONHUMAN; NUTRITIONAL STATUS; PROTEIN EXPRESSION; PROTEIN RESTRICTION; RANDOMIZED CONTROLLED TRIAL (TOPIC); REPERFUSION INJURY; REVIEW; TREATMENT DURATION; TREATMENT RESPONSE; ANIMAL; ISCHEMIA; KIDNEY; PATHOLOGY; TRANSLATIONAL RESEARCH; TREATMENT OUTCOME; VASCULARIZATION;

ANIMALS; HUMANS; ISCHEMIA; KIDNEY; KIDNEY TRANSPLANTATION; REPERFUSION INJURY; TRANSLATIONAL MEDICAL RESEARCH; TREATMENT OUTCOME;

EID: 84958900596     PISSN: None     EISSN: 14795876     Source Type: Journal    
DOI: 10.1186/s12967-016-0767-2     Document Type: Review

References (120)

1. Klein AS, et al. Organ donation and utilization in the United States, 1999-2008. Am J Transplant. 2010;10(4 Pt 2):973-86.
2. Tonelli M, et al. Systematic review: kidney transplantation compared with dialysis in clinically relevant outcomes. Am J Transplant. 2011;11(10):2093-109.
3. Gjertson DW, Cecka JM. Living unrelated donor kidney transplantation. Kidney Int. 2000;58(2):491-9.
4. Chkhotua AB, et al. Kidney transplantation from living-unrelated donors: comparison of outcome with living-related and cadaveric transplants under current immunosuppressive protocols. Urology. 2003;62(6):1002-6.
5. Sapir-Pichhadze R, Young A, Joseph Kim S. Living donor age and kidney transplant outcomes: an assessment of risk across the age continuum. Transpl Int. 2013;26(5):493-501.
6. Le Dinh H, et al. Delayed graft function does not harm the future of donation-after-cardiac death in kidney transplantation. Transplant Proc. 2012;44(9):2795-802.
7. Schuurs TA, et al. Time-dependent changes in donor brain death related processes. Am J Transplant. 2006;6(12):2903-11.
8. Nijboer WN, et al. How important is the duration of the brain death period for the outcome in kidney transplantation? Transpl Int. 2011;24(1):14-20.
9. Nagaraja P, et al. Influence of delayed graft function and acute rejection on outcomes after kidney transplantation from donors after cardiac death. Transplantation. 2012;94(12):1218-23.
10. Wadei HM, et al. Comparison of kidney function between donation after cardiac death and donation after brain death kidney transplantation. Transplantation. 2013;96(3):274-81.
11. Eurotransplant International Foundation. Annual report 2013, edited by Rahmel A. Eurotransplant Foundation, Leiden. https://www.eurotransplant.org/cms/mediaobject.php?file=AR20135.pdf.
12. Pascual J, Zamora J, Pirsch JD. A systematic review of kidney transplantation from expanded criteria donors. Am J Kidney Dis. 2008;52(3):553-86.
13. Martinez-Vaquera S, et al. Outcomes in renal transplantation with expanded-criteria donors. Transplant Proc. 2013;45(10):3595-8.
14. Balaz P, et al. Identification of expanded-criteria donor kidney grafts at lower risk of delayed graft function. Transplantation. 2013;96(7):633-8.
15. Domagala P, et al. Assessment of kidneys procured from expanded criteria donors before transplantation. Transplant Proc. 2009;41(8):2966-9.
16. Johnson KJ, Weinberg JM. Postischemic renal injury due to oxygen radicals. Curr Opin Nephrol Hypertens. 1993;2(4):625-35.
17. Kusch A, et al. Novel signalling mechanisms and targets in renal ischaemia and reperfusion injury. Acta Physiol (Oxf). 2013;208(1):25-40.
18. Jang HR, et al. The interaction between ischemia-reperfusion and immune responses in the kidney. J Mol Med (Berl). 2009;87(9):859-64.
19. Perico N, et al. Delayed graft function in kidney transplantation. Lancet. 2004;364(9447):1814-27.
20. Bonventre JV, Yang L. Cellular pathophysiology of ischemic acute kidney injury. J Clin Invest. 2011;121(11):4210-21.
21. Kosieradzki M, Rowinski W. Ischemia/reperfusion injury in kidney transplantation: mechanisms and prevention. Transplant Proc. 2008;40(10):3279-88.
22. Ali S, Sheerin NS. Biomarkers of acute injury: predicting the long-term outcome after transplantation. Kidney Int. 2013;84(6):1072-4.
23. Devarajan P, et al. Gene expression in early ischemic renal injury: clues towards pathogenesis, biomarker discovery, and novel therapeutics. Mol Genet Metab. 2003;80(4):365-76.
24. Fletcher JT, Nankivell BJ, Alexander SI. Chronic allograft nephropathy. Pediatr Nephrol. 2009;24(8):1465-71.
25. van der Vliet JA, Warle MC. The need to reduce cold ischemia time in kidney transplantation. Curr Opin Organ Transplant. 2013;18(2):174-8.
26. Thurman JM. Triggers of inflammation after renal ischemia/reperfusion. Clin Immunol. 2007;123(1):7-13.
27. Castaneda MP, et al. Activation of mitochondrial apoptotic pathways in human renal allografts after ischemiareperfusion injury. Transplantation. 2003;76(1):50-4.
28. Robertson LT, Mitchell JR. Benefits of short-term dietary restriction in mammals. Exp Gerontol. 2013;48:1043-8.
29. Gallinetti J, Harputlugil E, Mitchell JR. Amino acid sensing in dietary-restriction-mediated longevity: roles of signal-transducing kinases GCN2 and TOR. Biochem J. 2013;449(1):1-10.
30. Mitchell JR, et al. Short-term dietary restriction and fasting precondition against ischemia reperfusion injury in mice. Aging Cell. 2010;9(1):40-53.
31. Verweij M, et al. Glucose supplementation does not interfere with fasting-induced protection against renal ischemia/reperfusion injury in mice. Transplantation. 2011;92(7):752-8.
32. Peng W, et al. Surgical stress resistance induced by single amino acid deprivation requires Gcn2 in mice. Sci Transl Med. 2012;4(118):118ra11.
33. Mair W, Piper MD, Partridge L. Calories do not explain extension of life span by dietary restriction in Drosophila. PLoS Biol. 2005;3(7):e223.
34. Min KJ, Tatar M. Restriction of amino acids extends lifespan in Drosophila melanogaster. Mech Ageing Dev. 2006;127(7):643-6.
35. Nygren J. The metabolic effects of fasting and surgery. Best Pract Res Clin Anaesthesiol. 2006;20(3):429-38.
36. Stuart PC. The evidence base behind modern fasting guidelines. Best Pract Res Clin Anaesthesiol. 2006;20(3):457-69.
37. Redman LM, et al. Effect of calorie restriction with or without exercise on body composition and fat distribution. J Clin Endocrinol Metab. 2007;92(3):865-72.
38. Rochon J, et al. Design and conduct of the CALERIE study: comprehensive assessment of the long-term effects of reducing intake of energy. J Gerontol A Biol Sci Med Sci. 2011;66(1):97-108.
39. van Ginhoven TM, et al. Pre-operative dietary restriction is feasible in live-kidney donors. Clin Transplant. 2011;25(3):486-94.
40. Hoeger S, et al. UW is superior compared with HTK after prolonged preservation of renal grafts. J Surg Res. 2011;170(1):e149-57.
41. Straatsburg IH, et al. Evaluation of rat liver apoptotic and necrotic cell death after cold storage using UW, HTK, and Celsior. Transplantation. 2002;74(4):458-64.
42. Stubenitsky BM, et al. Regeneration of ATP in kidney slices after warm ischemia and hypothermic preservation. Transpl Int. 1995;8(4):293-7.
43. Chatauret N, Thuillier R, Hauet T. Preservation strategies to reduce ischemic injury in kidney transplantation: pharmacological and genetic approaches. Curr Opin Organ Transplant. 2011;16(2):180-7.
44. Moers C, et al. Machine perfusion or cold storage in deceased-donor kidney transplantation. N Engl J Med. 2009;360(1):7-19.
45. Burgos Revilla FJ, et al. Machine perfusion: initial results in an expanded criteria donor kidney transplant program. Transplant Proc. 2015;47(1):19-22.
46. Jochmans I, et al. Hypothermic machine perfusion of kidneys retrieved from standard and high-risk donors. Transpl Int. 2015;28(6):665-76.
47. Nicholson ML, Hosgood SA. Renal transplantation after ex vivo normothermic perfusion: the first clinical study. Am J Transplant. 2013;13(5):1246-52.
48. Deng R, et al. Machine perfusion versus cold storage of kidneys derived from donation after cardiac death: a meta-analysis. PLoS One. 2013;8(3):e56368.
49. Hosgood SA, van Heurn E, Nicholson ML. Normothermic machine perfusion of the kidney: better conditioning and repair? Transpl Int. 2015;28(6):657-64.
50. Kierulf-Lassen C, et al. Molecular Mechanisms of Renal Ischemic Conditioning Strategies. Eur Surg Res. 2015;55(3):151-83.
51. Murry CE, Jennings RB, Reimer KA. Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation. 1986;74(5):1124-36.
52. Candilio L, Malik A, Hausenloy DJ. Protection of organs other than the heart by remote ischemic conditioning. J Cardiovasc Med (Hagerstown). 2013;14(3):193-205.
53. Wever KE, et al. Ischemic preconditioning in the animal kidney, a systematic review and meta-analysis. PLoS One. 2012;7(2):e32296.
54. Riksen NP, Hausenloy DJ, Yellon DM. Erythropoietin: ready for prime-time cardioprotection. Trends Pharmacol Sci. 2008;29(5):258-67.
55. Hausenloy DJ, et al. Effect of remote ischaemic preconditioning on myocardial injury in patients undergoing coronary artery bypass graft surgery: a randomised controlled trial. Lancet. 2007;370(9587):575-9.
56. Jiang H, et al. Protective effects of three remote ischemic conditioning procedures against renal ischemic/reperfusion injury in rat kidneys: a comparative study. Ir J Med Sci. 2014;184(3):647-53.
57. Bedir S, et al. Ineffectiveness of Remote Ischemic Renal Preconditioning in a Porcine Solitary-Kidney Model. J Endourol. 2015;29(5):590-4.
58. Wu J, et al. Remote ischemic conditioning enhanced the early recovery of renal function in recipients after kidney transplantation: a randomized controlled trial. J Surg Res. 2014;188(1):303-8.
59. Krogstrup NV, et al. Remote ischaemic conditioning on recipients of deceased renal transplants, effect on immediate and extended kidney graft function: a multicentre, randomised controlled trial protocol (CONTEXT). BMJ Open. 2015;5(8):e007941.
60. Zhao ZQ, et al. Inhibition of myocardial injury by ischemic postconditioning during reperfusion: comparison with ischemic preconditioning. Am J Physiol Heart Circ Physiol. 2003;285(2):H579-88.
61. Mykytenko J, et al. Long-term inhibition of myocardial infarction by postconditioning during reperfusion. Basic Res Cardiol. 2007;102(1):90-100.
62. Hausenloy DJ, Yellon DM. The therapeutic potential of ischemic conditioning: an update. Nat Rev Cardiol. 2011;8(11):619-29.
63. van den Akker EK, et al. Protection against renal ischemia-reperfusion injury by ischemic postconditioning. Transplantation. 2013;95(11):1299-305.
64. Eldaif SM, et al. Attenuation of renal ischemia-reperfusion injury by postconditioning involves adenosine receptor and protein kinase C activation. Transpl Int. 2010;23(2):217-26.
65. Jiang B, et al. Ischemic postconditioning attenuates renal ischemic/reperfusion injury in mongrel dogs. Urology. 2010;76(6):1519 e1.
66. Miklos Z, et al. Ischaemic postconditioning reduces serum and tubular TNF-alpha expression in ischaemic-reperfused kidney in healthy rats. Clin Hemorheol Microcirc. 2012;50(3):167-78.
67. Weng X, et al. Ischemic postconditioning inhibits the renal fibrosis induced by ischemia-reperfusion injury in rats. Urology. 2012;80(2):484 e1.
68. Kadkhodaee M, et al. First report of the protective effects of remote per- and postconditioning on ischemia/reperfusion-induced renal injury. Transplantation. 2011;92(10):e55.
69. van den Akker EK, et al. Ischemic postconditioning in human DCD kidney transplantation is feasible and appears safe. Transpl Int. 2014;27(2):226-34.
70. Masoud MS, et al. Pre-conditioned mesenchymal stem cells ameliorate renal ischemic injury in rats by augmented survival and engraftment. J Transl Med. 2012;10:243.
71. Chen YT, et al. Adipose-derived mesenchymal stem cell protects kidneys against ischemia-reperfusion injury through suppressing oxidative stress and inflammatory reaction. J Transl Med. 2011;9:51.
72. Zhuo W, et al. Mesenchymal stem cells ameliorate ischemia-reperfusion-induced renal dysfunction by improving the antioxidant/oxidant balance in the ischemic kidney. Urol Int. 2011;86(2):191-6.
73. Zhuo W, et al. Efficiency of endovenous versus arterial administration of mesenchymal stem cells for ischemia-reperfusion-induced renal dysfunction in rats. Transplant Proc. 2013;45(2):503-10.
74. Cao H, et al. Mesenchymal stem cells derived from human umbilical cord ameliorate ischemia/reperfusion-induced acute renal failure in rats. Biotechnol Lett. 2010;32(5):725-32.
75. Semedo P, et al. Early modulation of inflammation by mesenchymal stem cell after acute kidney injury. Int Immunopharmacol. 2009;9(6):677-82.
76. Behr L, et al. Evaluation of the effect of autologous mesenchymal stem cell injection in a large-animal model of bilateral kidney ischaemia reperfusion injury. Cell Prolif. 2009;42(3):284-97.
77. Behr L, et al. Intra renal arterial injection of autologous mesenchymal stem cells in an ovine model in the postischemic kidney. Nephron Physiol. 2007;107(3):65-76.
78. Hoogduijn MJ, et al. Mesenchymal stem cells induce an inflammatory response after intravenous infusion. Stem Cells Dev. 2013;22(21):2825-35.
79. Burst VR, et al. Poor cell survival limits the beneficial impact of mesenchymal stem cell transplantation on acute kidney injury. Nephron Exp Nephrol. 2010;114(3):e107-16.
80. Luo J, et al. Mesenchymal-like progenitors derived from human embryonic stem cells promote recovery from acute kidney injury via paracrine actions. Cytotherapy. 2013;15(6):649-62.
81. Murry CE, et al. Haematopoietic stem cells do not transdifferentiate into cardiac myocytes in myocardial infarcts. Nature. 2004;428(6983):664-8.
82. Balsam LB, et al. Haematopoietic stem cells adopt mature haematopoietic fates in ischaemic myocardium. Nature. 2004;428(6983):668-73.
83. Perico N, et al. Autologous mesenchymal stromal cells and kidney transplantation: a pilot study of safety and clinical feasibility. Clin J Am Soc Nephrol. 2011;6(2):412-22.
84. Reinders ME, et al. Autologous bone marrow-derived mesenchymal stromal cells for the treatment of allograft rejection after renal transplantation: results of a phase I study. Stem Cells Transl Med. 2013;2(2):107-11.
85. Peng Y, et al. Donor-derived mesenchymal stem cells combined with low-dose tacrolimus prevent acute rejection after renal transplantation: a clinical pilot study. Transplantation. 2013;95(1):161-8.
86. Luk F, et al. Efficacy of immunotherapy with mesenchymal stem cells in man: a systematic review. Expert Rev Clin Immunol. 2015;11(5):617-36.
87. Brunstein CG, et al. Infusion of ex vivo expanded T regulatory cells in adults transplanted with umbilical cord blood: safety profile and detection kinetics. Blood. 2011;117(3):1061-70.
88. Kinsey GR, Sharma R, Okusa MD. Regulatory T cells in AKI. J Am Soc Nephrol. 2013;24(11):1720-6.
89. Kinsey GR, et al. Regulatory T cells suppress innate immunity in kidney ischemia-reperfusion injury. J Am Soc Nephrol. 2009;20(8):1744-53.
90. Dijke IE, et al. Discarded human thymus is a novel source of stable and long-lived therapeutic regulatory T cells. Am J Transplant. 2015;16(1):58-71.
91. Bajwa A, Kinsey GR, Okusa MD. Immune mechanisms and novel pharmacological therapies of acute kidney injury. Curr Drug Targets. 2009;10(12):1196-204.
92. Attallah N, et al. The potential role of statins in contrast nephropathy. Clin Nephrol. 2004;62(4):273-8.
93. Khanal S, et al. Statin therapy reduces contrast-induced nephropathy: an analysis of contemporary percutaneous interventions. Am J Med. 2005;118(8):843-9.
94. Jo SH, et al. Prevention of radiocontrast medium-induced nephropathy using short-term high-dose simvastatin in patients with renal insufficiency undergoing coronary angiography (PROMISS) trial-a randomized controlled study. Am Heart J. 2008;155(3):499 e1-8.
95. Philips B, MacPhee I. Do statins prevent acute kidney injury? Expert Opin Drug Saf. 2015;14(10):1547-61.
96. Ishii Y, et al. Renoprotective effect of erythropoietin against ischaemia-reperfusion injury in a non-human primate model. Nephrol Dial Transplant. 2011;26(4):1157-62.
97. Zhang J, et al. Erythropoietin pretreatment ameliorates renal ischaemia-reperfusion injury by activating PI3K/Akt signalling. Nephrology (Carlton). 2015;20(4):266-72.
98. Song YR, et al. Prevention of acute kidney injury by erythropoietin in patients undergoing coronary artery bypass grafting: a pilot study. Am J Nephrol. 2009;30(3):253-60.
99. Xin H, et al. Effect of high-dose erythropoietin on graft function after kidney transplantation: a meta-analysis of randomized controlled trials. Biomed Pharmacother. 2015;69:29-33.
100. Vlachopanos G, Kassimatis TI, Agrafiotis A. Perioperative administration of high-dose recombinant human erythropoietin for delayed graft function prevention in kidney transplantation: a meta-analysis. Transpl Int. 2015;28(3):330-40.
101. Brines M, et al. Nonerythropoietic, tissue-protective peptides derived from the tertiary structure of erythropoietin. Proc Natl Acad Sci USA. 2008;105(31):10925-30.
102. Yang C, et al. A novel proteolysis-resistant cyclic helix B peptide ameliorates kidney ischemia reperfusion injury. Biochim Biophys Acta. 2014;1842(11):2306-17.
103. Yang C. Cyclic helix B peptide in preservation solution and autologous blood perfusate ameliorates ichemia-reperfusion injury in isolated porcine kidneys. Transplantation Direct. 2015;1(2):1-9.
104. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell. 2004;116(2):281-97.
105. Weber JA, et al. The microRNA spectrum in 12 body fluids. Clin Chem. 2010;56(11):1733-41.
106. Sui W, et al. Microarray analysis of MicroRNA expression in acute rejection after renal transplantation. Transpl Immunol. 2008;19(1):81-5.
107. Anglicheau D, et al. MicroRNA expression profiles predictive of human renal allograft status. Proc Natl Acad Sci USA. 2009;106(13):5330-5.
108. Godwin JG, et al. Identification of a microRNA signature of renal ischemia reperfusion injury. Proc Natl Acad Sci USA. 2010;107(32):14339-44.
109. van den Akker EK, et al. MicroRNAs in kidney transplantation: living up to their expectations? J Transplant. 2015;2015:354826.
110. Rowinski W, Paczek L. Transplantation ethics: are we approaching the crossroads? Transplant Proc. 2012;44(7):2171-2.
111. Sachs DH. Tolerance: of mice and men. J Clin Invest. 2003;111(12):1819-21.
112. Sachdeva M, et al. Obesity as a barrier to living kidney donation: a center-based analysis. Clin Transplant. 2013;27(6):882-7.
113. Hourmant M, Lerat L, Karam G. Donation from old living donors: how safe is it? Nephrol Dial Transplant. 2013;28(8):2010-4.
114. Chapman JR, Nankivell BJ. Nephrotoxicity of ciclosporin A: short-term gain, long-term pain? Nephrol Dial Transplant. 2006;21(8):2060-3.
115. Nankivell BJ, et al. The natural history of chronic allograft nephropathy. N Engl J Med. 2003;349(24):2326-33.
116. Nankivell BJ, et al. Calcineurin inhibitor nephrotoxicity: longitudinal assessment by protocol histology. Transplantation. 2004;78(4):557-65.
117. Budde K, et al. Everolimus-based, calcineurin-inhibitor-free regimen in recipients of de-novo kidney transplants: an open-label, randomised, controlled trial. Lancet. 2011;377(9768):837-47.
118. Ponticelli C. Herpes viruses and tumours in kidney transplant recipients. The role of immunosuppression. Nephrol Dial Transplant. 2011;26(6):1769-75.
119. Carroll RP, et al. Incidence and prediction of nonmelanoma skin cancer post-renal transplantation: a prospective study in Queensland, Australia. Am J Kidney Dis. 2003;41(3):676-83.
120. ter Riet G, et al. Publication bias in laboratory animal research: a survey on magnitude, drivers, consequences and potential solutions. PLoS One. 2012;7(9):e43404.