Role of warm ischemia on innate and adaptive responses in a preclinical renal auto-transplanted porcine model

Journal of Translational Medicine

Volumn 11, Issue 1, 2013, Pages

  Rossard, Ludivine ^a   Favreau, Frédéric ^a,b,c   Giraud, Sebastien ^a,c   Thuillier, Raphael ^a,c   Le Pape, Sylvain ^a,b   Goujon, Jean M ^a,b,c   Valagier, Alexandre ^a   Hauet, Thierry ^a,b,c,d  

^a INSERM   (France)

^b UNIVERSITÉ DE POITIERS   (France)

^c POITIERS UNIVERSITY HOSPITAL   (France)

^d CEMAGREF   (France)

Author keywords

Adaptive immune response; Innate immune response; Ischemia reperfusion; Kidney transplantation; Preclinical porcine model

Indexed keywords

ADAPTIVE IMMUNITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL INFILTRATION; COLD ISCHEMIA; CONTROLLED STUDY; DELAYED GRAFT FUNCTION; DISEASE SEVERITY; INNATE IMMUNITY; KIDNEY AUTOTRANSPLANTATION; KIDNEY FIBROSIS; KIDNEY FUNCTION; KIDNEY ISCHEMIA; KIDNEY TUBULE DAMAGE; MALE; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; REPERFUSION INJURY; ANIMAL; AUTOTRANSPLANTATION; CELL DEATH; COLD; FIBROSIS; IMMUNOLOGY; INFLAMMATION; ISCHEMIA; KIDNEY FUNCTION TEST; KIDNEY TRANSPLANTATION; KIDNEY TUBULE; OXIDATION REDUCTION REACTION; PATHOLOGY; SWINE; TIME; URINE;

ADAPTIVE IMMUNITY; ANIMALS; CELL DEATH; COLD TEMPERATURE; FIBROSIS; IMMUNITY, INNATE; INFLAMMATION; KIDNEY FUNCTION TESTS; KIDNEY TRANSPLANTATION; KIDNEY TUBULES; MALE; MODELS, ANIMAL; OXIDATION-REDUCTION; REPERFUSION INJURY; SUS SCROFA; TIME FACTORS; TRANSPLANTATION, AUTOLOGOUS; WARM ISCHEMIA;

EID: 84878413153     PISSN: None     EISSN: 14795876     Source Type: Journal    
DOI: 10.1186/1479-5876-11-129     Document Type: Article

References (39)

1. Salahudeen AK, Haider N, May W. Cold ischemia and the reduced long-term survival of cadaveric renal allografts. Kidney Int 2004, 65:713-718. 10.1111/j.1523-1755.2004.00416.x, 14717946.
2. Hauet T, Goujon JM, Baumert H, Petit I, Carretier M, Eugene M, Vandewalle A. Polyethylene glycol reduces the inflammatory injury due to cold ischemia/reperfusion in autotransplanted pig kidneys. Kidney Int 2002, 62:654-667. 10.1046/j.1523-1755.2002.00473.x, 12110031.
3. Bon D, Chatauret N, Giraud S, Thuillier R, Favreau F, Hauet T. New strategies to optimize kidney recovery and preservation in transplantation. Nat Rev Nephrol 2012, 8:339-347. 10.1038/nrneph.2012.83, 22549229.
4. Bonventre JV. Pathophysiology of AKI: injury and normal and abnormal repair. Contrib Nephrol 2010, 165:9-17.
5. van der Vliet JA, Warle MC. The need to reduce cold ischemia time in kidney transplantation. Curr Opin Organ Transplant 2013, 18:174-178. 10.1097/MOT.0b013e32835e2a08, 23337956.
6. Mikhalski D, Wissing KM, Ghisdal L, Broeders N, Touly M, Hoang AD, Loi P, Mboti F, Donckier V, Vereerstraeten P, Abramowicz D. Cold ischemia is a major determinant of acute rejection and renal graft survival in the modern era of immunosuppression. Transplantation 2008, 85:S3-S9. 10.1097/TP.0b013e318169c29e, 18401260.
7. Jochmans I, Lerut E, Heedfeld V, Wylin T, Pirenne J, Monbaliu D. Reproducible model for kidney autotransplantation in pigs. Transplant Proc 2009, 41:3417-3421. 10.1016/j.transproceed.2009.09.024, 19857760.
8. Giraud S, Favreau F, Chatauret N, Thuillier R, Maiga S, Hauet T. Contribution of large pig for renal ischemia-reperfusion and transplantation studies: the preclinical model. J Biomed Biotechnol 2011, 2011:532127. 3051176, 21403881.
9. Jayle C, Faure JP, Thuillier R, Goujon JM, Richer JP, Hauet T. Influence of nephron mass and a phosphorylated 38 mitogen-activated protein kinase inhibitor on the development of early and long-term injury after renal warm ischaemia. Br J Surg 2009, 96:799-808. 10.1002/bjs.6589, 19526623.
10. Cau J, Favreau F, Zhang K, Febrer G, de la Motte GR, Ricco JB, Goujon JM, Hauet T. FR167653 improves renal recovery and decreases inflammation and fibrosis after renal ischemia reperfusion injury. J Vasc Surg 2009, 49:728-740. 10.1016/j.jvs.2008.09.056, 19268775.
11. Doucet C, Zhang K, Desurmont T, Hebrard W, Scepi M, Nadeau C, Cau J, Leyre P, Febrer G, Carretier M. Influence of warm ischemia time on peripheral-type benzodiazepine receptor: a new aspect of the role of mitochondria. Nephron Exp Nephrol 2007, 107:e1-e11. 10.1159/000105139, 17622771.
12. Jayle C, Favreau F, Zhang K, Doucet C, Goujon JM, Hebrard W, Carretier M, Eugene M, Mauco G, Tillement JP, Hauet T. Comparison of protective effects of trimetazidine against experimental warm ischemia of different durations: early and long-term effects in a pig kidney model. Am J Physiol Renal Physiol 2007, 292:F1082-F1093.
13. Favreau F, Thuillier R, Cau J, Milin S, Manguy E, Mauco G, Zhu X, Lerman LO, Hauet T. Anti-thrombin therapy during warm ischemia and cold preservation prevents chronic kidney graft fibrosis in a DCD model. Am J Transplant 2010, 10:30-39. 10.1111/j.1600-6143.2009.02924.x, 2807130, 19958330.
14. Chade AR, Rodriguez-Porcel M, Grande JP, Zhu X, Sica V, Napoli C, Sawamura T, Textor SC, Lerman A, Lerman LO. Mechanisms of renal structural alterations in combined hypercholesterolemia and renal artery stenosis. Arterioscler Thromb Vasc Biol 2003, 23:1295-1301. 10.1161/01.ATV.0000077477.40824.52, 12750121.
15. Loukogeorgakis SP, van den Berg MJ, Sofat R, Nitsch D, Charakida M, Haiyee B, de Groot E, MacAllister RJ, Kuijpers TW, Deanfield JE. Role of NADPH oxidase in endothelial ischemia/reperfusion injury in humans. Circulation 2010, 121:2310-2316. 10.1161/CIRCULATIONAHA.108.814731, 20479156.
16. Arslan F, Keogh B, McGuirk P, Parker AE. TLR2 and TLR4 in ischemia reperfusion injury. Mediators Inflamm 2010, 2010 704202:1-8.
17. Pulskens WP, Teske GJ, Butter LM, Roelofs JJ, van der Poll T, Florquin S, Leemans JC. Toll-like receptor-4 coordinates the innate immune response of the kidney to renal ischemia/reperfusion injury. PLoS One 2008, 3:e3596. 10.1371/journal.pone.0003596, 2570789, 18974879.
18. Jang HR, Ko GJ, Wasowska BA, Rabb H. The interaction between ischemia-reperfusion and immune responses in the kidney. J Mol Med 2009, 87:859-864. 10.1007/s00109-009-0491-y, 19562316.
19. Jang HR, Rabb H. The innate immune response in ischemic acute kidney injury. Clin Immunol 2009, 130:41-50. 10.1016/j.clim.2008.08.016, 2646108, 18922742.
20. Eltzschig HK, Eckle T. Ischemia and reperfusion-from mechanism to translation. Nat Med 2011, 17:1391-1401. 10.1038/nm.2507, 22064429.
21. Hosgood SA, Bagul A, Yang B, Nicholson ML. The relative effects of warm and cold ischemic injury in an experimental model of nonheartbeating donor kidneys. Transplantation 2008, 85:88-92. 10.1097/01.tp.0000296055.76452.1b, 18192917.
22. Wynn TA. Common and unique mechanisms regulate fibrosis in various fibroproliferative diseases. J Clin Invest 2007, 117:524-529. 10.1172/JCI31487, 1804380, 17332879.
23. Nakagawa T, Kang DH, Ohashi R, Suga S, Herrera-Acosta J, Rodriguez-Iturbe B, Johnson RJ. Tubulointerstitial disease: role of ischemia and microvascular disease. Curr Opin Nephrol Hypertens 2003, 12:233-241. 10.1097/00041552-200305000-00003, 12698060.
24. Liang HL, Hilton G, Mortensen J, Regner K, Johnson CP, Nilakantan V. MnTMPyP, a cell-permeant SOD mimetic, reduces oxidative stress and apoptosis following renal ischemia-reperfusion. Am J Physiol Renal Physiol 2009, 296:F266-F276. 2643863, 19091787.
25. Meldrum KK, Hile K, Meldrum DR, Crone JA, Gearhart JP, Burnett AL. Simulated ischemia induces renal tubular cell apoptosis through a nuclear factor-kappaB dependent mechanism. J Urol 2002, 168:248-252. 10.1016/S0022-5347(05)64902-6, 12050551.
26. Castaneda MP, Swiatecka-Urban A, Mitsnefes MM, Feuerstein D, Kaskel FJ, Tellis V, Devarajan P. Activation of mitochondrial apoptotic pathways in human renal allografts after ischemiareperfusion injury. Transplantation 2003, 76:50-54. 10.1097/01.TP.0000069835.95442.9F, 12865785.
27. Burns AT, Davies DR, McLaren AJ, Cerundolo L, Morris PJ, Fuggle SV. Apoptosis in ischemia/reperfusion injury of human renal allografts. Transplantation 1998, 66:872-876. 10.1097/00007890-199810150-00010, 9798696.
28. Leemans JC, Stokman G, Claessen N, Rouschop KM, Teske GJ, Kirschning CJ, Akira S, van der Poll T, Weening JJ, Florquin S. Renal-associated TLR2 mediates ischemia/reperfusion injury in the kidney. J Clin Invest 2005, 115:2894-2903. 10.1172/JCI22832, 1201659, 16167081.
29. Wu H, Chen G, Wyburn KR, Yin J, Bertolino P, Eris JM, Alexander SI, Sharland AF, Chadban SJ. TLR4 activation mediates kidney ischemia/reperfusion injury. J Clin Invest 2007, 117:2847-2859. 10.1172/JCI31008, 1974864, 17853945.
30. Thurman JM. Triggers of inflammation after renal ischemia/reperfusion. Clin Immunol 2007, 123:7-13. 10.1016/j.clim.2006.09.008, 1888143, 17064966.
31. Yamada Y, Fujii T, Ishijima R, Tachibana H, Yokoue N, Takasawa R, Tanuma S. DR396, an apoptotic DNase gamma inhibitor, attenuates high mobility group box 1 release from apoptotic cells. Bioorg Med Chem 2011, 19:168-171. 10.1016/j.bmc.2010.11.037, 21167721.
32. Chang WJ, Toledo-Pereyra LH. Toll-like receptor signaling in liver ischemia and reperfusion. J Invest Surg 2012, 25:271-277. 10.3109/08941939.2012.687802, 22853814.
33. Wu H, Ma J, Wang P, Corpuz TM, Panchapakesan U, Wyburn KR, Chadban SJ. HMGB1 contributes to kidney ischemia reperfusion injury. J Am Soc Nephrol 2010, 21:1878-1890. 10.1681/ASN.2009101048, 3014003, 20847143.
34. Wanderer AA. Rationale and timeliness for IL-1beta-targeted therapy to reduce allogeneic organ injury at procurement and to diminish risk of rejection after transplantation. Clin Transplant 2010, 24:307-311.
35. Deng J, Kohda Y, Chiao H, Wang Y, Hu X, Hewitt SM, Miyaji T, McLeroy P, Nibhanupudy B, Li S, Star RA. Interleukin-10 inhibits ischemic and cisplatin-induced acute renal injury. Kidney Int 2001, 60:2118-2128. 10.1046/j.1523-1755.2001.00043.x, 11737586.
36. Thuillier R, Favreau F, Celhay O, Macchi L, Milin S, Hauet T. Thrombin inhibition during kidney ischemia-reperfusion reduces chronic graft inflammation and tubular atrophy. Transplantation 2010, 90:612-621.
37. Boor P, Floege J. Chronic kidney disease growth factors in renal fibrosis. Clin Exp Pharmacol Physiol 2011, 38:441-450. 10.1111/j.1440-1681.2011.05487.x, 21276040.
38. Grandaliano G, Di Paolo S, Monno R, Stallone G, Ranieri E, Pontrelli P, Gesualdo L, Schena FP. Protease-activated receptor 1 and plasminogen activator inhibitor 1 expression in chronic allograft nephropathy: the role of coagulation and fibrinolysis in renal graft fibrosis. Transplantation 2001, 72:1437-1443. 10.1097/00007890-200110270-00018, 11685117.
39. Chatauret N, Thuillier R, Hauet T. Preservation strategies to reduce ischemic injury in kidney transplantation: pharmacological and genetic approaches. Curr Opin Organ Transplant 2011, 16:180-187. 10.1097/MOT.0b013e3283446b1d, 21415820.