CORMs protect endothelial cells during cold preservation, resulting in inhibition of intimal hyperplasia after aorta transplantation in rats

Transplant International

Volumn 23, Issue 11, 2010, Pages 1144-1153

  Song, Hui ^a,b   Hoeger, Simone ^a   Hillebrands, Jan Luuk ^c   Mandel, Isabell ^a   Loesel, Ralf ^d   Beck, Grietje ^a   Schilling, Lothar ^e   Schnuelle, Peter ^a   Yard, Benito ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b SHANDONG UNIVERSITY   (China)

^c UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^d University of Applied Sciences Nuernberg   (Germany)

^e MEDICAL FACULTY MANNHEIM HEIDELBERG UNIVERSITY   (Germany)

Author keywords

carbon monoxide releasing molecules; cold preservation; experimental transplantation; intimal hyperplasia; vascular function

Indexed keywords

ACETYLCHOLINE; CARBON MONOXIDE; CARBON MONOXIDE RELEASING MOLECULE 3; RUTHENIUM DERIVATIVE; UNCLASSIFIED DRUG; UNIVERSITY OF WISCONSIN SOLUTION;

ABDOMINAL AORTA; ADVENTITIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA GRAFT; ARTERY INTIMA PROLIFERATION; ARTICLE; BLOOD VESSEL INJURY; CELL PROTECTION; CONTROLLED STUDY; CRYOPRESERVATION; ENDOTHELIUM CELL; EXPERIMENTAL TRANSPLANTATION; HUMAN; HUMAN CELL; LEWIS RAT; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; RAT STRAIN; VASODILATATION;

ANIMALS; AORTA; BLOOD VESSEL PROSTHESIS; CARBON MONOXIDE; COLD TEMPERATURE; CRYOPRESERVATION; ENDOTHELIUM, VASCULAR; HUMANS; HYPERPLASIA; MALE; ORGAN PRESERVATION SOLUTIONS; ORGANOMETALLIC COMPOUNDS; RATS; RATS, INBRED F344; RATS, INBRED LEW; TISSUE AND ORGAN HARVESTING; TUNICA INTIMA;

EID: 77957602846     PISSN: 09340874     EISSN: 14322277     Source Type: Journal    
DOI: 10.1111/j.1432-2277.2010.01102.x     Document Type: Article

References (40)

1. de Perrot M, Liu M, Waddell TK, Keshavjee S. Ischemia-reperfusion-induced lung injury. Am J Respir Crit Care Med 2003 167 : 490.
2. Yard B, Beck G, Schnuelle P, et al. Prevention of cold-preservation injury of cultured endothelial cells by catecholamines and related compounds. Am J Transplant 2004 4 : 22.
3. Ikeyama K, Sakai H, Omasa M, et al. Effects of cold preservation on the lung mechanical properties in rats. Eur Surg Res 2005 37 : 85.
4. Salahudeen AK, Haider N, May W. Cold ischemia and the reduced long-term survival of cadaveric renal allografts. Kidney Int 2004 65 : 713.
5. Salahudeen AK. Consequences of cold ischemic injury of kidneys in clinical transplantation. J Investig Med 2004 52 : 296.
6. Kieran NE, Rabb H. Immune responses in kidney preservation and reperfusion injury. J Investig Med 2004 52 : 310.
7. Dragun D, Hoff U, Park JK, et al. Prolonged cold preservation augments vascular injury independent of renal transplant immunogenicity and function. Kidney Int 2001 60 : 1173.
8. Schnuelle P, Berger S, de Boer J, Persijn G, van der Woude FJ. Effects of catecholamine application to brain-dead donors on graft survival in solid organ transplantation. Transplantation 2001 72 : 455.
9. Schnuelle P, Yard BA, Braun C, et al. Impact of donor dopamine on immediate graft function after kidney transplantation. Am J Transplant 2004 4 : 419.
10. Libby P, Pober JS. Chronic rejection. Immunity 2001 14 : 387.
11. Hillebrands JL, Klatter FA, van den Hurk BM, Popa ER, Nieuwenhuis P, Rozing J. Origin of neointimal endothelium and alpha-actin-positive smooth muscle cells in transplant arteriosclerosis. J Clin Invest 2001 107 : 1411.
12. Hillebrands JL, Onuta G, Rozing J. Role of progenitor cells in transplant arteriosclerosis. Trends Cardiovasc Med 2005 15 : 1.
13. Sammut IA, Foresti R, Clark JE, et al. Carbon monoxide is a major contributor to the regulation of vascular tone in aortas expressing high levels of haeme oxygenase-1. Br J Pharmacol 1998 125 : 1437.
14. Motterlini R, Gonzales A, Foresti R, Clark JE, Green CJ, Winslow RM. Heme oxygenase-1-derived carbon monoxide contributes to the suppression of acute hypertensive responses in vivo. Circ Res 1998 83 : 568.
15. Morita T, Mitsialis SA, Koike H, Liu Y, Kourembanas S. Carbon monoxide controls the proliferation of hypoxic vascular smooth muscle cells. J Biol Chem 1997 272 : 32804.
16. Durante W, Schafer AI. Carbon monoxide and vascular cell function (review). Int J Mol Med 1998 2 : 255.
17. Zhang X, Shan P, Otterbein LE, et al. Carbon monoxide inhibition of apoptosis during ischemia-reperfusion lung injury is dependent on the p38 mitogen-activated protein kinase pathway and involves caspase 3. J Biol Chem 2003 278 : 1248.
18. Otterbein LE, Bach FH, Alam J, et al. Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway. Nat Med 2000 6 : 422.
19. Nakao A, Neto JS, Kanno S, et al. Protection against ischemiareperfusion injury in cardiac and renal transplantation with carbon monoxide, biliverdin and both. Am J Transplant 2005 5 : 282.
20. Matsumoto M, Makino Y, Tanaka T, et al. Induction of renoprotective gene expression by cobalt ameliorates ischemic injury of the kidney in rats. J Am Soc Nephrol 2003 14 : 1825.
21. Kaizu T, Nakao A, Tsung A, et al. Carbon monoxide inhalation ameliorates cold ischemiareperfusion injury after rat liver transplantation. Surgery 2005 138 : 229.
22. Kohmoto J, Nakao A, Kaizu T, et al. Low-dose carbon monoxide inhalation prevents ischemiareperfusion injury of transplanted rat lung grafts. Surgery 2006 140 : 179.
23. Nakao A, Toyokawa H, Tsung A, et al. Ex vivo application of carbon monoxide in University of Wisconsin solution to prevent intestinal cold ischemiareperfusion injury. Am J Transplant 2006 6 : 2243.
24. Motterlini R, Mann BE, Johnson TR, Clark JE, Foresti R, Green CJ. Bioactivity and pharmacological actions of carbon monoxide-releasing molecules. Curr Pharm Des 2003 9 : 2525.
25. Musameh MD, Green CJ, Mann BE, Fuller BJ, Motterlini R. Improved myocardial function after cold storage with preservation solution supplemented with a carbon monoxide-releasing molecule (CORM-3). J Heart Lung Transplant 2007 26 : 1192.
26. Kerkweg U, Jacob M, De Groot H, Mannherz HG, Rauen U. Cold-induced apoptosis of rat liver endothelial cells: contribution of mitochondrial alterations. Transplantation 2003 76 : 501.
27. Clark JE, Naughton P, Shurey S, et al. Cardioprotective actions by a water-soluble carbon monoxide-releasing molecule. Circ Res 2003 93 : e2.
28. Witte K, Reitenbach I, Stolpe K, Schilling L, Kirchengast M, Lemmer B. Effects of the endothelin a receptor antagonist darusentan on blood pressure and vascular contractility in type 2 diabetic Goto-Kakizaki rats. J Cardiovasc Pharmacol 2003 41 : 890.
29. Sandouka A, Fuller BJ, Mann BE, Green CJ, Foresti R, Motterlini R. Treatment with CO-RMs during cold storage improves renal function at reperfusion. Kidney Int 2006 69 : 239.
30. Otterbein LE, Zuckerbraun BS, Haga M, et al. Carbon monoxide suppresses arteriosclerotic lesions associated with chronic graft rejection and with balloon injury. Nat Med 2003 9 : 183.
31. Radovits T, Lin LN, Zotkina J, et al. Endothelial dysfunction after long-term cold storage in HTK organ preservation solutions: effects of iron chelators and N-alpha-acetyl-L-histidine. J Heart Lung Transplant 2008 27 : 208.
32. Knight RJ, Liu H, Fishman E, Reis ED. Cold ischemic injury, aortic allograft vasculopathy, and pro-inflammatory cytokine expression. J Surg Res 2003 113 : 201.
33. Nakao A, Kaczorowski DJ, Wang Y, et al. Amelioration of rat cardiac cold ischemiareperfusion injury with inhaled hydrogen or carbon monoxide, or both. J Heart Lung Transplant 2010 29 : 544.
34. Brinkkoetter PT, Song H, Losel R, et al. Hypothermic injury: the mitochondrial calcium, ATP and ROS love-hate triangle out of balance. Cell Physiol Biochem 2008 22 : 195.
35. Song H, Bergstrasser C, Rafat N, et al. The carbon monoxide releasing molecule (CORM-3) inhibits expression of vascular cell adhesion molecule-1 and E-selectin independently of haem oxygenase-1 expression. Br J Pharmacol 2009 157 : 769.
36. Stoltenberg RL, Geraghty J, Steele DM, Kennedy E, Hullett DA, Sollinger HW. Inhibition of intimal hyperplasia in rat aortic allografts with cyclosporine. Transplantation 1995 60 : 993.
37. Herrero-Fresneda I, Torras J, Vidal A, Lloberas N, Cruzado JM, Grinyo JM. Reduction of postischemic immune inflammatory response: an effective strategy for attenuating chronic allograft nephropathy. Transplantation 2005 79 : 165.
38. Pascher A, Reutzel-Selke A, Jurisch A, et al. Alterations of the immune response with increasing recipient age are associated with reduced long-term organ graft function of rat kidney allografts. Transplantation 2003 76 : 1560.
39. Martins PN, Kessler H, Jurisch A, et al. Induction of heme oxygenase-1 in the donor reduces graft immunogenicity. Transplant Proc 2005 37 : 384.
40. Wang H, Lee SS, Gao W, et al. Donor treatment with carbon monoxide can yield islet allograft survival and tolerance. Diabetes 2005 54 : 1400.