Carbon monoxide protects rat lung transplants from ischemia-reperfusion injury via a mechanism involving p38 MAPK pathway

American Journal of Transplantation

Volumn 7, Issue 10, 2007, Pages 2279-2290

  Kohmoto, J ^a,b   Nakao, A ^a   Stolz, D B ^b   Kaizu, T ^a   Tsung, A ^a   Ikeda, A ^a   Shimizu, H ^c   Takahashi, T ^c   Tomiyama, K ^a   Sugimoto, R ^a,b   Choi, A M K ^d   Billiar, T R ^a   Murase, N ^a   McCurry, K R ^a,b  

^a UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

^b UNIVERSITY OF PITTSBURGH   (United States)

^c OKAYAMA UNIVERSITY   (Japan)

^d UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Carbon monoxide; Heme oxygenase 1; Ischemia reperfusion; Lung transplantation; p38 MAPK

Indexed keywords

CARBON MONOXIDE; MITOGEN ACTIVATED PROTEIN KINASE P38; MITOGEN ACTIVATED PROTEIN KINASE P38 INHIBITOR;

ANALYTIC METHOD; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL ULTRASTRUCTURE; COLD ISCHEMIA; COMPARATIVE STUDY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CRYOPRESERVATION; ENDOTHELIUM CELL; ENZYME PHOSPHORYLATION; LUNG GRAFT REJECTION; LUNG TRANSPLANTATION; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; REPERFUSION INJURY; SIGNAL TRANSDUCTION;

ANIMALS; ANTI-INFLAMMATORY AGENTS; CARBON MONOXIDE; CYCLOOXYGENASE 2; INTERLEUKINS; LUNG; LUNG TRANSPLANTATION; MALE; MITOGEN-ACTIVATED PROTEIN KINASE 14; NEUTROPHILS; NITRIC OXIDE SYNTHASE TYPE II; RATS; RATS, INBRED LEW; REPERFUSION INJURY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TRANSPLANTATION, HOMOLOGOUS; TRANSPLANTATION, ISOGENEIC;

EID: 34548331673     PISSN: 16006135     EISSN: 16006143     Source Type: Journal    
DOI: 10.1111/j.1600-6143.2007.01940.x     Document Type: Article

References (45)

1. Trulock EP, Edwards LB, Taylor DO, Boucek MM, Keck BM, Hertz MI. Registry of the International Society for Heart and Lung Transplantation: Twenty-third official adult lung and heart-lung transplantation report-2006. J Heart Lung Transplant 2006 25 : 880 892.
2. de Perrot M, Liu M, Waddell TK, Keshavjee S. Ischemia-reperfusion-induced lung injury. Am J Respir Crit Care Med 2003 167 : 490 511.
3. Christie JD, Bavaria JE, Palevsky HI et al. Primary graft failure following lung transplantation. Chest 1998 114 : 51 60.
4. Fiser SM, Tribble CG, Long SM et al. Ischemia-reperfusion injury after lung transplantation increases risk of late bronchiolitis obliterans syndrome. Ann Thorac Surg 2002 73 : 1041 1047 discussion 1047-1048.
5. Fisher AJ, Donnelly SC, Hirani N et al. Enhanced pulmonary inflammation in organ donors following fatal non-traumatic brain injury. Lancet 1999 353 : 1412 1413.
6. Poss KD, Tonegawa S. Heme oxygenase 1 is required for mammalian iron reutilization. Proc Natl Acad Sci U S A 1997 94 : 10919 10924.
7. Otterbein LE, Choi AM. Heme oxygenase: Colors of defense against cellular stress. Am J Physiol Lung Cell Mol Physiol 2000 279 : L1029 L1037.
8. Zuckerbraun BS, McCloskey CA, Gallo D et al. Carbon monoxide prevents multiple organ injury in a model of hemorrhagic shock and resuscitation. Shock 2005 23 : 527 532.
9. Otterbein LE, Mantell LL, Choi AM. Carbon monoxide provides protection against hyperoxic lung injury. Am J Physiol 1999 276 (4 Pt 1 L688 L694.
10. Kyokane T, Norimizu S, Taniai H et al. Carbon monoxide from heme catabolism protects against hepatobiliary dysfunction in endotoxin-treated rat liver. Gastroenterology 2001 120 : 1227 1240.
11. Nakao A, Kimizuka K, Stolz DB et al. Protective effect of carbon monoxide inhalation for cold-preserved small intestinal grafts. Surgery 2003 134 : 285 292.
12. Nakao A, Moore BA, Murase N et al. Immunomodulatory effects of inhaled carbon monoxide on rat syngeneic small bowel graft motility. Gut 2003 52 : 1278 1285.
13. Nakao A, Kimizuka K, Stolz DB et al. Carbon monoxide inhalation protects rat intestinal grafts from ischemia/reperfusion injury. Am J Pathol 2003 163 : 1587 1598.
14. Kaizu T, Nakao A, Tsung A et al. Carbon monoxide inhalation ameliorates cold ischemia/reperfusion injury after rat liver transplantation. Surgery 2005 138 : 229 235.
15. Neto JS, Nakao A, Kimizuka K et al. Protection of transplant-induced renal ischemia-reperfusion injury with carbon monoxide. Am J Physiol Renal Physiol 2004 287 : F979-F989.
16. Akamatsu Y, Haga M, Tyagi S et al. Heme oxygenase-1-derived carbon monoxide protects hearts from transplant associated ischemia reperfusion injury. FASEB J 2004 18 : 771 772.
17. Mishra S, Fujita T, Lama VN et al. Carbon monoxide rescues ischemic lungs by interrupting MAPK-driven expression of early growth response 1 gene and its downstream target genes. Proc Natl Acad Sci U S A 2006 103 : 5191 5196.
18. Kohmoto J, Nakao A, Kaizu T et al. Low-dose carbon monoxide inhalation prevents ischemia/reperfusion injury of transplanted rat lung grafts. Surgery 2006 140 : 179 185.
19. Mizuta T, Kawaguchi A, Nakahara K, Kawashima Y. Simplified rat lung transplantation using a cuff technique. J Thorac Cardiovasc Surg 1989 97 : 578 581.
20. Nakao A, Toyokawa H, Tsung A et al. Ex vivo application of carbon monoxide in University of Wisconsin Solution to prevent intestinal cold ischemia/reperfusion injury. Am J Transplant 2006 6 : 2243 2255.
21. Nakao A, Neto JS, Kanno S et al. Protection against ischemia/reperfusion injury in cardiac and renal transplantation with carbon monoxide, biliverdin and both. Am J Transplant 2005 5 : 282 291.
22. Takahashi Y, Ganster RW, Gambotto A et al. Role of NF-kappaB on liver cold ischemia-reperfusion injury. Am J Physiol Gastrointest Liver Physiol 2002 283 : G1175-G1184.
23. Sunderman FW, Jr., Downs JR, Reid MC, Bibeau LM. Gas-chromatographic assay for heme oxygenase activity. Clin Chem 1982 28 : 2026 2032.
24. Fischer S, Cassivi SD, Xavier AM et al. Cell death in human lung transplantation: Apoptosis induction in human lungs during ischemia and after transplantation. Ann Surg 2000 231 : 424 431.
25. Fischer S, Maclean AA, Liu M et al. Dynamic changes in apoptotic and necrotic cell death correlate with severity of ischemia-reperfusion injury in lung transplantation. Am J Respir Crit Care Med 2000 162 : 1932 1939.
26. de Perrot M, Fischer S, Liu M et al. Impact of human interleukin-10 on vector-induced inflammation and early graft function in rat lung transplantation. Am J Respir Cell Mol Biol 2003 28 : 616 625.
27. Eppinger MJ, Deeb GM, Bolling SF, Ward PA. Mediators of ischemia-reperfusion injury of rat lung. Am J Pathol 1997 150 : 1773 1184.
28. Serrick C, Adoumie R, Giaid A, Shennib H. The early release of interleukin-2, tumor necrosis factor-alpha and interferon-gamma after ischemia reperfusion injury in the lung allograft. Transplantation 1994 58 : 1158 1162.
29. 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 : 422 428.
30. Moore BA, Otterbein LE, Turler A, Choi AM, Bauer AJ. Inhaled carbon monoxide suppresses the development of postoperative ileus in the murine small intestine. Gastroenterology 2003 124 : 377 391.
31. Eppinger MJ, Ward PA, Bolling SF, Deeb GM. Regulatory effects of interleukin-10 on lung ischemia-reperfusion injury. J Thorac Cardiovasc Surg 1996 112 : 1301 1305 discussion 1305-1306.
32. Teoh N, Dela Pena A, Farrell G. Hepatic ischemic preconditioning in mice is associated with activation of NF-kappaB, p38 kinase, and cell cycle entry. Hepatology 2002 36 : 94 102.
33. Kunduzova OR, Bianchi P, Pizzinat N et al. Regulation of JNK/ERK activation, cell apoptosis, and tissue regeneration by monoamine oxidases after renal ischemia-reperfusion. FASEB J 2002 16 : 1129 1131.
34. Khandoudi N, Delerive P, Berrebi-Bertrand I, Buckingham RE, Staels B, Bril A. Rosiglitazone, a peroxisome proliferator-activated receptor-gamma, inhibits the Jun NH(2)-terminal kinase/activating protein 1 pathway and protects the heart from ischemia/reperfusion injury. Diabetes 2002 51 : 1507 1514.
35. Bradham CA, Stachlewitz RF, Gao W et al. Reperfusion after liver transplantation in rats differentially activates the mitogen-activated protein kinases. Hepatology 1997 25 : 1128 1135.
36. 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 1258.
37. Amersi F, Shen XD, Anselmo D et al. Ex vivo exposure to carbon monoxide prevents hepatic ischemia/reperfusion injury through p38 MAP kinase pathway. Hepatology 2002 35 : 815 823.
38. Brouard S, Berberat PO, Tobiasch E, Seldon MP, Bach FH, Soares MP. Heme oxygenase-1-derived carbon monoxide requires the activation of transcription factor NF-kappa B to protect endothelial cells from tumor necrosis factor-alpha-mediated apoptosis. J Biol Chem 2002 277 : 17950 17961.
39. Fujimoto H, Ohno M, Ayabe S et al. Carbon monoxide protects against cardiac ischemia-reperfusion injury in vivo via MAPK and Akt-eNOS pathways. Arterioscler Thromb Vasc Biol 2004 24 : 1848 1853.
40. Von Burg R. Carbon monoxide. J Appl Toxicol 1999 19 : 379 386.
41. Mayr FB, Spiel A, Leitner J et al. Effects of carbon monoxide inhalation during experimental endotoxemia in humans. Am J Respir Crit Care Med 2005 171 : 354 360.
42. Fujita T, Toda K, Karimova A et al. Paradoxical rescue from ischemic lung injury by inhaled carbon monoxide driven by derepression of fibrinolysis. Nat Med 2001 7 : 598 604.
43. Soccal PM, Gasche Y, Miniati DN et al. Matrix metalloproteinase inhibition decreases ischemia-reperfusion injury after lung transplantation. Am J Transplant 2004 4 : 41 50.
44. Davies SP, Reddy H, Caivano M, Cohen P. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem J 2000 351 (Pt 1 95 105.
45. Weber NC, Toma O, Wolter JI et al. The noble gas xenon induces pharmacological preconditioning in the rat heart in vivo via induction of PKC-epsilon and p38 MAPK. Br J Pharmacol 2005 144 : 123 132.