Biliverdin Protects against Liver Ischemia Reperfusion Injury in Swine

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Andria, Barbara ^a   Bracco, Adele ^a   Attanasio, Chiara ^a   Castaldo, Sigismondo ^a   Cerrito, Maria Grazia ^c   Cozzolino, Santolo ^a   Di Napoli, Daniele ^a   Giovannoni, Roberto ^c   Mancini, Antonio ^a   Musumeci, Antonino ^b   Mezza, Ernesto ^b   Nasti, Mario ^b   Scuderi, Vincenzo ^a   Staibano, Stefania ^b   Lavitrano, Marialuisa ^c   Otterbein, Leo E ^d   Calise, Fulvio ^a  

^a CARDARELLI HOSPITAL   (Italy)

^b UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^c UNIVERSITY OF MILANO BICOCCA   (Italy)

^d BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMMONIA; ASPARTATE AMINOTRANSFERASE; BILIRUBIN; BILIVERDIN; UREA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; BILIRUBIN BLOOD LEVEL; CELL PROLIFERATION; CONTROLLED STUDY; DRUG EFFICACY; FEMALE; HISTOPATHOLOGY; LIVER DYSFUNCTION; LIVER GRAFT; LIVER ISCHEMIA; LIVER NECROSIS; LIVER PROTECTION; NEUTROPHIL CHEMOTAXIS; NONHUMAN; REPERFUSION INJURY; SWINE;

ANIMALS; BILIVERDINE; LIVER; REPERFUSION INJURY; SWINE;

EID: 84880776970     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0069972     Document Type: Article

References (33)

1. Scuderi V, Ceriello A, Maida P, Aragiusto G, Arenga G, et al. (2006) The marginal donor: a single center experience in orthotopic liver transplantation. Transplant Proc 38: 1069-1073.
2. Busuttil RW, Tanaka K, (2003) The utility of marginal donors in liver transplantation. Liver Transpl 9: 651-663.
3. Fondevila C, Busuttil RW, Kupiec-Weglinski JW, (2003) Hepatic ischemia/reperfusion injury-a fresh look. Exp Mol Pathol. 74: 86-93.
4. Selzner N, Rudiger H, Graf R, Clavien PA, (2003) Protective strategies against ischemic injury of the liver. Gastroenterology 125: 917-936.
5. Jaeschke H, Farhood A, (1991) Neutrophil and Kupffer cell-induced oxidant stress and ischemia-reperfusion injury in rat liver. Am J Physiol 260: 355-362.
6. Ar'Rajab A, Dawidson I, Fabia R, (1996) Reperfusion injury. New Horiz 4: 224-234.
7. Otterbein LE, Soares MP, Yamashita K, Bach FH, (2003) Heme oxygenase-1: unleashing the protective properties of heme. Trends in Immunol 24: 449-455.
8. Bach FH, (2005) Heme oxygenase-1: a therapeutic amplification funnel. FASEB J 19: 1216-1219.
9. Nakai M, Murata N, Yoda T, Yoshikawa Y, Watanabe K, et al. (2011) Binding of mammalian and avian ferritins with biotinylated hemin: demonstration of preferential binding of the H subunit to heme. J Vet Med Sci 73: 313-318.
10. Ryter SW, Alam J, Choi AM, (2006) Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol Rev 86: 583-650.
11. Nath KA, (2006) Heme oxygenase-1: a provenance for cytoprotective pathways in the kidney and other tissues. Kidney Int 70: 432-443.
12. Motterlini R, Otterbein LE, (2010) The therapeutic potential of carbon monoxide. Nat Rev Drug Discov 9: 728-43.
13. Wegiel B, Hanto DW, Otterbein LE, (2013) The social network of carbon monoxide in medicine. Trends Mol Med 1: 3-11.
14. Wegiel B, Otterbein LE, (2012) Go green: the anti-inflammatory effects of biliverdin reductase. Front Pharmacol 3: 47.
15. Lavitrano M, Smolenski RT, Musumeci A, Maccherini M, Slominska E, et al. (2004) Carbon monoxide improves cardiac energetics and safeguards the heart during reperfusion after cardiopulmonary bypass in pigs. FASEB J 18: 1093-1095.
16. Vanden Hoek TL. (2002) Preconditioning and post-resuscitation injury. Crit Care Med 30(4 Suppl): 172-175.
17. Brouard S, Berberat PO, Tobiasch E, Seldon MP, Bach FH, et al. (2002) 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 277: 17950-17961.
18. Moore BA, Overhaus M, Whitcomb J, Ifedigbo E, Choi AM, et al. (2005) Inhalation of low-dose carbon monoxide protects rodents and swine from postoperative ileus. Crit Care Med 33: 1317-1326.
19. Raman KG, Barbato JE, Ifedigbo E, Ozanich BA, Zenati MS, et al. (2006) Inhaled carbon monoxide inhibits intimal hyperplasia and provides added benefit with nitric oxide. J Vasc Surg 44: 151-158.
20. Zuckerbraun BS, Billiar TR, Otterbein SL, Kim PK, Liu F, et al. (2003) Carbon monoxide protects against liver failure through nitric oxide-induced heme oxygenase-1. J Exp Med 198: 1707-1716.
21. Kim HP, Wang X, Zhang J, Suh GY, Benjamin IJ, et al. (2005) Heat shock protein-70 mediates the cytoprotective effect of carbon monoxide: involvement of p38 beta MAPK and heat shock factor-1. J Immunol 175: 2622-2629.
22. Wegiel B, Gallo D, Csizmadia E, Roger T, Kaczmarek E, et al. (2011) Biliverdin inhibits Toll-like receptor-4 (TLR4) expression through nitric oxide-dependent nuclear translocation of biliverdin reductase. Proc Natl Acad Sci USA 108: 18849-18854.
23. Wegiel B, Baty CJ, Gallo D, Csizmadia E, Scott JR, et al. (2009) Cell surface biliverdin reductase mediates biliverdin-induced anti-inflammatory effects via phosphatidylinositol 3-kinase and Akt. J Biol Chem 284: 21369-21378.
24. Bulmer AC, Coombes JS, Blanchfield JT, Toth I, Fassett RGet al, (2011) Bile pigment pharmacokinetics and absorption in the rat: therapeutic potential for enteral administration. Br J Pharmacol 164: 1857-70.
25. Akamatsu Y, Haga M, Tyagi S, Yamashita K, Graça-Souza AV, et al. (2004) Heme oxygenase-1-derived carbon monoxide protects hearts from transplant associated ischemia reperfusion injury. FASEB J 18: 771-772.
26. Nakao A, Neto JS, Kanno S, Stolz DB, Kimizuka K, et al. (2005) Protection against ischemia/reperfusion injury in cardiac and renal transplantation with carbon monoxide, biliverdin and both. Am J Transplant 5: 282-291.
27. Nakao A, Toyokawa H, Tsung A, Nalesnik MA, Stolz DB, et al. (2006) Ex vivo application of carbon monoxide in University of Wisconsin solution to prevent intestinal cold ischemia/reperfusion injury. Am J Transplant 6: 2243-22455.
28. Hanto DW, Maki T, Yoon MH, Csizmadia E, Chin BY, et al. (2010) Intraoperative administration of inhaled carbon monoxide reduces delayed graft function in kidney allografts in swine. Am J Transplant. 10: 2421-30.
29. Fondevila C, Shen XD, Tsuchiyashi S, Yamashita K, Csizmadia E, et al. (2004) Biliverdin therapy protects rat livers from ischemia and reperfusion injury. Hepatology 40: 1333-1341.
30. Kato Y, Shimazu M, Kondo M, Uchida K, Kumamoto Y, et al. (2003) Bilirubin rinse: A simple protectant against the rat liver graft injury mimicking heme oxygenase-1 preconditioning. Hepatology 38: 364-373.
31. Wang H, Lee SS, Gao W, Czismadia E, McDaid J, et al. (2005) Donor treatment with carbon monoxide can yield islet allograft survival and tolerance. Diabetes 54: 1400-1406.
32. Yang XF, Chen YZ, Su JL, Wang FY, Wang LX, (2009) Relationship between serum bilirubin and carotid atherosclerosis in hypertensive patients. Intern Med 48: 1595-1599.
33. Vítek L, Novotný L, Sperl M, Holaj R, Spácil J, (2006) The inverse association of elevated serum bilirubin levels with subclinical carotid atherosclerosis. Cerebrovasc Dis 21: 408-414.