Hemoglobin-Glutamer 200 Reduces Reperfusion Injury of the Cold Preserved Rat Liver by Induction of Heme Oxygenase-1

Journal of Surgical Research

Volumn 150, Issue 2, 2008, Pages 243-254

  Topp, Stefan A ^a   Krieg, Andreas ^a   Koch, Alexander ^b   Tidden, Carina M ^a   Ramp, Uwe ^a   Hohlfeld, Thomas ^a   Macher, Arne ^a   Schulte am Esch II, Jan ^a   Eisenberger, Claus F ^a   Stoecklein, Nikolas H ^a   Knoefel, Wolfram T ^a  

^a UNIVERSITY HOSPITAL DÜSSELDORF   (Germany)

^b UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

HBOC; hemoglobin glutamer; HO 1; IPRL; ischemia reperfusion; liver preservation; oxyglobin

Indexed keywords

ALANINE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; HEME OXYGENASE 1; HEMOGLOBIN GLUTAMER 200; PROTOPORPHYRIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; COLD ISCHEMIA; CONTROLLED STUDY; ENZYME ACTIVITY; LIPID PEROXIDATION; LIVER FUNCTION; LIVER INJURY; LIVER PRESERVATION; MALE; NONHUMAN; PORTAL VEIN BLOOD FLOW; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REPERFUSION INJURY;

ANIMALS; APOPTOSIS; COLD ISCHEMIA; ENZYME INDUCTION; HEME OXYGENASE (DECYCLIZING); HEMOGLOBINS; LIPID PEROXIDATION; LIVER; LIVER CIRCULATION; LIVER FUNCTION TESTS; MALE; ORGAN PRESERVATION; RATS; RATS, WISTAR; REPERFUSION; REPERFUSION INJURY;

EID: 56449105931     PISSN: 00224804     EISSN: 10958673     Source Type: Journal    
DOI: 10.1016/j.jss.2008.02.033     Document Type: Article

References (59)

1. Belzer F.O., D'Alessandro A.M., Hoffmann R.M., et al. The use of UW solution in clinical transplantation. A 4-year experience. Ann Surg 215 (1992) 579
2. Jain A., Reyes J., Kashyap R., et al. Long-term survival after liver transplantation in 4000 consecutive patients at a single center. Ann Surg 232 (2000) 490
3. Ploeg R.J., D'Alessandro A.M., Knechtle S.J., et al. Risk factors for primary dysfunction after liver transplantation-a multivariate analysis. Transplantation 55 (1993) 807
4. Strasberg S.M., Howard T.K., Molmenti E.P., et al. Selecting the donor liver: Risk factors for poor function after orthotopic liver transplantation. Hepatology 20 (1994) 829
5. Mor E., Klintmalm G.B., Gonwa T.A., et al. The use of marginal donors for liver transplantation. A retrospective study of 365 liver donors. Transplantation 53 (1992) 383
6. Caldwell-Kenkel J.C., Thurman R.G., and Lemasters J.J. Selective loss of nonparenchymal cell viability after cold ischemic storage of rat livers. Transplantation 45 (1988) 834
7. McKeown C.M., Edwards V., Phillips M.J., et al. Sinusoidal lining cell damage: The critical injury in cold preservation of liver allografts in the rat. Transplantation 46 (1988) 178
8. Upadhya G.A., and Strasberg S.M. Evidence that actin disassembly is a requirement for matrix metalloproteinase secretion by sinusoidal endothelial cells during cold preservation in the rat. Hepatology 30 (1999) 169
9. Upadhya G.A., Topp S.A., Hotchkiss R.S., et al. Effect of cold preservation on intracellular calcium concentration and calpain activity in rat sinusoidal endothelial cells. Hepatology 37 (2003) 313
10. Clavien P.A., Morgan G.R., Sanabria J.R., et al. Effect of cold preservation on lymphocyte adherence in the perfused rat liver. Transplantation 52 (1991) 412
11. Cywes R., Packham M.A., Tietze L., et al. Role of platelets in hepatic allograft preservation injury in the rat. Hepatology 18 (1993) 635
12. Cywes R., Mullen J.B., Stratis M.A., et al. Prediction of the outcome of transplantation in man by platelet adherence in donor liver allografts. Evidence of the importance of pre-preservation injury. Transplantation 56 (1993) 316
13. Thiel M., Imendorffer S., Chouker A., et al. Expression of adhesion molecules on circulating polymorphonuclear leukocytes during orthotopic liver transplantation. Hepatology 28 (1998) 1538
14. Chun K., Zhang J., Biewer J., et al. Microcirculatory failure determines lethal hepatocyte injury in ischemic/reperfused rat livers. Shock 1 (1994)
15. Koo A., Komatsu H., Tao G., et al. Contribution of no-reflow phenomenon to hepatic injury after ischemia-reperfusion: Evidence for a role for superoxide anion. Hepatology 15 (1992) 507
16. Menger M.D., Richter S., Yamauchi J., et al. Role of microcirculation in hepatic ischemia/reperfusion injury. Hepatogastroenterology 46 Suppl 2 (1999) 1452
17. Driessen B., Jahr J.S., Lurie F., et al. Effects of hemoglobin-based oxygen carrier hemoglobin glutamer-200 (bovine) on intestinal perfusion and oxygenation in a canine hypovolemia model. Br J Anaesth 86 (2001) 683
18. Driessen B., Jahr J.S., Lurie F., et al. Arterial oxygenation and oxygen delivery after hemoglobin-based oxygen carrier infusion in canine hypovolemic shock: A dose-response study. Crit Care Med 31 (2003) 1771
19. Standl T., Horn P., Wilhelm S., et al. Bovine hemoglobin is more potent than autologous red blood cells in restoring muscular tissue oxygenation after profound isovolemic hemodilution in dogs. Can J Anaesth 43 (1996) 714
20. Freitag M., Standl T.G., Gottschalk A., et al. Enhanced central organ oxygenation after application of bovine cell-free hemoglobin HBOC-201. Can J Anaesth 52 (2005) 904
21. Johnson T., Arnaud F., Dong F., et al. Bovine polymerized hemoglobin (hemoglobin-based oxygen carrier-201) resuscitation in three swine models of hemorrhagic shock with militarily relevant delayed evacuation-effects on histopathology and organ function. Crit Care Med 34 (2006) 1464
22. Katz L.M., Manning J.E., McCurdy S., et al. HBOC-201 improves survival in a swine model of hemorrhagic shock and liver injury. Resuscitation 54 (2002) 77
23. Knudson M.M., Lee S., Erickson V., et al. Tissue oxygen monitoring during hemorrhagic shock and resuscitation: A comparison of lactated Ringer's solution, hypertonic saline dextran, and HBOC-201. J Trauma 54 (2003) 242
24. Burmeister M.A., Rempf C., Standl T.G., et al. Effects of prophylactic or therapeutic application of bovine hemoglobin HBOC-200 on ischemia-reperfusion injury following acute coronary ligature in rats. Br J Anaesth 95 (2005) 737
25. Caswell J.E., Strange M.B., Rimmer III D.M., et al. A novel hemoglobin-based blood substitute protects against myocardial reperfusion injury. Am J Physiol Heart Circ Physiol 288 (2005) H1796
26. Redaelli C.A., Tian Y.H., Schaffner T., et al. Extended preservation of rat liver graft by induction of heme oxygenase-1. Hepatology 35 (2002) 1082
27. Miller L.L., Bly C.G., Watson M.L., et al. The dominant role of the liver in plasma protein synthesis: A direct study of the isolated perfused rat liver with the aid of lysine-epsilon-C14. J Exp Med 94 (1951) 431
28. Willis D., Moore A.R., Frederick R., et al. Heme oxygenase: A novel target for the modulation of the inflammatory response. Nat Med 2 (1996) 87
29. Ledergerber D., and Hartmann R.W. Development of a screening assay for the in vitro evaluation of thromboxane A2 synthase inhibitors. J Enzyme Inhib 9 (1995) 253
30. Camargo Jr. C.A., Madden J.F., Gao W., et al. Interleukin-6 protects liver against warm ischemia/reperfusion injury and promotes hepatocyte proliferation in the rodent. Hepatology 26 (1997) 1513
31. Kato Y., Shimazu M., Kondo M., et al. Bilirubin rinse: A simple protectant against the rat liver graft injury mimicking heme oxygenase-1 preconditioning. Hepatology 38 (2003) 364
32. Katori M., Busuttil R.W., and Kupiec-Weglinski J.W. Heme oxygenase-1 system in organ transplantation. Transplantation 74 (2002) 905
33. Cabrales P., Tsai A.G., and Intaglietta M. Increased tissue PO2 and decreased O2 delivery and consumption after 80% exchange transfusion with polymerized hemoglobin. Am J Physiol Heart Circ Physiol 287 (2004) H2825
34. Page T.C., Light W.R., McKay C.B., et al. Oxygen transport by erythrocyte/hemoglobin solution mixtures in an in vitro capillary as a model of hemoglobin-based oxygen carrier performance. Microvasc Res 55 (1998) 54
35. Doherty D.H., Doyle M.P., Curry S.R., et al. Rate of reaction with nitric oxide determines the hypertensive effect of cell-free hemoglobin. Nat Biotechnol 16 (1998) 672
36. Hess J.R., MacDonald V.W., and Brinkley W.W. Systemic and pulmonary hypertension after resuscitation with cell-free hemoglobin. J Appl Physiol 74 (1993) 1769
37. Olson J.S., Foley E.W., Rogge C., et al. No scavenging and the hypertensive effect of hemoglobin-based blood substitutes. Free Radical Biol Med 36 (2004) 685
38. Sharma A.C., Singh G., and Gulati A. Role of NO mechanism in cardiovascular effects of diaspirin cross-linked hemoglobin in anesthetized rats. Am J Physiol 269 (1995) H1379
39. Winslow R.M. Current status of blood substitute research: Towards a new paradigm. J Intern Med 253 (2003) 508
40. Pannen B.H., Al-Adili F., Bauer M., et al. Role of endothelin and nitric oxide in hepatic reperfusion injury in the rat. Hepatology 27 (1998) 755
41. Shah V., Haddad F.G., Garcia-Cardena G., et al. Liver sinusoidal endothelial cells are responsible for nitric oxide modulation of resistance in the hepatic sinusoids. J Clin Invest 100 (1997) 2923
42. Zhang J.X., Pegoli Jr. W., and Clemens M.G. Endothelin-1 induces direct constriction of hepatic sinusoids. Am J Physiol 266 (1994) G624
43. Rensing H., Bauer I., Zhang J.X., et al. Endothelin-1 and heme oxygenase-1 as modulators of sinusoidal tone in the stress-exposed rat liver. Hepatology 36 (2002) 1453
44. Suematsu M., Goda N., Sano T., et al. Carbon monoxide: An endogenous modulator of sinusoidal tone in the perfused rat liver. J Clin Invest 96 (1995) 2431
45. Clemens M.G., Bauer M., Pannen B.H., et al. Remodeling of hepatic microvascular responsiveness after ischemia/reperfusion. Shock 8 (1997) 80
46. Federspiel W.J., and Popel A.S. A theoretical analysis of the effect of the particulate nature of blood on oxygen release in capillaries. Microvasc Res 32 (1986) 164
47. Horn E.P., Standl T., Wilhelm S., et al. Bovine hemoglobin increases skeletal muscle oxygenation during 95% artificial arterial stenosis. Surgery 121 (1997) 411
48. Hughes Jr. G.S., Antal E.J., Locker P.K., et al. Physiology and pharmacokinetics of a novel hemoglobin-based oxygen carrier in humans. Crit Care Med 24 (1996) 756
49. Clavien P.A., Harvey P.R., and Strasberg S.M. Preservation and reperfusion injuries in liver allografts. An overview and synthesis of current studies. Transplantation 53 (1992) 957
50. Ferguson D.M., Gores G.J., Ludwig J., et al. UW solution protects against reperfusion injury by inhibiting lipid peroxidation. Transplant Proc 23 (1991) 1552
51. Maines M.D. The heme oxygenase system: A regulator of second messenger gases. Annu Rev Pharmacol Toxicol 37 (1997) 517
52. Tenhunen R., Marver H.S., and Schmid R. The enzymatic conversion of heme to bilirubin by microsomal heme oxygenase. Proc Natl Acad Sci USA 61 (1968) 748
53. Bauer M. Heme oxygenase in liver transplantation: Heme catabolism and metabolites in the search of function. Hepatology 38 (2003) 286
54. Carraway M.S., Ghio A.J., Taylor J.L., et al. Induction of ferritin and heme oxygenase-1 by endotoxin in the lung. Am J Physiol 275 (1998) L583
55. Schmidt R., Tritschler E., Hoetzel A., et al. Heme oxygenase-1 induction by the clinically used anesthetic isoflurane protects rat livers from ischemia/reperfusion injury. Ann Surg 245 (2007) 931
56. Fondevila C., Shen X.D., Tsuchiyashi S., et al. Biliverdin therapy protects rat livers from ischemia and reperfusion injury. Hepatology 40 (2004) 1333
57. Gao W., Bentley R.C., Madden J.F., et al. Apoptosis of sinusoidal endothelial cells is a critical mechanism of preservation injury in rat liver transplantation. Hepatology 27 (1998) 1652
58. Natori S., Selzner M., Valentino K.L., et al. Apoptosis of sinusoidal endothelial cells occurs during liver preservation injury by a caspase-dependent mechanism. Transplantation 68 (1999) 89
59. Brouard S., Otterbein L.E., Anrather J., et al. Carbon monoxide generated by heme oxygenase 1 suppresses endothelial cell apoptosis. J Exp Med 192 (2000) 1015