Heme is a potent inducer of inflammation in mice and is counteracted by heme oxygenase

Robbins, 1999, Pathological basis of disease., 6th ed. Bevilacqua, 1993, Endothelial-leukocyte adhesion molecules., Annu Rev Immunol., 11, 767, 10.1146/annurev.iy.11.040193.004003 Sacks, 1978, Oxygen radicals mediate endothelial cell damage by complement-stimulated granulocytes: an in vitro model of immune vascular damage., J Clin Invest., 61, 1161, 10.1172/JCI109031 Mullane, 1988, Activated neutrophils release mediators that may contribute to myocardial injury and dysfunction associated with ischemia and reperfusion., Ann N Y Acad Sci., 524, 103, 10.1111/j.1749-6632.1988.tb38534.x Beri, 1993, Chemistry and biology of heme: effect of metal salts, organometals, and metalloporphyrins on heme synthesis and catabolism, with special reference to clinical implications and interactions with cytochrome P-450., Drug Metab Rev., 25, 49, 10.3109/03602539308993973 Balla, 1993, Enothelial-cell heme uptake from heme proteins: induction of sensitization and desensitization to oxidant damage., Proc Natl Acad Sci U S A., 90, 9285, 10.1073/pnas.90.20.9285 Balla, 1991, Hemin: a possible physiological mediator of low density lipoprotein oxidation and endothelial injury., Arterioscler Thromb., 11, 1700, 10.1161/01.ATV.11.6.1700 Muller-Eberhard, 1968, Plasma concentrations of hemopexin, haptoglobin and heme in patients with various hemolytic diseases., Blood., 32, 811, 10.1182/blood.V32.5.811.811 Moore, 1998, A causative role for redox cycling of myoglobin and its inhibition by alkalinization in the pathogenesis and treatment of rhabdomyolysis-induced renal failure., J Biol Chem., 273, 31731, 10.1074/jbc.273.48.31731 Gorbunov, 1997, Air blast-induced pulmonary oxidative stress: interplay among hemoglobin, antioxidants, and lipid peroxidation., Am J Physiol., 272, L320 Letarte, 1993, Hemin: levels in experimental subarachnoid hematoma and effects on dissociated vascular smooth-muscle cells., J Neurosurg., 79, 252, 10.3171/jns.1993.79.2.0252 Holt, 2000, Pathogenesis of renal failure in rhabdomyolysis: the role of myoglobin., Exp Nephrol., 8, 72, 10.1159/000020651 Bunn, 1968, Exchange of heme among hemoglobins and between hemoglobin and albumin., J Biol Chem., 243, 465, 10.1016/S0021-9258(18)93628-8 Pohlman, 2000, Adaptive responses of the endothelium to stress., J Surg Res., 89, 85, 10.1006/jsre.1999.5801 Wagener, 1997, Heme induces the expression of adhesion molecules ICAM-1, VCAM-1 and E selectin in vascular endothelial cells., Proc Soc Exp Biol Med., 216, 456, 10.3181/00379727-216-44197 Hancock, 1998, Antibody-induced transplant arteriosclerosis is prevented by graft expression of anti-oxidant and anti-apoptotic genes., Nat Med., 4, 1392, 10.1038/3982 Tenhunen, 1968, The enzymatic conversion of heme to bilirubin by microsomal heme oxygenase., Proc Natl Acad Sci U S A., 61, 748, 10.1073/pnas.61.2.748 Abraham, 1996, The biological significance and physiological role of heme oxygenase., Cell Physiol Biochem., 6, 129, 10.1159/000154819 Vogt, 1995, Acquired resistance to acute oxidative stress: possible role of heme oxygenase and ferritin., Lab Invest., 72, 474 Maines, 2000, The heme oxygenase system and its functions in the brain., Cell Mol Biol (Noisy-le-grand)., 46, 573 Maines, 1997, The heme oxygenase system: a regulator of second messenger gases., Annu Rev Pharmacol Toxicol., 37, 517, 10.1146/annurev.pharmtox.37.1.517 McCoubrey, 1997, Isolation and characterization of a cDNA from the rat brain that encodes hemoprotein heme oxygenase-3., Eur J Biochem., 247, 2725, 10.1111/j.1432-1033.1997.00725.x Willis, 1996, Heme oxygenase: a novel target for the modulation of the inflammatory response., Nat Med., 2, 87, 10.1038/nm0196-87 Abraham, 1995, Transfection of the human heme oxygenase gene into rabbit coronary microvessel endothelial cells: protective effect against heme and hemoglobin toxicity., Proc Natl Acad Sci U S A., 92, 6798, 10.1073/pnas.92.15.6798 Yang, 1999, Retrovirus-mediated HO gene transfer into endothelial cells protects against oxidant-induced injury., Am J Physiol., 227, L127 Yachie, 1999, Oxidative stress causes enhanced endothelial cell injury in human heme oxygenase-1 deficiency., J Clin Invest., 103, 129, 10.1172/JCI4165 Poss, 1997, Reduced stress defense in heme oxygenase 1-deficient cells., Proc Natl Acad Sci U S A., 94, 10925, 10.1073/pnas.94.20.10925 Wagener, 1999, Differential effects of heme oxygenase isoforms on heme-mediated endothelial ICAM-1 expression., J Pharmacol Exp Ther., 291, 416 Hayashi, 1999, Induction of heme oxygenase-1 suppresses venular leukocyte adhesion elicited by oxidative stress: role of bilirubin generated by the enzyme., Circ Res., 85, 663, 10.1161/01.RES.85.8.663 Vachharajani, 2000, Heme oxygenase modulates selectin expression in different regional vascular beds., Am J Physiol., 278, H1613 Johnson, 1999, Carbon monoxide: from toxin to endogenous modulator of cardiovascular functions., Braz J Med Biol Res., 32, 1, 10.1590/S0100-879X1999000100001 Brouard, 2000, Carbon monoxide generated by heme oxygenase 1 suppresses endothelial cell apoptosis., J Exp Med., 192, 1015, 10.1084/jem.192.7.1015 Stocker, 1987, Bilirubin is an antioxidant of possible physiological importance., Science., 235, 1043, 10.1126/science.3029864 Otterbein, 2000, Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway., Nat Med., 6, 422, 10.1038/74680 Marks, 1991, Does carbon monoxide have a physiological function?, Eur J Pharmacol., 232, R1 Kappas, 1995, Direct comparison of Sn-mesoporphyrin, an inhibitor of bilirubin production, and phototherapy in controlling hyperbilirubinemia in term and near-term newborn., Pediatrics., 85, 468, 10.1542/peds.95.4.468 Chernick, 1989, Sensitivity of human tissue heme oxygenase to a new synthetic metalloporphyrin., Hepatology., 10, 365, 10.1002/hep.1840100320 Paul, 1953, The molar light absorption of pyridine ferroprotoporphyrin (pyridine haemochromogen)., Acta Chem Scand., 7, 1284, 10.3891/acta.chem.scand.07-1284 Laverman, 1999, A novel method to label liposomes with Tc-99m via the nicotinyl hydrazino derivative., J Nucl Med., 40, 192 Laverman, 1999, Liposomes for scintigraphic detection of infection and inflammation., Adv Drug Deliv Rev., 37, 225, 10.1016/S0169-409X(98)00095-7 Laverman, 2000, Preclinical and clinical evidence for disappearance of long-circulating characteristics of polyethylene glycol liposomes at low lipid dose., J Pharmacol Exp Ther., 293, 996 Peters, 1987, The value of indium-labeled leucocytes in clinical practice., Blood Rev., 1, 65, 10.1016/0268-960X(87)90021-X Lagasse, 1996, Flow cytometric identification of murine neutrophils and monocytes., J Immunol Methods., 197, 139, 10.1016/0022-1759(96)00138-X Hafner, 1995, Benzidine stain for the histochemical detection of hemoglobin in splinter hemorrhage (subungual hematoma) and black heel., Am J Dermatopathol., 17, 362, 10.1097/00000372-199508000-00010 Nishide, 1977, Dissociation of aggregated ferroheme complexes and protoporphyrin IX by water-soluble polymers., Biochim Biophys Acta., 498, 208, 10.1016/0304-4165(77)90100-3 Bignold, 1980, Importance of platelets in increased vascular permeability evoked by experimental haemarthrosis in synovium of the rat., Pathology., 12, 169, 10.3109/00313028009060070 Xue, 2000, Intracerebral injection of autologous whole blood in rats: time course of inflammation and cell death., Neurosci Lett., 283, 230, 10.1016/S0304-3940(00)00971-X Baldwin, 1999, Modified hemoglobins produce venular interendothelial gaps and albumin leakage in the rat mesentery., Am J Physiol., 277, H650 Johnston, 1999, Nitric oxide inhibits microvascular protein leakage induced by leukocyte adhesion-independent and adhesion-dependent inflammatory mediators., Microcirculation., 6, 153, 10.1080/713773949 Rizzardini, 1998, Kupffer cell depletion partially prevents hepatic heme oxygenase 1 messenger RNA accumulation in systemic inflammation in mice: role of interleukin1beta., Hepatology., 27, 703, 10.1002/hep.510270311 Kyokane, 2001, Carbon monoxide from heme catabolism protects against hepatobiliary dysfunction in endotoxin-treated rat., Gastroenterology., 120, 1227, 10.1053/gast.2001.23249 Henningsson, 2001, Evaluation of islet heme oxygenase–CO and nitric oxide synthase–NO pathways during acute endotoxemia., Am J Physiol., 280, C1242, 10.1152/ajpcell.2001.280.5.C1242 Gabay, 1999, Acute-phase proteins and other systemic responses to inflammation., N Engl J Med., 340, 448, 10.1056/NEJM199902113400607 Hunt, 1996, Heme-mediated reactive oxygen species toxicity to retinal pigment epithelial cells is reduced by hemopexin., J Cell Physiol., 168, 181, 10.1002/(SICI)1097-4652(199607)168:1<81::AID-JCP10>3.0.CO;2-S Tolosano, 1999, Defective recovery and severe renal damage after acute hemolysis in hemopexin-deficient mice., Blood., 94, 3906, 10.1182/blood.V94.11.3906 Miller, 1996, Role of hemopexin in protection of low-density lipoprotein against hemoglobin-induced oxidation., Biochemistry., 35, 13112, 10.1021/bi960737u Ho, 1999, Supplementation of N-acetylcysteine inhibits NF-κB activation and protects against alloxan-induced diabetes in CD-1 mice., FASEB J., 13, 1845, 10.1096/fasebj.13.13.1845 Spiecker, 1997, Inhibition of endothelial vascular cell adhesion molecule-1 expression by nitric oxide involves the induction and nuclear translocation of IκBα., J Biol Chem., 272, 30969, 10.1074/jbc.272.49.30969 Ishikawa, 1997, Induction of heme oxygenase-1 inhibits the monocyte transmigration induced by mildly oxidized LDL., J Clin Invest., 100, 1209, 10.1172/JCI119634 Szabo, 1998, Ischemia reperfusion injury and chronic allograft rejection., Transplant Proc., 30, 4281, 10.1016/S0041-1345(98)01414-6 Bock, 1997, Pathogenesis of acute renal failure: new aspects., Nephron., 76, 130, 10.1159/000190160 Fruchterman, 1998, Selective microvascular endothelial cell dysfunction in the small intestine following resuscitated hemorrhagic shock., Shock., 10, 417, 10.1097/00024382-199812000-00007 Kakishita, 2000, Pathophysiology and treatment of thrombotic thrombocytopenic purpura/hemolytic uremic syndrome (TTP/HUS)., Int J Hematol., 71, 320 Wada, 1998, Poor outcome in disseminated intravascular coagulation or thrombotic thrombocytopenic purpura patients with severe vascular endothelial cell injuries., Am J Hematol., 58, 189, 10.1002/(SICI)1096-8652(199807)58:3<189::AID-AJH5>3.0.CO;2-N Wagener, 2001, Heme-induced cell adhesion in the pathogenesis of sickle cell disease and inflammation., Trends Pharmacol Sci., 22, 52, 10.1016/S0165-6147(00)01609-6 Nath, 2001, Oxidative stress and induction of heme oxygenase-1 in the kidney in sickle cell disease., Am J Pathol., 158, 893, 10.1016/S0002-9440(10)64037-0 Choi, 1986, Experimental haemarthrosis produces mild inflammation associated with intracellular Maltese crosses., Ann Rheum Dis., 45, 1025, 10.1136/ard.45.12.1025 Rodriguez-Merchan, 1998, The destructive capabilities of the synovium in the haemophilic joint., Haemophilia., 4, 506, 10.1046/j.1365-2516.1998.440506.x Simionatto, 1988, Thrombophlebitis and disturbed hemostasis following administration of intravenous hematin in normal volunteers., Am J Med., 85, 538, 10.1016/S0002-9343(88)80092-5 Suzuki, 1999, Endurance exercise causes interaction among stress hormones, cytokines, neutrophil dynamics, and muscle damage., J Appl Physiol., 87, 1360, 10.1152/jappl.1999.87.4.1360 Elin, 1982, Quantification of acute phase reactants after muscle biopsy., J Lab Clin Med., 100, 566 Fabian, 1994, Neutrophil CD18 expression and blockade after traumatic shock and endotoxin challenge., Ann Surg., 220, 552, 10.1097/00000658-199410000-00013