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

Blood

Volumn 98, Issue 6, 2001, Pages 1802-1811

  Wagener, Frank A D T G ^a,b   Eggert, Andreas ^a,b   Boerman, Otto C ^a,b   Oyen, Wim J G ^a,b   Verhofstad, Albert ^a,b   Abraham, Nader G ^a,b   Adema, Gosse ^a,b   Van Kooyk, Yvette ^a,b   De Witte, Theo ^a,b   Figdor, Carl G ^a,b  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b NEW YORK MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL ADHESION MOLECULE; FIBRONECTIN; HEME; HEME OXYGENASE; HEME OXYGENASE 1; HEME OXYGENASE 2; INDIUM 111; INTERCELLULAR ADHESION MOLECULE 1; LIPOSOME; MACROGOL 2000; PADGEM PROTEIN; TECHNETIUM 99M; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL PERMEABILITY; CONTROLLED STUDY; DIFFUSION; GRANULOCYTE; IMMUNOHISTOCHEMISTRY; INFLAMMATION; INFLAMMATORY INFILTRATE; ISOTOPE LABELING; LEUKOCYTE; MALE; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

EID: 0035885926     PISSN: 00064971     EISSN: None     Source Type: Journal    
DOI: 10.1182/blood.V98.6.1802     Document Type: Article

References (72)

1. Robbins SL, Cotran RS, Kumar V, Collins T, Albert DM. Pathological basis of disease. 6th ed. Philadelphia, PA: WB Saunders; 1999.
2. Bevilacqua MP. Endothelial-leukocyte adhesion molecules. Annu Rev Immunol. 1993;11:767-804.
3. Sacks T, Moldow CF, Craddock PR, Bowers TK, Jacob HS. Oxygen radicals mediate endothelial cell damage by complement-stimulated granulocytes: an in vitro model of immune vascular damage. J Clin Invest. 1978;61:1161-1167.
4. Mullane KM, Westlin W, Kraemer R. Activated neutrophils release mediators that may contribute to myocardial injury and dysfunction associated with ischemia and reperfusion. Ann N Y Acad Sci. 1988;524:103-121.
5. Beri R, Chandra R. 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. 1993;25:49-152.
6. Balla J, Jacob HS, Balla G, Nath K, Eaton JW, Vercellotti GM. Enothelial-cell heme uptake from heme proteins: induction of sensitization and desensitization to oxidant damage. Proc Natl Acad Sci U S A. 1993;90:9285-9289.
7. Balla G, Jacob HS, Eaton JW, Belcher JD, Vercellotti GM. Hemin: a possible physiological mediator of low density lipoprotein oxidation and endothelial injury. Arterioscler Thromb. 1991;11:1700-1711.
8. Muller-Eberhard U, Javid J, Liem HH, Hanstein A, Hanna M. Plasma concentrations of hemopexin, haptoglobin and heme in patients with various hemolytic diseases. Blood. 1968;32:811-815.
9. Moore KP, Holt SG, Patel RP, et al. 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. 1998;273:31731-31737.
10. Gorbunov NV, Elsayed NM, Kisin ER, Kozlov AV, Kagan VE. Air blast-induced pulmonary oxidative stress: interplay among hemoglobin, antioxidants, and lipid peroxidation. Am J Physiol. 1997;272:L320-L334.
11. Letarte PB, Lieberman K, Nagatani K, Haworth RA, Odell GB, Duff TA. Hemin: levels in experimental subarachnoid hematoma and effects on dissociated vascular smooth-muscle cells. J Neurosurg. 1993;79:252-255.
12. Holt S, Moore K. Pathogenesis of renal failure in rhabdomyolysis: the role of myoglobin. Exp Nephrol. 2000;8:72-76.
13. Bunn HF, Jandl JH. Exchange of heme among hemoglobins and between hemoglobin and albumin. J Biol Chem. 1968;243:465-475.
14. Pohlman TH, Harlan JM. Adaptive responses of the endothelium to stress. J Surg Res. 2000;89:85-119.
15. Wagener FADTG, Feldman E, Witte de T, Abraham NG. Heme induces the expression of adhesion molecules ICAM-1, VCAM-1 and E selectin in vascular endothelial cells. Proc Soc Exp Biol Med. 1997;216:456-463.
16. Hancock WW, Buelow R, Sayegh MH, Turka LA. Antibody-induced transplant arteriosclerosis is prevented by graft expression of anti-oxidant and anti-apoptotic genes. Nat Med. 1998;4:1392-1396.
17. Tenhunen R, Marver HS, Schmid R. The enzymatic conversion of heme to bilirubin by microsomal heme oxygenase. Proc Natl Acad Sci U S A. 1968;61:748-755.
18. Abraham NG, Drummond GS, Lutton JD, Kappas A. The biological significance and physiological role of heme oxygenase. Cell Physiol Biochem. 1996;6:129-168.
19. Vogt BA, Alam J, Croatt AJ, Vercellotti GM, Nath KA. Acquired resistance to acute oxidative stress: possible role of heme oxygenase and ferritin. Lab Invest. 1995;72:474-483.
20. Maines MD. The heme oxygenase system and its functions in the brain. Cell Mol Biol (Noisy-legrand). 2000;46:573-585.
21. Maines MD. The heme oxygenase system: a regulator of second messenger gases. Annu Rev Pharmacol Toxicol. 1997;37:517-554.
22. McCoubrey WK Jr, Huang TJ, Maines MD. Isolation and characterization of a cDNA from the rat brain that encodes hemoprotein heme oxygenase-3. Eur J Biochem. 1997;247:2725-2732.
23. Willis D, Moore AR, Frederick R, Willoughby DA. Heme oxygenase: a novel target for the modulation of the inflammatory response. Nat Med. 1996;2:87-90.
24. Abraham NG, Lavrovsky Y, Schwartzman ML, et al. 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. 1995;92:6798-6802.
25. Yang L, Quan S, Abraham NG. Retrovirus-mediated HO gene transfer into endothelial cells protects against oxidant-induced injury. Am J Physiol. 1999;227:L127-L133.
26. Yachie A; Niida Y, Wada T, et al. Oxidative stress causes enhanced endothelial cell injury in human heme oxygenase-1 deficiency. J Clin Invest. 1999;103:129-135.
27. Poss KD, Tonegawa S. Reduced stress defense in heme oxygenase 1-deficient cells. Proc Natl Acad Sci U S A. 1997;94:10925-10930.
28. Wagener FADTG, Da Silva J-L, Farley T, de Witte T, Kappas A, Abraham NG. Differential effects of heme oxygenase isoforms on heme-mediated endothelial ICAM-1 expression. J Pharmacol Exp Ther. 1999;291:416-423.
29. Hayashi S, Takamiya R, Yamaguchi T, et al. Induction of heme oxygenase-1 suppresses venular leukocyte adhesion elicited by oxidative stress: role of bilirubin generated by the enzyme. Circ Res. 1999;85:663-671.
30. Vachharajani TJ, Work J, Issekutz AC, Granger DN. Heme oxygenase modulates selectin expression in different regional vascular beds. Am J Physiol. 2000;278:H1613-H1617.
31. Johnson RA, Kozma F, Colombari E. Carbon monoxide: from toxin to endogenous modulator of cardiovascular functions. Braz J Med Biol Res. 1999;32:1-14.
32. Brouard S, Otterbein LE, Anrather J, et al. Carbon monoxide generated by heme oxygenase 1 suppresses endothelial cell apoptosis. J Exp Med. 2000;192:1015-1026.
33. Stocker R, Yamamoto Y, McDonagh AF, Glazer AN, Ames BN. Bilirubin is an antioxidant of possible physiological importance. Science. 1987;235:1043-1046.
34. 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.
35. Marks GS, Brien JF, Nakakatsa K, McLaughlin BE. Does carbon monoxide have a physiological function? Eur J Pharmacol. 1991;232:R1-R2.
36. Kappas A, Drummond GS, Henschke C, Valaes T. Direct comparison of Sn-mesoporphyrin, an inhibitor of bilirubin production, and phototherapy in controlling hyperbilirubinemia in term and near-term newborn. Pediatrics. 1995;85:468-474.
37. Chernick RJ, Martasek P, Levere RD, Margreiter R, Abraham NG. Sensitivity of human tissue heme oxygenase to a new synthetic metalloporphyrin. Hepatology. 1989;10:365-369.
38. Paul KG, Theorell H, Akeson A. The molar light absorption of pyridine ferroprotoporphyrin (pyridine haemochromogen). Acta Chem Scand. 1953;7:1284-1287.
39. Laverman P, Dams ETM, Oyen WJG, et al. A novel method to label liposomes with Tc-99m via the nicotinyl hydrazino derivative. J Nucl Med. 1999;40:192-197.
40. Laverman P, Boerman OC, Oyen WJ, Dams ET, Storm G, Corstens FH. Liposomes for scintigraphic detection of infection and inflammation. Adv Drug Deliv Rev. 1999;37:225-235.
41. Laverman P, Brouwers AH, Dams ET, et al. Preclinical and clinical evidence for disappearance of long-circulating characteristics of polyethylene glycol liposomes at low lipid dose. J Pharmacol Exp Ther. 2000;293:996-1001.
42. Peters AM, Saverymuttu SH. The value of indium-labeled leucocytes in clinical practice. Blood Rev. 1987;1:65-76.
43. Lagasse E, Weissman IL. Flow cytometric identification of murine neutrophils and monocytes. J Immunol Methods. 1996;197:139-150.
44. Hafner J, Haenseler E, Ossent P, Burg G, Panizzon RG. Benzidine stain for the histochemical detection of hemoglobin in splinter hemorrhage (subungual hematoma) and black heel. Am J Dermatopathol. 1995;17:362-367.
45. Nishide H, Mihayashi K, Tsuchida E. Dissociation of aggregated ferroheme complexes and protoporphyrin IX by water-soluble polymers. Biochim Biophys Acta. 1977;498:208-214.
46. Bignold LP. Importance of platelets in increased vascular permeability evoked by experimental haemarthrosis in synovium of the rat. Pathology. 1980;12:169-179.
47. Xue M, Del Bigio MR. Intracerebral injection of autologous whole blood in rats: time course of inflammation and cell death. Neurosci Lett. 2000;283:230-232.
48. Baldwin AL. Modified hemoglobins produce venular interendothelial gaps and albumin leakage in the rat mesentery. Am J Physiol. 1999;277:H650-H659.
49. Johnston B, Gaboury JP, Suematsu M, Kubes P. Nitric oxide inhibits microvascular protein leakage induced by leukocyte adhesion-independent and adhesion-dependent inflammatory mediators. Microcirculation. 1999;6:153-162.
50. Rizzardini M, Zappone M, Villa P, et al. Kupffer cell depletion partially prevents hepatic heme oxygenase 1 messenger RNA accumulation in systemic inflammation in mice: role of interleukin-1 beta. Hepatology. 1998;27:703-710.
51. Kyokane T, Norimizu S, Taniai H, et al. Carbon monoxide from heme catabolism protects against hepatobiliary dysfunction in endotoxin-treated rat. Gastroenterology. 2001;120:1227-1240.
52. Henningsson R, Alm P, Lundquist I. Evaluation of islet heme oxygenase-CO and nitric oxide synthase-NO pathways during acute endotoxemia. Am J Physiol. 2001;280:C1242-C1254.
53. Gabay C, Kushner I. Acute-phase proteins and other systemic responses to inflammation. N Engl J Med. 1999;340:448-454.
54. Hunt RC, Handy I, Smith A. Heme-mediated reactive oxygen species toxicity to retinal pigment epithelial cells is reduced by hemopexin. J Cell Physiol. 1996;168:181-186.
55. Tolosano E, Hirsch E, Patrucco E, et al. Defective recovery and severe renal damage after acute hemolysis in hemopexin-deficient mice. Blood. 1999;94:3906-3914.
56. Miller YI, Smith A, Morgan WT, Shaklai N. Role of hemopexin in protection of low-density lipoprotein against hemoglobin-induced oxidation. Biochemistry. 1996;35:13112-13117.
57. Ho E, Chen G, Bray TM. Supplementation of N-acetylcysteine inhibits NF-κB activation and protects against alloxan-induced diabetes in CD-1 mice. FASEB J. 1999;13:1845-1854.
58. Spiecker M, Peng HB, Liao JK. Inhibition of endothelial vascular cell adhesion molecule-1 expression by nitric oxide involves the induction and nuclear translocation of IκBα. J Biol Chem. 1997;272:30969-30974.
59. Ishikawa K, Navab M, Leitinger N, Fogelman AM, Lusis AJ. Induction of heme oxygenase-1 inhibits the monocyte transmigration induced by mildly oxidized LDL. J Clin Invest. 1997;100:1209-1216.
60. Szabo A, Heemann U. Ischemia reperfusion injury and chronic allograft rejection. Transplant Proc. 1998;30:4281-4284.
61. Bock HA. Pathogenesis of acute renal failure: new aspects. Nephron. 1997;76:130-142.
62. Fruchterman TM, Spain DA, Wilson MA, Harris PD, Garrison RN. Selective microvascular endothelial cell dysfunction in the small intestine following resuscitated hemorrhagic shock. Shock. 1998;10:417-422.
63. Kakishita E. Pathophysiology and treatment of thrombotic thrombocytopenic purpura/hemolytic uremic syndrome (TTP/HUS). Int J Hematol. 2000;71:320-327.
64. Wada H, Mori Y, Shimura M, et al. Poor outcome in disseminated intravascular coagulation or thrombotic thrombocytopenic purpura patients with severe vascular endothelial cell injuries. Am J Hematol. 1998;58:189-194.
65. Wagener FADTG, Abraham NG, Van Kooyk Y, De Witte T, Figdor CG. Heme-induced cell adhesion in the pathogenesis of sickle cell disease and inflammation. Trends Pharmacol Sci. 2001;22:52-54.
66. Nath KA, Grande JP, Haggard JJ, et al. Oxidative stress and induction of heme oxygenase-1 in the kidney in sickle cell disease. Am J Pathol. 2001;158:893-903.
67. Choi SJ, Schumacher HR Jr, Clayburne G. Experimental haemarthrosis produces mild inflammation associated with intracellular Maltese crosses. Ann Rheum Dis. 1986;45:1025-1028.
68. Rodriguez-Merchan EC. The destructive capabilities of the synovium in the haemophilic joint. Haemophilia. 1998;4:506-510.
69. Simionatto CS, Cabal R, Jones RL, Galbraith RA. Thrombophlebitis and disturbed hemostasis following administration of intravenous hematin in normal volunteers. Am J Med. 1988;85:538-540.
70. Suzuki K, Totsuka M, Nakaji S, et al. Endurance exercise causes interaction among stress hormones, cytokines, neutrophil dynamics, and muscle damage. J Appl Physiol. 1999;87:1360-1367.
71. Elin RJ, Foidart M, Adornato BT, Engel WK, Gralnick HR. Quantification of acute phase reactants after muscle biopsy. J Lab Clin Med. 1982;100:566-573.
72. Fabian TC, Croce MA, Stewart RM, Dockter ME, Proctor KG. Neutrophil CD18 expression and blockade after traumatic shock and endotoxin challenge. Ann Surg. 1994;220:552-561.