Induction of heme oxygenase-1 suppresses venular leukocyte adhesion elicited by oxidative stress: Role of bilirubin generated by the enzyme

Circulation Research

Volumn 85, Issue 8, 1999, Pages 663-671

  Hayashi, Shinobu ^a   Takamiya, Rina ^a   Yamaguchi, Tokio ^a   Matsumoto, Kenji ^a   Tojo, Shinichiro J ^c   Tamatani, Takuya ^b   Kitajima, Masaki ^a   Makino, Nobuya ^a   Ishimura, Yuzuru ^a   Suematsu, Makoto ^a  

^a KEIO UNIVERSITY   (Japan)

^b Pharmaceutical Frontier Res Labs   (Japan)

^c DAINIPPON SUMITOMO PHARMA CO LTD   (Japan)

Author keywords

Bilirubin; Carbon monoxide; Endothelial cell; Heme oxygenase; Oxidative stress

Indexed keywords

BILIRUBIN; CARBON MONOXIDE; COPPER; HEME OXYGENASE; HEMIN; HYDROGEN PEROXIDE; N(G) NITROARGININE METHYL ESTER; PROTOPORPHYRIN ZINC;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL FUNCTION; CELL INTERACTION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME ACTIVITY; ENZYME INDUCTION; ISCHEMIA; LEUKOCYTE ADHERENCE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; REPERFUSION;

EID: 0033570168     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.RES.85.8.663     Document Type: Article

References (49)

1. Stocker R, Glazer AN, Ames BN. Antioxidant activity of albumin-bound bilirubin. Proc Natl Acad Sci U S A. 1987;84:5918-5922.
2. Shibahara S, Müller R, Taguchi H, Yoshida T. Cloning and expression of cDNA of rat heme oxygenase. Proc Natl Acad Sci U S A. 1985;82: 7865-7869.
3. Maines MD, Trakshel GM, Kutty RK. Characterization of two constitutive forms of rat liver microsomal heme oxygenase: only one molecular species of the enzyme is inducible. J Biol Chem. 1986;261: 411-419.
4. 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;247:725-732.
5. Maines MD. Heme oxygenase: function, multiplicity, regulatory mechanisms, and clinical applications. FASEB J. 1988;2:2557-2568.
6. Willis D, Moore AR, Frederick R, Willoughby DA. Heme oxygenase: a novel target for the modulation of the inflammatory response. Nat Med. 1996;2:87-89.
7. Choi AMK, Alam J. Heme oxygenase-1: function, regulation and implication of a novel stress-inducible protein in oxidant-induced lung injury. Am J Respir Cell Mol Biol. 1996;15:9-19.
8. Otterbein L, Chin BY, Otterbein SL, Lowe JB, Fessler H, Choi AMK. Mechanism of hemoglobin-induced protection against endotoxemia in rats: a ferritin-independent pathway. Am J Physiol. 1997;272: L268-L275.
9. Yet S-F, Pellacani A, Patterson C, Tan L, Folta SC, Foster L, Lee W-S, Hsieh C-M, Perrella MA. Induction of heme oxygenase-1 expression in vascular smooth muscle cells. J Biol Chem. 1997;272: 4296-4301.
10. Mulligan MS, Paulson JC, Frees SD, Zheng Z-L, Lowe JB, Ward PA. Protective effects of oligosaccharides in P-selectin-dependent lung injury. Nature. 1993;364:149-151.
11. Mulligan MS, Policy MJ, Bayer RJ, Nunn MF, Paulson JC, Ward PA. Neutrophil-dependent acute lung injury: requirement for P-selectin (GMP-140). J Clin Invest. 1992;90:1600-1607.
12. Winn RK, Liggitt D, Vedder NB, Paulson JC, Harlan JM. Anti-P-selectin monoclonal antibody attenuates reperfusion injury to the rabbit ear. J Clin Invest. 1993;92:2042-2047.
13. Mayadas TN, Johnson RC, Rayburn H, Hynes RO, Wagner DD. Leukocyte rolling and extravasation are severely compromised in P-selectin-deficient mice. Cell. 1993;74:541-554.
14. Zimmerman BJ, Paulson JC, Arrhenius TS, Gaeta FCA, Granger DN. Thrombin receptor peptide-mediated leukocyte rolling in rat mesemeric venules: roles of P-selectin and sialyl Lewis X. Am J Physiol. 1994;267:H1049-H1053.
15. 1 receptors and P-selectin in histamine-induced leukocyte rolling and adhesion in postcapillary venules. J Clin Invest. 1994;93:1508-1515.
16. Kubes P, Kanwar S. Histamine induces leukocyte rolling in postcapillary venules. J Immunol. 1994;152:3570-3577.
17. Patel KD, Zimmerman GA, Prescott SM, McEver RP, McIntyre TM. Oxygen radicals induce human endothelial cells to express GMP-140 and bind neutrophils. J Cell Biol. 1991;112:749-759.
18. Suematsu M, Suzuki H, Tamatani T, Iigou Y, DeLano F, Miyasaka M, Forrest M, Kannagi R, Zweifach B, Ishimura Y, Schmid-Schoenbein GW. Impairment of selectin-mediated leukocyte adhesion to venular endothelium in spontaneously hypertensive rats. J Clin Invest. 1995; 96:2009-2016.
19. Kubes P, Suzuki M, Granger DN. Nitric oxide: an endogenous modulator of leukocyte adhesion. Proc Natl Acad Sci U S A. 1991;88: 4651-4655.
20. Suematsu M, Tamatani T, DeLano FA, Miyasaka M, Forrest M, Suzuki H, Schmid-Schoenbein GW. Microvascular oxidative stress preceding leukocyte activation elicited by in vivo nitric oxide suppression. Am J Physiol. 1994;266:H2410-H2415.
21. Goda N, Suzuki K, Naito M, Takeoka S, Tsuchida E, Ishimura Y, Tamatani T, Suematsu M. Distribution of heme oxygenase isoforms in rat liver: topographic basis for carbon monoxide-mediated microvascular relaxation. J Clin Invest. 1998;101:604-612.
22. Yamaguchi T, Wakabayashi Y, Tanaka M, Sano T, Ishikawa H, Nakajima H, Suematsu M, Ishimura Y. Taurocholate induces directional transport of bilirubin into bile in the perfused rat liver. Am J Physiol. 1996;270:G1028-G1032.
23. Shinoda Y, Suematsu M, Wakabayashi Y, Suzuki T, Goda N, Saito S, Yamaguchi T, Ishimura Y. Carbon monoxide as a regulator of bile canalicular contractility in cultured rat hepatocytes. Hepatology. 1998;28:286-295.
24. Prabhakar NR, Dinerman JL, Agani FH, Snyder SH. Carbon monoxide: a role in carotid body chemoreception. Proc Natl Acad Sci U S A. 1995;92:1994-1997.
25. Suematsu M, Goda N, Sano T, Kashiwagi S, Shinoda Y, Ishimura Y. Carbon monoxide: an endogenous modulator of sinusoidal tone in the perfused rat liver. J Clin Invest. 1995;96:2431-2437.
26. Nishio K, Suzuki Y, Aoki T, Suzuki K, Miyata A, Sato N, Naoki K, Kudo H, Tsumura H, Serizawa H, Morooka S, Ishimura Y, Suematsu M, Yamaguchi K. Differential contribution of various adhesion molecules to leukocyte kinetics in pulmonary microvessels of hypoxia-exposed rat lungs. Am J Respir Crit Care Med. 1998;157: 599-609.
27. Suematsu M, Schmid-Schoenbein GW, Chavez-Chavez RH, Yee TT, DeLano FA, Tamatani T, Miyasaka M, Zweifach BW. In vivo visualization of oxidative changes in microvessels during neutrophil activation. Am J Physiol. 1993;264:H881-H891.
28. Barroso-Aranda J, Chavez-Chavez RH, Mathison JC, Suematsu M, Schmid-Schoenbein GW. Circulating neutrophil kinetics during tolerance in hemorrhagic shock using bacterial lipopolysaccharide. Am J Physiol. 1994;266:H415-H422.
29. Tamatani T, Suematsu M, Tezuka K, Hanzawa N, Tsuji T, Ishimura Y, Kannagi R, Toyoshima S, Homma M. Recognition of consensus carbohydrate structure in ligands for selectins by novel antibody against sialyl Lewis X. Am J Physiol. 1995;269:H1282-H1287.
30. Schwartz L, Austen FK, Kasserman S. Immunologic release of β-hexosaminidase and β-glucuronidase from purified rat serosal mast cells. J Immunol. 1979;123:1445-1450.
31. 2. J Immunol. 1993;151:5675-5684.
32. Suzuki H, Suematsu M, Shan Y, Kurose I, Fukumura D, Miura S, Tsuchiya M. Mast cell degranulation during microcirculatory disturbances revealed by toluidine blue vital staining method. In: Tsuchiya M, ed. International Conference on Mucosal Immunology. Tokyo, Japan: Elsevier; 1991:549-550.
33. Iigou Y, Suematsu M, Higashida T, Oheda J, Matsumoto K, Wakabayashi Y, Ishimura Y, Miyasaka M, Takashi T. In vivo constitutive expression of ICAM-1 in rat microvascular systems analyzed by laser confocal microscopy. Am J Physiol. 1997;273:H138-H147.
34. Morisaki H, Suematsu M, Wakabayashi Y, Moro-oka S, Fukushima K, Ishimura Y, Takeda J. Leukocyte-endothelium interaction in the rat mesenteric microcirculation during halothane or sevoflurane anesthesia. Anesthesiology. 1997;87:591-598.
35. Suzuki M, Asako H, Kubes P, Jennings S, Grisham MB, Granger DN. Neutrophil-derived oxidants promote leukocyte adherence in postcapillary venules. Microvasc Res. 1991;42:125-138.
36. Kubes P, Kanwar S, Niu X-F, Gaboury JP. Nitric oxide synthesis inhibition induces leukocyte adhesion via superoxide and mast cells. FASEB J. 1993;7:1293-1299.
37. Abraham NG, Lavrovsky Y, Schwartzman ML, Stolz RA, Levere RD, Gerritsen ME, Shibahara S, Kappas A. Transfection of 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.
38. Lee PJ, Alam J, Wiegand GW, Choi AMK. Overexpression of heme oxygenase-1 in human pulmonary epithelial cells results in cell growth arrest and increased resistance to hyperoxia. Proc Natl Acad Sci U S A. 1996;93:10393-10398.
39. Buttery LDK, Evans TJ, Springall DR, Carpenter A, Cohen J, Polak JM. Immunohistochemical localization of inducible nitric oxide synthase in endotoxin-treated rats. Lab Invest. 1994;71:755-764.
40. Poss KD, Tonegawa S. Heme oxygenase 1 is required for mammalian iron reutilization. Proc Natl Acad Sci U S A. 1997;94:10919-10924.
41. Balla G, Vercellotti GM, Muller-Eberhard U, Eaton J, Jacob HS. Exposure of endothelial cells to free heme potentiates damage mediated by granulocytes and toxic oxygen species. Lab Invest. 1991; 64:648-655.
42. Yamaguchi T, Horio F, Hashizume T, Tanaka M, Ikeda S, Kakinuma A, Nakajima H. Bilirubin is oxidized in rats treated with endotoxin and acts as a physiological antioxidant synergistically with ascorbic acid in vivo. Biochem Biophys Res Commun. 1995;214:11-19.
43. Capdevila J, Chacos N, Werringloer J, Prough R, Estabrook R. Liver microsomal cytochrome P-450 and oxidative metabolism of arachidonic acid. Proc Natl Acad Sci U S A. 1982:78:5362-5366.
44. 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.
45. Vachharajani TJ, Work J, Granger DN. Modulation of endothelial cell adhesion molecule expression by heme oxygenase. FASEB J. 1999; 13:A89. Abstract.
46. Broderson R, Bartels P. Enzymatic oxidation of bilirubin. Eur J Biochem. 1969;10:468-473.
47. Nath KA. Induction of heme oxygenase is a rapid, protective response in rhabdomyolysis in the rat. J Clin Invest. 1992;90:267-270.
48. Schoendorf TH, Rosenberg M, Beller FK. Endotoxin-induced disseminated intravascular coagulation in nonpregnant rats: a new experimental model. Am J Pathol. 1971;65:51-58.
49. Bauer M, Pannen BHJ, Bauer I, Herzog C, Wanner GA, Hanselmann R, Zhang JX, Clemens MG, Larsen R. Evidence for a functional link between stress response and vascular control in hepatic portal circulation. Am J Physiol. 1996;271:G929-G935.