© 1999 American Heart Association, Inc.
Molecular Medicine |
Induction of Heme Oxygenase-1 Suppresses Venular Leukocyte Adhesion Elicited by Oxidative Stress
Role of Bilirubin Generated by the Enzyme
From the Departments of Biochemistry (R.T., T.Y., N.M., Y.I., M.S.) and Department of Surgery (S.H., K.M., M.K.), School of Medicine, Keio University, Tokyo; Pharmaceutical Frontier Research Laboratories (T.T.), JT Inc, Kanagawa; and Research Center (S.J.T.), Sumitomo Pharmaceutical Co Ltd, Osaka, Japan.
Correspondence to Makoto Suematsu, MD, PhD, Associate Professor, Department of Biochemistry, School of Medicine, Keio University, 35 Shinanomachi, Shinjuku-ku, Tokyo 160, Japan. E-mail msuem{at}mc.med.keio.ac.jp
Abstract—This study aimed to
examine whether an elevated activity of heme oxygenase
(HO)-1 in the tissue attenuates endothelial
cell–leukocyte interactions microvessels in vivo. When rats were
pretreated with an intraperitoneal injection of
hemin, an HO-1 inducer, mesenteric tissues, including their
microvessels, displayed a marked induction of HO-1 concurrent with an
increase in plasma concentrations of bilirubin-IX
, the product
of HO-catalyzed degradation of protoheme IX. In these rats, oxidative
stress such as superfusion with H2O2 and
ischemia-reperfusion of the tissues neither induced rolling nor
exhibited adherent responses of leukocytes in venules. In contrast, the
oxidative stresses evoked marked rolling and adhesion of leukocytes in
the control rats without HO-1 induction. The HO-1 induction also
downregulated leukocyte adhesion elicited by other pro-oxidant stimuli
such as N
-nitro-L-arginine
methyl ester. The decreases in the oxidant-elicited leukocyte adhesive
responses under HO-1–inducing conditions were restored by perfusion
with zinc protoporphyrin-IX, an HO inhibitor, but not with
copper protoporphyrin-IX, which did not inhibit the enzyme.
Furthermore, the effects of zinc protoporphyrin-IX were repressed by
superfusion with bilirubin or biliverdin at the micromolar level, but
not by the same concentration of carbon monoxide, another product
of HO. These results indicate that induction of the HO-1 activity
serves as a potential stratagem to prevent oxidant-induced
microvascular leukocyte adhesion through the action of bilirubin, a
product of HO reaction.
Key Words: heme oxygenase • bilirubin • carbon monoxide • oxidative stress • endothelial cell
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T. Katayama, Y. Ikeda, M. Handa, T. Tamatani, S. Sakamoto, M. Ito, Y. Ishimura, and M. Suematsu Immunoneutralization of Glycoprotein Ib{alpha} Attenuates Endotoxin-Induced Interactions of Platelets and Leukocytes With Rat Venular Endothelium In Vivo Circ. Res., May 26, 2000; 86(10): 1031 - 1037. [Abstract] [Full Text] [PDF]
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T. J. Vachharajani, J. Work, A. C. Issekutz, and D. N. Granger Heme oxygenase modulates selectin expression in different regional vascular beds Am J Physiol Heart Circ Physiol, May 1, 2000; 278(5): H1613 - H1617. [Abstract] [Full Text] [PDF]
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C. Wunder, R. W Brock, S. D McCarter, A. Bihari, K. Harris, O. Eichelbronner, and R. F Potter Inhibition of haem oxygenase activity increases leukocyte accumulation in the liver following limb ischaemia-reperfusion in mice J. Physiol., May 1, 2002; 540(3): 1013 - 1021. [Abstract] [Full Text] [PDF]
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T. Imai, T. Morita, T. Shindo, R. Nagai, Y. Yazaki, H. Kurihara, M. Suematsu, and S. Katayama Vascular Smooth Muscle Cell-Directed Overexpression of Heme Oxygenase-1 Elevates Blood Pressure Through Attenuation of Nitric Oxide-Induced Vasodilation in Mice Circ. Res., July 6, 2001; 89(1): 55 - 62. [Abstract] [Full Text] [PDF]
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M. Sano, K. Fukuda, T. Sato, H. Kawaguchi, M. Suematsu, S. Matsuda, S. Koyasu, H. Matsui, K. Yamauchi-Takihara, M. Harada, et al. ERK and p38 MAPK, but not NF-{kappa}B, Are Critically Involved in Reactive Oxygen Species-Mediated Induction of IL-6 by Angiotensin II in Cardiac Fibroblasts Circ. Res., October 12, 2001; 89(8): 661 - 669. [Abstract] [Full Text] [PDF]
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