Carbon Monoxide Generated by Heme Oxygenase 1 Suppresses Endothelial Cell Apoptosis

doi:10.1084/jem.192.7.1015

Published online 2 October 2000.

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© The Rockefeller University Press, 0022-1007/2000/10/1015/ $5.00
The Journal of Experimental Medicine, Volume 192, Number 7, October 2, 2000 1015-1026

Original Article

Carbon Monoxide Generated by Heme Oxygenase 1 Suppresses Endothelial Cell Apoptosis

Sophie Brouard^a, Leo E. Otterbein^b, Josef Anrather^c, Edda Tobiasch^a, Fritz H. Bach^a, Augustine M.K. Choi^b, and Miguel P. Soares^a
^a Immunobiology Research Center, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, Massachusetts 02215
^b Department of Internal Medicine, Pulmonary and Critical Care Section, Yale University, School of Medicine, New Haven, Connecticut 06520
^c Department of Neurobiology, Weill Medical College of Cornell University, New York, New York 10021

Correspondence to: Miguel P. Soares, Immunobiology Research Center, Beth Israel Deaconess Medical Center, Harvard Medical School, 99 Brookline Ave., Boston, MA 02215. Tel:617-632-0885 Fax:617-632-0880

Heme oxygenase 1 (HO-1) inhibits apoptosis by regulating cellularprooxidant iron. We now show that there is an additional mechanismby which HO-1 inhibits apoptosis, namely by generating the gaseousmolecule carbon monoxide (CO). Overexpression of HO-1, or inductionof HO-1 expression by heme, protects endothelial cells (ECs)from apoptosis. When HO-1 enzymatic activity is blocked by tinprotoporphyrin (SnPPIX) or the action of CO is inhibited byhemoglobin (Hb), HO-1 no longer prevents EC apoptosis whilethese reagents do not affect the antiapoptotic action of bcl-2.Exposure of ECs to exogenous CO, under inhibition of HO-1 activityby SnPPIX, substitutes HO-1 in preventing EC apoptosis. Themechanism of action of HO-1/CO is dependent on the activationof the p38 mitogen-activated protein kinase (MAPK) signalingtransduction pathway. Expression of HO-1 or exposure of ECsto exogenous CO enhanced p38 MAPK activation by TNF- ${alpha}$ . Specificinhibition of p38 MAPK activation by the pyridinyl imidazolSB203580 or through overexpression of a p38 MAPK dominant negativemutant abrogated the antiapoptotic effect of HO-1. Taken together,these data demonstrate that the antiapoptotic effect of HO-1in ECs is mediated by CO and more specifically via the activationof p38 MAPK by CO.

Key Words: apoptosis, endothelial cells, heme oxygenase 1, carbon monoxide,p38 mitogen-activated protein kinase

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