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*
Immunobiology Research Center, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA 02215;
Department of Medicine, University Medical School of Debrcen, Hungary;
Yale University, School of Medicine, Department of Internal Medicine, Pulmonary and Critical Care Section, New Haven, CT 06520;
Department of Pathology, Massachusetts General Hospital, Boston, MA 02114; and
¶ Division of Hematology, University of Minnesota, Minneapolis, MN 55455
Mouse-to-rat cardiac transplants survive long term after transient complement depletion by cobra venom factor and T cell immunosuppression by cyclosporin A. Expression of heme oxygenase-1 (HO-1) by the graft vasculature is critical to achieve graft survival. In the present study, we asked whether this protective effect was attributable to the generation of one of the catabolic products of HO-1, carbon monoxide (CO). Our present data suggests that this is the case. Under the same immunosuppressive regimen that allows mouse-to-rat cardiac transplants to survive long term (i.e., cobra venom factor plus cyclosporin A), inhibition of HO-1 activity by tin protoporphyrin, caused graft rejection in 3–7 days. Rejection was associated with widespread platelet sequestration, thrombosis of coronary arterioles, myocardial infarction, and apoptosis of endothelial cells as well as cardiac myocytes. Under inhibition of HO-1 activity by tin protoporphyrin, exogenous CO suppressed graft rejection and restored long-term graft survival. This effect of CO was associated with inhibition of platelet aggregation, thrombosis, myocardial infarction, and apoptosis. We also found that expression of HO-1 by endothelial cells in vitro inhibits platelet aggregation and protects endothelial cells from apoptosis. Both these actions of HO-1 are mediated through the generation of CO. These data suggests that HO-1 suppresses the rejection of mouse-to-rat cardiac transplants through a mechanism that involves the generation of CO. Presumably CO suppresses graft rejection by inhibiting platelet aggregation that facilitates vascular thrombosis and myocardial infarction. Additional mechanisms by which CO overcomes graft rejection may involve its ability to suppress endothelial cell apoptosis.
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 A Nakao, B A Moore, N Murase, F Liu, B S Zuckerbraun, F H Bach, A M K Choi, M A Nalesnik, L E Otterbein, and A J Bauer Immunomodulatory effects of inhaled carbon monoxide on rat syngeneic small bowel graft motility Gut, September 1, 2003; 52(9): 1278 - 1285. [Abstract] [Full Text]
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 H. Hirai, H. Kubo, M. Yamaya, K. Nakayama, M. Numasaki, S. Kobayashi, S. Suzuki, S. Shibahara, and H. Sasaki Microsatellite polymorphism in heme oxygenase-1 gene promoter is associated with susceptibility to oxidant-induced apoptosis in lymphoblastoid cell lines Blood, September 1, 2003; 102(5): 1619 - 1621. [Abstract] [Full Text] [PDF]
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J. A. Araujo, L. Meng, A. D. Tward, W. W. Hancock, Y. Zhai, A. Lee, K. Ishikawa, S. Iyer, R. Buelow, R. W. Busuttil, et al. Systemic Rather Than Local Heme Oxygenase-1 Overexpression Improves Cardiac Allograft Outcomes in a New Transgenic Mouse J. Immunol., August 1, 2003; 171(3): 1572 - 1580. [Abstract] [Full Text] [PDF]
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J. E. Clark, P. Naughton, S. Shurey, C. J. Green, T. R. Johnson, B. E. Mann, R. Foresti, and R. Motterlini Cardioprotective Actions by a Water-Soluble Carbon Monoxide-Releasing Molecule Circ. Res., July 25, 2003; 93 (2): e2 - e8. [Abstract] [Full Text] [PDF]
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 R. D. Mayer, X. Wang, and M. D. Maines Nitric Oxide Inhibitor N{omega}-Nitro-L-arginine Methyl Ester Potentiates Induction of Heme Oxygenase-1 in Kidney Ischemia/Reperfusion Model: A Novel Mechanism for Regulation of the Oxygenase J. Pharmacol. Exp. Ther., July 1, 2003; 306(1): 43 - 50. [Abstract] [Full Text] [PDF]
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R. Song, M. Kubo, D. Morse, Z. Zhou, X. Zhang, J. H. Dauber, J. Fabisiak, S. M. Alber, S. C. Watkins, B. S. Zuckerbraun, et al. Carbon Monoxide Induces Cytoprotection in Rat Orthotopic Lung Transplantation via Anti-Inflammatory and Anti-Apoptotic Effects Am. J. Pathol., July 1, 2003; 163(1): 231 - 242. [Abstract] [Full Text] [PDF]
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X. Zhang, P. Shan, J. Alam, R. J. Davis, R. A. Flavell, and P. J. Lee Carbon Monoxide Modulates Fas/Fas Ligand, Caspases, and Bcl-2 Family Proteins via the p38{alpha} Mitogen-activated Protein Kinase Pathway during Ischemia-Reperfusion Lung Injury J. Biol. Chem., June 6, 2003; 278(24): 22061 - 22070. [Abstract] [Full Text] [PDF]
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 Y.-H. Chen, S.-F. Yet, and M. A. Perrella Role of Heme Oxygenase-1 in the Regulation of Blood Pressure and Cardiac Function Experimental Biology and Medicine, May 1, 2003; 228(5): 447 - 453. [Abstract] [Full Text] [PDF]
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T. D. Blydt-Hansen, M. Katori, C. Lassman, B. Ke, A. J. Coito, S. Iyer, R. Buelow, R. Ettenger, R. W. Busuttil, and J. W. Kupiec-Weglinski Gene Transfer-Induced Local Heme Oxygenase-1 Overexpression Protects Rat Kidney Transplants From Ischemia/Reperfusion Injury J. Am. Soc. Nephrol., March 1, 2003; 14(3): 745 - 754. [Abstract] [Full Text] [PDF]
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X. Zhang, P. Shan, L. E. Otterbein, J. Alam, R. A. Flavell, R. J. Davis, A. M. K. Choi, and P. J. Lee Carbon Monoxide Inhibition of Apoptosis during Ischemia-Reperfusion Lung Injury Is Dependent on the p38 Mitogen-activated Protein Kinase Pathway and Involves Caspase 3 J. Biol. Chem., January 3, 2003; 278(2): 1248 - 1258. [Abstract] [Full Text] [PDF]
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J. K. Sarady, S. L. Otterbein, F. Liu, L. E. Otterbein, and A. M. K. Choi Carbon Monoxide Modulates Endotoxin-Induced Production of Granulocyte Macrophage Colony-Stimulating Factor in Macrophages Am. J. Respir. Cell Mol. Biol., December 1, 2002; 27(6): 739 - 745. [Abstract] [Full Text] [PDF]
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R. Song, R. S. Mahidhara, F. Liu, W. Ning, L. E. Otterbein, and A. M. K. Choi Carbon Monoxide Inhibits Human Airway Smooth Muscle Cell Proliferation via Mitogen-Activated Protein Kinase Pathway Am. J. Respir. Cell Mol. Biol., November 1, 2002; 27(5): 603 - 610. [Abstract] [Full Text] [PDF]
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W. Ning, R. Song, C. Li, E. Park, A. Mohsenin, A. M. K. Choi, and M. E. Choi TGF-beta 1 stimulates HO-1 via the p38 mitogen-activated protein kinase in A549 pulmonary epithelial cells Am J Physiol Lung Cell Mol Physiol, November 1, 2002; 283(5): L1094 - L1102. [Abstract] [Full Text] [PDF]
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S. R. Vulapalli, Z. Chen, B. H. L. Chua, T. Wang, and C.-S. Liang Cardioselective overexpression of HO-1 prevents I/R-induced cardiac dysfunction and apoptosis Am J Physiol Heart Circ Physiol, August 1, 2002; 283(2): H688 - H694. [Abstract] [Full Text] [PDF]
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D. Morse and A. M. K. Choi Heme Oxygenase-1 . The "Emerging Molecule" Has Arrived Am. J. Respir. Cell Mol. Biol., July 1, 2002; 27(1): 8 - 16. [Abstract] [Full Text] [PDF]
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S. Brouard, P. O. Berberat, E. Tobiasch, M. P. Seldon, F. H. Bach, and M. P. Soares Heme Oxygenase-1-derived Carbon Monoxide Requires the Activation of Transcription Factor NF-kappa B to Protect Endothelial Cells from Tumor Necrosis Factor-alpha -mediated Apoptosis J. Biol. Chem., May 10, 2002; 277(20): 17950 - 17961. [Abstract] [Full Text] [PDF]
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L. Gunther, P. O. Berberat, M. Haga, S. Brouard, R. N. Smith, M. P. Soares, F. H. Bach, and E. Tobiasch Carbon Monoxide Protects Pancreatic {beta}-Cells From Apoptosis and Improves Islet Function/Survival After Transplantation Diabetes, April 1, 2002; 51(4): 994 - 999. [Abstract] [Full Text] [PDF]
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R. Motterlini, J. E. Clark, R. Foresti, P. Sarathchandra, B. E. Mann, and C. J. Green Carbon Monoxide-Releasing Molecules: Characterization of Biochemical and Vascular Activities Circ. Res., February 8, 2002; 90 (2): e17 - e24. [Abstract] [Full Text] [PDF]
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A. M.K. Choi Heme Oxygenase-1 Protects the Heart Circ. Res., July 20, 2001; 89(2): 105 - 107. [Full Text] [PDF]
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R. Motterlini, J. E. Clark, R. Foresti, P. Sarathchandra, B. E. Mann, and C. J. Green Carbon Monoxide-Releasing Molecules: Characterization of Biochemical and Vascular Activities Circ. Res., February 8, 2002; 90 (2): e17 - e24. [Abstract] [Full Text] [PDF]
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