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Department of Medicine, Division of Pulmonary, Allergy, and Critical Care Medicine, The University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania; and Department of Molecular Genetics, Alton Ochsner Medical Foundation, Louisiana State University Medical Center, New Orleans, Louisiana
The heme oxygenases, which consist of constitutive and inducible isozymes (HO-1, HO-2), catalyze the rate-limiting step in the metabolic conversion of heme to the bile pigments (i.e., biliverdin and bilirubin) and thus constitute a major intracellular source of iron and carbon monoxide (CO). In recent years, endogenously produced CO has been shown to possess intriguing signaling properties affecting numerous critical cellular functions including but not limited to inflammation, cellular proliferation, and apoptotic cell death. The era of gaseous molecules in biomedical research and human diseases initiated with the discovery that the endothelial cell-derived relaxing factor was identical to the gaseous molecule nitric oxide (NO). The discovery that endogenously produced gaseous molecules such as NO and now CO can impart potent physiological and biological effector functions truly represented a paradigm shift and unraveled new avenues of intense investigations. This review covers the molecular and biochemical characterization of HOs, with a discussion on the mechanisms of signal transduction and gene regulation that mediate the induction of HO-1 by environmental stress. Furthermore, the current understanding of the functional significance of HO shall be discussed from the perspective of each of the metabolic by-products, with a special emphasis on CO. Finally, this presentation aspires to lay a foundation for potential future clinical applications of these systems.
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 K. El Fadili, M. Imbeault, N. Messier, G. Roy, B. Gourbal, M. Bergeron, M. J. Tremblay, D. Legare, and M. Ouellette Modulation of Gene Expression in Human Macrophages Treated with the Anti-Leishmania Pentavalent Antimonial Drug Sodium Stibogluconate Antimicrob. Agents Chemother., February 1, 2008; 52(2): 526 - 533. [Abstract] [Full Text] [PDF]
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A. L. Lagan, D. D. Melley, T. W. Evans, and G. J. Quinlan Pathogenesis of the systemic inflammatory syndrome and acute lung injury: role of iron mobilization and decompartmentalization Am J Physiol Lung Cell Mol Physiol, February 1, 2008; 294(2): L161 - L174. [Abstract] [Full Text] [PDF]
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L. S. Nobre, J. D. Seixas, C. C. Romao, and L. M. Saraiva Antimicrobial Action of Carbon Monoxide-Releasing Compounds Antimicrob. Agents Chemother., December 1, 2007; 51(12): 4303 - 4307. [Abstract] [Full Text] [PDF]
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 A. Kobayashi, K. Ishikawa, H. Matsumoto, S. Kimura, Y. Kamiyama, and Y. Maruyama Synergetic Antioxidant and Vasodilatory Action of Carbon Monoxide in Angiotensin II Induced Cardiac Hypertrophy Hypertension, December 1, 2007; 50(6): 1040 - 1048. [Abstract] [Full Text] [PDF]
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 A. Meiller, S. Alvarez, P. Drane, C. Lallemand, B. Blanchard, M. Tovey, and E. May p53-dependent stimulation of redox-related genes in the lymphoid organs of {gamma}-irradiated mice identification of Haeme-oxygenase 1 as a direct p53 target gene Nucleic Acids Res., November 29, 2007; 35(20): 6924 - 6934. [Abstract] [Full Text] [PDF]
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A. L. True, M. Olive, M. Boehm, H. San, R. J. Westrick, N. Raghavachari, X. Xu, E. G. Lynn, M. N. Sack, P. J. Munson, et al. Heme Oxygenase-1 Deficiency Accelerates Formation of Arterial Thrombosis Through Oxidative Damage to the Endothelium, Which Is Rescued by Inhaled Carbon Monoxide Circ. Res., October 26, 2007; 101(9): 893 - 901. [Abstract] [Full Text] [PDF]
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R. Schmidt Cobalt protoporphyrin as a potential therapeutic agent? FASEB J, September 1, 2007; 21(11): 2639 - 2639. [Full Text] [PDF]
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 S. Pugazhenthi, L. Akhov, G. Selvaraj, M. Wang, and J. Alam Regulation of heme oxygenase-1 expression by demethoxy curcuminoids through Nrf2 by a PI3-kinase/Akt-mediated pathway in mouse beta-cells Am J Physiol Endocrinol Metab, September 1, 2007; 293(3): E645 - E655. [Abstract] [Full Text] [PDF]
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R. C.M. Siow and A. T. Churchman Adventitial growth factor signalling and vascular remodelling: Potential of perivascular gene transfer from the outside-in Cardiovasc Res, September 1, 2007; 75(4): 659 - 668. [Abstract] [Full Text] [PDF]
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 T. Yoshida and R. M. Tuder Pathobiology of Cigarette Smoke-Induced Chronic Obstructive Pulmonary Disease Physiol Rev, July 1, 2007; 87(3): 1047 - 1082. [Abstract] [Full Text] [PDF]
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B. Biteman, I. R. Hassan, E. Walker, A. J. Leedom, M. Dunn, F. Seta, M. Laniado-Schwartzman, and K. Gronert Interdependence of lipoxin A4 and heme-oxygenase in counter-regulating inflammation during corneal wound healing FASEB J, July 1, 2007; 21(9): 2257 - 2266. [Abstract] [Full Text] [PDF]
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X. Liu, J. A. Simpson, K. R. Brunt, C. A. Ward, S. R. R. Hall, R. T. Kinobe, V. Barrette, M. Y. Tse, S. C. Pang, A. S. Pachori, et al. Preemptive heme oxygenase-1 gene delivery reveals reduced mortality and preservation of left ventricular function 1 yr after acute myocardial infarction Am J Physiol Heart Circ Physiol, July 1, 2007; 293(1): H48 - H59. [Abstract] [Full Text] [PDF]
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P. E. Milbury, B. Graf, J. M. Curran-Celentano, and J. B. Blumberg Bilberry (Vaccinium myrtillus) Anthocyanins Modulate Heme Oxygenase-1 and Glutathione S-Transferase-pi Expression in ARPE-19 Cells Invest. Ophthalmol. Vis. Sci., May 1, 2007; 48(5): 2343 - 2349. [Abstract] [Full Text] [PDF]
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A. Haschemi, O. Wagner, R. Marculescu, B. Wegiel, S. C. Robson, N. Gagliani, D. Gallo, J.-F. Chen, F. H. Bach, and L. E. Otterbein Cross-Regulation of Carbon Monoxide and the Adenosine A2a Receptor in Macrophages J. Immunol., May 1, 2007; 178(9): 5921 - 5929. [Abstract] [Full Text] [PDF]
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A. D. Sheftel, S. F. Kim, and P. Ponka Non-heme Induction of Heme Oxygenase-1 Does Not Alter Cellular Iron Metabolism J. Biol. Chem., April 6, 2007; 282(14): 10480 - 10486. [Abstract] [Full Text] [PDF]
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Y. Zhu, Y. Zhang, B. A. Ojwang, M. A. Brantley Jr, and J. M. Gidday Long-Term Tolerance to Retinal Ischemia by Repetitive Hypoxic Preconditioning: Role of HIF-1{alpha} and Heme Oxygenase-1 Invest. Ophthalmol. Vis. Sci., April 1, 2007; 48(4): 1735 - 1743. [Abstract] [Full Text] [PDF]
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A.-L. Levonen, M. Inkala, T. Heikura, S. Jauhiainen, H.-K. Jyrkkanen, E. Kansanen, K. Maatta, E. Romppanen, P. Turunen, J. Rutanen, et al. Nrf2 Gene Transfer Induces Antioxidant Enzymes and Suppresses Smooth Muscle Cell Growth In Vitro and Reduces Oxidative Stress in Rabbit Aorta In Vivo Arterioscler Thromb Vasc Biol, April 1, 2007; 27(4): 741 - 747. [Abstract] [Full Text] [PDF]
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K. Liby, D. B. Royce, C. R. Williams, R. Risingsong, M. M. Yore, T. Honda, G. W. Gribble, E. Dmitrovsky, T. A. Sporn, and M. B. Sporn The Synthetic Triterpenoids CDDO-Methyl Ester and CDDO-Ethyl Amide Prevent Lung Cancer Induced by Vinyl Carbamate in A/J Mice Cancer Res., March 15, 2007; 67(6): 2414 - 2419. [Abstract] [Full Text] [PDF]
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 S. Immenschuh, Y. Shan, H. Kroll, S. Santoso, W. Wossmann, G. Bein, and H. L. Bonkovsky Marked Hyperbilirubinemia Associated With the Heme Oxygenase-1 Gene Promoter Microsatellite Polymorphism in a Boy With Autoimmune Hemolytic Anemia Pediatrics, March 1, 2007; 119(3): e764 - e767. [Abstract] [Full Text] [PDF]
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M. A. Perrella Heme Oxygenase-1: A Multifaceted Triple-Threat Molecule Am. J. Respir. Cell Mol. Biol., February 1, 2007; 36(2): 137 - 137. [Full Text] [PDF]
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S. W. Ryter, D. Morse, and A. M. K. Choi Carbon Monoxide and Bilirubin: Potential Therapies for Pulmonary/Vascular Injury and Disease Am. J. Respir. Cell Mol. Biol., February 1, 2007; 36(2): 175 - 182. [Abstract] [Full Text] [PDF]
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J. Alam and J. L. Cook How Many Transcription Factors Does It Take to Turn On the Heme Oxygenase-1 Gene? Am. J. Respir. Cell Mol. Biol., February 1, 2007; 36(2): 166 - 174. [Abstract] [Full Text] [PDF]
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X. Wang, Y. Wang, H. P. Kim, K. Nakahira, S. W. Ryter, and A. M. K. Choi Carbon Monoxide Protects against Hyperoxia-induced Endothelial Cell Apoptosis by Inhibiting Reactive Oxygen Species Formation J. Biol. Chem., January 19, 2007; 282(3): 1718 - 1726. [Abstract] [Full Text] [PDF]
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R. Stocker and M. A. Perrella Heme Oxygenase-1: A Novel Drug Target for Atherosclerotic Diseases? Circulation, November 14, 2006; 114(20): 2178 - 2189. [Full Text] [PDF]
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M. S. Wolin and N. G. Abraham Heme Oxygenase-1 Inhibition of Nox Oxidase Activation Is a Microvascular Endothelial Antioxidant Effect of NO Hypertension, November 1, 2006; 48(5): 826 - 827. [Full Text] [PDF]
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N. G. Abraham and G. Drummond CD163-Mediated Hemoglobin-Heme Uptake Activates Macrophage HO-1, Providing an Antiinflammatory Function Circ. Res., October 27, 2006; 99(9): 911 - 914. [Full Text] [PDF]
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