Heme oxygenase and iron: from bacteria to humans

References

• Posey JE, Gherardini FC. Lack of a role for iron in the Lyme disease pathogen. Science 2000; 288: 1651–1653.
   PubMed Web of Science ®Google Scholar
• Wagener FA, Volk HD, Willis D et al. Different faces of the heme—heme oxygenase system in inflammation. Pharmacol Rev 2003; 55: 551–571.
   PubMed Web of Science ®Google Scholar
• Ortiz de Montellano PR. The mechanism of heme oxygenase. Curr Opin Chem Rio! 2000; 4: 221–227.
   PubMed Web of Science ®Google Scholar
• Liu Y, Ortiz de Montellano PR. Reaction intermediates and single turnover rate constants for the oxidation of heme by human heme oxygenase-1. J Biol Chem 2000; 275: 5297–5307.
   PubMed Web of Science ®Google Scholar
• George JW, Nulk K, Weiss A, Bruss ML, Cornelius CE. Biliverdin reductase activity in cattle, sheep, rabbits and rats. Int J Biochem 1989; 21: 477–481.
   PubMedGoogle Scholar
• McDonagh AF. Bile pigments: bilatrienes and 1,15-biladienes. In: Dolphin D. (ed) The Porphyrins, vol VI. New York: Academic Press, 1979; 293–491.
   Google Scholar
• Terry MJ, Linley PJ, Kohchi T. Making light of it: the role of plant haem oxygenases in phytochrome chromophore synthesis. Biochem Soc Trans 2002; 30: 604–609.
   PubMed Web of Science ®Google Scholar
• Maines MD. The heme oxygenase system: a regulator of second messenger gases. Annu Rev Pharmacol Toxicol 1997; 37: 517–554.
   PubMed Web of Science ®Google Scholar
• Ryter SW, Alam J, Choi AM. Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol Rev 2006; 86: 583–650.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Bullen JJ. The significance of iron in infection. Rev Infect Dis 1981; 3: 1127–1138.
   PubMedGoogle Scholar
• Skaar EP, Humayun M, Bae T, DeBord KL, Schneewind O. Iron-source preference of Staphylococcus aureus infections. Science 2004; 305: 1626–1628.
   PubMed Web of Science ®Google Scholar
• Zhu W, Wilks A, Stojiljkovic I. Degradation of heme in Gram-negative bacteria: the product of the hem() gene of Neisseriae is a heme oxygenase. J Bacteriol 2000; 182: 6783–6790.
   PubMed Web of Science ®Google Scholar
• Schmitt MP. Utilization of host iron sources by Corynebacterium diphtheriae: identification of a gene whose product is homologous to eukaryotic heme oxygenases and is required for acquisition of iron from heme and hemoglobin. J Bacteriol 1997; 179: 838–845.
   PubMed Web of Science ®Google Scholar
• Skaar EP, Gaspar AH, Schneewind O. IsdG and IsdI, heme-degrading enzymes in the cytoplasm of Staphylococcus aureus. J Biol Chem 2004; 279: 436–443.
   PubMed Web of Science ®Google Scholar
• Ratliff M, Zhu W, Deshmukh R, Wilks A, Stojiljkovic I. Homologues of neisserial heme oxygenase in Gram-negative bacteria: degradation of heme by the product of the pigA gene of Pseudomonas aeruginosa. J Bacteriol 2001; 183: 6394–6403.
   PubMed Web of Science ®Google Scholar
• Wilks A. Heme oxygenase: evolution, structure, and mechanism. Antioxid Redox Signal 2002; 4: 603–614.
   PubMed Web of Science ®Google Scholar
• Schmitt MP. Transcription of the Corynebacterium diphtheriae hmu0 gene is regulated by iron and heme. Infect Immun 1997; 65: 4634–4641.
   PubMed Web of Science ®Google Scholar
• Pendrak ML, Chao MP, Yan SS, Roberts DD. Heme oxygenase in Candida albicans is regulated by hemoglobin and is necessary for metabolism of exogenous heme and hemoglobin to alpha-biliverdin. J Biol Chem 2004; 279: 3426–3433.
   PubMed Web of Science ®Google Scholar
• Protchenko O, Philpott CC. Regulation of intracellular heme levels by HMX1, a homologue of heme oxygenase, in Saccharomyces cerevisiae. J Biol Chem 2003; 278: 36582–36587.
   PubMed Web of Science ®Google Scholar
• Ueta R, Fujiwara N, Iwai K, Yamaguchi-Iwai Y. Mechanism underlying the iron-dependent nuclear export of the iron-responsive transcription factor Aftlp in Saccharomyces cerevisiae. Mol Biol Cell 2007; 18: 2980–2990.
   PubMed Web of Science ®Google Scholar
• Koury MJ, Ponka P. New insights into erythropoiesis: the roles of folate, vitamin B12, andiron. Annu Rev Nutr 2004; 24: 105–131.
   PubMed Web of Science ®Google Scholar
• Ponka P. Tissue-specific regulation of iron metabolism and heme synthesis: distinct control mechanisms in erythroid cells. Blood 1997; 89: 1–25.
   PubMed Web of Science ®Google Scholar
• Andrews NC. Disorders of iron metabolism. N Engl J Med 1999; 341: 1986–1995.
   PubMed Web of Science ®Google Scholar
• Cook JD, Barry WE, Hershko C, Fillet G, Finch CA. Iron kinetics with emphasis on iron overload. Am J Pathol 1973; 72: 337–344.
   PubMed Web of Science ®Google Scholar
• Green R, Charlton R, Seftel H et al. Body iron excretion in man: a collaborative study. Am J Med 1968; 45: 336–353.
   PubMed Web of Science ®Google Scholar
• Poss KD, Tonegawa S. Heme oxygenase 1 is required for mammalian iron reutilization. Proc Natl Acad Sci USA 1997; 94: 10919–10924.
   PubMed Web of Science ®Google Scholar
• Poss KD, Thomas MJ, Ebralidze AK, O'Dell TJ, Tonegawa S. Hippocampal long-term potentiation is normal in heme oxygenase-2 mutant mice. Neuron 1995; 15: 867–873.
   PubMed Web of Science ®Google Scholar
• Yachie A, Niida Y, Wada T et al. Oxidative stress causes enhanced endothelial cell injury in human heme oxygenase-1 deficiency. J Clin Invest 1999; 103: 129–135.
   PubMed Web of Science ®Google Scholar
• Kawashima A, Oda Y, Yachie A, Koizumi S, Nakanishi I. Heme oxygenase-1 deficiency: the first autopsy case. Hum Pathol 2002; 33: 125–130.
   PubMed Web of Science ®Google Scholar
• Poss KD, Tonegawa S. Reduced stress defense in heme oxygenase 1-deficient cells. Proc Natl Acad Sci USA 1997; 94: 10925–10930.
   PubMed Web of Science ®Google Scholar
• Balla G, Jacob HS, Eaton JW, Belcher JD, Vercellotti GM. Hemin: a possible physiological mediator of low density lipoprotein oxidation and endothelial injury. Arterioscler Thromb 1991; 11: 1700–1711.
   PubMedGoogle Scholar
• Maines MD, Gibbs PEM. 30 years of heme oxygenase: From a ‘molecular wrecking ball’ to a ‘mesmerizing’ trigger of cellular events. Biochem Biophys Res Commun 2005; 338: 568–577.
   PubMed Web of Science ®Google Scholar
• Bothwell TH, Charlton RW, Cook JD, Finch CA. Iron metabolism in man. Oxford: Blackwell, 1979.
   Google Scholar
• Sassa S. Why heme needs to be degraded to iron, biliverdin IXalpha, and carbon monoxide? Antioxid Redox Signal 2004; 6: 819–824.
   PubMed Web of Science ®Google Scholar
• Kakhlon O, Cabantchik ZI. The labile iron pool: characterization, measurement, and participation in cellular processes. Free Radic Biol Med 2002; 33: 1037–1046.
   PubMed Web of Science ®Google Scholar
• Quan S, Yang L, Abraham NG, Kappas A. Regulation of human heme oxygenase in endothelial cells by using sense and antisense retroviral constructs. Proc Natl Acad Sci USA 2001; 98: 12203–12208.
   PubMed Web of Science ®Google Scholar
• Suttner DM, Dennery PA. Reversal of HO-1 related cytoprotection with increased expression is due to reactive iron. FASEB J 1999; 13: 1800–1809.
   PubMed Web of Science ®Google Scholar
• Ferris CD, Jaffrey SR, Sawa A et al. Haem oxygenase-1 prevents cell death by regulating cellular iron. Nat Cell Biol 1999; 1: 152–157.
   PubMed Web of Science ®Google Scholar
• Hill M, Pereira V, Chauveau C et al. Heme oxygenase-1 inhibits rat and human breast cancer cell proliferation: mutual cross inhibition with indoleamine 2,3-dioxygenase. FASEB J2005; 19: 1957-1968.
   Google Scholar
• Taille C, El-Benna J, Lanone Set al. Induction of heme oxygenase-1 inhibits NAD(P)H oxidase activity by down-regulating cytochrome b558 expression via the reduction of heme availability. J Biol Chem 2004; 279: 28681–28688.
   PubMed Web of Science ®Google Scholar
• Petrat F, de Groot H, Rauen U. Determination of the chelatable iron pool of single intact cells by laser scanning microscopy. Arch Biochem Biophys 2000; 376: 74–81.
   PubMed Web of Science ®Google Scholar
• Watts RN, Richardson DR. Differential effects on cellular iron metabolism of the physiologically relevant diatomic effector molecules, NO and CO, that bind iron. Biochim Biophys Acta 2004; 1692: 1–15.
   PubMed Web of Science ®Google Scholar
• Knutson MD, Oukka M, Koss LM, Aydemir F, Wessling-Resnick M. Iron release from macrophages after erythrophagocytosis is up-regulated by ferroportin 1 overexpression and down-regulated by hepcidin. Proc Natl Acad Sci USA 2005; 102: 1324–1328.
   PubMed Web of Science ®Google Scholar
• Delaby C, Pilard N, Puy H, Canonne-Hergaux F. Sequential regulation of ferroportin expression after erythrophagocytosis in murine macrophages: early mRNA induction by haem, followed by iron-dependent protein expression. Biochem J2008; 411: 123-131.
   Google Scholar
• De Domenico I, Ward DM, di Patti MC et al. Ferroxidase activity is required for the stability of cell surface ferroportin in cells expressing GPI-ceruloplasmin. EMBO J2007; 26: 2823-2831.
   Google Scholar
• Harrison PM, Arosio P. The ferritins: molecular properties, iron storage function and cellular regulation. Biochim Biophys Acta 1996; 1275: 161–203.
   PubMed Web of Science ®Google Scholar
• Balla J, Vercellotti GM, Nath K et al. Haem, haem oxygenase and ferritin in vascular endothelial cell injury. Nephrol Dial Transplant 2003; 18 (Suppl 5): v8–v12.
   PubMed Web of Science ®Google Scholar
• Balla G, Jacob HS, Balla J et al. Ferritin: a cytoprotective antioxidant stratagem of endothelium. J Biol Chem 1992; 267: 18148–18153.
   PubMed Web of Science ®Google Scholar
• Balla J, Nath KA, Balla G, Juckett MB, Jacob HS, Vercellotti GM. Endothelial cell heme oxygenase and ferritin induction in rat lung by hemoglobin in vivo. Am J Physiol 1995; 268: L321–L327.
   PubMed Web of Science ®Google Scholar
• Vile GF, Tyrrell RM. Oxidative stress resulting from ultraviolet A irradiation of human skin fibroblasts leads to a heme oxygenase-dependent increase in ferritin. J Biol Chem 1993; 268: 14678–14681.
   PubMed Web of Science ®Google Scholar
• Juckett MB, Weber M, Balla J, Jacob HS, Vercellotti GM. Nitric oxide donors modulate ferritin and protect endothelium from oxidative injury. Free Radic Biol Med 1996; 20: 63–73.
   PubMed Web of Science ®Google Scholar
• Miller LL, Miller SC, Torti SV, Tsuji Y, Torti FM. Iron-independent induction of ferritin H chain by tumor necrosis factor. Proc Natl Acad Sci USA 1991; 88: 4946–4950.
   PubMed Web of Science ®Google Scholar
• Bevilacqua MA, Faniello MC, Russo T, Cimino F, Costanzo E Transcriptional regulation of the human H ferritin-encoding gene (FERH) in G418-treated cells: role of the B-box-binding factor. Gene 1994; 141: 287–291.
   PubMed Web of Science ®Google Scholar
• Stocker R, Perrella MA. Heme oxygenase-1. A novel drug target for atherosclerotic diseases? Circulation 2006; 114: 2178–2189.
   Google Scholar
• Bach FH. Heme oxygenase-1: a therapeutic amplification funnel. FASEB J 2005; 19: 1216–1219.
   PubMed Web of Science ®Google Scholar
• Stocker R. Induction of haem oxygenase as a defence against oxidative stress. Free Radic Res Commun 1990; 9: 101–112.
   PubMed Web of Science ®Google Scholar
• Abraham NG, Lin JH-C, Schwartzman ML, Levere RD, Shibahara S. The physiological significance of heme oxygenase. Int J Biochem 1988; 20: 543–558.
   PubMedGoogle Scholar
• Belcher JD, Mahaseth H, Welch TE, Otterbein LE, Hebbel RP, Vercellotti GM. Heme oxygenase-1 is a modulator of inflammation and vaso-occlusion in transgenic sickle mice. J CIM Invest 2006; 116: 808–816.
   PubMed Web of Science ®Google Scholar
• Pamplona A, Ferreira A, Balla Jet al. Heme oxygenase-1 and carbon monoxide suppress the pathogenesis of experimental cerebral malaria. Nat Med 2007; 13: 703–710.
   PubMed Web of Science ®Google Scholar
• Vera T, Kelsen S, Stec DE. Kidney-specific induction of heme oxygenase-1 prevents angiotensin II hypertension. Hypertension 2008; 52: 660–665.
   PubMed Web of Science ®Google Scholar
• Jazwa A, Loboda A, Golda S et al. Effect of heme and heme oxygenase-1 on vascular endothelial growth factor synthesis and angiogenic potency of human keratinocytes. Free Radic Biol Med 2006; 40: 1250–1263.
   PubMed Web of Science ®Google Scholar
• Soares MP, Seldon MP, Gregoire IP et al. Heme oxygenase-1 modulates the expression of adhesion molecules associated with endothelial cell activation. J Immunol 2004; 172: 3553–3563.
   PubMed Web of Science ®Google Scholar
• Seldon MP, Silva G, Pejanovic N et al. Heme oxygenase-1 inhibits the expression of adhesion molecules associated with endothelial cell activation via inhibition of NF-kappaB RelA phosphorylation at serine 276. J Immunol 2007; 179: 7840–7851.
   PubMed Web of Science ®Google Scholar
• Dennery PA, Sridhar KJ, Lee CS et al. Heme oxygenase-mediated resistance to oxygen toxicity in hamster fibroblasts. J Biol Chem 1997; 272: 14937–14942.
   PubMed Web of Science ®Google Scholar
• Ryter SW, Tyrrell RM. The heme synthesis and degradation pathways: role in oxidant sensitivity. Free Radic Biol Med 2000; 28: 289–309.
   PubMed Web of Science ®Google Scholar
• Lamb NJ, Quinlan GJ, Mumby S, Evans TW, Gutteridge JM. Haem oxygenase shows pro-oxidant activity in microsomal and cellular systems: implications for the release of low-molecular-mass iron. Biochem J1999; 344: 153-158.
   Google Scholar
• Eisenstein RS. Iron regulatory proteins and the molecular control of mammalian iron metabolism. Annu Rev Nutr 2000; 20: 627–662.
   PubMed Web of Science ®Google Scholar
• Li C, Hossieny P, Wu BJ, Qawasmeh A, Beck K, Stocker R. Pharmacologic induction of heme oxygenase-1. Antioxid Redox Signal 2007; 9: 2227–2240.
   PubMed Web of Science ®Google Scholar