Mechanisms of Cell Protection by Heme Oxygenase-1
Abstract
Heme oxygenases (HO) catabolize free heme, that is, iron (Fe) protoporphyrin (IX), into equimolar amounts of Fe 2+ , carbon monoxide (CO), and biliverdin. The stress-responsive HO-1 isoenzyme affords protection against programmed cell death. The mechanism underlying this cytoprotective effect relies on the ability of HO-1 to catabolize free heme and prevent it from sensitizing cells to undergo programmed cell death. This cytoprotective effect inhibits the pathogenesis of a variety of immune-mediated inflammatory diseases.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
HO-1 exerts cytoprotective effects by reducing the pro-oxidative activity of heme and by re-programming metabolic traits, thereby limiting tissue damage in inflammatory processes, including sepsis.
“Thus, HO-1 exerts cytoprotective effects by reducing the pro-oxidative activity of heme and by re-programming metabolic traits, thereby limiting tissue damage in the course of inflammatory processes, including sepsis (Gozzelino et al., 2010; Weis et al., 2017).”
From The Role of Iron Regulation in Immunometabolism and Immune-Related Disease (2019) · cites this paper as Gozzelino et al., 2010
Heme-mediated cytotoxicity occurs via a Fenton reaction producing hydroxyl radicals.
“Presumably, this occurs via a mechanism driven via the Fenton reaction in which hydrogen peroxide (H 2 O 2 ) oxidizes Fe 2+ , either within the context of the tetrapyrrole ring or when Fe is released from heme, to produce highly reactive hydroxyl radicals (OH .) [38,212].”
From The Iron age of host–microbe interactions (2015) · cites this paper as [38]
Labile heme sensitizes parenchyma cells to undergo programmed cell death in response to proinflammatory cytokines such as TNF, as well as Fas, ROS, and RNS.
“Briefly, labile heme sensitizes parenchyma cells to undergo programmed cell death in response to proinflammatory cytokines such as TNF [106] as well as other agonists such as Fas as well as ROS and RNS [38,190].”
From The Iron age of host–microbe interactions (2015) · cites this paper as [38]
Once released from hemoglobin, labile heme becomes pro-oxidant and cytotoxic.
“Once released from hemoglobin, the redox activity of labile heme becomes pro-oxidant and cytotoxic [38,106,107,190] (Fig 4).”
From The Iron age of host–microbe interactions (2015) · cites this paper as [38]
The pathogenic effects of extracellular hemoglobin and labile heme are countered by adaptive responses converging on heme catabolism by HO-1, providing tissue damage control and disease tolerance to systemic infections.
“The pathogenic effects exerted by extracellular hemoglobin and labile heme are countered by adaptive responses that converge at the level of heme catabolism by HO-1 [38,219], providing tissue damage control and disease tolerance to systemic infections [103,105,106] (Fig 4).”
From The Iron age of host–microbe interactions (2015) · cites this paper as [38]
HO-1 avoids tissue Fe overload and tissue damage while sustaining Fe supply to erythropoiesis to maintain Fe homeostasis during infection.
“When coupled to other mechanisms regulating Fe homeostasis, HO-1 avoids tissue Fe overload and tissue damage while sustaining Fe supply to erythropoiesis to maintain Fe homeostasis during infection [38,54,219,220] (Fig 4).”
From The Iron age of host–microbe interactions (2015) · cites this paper as [38]
The most abundant pool of Fe in mammals are the prosthetic heme groups of hemoglobin in RBC, followed by myoglobin and cytochromes.
“The most abundant pool of Fe in mammals are the prosthetic heme groups of hemoglobin in red blood cells (RBC), followed by the heme groups of myoglobin in muscle cells and those of cytochromes and other ubiquitously expressed hemoproteins in all cells[38,54].”
From The Iron age of host–microbe interactions (2015) · cites this paper as [38]
Recent studies demonstrate the mechanisms leading to the unfavorable effects of free hemoglobin including oxidation and production of ferryl hemoglobin and heme generation.
“Moreover, recent studies demonstrate the mechanisms leading to the unfavorable effects of free hemoglobin including oxidation and production of ferryl hemoglobin and heme generation [36-38].”
From Free hemoglobin concentration in severe sepsis: methods of measurement and prediction of outcome (2012) · cites this paper as [38]
Reduced abundance of CO and bilirubin contributes to increased or prolonged oxidative stress because these molecules have radical scavenging and anti-inflammatory activities.
“In addition, the reduced abundance of CO and bilirubin, two end-products of the HO-1 pathway, further contributes to increased or prolonged oxidative stress, as these molecules have radical scavenging capacities and anti-inflammatory activities (Gozzelino et al., 2010).”
From Heme oxygenase 1 controls early innate immune response of macrophages to<i>Salmonella</i>Typhimurium infection: Heme oxygenase 1 expression affects Salmonella<i>infection</i> (2016) · cites this paper as Gozzelino et al., 2010
Up-regulation of HO-1 during malaria or sepsis is associated with infection tolerance and limitation of tissue damage resulting in improved survival.
“Up-regulation of HO-1 during malaria or sepsis was demonstrated in association with infection tolerance and limitation of tissue damage resulting in an improved survival (Gozzelino et al., 2010; Larsen et al., 2010).”
From Heme oxygenase 1 controls early innate immune response of macrophages to<i>Salmonella</i>Typhimurium infection: Heme oxygenase 1 expression affects Salmonella<i>infection</i> (2016) · cites this paper as Gozzelino et al., 2010
Cites
1 retracted
Biswas, D., Banerjee, M., Sen, G., Das, J. K., Banerjee, A., Sau, T. J., Pandit, S., Giri, A. K., & Biswas, T. (2008) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2008.02.003 · Cited by 109 · see citing works
RetractedApoptosis: A Basic Biological Phenomenon with Wideranging Implications in Tissue Kinetics
Kerr, J. F. R., Wyllie, A. H., & Currie, A. R. (1972) · British Journal of Cancer · doi:10.1038/bjc.1972.33 · Cited by 15,673 · see citing works
Hengartner, M. O. (2000) · Nature · doi:10.1038/35037710 · Cited by 7,295 · see citing works
Origin and physiological roles of inflammation
Medzhitov, R. (2008) · Nature · doi:10.1038/nature07201 · Cited by 6,618 · see citing works
Cleavage of BID by Caspase 8 Mediates the Mitochondrial Damage in the Fas Pathway of Apoptosis
Li, H., Zhu, H., Xu, C.-J., & Yuan, J. (1998) · Cell · doi:10.1016/s0092-8674(00)81590-1 · Cited by 4,445 · see citing works
Release of chromatin protein HMGB1 by necrotic cells triggers inflammation
Scaffidi, P., Misteli, T., & Bianchi, M. E. (2002) · Nature · doi:10.1038/nature00858 · Cited by 4,221 · see citing works
Bilirubin Is an Antioxidant of Possible Physiological Importance
Stocker, R., Yamamoto, Y., McDonagh, A. F., Glazer, A. N., & Ames, B. N. (1987) · Science · doi:10.1126/science.3029864 · Cited by 3,502 · see citing works
The Pathophysiology of Mitochondrial Cell Death
Green, D. R., & Kroemer, G. (2004) · Science · doi:10.1126/science.1099320 · Cited by 3,416 · see citing works
LXXIII.—Oxidation of tartaric acid in presence of iron
Fenton, H. J. H. (1894) · J. Chem. Soc., Trans. · doi:10.1039/ct8946500899 · Cited by 3,179 · see citing works
An Essential Role for NF-κB in Preventing TNF-α-Induced Cell Death
Beg, A. A., & Baltimore, D. (1996) · Science · doi:10.1126/science.274.5288.782 · Cited by 3,047 · see citing works
Wang, C.-Y., Mayo, M., Korneluk, R., Goeddel, D., & Baldwin, A. (1998) · Science · doi:10.1126/science.281.5383.1680 · Cited by 2,950 · see citing works
Signalling pathways of the TNF superfamily: a double-edged sword
Aggarwal, B. B. (2003) · Nature Reviews Immunology · doi:10.1038/nri1184 · Cited by 2,793 · see citing works
Points of control in inflammation
Nathan, C. (2002) · Nature · doi:10.1038/nature01320 · Cited by 2,738 · see citing works
Induction of TNF receptor I-mediated apoptosis via two sequential signaling complexes
Micheau, O., & Tschopp, J. (2003) · Cell · doi:10.1016/s0092-8674(03)00521-x · Cited by 2,738 · see citing works
The ferritins: molecular properties, iron storage function and cellular regulation
Harrison, P. M., & Arosio, P. (1996) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/0005-2728(96)00022-9 · Cited by 2,667 · see citing works
Integrating cell-signalling pathways with NF-κB and IKK function
Perkins, N. D. (2007) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2083 · Cited by 2,350 · see citing works
IκB: a Specific Inhibitor of the NF-κB Transcription Factor
Baeuerle, P. A., & Baltimore, D. (1988) · Science · doi:10.1126/science.3140380 · Cited by 2,154 · see citing works
Molecular mechanisms of caspase regulation during apoptosis
Riedl, S. J., & Shi, Y. (2004) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1496 · Cited by 1,893 · see citing works
The enzymatic conversion of heme to bilirubin by microsomal heme oxygenase.
Tenhunen, R., Marver, H. S., & Schmid, R. (1968) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.61.2.748 · Cited by 1,803 · see citing works
Kamata, H., Honda, S.-I., Maeda, S., Chang, L., Hirata, H., & Karin, M. (2005) · Cell · doi:10.1016/j.cell.2004.12.041 · Cited by 1,792 · see citing works
The pathogenic basis of malaria
Miller, L. H., Baruch, D. I., Marsh, K., & Doumbo, O. K. (2002) · Nature · doi:10.1038/415673a · Cited by 1,754 · see citing works
Identification of the haemoglobin scavenger receptor
Kristiansen, M., Graversen, J. H., Jacobsen, C., Sonne, O., Hoffman, H.-J., Law, S. K. A., & Moestrup, S. K. (2001) · Nature · doi:10.1038/35051594 · Cited by 1,712 · see citing works
The Clinical Sequelae of Intravascular Hemolysis and Extracellular Plasma Hemoglobin
Rother, R. P., Bell, L. B., Hillmen, P., & Gladwin, M. T. (2005) · JAMA · doi:10.1001/jama.293.13.1653 · Cited by 1,551 · see citing works
Oxidation of tartaric acid in presence of iron
Fenton, H. J. H. (1894) · Journal of the Chemical Society (Resumed) · Cited by 1,498 · see citing works
Control of IκB-α Proteolysis by Site-Specific, Signal-Induced Phosphorylation
Brown, K., Gerstberger, S., Carlson, L., Franzoso, G., & Siebenlist, U. (1995) · Science · doi:10.1126/science.7878466 · Cited by 1,434 · see citing works
Mitogen-activated protein kinases in apoptosis regulation
Wada, T., & Penninger, J. M. (2004) · Oncogene · doi:10.1038/sj.onc.1207556 · Cited by 1,432 · see citing works
Rhee, S. G., Chae, H. Z., & Kim, K. (2005) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2005.02.026 · Cited by 1,409 · see citing works
Cell-free hemoglobin limits nitric oxide bioavailability in sickle-cell disease
Reiter, C. D., Wang, X., Tanus-Santos, J. E., Hogg, N., Cannon, R. O., Schechter, A. N., & Gladwin, M. T. (2002) · Nature Medicine · doi:10.1038/nm1202-799 · Cited by 1,330 · see citing works
TUMOR NECROSIS FACTOR RECEPTOR AND Fas SIGNALING MECHANISMS
Wallach, D., Varfolomeev, E. E., Malinin, N. L., Goltsev, Y. V., Kovalenko, A. V., & Boldin, M. (1999) · Annual Review of Immunology · doi:10.1146/annurev.immunol.17.1.331 · Cited by 1,299 · see citing works
Reduced stress defense in heme oxygenase 1-deficient cells
Poss, K. D., & Tonegawa, S. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.20.10925 · Cited by 1,293 · see citing works
Nrf2, a Cap'n'Collar Transcription Factor, Regulates Induction of the Heme Oxygenase-1 Gene
Alam, J., Stewart, D. P., Touchard, C. L., Boinapally, S., Choi, A. M. K., & Cook, J. L. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.37.26071 · Cited by 1,284 · see citing works
Chen, Z., Hagler, J., Palombella, V. J., Melandri, F. D., Scherer, D. C., Ballard, D. W., & Maniatis, T. (1995) · Genes & Development · doi:10.1101/gad.9.13.1586 · Cited by 1,270 · see citing works
Oxidative stress causes enhanced endothelial cell injury in human heme oxygenase-1 deficiency
Yachie, A., Niida, Y., Wada, T., Igarashi, N., Kaneda, H., Toma, T., Ohta, K., Kasahara, Y., & Koizumi, S. (1999) · Journal of Clinical Investigation · doi:10.1172/jci4165 · Cited by 1,256 · see citing works
Shaping the nuclear action of NF-κB
Chen, L., & Greene, W. C. (2004) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1368 · Cited by 1,219 · see citing works
Zhong, H., Voll, R. E., & Ghosh, S. (1998) · Molecular Cell · doi:10.1016/s1097-2765(00)80066-0 · Cited by 1,210 · see citing works
Variation in the TNF-α promoter region associated with susceptibility to cerebral malaria
McGuire, W. L., Hill, A. V. S., Allsopp, C. E. M., Greenwood, B. M., & Kwiatkowski, D. P. (1994) · Nature · doi:10.1038/371508a0 · Cited by 1,166 · see citing works
Heme oxygenase-1: unleashing the protective properties of heme
Otterbein, L. E., Soares, M. P., Yamashita, K., & Bach, F. H. (2003) · Trends in Immunology · doi:10.1016/s1471-4906(03)00181-9 · Cited by 1,166 · see citing works
Self-citationChoi, A. M., & Alam, J. (1996) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/ajrcmb.15.1.8679227 · Cited by 1,126 · see citing works
Pharmacological and Clinical Aspects of Heme Oxygenase
Abraham, N. G., & Kappas, A. (2008) · Pharmacological Reviews · doi:10.1124/pr.107.07104 · Cited by 1,115 · see citing works
Rapid proteolysis of IκB-α is necessary for activation of transcription factor NF-κB
Henkel, T., Machleidt, T., Alkalay, I., Krönke, M., Ben‐Neriah, Y., & Baeuerle, P. A. (1993) · Nature · doi:10.1038/365182a0 · Cited by 1,103 · see citing works
Ferritin: a cytoprotective antioxidant strategem of endothelium.
Balla, G., Jacob, H., Balla, J., Rosenberg, M. E., Nath, K. A., Apple, F., Eaton, J. W., & Vercellotti, G. M. (1992) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)37165-0 · Cited by 1,097 · see citing works
Cell-free hemoglobin limits nitric oxide bioavailability in sickle-cell disease
Reiter, C. D., Wang, X., Tanus-Santos, J. E., et al. (2002) · Nature Medicine · doi:10.1038/nm799 · Cited by 1,097 · see citing works
Indicators of Life-Threatening Malaria in African Children
Marsh, K., Forster, D., Waruiru, C., Mwangi, I., Winstanley, M., Marsh, V., Newton, C. R. J. C., Winstanley, P., Warn, P. A., Peshu, N. M., et al. (1995) · New England Journal of Medicine · doi:10.1056/nejm199505253322102 · Cited by 1,093 · see citing works
Biliverdin reductase: A major physiologic cytoprotectant
Barañano, D. E., Rao, M., Ferris, C. D., & Snyder, S. H. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.252626999 · Cited by 1,091 · see citing works
Heme oxygenase-1 mediates the anti-inflammatory effect of interleukin-10 in mice
Lee, T.-S., & Chau, L.-Y. (2002) · Nature Medicine · doi:10.1038/nm0302-240 · Cited by 1,019 · see citing works
p16INK4a induces an age-dependent decline in islet regenerative potential
Krishnamurthy, J., Ramsey, M. R., Ligon, K. L., Torrice, C., Koh, A., Bonner-Weir, S., & Sharpless, N. E. (2006) · Nature · doi:10.1038/nature05092 · Cited by 1,003 · see citing works
Hitomi, J., Christofferson, D. E., Ng, A., Yao, J., Degterev, A., Xavier, R. J., & Yuan, J. (2008) · Cell · doi:10.1016/j.cell.2008.10.044 · Cited by 989 · see citing works
Carbon Monoxide Generated by Heme Oxygenase 1 Suppresses Endothelial Cell Apoptosis
Brouard, S., Otterbein, L. E., Anrather, J., Tobiasch, E., Bach, F. H., Choi, A. M. K., & Soares, M. P. (2000) · The Journal of Experimental Medicine · doi:10.1084/jem.192.7.1015 · Cited by 984 · see citing works
Self-citationThe lipocalin protein family: structural and sequence overview
Flower, D. R., North, A. C. T., & Sansom, C. E. (2000) · Biochimica et Biophysica Acta (BBA) - Protein Structure and Molecular Enzymology · doi:10.1016/s0167-4838(00)00148-5 · Cited by 868 · see citing works
More than one way to die: apoptosis, necrosis and reactive oxygen damage
Fiers, W. C., Beyaert, R., Declercq, W., & Vandenabeele, P. (1999) · Oncogene · doi:10.1038/sj.onc.1203249 · Cited by 858 · see citing works
Cleavage of the death domain kinase RIP by Caspase-8 prompts TNF-induced apoptosisPreprint
Lin, Y., Devin, A., Rodriguez, Y., & Liu, Z.-G. (1999) · Genes & Development · doi:10.1101/gad.13.19.2514 · Cited by 835 · see citing works
Identification of an Intestinal Heme Transporter
Shayeghi, M., Latunde-Dada, G. O., Oakhill, J. S., Laftah, A. H., Takeuchi, K., Halliday, N., Khan, Y., Warley, A., McCann, F. E., Hider, R. C., et al. (2005) · Cell · doi:10.1016/j.cell.2005.06.025 · Cited by 755 · see citing works
Tumor Necrosis Factor (Cachectin) as an Essential Mediator in Murine Cerebral Malaria
Grau, G. E., Fajardo, L. F., Piguet, P., Allet, B., Lambert, P., & VASSALLI, P. (1987) · Science · doi:10.1126/science.3306918 · Cited by 735 · see citing works
Festjens, N., Vanden Berghe, T., & Vandenabeele, P. (2006) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2006.06.014 · Cited by 710 · see citing works
Chang, L., Kamata, H., Solinas, G., Luo, J.-L., Maeda, S., Venuprasad, K., Liu, Y.-C., & Karin, M. (2006) · Cell · doi:10.1016/j.cell.2006.01.021 · Cited by 706 · see citing works
Doré, S., Takahashi, M., Ferris, C. D., Hester, L. D., Guastella, D. B., & Snyder, S. H. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.5.2445 · Cited by 699 · see citing works
Pham, C. G., Bubici, C., Zazzeroni, F., Papa, S., Jones, J., Alvarez, K., Jayawardena, S., De Smaele, E., Cong, R., Beaumont, C., et al. (2004) · Cell · doi:10.1016/j.cell.2004.10.017 · Cited by 663 · see citing works
The Stem Cell Marker Bcrp/ABCG2 Enhances Hypoxic Cell Survival through Interactions with Heme
Krishnamurthy, P. C., Ross, D. D., Nakanishi, T., Bailey-Dell, K., Zhou, S., Mercer, K. E., Sarkadi, B., Sorrentino, B. P., & Schuetz, J. D. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m313599200 · Cited by 661 · see citing works
Hemoprotein Bach1 regulates enhancer availability of heme oxygenase‐1 gene
Sun, J., Hoshino, H., Takaku, K., Nakajima, O., Muto, A., Suzuki, H., Tashiro, S., Takahashi, S., Shibahara, S., Alam, J., et al. (2002) · The EMBO Journal · doi:10.1093/emboj/cdf516 · Cited by 637 · see citing works
Pro-oxidant and cytotoxic effects of circulating heme
Jeney, V., Balla, J., Yachie, A., Varga, Z., Vercellotti, G. M., Eaton, J. W., & Balla, G. (2002) · Blood · doi:10.1182/blood.v100.3.879 · Cited by 633 · see citing works
Self-citationThe endoplasmic reticulum stress response in immunity and autoimmunity
Todd, D. J., Lee, A., & Glimcher, L. H. (2008) · Nature reviews. Immunology · doi:10.1038/nri2359 · Cited by 621 · see citing works
Expression of heme oxygenase-1 can determine cardiac xenograft survival
Soares, M. P., Lin, Y., Anrather, J., Csizmadia, E., Takigami, K., Sato, K., Grey, S. T., Colvin, R. B., Choi, A. M. K., Poss, K. D., et al. (1998) · Nature Medicine · doi:10.1038/2063 · Cited by 613 · see citing works
Self-citationBalla, J., Jacob, H. S., Balla, G., Nath, K. A., Eaton, J. W., & Vercellotti, G. M. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.20.9285 · Cited by 591 · see citing works
Necroptosis: A Specialized Pathway of Programmed Necrosis
Galluzzi, L., & Kroemer, G. (2008) · Cell · doi:10.1016/j.cell.2008.12.004 · Cited by 561 · cited 1× · see citing works
“In addition, engagement of death receptors such as Fas (137) or TNFR-1 can induce a form of programmed cell death related to necrosis but that shares some biochemical features of apoptosis, that is, necroptosis (138, 139).”
BackgroundHeme oxygenase-1 and carbon monoxide suppress the pathogenesis of experimental cerebral malaria
Pamplona, A., Ferreira, A., Balla, J., Jeney, V., Balla, G., Epiphanio, S., Chora, Â., Rodrigues, C. D., Gregoire, I. P., Cunha-Rodrigues, M., et al. (2007) · Nature Medicine · doi:10.1038/nm1586 · Cited by 560 · see citing works
Self-citationBoth cIAP1 and cIAP2 regulate TNFα-mediated NF-κB activation
Mahoney, D. J., Cheung, H. H., Mrad, R. L., Plenchette, S., Simard, C., Enwere, E., Arora, V., Mak, T. W., Lacasse, E. C., Waring, J., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0711122105 · Cited by 540 · see citing works
Different Faces of the Heme-Heme Oxygenase System in Inflammation
Wagener, F. A. D. T. G., Volk, H., Willis, D., Abraham, N. G., Soares, M. P., Adema, G. J., & Figdor, C. G. (2003) · Pharmacological Reviews · doi:10.1124/pr.55.3.5 · Cited by 537 · see citing works
Self-citationOgawa, K., Sun, J., Taketani, S., Nakajima, O., Nishitani, C., Sassa, S., Hayashi, N., Yamamoto, M., Shibahara, S., Fujita, H., et al. (2001) · The EMBO Journal · doi:10.1093/emboj/20.11.2835 · Cited by 532 · see citing works
Bilirubin and glutathione have complementary antioxidant and cytoprotective roles
Sedlak, T. W., Saleh, M., Higginson, D. S., Paul, B. D., Juluri, K. R., & Snyder, S. H. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0813132106 · Cited by 532 · see citing works
Heme oxygenase 1 mediates an adaptive response to oxidative stress in human skin fibroblasts.
Vile, G. F., Modak, S. B., Waltner, C., & Tyrrell, R. M. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.7.2607 · Cited by 517 · see citing works
Kim, Y., Morgan, M. J., Choksi, S., & Liu, Z.-G. (2007) · Molecular Cell · doi:10.1016/j.molcel.2007.04.021 · Cited by 517 · see citing works
Haem oxygenase-1 prevents cell death by regulating cellular iron
Ferris, C. D., Jaffrey, S. R., Sawa, A., Takahashi, M., Brady, S. D., Barrow, R. K., Tysoe, S. A., Wolosker, H., Barañano, D. E., Doré, S., et al. (1999) · Nature Cell Biology · doi:10.1038/11072 · Cited by 509 · see citing works
Mustafa, A. K., Gadalla, M. M., & Snyder, S. H. (2009) · Science Signaling · doi:10.1126/scisignal.268re2 · Cited by 491 · see citing works
Philippidis, P., Mason, J. C., Evans, B. J., Nadra, I., Taylor, K. M., Haskard, D. O., & Landis, R. C. (2004) · Circulation Research · doi:10.1161/01.res.0000109414.78907.f9 · Cited by 476 · see citing works
Identification of the receptor scavenging hemopexin-heme complexes
Hvidberg, V., Maniecki, M. B., Jacobsen, C., Højrup, P., Møller, H. J., & Moestrup, S. K. (2005) · Blood · doi:10.1182/blood-2005-03-1185 · Cited by 473 · see citing works
Soares, M. P., Seldon, M. P., Grégoire, I. P., Vassilevskaia, T. D., Berberat, P. O., Yu, J. H., Tsui, T., & Bach, F. H. (2004) · The Journal of Immunology · doi:10.4049/jimmunol.172.6.3553 · Cited by 464 · see citing works
Self-citationSato, K., Balla, J., Otterbein, L. E., Smith, R. N., Brouard, S., Lin, Y., Csizmadia, E., Sévigny, J., Robson, S. C., Vercellotti, G. M., et al. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.166.6.4185 · Cited by 462 · see citing works
Self-citationCarbon monoxide provides protection against hyperoxic lung injury
Otterbein, L. E., Mantell, L. L., & Choi, A. M. K. (1999) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.1999.276.4.l688 · Cited by 439 · see citing works
CO AS A CELLULAR SIGNALING MOLECULE
Kim, H. P., Ryter, S. W., & Choi, A. M. K. (2005) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev.pharmtox.46.120604.141053 · Cited by 426 · see citing works
Identification of a Human Heme Exporter that Is Essential for Erythropoiesis
Quigley, J. G., Yang, Z., Worthington, M., Phillips, J. D., Sabo, K. M., Sabath, D. E., Berg, C. L., Sassa, S., Wood, B. L., & Abkowitz, J. L. (2004) · Cell · doi:10.1016/j.cell.2004.08.014 · Cited by 423 · see citing works
Balla, G., Jacob, H. S., Eaton, J. W., Belcher, J. D., & Vercellotti, G. M. (1991) · Arteriosclerosis and Thrombosis A Journal of Vascular Biology · doi:10.1161/01.atv.11.6.1700 · Cited by 421 · see citing works
Lin, Q., Weis, S., Yang, G., Weng, Y., Helston, R. M., Rish, K. R., Smith, A., Bordner, J., Polte, T., Gaunitz, F., et al. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m607954200 · Cited by 416 · see citing works
Hypoxia induces severe right ventricular dilatation and infarction in heme oxygenase-1 null mice
Yet, S., Perrella, M. A., Layne, M. D., Hsieh, C.-M., Maemura, K., Kobzik, L., Wiesel, P., Christou, H. A., Kourembanas, S., & Lee, M.-E. (1999) · Journal of Clinical Investigation · doi:10.1172/jci6163 · Cited by 407 · see citing works
A Heme Export Protein Is Required for Red Blood Cell Differentiation and Iron Homeostasis
Keel, S. B., Doty, R. T., Yang, Z., Quigley, J. G., Chen, J., Knoblaugh, S., Kingsley, P. D., De Domenico, I., Vaughn, M. B., Kaplan, J., et al. (2008) · Science · doi:10.1126/science.1151133 · Cited by 404 · see citing works
Fujita, T., Toda, K., Karimova, A., Yan, S., Naka, Y., Yet, S., & Pinsky, D. J. (2001) · Nature Medicine · doi:10.1038/87929 · Cited by 399 · see citing works
Hemoglobin research and the origins of molecular medicine
Schechter, A. N. (2008) · Blood · doi:10.1182/blood-2008-04-078188 · Cited by 382 · see citing works
Programmed cell death in Caenorhabditis elegans
Hengartner, M. O., & Horvitz, H. R. (1994) · Current Opinion in Genetics & Development · doi:10.1016/0959-437x(94)90076-f · Cited by 378 · see citing works
How Many Transcription Factors Does It Take to Turn On the Heme Oxygenase-1 Gene?
Alam, J., & Cook, J. L. (2006) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2006-0340tr · Cited by 378 · see citing works
Suppression of Inflammatory Cytokine Production by Carbon Monoxide Involves the JNK Pathway and AP-1
Morse, D., Pischke, S. E., Zhou, Z., Davis, R. J., Flavell, R. A., Loop, T., Otterbein, S. L., Otterbein, L. E., & Choi, A. M. K. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m302942200 · Cited by 373 · see citing works
Haptoglobin, inflammation and disease
Quaye, I. K. (2008) · Transactions of the Royal Society of Tropical Medicine and Hygiene · doi:10.1016/j.trstmh.2008.04.010 · Cited by 371 · see citing works
The role of heme oxygenase-1 promoter polymorphisms in human disease
Exner, M., Minar, E., Wagner, O. F., & Schillinger, M. (2004) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2004.07.008 · Cited by 359 · see citing works
Identification of a mammalian mitochondrial porphyrin transporter
Krishnamurthy, P. C., Du, G., Fukuda, Y., Sun, D., Sampath, J., Mercer, K. E., Wang, J., Sosa‐Pineda, B., Murti, K. G., & Schuetz, J. D. (2006) · Nature · doi:10.1038/nature05125 · Cited by 358 · see citing works
ROLE OF ABCG2/BCRP IN BIOLOGY AND MEDICINE
Krishnamurthy, P., & Schuetz, J. D. (2005) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev.pharmtox.46.120604.141238 · Cited by 357 · see citing works
Krüger, B., Krick, S., Dhillon, N. K., Lerner, S., Ames, S. A., Bromberg, J. S., Lin, M., Walsh, L., Vella, J. P., Fischereder, M., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0810169106 · Cited by 351 · see citing works
Tumor necrosis factor's cytotoxic activity is signaled by the p55 TNF receptor
Tartaglia, L. A., Rothe, M., Hu, Y.-F., & Goeddel, D. V. (1993) · Cell · doi:10.1016/0092-8674(93)90222-c · Cited by 339 · see citing works
Structure-function analysis of the antioxidant properties of haptoglobin
Melamed‐Frank, M., Lache, O., Enav, B. I., Szafranek, T., Levy, N. S., Ricklis, R. M., & Levy, A. P. (2001) · Blood · doi:10.1182/blood.v98.13.3693 · Cited by 339 · see citing works
Disorders of red cell membrane
An, X., & Mohandas, N. (2008) · British Journal of Haematology · doi:10.1111/j.1365-2141.2008.07091.x · Cited by 338 · see citing works
Heme Induces Ubiquitination and Degradation of the Transcription Factor Bach1
Zenke-Kawasaki, Y., Dohi, Y., Katoh, Y., Ikura, T., Ikura, M., Asahara, T., Tokunaga, F., Iwaï, K., & Igarashi, K. (2007) · Molecular and Cellular Biology · doi:10.1128/mcb.02415-06 · Cited by 330 · see citing works
Chung, S. W., Liu, X., Macias, A. A., Baron, R. M., & Perrella, M. A. (2008) · Journal of Clinical Investigation · doi:10.1172/jci32730 · Cited by 325 · see citing works
Zuckerbraun, B. S., Chin, B. Y., Bilban, M., d'Avila, J. D. C., Rao, J., Billiar, T. R., & Otterbein, L. E. (2007) · The FASEB Journal · doi:10.1096/fj.06-6644com · Cited by 323 · see citing works
Peroxiredoxins, Oxidative Stress, and Cell Proliferation
Immenschuh, S., & Baumgart-Vogt, E. (2005) · Antioxidants and Redox Signaling · doi:10.1089/ars.2005.7.768 · Cited by 321 · see citing works
Haem homeostasis is regulated by the conserved and concerted functions of HRG-1 proteins
Rajagopal, A., Rao, A. U., Amigo, J., Tian, M., Upadhyay, S. K., Hall, C., Uhm, S., Mathew, M. K., Fleming, M. D., Paw, B. H., et al. (2008) · Nature · doi:10.1038/nature06934 · Cited by 316 · see citing works
The biochemistry of heme biosynthesis
Heinemann, I. U., Jahn, M., & Jahn, D. (2008) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2008.02.015 · Cited by 311 · see citing works
Regulation of ferritin and heme oxygenase synthesis in rat fibroblasts by different forms of iron.
Eisenstein, R. S., García-Mayol, D., Pettingell, W. H., & Munro, H. N. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.3.688 · Cited by 308 · see citing works
Brouard, S., Berberat, P. O., Tobiasch, E., Seldon, M. P., Bach, F. H., & Soares, M. P. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m108317200 · Cited by 306 · see citing works
Self-citationStromal cell–derived factor 1 promotes angiogenesis via a heme oxygenase 1–dependent mechanism
Deshane, J. S., Chen, S., Caballero, S., Grochot‐Przeczek, A., Waś, H., Calzi, S. L., Lach, R., Hock, T., Chen, B., Hill‐Kapturczak, N., et al. (2007) · The Journal of Experimental Medicine · doi:10.1084/jem.20061609 · Cited by 284 · see citing works
Regulation by Heme of Mitochondrial Protein Transport Through a Conserved Amino Acid Motif
Lathrop, J. T., & Timko, M. P. (1993) · Science · doi:10.1126/science.8424176 · Cited by 282 · see citing works
Carbon monoxide, reactive oxygen signaling, and oxidative stress
Piantadosi, C. A. (2008) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2008.05.013 · Cited by 281 · see citing works
Hemoglobin and heme scavenging
Ascenzi, P., Bocedi, A., Visca, P., Altruda, F., Tolosano, E., Beringhelli, T., & Fasano, M. (2005) · IUBMB Life (International Union of Biochemistry and Molecular Biology: Life) · doi:10.1080/15216540500380871 · Cited by 280 · see citing works
Absence of heme oxygenase‐1 exacerbates atherosclerotic lesion formation and vascular remodeling
Yet, S., Layne, M. D., Liu, X., Chen, Y., Ith, B., Sibinga, N. E. S., & Perrella, M. A. (2003) · The FASEB Journal · doi:10.1096/fj.03-0187fje · Cited by 280 · see citing works
Heme oxygenase-1 affords protection against noncerebral forms of severe malaria
Seixas, E., Gozzelino, R., Chora, Â., Ferreira, A., Silva, G., Larsen, R., Rebelo, S., Penido, C., Smith, N. R., Coutinho, A., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0903419106 · Cited by 275 · see citing works
Self-citationBrain Injury After Intracerebral Hemorrhage: The Role of Thrombin and Iron
Hua, Y., Keep, R. F., Hoff, J. T., & Xi, G. (2007) · Stroke · doi:10.1161/01.str.0000247868.97078.10 · Cited by 273 · see citing works
Heme oxygenase-1: from biology to therapeutic potential
Soares, M. P., & Bach, F. H. (2009) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2008.12.004 · Cited by 257 · see citing works
Self-citationBaker, E. N., Paoli, M., Anderson, B. F., Baker, H. M., Morgan, W. T., & Smith, A. (1999) · Nature Structural Biology · doi:10.1038/13294 · Cited by 249 · see citing works
Salinas, M., Díaz, R. G., Abraham, N. G., de Galarreta, C. M. R., & Cuadrado, A. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m209164200 · Cited by 247 · see citing works
Dealing with iron: Common structural principles in proteins that transport iron and heme
Baker, H. M., Anderson, B. F., & Baker, E. N. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0637295100 · Cited by 243 · see citing works
Öllinger, R., Bilban, M., Erat, A., Froio, A., McDaid, J., Tyagi, S., Csizmadia, E., Graça-Souza, A. V., Liloia, A., Soares, M. P., et al. (2005) · Circulation · doi:10.1161/circulationaha.104.528802 · Cited by 241 · see citing works
Self-citationNecrotic Death Pathway in FAS Receptor Signaling
Matsumura, H., Shimizu, Y., Ohsawa, Y., Kawahara, A., Uchiyama, Y., & Nagata, S. (2000) · The Journal of Cell Biology · doi:10.1083/jcb.151.6.1247 · Cited by 240 · see citing works
Red cell pyruvate kinase deficiency: molecular and clinical aspects
Zanella, A., Fermo, E., Bianchi, P. I., & Valentini, G. (2005) · British Journal of Haematology · doi:10.1111/j.1365-2141.2005.05527.x · Cited by 240 · see citing works
Vercaemst, L. (2008) · Journal of ExtraCorporeal Technology · doi:10.1051/ject/200840257 · Cited by 238 · see citing works
Heme oxygenase: Protective gene or Trojan horse
Platt, J. L., & Nath, K. A. (1998) · Nature Medicine · doi:10.1038/3947 · Cited by 236 · see citing works
The story so far: molecular regulation of the heme oxygenase-1 gene in renal injury
Sikorski, E. M., Hock, T., Hill‐Kapturczak, N., & Agarwal, A. (2004) · American Journal of Physiology-Renal Physiology · doi:10.1152/ajprenal.00297.2003 · Cited by 236 · see citing works
Regulation of reactive oxygen species, DNA damage and c-Myc function by peroxiredoxin 1
Egler, R. A., Fernandes, E. R., Rothermund, K. D., Sereika, S. M., de Souza-Pinto, N. C., Jaruga, P., Dizdaroğlu, M., & Prochownik, E. V. (2005) · Oncogene · doi:10.1038/sj.onc.1208821 · Cited by 231 · see citing works
The effect of hemin on the synthesis of globin
Bruns, G. P., & London, I. M. (1965) · Biochemical and Biophysical Research Communications · doi:10.1016/0006-291x(65)90746-1 · Cited by 229 · see citing works
Chin, B. Y., Jiang, G., Wegiel, B., Wang, H. J., MacDonald, T. Y., Zhang, X., Gallo, D. J., Cszimadia, E., Bach, F. H., Lee, P. J., et al. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0609611104 · Cited by 228 · see citing works
p38α Mitogen-activated Protein Kinase Sensitizes Cells to Apoptosis Induced by Different Stimuli
Porrás, A., Zuluaga, S., Black, E. V. I., Valladares, A., Alvarez, A. M., Ambrosino, C., Benito, M., & Nebreda, Á. R. (2003) · Molecular Biology of the Cell · doi:10.1091/mbc.e03-08-0592 · Cited by 227 · see citing works
Carbon Monoxide Protects against Liver Failure through Nitric Oxide–induced Heme Oxygenase 1
Zuckerbraun, B. S., Billiar, T. R., Otterbein, S. L., Kim, P. K. M., Liu, F., Choi, A. M. K., Bach, F. H., & Otterbein, L. E. (2003) · The Journal of Experimental Medicine · doi:10.1084/jem.20031003 · Cited by 220 · see citing works
Biliverdin administration protects against endotoxin-induced acute lung injury in rats
Sarady, J. K., Liu, F., Gallo, D. J., Nakao, A., Overhaus, M., Öllinger, R., Choi, A. M. K., & Otterbein, L. E. (2005) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00458.2004 · Cited by 220 · see citing works
Alam, J., Camhi, S. L., & Choi, A. M. K. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.20.11977 · Cited by 219 · see citing works
Lee, T., Tsai, H.-L., & Chau, L. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m300498200 · Cited by 211 · see citing works
Stocker, R., & Perrella, M. A. (2006) · Circulation · doi:10.1161/circulationaha.105.598698 · Cited by 209 · see citing works
GBalla, SJacob, H., WEaton, J., DBelcher, J., & MVercellotti, G. (1991) · Arteriosclerosis and Thrombosis A Journal of Vascular Biology · Cited by 209 · see citing works
Berberat, P. O., Katori, M., Kaczmarek, E., Anselmo, D., Lassman, C., Ke, B., Shen, X., Busuttil, R. W., Yamashita, K., Csizmadia, E., et al. (2003) · The FASEB Journal · doi:10.1096/fj.03-0229fje · Cited by 207 · see citing works
Self-citationA central role for free heme in the pathogenesis of severe malaria: the missing link?
Ferreira, A., Balla, J., Jeney, V., Balla, G., & Soares, M. P. (2008) · Journal of Molecular Medicine · doi:10.1007/s00109-008-0368-5 · Cited by 205 · see citing works
Self-citationMyeloid heme oxygenase–1 regulates innate immunity and autoimmunity by modulating IFN-β production
Tzima, S., Victoratos, P., Kranidioti, K., Alexiou, M. V., & Kollias, G. A. (2009) · The Journal of Experimental Medicine · doi:10.1084/jem.20081582 · Cited by 204 · see citing works
Heme Oxygenase: Evolution, Structure, and Mechanism
Wilks, A. (2002) · Antioxidants and Redox Signaling · doi:10.1089/15230860260220102 · Cited by 204 · see citing works
Akamatsu, Y., Haga, M., Tyagi, S., Yamashita, K., Graça-Souza, A. V., Öllinger, R., Czismadia, E., May, G. A., Ifedigbo, E., Otterbein, L. E., et al. (2004) · The FASEB Journal · doi:10.1096/fj.03-0921fje · Cited by 201 · see citing works
Self-citationBussolati, B., Ahmed, A., Pemberton, H. N., Landis, R. C., Carlo, F. D., Haskard, D. O., & Mason, J. C. (2003) · Blood · doi:10.1182/blood-2003-06-1974 · Cited by 199 · see citing works
Zhang, X., Shan, P., Alam, J., Fu, X.-Y., & Lee, P. J. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m408092200 · Cited by 198 · see citing works
Wiesel, P., Patel, A. P., DiFonzo, N., Marria, P. B., Sim, C. U., Pellacani, A. U. E., Maemura, K., LeBlanc, B. W., Marino, K., Doerschuk, C. M., et al. (2000) · Circulation · doi:10.1161/01.cir.102.24.3015 · Cited by 191 · see citing works
Anrather, J., Csizmadia, V., Soares, M. P., & Winkler, H. J. S. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.19.13594 · Cited by 185 · see citing works
Self-citationVercaemst, L. (2008) · PubMed · doi:10.1051/ject/200840257/pdf · Cited by 181 · see citing works
Biliverdin, a natural product of heme catabolism, induces tolerance to cardiac allografts
Yamashita, K., McDaid, J., Öllinger, R., Tsui, T., Berberat, P. O., Usheva, A., Csizmadia, E., Smith, R. N., Soares, M. P., & Bach, F. H. (2004) · The FASEB Journal · doi:10.1096/fj.03-0839fje · Cited by 180 · see citing works
Self-citationKapitulnik, J., & Maines, M. D. (2009) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2008.12.003 · Cited by 178 · see citing works
Kim, K. M., Pae, H., Zheng, M., Park, R., Kim, Y., & Chung, H. (2007) · Circulation Research · doi:10.1161/circresaha.107.154781 · Cited by 178 · see citing works
Maitland, K., Pamba, A., English, M., Peshu, N. M., Marsh, K., Newton, C. R. J. C., & Levin, M. (2005) · Clinical Infectious Diseases · doi:10.1086/427505 · Cited by 174 · see citing works
Toll‐Like Receptor and Heme Oxygenase‐1 Signaling in Hepatic Ischemia/Reperfusion Injury
Shen, X., Ke, B., Zhai, Y., Gao, F., Busuttil, R. W., Cheng, G., & Kupiec‐Weglinski, J. W. (2005) · American Journal of Transplantation · doi:10.1111/j.1600-6143.2005.00932.x · Cited by 171 · see citing works
Kimpara, T., Takeda, A., Watanabe, K., Itoyama, Y., Ikawa, S., Watanabe, M., Arai, H., Sasaki, H., Higuchi, S., Okita, N., et al. (1997) · Human Genetics · doi:10.1007/s004390050480 · Cited by 169 · see citing works
Biliverdin Therapy Protects Rat Livers From Ischemia and Reperfusion Injury
Fondevila, C., Shen, X.-D., Tsuchiyashi, S., Yamashita, K., Csizmadia, E., Lassman, C., Busuttil, R. W., Kupiec‐Weglinski, J. W., & Bach, F. H. (2004) · Hepatology · doi:10.1002/hep.20480 · Cited by 167 · see citing works
Hirai, H., Kubo, H., Yamaya, M., Nakayama, K., Numasaki, M., Kobayashi, S., Suzuki, S., Shibahara, S., & Sasaki, H. (2003) · Blood · doi:10.1182/blood-2002-12-3733 · Cited by 164 · see citing works
The antioxidant defense protein heme oxygenase 1 is a novel target for statins in endothelial cells
Grosser, N., Hemmerle, A., Berndt, G., Erdmann, K., Hinkelmann, U., Schürger, S., Wijayanti, N., Immenschuh, S., & Schröder, H. (2004) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2004.09.009 · Cited by 161 · see citing works
Katori, M., Buelow, R., Ke, B., Ma, J., Coito, A. J., Iyer, S., Southard, D., Busuttil, R. W., & Kupiec‐Weglinski, J. W. (2002) · Transplantation · doi:10.1097/00007890-200201270-00023 · Cited by 157 · see citing works
Carbon Monoxide Orchestrates a Protective Response through PPARγ
Bilban, M., Bach, F. H., Otterbein, S. L., Ifedigbo, E., d’Avila, J. C., Esterbauer, H., Chin, B. Y., Usheva, A., Robson, S. C., Wagner, O. F., et al. (2006) · Immunity · doi:10.1016/j.immuni.2006.03.012 · Cited by 156 · see citing works
Alam, J., Cai, J., & Smith, A. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)42211-3 · Cited by 152 · see citing works
Heme oxygenase-1 induction may explain the antioxidant profile of aspirin
Grosser, N., Abate, A., Oberle, S., Vreman, H. J., Dennery, P. A., Becker, J. C., Pohle, T., Seidman, D. S., & Schröder, H. (2003) · Biochemical and Biophysical Research Communications · doi:10.1016/s0006-291x(03)01504-3 · Cited by 151 · see citing works
Defective Recovery and Severe Renal Damage After Acute Hemolysis in Hemopexin-Deficient Mice
Tolosano, E., Hirsch, E., Patrucco, E., Camaschella, C., Navone, R., Silengo, L., & Altruda, F. (1999) · Blood · doi:10.1182/blood.v94.11.3906 · Cited by 149 · see citing works
Heme Inhibits Human Neutrophil Apoptosis: Involvement of Phosphoinositide 3-Kinase, MAPK, and NF-κB
Arruda, M. A., Rossi, A. G., de Freitas, M. S., Barja‐Fidalgo, C., & Graça-Souza, A. V. (2004) · The Journal of Immunology · doi:10.4049/jimmunol.173.3.2023 · Cited by 147 · see citing works
Wickrema, A., Krantz, S. B., Winkelmann, J., & Bondurant, M. C. (1992) · Blood · doi:10.1182/blood.v80.8.1940.1940 · Cited by 146 · see citing works
Kinetics of hemin distribution in plasma reveals its role in lipoprotein oxidation
Miller, Y. I., & Shaklai, N. (1999) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/s0925-4439(99)00027-7 · Cited by 145 · see citing works
Purification, characterization, and cloning of a heme-binding protein (23 kDa) in rat liver cytosol
Iwahara, S.-I., Satoh, H., Song, D.-X., Webb, J., Burlingame, A. L., Nagae, Y., & Müller‐Eberhard, U. (1995) · Biochemistry · doi:10.1021/bi00041a017 · Cited by 140 · see citing works
Quigley, J. G., Burns, C. C., Anderson, M. M., Lynch, E. D., Sabo, K. M., Overbaugh, J. M., & Abkowitz, J. L. (2000) · Blood · doi:10.1182/blood.v95.3.1093.003k01_1093_1099 · Cited by 139 · see citing works
Therapeutic Applications of Bilirubin and Biliverdin in Transplantation
Öllinger, R., Wang, H., Yamashita, K., Wegiel, B., Thomas, M. N., Margreiter, R., & Bach, F. H. (2007) · Antioxidants and Redox Signaling · doi:10.1089/ars.2007.1807 · Cited by 139 · see citing works
A Mammalian Iron ATPase Induced by Iron
Barañano, D. E., Wolosker, H., Bae, B.-I., Barrow, R. K., Snyder, S. H., & Ferris, C. D. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.275.20.15166 · Cited by 134 · see citing works
Camejo, G., Halberg, C., Manschik-Lundin, A., Hurt‐Camejo, E., Rosengren, B. E., Olsson, H., Hansson, G. I., Forsberg, G., & Ylhen, B. (1998) · Journal of Lipid Research · doi:10.1016/s0022-2275(20)32564-5 · Cited by 134 · see citing works
Modulation of Endothelial Cell Apoptosis by Heme Oxygenase-1-Derived Carbon Monoxide
Soares, M. P., Usheva, A., Brouard, S., Berberat, P. O., Günther, L., Tobiasch, E., & Bach, F. H. (2002) · Antioxidants and Redox Signaling · doi:10.1089/152308602753666370 · Cited by 132 · see citing works
Self-citationSeldon, M. P., Silva, G. P. D. L., Pejanovic, N., Larsen, R., Grégoire, I. P., Filipe, J. C.-R., Anrather, J., & Soares, M. P. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.179.11.7840 · Cited by 132 · see citing works
Self-citationBiliverdin Reductase of Guinea Pig Liver
Singleton, J. W., & Laster, L. (1965) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)97023-7 · Cited by 130 · see citing works
Galonek, H. L., & Hardwick, J. M. (2006) · Nature Cell Biology · doi:10.1038/ncb1206-1317 · Cited by 128 · see citing works
Ke, B., Buelow, R., Shen, X., Melinek, J., Amersi, F. F., Gao, F., Ritter, T., Volk, H., Busuttil, R. W., & Kupiec‐Weglinski, J. W. (2002) · Human Gene Therapy · doi:10.1089/104303402320138970 · Cited by 127 · see citing works
The molecular biology of thrombotic microangiopathy
Tsai, H. (2006) · Kidney International · doi:10.1038/sj.ki.5001535 · Cited by 125 · see citing works
Allhorn, M., Berggård, T., Nordberg, J., Olsson, M. L., & Åkerström, B. (2002) · Blood · doi:10.1182/blood.v99.6.1894 · Cited by 124 · see citing works
Hira, S., Tomita, T., Matsui, T., Igarashi, K., & Ikeda‐Saito, M. (2007) · IUBMB Life · doi:10.1080/15216540701225941 · Cited by 118 · see citing works
Heme oxygenase‐1: a therapeutic amplification funnel
Bach, F. H. (2005) · The FASEB Journal · doi:10.1096/fj.04-3485cmt · Cited by 114 · see citing works
Hamilton, J. W., Bement, W. J., Sinclair, P. R., Sinclair, J. F., Alcedo, J., & Wetterhahn, K. E. (1991) · Archives of Biochemistry and Biophysics · doi:10.1016/0003-9861(91)90428-l · Cited by 114 · see citing works
Recent advances in mammalian haem transport
Latunde-Dada, G. O., Simpson, R. J., & McKie, A. T. (2006) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2006.01.005 · Cited by 113 · see citing works
Induction of heme oxygenase-1 by hypoxia and free radicals in human dermal fibroblasts
Panchenko, M. V., Farber, H. W., & Korn, J. H. (2000) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.2000.278.1.c92 · Cited by 113 · see citing works
Akech, S., Gwer, S., Idro, R., Fegan, G., Eziefula, C., Newton, C. R. J. C., Levin, M., & Maitland, K. (2006) · PLoS Clinical Trials · doi:10.1371/journal.pctr.0010021 · Cited by 112 · see citing works
Heme oxygenase induction mediates the photoimmunoprotective activity of UVA radiation in the mouse
Reeve, V. E., & Tyrrell, R. M. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.16.9317 · Cited by 111 · see citing works
Rapamycin Induces Heme Oxygenase-1 in Human Pulmonary Vascular Cells
Visner, G. A., Lu, F., Zhou, H., Liu, J., Kazemfar, K., & Agarwal, A. (2003) · Circulation · doi:10.1161/01.cir.0000048191.75585.60 · Cited by 110 · see citing works
Protein kinase Akt/PKB phosphorylates heme oxygenase‐1 in vitro and in vivo
Salinas, M., Wang, J., de Sagarra, M. R., Martı́n, D., Rojo, A. I., Martı́n-Pérez, J., de Montellano, P. R. O., & Cuadrado, A. (2004) · FEBS Letters · doi:10.1016/j.febslet.2004.10.077 · Cited by 110 · see citing works
Redox regulation of the transcriptional repressor Bach1
Ishikawa, M., Numazawa, S., & Yoshida, T. (2005) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2005.01.021 · Cited by 109 · see citing works
Hemin-induced necroptosis involves glutathione depletion in mouse astrocytes
Laird, M. D., Wakade, C. G., Alleyne, C. H., & Dhandapani, K. M. (2008) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2008.07.003 · Cited by 108 · see citing works
Wickrema, A., Krantz, S. B., Winkelmann, J., et al. (1992) · Blood · doi:10.1182/blood.v80.8.1940.bloodjournal8081940 · Cited by 108 · see citing works
Maghzal, G. J., Leck, M.-C., Collinson, E. J., Li, C., & Stocker, R. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.037119 · Cited by 106 · see citing works
Transfer of heme from heme-albumin to hemopexin
Morgan, W. T., Liem, H. H., Sutor, R. P., & Müller‐Eberhard, U. (1976) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/0304-4165(76)90387-1 · Cited by 106 · see citing works
Probucol Protects Against Smooth Muscle Cell Proliferation by Upregulating Heme Oxygenase-1
Deng, Y., Wu, B. J., Witting, P. K., & Stocker, R. (2004) · Circulation · doi:10.1161/01.cir.0000142610.10530.25 · Cited by 106 · see citing works
The ABC Transporter Abcg2/Bcrp: Role in Hypoxia Mediated Survival
Krishnamurthy, P. C., & Schuetz, J. D. (2005) · BioMetals · doi:10.1007/s10534-005-3709-7 · Cited by 104 · see citing works
Silva, G. P. D. L., Cunha, A., Grégoire, I. P., Seldon, M. P., & Soares, M. P. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.177.3.1894 · Cited by 103 · see citing works
Self-citationPachori, A. S., Smith, A. M., McDonald, P. H., Zhang, L., Dzau, V. J., & Melo, L. G. (2007) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2007.08.003 · Cited by 103 · see citing works
Exchange of heme among hemoglobin molecules.
Bunn, H. F., & Jandl, J. H. (1966) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.56.3.974 · Cited by 103 · see citing works
Sinha, S., Mishra, S. K., Sharma, S., Patibandla, P. K., Mallick, P. K., Sharma, S. K., Mohanty, S., Pati, S. S., Mishra, S. K., Ramteke, B. K., et al. (2008) · Malaria Journal · doi:10.1186/1475-2875-7-13 · Cited by 100 · see citing works
Biliverdin protects against polymicrobial sepsis by modulating inflammatory mediators
Overhaus, M., Moore, B. A., Barbato, J. E., Behrendt, F. F., Doering, J. G., & Bauer, A. J. (2006) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00152.2005 · Cited by 100 · see citing works
Brunt, K. R., Fenrich, K. K., Kiani, G., Tse, M. Y., Pang, S. C.-N., Ward, C. A., & Melo, L. G. (2006) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.0000236204.37119.8d · Cited by 98 · see citing works
Immunoregulatory effects of HO-1: how does it work?
Soares, M. P., Marguti, I., Cunha, A., & Larsen, R. (2009) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2009.05.008 · Cited by 97 · see citing works
Self-citationLong range interaction of cis‐DNA elements mediated by architectural transcription factor Bach1
Yoshida, C., Tokumasu, F., Hohmura, K. I., Bungert, J., Hayashi, N., Nagasawa, T., Engel, J. D., Yamamoto, M. P., Takeyasu, K., & Igarashi, K. (1999) · Genes to Cells · doi:10.1046/j.1365-2443.1999.00291.x · Cited by 96 · see citing works
Temkin, V., & Karin, M. (2007) · Immunological Reviews · doi:10.1111/j.1600-065x.2007.00560.x · Cited by 96 · see citing works
Anrather, J., Racchumi, G., & Iadecola, C. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m409344200 · Cited by 93 · see citing works
ALI, F., Hamdulay, S., Kinderlerer, A. R., Boyle, J. J., Lidington, E. A., Yamaguchi, T., Soares, M. P., Haskard, D. O., RANDI, A. M., & Mason, J. C. (2007) · Journal of Thrombosis and Haemostasis · doi:10.1111/j.1538-7836.2007.02787.x · Cited by 92 · see citing works
Self-citationCellular Protection Mechanisms against Extracellular Heme
Eskew, J. D., Vanacore, R., Sung, L., Morales, P. J. C., & Smith, A. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.2.638 · Cited by 91 · see citing works
Heme Oxygenases in Pregnancy II: HO‐2 is Downregulated in Human Pathologic Pregnancies
Zenclussen, A. C., Lim, E., Knoeller, S., Knackstedt, M., Hertwig, K., Hagen, E. H., Klapp, B. F., & Arck, P. (2003) · American Journal of Reproductive Immunology · doi:10.1034/j.1600-0897.2003.00047.x · Cited by 91 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Modulation of oxidative stress as an anticancer strategy
Gorrini, C., Harris, I. S., & Mak, T. W. (2013) · Nature Reviews Drug Discovery · doi:10.1038/nrd4002 · Cited by 3,579 · see citing works
Hayes, J. D., Dinkova-Kostova, A. T., & Tew, K. D. (2020) · Cancer Cell · doi:10.1016/j.ccell.2020.06.001 · Cited by 2,654 · see citing works
Łoboda, A., Damulewicz, M., Pyza, E., Józkowicz, A., & Dulak, J. (2016) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-016-2223-0 · Cited by 2,654 · see citing works
Transcriptional Regulation by Nrf2
Tonelli, C., Chio, I. I. C., & Tuveson, D. A. (2017) · Antioxidants and Redox Signaling · doi:10.1089/ars.2017.7342 · Cited by 2,206 · see citing works
Disease Tolerance as a Defense Strategy
Medzhitov, R., Schneider, D. S., & Soares, M. P. (2012) · Science · doi:10.1126/science.1214935 · Cited by 1,718 · see citing works
Self-citationNitric oxide synthase in innate and adaptive immunity: an update
Bogdan, C. (2015) · Trends in Immunology · doi:10.1016/j.it.2015.01.003 · Cited by 862 · see citing works
Signaling to heme oxygenase-1 and its anti-inflammatory therapeutic potential
Paine, A., Eiz‐Vesper, B., Blasczyk, R., & Immenschuh, S. (2010) · Biochemical Pharmacology · doi:10.1016/j.bcp.2010.07.014 · Cited by 698 · see citing works
BACH1 Stabilization by Antioxidants Stimulates Lung Cancer Metastasis
Wiel, C., Le Gal, K., Ibrahim, M. X., Jahangir, C. A., Kashif, M., Yao, H., Ziegler, D. V., Xu, X., Ghosh, T., Mondal, T., et al. (2019) · Cell · doi:10.1016/j.cell.2019.06.005 · Cited by 579 · see citing works
Nrf2 Activation Promotes Lung Cancer Metastasis by Inhibiting the Degradation of Bach1
Lignitto, L., LeBoeuf, S. E., Homer, H., Jiang, S., Askenazi, M., Karakousi, T. R., Pass, H. I., Bhutkar, A. J., Tsirigos, A., Ueberheide, B., et al. (2019) · Cell · doi:10.1016/j.cell.2019.06.003 · Cited by 573 · see citing works
Jaeger, U., Barcellini, W., Broome, C. M., Gertz, M. A., Hill, A., Hill, Q. A., Jilma, B., Kuter, D. J., Michel, M., Montillo, M., et al. (2019) · Blood Reviews · doi:10.1016/j.blre.2019.100648 · Cited by 568 · see citing works
Are Reactive Oxygen Species Always Detrimental to Pathogens?
Paiva, C. N., & Bozza, M. T. (2013) · Antioxidants and Redox Signaling · doi:10.1089/ars.2013.5447 · Cited by 559 · see citing works
Iron homeostasis and iron-regulated ROS in cell death, senescence and human diseases
Nakamura, T., Naguro, I., & Ichijo, H. (2019) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2019.06.010 · Cited by 523 · see citing works
Ayres, J. S., & Schneider, D. S. (2012) · Annual Review of Immunology · doi:10.1146/annurev-immunol-020711-075030 · Cited by 475 · see citing works
A Central Role for Free Heme in the Pathogenesis of Severe Sepsis
Larsen, R., Gozzelino, R., Jeney, V., Tokaji, L., Bozza, F. A., Japiassú, A. M., Bonaparte, D., Cavalcante, M. M., Chora, Â., Ferreira, A., et al. (2010) · Science Translational Medicine · doi:10.1126/scitranslmed.3001118 · Cited by 483 · see citing works
Self-citationA Dual Role of Heme Oxygenase-1 in Cancer Cells
Chiang, S.-K., Chen, S., & Chang, L. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms20010039 · Cited by 466 · see citing works
Heme in pathophysiology: a matter of scavenging, metabolism and trafficking across cell membranes
Chiabrando, D., Vinchi, F., Fiorito, V., Mercurio, S., & Tolosano, E. (2014) · Frontiers in Pharmacology · doi:10.3389/fphar.2014.00061 · Cited by 455 · see citing works
NLRP12-PANoptosome activates PANoptosis and pathology in response to heme and PAMPs
Sundaram, B., Nagakannan, P., Mall, R., Wang, Y., Sarkar, R., Kim, H. J., Malireddi, R. K. S., Karki, R., Janke, L. J., Vogel, P., et al. (2023) · Cell · doi:10.1016/j.cell.2023.05.005 · Cited by 435 · see citing works
Cellular Metabolism and Macrophage Functional Polarization
Zhu, L., Zhao, Q., Yang, T., Ding, W., & Zhao, Y. X. (2014) · International Reviews of Immunology · doi:10.3109/08830185.2014.969421 · Cited by 428 · see citing works
The Concise Guide to PHARMACOLOGY 2013/14: Enzymes
Alexander, S. P. H., Benson, H. E., Faccenda, E., Pawson, A. J., Sharman, J. L., Spedding, M., Peters, J. A., Harmar, A. J., & Collaborators, C. (2013) · British Journal of Pharmacology · doi:10.1111/bph.12451 · Cited by 423 · see citing works
Regulation of inflammation by the antioxidant haem oxygenase 1
Campbell, N. K., Fitzgerald, H. K., & Dunne, A. (2021) · Nature reviews. Immunology · doi:10.1038/s41577-020-00491-x · Cited by 428 · see citing works
Macrophages and Iron Metabolism
Soares, M. P., & Hamza, I. (2016) · Immunity · doi:10.1016/j.immuni.2016.02.016 · Cited by 401 · see citing works
Self-citationDisease tolerance and immunity in host protection against infection
Soares, M. P., Teixeira, L., & Moita, L. F. (2017) · Nature reviews. Immunology · doi:10.1038/nri.2016.136 · Cited by 376 · see citing works
Self-citationLuo, P., Liu, D., Zhang, Q., Yang, F., Wong, Y., Xia, F., Zhang, J., Chen, J., Tian, Y., Yang, C., et al. (2021) · Acta Pharmaceutica Sinica B · doi:10.1016/j.apsb.2021.12.007 · Cited by 388 · see citing works
Targeting heme oxygenase-1 and carbon monoxide for therapeutic modulation of inflammation
Ryter, S. W., & Choi, A. M. K. (2015) · Translational research · doi:10.1016/j.trsl.2015.06.011 · Cited by 363 · see citing works
Kell, D. B. (2010) · Archives of Toxicology · doi:10.1007/s00204-010-0577-x · Cited by 361 · see citing works
Hemolysis-induced lethality involves inflammasome activation by heme
Dutra, F. F., Alves, L. S., Rodrigues, D., Fernandez, P. L., de Oliveira, R. B., Golenbock, D. T., Zamboni, D. S., & Bozza, M. T. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1405023111 · Cited by 353 · see citing works
Heme on innate immunity and inflammation
Dutra, F. F., & Bozza, M. T. (2014) · Frontiers in Pharmacology · doi:10.3389/fphar.2014.00115 · Cited by 355 · see citing works
Sickle Hemoglobin Confers Tolerance to Plasmodium Infection
Ferreira, A., Marguti, I., Bechmann, I., Jeney, V., Chora, Â., Palha, N. R., Rebelo, S., Henri, A., Beuzard, Y., & Soares, M. P. (2011) · Cell · doi:10.1016/j.cell.2011.03.049 · Cited by 340 · see citing works
Self-citationMomen‐Heravi, F., Bala, S., Kodys, K., & Szabó, G. (2015) · Scientific Reports · doi:10.1038/srep09991 · Cited by 348 · see citing works
Tardito, S., Bassanetti, I., Bignardi, C., Elviri, L., Tegoni, M., Mucchino, C., Bussolati, O., Franchi‐Gazzola, R., & Marchiò, L. (2011) · Journal of the American Chemical Society · doi:10.1021/ja109413c · Cited by 325 · see citing works
Iron trafficking and metabolism in macrophages: contribution to the polarized phenotype.
Cairo, G., Recalcati, S., Mantovani, A., & Locati, M. (2011) · Trends in Immunology · doi:10.1016/j.it.2011.03.007 · Cited by 312 · see citing works
The Role of Iron Regulation in Immunometabolism and Immune-Related Disease
Cronin, S. J. F., Woolf, C. J., Weiss, G., & Penninger, J. M. (2019) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2019.00116 · Cited by 299 · see citing works
Evstatiev, R., & Gasché, C. (2011) · Gut · doi:10.1136/gut.2010.214312 · Cited by 292 · see citing works
Krifka, S., Spagnuolo, G., Schmalz, G., & Schweikl, H. (2013) · Biomaterials · doi:10.1016/j.biomaterials.2013.03.019 · Cited by 289 · see citing works
Heme Oxygenase-1 Signaling and Redox Homeostasis in Physiopathological Conditions
Consoli, V., Sorrenti, V., Grosso, S., & Vanella, L. (2021) · Biomolecules · doi:10.3390/biom11040589 · Cited by 288 · see citing works
Reinisalo, M., Kårlund, A., Koskela, A. K. J., Kaarniranta, K., & Karjalainen, R. (2015) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2015/340520 · Cited by 285 · see citing works
ATF4-dependent induction of heme oxygenase 1 prevents anoikis and promotes metastasis
Dey, S., Sayers, C. M., Verginadis, I. I., Lehman, S. L., Cheng, Y., Cerniglia, G. J., Tuttle, S. W., Feldman, M. D., Zhang, P. J. L., Fuchs, S. Y., et al. (2015) · Journal of Clinical Investigation · doi:10.1172/jci78031 · Cited by 282 · see citing works
Endale, M., Park, S., Kim, S., Kim, S., Yang, Y., Cho, J. Y., & Rhee, M. H. (2013) · Immunobiology · doi:10.1016/j.imbio.2013.04.019 · Cited by 282 · see citing works
Vinchi, F., Costa da Silva, M., Ingoglia, G., Petrillo, S., Brinkman, N., Zuercher, A., Cerwenka, A., Tolosano, E., & Muckenthaler, M. U. (2016) · Blood · doi:10.1182/blood-2015-08-663245 · Cited by 269 · see citing works
Oxidative stress and the role of redox signalling in chronic kidney disease
Kishi, S., Nagasu, H., Kidokoro, K., & Kashihara, N. (2023) · Nature Reviews Nephrology · doi:10.1038/s41581-023-00775-0 · Cited by 283 · see citing works
Broekgaarden, M., Weijer, R., van Gulik, T. M., Hamblin, M. R., & Heger, M. (2015) · Cancer and Metastasis Reviews · doi:10.1007/s10555-015-9588-7 · Cited by 261 · see citing works
Regulation of mitochondrial biogenesis and PGC-1α under cellular stress
Wenz, T. (2013) · Mitochondrion · doi:10.1016/j.mito.2013.01.006 · Cited by 259 · see citing works
Heme induces programmed necrosis on macrophages through autocrine TNF and ROS production
Fortes, G. B., Alves, L. S., de Oliveira, R., Dutra, F. F., Rodrigues, D., Fernandez, P. L., Souto-Padron, T., De Rosa, M. J., Kelliher, M., Golenbock, D., et al. (2012) · Blood · doi:10.1182/blood-2011-08-375303 · Cited by 246 · see citing works
Piantadosi, C. A., Withers, C. M., Bartz, R. R., MacGarvey, N. C., Fu, P. P., Sweeney, T. E., Welty‐Wolf, K. E., & Suliman, H. B. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.207738 · Cited by 250 · see citing works
Hypoxia and Inflammation: Insights From High-Altitude Physiology
Pham, K., Parikh, K. D., & Heinrich, E. C. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.676782 · Cited by 250 · see citing works
Oxidative Stress and the Homeodynamics of Iron Metabolism
Bresgen, N., & Eckl, P. (2015) · Biomolecules · doi:10.3390/biom5020808 · Cited by 247 · see citing works
Yun, N., Kang, J., & Lee, S. (2011) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2011.06.018 · Cited by 239 · see citing works
Vinchi, F., Franceschi, L. D., Ghigo, A., Townes, T. M., Cimino, J. J., Silengo, L., Hirsch, E., Altruda, F., & Tolosano, E. (2013) · Circulation · doi:10.1161/circulationaha.112.130179 · Cited by 233 · see citing works
Cunnington, A. J., de Souza, J. B., Walther, M., & Riley, E. M. (2012) · Nature Medicine · doi:10.1038/nm.2601 · Cited by 231 · see citing works
The Iron age of host–microbe interactions
Soares, M. P., & Weiss, G. (2015) · The EMBO Reports · doi:10.15252/embr.201540558 · Cited by 227 · see citing works
Self-citationNLRC5 senses NAD+ depletion, forming a PANoptosome and driving PANoptosis and inflammation
Sundaram, B., Nagakannan, P., Kim, H. J., Abdelaal, H. M., Mall, R., Indari, O., Sarkar, R., Tweedell, R. E., Alonzo, E. Q., Klein, J. D., et al. (2024) · Cell · doi:10.1016/j.cell.2024.05.034 · Cited by 232 · see citing works
HO-1 Induction in Cancer Progression: A Matter of Cell Adaptation
Nitti, M., Piras, S., Marinari, U. M., Moretta, L., Pronzato, M. A., & Furfaro, A. L. (2017) · Antioxidants · doi:10.3390/antiox6020029 · Cited by 222 · see citing works
Kim, Y., Pae, H., Park, J. E., Lee, Y. C., Woo, J. M., Kim, N., Choi, Y. K., Lee, B.-S., Kim, S. R., & Chung, H. (2010) · Antioxidants and Redox Signaling · doi:10.1089/ars.2010.3153 · Cited by 222 · see citing works
HCV and Oxidative Stress in the Liver
Ivanov, A. V., Bartosch, B., Smirnova, O. A., Isaguliants, M. G., & Kochetkov, S. N. (2013) · Viruses · doi:10.3390/v5020439 · Cited by 220 · see citing works
Pro-inflammatory Actions of Heme and Other Hemoglobin-Derived DAMPs
Bozza, M. T., & Jeney, V. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.01323 · Cited by 205 · see citing works
Self-citationIron Regulation: Macrophages in Control
Sukhbaatar, N., & Weichhart, T. (2018) · Pharmaceuticals · doi:10.3390/ph11040137 · Cited by 201 · see citing works
Single cell analysis of M. tuberculosis phenotype and macrophage lineages in the infected lung
Pisu, D., Huang, L., Narang, V., Theriault, M. E., Lê-Bury, G., Lee, B. T. K., Lakudzala, A. E., Mzinza, D. T., Mhango, D. V., Mitini-Nkhoma, S. C., et al. (2021) · The Journal of Experimental Medicine · doi:10.1084/jem.20210615 · Cited by 193 · see citing works
Parada, E., Egea, J., Buendía, I., Negredo, P., Cunha, A. C., Cardoso, S., Soares, M. P., & López, M. G. (2013) · Antioxidants and Redox Signaling · doi:10.1089/ars.2012.4671 · Cited by 203 · see citing works
Self-citationTherapeutic Potential of Cannabidiol (CBD) for Skin Health and Disorders
Baswan, S. M., Klosner, A. E., Glynn, K. M., Rajgopal, A., Malik, K. A., Yim, S., & Stern, N. (2020) · Clinical Cosmetic and Investigational Dermatology · doi:10.2147/ccid.s286411 · Cited by 194 · see citing works
Advances in predictive in vitro models of drug-induced nephrotoxicity
Soo, J. Y.-C., Jansen, J., Masereeuw, R., & Little, M. H. (2018) · Nature Reviews Nephrology · doi:10.1038/s41581-018-0003-9 · Cited by 191 · see citing works
Tissue damage control in disease tolerance
Soares, M. P., Gozzelino, R., & Weis, S. (2014) · Trends in Immunology · doi:10.1016/j.it.2014.08.001 · Cited by 187 · see citing works
Self-citationŁoboda, A., Józkowicz, A., & Dulak, J. (2015) · Vascular Pharmacology · doi:10.1016/j.vph.2015.09.004 · Cited by 186 · see citing works
Fang, J., Yang, J., Wu, X., Zhang, G., Li, T., Wang, X., Zhang, H., Wang, C., Liu, G., & Wang, L. (2018) · Aging Cell · doi:10.1111/acel.12765 · Cited by 179 · see citing works
Bach2 maintains T cells in a naive state by suppressing effector memory-related genes
Tsukumo, S.-I., Unno, M., Muto, A., Takeuchi, A., Kometani, K., Kurosaki, T., Igarashi, K., & Saito, T. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1306691110 · Cited by 168 · see citing works
Cannabidiol induces antioxidant pathways in keratinocytes by targeting BACH1
Casares, L., García, V., Garrido‐Rodríguez, M., Millán, E., Collado, J. A., García‐Martín, A., Peñarando, J., Calzado, M. A., de la Vega, L., & Muñóz, E. (2019) · Redox Biology · doi:10.1016/j.redox.2019.101321 · Cited by 174 · see citing works
Stappen, C. V., Deng, Y., Liu, Y., Heidari, H., Wang, J., Zhou, Y., Ledray, A. P., & Lu, Y. (2022) · Chemical Reviews · doi:10.1021/acs.chemrev.2c00106 · Cited by 178 · see citing works
The Influence of Parasite Infections on Host Immunity to Co-infection With Other Pathogens
Mabbott, N. A. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.02579 · Cited by 173 · see citing works
Atherogenesis and iron: from epidemiology to cellular level
Vinchi, F., Muckenthaler, M. U., da Silva, M. C., Balla, G. J., Balla, J., & Jeney, V. (2014) · Frontiers in Pharmacology · doi:10.3389/fphar.2014.00094 · Cited by 173 · see citing works
Self-citationOxidative stress fuels Trypanosoma cruzi infection in mice
Paiva, C. N., Feijó, D. F., Dutra, F. F., Carneiro, V. C., de Freitas, G. B., Alves, L. S., Mesquita, J. S., Fortes, G. B., Figueiredo, R. T., de Souza, H. S. P., et al. (2012) · Journal of Clinical Investigation · doi:10.1172/jci58525 · Cited by 169 · see citing works
Hebbel, R. P. (2010) · American Journal of Hematology · doi:10.1002/ajh.21952 · Cited by 167 · see citing works
Curcumin exerts a protective effect against premature ovarian failure in mice
Yan, Z., Dai, Y., Fu, H., Zheng, Y., Bao, D., Yin, Y., Chen, Q., Nie, X., Hao, Q., Hou, D., et al. (2018) · Journal of Molecular Endocrinology · doi:10.1530/jme-17-0214 · Cited by 164 · see citing works
Innate immunity to intracellular pathogens: macrophage receptors and responses to microbial entry
Plüddemann, A., Mukhopadhyay, S., & Gordon, S. (2011) · Immunological Reviews · doi:10.1111/j.1600-065x.2010.00989.x · Cited by 162 · see citing works
Nitti, M., Piras, S., Brondolo, L., Marinari, U. M., Pronzato, M. A., & Furfaro, A. L. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19082260 · Cited by 161 · see citing works
Effect of curcumin on glycerol-induced acute kidney injury in rats
Wu, J., Pan, X., Fu, H., Zheng, Y., Dai, Y., Yin, Y., Chen, Q., Hao, Q., Bao, D., & Hou, D. (2017) · Scientific Reports · doi:10.1038/s41598-017-10693-4 · Cited by 160 · see citing works
Wu, Q., Wang, Y., Senitko, M., Meyer, C. J., Wigley, W. C., Ferguson, D. A., Grossman, E. B., Chen, J., Zhou, X. J., Hartono, J. R., et al. (2011) · American Journal of Physiology-Renal Physiology · doi:10.1152/ajprenal.00353.2010 · Cited by 158 · see citing works
Disease Tolerance as an Inherent Component of Immunity
Martins, R., Carlos, A. R., Braza, F., Thompson, J. A., Bastos-Amador, P., Ramos, S., & Soares, M. P. (2019) · Annual Review of Immunology · doi:10.1146/annurev-immunol-042718-041739 · Cited by 149 · see citing works
Self-citationRed alert: labile heme is an alarmin
Soares, M. P., & Bozza, M. T. (2016) · Current Opinion in Immunology · doi:10.1016/j.coi.2015.11.006 · Cited by 148 · see citing works
Self-citationOnda, K., Tong, S., Beard, S., Binder, N. K., Muto, M., Senadheera, S. N., Parry, L. J., Dilworth, M., Renshall, L., Brownfoot, F., et al. (2017) · Hypertension · doi:10.1161/hypertensionaha.116.08408 · Cited by 154 · see citing works
Opzoomer, J. W., Sosnowska, D., Anstee, J. E., Spicer, J. F., & Arnold, J. N. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.01654 · Cited by 150 · see citing works
Coupling Heme and Iron Metabolism <i>via</i> Ferritin H Chain
Gozzelino, R., & Soares, M. P. (2014) · Antioxidants & Redox Signaling · doi:10.1089/ars.2013.5666 · Cited by 151 · see citing works
Self-citationHeme drives hemolysis-induced susceptibility to infection via disruption of phagocyte functions
Martins, R., Maier, J., Gorki, A.-D., Huber, K. V. M., Sharif, O., Starkl, P., Saluzzo, S., Quattrone, F., Gawish, R., Lakovits, K., et al. (2016) · Nature Immunology · doi:10.1038/ni.3590 · Cited by 142 · see citing works
Heme: Modulator of Plasma Systems in Hemolytic Diseases
Roumenina, L. T., Rayes, J., Lacroix‐Desmazes, S., & Dimitrov, J. D. (2016) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2016.01.004 · Cited by 149 · see citing works
Fractalkine activates NRF2/NFE2L2 and heme oxygenase 1 to restrain tauopathy-induced microgliosis
Lastres-Becker, I., Innamorato, N. G., Jaworski, T., Rábano, A., Kügler, S., Van Leuven, F., & Cuadrado, A. (2014) · Brain · doi:10.1093/brain/awt323 · Cited by 160 · see citing works
Wei, Y., Gong, J., Yoshida, T., Eberhart, C. G., Xu, Z., Kombairaju, P., Sporn, M. B., Handa, J. T., & Duh, E. J. (2011) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2011.04.026 · Cited by 143 · see citing works
Heme Oxygenase 1 as a Therapeutic Target in Acute Kidney Injury
Bolisetty, S., Zarjou, A., & Agarwal, A. (2017) · American Journal of Kidney Diseases · doi:10.1053/j.ajkd.2016.10.037 · Cited by 143 · see citing works
Hemoglobin-based oxygen carriers: from mechanisms of toxicity and clearance to rational drug design
Buehler, P. W., D’Agnillo, F., & Schaer, D. J. (2010) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2010.07.006 · Cited by 142 · see citing works
Al‐Megrin, W. A. I., ALKHURIJI, A. F., Yousef, A. O. S., Metwally, D. M., Habotta, O. A., Kassab, R. B., Moneim, A. E. A., & El‐Khadragy, M. F. (2019) · Antioxidants · doi:10.3390/antiox9010010 · Cited by 138 · see citing works
Free hemoglobin concentration in severe sepsis: methods of measurement and prediction of outcome
Adamzik, M., Hamburger, T., Petrat, F., Peters, J., de Groot, H., & Hartmann, M. (2012) · Critical Care · doi:10.1186/cc11425 · Cited by 137 · see citing works
Heme Oxygenase-1 in Kidney Health and Disease
Lever, J. M., Boddu, R., George, J. F., & Agarwal, A. (2016) · Antioxidants and Redox Signaling · doi:10.1089/ars.2016.6659 · Cited by 134 · see citing works
Macrophages are exploited from an innate wound healing response to facilitate cancer metastasis
Muliaditan, T., Caron, J., Okesola, M., Opzoomer, J. W., Kosti, P., Georgouli, M., Gordon, P., Lall, S. K., Kuzeva, D. M., Pedro, L., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-05346-7 · Cited by 133 · see citing works
A Review on Hemeoxygenase-2: Focus on Cellular Protection and Oxygen Response
Muñoz‐Sánchez, J., & Chánez‐Cárdenas, M. E. (2014) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2014/604981 · Cited by 132 · see citing works
IL-22 controls iron-dependent nutritional immunity against systemic bacterial infections
Sakamoto, K., Kim, Y.-G., Hara, H., Kamada, N., Caballero-Flores, G., Tolosano, E., Soares, M. P., Puente, J. L., Inohara, N., & Núñez, G. (2017) · Science Immunology · doi:10.1126/sciimmunol.aai8371 · Cited by 127 · see citing works
Self-citationActivation of necroptosis in human and experimental cholestasis
Afonso, M. B., Rodrigues, P., Simão, A., Ofengeim, D., Carvalho, T., Amaral, J. D., Gaspar, M. M., Cortez-Pinto, H., Castro, R., Yuan, J., et al. (2016) · Cell Death and Disease · doi:10.1038/cddis.2016.280 · Cited by 126 · see citing works
Heme as a Target for Therapeutic Interventions
Immenschuh, S., Vijayan, V., Janciauskiene, S. M., & Gueler, F. (2017) · Frontiers in Pharmacology · doi:10.3389/fphar.2017.00146 · Cited by 130 · see citing works
Barone, E., Di Domenico, F., Mancuso, C., & Butterfield, D. A. (2014) · Neurobiology of Disease · doi:10.1016/j.nbd.2013.09.018 · Cited by 127 · see citing works
Guan, S., Tee, W. S. N., Ng, D. S. W., Chan, T., Peh, H. Y., Ho, W. E., Cheng, C., Mak, J., & Wong, W. S. F. (2012) · British Journal of Pharmacology · doi:10.1111/bph.12054 · Cited by 129 · see citing works
The role of vitamin C in stress-related disorders
Moritz, B., Schmitz, A. E., Rodrigues, A. L. S., Dafré, A. L., & Cunha, M. P. (2020) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2020.108459 · Cited by 133 · see citing works
A cell membrane-anchored fluorescent probe for monitoring carbon monoxide release from living cells
Xu, S., Liu, H., Yin, X., Yuan, L., Huan, S., & Zhang, X. (2018) · Chemical Science · doi:10.1039/c8sc03584a · Cited by 125 · see citing works
Iron and innate antimicrobial immunity-depriving the pathogen, defending the host
Nairz, M., Dichtl, S., Schroll, A., Haschka, D., Tymoszuk, P., Theurl, I., & Weiss, G. (2018) · Journal of Trace Elements in Medicine and Biology · doi:10.1016/j.jtemb.2018.03.007 · Cited by 123 · see citing works
A Quantitative Approach to Screen for Nephrotoxic Compounds In Vitro
Adler, M., Ramm, S., Hafner, M. A., Muhlich, J. L., Gottwald, E. M., Weber, E. J., Jaklic, A., Ajay, A. K., Svoboda, D. L., Auerbach, S. S., et al. (2015) · Journal of the American Society of Nephrology · doi:10.1681/asn.2015010060 · Cited by 124 · see citing works
- Authors
- Gozzelino, R., Jeney, V., & Soares, M. P.
- Affiliations
- Instituto Gulbenkian de Ciência (PT)
- Instituto Gulbenkian de Ciência, Oeiras, Portugal;
- Venue
- Annual Review of Pharmacology and Toxicology
- Publisher
- Annual Reviews
- Published
- 2010-02-01
- Volume
- 50
- Issue
- 1
- Pages
- 323-354
- ISSN
- 0362-1642 (ISSN-L)
- 1545-4304
- OpenAlex
- W2162853795
- Cited by
- 1,241
- References
- 237
- Citations by year
- 2026: 66 · 2025: 61 · 2024: 55 · 2023: 72 · 2022: 92 · 2021: 114 · 2020: 101 · 2019: 60 · 2018: 87 · 2017: 75 · 2016: 65 · 2015: 99 · 2014: 77 · 2013: 69 · 2012: 74
- FWCI
- 6.01
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The Annual Review of Pharmacology and Toxicology (publishedVersion)
- PubMed (publishedVersion)
- University of Debrecen Electronic Archive (University of Debrecen) (submittedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Heme Oxygenase-1 and Carbon Monoxide
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Hemoglobin structure and function
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Porphyrin Metabolism and Disorders
- Keywords
- heme oxygenase-1, heme degradation, carbon monoxide, biliverdin, bilirubin, programmed cell death, cytoprotection, immune-mediated inflammatory diseases, stress response
- MeSH terms
- Animals, Biliverdine, Carbon Monoxide, Heme, Humans, Inflammation, Tumor Necrosis Factor-alpha, Gene Expression Regulation, Enzymologic, Apoptosis, Cytoprotection, Heme Oxygenase-1
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
