Macrophages and Iron Metabolism

Soares, Miguel P.; Hamza, Iqbal

doi:10.1016/j.immuni.2016.02.016

Cited by 403Iron Metabolism and DisordersImmune cells in cancerHemoglobin structure and function

Macrophages and Iron Metabolism

Open access

Soares, Miguel P., Hamza, Iqbal·2016·Immunity

DOI 10.1016/j.immuni.2016.02.016PMC PMC4794998

Open this paper in CoChat — free account Open PDF

Abstract

Iron is a transition metal that due to its inherent ability to exchange electrons with a variety of molecules is essential to support life. In mammals, iron exists mostly in the form of heme, enclosed within an organic protoporphyrin ring and functioning primarily as a prosthetic group in proteins. Paradoxically, free iron also has the potential to become cytotoxic when electron exchange with oxygen is unrestricted and catalyzes the production of reactive oxygen species. These biological properties demand that iron metabolism is tightly regulated such that iron is available for core biological functions while preventing its cytotoxic effects. Macrophages play a central role in establishing this delicate balance. Here, we review the impact of macrophages on heme-iron metabolism and, reciprocally, how heme-iron modulates macrophage function.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Integrity signals

Registry

Crossref · 10.1016/j.immuni.2016.02.016

Cites

150 of 150 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

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?

Macrophages play a central role in iron metabolism, including heme-iron turnover in senescent red blood cells, hepcidin regulation and lipocalin system.
“Macrophage plays a central role in iron metabolism, including heme-iron turnover in senescent red blood cells, hepcidin regulation and lipocalin system [68].”
From Asbestos conceives Fe(II)-dependent mutagenic stromal milieu through ceaseless macrophage ferroptosis and β-catenin induction in mesothelium (2020) · cites this paper as [68]
The Abstract and “Macrophage regulation of heme-iron homeostasis” section describe macrophages’ central role in iron metabolism and their recycling of iron from senescent red blood cells. “Macrophage heme-iron metabolism and resistance to infection” also links macrophage iron export to LCN2 (lipocalin 2). But it says hepatocytes secrete hepcidin, which then suppresses iron export from macrophages; it does not support macrophages regulating hepcidin itself. Page numbers are unavailable in our copy. (LLM, conf=0.84)
Experimental — accuracy not yet measured
Degradation of Bach1 induces expression of SpiC independently of Nrf2.
“Second, the degradation of Bach1 induces expression of the transcription factor (an E26 transformation-specific transcription factor of the Spi subfamily) SpiC independently of Nrf2 [116, 211].”
From “Pumping iron”—how macrophages handle iron at the systemic, microenvironmental, and cellular levels (2017) · cites this paper as [211]
Iron in red blood cell hemoglobin is recycled mainly by erythrophagocytic macrophages in the splenic red pulp engulfing and digesting senescent or damaged red blood cells.
“This is circumvented by the recycling of the Fe contained in the heme groups of Hb inside RBC (14–16), achieved largely via the continuous engulfment and digestion of senescent or damaged RBC by erythrophagocytic macrophages (EM) in the red pulp of the spleen (15) (Figure 1).”
From Innate Nutritional Immunity (2018) · cites this paper as [15]
This recycling extracts heme iron and sends it to bone marrow for erythropoiesis, where iron is inserted into nascent hemoglobin.
“This process allows for the Fe contained in the heme groups of Hb to be extracted and directed into the bone marrow to support erythropoiesis, where Fe is inserted in the last step of heme biosynthesis and incorporated into nascent Hb (15) (Figure 1).”
From Innate Nutritional Immunity (2018) · cites this paper as [15]
Pathogen sensing through PRRs also promotes innate immune resistance mechanisms that withhold heme-iron from pathogens.
“In addition, pathogen sensing via PRRs promotes resistance mechanisms in innate immune cells, which withhold heme-Fe from pathogens (15) (Figure 3).”
From Innate Nutritional Immunity (2018) · cites this paper as [15]

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Ferroptosis: An Iron-Dependent Form of Nonapoptotic Cell Death
Dixon, S. J., Lemberg, K. M., Lamprecht, M. R., Skouta, R., Zaitsev, E. M., Gleason, C. E., Patel, D. N., Bauer, A. J., Cantley, A. M., Yang, W. S., et al. (2012) · Cell · doi:10.1016/j.cell.2012.03.042 · Cited by 18,691 · see citing works
Innate immune recognition
Janeway, C. A., & Medzhitov, R. (2002) · Annual Review of Immunology · doi:10.1146/annurev.immunol.20.083001.084359 · Cited by 8,394 · see citing works
The NOX Family of ROS-Generating NADPH Oxidases: Physiology and Pathophysiology
Bedard, K., & Krause, K.-H. (2007) · Physiological Reviews · doi:10.1152/physrev.00044.2005 · Cited by 6,989 · see citing works
Origin and physiological roles of inflammation
Medzhitov, R. (2008) · Nature · doi:10.1038/nature07201 · Cited by 6,618 · see citing works
Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and ugly
Beckman, J. S., & Koppenol, W. H. (1996) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.1996.271.5.c1424 · Cited by 5,513 · see citing works
Macrophage biology in development, homeostasis and disease
Wynn, T. A., Chawla, A., & Pollard, J. W. (2013) · Nature · doi:10.1038/nature12034 · Cited by 4,684 · cited 2× · see citing works
“However, intracellular iron also downregulates NOS2 transcription in response to IFN-g (Weiss et al., 1992) via a mechanism involving STAT inhibition (Xie et al., 1994).”
Background
Hypoxia-inducible factors in physiology and medicine
Semenza, G. L. (2012) · Cell · doi:10.1016/j.cell.2012.01.021 · Cited by 3,645 · see citing works
Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain
Itoh, K., Wakabayashi, N., Katoh, Y., Ishii, T., Igarashi, K., Engel, J. D., & Yamamoto, M. (1999) · Genes & Development · doi:10.1101/gad.13.1.76 · Cited by 3,634 · see citing works
Cell Survival Responses to Environmental Stresses Via the Keap1-Nrf2-ARE Pathway
Kensler, T. W., Wakabayashi, N., & Biswal, S. (2007) · Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev.pharmtox.46.120604.141046 · Cited by 3,630 · see citing works
Targeting the KEAP1-NRF2 system to prevent kidney disease progression
Nezu, M., Suzuki, N., & Yamamoto, M. (2017) · American Journal of Nephrology · doi:10.1159/000475890 · Cited by 3,447 · see citing works
Nitric oxide synthases: Roles, tolls, and controls
Nathan, C., & Xie, Q. W. (1994) · Cell · doi:10.1016/0092-8674(94)90266-6 · Cited by 2,920 · 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
Transcriptional Profiling of the Human Monocyte-to-Macrophage Differentiation and Polarization: New Molecules and Patterns of Gene Expression
Martínez, F. O., Gordon, S., Locati, M., & Mantovani, A. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.177.10.7303 · Cited by 2,336 · see citing works
Transcriptional regulation of macrophage polarization: enabling diversity with identity
Lawrence, T., & Natoli, G. (2011) · Nature Reviews Immunology · doi:10.1038/nri3088 · Cited by 2,284 · see citing works
mTOR- and HIF-1α–mediated aerobic glycolysis as metabolic basis for trained immunity
Cheng, S.-C., Quintin, J., Cramer, R. A., Shepardson, K. M., Saeed, S., Kumar, V., Giamarellos-Bourboulis, E. J., Martens, J. H. A., Rao, N. A., Aghajanirefah, A., et al. (2014) · Science · doi:10.1126/science.1250684 · Cited by 2,224 · see citing works
Role of transcription factor NF-kappa B/Rel in induction of nitric oxide synthase.
Xie, Q. W., Kashiwabara, Y., & Nathan, C. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)37600-7 · Cited by 2,212 · cited 7× · see citing works
“Nrf2 activation triggers the transcription of genes involved in the regulation of cellular heme-iron metabolism, such as HMOX1 (Alam et al., Immunity 44, March 15, 2016 ª2016 Elsevier Inc. 495 ARE Bach1 sMaf Bach1Ub Ub Ub Hoil Heme Heme 26S Proteasome HIF1α PHD2 HIF1α Ub Ub Ub Cul2 VHL HIF1α HRE Iron pO2 26S Proteasom…”
BackgroundInfluential
The Nrf2 regulatory network provides an interface between redox and intermediary metabolism
Hayes, J. D., & Dinkova‐Kostova, A. T. (2014) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2014.02.002 · Cited by 2,158 · see citing works
Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway
Otterbein, L. E., Bach, F. H., Alam, J., Soares, M., Tao Lu, H., Wysk, M., Davis, R. J., Flavell, R. A., & Choi, A. M. K. (2000) · Nature Medicine · doi:10.1038/74680 · Cited by 2,153 · see citing works
Self-citation
Tissue-resident macrophages
Davies, L. C., Jenkins, S. J., Allen, J. E., & Taylor, P. R. (2013) · Nature Immunology · doi:10.1038/ni.2705 · Cited by 2,096 · see citing works
Quantitative proteomics identifies NCOA4 as the cargo receptor mediating ferritinophagy
Mancias, J. D., Wang, X., Gygi, S. P., Harper, J. W., & Kimmelman, A. C. (2014) · Nature · doi:10.1038/nature13148 · Cited by 2,084 · see citing works
HIF-1α is essential for myeloid cell-mediated inflammation
Cramer, T., Yamanishi, Y., Clausen, B. E., Förster, I., Pawlinski, R., Mackman, N., Haase, V. H., Jaenisch, R., Corr, M., Nizet, V., et al. (2003) · Cell · doi:10.1016/s0092-8674(03)00154-5 · Cited by 2,046 · see citing works
Gene-expression profiles and transcriptional regulatory pathways that underlie the identity and diversity of mouse tissue macrophages
the Immunological Genome Consortium, Gautier, E. L., Shay, T., Miller, J., Greter, M., Jakubzick, C., Ivanov, S., Helft, J., Chow, A., Elpek, K. G., et al. (2012) · Nature Immunology · doi:10.1038/ni.2419 · Cited by 1,972 · cited 12× · see citing works
“Heme inducesmonocyte differentiation into the erythrophagocytic macrophage lineage via activation of a signal transduction pathway releasing Bach1 and allowing the activation of SPI-C Immunity 44, March 15, 2016 ª2016 Elsevier Inc. 497 (Haldar et al., 2014; Kohyama et al., 2009).”
BackgroundInfluential
Lipocalin 2 mediates an innate immune response to bacterial infection by sequestrating iron
Flo, T. H., Smith, K. D., Sato, S., Rodriguez, D. J., Holmes, M. A., Strong, R. K., Akira, S., & Aderem, A. (2004) · Nature · doi:10.1038/nature03104 · Cited by 1,877 · see citing works
Metabolic reprogramming in macrophages and dendritic cells in innate immunity
Kelly, B., & O'Neill, L. A. (2015) · Cell Research · doi:10.1038/cr.2015.68 · Cited by 1,876 · 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-citation
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
NF-κB links innate immunity to the hypoxic response through transcriptional regulation of HIF-1α
Rius, J., Guma, M., Schachtrup, C., Akassoglou, K., Zinkernagel, A. S., Nizet, V., Johnson, R. S., Haddad, G. G., & Karin, M. (2008) · Nature · doi:10.1038/nature06905 · Cited by 1,614 · see citing works
Reactive oxygen and nitrogen intermediates in the relationship between mammalian hosts and microbial pathogens
Nathan, C., & Shiloh, M. U. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.16.8841 · Cited by 1,469 · see citing works
Hepcidin, a putative mediator of anemia of inflammation, is a type II acute-phase protein
Nemeth, E., Valore, E. V., Territo, M., Schiller, G., Lichtenstein, A., & Ganz, T. (2003) · Blood · doi:10.1182/blood-2002-10-3235 · Cited by 1,417 · 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
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
Mechanisms of Cell Protection by Heme Oxygenase-1
Gozzelino, R., Jeney, V., & Soares, M. P. (2010) · Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev.pharmtox.010909.105600 · Cited by 1,241 · see citing works
Self-citation
Iron in infection and immunity
Cassat, J. E., & Skaar, E. P. (2013) · Cell Host & Microbe · doi:10.1016/j.chom.2013.04.010 · Cited by 1,214 · see citing works
Homeostasis, Inflammation, and Disease Susceptibility
Kotas, M. E., & Medzhitov, R. (2015) · Cell · doi:10.1016/j.cell.2015.02.010 · Cited by 1,213 · see citing works
Indoleamine 2,3 dioxygenase and metabolic control of immune responses
Munn, D. H., & Mellor, A. L. (2013) · Trends in Immunology · doi:10.1016/j.it.2012.10.001 · Cited by 1,037 · see citing works
Nrf2 is a critical regulator of the innate immune response and survival during experimental sepsis
Thimmulappa, R. K. (2006) · Journal of Clinical Investigation · doi:10.1172/jci25790 · Cited by 1,028 · 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
Heme oxygenase 1 is required for mammalian iron reutilization
Poss, K. D., & Tonegawa, S. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.20.10919 · Cited by 1,016 · 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-citation
The aryl hydrocarbon receptor: multitasking in the immune system
Stockinger, B., Meglio, P. D., Gialitakis, M., & Duarte, J. H. (2014) · Annual Review of Immunology · doi:10.1146/annurev-immunol-032713-120245 · Cited by 909 · see citing works
Iron homeostasis in host defence and inflammation
Ganz, T., & Nemeth, E. (2015) · Nature Reviews Immunology · doi:10.1038/nri3863 · Cited by 843 · see citing works
Systems biology approaches identify ATF3 as a negative regulator of Toll-like receptor 4
Gilchrist, M., Thórsson, V., Li, B., Rust, A. G., Korb, M., Kennedy, K., Hai, T., Bolouri, H., & Aderem, A. A. (2006) · Nature · doi:10.1038/nature04768 · Cited by 796 · see citing works
Does nitric oxide modulate mitochondrial energy generation and apoptosis?
Moncada, S., & Erusalimsky, J. D. (2002) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm762 · Cited by 789 · see citing works
Two ways to survive infection: what resistance and tolerance can teach us about treating infectious diseases
Schneider, D. S., & Ayres, J. S. (2008) · Nature Reviews Immunology · doi:10.1038/nri2432 · Cited by 783 · see citing works
Stress-activated cap’n’collar transcription factors in aging and human disease
Sykiotis, G. P., & Bohmann, D. (2010) · Science Signaling · doi:10.1126/scisignal.3112re3 · Cited by 776 · see citing works
Interdependence of hypoxic and innate immune responses
Nizet, V., & Johnson, R. S. (2009) · Nature Reviews Immunology · doi:10.1038/nri2607 · Cited by 708 · see citing works
Rev-erbα, a Heme Sensor That Coordinates Metabolic and Circadian Pathways
Yin, L., Wu, N., Curtin, J. C., Qatanani, M., Szwergold, N. R., Reid, R. A., Waitt, G. M., Parks, D. J., Pearce, K. H., Wisely, G. B., et al. (2007) · Science · doi:10.1126/science.1150179 · Cited by 707 · see citing works
Stress, Inflammation, and Defense of Homeostasis
Chovatiya, R., & Medzhitov, R. (2014) · Molecular Cell · doi:10.1016/j.molcel.2014.03.030 · Cited by 704 · see citing works
HIF-1α expression regulates the bactericidal capacity of phagocytes
Peyssonnaux, C., Datta, V., Cramer, T., Doedens, A. L., Theodorakis, E. A., Gallo, R. L., Hurtado‐Ziola, N., Nizet, V., & Johnson, R. S. (2005) · Journal of Clinical Investigation · doi:10.1172/jci23865 · Cited by 702 · see citing works
Cyclooxygenases: structural and functional insights
Rouzer, C. A., & Marnett, L. J. (2008) · Journal of Lipid Research · doi:10.1194/jlr.r800042-jlr200 · Cited by 690 · see citing works
Hepcidin and the iron-infection axis
Drakesmith, H., & Prentice, A. M. (2012) · Science · doi:10.1126/science.1224577 · Cited by 686 · see citing works
Induction of heme oxygenase is a rapid, protective response in rhabdomyolysis in the rat.
Nath, K. A., Balla, G., Vercellotti, G. M., Balla, J., Jacob, H. S., Levitt, M. D., & Rosenberg, M. E. (1992) · Journal of Clinical Investigation · doi:10.1172/jci115847 · Cited by 685 · see citing works
Regulation of macrophage development and function in peripheral tissues
Lavin, Y., Mortha, A., Rahman, A., & Merad, M. (2015) · Nature Reviews Immunology · doi:10.1038/nri3920 · Cited by 680 · see citing works
Aryl hydrocarbon receptor control of a disease tolerance defence pathway
Bessede, A., Gargaro, M., Pallotta, M. T., Matino, D., Servillo, G., Brunacci, C., Bicciato, S., Mazza, E. M. C., Macchiarulo, A., Vacca, C., et al. (2014) · Nature · doi:10.1038/nature13323 · Cited by 676 · see citing works
Ferritin heavy chain upregulation by NF-κB inhibits TNFα-induced apoptosis by suppressing reactive oxygen species
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
Soluble Guanylate Cyclase from Bovine Lung: Activation with Nitric Oxide and Carbon Monoxide and Spectral Characterization of the Ferrous and Ferric States
Stone, J. R., & Marletta, M. A. (1994) · Biochemistry · doi:10.1021/bi00184a036 · Cited by 647 · see citing works
Circadian Clock Proteins and Immunity
Curtis, A. M., Bellet, M. M., Sassone‐Corsi, P., & O'Neill, L. A. J. (2014) · Immunity · doi:10.1016/j.immuni.2014.02.002 · Cited by 644 · 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
Tissue biology perspective on macrophages
Okabe, Y., & Medzhitov, R. M. (2015) · Nature Immunology · doi:10.1038/ni.3320 · Cited by 633 · see citing works
Nitric oxide synthase is a cytochrome P-450 type hemoprotein
White, K. A., & Marletta, M. A. (1992) · Biochemistry · doi:10.1021/bi00144a001 · Cited by 615 · see citing works
Tnf dually mediates resistance and susceptibility to mycobacteria via mitochondrial reactive oxygen species
Roca, F. J., & Ramakrishnan, L. (2013) · Cell · doi:10.1016/j.cell.2013.03.022 · Cited by 592 · see citing works
Characterization of Heme as Activator of Toll-like Receptor 4
Figueiredo, R. T., Fernandez, P. L., Mourao-Sa, D. S., Porto, B. N., Dutra, F. F., Alves, L. S., Oliveira, M. F., Oliveira, P. L., Graça-Souza, A. V., & Bozza, M. T. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m610737200 · Cited by 576 · see citing works
Identification of heme as the ligand for the orphan nuclear receptors REV-ERBα and REV-ERBβ
Raghuram, S., Stayrook, K. R., Huang, P., Rogers, P. M., Nosie, A. K., McClure, D. B., Burris, L. L., Khorasanizadeh, S., Burris, T. P., & Rastinejad, F. (2007) · Nature Structural & Molecular Biology · doi:10.1038/nsmb1344 · Cited by 560 · see citing works
Heme 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-citation
Rev-Erbs repress macrophage gene expression by inhibiting enhancer-directed transcription
Lam, M. T. Y., Cho, H., Lesch, H. P., Gosselin, D., Heinz, S., Tanaka-Oishi, Y., Benner, C., Kaikkonen, M. U., Kim, A. S., Kosaka, M., et al. (2013) · Nature · doi:10.1038/nature12209 · Cited by 548 · see citing works
The updated biology of hypoxia-inducible factor
Greer, S. N., Metcalf, J. L., Wang, Y., & Ohh, M. (2012) · The EMBO Journal · doi:10.1038/emboj.2012.125 · Cited by 545 · see citing works
Heme mediates derepression of Maf recognition element through direct binding to transcription repressor Bach1
Ogawa, 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
Signaling by Gasotransmitters
Mustafa, A. K., Gadalla, M. M., & Snyder, S. H. (2009) · Science Signaling · doi:10.1126/scisignal.268re2 · Cited by 497 · 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-citation
Role for Spi-C in the development of red pulp macrophages and splenic iron homeostasis
Kohyama, M., Ise, W., Edelson, B. T., Wilker, P. R., Hildner, K., Mejia, C., Frazier, W. A., Murphy, T. L., & Murphy, K. M. (2009) · Nature · doi:10.1038/nature07472 · Cited by 479 · see citing works
Iron release from macrophages after erythrophagocytosis is up-regulated by ferroportin 1 overexpression and down-regulated by hepcidin
Knutson, M. D., Oukka, M., Koss, L. M., Aydemir, F., & Wessling-Resnick, M. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0409409102 · Cited by 479 · 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
Lipocalin 2-deficient mice exhibit increased sensitivity to Escherichia coli infection but not to ischemia-reperfusion injury
Berger, T., Togawa, A., Duncan, G. S., Elia, A. J., You-Ten, A., Wakeham, A., Fong, H. E. H., Cheung, C. C., & Mak, T. W. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0510847103 · Cited by 460 · see citing works
Serum ferritin is derived primarily from macrophages through a nonclassical secretory pathway
Cohen, L. A., Gutierrez, L., Weiss, A., Leichtmann-Bardoogo, Y., Zhang, D.-L., Crooks, D. R., Sougrat, R., Morgenstern, A., Galy, B., Hentze, M. W., et al. (2010) · Blood · doi:10.1182/blood-2009-11-253815 · Cited by 452 · see citing works
Differential regulation of iron homeostasis during human macrophage polarized activation
Recalcati, S., Locati, M., Marini, A., Santambrogio, P., Zaninotto, F., De Pizzol, M., Zammataro, L., Girelli, D., & Cairo, G. (2010) · European Journal of Immunology · doi:10.1002/eji.200939889 · Cited by 438 · see citing works
Heme-mediated SPI-C induction promotes monocyte differentiation into iron-recycling macrophages
Haldar, M., Kohyama, M., So, A. Y.-L., KC, W., Wu, X., Briseño, C. G., Satpathy, A. T., Kretzer, N. M., Arase, H., Rajasekaran, N. S., et al. (2014) · Cell · doi:10.1016/j.cell.2014.01.069 · Cited by 431 · see citing works
Divalent-metal transport by NRAMP proteins at the interface of host–pathogen interactions
Forbes, J. R., & Gros, P. (2001) · Trends in Microbiology · doi:10.1016/s0966-842x(01)02098-4 · Cited by 424 · see citing works
The physiology of lactoferrin
Brock, J. H. (2002) · Biochemistry and Cell Biology · doi:10.1139/o01-212 · Cited by 401 · see citing works
NF-κB Regulates Phagocytic NADPH Oxidase by Inducing the Expression of gp91
Anrather, J., Racchumi, G., & Iadecola, C. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m506172200 · Cited by 387 · see citing works
Natural Resistance to Intracellular Infections
Jabado, N., Jankowski, A., Dougaparsad, S., Picard, V., Grinstein, S., & Gros, P. (2000) · The Journal of Experimental Medicine · doi:10.1084/jem.192.9.1237 · Cited by 372 · see citing works
Heme regulates the dynamic exchange of Bach1 and NF-E2-related factors in the Maf transcription factor network
Sun, J., Brand, M., Zenke, Y., Tashiro, S., Groudine, M., & Igarashi, K. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0308083100 · Cited by 364 · 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
Nutritional Immunity: Host's Attempt to Withhold Iron From Microbial Invaders
Weinberg, E. D. (1975) · JAMA · doi:10.1001/jama.1975.03240130021018 · Cited by 342 · see citing works
Reciprocal regulation of haem biosynthesis and the circadian clock in mammals
Kaasik, K., & Lee, C. C. (2004) · Nature · doi:10.1038/nature02724 · Cited by 341 · 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-citation
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
Carbon monoxide signals via inhibition of cytochrome c oxidase and generation of mitochondrial reactive oxygen species
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
The circadian clock regulates rhythmic activation of the NRF2/glutathione-mediated antioxidant defense pathway to modulate pulmonary fibrosisPreprint
Pekovic‐Vaughan, V., Gibbs, J. E., Yoshitane, H., Yang, N., Pathiranage, D. R., Guo, B., Sagami, A., Taguchi, K., Bechtold, D. A., Loudon, A. S. I., et al. (2014) · Genes & Development · doi:10.1101/gad.237081.113 · Cited by 322 · see citing works
Activation of the Ah Receptor Signal Transduction Pathway by Bilirubin and Biliverdin
Phelan, D., Winter, G. M., Rogers, W. J., Lam, J., & Denison, M. S. (1998) · Archives of Biochemistry and Biophysics · doi:10.1006/abbi.1998.0814 · Cited by 318 · 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
Self-citation
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 · cited 13× · see citing works
“Cytoplasmic iron is stored in ferritin or secreted extracellularly by FPN1.”
BackgroundInfluential
Heme controls ferroportin1 (FPN1) transcription involving Bach1, Nrf2 and a MARE/ARE sequence motif at position -7007 of the FPN1 promoter
Marro, S., Chiabrando, D., Messana, E., Stolte, J., Turco, E., Tolosano, E., & Muckenthaler, M. U. (2010) · Haematologica · doi:10.3324/haematol.2009.020123 · Cited by 297 · see citing works
Hepcidin regulation by innate immune and infectious stimuli
Armitage, A. E., Eddowes, L. A., Gileadi, U., Cole, S., Spottiswoode, N., Selvakumar, T. A., Ho, L.-P., Townsend, A. R. M., & Drakesmith, H. (2011) · Blood · doi:10.1182/blood-2011-04-351957 · Cited by 294 · see citing works
Feedback control of cyclooxygenase-2 expression through PPARγ
Inoue, H., Tanabe, T., & Umesono, K. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m001387200 · Cited by 276 · 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-citation
Dysfunction of the heme recycling system in heme oxygenase 1–deficient mice: effects on macrophage viability and tissue iron distribution
Kovtunovych, G., Eckhaus, M., Ghosh, M. C., Ollivierre, H., & Rouault, T. A. (2010) · Blood · doi:10.1182/blood-2010-03-272138 · Cited by 273 · see citing works
Heme Oxygenase-1 Drives Metaflammation and Insulin Resistance in Mouse and Man
Jaïs, A., Einwallner, E., Sharif, O., Gossens, K., Lu, T. T.-H., Soyal, S. M., Medgyesi, D., Neureiter, D., Paier-Pourani, J., Dalgaard, K., et al. (2014) · Cell · doi:10.1016/j.cell.2014.04.043 · Cited by 270 · see citing works
Heme oxygenase-1 is a modulator of inflammation and vaso-occlusion in transgenic sickle mice
Belcher, J. D. (2006) · Journal of Clinical Investigation · doi:10.1172/jci26857 · Cited by 265 · 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
Mitochondrial Respiratory Chain and NAD(P)H Oxidase Are Targets for theAntiproliferative Effect of Carbon Monoxide in Human Airway SmoothMuscle
Taillé, C., El-Benna, J., Lanone, S., Boczkowski, J., & Motterlini, R. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m503512200 · Cited by 246 · cited 2× · see citing works
“In addition, heme catabolism by HO-1 generates the gasotransmitter CO that can bind iron within the heme groups of various hemoproteins and modulate in this manner their activity, as exemplified for the inhibition of NOX2 activity (Taillé et al., 2005).”
Background
Natural resistance to intracellular infections: Nramp1 encodes a membrane phosphoglycoprotein absent in macrophages from susceptible (Nramp1 D169) mouse strains
Vidal, S. M., Pinner, E., Lepage, P., Gauthier, S., & Gros, P. (1996) · The Journal of Immunology · doi:10.4049/jimmunol.157.8.3559 · Cited by 241 · see citing works
HRG1 Is Essential for Heme Transport from the Phagolysosome of Macrophages during Erythrophagocytosis
White, C., Yuan, X., Schmidt, P. J., Bresciani, E., Samuel, T. K., Campagna, D. R., Hall, C., Bishop, K. S., Calicchio, M. L., Lapierre, A., et al. (2013) · Cell Metabolism · doi:10.1016/j.cmet.2013.01.005 · Cited by 237 · see citing works
Self-citation
One ring to rule them all: Trafficking of heme and heme synthesis intermediates in the metazoans
Hamza, I., & Dailey, H. A. (2012) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2012.04.009 · Cited by 237 · see citing works
Self-citation
Hypoxia-inducible factor 1α stabilization by carbon monoxide results in cytoprotective preconditioning
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
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-citation
Mycobacterium tuberculosis Senses Host-Derived Carbon Monoxide during Macrophage Infection
Shiloh, M. U., Manzanillo, P. S., & Cox, J. S. (2008) · Cell Host & Microbe · doi:10.1016/j.chom.2008.03.007 · Cited by 217 · see citing works
Conformational control of cofactors in nature – the influence of protein-induced macrocycle distortion on the biological function of tetrapyrroles
Senge, M. O., MacGowan, S. A., & O’Brien, J. M. (2015) · Chemical Communications · doi:10.1039/c5cc06254c · Cited by 211 · see citing works
Induction of Heme Oxygenase-1 Expression in Murine Macrophages Is Essential for the Anti-inflammatory Effect of Low Dose 15-Deoxy-Δ12,14-prostaglandin J2
Lee, T., Tsai, H.-L., & Chau, L. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m300498200 · Cited by 211 · see citing works
A 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-citation
Nitric oxide–mediated regulation of ferroportin-1 controls macrophage iron homeostasis and immune function in Salmonella infection
Nairz, M., Schleicher, U., Schroll, A., Sonnweber, T., Theurl, I., Ludwiczek, S., Talasz, H., Brandacher, G., Moser, P. L., Muckenthaler, M. U., et al. (2013) · Journal of Experimental Medicine · doi:10.1084/jem.20121946 · Cited by 204 · see citing works
Gp91 phox is the heme binding subunit of the superoxide-generating NADPH oxidase
Yu, L., Quinn, M. T., Cross, A. R., & Dinauer, M. C. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.14.7993 · Cited by 202 · see citing works
Macrophages and iron trafficking at the birth and death of red cells
Korolnek, T., & Hamza, I. (2015) · Blood · doi:10.1182/blood-2014-12-567776 · Cited by 196 · see citing works
Self-citation
ROS-induced ATF3 causes susceptibility to secondary infections during sepsis-associated immunosuppression
Hoetzenecker, W., Echtenacher, B., Guenova, E., Hoetzenecker, K., Woelbing, F., Brück, J., Teske, A., Valtcheva, N., Fuchs, K., Kneilling, M., et al. (2011) · Nature Medicine · doi:10.1038/nm.2557 · Cited by 192 · see citing works
Role for NF-κB in the regulation of ferritin H by tumor necrosis factor-α
Kwak, E. L., Larochelle, D. A., Beaumont, C., Torti, S. V., & Torti, F. M. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.25.15285 · Cited by 189 · see citing works
The BTB and CNC Homology 1 (BACH1) Target Genes Are Involved in the Oxidative Stress Response and in Control of the Cell Cycle
Warnatz, H.-J., Schmidt, D., Manke, T., Piccini, I., Sultan, M., Borodina, T. A., Balzereit, D., Wruck, W., Солдатов, А. В., Vingron, M., et al. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.220178 · Cited by 188 · 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-citation
Lipopolysaccharide-Induced Heme Oxygenase-1 Expression in Human Monocytic Cells Is Mediated via Nrf2 and Protein Kinase C
Rushworth, S. A., Chen, X.-L., Mackman, N., Ogborne, R. M., & O'Connell, M. A. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.175.7.4408 · Cited by 185 · see citing works
Nuclear Factor E2-related Factor-2 (Nrf2) Is Required for NLRP3 and AIM2 Inflammasome Activation
Zhao, C., Gillette, D. D., Li, X., Zhang, Z., & Wen, H. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.563114 · Cited by 185 · see citing works
Physiological and pharmacological features of the novel gasotransmitter: Hydrogen sulfide
Mancardi, D., Penna, C. R. R., Merlino, A., Soldato, P. D., Wink, D. A., & Pagliaro, P. (2009) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2009.03.005 · Cited by 184 · see citing works
Macrophages sense and kill bacteria through carbon monoxide–dependent inflammasome activation
Wegiel, B., Larsen, R., Gallo, D. J., Chin, B. Y., Harris, C. E., Mannam, P., Kaczmarek, E., Lee, P. J., Zuckerbraun, B. S., Flavell, R. A., et al. (2014) · Journal of Clinical Investigation · doi:10.1172/jci72853 · Cited by 183 · see citing works
Self-citation
Endogenous NO regulates superoxide production at low oxygen concentrations by modifying the redox state of cytochrome c oxidase
Palacios‐Callender, M., Quintero, M., Hollis, V., Springett, R., & Moncada, S. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0401723101 · Cited by 181 · see citing works
Induction of Heme Oxygenase-1 Inhibits NAD(P)H Oxidase Activity by Down-regulating Cytochrome b558 Expression via the Reduction of Heme Availability
Taillé, C., Benna, J. E., Lanone, S., Dang, M.-C., Ogier‐Denis, É., Aubier, M., & Boczkowski, J. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m310661200 · Cited by 181 · 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
Coupling Heme and Iron Metabolism via 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-citation
Red 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-citation
Anaemia in inflammatory rheumatic diseases
Weiss, G., & Schett, G. (2013) · Nature Reviews Rheumatology · doi:10.1038/nrrheum.2012.183 · Cited by 146 · see citing works
Hemoglobin, a newly recognized lipopolysaccharide (LPS)-binding protein that enhances LPS biological activity.
Kaca, W., Roth, R. I., & Levin, J. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)31501-6 · Cited by 137 · see citing works
Macrophages function as a ferritin iron source for cultured human erythroid precursors
Leimberg, M. J., Prus, E., Konijn, A. M., & Fibach, E. (2007) · Journal of Cellular Biochemistry · doi:10.1002/jcb.21499 · Cited by 137 · see citing works
Heme oxygenase 1 expression induced by IL-10 requires STAT-3 and phosphoinositol-3 kinase and is inhibited by lipopolysaccharide
Ricchetti, G., Williams, L. M., & Foxwell, B. M. J. (2004) · Journal of Leukocyte Biology · doi:10.1189/jlb.0104046 · Cited by 134 · see citing works
Untitled work
(1992) · PubMed · Cited by 127 · see citing works
Redox Cycling in Iron Uptake, Efflux, and Trafficking
Kosman, D. J. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.r110.113217 · Cited by 123 · see citing works
On the haemoprotein character of prostaglandin endoperoxide synthetase
van der Ouderaa, F. J., Buytenhek, M., Slikkerveer, F. J., & van Dorp, D. A. (1979) · Biochimica et Biophysica Acta (BBA) - Lipids and Lipid Metabolism · doi:10.1016/0005-2760(79)90197-8 · Cited by 118 · see citing works
Ferritin-Mediated Iron Sequestration Stabilizes Hypoxia-Inducible Factor-1α upon LPS Activation in the Presence of Ample Oxygen
Siegert, I., Schödel, J., Nairz, M., Schatz, V., Dettmer, K., Dick, C., Kalucka, J., Franke, K., Ehrenschwender, M., Schley, G., et al. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.11.005 · Cited by 110 · cited 7× · see citing works
“Namely, lowering intracellular hemeiron in macrophages promotes the induction of NOS2, TNF, IL-6, IL-12, and histocompatibility (MHC) class II expression in response to IFN-g, an effect mediated in part by NRAMP1 (Fritsche et al., 2008) and involving the transcription factors HIF1a, nuclear factor for IL-6 (NF-IL6), a…”
BackgroundInfluential
Negative feedback regulation of lipopolysaccharide-induced inducible nitric oxide synthase gene expression by heme oxygenase-1 induction in macrophages
Ashino, T., Yamanaka, R., Yamamoto, M. P., Shimokawa, H., Sekikawa, K., Iwakura, Y., Shioda, S., Numazawa, S., & Yoshida, T. (2007) · Molecular Immunology · doi:10.1016/j.molimm.2007.10.011 · Cited by 107 · see citing works
Biological Significance and Applications of Heme c Proteins and Peptides
Kleingardner, J. G., & Bren, K. L. (2015) · Accounts of Chemical Research · doi:10.1021/acs.accounts.5b00106 · Cited by 104 · see citing works
Regulation of Cyclooxygenase by the Heme-Heme Oxygenase System in Microvessel Endothelial Cells
Haider, A. S., Olszanecki, R., Gryglewski, R., Schwartzman, M. L., Lianos, E. A., Kappas, A., Nasjletti, A., & Abraham, N. G. (2002) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.300.1.188 · Cited by 99 · see citing works
Heme Amplifies the Innate Immune Response to Microbial Molecules through Spleen Tyrosine Kinase (Syk)-dependent Reactive Oxygen Species Generation*
Fernandez, P. L., Dutra, F. F., Alves, L., Figueiredo, R. T., Mourão-Sa, D., Fortes, G. B., Bergstrand, S., Lönn, D., Cevallos, R. R., Pereira, R. M. S., et al. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.146076 · Cited by 95 · see citing works
A Novel Heme-Regulatory Motif Mediates Heme-Dependent Degradation of the Circadian Factor Period 2
Yang, J., Kim, K. D., Lucas, A. T., Drahos, K. E., Santos, C. S., Mury, S. P., Capelluto, D. G. S., & Finkielstein, C. V. (2008) · Molecular and Cellular Biology · doi:10.1128/mcb.00236-08 · Cited by 93 · see citing works
Role of the Tumor Suppressor PTEN in Antioxidant Responsive Element-mediated Transcription and Associated Histone Modifications
Sakamoto, K., Iwasaki, K., Sugiyama, H., & Tsuji, Y. (2009) · Molecular Biology of the Cell · doi:10.1091/mbc.e08-07-0762 · Cited by 92 · see citing works
Heme Catabolism by Heme Oxygenase-1 Confers Host Resistance to Mycobacterium Infection
Silva-Gomes, S., Appelberg, R., Larsen, R., Soares, M. P., & Gomes, M. S. (2013) · Infection and Immunity · doi:10.1128/iai.00251-13 · Cited by 85 · see citing works
Self-citation
Expression of stress-response ATF3 is mediated by Nrf2 in astrocytes
Kim, K., Jeong, J., Surh, Y., & Kim, K. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkp865 · Cited by 77 · see citing works
Properties of an unusual heme cofactor in PLP-dependent cystathionine β-synthase
Singh, S., Madzelan, P., & Banerjee, R. V. (2007) · Natural Product Reports · doi:10.1039/b604182p · Cited by 70 · see citing works
The multifaceted role of the E3 ubiquitin ligase HOIL ‐1: beyond linear ubiquitination
Elton, L., Carpentier, I., Verhelst, K., Staal, J., & Beyaert, R. (2015) · Immunological Reviews · doi:10.1111/imr.12307 · Cited by 59 · see citing works
Nramp1‐functionality increases iNOS expression via repression of IL‐10 formation
Fritsche, G., Nairz, M., Werner, E. R., Barton, H. C., & Weiss, G. (2008) · European Journal of Immunology · doi:10.1002/eji.200838449 · Cited by 57 · see citing works
Identification of a cis-Regulatory Element for Δ12-Prostaglandin J2-induced Expression of the Rat Heme Oxygenase Gene
Koizumi, T., Odani, N., Okuyama, T., Ichikawa, A., & Negishi, M. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.37.21779 · Cited by 47 · see citing works
High Affinity Heme Binding to a Heme Regulatory Motif on the Nuclear Receptor Rev-erbβ Leads to Its Degradation and Indirectly Regulates Its Interaction with Nuclear Receptor Corepressor
Carter, E. L., Gupta, N., & Ragsdale, S. W. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.m115.670281 · Cited by 46 · see citing works
Heme oxygenase-1 promotes granuloma development and protects against dissemination of mycobacteria
Regev, D., Surolia, R., Karki, S., Zolak, J., Montes- Worboys, A., Oliva, O., Guroji, P., Saini, V., Steyn, A. J., Agarwal, A., et al. (2012) · Laboratory Investigation · doi:10.1038/labinvest.2012.125 · Cited by 44 · see citing works
Rapid reprogramming of haemoglobin structure‐function exposes multiple dual‐antimicrobial potencies
Du, R., Ho, B., & Ding, J. L. (2010) · The EMBO Journal · doi:10.1038/emboj.2009.380 · Cited by 42 · see citing works
Monocyte Differentiation, Activation, and Mycobacterial Killing Are Linked to Transsulfuration-dependent Redox Metabolism
Garg, S., Vitvitsky, V., Gendelman, H. E., & Banerjee, R. V. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m606235200 · Cited by 36 · see citing works
Tryptophan 2,3-dioxygenase: A review of the roles of the heme and copper cofactors in catalysis
Brady, F. (1975) · Bioinorganic Chemistry · doi:10.1016/s0006-3061(00)80058-7 · Cited by 13 · see citing works

Flagged first, then by citations

2 of the 152 references couldn’t be matched to a known paper.

Sorted by citations

Cross-tissue immune cell analysis reveals tissue-specific features in humans
Conde, C. D., Xu, C., Jarvis, L. B., Rainbow, D. B., Wells, S. B., Gomes, T., Howlett, S. K., Suchánek, O., Polański, K., King, H. W., et al. (2022) · Science · doi:10.1126/science.abl5197 · Cited by 1,165 · see citing works
Lipid Peroxidation and Iron Metabolism: Two Corner Stones in the Homeostasis Control of Ferroptosis
Rochette, L., Dogon, G., Rigal, E., Zeller, M., Cottin, Y., & Vergely, C. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms24010449 · Cited by 932 · see citing works
The Phagocytic Function of Macrophage-Enforcing Innate Immunity and Tissue Homeostasis
Hirayama, D., Iida, T., & Nakase, H. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms19010092 · Cited by 927 · see citing works
Phagocytosis: An Immunobiologic Process
Gordon, S. (2016) · Immunity · doi:10.1016/j.immuni.2016.02.026 · Cited by 902 · see citing works
Tissue macrophages: heterogeneity and functions
Gordon, S., & Plüddemann, A. (2017) · BMC Biology · doi:10.1186/s12915-017-0392-4 · Cited by 601 · see citing works
On Iron Metabolism and Its Regulation
Vogt, A. S., Arsiwala, T., Mohsen, M. O., Vogel, M., Manolova, V., & Bachmann, M. F. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22094591 · Cited by 473 · 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
On-demand erythrocyte disposal and iron recycling requires transient macrophages in the liver
Theurl, I., Hilgendorf, I., Nairz, M., Tymoszuk, P., Haschka, D., Asshoff, M., He, S., Gerhardt, L. M. S., Holderried, T. A. W., Seifert, M., et al. (2016) · Nature Medicine · doi:10.1038/nm.4146 · Cited by 412 · see citing works
Hypoxia inhibits ferritinophagy, increases mitochondrial ferritin, and protects from ferroptosis
Fuhrmann, D. C., Mondorf, A. W., Beifuß, J., Jung, M., & Brüne, B. (2020) · Redox Biology · doi:10.1016/j.redox.2020.101670 · Cited by 409 · see citing works
Disease 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-citation
Macrophages in Renal Injury and Repair
Huen, S. C., & Cantley, L. G. (2017) · Annual Review of Physiology · doi:10.1146/annurev-physiol-022516-034219 · Cited by 377 · see citing works
Tissue macrophages: origin, heterogenity, biological functions, diseases and therapeutic targets
Guan, F., Wang, R., Yi, Z., Luo, P., Liu, W., Xie, Y., Liu, Z., Xia, Z., Zhang, H., & Cheng, Q. (2025) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-025-02124-y · Cited by 371 · see citing works
Dual RNA-Seq of Mtb-Infected Macrophages In Vivo Reveals Ontologically Distinct Host-Pathogen Interactions
Pisu, D., Huang, L., Grenier, J., & Russell, D. (2020) · Cell Reports · doi:10.1016/j.celrep.2019.12.033 · Cited by 230 · see citing works
Iron Metabolism and Immune Regulation
Ni, S., Yuan, Y., Kuang, Y., & Li, X. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.816282 · Cited by 266 · see citing works
Metabolic regulation of macrophage phenotype and function
Saha, S., Shalova, I. N., & Biswas, S. K. (2017) · Immunological Reviews · doi:10.1111/imr.12603 · Cited by 252 · see citing works
Macrophage immunometabolism in inflammatory bowel diseases: From pathogenesis to therapy
Pan, X., Zhu, Q., Pan, L., & Sun, J. T. (2022) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2022.108176 · Cited by 251 · see citing works
The lysosome as a master regulator of iron metabolism
Rizzollo, F., More, S., Vangheluwe, P., & Agostinis, P. (2021) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2021.07.003 · Cited by 234 · see citing works
Resident cardiac macrophages mediate adaptive myocardial remodeling
Wong, N. R., Mohan, J., Kopecky, B. J., Guo, S., Du, L., Leid, J. M., Feng, G., Lokshina, I., Dmytrenko, O., Luehmann, H. P., et al. (2021) · Immunity · doi:10.1016/j.immuni.2021.07.003 · Cited by 229 · see citing works
Macrophage plasticity, polarization and function in response to curcumin, a diet-derived polyphenol, as an immunomodulatory agent
Mohammadi, A., Blesso, C. N., Barreto, G. E., Banach, M., Majeed, M. A., & Sahebkar, A. (2018) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2018.12.005 · Cited by 226 · see citing works
Inflammatory microglia are glycolytic and iron retentive and typify the microglia in APP/PS1 mice
Holland, R., McIntosh, A. L., Finucane, O. M., Mela, V., Rubio‐Araiz, A., Timmons, G. A., McCarthy, S. A., Gun’ko, Y. K., & Lynch, M. A. (2017) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2017.10.017 · Cited by 218 · see citing works
Iron 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
Coordinatively Unsaturated Fe 3+ Based Activatable Probes for Enhanced MRI and Therapy of Tumors
Zhang, P., Hou, Y., Zeng, J., Li, Y., Wang, Z., Zhu, R., Ma, T., & Gao, M. (2019) · Angewandte Chemie International Edition · doi:10.1002/anie.201904880 · Cited by 191 · see citing works
Increased erythrophagocytosis induces ferroptosis in red pulp macrophages in a mouse model of transfusion
Youssef, L. A., Rebbaa, A., Pampou, S., Weisberg, S. P., Stockwell, B. R., Hod, E. A., & Spitalnik, S. L. (2018) · Blood · doi:10.1182/blood-2017-12-822619 · Cited by 186 · see citing works
M2 macrophages in kidney disease: biology, therapies, and perspectives
Chen, T., Cao, Q., Wang, Y., & Harris, D. C. H. (2019) · Kidney International · doi:10.1016/j.kint.2018.10.041 · Cited by 189 · see citing works
Immunomodulatory bioactive glasses for tissue regeneration
Zheng, K., Niu, W., Lei, B., & Boccaccini, A. R. (2021) · Acta Biomaterialia · doi:10.1016/j.actbio.2021.08.023 · Cited by 190 · see citing works
Cell iron status influences macrophage polarization
Agoro, R., Taleb, M., Quesniaux, V. F. J., & Mura, C. (2018) · PLoS ONE · doi:10.1371/journal.pone.0196921 · Cited by 177 · see citing works
“Pumping iron”—how macrophages handle iron at the systemic, microenvironmental, and cellular levels
Nairz, M., Theurl, I., Swirski, F. K., & Weiss, G. (2017) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-017-1944-8 · Cited by 178 · see citing works
Single-cell atlases: shared and tissue-specific cell types across human organs
Elmentaite, R., Conde, C. D., Yang, L., & Teichmann, S. A. (2022) · Nature Reviews Genetics · doi:10.1038/s41576-022-00449-w · Cited by 171 · see citing works
Immunology of COVID‐19: Mechanisms, clinical outcome, diagnostics, and perspectives—A report of the European Academy of Allergy and Clinical Immunology (EAACI)
Sokołowska, M., Łukasik, Z. M., Agache, I. O., Akdiş, C. A., Akdiş, D., Akdiş, M., Barcik, W., Brough, H. A., Eiwegger, T., Eljaszewicz, A., et al. (2020) · Allergy · doi:10.1111/all.14462 · Cited by 169 · see citing works
Iron induces anti-tumor activity in tumor-associated macrophages
Costa da Silva, M., Breckwoldt, M. O., Vinchi, F., Correia, M. P., Stojanovic, A., Thielmann, C. M., Meister, M., Muley, T., Warth, A., Platten, M., et al. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.01479 · Cited by 164 · see citing works
Ferroptotic stress promotes macrophages against intracellular bacteria
Ma, R., Fang, L., Chen, L., Wang, X., Jiang, J., & Gao, L. (2022) · Theranostics · doi:10.7150/thno.66663 · Cited by 167 · see citing works
Bioinorganics and Wound Healing
Dalisson, B., & Barralet, J. E. (2019) · Advanced Healthcare Materials · doi:10.1002/adhm.201900764 · Cited by 165 · see citing works
The role of iron in host–microbiota crosstalk and its effects on systemic glucose metabolism
Mayneris‐Perxachs, J., Moreno‐Navarrete, J. M., & Fernández‐Real, J. M. (2022) · Nature Reviews Endocrinology · doi:10.1038/s41574-022-00721-3 · Cited by 158 · see citing works
Signaling pathways in macrophages: molecular mechanisms and therapeutic targets
Li, M., Wang, M., Wen, Y., Zhang, H., Zhao, G., & Gao, Q. (2023) · MedComm · doi:10.1002/mco2.349 · Cited by 153 · see citing works
Acute Iron Deprivation Reprograms Human Macrophage Metabolism and Reduces Inflammation In Vivo
Pereira, M., Chen, T., Buang, N. B., Olona, A., Ko, J., Prendecki, M. F., Costa, A. S. H., Nikitopoulou, E., Tronci, L., Pusey, C. D., et al. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.06.039 · Cited by 138 · see citing works
Control of tumor-associated macrophage responses by nutrient acquisition and metabolism
Zhang, X., Ji, L., & Li, M. O. (2023) · Immunity · doi:10.1016/j.immuni.2022.12.003 · Cited by 134 · see citing works
Leishmaniasis: the act of transmission
Serafim, T. D., Coutinho-Abreu, I. V., Dey, R., Kissinger, R., Valenzuela, J. G., Oliveira, F., & Kamhawi, S. (2021) · Trends in Parasitology · doi:10.1016/j.pt.2021.07.003 · Cited by 131 · 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-citation
Pegilodecakin combined with pembrolizumab or nivolumab for patients with advanced solid tumours (IVY): a multicentre, multicohort, open-label, phase 1b trial
Naing, A., Wong, D. J. L., Infante, J. R., Korn, W. M., Aljumaily, R. M., Papadopoulos, K. P., Autio, K. A., Pant, S., Bauer, T. M., Drakaki, A., et al. (2019) · The Lancet Oncology · doi:10.1016/s1470-2045(19)30514-5 · Cited by 122 · see citing works
Adipose tissue macrophages: Unique polarization and bioenergetics in obesity
Caslin, H. L., Bhanot, M., Bolus, W. R., & Hasty, A. H. (2020) · Immunological Reviews · doi:10.1111/imr.12853 · Cited by 121 · see citing works
Studying tissue macrophages in vitro: are iPSC-derived cells the answer?
Lee, C., Kozaki, T., & Ginhoux, F. (2018) · Nature reviews. Immunology · doi:10.1038/s41577-018-0054-y · Cited by 118 · see citing works
Macrophage metabolic reprogramming during chronic lung disease
Ogger, P. P., & Byrne, A. J. (2020) · Mucosal Immunology · doi:10.1038/s41385-020-00356-5 · Cited by 119 · see citing works
The microbiota regulates hematopoietic stem cell fate decisions by controlling iron availability in bone marrow
Zhang, D.-C., Gao, X., Li, H., Borger, D. K., Wei, Q.-Z., Yang, E., Xu, C.-L., Pinho, S., & Frenette, P. (2022) · Cell Stem Cell · doi:10.1016/j.stem.2021.12.009 · Cited by 95 · see citing works
Innate Nutritional Immunity
Núñez, G., Sakamoto, K., & Soares, M. P. (2018) · The Journal of Immunology · doi:10.4049/jimmunol.1800325 · Cited by 115 · see citing works
Self-citation
Why cells need iron: a compendium of iron utilisation
Teh, M. R., Armitage, A. E., & Drakesmith, H. (2024) · Trends in Endocrinology & Metabolism · doi:10.1016/j.tem.2024.04.015 · Cited by 114 · see citing works
Metabolic regulation of macrophages during tissue repair: insights from skeletal muscle regeneration
Juban, G., & Chazaud, B. (2017) · FEBS Letters · doi:10.1002/1873-3468.12703 · Cited by 103 · see citing works
Roles and regulation of microglia activity in multiple sclerosis: insights from animal models
Distéfano‐Gagné, F., Bitarafan, S., Lacroix, S., & Gosselin, D. (2023) · Nature reviews. Neuroscience · doi:10.1038/s41583-023-00709-6 · Cited by 112 · see citing works
Understanding terminal erythropoiesis: An update on chromatin condensation, enucleation, and reticulocyte maturation
Mei, Y., Liu, Y., & Ji, P. (2020) · Blood Reviews · doi:10.1016/j.blre.2020.100740 · Cited by 109 · see citing works
Iron homeostasis and disorders revisited in the sepsis
Liu, Q., Wu, J., Zhang, X., Wu, X., Zhao, Y., & Ren, J. (2021) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2021.01.025 · Cited by 112 · see citing works
Ferritin Light Chain Confers Protection Against Sepsis-Induced Inflammation and Organ Injury
Zarjou, A., Black, L. M., McCullough, K., Hull, T. D., Esman, S. K., Boddu, R., Varambally, S., Chandrashekar, D. S., Feng, W., Arosio, P., et al. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.00131 · Cited by 106 · see citing works
Iron Metabolism in Cancer Progression
Forciniti, S., Greco, L., Grizzi, F., Malesci, A., & Laghi, L. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21062257 · Cited by 101 · see citing works
Ironing Out the Details: How Iron Orchestrates Macrophage Polarization
Xia, Y., Li, Y., Wu, X., Zhang, Q., Chen, S., Ma, X., & Yu, M. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.669566 · Cited by 98 · see citing works
Macrophage mediation in normal and diabetic wound healing responses
Ganesh, G. V., & Ramkumar, K. M. (2020) · Inflammation Research · doi:10.1007/s00011-020-01328-y · Cited by 98 · see citing works
Glutamine via α-ketoglutarate dehydrogenase provides succinyl-CoA for heme synthesis during erythropoiesis
Burch, J. S., Marcero, J. R., Maschek, J. A., Cox, J. E., Jackson, L. K., Medlock, A. E., Phillips, J. D., & Dailey, H. A. (2018) · Blood · doi:10.1182/blood-2018-01-829036 · Cited by 92 · see citing works
Heme-Derived Metabolic Signals Dictate Immune Responses
Canesin, G., Hejazi, S. M., Swanson, K. D., & Wegiel, B. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.00066 · Cited by 90 · see citing works
Maresin conjugates in tissue regeneration-1 suppresses ferroptosis in septic acute kidney injury
Xiao, J., Yang, Q., Zhang, Y., Xu, H., Ye, Y., Li, L., Yang, Y., & Jin, S. (2021) · Cell & Bioscience · doi:10.1186/s13578-021-00734-x · Cited by 87 · see citing works
The importance of inflammation control for the treatment of chronic diabetic wounds
Worsley, A., Lui, D. H., Ntow‐Boahene, W., Song, W., Good, L., & Tsui, J. C. S. (2022) · International Wound Journal · doi:10.1111/iwj.14048 · Cited by 83 · see citing works
Nebulized Therapy of Early Orthotopic Lung Cancer by Iron-Based Nanoparticles: Macrophage-Regulated Ferroptosis of Cancer Stem Cells
Feng, Q., Fang, W., Guo, Y., Hu, P., & Shi, J. (2023) · Journal of the American Chemical Society · doi:10.1021/jacs.3c08032 · Cited by 83 · see citing works
Renal control of disease tolerance to malaria
Ramos, S., Carlos, A. R., Sundaram, B., Jeney, V., Ribeiro, A. C., Gozzelino, R., Bank, C., Gjini, E., Braza, F., Martins, R., et al. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1822024116 · Cited by 77 · see citing works
Self-citation
Time-course assessment of the aggregation and metabolization of magnetic nanoparticles
Rojas, J. M., Gavilán, H., del Dedo, V., Lorente-Sorolla, E., Sanz-Ortega, L., da Silva, G. B., Costo, R., Pérez-Yagüe, S., Talelli, M., Marciello, M., et al. (2017) · Acta Biomaterialia · doi:10.1016/j.actbio.2017.05.047 · Cited by 76 · see citing works
Iron and iron-dependent reactive oxygen species in the regulation of macrophages and fibroblasts in non-healing chronic wounds
Wlaschek, M., Singh, K., Sindrilaru, A., Crisan, D., & Scharffetter-Kochanek, K. (2019) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2018.09.036 · Cited by 76 · see citing works
“rophages, essential for the switch from the inflammatory phase to the granulation tissue formation phase of wound healing, intimately correlates with the metabolism of heme-iron in involved cells [11].”
Background
Adipose tissue macrophages exert systemic metabolic control by manipulating local iron concentrations
Joffin, N., Gliniak, C. M., Funcke, J., Paschoal, V. A., Crewe, C., Chen, S., Gordillo, R., Kusminski, C. M., Oh, D. Y., Geldenhuys, W. J., et al. (2022) · Nature Metabolism · doi:10.1038/s42255-022-00664-z · Cited by 75 · see citing works
Reversal of Insulin Resistance in Overweight and Obese Subjects by trans-Resveratrol and Hesperetin Combination—Link to Dysglycemia, Blood Pressure, Dyslipidemia, and Low-Grade Inflammation
Rabbani, N., Xue, M., Weickert, M. O., & Thornalley, P. J. (2021) · Nutrients · doi:10.3390/nu13072374 · Cited by 74 · see citing works
Molecular Imaging of Labile Heme in Living Cells Using a Small Molecule Fluorescent Probe
Kawai, K., Hirayama, T., Imai, H., Murakami, T., Inden, M., Hozumi, I., & Nagasawa, H. (2022) · Journal of the American Chemical Society · doi:10.1021/jacs.1c08485 · Cited by 73 · see citing works
Gut microbiota-testis axis: FMT improves systemic and testicular micro-environment to increase semen quality in type 1 diabetes
Hao, Y., Feng, Y., Yan, X. S., Chen, L., Zhong, R., Tang, X., Shen, W., Sun, Q., Sun, Z., Ren, Y., et al. (2022) · Molecular Medicine · doi:10.1186/s10020-022-00473-w · Cited by 77 · see citing works
Ferroptosis and its Role in Gastric Cancer
Gu, R., Xia, Y., Li, P., Zou, D., Lu, K., Ren, L., Zhang, H., & Sun, Z. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.860344 · Cited by 72 · see citing works
Characterization of plasma labile heme in hemolytic conditions
Gouveia, Z., Carlos, A. R., Yuan, X., Aires‐da‐Silva, F., Stocker, R., Maghzal, G. J., Leal, S. S., Gomes, C. M., Todorovic, S., Iranzo, O., et al. (2017) · The FEBS Journal · doi:10.1111/febs.14192 · Cited by 70 · see citing works
Self-citation
H-Ferritin is essential for macrophages’ capacity to store or detoxify exogenously added iron
Mesquita, G., Silva, T., Gomes, A. C., Oliveira, P. F., Alves, M. G., Fernandes, R., Almeida, A. A., Moreira, A. C., & Gomes, M. S. (2020) · Scientific Reports · doi:10.1038/s41598-020-59898-0 · Cited by 70 · see citing works
Ferritin H Deficiency in Myeloid Compartments Dysregulates Host Energy Metabolism and Increases Susceptibility to Mycobacterium tuberculosis Infection
Reddy, V. P., Chinta, K. C., Saini, V., Glasgow, J. N., Hull, T. D., Traylor, A., Rey-Stolle, F., Soares, M. P., Madansein, R., Rahman, M. A., et al. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.00860 · Cited by 67 · see citing works
Self-citation
Bone marrow stromal cells from β-thalassemia patients have impaired hematopoietic supportive capacity
Crippa, S., Rossella, V., Aprile, A., Silvestri, L., Rivis, S., Scaramuzza, S., Pirroni, S., Avanzini, M. A., Ricci, L. B., Hernández, R. J., et al. (2019) · Journal of Clinical Investigation · doi:10.1172/jci123191 · Cited by 66 · see citing works
Type I Interferon Response Dysregulates Host Iron Homeostasis and Enhances Candida glabrata Infection
Riedelberger, M., Penninger, P., Tscherner, M., Seifert, M., Jenull, S., Brunnhofer, C., Scheidl, B., Tsymala, I., Bourgeois, C., Petryshyn, A., et al. (2020) · Cell Host & Microbe · doi:10.1016/j.chom.2020.01.023 · Cited by 64 · see citing works
Modulating ferroptosis sensitivity: environmental and cellular targets within the tumor microenvironment
Hua, Y., Yang, S., Zhang, Y., Li, J., Wang, M., Yeerkenbieke, P., Liao, Q., & Liu, Q. (2024) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-023-02925-5 · Cited by 69 · see citing works
Haemin-induced cell death in human monocytic cells is consistent with ferroptosis
Imoto, S., Kono, M., Suzuki, T., Shibuya, Y., Sawamura, T., Mizokoshi, Y., Sawada, H., Ohbuchi, A., & Saigo, K. (2018) · Transfusion and Apheresis Science · doi:10.1016/j.transci.2018.05.028 · Cited by 68 · see citing works
Ferritin regulates organismal energy balance and thermogenesis
Blankenhaus, B., Braza, F., Martins, R., Bastos-Amador, P., González‐García, I., Carlos, A. R., Mahú, I., Faísca, P., Nunes, J. M., Ventura, P., et al. (2019) · Molecular Metabolism · doi:10.1016/j.molmet.2019.03.008 · Cited by 64 · see citing works
Self-citation
Friend or Foe? Recent Strategies to Target Myeloid Cells in Cancer
Chaib, M., Chauhan, S., & Makowski, L. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.00351 · Cited by 62 · see citing works
Cancer Related Anemia: An Integrated Multitarget Approach and Lifestyle Interventions
Natalucci, V., Virgili, E., Calcagnoli, F., Valli, G., Agostini, D., Zeppa, S. D., Barbieri, E., & Emili, R. (2021) · Nutrients · doi:10.3390/nu13020482 · Cited by 70 · see citing works
The Heme Connection: Linking Erythrocytes and Macrophage Biology
Alam, M. Z., Devalaraja, S., & Haldar, M. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.00033 · Cited by 66 · see citing works
Heme and hemolysis in innate immunity: adding insult to injury.
Martins, R., & Knapp, S. (2018) · Current Opinion in Immunology · doi:10.1016/j.coi.2017.10.005 · Cited by 60 · see citing works
Iron and Heme Metabolism at the Leishmania–Host Interface
Laranjeira‐Silva, M. F., Hamza, I., & Pérez-Victoria, J. M. (2020) · Trends in Parasitology · doi:10.1016/j.pt.2019.12.010 · Cited by 64 · see citing works
Self-citation
Counter Regulation of Spic by NF-κB and STAT Signaling Controls Inflammation and Iron Metabolism in Macrophages
Alam, Z., Devalaraja, S., Li, M., To, T. K. J., Folkert, I. W., Mitchell-Velasquez, E., Dang, M. T., Young, P. A., Wilbur, C. J., Silverman, M. A., et al. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.107825 · Cited by 64 · see citing works
Scavenging of Labile Heme by Hemopexin Is a Key Checkpoint in Cancer Growth and Metastases
Canesin, G., Ruscio, A. D., Li, M., Ummarino, S., Hedblom, A., Choudhury, R., Krzyzanowska, A., Csizmadia, E., Palominos, M., Stiehm, A., et al. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.108181 · Cited by 61 · see citing works
Intracellular iron and heme trafficking and metabolism in developing erythroblasts
Kafina, M. D., & Paw, B. H. (2017) · Metallomics · doi:10.1039/c7mt00103g · Cited by 62 · see citing works
Macrophage ferroportin is essential for stromal cell proliferation in wound healing
Recalcati, S., Gammella, E., Buratti, P., Doni, A., Anselmo, A., Locati, M., & Cairo, G. (2018) · Haematologica · doi:10.3324/haematol.2018.197517 · Cited by 57 · see citing works
Cutting Edge: Activation-Induced Iron Flux Controls CD4 T Cell Proliferation by Promoting Proper IL-2R Signaling and Mitochondrial Function
Yarosz, E. L., Ye, C., Kumar, A., Black, C., Choi, E., Seo, Y. A., & Chang, C. (2020) · The Journal of Immunology · doi:10.4049/jimmunol.1901399 · Cited by 63 · see citing works
Exerkine FNDC5/irisin‐enriched exosomes promote proliferation and inhibit ferroptosis of osteoblasts through interaction with Caveolin‐1
Tao, L., Wang, J., Wang, K., Liu, Q., Li, H., Xu, S., Gu, C., & Zhu, Y. (2024) · Aging Cell · doi:10.1111/acel.14181 · Cited by 64 · see citing works
Effects of DNA, RNA, and Protein Methylation on the Regulation of Ferroptosis
Wang, X., Kong, X., Feng, X., & Jiang, D. (2023) · International Journal of Biological Sciences · doi:10.7150/ijbs.85454 · Cited by 61 · see citing works
SIRT3 Regulates Clearance of Apoptotic Cardiomyocytes by Deacetylating Frataxin
Gao, J., Huang, C., Kong, L., Zhou, W., Sun, M., Wei, T., & Shen, W. (2023) · Circulation Research · doi:10.1161/circresaha.123.323160 · Cited by 60 · see citing works
The critical roles of iron during the journey from fetus to adolescent: Developmental aspects of iron homeostasis
Donker, A. E., van der Staaij, H., & Swinkels, D. W. (2021) · Blood Reviews · doi:10.1016/j.blre.2021.100866 · Cited by 70 · see citing works
Nanomaterial-Based Repurposing of Macrophage Metabolism and Its Applications
Meng, T., He, D., Han, Z., Shi, R., Wang, Y., Ren, B., Zhang, C., Mao, Z., Luo, G., & Deng, J. (2024) · Nano-Micro Letters · doi:10.1007/s40820-024-01455-9 · Cited by 63 · see citing works
Stressed erythrophagocytosis induces immunosuppression during sepsis through heme-mediated STAT1 dysregulation
Olonisakin, T. F., Suber, T. L., Gonzalez-Ferrer, S., Xiong, Z., Peñaloza, H. F., van der Geest, R., Xiong, Y., Osei-Hwedieh, D. O., Tejero, J., Rosengart, M. R., et al. (2020) · Journal of Clinical Investigation · doi:10.1172/jci137468 · Cited by 54 · see citing works
The path to leptomeningeal metastasis
Remšík, J., & Boire, A. A. (2024) · Nature reviews. Cancer · doi:10.1038/s41568-024-00700-y · Cited by 58 · see citing works
Tumor-derived erythropoietin acts as an immunosuppressive switch in cancer immunity
Chiu, D. K., Zhang, X., Cheng, B. Y.-L., Liu, Q., Hayashi, K., Yu, B., Lee, R. C., Zhang, C. R., An, X., Rajadas, J., et al. (2025) · Science · doi:10.1126/science.adr3026 · Cited by 55 · see citing works
Molecular regulation of cellular iron balance
Recalcati, S., Gammella, E., Buratti, P., & Cairo, G. (2017) · IUBMB Life · doi:10.1002/iub.1628 · Cited by 55 · see citing works
Humoral regulation of iron metabolism by extracellular vesicles drives antibacterial response
Kuang, H., Dou, G., Cheng, L., Wang, X., Xu, H., Liu, X., Ding, F., Yang, X., Liu, S., Bao, L., et al. (2023) · Nature Metabolism · doi:10.1038/s42255-022-00723-5 · Cited by 53 · see citing works
Iron Metabolism and the Inflammatory Response
Martins, A. C., Almeida, J. I., Lima, I. S., Kapitão, A., & Gozzelino, R. (2017) · IUBMB Life · doi:10.1002/iub.1635 · Cited by 52 · see citing works
Molybdenum and tungsten enzymes redox properties – A brief overview
Cordas, C. M., & Moura, J. J. G. (2019) · Coordination Chemistry Reviews · doi:10.1016/j.ccr.2019.05.005 · Cited by 52 · see citing works
Iron-rich Kupffer cells exhibit phenotypic changes during the development of liver fibrosis in NASH
Kanamori, Y., Tanaka, M., Itoh, M., Ochi, K., Ito, A., Hidaka, I., Sakaida, I., Ogawa, Y., & Suganami, T. (2021) · iScience · doi:10.1016/j.isci.2020.102032 · Cited by 45 · see citing works
Crosstalk between Heme Oxygenase-1 and Iron Metabolism in Macrophages: Implications for the Modulation of Inflammation and Immunity
de Oliveira, J., Denadai, M. B., & Costa, D. L. (2022) · Antioxidants · doi:10.3390/antiox11050861 · Cited by 53 · see citing works
Immune effects of glycolysis or oxidative phosphorylation metabolic pathway in protecting against bacterial infection
Li, Y., Jia, A., Wang, Y., Dong, L. R., Wang, Y., He, Y., Wang, S., Cao, Y., Yang, H., Bi, Y., et al. (2019) · Journal of Cellular Physiology · doi:10.1002/jcp.28630 · Cited by 51 · see citing works

Macrophages and Iron: A Special Relationship
Recalcati, S., & Cairo, G. (2021) · Biomedicines · doi:10.3390/biomedicines9111585 · Cited by 74 · see citing works
‘Ride on the ferrous wheel’ – The cycle of iron in macrophages in health and disease
Nairz, M., Schroll, A., Demetz, E., Tancevski, I., Theurl, I., & Weiss, G. (2015) · Immunobiology · doi:10.1016/j.imbio.2014.09.010 · Cited by 89 · see citing works
Ironing out Macrophage Immunometabolism
Recalcati, S., Gammella, E., & Cairo, G. (2019) · Pharmaceuticals · doi:10.3390/ph12020094 · Cited by 34 · see citing works
Advances in the study of iron metabolism by macrophages and its effects on organism immunity
Ru, Z. (2013) · Journal of Pathogen Biology
Crosstalk between Heme Oxygenase-1 and Iron Metabolism in Macrophages: Implications for the Modulation of Inflammation and Immunity
de Oliveira, J., Denadai, M. B., & Costa, D. L. (2022) · Antioxidants · doi:10.3390/antiox11050861 · Cited by 53 · see citing works

Authors: Soares, M. P., & Hamza, I.
Affiliations: Instituto Gulbenkian de Ciência (PT)
University of Maryland, College Park (US)
Corresponding author: Soares, Miguel P.
ORCID: Soares, Miguel P.
Hamza, Iqbal
Venue: Immunity
Publisher: Elsevier BV
Published: 2016-03
Volume: 44
Issue: 3
Pages: 492-504
ISSN: 1074-7613 (ISSN-L)
DOI: 10.1016/j.immuni.2016.02.016
PMC: PMC4794998
OpenAlex: W2298261633
Cited by: 401
References: 152
Citations by year: 2026: 39 · 2025: 47 · 2024: 38 · 2023: 44 · 2022: 50 · 2021: 53 · 2020: 42 · 2019: 31 · 2018: 24 · 2017: 28 · 2016: 4 · 2012: 1
FWCI: 4.10
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 379 d)
Locations: Immunity (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: National Institute of Allergy and Infectious Diseases (R01AI067979, R41AI113998)
National Institute of Diabetes and Digestive and Kidney Diseases (R01DK085035, R01DK074797)
National Institute of Environmental Health Sciences (R21ES025661, R33ES025661)
Topics: Health Sciences › Medicine › Hematology › Iron Metabolism and Disorders
Life Sciences › Immunology and Microbiology › Immunology › Immune cells in cancer
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Hemoglobin structure and function
Keywords: macrophages, iron metabolism, heme iron, reactive oxygen species, iron regulation, macrophage function
MeSH terms: Animals, Heme, Humans, Iron, Macrophages, Protoporphyrins, Reactive Oxygen Species

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

Macrophages and Iron Metabolism

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Self-check

Cites

Cited by

Related

Record

About these checks