Cited by 299Iron Metabolism and DisordersFerroptosis and cancer prognosisImmune cells in cancer

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The Role of Iron Regulation in Immunometabolism and Immune-Related Disease

Open access
Cronin, Shane J. F., Woolf, Clifford J., Weiss, Guenter, Penninger, Josef M.·2019·Frontiers in Molecular Biosciences

Abstract

Immunometabolism explores how the intracellular metabolic pathways in immune cells can regulate their function under different micro-environmental and (patho-)-physiological conditions (Pearce, 2010; Buck et al., 2015; O'Neill and Pearce, 2016). In the last decade great advances have been made in studying and manipulating metabolic programs in immune cells. Immunometabolism has primarily focused on glycolysis, the TCA cycle and oxidative phosphorylation (OXPHOS) as well as free fatty acid synthesis and oxidation. These pathways are important for providing the energy needs of cell growth, membrane rigidity, cytokine production and proliferation. In this review, we will however, highlight the specific role of iron metabolism at the cellular and organismal level, as well as how the bioavailability of this metal orchestrates complex metabolic programs in immune cell homeostasis and inflammation. We will also discuss how dysregulation of iron metabolism contributes to alterations in the immune system and how these novel insights into iron regulation can be targeted to metabolically manipulate immune cell function under pathophysiological conditions, providing new therapeutic opportunities for autoimmunity and cancer.

Overview

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Written from the paper’s full text.

TL;DR

This review synthesizes how iron uptake, storage, export, and mitochondrial utilization regulate immune cell metabolism and function, with emphasis on nutritional immunity, macrophage polarization, T cell activation, and BH4-dependent iron reduction. It argues that targeting iron/BH4 pathways offers therapeutic opportunities in autoimmunity and cancer.

Key findings

  • The iron cycle is tightly controlled: humans absorb 1–2 mg of iron daily, macrophages recycle ~90–95% of daily iron needs, and hepcidin degrades ferroportin to retain iron intracellularly. Hepatic iron deposits normally range from 300 mg to 1 g but can reach 25–30 g in hereditary hemochromatosis.
  • Nutritional immunity shapes infection outcomes: iron overload increases susceptibility to pathogens such as *Vibrio vulnificus*, while mild iron deficiency is protective against *Plasmodium falciparum* malaria; pathogens can hijack transferrin/ferroportin, and lipocalin-2 counters siderophore-mediated bacterial iron acquisition.
  • Immune cell subsets use iron differently: neutrophils rely on myeloperoxidase (~5% of total neutrophil protein) and iron-scavenging lactoferrin/calprotectin; M1 macrophages are iron-retaining whereas M2 macrophages are iron-releasing; T cells upregulate transferrin receptor (TFR/CD71) within a minute of TCR engagement, and TFRC mutation causes combined immunodeficiency.
  • BH4 links iron to T cell metabolism: GCH1 is induced after TCR stimulation, BH4 reduces cytochrome C-Fe3+ to cytochrome C-Fe2+, and BH4 deficiency impairs mitochondrial respiration, increases ROS, and alters mitoferrin, HO-1, ferritin, and frataxin; the SPR inhibitor QM385 blocks T cell proliferation at nanomolar potency and reduces autoimmunity in several models.

Methods

  • Narrative review; no primary experiments or systematic analysis.
  • Synthesizes literature on cellular and systemic iron metabolism, immunometabolism, immune-related disease, and the authors’ prior work on BH4 in T cells.
  • Main analysis is conceptual, with Figure 1, Figure 2, Figure 4, and Table 1 summarizing iron cycle components and regulatory mechanisms.

Limitations

  • Not stated in the paper: the review does not include an explicit limitations section.
  • Evident: as a narrative review, it lacks a systematic search strategy, meta-analysis, or primary data to assess bias or effect sizes.
  • Evident: conclusions rely on cited studies and the authors’ own prior BH4 work, and the broad scope means some areas are covered selectively rather than exhaustively.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.3389/fmolb.2019.00116

Cites

208 of 208 references verified0 citation errors · 0 not checkable

Statistics

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Figures

Figure 1 Iron metabolism in the cell. Intracellular iron levels are strictly controlled as too little or too much can be detrimental to the health of the cell. Therefore, (1)-iron uptake, (2)-utilization, (3)-storage and (4)-export need to be managed in a coordinated manner, as well as the conversion between the oxidation states of iron (Fe2+ and Fe3+) in the cell. (1) Iron-bound transferrin (TF-Fe3+) and NTBI (non-transferrin-bound iron) are taken up into the cell by the iron importers DMT1 and ZIP14. STEAP3 is a ferrireductase which reduces Fe3+ to Fe2+, which can then be imported. (2) Once inside the cell, the bioavailable and more soluble Fe2+ is used for various biological processes– DNA replication, ROS production via Fenton/Haber-Weiss (F/H-W) chemistry, mitochondrial bioenergetics, Fe-S and heme biosynthesis, as well as a plethora of proteins which utilize the metal to carry out their functions. (3) Excess Fe2+ iron is dangerous due to its role in ROS production. Therefore, it needs to be stored but, at the same time, be readily available for use. This is achieved by a particular arrangement of ferritin proteins designated the “ferritin cage” which stores the more inert, insoluble Fe3+ form of iron. When intracellular levels are low, this ferritin cage is signaled for destruction by NCOA4 thus releasing the stored iron. (4) If intracellular iron levels are saturated, then the iron must be exported out of the cell. This is achieved by the iron exporter ferroportin (FPN). Once outside the cell the Fe2+ iron is oxidized to Fe3+ (via CP, HEPH, HEPHL). (5) Finally, Fe3+ iron is then bound to transferrin (Tf-Fe3+) and enters the circulation to begin the cycle again. Notably, hepcidin is an iron-controlling hormone produced by the liver. When systemic iron levels are high in the blood, hepcidin is produced and leads to the degradation of FPN on cells thus preventing cellular release of iron into the blood. Conversely, when iron blood levels are low, hepcidin expression is reduced.
Figure 1 Iron metabolism in the cell. Intracellular iron levels are strictly controlled as too little or too much can be detrimental to the health of the cell. Therefore, (1)-iron uptake, (2)-utilization, (3)-storage and (4)-export need to be managed in a coordinated manner, as well as the conversion between the oxidation states of iron (Fe2+ and Fe3+) in the cell. (1) Iron-bound transferrin (TF-Fe3+) and NTBI (non-transferrin-bound iron) are taken up into the cell by the iron importers DMT1 and ZIP14. STEAP3 is a ferrireductase which reduces Fe3+ to Fe2+, which can then be imported. (2) Once inside the cell, the bioavailable and more soluble Fe2+ is used for various biological processes– DNA replication, ROS production via Fenton/Haber-Weiss (F/H-W) chemistry, mitochondrial bioenergetics, Fe-S and heme biosynthesis, as well as a plethora of proteins which utilize the metal to carry out their functions. (3) Excess Fe2+ iron is dangerous due to its role in ROS production. Therefore, it needs to be stored but, at the same time, be readily available for use. This is achieved by a particular arrangement of ferritin proteins designated the “ferritin cage” which stores the more inert, insoluble Fe3+ form of iron. When intracellular levels are low, this ferritin cage is signaled for destruction by NCOA4 thus releasing the stored iron. (4) If intracellular iron levels are saturated, then the iron must be exported out of the cell. This is achieved by the iron exporter ferroportin (FPN). Once outside the cell the Fe2+ iron is oxidized to Fe3+ (via CP, HEPH, HEPHL). (5) Finally, Fe3+ iron is then bound to transferrin (Tf-Fe3+) and enters the circulation to begin the cycle again. Notably, hepcidin is an iron-controlling hormone produced by the liver. When systemic iron levels are high in the blood, hepcidin is produced and leads to the degradation of FPN on cells thus preventing cellular release of iron into the blood. Conversely, when iron blood levels are low, hepcidin expression is reduced.CC BY · PubMed Central
Figure 2 Regulation of iron metabolism by IRP1. When cellular iron levels are low, Fe-S biogenesis in the mitochondria is reduced and IRP1 loses its Fe-S cluster component. This allows IRP1 to now bind to the IRE sequence in target mRNAs. IRP1 binds to the IREs at either the 3′ (for example transferrin mRNA) or 5′ (for example ferroportin mRNA) untranslated region (UTR) of the targeted mRNA. Binding to the 5′ UTR blocks translation while binding to the 3′ UTR stabilizes the mRNA against endonuclease cleavage. Thus, when iron levels are low (left panel), transferrin protein is enhanced while ferroportin protein is reduced resulting in increased iron import and reduced export, to ultimately increase intracellular iron levels. When iron levels are high (right panel), this leads to reduced iron uptake and increased export.
Figure 2 Regulation of iron metabolism by IRP1. When cellular iron levels are low, Fe-S biogenesis in the mitochondria is reduced and IRP1 loses its Fe-S cluster component. This allows IRP1 to now bind to the IRE sequence in target mRNAs. IRP1 binds to the IREs at either the 3′ (for example transferrin mRNA) or 5′ (for example ferroportin mRNA) untranslated region (UTR) of the targeted mRNA. Binding to the 5′ UTR blocks translation while binding to the 3′ UTR stabilizes the mRNA against endonuclease cleavage. Thus, when iron levels are low (left panel), transferrin protein is enhanced while ferroportin protein is reduced resulting in increased iron import and reduced export, to ultimately increase intracellular iron levels. When iron levels are high (right panel), this leads to reduced iron uptake and increased export.CC BY · PubMed Central
Figure 3 Essential role of iron for various cell types. Iron is needed by many different cell types to perform very distinct functions from oxygen carrying abilities of red blood cells (RBCs) to oxygen storage in muscle cells. Moreover, iron dysregulation has been observed in the pathogenesis of many diseases such as the neurodegenerative diseases Alzheimer's and Parkinson's. Importantly various immune cells regulate iron metabolism to induce their various effector functions. Notably, as iron is so essential for cell division, one of the earliest tasks of invading pathogens is to capture host iron in the circulation to aid their own growth and expansion. Therefore, restricting free iron is a first line of defense against invading pathogens.
Figure 3 Essential role of iron for various cell types. Iron is needed by many different cell types to perform very distinct functions from oxygen carrying abilities of red blood cells (RBCs) to oxygen storage in muscle cells. Moreover, iron dysregulation has been observed in the pathogenesis of many diseases such as the neurodegenerative diseases Alzheimer's and Parkinson's. Importantly various immune cells regulate iron metabolism to induce their various effector functions. Notably, as iron is so essential for cell division, one of the earliest tasks of invading pathogens is to capture host iron in the circulation to aid their own growth and expansion. Therefore, restricting free iron is a first line of defense against invading pathogens.CC BY · PubMed Central
Figure 4 BH4 enhances iron-dependent mechanisms upon T cell activation. Upon T cell receptor (TCR) stimulation, T cells alter their metabolic programming, such as promoting energy-producing mitochondria and electron transport chain (ETC) activity, to be able to proliferate and carry out effector functions. These increased metabolic needs require additional regulators for efficient ETC function to limit dangerous ROS byproducts due to the increased energy demands. To accomplish this, T cells induce the expression of the enzyme GCH1 which produces the metabolite BH4 after stimulation. BH4 can not only act as a superoxide ROS scavenger but also directly reduce Fe3+ to Fe2+ and therefore affect cytochrome C (cyto-C) activity in the ETC. Other iron-regulated processes such as heme and Fe-S biogenesis, as well as the function of various iron-dependent metalloproteins, may also be affected. Under BH4 deficiency, T cells show dysfunctional ETC, enhanced ROS, and reduced ATP production in activated T cells. Moreover, the T cells show dysregulated Mitoferrin, Frataxin, HO-1, Ferritin and overall reduced iron levels in the cell suggesting that BH4 deficiency affects iron metabolism and the cell compensates by trying to increase Fe2+ levels in the mitochondria. GTP, guanosine triphosphate; PTPS, 6-pyruvoyl tetrahydropterin synthase; SPR, sepiapterin reductase; DHTP, dihydroneopterin triphosphate; 6-PTH, 6-pyruvoyl tetrahydropterin; BH4, tetrahydrobiopterin; ROS, reactive oxygen radicals; ALAS, aminolevulinic acid synthase; e-, electron.
Figure 4 BH4 enhances iron-dependent mechanisms upon T cell activation. Upon T cell receptor (TCR) stimulation, T cells alter their metabolic programming, such as promoting energy-producing mitochondria and electron transport chain (ETC) activity, to be able to proliferate and carry out effector functions. These increased metabolic needs require additional regulators for efficient ETC function to limit dangerous ROS byproducts due to the increased energy demands. To accomplish this, T cells induce the expression of the enzyme GCH1 which produces the metabolite BH4 after stimulation. BH4 can not only act as a superoxide ROS scavenger but also directly reduce Fe3+ to Fe2+ and therefore affect cytochrome C (cyto-C) activity in the ETC. Other iron-regulated processes such as heme and Fe-S biogenesis, as well as the function of various iron-dependent metalloproteins, may also be affected. Under BH4 deficiency, T cells show dysfunctional ETC, enhanced ROS, and reduced ATP production in activated T cells. Moreover, the T cells show dysregulated Mitoferrin, Frataxin, HO-1, Ferritin and overall reduced iron levels in the cell suggesting that BH4 deficiency affects iron metabolism and the cell compensates by trying to increase Fe2+ levels in the mitochondria. GTP, guanosine triphosphate; PTPS, 6-pyruvoyl tetrahydropterin synthase; SPR, sepiapterin reductase; DHTP, dihydroneopterin triphosphate; 6-PTH, 6-pyruvoyl tetrahydropterin; BH4, tetrahydrobiopterin; ROS, reactive oxygen radicals; ALAS, aminolevulinic acid synthase; e-, electron.CC BY · PubMed Central

Verification

Claims the paper makes

180 Not checked yet · 7 Own interpretation · 5 No basis given · 1 Sources not found

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  • It may state two separate claims as one. 75
  • Probably not a substantial claim. 18
86 of 86
  • The paper relies on this without support.

    Iron is essential to almost all organisms.

    “Iron is one of the most abundant elements on Earth and essential to almost all organisms.”
  • The paper relies on this without support.

    Normal physiology is a balance between reactive oxygen species and antioxidants, with antioxidants maintaining useful ROS levels while minimizing bystander damage.

    “Normal physiology is a balance between the two: antioxidants maintain levels of ROS that permit them to perform useful biological functions, such as neutrophil-mediated killing of phagocytosed bacteria or enhanced T cell proliferation after TCR stimulation, while minimizing by-stander damage.”
  • The paper relies on this without support.

    Iron is essential for many physiological processes including erythropoiesis, immune function, host defense, DNA replication and repair, mitochondrial function including OXPHOS, and enzymatic reactions requiring iron as a cofactor.

    “Iron is essential for many physiological processes in the body including erythropoiesis, immune function and host defense, as well as essential cellular activities such as DNA replication and repair, mitochondrial function including OXPHOS and enzymatic reactions which require iron as a cofactor.”
  • The paper relies on this without support.

    There exists no effective excretion mechanism for iron surplus.

    “As there exists no effective excretion mechanism for iron surplus, iron is stored in parenchymal organs, mainly the liver.”
  • The paper relies on this without support.

    Intracellular iron levels are tightly controlled.

    “Similar to systemic iron levels in the bloodstream, the intracellular iron levels are tightly controlled.”
  • The paper relies on this without support.

    The iron cycle is present in almost all cells of the body.

    “The iron cycle is present in almost all cells of the body, and so the regulatory networks described above are also essential to the cells of the immune system.”
  • The paper relies on this without support.

    Both iron deficiency and iron excess can influence both the innate and adaptive arms of the immune system.

    “Both iron deficiency and iron excess can influence both the innate and adaptive arms of the immune system.”
  • The paper relies on this without support.

    Iron is essential for cell division.

    “Notably, as iron is so essential for cell division, one of the earliest tasks of invading pathogens is to capture host iron in the circulation to aid their own growth and expansion.”
  • The paper relies on this without support.

    Restricting free iron is a first line of defense against invading pathogens.

    “Therefore, restricting free iron is a first line of defense against invading pathogens.”
  • The paper relies on this without support.

    Hepcidin promotes intracellular iron retention, thus restricting its availability for pathogens in the circulation.

    “Hepcidin is an important gatekeeper which promotes intracellular iron retention thus restricting its availability for pathogens in the circulation.”
  • The paper relies on this without support.

    The increase of hepcidin within hours of an infection or inflammatory insult results in a dramatic reduction of plasma iron levels.

    “The increase of hepcidin within hours of an infection or inflammatory insult, results in a dramatic reduction of plasma iron levels.”
  • The paper relies on this without support.

    Iron is essential for ferroptosis because Fe2+ converts hydrogen peroxide produced by mitochondrial respiration into hydroxyl radical through Fenton chemistry, which then takes electrons from lipids resulting in lipid peroxidation and ferroptosis.

    “Iron is essential for the process of ferroptosis as free divalent iron (Fe2+) converts the hydrogen peroxide (H2O2) produced by mitochondrial respiration into the toxic free hydroxyl radical (OH•) through Fenton chemistry which then “takes” electrons from lipids resulting in lipid peroxidation and ferroptosis.”
  • The paper relies on this without support.

    Iron homeostasis, its regulation through uptake, use, storage and export, influences the activity of metabolic pathways to couple the activation, growth and survival of T cells.

    “Iron homeostasis, its regulation through uptake, use, storage and export, influences the activity of metabolic pathways to couple the activation, growth and survival of T cells.”
  • The paper relies on this without support.

    Fe2+ is needed for metalloproteins like cytochrome-C to function optimally, for Fe-S cluster biogenesis, which are essential for complex I and II activity of the ETC, and for heme production.

    “Fe2+ is not only needed for metalloproteins like cytochrome-C to function optimally but also for Fe-S cluster biogenesis, which are essential for complex I and II activity of the ETC, and heme production (Figure 4).”
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Metadata

Authors
Cronin, S. J. F., Woolf, C. J., Weiss, G., & Penninger, J. M.
Affiliations
  • Institute of Molecular Biotechnology (AT)
  • Boston Children's Hospital (US)
Corresponding author
Penninger, Josef M.
Venue
Frontiers in Molecular Biosciences
Published
2019-11-22
Volume
6
Pages
116-116
ISSN
2296-889X (ISSN-L)
OpenAlex
W2991203943
Cited by
299
References
214
Citations by year
2026: 28 · 2025: 50 · 2024: 49 · 2023: 45 · 2022: 56 · 2021: 47 · 2020: 24
FWCI
5.06
Type
journal article
Language
en
Open access
Locations
  • Frontiers in Molecular Biosciences (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Topics
  • Health Sciences › Medicine › Hematology › Iron Metabolism and Disorders
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Ferroptosis and cancer prognosis
  • Life Sciences › Immunology and Microbiology › Immunology › Immune cells in cancer
Keywords
iron metabolism, immunometabolism, immune cell metabolism, iron bioavailability, immune cell homeostasis, inflammation, autoimmunity, tumor immunology, metabolic reprogramming, immune-related diseases

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