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Nutritional immunity: the impact of metals on lung immune cells and the airway microbiome during chronic respiratory disease

Healy, Claire, Munoz-Wolf, Natalia, Strydom, Janné, Faherty, Lynne, Williams, Niamh C., Kenny, Sarah, Donnelly, Seamas C., Cloonan, Suzanne M.·2021·Respiratory Research
DOI 10.1186/s12931-021-01722-yPMC PMC8082489
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Abstract

Nutritional immunity is the sequestration of bioavailable trace metals such as iron, zinc and copper by the host to limit pathogenicity by invading microorganisms. As one of the most conserved activities of the innate immune system, limiting the availability of free trace metals by cells of the immune system serves not only to conceal these vital nutrients from invading bacteria but also operates to tightly regulate host immune cell responses and function. In the setting of chronic lung disease, the regulation of trace metals by the host is often disrupted, leading to the altered availability of these nutrients to commensal and invading opportunistic pathogenic microbes. Similarly, alterations in the uptake, secretion, turnover and redox activity of these vitally important metals has significant repercussions for immune cell function including the response to and resolution of infection. This review will discuss the intricate role of nutritional immunity in host immune cells of the lung and how changes in this fundamental process as a result of chronic lung disease may alter the airway microbiome, disease progression and the response to infection.

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Fig. 1 Macrophage Metal Metabolism. This brief summary of the metal metabolism of a generic macrophage highlights several mechanisms by which a macrophage can obtain metals. There are numerous metal transport proteins and receptors involved to ensure an adequate supply of these essential metals to the macrophage. (1) Macrophages obtain iron from various sources. Free circulating iron is first reduced from ferric to ferrous iron and then imported into the macrophage via protein transporters such as DMT1 and ZIP14. Transferrin-bound iron is bound to the transferrin receptor on the cell surface and imported via receptor-mediated endocytosis. Some macrophages also have the ability to obtain iron via erythrophagocytosis while others express receptors such as CD163 and CD64 allowing for the uptake of haemoglobin-haptoglobin and heme-hemopexin complexes, respectively. Once iron enters the macrophage it has numerous fates depending on the activation state of the cell. It can be stored in its ferrous state within the ferritin complex or utilized in the mitochondria for Fe-S cluster and heme biosynthesis. Iron is exported out of the macrophage through the only known iron export protein, ferroportin (FPN) whose expression is regulated by the hormone hepcidin. Further post-transcriptional regulation of intracellular iron levels is carried out by cytosolic regulatory proteins IRP1 and IRP2. (2) Intracellular zinc supply is mediated by two families of transport proteins; SLC39A (ZIPs) import zinc into the cell while SLC30A mediates zinc export out of the cell. (3) The copper importers Ctr1 and ATPase metal pump, ATP7A are two known copper transporters within the macrophage and gets upregulated to facilitate copper mediated host defence mechanisms
Fig. 1 Macrophage Metal Metabolism. This brief summary of the metal metabolism of a generic macrophage highlights several mechanisms by which a macrophage can obtain metals. There are numerous metal transport proteins and receptors involved to ensure an adequate supply of these essential metals to the macrophage. (1) Macrophages obtain iron from various sources. Free circulating iron is first reduced from ferric to ferrous iron and then imported into the macrophage via protein transporters such as DMT1 and ZIP14. Transferrin-bound iron is bound to the transferrin receptor on the cell surface and imported via receptor-mediated endocytosis. Some macrophages also have the ability to obtain iron via erythrophagocytosis while others express receptors such as CD163 and CD64 allowing for the uptake of haemoglobin-haptoglobin and heme-hemopexin complexes, respectively. Once iron enters the macrophage it has numerous fates depending on the activation state of the cell. It can be stored in its ferrous state within the ferritin complex or utilized in the mitochondria for Fe-S cluster and heme biosynthesis. Iron is exported out of the macrophage through the only known iron export protein, ferroportin (FPN) whose expression is regulated by the hormone hepcidin. Further post-transcriptional regulation of intracellular iron levels is carried out by cytosolic regulatory proteins IRP1 and IRP2. (2) Intracellular zinc supply is mediated by two families of transport proteins; SLC39A (ZIPs) import zinc into the cell while SLC30A mediates zinc export out of the cell. (3) The copper importers Ctr1 and ATPase metal pump, ATP7A are two known copper transporters within the macrophage and gets upregulated to facilitate copper mediated host defence mechanismsCC BY · PubMed Central
Fig. 2 Host Bactericidal Immune Defence Facilitated by Trace Metals. Metals play a pivotal role in contributing to the host immune response during bacterial infection. They can be used by immune cells to either mediate metal toxicity to rapidly kill the bacteria or be sequestered away in order to deprive the bacteria of essential metals in order to limit bacterial growth and replication. Whether the metals are sequestered or used to facilitate toxicity mechanisms is highly dependent on the nature of the bacterial infection. (1) Intracellular bacteria are mainly located within the phagosome of their host cell. Here they release siderophores allowing them to scavenge iron within the cell. In response, the host limits bacterial iron supply by exporting iron out of the infected phagosome via the NRAMP1 transporter. Furthermore, the host employs toxicity mechanisms by which both zinc and copper are pumped into the infected phagosome via their respective transporters in order to limit bacterial growth and replication. (2) Extracellular bacteria produce numerous different proteins to mediate metal acquisition from the host. The majority produce siderophores, which vary between bacterial species. However, they all function to supply the bacteria with an adequate amount of iron. The host also employs mechanisms to limit the amount of metals available to the bacteria in the extracellular space. Iron is sequestered by the upregulation of hepcidin resulting in the degradation of FPN which reduces the amount of iron exported from the cell. Furthermore, the iron importer DMT1 is also upregulated in both macrophages and neutrophils. Several metal binding proteins have also been shown to be produced mainly by neutrophils to bind extracellular metals. Lipocalin2, produced in secondary granules of neutrophils, binds bacterial siderophores and shuttles them away from the bacteria to the host cell. S100 proteins such as Calprotectin that binds zinc and manganese, and Calgranulin C binding zinc and copper also sequester these metals out of the extracellular space
Fig. 2 Host Bactericidal Immune Defence Facilitated by Trace Metals. Metals play a pivotal role in contributing to the host immune response during bacterial infection. They can be used by immune cells to either mediate metal toxicity to rapidly kill the bacteria or be sequestered away in order to deprive the bacteria of essential metals in order to limit bacterial growth and replication. Whether the metals are sequestered or used to facilitate toxicity mechanisms is highly dependent on the nature of the bacterial infection. (1) Intracellular bacteria are mainly located within the phagosome of their host cell. Here they release siderophores allowing them to scavenge iron within the cell. In response, the host limits bacterial iron supply by exporting iron out of the infected phagosome via the NRAMP1 transporter. Furthermore, the host employs toxicity mechanisms by which both zinc and copper are pumped into the infected phagosome via their respective transporters in order to limit bacterial growth and replication. (2) Extracellular bacteria produce numerous different proteins to mediate metal acquisition from the host. The majority produce siderophores, which vary between bacterial species. However, they all function to supply the bacteria with an adequate amount of iron. The host also employs mechanisms to limit the amount of metals available to the bacteria in the extracellular space. Iron is sequestered by the upregulation of hepcidin resulting in the degradation of FPN which reduces the amount of iron exported from the cell. Furthermore, the iron importer DMT1 is also upregulated in both macrophages and neutrophils. Several metal binding proteins have also been shown to be produced mainly by neutrophils to bind extracellular metals. Lipocalin2, produced in secondary granules of neutrophils, binds bacterial siderophores and shuttles them away from the bacteria to the host cell. S100 proteins such as Calprotectin that binds zinc and manganese, and Calgranulin C binding zinc and copper also sequester these metals out of the extracellular spaceCC BY · PubMed Central

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Metadata

Authors
Healy, C., Munoz-Wolf, N., Strydom, J., Faherty, L., Williams, N. C., Kenny, S., Donnelly, S. C., & Cloonan, S. M.
ORCID
Cloonan, Suzanne M.
Venue
Respiratory Research
Publisher
Springer Science and Business Media LLC
Published
2021-04-29
Volume
22
Issue
1
ISSN
1465-993X
DOI
10.1186/s12931-021-01722-y
PMC
PMC8082489
Cited by
78
References
55
Language
en
Licence
Funders
  • Science Foundation Ireland (FRL4862</)
  • Health Research Board (EIA-2019-004)

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