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Elemental Ingredients in the Macrophage Cocktail: Role of ZIP8 in Host Response to Mycobacterium tuberculosis

Pyle, Charlie, Azad, Abul, Papp, Audrey, Sadee, Wolfgang, Knoell, Daren, Schlesinger, Larry·2017·International Journal of Molecular Sciences
DOI 10.3390/ijms18112375PMC PMC5713344
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Abstract

Tuberculosis (TB) is a global epidemic caused by the infection of human macrophages with the world’s most deadly single bacterial pathogen, Mycobacterium tuberculosis (M.tb). M.tb resides in a phagosomal niche within macrophages, where trace element concentrations impact the immune response, bacterial metal metabolism, and bacterial survival. The manipulation of micronutrients is a critical mechanism of host defense against infection. In particular, the human zinc transporter Zrt-/Irt-like protein 8 (ZIP8), one of 14 ZIP family members, is important in the flux of divalent cations, including zinc, into the cytoplasm of macrophages. It also has been observed to exist on the membrane of cellular organelles, where it can serve as an efflux pump that transports zinc into the cytosol. ZIP8 is highly inducible in response to M.tb infection of macrophages, and we have observed its localization to the M.tb phagosome. The expression, localization, and function of ZIP8 and other divalent cation transporters within macrophages have important implications for TB prevention and dissemination and warrant further study. In particular, given the importance of zinc as an essential nutrient required for humans and M.tb, it is not yet clear whether ZIP-guided zinc transport serves as a host protective factor or, rather, is targeted by M.tb to enable its phagosomal survival.

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Figure 1 Macrophage zinc transporter mRNA expression during M.tb infection. Zrt-Irt-like-Protein (ZIP) and zinc transport protein (ZnT) mRNA expression is altered by infection with Mycobacterium tuberculosis (M.tb) H37Rv using a multiplicity of infection (MOI) of 5:1 for (A) 8 h in monocyte-derived macrophages (MDMs) in the absence or presence of ZnSO4 18 μM, as determined by qRT-PCR relative to GAPDH (n = 3) or (B) for 24 or 72 h in human alveolar macrophages (hAMs) infected by M.tb H37Rv, as determined by AmpliSeq Transcriptome analysis (n = 6). (C) The mRNA expression of ZIP8 is increased and ZnT1, ZIP1, and ZIP10 are decreased in M.marinum-infected zebrafish granulomas compared to resting macrophages, as determined by RNA-Seq. (A and B are unpublished data; C was generated using supplementary data published in Cronan et al. [53]) (mean ± SEM; *** p < 0.001; **** p < 0.0001; Prism-7: one-tailed Students t-test). MDM [54] and hAM [55] isolation, culture, and infection with M.tb, as well as the assay of human zinc transporters by qRT-PCR in MDMs [56] and AmpliSeq Transcriptome analysis in hAMs [52], were performed as previously described.
Figure 1 Macrophage zinc transporter mRNA expression during M.tb infection. Zrt-Irt-like-Protein (ZIP) and zinc transport protein (ZnT) mRNA expression is altered by infection with Mycobacterium tuberculosis (M.tb) H37Rv using a multiplicity of infection (MOI) of 5:1 for (A) 8 h in monocyte-derived macrophages (MDMs) in the absence or presence of ZnSO4 18 μM, as determined by qRT-PCR relative to GAPDH (n = 3) or (B) for 24 or 72 h in human alveolar macrophages (hAMs) infected by M.tb H37Rv, as determined by AmpliSeq Transcriptome analysis (n = 6). (C) The mRNA expression of ZIP8 is increased and ZnT1, ZIP1, and ZIP10 are decreased in M.marinum-infected zebrafish granulomas compared to resting macrophages, as determined by RNA-Seq. (A and B are unpublished data; C was generated using supplementary data published in Cronan et al. [53]) (mean ± SEM; *** p < 0.001; **** p < 0.0001; Prism-7: one-tailed Students t-test). MDM [54] and hAM [55] isolation, culture, and infection with M.tb, as well as the assay of human zinc transporters by qRT-PCR in MDMs [56] and AmpliSeq Transcriptome analysis in hAMs [52], were performed as previously described.CC BY · PubMed Central
Figure 2 ZIP8 protein is induced and localizes with M.tb in human macrophages. MDM production of ZIP8: (A) mRNA is significantly induced for 24 h, following infection with M.tb H37Rv (MOI 5:1), as determined by qRT-PCR relative to GAPDH (n = 3) and (B) ZIP8 protein is robustly increased by infection with M.tb H37Rv or M.bovis BCG (MOI 5:1) between 24 and 72 h, as determined by Western blot relative to β-actin (n = 3). (C) The infection of MDMs with mCherry expressing M.tb H37Rv (MOI 5:1) for 48 h leads to the extensive co-localization of ZIP8 with M.tb (yellow; indicated by arrow heads) and TfR1 (abundant white; in merged upper panel) but very limited co-localization with LAMP-1 (negligible white; in merged lower panel) (A, B, and C are unpublished data) (mean ± SEM; * p < 0.05; Prism-7: one-tailed Students t-test). MDM isolation, culture, and infection [54]; qRT-PCR and Western blot of ZIP8 in MDMs [56]; and confocal fluorescence microscopy using an Olympus FV1000-Spectral System at 60× magnification in infected MDMs [67] were performed as previously described. Rabbit polyclonal antiserum anti-peptide to amino acid residues 225 to 243 of human ZIP8 was purchased from Covance (Princeton, NJ, USA). Mouse anti-human monoclonal β-actin (#69101) antibody was purchased from MP Biomedicals (Santa Ana, CA, USA). Mouse anti-human monoclonal CD71 (#334102) antibody was purchased from Biolegend (San Diego, CA, USA). Mouse anti-human monoclonal LAMP-1 (#ab25630) antibody was purchased from Abcam (Cambridge, UK).
Figure 2 ZIP8 protein is induced and localizes with M.tb in human macrophages. MDM production of ZIP8: (A) mRNA is significantly induced for 24 h, following infection with M.tb H37Rv (MOI 5:1), as determined by qRT-PCR relative to GAPDH (n = 3) and (B) ZIP8 protein is robustly increased by infection with M.tb H37Rv or M.bovis BCG (MOI 5:1) between 24 and 72 h, as determined by Western blot relative to β-actin (n = 3). (C) The infection of MDMs with mCherry expressing M.tb H37Rv (MOI 5:1) for 48 h leads to the extensive co-localization of ZIP8 with M.tb (yellow; indicated by arrow heads) and TfR1 (abundant white; in merged upper panel) but very limited co-localization with LAMP-1 (negligible white; in merged lower panel) (A, B, and C are unpublished data) (mean ± SEM; * p < 0.05; Prism-7: one-tailed Students t-test). MDM isolation, culture, and infection [54]; qRT-PCR and Western blot of ZIP8 in MDMs [56]; and confocal fluorescence microscopy using an Olympus FV1000-Spectral System at 60× magnification in infected MDMs [67] were performed as previously described. Rabbit polyclonal antiserum anti-peptide to amino acid residues 225 to 243 of human ZIP8 was purchased from Covance (Princeton, NJ, USA). Mouse anti-human monoclonal β-actin (#69101) antibody was purchased from MP Biomedicals (Santa Ana, CA, USA). Mouse anti-human monoclonal CD71 (#334102) antibody was purchased from Biolegend (San Diego, CA, USA). Mouse anti-human monoclonal LAMP-1 (#ab25630) antibody was purchased from Abcam (Cambridge, UK).CC BY · PubMed Central
Figure 3 The hypothetical impact of ZIP8 on MTF-1 expression, as well as the localization and direction of trace element transport in macrophages during early infection with M.tb. Arrows indicate the direction of trace element transport.
Figure 3 The hypothetical impact of ZIP8 on MTF-1 expression, as well as the localization and direction of trace element transport in macrophages during early infection with M.tb. Arrows indicate the direction of trace element transport.CC BY · PubMed Central

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Metadata

Authors
Pyle, C., Azad, A., Papp, A., Sadee, W., Knoell, D., & Schlesinger, L.
Affiliations
  • Department of Molecular Genetics and Microbiology, Duke University, Durham, NC 27710, USA
  • Texas Biomedical Research Institute, San Antonio, TX 78227, USA
  • Center for Pharmacogenomics, Department of Cancer Biology and Genetics, College of Medicine, The Ohio State University Wexner Medical Center, Columbus, OH 43085, USA
  • College of Pharmacy, The University of Nebraska Medical Center, Omaha, NE 68198-6120, USA
Venue
International Journal of Molecular Sciences
Publisher
MDPI AG
Published
2017-11-09
Volume
18
Issue
11
Pages
2375
ISSN
1422-0067
DOI
10.3390/ijms18112375
PMC
PMC5713344
Cited by
31
References
15
Language
en
Licence
creativecommons.org/licenses/by/4.0/ (vor)
Funders
Bill and Melinda Gates Foundation (OPP1130674​)

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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 ›

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