PMCID
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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Data are pooled from multiple fields of view in 2 mice.
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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p < 0.001 Student’s t test. (
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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L) Mice (29-week-old) were treated with 3.5 mg/kg LPS or PBS and 2 h later, livers were harvested without the capsule.
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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KCs and LAMs were FACS-purified and expression of Il1b, Tnf, IL10, and Il18 was examined by qPCR, compared with b-actin.
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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p < 0.05, p < 0.01, p < 0.001, p < 0.0001, one-way ANOVA with Bonferroni post-test.
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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See also Figure S3 and Table S2.
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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To locate the cells identified we performed spatial transcriptomics analysis using Visium.
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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For this, we cut the liver in two distinct orientations to profile both the liver tissue and the capsule (Figures 1C and S2K).
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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We ordered each Visium spot along a spatial trajectory, and annotated portal, periportal, mid, and central zones based on known hepatocyte zonation markers (Halpern et al., 2017; Figures 1D, 1E, and S2L) and confirmed this annotation using confocal microscopy (Figure S2M).
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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By using the reference sc/snRNA-seq data, we then deconvolved each spot into its constituent cell types and investigated how cell abundance changed with zonation (Figures 1F, 1G, and S2N).
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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Validating this approach, cholangiocytes mapped specifically to the portal zones (Aizarani et al., 2019), while KCs were preferentially located in periportal and mid zones (Bonnardel et al., 2019; Gola et al., 2021).
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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While KC location is zonated, we did not identify a strong zonation pattern in the gene expression profiles of KCs (data not shown).
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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We further identified B cells, T cells, endothelial cells (ECs), and stromal cells (SCs) across all zones, while conventional dendritic cells (cDCs) were found at the portal vein (PV), with a minor presence at the central vein (CV) (Figures 1F, 1G, and S2N).
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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To validate these locations at single-cell resolution, we next sought to identify the best cell-specific surface markers that would also work by confocal microscopy.
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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As the fixation step utilized for confocal microscopy often affects the integrity of protein epitopes, it is not possible to predict which antibodies will work spatially on fixed tissue slices.
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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Therefore, to simultaneously screen multiple antibodies to identify those working by microscopy, we performed a second Visium analysis which we complemented with 100 oligo-conjugated antibodies, chosen based on the CITE-seq results (Figure 1H).
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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The antibodies identified to work spatially were then validated at single-cell resolution, using MACSima™ Imaging Cyclic Staining (MICS) technology and a 60-plex antibody panel (Figure 1I).
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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Unfortunately, we could not identify useful surface markers for all populations.
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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For example, we did not identify enough discriminatory surface markers that worked by confocal microscopy to distinguish the cDC subsets.
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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Notably, while CD103 has previously been proposed to distinguish hepatic cDC1s from cDC2s (Eckert et al., 2015), our data demonstrate that this is only expressed by a fraction of these cells (Figure S2O).
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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To confirm the locations of the cDC subsets, we thus turned to Molecular Cartography™ (Resolve BioSciences) that allows for 100-plex spatial mRNA analysis.
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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Genes were selected based on the DEGs from the sc/snRNA-seq data that were also spatially resolved according to Visium.
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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We also identified the portal-central trajectory in this dataset using cholangiocytes genes (Epcam and Spp1) and known zonated hepatocyte genes (Glul, Cyp2e1, Hal, and Sds; Figure S2P).
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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Using expression of Xcr1, Clec9a (cDC1s) and Cd209a, Mgl2, and Clec10a (cDC2s), we confirmed that both cDC1s and cDC2s were localized primarily at the PV (Figure 1J).
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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As cDC2s shared a number of genes with monocyte-derived cells (Figure S2A), we also examined the expression of general monocyte/mac (Cd14, Adgre1, Axl, Mafb, Cx3cr1, and C5ar1) and KC-specific genes (Cd5l and Vsig4) to further validate their identification as bona fide cDC2s (Figure 1J).
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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The punctate nature of mRNA expression in these analyses combined with the dendritic shape of myeloid cells renders it difficult to convincingly determine cell boundaries and to conclude these cDC2s and macs were distinct cells.
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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To validate this, we therefore developed a protocol that combines mRNA detection (RNAScope) with surface protein detection.
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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Examining expression of cDC- or mac-specific mRNAs combined with protein surface markers confirmed the presence of PV cDC1, cDC2s, and non-KC macs (Figure 1K).
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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Taken together, by combining multiple spatial transcriptomic and proteomic approaches, we located all the cells within the murine liver and identified additional heterogeneity within the myeloid cells, not revealed when examining the sc/sn-RNA-seq dataset in isolation.
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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This highlights the power of combining single-cell and spatial proteogenomic techniques to investigate cellular heterogeneity.
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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To better understand the non-KC macs, we zoomed in on myeloid cells (cDCs, KCs, monocytes, and monocyte-derived cells) in our sc/snRNA-seq analysis defining 11 populations (Figures 2A–2C; Table S2).
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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This included KCs, 3 populations of non-KC macs and cells that had a profile intermediate between monocytes and patrolling monocytes or macs, termed transitioning monocytes.
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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Closer inspection of the non-KC macs identified cluster6 as peritoneal macs (Figure 2B).
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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The DEGs between the remaining populations suggested that cluster7 likely resembles capsule macs (Sierro et al., 2017), expressing Cd207 and Cx3cr1 while cluster8 resembles GpnmbSpp1 lipid-associated macrophages (LAMs) we recently described in the fatty liver (Remmerie et al., 2020; Figures 2A–2D).
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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Conversion of the CITE-seq data into an FCS file allowed an in silico gating strategy to be defined (Figure S3A).
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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Validating this, we utilized the strategy to FACS-purify the populations and assess gene expression (Figures S3B–S3D).
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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Fitting with a recent report (Jin et al., 2021), washing the liver prior to digestion enriched the peritoneal macs in the wash fraction, demonstrating these were contaminants on the liver surface rather than being present in the liver tissue itself (Figure S3E).
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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While the CITE-seq markers did not discriminate between cluster7 and cluster8, adding CD207 to the panel enabled the non-KCs to be divided into CD207 and CD207 macs (Figure S3F).
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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Fitting with their designation as capsule macs, the relative abundance of CD207 macs was increased if we dissected and digested the capsule (Figure S3F).
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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However, although Molecular Cartography confirmed the presence of Cd207 macs in the capsule, it also revealed Cd207 macs at the CV, which were rarely found at the PV (Figures 2E–2H and S3G–S3J).
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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Thus, cluster7 consists of both capsule and CV CD207 macs.
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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This finding further demonstrates the need for spatial approaches to confirm cell identities.
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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Molecular Cartography also identified macs at the PVs and CVs expressing Ccr2 and Chil3 (Figures 2G, 2H, S3H, and S3J), resembling transitioning monocytes (cluster11).
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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Finally, a population of Gpnmb-expressing macs were found to be enriched around the bile ducts (Figures 2G, 2H, S3H, S3K, and S3L).
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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As Gpnmb expression is cluster8 specific (Figure 2B), and these cells resemble LAMs (Remmerie et al., 2020), we termed these cells bile-duct LAMs.
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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Figure S3Validated flow cytometry gating strategy for murine myeloid cells, related to Figure 2(A) CITE-seq data from the murine myeloid cells in Figure 2A were exported as an FCS file and an in silico gating strategy identified in FlowJo software.(B) Application of the in silico gating strategy with a 21-color flow cytometry panel.
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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Myeloid cells were pre-gated as live CD45 lineage cells (Ly6GCD19NK1.1B220CD3).
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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Data are representative of 3 experiments with 3–6 mice per experiment.(C) cDC1s, cDC2s, migratory cDCs (Mig.
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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cDCs), peritoneal macs (Peri.
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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Macs), KCs, and non-KC macs (non-KCs) were FACS-purified using gating strategy in (B), mRNA was isolated and qPCR performed to examine expression of indicated genes defining each population to validate their identity.
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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Data are representative of 2 experiments with n = 3–6.(D) Putative peritoneal macs were FACS-purified using gating strategy in (B) and expression of Gata6 was examined by qPCR compared with other hepatic myeloid populations.
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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Data are from a single experiment with n = 6.(E) Peritoneal macs as a % of total macs recovered from the liver using different digestion techniques (in vivo, ex vivo, or capsule) or in supernatants in which livers were washed following removal from the mouse but prior to digestion (wash).
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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Data are from a single experiment with n = 4.
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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p < 0.05, p < 0.01 one-way ANOVA with Bonferroni post-test compared with wash data.(F) Expression of CD14 and CD207 within the non-KC mac population from (B) (left) and % of CD207 and CD207 populations among total macs in livers digested using the ex vivo or in vivo protocols or in dissected and digested liver capsule (right).
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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Data are representative of two experiments with n = 4–5 mice per experiment.
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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p < 0.0001 mixed effects analysis with Tukey’s multiple comparison test.(G) Expression of VSIG4, F4/80, GLUL, and DAPI by confocal microscopy.
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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Insets represent zones featured in Figures 2E, 2G, and S3I.(H) Molecular Cartography of indicated genes and cell types.
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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Insets represent zones featured in Figures 2F, 2H, and S3J.(I) Expression of VSIG4, F4/80, GLUL, and DAPI by confocal microscopy at the central vein.
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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Scale bars, 50 μm.(J) Molecular Cartography of indicated genes and cell types at central vein.(K) Expression of F4/80, EPCAM, CCR2, GPNMB, and DAPI by confocal microscopy at a portal vein (top) or F4/80 or GPNMB alone (bottom).
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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Scale bars, 25 μm.(L) Quantification of % of Gpnmb & Trem2 counts over Adgre1 counts in indicated regions of tissue as assessed using Molecular Cartography data.
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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Each dot represents an individual region.
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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p < 0.05, p > 0.0001 one-way ANOVA with Bonferroni post-test.(M) Expression of DESMIN and F4/80 at the liver capsule and underlying parenchyma (left) or EPCAM, DESMIN and F4/80 at the bile duct by confocal microscopy.
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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PV, portal vein; CV, central vein; HA, hepatic artery; BD, bile duct.
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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Arrows indicate specific cell types, where color corresponds to cell type/markers.
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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All images are representative of 2–6 mice.
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
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Figure S4Protein markers of murine CD45 cell subsets, related to Figure 3(A) CITE-seq data from the murine CD45 cells in Figure 3A were exported as an FCS file and an in silico gating strategy identified in FlowJo.(B) Gated cell overlay of populations identified using strategy in (A).(C) Expression of CD90, CD204, CD73, and CD29 markers by indicated cell types.(D) Expression of indicated protein markers in 60-plex MICS analysis in endothelial cells.(E) Expression of DESMIN, EPCAM, LYVE1, and CD31 at a portal triad (left) with inset (right).(F) Expression of indicated protein markers in 60-plex MICS analysis in stromal cells.(G) Molecular Cartography of indicated genes and cell types at portal vein.
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PMC8809252
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Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
|
PV, portal vein; CV, central vein.
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PMC8809252
|
Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
|
Arrows indicate specific cell types, where color corresponds to cell type/markers.
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PMC8809252
|
Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
|
All images are representative of 2–6 mice.
|
PMC8809252
|
Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
|
Validated flow cytometry gating strategy for murine myeloid cells, related to Figure 2 (A) CITE-seq data from the murine myeloid cells in Figure 2A were exported as an FCS file and an in silico gating strategy identified in FlowJo software. (
|
PMC8809252
|
Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
|
B) Application of the in silico gating strategy with a 21-color flow cytometry panel.
|
PMC8809252
|
Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
|
Myeloid cells were pre-gated as live CD45 lineage cells (Ly6GCD19NK1.1B220CD3).
|
PMC8809252
|
Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
|
Data are representative of 3 experiments with 3–6 mice per experiment. (
|
PMC8809252
|
Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
|
C) cDC1s, cDC2s, migratory cDCs (Mig.
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PMC8809252
|
Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
|
cDCs), peritoneal macs (Peri.
|
PMC8809252
|
Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
|
Macs), KCs, and non-KC macs (non-KCs) were FACS-purified using gating strategy in (B), mRNA was isolated and qPCR performed to examine expression of indicated genes defining each population to validate their identity.
|
PMC8809252
|
Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
|
Data are representative of 2 experiments with n = 3–6. (
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PMC8809252
|
Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
|
D) Putative peritoneal macs were FACS-purified using gating strategy in (B) and expression of Gata6 was examined by qPCR compared with other hepatic myeloid populations.
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PMC8809252
|
Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
|
Data are from a single experiment with n = 6. (
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PMC8809252
|
Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
|
E) Peritoneal macs as a % of total macs recovered from the liver using different digestion techniques (in vivo, ex vivo, or capsule) or in supernatants in which livers were washed following removal from the mouse but prior to digestion (wash).
|
PMC8809252
|
Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
|
Data are from a single experiment with n = 4.
|
PMC8809252
|
Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
|
p < 0.05, p < 0.01 one-way ANOVA with Bonferroni post-test compared with wash data. (
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PMC8809252
|
Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
|
F) Expression of CD14 and CD207 within the non-KC mac population from (B) (left) and % of CD207 and CD207 populations among total macs in livers digested using the ex vivo or in vivo protocols or in dissected and digested liver capsule (right).
|
PMC8809252
|
Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
|
Data are representative of two experiments with n = 4–5 mice per experiment.
|
PMC8809252
|
Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
|
p < 0.0001 mixed effects analysis with Tukey’s multiple comparison test. (
|
PMC8809252
|
Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
|
G) Expression of VSIG4, F4/80, GLUL, and DAPI by confocal microscopy.
|
PMC8809252
|
Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
|
Insets represent zones featured in Figures 2E, 2G, and S3I. (
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PMC8809252
|
Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
|
H) Molecular Cartography of indicated genes and cell types.
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PMC8809252
|
Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
|
Insets represent zones featured in Figures 2F, 2H, and S3J. (
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PMC8809252
|
Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
|
I) Expression of VSIG4, F4/80, GLUL, and DAPI by confocal microscopy at the central vein.
|
PMC8809252
|
Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
|
Scale bars, 50 μm. (
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PMC8809252
|
Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
|
J) Molecular Cartography of indicated genes and cell types at central vein. (
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PMC8809252
|
Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
|
K) Expression of F4/80, EPCAM, CCR2, GPNMB, and DAPI by confocal microscopy at a portal vein (top) or F4/80 or GPNMB alone (bottom).
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PMC8809252
|
Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
|
Scale bars, 25 μm. (
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PMC8809252
|
Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
|
L) Quantification of % of Gpnmb & Trem2 counts over Adgre1 counts in indicated regions of tissue as assessed using Molecular Cartography data.
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PMC8809252
|
Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
|
Each dot represents an individual region.
|
PMC8809252
|
Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
|
p < 0.05, p > 0.0001 one-way ANOVA with Bonferroni post-test. (
|
PMC8809252
|
Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
|
M) Expression of DESMIN and F4/80 at the liver capsule and underlying parenchyma (left) or EPCAM, DESMIN and F4/80 at the bile duct by confocal microscopy.
|
PMC8809252
|
Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
|
PV, portal vein; CV, central vein; HA, hepatic artery; BD, bile duct.
|
PMC8809252
|
Spatial proteogenomics reveals distinct and evolutionarily conserved hepatic macrophage niches.
|
Arrows indicate specific cell types, where color corresponds to cell type/markers.
|
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