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Gene-expression profiles and transcriptional regulatory pathways that underlie the identity and diversity of mouse tissue macrophages
Open accessAbstract
We assessed gene expression in tissue macrophages from various mouse organs. The diversity in gene expression among different populations of macrophages was considerable. Only a few hundred mRNA transcripts were selectively expressed by macrophages rather than dendritic cells, and many of these were not present in all macrophages. Nonetheless, well-characterized surface markers, including MerTK and FcγR1 (CD64), along with a cluster of previously unidentified transcripts, were distinctly and universally associated with mature tissue macrophages. TCEF3, C/EBP-α, Bach1 and CREG-1 were among the transcriptional regulators predicted to regulate these core macrophage-associated genes. The mRNA encoding other transcription factors, such as Gata6, was associated with single macrophage populations. We further identified how these transcripts and the proteins they encode facilitated distinguishing macrophages from dendritic cells.
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“Microglia also express hundreds of genes at higher levels than other macrophage subsets (24–26) that may be influenced by factors present in the CNS microenvironment (25, 27), suggesting mechanisms by which the brain environment influences the activity and functions of one of its primary support cells.”
From An environment-dependent transcriptional network specifies human microglia identity (2017) · cites this paper as [24]
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“Recent work demonstrated that all tissue resident macrophages are different to an extent yet cluster together when compared to monocytes and DCs and that spleen red pulp macrophages were closely associated with microglia14.”
From Identification of a unique TGF-β–dependent molecular and functional signature in microglia (2014) · cites this paper as [14]
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“We also found that organ-resident macrophages in the gut and liver are “microglia-like” as they express Gas6 and Mertk and these genes may have a role in maintaining tissue homeostasis which is consistent with a recent transcriptional profiling of murine tissue macrophages14.”
From Identification of a unique TGF-β–dependent molecular and functional signature in microglia (2014) · cites this paper as [14]
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“FFAR2-deficient mice displayed microglia reminiscent of those found in GF mice (103).”
From The Role of Short-Chain Fatty Acids From Gut Microbiota in Gut-Brain Communication (2020) · cites this paper as [103]
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“we found increased microglial expression of C1q, Csfr1 and Cd34 genes, which are known to be expressed on tissue resident macrophages14.”
From Identification of a unique TGF-β–dependent molecular and functional signature in microglia (2014) · cites this paper as [14]
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“Because macrophages and dendritic cells have similar transcriptomic profiles23–25, we repeated SingleR analysis using published RNA-seq datasets of mouse lung macrophages and dendritic cells26,27 to isolate the macrophages”
From Reference-based analysis of lung single-cell sequencing reveals a transitional profibrotic macrophage (2019) · cites this paper as [25]
In the citing paper
“microglia — but not peripheral myeloid cells — were shown to express P2Y purinoceptor 12 (P2ry12), transmembrane protein 119 (Tmem119), sialic acid binding Ig-like lectin H (Siglech), probable G protein coupled receptor 34 (Gpr34), suppressor of cytokine signalling 3 (Socs3), β-hexosaminidase subunit β (Hexb), olfactomedin-like protein 3 (Olfml3) and Fc receptor-like S, scavenger receptor (Fcrls).”
From Microglial signatures and their role in health and disease (2018) · cites this paper as [29]
In the citing paper
“In the healthy brain, they exhibit a unique molecular homeostatic ‘signature’, consisting of a specific transcriptional profile and surface protein expression pattern, which differs from that of tissue macrophages.”
From Microglial signatures and their role in health and disease (2018) · cites this paper as [29]
In the citing paper
“Tissue micro-environmental factors activate cascades resulting in co-operative binding of certain transcription factors with PU.1, leading to a unique enhancer profile enabling microglial dynamic response to its surrounding micro-environment [24, 72].”
From Transcriptional and Epigenetic Regulation of Microglia in Health and Disease (2019) · cites this paper as [72]
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Nonclassical Ly6C− Monocytes Drive the Development of Inflammatory Arthritis in Mice
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Randolph, G. J., Ivanov, S., Zinselmeyer, B. H., & Scallan, J. P. (2017) · Annual Review of Immunology · doi:10.1146/annurev-immunol-041015-055354 · Cited by 338
“nonlymphoid tissue, is the production of cytokines, which may be coordinated with the expression of molecules like LYVE-1 (66) and TLR-4, which is highly expressed by lymphatic endothelial cells and macrophages, but not DCs, as commonly thought (112, 115).”
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Schraml, B. U., van Blijswijk, J., Zelenay, S., Whitney, P. G., Filby, A. J., Acton, S. E., Rogers, N. C., Moncaut, N., Carvajal, J. J., & Sousa, C. R. E. (2013) · Cell · doi:10.1016/j.cell.2013.07.014 · Cited by 312
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Cardiac macrophages and their role in ischaemic heart disease
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“org) provides an excellent resource for further information.(3) Macrophages have a plethora of divergent functions.”
BackgroundChittezhath, M., Dhillon, M. K., Lim, J. Y., Laoui, D., Shalova, I. N., Teo, Y. L., Chen, J., Kamaraj, R., Raman, L. N. M., Lum, J., et al. (2014) · Immunity · doi:10.1016/j.immuni.2014.09.014 · Cited by 317
“Because NF-kB is a master regulator of many genes known to modulate tumor development, e.g., TNFA, IL6, VEGFA, PTGS2, andMMP (hereafter termed ‘‘protumor genes’’) (Biswas and Lewis, 2010; Karin and Greten, 2005), we began by investigating whether NF-kB activation was responsible for inducing a protumor phenotype in RC…”
BackgroundInfluentialPatel, B., Bansal, S. S., Ismahil, M. A., Hamid, T., Rokosh, G., Mack, M., & Prabhu, S. D. (2018) · JACC: Basic to Translational Science · doi:10.1016/j.jacbts.2017.12.006 · Cited by 297
“Although various phenotypic markers have been used to identify cardiac macrophages (3,4,9,11–14), here we used a gating strategy to differentiate tissue resident and monocyte-derived macrophages using both classical (F4/80) and core (MerTK and CD64) macrophage markers along with CCR2 (12).”
BackgroundMethodInfluentialThe identity and function of microglia in neurodegeneration
Song, W. M., & Colonna, M. (2018) · Nature Immunology · doi:10.1038/s41590-018-0212-1 · Cited by 308
The Many Alternative Faces of Macrophage Activation
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“They claimed to have identified a DC signature (38) as well as markers (Cd64 and Mertk) that defined macrophages as a separate cell type (39).”
BackgroundPulmonary macrophage transplantation therapy
Suzuki, T., Arumugam, P. I., Sakagami, T., Lachmann, N., Chalk, C., Sallese, A., Abe, S., Trapnell, C., Carey, B. C., Moritz, T., et al. (2014) · Nature · doi:10.1038/nature13807 · Cited by 304
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Cytokine Storm—Definition, Causes, and Implications
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Macrophage Plasticity and the Role of Inflammation in Skeletal Muscle Repair
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“In addition to problems of classifying polarized macrophages in different tissues and repair models, a recent study has also suggested that there is considerable heterogeneity in the gene expression pattern of different resident macrophage populations in different tissues [52].”
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Kourtzelis, I., Hajishengallis, G., & Chavakis, T. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.00553 · Cited by 321
Inflammatory dendritic cells in mice and humans
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Macrophage reaction against biomaterials in the mouse model–phenotypes, functions and markers
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Microglial TREM2/DAP12 signaling: a double-edged sword in neural diseases
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“However, microglia are distinct from macrophages in terms of their molecular expression profile (Gautier et al., 2012; Hickman et al., 2013; Butovsky et al., 2014).”
BackgroundWhen Immune Cells Turn Bad—Tumor-Associated Microglia/Macrophages in Glioma
Roesch, S., Rapp, C., Dettling, S., & Herold‐Mende, C. C. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19020436 · Cited by 305
“CD68 X x human/murine [7,76] IBA1 X x human/murine [77] CD11b X x human/murine [78,79] F4/80 X x murine [80] CX3CR1+/CCR2− X human/murine [81,82] CX3CR1−/CCR2+ x human/murine [81,82] CD11b+/CD45low X human/murine [7,23] CD11b+/CD45high x human/murine [7,23] MHC IIhigh x human/murine [83,84] CD80high/CD86high x human/m…”
Macrophages: The Road Less Traveled, Changing Anticancer Therapy
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“A uthor M anuscript A uthor M anuscript A uthor M anuscript A uthor M anuscript expression across the 4 tissue specific macrophage populations; for example, MerTK, which is involved in the phagocytosis of apoptotic cells, as well as mRNA encoding CD14, CD64, and Toll-like receptors (TLR)-4, TLR7, TLR8 and TLR13 [49].”
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“Furthermore, R1 and R2 expressed a macrophage signature (e.g., Fcgr3 and Csf3r; Figure S1K; Gaut- ier et al., 2012) while clustering close to each other (Figures 1G and 1H) apart from the DC-committed precursors.”
Self-citationMetabolic and Epigenetic Coordination of T Cell and Macrophage Immunity
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“Consistent with this functional specialization, different tissue-resident macrophages express tissue-specific genes in addition to genes that enable core macrophage functions, such as phagocytosis and pathogen surveillance (Gautier et al., 2012).”
Single‐cell transcriptomics reveals distinct inflammation‐induced microglia signatures
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Microglia Versus Myeloid Cell Nomenclature during Brain Inflammation
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“In steady state conditions, microglia express surface markers typically present onmanyother tissuemacrophages and/ormonocytes such as CD11b, F4/80, Fc-gamma receptor 1 (CD64), and CD115 (Csf-1R), ionized calcium-binding adaptermolecule 1 (Iba-1) and proto-oncogene tyrosine-protein kinaseMER (MerTK) (Figure 1) (19).”
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“However, as a result of their adaptation to the CNS, microglia exhibit decreased expression of hundreds of transcripts compared with other tissue macrophage populations (93).”
BackgroundUral, B. B., Yeung, S. T., Damani‐Yokota, P., Devlin, J. C., de Vries, M., Vera‐Licona, P., Samji, T., Sawai, C. M., Jang, G., Perez, O. A., et al. (2020) · Science Immunology · doi:10.1126/sciimmunol.aax8756 · Cited by 298
Blood Monocytes and Their Subsets: Established Features and Open Questions
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“Interestingly, when searching for macrophage-specific transcripts in the mouse, CD64 and MerTK have emerged (20).”
BackgroundThe Transcription Factor ZEB2 Is Required to Maintain the Tissue-Specific Identities of Macrophages
Scott, C. L., T’Jonck, W., Martens, L., Todorov, H., Sichien, D., Soen, B., Bonnardel, J., De Prijck, S., Vandamme, N., Cannoodt, R., et al. (2018) · Immunity · doi:10.1016/j.immuni.2018.07.004 · Cited by 299
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“The extension of human DC, monocyte, and macrophage map- ping further enhances the utility of the ImmGen data repository.”
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Dubbelaar, M. L., Kracht, L., Eggen, B. J. L., & Boddeke, E. W. G. M. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.01753 · Cited by 260
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“Here, we primarily focus on tissueresident macrophages, which are characterized by high expression of F4/80, CD64, MerTK, and CD14, long-lived in most tissues and may be of embryonic or monocyte origin (6, 17, 27, 29, 31) (Fig.”
BackgroundMonocyte and macrophage contributions to cardiac remodeling
Hulsmans, M., Sam, F., & Nahrendorf, M. (2015) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2015.11.015 · Cited by 291
“These markers include CD11b, CD45, CD68, CD115, F4/80, Ly-6C and MAC-3 in addition to the core macrophage signature suggested by the Immunological Genome Project, which include FCGR1 and MerTK [75].”
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Macrophage MerTK Promotes Liver Fibrosis in Nonalcoholic Steatohepatitis
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“Macrophages express the highest levels of MerTK among all cell types, including in liver (Gautier et al., 2012; Petta et al., 2016).”
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Self-citationTissue-resident macrophages are locally programmed for silent clearance of apoptotic cells
Roberts, A. W., Lee, B. L., Deguine, J., John, S., Shlomchik, M. J., & Barton, G. M. (2017) · Immunity · doi:10.1016/j.immuni.2017.10.006 · Cited by 261
“For example, the transcription factor PPARg is required for the development and identity of alveolar macrophages as well as splenic red-pulp macrophages (Gautier et al., 2012a; Schneider et al., 2014).”
InfluentialCytosolic DNA‐STING‐NLRP3 axis is involved in murine acute lung injury induced by lipopolysaccharide
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“However, AMFs, unlike DCs, are highly autofluorescent and are F4/80, CD11b, MHCII, SIRPa, CD64, Siglec-F, and Ly-6C.(24,31,32) Although AMFs are mostly considered to be lung-resident cells, they have recently been proposed to migrate to the MLN.”
BackgroundInnate cell communication kick-starts pathogen-specific immunity
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“S1A), we designated these cells macrophages rather than dendritic cells (7, 23).”
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BackgroundAn interactive reference framework for modeling a dynamic immune system
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“For instance, while widely accepted in the literature as sensitive and specific markers of AMs, the use of F480 and CD64 for positive selection may have excluded AMs with lower expression of these molecules (58).”
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BackgroundThe Dual Role of Microglia in ALS: Mechanisms and Therapeutic Approaches
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“As resident macrophages of the brain, microglia have an elaborate repertoire of brain specific functions, sustained by a peculiar gene expression profiling (Gautier et al., 2012).”
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“Transcriptional analysis of mouse macrophage populations from different tissues demonstrates minimal overlap in mRNA expression, reflecting a divergence in gene expression patterns (77).”
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CX3CR1-dependent renal macrophage survival promotes Candida control and host survival
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“Of interest, while Cx3cr1 is important for control of Candida proliferation in kidney, liver, and brain, it is not in the spleen, the only organ among those examined in which resident macrophages are Cx3cr1negative (33) and do not depend on Cx3cr1 for tissue accumulation (32).”
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Phenotype Determines Nanoparticle Uptake by Human Macrophages from Liver and Blood
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“With the progressive acquisition of CD64 and the subsequent loss of Ly-6C, the Ly-6C/CD64 plot looked like a waterfall (arrows in Figure 6F), suggesting that lung monocytes might give rise to CpG IMs.”
InfluentialContribution of Microglia‐Mediated Neuroinflammation to Retinal Degenerative Diseases
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“[25] E.”
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“While F4/80 is present on all macrophages, co-expression of CD64 and MerTK exclusively distinguishes macrophages from monocytes 38 .”
BackgroundAdjustment of dendritic cells to the breast-cancer microenvironment is subset specific
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β2 Integrins As Regulators of Dendritic Cell, Monocyte, and Macrophage Function
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“Similarly, signatures for CD8 (CD11b-like) cDCs, pDCs and macrophages were previously identified.(28,29) We performed Agilent microarray analysis and calculated the coverage of genes overexpressed more than 3-fold in CD103 vs.”
MethodPhysiological roles of macrophages
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“Widespread distribution of macrophages is accompanied by substantial tissue-specific phenotypic and gene expression profile differences related to the specific environmental cues in each organ that foster tissue-specific macrophage function [25].”
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“In the yolk sac EMPs differentiate into premacrophages (pMacs) that express a core macrophage program that includes the receptors CX3CR1 and CSF1R, as well as the TFs Maf , Batf3 , Pparg , Irf8 , and zinc finger E-box binding homeobox-2 ( Zeb2 ) (27), a program that persists when these precursors infiltrate various or…”
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Microglia Gone Rogue: Impacts on Psychiatric Disorders across the Lifespan
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“Nonetheless, we are still in a conundrum as microglia have, until now, mostly been investigated as a single entity as compared to other cells of myeloid origin (Hickman et al., 2008; Butovsky et al., 2012, 2014; Gautier et al., 2012; Chiu et al., 2013).”
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“5 (BD Biosciences, 561116), and CD64 BV605 (BD Biosciences, 740406).”
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BackgroundSelf-citationErythrocyte efferocytosis modulates macrophages towards recovery after intracerebral hemorrhage
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“Consistent with the macrophage identity observed by flow cytometry and microscopy, Irf4 À/À monocytes cultured in GM- CSF and IL-4 induced high expression of macrophage-specific genes such as Mertk, Tlr4, and Tlr7 (Gautier et al., 2012) and, unlike WT Mo-DCs, failed to induce DC-associated genes such as Figure 3.”
BackgroundGautier, E. L., Ivanov, S., Williams, J. W., Huang, S. C., Marcelin, G., Fairfax, K. C., Wang, P. L., Francis, J. S., Leone, P., Wilson, D. B., et al. (2014) · The Journal of Experimental Medicine · doi:10.1084/jem.20140570 · Cited by 210
Self-citation
Metadata
- Authors
- the Immunological Genome Consortium, Gautier, E. L., Shay, T., Miller, J., Greter, M., Jakubzick, C., Ivanov, S., Helft, J., Chow, A., Elpek, K. G., Gordonov, S., Mazloom, A. R., Ma'ayan, A., Chua, W.-J., Hansen, T. H., Turley, S. J., Merad, M., & Randolph, G. J.
- Affiliations
- Icahn School of Medicine at Mount Sinai (US)
- Broad Institute (US)
- Mount Sinai Hospital (US)
- Washington University in St. Louis (US)
- Harvard University (US)
- Corresponding author
- Randolph, Gwendalyn J
- ORCID
- Venue
- Nature Immunology
- Published
- 2012-09-30
- Volume
- 13
- Issue
- 11
- Pages
- 1118-1128
- ISSN
- 1529-2908 (ISSN-L)
- 1529-2916
- PMC
- PMC3558276
- OpenAlex
- W2136188258
- Cited by
- 1,972
- References
- 41
- Citations by year
- 2026: 71 · 2025: 88 · 2024: 104 · 2023: 113 · 2022: 152 · 2021: 174 · 2020: 177 · 2019: 155 · 2018: 183 · 2017: 190 · 2016: 159 · 2015: 170 · 2014: 140 · 2013: 90 · 2012: 4
- FWCI
- 56.29
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Immunology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- HAL (submittedVersion)
- DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by-nc-sa)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- National Institute on Drug Abuse (T32DA007135)
- National Cancer Institute (R01CA154947)
- National Institute of General Medical Sciences (P50GM071558, R01GM098316)
- National Institute of Allergy and Infectious Diseases (R01AI049653, R01AI046553, R01AI061741, R24AI072073)
- National Institute of Diabetes and Digestive and Kidney Diseases (R01DK08854, P30DK020579)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Immune cells in cancer
- Life Sciences › Immunology and Microbiology › Immunology › Phagocytosis and Immune Regulation
- Life Sciences › Immunology and Microbiology › Immunology › Atherosclerosis and Cardiovascular Diseases
- Keywords
- tissue macrophages, macrophage heterogeneity, gene expression profiling, macrophage identity, dendritic cells, MERTK, C/EBPα, BACH1, GATA6, mouse organs
- MeSH terms
- Animals, Cell Differentiation, Dendritic Cells, Gene Expression Regulation, Liver, Lung, Macrophages, Organ Specificity, RNA, Messenger, Spleen, Transcription Factors, Transcription, Genetic, Genetic Variation, Antigens, CD, Microglia, Oligonucleotide Array Sequence Analysis, Gene Expression Profiling, Mice
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