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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]
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“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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“(C) Analysis of expression levels of core macrophage cell-surface markers in CD45+F4/80+CD11b+ tMφ for CX3CR1-GFP levels and in CD45+CX3CR1GFP+ for F4/80, CD11b, MCS FR, and MerTK in interstitial CD64hiMHC II− and peritubular CD64loMHC II+ tMφ.”
BackgroundInfluentialInhibition of the CCL2 receptor, CCR2, enhances tumor response to immune checkpoint therapy
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“Bach1 regulates the expression of core macrophage-associated genes, such as aldo-keto reductase family 1 member B10 (Akr1b10), biliverdin reductase B (Blvrb), calcium/calmodulin-dependent protein kinase 1 (Camk1), and glutamate-ammonia ligase (Glul) [68], and both Bach1 and Bach2 promote B-cell development by suppress…”
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BackgroundMethodResultInfluentialTissue-resident ductal macrophages survey the mammary epithelium and facilitate tissue remodelling
Dawson, C. A., Pal, B., Vaillant, F., Gandolfo, L. C., Liu, Z., Blériot, C., Ginhoux, F., Smyth, G. K., Lindeman, G. J., Mueller, S. N., et al. (2020) · Nature Cell Biology · doi:10.1038/s41556-020-0505-0 · Cited by 177
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Complement Factor H Inhibits CD47-Mediated Resolution of Inflammation
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“…contexts, we used a model of acute thioglycollate-induced peritonitis, characterized by an early accumulation of neutrophils, followed by recruited monocyte- derived inflammatory macrophages (recM4), both experiencing an apoptosis-driven elimination at different kinetics (Gautier et al., 2013).”
MethodSelf-citationFlow Cytometry Reveals Similarities Between Lung Macrophages in Humans and Mice
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“We then gated on CD11b++HLA-DR+ cells (6).”
InfluentialOntogeny of Tumor-Associated Macrophages and Its Implication in Cancer Regulation
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Nuclear Receptors License Phagocytosis by Trem2+Myeloid Cells in Mouse Models of Alzheimer's Disease
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“In addition, whereas Mertk is broadly expressed by all the different macrophage subpopulations, Mfge8 is essential for the phagocytosis of apoptotic cells by inflammation-activated macrophages.(11,36) Although the direct”
BackgroundNiche signals and transcription factors involved in tissue-resident macrophage development
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BackgroundPolyphenols: From Classification to Therapeutic Potential and Bioavailability
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Origins, Biology, and Diseases of Tissue Macrophages
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Efferocytosis produces a prometastatic landscape during postpartum mammary gland involution
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Macrophage Proliferation Sustains Adipose Tissue Inflammation in Formerly Obese Mice
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Barrier-tissue macrophages: functional adaptation to environmental challenges
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Macrophages and hepatocellular carcinoma
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The role of tissue resident cells in neutrophil recruitment
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“They also express CD11c, which led us in the past to wonder if they were closely related to DCs, but profiling studies clearly classified them as macrophages (Gautier et al., 2012).”
BackgroundMethodResultInfluentialSelf-citationImmunological Genome Project and systems immunology
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Macrophages in gastrointestinal homeostasis and inflammation
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Control of the Inflammatory Macrophage Transcriptional Signature by miR-155
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“The classical M1 and alternatively activated M2 phenotypes represent in vitro-derived extremes of a spectrum of in vivomacrophage phenotypes that change as a function of the inflammatory milieu [6,7,64].”
BackgroundCellular and Molecular Characterization of Microglia: A Unique Immune Cell Population
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“However, a vast literature suggests that this is only a simplification, with M1 and M2 macrophages representing only the two extremes of a huge spectrum of activation states [6,7].”
BackgroundA common framework of monocyte-derived macrophage activation
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Tissue-resident versus monocyte-derived macrophages in the tumor microenvironment
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Paradoxical role of the proto-oncogene Axl and Mer receptor tyrosine kinases in colon cancer
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“Remarkably, Mer has been recently defined as a distinctive and universal marker of mature, tissue-resident macrophages (38).”
BackgroundInfluentialBrain trauma elicits non-canonical macrophage activation states
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“2), although Fcgr1 has also been suggested to be a marker of monocyte ontogeny [29], in addition to polarization [12, 26].”
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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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