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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FFAR2-deficient mice displayed microglia reminiscent of those found in germ-free mice.
“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]
The Methods sections on mice and cell identification describe specific-pathogen-free mice and the isolation of resting brain microglia, but do not report an FFAR2-deficient or germ-free comparison (page unavailable). Searches for FFAR2-deficient mice and germ-free microglia found no passage addressing the claimed resemblance. (LLM, conf=0.76)
Experimental — accuracy not yet measuredMacrophages and dendritic cells have similar transcriptomic profiles.
“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]
Microglia, but not peripheral myeloid cells, express P2ry12, Tmem119, Siglech, Gpr34, Socs3, Hexb, Olfml3, and Fcrls.
“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 healthy brain, microglia have a unique homeostatic molecular signature, comprising a distinct transcriptional profile and surface protein expression pattern, which differs from that of tissue macrophages.
“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]
Tissue microenvironmental factors trigger cascades that lead certain transcription factors to bind cooperatively with PU.1, creating a unique enhancer profile that lets microglia respond dynamically to their surroundings.
“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]
Microglia express hundreds of genes at higher levels than other macrophage subsets.
“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]
All tissue resident macrophages are different to an extent yet cluster together when compared to monocytes and DCs, and spleen red pulp macrophages are closely associated with microglia.
“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]
Gas6 and Mertk may have a role in maintaining tissue homeostasis.
“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]
C1q, Csfr1 and Cd34 genes are known to be expressed on tissue resident macrophages.
“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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BackgroundThe cellular and molecular origin of tumor-associated macrophages
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BackgroundCross-tissue organization of the fibroblast lineage
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“Because cardiomyocytes express Cx43 at high levels, we ensured the purity and identity of sorted AV node macrophages by measuring different macrophage(Gautier et al., 2012) and cardiomyocyte-specific markers (Park and Fishman, 2011) in FACS-purified cells.”
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BackgroundMonocyte differentiation and antigen-presenting functions
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Self-citationThe role of macrophages in the resolution of inflammation
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BackgroundReview: Activation patterns of microglia and their identification in the human brain
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Self-Renewing Resident Cardiac Macrophages Limit Adverse Remodeling Following Myocardial Infarction
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“The signatures of adult tissue-resident macrophages of the brain, lung, and liver previously defined by independent research (7, 25, 28) were progressively enriched in our developing resident macrophage populations (fig.”
BackgroundMethodResultFlow Cytometric Analysis of Macrophages and Dendritic Cell Subsets in the Mouse Lung
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“Although CD64/Fcgr1 is often solely expressed by macrophages and monocytes (22), cDC2 can also express CD64 in certain tissues (38) or under specific inflammatory conditions (13).”
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“Consistent with the previous study (Gautier et al., 2012), we found that zinc finger transcription factor GATA6 is uniquely expressed at a high level in peritoneal macrophages compared to tissue-derived, bone-marrow-derived (BMDM) and fetalliver-derivedmacrophages (Figure 1B).”
Bone marrow-derived monocytes give rise to self-renewing and fully differentiated Kupffer cells
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MethodMicroglia in neuropathic pain: cellular and molecular mechanisms and therapeutic potential
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“…Tamoutounour et al., 2012) and inflammatory lung (Plan- tinga et al., 2013) and muscle (Langlet et al., 2012) DCs. Gautier et al. also highlighted heterogeneity within lung CD11b+ DCs, describing CD24+CD64 cells potentially as DCs and CD24 CD64+ cells as macrophages (Gautier et al., 2012).”
BackgroundUnsupervised High-Dimensional Analysis Aligns Dendritic Cells across Tissues and Species
Guilliams, M., Dutertre, C., Scott, C. L., McGovern, N. N., Sichien, D., Chakarov, S., Gassen, S. V., Chen, J., Poidinger, M., Prijck, S. D., et al. (2016) · Immunity · doi:10.1016/j.immuni.2016.08.015 · Cited by 824 · see citing works
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Self-citationNeuroimmunology of Traumatic Brain Injury: Time for a Paradigm Shift
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BackgroundMacrophage heterogeneity in tissues: phenotypic diversity and functions
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“reported in 2012 (157), as part of the Immgen project, on the identity and differences in mouse tissue macrophages; four populations were assessed as a whole, peritoneal, red pulp splenic, lung macrophages, and microglia.”
BackgroundThe human heart contains distinct macrophage subsets with divergent origins and functions
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“We next compared microglia microarray data with data from 22 other myeloid cell types collected by the Immunological Genome Project (ImmGen), including subsets of neutrophils, peripheral macrophages, and monocytes (Gautier et al., 2012).”
Macrophage heterogeneity in the context of rheumatoid arthritis
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Regulation of macrophage development and function in peripheral tissues
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Exosome-Based Cell-Cell Communication in the Tumor Microenvironment
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“In general, based on Th1/Th2 polarization, M1 macrophages are pro-inflammatory and tumoricidal (classically activated), while M2 are anti-inflammatory and tumor supportive (alternatively activated) (Martinez et al., 2008; Gautier et al., 2012; Xue et al., 2014; You et al., 2015).”
BackgroundNeuro-immune Interactions Drive Tissue Programming in Intestinal Macrophages
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Alternatively activated microglia and macrophages in the central nervous system
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TAM receptors regulate multiple features of microglial physiology
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Pleiotropic actions of insulin resistance and inflammation in metabolic homeostasis
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Tissue biology perspective on macrophages
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Role of innate and adaptive immune mechanisms in cardiac injury and repair
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Targeting macrophages in cancer immunotherapy
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Self-citationTissue-specific macrophages: how they develop and choreograph tissue biology
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Macrophage Ontogeny Underlies Differences in Tumor-Specific Education in Brain Malignancies
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“Normalized gene expression data for the Immunological Genome Project (ImmGen) was obtained from the GEO under accession GSE15907 (Gautier et al., 2012).”
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“A useful approach to this comes from recent work that has demonstrated that expression of CD64 (the high affinity FcRc1), F4/80 and MerTK (12, 16, 17), can be used in combination with CD11c and MHCII to define functionally distinct MP populations in mice.”
Method
- 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
About these checks
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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