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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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Does niche competition determine the origin of tissue-resident macrophages?
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“Monocytes are (F4/80/I-Ab/CD11c)low, whereas macrophages are (F4/80/I-Ab/CD11c)high.97 CD64 and myeloid epithelial reproductive tyrosine kinase (MERTK) can also distinguish cardiac monocytes from cardiac macrophages, with macrophages expressing both CD64 and MERTK and monocytes expressing CD64 and not MERTK.19,98 In t…”
BackgroundA local macrophage chemokine network sustains protective tissue-resident memory CD4 T cells
Iijima, N., & Iwasaki, A. (2014) · Science · doi:10.1126/science.1257530 · Cited by 420
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Self-citationTranscription factor IRF4 drives dendritic cells to promote Th2 differentiation
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M1 and M2 Macrophages: The Chicken and the Egg of Immunity
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Fetal monocytes and the origins of tissue-resident macrophages
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Role of Cardiac Macrophages on Cardiac Inflammation, Fibrosis and Tissue Repair
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“In addition, depletion of CMs or deletion of the phagocytic receptor MerTK results in defective elimination of the exophores and mitochondria accumulation in the heart extracellular space, which leads to inflammasome activation, blockage of cardiomyocyte autophagy, accumulation of anomalous mitochondria in cardiomyocy…”
BackgroundAryl hydrocarbon receptor Controls Monocyte Differentiation into dendritic Cells versus Macrophages
Goudot, C., Coillard, A., Villani, A.-C., Gueguen, P., Cros, A., Sarkizova, S., Tang-Huau, T.-L., Bohec, M., Baulande, S., Hacohen, N., et al. (2017) · Immunity · doi:10.1016/j.immuni.2017.08.016 · Cited by 382
Ontogeny and homeostasis of CNS myeloid cells
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Electronic cigarettes disrupt lung lipid homeostasis and innate immunity independent of nicotine
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“Gene expression profiling of resident alveolar macrophages is consistent with an enrichment of genes associated with lipid metabolism, thus highlighting their significant role in pulmonary surfactant homeostasis (36, 37).”
BackgroundTissue-resident macrophages in the intestine are long lived and defined by Tim-4 and CD4 expression
Shaw, T. N., Houston, S. A., Wemyss, K., Bridgeman, H. M., Barbera, T. A., Zangerle-Murray, T., Strangward, P., Ridley, A. J. L., Wang, P., Tamoutounour, S., et al. (2018) · The Journal of Experimental Medicine · doi:10.1084/jem.20180019 · Cited by 395
“1 J, blue highlight; Gautier et al., 2012).”
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“However, this area of investigation has been facilitated by recent high-content molecular studies that have identified homeostatic signature genes (Gautier et al., 2012; Chiu et al., 2013; Orre et al., 2014; Zhang et al., 2014), surface receptors and molecules that constitute a “sensome” (Hickman et al.”
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The Transcription Factor Gata6 Links Tissue Macrophage Phenotype and Proliferative Renewal
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“An additional study (16) identified genes specific to peritoneal macrophages when compared to other tissues and there was a similar over-representation of genes from this list that were down regulated in the absence of Gata6 (Fig.”
Monocytes and macrophages in tissue repair: Implications for immunoregenerative biomaterial design
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Tissue macrophages: origin, heterogenity, biological functions, diseases and therapeutic targets
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“In contrast to DCs, five out of 14 mature macrophage signature genes were differentially expressed, of which three were up-regulated (Gautier et al, 2012).”
ResultNLRP3 inflammasome-driven pathways in depression: clinical and preclinical findings
Kaufmann, F. N., Costa, A. P., Ghisleni, G., Diaz, A. P., Rodrigues, A. L. S., Peluffo, H., & Kaster, M. P. (2017) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2017.03.002 · Cited by 370
“This problem has been solved very recently due to RNAseq profiling of acutely isolated microglia and macrophages from different origins, enabling the establishment of a microglial signature (Gautier et al., 2012; Hickman et al., 2013; Butovsky et al., 2014; Bennett et al., 2016).”
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“CD64 and/or CD24 expression has previously been shown to distinguish macrophages from DC in lungs, peritoneum, and intestines [14, 16].”
BackgroundMethodResultMonocyte and Macrophage Heterogeneity in the Heart
Nahrendorf, M., & Świrski, F. K. (2013) · Circulation Research · doi:10.1161/circresaha.113.300890 · Cited by 376
High-dimensional analysis of the murine myeloid cell system
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Self-citationInfluenza-induced monocyte-derived alveolar macrophages confer prolonged antibacterial protection
Aegerter, H., Kulikauskaite, J., Crotta, S., Patel, H., Kelly, G. P., Hessel, E. M., Mack, M., Beinke, S., & Wack, A. (2020) · Nature Immunology · doi:10.1038/s41590-019-0568-x · Cited by 367
“Overlap of our transcriptional dataset with others 17,29–31 allowed us to retrieve common genes related to a resident, embryonic origin of AMs, such as Marco .”
Microglial Physiology and Pathophysiology: Insights from Genome-wide Transcriptional Profiling
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“Furthermore, when compared to different tissue-resident macrophage subsets, microglia showed a specific or enhanced expression of such genes as Hexb, Tmem119, Siglech, Olfml3, Cx3cr1, Gpr84, Trem2, Socs3, and Fcrls (Gautier et al., 2012).”
BackgroundMethodResultInfluentialThe Cytokine TGF-β Promotes the Development and Homeostasis of Alveolar Macrophages
Yu, X., Buttgereit, A., Lelios, I., Utz, S. G., Cansever, D., Becher, B., & Greter, M. (2017) · Immunity · doi:10.1016/j.immuni.2017.10.007 · Cited by 367
Self-citationPhagocytosis executes delayed neuronal death after focal brain ischemia
Neher, J. J., Emmrich, J., Fricker, M., Mander, P. K., Théry, C., & Brown, G. C. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1308679110 · Cited by 357
“In contrast, MFG-E8 and MerTK show only low expression levels in the naïve brain (20, 21), but are upregulated in response to inflammatory stimuli (9, 22), in accordance with a partially activated microglial phenotype in vitro (23).”
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Bain, C. C., Hawley, C. A., Garner, H., Scott, C. L., Schridde, A., Steers, N. J., Mack, M., Joshi, A., Guilliams, M., Mowat, A. M. I., et al. (2016) · Nature Communications · doi:10.1038/ncomms11852 · Cited by 527
Origin, Differentiation, and Function of Intestinal Macrophages
Bain, C. C., & Schridde, A. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.02733 · Cited by 364
Transcriptional insights into the CD8+ T cell response to infection and memory T cell formation
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Metabolism as a guiding force for immunity
Jung, J., Zeng, H., & Horng, T. (2018) · Nature Cell Biology · doi:10.1038/s41556-018-0217-x · Cited by 354
The Role of Macrophages in Staphylococcus aureus Infection
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The Role of Macrophage Polarization in Infectious and Inflammatory Diseases
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Tissue‐resident macrophages: then and now
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Arg1 expression defines immunosuppressive subsets of tumor-associated macrophages
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“These cells also expressed other canonical macrophage markers (Mrc1, Fn1, Chil3, Ctsb, Stab1, Vegfa, Fcgr1) [30,31].”
Background
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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