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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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Self-citationFreeman, C. M., Crudgington, S., Stolberg, V. R., Brown, J. P., Sonstein, J., Alexis, N. E., Doerschuk, C. M., Basta, P. V., Carretta, E. E., Couper, D. J., et al. (2015) · Journal of Translational Medicine · doi:10.1186/s12967-014-0374-z · Cited by 48
“This approach was chosen after a preliminary analysis of a variety of alternative gating approaches, including use of Mertk (a putative pan-Mø marker in mice) [26], as the one giving the most unambiguous distinction of mature AMø.”
MethodMacrophage Polarization in IL-10 Treatment of Particle-Induced Inflammation and Osteolysis
Jiang, J., Jia, T., Gong, W., Ning, B., Wooley, P. H., & Yang, S. (2015) · American Journal Of Pathology · doi:10.1016/j.ajpath.2015.09.006 · Cited by 48
Macrophage origin limits functional plasticity in helminth-bacterial co-infection
Rückerl, D., Campbell, S. M., Duncan, S., Sutherland, T. E., Jenkins, S. J., Hewitson, J. P., Barr, T. A., Jackson-Jones, L. H., Maizels, R. M., & Allen, J. E. (2017) · PLoS Pathogens · doi:10.1371/journal.ppat.1006233 · Cited by 47
Phagocytosis of Apoptotic Cells Is Specifically Upregulated in ApoE4 Expressing Microglia in vitro
Muth, C., Hartmann, A., Falla, D. S., Glatzel, M., & Krasemann, S. (2019) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2019.00181 · Cited by 47
Zimmer, T. S., Broekaart, D. W. M., Gruber, V.-E., van Vliet, E. A., Mühlebner, A., & Aronica, E. (2020) · Frontiers in Neurology · doi:10.3389/fneur.2020.01028 · Cited by 48
McFarland, K. N., & Chakrabarty, P. (2022) · Neurotherapeutics · doi:10.1007/s13311-021-01179-3 · Cited by 48
“Homeostatic or resting state microglia constantly surveil the brain, hunting for injury or insult, and express a transcriptional repertoire that includes transmembrane proteins and receptors involved in sensing and responding to environmental signals (the sensome) [149] and rely on TGF-β signaling [150, 151].”
BackgroundUnravelling the sex-specific diversity and functions of adrenal gland macrophages
Dolfi, B., Gallerand, A., Firulyova, M. M., Xu, Y., Merlin, J., Dumont, A., Castiglione, A., Vaillant, N., Quemener, S., Gerke, H., et al. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.110949 · Cited by 50
Self-citationCoagulation signaling and cancer immunotherapy
Ruf, W., & Graf, C. (2020) · Thrombosis Research · doi:10.1016/s0049-3848(20)30406-0 · Cited by 47
Current tools to interrogate microglial biology
Dumas, A. A., Borst, K., & Prinz, M. (2021) · Neuron · doi:10.1016/j.neuron.2021.07.004 · Cited by 47
Microglia and macrophages in glioblastoma: landscapes and treatment directions
Solomou, G., Young, A. M. H., & Bulstrode, H. J. C. J. (2024) · Molecular Oncology · doi:10.1002/1878-0261.13657 · Cited by 54
Heart failure promotes multimorbidity through innate immune memory
Nakayama, Y., Fujiu, K., Oshima, T., Matsuda, J., Sugita, J., Matsubara, T. J., Liu, Y., Goto, K., Kani, K., Uchida, R., et al. (2024) · Science Immunology · doi:10.1126/sciimmunol.ade3814 · Cited by 51
Tyro3, Axl, and Mertk Receptor Signaling in Inflammatory Bowel Disease and Colitis-associated Cancer
Rothlin, C. V., Leighton, J. A., & Ghosh, S. (2014) · Inflammatory Bowel Diseases · doi:10.1097/mib.0000000000000050 · Cited by 48
“More recently, large scale gene expression profiling of tissue resident macrophages including peritoneal macrophages, red pulp splenic macrophages, lung macrophages, and microglia identified Mertk as an universal marker of mature tissue resident macrophages.(70) Axl is more broadly expressed in both hematopoietic and…”
BackgroundF11R Is a Novel Monocyte Prognostic Biomarker for Malignant Glioma
Pong, W. W., Walker, J., Wylie, T., Magrini, V. J., Luo, J. R., Emnett, R. J., Choi, J., Cooper, M. L., Griffith, M., Griffith, O. L., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0077571 · Cited by 50
Bagaitkar, J., Pech, N. K., Ivanov, S., Austin, A. M., Zeng, M. Y., Pallat, S., Huang, G., Randolph, G. J., & Dinauer, M. C. (2015) · Blood · doi:10.1182/blood-2015-05-644773 · Cited by 47
Self-citationKishimoto, D., Kirino, Y., Tamura, M., Takeno, M., Kunishita, Y., Takase‐Minegishi, K., Nakano, H., Kato, I., Nagahama, K., Yoshimi, R., et al. (2018) · Arthritis Research & Therapy · doi:10.1186/s13075-018-1568-1 · Cited by 46
“In contrast, a primary source of Bach1 is monocytes (BioGPS GeneAtlas U133A, gcrma), and Bach1 was identified as one of the core Mφ-associated genes in mice [41], suggesting that Bach1 plays a strong role in innate immunity.”
BackgroundMacrophage‐fibroblast circuits in the spleen
Bellomo, A., Gentek, R., Golub, R., & Bajénoff, M. (2021) · Immunological Reviews · doi:10.1111/imr.12979 · Cited by 45
An inducible transgene reports activation of macrophages in live zebrafish larvae
Sanderson, L. E., Chien, A.-T., Astin, J. W., Crosier, K. E., Crosier, P. S., & Hall, C. J. (2015) · Developmental & Comparative Immunology · doi:10.1016/j.dci.2015.06.013 · Cited by 47
Development of an Optimized Culture System for Generating Mouse Alveolar Macrophage–like Cells
Luo, M., Lai, W., He, Z., & Wu, L. (2021) · The Journal of Immunology · doi:10.4049/jimmunol.2100185 · Cited by 44
Macrophage Involvement in Aging-Associated Skeletal Muscle Regeneration
Cui, C., Ferrucci, L., & Gorospe, M. (2023) · Cells · doi:10.3390/cells12091214 · Cited by 49
“Such tissue-dependent patterns of transcription by macrophages can be determined at least in part by specific tissue microenvironments, which promote the formation of a tissue-specific enhancer landscape and thus establish tissue-dependent gene expression patterns and identities [90,92].”
BackgroundGileles‐Hillel, A., Almendros, I., Khalyfa, A., et al. (2014) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.201406-1149le · Cited by 46
Alveolar-like Stem Cell–derived Myb − Macrophages Promote Recovery and Survival in Airway Disease
Litvack, M. L., Wigle, T. J., Lee, J., Wang, J., Ackerley, C. A., Grunebaum, E., & Post, M. (2016) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.201509-1838oc · Cited by 46
Microglia: A Unique Versatile Cell in the Central Nervous System
Masuda, T., & Prinz, M. (2016) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.5b00317 · Cited by 46
Barreiro, O., Cibrián, D., Clemente, C., Álvarez, D., Moreno, V., Valiente, Í., Bernad, A., Vestweber, D., Arroyo, A. G., Martı́n, P., et al. (2016) · eLife · doi:10.7554/elife.15251 · Cited by 46
“…CD11b+ and expressed similar levels of other myeloid markers such as Ly6C and CD115, as well as of the prototypic macrophage markers CD68 and CD64-MertK (whose combined expression is associated with mature tissue macrophages [Gautier et al., 2012]) (Figure 6A and Figure 6—figure supplement 1A).”
BackgroundLiyanage, S. E., Gardner, P. J., Ribeiro, J., Cristante, E., Sampson, R. D., Luhmann, U. F. O., Ali, R. R., & Bainbridge, J. W. (2016) · Experimental Eye Research · doi:10.1016/j.exer.2016.08.007 · Cited by 49
Makinde, H. M., Winter, D. R., Procissi, D., Mike, E. V., Stock, A. D., Kando, M. J., Gadhvi, G. T., Droho, S., Bloomfield, C. L., Dominguez, S. T., et al. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.00230 · Cited by 45
“1+CD45hi), macrophages (CD11b+CD64+CD45hi), monocytes (CD11b+CD64−CD45hi), as well as microglia (CD11b+CD64+CD45lo).”
BackgroundInfluentialSterile Injury Repair and Adhesion Formation at Serosal Surfaces
Zwicky, S. N., Stroka, D., & Zindel, J. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.684967 · Cited by 46
Saljoughian, N., Wu, Q., Kumar, N., Ganesan, L. P., Lafuse, W. P., & Rajaram, M. V. S. (2021) · Aging Cell · doi:10.1111/acel.13438 · Cited by 48
Immunomodulatory Role of Neuropeptides in the Cornea
Puri, S., Kenyon, B. M., & Hamrah, P. (2022) · Biomedicines · doi:10.3390/biomedicines10081985 · Cited by 44
Chim, L. K., Williams, I. L., Bashor, C. J., & Mikos, A. G. (2023) · Biomaterials · doi:10.1016/j.biomaterials.2023.122076 · Cited by 47
Innate immune sensing of HIV infection
Silvin, A., & Manel, N. (2015) · Current Opinion in Immunology · doi:10.1016/j.coi.2014.12.003 · Cited by 49
Exploring the activated adipogenic niche: Interactions of macrophages and adipocyte progenitors
Lee, Y., Thacker, R. I., Hall, B. K., Kong, R., & Granneman, J. G. (2014) · Cell Cycle · doi:10.4161/cc.27647 · Cited by 46
“Macrophages have been categorized into functionally distinct subsets based on cell surface markers and patterns of cytokine expression.(34,35) Beyond the heterogeneity between tissues, macrophages are often classified according to their activation status.”
BackgroundThe role of chromatin dynamics in immune cell development
Winter, D. R., & Amit, I. (2014) · Immunological Reviews · doi:10.1111/imr.12200 · Cited by 44
“A ImmGen study of expression found great diversity across tissue-resident macrophages from four different tissues (96).”
BackgroundThe renal microenvironment modifies dendritic cell phenotype
Chessa, F., Mathow, D., Wang, S., Hielscher, T., Atzberger, A., Porubský, Š., Gretz, N., Burgdorf, S., Gröne, H., & Popović, Z. V. (2015) · Kidney International · doi:10.1038/ki.2015.292 · Cited by 46
Adult Stem Cells and Skeletal Muscle Regeneration
Costamagna, D., Berardi, E., Ceccarelli, G., & Sampaolesi, M. (2015) · Current Gene Therapy · doi:10.2174/1566523215666150630121024 · Cited by 46
Wei, L., Tokizane, K., Konishi, H., Yu, H., & Kiyama, H. (2017) · Journal of Neuroinflammation · doi:10.1186/s12974-017-0970-y · Cited by 45
“In the central nervous system (CNS), several transcriptome studies have reported GPR84 as one of the signature microglial genes [31, 32].”
Wierer, M., Prestel, M., Schiller, H. B., Yan, G., Schaab, C., Azghandi, S., Werner, J., Kessler, T., Malik, R., Murgia, M., et al. (2017) · Molecular & Cellular Proteomics · doi:10.1074/mcp.ra117.000315 · Cited by 47
“Bioinformatic “annotation enrichment analysis” in Cluster 4 revealed a high prevalence of proteins of the matrisome compartment (25, 26), immune cell gene signatures (45, 46) (p 0.”
BackgroundMethodSelective proliferative response of microglia to alternative polarization signals
Pepe, G., de Maglie, M., Minoli, L., Villa, A., Maggi, A., & Vegeto, E. (2017) · Journal of Neuroinflammation · doi:10.1186/s12974-017-1011-6 · Cited by 10
The diversity of myeloid immune cells shaping wound repair and fibrosis in the lung
Florez‐Sampedro, L., Song, S., & Melgert, B. N. (2018) · Regeneration · doi:10.1002/reg2.97 · Cited by 46
“Depending on their phenotype and role, macrophages can be broadly classified as M1 and M2, although in reality there is a spectrum of phenotypes (Gautier et al., 2012; Hume, 2015).”
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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