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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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“…differ from macrophages that reside in other tissues based on their cellspecific gene expression signatures, distinct ontogeny and differential functions (Butovsky et al., 2012; Gautier et al., 2012; Ginhoux et al., 2010; Kierdorf et al., 2013; Prinz and Priller, 2014; Schulz et al., 2012).”
CXCL17 Is a Major Chemotactic Factor for Lung Macrophages
Burkhardt, A. M., Maravillas‐Montero, J. L., Carnevale, C. D., Vilches‐Cisneros, N., Flores, J. P., Hevezi, P. A., & Zlotnik, A. (2014) · The Journal of Immunology · doi:10.4049/jimmunol.1400551 · Cited by 74
Elpek, K. G., Cremasco, V., Shen, H., Harvey, C. J., Wucherpfennig, K. W., Goldstein, D. R., Monach, P. A., & Turley, S. J. (2014) · Cancer Immunology Research · doi:10.1158/2326-6066.cir-13-0209 · Cited by 77
“DC- and macrophage-associated genes were determined previously (12, 13), and a similar analysis was performed to identify neutrophil-associated genes (unpublished data; K.”
BackgroundSelf-citationAre “Resting” Microglia More “M2”?
Cherry, J. D., Olschowka, J. A., & O’Banion, M. K. (2014) · Frontiers in Immunology · doi:10.3389/fimmu.2014.00594 · Cited by 77
“However, it seems that other tissue macrophage cells such as peritoneal, lung, or splenic red pulp macrophages all exhibit greater diversity in their normal gene expression and most likely, basal function when compared to microglia, even though they a share common yolk sac progenitor (1, 34).”
BackgroundLeach, S. M., Gibbings, S. L., Tewari, A., Atif, S. M., Vestal, B. E., Danhorn, T., Janssen, W. J., Wager, T. D., & Jakubzick, C. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.108337 · Cited by 74
“In mice, the co-expression of F4/80 (EMR1) Ly6C, MerTK, and CD64 has helped distinguish DCs from macrophage and monocytes (Atif et al., 2018a, Yu et al., 2015, Misharin et al., 2013, Gautier et al., 2012).”
BackgroundInfluentialSelf-citationCOVID-19 and RA share an SPP1 myeloid pathway that drives PD-L1+ neutrophils and CD14+ monocytes
MacDonald, L., Alivernini, S., Tolusso, B., Elmesmari, A., Somma, D., Perniola, S., Paglionico, A., Petricca, L., Bosello, S. L., Carfì, A., et al. (2021) · JCI Insight · doi:10.1172/jci.insight.147413 · Cited by 72
“TAM pathways are widely expressed by resident macrophages in many tissues (59, 60), and their deregulation has proinflammatory/autoimmune consequences in preclinical animal models (61, 62) and in patients with RA (19).”
BackgroundHaubruck, P., Pinto, M. M., Moradi, B., Little, C. B., & Gentek, R. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.763702 · Cited by 83
The Emerging Understanding of Myeloid Cells as Partners and Targets in Tumor Rejection
Broz, M. L., & Krummel, M. F. (2015) · Cancer Immunology Research · doi:10.1158/2326-6066.cir-15-0041 · Cited by 78
“However, recent advances in the study of the mononuclear phagocytic system in healthy tissues, notably those undertaken by the Immunological Genome Project (ImmGen), have helped to define surface markers and especially geneexpression profiles that more clearly delineate DC, macrophages, and monocytes (23, 24).”
BackgroundDevelopment and Function of Arterial and Cardiac Macrophages
Świrski, F. K., Robbins, C. S., & Nahrendorf, M. (2015) · Trends in Immunology · doi:10.1016/j.it.2015.11.004 · Cited by 78
“Because macrophages arise from different sources and occupy such divergent tissues, do they participate in tissue-specific processes other than phagocytosis? At the molecular level, macrophages from various tissues differ from each other, although they share a transcriptional signature that distinguishes them from oth…”
BackgroundNoristani, H. N., Gerber, Y. N., Sabourin, J.-C., Corre, M. L., Lonjon, N., Mestre‐Francés, N., Hirbec, H., & Perrin, F. E. (2017) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2017.00090 · Cited by 75
Lipid-loaded macrophages as new therapeutic target in cancer
Marelli, G., Morina, N., Portale, F., Pandini, M., Iovino, M., Di Conza, G., Ho, P.-C., & Di Mitri, D. (2022) · Journal for ImmunoTherapy of Cancer · doi:10.1136/jitc-2022-004584 · Cited by 69
Cholesterol 25-hydroxylase promotes efferocytosis and resolution of lung inflammation
Madenspacher, J. H., Morrell, E. D., Gowdy, K. M., McDonald, J. G., Thompson, B. M., Muse, G. W., Martinez, J., Thomas, S. Y., Mikacenic, C. R., Nick, J. A., et al. (2020) · JCI Insight · doi:10.1172/jci.insight.137189 · Cited by 75
“protect cells from 25HC-induced ER stress (43) and is reportedly much more highly expressed in AMs than in macrophages from other tissues (44).”
BackgroundLee, J., Boyce, S., Powers, J., Baer, C. E., Sassetti, C. M., & Behar, S. M. (2020) · PLoS Pathogens · doi:10.1371/journal.ppat.1008621 · Cited by 70
“Using well-described transcriptional gene signatures for DC [32] or macrophages [31], YFP AM, CD11c MDC, and RM were compared to well-defined lung myeloid cell populations from uninfected mice (data from www.”
Cell barrier function of resident peritoneal macrophages in post-operative adhesions
Ito, T., Shintani, Y., Fields, L., Shiraishi, M., Podaru, M., Kainuma, S., Yamashita, K., Kobayashi, K., Perretti, M., Lewis, F., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-22536-y · Cited by 72
Border-associated macrophages as gatekeepers of brain homeostasis and immunity
Vara‐Pérez, M., & Movahedi, K. (2025) · Immunity · doi:10.1016/j.immuni.2025.04.005 · Cited by 84
Macrophage Responses to Environmental Stimuli During Homeostasis and Disease
Rasheed, A., & Rayner, K. J. (2021) · Endocrine Reviews · doi:10.1210/endrev/bnab004 · Cited by 83
Fibroblasts and macrophages: Collaborators in tissue homeostasis
Franklin, R. A. (2021) · Immunological Reviews · doi:10.1111/imr.12989 · Cited by 71
McCowan, J., Fercoq, F., Kirkwood, P. M., T’Jonck, W., Hegarty, L. M., Mawer, C. M., Cunningham, R., Mirchandani, A. S., Hoy, A. M., Humphries, D. C., et al. (2021) · Science Immunology · doi:10.1126/sciimmunol.abj2132 · Cited by 72
“Moreover, about 30% of the core alveolar macrophage signature identified by the ImmGen Consortium (12) was altered by Egr2 deficiency (32 genes) (Fig.”
BackgroundResultInfluentialSiglec‐h on activated microglia for recognition and engulfment of glioma cells
Kopatz, J., Beutner, C., Welle, K., Bodea, L., Reinhardt, J., Claude, J., Linnartz‐Gerlach, B., & Neumann, H. (2013) · Glia · doi:10.1002/glia.22501 · Cited by 76
Can DCs be distinguished from macrophages by molecular signatures?
Hume, D. A., Mabbott, N., Raza, S., & Freeman, T. C. (2013) · Nature Immunology · doi:10.1038/ni.2516 · Cited by 69
Zadran, S., Remacle, F., & Levine, R. D. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1316991110 · Cited by 71
Li, X., Kolling, F., Aridgides, D. S., Mellinger, D., Ashare, A., & Jakubzick, C. (2022) · Life Science Alliance · doi:10.26508/lsa.202201458 · Cited by 76
“Using a curated gene list, we identified twelve major cell types (Complete list of genes: Table E1 and Figure 1B-1D) (17, 18, 26-35).”
MethodSelf-citationHirbec, H., Noristani, H. N., & Perrin, F. E. (2017) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2017.00227 · Cited by 78
“Recent advances in cell-specific transcriptome profiling have been instrumental in uncovering microglial role in both physiological (Bédard et al., 2007; Gautier et al., 2012; Parakalan et al., 2012; Beutner et al., 2013; Butovsky et al., 2014; Orre et al., 2014a; Zhang et al., 2014; Solga et al., 2015; Bennett et al.…”
BackgroundYu, X., Qiu, W., Yang, L., Zhang, Y., He, M., Li, L., & Xu, C. (2019) · The EMBO Journal · doi:10.15252/embj.2018100164 · Cited by 72
Murphy, P. S., Wang, J., Bhagwat, S. P., Munger, J. C., Janssen, W. J., Wright, T. W., & Elliott, M. R. (2017) · Cell Death and Differentiation · doi:10.1038/cdd.2016.159 · Cited by 70
“Adenine nucleotides released by apoptotic cells are converted to adenosine by cell-surface CD73.”
BackgroundInfluentialTranscriptional control of monocyte and macrophage development
Kurotaki, D., Sasaki, H., & Tamura, T. (2017) · International Immunology · doi:10.1093/intimm/dxx016 · Cited by 75
Walter, W., Alonso-Herranz, L., Trappetti, V., Crespo, I., Ibberson, M. R., Cedenilla, M., Karaszewska, A., Núñez, V., Xénarios, I., Arroyo, A. G., et al. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.03.029 · Cited by 71
Notch and TLR signaling coordinate monocyte cell fate and inflammation
Gamrekelashvili, J., Kapanadze, T. G., Sablotny, S., Rațiu, C., Dastagir, K., Lochner, M., Karbach, S. H., Wenzel, P., Sitnow, A., Fleig, S. V., et al. (2020) · eLife · doi:10.7554/elife.57007 · Cited by 73
“, 2015), and published transcriptomic signatures (Chakarov et al., 2019; Gautier et al., 2012; Schlitzer et al., 2015; Vu Manh, Bertho, Hosmalin, Schwartz-Cornil, & Dalod, 2015) were used to assess and visualize the enrichment of obtained gene sets for myeloid populations and define the nature of the”
MethodLi, P. Y., Bearoff, F. M., Zhu, P., Fan, Z., Zhu, Y., Fan, M., Cort, L., Kambayashi, T., Blankenhorn, E. P., & Cheng, H. (2021) · Journal of Controlled Release · doi:10.1016/j.jconrel.2021.01.013 · Cited by 70
“5-MHC-II, FITC-F4/80, APC/Cy7CD86, PE/Cy7-F4/80, and FITC-CD19.”
BackgroundInfluentialCotechini, T., Atallah, A., & Grossman, A. (2021) · Cells · doi:10.3390/cells10040960 · Cited by 74
“Genomic studies have revealed that there is significant genetic diversity among tissue-resident macrophage populations [39] despite sharing a common developmental origin.”
BackgroundGu, C., Geng, X., Wu, Y., Dai, Y., Zeng, J., wang, Z., Fang, H., Sun, Y., & Chen, X. (2023) · Small · doi:10.1002/smll.202305659 · Cited by 76
Transcriptomic Hallmarks of Tumor Plasticity and Stromal Interactions in Brain Metastasis
Wingrove, E., Liu, Z. Z., Patel, K. D., Estape, A. A., Cai, W. L., Melnick, M., Politi, K. A., Monteiro, C., Zhu, L., Valiente, M., et al. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.03.085 · Cited by 67
Aligning bona fide dendritic cell populations across species
Dutertre, C., Wang, L., & Ginhoux, F. (2014) · Cellular Immunology · doi:10.1016/j.cellimm.2014.08.006 · Cited by 69
Macrophages: The Potent Immunoregulatory Innate Immune Cells
Kumar, V. (2019) · IntechOpen eBooks · doi:10.5772/intechopen.88013 · Cited by 76
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Pervizaj-Oruqaj, L., Ferrero, M. R., Matt, U., & Herold, S. (2024) · European Respiratory Review · doi:10.1183/16000617.0263-2023 · Cited by 78
“Their distinct transcriptional signature in mice is characterised by the expression of Ear1, Pparg, Ear1, Chil3, Fabp4/5 and the surface markers F4/80, tyrosine-protein kinase Mer (MerTK), CD64, CD206, CD11c and SiglecF, while lacking CD11b expression [19 – 23].”
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Role of Macrophages in Cardioprotection
Yap, J., Cabrera-Fuentes, H. A., Irei, J. S., Hausenloy, D. J., & Boisvert, W. A. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20102474 · Cited by 72
“Determination between monocytes and macrophages in mouse models is achieved by the differential expression of F4/80/I-Ab/CD11c as well as CD64 and MerTK.”
BackgroundTranscriptomic characterization of microglia activation in a rat model of ischemic stroke
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Conventional Dendritic Cells Impair Recovery after Myocardial Infarction
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Identification and isolation of splenic tissue-resident macrophage sub-populations by flow cytometry
Fujiyama, S., Nakahashi-Oda, C., Abe, F., Wang, Y., Satoh, K., & Shibuya, A. (2018) · International Immunology · doi:10.1093/intimm/dxy064 · Cited by 72
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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