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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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“and enhancer-associated histone modifications unique to a local microenvironment.(11,12)”
BackgroundHigh Endothelial Venules: A Vascular Perspective on Tertiary Lymphoid Structures in Cancer
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BackgroundMethodResident tissue macrophages: Key coordinators of tissue homeostasis beyond immunity
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“In summary, the identity of RTMs is fully established in their tissue of residency, and therefore, RTMs are different in every tissue and in every organ ( 26 , 31 – 33 ).”
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“Recent data of gene expression profiles from distinct mouse tissue macrophages suggest that Siglece is also detected in microglia (Gautier et al., 2012), the resident immune cells of the CNS. Microglia execute innate immunity, participate in adaptive immune responses, and facilitate tissue…”
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Subretinal mononuclear phagocytes induce cone segment loss via IL-1β
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“In the meanwhile, genes related to proinflammatory cytokines, including lysozyme (LYZ), S100A8 and S100 calcium binding protein A9 (S100A9) were also highly expressed in cluster 1[33, 34].”
BackgroundBussi, C., Heunis, T. D. J., Pellegrino, E., Bernard, E. M., Bah, N. K., dos Santos, M. S., Santucci, P., Aylan, B., Rodgers, A., Fearns, A., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-34632-8 · Cited by 98
Apoptotic cell identity induces distinct functional responses to IL-4 in efferocytic macrophages
Liebold, I., Al Jawazneh, A., Casar, C., Lanzloth, C., Leyk, S., Hamley, M., Wong, M. N., Kylies, D., Gräfe, S. K., Edenhofer, I., et al. (2024) · Science · doi:10.1126/science.abo7027 · Cited by 96
“…a limited repertoire of phagocytic receptors by macrophages, dependent on their state of activation ( 42 ), origin ( 43 ), and tissue localization ( 44 ), might contribute to differences in the efficiency of wound healing across various tissues that would be depending on the surrounding milieu of…”
BackgroundThe Multifaceted Roles of Macrophages in NAFLD Pathogenesis
Vonderlin, J., Chavakis, T., Sieweke, M., & Tacke, F. (2023) · Cellular and Molecular Gastroenterology and Hepatology · doi:10.1016/j.jcmgh.2023.03.002 · Cited by 96
From top to bottom: midkine and pleiotrophin as emerging players in immune regulation
Sorrelle, N. B., Dominguez, A. T. A., & Brekken, R. A. (2017) · Journal of Leukocyte Biology · doi:10.1189/jlb.3mr1116-475r · Cited by 92
Poznyak, A. V., Nikiforov, N. G., Starodubova, A. V., Попкова, Т. В., & Orekhov, A. N. (2021) · Biomedicines · doi:10.3390/biomedicines9091221 · Cited by 106
“Moreover, it is also important to determine whether the results in mice can be translated into human plaques that have clear phenotypic differences (such as hemorrhage and rupture), in order to develop treatments aimed at reducing the risk of residual inflammation associated with macrophages [58].”
BackgroundNeuroplasticity related to chronic pain and its modulation by microglia
Hiraga, S.-I., Itokazu, T., Nishibe, M., & Yamashita, T. (2022) · Inflammation and Regeneration · doi:10.1186/s41232-022-00199-6 · Cited by 101
Poczobutt, J. M., De, S., Yadav, V. K., Nguyen, T. T., Li, H. Y., Sippel, T. R., Weiser-Evans, M. C. M., & Nemenoff, R. A. (2016) · The Journal of Immunology · doi:10.4049/jimmunol.1502364 · Cited by 97
Johansson, J. U., Pradhan, S., Lokteva, L. A., Woodling, N. S., Ko, N., Brown, H. D., Wang, Q., Loh, C., Cekanaviciute, E., Buckwalter, M., et al. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.2203-13.2013 · Cited by 96
“Interestingly, we noted a 28-fold reduction in levels of microglial EP2 expression as compared with peritoneal macrophage levels, consistent with the broad diversity of gene expression in subpopulations of organspecific macrophages (Gautier et al., 2012) that may in part reflect differences in local microenvironments…”
ResultThe immunological mechanisms that control pneumococcal carriage
Jochems, S. P., Weiser, J. N., Malley, R., & Ferreira, D. M. (2017) · PLoS Pathogens · doi:10.1371/journal.ppat.1006665 · Cited by 98
“Three pneumococcal vaccine formulations are currently licensed, all of which induce humoral responses against a subset of the 98 currently described immunologically distinct capsular polysaccharide serotypes [22, 23].”
BackgroundCecal Ligation and Puncture Results in Long-Term Central Nervous System Myeloid Inflammation
Singer, B. H., Newstead, M. W., Zeng, X., Cooke, C. L., Thompson, R. C., Singer, K., Ghantasala, R., Parent, J. M., Murphy, G. G., Iwashyna, T. J., et al. (2016) · PLoS ONE · doi:10.1371/journal.pone.0149136 · Cited by 104
“CD45/CD11b cells expressed the microglial markers CX3CR1 and CD64 [45] (Fig 4C) and were negative for CCR2 (Fig 4C).”
BackgroundInfluentialFinkernagel, F., Reinartz, S., Lieber, S., Adhikary, T., Wortmann, A., Hoffmann, N., Bieringer, T., Nist, A., Stiewe, T., Jansen, J. M., et al. (2016) · Oncotarget · doi:10.18632/oncotarget.12180 · Cited by 95
Animal Toxins as Therapeutic Tools to Treat Neurodegenerative Diseases
de Souza, J. M., Gonçalves, B. D. C., Gomez, M. V., Vieira, L. B., & Ribeiro, F. M. (2018) · Frontiers in Pharmacology · doi:10.3389/fphar.2018.00145 · Cited by 94
“However, several other studies show opposite results and do not support this notion that M1 is pro and M2 is anti-inflammatory (Gautier et al., 2012; Miller et al., 2012).”
ResultCytomegalovirus subverts macrophage identity
Baasch, S., Giansanti, P., Kolter, J., Riedl, A., Forde, A. J., Runge, S., Zenke, S., Elling, R., Halenius, A., Brabletz, S., et al. (2021) · Cell · doi:10.1016/j.cell.2021.05.009 · Cited by 92
Orchestration of plasma cell differentiation by Bach2 and its gene regulatory network
Igarashi, K., Ochiai, K., Itoh‐Nakadai, A., & Muto, A. (2014) · Immunological Reviews · doi:10.1111/imr.12201 · Cited by 93
“A recent study (70) established that, while tissue macrophages share a signature gene set, they also show distinct patterns of the gene expression depending on their location.”
BackgroundStress and aging act through common mechanisms to elicit neuroinflammatory priming
Fonken, L. K., Frank, M. G., Gaudet, A. D., & Maier, S. F. (2018) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2018.07.012 · Cited by 98
Transcriptional landscape of Mycobacterium tuberculosis infection in macrophages
Roy, S., Schmeier, S., Kaczkowski, B., Arner, E., Alam, T., Ozturk, M., Tamgue, O., Parihar, S. P., Kawaji, H., Itoh, M., et al. (2018) · Scientific Reports · doi:10.1038/s41598-018-24509-6 · Cited by 90
CD11b+ lung dendritic cells at different stages of maturation induce Th17 or Th2 differentiation
Izumi, G., Nakano, H., Nakano, K., Whitehead, G. S., Grimm, S. A., Fessler, M. B., Karmaus, P. W. F., & Cook, D. N. (2021) · Nature Communications · doi:10.1038/s41467-021-25307-x · Cited by 99
Ostkamp, P., Deffner, M., Schulte‐Mecklenbeck, A., Wünsch, C., Lu, I., Wu, G. F., Goelz, S. E., Jager, P. L. D., Kuhlmann, T., Groß, C. C., et al. (2022) · Science Translational Medicine · doi:10.1126/scitranslmed.adc9778 · Cited by 93
Maisonnasse, P., Bouguyon, E., Piton, G., Ezquerra, Á., Urien, C., Deloizy, C., Bourge, M., Leplat, J.-J., Simon, G., Chevalier, C., et al. (2015) · Mucosal Immunology · doi:10.1038/mi.2015.105 · Cited by 94
Metabolic regulation of macrophages in tissues
den Bossche, J. V., & Saraber, D. L. (2018) · Cellular Immunology · doi:10.1016/j.cellimm.2018.01.009 · Cited by 92
Gene expression profiling reveals a conserved microglia signature in larval zebrafish
Mazzolini, J., Clerc, S. L., Morisse, G., Coulonges, C., Kuil, L. E., van Ham, T. J., Zagury, J., & Sieger, D. (2019) · Glia · doi:10.1002/glia.23717 · Cited by 94
“Among other genes, this core signature includes the genes Cx3cr1, Hexb, Itgb5, Olfml3, P2ry12, P2ry13, Rnase4, Slc2a5, Tmem119, Trem2, Gpr34, Siglech, Gpr84, and Socs3 (Beutner et al., 2013; Butovsky et al., 2013; Chiu et al., 2013; Gautier et al., 2012; Hickman et al., 2013; Zhang et al., 2014).”
Deinhardt‐Emmer, S., Rennert, K., Schicke, E., Cseresnyés, Z., Windolph, M., Nietzsche, S., Heller, R., Siwczak, F., Haupt, K. F., Carlstedt, S., et al. (2020) · Biofabrication · doi:10.1088/1758-5090/ab7073 · Cited by 91
Skeletal muscle inflammation and atrophy in heart failure
Lavine, K. J., & Sierra, O. L. (2017) · Heart Failure Reviews · doi:10.1007/s10741-016-9593-0 · Cited by 96
“While some have considered these monocytes to be Bvascular macrophages,^ they transcriptionally cluster with monocytes and do not express core macrophage transcripts, including Mer tyrosine kinase [33, 48].”
BackgroundProfibrotic Activation of Human Macrophages in Systemic Sclerosis
Bhandari, R., Ball, M. S., Martyanov, V., Popovich, D., Schaafsma, E., Han, S., ElTanbouly, M. A., Orzechowski, N. M., Carns, M. A., Arroyo, E., et al. (2020) · Arthritis & Rheumatology · doi:10.1002/art.41243 · Cited by 90
Lee, S. H., Chaves, M. M., Kamenyeva, O., Gazzinelli-Guimarães, P. H., Kang, B., Pessenda, G., Passelli, K., Tacchini‐Cottier, F., Kabát, J., Jacobsen, E. A., et al. (2020) · Science Immunology · doi:10.1126/sciimmunol.aaz4415 · Cited by 88
“Their ontogeny and tissuespecific cues contribute to the heterogeneity of TRMs (4, 5).”
BackgroundNascimento, M., Huang, S. C., Smith, A. M., Everts, B., Lam, W. Y., Bassity, E., Gautier, E. L., Randolph, G. J., & Pearce, E. J. (2014) · PLoS Pathogens · doi:10.1371/journal.ppat.1004282 · Cited by 90
“However, previous reports preceded the identification of stringent markers of macrophages [19].”
BackgroundResultInfluentialSelf-citationMicroglia metabolism in health and disease
Borst, K., Schwabenland, M., & Prinz, M. (2019) · Neurochemistry International · doi:10.1016/j.neuint.2018.11.006 · Cited by 95
Hawley, C. A., Rojo, R., Raper, A., Sauter, K. A. D., Lisowski, Z. M., Grabert, K., Bain, C. C., Davis, G. M., Louwe, P. A., Ostrowski, M. C., et al. (2018) · The Journal of Immunology · doi:10.4049/jimmunol.1701488 · Cited by 91
Winnall, W. R., & Hedger, M. P. (2013) · Journal of Reproductive Immunology · doi:10.1016/j.jri.2013.01.001 · Cited by 88
Jiang, W., Li, D., Han, R., Zhang, C., Jin, W.-N., Wood, K., Liu, Q., Shi, F., & Hao, J. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1705491114 · Cited by 88
Mouse macrophages show different requirements for phosphatidylserine receptor Tim4 in efferocytosis
Yanagihashi, Y., Segawa, K., Maeda, R., Nabeshima, Y.-I., & Nagata, S. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1705365114 · Cited by 87
Protective features of peripheral monocytes/macrophages in stroke
Gliem, M., Schwaninger, M., & Jander, S. (2016) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2015.11.004 · Cited by 88
van Dinther, D., Stolk, D. A., van de Ven, R., van Kooyk, Y., de Gruijl, T. D., & den Haan, J. M. M. (2017) · Journal of Leukocyte Biology · doi:10.1189/jlb.5mr0217-059rr · Cited by 88
Role of microglia-neuron interactions in diabetic encephalopathy
Liu, Y., Li, M., Zhang, Z., Ye, Y., & Zhou, J. (2017) · Ageing Research Reviews · doi:10.1016/j.arr.2017.12.005 · Cited by 88
Liu, X., Chen, W., Li, W., Li, Y., Priest, J. R., Zhou, B., Wang, J., & Zhou, Z. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.06.092 · Cited by 87
TLR9 Signaling in the Tumor Microenvironment Initiates Cancer Recurrence after Radiotherapy
Gao, C., Kozłowska, A. K., Nechaev, S., Li, H., Zhang, Q., Hossain, D. M. S., Kowolik, C. M., Chu, P. G., Swiderski, P. M., Diamond, D. J., et al. (2013) · Cancer Research · doi:10.1158/0008-5472.can-13-1314 · Cited by 89
Microglia heterogeneity along a spatio–temporal axis: More questions than answers
Silvin, A., & Ginhoux, F. (2018) · Glia · doi:10.1002/glia.23458 · Cited by 90
Chamseddine, A. N., Assi, T., Mir, O., & Chouaïb, S. (2021) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2021.107986 · Cited by 89
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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