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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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BackgroundRNA sensing by conventional dendritic cells is central to the development of lupus nephritis
Celhar, T., Hopkins, R., Thornhill, S. I., Magalhães, R., Hwang, S., Lee, H.-Y., Yasuga, H., Jones, L. A., Casco, J., Lee, B. T. K., et al. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1507052112 · Cited by 58
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“Using novel flow cytometry approaches developed for examining innate immune cells in the lung [26-28] we have been able to quantify changes in several distinct populations during cancer progression.”
BackgroundResultSpronk, H. M. H., Padró, T., Siland, J. E., Prochaska, J. H., Winters, J., van der Wal, A. C., Posthuma, J. J., Lowe, G. D. O., D’Alessandro, E., Wenzel, P., et al. (2018) · Thrombosis and Haemostasis · doi:10.1160/th17-07-0492 · Cited by 62
Harnessing Microglia and Macrophages for the Treatment of Glioblastoma
Prionisti, I., Bühler, L. H., Walker, P. R., & Jolivet, R. (2019) · Frontiers in Pharmacology · doi:10.3389/fphar.2019.00506 · Cited by 63
“However, gene expression profiles and immunophenotyping can provide insights into the functions of the different cell types of the CNS under normal and pathological conditions (Ginhoux et al., 2010; Gautier et al., 2012; Lavin et al., 2014; Zhang et al., 2014; Wieghofer et al., 2015).”
BackgroundMethodTargeting monocytes/macrophages in fibrosis and cancer diseases: Therapeutic approaches
Conte, E. (2021) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2021.108031 · Cited by 61
Kotlyarov, S. N., & Котлярова, А. А. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222312803 · Cited by 59
Park, I., Goddard, M. E., Cole, J. E., Zanin, N., Lyytikäinen, L., Lehtimäki, T. J., Andreakos, E., Feldmann, M., Udalova, I. A., Drozdov, I. A., et al. (2022) · Nature Communications · doi:10.1038/s41467-021-27862-9 · Cited by 61
Holtman, I. R., Noback, M. A., Bijlsma, M., Duong, K. N., van der Geest, M. A., Ketelaars, P. T., Brouwer, N., Vainchtein, I. D., Eggen, B. J. L., & Boddeke, H. W. G. M. (2015) · Glia · doi:10.1002/glia.22810 · Cited by 57
“Studies included are (Beckervordersandforth et al., 2010; Beutner et al., 2013; Cahoy et al., 2008; Chiu et al, 2013; Doyle et al., 2008; Gautier et al., 2012; Hickman et al., 2013; Lovatt et al., 2007; Olah et al., 2012; Orre et al., 2014a, 2014b; Parakalan et al., 2012; Raj et al., 2014;…”
BackgroundTranscriptomic analysis of mononuclear phagocyte differentiation and activation
Hume, D. A., & Freeman, T. C. (2014) · Immunological Reviews · doi:10.1111/imr.12211 · Cited by 60
“They identified a putative DC signature (54) and a set of markers including Cd64 and Mertk that were said to define macrophages (55).”
BackgroundHill, A. A., Anderson‐Baucum, E. K., Kennedy, A. J., Webb, C. D., Yull, F. E., & Hasty, A. H. (2015) · Molecular Metabolism · doi:10.1016/j.molmet.2015.07.005 · Cited by 68
Carpentier, S., Manh, T. V., Chelbi, R., Henri, S., MALISSEN, B., Haniffa, M. A., Ginhoux, F., & Dalod, M. (2016) · Journal of Immunological Methods · doi:10.1016/j.jim.2016.02.023 · Cited by 66
Selective recruitment of non-classical monocytes promotes skeletal muscle repair
Emeterio, C. L. S., Olingy, C. E., Chu, Y., & Botchwey, E. A. (2016) · Biomaterials · doi:10.1016/j.biomaterials.2016.11.021 · Cited by 59
The Innate Immune Response in Myocardial Infarction, Repair, and Regeneration
Gentek, R., & Hoeffel, G. (2017) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-57613-8_12 · Cited by 58
Corneal pain and experimental model development
McKay, T. B., Seyed‐Razavi, Y., Ghezzi, C. E., Dieckmann, G., Nieland, T. J. F., Cairns, D. M., Pollard, R. E., Hamrah, P., & Kaplan, D. L. (2018) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2018.11.005 · Cited by 58
Mitochondria orchestrate macrophage effector functions in atherosclerosis
Dumont, A., Lee, M., Barouillet, T., Murphy, A. J., & Yvan‐Charvet, L. (2020) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2020.100922 · Cited by 60
Tissue-Resident Macrophages in Fungal Infections
Xu, S., & Shinohara, M. L. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.01798 · Cited by 57
“Distinct gene expression patterns were identified among local TRMs from various tissues (6, 7, 16, 17), and are often reflected at the epigenetic level, particularly indicated by differential histone marks on the enhancer landscape (6, 7).”
BackgroundStengel, S., Quickert, S., Lutz, P. L., Ibidapo-Obe, O., Steube, A., Köse-Vogel, N., Yarbakht, M., Reuken, P. A., Busch, M., Brandt, A., et al. (2020) · Gastroenterology · doi:10.1053/j.gastro.2020.01.029 · Cited by 55
Imaging dendritic cell functions*
Bošnjak, B., Do, K. T. H., Förster, R., & Hammerschmidt, S. I. (2021) · Immunological Reviews · doi:10.1111/imr.13050 · Cited by 59
The Gut Microbiome–Brain Crosstalk in Neurodegenerative Diseases
Ghezzi, L., Cantoni, C., Rotondo, E., & Galimberti, D. (2022) · Biomedicines · doi:10.3390/biomedicines10071486 · Cited by 61
“Although the mechanisms involved in controlling the maturation and function of microglia by SCFAs remain unknown, the activation of FFAR2 seems to be involved, since FFAR2-deficient mice displayed the same microglia defect as GF mice [47].”
BackgroundManh, T. V., Marty, H., Sibille, P., Vern, Y. L., Kaspers, B., Dalod, M., Schwartz-Cornil, I., & Quéré, P. (2014) · The Journal of Immunology · doi:10.4049/jimmunol.1303405 · Cited by 57
Molecular Mechanisms of Induction of Tolerant and Tolerogenic Intestinal Dendritic Cells in Mice
Steimle, A., & Frick, J.-S. (2016) · Journal of Immunology Research · doi:10.1155/2016/1958650 · Cited by 57
“The only MPs in the murine intestine that express the proteins CD14, MerTK [9, 14], F4/80, and CD64 [15] are intestinal MΦ.”
Transcriptome Analysis in Domesticated Species: Challenges and Strategies
Hekman, J. P., Johnson, J. L., & Kukekova, A. V. (2015) · Bioinformatics and Biology Insights · doi:10.4137/bbi.s29334 · Cited by 62
Dendritic cell development—History, advances, and open questions
Puhr, S., Lee, J., Zvezdova, E., Zhou, Y. J., & Liu, K. (2015) · Seminars in Immunology · doi:10.1016/j.smim.2016.03.012 · Cited by 71
“Such analyses identified a core set of DC signature genes that differentiate DCs from macrophages, including Flt3, CCR7, Zbtb46, Kit, Btla (encoding CD272) and Dpp (encoding CD26), many of which are consistent with the morphological, behavioral and developmental distinction between DCs and macrophages [67, 69].”
BackgroundAlveolar macrophage development in mice requires L-plastin for cellular localization in alveoli
Todd, E. M., Zhou, J. Y., Szasz, T. P., Deady, L. E., D’Angelo, J. A., Cheung, M. D., Kim, A. H. J., & Morley, S. C. (2016) · Blood · doi:10.1182/blood-2016-03-705962 · Cited by 59
Oh, M. H., Collins, S. L., Sun, I., Tam, A. J., Patel, C. H., Arwood, M. L., Chan‐Li, Y., Powell, J. D., & Horton, M. R. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.08.046 · Cited by 58
“A thorough characterization of ResM4s is relatively lacking; however, transcriptional profiling suggests that ResM4s have a unique gene expression signature (Gautier et al., 2012; Gosselin et al., 2014; Lavin et al., 2014).”
Understanding microglial diversity and implications for neuronal function in health and disease
Schepper, S. D., Crowley, G., & Hong, S. Y. (2020) · Developmental Neurobiology · doi:10.1002/dneu.22777 · Cited by 54
“A key hallmark of tissue-resident macrophages is their unique plasticity to adapt to functional demands of the tissue in which these cells reside (Gautier et al., 2012; Okabe & Medzhitov, 2014).”
BackgroundTools and Approaches for Studying Microglia In vivo
Eme‐Scolan, E., & Dando, S. J. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.583647 · Cited by 60
Sensing the neuronal glycocalyx by glial sialic acid binding immunoglobulin-like lectins
Linnartz-Gerlach, B., Mathews, M., & Neumann, H. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.05.061 · Cited by 54
Alveolar Macrophages: Adaptation to Their Anatomic Niche during and after Inflammation
Martin, F. P., Jacqueline, C., Poschmann, J., & Roquilly, A. (2021) · Cells · doi:10.3390/cells10102720 · Cited by 56
“On the whole-body scale, tissue macrophages differentiation depends on signals given by the macrophage niche [26] but as far as the intrinsic macrophage genetic program is concerned, it is hypothesized that the microenvironment represses proinflammatory genes and promotes an immune tolerance which does make sense in a…”
BackgroundMinireview: Emerging Concepts in Islet Macrophage Biology in Type 2 Diabetes
Morris, D. L. (2015) · Molecular Endocrinology · doi:10.1210/me.2014-1393 · Cited by 57
Bantikassegn, A., Song, X., & Politi, K. A. (2014) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2014-0312ma · Cited by 57
The force awakens: insights into the origin and formation of microglia
Tay, T. L., Hagemeyer, N., & Prinz, M. (2016) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2016.04.003 · Cited by 59
Irvine, K. M., Banh, X., Gadd, V. L., Wojcik, K., Ariffin, J. K., Jose, S., Lukowski, S. W., Baillie, G. J., Sweet, M. J., & Powell, E. E. (2016) · JCI Insight · doi:10.1172/jci.insight.86914 · Cited by 56
“5 (GHI/61), HLA-DR-FITC (L243), CD62L-FITC (DREG-56), SIGLEC-1-APC (7-239), CD11BAPC (ICRF44), and CSF1R-PE (9-4D2-1E4) (all BioLegend); CD16-APC-H7 (3G8; BD Biosciences); CCR2-APC (48607) and CD49F-AF488 (GoH3) (both R&D Systems); and CRIg-PE (6H8, Santa Cruz).”
BackgroundMethodInfluentialExosome and Macrophage Crosstalk in Sleep-Disordered Breathing-Induced Metabolic Dysfunction
Khalyfa, A., Gozal, D., & Gozal, D. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19113383 · Cited by 57
Elsaid, R., Meunier, S., Burlen‐Defranoux, O., Soares‐da‐Silva, F., Perchet, T., Iturri, L., Freyer, L., Vieira, P., Pereira, P., Golub, R., et al. (2020) · Blood · doi:10.1182/blood.2020006779 · Cited by 59
Improved Angiogenesis in Response to Localized Delivery of Macrophage-Recruiting Molecules
Hsu, C.-W., Poché, R. A., Saik, J. E., Ali, S., Wang, S., Yosef, N., Calderon, G. A., Scott, L., Vadakkan, T. J., Larina, I. V., et al. (2015) · PLOS ONE · doi:10.1371/journal.pone.0131643 · Cited by 56
“While our data clearly point to a pro-angiogenic role for macrophages, it is important to consider their tremendous heterogeneity in terms of gene expression and cellular function [70,71].”
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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