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Stroma-Derived Interleukin-34 Controls the Development and Maintenance of Langerhans Cells and the Maintenance of Microglia
Open accessAbstract
Colony stimulating factor-1 (Csf-1) receptor and its ligand Csf-1 control macrophage development, maintenance, and function. The development of both Langerhans cells (LCs) and microglia is highly dependent on Csf-1 receptor signaling but independent of Csf-1. Here we show that in both mice and humans, interleukin-34 (IL-34), an alternative ligand for Csf-1 receptor, is produced by keratinocytes in the epidermis and by neurons in the brain. Mice lacking IL-34 displayed a marked reduction of LCs and a decrease of microglia, whereas monocytes, dermal, and lymphoid tissue macrophages and DCs were unaffected. We identified IL-34 as a nonredundant cytokine for the development of LCs during embryogenesis as well as for their homeostasis in the adult skin. Whereas inflammation-induced repopulation of LCs appears to be dependent on Csf-1, once inflammation is resolved, LC survival is again IL-34-dependent. In contrast, microglia and their yolk sac precursors develop independently of IL-34 but rely on it for their maintenance in the adult brain.
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“Langerhans cells are a unique cell population to the skin organ, where fate‐mapping of macrophages demonstrates in situ proliferation to Langerhans cells in the skin during embryonic development.[ 78 , 79 , 80 , 81 ]”
From Coordinated Development of Immune Cell Populations in Vascularized Skin Organoids from Human Induced Pluripotent Stem Cells (2025) · cites this paper as [81]
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“In the brain, interleukin-34 (IL-34) is an alternative CSF1R ligand supporting microglia survival and differentiation (Greter et al., 2012), and microglia adopt an increasingly ramified morphology and continued maturation far beyond birth.”
From A highly efficient human pluripotent stem cell microglia model displays a neuronal-co-culture-specific expression profile and inflammatory response (2017) · cites this paper as Greter et al., 2012
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“This lineage is mainly regulated by CSFR14 and its ligand, IL-347.”
From Identification of a unique TGF-β–dependent molecular and functional signature in microglia (2014) · cites this paper as [7]
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“Several groups have attempted different cell culture conditions to maintain homeostatic microglia signature and ramified morphology In vitro using a variety of cytokines, such as CSF1, GM-CSF, TGFβ, and IL-34 [73-76].”
From Transcriptional and Epigenetic Regulation of Microglia in Health and Disease (2019) · cites this paper as [75]
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“These factors include IL-34 and TGFβ-1 (Butovsky et al., 2014; Greter et al., 2012; Wang et al., 2012; Yamasaki et al., 2014).”
From iPSC-derived human microglia-like cells to study neurological diseases (2017) · cites this paper as Greter et al., 2012
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“Recently, murine studies identified key cytokines, cell receptors, and transcription factors required for microglia development and survival in vivo.”
From iPSC-derived human microglia-like cells to study neurological diseases (2017) · cites this paper as Greter et al., 2012
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Metadata
- Authors
- Greter, M., Lelios, I., Pelczar, P., Hoeffel, G., Price, J., Leboeuf, M., Kündig, T. M., Frei, K., Ginhoux, F., Merad, M., & Becher, B.
- Affiliations
- University of Zurich (CH)
- Agency for Science, Technology and Research (SG)
- Icahn School of Medicine at Mount Sinai (US)
- University Hospital Zurich (CH)
- Corresponding author
- Greter, Melanie
- ORCID
- Venue
- Immunity
- Publisher
- Elsevier BV
- Published
- 2012-12
- Volume
- 37
- Issue
- 6
- Pages
- 1050-1060
- ISSN
- 1074-7613 (ISSN-L)
- PMC
- PMC4291117
- OpenAlex
- W2033985800
- Cited by
- 630
- References
- 28
- Citations by year
- 2026: 35 · 2025: 46 · 2024: 45 · 2023: 40 · 2022: 33 · 2021: 49 · 2020: 56 · 2019: 53 · 2018: 51 · 2017: 52 · 2016: 43 · 2015: 47 · 2014: 49 · 2013: 31
- FWCI
- 20.46
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Immunity (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Zurich Open Repository and Archive (University of Zurich) (submittedVersion)
- Funders
- National Institutes of Health
- Neuroscience Center Zurich, University of Zurich
- National Heart, Lung, and Blood Institute (HL086899, R01HL086899)
- National Cancer Institute (R01CA112100, CA112100)
- National Institute of Allergy and Infectious Diseases (U01AI095611, AI080884, R01AI080884)
- Topics
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Immunology and Microbiology › Immunology › Cytokine Signaling Pathways and Interactions
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Keywords
- IL-34, Langerhans cells, microglia, CSF-1 receptor, keratinocytes, neurons, macrophage development, embryonic development, skin homeostasis, dendritic cells, monocytes
- MeSH terms
- Animals, Brain, Cell Differentiation, Epidermis, Homeostasis, Humans, Inflammation, Interleukins, Langerhans Cells, Psoriasis, Skin, Signal Transduction, Keratinocytes, Receptor, Macrophage Colony-Stimulating Factor, Stromal Cells, Microglia, Mice
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