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A stromal cell population that inhibits adipogenesis in mammalian fat depots
Open accessAbstract
Adipocyte development and differentiation have an important role in the aetiology of obesity and its co-morbidities 1,2 . Although multiple studies have investigated the adipogenic stem and precursor cells that give rise to mature adipocytes 3-14 , our understanding of their in vivo origin and properties is incomplete 2,15,16 . This is partially due to the highly heterogeneous and unstructured nature of adipose tissue depots 17 , which has proven difficult to molecularly dissect using classical approaches such as fluorescence-activated cell sorting and Cre-lox lines based on candidate marker genes 16,18 . Here, using the resolving power of single-cell transcriptomics 19 in a mouse model, we reveal distinct subpopulations of adipose stem and precursor cells in the stromal vascular fraction of subcutaneous adipose tissue. We identify one of these subpopulations as CD142 + adipogenesis-regulatory cells, which can suppress adipocyte formation in vivo and in vitro in a paracrine manner. We show that adipogenesis-regulatory cells are refractory to adipogenesis and that they are functionally conserved in humans. Our findings point to a potentially critical role for adipogenesis-regulatory cells in modulating adipose tissue plasticity, which is linked to metabolic control, differential insulin sensitivity and type 2 diabetes.
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“scRNA-seq has been used to characterize the dynamics of cell populations underlying adipose tissue remodeling, with a focus on the cell types within stromal vascular fractions, particularly preadipocytes (Schwalie et al., 2018; Burl et al., 2018; Hepler et al., 2018; Merrick et al., 2019).”
From Robust single-nucleus RNA sequencing reveals depot-specific cell population dynamics in adipose tissue remodeling during obesity (2025) · cites this paper as Schwalie et al., 2018
In the citing paper
“APC3 was identified as ‘adipose regulatory cells’, expressing F3 (encoding CD142) and showed strong expression of secretory signaling proteins (Figure 3A, Figure 3—figure supplement 1C), supporting its paracrine regulatory role (Schwalie et al., 2018).”
From Robust single-nucleus RNA sequencing reveals depot-specific cell population dynamics in adipose tissue remodeling during obesity (2025) · cites this paper as Schwalie et al., 2018
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MethodOmega-3 Fatty Acids Activate Ciliary FFAR4 to Control Adipogenesis
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BackgroundLive-seq enables temporal transcriptomic recording of single cells
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“, 2012); however, as we have demonstrated that culturing changes the transcriptional profile of adipocyte precursors substantially (Schwalie et al., 2018), it is possible that the molecular signature of these cells might be altered.”
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“Interestingly, these populations showed different tendencies towards adipocyte differentiation, including a novel “Areg” population shown to inhibit adipocyte differentiation in a paracrine manner in both mice and humans (46).”
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Deciphering White Adipose Tissue Heterogeneity
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“These include a subpopulation marked by CD142 expression that has the ability to inhibit adipocyte formation termed Adipocyte regulators cells (Areg) [100].”
BackgroundDevelopmental and functional heterogeneity of white adipocytes within a single fat depot
Lee, K. Y., Luong, Q. V., Sharma, R., Dreyfuss, J. M., Ussar, S., & Kahn, C. R. (2018) · The EMBO Journal · doi:10.15252/embj.201899291 · Cited by 118
“This might represent the CD142 + population that was recently discovered to have anti-adipogenic properties (Schwalie et al , 2018) or some other negatively regulatory cell type.”
Aging-dependent regulatory cells emerge in subcutaneous fat to inhibit adipogenesis
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“In obesity, we found changes in vWAT specifically, with ASCs showing increased CD142+ cells, consistent with previous results (Merrick et al., 2019; Schwalie et al., 2018).”
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“19,20 To conclude, scRNA-seq allowed unprecedented direct visualization of MSC heterogeneity, revealing 2 distinct clusters with discrete signature gene sets and signaling pathways.”
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Unveiling adipose populations linked to metabolic health in obesity
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Self-citationPathologic HIF1α signaling drives adipose progenitor dysfunction in obesity
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“identified anti-adipogenic cells in iWAT (termed “Aregs”) that are defined by the expression of F3 (CD142) and Abcg1 (Schwalie et al., 2018).”
BackgroundInfluentialEarly-life inflammation primes a T helper 2 cell–fibroblast niche in skin
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“Indeed, a newly discovered cell population in the perivascular compartment of adipose tissue has been demonstrated to negatively regulate adipogenesis in cell culture and Matrigel implantation models through a paracrine mechanism (Schwalie et al., 2018).”
BackgroundModeling Adipogenesis: Current and Future Perspective
Bahmad, H. F., Daouk, R., Azar, J. H., Sapudom, J., Teo, J. C. M., Abou-Kheir, W. G., & Al‐Sayegh, M. (2020) · Cells · doi:10.3390/cells9102326 · Cited by 74
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Single cell approaches to address adipose tissue stromal cell heterogeneity
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Self-assembling manifolds in single-cell RNA sequencing data
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Mammary gland adipocytes in lactation cycle, obesity and breast cancer
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Interstitial Cell Remodeling Promotes Aberrant Adipogenesis in Dystrophic Muscles
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“Recently, a cell population has been discovered in fat depots that inhibits adipogenesis (Schwalie et al., 2018).”
BackgroundSingle-nucleus transcriptomics identifies separate classes of UCP1 and futile cycle adipocytes
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Self-citationWnt signaling preserves progenitor cell multipotency during adipose tissue development
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Prrx1 marks stem cells for bone, white adipose tissue and dermis in adult mice
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“discovered that there is a new adipocyte subpopulation, CD142+, termed adipocyte regulator cells, which have paracrine actions in regulating adipocytes formation and are more abundant in VAT than in SAT and increased in obesity [49].”
BackgroundTwo Faces of White Adipose Tissue with Heterogeneous Adipogenic Progenitors
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Identification of a regulatory pathway inhibiting adipogenesis via RSPO2
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Self-citationHarnessing adipogenesis to prevent obesity
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“regulating de novo adipogenic capacity of WAT [11].”
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“Most intriguingly, PVAT’s origin largely remains unknown, despite the development of cellular fate mapping and lineage tracing in other fat depots (Sanchez-Gurmaches et al., 2016; Guimaraes-Camboa et al., 2017; Schwalie et al., 2018; Merrick et al., 2019; Shao et al., 2019; Cattaneo et al., 2020).”
BackgroundMosaic Mutant Analysis Identifies PDGFRα/PDGFRβ as Negative Regulators of Adipogenesis
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“Aside from Pdgfr expression and lineage analysis, an important question relates to the in vivo function of PDGFRs in mesenchymal progenitors.”
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Generation of immune cell containing adipose organoids for in vitro analysis of immune metabolism
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“Pro-inflammatory, anti-adipogenic ASC have been found to appear in higher abundance in SAT of aged mice [81, 88, 89] Interestingly, subpopulations of ASC give rise to adipocytes that differ in metabolic properties such as lipolytic activity and fatty acid uptake [87].”
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“…cell types within SVF only, with minimal detection efficiencies for mature adipocytes either in animal models (Burl et al. 2018; Hepler et al. 2018; Schwalie et al. 2018; The Tabula Muris Consortium 2018; Cho et al. 2019; Gu et al. 2019; Jaitin et al. 2019; Merrick et al. 2019; Henriques et al.…”
Adipogenic and SWAT cells separate from a common progenitor in human brown and white adipose depots
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Self-citationEosinophils regulate intra-adipose axonal plasticity
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Novel insights into adipose tissue heterogeneity
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“1 3 (iii) Cd142+ population (PP3) [22].”
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The Impact of Single-Cell Genomics on Adipose Tissue Research
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“Notably, Aregs are functionally conserved in mouse visceral white adipose tissue (WAT) and human adipose tissue, with higher proportions in visceral fat and in all depots of obese individuals.[19] Figure .”
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“The top eight major subclusters constituted 97% of all dFB cells and were defined as reticular/pAD (RET/pAD) dFBs (C1, ~38%, Col1a1+;Cd36+;Icam1+; Cebpb+;Pparg+), RET interstitial (RI) adipogenesis-regulatory (AREG) cells–I (C2, ~16%, F3+;GPX3+) (25), dermal sheath (C3, ~12%, Tagln+;Mest+), dermal papillae (C4, ~10%,…”
BackgroundAdventitial Cuffs: Regional Hubs for Tissue Immunity
Dahlgren, M. W., & Molofsky, A. B. (2019) · Trends in Immunology · doi:10.1016/j.it.2019.08.002 · Cited by 58
“Transcriptionally similar subsets of PGDFRα+ stromal cells have been identified by single cell RNA sequencing of several other mouse tissues, suggesting that ASCs are a functionally conserved adventitial population across multiple organs [37,38], consistent with possible conserved immunologic functions that regulate r…”
BackgroundDistinct adipose progenitor cells emerging with age drive active adipogenesis
Wang, G., Li, G., Song, A., Zhao, Y., Yu, J., Wang, Y., Dai, W., Salas, M. C., Qin, H., Medrano, L. J., et al. (2025) · Science · doi:10.1126/science.adj0430 · Cited by 47
Multilayered omics reveal sex- and depot-dependent adipose progenitor cell heterogeneity
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“Our study is consistent with previous investigations that described analogous cell populations in both humans and mice (Burl et al, 2018; Hepler et al, 2018; Schwalie et al, 2018; Merrick et al, 2019).”
Adipose stem cells in obesity: challenges and opportunities
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Dpp4+ interstitial progenitor cells contribute to basal and high fat diet-induced adipogenesis
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Importance of the Microenvironment and Mechanosensing in Adipose Tissue Biology
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Contribution of adipocytes in the tumor microenvironment to breast cancer metabolism
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MHO or MUO? White adipose tissue remodeling
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“39 The differentiation of APCs into adipocytes, or adipogenesis, is critical for maintaining AT homeostasis, regeneration, and expansion.”
BackgroundSingle-cell sequencing technology in skin wound healing
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“In studies using animal tissues and cells,Schwalie et al. [61] used scRNA-seq to investigate the process of adipogenesis in mammalian fat depots and identified stromal cell populations that inhibit this process.”
Background
Metadata
- Authors
- Schwalie, P. C., Dong, H., Zachara, M., Russeil, J., Alpern, D., Akchiche, N., Caprara, C., Sun, W., Schlaudraff, K.-U., Soldati, G., Wolfrum, C., & Deplancke, B.
- Affiliations
- SIB Swiss Institute of Bioinformatics (CH)
- ETH Zurich (CH)
- Swiss Stem Cell Foundation (CH)
- Corresponding author
- Wolfrum, Christian
- Deplancke, Bart
- ORCID
- Venue
- Nature
- Published
- 2018-06-20
- Volume
- 559
- Issue
- 7712
- Pages
- 103-108
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W2809355409
- Cited by
- 463
- References
- 49
- Citations by year
- 2026: 23 · 2025: 51 · 2024: 77 · 2023: 55 · 2022: 73 · 2021: 77 · 2020: 54 · 2019: 43 · 2018: 10
- FWCI
- 31.71
- Type
- journal article
- Language
- en
- Open access
- green
- infoscience.epfl.ch
- Licence
- cc-by-nc-nd
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Infoscience (Ecole Polytechnique Fédérale de Lausanne) (submittedVersion, cc-by-nc-nd)
- Funders
- Stiftelsen Kristian Gerhard Jebsen
- Public Health Agency of Canada
- École Polytechnique Fédérale de Lausanne
- Topics
- Health Sciences › Medicine › Physiology (medical) › Adipose Tissue and Metabolism
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Adipokines, Inflammation, and Metabolic Diseases
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Peroxisome Proliferator-Activated Receptors
- Keywords
- adipogenesis, adipose-derived stem cells, adipose precursor cells, stromal vascular fraction, paracrine signaling, adipose tissue plasticity, subcutaneous adipose tissue, obesity, type 2 diabetes, insulin sensitivity
- MeSH terms
- Animals, Diabetes Mellitus, Type 2, Female, Humans, Insulin Resistance, Male, Stem Cells, Thromboplastin, Stromal Cells, Adipocytes, Paracrine Communication, Gene Expression Profiling, Subcutaneous Fat, Adipogenesis, Mice, Single-Cell Analysis
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