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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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STAR: ultrafast universal RNA-seq aligner
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Cutadapt removes adapter sequences from high-throughput sequencing reads
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HTSeq—a Python framework to work with high-throughput sequencing data
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Items 101–200 of 400
Liu, Q., Long, Q., Zhao, J., Wu, W., Lin, Z., Sun, W., Gu, P., Deng, T., Loomes, K. M., Wu, D., et al. (2023) · Research · doi:10.34133/research.0182 · Cited by 42
“The 2 disseminating work to carry out the scRNA-seq study in adipose stromal cells identified the Areg cell as a subpopulation of ASPC, which is characterized by high CD142 expression [9,10].”
BackgroundSelf-citationLiu, S., Shen, S., Yan, Y., Sun, C., Lu, Z., Feng, H., Ma, Y., Tang, Z., Yu, J., Wu, Y., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-31154-1 · Cited by 55
“Additionally, the top group-defining genes reported in previous studies by Burl et al15., Schwalie et al18., and Hepler et al16. were overlaid on our scRNA-seq data for comparison, which revealed similarities for group-defining genes between ours and others (Supplementary Fig.”
ResultDeconstructing cold-induced brown adipocyte neogenesis in mice
Burl, R. B., Rondini, E. A., Wei, H., Piqué-Regi, R., & Granneman, J. G. (2022) · eLife · doi:10.7554/elife.80167 · Cited by 51
“…expression of common mesenchymal stem cell markers Pdgfra, Cd34, and lymphocyte antigen 6 complex locus A (Ly6a, a.k.a. Sca1) (Supplementary Figure 2A) that are often used for identification of adipocyte progenitors (Burl et al. 2018; Hepler et al. 2018; Merrick et al. 2019; Schwalie et al. 2018).”
BackgroundResultInfluentialBrown adipose tissue involution associated with progressive restriction in progenitor competence
Huang, Z., Zhang, Z., Moazzami, Z., Heck, R., Hu, P., Nanda, H. A., Ren, K., Sun, Z., Bartolomucci, A., Gao, Y., et al. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.110575 · Cited by 50
“It colocalized with bona fide mesenchymal markers, including DLK1 and THY1 at the single-cell level, particularly within neonatal group 2 cells (Figures 5A and 5B), suggesting that FSTL1high cells are not likely to be a group of adipogenesis-regulatory cells (Schwalie et al., 2018).”
BackgroundTranscriptional networks controlling stromal cell differentiation
Rauch, A., & Mandrup, S. (2021) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-021-00357-7 · Cited by 57
Tawil, N., Bassawon, R., & Rak, J. W. (2019) · Seminars in Thrombosis and Hemostasis · doi:10.1055/s-0039-1687891 · Cited by 51
Revisiting the multiple roles of T-cadherin in health and disease
Rubina, K. A., Semina, E. V., Kalinina, N., Sysoeva, V., Balatskiy, A. V., & Va, T. (2021) · European Journal of Cell Biology · doi:10.1016/j.ejcb.2021.151183 · Cited by 48
Towards a consensus atlas of human and mouse adipose tissue at single-cell resolution
Loft, A., Emont, M. P., Weinstock, A., Divoux, A., Ghosh, A., Wagner, A., Hertzel, A. V., Maniyadath, B., Deplancke, B., Liu, B., et al. (2025) · Nature Metabolism · doi:10.1038/s42255-025-01296-9 · Cited by 53
“…unique challenges for single-cell sequencing technologies, particularly due to the fragile nature of adipocytes. scRNA-seq approaches have been widely used to profile cells originating from the stromal vascular fraction, such as ASPCs, ECs and immune cells 1,32,81,83,88,90,97,98,113,129–133 .”
Self-citationResident T H 2 cells orchestrate adipose tissue remodeling at a site adjacent to infection
Kabat, A. M., Hackl, A., Sanin, D. E., Zeis, P., Grzes, K. M., Baixauli, F., Kyle, R. L., Caputa, G., Edwards-Hicks, J., Villa, M., et al. (2022) · Science Immunology · doi:10.1126/sciimmunol.add3263 · Cited by 43
“Using published transcription profiles to delineate adipocyte differentiation stages, we identifiedDpp4+ Pi16+ CD55+MPC (C2), intermediate uncommitted cells (C0), and Fabp4+ Pparg+ committed preadipocytes (C1) (16, 42, 43).”
MethodAcetyl-CoA and Metabolite Fluxes Regulate White Adipose Tissue Expansion
Felix, J. B., Cox, A. R., & Hartig, S. M. (2021) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2021.02.008 · Cited by 52
Progenitor-like characteristics in a subgroup of UCP1+ cells within white adipose tissue
Park, J., Shin, S., Liu, L., Jahan, I., Ong, S., Xu, P., Berry, D. C., & Jiang, Y. (2021) · Developmental Cell · doi:10.1016/j.devcel.2021.02.018 · Cited by 45
Enhancing adipose tissue plasticity: progenitor cell roles in metabolic health
Lecoutre, S., Rebière, C., Maqdasy, S., Lambert, M., Dussaud, S., Abatan, J. B., Dugail, I., Gautier, E. L., Clément, K., & Marcelin, G. (2025) · Nature Reviews Endocrinology · doi:10.1038/s41574-024-01071-y · Cited by 52
“Several lines of evidence support the presence of at least three functionally distinct groups of stromal cells in scWAT and vWAT of mice (Supplementary Table 1): the adipocyte stem cells (ASCs), the preadipocytes and the anti-adipogenic progenitors (AAPs) 30–34 ,86 ,92,”
InfluentialYang, Z., Chen, F., Zhang, Y., Ou, M., Tan, P., Xu, X., Li, Q., & Zhou, S. (2024) · MedComm · doi:10.1002/mco2.560 · Cited by 48
“53 Functionally, these cells showed resistance to adipogenesis in vitro and inhibited adipocyte development both in vivo and in vitro through paracrine mechanisms.”
BackgroundInfluentialPlasticity and heterogeneity of thermogenic adipose tissue
Sun, W., Modica, S., Dong, H., & Wolfrum, C. (2021) · Nature Metabolism · doi:10.1038/s42255-021-00417-4 · Cited by 52
Self-citationAdipose tissue plasticity and the pleiotropic roles of BMP signaling
Qian, S., Tang, Y., & Tang, Q. (2021) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2021.100678 · Cited by 56
Transcription factors regulate adipocyte differentiation in beef cattle.
Liu, S., Huang, J., Wang, X., & Ma, Y. (2020) · Animal Genetics · doi:10.1111/age.12931 · Cited by 40
Adipose Stromal Cell Expansion and Exhaustion: Mechanisms and Consequences
Eckel‐Mahan, K. L., Ribas‐Latre, A., & Kolonin, M. G. (2020) · Cells · doi:10.3390/cells9040863 · Cited by 41
“While these populations appear to be conserved in humans [178], relationships between them appear to be depot-specific and remain debated [61].”
BackgroundLiu, X., Yuan, M., Xiang, Q., Li, Z., Xu, F., Chen, W., Chen, J., Huang, J., Yu, N., Zhou, Z., et al. (2022) · Cell Discovery · doi:10.1038/s41421-022-00402-5 · Cited by 55
Retinoic acid signaling in development and differentiation commitment and its regulatory topology
Wu, D., Khan, F. A., Zhang, K., Pandupuspitasari, N. S., Negara, W., Guan, K., Sun, F., & Huang, C. (2023) · Chemico-Biological Interactions · doi:10.1016/j.cbi.2023.110773 · Cited by 37
Immune Cells Gate White Adipose Tissue Expansion
Cox, A. R., Chernis, N., Masschelin, P. M., & Hartig, S. M. (2019) · Endocrinology · doi:10.1210/en.2019-00266 · Cited by 39
Han, J. S., Wang, Y., Qiu, Y., Sun, D., Liu, Y., Li, Z., Zhou, B. Z., Zhang, H., Xiao, Y., Wu, G., et al. (2022) · Cell Discovery · doi:10.1038/s41421-022-00466-3 · Cited by 50
Perivascular stromal cells: Directors of tissue immune niches
Sbierski‐Kind, J., Mroz, N. M., & Molofsky, A. B. (2021) · Immunological Reviews · doi:10.1111/imr.12984 · Cited by 35
Septal LYVE1 + macrophages control adipocyte stem cell adipogenic potential
Yu, X., Hu, Y., Lim, H. Y., Li, Z., Jaitin, D. A., Yang, K. L., Kong, W. T., Xu, J., Bejarano, D. A., Bied, M., et al. (2025) · Science · doi:10.1126/science.adg1128 · Cited by 35
Qi, L., Li, Y., Zhang, L., Li, S., Zhang, X., Li, W., Qin, J., Chen, X., Ji, Y., Xue, Z., et al. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1297484 · Cited by 39
The Heating Microenvironment: Intercellular Cross Talk Within Thermogenic Adipose Tissue
Knights, A. J., Wu, J., & Tseng, Y. (2020) · Diabetes · doi:10.2337/db20-0303 · Cited by 35
Adipose tissue ageing: implications for metabolic health and lifespan
Wang, G., Song, A., & Wang, Q. A. (2025) · Nature Reviews Endocrinology · doi:10.1038/s41574-025-01142-8 · Cited by 40
“…have been discovered to be resistant to adipogenesis and capable of blocking adipogenesis of other APC subpopulations 83–85 , including CD142 + adipogenesis regulator cells in sWAT 84 and PDGFRβ + Ly6C + fibro-inflammatory progenitors in vWAT 83 , which have an anti-adipogenic effect.”
Aging human abdominal subcutaneous white adipose tissue at single cell resolution
Whytock, K. L., Divoux, A., Sun, Y., Pino, M. F., Yu, G., Jin, C. A., Robino, J. J., Plekhanov, A., Varlamov, O., Smith, S. R., et al. (2024) · Aging Cell · doi:10.1111/acel.14287 · Cited by 39
“Stem_2 had an upregulation of F3 (CD142), which is marker of adipogenesis-regulatory (Aregs) cells that are refractory to adipogenesis (Merrick et al., 2019; Schwalie et al., 2018), and aligned with FAP1 marker FOXP2 from Sárvári et al. (2021).”
Cellular origin and clonal evolution of human dedifferentiated liposarcoma
Gruel, N., Quignot, C., Lesage, L., Zein, S. E., Bonvalot, S., Tzanis, D., Raïs, K. A., Quinquis, F., Manciot, B., Vibert, J., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-52067-1 · Cited by 34
“ASC have been widely studied and isolated in mice and human white adipose tissue 34 – 36, 46, 47 .”
Bo, S., Shao, M.-L., Zhang, Q.-B., An, Y. A., Vishvanath, L., & Gupta, R. K. (2021) · Genes & Development · doi:10.1101/gad.348762.121 · Cited by 30
Anti-adipogenic signals at the onset of obesity-related inflammation in white adipose tissue
Caputo, T., Tran, V. D. T., Bararpour, N., Winkler, C., Aguileta, G., Trang, B. K., Attianese, G. M. P. G., Wilson, A., Thomas, A., Pagni, M., et al. (2020) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-020-03485-z · Cited by 31
Adipose Tissue Plasticity: A Comprehensive Definition and Multidimensional Insight
Mo, Y.-Y., Han, Y., Xu, S., Jiang, H., Wu, H., Cai, J., Li, L., Bu, Y., Xiao, F., Liang, H., et al. (2024) · Biomolecules · doi:10.3390/biom14101223 · Cited by 31
Cardiometabolic implications of adipose tissue aging
Ahmed, B., Farb, M. G., & Gokce, N. (2024) · Obesity Reviews · doi:10.1111/obr.13806 · Cited by 32
“45,46 However mechanisms leading to the emergence of ARC sub-populations and how age-related changes in regulatory progenitor function shape body fat patterning or contribute to metabolic disease are not well known.”
Diet Change Improves Obesity and Lipid Deposition in High-Fat Diet-Induced Mice
Ji, T., Fang, B., Wu, F., Liu, Y., Cheng, L., Li, Y., Wang, R., & Zhu, L. (2023) · Nutrients · doi:10.3390/nu15234978 · Cited by 38
“Cells were incubated with the antibody cocktail for 30 min on ice, protected from light, and subjected to fluorescence-activated cell sorting (FACS) using a Becton Dickinson, Franklin Lakes, NJ, USA, FACSAria TM III [32].”
MethodFate of adipocyte progenitors during adipogenesis in mice fed a high-fat diet
Bilal, M., Nawaz, A., Kado, T., Aslam, M. R., Igarashi, Y., Nishimura, A., Watanabe, Y., Kuwano, T., Liu, J., Miwa, H., et al. (2021) · Molecular Metabolism · doi:10.1016/j.molmet.2021.101328 · Cited by 32
Fate of Adipose Progenitor Cells in Obesity-Related Chronic Inflammation
Pyrina, I., Chung, K., Michailidou, Z., Koutsilieris, M., Chavakis, T., & Chatzigeorgiou, A. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.00644 · Cited by 35
MIF-ACKR3 causes irreversible fat loss by impairing adipogenesis in cancer cachexia
Cui, Q., Li, S., Liu, X., Liu, J., Chen, W., Ye, S., Xie, P., Jin, L., Zeng, F., Lv, F., et al. (2025) · Cell Metabolism · doi:10.1016/j.cmet.2025.01.018 · Cited by 31
Zeng, X., Wang, T., Yamaguchi, K., Hatakeyama, S., Yamazaki, S., Shimizu, E., Imoto, S., Furukawa, Y., Johmura, Y., & Nakanishi, M. (2024) · Molecular Metabolism · doi:10.1016/j.molmet.2024.101943 · Cited by 30
“The existence of Ly6C þ fi bro-in fl ammatory progenitors (FIPs) [40], CD142 þ adipose-regulatory cells (Aregs) [41], and Lgals3 þ age-dependent regulatory cells (ARCs) [42] were identi fi ed by scRNA-seq techniques recently.”
BackgroundZachara, M., Rainer, P. Y., Russeil, J., Hashimi, H., Alpern, D., Ferrero, R., Litovchenko, M., & Deplancke, B. (2022) · The EMBO Journal · doi:10.15252/embj.2021108206 · Cited by 36
“Given the particular interest in the F3 + cluster, which was previously identified as representing cells that have inhibitory properties towards adipogenesis (Schwalie et al , 2018), we set out to better understand the specific molecular markers of this population.”
BackgroundMethodResultInfluentialSelf-citationDeconstructing Adipose Tissue Heterogeneity One Cell at a Time
Duerre, D. J., & Galmozzi, A. (2022) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.847291 · Cited by 35
“Specifically, this Areg population exerts anti-adipogenic effects on uncommitted precursors through a Wnt/b-catenin signaling cascade mediated by Rspo2 and Lgr4 (89) Interestingly, Aregs also express high levels ofMeox2 (84), a transcription factor that plays an important role in myogenic differentiation (80).”
BackgroundInfluentialThe Role of Adipocyte Precursors in Development and Obesity
Ying, T., & Simmons, R. A. (2021) · Frontiers in Endocrinology · doi:10.3389/fendo.2020.613606 · Cited by 35
“Functional studies in vitro suggest that they are adipogenesis-regulatory cells (22).”
BackgroundMarcelin, G., Cunha, C. D., Gamblin, C., Suffee, N., Rouault, C., Leclerc, A., Lacombe, A., Sokolovska, N., Gautier, E. L., Clément, K., et al. (2020) · Autophagy · doi:10.1080/15548627.2020.1717129 · Cited by 35
Scalzo, R. L., Foright, R. M., Hull, S., Knaub, L. A., Johnson-Murguia, S., Kinanee, F., Kaplan, J., Houck, J. A., Johnson, G. C., Sharp, R. R., et al. (2021) · Endocrinology · doi:10.1210/endocr/bqab174 · Cited by 29
“3E; Figure 3F (38)), which have previously been described to associate with a negative adipogenic regulatory cell type (AREGs) (47).”
BackgroundFaust, H. J., Cheng, T., Korsunsky, I., Watts, G. F. M., Gal-Oz, S. T., Trim, W. V., Kongthong, S., Jonsson, A. H., Simmons, D. P., Zhang, F., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-52586-x · Cited by 31
“This cluster is negatively enriched for genes involved in adipogenesis and expresses high levels of VIT (encoding the ECM protein VITRIN), which has been shown to actively suppress adipogenesis 29 .”
Circadian mechanisms in adipose tissue bioenergetics and plasticityPreprint
Hepler, C., & Bass, J. T. (2023) · Genes & Development · doi:10.1101/gad.350759.123 · Cited by 35
“Two additional smaller subpopulations were identified and functionally characterized as antiadipogenic: adipose-regulatory cells (Aregs; CD142 and SCA1) and aging-dependent regulatory cells (ARCs; CD36 and Lgals3) (Schwalie et al. 2018; Nguyen et al. 2021).”
BackgroundQuantification of adipocyte numbers following adipose tissue remodeling
Moser, C., Straub, L. G., Rachamin, Y., Dapito, D. H., Kulenkampff, E., Ding, L., Sun, W., Modica, S., Baláž, M., & Wolfrum, C. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109023 · Cited by 27
Self-citationMarrow adipogenic lineage precursor: A new cellular component of marrow adipose tissue
Zhong, L., Yao, L., Seale, P., & Qin, L. (2021) · Best Practice & Research Clinical Endocrinology & Metabolism · doi:10.1016/j.beem.2021.101518 · Cited by 30
Sun, W., von Meyenn, F., Peleg‐Raibstein, D., & Wolfrum, C. (2019) · Advanced Science · doi:10.1002/advs.201900275 · Cited by 31
Self-citationSphingosine 1-Phosphate Regulates Obesity and Glucose Homeostasis
Kajita, K., Ishii, I., Mori, I., Asano, M., Fuwa, M., & Morita, H. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25020932 · Cited by 31
“Thus, visceral adipocytes are substantially different from subcutaneous adipocytes, and single-cell sequencing has recently been used to reveal heterogeneity in adipogenic cells [21,22].”
BackgroundEstradiol cycling drives female obesogenic adipocyte hyperplasia
Saavedra-Peña, R. D. M., Taylor, N., Flannery, C. A., & Rodeheffer, M. S. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.112390 · Cited by 31
Constitutive loss of DNMT3A causes morbid obesity through misregulation of adipogenesis
Tovy, A., Reyes, J. M., Zhang, L., Huang, Y.-H., Rosas, C., Daquinag, A. C., Guzman, A., Ramabadran, R., Chen, C., Gu, T.-P., et al. (2021) · bioRxiv · doi:10.1101/2021.09.13.460063 · Cited by 25
Guo, P., Liu, X., Zhang, P., He, Z., Li, Z., Alini, M., Richards, R. G., Grad, S., Stoddart, M. J., Zhou, G., et al. (2021) · Bioactive Materials · doi:10.1016/j.bioactmat.2021.08.009 · Cited by 27
Cheong, L. Y., & Xu, A. (2021) · Journal of Molecular Cell Biology · doi:10.1093/jmcb/mjab038 · Cited by 28
Thermogenic adipocytes: lineage, function and therapeutic potential
Pollard, A., & Carling, D. (2020) · Biochemical Journal · doi:10.1042/bcj20200298 · Cited by 30
Cell-based therapies for vascular regeneration: Past, present and future
Aghazadeh, Y., Khan, S. T., Nkennor, B., & Nunes, S. S. (2021) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2021.107976 · Cited by 27
Michelotti, T., Kisby, B. R., Flores, L. S., Tegeler, A., Fokar, M., Crasto, C., Menarim, B., Loux, S., & Strieder-Barboza, C. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.1025240 · Cited by 23
Adipocytes Are the Control Tower That Manages Adipose Tissue Immunity by Regulating Lipid Metabolism
Park, J., Sohn, J. H., Han, S. M., Park, Y. J., Huh, J. Y., Choe, S. S., & Kim, J. B. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2020.598566 · Cited by 22
“In the last several years, single cell RNAsequencing (scRNA-seq) has been used to reveal subpopulation and characteristics of ASCs, providing compelling evidence that ASCs would exhibit molecular heterogeneity and functional diversity (94, 95).”
MethodFunctional Heterogeneity of Protein Kinase A Activation in Multipotent Stromal Cells
Tyurin-Kuzmin, P., Karagyaur, M., Kulebyakin, K., Dyikanov, D., Chechekhin, V. I., Ivanova, A. M., Skryabina, M., Arbatskiy, M. S., Sysoeva, V., Kalinina, N., et al. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21124442 · Cited by 23
“Raw data were downloaded from databases ArrayExpress (EBI) иGEO (NCBI, SRA): mouse-derived MSC (E-MTAB-6677) [3], (SRP145475) [4], and human-derived MSC (SRP148833) [19].”
BackgroundMethodInfluentialAdipocyte–progenitor cell communication that influences adipogenesis
Haylett, W. L., & Ferris, W. F. (2019) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-019-03256-5 · Cited by 33
“Recent reports suggest that different subpopulations of ADSCs may influence adipogenic differentiation in a paracrine manner [71].”
Kulebyakin, K. Y., Tyurin‐Kuzmin, P. A., Efimenko, A. Y., Сергеевич, В. Н., Kartoshkin, A., Karagyaur, M. N., Grigorieva, O., Novoseletskaya, E. S., Sysoeva, V., Макаревич, П. И., et al. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.662078 · Cited by 26
“Moreover, published data describe specific populations of MSCs that take the regulatory role and control differentiation processes in surrounding cells (Schwalie et al., 2018).”
BackgroundRondini, E. A., Ramseyer, V. D., Burl, R. B., Piqué-Regi, R., & Granneman, J. G. (2021) · Molecular Metabolism · doi:10.1016/j.molmet.2021.101307 · Cited by 28
A CCL2+DPP4+ subset of mesenchymal stem cells expedites aberrant formation of creeping fat in humans
Wu, F., Wu, F., Zhou, Q., Liu, X., Fei, J., Zhang, D., Wang, W., Tao, Y., Lin, Y., Lin, Q., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-41418-z · Cited by 29
“Previous studies have suggested that MSCs in subcutaneous adipose tissue orchestrate both the expansion and elimination of adipose tissue 15,16 .”
Ni, G., Yang, X., Li, J., Wu, X., Liu, Y., Li, H., Chen, S., Fogarty, C. E., Frazer, I. H., Chen, G., et al. (2021) · Clinical & Translational Immunology · doi:10.1002/cti2.1335 · Cited by 22
PAQR4 regulates adipocyte function and systemic metabolic health by mediating ceramide levels
Zhu, Q., Chen, S., Funcke, J., Straub, L. G., Lin, Q., Zhao, S., Joung, C., Zhang, Z., Kim, D.-S., Li, N., et al. (2024) · Nature Metabolism · doi:10.1038/s42255-024-01078-9 · Cited by 20
“Schwalie et al. 30 defined an anti-adipogenic population of adipogenesis regulators (termed ‘Aregs’), which expressed F3 and Abcg1 ; however, we did not detect Abcg1 in the P3 ( F3 + ) population (Supplementary Fig.”
Wang, H., Du, Y., Huang, S., Sun, X., Ye, Y., Sun, H., Chu, X., Shan, X., Yuan, Y., Shen, L., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-48914-w · Cited by 25
A PPARγ/long noncoding RNA axis regulates adipose thermoneutral remodeling in mice
Zhang, Z., Cui, Y., Su, V., Wang, D., Tol, M. J. P. M., Cheng, L., Wu, X., Kim, J., Rajbhandari, P., Zhang, S., et al. (2023) · Journal of Clinical Investigation · doi:10.1172/jci170072 · Cited by 24
“( 43).”
Single-cell analysis of white adipose tissue reveals the tumor-promoting adipocyte subtypes
Liu, S.-Q., Chen, D.-Y., Li, B., Gao, Z., Feng, H.-F., Yu, X., Liu, Z., Wang, Y., Li, W., Sun, S., et al. (2023) · Journal of Translational Medicine · doi:10.1186/s12967-023-04256-7 · Cited by 21
“Adipocytes, as the most dominant component of WAT, are consist of mature adipocytes and adipose stem and progenitor cells (ASPCs), which are the cells that give birth to mature adipocytes [2].”
BackgroundInfluentialNew discoveries in the field of metabolism by applying single-cell and spatial omics
Xie, B., Gao, D., Zhou, B., Chen, S., & Wang, L. (2023) · Journal of Pharmaceutical Analysis · doi:10.1016/j.jpha.2023.06.002 · Cited by 21
Exploring the heterogeneity of white adipose tissue in mouse and man
Emont, M. P., & Rosen, E. D. (2023) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2023.102045 · Cited by 22
Yoshitake, R., Chang, G., Saeki, K., Ha, D., Wu, X., Wang, J., & Chen, S. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.850568 · Cited by 21
“Fib_3 cells were positive for Gdf10 and F3, which were identified to be the markers for “adipo-regulatory cells” observed in mouse white adipose tissues and skeletal muscle in recent studies (Schwalie et al., 2018; Camps et al., 2020).”
BackgroundAsc-1 regulates white versus beige adipocyte fate in a subcutaneous stromal cell population
Suwandhi, L., Altun, I., Karlina, R., Miok, V., Wiedemann, T., Fischer, D. S., Walzthoeni, T., Lindner, C., Böttcher, A., Heinzmann, S. S., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-21826-9 · Cited by 34
Ladoux, A., Peraldi, P., Chignon‐Sicard, B., & Dani, C. (2021) · Biomedicines · doi:10.3390/biomedicines9010040 · Cited by 26
Lu, S., & Qiao, X. (2020) · Gene · doi:10.1016/j.gene.2020.145347 · Cited by 22
Constantin, A. L., Filippi, A., Alexandru, N., Nemecz, M., & Georgescu, A. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21249598 · Cited by 20
Beisang, D. J., Smith, K. A., Yang, L., Benyumov, A. O., Gilbertsen, A. J., Herrera, J., Lock, E. F., Racila, E. V., Forster, C. L., Sandri, B. J., et al. (2020) · Scientific Reports · doi:10.1038/s41598-020-66630-5 · Cited by 37
Clinical application of single‐cell RNA sequencing in disease and therapy
Nadukkandy, A. S., Kalaiselvan, S., Lin, L., & Luo, Y. (2025) · Clinical and Translational Medicine · doi:10.1002/ctm2.70512 · Cited by 21
“58,59 Combining scRNA-seq and cell trajectory analysis, researchers have identified a new subpopulation of adipocyte progenitor cells, the dipeptidyl peptidase 4 positive DPP4 + population, predominantly within the mesenchyme.”
Advances in Adipose Tissue Biology
Corvera, S., Rajan, A., Townsend, K. L., Shamsi, F., Wu, J., Svensson, K. J., Zeltser, L. M., Collins, S., Reis, T., Tseng, Y., et al. (2025) · Endocrine Reviews · doi:10.1210/endrev/bnaf032 · Cited by 27
Yi, X., Feng, M., Zhu, J., Yu, H., He, Z., Zhang, Z., Zhao, T., Zhang, Q., & Pang, W. (2024) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.4c01044 · Cited by 19
Huang, D., Jiao, X., Huang, S., Liu, J., Si, H., Qi, D., Pei, X., Lu, D., Wang, Y., & Li, Z. (2024) · The Ocular Surface · doi:10.1016/j.jtos.2024.06.005 · Cited by 23
White Adipose Tissue Heterogeneity in the Single-Cell Era: From Mice and Humans to Cattle
Ford, H. R., Liu, Q., Fu, X., & Strieder‐Barboza, C. (2023) · Biology · doi:10.3390/biology12101289 · Cited by 21
“Schwalie et al. [106] had also previously identified an ASPC population with an antiadi-pogenic capacity.”
BackgroundResultInfluentialMesenchymal stromal cells as conductors of adipose tissue remodelingPreprint
Cannavino, J., & Gupta, R. K. (2023) · Genes & Development · doi:10.1101/gad.351069.123 · Cited by 25
“Schwalie et al. (2018) de-finedapreviouslyunrecognizedpopulationofstromalcellsinmice,termed “ Aregs, ” that exerts an antiadipogenic effect on preadipocytes through the production of secreted molecules.”
BackgroundEntropy subspace separation-based clustering for noise reduction (ENCORE) of scRNA-seq data
Song, J., Liu, Y., Zhang, X., Wu, Q.-Y., Gao, J., Wang, W., Li, J., Song, Y.-L., & Yang, C. (2020) · Nucleic Acids Research · doi:10.1093/nar/gkaa1157 · Cited by 19
“Despite the heterogeneity of preadipocytes, it is difficult to identify clearly separated clusters and distinctly expressed markers from scRNA-seq datasets (27,33).”
BackgroundImmune Cell Therapies to Improve Regeneration and Revascularization of Non-Healing Wounds
Groppa, E., Colliva, A., Vuerich, R., Kocijan, T., & Zacchigna, S. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21155235 · Cited by 20
Jossen, V., Muoio, F., Panella, S., Harder, Y., Tallone, T., & Eibl, R. (2020) · Bioengineering · doi:10.3390/bioengineering7030077 · Cited by 19
So, J., Strobel, O., Wann, J., Kim, K., Paul, A., Acri, D. J., Dabin, L. C., Kim, J., Peng, G., & Roh, H. C. (2025) · eLife · doi:10.7554/elife.97981 · Cited by 18
Ferrero, R., Rainer, P. Y., Rumpler, M., Russeil, J., Zachara, M., Pezoldt, J., van Mierlo, G., Gardeux, V., Saelens, W., Alpern, D., et al. (2024) · Cell Metabolism · doi:10.1016/j.cmet.2024.04.017 · Cited by 29
Self-citationIdentification of an adipose tissue-resident pro-preadipocyte population
Chen, M., Kim, S., Li, L., Chattopadhyay, S., Rando, T. A., & Feldman, B. J. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.112440 · Cited by 22
Comprehensive analysis of intercellular communication in the thermogenic adipose niche
Shamsi, F., Zheng, R., Ho, L., Chen, K., & Tseng, Y. (2023) · Communications Biology · doi:10.1038/s42003-023-05140-2 · Cited by 20
“In recent years, single-cell RNA-sequencing (scRNA-seq) analyses of different adipose depots have provided a comprehensive map of adipose resident cell populations, including adipocytes and their progenitors, fibroblasts, different types of immune cells, endothelial cells, vascular smooth muscles, and Schwann cells[8-…”
Transcriptional and epigenetic control of adipocyte remodeling during obesity
Barilla, S., Treuter, E., & Venteclef, N. (2021) · Obesity · doi:10.1002/oby.23248 · Cited by 20
“Furthermore, a newly discovered subpopulation in the SVF of subcutaneous adipose tissue, characterized by high CD124 and ABCG1 expression, was demonstrated to negatively regulate adipogenesis in a paracrine manner (60).”
BackgroundChemically Defined Xeno- and Serum-Free Cell Culture Medium to Grow Human Adipose Stem Cells
Panella, S., Muoio, F., Jossen, V., Harder, Y., Eibl, R., & Tallone, T. (2021) · Cells · doi:10.3390/cells10020466 · Cited by 19
“The results obtained thanks to scRNAseq technology and published recently by a few research groups [45,62,63], reviewed in [130], are very important and cannot be ignored.”
BackgroundInfluentialLischetti, U., Liang, C.-Y., Carrara, M., Coelho, R., Hanns, A., Lombardo, F. C., Dondi, A., Goetze, S., Hensler, M., Kurzeder, C., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-67557-z · Cited by 19
So, J., Strobel, O., Wann, J., Kim, K., Paul, A., Acri, D. J., Dabin, L., Kim, J., & Roh, H. C. (2024) · bioRxiv · doi:10.1101/2024.04.08.588525 · Cited by 17
“…tissues have smaller adipocytes with lower levels of inflammation and hypoxia 15 . 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 18–21 .”
Sinton, M. C., Chandrasegaran, P. R. G., Capewell, P., Cooper, A., Girard, A., Ogunsola, J. O., Perona‐Wright, G., Ngoyi, D. M., Swar, N.-R. K., Bucheton, B., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-42918-8 · Cited by 23
“…committed preadipocyte cluster ( Col4a1 + , Col4a2 + , Col15a1 + , Fabp4 + , Plin2 + ), which represent a transitional state between stem-like preadipocytes and mature adipocytes, and an adipogenesis-regulatorycellcluster( Fmo2 + , F3 + , Clec11a + ),whichareabletosuppress adipogenesis in vivo 50 .”
Liu, J., Si, H., Huang, D., Lu, D., Zou, S., Qi, D., Pei, X., Huang, S., & Li, Z. (2023) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.64.12.18 · Cited by 17
Gupta, A., Efthymiou, V., Kodani, S. D., Shamsi, F., Patti, M., Tseng, Y., & Streets, A. (2023) · Molecular Metabolism · doi:10.1016/j.molmet.2023.101746 · Cited by 23
Neonatal intake of Omega-3 fatty acids enhances lipid oxidation in adipocyte precursors
Varshney, R., Das, S., Trahan, G. D., Farriester, J. W., Mullen, G. P., Kyere-Davies, G., Presby, D. M., Houck, J. A., Webb, P. G., Dzieciątkowska, M., et al. (2022) · iScience · doi:10.1016/j.isci.2022.105750 · Cited by 19
“These findings are consistent with single-cell RNA sequencing findings from others, supporting the possibility of independent APC subtypes.(35,36,39,60)”
ResultThe neutral amino acid transporter SLC7A10 in adipose tissue, obesity and insulin resistance
Jersin, R. Å., Jonassen, L. R., & Dankel, S. N. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.974338 · Cited by 19
“Recent flow cytometry and single-cell RNA sequencing experiments have revealed different compositions of functionally distinct adipocyte progenitor cells within different adipose tissue depots throughout the body, with relevance for insulin resistance and type 2 diabetes (Schwalie et al., 2018; Lee et al., 2019; Raaje…”
BackgroundAdipogenesis in Different Body Depots and Tumor Development
Trivanović, D. I., Vignjević, S., Djordjević, I. O., Кукољ, Т., Bugarski, D. S., & Jauković, A. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.571648 · Cited by 18
Single Cell Gene Expression to Understand the Dynamic Architecture of the Heart
Massaia, A., Cháves, P., Samari, S., Miragaia, R. J., Meyer, K. B., Teichmann, S. A., & Noseda, M. (2018) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2018.00167 · Cited by 20
Characteristic and fate determination of adipose precursors during adipose tissue remodeling
Ye, J., Gao, C. D., Liang, Y., Hou, Z., Shi, Y., & Wang, Y. (2023) · Cell Regeneration · doi:10.1186/s13619-023-00157-8 · Cited by 19
Ciliary control of adipocyte progenitor cell fate regulates energy storage
Scamfer, S. R., Lee, M. D., & Hilgendorf, K. I. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.1083372 · Cited by 19
“These progenitor populations were shown to be functionally similar to the previously identified subpopulations of committed, inhibitory, and pluripotent murine APCs described above (Hepler et al., 2018; Schwalie et al., 2018; Merrick et al., 2019).”
BackgroundResultInfluential
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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