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.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
scRNA-seq has been used to characterize dynamics of cell populations underlying adipose tissue remodeling, focusing on cell types within stromal vascular fractions, particularly preadipocytes.
“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
APC3 was identified as adipose regulatory cells, expressing F3 (encoding CD142) and showing strong expression of secretory signaling proteins, supporting its paracrine regulatory role.
“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
Cites
STAR: ultrafast universal RNA-seq aligner
Dobin, A., Davis, C. A., Schlesinger, F., Drenkow, J., Zaleski, C., Jha, S., Batut, P., Chaisson, M., & Gingeras, T. R. (2013) · Bioinformatics · doi:10.1093/bioinformatics/bts635 · Cited by 51,709 · see citing works
Cutadapt removes adapter sequences from high-throughput sequencing reads
Martin, M. (2011) · EMBnet.journal · doi:10.14806/ej.17.1.200 · Cited by 33,889 · see citing works
A perivascular origin for mesenchymal stem cells in multiple human organs
Crisan, M., Yap, S., Casteilla, L., Chen, C.-W., Corselli, M., Park, T. S., Andriolo, G., Sun, B., Zheng, B., Zhang, L., et al. (2008) · Cell Stem Cell · doi:10.1016/j.stem.2008.07.003 · Cited by 3,991 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Adipogenesis and metabolic health
Ghaben, A. L., & Scherer, P. E. (2019) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-018-0093-z · Cited by 1,395 · see citing works
Cross-tissue organization of the fibroblast lineage
Buechler, M. B., Pradhan, R., Krishnamurty, A. T., Cox, C. B., Calviello, A. K., Wang, A. W., Yang, Y. A., Tam, L., Caothien, R. H., Roose‐Girma, M., et al. (2021) · Nature · doi:10.1038/s41586-021-03549-5 · Cited by 1,073 · see citing works
Adipose-tissue plasticity in health and disease
Sakers, A. P., Siqueira, M. K. D., Seale, P., & Villanueva, C. J. (2022) · Cell · doi:10.1016/j.cell.2021.12.016 · Cited by 1,061 · see citing works
A single-cell atlas of human and mouse white adipose tissue
Emont, M. P., Jacobs, C., Essene, A. L., Pant, D., Tenen, D., Colleluori, G., Di Vincenzo, A., Jørgensen, A. M., Dashti, H., Stefek, A., et al. (2022) · Nature · doi:10.1038/s41586-022-04518-2 · Cited by 840 · see citing works
Identification of a mesenchymal progenitor cell hierarchy in adipose tissue
Merrick, D., Sakers, A., Irgebay, Z., Okada, C., Calvert, C., Morley, M. P., Percec, I., & Seale, P. (2019) · Science · doi:10.1126/science.aav2501 · Cited by 664 · see citing works
“Recent reports by other investigators using similar methods identified analogous cell groups (24, 28, 29), demonstrating that these cell populations are present across a wide variety of adipose sources from animals of different ages and metabolic statuses.”
BackgroundResultInfluentialContribution of adipogenesis to healthy adipose tissue expansion in obesity
Vishvanath, L., & Gupta, R. K. (2019) · Journal of Clinical Investigation · doi:10.1172/jci129191 · Cited by 558 · see citing works
“(81) identify functionally distinct subpopulations of adipose precursors in inguinal WAT of adult mice.”
BackgroundAltered adipose tissue and adipocyte function in the pathogenesis of metabolic syndrome
Kahn, C. R., Wang, G., & Lee, K. Y. (2019) · Journal of Clinical Investigation · doi:10.1172/jci129187 · Cited by 656 · see citing works
“Fat also contains dipeptidyl peptidase-4–expressing (DPP4+) multipotent progenitors that give rise to committed preadipocytes and CD142+ cells, which have anti-adipogenic properties (12).”
BackgroundMyofibroblast proliferation and heterogeneity are supported by macrophages during skin repair
Shook, B. A., Wasko, R. R., Rivera-Gonzalez, G. C., Salazar-Gatzimas, E., López-Giráldez, F., Dash, B. C., Muñoz-Rojas, A. R., Aultman, K. D., Zwick, R. K., Lei, V., et al. (2018) · Science · doi:10.1126/science.aar2971 · Cited by 519 · see citing works
The cellular and functional complexity of thermogenic fat
Cohen, P., & Kajimura, S. (2021) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-021-00350-0 · Cited by 553 · see citing works
Single-cell analysis of human adipose tissue identifies depot- and disease-specific cell types
Vijay, J., Gauthier, M., Biswell, R. L., Louiselle, D. A., Johnston, J. J., Cheung, W., Belden, B., Pramatarova, A., Biertho, L. D., Gibson, M., et al. (2019) · Nature Metabolism · doi:10.1038/s42255-019-0152-6 · Cited by 456 · see citing works
Metabolic adaptation and maladaptation in adipose tissue
Chouchani, E. T., & Kajimura, S. (2019) · Nature Metabolism · doi:10.1038/s42255-018-0021-8 · Cited by 383 · see citing works
Hepler, C., Shan, B., Zhang, Q., Henry, G. H., Shao, M., Vishvanath, L., Ghaben, A. L., Mobley, A. B., Strand, D., Hon, G. C., et al. (2018) · eLife · doi:10.7554/elife.39636 · Cited by 346 · see citing works
“identified anti-adipogenic stromal cells within the inguinal WAT of mice (Schwalie et al., 2018).”
BackgroundSárvári, A. K., Hauwaert, E. L. V., Markussen, L. K., Gammelmark, E., Marcher, A.-B., Ebbesen, M. F., Nielsen, R., Brewer, J. R., Madsen, J. G. S., & Mandrup, S. (2020) · Cell Metabolism · doi:10.1016/j.cmet.2020.12.004 · Cited by 368 · see citing works
Adiponectin, Leptin and Cardiovascular Disorders
Zhao, S., Kusminski, C. M., & Scherer, P. E. (2021) · Circulation Research · doi:10.1161/circresaha.120.314458 · Cited by 398 · see citing works
Bao, H., Cao, J., Chen, M., Min, C., Chen, W., Chen, X., Chen, Y., Chen, Y., Chen, Y., Chen, Z., et al. (2023) · Science China Life Sciences · doi:10.1007/s11427-023-2305-0 · Cited by 389 · see citing works
Adipose tissue retains an epigenetic memory of obesity after weight loss
Hinte, L. C., Castellano‐Castillo, D., Ghosh, A., Melrose, K., Gasser, E., Noé, F., Massier, L., Dong, H., Sun, W., Hoffmann, A., et al. (2024) · Nature · doi:10.1038/s41586-024-08165-7 · Cited by 300 · see citing works
“Clusters were then annotated on the basis of known markers from literature 34,36,37,46,79,80 .”
Self-citationCD81 controls beige fat progenitor cell growth and energy balance via FAK signaling
Oguri, Y., Shinoda, K., Kim, H., Alba, D. L., Bolus, W. R., Wang, Q., Brown, Z., Pradhan, R., Tajima, K., Yoneshiro, T., et al. (2020) · Cell · doi:10.1016/j.cell.2020.06.021 · Cited by 250 · see citing works
“We employed the Fluidigm C1 system that allowed for deeper sequencing ( 1–2 million reads/cell) despite fewer number of cells, as compared to the 10X Genomics platform that has been applied to adipose tissues (Burl et al., 2018; Hepler et al., 2018; Merrick et al., 2019; Schwalie et al., 2018).”
MethodOmega-3 Fatty Acids Activate Ciliary FFAR4 to Control Adipogenesis
Hilgendorf, K. I., Johnson, C. T., Mezger, A., Rice, S. L., Norris, A. M., Demeter, J., Greenleaf, W. J., Reiter, J. F., Kopinke, D., & Jackson, P. K. (2019) · Cell · doi:10.1016/j.cell.2019.11.005 · Cited by 247 · see citing works
“It would be particularly interesting to examine ciliation in preadipocyte subpopulations within fat tissue, as recently revealed through the use of single cell sequencing (Burl et al., 2018; Hepler et al., 2018; Merrick et al., 2019; Schwalie et al., 2018).”
Deciphering the cellular interplays underlying obesity-induced adipose tissue fibrosis
Marcelin, G., Silveira, A. L. M., Martins, L. B., Ferreira, A. V. M., & Clément, K. (2019) · Journal of Clinical Investigation · doi:10.1172/jci129192 · Cited by 274 · see citing works
“Notably, in a separate work, a subpopulation identified as CD142+ displays adipogenesis-regulating properties, as these cells can suppress adipocyte formation in a paracrine manner without adipogenic potential (35).”
BackgroundLive-seq enables temporal transcriptomic recording of single cells
Chen, W., Guillaume-Gentil, O. J., Rainer, P. Y., Gäbelein, C. G., Saelens, W., Gardeux, V., Klaeger, A., Dainese, R., Zachara, M., Zambelli, T., et al. (2022) · Nature · doi:10.1038/s41586-022-05046-9 · Cited by 257 · see citing works
Self-citationAlpern, D., Gardeux, V., Russeil, J., Mangeat, B., Meireles-Filho, A. C. A., Breysse, R., Hacker, D., & Deplancke, B. (2019) · Genome Biology · doi:10.1186/s13059-019-1671-x · Cited by 216 · see citing works
“To do so, we turned to a familiar model system that was also used in the original SCRB-seq paper [13]: adipocyte formation from human adipose stromal cells (hASCs), since a large number of genes show differential expression along this differentiation trajectory [23].”
MethodSelf-citationIdentification, discrimination and heterogeneity of fibroblasts
Lendahl, U., Muhl, L., & Betsholtz, C. (2022) · Nature Communications · doi:10.1038/s41467-022-30633-9 · Cited by 242 · see citing works
Mechanisms of insulin resistance related to white, beige, and brown adipocytes
Czech, M. (2020) · Molecular Metabolism · doi:10.1016/j.molmet.2019.12.014 · Cited by 245 · see citing works
“A stromal cell population has been identified that inhibits adipocyte progenitor proliferation [72].”
BackgroundSpallanzani, R. G., Zemmour, D., Xiao, T., Jayewickreme, T., Li, C., Bryce, P. J., Benoist, C. O., & Mathis, D. J. (2019) · Science Immunology · doi:10.1126/sciimmunol.aaw3658 · Cited by 228 · see citing works
An integrated single cell and spatial transcriptomic map of human white adipose tissue
Massier, L., Jalkanen, J., Elmastas, M., Zhong, J., Wang, T., Nono Nankam, P. A., Frendo-Cumbo, S., Bäckdahl, J., Subramanian, N., Sekine, T., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-36983-2 · Cited by 195 · see citing works
“There were no overlaps with any of the route 2-localized FAPs indicating that clusters along this trajectory are not overlapping with the Lin/SCA cells preselected in the studies by Schwalie et al.(3) and Dong et al.”
ResultSelf-citationA PRDM16-Driven Metabolic Signal from Adipocytes Regulates Precursor Cell Fate
Wang, W., Ishibashi, J., Trefely, S., Shao, M., Cowan, A. J., Sakers, A. P., Lim, H., O’Connor, S., Doan, M. T., Cohen, P., et al. (2019) · Cell Metabolism · doi:10.1016/j.cmet.2019.05.005 · Cited by 225 · see citing works
“186 Cell Metabolism 30, 174–189, July 2, 2019 Limitations of Study Emerging studies indicate that adipose precursor cells, marked by their expression of PDGFRa, represent a heterogeneous cell compartment, comprising different cell types, including several putative fibrogenic populations (Burl et al., 2018; Hepler et a…”
BackgroundAging, obesity, sarcopenia and the effect of diet and exercise intervention
Colleluori, G., & Villareal, D. T. (2021) · Experimental Gerontology · doi:10.1016/j.exger.2021.111561 · Cited by 207 · see citing works
Adipose tissue at single-cell resolution
Maniyadath, B., Zhang, Q., Gupta, R. K., & Mandrup, S. (2023) · Cell Metabolism · doi:10.1016/j.cmet.2023.02.002 · Cited by 207 · see citing works
The regulation of adipose tissue health by estrogens
Steiner, B. M., & Berry, D. C. (2022) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.889923 · Cited by 171 · see citing works
Cellular heterogeneity in adipose tissues
Corvera, S. (2021) · Annual Review of Physiology · doi:10.1146/annurev-physiol-031620-095446 · Cited by 171 · see citing works
Xie, X.-H. P., Laks, D., Sun, D., Ganbold, M., Wang, Z.-L., Pedraza, A. M., Bale, T., Tabar, V., Brennan, C. W., Zhou, X.-P., et al. (2022) · Developmental Cell · doi:10.1016/j.devcel.2021.12.007 · Cited by 169 · see citing works
Tang, S., Yao, L., Ruan, J., Kang, J., Cao, Y., Nie, X., Lan, W., Zhu, Z., Han, W., Liu, Y., et al. (2024) · Science Translational Medicine · doi:10.1126/scitranslmed.adf4590 · Cited by 173 · see citing works
Cellular Origins of Beige Fat Cells Revisited
Shao, M.-L., Wang, Q. A., Song, A., Vishvanath, L., Busbuso, N. C., Scherer, P., & Gupta, R. K. (2019) · Diabetes · doi:10.2337/db19-0308 · Cited by 155 · see citing works
The evolving view of thermogenic adipocytes — ontogeny, niche and function
Shamsi, F., Wang, C.-H., & Tseng, Y.-H. (2021) · Nature Reviews Endocrinology · doi:10.1038/s41574-021-00562-6 · Cited by 154 · see citing works
Multipotent stromal cells: One name, multiple identities
Soliman, H., Theret, M., Scott, W., Hill, L., Underhill, T. M., Hinz, B., & Rossi, F. M. V. (2021) · Cell Stem Cell · doi:10.1016/j.stem.2021.09.001 · Cited by 147 · see citing works
Conditioned Medium from Human Mesenchymal Stromal Cells: Towards the Clinical Translation
Sagaradze, G., Grigorieva, O., Nimiritsky, P., Basalova, N., Kalinina, N., Akopyan, Z., & Efimenko, A. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20071656 · Cited by 147 · see citing works
The Importance of Breast Adipose Tissue in Breast Cancer
Kothari, C., Diorio, C., & Durocher, F. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21165760 · Cited by 171 · see citing works
“population could be a new therapeutic approach [243].”
BackgroundInfluentialIdentification of Metabolically Distinct Adipocyte Progenitor Cells in Human Adipose Tissues
Raajendiran, A., Ooi, G., Bayliss, J., O’Brien, P. E., Schittenhelm, R. B., Clark, A. K., Taylor, R. A., Rodeheffer, M. S., Burton, P. R., & Watt, M. J. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.04.010 · Cited by 152 · see citing works
Min, S. Y., Desai, A., Yang, Z., Sharma, A., DeSouza, T., Genga, R. M. J., Küçükural, A., Lifshitz, L. M., Nielsen, S. J., Scheele, C. C., et al. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1906512116 · Cited by 141 · see citing works
“Single-cell transcriptomics of adipose tissue progenitor cells in mouse fat has revealed specific populations primed to expand in response to adrenergic stimulation (13), stromal cells capable of inhibiting adipogenesis (11), and cells with enhanced adipogenic or fibro-inflammatory properties (14).”
BackgroundAdipose Tissue Fibrosis: Mechanisms, Models, and Importance
DeBari, M. K., & Abbott, R. D. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21176030 · Cited by 141 · see citing works
Brown Adipose Tissue Development and Metabolism
Jung, S. M., Sánchez-Gurmaches, J., & Guertin, D. A. (2018) · Handbook of experimental pharmacology · doi:10.1007/164_2018_168 · Cited by 144 · see citing works
“…on adipocytes that will undoubtedly usher more, singlecell RNA sequencing of the ASPCs population in WAT identified at least three different cell populations involved in adipocyte regulation, one of which surprisingly secretes an unknown signal that inhibits adipogenesis (Schwalie et al. 2018).”
Toward a Consensus View of Mammalian Adipocyte Stem and Progenitor Cell Heterogeneity.
Ferrero, R., Rainer, P., & Deplancke, B. (2020) · Trends in Cell Biology · doi:10.1016/j.tcb.2020.09.007 · Cited by 114 · see citing works
Self-citationAngiogenesis in adipose tissue and obesity
Corvera, S., Solivan-Rivera, J., & Yang, Z. (2022) · Angiogenesis · doi:10.1007/s10456-022-09848-3 · Cited by 125 · see citing works
Distinct properties of adipose stem cell subpopulations determine fat depot-specific characteristics
Nahmgoong, H., Jeon, Y. G., Park, E. S., Choi, Y. H., Han, S. M., Park, J., Ji, Y., Sohn, J. H., Han, J. S., Kim, Y. Y., et al. (2022) · Cell Metabolism · doi:10.1016/j.cmet.2021.11.014 · Cited by 135 · see citing works
BATLAS: Deconvoluting Brown Adipose Tissue.
Perdikari, A., Leparc, G., Baláž, M., Pires, N. D., Lidell, M. E., Sun, W., Fernández-Albert, F., Müller, S., Akchiche, N., Dong, H., et al. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.09.044 · Cited by 104 · see citing works
“, 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.”
BackgroundSelf-citationTranscriptional Control of Brown and Beige Fat Development and Function
Shapira, S. N., & Seale, P. (2018) · Obesity · doi:10.1002/oby.22334 · Cited by 108 · see citing works
“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).”
BackgroundSex Differences in Genomic Drivers of Adipose Distribution and Related Cardiometabolic Disorders
Lumish, H. S., O'Reilly, M. E., & Reilly, M. P. (2019) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.119.313154 · Cited by 118 · see citing works
Deciphering White Adipose Tissue Heterogeneity
Luong, Q. V., Huang, J. R., & Lee, K. Y. (2019) · Biology · doi:10.3390/biology8020023 · Cited by 102 · see citing works
“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., Sharma, R., Dreyfuss, J., Ussar, S., & Kahn, C. R. (2018) · EMBO Journal · doi:10.15252/embj.201899291 · Cited by 95 · see citing works
“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
Nguyen, H. P., Lin, F., Yi, D., Xie, Y., Dinh, J., Xue, P., & Sul, H. S. (2021) · Developmental Cell · doi:10.1016/j.devcel.2021.03.026 · Cited by 116 · see citing works
Sun, C., Wang, L., Wang, H., Huang, T., Yao, W., Li, J., & Zhang, X. (2020) · Stem Cell Research & Therapy · doi:10.1186/s13287-020-01660-4 · Cited by 108 · see citing works
Yang, J., Vamvini, M. T., Nigro, P., Ho, L., Galani, K., Alvarez, M., Tanigawa, Y., Renfro, A., Carbone, N. P., Laakso, M., et al. (2022) · Cell Metabolism · doi:10.1016/j.cmet.2022.09.004 · Cited by 108 · see citing works
“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).”
ResultGu, W., Nowak, W. N., Xie, Y., Bras, A. L., Hu, Y., Deng, J., Bhaloo, S. I., Lu, Y., Yuan, H., Fidanis, E., et al. (2019) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.119.312732 · Cited by 95 · see citing works
“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.”
Tratwal, J., Labella, R., Bravenboer, N., Kerckhofs, G., Douni, E., Scheller, E., Badr, S., Karampinos, D., Beck-Cormier, S., Palmisano, B., et al. (2020) · Frontiers in Endocrinology · doi:10.3389/fendo.2020.00065 · Cited by 82 · see citing works
Two distinct molecular faces of preeclampsia revealed by single-cell transcriptomics
Admati, I., Skarbianskis, N., Hochgerner, H., Ophir, O., Weiner, Z., Yagel, S., Solt, I., & Zeisel, A. (2023) · Med · doi:10.1016/j.medj.2023.07.005 · Cited by 82 · see citing works
Unveiling adipose populations linked to metabolic health in obesity
Reinisch, I., Ghosh, A., Noé, F., Sun, W., Dong, H., Leary, P., Dietrich, A., Hoffmann, A., Blüher, M., & Wolfrum, C. (2024) · Cell Metabolism · doi:10.1016/j.cmet.2024.11.006 · Cited by 86 · see citing works
Self-citationPathologic HIF1α signaling drives adipose progenitor dysfunction in obesity
Shao, M., Hepler, C., Zhang, Q., Shan, B., Vishvanath, L., Henry, G. H., Zhao, S., An, Y., Wu, Y., Strand, D. W., et al. (2021) · Cell stem cell · doi:10.1016/j.stem.2020.12.008 · Cited by 86 · see citing works
“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
Boothby, I., Kinet, M. J., Boda, D. P., Kwan, E., Clancy, S., Cohen, J. N., Habrylo, I. B., Lowe, M., Pauli, M., Yates, A. E., et al. (2021) · Nature · doi:10.1038/s41586-021-04044-7 · Cited by 79 · see citing works
Assembling the adipose organ: adipocyte lineage segregation and adipogenesis in vivo
Sebo, Z. L., & Rodeheffer, M. S. (2019) · Development · doi:10.1242/dev.172098 · Cited by 86 · see citing works
“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 · see citing works
Visceral adipose tissue Tregs and the cells that nurture them
Li, C., Spallanzani, R. G., & Mathis, D. J. (2020) · Immunological Reviews · doi:10.1111/imr.12850 · Cited by 73 · see citing works
Single cell approaches to address adipose tissue stromal cell heterogeneity
Rondini, E. A., & Granneman, J. G. (2020) · Biochemical Journal · doi:10.1042/bcj20190467 · Cited by 87 · see citing works
Self-assembling manifolds in single-cell RNA sequencing data
Tarashansky, A. J., Xue, Y., Li, P.-Y., Quake, S., & Wang, B. (2018) · bioRxiv · doi:10.1101/364166 · Cited by 70
Mammary gland adipocytes in lactation cycle, obesity and breast cancer
Colleluori, G., Perugini, J., Barbatelli, G., & Cinti, S. (2021) · Reviews in Endocrine and Metabolic Disorders · doi:10.1007/s11154-021-09633-5 · Cited by 82 · see citing works
Interstitial Cell Remodeling Promotes Aberrant Adipogenesis in Dystrophic Muscles
Camps, J., Breuls, N., Sifrim, A., Giarratana, N., Corvelyn, M., Danti, L., Grosemans, H., Vanuytven, S., Thiry, I., Belicchi, M., et al. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.107597 · Cited by 86 · see citing works
“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.
Wang, T., Sharma, A., Wu, C., Maushart, C., Ghosh, A., Yang, W., Stefanicka, P., Kovaničová, Z., Ukropec, J., Zhang, J., et al. (2024) · Cell Metabolism · doi:10.1016/j.cmet.2024.07.005 · Cited by 67 · see citing works
Self-citationWnt signaling preserves progenitor cell multipotency during adipose tissue development
Yang, Z., Joyce, S., DeSouza, T., Solivan-Rivera, J., Desai, A., Skritakis, P., Yang, Q., Ziegler, R., Zhong, D., Nguyen, T., et al. (2023) · Nature Metabolism · doi:10.1038/s42255-023-00813-y · Cited by 82 · see citing works
Prrx1 marks stem cells for bone, white adipose tissue and dermis in adult mice
Liu, H.-J., Li, P., Zhang, S.-Y., Xiang, J.-N., Yang, R.-C., Liu, J.-J., Shafiquzzaman, M., Biswas, S., Wei, Z.-Y., Zhang, Z.-L., et al. (2022) · Nature Genetics · doi:10.1038/s41588-022-01227-4 · Cited by 65 · see citing works
Fitzgerald, G., Turiel, G., Gorski, T., Soro-Arnáiz, I., Zhang, J., Casartelli, N. C., Masschelein, E., Maffiuletti, N. A., Sutter, R., Leunig, M., et al. (2023) · Communications Biology · doi:10.1038/s42003-023-04504-y · Cited by 78 · see citing works
Adipogenesis: A Necessary but Harmful Strategy
Hafidi, M. E., Buelna‐Chontal, M., Sánchez‐Muñoz, F., & Carbó, R. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20153657 · Cited by 80 · see citing works
“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
Hwang, I., & Kim, J. B. (2019) · Diabetes & Metabolism Journal · doi:10.4093/dmj.2019.0174 · Cited by 72 · see citing works
Identification of a regulatory pathway inhibiting adipogenesis via RSPO2
Dong, H., Sun, W., Shen, Y., Baláž, M., Balážová, L., Ding, L., Löffler, M. C., Hamilton, B. S., Klöting, N., Blüher, M., et al. (2022) · Nature Metabolism · doi:10.1038/s42255-021-00509-1 · Cited by 70 · see citing works
Self-citationHarnessing adipogenesis to prevent obesity
Haider, N., & Larose, L. (2019) · Adipocyte · doi:10.1080/21623945.2019.1583037 · Cited by 71 · see citing works
“regulating de novo adipogenic capacity of WAT [11].”
BackgroundRegional Heterogeneity of Perivascular Adipose Tissue: Morphology, Origin, and Secretome
Li, X., Ma, Z., & Zhu, Y. Z. (2021) · Frontiers in Pharmacology · doi:10.3389/fphar.2021.697720 · Cited by 62 · see citing works
“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
Sun, C.-Y., Sakashita, H., Kim, J. H., Tang, Z., Upchurch, G., Yao, L., Berry, W. L., Griffin, T. M., & Olson, L. (2020) · Cell Stem Cell · doi:10.1016/j.stem.2020.03.004 · Cited by 56 · see citing works
“Aside from Pdgfr expression and lineage analysis, an important question relates to the in vivo function of PDGFRs in mesenchymal progenitors.”
BackgroundInfluentialChen, P., Tang, S., Li, M., Wang, D., Chen, C., Qiu, Y., Fang, Z., Zhang, H., Gao, H., Weng, H., et al. (2022) · Advanced Science · doi:10.1002/advs.202204786 · Cited by 62 · see citing works
Generation of immune cell containing adipose organoids for in vitro analysis of immune metabolism
Taylor, J., Sellin, J., Kuerschner, L., Krähl, L., Majlesain, Y., Förster, I., Thiele, C., Weighardt, H., & Weber, E. (2020) · Scientific Reports · doi:10.1038/s41598-020-78015-9 · Cited by 60 · see citing works
Scheidl, T. B., Brightwell, A. L., Easson, S., & Thompson, J. A. (2023) · BMC Medicine · doi:10.1186/s12916-023-02730-z · Cited by 57 · see citing works
“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].”
BackgroundWhytock, K. L., Sun, Y., Divoux, A., Yu, G., Smith, S. R., Walsh, M. J., & Sparks, L. M. (2022) · iScience · doi:10.1016/j.isci.2022.104772 · Cited by 53 · see citing works
Gupta, A., Shamsi, F., Altemose, N., Dorlhiac, G. F., Cypess, A. M., White, A. P., Yosef, N., Patti, M., Tseng, Y.-H., & Streets, A. (2022) · Genome Research · doi:10.1101/gr.275509.121 · Cited by 48 · see citing works
“…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
Palani, N. P., Horváth, C., Timshel, P. N., Folkertsma, P., Grønning, A. G. B., Henriksen, T. I., Peijs, L., Hirschberg, V., Sun, W., Jespersen, N. Z., et al. (2023) · Nature Metabolism · doi:10.1038/s42255-023-00820-z · Cited by 60 · see citing works
Self-citationEosinophils regulate intra-adipose axonal plasticity
Meng, X., Qian, X., Ding, X., Wang, W., Yin, X., Zhuang, G., & Zeng, W. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2112281119 · Cited by 59 · see citing works
Novel insights into adipose tissue heterogeneity
Wang, T., Sharma, A. K., & Wolfrum, C. (2021) · Reviews in Endocrine and Metabolic Disorders · doi:10.1007/s11154-021-09703-8 · Cited by 51 · see citing works
“1 3 (iii) Cd142+ population (PP3) [22].”
BackgroundInfluentialSelf-citationFarup, J., Just, J., de Paoli, F. D., Lin, L., Jensen, J., Billeskov, T., Román, I. S., Cömert, C., Møller, A., Madaro, L., et al. (2020) · bioRxiv · doi:10.1101/2020.08.25.243907 · Cited by 50
The Impact of Single-Cell Genomics on Adipose Tissue Research
Deutsch, A., Feng, D., Pessin, J. E., & Shinoda, K. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21134773 · Cited by 62 · see citing works
“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 .”
BackgroundInfluentialZhang, L., Guerrero‐Juarez, C. F., Chen, S., Zhang, X., Yin, M., Li, F., Wu, S., Chen, J., Li, M., Liu, Y., et al. (2021) · Science Translational Medicine · doi:10.1126/scitranslmed.abb5280 · Cited by 59 · see citing works
“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 · see citing works
“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 46 · see citing works
Multilayered omics Reveal Sex- and Depot-Dependent Adipose Progenitor Cell Heterogeneity
Bo, S., Barker, C., Shao, M.-L., Zhang, Q.-B., Gupta, R. K., & Wu, Y. (2022) · Cell Metabolism · doi:10.1016/j.cmet.2022.03.012 · Cited by 48 · see citing works
Rabhi, N., Desevin, K., Belkina, A. C., Tilston-Lünel, A., Varelas, X., Layne, M. D., & Farmer, S. R. (2022) · Life Science Alliance · doi:10.26508/lsa.202101286 · Cited by 54 · see citing works
“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
Shin, S., El-Sabbagh, A. S., Lukas, B., Tanneberger, S. J., & Jiang, Y. (2020) · Bioscience Reports · doi:10.1042/bsr20194076 · Cited by 54 · see citing works
Ramirez, A. K., Dankel, S., Rastegarpanah, B., Cai, W., Xue, R.-D., Crovella, M., Tseng, Y.-H., Kahn, C., & Kasif, S. (2020) · Nature Communications · doi:10.1038/s41467-020-16019-9 · Cited by 48 · see citing works
Cho, D. S., Lee, B., & Doles, J. D. (2019) · Life Science Alliance · doi:10.26508/lsa.201900561 · Cited by 59 · see citing works
Dpp4+ interstitial progenitor cells contribute to basal and high fat diet-induced adipogenesis
Stefkovich, M. L., Traynor, S., Cheng, L., Merrick, D., & Seale, P. (2021) · Molecular Metabolism · doi:10.1016/j.molmet.2021.101357 · Cited by 56 · see citing works
Importance of the Microenvironment and Mechanosensing in Adipose Tissue Biology
Lecoutre, S., Lambert, M., Drygalski, K., Dugail, I., Maqdasy, S., Hautefeuille, M., & Clément, K. (2022) · Cells · doi:10.3390/cells11152310 · Cited by 48 · see citing works
Xu, D., Wan, B., Qiu, K., Wang, Y., Zhang, X., Jiao, N., Yan, E., Wu, J. W., Yu, R., Gao, S., et al. (2023) · Advanced Science · doi:10.1002/advs.202305080 · Cited by 53 · see citing works
Contribution of adipocytes in the tumor microenvironment to breast cancer metabolism
Lyu, X., Zhang, Q., Fares, H. M., Wang, Y., Han, Y., & Sun, L. (2022) · Cancer Letters · doi:10.1016/j.canlet.2022.215616 · Cited by 48 · see citing works
Shin, S., Pang, Y., Park, J., Liu, L., Lukas, B., Kim, S. H., Kim, K.-W., Xu, P., Berry, D. C., & Jiang, Y. (2020) · eLife · doi:10.7554/elife.56189 · Cited by 58 · see citing works
MHO or MUO? White adipose tissue remodeling
Zhao, J. Y., Li, Z., Ma, K. L., Hao, R., & Li, M. (2024) · Obesity Reviews · doi:10.1111/obr.13691 · Cited by 46 · see citing works
“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
Xu, C., Wang, Z., Rui, W., Feng, Z., Shuai, H., & Wang, Z. (2024) · Burns & Trauma · doi:10.1093/burnst/tkae043 · Cited by 46 · see citing works
“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
- 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 › Adipose Tissue and Metabolism
- Health Sciences › Medicine › Epidemiology › 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
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
