Visceral and subcutaneous fat have different origins and evidence supports a mesothelial source
Open accessAbstract
Fuelled by the obesity epidemic, there is considerable interest in the developmental origins of white adipose tissue (WAT) and the stem and progenitor cells from which it arises. Whereas increased visceral fat mass is associated with metabolic dysfunction, increased subcutaneous WAT is protective. There are six visceral fat depots: perirenal, gonadal, epicardial, retroperitoneal, omental and mesenteric, and it is a subject of much debate whether these have a common developmental origin and whether this differs from that for subcutaneous WAT. Here we show that all six visceral WAT depots receive a significant contribution from cells expressing Wt1 late in gestation. Conversely, no subcutaneous WAT or brown adipose tissue arises from Wt1-expressing cells. Postnatally, a subset of visceral WAT continues to arise from Wt1-expressing cells, consistent with the finding that Wt1 marks a proportion of cell populations enriched in WAT progenitors. We show that all visceral fat depots have a mesothelial layer like the visceral organs with which they are associated, and provide several lines of evidence that Wt1-expressing mesothelium can produce adipocytes. These results reveal a major ontogenetic difference between visceral and subcutaneous WAT, and pinpoint the lateral plate mesoderm as a major source of visceral WAT. They also support the notion that visceral WAT progenitors are heterogeneous, and suggest that mesothelium is a source of adipocytes.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
Subcutaneous and visceral adipocytes arise from different cell lineages.
“Subcutaneous and visceral adipocytes arise from different cell lineages,30 and we tested whether glucocorticoids have depot‐specific effects in paired subcutaneous and visceral adipocytes.”
From Acute physiological effects of glucocorticoids on fuel metabolism in humans are permissive but not direct (2017) · cites this paper as [30]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
A global double-fluorescent Cre reporter mouse
Muzumdar, M. D., Tasic, B., Miyamichi, K., Li, L., & Luo, L. (2007) · genesis · doi:10.1002/dvg.20335 · Cited by 3,491 · see citing works
White Fat Progenitor Cells Reside in the Adipose Vasculature
Tang, W., Zeve, D., Suh, J. M., Bosnakovski, D., Kyba, M., Hammer, R. E., Tallquist, M. D., & Graff, J. M. (2008) · Science · doi:10.1126/science.1156232 · Cited by 1,113 · see citing works
Rosito, G. A., Massaro, J. M., Hoffmann, U., Ruberg, F. L., Mahabadi, A. A., Vasan, R. S., O’Donnell, C. J., & Fox, C. S. (2008) · Circulation · doi:10.1161/circulationaha.107.743062 · Cited by 1,021 · see citing works
Identification of White Adipocyte Progenitor Cells In Vivo
Rodeheffer, M. S., Birsoy, K., & Friedman, J. M. (2008) · Cell · doi:10.1016/j.cell.2008.09.036 · Cited by 945 · see citing works
Characterization of the adipocyte cellular lineage in vivo
Berry, R., & Rodeheffer, M. S. (2013) · Nature Cell Biology · doi:10.1038/ncb2696 · Cited by 542 · see citing works
Self-citationDing, J., Hsu, F., Harris, T. B., Liu, Y., Kritchevsky, S. B., Szklo, M., Ouyang, P., Espeland, M. A., Lohman, K. K., Criqui, M. H., et al. (2009) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.2008.27358 · Cited by 476 · see citing works
The Vascular Endothelium of the Adipose Tissue Gives Rise to Both White and Brown Fat Cells
Tran, K., Gealekman, O., Frontini, A., Zingaretti, M. C., Morroni, M., Giordano, A., Smorlesi, A., Perugini, J., Matteis, R. D., Sbarbati, A., et al. (2012) · Cell Metabolism · doi:10.1016/j.cmet.2012.01.008 · Cited by 381 · see citing works
Martínez-Estrada, O. M., Lettice, L. A., Essafi, A., Guadix, J. A., Slight, J., Velecela, V., Hall, E. A., Reichmann, J., Devenney, P. S., Hohenstein, P., et al. (2009) · Nature Genetics · doi:10.1038/ng.494 · Cited by 369 · see citing works
Self-citationTchkonia, T., Lenburg, M. E., Thomou, T., Giorgadze, N., Frampton, G. M., Pirtskhalava, T., Cartwright, A., Cartwright, M., Flanagan, J. N., Karagiannides, I., et al. (2006) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00202.2006 · Cited by 349 · see citing works
Sánchez-Gurmaches, J., Hung, C., Sparks, C. A., Tang, Y., Li, H., & Guertin, D. A. (2012) · Cell Metabolism · doi:10.1016/j.cmet.2012.08.003 · Cited by 342 · see citing works
The serosal mesothelium is a major source of smooth muscle cells of the gut vasculature
Wilm, B., Ipenberg, A., Hastie, N., Burch, J., & Bader, D. (2005) · Development · doi:10.1242/dev.02141 · Cited by 328 · see citing works
Self-citationAsahina, K., Zhou, B., Pu, W. T., & Tsukamoto, H. (2010) · Hepatology · doi:10.1002/hep.24119 · Cited by 308 · see citing works
Intrinsic Differences in Adipocyte Precursor Cells From Different White Fat Depots
Macotela, Y., Emanuelli, B., Mori, M. A., Gesta, S., Schulz, T. J., Tseng, Y., & Kahn, C. R. (2012) · Diabetes · doi:10.2337/db11-1753 · Cited by 300 · see citing works
Wessels, A., van den Hoff, M. J. B., Adamo, R. F., Phelps, A. L., Lockhart, M. M., Sauls, K., Briggs, L. E., Norris, R. A., van Wijk, B., Perez-Pomares, J. M., et al. (2012) · Developmental Biology · doi:10.1016/j.ydbio.2012.04.020 · Cited by 263 · see citing works
Mesothelium contributes to vascular smooth muscle and mesenchyme during lung development
Que, J., Wilm, B., Hasegawa, H., Wang, F., Bader, D. M., & Hogan, B. L. M. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0808649105 · Cited by 258 · see citing works
The spatiotemporal development of adipose tissue
Han, J., Lee, J.-E., Jin, J., Lim, J. S., Oh, N., Kim, K., Chang, S.-I., Shibuya, M., Kim, H., & Koh, G. Y. (2011) · Development · doi:10.1242/dev.067686 · Cited by 212 · see citing works
Rinkevich, Y., Mori, T., Sahoo, D., Xu, P., Bermingham, J. R., & Weissman, I. L. (2012) · Nature Cell Biology · doi:10.1038/ncb2610 · Cited by 187 · see citing works
Adipose Depots Possess Unique Developmental Gene Signatures
Yamamoto, Y., Gesta, S., Lee, K. Y., Tran, T. T., Saadatirad, P., & Kahn, C. R. (2010) · Obesity · doi:10.1038/oby.2009.512 · Cited by 185 · see citing works
del Monte‐Nieto, G., Casanova, J. C., Guadix, J. A., MacGrogan, D., Burch, J. B. E., Pérez-Pomares, J. M., & de la Pompa, J. L. (2011) · Circulation Research · doi:10.1161/circresaha.110.229062 · Cited by 173 · see citing works
Essafi, A., Webb, A., Berry, R. L., Slight, J., Burn, S. F., Spraggon, L., Velecela, V., Martínez-Estrada, O. M., Wiltshire, J. H., Roberts, S. G. E., et al. (2011) · Developmental Cell · doi:10.1016/j.devcel.2011.07.014 · Cited by 165 · see citing works
Self-citationDevelopmental Origins of the Adipocyte Lineage: New Insights from Genetics and Genomics Studies
Billon, N., & Dani, C. (2011) · Stem Cell Reviews and Reports · doi:10.1007/s12015-011-9242-x · Cited by 138 · see citing works
Acute Multiple Organ Failure in Adult Mice Deleted for the Developmental Regulator Wt1
Chau, Y.-Y., Brownstein, D. G., Mjoseng, H. K., Lee, W., Buza-Vidas, N., Nerlov, C., Jacobsen, S. E. W., Perry, P., Berry, R. L., Thornburn, A., et al. (2011) · PLoS Genetics · doi:10.1371/journal.pgen.1002404 · Cited by 128 · see citing works
Self-citationWt1 and retinoic acid signaling are essential for stellate cell development and liver morphogenesis
IJpenberg, A., Pérez-Pomares, J. M., Guadix, J. A., Carmona, R., Portillo-Sánchez, V., Macías, D., Hohenstein, P., Miles, C., Hastie, N. D., & Muñoz‐Chápuli, R. (2007) · Developmental Biology · doi:10.1016/j.ydbio.2007.09.014 · Cited by 126 · see citing works
Self-citationHosen, N., Shirakata, T., Nishida, S., Yanagihara, M., Tsuboi, A., Kawakami, M., Oji, Y., Oka, Y., Okabe, M., Tan, B. T., et al. (2007) · Leukemia · doi:10.1038/sj.leu.2404752 · Cited by 94 · see citing works
LRRN4 and UPK3B Are Markers of Primary Mesothelial Cells
Kanamori-Katayama, M., Kaiho, A., Ishizu, Y., Okamura-Oho, Y., Hino, O., Abe, M., Kishimoto, T., Sekihara, H., Nakamura, Y., Suzuki, H., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0025391 · Cited by 92 · see citing works
Wt1-expressing progenitors contribute to multiple tissues in the developing lung
Cano, E., Carmona, R., & Muñoz‐Chápuli, R. (2013) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00424.2012 · Cited by 74 · see citing works
The role of Wt1 in regulating mesenchyme in cancer, development, and tissue homeostasis
Chau, Y.-Y., & Hastie, N. D. (2012) · Trends in Genetics · doi:10.1016/j.tig.2012.04.004 · Cited by 67 · see citing works
Self-citationCarmona, R., Cano, E., Mattiotti, A., Casellas, J. G., & Muñoz‐Chápuli, R. (2013) · PLoS ONE · doi:10.1371/journal.pone.0055890 · Cited by 46 · see citing works
Berry, R. L., Harewood, L., Pei, L., Fisher, M. E., Brownstein, D. G., Ross, A., Alaynick, W. A., Moss, J., Hastie, N. D., Hohenstein, P., et al. (2010) · Human Molecular Genetics · doi:10.1093/hmg/ddq530 · Cited by 36 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Metabolism disrupting chemicals and metabolic disorders
Heindel, J. J., Blumberg, B., Cave, M., Machtinger, R., Mantovani, A., Mendez, M. A., Nadal, A., Palanza, P., Panzica, G., Sargis, R., et al. (2017) · Reproductive Toxicology · doi:10.1016/j.reprotox.2016.10.001 · Cited by 1,101 · 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
Control of brown and beige fat development
Wang, W., & Seale, P. (2016) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm.2016.96 · Cited by 697 · see citing works
Adipose tissue in control of metabolism
Luo, L., & Liu, M. (2016) · Journal of Endocrinology · doi:10.1530/joe-16-0211 · Cited by 707 · see citing works
Fuster, J. J., Ouchi, N., Gokce, N., & Walsh, K. X. (2016) · Circulation Research · doi:10.1161/circresaha.115.306885 · Cited by 669 · see citing works
Contribution 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
Huang, H., Wang, Z., Zhang, Y., Pradhan, R. N., Ganguly, D., Chandra, R., Murimwa, G., Wright, S., Gu, X., Maddipati, R., et al. (2022) · Cancer Cell · doi:10.1016/j.ccell.2022.04.011 · Cited by 542 · see citing works
Biology of upper-body and lower-body adipose tissue—link to whole-body phenotypes.
Karpe, F., & Pinnick, K. E. (2015) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2014.185 · Cited by 543 · 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
Adipose tissue plasticity: how fat depots respond differently to pathophysiological cues
Pellegrinelli, V., Carobbio, S., & Vidal-Puig, A. (2016) · Diabetologia · doi:10.1007/s00125-016-3933-4 · Cited by 432 · see citing works
Rapid depot-specific activation of adipocyte precursor cells at the onset of obesity
Jeffery, E., Church, C. D., Holtrup, B., Colman, L., & Rodeheffer, M. S. (2015) · Nature Cell Biology · doi:10.1038/ncb3122 · Cited by 404 · see citing works
Koyama, S., Ito, K., Terao, C. C., Akiyama, M., Horikoshi, M., Momozawa, Y., Matsunaga, H., Ieki, H., Ozaki, K., Onouchi, Y., et al. (2020) · Nature Genetics · doi:10.1038/s41588-020-0705-3 · Cited by 349 · see citing works
The adipose tissue microenvironment regulates depot-specific adipogenesis in obesity
Jeffery, E., Wing, A., Holtrup, B., Sebo, Z., Kaplan, J. L., Saavedra-Peña, R., Church, C. D., Colman, L., Berry, R., & Rodeheffer, M. S. (2016) · Cell Metabolism · doi:10.1016/j.cmet.2016.05.012 · Cited by 352 · see citing works
Self-citationHepler, 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
Vishvanath, L., MacPherson, K. A., Hepler, C., Wang, Q. A., Shao, M., Spurgin, S. B., Wang, M. Y., Kusminski, C. M., Morley, T. S., & Gupta, R. K. (2015) · Cell Metabolism · doi:10.1016/j.cmet.2015.10.018 · Cited by 326 · see citing works
Immunological Functions of the Omentum
Meza‐Perez, S., & Randall, T. D. (2017) · Trends in Immunology · doi:10.1016/j.it.2017.03.002 · Cited by 327 · see citing works
A stringent validation of mouse adipose tissue identity markers
de Jong, J. M. A., Larsson, O. S., Cannon, B., & Nedergaard, J. (2015) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00023.2015 · Cited by 294 · see citing works
Chi, J., Wu, Z., Choi, C. H. J., Nguyen, L., Tegegne, S., Ackerman, S. E., Crane, A., Marchildon, F., Tessier-Lavigne, M., & Cohen, P. (2018) · Cell Metabolism · doi:10.1016/j.cmet.2017.12.011 · Cited by 285 · see citing works
Heterogeneity of white adipose tissue: molecular basis and clinical implications
Kwok, K. H. M., Lam, K. S. L., & Xu, A. (2016) · Experimental & Molecular Medicine · doi:10.1038/emm.2016.5 · Cited by 250 · see citing works
Convertible visceral fat as a therapeutic target to curb obesity
Giordano, A., Frontini, A., & Cinti, S. (2016) · Nature Reviews Drug Discovery · doi:10.1038/nrd.2016.31 · Cited by 232 · see citing works
Stromal cells maintain immune cell homeostasis in adipose tissue via production of interleukin-33
Mahlakõiv, T., Flamar, A.-L., Johnston, L. K., Moriyama, S., Putzel, G., Bryce, P. J., & Artis, D. (2019) · Science Immunology · doi:10.1126/sciimmunol.aax0416 · Cited by 218 · see citing works
‘Adipaging’: ageing and obesity share biological hallmarks related to a dysfunctional adipose tissue
Pérez, L. M., Pareja‐Galeano, H., Sanchis‐Gomar, F., Emanuele, E., Lucia, A., & Gálvez, B. G. (2016) · The Journal of Physiology · doi:10.1113/jp271691 · Cited by 215 · see citing works
Motohara, T., Masuda, K., Morotti, M., Zheng, Y., El-Sahhar, S., Chong, K. Y., Wietek, N., Alsaadi, A., Carrami, E. M., Hu, Z., et al. (2019) · Oncogene · doi:10.1038/s41388-018-0637-x · Cited by 218 · see citing works
Emerging Complexities in Adipocyte Origins and Identity
Sánchez-Gurmaches, J., Hung, C., & Guertin, D. A. (2016) · Trends in Cell Biology · doi:10.1016/j.tcb.2016.01.004 · Cited by 214 · see citing works
Heterogeneity of adipose tissue in development and metabolic function
Schöttl, T., Kapser-Fischer, I., & Ussar, S. (2018) · Journal of Experimental Biology · doi:10.1242/jeb.162958 · Cited by 215 · see citing works
Wilms' tumour 1 (WT1) in development, homeostasis and disease
Hastie, N. D. (2017) · Development · doi:10.1242/dev.153163 · Cited by 216 · see citing works
Self-citationCell transcriptomic atlas of the non-human primate Macaca fascicularis
Han, L., Wei, X., Liu, C., Volpe, G., Zhuang, Z., Zou, X., Wang, Z., Pan, T., Yuan, Y., Zhang, X., et al. (2022) · Nature · doi:10.1038/s41586-022-04587-3 · Cited by 209 · 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 Role of the Epicardium During Heart Development and Repair
Quijada, P., Trembley, M. A., & Small, E. M. (2020) · Circulation Research · doi:10.1161/circresaha.119.315857 · Cited by 201 · see citing works
Human Adipocytes Induce Inflammation and Atrophy in Muscle Cells During Obesity
Pellegrinelli, V., Rouault, C., Rodríguez‐Cuenca, S., Albert, V., Edom‐Vovard, F., Vidal‐Puig, A., Clément, K., Butler-Browne, G. S., & Lacasa, D. (2015) · Diabetes · doi:10.2337/db14-0796 · Cited by 197 · see citing works
Adipose Tissue Function and Expandability as Determinants of Lipotoxicity and the Metabolic Syndrome
Carobbio, S., Pellegrinelli, V., & Vidal‐Puig, A. (2017) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-48382-5_7 · Cited by 191 · see citing works
The effects of growth hormone on adipose tissue: old observations, new mechanisms
Kopchick, J. J., Berryman, D. E., Puri, V., Lee, K. Y., & Jørgensen, J. O. L. (2019) · Nature Reviews Endocrinology · doi:10.1038/s41574-019-0280-9 · Cited by 191 · see citing works
Adipose Tissue-Derived Stem Cells: Immunomodulatory Effects and Therapeutic Potential
Al-Ghadban, S. I., & Bunnell, B. A. (2020) · Physiology · doi:10.1152/physiol.00021.2019 · Cited by 190 · see citing works
Adipose Tissue Fibrosis in Obesity: Etiology and Challenges
Marcelin, G., Gautier, E. L., & Clément, K. (2021) · Annual Review of Physiology · doi:10.1146/annurev-physiol-060721-092930 · Cited by 185 · see citing works
Simultaneous dual-colour tracking lipid droplets and lysosomes dynamics using a fluorescent probe
Zheng, X., Zhu, W., Ni, F., Ai, H., Gong, S., Zhou, X., Sessler, J. L., & Yang, C. (2018) · Chemical Science · doi:10.1039/c8sc04462g · Cited by 178 · 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
Yamaguchi, Y., Cavallero, S., Patterson, M., Shen, H. M., Xu, J., Kumar, S. R., & Sucov, H. M. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1417232112 · Cited by 173 · 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
Wnt/β-Catenin Signaling and Obesity
Chen, N., & Wang, J. (2018) · Frontiers in Physiology · doi:10.3389/fphys.2018.00792 · Cited by 169 · see citing works
Vasan, S. K., Osmond, C., Canoy, D., Christodoulides, C., Neville, M. J., Gravio, C. D., Fall, C. H. D., & Karpe, F. (2017) · International Journal of Obesity · doi:10.1038/ijo.2017.289 · Cited by 164 · see citing works
Adipose Organ Development and Remodeling
Cinti, S. (2018) · Comprehensive physiology · doi:10.1002/cphy.c170042 · Cited by 187 · see citing works
Fried, S. K., Lee, M., & Karastergiou, K. (2015) · Obesity · doi:10.1002/oby.21133 · Cited by 162 · see citing works
Self-citationFree radicals and male reproduction.
Agarwal, A. K., & Allamaneni, S. S. R. (2011) · PubMed · Cited by 154 · see citing works
Prummel, K. D., Nieuwenhuize, S., & Mosimann, C. (2020) · Development · doi:10.1242/dev.175059 · Cited by 162 · see citing works
Buechler, M. B., Kim, K.-W., Onufer, E. J., Williams, J. W., Little, C. C., Dominguez, C. X., Li, Q., Sandoval, W. N., Cooper, J. E., Harris, C. A., et al. (2019) · Immunity · doi:10.1016/j.immuni.2019.05.010 · Cited by 161 · see citing works
Proinflammatory Phenotype of Perivascular Adipocytes
Omar, A., Chatterjee, T. K., Tang, Y., Hui, D. Y., & Weintraub, N. L. (2014) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.114.303030 · Cited by 160 · see citing works
Identification 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
Role of Epicardial Adipose Tissue in Health and Disease: A Matter of Fat?
Gaborit, B., Sengenès, C., Ancel, P., Jacquier, A., & Dutour, A. (2017) · Comprehensive physiology · doi:10.1002/cphy.c160034 · Cited by 174 · see citing works
Perirenal Fat: A Unique Fat Pad and Potential Target for Cardiovascular Disease
Liu, B.-X., Sun, W. Y., & Kong, X. (2018) · Angiology · doi:10.1177/0003319718799967 · Cited by 150 · see citing works
Retroperitoneal Liposarcoma: Current Insights in Diagnosis and Treatment
Matthyssens, L., Creytens, D., & Ceelen, W. P. (2015) · Frontiers in Surgery · doi:10.3389/fsurg.2015.00004 · Cited by 147 · see citing works
The Diabetes Gene and Wnt Pathway Effector TCF7L2 Regulates Adipocyte Development and Function
Chen, X., Ayala, I., Shannon, C. E., Fourcaudot, M. J., Acharya, N., Jenkinson, C. P., Heikkinen, S., & Norton, L. (2018) · Diabetes · doi:10.2337/db17-0318 · Cited by 140 · see citing works
Choi, M., Kim, Y., Kwon, E., Ryoo, J. Y., Kim, S. R., & Jung, U. J. (2015) · British Journal Of Nutrition · doi:10.1017/s0007114515000100 · Cited by 139 · see citing works
Distinct regulatory mechanisms governing embryonic versus adult adipocyte maturation
Wang, Q. A., Tao, C., Jiang, L., Shao, M., Ye, R., Zhu, Y., Gordillo, R., Ali, A., Lian, Y., Holland, W. L., et al. (2015) · Nature Cell Biology · doi:10.1038/ncb3217 · Cited by 134 · see citing works
Jin, L. G., Tang, Q., Hu, S., Chen, Z., Zhou, X., Zeng, B., Wang, Y., He, M., Li, Y., Gui, L., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-23560-8 · Cited by 135 · see citing works
The developmental basis of mesenchymal stem/stromal cells (MSCs)
Sheng, G. (2015) · BMC Developmental Biology · doi:10.1186/s12861-015-0094-5 · Cited by 135 · see citing works
Gao, Z., Daquinag, A. C., Su, F., Snyder, B., & Kolonin, M. G. (2017) · Development · doi:10.1242/dev.155861 · Cited by 133 · see citing works
Qian, J., LeSavage, B. L., Hubka, K. M., Ma, C., Natarajan, S., Eggold, J. T., Xiao, Y., Fuh, K. C., Krishnan, V., Enejder, A. M. K., et al. (2021) · Journal of Clinical Investigation · doi:10.1172/jci146186 · Cited by 132 · see citing works
Sorting out adipocyte precursors and their role in physiology and diseasePreprint
Hepler, C., Vishvanath, L., & Gupta, R. K. (2017) · Genes & Development · doi:10.1101/gad.293704.116 · Cited by 132 · see citing works
Bizino, M. B., Jazet, I. M., de Heer, P., van Eyk, H. J., Dekkers, I. A., Rensen, P. C. N., Paiman, E. H. M., Lamb, H. J., & Smit, J. W. (2020) · Diabetologia · doi:10.1007/s00125-019-05021-6 · Cited by 123 · see citing works
The Ontogeny of Brown Adipose Tissue
Symonds, M. E., Pope, M., & Budge, H. (2015) · Annual Review of Nutrition · doi:10.1146/annurev-nutr-071813-105330 · Cited by 122 · see citing works
Transforming Growth Factor-β3 Regulates Adipocyte Number in Subcutaneous White Adipose Tissue
Petrus, P., Mejhert, N., Corrales, P., Lecoutre, S., Li, Q., Maldonado, E., Kulyté, A., López, Y., Campbell, M., Acosta, J. R., et al. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.09.069 · Cited by 123 · see citing works
Martínez-Colón, G. J., Ratnasiri, K., Chen, R., Jiang, S., ZANLEY, E. J., Rustagi, A., Verma, R., Chen, H. M., Andrews, J. R., Mertz, K. D., et al. (2022) · Science Translational Medicine · doi:10.1126/scitranslmed.abm9151 · Cited by 136 · see citing works
Eymard, F., Pigenet, A., Citadelle, D., Tordjman, J., Foucher, L., Rose, C., Flouzat–Lachaniette, C.-H., Rouault, C., Clément, K., Berenbaum, F., et al. (2017) · Annals of the Rheumatic Diseases · doi:10.1136/annrheumdis-2016-210478 · Cited by 120 · see citing works
Sun, Q., Xing, X., Wang, H., Wan, K., Fan, R., Liu, C., Wang, Y., Wu, W., Wang, Y., & Wang, R. (2023) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2023.115586 · Cited by 120 · see citing works
MiR-93 Controls Adiposity via Inhibition of Sirt7 and Tbx3
Cioffi, M., Vallespinos-Serrano, M., Trabulo, S. M., Fernandez-Marcos, P. J., Firment, A. N., Vazquez, B. N., Vieira, C. R., Mulero, F., Camara, J. A., Cronin, U. P., et al. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.08.006 · Cited by 116 · see citing works
Developmental 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
Wu, L., Dalal, R., Cao, C. D., Postoak, J. L., Yang, G., Zhang, Q., Wang, Z., Lal, H., & Kaer, L. V. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1911464116 · Cited by 115 · see citing works
Characterization of Cre Recombinase Activity for In Vivo Targeting of Adipocyte Precursor Cells
Krueger, K. C., Costa, M. J. D. C., Du, H., & Feldman, B. J. (2014) · Stem Cell Reports · doi:10.1016/j.stemcr.2014.10.009 · Cited by 110 · see citing works
Highly Selective In Vivo Labeling of Subcutaneous White Adipocyte Precursors with Prx1-Cre
Sánchez-Gurmaches, J., Hsiao, W., & Guertin, D. A. (2015) · Stem Cell Reports · doi:10.1016/j.stemcr.2015.02.008 · Cited by 107 · see citing works
The Beige Adipocyte as a Therapy for Metabolic Diseases
Lizcano, F. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20205058 · Cited by 106 · 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
Mechanisms underlying UCP1 dependent and independent adipocyte thermogenesis
Chang, S., Song, N., Choi, J. H., Yun, U. J., & Park, K. W. (2018) · Obesity Reviews · doi:10.1111/obr.12796 · Cited by 104 · see citing works
Adventitia and Perivascular Cells
Majesky, M. W. (2015) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.115.306088 · Cited by 101 · see citing works
Flow Cytometry of Mouse and Human Adipocytes for the Analysis of Browning and Cellular Heterogeneity
Hagberg, C. E., Li, Q., Kutschke, M., Bhowmick, D., Kiss, E., Shabalina, I. G., Harms, M. J., Shilkova, O., Kozina, V., Nedergaard, J., et al. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.08.006 · Cited by 101 · see citing works
The ontogeny, activation and function of the epicardium during heart development and regeneration
Simões, F. C., & Riley, P. R. (2018) · Development · doi:10.1242/dev.155994 · Cited by 99 · see citing works
Obesity results in adipose tissue T cell exhaustion
Porsche, C. E., DelProposto, J. B., Geletka, L. M., O’Rourke, R. W., & Lumeng, C. N.-K. (2021) · JCI Insight · doi:10.1172/jci.insight.139793 · Cited by 100 · see citing works
Adipose morphology and metabolic disease
Tandon, P., Wafer, R., & Minchin, J. E. N. (2018) · Journal of Experimental Biology · doi:10.1242/jeb.164970 · Cited by 100 · see citing works
Atrial natriuretic peptide regulates adipose tissue accumulation in adult atria
Suffee, N., Moore‐Morris, T., Farahmand, P., Rücker‐Martin, C., Dilanian, G., Fradet, M., Sawaki, D., Dérumeaux, G., Leprince, P. N., Clément, K., et al. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1610968114 · Cited by 98 · see citing works
Berry, D. C., Jiang, Y., & Graff, J. M. (2016) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2016.05.001 · Cited by 95 · see citing works
Jackson-Jones, L. H., Smith, P., Portman, J. R., Pinto, M. M., Mylonas, K. J., Vermeren, M., Nixon, M., Henderson, B. E. P., Dobie, R., Vermeren, S., et al. (2020) · Immunity · doi:10.1016/j.immuni.2020.03.011 · Cited by 95 · see citing works
The burden of metabolic syndrome on osteoarthritic joints
Dickson, B. M., Roelofs, A. J., Rochford, J. J., Wilson, H. M., & Bari, C. D. (2019) · Arthritis Research & Therapy · doi:10.1186/s13075-019-2081-x · Cited by 96 · see citing works
Age-associated telomere attrition in adipocyte progenitors predisposes to metabolic disease
Gao, Z., Daquinag, A. C., Fussell, C., Zhao, Z., Dai, Y., Rivera, A., Snyder, B. E., Eckel-Mahan, K. L., & Kolonin, M. G. (2020) · Nature Metabolism · doi:10.1038/s42255-020-00320-4 · Cited by 92 · see citing works
GABA-stimulated adipose-derived stem cells suppress subcutaneous adipose inflammation in obesity
Hwang, I., Jo, K., Shin, K. C., Kim, J. I., Ji, Y., Park, Y. J., Park, J., Jeon, Y. G., Ka, S., Suk, S., et al. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1822067116 · Cited by 91 · see citing works
Chen, X., Mao, Y., Hu, J., Han, S., Gong, L., Luo, T., Yang, S., Qing, H., Wang, Y., Du, Z., et al. (2021) · Diabetes · doi:10.2337/db20-1031 · Cited by 92 · see citing works
Zangi, L., Oliveira, M. S., Ye, L. Y., Ma, Q., Sultana, N., Hadas, Y., Chepurko, E., Später, D., Zhou, B., Chew, W. L., et al. (2016) · Circulation · doi:10.1161/circulationaha.116.022064 · Cited by 90 · see citing works
A mesodermal fate map for adipose tissue
Sebo, Z. L., Jeffery, E. C., Holtrup, B., & Rodeheffer, M. S. (2018) · Development · doi:10.1242/dev.166801 · Cited by 89 · see citing works
The expanding problem of adipose depot remodeling and postnatal adipocyte progenitor recruitment
Hepler, C., & Gupta, R. K. (2016) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2016.10.011 · Cited by 87 · see citing works
Cattaneo, P., Mukherjee, D., Spinozzi, S., Zhang, L., Larcher, V., Stallcup, W. B., Kataoka, H., Chen, J., Dimmeler, S., Evans, S. Μ., et al. (2020) · Cell Reports · doi:10.1016/j.celrep.2019.12.046 · Cited by 89 · see citing works
Specific Biological Features of Adipose Tissue, and Their Impact on HIV Persistence
Bourgeois, C., Gorwood, J., Barrail‐Tran, A., Lagathu, C., Capeau, J., Desjardins, D., Grand, R. L., Damouche, A., Béréziat, V., & Lambotte, O. (2019) · Frontiers in Microbiology · doi:10.3389/fmicb.2019.02837 · Cited by 89 · see citing works
MTCH2 promotes adipogenesis in intramuscular preadipocytes via an m 6 A‐YTHDF1‐dependent mechanism
Jiang, Q. L., Sun, B., Liu, Q., Cai, M., Wu, R., Wang, F., Yao, Y., Wang, Y., & Wang, X. (2018) · The FASEB Journal · doi:10.1096/fj.201801393rrr · Cited by 87 · see citing works
Adipose stem cell niche reprograms the colorectal cancer stem cell metastatic machinery
Di Franco, S., Bianca, P., Sardina, D. S., Turdo, A., Gaggianesi, M., Veschi, V., Nicotra, A., Mangiapane, L. R., Lo Iacono, M., Pillitteri, I., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-25333-9 · Cited by 80 · 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
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
Role of adipose tissue macrophages in obesity-related disorders
Chakarov, S., Blériot, C., & Ginhoux, F. (2022) · The Journal of Experimental Medicine · doi:10.1084/jem.20211948 · Cited by 86 · 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
Ritter, A., Friemel, A., Fornoff, F., Adjan, M., Solbach, C., Yuan, J., & Louwen, F. (2015) · Oncotarget · doi:10.18632/oncotarget.5922 · Cited by 85 · see citing works
Hong, K. Y., Bae, H., Park, I., Park, D. Y., Kim, K. H., Kubota, Y., Cho, E., Kim, H., Adams, R. H., Yoo, O., et al. (2015) · Development · doi:10.1242/dev.125336 · Cited by 84 · see citing works
Hammoud, S. H., AlZaim, I., Al-Dhaheri, Y., Eid, A. H., & El-Yazbi, A. F. (2021) · Frontiers in Endocrinology · doi:10.3389/fendo.2021.707126 · Cited by 87 · see citing works
Subcutaneous and Visceral Adipose-Derived Mesenchymal Stem Cells: Commonality and Diversity
Ritter, A., Friemel, A., Roth, S., Kreis, N., Hoock, S. C., Safdar, B. K., Fischer, K., Möllmann, C. J., Solbach, C., Louwen, F., et al. (2019) · Cells · doi:10.3390/cells8101288 · Cited by 80 · see citing works
The role of estrogens in the adipose tissue milieu
Bracht, J. R., Vieira‐Potter, V. J., De Souza Santos, R., Öz, O. K., Palmer, B. F., & Clegg, D. J. (2020) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.14281 · Cited by 80 · see citing works
- Authors
- Chau, Y.-Y., Bandiera, R., Serrels, A., Martínez-Estrada, O. M., Qing, W., Lee, M., Slight, J., Thornburn, A., Berry, R., McHaffie, S., Stimson, R. H., Walker, B. R., Chapuli, R. M., Schedl, A., & Hastie, N.
- Affiliations
- Western General Hospital (GB)
- Inserm (FR)
- Universitat de Barcelona (ES)
- The Queen's Medical Research Institute (GB)
- Corresponding author
- Chau, You-Ying
- Hastie, Nick
- ORCID
- Venue
- Nature Cell Biology
- Published
- 2014-03-09
- Volume
- 16
- Issue
- 4
- Pages
- 367-375
- ISSN
- 1465-7392 (ISSN-L)
- 1476-4679
- PMC
- PMC4060514
- OpenAlex
- W2081513869
- Cited by
- 518
- References
- 29
- Citations by year
- 2026: 17 · 2025: 27 · 2024: 45 · 2023: 28 · 2022: 49 · 2021: 57 · 2020: 50 · 2019: 53 · 2018: 50 · 2017: 36 · 2016: 50 · 2015: 41 · 2014: 14
- FWCI
- 30.96
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Cell Biology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- RECERCAT (Consorci de Serveis Universitaris de Catalunya) (acceptedVersion)
- Edinburgh Research Explorer (University of Edinburgh) (submittedVersion, other-oa)
- HAL (submittedVersion)
- Dipòsit Digital de la Universitat de Barcelona (Universitat de Barcelona) (submittedVersion, public-domain)
- Newcastle University ePrints (Newcastle Univesity)
- Funders
- Universidad de Málaga
- Wellcome Trust (091374/Z/10/Z)
- British Heart Foundation (RG/11/4/28734)
- Agence Nationale de la Recherche
- Directorate for Biological Sciences
- Medical Research Council (MR/K010271/1)
- Topics
- Health Sciences › Medicine › Physiology › Adipose Tissue and Metabolism
- Health Sciences › Medicine › Epidemiology › Adipokines, Inflammation, and Metabolic Diseases
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiovascular Disease and Adiposity
- Keywords
- visceral adipose tissue, subcutaneous adipose tissue, mesothelium, WT1, adipocyte origin, adipose tissue development, lateral plate mesoderm, brown adipose tissue, adipose tissue heterogeneity, obesity
- MeSH terms
- Animals, Adipose Tissue, Brown, Mesoderm, Tamoxifen, Adipocytes, Antineoplastic Agents, Hormonal, Cell Lineage, WT1 Proteins, Green Fluorescent Proteins, Mice, Adipose Tissue, White, Gene Knock-In Techniques
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