White Fat Progenitor Cells Reside in the Adipose Vasculature
Open accessAbstract
White adipose (fat) tissues regulate metabolism, reproduction, and life span. Adipocytes form throughout life, with the most marked expansion of the lineage occurring during the postnatal period. Adipocytes develop in coordination with the vasculature, but the identity and location of white adipocyte progenitor cells in vivo are unknown. We used genetically marked mice to isolate proliferating and renewing adipogenic progenitors. We found that most adipocytes descend from a pool of these proliferating progenitors that are already committed, either prenatally or early in postnatal life. These progenitors reside in the mural cell compartment of the adipose vasculature, but not in the vasculature of other tissues. Thus, the adipose vasculature appears to function as a progenitor niche and may provide signals for adipocyte development.
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White adipocyte progenitors have been identified in the mural compartment of vascular structures.
“Interestingly, populations of white adipocyte progenitors have been identified in the mural compartment of vascular structures.”
From The ominous triad of adipose tissue dysfunction: inflammation, fibrosis, and impaired angiogenesis. (2017) · cites this paper as [20]
Mural cells with high adipogenic potential can be identified by PDGFR-β expression.
“Tang et al. demonstrated that these mural cells with high adipogenic potential can be identified by expression of PDGFR-β (20).”
From The ominous triad of adipose tissue dysfunction: inflammation, fibrosis, and impaired angiogenesis. (2017) · cites this paper as [20]
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Cites
Generalized lacZ expression with the ROSA26 Cre reporter strain
Soriano, P. (1999) · Nature Genetics · doi:10.1038/5007 · Cited by 5,237 · see citing works
Kopelman, P. G. (2000) · Nature · doi:10.1038/35007508 · Cited by 4,795 · see citing works
Lehmann, J. M., Moore, L. B., Smith-Oliver, T. A., Wilkison, W. O., Willson, T. M., & Kliewer, S. A. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.22.12953 · Cited by 3,626 · see citing works
Adipocyte differentiation from the inside out
Rosen, E. D., & MacDougald, O. A. (2006) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2066 · Cited by 2,607 · see citing works
Endothelial/Pericyte Interactions
Armulik, A., Abramsson, A., & Betsholtz, C. (2005) · Circulation Research · doi:10.1161/01.res.0000182903.16652.d7 · Cited by 2,048 · see citing works
Defining the Epithelial Stem Cell Niche in Skin
Tumbar, T., Guasch, G., Greco, V., Blanpain, C., Lowry, W. E., Rendl, M., & Fuchs, E. (2004) · Science · doi:10.1126/science.1092436 · Cited by 2,031 · see citing works
Transcriptional control of adipocyte formation
Farmer, S. R. (2006) · Cell Metabolism · doi:10.1016/j.cmet.2006.07.001 · Cited by 1,836 · see citing works
Developmental Origin of Fat: Tracking Obesity to Its Source
Gesta, S., Tseng, Y.-H., & Kahn, C. R. (2007) · Cell · doi:10.1016/j.cell.2007.10.004 · Cited by 1,508 · see citing works
Kanda, T., Sullivan, K., & Wahl, G. (1998) · Current Biology · doi:10.1016/s0960-9822(98)70156-3 · Cited by 1,040 · see citing works
Pericytes of human skeletal muscle are myogenic precursors distinct from satellite cells
Dellavalle, A., Sampaolesi, M., Tonlorenzi, R., Tagliafico, E., Sacchetti, B., Perani, L., Innocenzi, A., Gálvez, B. G., Messina, G., Roberta Morosetti, A., et al. (2007) · Nature Cell Biology · doi:10.1038/ncb1542 · Cited by 1,001 · see citing works
Adipose tissue mass can be regulated through the vasculature
Rupnick, M. A., Panigrahy, D., Zhang, C.-Y., Dallabrida, S. M., Lowell, B. B., Langer, R., & Folkman, M. J. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.162349799 · Cited by 845 · see citing works
No place like home: anatomy and function of the stem cell niche
Jones, D. L., & Wagers, A. J. (2007) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2319 · Cited by 794 · see citing works
Adipocyte Differentiation and Gene Expression
Ntambi, J. M., & Kim, Y. (2000) · Journal of Nutrition · doi:10.1093/jn/130.12.3122s · Cited by 780 · see citing works
Doxycycline-mediated quantitative and tissue-specific control of gene expression in transgenic mice.
Kistner, A., Gossen, M., Zimmermann, F., Jerecic, J., Ullmer, C., Lübbert, H., & Bujard, H. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.20.10933 · Cited by 780 · see citing works
Cellular and Molecular Aspects of Adipose Tissue Development
Ailhaud, G. P., Grimaldi, P., & Négrel, R. (1992) · Annual Review of Nutrition · doi:10.1146/annurev.nu.12.070192.001231 · Cited by 679 · see citing works
Kuo, L. E., Kitlinska, J. B., Tilan, J. U., Li, L., Baker, S. B., Johnson, M. D., Lee, E. W., Burnett, M. S., Fricke, S. T., Kvetnansky, R., et al. (2007) · Nature Medicine · doi:10.1038/nm1611 · Cited by 656 · see citing works
Reversal of obesity by targeted ablation of adipose tissue
Kolonin, M. G., Saha, P., Chan, L., Pasqualini, R., & Arap, W. (2004) · Nature Medicine · doi:10.1038/nm1048 · Cited by 596 · see citing works
LRP: Role in Vascular Wall Integrity and Protection from Atherosclerosis
Boucher, P., Gotthardt, M., Li, W., Anderson, R. G. W., & Herz, J. (2003) · Science · doi:10.1126/science.1082095 · Cited by 581 · see citing works
Adipose Development: From Stem Cell to Adipocyte
Otto, T. C., & Lane, M. D. (2005) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.1080/10409230591008189 · Cited by 531 · see citing works
Nishimura, S., Manabe, I., Nagasaki, M., Hosoya, Y., Yamashita, H., Fujita, H., Ohsugi, M., Tobe, K., Kadowaki, T., Nagai, R., et al. (2007) · Diabetes · doi:10.2337/db06-1749 · Cited by 440 · see citing works
Ephrin-B2 Controls Cell Motility and Adhesion during Blood-Vessel-Wall Assembly
Foo, S. S. C., Turner, C. J., Adams, S., Compagni, A., Aubyn, D., Kogata, N., Lindblom, P., Shani, M., Zicha, D., & Adams, R. H. (2006) · Cell · doi:10.1016/j.cell.2005.10.034 · Cited by 439 · see citing works
Altiok, S., Xu, M. J., & Spiegelman, B. M. (1997) · Genes & Development · doi:10.1101/gad.11.15.1987 · Cited by 378 · see citing works
Lazar, M. A. (2004) · Biochimie · doi:10.1016/j.biochi.2004.10.021 · Cited by 138 · see citing works
A morphological study of the adipocyte precursor.
Cinti, S., CIGOLINI, M., Bosello, O., & Björntorp, P. A. (1984) · PubMed · Cited by 85 · see citing works
Iyama, K., Ohzono, K., & Usuku, G. (1979) · Virchows Archiv B Cell Pathology Including Molecular Pathology · doi:10.1007/bf02889932 · Cited by 76 · see citing works
Graves, R. A., Tontonoz, P., Platt, K. A., et al. (1992) · Journal of Cellular Biochemistry · doi:10.1002/jcb.240490303 · Cited by 67 · see citing works
Temporally regulated expression of Cre recombinase in neural stem cells
Yu, T., Dandekar, M., Monteggia, L. M., Parada, L. F., & Kernie, S. G. (2005) · genesis · doi:10.1002/gene.20110 · Cited by 62 · see citing works
Klaus, S., Cassard, A., & Ricquier, D. (1991) · The Journal of Cell Biology · doi:10.1083/jcb.115.6.1783 · Cited by 61 · see citing works
sn-glycerol-3-phosphate dehydrogenase gene expression during mouse adipocyte development in vivo
Cook, J. R., & Kozak, L. P. (1982) · Developmental Biology · doi:10.1016/0012-1606(82)90189-0 · Cited by 34 · see citing works
Flagged first, then by citations
Research works printed but not linked: 1
- [25]Cinti S Cigolini M Bosello O Bjorntorp P J Submicrosc Cytol 1984 16 243 6325721
Cited by
Sorted by citations
Satellite Cells and the Muscle Stem Cell Niche
Yin, H., Price, F., & Rudnicki, M. A. (2013) · Physiological Reviews · doi:10.1152/physrev.00043.2011 · Cited by 2,166 · see citing works
Mesenchymal stem cell perspective: cell biology to clinical progress
Pittenger, M. F., Discher, D. E., Péault, B. M., Phinney, D. G., Hare, J. M., & Caplan, A. I. (2019) · npj Regenerative Medicine · doi:10.1038/s41536-019-0083-6 · Cited by 2,008 · see citing works
PPARγ signaling and metabolism: the good, the bad and the future
Ahmadian, M., Suh, J. M., Hah, N., Liddle, C., Atkins, A. R., Downes, M., & Evans, R. M. (2013) · Nature Medicine · doi:10.1038/nm.3159 · Cited by 2,016 · see citing works
Self-citationMuscle injury activates resident fibro/adipogenic progenitors that facilitate myogenesis
Joe, A. W. B., Yi, L., Natarajan, A., Le Grand, F., So, L., Wang, J., Rudnicki, M. A., & Rossi, F. M. V. (2010) · Nature Cell Biology · doi:10.1038/ncb2015 · Cited by 1,690 · see citing works
Mechanisms involved in the therapeutic properties of mesenchymal stem cells
da Silva Meirelles, L., Fontes, A. M., Covas, D. T., & Caplan, A. I. (2009) · Cytokine & Growth Factor Reviews · doi:10.1016/j.cytogfr.2009.10.002 · Cited by 1,436 · see citing works
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
Hypoxia-inducible factors regulate tumorigenic capacity of glioma stem cells
Li, Z., Bao, S., Wu, Q., Wang, H., Eyler, C., Sathornsumetee, S., Shi, Q., Cao, Y., Lathia, J., McLendon, R. E., et al. (2009) · Cancer Cell · doi:10.1016/j.ccr.2009.03.018 · Cited by 1,354 · see citing works
Petrovic, N., Walden, T. B., Shabalina, I. G., Timmons, J. A., Cannon, B., & Nedergaard, J. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.053942 · Cited by 1,263 · see citing works
Fat tissue, aging, and cellular senescence
Tchkonia, T., Morbeck, D. E., Von Zglinicki, T., Van Deursen, J., Lustgarten, J., Scrable, H., Khosla, S., Jensen, M. D., & Kirkland, J. L. (2010) · Aging Cell · doi:10.1111/j.1474-9726.2010.00608.x · Cited by 1,094 · see citing works
Adipose tissue expandability, lipotoxicity and the Metabolic Syndrome — An allostatic perspective
Virtue, S., & Vidal-Puig, A. (2010) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2009.12.006 · Cited by 1,013 · see citing works
Ambrosi, T. H., Scialdone, A., Graja, A., Gohlke, S., Jank, A.-M., Bocian, C., Woelk, L., Fan, H., Logan, D. W., Schürmann, A., et al. (2017) · Cell Stem Cell · doi:10.1016/j.stem.2017.02.009 · Cited by 856 · see citing works
The ominous triad of adipose tissue dysfunction: inflammation, fibrosis, and impaired angiogenesis.
Crewe, C., An, Y. A., & Scherer, P. E. (2017) · Journal of Clinical Investigation · doi:10.1172/jci88883 · Cited by 732 · 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
Regeneration of fat cells from myofibroblasts during wound healing
Plikus, M. V., Guerrero-Juarez, C. F., Ito, M., Li, Y. R., Dedhia, P. H., Zheng, Y., Shao, M., Gay, D. L., Ramos, R., Hsi, T.-C., et al. (2017) · Science · doi:10.1126/science.aai8792 · Cited by 584 · see citing works
Butler, J. M., Kobayashi, H., & Rafii, S. (2010) · Nature Reviews Cancer · doi:10.1038/nrc2791 · Cited by 578 · 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
The cell biology of fat expansion
Rutkowski, J. M., Stern, J. H., & Scherer, P. E. (2015) · Journal of Cell Biology · doi:10.1083/jcb.201409063 · Cited by 541 · see citing works
Visceral and subcutaneous fat have different origins and evidence supports a mesothelial source
Chau, Y.-Y., Bandiera, R., Serrels, A., Martínez-Estrada, O. M., Qing, W., Lee, M., Slight, J., Thornburn, A., Berry, R., McHaffie, S., et al. (2014) · Nature Cell Biology · doi:10.1038/ncb2922 · Cited by 518 · see citing works
Frenette, P. S., Pinho, S., Lucas, D., & Scheiermann, C. (2013) · Annual Review of Immunology · doi:10.1146/annurev-immunol-032712-095919 · Cited by 462 · see citing works
Gupta, R. K., Mepani, R. J., Kleiner, S., Lo, J. C., Khandekar, M. J., Cohen, P., Frontini, A., Bhowmick, D. C., Ye, L., Cinti, S., et al. (2012) · Cell Metabolism · doi:10.1016/j.cmet.2012.01.010 · Cited by 426 · see citing works
Transdifferentiation properties of adipocytes in the adipose organ
Cinti, S. (2009) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00183.2009 · Cited by 379 · see citing works
Walter, M., Liang, S., Ghosh, S., Hornsby, P. J., & Li, R. (2009) · Oncogene · doi:10.1038/onc.2009.130 · Cited by 312 · see citing works
Davis, K. E., D. Neinast, M., Sun, K., M. Skiles, W., D. Bills, J., A. Zehr, J., Zeve, D., D. Hahner, L., W. Cox, D., M. Gent, L., et al. (2013) · Molecular Metabolism · doi:10.1016/j.molmet.2013.05.006 · Cited by 278 · see citing works
Self-citationEllis, B. L., Hirsch, M. L., Barker, J. C., Connelly, J. P., Steininger, R. J., & Porteus, M. H. (2013) · Virology Journal · doi:10.1186/1743-422x-10-74 · Cited by 252 · see citing works
Adipose-derived stromal cells: their identity and uses in clinical trials, an update
Casteilla, L. (2011) · World Journal of Stem Cells · doi:10.4252/wjsc.v3.i4.25 · Cited by 235 · see citing works
Mesenchymal markers on human adipose stem/progenitor cells
Zimmerlin, L., Donnenberg, V. S., Rubin, J. P., & Donnenberg, A. D. (2013) · Cytometry Part A · doi:10.1002/cyto.a.22227 · Cited by 225 · see citing works
Activin A Plays a Critical Role in Proliferation and Differentiation of Human Adipose Progenitors
Zaragosi, L.-E., Wdziekonski, B., Villageois, P., Keophiphath, M., Maumus, M., Tchkonia, T., Bourlier, V., Mohsen-Kanson, T., Ladoux, A., Elabd, C., et al. (2010) · Diabetes · doi:10.2337/db10-0013 · Cited by 184 · 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
Brown adipose tissue: Development, metabolism and beyond
Schulz, T. J., & Tseng, Y.-H. (2013) · Biochemical Journal · doi:10.1042/bj20130457 · Cited by 173 · see citing works
PDGFRα signaling drives adipose tissue fibrosis by targeting progenitor cell plasticity
Iwayama, T., Steele, C., Yao, L., Dozmorov, M. G., Karamichos, D., Wren, J. D., & Olson, L. E. (2015) · Genes & Development · doi:10.1101/gad.260554.115 · Cited by 164 · see citing works
Emerging role of bone morphogenetic proteins in adipogenesis and energy metabolism
Schulz, T. J., & Tseng, Y.-H. (2009) · Cytokine & Growth Factor Reviews · doi:10.1016/j.cytogfr.2009.10.019 · 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
Jiang, Y., Berry, D. C., & Graff, J. M. (2017) · eLife · doi:10.7554/elife.30329 · Cited by 135 · see citing works
Self-citationMacrophages and the Regulation of Adipose Tissue Remodeling
Martinez-Santibañez, G., & Nien-Kai Lumeng, C. (2014) · Annual Review of Nutrition · doi:10.1146/annurev-nutr-071812-161113 · Cited by 111 · see citing works
Tam, J., Duda, D. G., Perentes, J. Y., Quadri, R. S., Fukumura, D., & Jain, R. K. (2009) · PLoS ONE · doi:10.1371/journal.pone.0004974 · Cited by 99 · see citing works
Genetic Link Between Obesity and <i>MMP14</i>-Dependent Adipogenic Collagen Turnover
Chun, T.-H., Inoue, M., Morisaki, H., Yamanaka, I., Miyamoto, Y., Okamura, T., Sato-Kusubata, K., & Weiss, S. J. (2010) · Diabetes · doi:10.2337/db10-0073 · Cited by 97 · 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
Molecular Nutrition Research—The Modern Way Of Performing Nutritional Science
Norheim, F., Gjelstad, I., Hjorth, M., Vinknes, K., Langleite, T., Holen, T., Jensen, J., Dalen, K., Karlsen, A., Kielland, A., et al. (2012) · Nutrients · doi:10.3390/nu4121898 · Cited by 83 · see citing works
Tipping the scale: muscle versus fat
Rodeheffer, M. S. (2010) · Nature Cell Biology · doi:10.1038/ncb0210-102 · Cited by 51 · see citing works
Luo, X., Jia, R., Yao, Q., Xu, Y., Luo, Z., Luo, X., & Wang, N. (2016) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201500714 · Cited by 30 · see citing works
Activatin’ human adipose progenitors in obesity
Sethi, J. K. (2010) · Diabetes · doi:10.2337/db10-0923 · Cited by 25 · see citing works
Tchoukalova, Y. D., Krishnapuram, R., White, U. A., Burk, D., Fang, X., Nijland, M. J., & Nathanielsz, P. W. (2014) · International Journal of Obesity · doi:10.1038/ijo.2013.106 · Cited by 19 · see citing works
Rubinow, K. B., Wang, S., den Hartigh, L. J., Subramanian, S., Morton, G. J., Buaas, F. W., Lamont, D., Gray, N., Braun, R. E., & Page, S. T. (2015) · Andrology · doi:10.1111/andr.12055 · Cited by 16 · see citing works
- Authors
- Tang, W., Zeve, D., Suh, J. M., Bosnakovski, D., Kyba, M., Hammer, R. E., Tallquist, M. D., & Graff, J. M.
- Affiliations
- The University of Texas Southwestern Medical Center (US)
- Corresponding author
- Graff, Jonathan M.
- Venue
- Science
- Published
- 2008-10-24
- Volume
- 322
- Issue
- 5901
- Pages
- 583-586
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- PMC
- PMC2597101
- OpenAlex
- W1997432717
- Cited by
- 1,113
- References
- 29
- Citations by year
- 2026: 19 · 2025: 30 · 2024: 35 · 2023: 52 · 2022: 49 · 2021: 49 · 2020: 47 · 2019: 69 · 2018: 77 · 2017: 74 · 2016: 72 · 2015: 73 · 2014: 79 · 2013: 102 · 2012: 77
- FWCI
- 46.95
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Goce Delchev University Repository (Goce Delčev University of Štip) (acceptedVersion)
- Funders
- National Institutes of Health (5r01dk064261-10)
- National Heart, Lung, and Blood Institute (R01HL074257)
- National Institute of Diabetes and Digestive and Kidney Diseases (R01-DK064261, R01DK066556, 1R01DK064261)
- 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
- white adipose tissue, adipose progenitor cells, adipocyte development, adipogenesis, mural cells, adipose tissue regeneration
- MeSH terms
- Adipose Tissue, Animals, Blood Vessels, Cell Separation, Cells, Cultured, Doxycycline, Mice, Transgenic, Antigens, CD, Stromal Cells, Cell Lineage, Gene Expression Profiling, Multipotent Stem Cells, PPAR gamma, Cell Proliferation, Adipogenesis, Mice, Adipocytes, White
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