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PRDM16 controls a brown fat/skeletal muscle switch
Open accessAbstract
Brown fat can increase energy expenditure and protect against obesity through a specialized program of uncoupled respiration. Here we show by in vivo fate mapping that brown, but not white, fat cells arise from precursors that express Myf5, a gene previously thought to be expressed only in the myogenic lineage. We also demonstrate that the transcriptional regulator PRDM16 (PRD1-BF1-RIZ1 homologous domain containing 16) controls a bidirectional cell fate switch between skeletal myoblasts and brown fat cells. Loss of PRDM16 from brown fat precursors causes a loss of brown fat characteristics and promotes muscle differentiation. Conversely, ectopic expression of PRDM16 in myoblasts induces their differentiation into brown fat cells. PRDM16 stimulates brown adipogenesis by binding to PPAR-gamma (peroxisome-proliferator-activated receptor-gamma) and activating its transcriptional function. Finally, Prdm16-deficient brown fat displays an abnormal morphology, reduced thermogenic gene expression and elevated expression of muscle-specific genes. Taken together, these data indicate that PRDM16 specifies the brown fat lineage from a progenitor that expresses myoblast markers and is not involved in white adipogenesis.
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“Emerging evidence suggests that brown adipocytes located in different anatomical locations may arise from different developmental origins.”
From Cellular bioenergetics as a target for obesity therapy (2010) · cites this paper as [92]
In the citing paper
“Most recently, lineage-tracing studies have indicated that myf5-expressing progenitors can give rise to both skeletal muscle and the preformed BAT, in the interscapular and peri-renal depots 92 (Figure 3).”
From Cellular bioenergetics as a target for obesity therapy (2010) · cites this paper as [92]
In the citing paper
“However, not all brown fat cells are derived from myf5-expressing progenitors. For example, the brown fat cells emerging in white fat in response to β3-adrenergic stimulation are not marked by the myf5-driven fluorescent protein 92.”
From Cellular bioenergetics as a target for obesity therapy (2010) · cites this paper as [92]
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“Current data suggest that in rodents, PRDM16 plays an important role in specifying brown fat cell fate for the interscapular, but not systemic brown adipose depots 92.”
From Cellular bioenergetics as a target for obesity therapy (2010) · cites this paper as [92]
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“The genetic program leading to brown adipose tissue development, and potentially to the high abundance of mitochondria, is initiated by the zinc-finger protein PRDM16 (202)(203)(204).”
From The role of mitochondria in the pathogenesis of type 2 diabetes (2010) · cites this paper as [203]
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Puar, T. H. K., van Berkel, A., Gotthardt, M., Havekes, B., Hermus, A. R., Lenders, J. W. M., Lichtenbelt, W. D. V. M., Xu, Y., Brans, B. T., & Timmers, H. J. L. M. (2015) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2015-3205 · Cited by 37
Kwon, M., Lim, S.-J., Joung, E., Lee, B., Oh, C., & Kim, H. (2018) · Journal of Functional Foods · doi:10.1016/j.jff.2018.05.063 · Cited by 37
Ran, C., Graae, L., Magnusson, P. K. E., Pedersen, N. L., Olson, L., & Belin, A. C. (2014) · BMC Medical Genetics · doi:10.1186/1471-2350-15-38 · Cited by 36
Formation and activation of thermogenic fat
Wu, J., Jun, H., & McDermott, J. R. (2015) · Trends in Genetics · doi:10.1016/j.tig.2015.03.003 · Cited by 37
“These shPRDM16 brown preadipocytes differentiated into muscle-like cells instead of the expected white fat cells [16].”
BackgroundInfluentialMozzetta, C., Pontis, J., & Ait‐Si‐Ali, S. (2014) · Antioxidants and Redox Signaling · doi:10.1089/ars.2014.6116 · Cited by 37
Fritah, A., Steel, J. H., Parker, N., Nikolopoulou, E., Christian, M., Carling, D., & Parker, M. G. (2012) · PLoS ONE · doi:10.1371/journal.pone.0032520 · Cited by 37
The Role of Thyrotropin Receptor Activation in Adipogenesis and Modulation of Fat Phenotype
Draman, M. S., Stechman, M., Scott-Coombes, D. M., Dayan, C. M., Rees, D. A., Ludgate, M. E., & Zhang, L. (2017) · Frontiers in Endocrinology · doi:10.3389/fendo.2017.00083 · Cited by 37
“WAT and BAT are derived from distinct lineages of mesenchymal stem cells (MSCs), Myf5 + for BAT (also muscle progenitors) but Myf5 − for WAT (27). two adipose types also differ morphologically with WAT having a single large fat vacuole and BAT having many smaller fat droplets and higher numbers of…”
Tamucci, K. A., Namwanje, M., Fan, L., & Qiang, L. (2017) · Protein & Cell · doi:10.1007/s13238-017-0434-2 · Cited by 39
“These beige adipocyte progenitors are smooth muscle-like pericytes that express platelet-derived growth factor (PDGF) receptor α but not Myf-5 (PDGFRα; Myf5) (Seale et al. 2008; Lee et al. 2012; Sanchez-Gurmaches et al. 2012; Long et al. 2014).”
BackgroundWang, Y., Paulo, E., Wu, D., Wu, Y., Huang, W., Chawla, A., & Wang, B. (2017) · Diabetes · doi:10.2337/db17-0296 · Cited by 36
“Classic, also called constitutive, brown adipocytes are present in interscapular and perirenal adipose tissues, and they originate from Myf5/Pax7 skeletal muscle progenitors (8).”
BackgroundJiang, J., Li, P., Ling, H., Xu, Z., Yi, B., & Zhu, S. (2018) · Human Cell · doi:10.1007/s13577-018-0210-5 · Cited by 35
Choi, J. H., Song, N., Lee, A. R., Lee, D. H., Seo, M.-J., Kim, S., Chang, S., Yang, D. K., Hwang, Y.-J., Hwang, K., et al. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms20010026 · Cited by 36
Association of uncoupling protein (Ucp) gene polymorphisms with cardiometabolic diseases
Pravednikova, A. E., Shevchenko, S. Y., Kerchev, V. V., Схиртладзе, М. Р., Николаевна, Л. С., Kachaev, Z. M., Egorov, A. D., & Shidlovskii, Y. V. (2020) · Molecular Medicine · doi:10.1186/s10020-020-00180-4 · Cited by 37
“PRDM16 was identified as a universal brown fat cell-fate determination factor (Seale et al. 2007) that promotes differentiation of Myf5-positive myogenic precursor cells into brown adipocytes while banning myogenic differentiation (Seale et al. 2008).”
BackgroundProstaglandin E2signals white-to-brown adipogenic differentiation
García‐Alonso, V., & Clària, J. (2014) · Adipocyte · doi:10.4161/adip.29993 · Cited by 38
“For example, PRDM16 is a BAT-specific transcription factor that interacts with PGC-1a (a PPARg co-activator) and C/EBPb to trigger a brown adipocyte differentiation program.(18) On the other hand, C/EBPa induces PPARg in a positive feedback loop, thereby maintaining the differentiated cell state of adipocytes.”
BackgroundAdipogenic potential of skeletal muscle satellite cells
Sanna, M., Franzin, C., Pozzobon, M., Favaretto, F., Rossi, C. A., Calcagno, A., Scarda, A., Prà, C. D., Pilon, C., Milan, G., et al. (2009) · Clinical Lipidology · doi:10.2217/clp.09.8 · Cited by 36
A Comparative Perspective on Wnt/β-Catenin Signalling in Cell Fate Determination
Garcin, C. L., & Habib, S. J. (2017) · Results and problems in cell differentiation · doi:10.1007/978-3-319-53150-2_15 · Cited by 40
The evolution of metabolic regulation in animals
Seebacher, F. (2017) · Comparative Biochemistry and Physiology Part B Biochemistry and Molecular Biology · doi:10.1016/j.cbpb.2017.11.002 · Cited by 38
Sexual Dimorphism in Brown Adipose Tissue Activation and White Adipose Tissue Browning
Gómez-García, I., Trepiana, J., Fernández‐Quintela, A., Giralt, M., & Portillo, M. P. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23158250 · Cited by 35
“Nevertheless, the beige adipocytes that develop in the WAT do not share the same provenance as the classic brown adipocytes that emerge before birth [9].”
BackgroundStage-specific nutritional management and developmental programming to optimize meat production
Zhao, L., Liu, X., Gomez, N. A., Gao, Y., Son, J. S., Chae, S. A., Zhu, M. J., & Du, . (2023) · Journal of Animal Science and Biotechnology/Journal of animal science and biotechnology · doi:10.1186/s40104-022-00805-0 · Cited by 39
Metabolaging: a new geroscience perspective linking aging pathologies and metabolic dysfunction
Khalaf, F., Barayan, D., Saldanha, S., & Jeschke, M. G. (2025) · Metabolism · doi:10.1016/j.metabol.2025.156158 · Cited by 43
Inhibition of CK2 binding to BMPRIa induces C2C12 differentiation into osteoblasts and adipocytes
Moseychuk, O., Akkiraju, H., Dutta, J., D’Angelo, A., Bragdon, B. C., Duncan, R. L., & Nohe, A. (2013) · Journal of Cell Communication and Signaling · doi:10.1007/s12079-013-0199-1 · Cited by 36
Bogani, D., Morgan, M. A., Nelson, A., Costello, I., McGouran, J. F., Kessler, B. M., Robertson, E. J., & Bikoff, E. K. (2013) · Molecular and Cellular Biology · doi:10.1128/mcb.00498-13 · Cited by 34
Brown Adipose Tissue in Cetacean Blubber
Hashimoto, O., Ohtsuki, H., Kakizaki, T., Amou, K., Sato, R., Doi, S., Sara, K., Matsuda, A., Sugiyama, M., Funaba, M., et al. (2015) · PLoS ONE · doi:10.1371/journal.pone.0116734 · Cited by 37
Urano, T., Shiraki, M., Sasaki, N., Ouchi, Y., & Inoue, S. (2014) · Aging Cell · doi:10.1111/acel.12228 · Cited by 34
“PRDM16 plays an important role in controlling of differentiation of the brown fat lineage from a progenitor that expresses myoblast markers (Seale et al., 2008; Yin et al., 2013).”
BackgroundInduced pluripotent stem cells and the stability of the differentiated state
Colman, A., & Dreesen, O. (2009) · EMBO Reports · doi:10.1038/embor.2009.142 · Cited by 41
“Overexpression of PRDM16, which interacts with PPARγ—a master regulator of adipogenesis—in myoblasts, facilitates their differentiation into brown fat cells”
BackgroundComparative analysis of microRNA expression in mouse and human brown adipose tissue
Güller, I., McNaughton, S. A., Crowley, T. M., Gilsanz, V., Kajimura, S., Watt, M. J., & Russell, A. P. (2015) · BMC Genomics · doi:10.1186/s12864-015-2045-8 · Cited by 35
Self-citationCellular mechanisms of MR regulation of adipose tissue physiology and pathophysiology
Armani, A., Marzolla, V., Fabbri, A., & Caprio, M. (2015) · Journal of Molecular Endocrinology · doi:10.1530/jme-15-0122 · Cited by 35
“…5 (myf5)-positive embryonic precursors, from which BAT and skeletal muscle derive, and should be considered as a distinct subtype of adipose cells (Seale et al. 2008). http://jme.endocrinology-journals.org 2015 Society for Endocrinology DOI: 10.1530/JME-15-0122 Printed in Great…”
BackgroundInfluentialFat tissues, the brite and the dark sides
Chen, Y., Pan, R., & Pfeifer, A. (2016) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-016-1884-8 · Cited by 36
“Although Myf5 was initially reported as a specific marker for precursors that give rise to brown adipocytes and muscle cells [41], recent studies in mice showed that Myf5-positive precursors also give rise to white adipocytes in anterior/dorsal depots indicating that Myf5 is rather a marker for cell position [39].”
BackgroundSwitching harmful visceral fat to beneficial energy combustion improves metabolic dysfunctions
Yang, X., Sui, W., Zhang, M., Dong, M., Lim, S., Seki, T., Guo, Z., Fischer, C., Lu, H., Zhang, C., et al. (2017) · JCI Insight · doi:10.1172/jci.insight.89044 · Cited by 35
Metadata
- Authors
- Seale, P., Bjork, B., Yang, W., Kajimura, S., Chin, S., Kuang, S., Scimè, A., Devarakonda, S., Conroe, H. M., Erdjument-Bromage, H., Tempst, P., Rudnicki, M. A., Beier, D. R., & Spiegelman, B. M.
- Affiliations
- Harvard University (US)
- Brigham and Women's Hospital (US)
- Memorial Sloan Kettering Cancer Center (US)
- Corresponding author
- Spiegelman, Bruce M.
- ORCID
- Venue
- Nature
- Published
- 2008-08
- Volume
- 454
- Issue
- 7207
- Pages
- 961-967
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC2583329
- OpenAlex
- W2104827888
- Cited by
- 2,347
- References
- 44
- Citations by year
- 2026: 77 · 2025: 71 · 2024: 118 · 2023: 115 · 2022: 129 · 2021: 134 · 2020: 141 · 2019: 134 · 2018: 168 · 2017: 165 · 2016: 139 · 2015: 167 · 2014: 157 · 2013: 181 · 2012: 134
- FWCI
- 71.30
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- American Heart Association
- National Institute of Diabetes and Digestive and Kidney Diseases (R37DK031405)
- National Institute of Arthritis and Musculoskeletal and Skin Diseases (R01AR044031)
- Topics
- Health Sciences › Medicine › Physiology (medical) › Adipose Tissue and Metabolism
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Peroxisome Proliferator-Activated Receptors
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Keywords
- PRDM16, brown adipose tissue, skeletal muscle, Myf5, brown adipogenesis, PPARγ, thermogenesis, myogenesis, energy expenditure, obesity
- MeSH terms
- Animals, Adipose Tissue, Brown, Cell Differentiation, Cell Line, Chlorocebus aethiops, DNA-Binding Proteins, Male, Transcription Factors, Muscle, Skeletal, Gene Expression Regulation, Developmental, COS Cells, Muscle Development, PPAR gamma, Mice, Myogenic Regulatory Factor 5, Adipocytes, Brown, Adipocytes, White
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