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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]
In the citing paper
“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]
In the citing paper
“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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Thyroid hormones and browning of adipose tissue
Weiner, J., Hankir, M. K., Heiker, J. T., Fenske, W. K., & Krause, K. (2017) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2017.01.011 · Cited by 64
“14 It should be noted that as well as having separate lineages (Seale et al., 2008), beige and brown 15 adipocytes possess differential gene expression profiles (Wu et al., 2012) with cluster of 16 differentiation 137 (CD137), transmembrane protein 26 (TMEM26) and T-box transcription 17 factor 1…”
BackgroundWang, S., Pan, M., Hung, W., Tung, Y., & Ho, C. (2019) · Food & Function · doi:10.1039/c8fo02154f · Cited by 64
Maurer, S., Harms, M., & Boucher, J. (2020) · FEBS Journal · doi:10.1111/febs.15470 · Cited by 65
Transcriptional targets in adipocyte biology
Rosen, E. D., Eguchi, J., & Xu, Z. (2009) · Expert Opinion on Therapeutic Targets · doi:10.1517/14728220903039706 · Cited by 61
“Mice lacking PRDM16 have abnormal brown fat with enhanced muscle gene expression, and the presence or absence of PRDM16 in cultured myoblasts determines which pathway they follow [94].”
BackgroundRyan, K. J. P., Daniel, Z. C. T. R., Craggs, L., Parr, T., & Brameld, J. M. (2013) · Journal of Endocrinology · doi:10.1530/joe-12-0234 · Cited by 64
“Recent findings from lineage tracing studies have shown that brown adipocytes develop in vivo from a MYF5-positive progenitor cell (Seale et al. 2008), suggesting that these myf5-expressing C2C12 cells might also be converting to brown adipocytes.”
BackgroundInfluentialRole of developmental transcription factors in white, brown and beige adipose tissues
Hilton, C., Karpe, F., & Pinnick, K. E. (2015) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2015.02.003 · Cited by 61
Brown Fat and Skeletal Muscle: Unlikely Cousins?
Farmer, S. R. (2008) · Cell · doi:10.1016/j.cell.2008.08.018 · Cited by 60
“A recent study published in Nature (Seale et al., 2008) identifies a population of progenitor cells that gives rise to brown fat and skeletal muscle but not white fat.”
BackgroundSuárez, J., Rivera, P., Arrabal, S., Crespillo, A., Serrano, A., Baixerás, E., Pavón, F. J., Cifuentes, M., Nogueiras, R., Ballesteros, J., et al. (2013) · Disease Models & Mechanisms · doi:10.1242/dmm.013110 · Cited by 63
“…16 (PRDM16), fibroblast growth factor (FGF)-21, PPARγ coactivator 1α (PGC-1α) and prostaglandins, have been proposed to induce a BAT-specific gene expression profile in response to adrenergic stimulation (Seale et al., 2007; Seale et al., 2008; Seale et al., 2011; Vegiopoulos et al., 2010).”
BackgroundNutritional regulation of fetal growth and implications for productive life in ruminants
Symonds, M. E., Sebert, S. P., & Budge, H. (2010) · animal · doi:10.1017/s1751731110000479 · Cited by 63
“Furthermore, it has also been suggested that brown adipocytes have the same lineage as skeletal myoblasts, a process that may be regulated by bone morphogenetic protein acting through PRD1-BF1RIZ1 homologous domain containing 16 gene (Seale et al., 2008; Tseng et al., 2008).”
BackgroundECM microenvironment unlocks brown adipogenic potential of adult human bone marrow-derived MSCs
Lee, M. H., Goralczyk, A. G., Kriszt, R., Ang, X. M., Badowski, C., Li, Y., Summers, S. A., Toh, S.-A. E. S., Yassin, M. S., Shabbir, A., et al. (2016) · Scientific Reports · doi:10.1038/srep21173 · Cited by 59
Parkin‐mediated mitophagy is downregulated in browning of white adipose tissue
Taylor, D., & Gottlieb, R. A. (2017) · Obesity · doi:10.1002/oby.21786 · Cited by 61
“In mice, brown and beige adipocytes are derived from distinct embryonic precursors and may be differentially regulated (5).”
Nishimoto, Y., & Tamori, Y. (2017) · Journal of Atherosclerosis and Thrombosis · doi:10.5551/jat.rv17011 · Cited by 62
The effect of type 2 diabetes mellitus and obesity on muscle progenitor cell function
Teng, S., & Huang, P. (2019) · Stem Cell Research & Therapy · doi:10.1186/s13287-019-1186-0 · Cited by 63
Combating Obesity With Thermogenic Fat: Current Challenges and Advancements
Pan, R., Zhu, X., Maretich, P., & Chen, Y. (2020) · Frontiers in Endocrinology · doi:10.3389/fendo.2020.00185 · Cited by 63
“Crucially, scientists have discovered that classical brown adipocytes share a common progenitor with skeletal myocytes (22).”
BackgroundZhou, J., Poudel, A., Chandramani-Shivalingappa, P., Xu, B., Welchko, R., & Li, L. (2019) · Endocrine · doi:10.1007/s12020-018-1826-7 · Cited by 59
Morozzi, G., Beccafico, S., Bianchi, R., Riuzzi, F., Bellezza, I., Giambanco, I., Arcuri, C., Minelli, A., & Donato, R. (2017) · Cell Death & Differentiation · doi:10.1038/cdd.2017.132 · Cited by 58
Two types of brown adipose tissue in humans
Lidell, M. E., Betz, M. J., & Enerbäck, S. (2013) · Adipocyte · doi:10.4161/adip.26896 · Cited by 61
“64 adipocyte Volume 3 Issue 1 of different developmental origin since lineage tracing experiments have demonstrated that classical brown adipocytes, but not beige adipocytes, derive from precursor cells that express Myf5, a gene encoding a regulatory factor crucial for myogenesis and previously thought to be expressed…”
BackgroundKim, W. K., Choi, H.-R., Park, S. G., Ko, Y., Bae, K., & Lee, S. C. (2011) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2011.11.004 · Cited by 59
“However, recent studies demonstrated that brown adipocytes have an origin that is distinct from white adipocytes and that they originate from myoblast precursor cells (Seale et al., 2007, 2008, 2009).”
BackgroundInfluentialNovel SNPs in the PRDM16 gene and their associations with performance traits in chickens
Han, R., Wei, Y., Kang, X., Chen, H., Sun, G., Li, G., Bai, Y., Tian, Y., & Huang, Y. (2011) · Molecular Biology Reports · doi:10.1007/s11033-011-1081-y · Cited by 58
Festuccia, W. T., Blanchard, P.-G., Richard, D., & Deshaies, Y. (2010) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00821.2009 · Cited by 58
“Interestingly, rosiglitazone increased mRNA levels of the orphan nuclear receptor SHP (NROB2), a negative regulator of PGC- expression and energy expenditure in brown adipocytes (40), and reduced those of both SIRT3, a protein involved in the control of BAT PGC- expression and mitochondrial biogenesis (31), and PRDM16…”
BackgroundChou, C., Lin, Y.-Y., Wang, H.-K., Zhu, X., Giovarelli, M., Briata, P., Gherzi, R., Garvey, W. T., & Chen, C. (2014) · Diabetes · doi:10.2337/db13-1901 · Cited by 58
Direct action of capsaicin in brown adipogenesis and activation of brown adipocytes
Kida, R., Yoshida, H., Murakami, M., Shirai, M., Hashimoto, O., Kawada, T., Matsui, T., & Funaba, M. (2016) · Cell Biochemistry and Function · doi:10.1002/cbf.3162 · Cited by 59
Regulation of adipocyte thermogenesis: mechanisms controlling obesity
Hussain, M. F., Roesler, A. A., & Kazak, L. (2020) · FEBS Journal · doi:10.1111/febs.15331 · Cited by 60
Duhoux, F. P., Ameye, G., Montano‐Almendras, C. P., Bahloula, K., Mozziconacci, M. J., Laibe, S., Włodarska, I., Michaux, L., Talmant, P., Richebourg, S., et al. (2011) · British Journal of Haematology · doi:10.1111/j.1365-2141.2011.08918.x · Cited by 61
“PRDM16 also plays a physiological role in tissue development (Warner et al, 2007; Seale et al, 2008; Kajimura et al, 2009; Bjork et al, 2010; Horn et al, 2011), a characteristic shared by many oncogenes.”
BackgroundChemical compound-based direct reprogramming for future clinical applications.
Takeda, Y., Harada, Y., Yoshikawa, T., & Dai, P. (2018) · Bioscience Reports · doi:10.1042/bsr20171650 · Cited by 57
Uncovering the Role of p38 Family Members in Adipose Tissue Physiology
Leiva, M., Matesanz, N., Pulgarín-Alfaro, M., Nikolić, I., & Sabio, G. (2020) · Frontiers in Endocrinology · doi:10.3389/fendo.2020.572089 · Cited by 62
Di, W., Zhang, W., Zhu, B. L., Li, X., Tang, Q., & Zhou, Y. (2020) · Journal of Cellular Physiology · doi:10.1002/jcp.30245 · Cited by 58
Gulbins, A., Horstmann, M., Daser, A., Flögel, U., Oeverhaus, M., Bechrakis, N. E., Banga, J. P., Keitsch, S., Wilker, B., Krause, G., et al. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1211473 · Cited by 58
“An in vivo MRI of the late group was performed and revealed a marked decrease of frontiersin.org01 Abbreviations: GD, Graves’ Disease; TED, thyroid eye di stimulating hormone receptor; IGF-1R, insulin-like growth I/IGF-II, insulin-like growth factor I/II; OFs, orbita Perfluorocarbon Nanoemulsion; WAT, white adipose ad…”
BackgroundInfluentialThe tumor suppressors pRB and p53 as regulators of adipocyte differentiation and function
Hallenborg, P., Feddersen, S., Madsen, L., & Kristiansen, K. (2009) · Expert Opinion on Therapeutic Targets · doi:10.1517/14712590802680141 · Cited by 62
“Moreover, RB +/- mice fed regular chow also displayed signs of increased insulin sensitivity when BMP: Bone-morphogenetic protein; C/EBP: CCAAT/enhancer binding protein; Foxc2: Forkhead box protein c2; Myf5: Myogenic factor 5; MyoD: Myogenic differentiation; PGC-1 α : PPAR γ -cofactor 1 α ; PPAR γ : Peroxisome prolife…”
BackgroundInfluentialFNDC5/irisin, a molecular target for boosting reward-related learning and motivation
Zsuga, J., Tajti, G., Papp, C., Juhász, B., & Gesztelyi, R. (2016) · Medical Hypotheses · doi:10.1016/j.mehy.2016.02.020 · Cited by 59
“Nonetheless, recently an intermediate form of adipocytes was identified called beige or brite (brown in white) adipocytes [25,26].”
BackgroundBrown and Beige Adipose Tissue
Mulya, A., & Kirwan, J. P. (2016) · Endocrinology and Metabolism Clinics of North America · doi:10.1016/j.ecl.2016.04.010 · Cited by 68
White adipose tissue browning and obesity
Cui, X., & Chen, S. (2017) · Journal of Biomedical Research · doi:10.7555/jbr.31.20160101 · Cited by 57
“Classical brown adipocytes originate from precursor cells in the embryonic mesoderm that express Myf5 and Pax7[4].”
BackgroundSeoane‐Collazo, P., Martínez‐Sánchez, N., Milbank, E., & Contreras, C. (2020) · Nutrients · doi:10.3390/nu12020472 · Cited by 61
Developmental programming of offspring adipose tissue biology and obesity risk
Rodgers, A., & Sferruzzi-Perri, A. N. (2021) · International Journal of Obesity · doi:10.1038/s41366-021-00790-w · Cited by 57
Prdm5 Regulates Collagen Gene Transcription by Association with RNA Polymerase II in Developing Bone
Galli, G. G., Honnens de Lichtenberg, K., Carrara, M., Hans, W., Wuelling, M., Mentz, B., Multhaupt, H. A., Fog, C. K., Jensen, K. T., Rappsilber, J., et al. (2012) · PLoS Genetics · doi:10.1371/journal.pgen.1002711 · Cited by 61
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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