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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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Citations
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Molchadsky, A., Ezra, O., Amendola, P. G., Krantz, D., Kogan-Sakin, I., Buganim, Y., Rivlin, N., Goldfinger, N., Folgiero, V., Falcioni, R., et al. (2013) · Cell Death and Differentiation · doi:10.1038/cdd.2013.9 · Cited by 117
“The induction of these cells into the brown fat lineage requires the expression of the transcription factor PRDM16, which, upon stable expression, commits these cells towards the differentiation into brown adipocytes.(25) To this end, C2 cells were infected with either a retroviral vector encoding for PRDM16 or a cont…”
BackgroundZhang, X., Lam, K. S. L., Ye, H., Chung, S. K., Zhou, M., Wang, Y., & Xu, A. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.135509 · Cited by 112
Differentiation of human adipose-derived stem cells into “brite” (brown-in-white) adipocytes
Pisani, D. F. (2011) · Frontiers in Endocrinology · doi:10.3389/fendo.2011.00087 · Cited by 124
Singh, S. P., Schragenheim, J., Cao, J. J., Falck, J. R., Abraham, N. G., & Bellner, L. (2016) · Prostaglandins & Other Lipid Mediators · doi:10.1016/j.prostaglandins.2016.07.004 · Cited by 113
Okla, M., Wang, W., Kang, I., Pashaj, A., Carr, T. P., & Chung, S. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.m115.677724 · Cited by 116
Follistatin Promotes Adipocyte Differentiation, Browning, and Energy Metabolism
Braga, M., Reddy, S. T., Vergnes, L., Pervin, S., Grijalva, V., Stout, D., David, J., Li, X., Tomasian, V., Reid, C. B., et al. (2014) · Journal of Lipid Research · doi:10.1194/jlr.m039719 · Cited by 111
Jimenez-Preitner, M., Berney, X. P., Uldry, M., Vitali, A., Cinti, S., Ledford, J. G., & Thorens, B. (2011) · Cell Metabolism · doi:10.1016/j.cmet.2011.08.008 · Cited by 110
Hung, C., Calejman, C. M., Sánchez-Gurmaches, J., Li, H., Clish, C. B., Hettmer, S., Wagers, A. J., & Guertin, D. A. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.06.007 · Cited by 113
“…Myf5 give rise to myocytes, brown adipocytes, and a subset of white adipocytes (Sanchez-Gurmaches and Guertin, 2014; Sanchez-Gurmaches et al., 2012; Seale et al., 2008), and several recent studies have used the Myf5-Cre knockin allele (Tallquist et al., 2000) to study BAT development (Harms et…”
BackgroundIrisin as a predictor of glucose metabolism in children: sexually dimorphic effects
Al‐Daghri, N. M., Alkharfy, K. M., Rahman, S., Amer, O. E., Vinodson, B., Sabico, S., Piya, M. K., Harte, A. L., McTernan, P. G., Alokail, M. S., et al. (2013) · European Journal of Clinical Investigation · doi:10.1111/eci.12196 · Cited by 110
Regulation and Functions of the Renin‐Angiotensin System in White and Brown Adipose Tissue
Pahlavani, M., Kalupahana, N. S., Ramalingam, L., & Moustaïd‐Moussa, N. (2017) · Comprehensive physiology · doi:10.1002/cphy.c160031 · Cited by 111
Caffeine exposure induces browning features in adipose tissue in vitro and in vivo
Veličković, K., Wayne, D., Leija, H. A. L., Bloor, I. D., Morris, D. E., Law, J., Budge, H., Sacks, H. S., Symonds, M. E., & Sottile, V. (2019) · Scientific Reports · doi:10.1038/s41598-019-45540-1 · Cited by 116
A Novel Therapeutic Approach to Treating Obesity through Modulation of TGFβ Signaling
Koncarevic, A., Kajimura, S., Cornwall-Brady, M. R., Andreucci, A., Pullen, A. E., Sako, D., Kumar, R., Grinberg, A. V., Liharska, K., Ucran, J. A., et al. (2012) · Endocrinology · doi:10.1210/en.2012-1016 · Cited by 111
Self-citationRegulation of glucose homoeostasis by brown adipose tissue
Peirce, V. J., & Vidal‐Puig, A. (2013) · The Lancet Diabetes & Endocrinology · doi:10.1016/s2213-8587(13)70055-x · Cited by 111
Transcriptional Control of Brown and Beige Fat Development and Function
Shapira, S. N., & Seale, P. (2018) · Obesity · doi:10.1002/oby.22334 · Cited by 111
“Loss of PRDM16 in cultured brown adipocytes abrogates brown fat gene expression and increases the expression of muscle genes under certain conditions (62).”
BackgroundSelf-citationResident and migratory adipose immune cells control systemic metabolism and thermogenesis
Man, K., Kallies, A., & Vasanthakumar, A. (2021) · Cellular and Molecular Immunology · doi:10.1038/s41423-021-00804-7 · Cited by 115
Brown vs white adipocytes: The PPARγ coregulator story
Koppen, A., & Kalkhoven, E. (2010) · FEBS Letters · doi:10.1016/j.febslet.2010.06.035 · Cited by 113
Lafontan, M. (2011) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00168.2011 · Cited by 118
Tissue Immunometabolism: Development, Physiology, and Pathobiology
Man, K., Kutyavin, V. I., & Chawla, A. (2016) · Cell Metabolism · doi:10.1016/j.cmet.2016.08.016 · Cited by 108
“For example, fate mapping with Myf5- or Pax7reporter mice shows that brown, but not beige, adipocytes arise from Myf5+/Pax7+ myogenic precursors (Lepper and Fan, 2010; Seale et al., 2008, 2011).”
BackgroundAn expanding job description for Blimp-1/PRDM1
Bikoff, E. K., Morgan, M. A., & Robertson, E. J. (2009) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2009.05.005 · Cited by 108
Hypothalamic control of brown adipose tissue thermogenesis
Labbé, S. M., Caron, A., Lanfray, D., Monge-Roffarello, B., Bartness, T. J., & Richard, D. (2015) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2015.00150 · Cited by 112
“Previous investigations (Timmons et al., 2007; Seale et al., 2008; Tseng et al., 2008) have provided compelling evidence that brown and white fat cells are not only distinct histologically, but that they also origin from different precursor cells (Shan et al., 2013; Sanchez-Gurmaches and Guertin,…”
BackgroundMohsen‐Kanson, T., Hafner, A.-L., Wdziekonski, B., Takashima, Y., Villageois, P., Carrière, A., Svensson, M. K. E., Bagnis, C., Chignon‐Sicard, B., Svensson, P., et al. (2013) · Stem Cells · doi:10.1002/stem.1607 · Cited by 116
Fighting Fat with Fat: The Expanding Field of Adipose Stem Cells
Zeve, D., Tang, W., & Graff, J. (2009) · Cell stem cell · doi:10.1016/j.stem.2009.10.014 · Cited by 109
“Yet this does not appear to be the case during the formation of BAT that, under the influence of external stimuli, is induced within WAT tissue (Seale et al., 2008).”
BackgroundAdipose-derived stromal/stem cells
Gimble, J. M., Bunnell, B. A., Frazier, T. P., Rowan, B. G., Shah, F. S., Thomas‐Porch, C., & Wu, X. (2013) · Organogenesis · doi:10.4161/org.24279 · Cited by 107
Vila‐Bedmar, R., Lorenzo, M., & Fernández‐Veledo, S. (2010) · Endocrinology · doi:10.1210/en.2009-0810 · Cited by 108
Adipose tissue and reproductive health
Mathew, H., Castracane, V. D., & Mantzoros, C. S. (2017) · Metabolism · doi:10.1016/j.metabol.2017.11.006 · Cited by 109
Obesity: Pathophysiology and Clinical Management
Gurevich-Panigrahi, T., Panigrahi, S., Wiecheć, E., & Łoś, M. (2009) · Current Medicinal Chemistry · doi:10.2174/092986709787315568 · Cited by 111
Noncoding RNAs, Emerging Regulators of Skeletal Muscle Development and Diseases
Nie, M., Deng, Z., Liu, J., & Wang, D. (2015) · BioMed Research International · doi:10.1155/2015/676575 · Cited by 105
“Since miR-133 has been recently implicated in the regulation of brown adipose differentiation by directly targeting PRDM16, a master transcription factor for brown adipogenesis [53], and there are common Myf5 positive progenitor cells for brown fat and skeletal muscle during embryonic development, miR-133 likely parti…”
BackgroundSeo, Y., Kim, K., Choi, J., Koh, E., & Lee, B.-Y. (2018) · Nutrients · doi:10.3390/nu10060712 · Cited by 111
“Activation of PGC-1α induces the expression of PRDM16 and UCP1, the dominant regulator of energy expenditure [54].”
BackgroundHuman Brown Adipose Tissue and Metabolic Health: Potential for Therapeutic Avenues
Singh, R., Barrios, A., Dirakvand, G., & Pervin, S. (2021) · Cells · doi:10.3390/cells10113030 · Cited by 114
Razzoli, M., Frontini, A., Gurney, A., Mondini, E., Çubuk, C., Katz, L. S., Cero, C., Bolan, P. J., Dopazo, J., Vidal‐Puig, A., et al. (2015) · Molecular Metabolism · doi:10.1016/j.molmet.2015.10.005 · Cited by 106
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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