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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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“This suggests a developmental relationship close to myocytes (Atit et al., 2006; Seale et al., 2008).”
BackgroundBeige Adipose Tissue Identification and Marker Specificity—Overview
Pilkington, A., Paz, H. A., & Wankhade, U. D. (2021) · Frontiers in Endocrinology · doi:10.3389/fendo.2021.599134 · Cited by 163
Yamamoto, M., Legendre, N. P., Biswas, A. A., Lawton, A., Yamamoto, S., Tajbakhsh, S., Kardon, G., & Goldhamer, D. J. (2018) · Stem Cell Reports · doi:10.1016/j.stemcr.2018.01.027 · Cited by 156
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
“Interestingly, these “systemic” brown adipocytes, such as those present in white fat and muscle, are not derived from myf5-expressing precursors (27), suggesting different developmental origins for these different pools of brown fat.”
BackgroundMethodMultipotent 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
Adipose tissue and fetal programming
Symonds, M. E., Pope, M., Sharkey, D., & Budge, H. (2012) · Diabetologia · doi:10.1007/s00125-012-2505-5 · Cited by 160
Defining skeletal muscle resident progenitors and their cell fate potentials
Pannérec, A., Formicola, L., Besson, V., Marazzi, G., & Sassoon, D. A. (2013) · Development · doi:10.1242/dev.089326 · Cited by 151
“…but can also give rise to white or ‘beige’ fat in vitro (Cannon and Nedergaard, 2012; Joe et al., 2010; Kajimura et al., 2008; Schulz et al., 2011; Seale et al., 2008; Seale et al., 2007) or in vivo (Joe et al., 2010; Kajimura et al., 2008; Schulz et al., 2011; Seale et al., 2008; Seale et al.,…”
BackgroundOntogenesis of muscle and adipose tissues and their interactions in ruminants and other species
Bonnet, M., Cassar‐Malek, I., Chilliard, Y., & Picard, B. B. (2010) · animal · doi:10.1017/s1751731110000601 · Cited by 168
“It may, however, be hypothesized that proteins such as PRDM16 and Wnt regulate the commitment and early differentiation of (i) a common progenitor that gives rise to either muscle and BAT, or muscle and WAT, depending on anatomical site, or (ii) different progenitors that give rise to muscle, BAT and WAT.”
BackgroundResultInfluentialIL‐10 prevents aging‐associated inflammation and insulin resistance in skeletal muscle
Dağdeviren, S., Jung, D. Y., Friedline, R. H., Noh, H. L., Kim, J. H., Patel, P. R., Tsitsilianos, N., Inashima, K., Tran, D. A., Hu, X., et al. (2016) · The FASEB Journal · doi:10.1096/fj.201600832r · Cited by 151
Bhlhb5 and Prdm8 form a repressor complex involved in neuronal circuit assembly
Ross, S. E., McCord, A. E., Jung, C., Atan, D., Mok, S. I., Hemberg, M., Kim, T.-K., Salogiannis, J., Hu, L., Cohen, S., et al. (2012) · Neuron · doi:10.1016/j.neuron.2011.09.035 · Cited by 137
Tissue-specific designs of stem cell hierarchies
Visvader, J. E., & Clevers, H. (2016) · Nature Cell Biology · doi:10.1038/ncb3332 · Cited by 150
“Notably, although MuSCs are unipotent within skeletal muscle, they have the capacity to generate brown adipocytes during embryogenesis or when challenged with cold exposure 63–65 .”
Zou, T., Chen, D., Yang, Q., Wang, B., Zhu, M. J., Nathanielsz, P. W., & Du, . (2016) · The Journal of Physiology · doi:10.1113/jp273478 · Cited by 150
“In addition, RES also alters maternal metabolism to change the intrauterine and early postnatal nutritional environments, which in turn affects the early programming of the offspring (Sun et al. 2012).”
Background3T3-L1 adipocytes display phenotypic characteristics of multiple adipocyte lineages
Morrison, S., & McGee, S. L. (2015) · Adipocyte · doi:10.1080/21623945.2015.1040612 · Cited by 149
“Brown adipocytes are thought to originate from a myogenic cell lineage that expresses the myogenic factor 5 (Myf5) protein, while white adipocytes arise from non-myogenic (Myf5 negative) cell lineages.(7,8) More recently, a sub-population of white adipocytes has been identified with some characteristics resembling tho…”
BackgroundMacrophage infiltration into obese adipose tissues suppresses the induction of UCP1 level in mice
Sakamoto, T., Nitta, T., Maruno, K., Yeh, Y., Kuwata, H., Tomita, K., Goto, T., Takahashi, N., & Kawada, T. (2016) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00028.2015 · Cited by 153
The Circadian Clock in White and Brown Adipose Tissue: Mechanistic, Endocrine, and Clinical Aspects
Froy, O., & Garaulet, M. (2018) · Endocrine Reviews · doi:10.1210/er.2017-00193 · Cited by 155
Discovery of molecular subtypes in leiomyosarcoma through integrative molecular profiling
Beck, A. H., Lee, C.-H., Witten, D., Gleason, B., Edris, B., Espinosa, Í., Zhu, S., Li, R., Montgomery, K. D., Marinelli, R. J., et al. (2009) · Oncogene · doi:10.1038/onc.2009.381 · Cited by 150
“Loss of PRDM16 from brown fat precursors promotes skeletal muscle differentiation and leads to elevated expression of muscle specific genes (Seale et al., 2008).”
BackgroundLombardi, R., Dong, J., Rodrı́guez, G., Bell, A., Leung, T. K., Schwartz, R. J., Willerson, J. T., Brugada, R., & Marian, A. J. (2009) · Circulation Research · doi:10.1161/circresaha.109.196899 · Cited by 150
Villanueva, C. J., Vergnes, L., Wang, J., Drew, B. G., Hong, C., Tu, Y., Hu, Y., Xu, P., Xu, F., Sáez, E., et al. (2013) · Cell Metabolism · doi:10.1016/j.cmet.2013.01.016 · Cited by 152
“Prdm16 binds directly to PPARg, and studies have established that the ability of Prdm16 to interact with PPARg and C/EBPb is critical for its ability to drive BAT development (Kajimura et al., 2009; Seale et al., 2008).”
BackgroundInfluentialPrdm16 is required for normal palatogenesis in mice
Bjork, B. C., Turbé-Doan, A., Prysak, M., Herron, B. J., & Beier, D. R. (2009) · Human Molecular Genetics · doi:10.1093/hmg/ddp543 · Cited by 141
Self-citationHarms, M., Lim, H., Ho, Y., Shapira, S. N., Ishibashi, J., Rajakumari, S., Steger, D. J., Lazar, M. A., Won, K., & Seale, P. (2015) · Genes & Development · doi:10.1101/gad.252734.114 · Cited by 143
“PRDM16 binding is enriched at BAT-selective genes PRDM16 induces the expression of brown fat-selective genes (Seale et al. 2007, 2008), but whether PRDM16 acts directly at these genes was unknown.”
InfluentialSelf-citationCold-activated brown adipose tissue in human adults: methodological issues
van der Lans, A. A. J. J., Wierts, R., Vosselman, M. J., Schrauwen, P., Brans, B. T., & Lichtenbelt, W. D. V. M. (2014) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00021.2014 · Cited by 155
“(42) showed in 2008 that “classical” BAT cells derive from a myf5 , a muscle-like lineage, whereas “inducible” cells derive from a myf5-cell lineage, a fat-like lineage (42).”
BackgroundMuscle lipogenesis balances insulin sensitivity and strength through calcium signaling
Funai, K., Song, H., Li, Y., Lodhi, I. J., Wei, X., Yoshino, J., Coleman, T., & Semenkovich, C. F. (2013) · Journal of Clinical Investigation · doi:10.1172/jci65726 · Cited by 142
miR-133a Regulates Adipocyte Browning In Vivo
Liu, W., Bi, P., Shan, T., Yang, X., Yin, H., Wang, Y.-X., Liu, N., Rudnicki, M. A., & Kuang, S. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003626 · Cited by 147
Self-citationTranscriptional Regulatory Circuits Controlling Brown Fat Development and Activation
Seale, P. (2015) · Diabetes · doi:10.2337/db15-0203 · Cited by 145
Self-citationIncreased cGMP promotes healthy expansion and browning of white adipose tissue
Mitschke, M. M., Hoffmann, L. S., Gnad, T., Scholz, D., Katja, K., Mayer, P., Haas, B., Sassmann, A., Pfeifer, A., & Kilić, A. (2013) · The FASEB Journal · doi:10.1096/fj.12-221580 · Cited by 148
PVAT and Its Relation to Brown, Beige, and White Adipose Tissue in Development and Function
Hildebrand, S., Stümer, J., & Pfeifer, A. (2018) · Frontiers in Physiology · doi:10.3389/fphys.2018.00070 · Cited by 143
“An earlier study identified PRDM16 as a key determinant of brown adipocyte commitment during development (Seale et al., 2008), but more recent investigations suggest that PRDM16 primarily maintains the BAT phenotype postnatally (Harms et al., 2014).”
Background
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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