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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]
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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BackgroundInfluentialSignaling Pathways Regulating Thermogenesis
Nakamura-Tabuchi, C., & Sul, H. S. (2021) · Frontiers in Endocrinology · doi:10.3389/fendo.2021.595020 · Cited by 95
Wu, T., Liang, Z., Zhang, Z., Liu, C., Zhang, L., Gu, Y., Peterson, K. L., Evans, S. M., Fu, X., & Chen, J. (2021) · Circulation · doi:10.1161/circulationaha.121.056666 · Cited by 89
Drummond, C. J., Hanna, J. A., Garcia, M. R., Devine, D. J., Heyrana, A. J., Finkelstein, D., Rehg, J. E., & Hatley, M. E. (2018) · Cancer Cell · doi:10.1016/j.ccell.2017.12.001 · Cited by 91
“Given that BAT and skeletal muscle share a common progenitor (Seale et al., 2008), and that adipocytes express aP2, we asked whether adipocytes are the origin of tumors in aP2-Cre;Smo (AS) mice.”
BackgroundInducible Brown Adipogenesis of Supraclavicular Fat in Adult Humans
Lee, P., Swarbrick, M. M., Zhao, J., & Ho, K. K. Y. (2011) · Endocrinology · doi:10.1210/en.2011-1349 · Cited by 89
Perilipin Overexpression in White Adipose Tissue Induces a Brown Fat-Like Phenotype
Sawada, T., Miyoshi, H., Shimada, K., Suzuki, A. K., Okamatsu‐Ogura, Y., Perfield, J. W., Kondo, T., Nagai, S., Shimizu, C., Yoshioka, N., et al. (2010) · PLoS ONE · doi:10.1371/journal.pone.0014006 · Cited by 88
The tumor secretory factor ZAG promotes white adipose tissue browning and energy wasting
Elattar, S., Dimri, M., & Ande, S. (2018) · The FASEB Journal · doi:10.1096/fj.201701465rr · Cited by 89
Interplay of cell–cell contacts and RhoA/MRTF‐A signaling regulates cardiomyocyte identity
Dorn, T., Kornherr, J., Parrotta, E. I., Zawada, D. M., Ayetey, H., Santamaria, G., Iop, L., Mastantuono, E., Sinnecker, D., Goedel, A., et al. (2018) · The EMBO Journal · doi:10.15252/embj.201798133 · Cited by 90
“…before initiation of pacing and culture in lipogenic milieu) already expressed higher levels of key genes directing preadipocyte differentiation, such as PPAR c , C/EBP a (Farmer, 2006), and PRDM16 , a transcriptional regulator of PPAR c that specifies the brown fat lineage (Seale et al , 2008).”
Nicklas, S., Otto, A., Wu, X., Miller, P., Stelzer, S., Wen, Y., Kuang, S., Wrogemann, K., Patel, K., Ding, H., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0030445 · Cited by 88
“), far beyond the time when wild type regeneration has been completed (approximately 10 days) suggesting that these cells have failed to differentiate even by this late stage. Finally, we noted the presence of regions containing adipocyte-like cells within the skeletal muscle tissue at 16 days post injury in the absen…”
Self-citationNovel Browning Agents, Mechanisms, and Therapeutic Potentials of Brown Adipose Tissue
Wankhade, U. D., Shen, M., Yadav, H., & Thakali, K. M. (2016) · BioMed Research International · doi:10.1155/2016/2365609 · Cited by 91
Nrf2 deficiency promotes apoptosis and impairs PAX7/MyoD expression in aging skeletal muscle cells
Narasimhan, M., Hong, J., Atieno, N., Muthusamy, V. R., Davidson, C. J., Abu-Rmaileh, N., Richardson, R. S., Gomes, A. V., Hoidal, J. R., & Rajasekaran, N. S. (2014) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2014.02.023 · Cited by 88
Paradoxical Roles of Perivascular Adipose Tissue in Atherosclerosis and Hypertension
Chang, L., Milton, H., Eitzman, D. T., & Chen, Y. E. (2012) · Circulation Journal · doi:10.1253/circj.cj-12-1393 · Cited by 86
Satellite-like cells contribute to pax7-dependent skeletal muscle repair in adult zebrafish
Berberoglu, M. A., Gallagher, T. L., Morrow, Z. T., Talbot, J. C., Hromowyk, K. J., Tenente, I. M., Langenau, D. M., & Amacher, S. L. (2017) · Developmental Biology · doi:10.1016/j.ydbio.2017.03.004 · Cited by 85
Adaptive facultative diet-induced thermogenesis in wild-type but not in UCP1-ablated mice
von Essen, G., Lindsund, E., Cannon, B., & Nedergaard, J. (2017) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00097.2017 · Cited by 90
Non-canonical mTORC2 Signaling Regulates Brown Adipocyte Lipid Catabolism through SIRT6-FoxO1
Jung, S. M., Hung, C., Hildebrand, S. R., Sánchez-Gurmaches, J., Martínez-Pastor, B., Gengatharan, J. M., Wallace, M., Mukhopadhyay, D., Calejman, C. M., Luciano, A. K., et al. (2019) · Molecular Cell · doi:10.1016/j.molcel.2019.07.023 · Cited by 88
Carré, N., & Binart, N. (2013) · Biochimie · doi:10.1016/j.biochi.2013.09.023 · Cited by 88
Mitochondria and endocrine function of adipose tissue
Medina‐Gómez, G. (2012) · Best Practice & Research Clinical Endocrinology & Metabolism · doi:10.1016/j.beem.2012.06.002 · Cited by 92
Shore, A., Karamitri, A., Kemp, P. R., Speakman, J. R., & Lomax, M. A. (2010) · Diabetologia · doi:10.1007/s00125-010-1701-4 · Cited by 86
“Lineage tracing studies have recently discovered that BAT shares a common cell progenitor with muscle and not WAT depot cells, as previously thought [ 38 ].”
ResultMetabolic regulation and the anti-obesity perspectives of human brown fat
Schéele, C., & Nielsen, S. J. (2017) · Redox Biology · doi:10.1016/j.redox.2017.04.011 · Cited by 92
Shimada, I. S., Acar, M., Burgess, R. J., Zhao, Z., & Morrison, S. J. (2017) · Genes & Development · doi:10.1101/gad.291773.116 · Cited by 88
“Prdm16 promotes stem cell maintenance in the fetal hematopoietic and nervous systems (Chuikov et al. 2010; Aguilo et al. 2011; Luchsinger et al. 2016) as well as brown fat cell differentiation from skeletal muscle precursors (Seale et al. 2008; Cohen et al. 2014).”
BackgroundBrown Adipose Tissue in Human Infants
Lidell, M. E. (2018) · Handbook of experimental pharmacology · doi:10.1007/164_2018_118 · Cited by 85
Adipose and skeletal muscle thermogenesis: studies from large animals
Fuller‐Jackson, J., & Henry, B. A. (2018) · Journal of Endocrinology · doi:10.1530/joe-18-0090 · Cited by 89
Assembling the adipose organ: adipocyte lineage segregation and adipogenesis in vivo
Sebo, Z. L., & Rodeheffer, M. S. (2019) · Development · doi:10.1242/dev.172098 · Cited by 95
“For brown adipogenesis, the core program is adjoined by unique transcriptional co-regulators, including PRDM16 and Ebf2, that physically interact with PPARγ to direct brown adipocyte-specific target gene expression (Rajakumari et al., 2013; Seale et al., 2008).”
BackgroundInfluentialWang, J., Li, D., Wang, P., Hu, X., & Chen, F. (2019) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2019.05.001 · Cited by 86
Zou, Y., Ju, X., Chen, W., Yuan, J., Wang, Z., Aluko, R. E., & He, R. (2020) · Food & Function · doi:10.1039/c9fo01524h · Cited by 84
Brown adipose tissue in humans
Enerbäck, S. (2010) · International Journal of Obesity · doi:10.1038/ijo.2010.183 · Cited by 94
Emerging roles of zinc finger proteins in regulating adipogenesis
Wei, S., Zhang, L., Zhou, X., Du, ., Jiang, Z., Hausman, G., Bergen, W. G., Zan, L., & Dodson, M. V. (2013) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-013-1395-0 · Cited by 87
“At this juncture, it needs to be mentioned that functional CACCC binding sites (one of the KLFs binding domains) were found in the control region of key adipogenic factors, such as C/eBPα and PPARγ [82], providing the structural basis for the adipogenic regulations of KLFs. Multiple KLFs are induced sequentially durin…”
BackgroundInfluentialMicroRNAs as pharmacological targets in diabetes
Mao, Y., Mohan, R., Zhang, S., & Tang, X. (2013) · Pharmacological Research · doi:10.1016/j.phrs.2013.06.005 · Cited by 87
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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