PreprintCited by 828Adipose Tissue and MetabolismAdipokines, Inflammation, and Metabolic DiseasesPeroxisome Proliferator-Activated Receptors

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Adaptive thermogenesis in adipocytes: Is beige the new brown?

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Wu, Jun, Cohen, Paul, Spiegelman, Bruce M.·2013·Genes & Development

DOI 10.1101/gad.211649.112PMC PMC3576510

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Abstract

One of the most promising areas in the therapeutics for metabolic diseases centers around activation of the pathways of energy expenditure. Brown adipose tissue is a particularly appealing target for increasing energy expenditure, given its amazing capacity to transform chemical energy into heat. In addition to classical brown adipose tissue, the last few years have seen great advances in our understanding of inducible thermogenic adipose tissue, also referred to as beige fat. A deeper understanding of the molecular processes involved in the development and function of these cell types may lead to new therapeutics for obesity, diabetes, and other metabolic diseases.

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Background
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Iyer, M. S., Paszkiewicz, R. L., Bergman, R. N., Richey, J. M., Woolcott, O. O., Bediako, I. A., Wu, Q., Kim, S. P., Stefanovski, D., Kolka, C. M., et al. (2019) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00539.2018 · Cited by 12
Brown adipose tissue estimated with the magnetic resonance imaging fat fraction is associated with glucose metabolism in adolescents
Lundström, E., Ljungberg, J., Andersson, J., Manell, H., Strand, R., Forslund, A. H., Bergsten, P., Weghuber, D., Mörwald, K., Zsoldos, F., et al. (2019) · Pediatric Obesity · doi:10.1111/ijpo.12531 · Cited by 12
“Potential therapies aiming at increasing the amount and/or thermogenic capacity of the two types of brown adipocytes have been discussed.(3,10) Despite the therapeutic potential, the knowledge of possible associations between BAT and glucose metabolism in humans is still relatively limited.”
Background
Stimulation of brown adipose tissue by polyphenols in extra virgin olive oil
Melguizo‐Rodríguez, L., Montes, R. I., Costela-Ruiz, V. J., & García‐Martínez, O. (2020) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2020.1799930 · Cited by 12
“This process has been designated adipose tissue browning (Wu, Cohen, and Spiegelman 2013; Montanari, Po s ci c, and Colitti 2017).”
Background
Quercetin May Improve Fat Graft Survival by Promoting Fat Browning Peripherally
Yu, P., Yang, Z., Lu, H., Jin, X., Yang, X., & Qi, Z. (2022) · Aesthetic Plastic Surgery · doi:10.1007/s00266-022-02857-z · Cited by 12
“The browning of fat depends on the enhancement of its mitochondrial function, and UCP1mediated mitochondrial thermogenesis is a hallmark of brown and beige adipocytes [19].”
Background
The Bone and Fat Connection in Inflammatory Bowel Diseases
Terzoudis, S., Zavos, C., & Κoutroubakis, I. E. (2014) · Inflammatory Bowel Diseases · doi:10.1097/mib.0000000000000111 · Cited by 13
“Brown adipocytes were thought to be the main site of thermogenesis in mammals, acting in response to increased lipid rich caloric intake in a process named adaptive thermogenesis, the main cause for energy dissipation.(15) However, white adipose tissue (WAT) was long considered merely to store energy and to protect th…”
Background
Recapitulation of anti-aging phenotypes by global, but not by muscle-specific, deletion of PAPP-A in mice
Li, X., Hager, M., McPherson, M., Lee, M., Hagalwadi, R., Skinner, M. E., Lombard, D. B., & Miller, R. A. (2022) · GeroScience · doi:10.1007/s11357-022-00692-3 · Cited by 11
“Brown and beige cells differ in many ways and are considered distinct cell types [19, 20].”
Background
Ubiquitin ligase RNF20 coordinates sequential adipose thermogenesis with brown and beige fat-specific substrates
Jeon, Y. G., Nahmgoong, H., Oh, J., Lee, D., Kim, D. W., Kim, Y. Y., Kim, Y. Y., Ji, Y., Han, J. S., Kim, S. M., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-45270-7 · Cited by 11
“1a – d), implying that RNF20 might not have a profound effect on brown adipogenesis, which appears to be different from white adipogenesis 14,33 .”
Molecular cloning, expression pattern analysis of porcine Rb1 gene and its regulatory roles during primary dedifferentiated fat cells adipogenic differentiation
Hu, X., Luo, P., Peng, X., Song, T., Zhou, Y., Wei, H., Peng, J., & Jiang, S. (2015) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2015.01.016 · Cited by 11
“Both brown and beige adipocytes are specialized in energy dissipation as heat during cold- and diet-induced thermogenesis (Gesta et al., 2007; Wu et al., 2012, 2013).”
Background
Polysaccharides from Enteromorpha prolifera improves insulin sensitivity and promotes adipose thermogenesis in diet-induced obese mice associated with activation of PGC-1α-FNDC5/irisin pathway
Xie, F., Zou, T., Chen, J., Liang, P., Wang, Z., & You, J. (2022) · Journal of Functional Foods · doi:10.1016/j.jff.2022.104994 · Cited by 11
Sodium salicylate induces browning of white adipocytes via M2 macrophage polarization by HO-1 upregulation
Choi, H., Jeon, E. J., Kim, D. Y., Choi, M. J., Yu, H., Kim, J. I., & Cheon, H. G. (2022) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2022.175085 · Cited by 11
Oncogenic role of an uncharacterized cold‐induced zinc finger protein 726 in breast cancer
Bandyopadhayaya, S., Yadav, P., Sharma, A., Dey, S. K., Nag, A., Maheshwari, R., Ford, B. M., & Mandal, C. C. (2023) · Journal of Cellular Biochemistry · doi:10.1002/jcb.30417 · Cited by 11
Functional modification of adipocytes by grape seed extract impairs their pro-tumorigenic signaling on colon cancer stem cells and the daughter cancer cells
Kumar, S., Kumar, D., Raina, K., Agarwal, R., & Agarwal, C. (2014) · Oncotarget · doi:10.18632/oncotarget.2467 · Cited by 11
Lecithin:Cholesterol Acyltransferase (LCAT) Deficiency Promotes Differentiation of Satellite Cells to Brown Adipocytes in a Cholesterol-dependent Manner
Nesan, D., Tavallaee, G., Koh, D., Bashiri, A., Abdin, R., & Ng, D. S. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.m115.676056 · Cited by 11
“The expression of PRDM16, a transcription factor originally identified as a bidirectional switch involved in cell fate determination of myf5 myoblasts (1), has recently been found to be sufficient to induce both (i) classical BAT differentiation and (ii) beiging of the white fat (2, 3) from their respective preadipocy…”
Background
Integrative analyses of translatome and transcriptome reveal important translational controls in brown and white adipose regulated by microRNAs
Reid, D. W., Xu, D., Chen, P., Yang, H., & Sun, L. (2017) · Scientific Reports · doi:10.1038/s41598-017-06077-3 · Cited by 11
Response gene to complement 32 suppresses adipose tissue thermogenic genes through inhibiting ß3‐adrenergic receptor/mTORC1 signaling
Chen, S., Mei, X., Yin, A., Yin, H., Cui, X., & Chen, S. (2018) · The FASEB Journal · doi:10.1096/fj.201701508r · Cited by 11
A Novel N‑Substituted Valine Derivative with Unique Peroxisome Proliferator-Activated Receptor γ Binding Properties and Biological Activities
Peiretti, F., Montanari, R., Capelli, D., Bonardo, B., Colson, C., Amri, E., Grimaldi, M., Balaguer, P., Ito, K., Roeder, R. G., et al. (2020) · Journal of Medicinal Chemistry · doi:10.1021/acs.jmedchem.0c01555 · Cited by 11
Effects of Vitamin A Status on Expression of Ucp1 and Brown/Beige Adipocyte-Related Genes in White Adipose Tissues of Beef Cattle
Kanamori, Y., Yamada, T., Asano, H., Kida, R., Qiao, Y., Eldaim, M. A. A., Tomonaga, S., Matsui, T., & Funaba, M. (2014) · Journal of Veterinary Medical Science · doi:10.1292/jvms.14-0137 · Cited by 11
“Beige adipocytes, also known as brite adipocytes, were originally called Ucp1-positive adipocytes and have been detected in murine white fat depots [25]; however, the molecular signatures of beige adipocytes were shown to differ from those of brown adipocytes in classical brown fat depots located at the interscapular…”
Background
Liver X receptor β: new player in the regulatory network of thyroid hormone and ‘browning’ of white fat
Miao, Y., Warner, M. N., & Gustafsson, J.-Α. (2016) · Adipocyte · doi:10.1080/21623945.2016.1142634 · Cited by 11
“These cells, called beige or brite fat cells, undergo a browning process upon cold exposure and share some molecular, histologic and functional characteristics with beige adipocytes found in the subcutaneous white adipose tissue (SAT) of mice.(10,11) This finding has raised a strong clinical interest in the possibilit…”
Background
New players of the adipose secretome: Therapeutic opportunities and challenges
Voilquin, L., Danneskiold‐Samsøe, N. B., Zhao, M., Allen, H., & Svensson, K. J. (2022) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2022.102302 · Cited by 10
Optogenetic activation of UCP1-dependent thermogenesis in brown adipocytes
Doucette, C. C., Nguyen, D. C., Barteselli, D., Blanchard, S., Pelletier, M., Kesharwani, D., Jachimowicz, E., Su, S., Karolak, M. J., & Brown, A. C. (2023) · iScience · doi:10.1016/j.isci.2023.106560 · Cited by 10
White-brown adipose tissue interplay in polycystic ovary syndrome: Therapeutic avenues
Abbasi, K., Zarezadeh, R., Valizadeh, A., Mehdizadeh, A., Hamishehkar, H., Nouri, M., & Darabi, M. (2023) · Biochemical Pharmacology · doi:10.1016/j.bcp.2023.116012 · Cited by 12
Guanidinoacetic acid ameliorates hepatic steatosis and inflammation and promotes white adipose tissue browning in middle-aged mice with high-fat-diet-induced obesity
Su, Y., Li, X., Jiamin, Z., Ji, B., Zhao, X., Feng, J., & Zhao, J. (2024) · Food & Function · doi:10.1039/d3fo05201j · Cited by 10
Effects of hypothyroidism on the mesenteric and omental adipose tissue in rats.
López-Fontana, C., Pennacchio, G., Zyla, L., Toneatto, J., Bruna, F., Ortiz, N., Sassi, P., Santiano, F. E., García, S., Sasso, C. V., et al. (2019) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2019.04.011 · Cited by 7
Dihydropyranocoumarins Exerted Anti-Obesity Activity In Vivo and its Activity Was Enhanced by Nanoparticulation with Polylactic-Co-Glycolic Acid
Hossin, A. Y., Inafuku, M., & Oku, H. (2019) · Nutrients · doi:10.3390/nu11123053 · Cited by 11
“…are needed to elucidate the underlying details of the mechanisms by which these activities have an e ﬀ ect on obesity, our study suggests the great potential for PLGA nanoparticle encapsulation to be carriers of the oral delivery of DPCs in the development of natural and safe anti-obesity agents.”
Brown adipose tissue and its therapeutic application
Yuan, X., Dong, M., Lee, H. J., & Jin, W. (2016) · 中国科学通报：英文版 · doi:10.1007/s11434-016-1051-9 · Cited by 11
“The browning of WAT also improves thermogenic function by burning glucose and fat to produce heat, resulting in a reduction of adipocity [17, 18].”
Background
Wnt3a regulates mitochondrial biogenesis through p38/CREB pathway
Ning, X., He, J., Shi, X., Yu, T., & Yang, G. (2016) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2016.05.004 · Cited by 10
High dose of linagliptin induces thermogenic beige adipocytes in the subcutaneous white adipose tissue in diet-induced obese C57BL/6 mice
Correia, B. R. D. O., Rachid, T. L., Glauser, J. S. D. O., Martins, F. F., Mandarim‐de‐Lacerda, C. A., & Souza‐Mello, V. (2019) · Endocrine · doi:10.1007/s12020-019-01969-y · Cited by 10
New Insights into Bioactive Compounds of Traditional Chinese Medicines for Insulin Resistance Based on Signaling Pathways
He, J., Wang, H., & Vijg, J. (2019) · Chemistry & Biodiversity · doi:10.1002/cbdv.201900176 · Cited by 10
“[78] Recent studies demonstrated that accelerating the white fat convert to brown fat could counteract the lipotoxicity-induced insulin resistance effectively.[79] Energy metabolism regulation, as a new and promising solution towards the treatment of metabolic diseases, has become a hot spot in research.”
Background
Macrophages and brown adipocytes cross-communicate to modulate a thermogenic program following methamphetamine exposure
Sánchez-Alavez, M., Bortell, N., Basova, L. V., Samad, F., & Marcondes, M. C. G. (2020) · International Journal of Hyperthermia · doi:10.1080/02656736.2020.1849822 · Cited by 10
Dysfunction of insulin-AKT-UCP1 signalling inhibits transdifferentiation of human and mouse white preadipocytes into brown-like adipocytes
Pan, J., Kothan, S., Moe, A. T. M., & Huang, K. (2022) · Adipocyte · doi:10.1080/21623945.2022.2062852 · Cited by 10
Bioactive Compounds and Adipocyte Browning Phenomenon
Manríquez-Núñez, J., & Ramos‐Gómez, M. (2022) · Current Issues in Molecular Biology · doi:10.3390/cimb44070210 · Cited by 11
“Recent studies have reported that increased fat utilization through thermogenic activity promotes browning in WAT and attenuates obesity-induced inflammation and insulin resistance by the modulation of tissue-resident macrophages [26].”
Background
Patch-Clamp Analysis of the Mitochondrial H+ Leak in Brown and Beige Fat
Bertholet, A. M., & Kirichok, Y. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2020.00326 · Cited by 11
Pycnogenol® Induces Browning of White Adipose Tissue through the PKA Signaling Pathway in Apolipoprotein E-Deficient Mice
Cong, H., Zhong, W., Wang, Y., Ikuyama, S., Fan, B., & Gu, J. (2018) · Journal of Diabetes Research · doi:10.1155/2018/9713259 · Cited by 9
“Thus, brown fat and beige fat are potential therapeutic targets for obesity [4, 7].”
Background
Ablation of Sam68 in adult mice increases thermogenesis and energy expenditure
Qiao, A., Ma, W., Deng, J., Zhou, J., Han, C., Zhang, E., Boriboun, C., Xu, S., Zhang, C., Jie, C., et al. (2021) · The FASEB Journal · doi:10.1096/fj.202100021r · Cited by 8
Relationships between the Planetary Health Diet Index, its food groups, and polygenic risk of obesity in the CARTaGENE cohort
Masip, G., & Nielsen, D. E. (2024) · Nutrition & Metabolism · doi:10.1186/s12986-024-00890-0 · Cited by 10
“Some of the genes involved in these expression pathways are the PPARG gene, which is involved in the adaptive thermogenesis pathway [50], the MC4R and the FTO genes, which are involved in the appetite pathway [51] and the energy regulation pathway along with the LEP gene [52].”
Is There a Need to “Modernize” and “Simplify” the Diagnostic Criteria of Protein-Energy Wasting?
Koppe, L., & MAK, R. H. K. (2023) · Seminars in Nephrology · doi:10.1016/j.semnephrol.2023.151403 · Cited by 10
What does indirect calorimetry really tell us?
Kaiyala, K. J. (2014) · Molecular Metabolism · doi:10.1016/j.molmet.2014.03.005 · Cited by 9
Nutraceutical Food: Composition, Biosynthesis, Therapeutic Properties, and Applications
do Prado, D. Z., Capoville, B. L., Delgado, C. H. O., Athanázio-Heliodoro, J. C., Pivetta, M. R., Pereira, M. S., Zanutto-Elgui, M. R., Novelli, P. K., Francisco, V. C. B., & Fleuri, L. F. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-811446-9.00004-6 · Cited by 9
Long Non-Coding RNAs in Brown Adipose Tissue
Lai, S., Du, K., Shi, Y., Cao, L., Wang, G., Hu, S., Jia, X., Wang, J., & Chen, S. (2020) · Diabetes Metabolic Syndrome and Obesity · doi:10.2147/dmso.s264830 · Cited by 9
Gochujang elicits anti-obesity effects by increasing capsaicin-independent brown adipogenesis and thermogenesis in high-fat diet induced obese mice
Lee, H., Song, J., Chung, S., Cha, Y., & Han, A. (2023) · Journal of Functional Foods · doi:10.1016/j.jff.2023.105886 · Cited by 9
Thermogenesis in Adipose Tissue: Adrenergic and Non-Adrenergic Pathways
Hossain, M. A., Poojari, A., & Rabiee, A. (2026) · Cells · doi:10.3390/cells15020131 · Cited by 8
“Conversely, deletion or pharmacological antagonism of REV-ERB α (using SR9009 or SR9011) markedly increases UCP1 levels, mitochondrial density, BAT recruitment, and 24 h EE while protecting against diet-induced obesity and glucose intolerance [233–235].”
Navigating Lipodystrophy: Insights from Laminopathies and Beyond
Krüger, P., Hartinger, R., & Djabali, K. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25158020 · Cited by 10
“This transformation is protective against obesity, making beige adipose tissue a promising therapeutic target for obesity and its related complications [20,44].”
Background

Authors: Wu, J., Cohen, P., & Spiegelman, B. M.
Affiliations: Harvard University (US)
Brigham and Women's Hospital (US)
ORCID: Wu, Jun
Cohen, Paul
Spiegelman, Bruce M.
Venue: Genes & Development
Publisher: Cold Spring Harbor Laboratory
Published: 2013-02-01
Volume: 27
Issue: 3
Pages: 234-250
ISSN: 0890-9369 (ISSN-L)
1549-5477
DOI: 10.1101/gad.211649.112
PMC: PMC3576510
OpenAlex: W2170874580
Cited by: 828
References: 204
Citations by year: 2026: 22 · 2025: 29 · 2024: 34 · 2023: 37 · 2022: 46 · 2021: 64 · 2020: 64 · 2019: 72 · 2018: 56 · 2017: 91 · 2016: 73 · 2015: 98 · 2014: 91 · 2013: 46
Type: posted content
Language: en
Open access: bronze
doi.org
Locations: Genes & Development (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion, cc-by)
Funders: Foundation for the National Institutes of Health
American Heart Association
JPB Foundation
National Institutes of Health (DK31405)
National Institute of Diabetes and Digestive and Kidney Diseases (R01DK031405, DK-31405, K01DK094824, RC4DK090861, DK90861, R37DK031405)
Topics: Health Sciences › Medicine › Physiology (medical) › Adipose Tissue and Metabolism
Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Adipokines, Inflammation, and Metabolic Diseases
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Peroxisome Proliferator-Activated Receptors
Keywords: beige adipocytes, brown adipose tissue, thermogenesis, energy expenditure, adaptive thermogenesis, obesity, diabetes mellitus, metabolic disorders, adipogenesis
MeSH terms: Uncoupling Protein 1, Adaptation, Physiological, Animals, Adipose Tissue, Brown, Humans, Ion Channels, Obesity, Adipocytes, Gene Expression Regulation, Developmental, Thermogenesis, Mitochondrial Proteins

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Adaptive thermogenesis in adipocytes: Is beige the new brown?

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