Brown and beige fat: Molecular parts of a thermogenic machine
Open accessAbstract
The epidemic of obesity and type 2 diabetes has increased interest in pathways that affect energy balance in mammalian systems. Brown fat, in all of its dimensions, can increase energy expenditure through the dissipation of chemical energy in the form of heat, using mitochondrial uncoupling and perhaps other pathways. We discuss here some of the thermodynamic and cellular aspects of recent progress in brown fat research. This includes studies of developmental lineages of UCP1(+) adipocytes, including the discovery of beige fat cells, a new thermogenic cell type. We also discuss the physiology and transcriptional control of brown and beige cells in rodents and the state of current knowledge about human brown fat.
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Increased total energy expenditure after exercise could result from a reestablished hypothalamic setpoint controlling energy expenditure, increased excess nutrient disposal, and thermogenesis by brown adipose tissue.
“Increased total energy expenditure could result from a reestablished hypothalamic setpoint in control of energy expenditure, increased excess nutrient disposal, and thermogenesis by BAT [34].”
From The Role of Exercise in the Interplay between Myokines, Hepatokines, Osteokines, Adipokines, and Modulation of Inflammation for Energy Substrate Redistribution and Fat Mass Loss: A Review (2020) · cites this paper as [34]
The Thermodynamics section says brown fat generates heat from fuel oxidation, and Therapeutic Potential discusses glucose and lipid disposal. The paper does not connect increased energy expenditure after exercise to these processes or discuss a reestablished hypothalamic setpoint; it also treats nutrient disposal as a possible benefit of brown fat rather than a separate cause of increased energy expenditure. (LLM, conf=0.86)
Experimental — accuracy not yet measuredThe greatest benefits of BAT have been suggested to result from redistribution of nutrient disposal rather than from thermogenesis per se.
“the greatest benefits of BAT have been suggested to result from the redistribution of nutrient disposal rather than from thermogenesis per se [34].”
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Cites
Identification and Importance of Brown Adipose Tissue in Adult Humans
Cypess, A. M., Lehman, S., Williams, G., Tal, I., Rodman, D., Goldfine, A. B., Kuo, F. C., Palmer, E. L., Tseng, Y.-H., Doria, A., et al. (2009) · New England Journal of Medicine · doi:10.1056/nejmoa0810780 · Cited by 4,399 · see citing works
A Cold-Inducible Coactivator of Nuclear Receptors Linked to Adaptive Thermogenesis
Puigserver, P., Wu, Z., Park, C. W., Graves, R., Wright, M., & Spiegelman, B. M. (1998) · Cell · doi:10.1016/s0092-8674(00)81410-5 · Cited by 3,864 · see citing works
Stimulation of adipogenesis in fibroblasts by PPARγ2, a lipid-activated transcription factor
Tontonoz, P., Hu, E., & Spiegelman, B. M. (1994) · Cell · doi:10.1016/0092-8674(94)90006-x · Cited by 3,533 · see citing works
Cold-Activated Brown Adipose Tissue in Healthy Men
van Marken Lichtenbelt, W. D., Vanhommerig, J. W., Smulders, N. M., Drossaerts, J. M. A. F. L., Kemerink, G. J., Bouvy, N. D., Schrauwen, P., & Teule, G. J. J. (2009) · New England Journal of Medicine · doi:10.1056/nejmoa0808718 · Cited by 3,452 · see citing works
Beige Adipocytes Are a Distinct Type of Thermogenic Fat Cell in Mouse and Human
Wu, J., Boström, P., Sparks, L. M., Li, Y., Choi, J. H., Giang, A.-H., Khandekar, M. J., Virtanen, K. A., Nuutila, P., Schaart, G., et al. (2012) · Cell · doi:10.1016/j.cell.2012.05.016 · Cited by 3,299 · see citing works
Functional Brown Adipose Tissue in Healthy Adults
Virtanen, K. A., Lidell, M. E., Orava, J., Heglind, M., Westergren, R., Niemi, T., Taittonen, M., Laine, J., Savisto, N.-J., Enerbäck, S., et al. (2009) · New England Journal of Medicine · doi:10.1056/nejmoa0808949 · Cited by 3,058 · see citing works
PRDM16 controls a brown fat/skeletal muscle switch
Seale, P., Bjork, B., Yang, W., Kajimura, S., Chin, S., Kuang, S., Scimè, A., Devarakonda, S., Conroe, H. M., Erdjument-Bromage, H., et al. (2008) · Nature · doi:10.1038/nature07182 · Cited by 2,347 · cited 2× · see citing works
“Conversely, the UCP1 cells induced in subcutaneous white fat depots by cold or b-adrenergic agonists come from a myf5(2) lineage (10).”
BackgroundBrown adipose tissue activity controls triglyceride clearance
Bartelt, A., Bruns, O. T., Reimer, R., Hohenberg, H., Ittrich, H., Peldschus, K., Kaul, M. G., Tromsdorf, U. I., Weller, H., Waurisch, C., et al. (2011) · Nature Medicine · doi:10.1038/nm.2297 · Cited by 1,608 · see citing works
Mice lacking mitochondrial uncoupling protein are cold-sensitive but not obese
Enerbäck, S., Jacobsson, A., Simpson, E. M., Guerra, C., Yamashita, H., Harper, M.-E., & Kozak, L. P. (1997) · Nature · doi:10.1038/387090a0 · Cited by 1,379 · see citing works
Feldmann, H. M., Golozoubova, V., Cannon, B., & Nedergaard, J. (2009) · Cell Metabolism · doi:10.1016/j.cmet.2008.12.014 · Cited by 1,318 · see citing works
Prdm16 determines the thermogenic program of subcutaneous white adipose tissue in mice
Seale, P., Conroe, H. M., Estall, J. L., Kajimura, S., Frontini, A., Ishibashi, J., Cohen, P., Cinti, S., & Spiegelman, B. M. (2010) · Journal of Clinical Investigation · doi:10.1172/jci44271 · Cited by 1,241 · see citing works
Transcriptional Control of Brown Fat Determination by PRDM16
Seale, P., Kajimura, S., Yang, W., Chin, S., Rohas, L. M., Uldry, M., Tavernier, G., Langin, D., & Spiegelman, B. M. (2007) · Cell Metabolism · doi:10.1016/j.cmet.2007.06.001 · Cited by 1,174 · see citing works
Development of obesity in transgenic mice after genetic ablation of brown adipose tissue
Lowell, B. B., S-Susulic, V., Hamann, A., Lawitts, J. A., Himms-Hagen, J., Boyer, B. B., Kozak, L. P., & Flier, J. S. (1993) · Nature · doi:10.1038/366740a0 · Cited by 1,075 · see citing works
Activation of Human Brown Adipose Tissue by a β3-Adrenergic Receptor Agonist
Cypess, A. M., Weiner, L. S., Roberts‐Toler, C., Franquet, E., Kessler, S., Kahn, P. A., English, J., Chatman, K., Trauger, S. A., Doria, A., et al. (2015) · Cell Metabolism · doi:10.1016/j.cmet.2014.12.009 · Cited by 1,030 · see citing works
Recruited brown adipose tissue as an antiobesity agent in humans
Yoneshiro, T., Aita, S., Matsushita, M., Kayahara, T., Kameya, T., Kawai, Y., Iwanaga, T., & Saito, M. (2013) · Journal of Clinical Investigation · doi:10.1172/jci67803 · Cited by 957 · see citing works
Cohen, P., Levy, J. D., Zhang, Y., Frontini, A., Kolodin, D., Svensson, K. J., Lo, J. C., Zeng, X., Ye, L., Khandekar, M. J., et al. (2014) · Cell · doi:10.1016/j.cell.2013.12.021 · Cited by 878 · see citing works
Adaptive thermogenesis in adipocytes: Is beige the new brown?
Wu, J., Cohen, P., & Spiegelman, B. M. (2013) · Genes & Development · doi:10.1101/gad.211649.112 · Cited by 828 · see citing works
Brown Remodeling of White Adipose Tissue by SirT1-Dependent Deacetylation of Pparγ
Qiang, L., Wang, L., Kon, N., Zhao, W., Lee, S., Zhang, Y., ROSENBAUM, M. S., Zhao, Y., Gu, W. J., Farmer, S. R., et al. (2012) · Cell · doi:10.1016/j.cell.2012.06.027 · Cited by 802 · see citing works
PPARγ agonists Induce a White-to-Brown Fat Conversion through Stabilization of PRDM16 Protein
Ohno, H., Shinoda, K., Spiegelman, B. M., & Kajimura, S. (2012) · Cell Metabolism · doi:10.1016/j.cmet.2012.01.019 · Cited by 749 · see citing works
Timmons, J. A., Wennmalm, K., Larsson, O., Walden, T. B., Lassmann, T., Petrovic, N., Hamilton, D. L., Gimeno, R. E., Wahlestedt, C., Baar, K., et al. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0610615104 · Cited by 732 · see citing works
Zingaretti, M. C., Crosta, F., Vitali, A., Guerrieri, M., Frontini, A., Cannon, B., Nedergaard, J., & Cinti, S. (2009) · The FASEB Journal · doi:10.1096/fj.09-133546 · Cited by 725 · see citing works
Initiation of myoblast to brown fat switch by a PRDM16–C/EBP-β transcriptional complex
Kajimura, S., Seale, P., Kubota, K., Lunsford, E., Frangioni, J. V., Gygi, S. P., & Spiegelman, B. M. (2009) · Nature · doi:10.1038/nature08262 · Cited by 703 · see citing works
Cypess, A. M., White, A. P., Vernochet, C., Schulz, T. J., Xue, R., Sass, C. A., Huang, T. L., Roberts‐Toler, C., Weiner, L. S., Sze, C., et al. (2013) · Nature Medicine · doi:10.1038/nm.3112 · Cited by 667 · see citing works
Evidence for two types of brown adipose tissue in humans
Lidell, M. E., Betz, M. J., Leinhard, O. D., Heglind, M., Elander, L., Slawik, M., Mussack, T., Nilsson, D., Romu, T., Nuutila, P., et al. (2013) · Nature Medicine · doi:10.1038/nm.3017 · Cited by 658 · see citing works
Uldry, M., Yang, W., St‐Pierre, J., Lin, J. D., Seale, P., & Spiegelman, B. M. (2006) · Cell Metabolism · doi:10.1016/j.cmet.2006.04.002 · Cited by 644 · see citing works
UCP1 in Brite/Beige Adipose Tissue Mitochondria Is Functionally Thermogenic
Shabalina, I. G., Petrovič, N., de Jong, J. M. A., Kalinovich, A., Cannon, B., & Nedergaard, J. (2013) · Cell Reports · doi:10.1016/j.celrep.2013.10.044 · Cited by 637 · see citing works
Guerra, C., Koza, R. A., Yamashita, H., Walsh, K., & Kozak, L. P. (1998) · Journal of Clinical Investigation · doi:10.1172/jci3155 · Cited by 635 · see citing works
Human BAT Possesses Molecular Signatures That Resemble Beige/Brite Cells
Sharp, L. Z., Shinoda, K., Ohno, H., Scheel, D. W., Tomoda, E., Ruiz, L., Hu, H., Wang, L. L., Pavlova, Z., Gilsanz, V., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0049452 · Cited by 635 · see citing works
Cederberg, A., Grønning, L. M., Åhrén, B., Taskén, K., Carlsson, P., & Enerbäck, S. (2001) · Cell · doi:10.1016/s0092-8674(01)00474-3 · Cited by 555 · see citing works
Jespersen, N. Z., Larsen, T. J., Peijs, L., Daugaard, S., Homøe, P., Loft, A., de Jong, J. M. A., Mathur, N., Cannon, B., Nedergaard, J., et al. (2013) · Cell Metabolism · doi:10.1016/j.cmet.2013.04.011 · Cited by 539 · see citing works
Regulation of the brown and white fat gene programs through a PRDM16/CtBP transcriptional complex
Kajimura, S., Seale, P., Tomaru, T., Erdjument-Bromage, H., Cooper, M. P., Ruas, J. L., Chin, S., Tempst, P., Lazar, M. A., & Spiegelman, B. M. (2008) · Genes & Development · doi:10.1101/gad.1666108 · Cited by 468 · see citing works
Genetic and functional characterization of clonally derived adult human brown adipocytes
Shinoda, K., Luijten, I. H. N., Hasegawa, Y., Hong, H., Sonne, S. B., Kim, M., Xue, R., Chondronikola, M., Cypess, A. M., Tseng, Y., et al. (2015) · Nature Medicine · doi:10.1038/nm.3819 · Cited by 428 · see citing works
Temperature-Acclimated Brown Adipose Tissue Modulates Insulin Sensitivity in Humans
Lee, P., Smith, S., Linderman, J. D., Courville, A. B., Brychta, R. J., Dieckmann, W., Werner, C., Chen, K. Y., & Celi, F. S. (2014) · Diabetes · doi:10.2337/db14-0513 · Cited by 398 · see citing works
Prdm16 Is Required for the Maintenance of Brown Adipocyte Identity and Function in Adult Mice
Harms, M. J., Ishibashi, J., Wang, W., Lim, H., Goyama, S., Sato, T., Kurokawa, M., Won, K., & Seale, P. (2014) · Cell Metabolism · doi:10.1016/j.cmet.2014.03.007 · Cited by 385 · see citing works
Inducible lineage tracing of Pax7‐descendant cells reveals embryonic origin of adult satellite cells
Lepper, C., & Fan, C. (2010) · genesis · doi:10.1002/dvg.20630 · Cited by 377 · see citing works
EBF2 Determines and Maintains Brown Adipocyte Identity
Rajakumari, S., Wu, J., Ishibashi, J., Lim, H., Giang, A.-H., Won, K., Reed, R. R., & Seale, P. (2013) · Cell Metabolism · doi:10.1016/j.cmet.2013.01.015 · Cited by 367 · see citing works
EHMT1 controls brown adipose cell fate and thermogenesis through the PRDM16 complex
Ohno, H., Shinoda, K., Ohyama, K., Sharp, L. Z., & Kajimura, S. (2013) · Nature · doi:10.1038/nature12652 · Cited by 331 · see citing works
Jacobsson, A., Stadler, U., Glotzer, M. A., & Kozak, L. P. (1985) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)36228-2 · Cited by 300 · see citing works
Development of insulin resistance in mice lacking PGC-1α in adipose tissues
Kleiner, S., Mepani, R. J., Laznik, D., Li, Y., Jurczak, M. J., Jornayvaz, F. R., Estall, J. L., Bhowmick, D. C., Shulman, G. I., & Spiegelman, B. M. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1207287109 · Cited by 286 · see citing works
Controlled-release mitochondrial protonophore reverses diabetes and steatohepatitis in rats
Perry, R. J., Zhang, D., Zhang, X.-M., Boyer, J. L., & Shulman, G. I. (2015) · Science · doi:10.1126/science.aaa0672 · Cited by 283 · see citing works
Fat cells directly sense temperature to activate thermogenesis
Li, Y., Wu, J., Cohen, P., Kazak, L., Khandekar, M. J., Jedrychowski, M. P., Zeng, X., Gygi, S. P., & Spiegelman, B. M. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1310261110 · Cited by 245 · see citing works
Evidence for mesothermy in dinosaurs
Grady, J. M., Enquist, B. J., Dettweiler‐Robinson, E., Wright, N. A., & Smith, F. A. (2014) · Science · doi:10.1126/science.1253143 · Cited by 169 · see citing works
Adaptive thermogenesis and thermal conductance in wild-type and UCP1-KO mice
Meyer, C. W., Willershäuser, M., Jastroch, M., Rourke, B. C., Fromme, T., Oelkrug, R., Heldmaier, G., & Klingenspor, M. (2010) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00021.2009 · Cited by 162 · see citing works
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 147 · see citing works
TLE3 Is a Dual-Function Transcriptional Coregulator of Adipogenesis
Villanueva, C. J., Waki, H., Godio, C., Nielsen, R., Chou, W.-L., Vargas, L., Wroblewski, K., Schmedt, C., Chao, L. C., Boyadjian, R., et al. (2011) · Cell Metabolism · doi:10.1016/j.cmet.2011.02.014 · Cited by 144 · see citing works
Brown Fat in Humans: Consensus Points and Experimental Guidelines
Cypess, A. M., Haft, C. R., Laughlin, M. R., & Hu, P. (2014) · Cell Metabolism · doi:10.1016/j.cmet.2014.07.025 · Cited by 137 · see citing works
Hurov, J., Huang, M., White, L. S., Lennerz, J. K., Choi, C. S., Cho, Y.-R., Kim, H., Prior, J. L., Piwnica-Worms, D., Cantley, L. C., et al. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0701179104 · Cited by 77 · see citing works
da Costa, D. C. F., & Landeira-Fernandez, A. M. (2009) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.90993.2008 · Cited by 16 · see citing works
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Adipose Tissue Remodeling: Its Role in Energy Metabolism and Metabolic Disorders
Choe, S. S., Huh, J. Y., Hwang, I. J., Kim, J. I., & Kim, J. B. (2016) · Frontiers in Endocrinology · doi:10.3389/fendo.2016.00030 · Cited by 1,206 · see citing works
Obesity and Cancer Mechanisms: Tumor Microenvironment and Inflammation
Iyengar, N. M., Gucalp, A., Dannenberg, A. J., & Hudis, C. A. (2016) · Journal of Clinical Oncology · doi:10.1200/jco.2016.67.4283 · Cited by 1,004 · see citing works
Obesity Pathogenesis: An Endocrine Society Scientific Statement
Schwartz, M. W., Seeley, R. J., Zeltser, L. M., Drewnowski, A., Ravussin, E., Redman, L. M., & Leibel, R. L. (2017) · Endocrine Reviews · doi:10.1210/er.2017-00111 · Cited by 727 · see citing works
Zhao, H., Shang, Q., Pan, Z., Bai, Y., Li, Z., Zhang, H., Zhang, Q., Guo, C., Zhang, L., & Wang, Q. (2018) · Diabetes · doi:10.2337/db17-0356 · Cited by 657 · see citing works
Non-alcoholic fatty liver disease
Neuschwander‐Tetri, B. A. (2017) · BMC Medicine · doi:10.1186/s12916-017-0806-8 · Cited by 452 · see citing works
Insulin resistance in obesity: an overview of fundamental alterations
Barazzoni, R., Cappellari, G. G., Ragni, M., & Nisoli, E. (2018) · Eating and Weight Disorders - Studies on Anorexia Bulimia and Obesity · doi:10.1007/s40519-018-0481-6 · Cited by 375 · see citing works
Blocking FSH induces thermogenic adipose tissue and reduces body fat
Liu, P., Ji, Y., Yuen, T., Rendina-Ruedy, E., DeMambro, V., Dhawan, S., Abu‐Amer, W., Izadmehr, S., Zhou, B., Shin, A. C., et al. (2017) · Nature · doi:10.1038/nature22342 · Cited by 343 · see citing works
Karczewski, J., Śledzińska, E., Baturo, A., Jończyk, I., Maleszko, A., Maleszko, A., Samborski, P., Krasińska, B., & Dobrowolska, A. (2018) · European Cytokine Network · doi:10.1684/ecn.2018.0415 · Cited by 315 · see citing works
Gonzalez-Gil, A. M., & Elizondo-Montemayor, L. (2020) · Nutrients · doi:10.3390/nu12061899 · Cited by 278 · see citing works
“In fact, the greatest benefits of BAT have been suggested to result from the redistribution of nutrient disposal rather than from thermogenesis per se [34].”
BackgroundBeyond Host Defense: Emerging Functions of the Immune System in Regulating Complex Tissue Physiology
Rankin, L. C., & Artis, D. (2018) · Cell · doi:10.1016/j.cell.2018.03.013 · Cited by 271 · see citing works
Adipose tissue inflammation: a cause or consequence of obesity-related insulin resistance?
Blüher, M. (2016) · Clinical Science · doi:10.1042/cs20160005 · Cited by 262 · see citing works
Linking the Microbiota, Chronic Disease, and the Immune System
Hand, T. W., Vujkovic-Cvijin, I., Ridaura, V. K., & Belkaid, Y. (2016) · Trends in Endocrinology & Metabolism · doi:10.1016/j.tem.2016.08.003 · Cited by 247 · see citing works
Shao, M., Ishibashi, J., Kusminski, C. M., Wang, Q. A., Hepler, C., Vishvanath, L., MacPherson, K. A., Spurgin, S. B., Sun, K., Holland, W. L., et al. (2016) · Cell Metabolism · doi:10.1016/j.cmet.2016.04.023 · Cited by 231 · see citing works
Cohen, P., & Spiegelman, B. M. (2016) · Molecular Biology of the Cell · doi:10.1091/mbc.e15-10-0749 · Cited by 211 · see citing works
Towards a multidisciplinary approach to understand and manage obesity and related diseases
Bischoff, S. C., Boirie, Y., Cederholm, T., Chourdakis, M., Cuerda, C., Delzenne, N. M., Deutz, N. E. P., Fouque, D. P., Genton, L., Gil, C., et al. (2016) · Clinical Nutrition · doi:10.1016/j.clnu.2016.11.007 · Cited by 211 · see citing works
Immunologic and endocrine functions of adipose tissue: implications for kidney disease
Zhu, Q., & Scherer, P. E. (2018) · Nature Reviews Nephrology · doi:10.1038/nrneph.2017.157 · Cited by 200 · see citing works
Mouse strains to study cold-inducible beige progenitors and beige adipocyte formation and function
Berry, D. C., Jiang, Y., & Graff, J. M. (2016) · Nature Communications · doi:10.1038/ncomms10184 · Cited by 185 · see citing works
Innate Immune Control of Adipose Tissue Homeostasis
Kane, H., & Lynch, L. (2019) · Trends in Immunology · doi:10.1016/j.it.2019.07.006 · Cited by 165 · see citing works
New developments in the biology of fibroblast growth factors
Ornitz, D. M., & Itoh, N. (2022) · WIREs Mechanisms of Disease · doi:10.1002/wsbm.1549 · Cited by 143 · see citing works
Schmidt, E. B., Dhaouadi, I., Gaziano, I., Oliverio, M., Klemm, P., Awazawa, M., Mitterer, G., Fernández‐Rebollo, E., Pradas-Juni, M., Wagner, W., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-05933-8 · Cited by 146 · see citing works
The Multifaceted Roles of PRDM16: Adipose Biology and Beyond
Chi, J., & Cohen, P. (2015) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2015.11.005 · Cited by 125 · see citing works
Perinatal Licensing of Thermogenesis by IL-33 and ST2
Odegaard, J. I., Lee, M.-W., Sogawa, Y., Bertholet, A. M., Locksley, R. M., Weinberg, D. E., Kirichok, Y., Deo, R. C., & Chawla, A. (2016) · Cell · doi:10.1016/j.cell.2016.06.040 · Cited by 119 · see citing works
Insights into the Link Between Obesity and Cancer
Ackerman, S. E., Blackburn, O. A., Marchildon, F., & Cohen, P. (2017) · Current Obesity Reports · doi:10.1007/s13679-017-0263-x · Cited by 115 · see citing works
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 112 · see citing works
Latorre-Muro, P., O’Malley, K., Bennett, C., Perry, E. A., Balsa, E., Tavares, C. D. J., Jedrychowski, M. P., Gygi, S., & Puigserver, P. (2021) · Cell Metabolism · doi:10.1016/j.cmet.2021.01.013 · Cited by 109 · see citing works
Liu, J., Li, Y., Yang, P., Wan, J., Chang, Q., Wang, T. T. Y., Lu, W., Zhang, Y., Wang, Q., & Yu, L. L. (2017) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.7b03382 · Cited by 105 · see citing works
The Beige Adipocyte as a Therapy for Metabolic Diseases
Lizcano, F. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20205058 · Cited by 106 · see citing works
FGF21 promotes thermogenic gene expression as an autocrine factor in adipocytes
Abu-Odeh, M., Zhang, Y., Reilly, S. M., Ebadat, N., Keinan, O., Valentine, J. M., Hafezi-Bakhtiari, M., Ashayer, H., Mamoun, L., Zhou, X., et al. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109331 · Cited by 106 · see citing works
Traveling from the hypothalamus to the adipose tissue: The thermogenic pathway
Contreras, C., Nogueiras, R., Diéguez, C., Rahmouni, K., & López, M. (2017) · Redox Biology · doi:10.1016/j.redox.2017.04.019 · Cited by 100 · see citing works
Intestinal Farnesoid X Receptor Signaling Modulates Metabolic Disease
Gonzalez, F. J., Jiang, C., Xie, C., & Patterson, A. D. (2017) · Digestive Diseases · doi:10.1159/000450908 · Cited by 96 · see citing works
Thyroid Hormone Action and Energy Expenditure
Yavuz, S., Prado, S. R. S. N. D., & Celi, F. S. (2019) · Journal of the Endocrine Society · doi:10.1210/js.2018-00423 · Cited by 103 · see citing works
Effects of thyroid hormones on thermogenesis and energy partitioning
Iwen, K. A., Oelkrug, R., & Brabant, G. E. (2018) · Journal of Molecular Endocrinology · doi:10.1530/jme-17-0319 · Cited by 97 · see citing works
Anti-Obesity Effects of Dietary Calcium: The Evidence and Possible Mechanisms
Zhang, F., Ye, J., Zhu, X., Wang, L., Gao, P., Shu, G., Jiang, Q., & Wang, S. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20123072 · Cited by 95 · see citing works
Interactions between central nervous system and peripheral metabolic organs
Zeng, W., Yang, F., Shen, W. L., Zhan, C., Zheng, P., & Hu, J. (2022) · Science China Life Sciences · doi:10.1007/s11427-021-2103-5 · Cited by 96 · see citing works
ATP-consuming futile cycles as energy dissipating mechanisms to counteract obesity
Brownstein, A. J., Veliova, M., Acín‐Pérez, R., Liesa, M., & Shirihai, O. S. (2021) · Reviews in Endocrine and Metabolic Disorders · doi:10.1007/s11154-021-09690-w · Cited by 90 · see citing works
Lsd1 Ablation Triggers Metabolic Reprogramming of Brown Adipose Tissue
Duteil, D., Vukotić, M., Lausecker, F., Nenseth, H. Z., Müller, J. M., Urban, S., Willmann, D., Petroll, K., Messaddeq, N., Arrigoni, L., et al. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.09.053 · Cited by 89 · see citing works
Monoacylglycerol signalling and ABHD6 in health and disease
Poursharifi, P., Madiraju, S. R. M., & Prentki, M. (2017) · Diabetes Obesity and Metabolism · doi:10.1111/dom.13008 · Cited by 89 · see citing works
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 88 · see citing works
Hu, T., Yuan, X., Wei, G., Luo, H., Lee, H. J., & Jin, W. (2017) · European Journal of Nutrition · doi:10.1007/s00394-017-1433-z · Cited by 85 · see citing works
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 85 · see citing works
Structure-Function Relationships of the Follicle-Stimulating Hormone Receptor
Ulloa‐Aguirre, A., Zariñán, T., Jardón‐Valadez, E., Gutiérrez‐Sagal, R., & Dias, J. A. (2018) · Frontiers in Endocrinology · doi:10.3389/fendo.2018.00707 · Cited by 84 · see citing works
Lizneva, D., Rahimova, A., Kim, S., Atabiekov, I., Javaid, S., Alamoush, B., Taneja, C., Khan, A., Sun, L., Azziz, R., et al. (2019) · Frontiers in Endocrinology · doi:10.3389/fendo.2019.00136 · Cited by 83 · see citing works
Neyrinck, A. M., Bindels, L. B., Geurts, L., Hul, M. V., Cani, P. D., & Delzenne, N. M. (2017) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2017.07.008 · Cited by 82 · see citing works
Adipose Signals Regulating Distal Organ Health and Disease
Gilani, A., Stoll, L., Homan, E. A., & Lo, J. C. (2024) · Diabetes · doi:10.2337/dbi23-0005 · Cited by 82 · see citing works
Adipogenesis: A Necessary but Harmful Strategy
Hafidi, M. E., Buelna‐Chontal, M., Sánchez‐Muñoz, F., & Carbó, R. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20153657 · Cited by 80 · see citing works
Brown adipose tissue: a potential target in the fight against obesity and the metabolic syndrome.
Poekes, L., Lanthier, N., & Leclercq, I. (2015) · Clinical science · doi:10.1042/cs20150339 · Cited by 77 · see citing works
Serotonergic Control of Metabolic Homeostasis
Wyler, S. C., Lord, C. C., Lee, S., Elmquist, J. K., & Liu, C. (2017) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2017.00277 · Cited by 79 · see citing works
Kim, H., Park, J., Jung, Y., Ahn, K. S., & Um, J. (2018) · Phytomedicine · doi:10.1016/j.phymed.2018.09.227 · Cited by 80 · see citing works
Human brown adipose tissue as a target for obesity management; beyond cold‐induced thermogenesis
Loh, R. K. C., Kingwell, B. A., & Carey, A. L. (2017) · Obesity Reviews · doi:10.1111/obr.12584 · Cited by 77 · see citing works
Insulin action in the brain: Roles in energy and glucose homeostasis
Dodd, G. T., & Tiganis, T. (2017) · Journal of Neuroendocrinology · doi:10.1111/jne.12513 · Cited by 75 · see citing works
Uncoupling mechanism and redox regulation of mitochondrial uncoupling protein 1 (UCP1)
Ježek, P., Jabůrek, M., & Porter, R. K. (2018) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2018.11.007 · Cited by 74 · see citing works
Porcine gut microbiota in mediating host metabolic adaptation to cold stress
Zhang, Y., Lan, S., Zhu, R. Y., Zhang, S., Liu, S., Wang, Y., Wu, Y., Xing, S.-C., Liao, X., & Mi, J. (2022) · npj Biofilms and Microbiomes · doi:10.1038/s41522-022-00283-2 · Cited by 73 · see citing works
FSH, Bone Mass, Body Fat, and Biological Aging
Zaidi, M., Lizneva, D., Kim, S., Sun, L., Iqbal, J. Z., New, M. I., Rosen, C. J., & Yuen, T. (2018) · Endocrinology · doi:10.1210/en.2018-00601 · Cited by 67 · see citing works
Sharma, R., Matsuzaka, T., Kaushik, M. K., Sugasawa, T., Ohno, H., Wang, Y., Motomura, K., Shimura, T., Okajima, Y., Mizunoe, Y., et al. (2019) · Scientific Reports · doi:10.1038/s41598-019-41631-1 · Cited by 65 · see citing works
The Complex Roles of Mechanistic Target of Rapamycin in Adipocytes and Beyond
Lee, P. L., Jung, S. M., & Guertin, D. A. (2017) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2017.01.004 · Cited by 64 · see citing works
Du, H., Wang, Q., Li, T., Ren, D., & Yang, X. (2021) · Food & Function · doi:10.1039/d1fo01361k · Cited by 62 · see citing works
Brown, E. L., Hazen, B. C., Eury, E., Wattez, J.-S., Gantner, M. L., Albert, V., Chau, S., Sánchez-Alavez, M., Conti, B., & Kralli, A. (2018) · iScience · doi:10.1016/j.isci.2018.03.005 · Cited by 55 · see citing works
Adipose stem cells in obesity: challenges and opportunities
Shin, S., El-Sabbagh, A. S., Lukas, B., Tanneberger, S. J., & Jiang, Y. (2020) · Bioscience Reports · doi:10.1042/bsr20194076 · Cited by 54 · see citing works
Tol, M. J. P. M., Ottenhoff, R., van Eijk, M., Zelcer, N., Aten, J., Houten, S. M., Geerts, D., van Roomen, C. P. A. A., Bierlaagh, M. C., Scheij, S. S., et al. (2016) · Diabetes · doi:10.2337/db16-0243 · Cited by 54 · see citing works
Ceramides are necessary and sufficient for diet-induced impairment of thermogenic adipocytes
Chaurasia, B., Li, Y., Talbot, C. L., Maschek, J. A., Cox, J. E., Schuchman, E. H., Hirabayashi, Y., Holland, W. L., & Summers, S. A. (2020) · Molecular Metabolism · doi:10.1016/j.molmet.2020.101145 · Cited by 53 · see citing works
Hepler, C., Shao, M., Xia, J. Y., Ghaben, A. L., Pearson, M. J., Vishvanath, L., Sharma, A. X., Morley, T. S., Holland, W. L., & Gupta, R. K. (2017) · eLife · doi:10.7554/elife.27669 · Cited by 50 · see citing works
Adipocyte β-arrestin-2 is essential for maintaining whole body glucose and energy homeostasis
Pydi, S. P., Jain, S., Tung, W., Cui, Y., Zhu, L., Sakamoto, W., Jain, S., Abel, B. S., Skarulis, M. C., Liu, J., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-11003-4 · Cited by 52 · see citing works
Sex differences in thermoregulation in mammals: Implications for energy homeostasis
Fernández‐Peña, C., Reimúndez, A., Viana, F., Arce, V. M., & Señarís, R. M. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1093376 · Cited by 52 · see citing works
Ginsenoside Rb2 Alleviates Obesity by Activation of Brown Fat and Induction of Browning of White Fat
Hong, Y., Lin, Y., Si, Q., Yang, L., Dong, W., & Gu, X. (2019) · Frontiers in Endocrinology · doi:10.3389/fendo.2019.00153 · Cited by 51 · see citing works
Redox control of non-shivering thermogenesis
Lettieri‐Barbato, D. (2019) · Molecular Metabolism · doi:10.1016/j.molmet.2019.04.002 · Cited by 50 · see citing works
Lee, K., Seo, Y., Song, J.-H., Chei, S., & Lee, B.-Y. (2018) · Journal of Ginseng Research · doi:10.1016/j.jgr.2018.07.005 · Cited by 50 · see citing works
Regulation of Energy Metabolism by Receptor Tyrosine Kinase Ligands
Zhao, M., Jung, Y., Jiang, Z., & Svensson, K. J. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2020.00354 · Cited by 51 · see citing works
Lee, H. S., Heo, C. U., Song, Y.-H., Lee, K., & Choi, C. (2023) · Archives of Pharmacal Research · doi:10.1007/s12272-023-01432-7 · Cited by 47 · see citing works
Multiple Myeloma and Fatty Acid Metabolism
Masarwi, M., DeSchiffart, A., Ham, J., & Reagan, M. R. (2019) · JBMR Plus · doi:10.1002/jbm4.10173 · Cited by 43 · see citing works
McClung, J. A., Levy, L., Garcia, V. G., Stec, D. E., Peterson, S. J., & Abraham, N. G. (2021) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2021.107975 · Cited by 47 · see citing works
Sarcolipin is a novel regulator of muscle metabolism and obesity
Maurya, S. K., & Periasamy, M. (2015) · Pharmacological Research · doi:10.1016/j.phrs.2015.10.020 · Cited by 47 · see citing works
Role of cell cycle regulators in adipose tissue and whole body energy homeostasis
López‐Mejía, I. C., Castillo‐Armengol, J., Lagarrigue, S., & Lluis Fajas, A. (2017) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-017-2668-9 · Cited by 45 · see citing works
Progenitor-like characteristics in a subgroup of UCP1+ cells within white adipose tissue
Park, J., Shin, S., Liu, L., Jahan, I., Ong, S., Xu, P., Berry, D. C., & Jiang, Y.-W. (2021) · Developmental Cell · doi:10.1016/j.devcel.2021.02.018 · Cited by 41 · see citing works
IL-6, cancer and cachexia: metabolic dysfunction creates the perfect storm
White, J. P. (2017) · Translational Cancer Research · doi:10.21037/tcr.2017.03.52 · Cited by 43 · see citing works
Silibinin Regulates Lipid Metabolism and Differentiation in Functional Human Adipocytes
Barbagallo, I. A., Vanella, L., Cambria, M. T., Tibullo, D., Godos, J., Guarnaccia, L., Zappalà, A., Galvano, F., & Volti, G. L. (2016) · Frontiers in Pharmacology · doi:10.3389/fphar.2015.00309 · Cited by 42 · see citing works
The Immune System in Obesity: Developing Paradigms Amidst Inconvenient Truths
Agrawal, M., Kern, P. A., & Nikolajczyk, B. S. (2017) · Current Diabetes Reports · doi:10.1007/s11892-017-0917-9 · Cited by 42 · see citing works
Combined training increases thermogenic fat activity in patients with overweight and type 2 diabetes
Bonfante, I. L. P., Monfort‐Pires, M., Duft, R. G., Mateus, K. C. D. S., Júnior, J. C. D. L., Trombeta, J. C. D. S., Finardi, E. A. R., Brunelli, D. T., Morari, J., de Lima, J. A. B., et al. (2022) · International Journal of Obesity · doi:10.1038/s41366-022-01086-3 · Cited by 41 · see citing works
Vargas‐Castillo, A., Sun, Y., Smythers, A. L., Grauvogel, L., Dumesic, P. A., Emont, M. P., Tsai, L. T.-Y., Rosen, E. D., Zammit, N. W., Shaffer, S. M., et al. (2024) · Cell Metabolism · doi:10.1016/j.cmet.2024.07.002 · Cited by 40 · see citing works
Qi, Y., Sun, L., & Yang, H. (2017) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2017.06.016 · Cited by 40 · see citing works
de Almeida, M. M., Dias-Rocha, C. P., Souza, A. S., Muros, M. F., Mendonca, L. S., Pazos-Moura, C. C., & Trevenzoli, I. H. (2017) · British Journal Of Nutrition · doi:10.1017/s0007114517002884 · Cited by 40 · see citing works
Mao, L., Wang, L. Y., Bennett, S., Xu, J., & Zou, J. (2022) · Frontiers in Physiology · doi:10.3389/fphys.2022.1043237 · Cited by 39 · see citing works
Li, X., Wei, T., Li, J., Yuan, Y., Wu, M. T., Chen, F., Deng, Z., & Luo, T. F. (2022) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.202101015 · Cited by 39 · see citing works
Biology of Beige Adipocyte and Possible Therapy for Type 2 Diabetes and Obesity
Lizcano, F., & Vargas, D. (2016) · International Journal of Endocrinology · doi:10.1155/2016/9542061 · Cited by 38 · see citing works
Leu, S., Tsai, Y.-C., Chen, W., Hsu, C., Lee, Y., & Cheng, P. (2018) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2018.01.017 · Cited by 39 · see citing works
Makwana, K., Chodavarapu, H., Morones, N., Chi, J., Barr, W., Novinbakht, E., wang, Y., Nguyen, P., Jovanović, P., Cohen, P., et al. (2021) · Molecular Metabolism · doi:10.1016/j.molmet.2021.101161 · Cited by 38 · see citing works
Bini, S., D'Erasmo, L., Costanzo, A. D., Minicocci, I., Pecce, V., & Arca, M. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22020742 · Cited by 36 · see citing works
Li, X., Zhao, Y., Qi, X., Cui, J., Zhou, Y., Tan, Y., Huang, X., & Ye, H. (2024) · Current Research in Food Science · doi:10.1016/j.crfs.2024.100683 · Cited by 38 · see citing works
Metabolic Syndrome, Thyroid Dysfunction, and Cardiovascular Risk: The Triptych of Evil
Pingitore, A., Gaggini, M., Mastorci, F., Sabatino, L., Cordiviola, L., & Vassalle, C. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms251910628 · Cited by 39 · see citing works
Mukherjee, J., Baranwal, A., & Schade, K. N. (2016) · Current Diabetes Reviews · doi:10.2174/1573399812666160517115450 · Cited by 35 · see citing works
Unraveling the connection between eosinophils and obesity
Calco, G. N., Fryer, A. D., & Nie, Z. (2020) · Journal of Leukocyte Biology · doi:10.1002/jlb.5mr0120-377r · Cited by 36 · see citing works
Switching harmful visceral fat to beneficial energy combustion improves metabolic dysfunctions
Yang, X., Sui, W., Zhang, M., Dong, M., Lim, S., Seki, T., Guo, Z., Fischer, C., Lu, H., Zhang, C., et al. (2017) · JCI Insight · doi:10.1172/jci.insight.89044 · Cited by 35 · see citing works
Shen, H. H., Peterson, S. J., Bellner, L., Choudhary, A., Levy, L., Gancz, L., Sasson, A., Trainer, J., Rezzani, R., Resnick, A., et al. (2020) · Antioxidants · doi:10.3390/antiox9060489 · Cited by 35 · see citing works
RetractedInflammation in Metabolic and Cardiovascular Disorders—Role of Oxidative Stress
Sun, Y., Rawish, E., Nording, H., & Langer, H. F. (2021) · Life · doi:10.3390/life11070672 · Cited by 35 · see citing works
Translational potential of mouse models of human metabolic disease
Farooqi, I. S., & Xu, Y. (2024) · Cell · doi:10.1016/j.cell.2024.07.011 · Cited by 35 · see citing works
Liu, L., Puri, N., Raffaele, M., Schragenheim, J., Singh, S. P., Bradbury, J. A., Bellner, L., Vanella, L., Zeldin, D. C., Cao, J. J., et al. (2018) · Prostaglandins & Other Lipid Mediators · doi:10.1016/j.prostaglandins.2018.07.004 · Cited by 34 · see citing works
Hepsin enhances liver metabolism and inhibits adipocyte browning in mice
Li, S., Peng, J., Wang, H., Zhang, W., Brown, J. M., Zhou, Y., & Wu, Q. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1918445117 · Cited by 34 · see citing works
Tu, W.-Z., Fu, Y.-B., & Xie, X. (2019) · Acta Pharmacologica Sinica · doi:10.1038/s41401-019-0264-2 · Cited by 33 · see citing works
A systems perspective on brown adipogenesis and metabolic activation
Pradhan, R., Zachara, M., & Deplancke, B. (2017) · Obesity Reviews · doi:10.1111/obr.12512 · Cited by 33 · see citing works
Adaptive thermogenesis in brown adipose tissue involves activation of pannexin-1 channels
Subramanian, S., Serbulea, V., Upchurch, C. M., Polanowska‐Grabowska, R., Mendu, S. K., Sahu, S., Jayaguru, P., Aylor, K. W., Chordia, M. D., Steinberg, L., et al. (2020) · Molecular Metabolism · doi:10.1016/j.molmet.2020.101130 · Cited by 32 · see citing works
Deconstructing Adipose Tissue Heterogeneity One Cell at a Time
Duerre, D. J., & Galmozzi, A. (2022) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.847291 · Cited by 32 · see citing works
- Authors
- Cohen, P., & Spiegelman, B. M.
- Affiliations
- Rockefeller University (US)
- Harvard University (US)
- Corresponding author
- Spiegelman, Bruce M.
- Venue
- Diabetes
- Publisher
- American Diabetes Association
- Published
- 2015-06-07
- Volume
- 64
- Issue
- 7
- Pages
- 2346-2351
- ISSN
- 0012-1797 (ISSN-L)
- 1939-327X
- PMC
- PMC4477363
- OpenAlex
- W2122275827
- Cited by
- 259
- References
- 48
- Citations by year
- 2026: 8 · 2025: 9 · 2024: 23 · 2023: 14 · 2022: 19 · 2021: 20 · 2020: 33 · 2019: 29 · 2018: 31 · 2017: 38 · 2016: 28 · 2015: 6
- FWCI
- 4.22
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Diabetes (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- American Heart Association
- National Institutes of Health (DK31495)
- JPB Foundation
- Topics
- Health Sciences › Medicine › Physiology › Adipose Tissue and Metabolism
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Peroxisome Proliferator-Activated Receptors
- Health Sciences › Medicine › Epidemiology › Adipokines, Inflammation, and Metabolic Diseases
- Keywords
- brown adipose tissue, beige adipose tissue, thermogenesis, mitochondrial uncoupling, UCP1, energy expenditure, energy balance, obesity, type 2 diabetes, transcriptional regulation
- MeSH terms
- Uncoupling Protein 1, Animals, Adipose Tissue, Brown, Cold Temperature, DNA-Binding Proteins, Energy Metabolism, Humans, Ion Channels, Thermodynamics, Transcription Factors, Transcription, Genetic, Adipocytes, Thermogenesis, Mitochondrial Proteins
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