Cold-Activated Brown Adipose Tissue in Healthy Men
Open accessAbstract
BACKGROUND: Studies in animals indicate that brown adipose tissue is important in the regulation of body weight, and it is possible that individual variation in adaptive thermogenesis can be attributed to variations in the amount or activity of brown adipose tissue. Until recently, the presence of brown adipose tissue was thought to be relevant only in small mammals and infants, with negligible physiologic relevance in adult humans. We performed a systematic examination of the presence, distribution, and activity of brown adipose tissue in lean and obese men during exposure to cold temperature. Brown-adipose-tissue activity was studied in relation to body composition and energy metabolism. METHODS: We studied 24 healthy men--10 who were lean (body-mass index [BMI] [the weight in kilograms divided by the square of the height in meters], < 25) and 14 who were overweight or obese (BMI, > or = 25)--under thermoneutral conditions (22 degrees C) and during mild cold exposure (16 degrees C). Putative brown-adipose-tissue activity was determined with the use of integrated (18)F-fluorodeoxyglucose positron-emission tomography and computed tomography. Body composition and energy expenditure were measured with the use of dual-energy x-ray absorptiometry and indirect calorimetry. RESULTS: Brown-adipose-tissue activity was observed in 23 of the 24 subjects (96%) during cold exposure but not under thermoneutral conditions. The activity was significantly lower in the overweight or obese subjects than in the lean subjects (P=0.007). BMI and percentage of body fat both had significant negative correlations with brown adipose tissue, whereas resting metabolic rate had a significant positive correlation. CONCLUSIONS: The percentage of young men with brown adipose tissue is high, but its activity is reduced in men who are overweight or obese. Brown adipose tissue may be metabolically important in men, and the fact that it is reduced yet present in most overweight or obese subjects may make it a target for the treatment of obesity.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
All groups showed major depots of metabolically active fat in the cervical-supraclavicular region, a slightly different site from that in rodents and children, where BAT is found mainly in the interscapular area.
“All the groups showed major depots of metabolically active fat in the cervical–supraclavicular region, a slightly different site from that in rodents and children, where BAT is found mainly situated in the interscapular area.”
From Mitochondrial fatty acid oxidation in obesity (2013) · cites this paper as [165]
In 2009, five independent groups used PET-CT to identify the presence and study the relevance of BAT in adult humans.
“However, the real breakthrough arrived in 2009 when five independent groups used PET-CT to identify the presence and study the relevance of BAT in adult humans ([30](#B30), [143](#B143), [165](#B165), [168](#B168), [181](#B181)).”
From Mitochondrial fatty acid oxidation in obesity (2013) · cites this paper as [165]
Expression of UCP1, DIO2, and the β3-adrenergic receptor was reported, indicating the potential responsiveness of human BAT to both hormonal and pharmacological stimuli.
“The expression of UCP1, DIO2, and the β3-adrenergic receptor was also reported, thereby indicating the potential responsiveness of human BAT to both hormonal and pharmacological stimuli.”
From Mitochondrial fatty acid oxidation in obesity (2013) · cites this paper as [165]
Recent studies have shown that adult humans maintain potentially active brown adipose tissue, making this high energetic tissue a real therapeutic target.
“Second, recent studies have shown that adult humans maintain potentially active brown adipose tissue, making this high energetic tissue a real therapeutic target 13–17.”
From Cellular bioenergetics as a target for obesity therapy (2010) · cites this paper as [14]
PET/CT imaging was used to prove conclusively that adult humans possess physiologically active UCP1-positive BAT.
“However, it was only during the past year PET/CT imaging was used to prove conclusively that adult humans possess physiologically active UCP1-positive BAT,13–17.”
From Cellular bioenergetics as a target for obesity therapy (2010) · cites this paper as [14]
Prospective studies using cold stimulation to increase BAT activity and detection via PET/CT show that among younger people, 96% have functional BAT.
“However, histological analysis of cervical fat biopsies show rates three times higher 17, and prospective studies using cold stimulation to increase BAT activity and detection via PET/CT show that among younger people, 96% have functional BAT 14.”
From Cellular bioenergetics as a target for obesity therapy (2010) · cites this paper as [14]
BAT activity correlates inversely with BMI and percentage body fat, suggesting a role in energy balance.
“More importantly, BAT activity correlates inversely with BMI13,14 and percentage body fat 13,14, suggesting a role in energy balance.”
From Cellular bioenergetics as a target for obesity therapy (2010) · cites this paper as [14]
The inverse correlation between BAT activity and obesity was seen despite the fact that lean and overweight subjects had similar resting metabolic rates in both thermoneutral and cold exposure, suggesting that overweight people increase their energy expenditure using different physiological mechanisms.
“This inverse correlation between BAT activity and obesity was seen despite the fact that the lean and overweight subjects had similar resting metabolic rates in both thermoneutral and cold exposure, suggesting that overweight people increase their energy expenditure using different physiological mechanisms 14.”
From Cellular bioenergetics as a target for obesity therapy (2010) · cites this paper as [14]
Adult human BAT is functional and may be involved in protecting against weight loss.
“Although it has only recently been proven that adult human BAT is functional and may be involved in protecting against weight loss 13–17, attempts to exploit BAT energy expenditure for treating obesity have been around for decades.”
From Cellular bioenergetics as a target for obesity therapy (2010) · cites this paper as [14]
The role of BAT in adult humans is controversial since its detection is dependent upon the approach employed.
“The role of BAT in adult humans is controversial since its detection is dependent upon the approach employed (Leitner et al., 2017; Porter et al., 2016; van Marken Lichtenbelt et al., 2009).”
From Origin and function of stress-induced IL-6 in murine models (2020) · cites this paper as van Marken Lichtenbelt et al., 2009
Humans express BAT in the neck region.
“This now needs to be reconsidered since very recent findings indicate that humans do express BAT in the neck region (78, 278, 318, 323) and the amount of BAT correlates inversely with body-mass index (78).”
From Mitochondrial Dysfunction in Diabetes: From Molecular Mechanisms to Functional Significance and Therapeutic Opportunities (2010) · cites this paper as [318]
Brown adipose tissue (BAT) is a druggable therapeutic target for stimulating energy expenditure.
“Recent studies utilizing fluoro-deoxyflucose positron emission tomographic scans have resuscitated brown adipose tissue (BAT) as a druggable therapeutic target for stimulating energy expenditure”
Such depots appear to be less active as a function of aging and/or obesity.
“Such depots appear to be less active as a function of aging and/or obesity (151, 164 -167).”
From The role of mitochondria in the pathogenesis of type 2 diabetes (2010) · cites this paper as [165]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
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 · see citing works
Unexpected evidence for active brown adipose tissue in adult humans
Nedergaard, J., Bengtsson, T., & Cannon, B. (2007) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00691.2006 · Cited by 1,824 · see citing works
Towards a molecular understanding of adaptive thermogenesis
Lowell, B. B., & Spiegelman, B. M. (2000) · Nature · doi:10.1038/35007527 · Cited by 1,630 · see citing works
Reduced Rate of Energy Expenditure as a Risk Factor for Body-Weight Gain
Ravussin, E., Lillioja, S., Knowler, W. C., Christin, L., Freymond, D., Abbott, W. G. H., Boyce, V., Howard, B. V., & Bogardus, C. (1988) · New England Journal of Medicine · doi:10.1056/nejm198802253180802 · Cited by 1,215 · 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
Determinants of 24-hour energy expenditure in man. Methods and results using a respiratory chamber.
Ravussin, E., Lillioja, S., Anderson, T. E., Christin, L., & Bogardus, C. (1986) · Journal of Clinical Investigation · doi:10.1172/jci112749 · Cited by 1,166 · see citing works
The distribution of brown adipose tissue in the human.
Heaton, J. M. (1972) · PubMed · Cited by 606 · see citing works
Hany, T. F., Gharehpapagh, E., Kamel, E. M., Buck, A., Himms-Hagen, J., & von Schulthess, G. K. (2002) · European Journal of Nuclear Medicine and Molecular Imaging · doi:10.1007/s00259-002-0902-6 · Cited by 511 · 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
Uptake in supraclavicular area fat ("USA-Fat"): description on 18F-FDG PET/CT.
Cohade, C., Osman, M., Pannu, H. K., & Wahl, R. L. (2003) · PubMed · Cited by 440 · see citing works
Skin-surface Temperature Gradients Correlate with Fingertip Blood Flow in Humans
Rubinstein, E. H., & Sessler, D. I. (1990) · Anesthesiology · doi:10.1097/00000542-199009000-00027 · Cited by 406 · see citing works
Evaluation of wireless determination of skin temperature using iButtons
VANMARKENLICHTENBELT, W., DAANEN, H., WOUTERS, L., FRONCZEK, R., RAYMANN, R., SEVERENS, N., & VANSOMEREN, E. (2006) · Physiology & Behavior · doi:10.1016/j.physbeh.2006.04.026 · Cited by 392 · see citing works
Self-citationYEUNG, H. W. D., Grewal, R. K., Gönen, M., Schöder, H. M., & Larson, S. M. (2003) · PubMed · Cited by 370 · see citing works
The occurrence of brown adipose tissue in outdoor workers
Huttunen, P., Hirvonen, J., & Kinnula, V. L. (1981) · European Journal of Applied Physiology · doi:10.1007/bf00422121 · Cited by 335 · see citing works
"USA-Fat": prevalence is related to ambient outdoor temperature-evaluation with 18F-FDG PET/CT.
Cohade, C., Mourtzikos, K. A., & Wahl, R. L. (2003) · PubMed · Cited by 295 · see citing works
Seasonal changes in metabolic and temperature responses to cold air in humans
VANOOIJEN, A., VANMARKENLICHTENBELT, W., VANSTEENHOVEN, A., & Westerterp, K. R. (2004) · Physiology & Behavior · doi:10.1016/j.physbeh.2004.05.001 · Cited by 165 · see citing works
Self-citationMetabolic rate and physical development in children at risk of obesity
Griffiths, M., Payne, P., Rivers, J. P. W., Cox, M., & Stunkard, A. J. (1990) · The Lancet · doi:10.1016/0140-6736(90)91592-x · Cited by 151 · see citing works
Wijers, S. L. J., Schrauwen, P., Saris, W. H. M., & van Marken Lichtenbelt, W. D. (2008) · PLoS ONE · doi:10.1371/journal.pone.0001777 · Cited by 135 · see citing works
Self-citationHeat Production and Body Temperature During Cooling and Rewarming in Overweight and Lean Men
van Ooijen, A. M. J., Westerterp, K. R., Wouters, L., Schoffelen, P. F. M., van Steenhoven, A. A., & Lichtenbelt, W. D. V. M. (2006) · Obesity · doi:10.1038/oby.2006.223 · Cited by 119 · see citing works
Individual Thermogenic Responses to Mild Cold and Overfeeding Are Closely Related
Wijers, S. L. J., Saris, W. H. M., & van Marken Lichtenbelt, W. D. (2007) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2007-1065 · Cited by 99 · see citing works
Self-citationBrown fat in breast cancer patients: analysis of serial 18F-FDG PET/CT scans
Rousseau, C., Bourbouloux, E., Campion, L., Fleury, N., Bridji, B., Chatal, J., Resche, I., & Campone, M. (2006) · European Journal of Nuclear Medicine and Molecular Imaging · doi:10.1007/s00259-006-0066-x · Cited by 92 · see citing works
Cannon, B., & Nedergaard, J. (2008) · Nature · doi:10.1038/454947a · Cited by 73 · see citing works
Prediction of body weight changes caused by changes in energy balance
Christiansen, E., & Garby, L. (2002) · European Journal of Clinical Investigation · doi:10.1046/j.1365-2362.2002.01036.x · Cited by 69 · see citing works
Does Brown Adipose Tissue (BAT) Have a Role in the Physiology or Treatment of Human Obesity?
Himms‐Hagen, J. (2001) · Reviews in Endocrine and Metabolic Disorders · doi:10.1023/a:1011856617047 · Cited by 45 · see citing works
Sturkenboom, M. G. G., Franssen, E. J. F., Berkhof, J. H., & Hoekstra, O. S. (2004) · Nuclear Medicine Communications · doi:10.1097/00006231-200411000-00007 · Cited by 29 · see citing works
Flagged first, then by citations
Research works printed but not linked: 1
- Cold-Activated Brown Adipose Tissue in Healthy Men etal muscle to thermogenesis induced by ephedrine in man. Am J Physiol 1985;248: E507-E515.
Cited by
Sorted by citations
Mitochondria: In Sickness and in Health
Nunnari, J., & Suomalainen, A. (2012) · Cell · doi:10.1016/j.cell.2012.02.035 · Cited by 3,479 · see citing works
Thyroid Hormone Regulation of Metabolism
Mullur, R., Liu, Y.-Y., & Brent, G. A. (2014) · Physiological Reviews · doi:10.1152/physrev.00030.2013 · Cited by 2,421 · see citing works
Brown and beige fat: Development, function and therapeutic potential
Harms, M., & Seale, P. (2013) · Nature Medicine · doi:10.1038/nm.3361 · Cited by 2,328 · see citing works
Brown 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
Autophagy in mammalian development and differentiation
Mizushima, N., & Levine, B. (2010) · Nature Cell Biology · doi:10.1038/ncb0910-823 · Cited by 1,555 · see citing works
<i>FTO</i> Obesity Variant Circuitry and Adipocyte Browning in Humans
Claussnitzer, M., Dankel, S. N., Kim, K.-H., Quon, G., Meuleman, W., Haugen, C., Glunk, V., Sousa, I. S., Beaudry, J. L., Puviindran, V., et al. (2015) · New England Journal of Medicine · doi:10.1056/nejmoa1502214 · Cited by 1,332 · see citing works
Petrovic, N., Walden, T. B., Shabalina, I. G., Timmons, J. A., Cannon, B., & Nedergaard, J. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.053942 · Cited by 1,263 · see citing works
Brown adipose tissue regulates glucose homeostasis and insulin sensitivity
Stanford, K. I., Middelbeek, R. J. W., Townsend, K. L., An, D., Nygaard, E. B., Hitchcox, K. M., Markan, K. R., Nakano, K., Hirshman, M. F., Tseng, Y.-H., et al. (2013) · Journal of Clinical Investigation · doi:10.1172/jci62308 · Cited by 1,180 · see citing works
Adipose tissue browning and metabolic health
Bartelt, A., & Heeren, J. (2014) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2013.204 · Cited by 1,177 · see citing works
Adipokines in health and disease
Fasshauer, M., & Blüher, M. (2015) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2015.04.014 · Cited by 1,050 · see citing works
Bordicchia, M., Liu, D., Amri, E.-Z., Ailhaud, G., Dessì-Fulgheri, P., Zhang, C., Takahashi, N., Sarzani, R., & Collins, S. (2012) · Journal of Clinical Investigation · doi:10.1172/jci59701 · Cited by 872 · see citing works
Mitochondrial proton and electron leaks
Jastroch, M., Divakaruni, A. S., Mookerjee, S., Treberg, J. R., & Brand, M. D. (2010) · Essays in Biochemistry · doi:10.1042/bse0470053 · Cited by 829 · 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
PPARs in Obesity-Induced T2DM, Dyslipidaemia and NAFLD
Gross, B., Pawlak, M., Lefebvre, P., & Staels, B. (2017) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2016.135 · Cited by 778 · see citing works
Irisin and FGF21 are cold-induced endocrine activators of brown fat function in humans
Lee, P., Linderman, J. D., Smith, S., Brychta, R. J., Wang, J., Idelson, C., Perron, R. M., Werner, C. D., Phan, G. Q., Kammula, U. S., et al. (2014) · Cell Metabolism · doi:10.1016/j.cmet.2013.12.017 · Cited by 802 · see citing works
Moreno-Navarrete, J. M., Ortega, F., Serrano, M., Guerra, E., Pardo, G., Tinahones, F., Ricart, W., & Fernández-Real, J. M. (2013) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2012-2749 · Cited by 788 · see citing works
Obesity and type 2 diabetes mellitus: connections in epidemiology, pathogenesis, and treatments
Ruze, R., Liu, T., Zou, X., Song, J., Chen, Y., Xu, R., Yin, X., & Xu, Q. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1161521 · Cited by 799 · see citing works
“in response to cold exposure (30), exercise (31), and endocrine signals (32).”
BackgroundMetabolic Flexibility as an Adaptation to Energy Resources and Requirements in Health and Disease
Smith, R. L., Soeters, M. R., Wüst, R. C. I., & Houtkooper, R. H. (2018) · Endocrine Reviews · doi:10.1210/er.2017-00211 · Cited by 787 · see citing works
Sivitz, W. I., & Yorek, M. A. (2010) · Antioxidants & Redox Signaling · doi:10.1089/ars.2009.2531 · Cited by 742 · see citing works
Brown adipose tissue is associated with cardiometabolic health
Becher, T., Palanisamy, S., Kramer, D. J., Eljalby, M., Marx, S. J., Wibmer, A. G., Butler, S. D., Jiang, C. S., Vaughan, R., Schöder, H., et al. (2021) · Nature Medicine · doi:10.1038/s41591-020-1126-7 · Cited by 743 · 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
Targeting adipose tissue in the treatment of obesity-associated diabetes
Kusminski, C. M., Bickel, P. E., & Scherer, P. E. (2016) · Nature Reviews Drug Discovery · doi:10.1038/nrd.2016.75 · Cited by 678 · see citing works
Butyrate reduces appetite and activates brown adipose tissue via the gut-brain neural circuit
Li, Z., Yi, C.-X., Katiraei, S., Kooijman, S., Zhou, E., Chung, C. K., Gao, Y., van den Heuvel, J. K., Meijer, O. C., Berbée, J. F. P., et al. (2018) · Gut · doi:10.1136/gutjnl-2017-314050 · Cited by 674 · see citing works
The therapeutic potential of FGF21 in metabolic diseases: from bench to clinic
Geng, L., Lam, K. S. L., & Xu, A. (2020) · Nature Reviews Endocrinology · doi:10.1038/s41574-020-0386-0 · Cited by 607 · see citing works
GLP-1 agonism stimulates brown adipose tissue thermogenesis and browning through hypothalamic AMPK
Beiroa, D., Imbernon, M., Gallego, R., Senra, A., Herranz, D., Villarroya, F., Serrano, M., Fernø, J., Salvador, J., Escalada, J., et al. (2014) · Diabetes · doi:10.2337/db14-0302 · Cited by 602 · see citing works
Thyroid dysfunction and diabetes mellitus: two closely associated disorders
Biondi, B., Kahaly, G. J., & Robertson, R. P. (2019) · Endocrine Reviews · doi:10.1210/er.2018-00163 · Cited by 598 · see citing works
Cellular bioenergetics as a target for obesity therapy
Tseng, Y.-H., Cypess, A. M., & Kahn, C. R. (2010) · Nature Reviews Drug Discovery · doi:10.1038/nrd3138 · Cited by 591 · see citing works
BMP8B Increases Brown Adipose Tissue Thermogenesis through Both Central and Peripheral Actions
Whittle, A. J., Carobbio, S., Martins, L., Slawik, M., Hondares, E., Vázquez, M. J., Morgan, D., Csikasz, R. I., Gallego, R., Rodriguez-Cuenca, S., et al. (2012) · Cell · doi:10.1016/j.cell.2012.02.066 · Cited by 573 · see citing works
Norheim, F., Langleite, T. M., Hjorth, M., Holen, T., Kielland, A., Stadheim, H. K., Gulseth, H. L., Birkeland, K. I., Jensen, J., & Drevon, C. A. (2014) · The FEBS Journal · doi:10.1111/febs.12619 · Cited by 563 · see citing works
The role of mitochondria in the pathogenesis of type 2 diabetes
Patti, M.-E., & Corvera, S. (2010) · Endocrine Reviews · doi:10.1210/er.2009-0027 · Cited by 551 · see citing works
Central circuitries for body temperature regulation and fever
Nakamura, K. (2011) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00109.2011 · Cited by 543 · see citing works
Landsberg, L., Aronne, L. J., Beilin, L. J., Burke, V., Igel, L. I., Lloyd‐Jones, D., & Sowers, J. (2013) · The Journal of Clinical Hypertension · doi:10.1111/jch.12049 · Cited by 528 · see citing works
Obesity and related consequences to ageing
Jura, M., & Kozak, L. P. (2016) · AGE · doi:10.1007/s11357-016-9884-3 · Cited by 473 · see citing works
Impaired adipogenesis and dysfunctional adipose tissue in human hypertrophic obesity
Hammarstedt, A., Gogg, S., Hedjazifar, S., Nerstedt, A., & Smith, U. (2018) · Physiological Reviews · doi:10.1152/physrev.00034.2017 · Cited by 462 · see citing works
Sympathetic and sensory innervation of brown adipose tissue
Bartness, T. J., Vaughan, C. H., & Song, C. K. (2010) · International Journal of Obesity · doi:10.1038/ijo.2010.182 · Cited by 459 · see citing works
Adipose tissue plasticity: how fat depots respond differently to pathophysiological cues
Pellegrinelli, V., Carobbio, S., & Vidal-Puig, A. (2016) · Diabetologia · doi:10.1007/s00125-016-3933-4 · Cited by 432 · see citing works
Leptin and Insulin Act on POMC Neurons to Promote the Browning of White Fat
Dodd, G. T., Decherf, S., Loh, K., Simonds, S. E., Wiede, F., Balland, E., Merry, T. L., Münzberg, H., Zhang, Z.-Y., Kahn, B. B., et al. (2015) · Cell · doi:10.1016/j.cell.2014.12.022 · Cited by 398 · see citing works
Mechanisms of Glucocorticoid-Induced Insulin Resistance
Geer, E. B., Islam, J., & Buettner, C. (2014) · Endocrinology and Metabolism Clinics of North America · doi:10.1016/j.ecl.2013.10.005 · Cited by 392 · see citing works
Transdifferentiation properties of adipocytes in the adipose organ
Cinti, S. (2009) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00183.2009 · Cited by 379 · see citing works
McKnight, J. R., Satterfield, M. C., Jobgen, W. S., Smith, S. B., Spencer, T. E., Meininger, C. J., McNeal, C. J., & Wu, G. (2010) · Amino Acids · doi:10.1007/s00726-010-0598-z · Cited by 376 · see citing works
Brown fat as a therapy for obesity and diabetes
Cypess, A. M., & Kahn, C. R. (2010) · Current Opinion in Endocrinology, Diabetes & Obesity · doi:10.1097/med.0b013e328337a81f · Cited by 376 · see citing works
Huh, J. Y., Mougios, V., Kabasakalis, A., Fatouros, I., Siopi, A., Douroudos, I. I., Filippaios, A., Panagiotou, G., Park, K. H., & Mantzoros, C. S. (2014) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2014-1437 · Cited by 363 · see citing works
Pten positively regulates brown adipose function, energy expenditure, and longevity
Ortega-Molina, A., Efeyan, A., Lopez-Guadamillas, E., Muñoz-Martin, M., Gómez-López, G., Cañamero, M., Mulero, F., Pastor, J., Martinez, S., Romanos, E., et al. (2012) · Cell Metabolism · doi:10.1016/j.cmet.2012.02.001 · Cited by 356 · see citing works
Adaptive thermogenesis in humans
Rosenbaum, M., & Leibel, R. L. (2010) · International Journal of Obesity · doi:10.1038/ijo.2010.184 · Cited by 349 · see citing works
Beige adipocyte maintenance is regulated by autophagy-induced mitochondrial clearance
Altshuler-Keylin, S., Shinoda, K., Hasegawa, Y., Ikeda, K., Hong, H., Kang, Q., Yang, Y., Perera, R. M., Debnath, J., & Kajimura, S. (2016) · Cell Metabolism · doi:10.1016/j.cmet.2016.08.002 · Cited by 349 · see citing works
Fitzgibbons, T. P., & Czech, M. P. (2014) · Journal of the American Heart Association · doi:10.1161/jaha.113.000582 · Cited by 331 · see citing works
Worthmann, A., John, C., Rühlemann, M. C., Baguhl, M., Heinsen, F.-A., Schaltenberg, N., Heine, M., Schlein, C., Evangelakos, I., Mineo, C., et al. (2017) · Nature Medicine · doi:10.1038/nm.4357 · Cited by 318 · see citing works
Origin and function of stress-induced IL-6 in murine models
Qing, H., Desrouleaux, R., Israni-Winger, K., Mineur, Y. S., Fogelman, N., Zhang, C., Rashed, S., Palm, N. W., Sinha, R., Picciotto, M. R., et al. (2020) · Cell · doi:10.1016/j.cell.2020.05.054 · Cited by 303 · see citing works
Yin, H., Pasut, A., Soleimani, V. D., Bentzinger, C. F., Antoun, G., Thorn, S., Seale, P., Fernando, P., van IJcken, W., Grosveld, F., et al. (2013) · Cell Metabolism · doi:10.1016/j.cmet.2013.01.004 · Cited by 293 · see citing works
Inter-organ cross-talk in metabolic syndrome
Priest, C., & Tontonoz, P. (2019) · Nature Metabolism · doi:10.1038/s42255-019-0145-5 · Cited by 279 · see citing works
Brown and beige fat: Molecular parts of a thermogenic machine
Cohen, P., & Spiegelman, B. M. (2015) · Diabetes · doi:10.2337/db15-0318 · Cited by 259 · see citing works
Wu, L., Zhang, L., Li, B., Jiang, H., Duan, Y., Xie, Z., Shuai, L., Li, J., & Li, J. (2018) · Frontiers in Physiology · doi:10.3389/fphys.2018.00122 · Cited by 255 · see citing works
Brown Adipose Tissue Responds to Cold and Adrenergic Stimulation by Induction of FGF21
Chartoumpekis, D. V., Habeos, I. G., Ziros, P. G., Psyrogiannis, A. I., Kyriazopoulou, V. E., & Papavassiliou, A. G. (2011) · Molecular Medicine · doi:10.2119/molmed.2011.00075 · Cited by 252 · see citing works
Human Multipotent Adipose-Derived Stem Cells Differentiate into Functional Brown Adipocytes
Elabd, C., Chiellini, C., Carmona, M., Galitzky, J., Cochet, O., Petersen, R., Pénicaud, L., Kristiansen, K., Bouloumié, A., Casteilla, L., et al. (2009) · Stem Cells · doi:10.1002/stem.200 · Cited by 252 · see citing works
Essential Role for miR-196a in Brown Adipogenesis of White Fat Progenitor Cells
Mori, M., Nakagami, H., Rodriguez-Araujo, G., Nimura, K., & Kaneda, Y. (2012) · PLoS Biology · doi:10.1371/journal.pbio.1001314 · Cited by 243 · see citing works
Mitochondrial fatty acid oxidation in obesity
Serra, D., Mera, P., Malandrino, M. I., Mir, J. F., & Herrero, L. (2013) · Antioxidants & Redox Signaling · doi:10.1089/ars.2012.4875 · Cited by 246 · see citing works
Neuronal control of peripheral insulin sensitivity and glucose metabolism
Ruud, J., Steculorum, S. M., & Brüning, J. C. (2017) · Nature Communications · doi:10.1038/ncomms15259 · Cited by 245 · see citing works
Skeletal muscle mitochondria as a target to prevent or treat type 2 diabetes mellitus
Hesselink, M. K. C., Schrauwen-Hinderling, V., & Schrauwen, P. (2016) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2016.104 · Cited by 242 · see citing works
Self-citationInduction of Adipose Tissue Browning as a Strategy to Combat Obesity
Kuryłowicz, A., & Puzianowska-Kuźnicka, M. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21176241 · Cited by 219 · see citing works
Tupone, D., Madden, C. J., Cano, G., & Morrison, S. F. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.3909-11.2011 · Cited by 228 · see citing works
Bertholet, A. M., Kazak, L., Chouchani, E. T., Bogaczyńska, M. G., Paranjpe, I., Wainwright, G. L., Bétourné, A., Kajimura, S., Spiegelman, B. M., & Kirichok, Y. (2017) · Cell Metabolism · doi:10.1016/j.cmet.2017.03.002 · Cited by 225 · see citing works
Human Brown Adipose Tissue: What We Have Learned So Far
Betz, M. J., & Enerbäck, S. (2015) · Diabetes · doi:10.2337/db15-0146 · Cited by 223 · see citing works
Paniagua, J. A. (2016) · World Journal of Diabetes · doi:10.4239/wjd.v7.i19.483 · Cited by 197 · see citing works
Postprandial Oxidative Metabolism of Human Brown Fat Indicates Thermogenesis
U Din, M., Saari, T., Raiko, J., Kudomi, N., Maurer, S. F., Lahesmaa, M., Fromme, T., Amri, E.-Z., Klingenspor, M., Solin, O., et al. (2018) · Cell Metabolism · doi:10.1016/j.cmet.2018.05.020 · Cited by 196 · see citing works
Low brown adipose tissue activity in endurance-trained compared with lean sedentary men
Vosselman, M. J., Hoeks, J., Brans, B., Pallubinsky, H., Nascimento, E. B. M., van der Lans, A. A. J. J., Broeders, E. P. M., Mottaghy, F. M., Schrauwen, P., & van Marken Lichtenbelt, W. D. (2015) · International Journal of Obesity · doi:10.1038/ijo.2015.130 · Cited by 193 · see citing works
Self-citationHypoxia and Adipocyte Physiology: Implications for Adipose Tissue Dysfunction in Obesity
Trayhurn, P. (2014) · Annual Review of Nutrition · doi:10.1146/annurev-nutr-071812-161156 · Cited by 194 · see citing works
Targeting fatty acid metabolism to improve glucose metabolism
Stinkens, R., Goossens, G. H., Jocken, J. W. E., & Blaak, E. E. (2015) · Obesity Reviews · doi:10.1111/obr.12298 · Cited by 183 · see citing works
Exercise-induced ’browning’ of adipose tissues
Aldiss, P., Betts, J., Sale, C., Pope, M., Budge, H., & Symonds, M. E. (2018) · Metabolism · doi:10.1016/j.metabol.2017.11.009 · Cited by 175 · see citing works
Brown adipose tissue: Development, metabolism and beyond
Schulz, T. J., & Tseng, Y.-H. (2013) · Biochemical Journal · doi:10.1042/bj20130457 · Cited by 173 · see citing works
Mitochondrial uncoupling and lifespan
Mookerjee, S. A., Divakaruni, A. S., Jastroch, M., & Brand, M. D. (2010) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2010.03.010 · Cited by 169 · see citing works
Adipose tissues and thyroid hormones
Obregon, M.-J. (2014) · Frontiers in Physiology · doi:10.3389/fphys.2014.00479 · Cited by 167 · see citing works
Ahmad, N. N., Pfalzer, A., & Kaplan, L. M. (2013) · International Journal of Obesity · doi:10.1038/ijo.2013.38 · Cited by 163 · see citing works
Evolutionary perspectives on the obesity epidemic: adaptive, maladaptive, and neutral viewpoints
Speakman, J. R. (2013) · Annual Review of Nutrition · doi:10.1146/annurev-nutr-071811-150711 · Cited by 163 · see citing works
Irisin as a muscle-derived hormone stimulating thermogenesis – A critical update
Hofmann, T., Elbelt, U., & Stengel, A. (2014) · Peptides · doi:10.1016/j.peptides.2014.01.016 · Cited by 162 · see citing works
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 · see citing works
The role of thyroid hormone and brown adipose tissue in energy homoeostasis
Bianco, A. C., & McAninch, E. A. (2013) · The Lancet Diabetes & Endocrinology · doi:10.1016/s2213-8587(13)70069-x · Cited by 154 · see citing works
Human and Mouse Brown Adipose Tissue Mitochondria Have Comparable UCP1 Function
Porter, C., Herndon, D. N., Chondronikola, M., Chao, T., Annamalai, P., Bhattarai, N., Saraf, M. K., Capek, K. D., Reidy, P. T., Daquinag, A. C., et al. (2016) · Cell Metabolism · doi:10.1016/j.cmet.2016.07.004 · Cited by 148 · see citing works
‘Browning’ the cardiac and peri-vascular adipose tissues to modulate cardiovascular risk
Aldiss, P., Davies, G., Woods, R., Budge, H., Sacks, H. S., & Symonds, M. E. (2017) · International Journal of Cardiology · doi:10.1016/j.ijcard.2016.11.074 · Cited by 148 · see citing works
Boucher, J., Mori, M. A., Lee, K. Y., Smyth, G., Liew, C. W., Macotela, Y., Rourk, M., Bluher, M., Russell, S. J., & Kahn, C. R. (2012) · Nature Communications · doi:10.1038/ncomms1905 · Cited by 142 · see citing works
Brown Adipose Tissue as a Regulator of Energy Expenditure and Body Fat in Humans
Saito, M. (2013) · Diabetes & Metabolism Journal · doi:10.4093/dmj.2013.37.1.22 · Cited by 146 · see citing works
Goldgof, M., Xiao, C., Chanturiya, T., Jou, W., Gavrilova, O., & Reitman, M. L. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.568204 · Cited by 138 · see citing works
Geerling, J. J., Boon, M. R., Kooijman, S., Parlevliet, E. T., Havekes, L. M., Romijn, J. A., Meurs, I. M., & Rensen, P. C. N. (2014) · Journal of Lipid Research · doi:10.1194/jlr.r045013 · Cited by 137 · see citing works
de Jong, J. M. A., Sun, W., Pires, N. D., Frontini, A., Balaz, M., Jespersen, N. Z., Feizi, A., Petrovic, K., Fischer, A. W., Bokhari, M. H., et al. (2019) · Nature Metabolism · doi:10.1038/s42255-019-0101-4 · Cited by 137 · see citing works
Jiang, Y., Berry, D. C., & Graff, J. M. (2017) · eLife · doi:10.7554/elife.30329 · Cited by 135 · see citing works
Psychogenic fever: how psychological stress affects body temperature in the clinical population
Oka, T. (2015) · Temperature · doi:10.1080/23328940.2015.1056907 · Cited by 127 · see citing works
A Functional Link between AMPK and Orexin Mediates the Effect of BMP8B on Energy Balance
Martins, L., Seoane-Collazo, P., Contreras, C., González-García, I., Martínez-Sánchez, N., González, F., Zalvide, J., Gallego, R., Diéguez, C., Nogueiras, R., et al. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.07.045 · Cited by 154 · see citing works
Brown Adipose Tissue: Mechanisms and Potential Therapeutic Targets
Tam, C. S., Lecoultre, V., & Ravussin, E. (2012) · Circulation · doi:10.1161/circulationaha.111.042929 · Cited by 116 · see citing works
Gamas, L., Matafome, P., & Seiça, R. (2015) · Journal of Diabetes Research · doi:10.1155/2015/359159 · Cited by 114 · see citing works
Reprogrammed marrow adipocytes contribute to myeloma-induced bone disease
Liu, H., He, J., Koh, S. P., Zhong, Y., Liu, Z., Wang, Z., Zhang, Y., Li, Z., Tam, B. T., Lin, P., et al. (2019) · Science Translational Medicine · doi:10.1126/scitranslmed.aau9087 · Cited by 113 · see citing works
Zhang, 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 · see citing works
Adaptive thermogenesis can make a difference in the ability of obese individuals to lose body weight
Tremblay, A., Royer, M.-M., Chaput, J.-P., & Doucet, É. (2013) · International Journal of Obesity · doi:10.1038/ijo.2012.124 · Cited by 108 · see citing works
Healthy excursions outside the thermal comfort zone
van Marken Lichtenbelt, W., Hanssen, M., Pallubinsky, H., Kingma, B., & Schellen, L. (2017) · Building Research & Information · doi:10.1080/09613218.2017.1307647 · Cited by 109 · see citing works
Self-citationHDAC11 suppresses the thermogenic program of adipose tissue via BRD2
Bagchi, R. A., Ferguson, B. S., Stratton, M. S., Hu, T., Cavasin, M. A., Sun, L., Lin, Y.-H., Liu, D., Londono, P., Song, K., et al. (2018) · JCI Insight · doi:10.1172/jci.insight.120159 · Cited by 110 · see citing works
Mechanisms of impaired brown adipose tissue recruitment in obesity
Alcalá, M., Calderon-Dominguez, M., Serra, D., Herrero, L., & Viana, M. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2019.00094 · Cited by 106 · see citing works
Pessentheiner, A. R., Pelzmann, H. J., Walenta, E., Schweiger, M., Groschner, L. N., Graier, W. F., Kolb, D., Uno, K., Miyazaki, T., Nitta, A., et al. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.491324 · Cited by 105 · see citing works
The influence of light on thermal responses
te Kulve, M., Schellen, L., Schlangen, L. J. M., & van Marken Lichtenbelt, W. D. (2016) · Acta Physiologica · doi:10.1111/apha.12552 · Cited by 105 · see citing works
Self-citationZhu, Y., Gao, Y., Tao, C., Shao, M., Zhao, S., Huang, W., Yao, T., Johnson, J. A., Liu, T., Cypess, A. M., et al. (2016) · Cell Metabolism · doi:10.1016/j.cmet.2016.08.005 · Cited by 100 · see citing works
Liu, X., Zhang, Z., Song, Y., Xie, H., & Dong, M. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.1065263 · Cited by 102 · see citing works
Okla, M., Zaher, W., Alfayez, M., & Chung, S. (2018) · Inflammation · doi:10.1007/s10753-017-0718-y · Cited by 96 · see citing works
Effects of exercise on brown and beige adipocytes
Dewal, R. S., & Stanford, K. I. (2019) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2018.04.013 · Cited by 92 · see citing works
- Authors
- 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.
- Affiliations
- Maastricht University (NL)
- Maastricht University Medical Centre (NL)
- Venue
- New England Journal of Medicine
- Publisher
- Massachusetts Medical Society
- Published
- 2009-04-09
- Volume
- 360
- Issue
- 15
- Pages
- 1500-1508
- ISSN
- 0028-4793 (ISSN-L)
- 1533-4406
- OpenAlex
- W2005827500
- Cited by
- 3,452
- References
- 25
- Citations by year
- 2026: 96 · 2025: 125 · 2024: 134 · 2023: 154 · 2022: 201 · 2021: 230 · 2020: 254 · 2019: 225 · 2018: 238 · 2017: 258 · 2016: 252 · 2015: 267 · 2014: 214 · 2013: 246 · 2012: 195
- FWCI
- 122.59
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- New England Journal of Medicine (publishedVersion)
- PubMed (publishedVersion)
- Research Publications (Maastricht University) (submittedVersion, other-oa)
- Topics
- Health Sciences › Medicine › Physiology › Adipose Tissue and Metabolism
- Health Sciences › Medicine › Epidemiology › Adipokines, Inflammation, and Metabolic Diseases
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiovascular Disease and Adiposity
- Keywords
- brown adipose tissue, cold exposure, thermogenesis, obesity, body composition, energy expenditure, resting metabolic rate, lean men, 18F-FDG PET, body fat percentage, obesity treatment
- MeSH terms
- Adolescent, Adult, Adipose Tissue, Brown, Cold Temperature, Energy Metabolism, Humans, Male, Obesity, Regression Analysis, Body Mass Index, Radiopharmaceuticals, Fluorodeoxyglucose F18, Positron-Emission Tomography, Adiposity, Overweight, Young Adult
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
