Emergence of brown adipocytes in white fat in mice is under genetic control. Effects on body weight and adiposity.
Open accessAbstract
The mRNA levels for the mitochondrial uncoupling protein (UCP1) in fat tissues of A/J and C57BL/6J inbred strains of mice varied in a regional-specific manner after stimulation of adrenergic signaling by cold exposure or treatment with a beta3-adrenergic agonist. While the differences between strains were minimal in interscapular brown fat, large differences occurred in white fat tissues, particularly in retroperitoneal fat. Among the AXB recombinant inbred strains, the Ucp1 mRNA levels varied up to 130-fold. This large induction at the mRNA level was accompanied by a corresponding increase in brown adipocytes as revealed by immunohistology with anti-UCP1 antibodies. A high capacity to induce brown fat in areas of traditional white fat had no impact on the ability to gain weight in response to high fat and sucrose diets, but did correlate with the loss of weight in response to treatment with a beta3-adrenergic agonist (CL 316,243). This genetic variation in mice provides an experimental approach to identify genes controlling the induction of brown adipocytes in white fat tissues.
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Induction of BAT in mice promotes energy expenditure, reduces adiposity, and protects mice from diet-induced obesity.
“Induction of BAT in mice promotes energy expenditure, reduces adiposity, and protects mice from diet-induced obesity 73,74.”
From Cellular bioenergetics as a target for obesity therapy (2010) · cites this paper as [74]
Systemic brown adipocytes are often found admixed with white fat cells; are more sensitive to β3-adrenergic stimulation and cold exposure; and their thermogenic capacity appears to be regulated by genetic background.
“These systemic brown adipocytes are often found admixed with white fat cells; are more sensitive to β3-adrenergic stimulation and cold exposure; and their thermogenic capacity appears to be regulated by genetic background 86,87,74.”
From Cellular bioenergetics as a target for obesity therapy (2010) · cites this paper as [74]
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Cites
Single-Step Method of RNA Isolation by Acid Guanidinium Thiocyanate–Phenol–Chloroform Extraction
Chomczynski, P., & Sacchi, N. (1987) · Analytical Biochemistry · doi:10.1006/abio.1987.9999 · Cited by 65,240 · see citing works
A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity
Feinberg, A. P., & Vogelstein, B. (1983) · Analytical Biochemistry · doi:10.1016/0003-2697(83)90418-9 · Cited by 24,512 · see citing works
A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity
(1984) · Analytical Biochemistry · doi:10.1016/0003-2697(84)90381-6 · Cited by 4,950 · see citing works
Uncoupling protein-2: a novel gene linked to obesity and hyperinsulinemia
Fleury, C., Neverova, M., Collins, S., Raimbault, S., Champigny, O., Lévi-Meyrueis, C., Bouillaud, F., Seldin, M. F., Surwit, R. S., Ricquier, D., et al. (1997) · Nature Genetics · doi:10.1038/ng0397-269 · Cited by 1,630 · see citing works
A role for brown adipose tissue in diet-induced thermogenesis
Rothwell, N. J., & Stock, M. J. (1979) · Nature · doi:10.1038/281031a0 · Cited by 1,606 · 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
Self-citationDiet-Induced Type II Diabetes in C57BL/6J Mice
Surwit, R. S., Kuhn, C. M., Cochrane, C., McCubbin, J. A., & Feinglos, M. N. (1988) · Diabetes · doi:10.2337/diab.37.9.1163 · Cited by 1,211 · see citing works
Boss, O., Samec, S., Paoloni‐Giacobino, A., Rossier, C., Dulloo, A. G., Seydoux, J., Muzzin, P., & Giacobino, J. (1997) · FEBS Letters · doi:10.1016/s0014-5793(97)00384-0 · Cited by 1,041 · see citing works
Gong, D., He, Y., Karas, M., & Reitman, M. L. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.39.24129 · Cited by 740 · see citing works
Smith, R. E., & Horwitz, B. A. (1969) · Physiological Reviews · doi:10.1152/physrev.1969.49.2.330 · Cited by 715 · see citing works
Vidal‐Puig, A., Solanes, G., Grujić, D., Flier, J. S., & Lowell, B. B. (1997) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1997.6740 · Cited by 711 · see citing works
Cousin, B., Cinti, S., Morroni, M., Raimbault, S., Ricquier, D., Pénicaud, L., & Casteilla, L. (1992) · Journal of Cell Science · doi:10.1242/jcs.103.4.931 · Cited by 665 · see citing works
Bailey, D. W. (1971) · Transplantation · doi:10.1097/00007890-197103000-00013 · Cited by 589 · see citing works
Kopecky, J., Clarke, G., Enerbäck, S., Spiegelman, B., & Kozak, L. P. (1995) · Journal of Clinical Investigation · doi:10.1172/jci118363 · Cited by 553 · see citing works
Self-citationTranscriptional control in the production of liver-specific mRNAs
Derman, E., Krauter, K. S., Walling, L. L., Weinberger, C., Ray, M., & Darnell, J. E., Jr. (1981) · Cell · doi:10.1016/0092-8674(81)90436-0 · Cited by 550 · see citing works
Tissue distribution of beta 3-adrenergic receptor mRNA in man
Krief, S., Lönnqvist, F., Raimbault, S., Baude, B., Van Spronsen, A., Arner, P., Strosberg, A. D., Ricquier, D., & Emorine, L. J. (1993) · Journal of Clinical Investigation · doi:10.1172/jci116191 · Cited by 528 · see citing works
Foster, D. O., & Frydman, M. L. (1979) · Canadian Journal of Physiology and Pharmacology · doi:10.1139/y79-039 · Cited by 518 · see citing works
Gimeno, R. E., Dembski, M., Weng, X., Deng, N., Shyjan, A. W., Gimeno, C. J., Iris, F., Ellis, S. J., Woolf, E. A., & Tartaglia, L. A. (1997) · Diabetes · doi:10.2337/diab.46.5.900 · Cited by 496 · see citing works
Targeted Disruption of the β3-Adrenergic Receptor Gene
Susulic, V. S., Frederich, R. C., Lawitts, J. A., Tozzo, E., Kahn, B. B., Harper, M., Himms‐Hagen, J., Flier, J. S., & Lowell, B. B. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.49.29483 · Cited by 493 · see citing works
Genetically lean mice result from targeted disruption of the RIIβ subunit of protein kinase A
Cummings, D. E., Brandon, E. P., Planas, J. V., Motamed, K., Idzerda, R. L., & McKnight, G. S. (1996) · Nature · doi:10.1038/382622a0 · Cited by 418 · see citing works
Himms‐Hagen, J., Cui, J. Z., Danforth, E., Taatjes, D. J., Lang, S. S., Waters, B. L., & Claus, T. H. (1994) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1994.266.4.r1371 · Cited by 382 · see citing works
Brown adipose tissue in the parametrial fat pad of the mouse
Young, P., Arch, J. R. S., & Ashwell, M. (1984) · FEBS Letters · doi:10.1016/0014-5793(84)80822-4 · Cited by 377 · see citing works
Festing, M. F. W. (1979) · doi:10.1007/978-1-349-03816-9_10 · Cited by 354 · see citing works
A Role for Brown Adipose Tissue in Diet‐Induced Thermogenesis
Rothwell, N. J., & Stock, M. J. (1997) · Obesity Research · doi:10.1002/j.1550-8528.1997.tb00591.x · Cited by 296 · see citing works
Strain-Specific Response toβ3-Adrenergic Receptor Agonist Treatment of Diet-Induced Obesity in Mice1
Collins, S., Daniel, K. W., Petro, A. E., & Surwit, R. S. (1997) · Endocrinology · doi:10.1210/endo.138.1.4829 · Cited by 265 · see citing works
Thermoregulatory and metabolic phenotypes of mice lacking noradrenaline and adrenaline
THOMAS, S. A., & Palmiter, R. D. (1997) · Nature · doi:10.1038/387094a0 · Cited by 258 · see citing works
Ghorbani, M., & Himms‐Hagen, J. (1997) · International Journal of Obesity · doi:10.1038/sj.ijo.0800432 · Cited by 250 · see citing works
Diet-induced type II diabetes in C57BL/6J mice
Surwit, R. S., Kuhn, C. M., Cochrane, C., et al. (1988) · Diabetes · doi:10.2337/diabetes.37.9.1163 · Cited by 229 · see citing works
Nagase, I., Yoshida, T., Kumamoto, K., UMEKAWA, T., Sakane, N., Nikami, H., Kawada, T., & Saito, M. (1996) · Journal of Clinical Investigation · doi:10.1172/jci118748 · Cited by 207 · see citing works
Ghorbani, M., Claus, T. H., & Himms-Hagen, J. (1997) · Biochemical Pharmacology · doi:10.1016/s0006-2952(97)00162-7 · Cited by 195 · see citing works
Bronnikov, G. E., Houštěk, J., & Nedergaard, J. (1992) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)46046-2 · Cited by 193 · see citing works
Tai, T.-A. C., Jennermann, C., Brown, K. K., Oliver, B. B., MacGinnitie, M. A., Wilkison, W. O., Brown, H. R., Lehmann, J. M., Kliewer, S. A., Morris, D. C., et al. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.47.29909 · Cited by 154 · see citing works
Champigny, O., Ricquier, D., Blondel, O., Mayers, R. M., BRISCOE, M. G., & Holloway, B. R. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.23.10774 · Cited by 137 · see citing works
Reduction of dietary obesity in aP2-Ucp transgenic mice: physiology and adipose tissue distribution
Kopecký, J., Hodný, Z., Rossmeisl, M., Syrový, I., & Kozak, L. P. (1996) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1996.270.5.e768 · Cited by 136 · see citing works
Self-citationBukowiecki, L. J., Géloën, A., & Collet, A. (1986) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.1986.250.6.c880 · Cited by 135 · see citing works
Surwit, R. S., Seldin, M. F., Kuhn, C. M., Cochrane, C., & Feinglos, M. N. (1991) · Diabetes · doi:10.2337/diab.40.1.82 · Cited by 131 · see citing works
The mitochondrial uncoupling protein gene. Correlation of exon structure to transmembrane domains.
Kozak, L. P., Britton, J. H., Kozak, U. C., & Wells, J. M. (1988) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)37751-2 · Cited by 121 · see citing works
Self-citationEpididymal white adipose tissue after cold stress in rats II. Mitochondrial changes
Lonćar, D., Afzelius, B. A., & Cannon, B. (1988) · Journal of Ultrastructure and Molecular Structure Research · doi:10.1016/0889-1605(88)90010-9 · Cited by 111 · see citing works
Transgenic Mice Overexpressing the β1-Adrenergic Receptor in Adipose Tissue Are Resistant to Obesity
Soloveva, V., Graves, R. A., Rasenick, M. M., Spiegelman, B. M., & Ross, S. R. (1997) · Molecular Endocrinology · doi:10.1210/mend.11.1.9870 · Cited by 109 · see citing works
Gimeno, R. E., Dembski, M., Weng, X., et al. (1997) · Diabetes · doi:10.2337/diabetes.46.5.900 · Cited by 98 · see citing works
Genetic Variants and Strains of the Laboratory Mouse
Deol, M. S. (1983) · Journal of Medical Genetics · doi:10.1136/jmg.20.4.317 · Cited by 82 · see citing works
Epididymal white adipose tissue after cold stress in rats I. Nonmitochondrial changes
Lonćar, D., Afzelius, B. A., & Cannon, B. (1988) · Journal of Ultrastructure and Molecular Structure Research · doi:10.1016/0889-1605(88)90001-8 · Cited by 80 · see citing works
Champigny, O., & Ricquier, D. (1996) · Journal of Lipid Research · doi:10.1016/s0022-2275(20)37555-6 · Cited by 52 · see citing works
Strain-Specific Response to 3-Adrenergic Receptor Agonist Treatment of Diet-Induced Obesity in Mice
Collins, S. (1997) · Endocrinology · doi:10.1210/en.138.1.405 · Cited by 47 · see citing works
Transgenic Mice Overexpressing the 1-Adrenergic Receptor in Adipose Tissue Are Resistant to Obesity
Soloveva, V. (1997) · Molecular Endocrinology · doi:10.1210/me.11.1.27 · Cited by 36 · see citing works
Surwit, R. S., Seldin, M. F., Kuhn, C. M., et al. (1991) · Diabetes · doi:10.2337/diabetes.40.1.82 · Cited by 35 · see citing works
Genetic mapping and embryonic expression of a novel, maternally transcribed gene Mem3
Hwang, S.-Y., Benjamin, L. E., Oh, B., Rothstein, J. L., Ackerman, S. L., Beddington, R. S. P., Solter, D., & Knowles, B. B. (1996) · Mammalian Genome · doi:10.1007/s003359900174 · Cited by 22 · see citing works
Broadhurst, P. L. (1978) · Springer eBooks · doi:10.1007/978-1-4613-3979-3_8 · Cited by 14 · see citing works
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Brown Adipose Tissue: Function and Physiological Significance
CANNON, B., & NEDERGAARD, J. (2004) · Physiological Reviews · doi:10.1152/physrev.00015.2003 · Cited by 6,433 · 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
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
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
High Incidence of Metabolically Active Brown Adipose Tissue in Healthy Adult Humans
Saito, M., Okamatsu-Ogura, Y., Matsushita, M., Watanabe, K., Yoneshiro, T., Nio-Kobayashi, J., Iwanaga, T., Miyagawa, M., Kameya, T., Nakada, K., et al. (2009) · Diabetes · doi:10.2337/db09-0530 · Cited by 1,848 · 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
Chait, A., & den Hartigh, L. J. (2020) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2020.00022 · Cited by 1,529 · see citing works
Molecular Regulation of Adipogenesis
Rosen, E. D., & Spiegelman, B. M. (2000) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.16.1.145 · Cited by 1,287 · 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
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
Klaman, L. D., Boss, O., Peroni, O. D., Kim, J. K., Martino, J. L., Zabolotny, J. M., Moghal, N., Lubkin, M., Kim, Y.-B., Sharpe, A. H., et al. (2000) · Molecular and Cellular Biology · doi:10.1128/mcb.20.15.5479-5489.2000 · Cited by 1,235 · 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
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
Brown and Beige Fat: Physiological Roles beyond Heat Generation
Kajimura, S., Spiegelman, B. M., & Seale, P. (2015) · Cell Metabolism · doi:10.1016/j.cmet.2015.09.007 · Cited by 1,004 · 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
Gut Microbiota Orchestrates Energy Homeostasis during Cold
Chevalier, C., Stojanović, O., Colin, D. J., Suarez-Zamorano, N., Tarallo, V., Veyrat-Durebex, C., Rigo, D., Fabbiano, S., Stevanović, A., Hagemann, S., et al. (2015) · Cell · doi:10.1016/j.cell.2015.11.004 · 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
Bi-directional interconversion of brite and white adipocytes
Rosenwald, M., Perdikari, A., Rülicke, T., & Wolfrum, C. (2013) · Nature Cell Biology · doi:10.1038/ncb2740 · Cited by 792 · see citing works
Barbatelli, G., Murano, I., Madsen, L., Hao, Q., Jimenez, M., Kristiansen, K., Giacobino, J., Matteis, R. D., & Cinti, S. (2010) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00600.2009 · Cited by 751 · see citing works
Protection from obesity and diabetes by blockade of TGF-β/smad3 signaling
Yadav, H., Quijano, C., Kamaraju, A. K., Gavrilova, O., Malek, R., Chen, W., Zerfas, P., Zhigang, D., Wright, E. C., Stuelten, C., et al. (2011) · Cell Metabolism · doi:10.1016/j.cmet.2011.04.013 · Cited by 709 · see citing works
Control of brown and beige fat development
Wang, W., & Seale, P. (2016) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm.2016.96 · Cited by 697 · see citing works
Adipose tissue in control of metabolism
Luo, L., & Liu, M. (2016) · Journal of Endocrinology · doi:10.1530/joe-16-0211 · Cited by 707 · see citing works
Cinti, S. (2005) · Prostaglandins Leukotrienes and Essential Fatty Acids · doi:10.1016/j.plefa.2005.04.010 · Cited by 690 · see citing works
Brown adipose tissue as a secretory organ
Villarroya, F., Cereijo, R., Villarroya, J., & Giralt, M. (2016) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2016.136 · Cited by 677 · 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
Ikeda, K., Kang, Q., Yoneshiro, T., Camporez, J. P., Maki, H., Homma, M., Shinoda, K., Chen, Y., Lü, X., Maretich, P., et al. (2017) · Nature Medicine · doi:10.1038/nm.4429 · Cited by 655 · see citing works
Multilocular fat cells in WAT of CL-316243-treated rats derive directly from white adipocytes
Himms-Hagen, J., Melnyk, A., Zingaretti, M. C., Ceresi, E., Barbatelli, G., & Cinti, S. (2000) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.2000.279.3.c670 · Cited by 593 · 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
Recruited vs. nonrecruited molecular signatures of brown, “brite,” and white adipose tissues
Waldén, T. B., Hansen, I. R., Timmons, J. A., Cannon, B., & Nedergaard, J. (2011) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00249.2011 · Cited by 565 · see citing works
White, Brown, Beige/Brite: Different Adipose Cells for Different Functions?
Giralt, M., & Villarroya, F. (2013) · Endocrinology · doi:10.1210/en.2013-1403 · Cited by 556 · see citing works
Collins, S., Martin, T. L., Surwit, R. S., & Robidoux, J. (2004) · Physiology & Behavior · doi:10.1016/j.physbeh.2004.02.006 · Cited by 486 · 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
Self-citationMitochondrial dysfunction in obesity
Bournat, J. C., & Brown, C. (2010) · Current Opinion in Endocrinology Diabetes and Obesity · doi:10.1097/med.0b013e32833c3026 · Cited by 471 · 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
The adipose organ of obesity-prone C57BL/6J mice is composed of mixed white and brown adipocytes
Vitali, A., Murano, I., Zingaretti, M. C., Frontini, A., Ricquier, D., & Cinti, S. (2012) · Journal of Lipid Research · doi:10.1194/jlr.m018846 · Cited by 461 · see citing works
Identification of inducible brown adipocyte progenitors residing in skeletal muscle and white fat
Schulz, T. J., Huang, T. L., Tran, T. T., Zhang, H., Townsend, K. L., Shadrach, J. L., Cerletti, M., McDougall, L. E., Giorgadze, N., Tchkonia, T., et al. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1010929108 · Cited by 459 · see citing works
Cyclooxygenase-2 Controls Energy Homeostasis in Mice by de Novo Recruitment of Brown Adipocytes
Vegiopoulos, A., Müller‐Decker, K., Strzoda, D., Schmitt, I. M., Chichelnitskiy, E., Ostertag, A., Díaz, M. B., Rozman, J., de Angelis, M. H., Nüsing, R. M., et al. (2010) · Science · doi:10.1126/science.1186034 · Cited by 459 · see citing works
Berberine activates thermogenesis in white and brown adipose tissue
Zhang, Z., Zhang, H., Li, B., Meng, X.-J., Wang, J., Zhang, Y., Yao, S., Ma, Q., Jin, L., Yang, J., et al. (2014) · Nature Communications · doi:10.1038/ncomms6493 · Cited by 439 · see citing works
Kajimura, S., & Saito, M. (2013) · Annual Review of Physiology · doi:10.1146/annurev-physiol-021113-170252 · Cited by 428 · see citing works
Adipose tissue reduction in mice lacking the translational inhibitor 4E-BP1
Tsukiyama–Kohara, K., Poulin, F., Kohara, M., DeMaria, C. T., Cheng, A., Wu, Z., Gingras, A., Katsume, A., Elchebly, M., Spiegelman, B. M., et al. (2001) · Nature Medicine · doi:10.1038/nm1001-1128 · Cited by 392 · see citing works
Cao, L., Choi, E., Liu, X., Martin, A. S., Wang, C., Xu, X., & During, M. J. (2011) · Cell Metabolism · doi:10.1016/j.cmet.2011.06.020 · Cited by 380 · see citing works
Gong, D., Monemdjou, S., Gavrilova, O., Leon, L. R., Marcus‐Samuels, B., Chou, C. J., Everett, C. A., Kozak, L. P., Li, C., Deng, C., et al. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m910177199 · Cited by 385 · see citing works
Self-citationBrown-fat paucity due to impaired BMP signalling induces compensatory browning of white fat
Schulz, T. J., Huang, P. C., Huang, T. L., Xue, R., McDougall, L. E., Townsend, K. L., Cypess, A. M., Mishina, Y. M., Gussoni, E., & Tseng, Y. (2013) · Nature · doi:10.1038/nature11943 · Cited by 378 · 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
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
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
Targeting thermogenesis in brown fat and muscle to treat obesity and metabolic disease
Betz, M. J., & Enerbäck, S. (2017) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2017.132 · Cited by 355 · see citing works
Cinti, S. (2012) · Disease Models & Mechanisms · doi:10.1242/dmm.009662 · Cited by 350 · 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
TRPV4 Is a Regulator of Adipose Oxidative Metabolism, Inflammation, and Energy Homeostasis
Li, Y., Kleiner, S., Wu, J., Sah, R., Gupta, R. K., Banks, A. S., Cohen, P., Khandekar, M. J., Boström, P., Mepani, R. J., et al. (2012) · Cell · doi:10.1016/j.cell.2012.08.034 · Cited by 340 · see citing works
Sarjeant, K., & Stephens, J. M. (2012) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a008417 · Cited by 328 · see citing works
Implications of nonshivering thermogenesis for energy balance regulation in humans
Lichtenbelt, W. D. V. M., & Schrauwen, P. (2011) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00652.2010 · Cited by 306 · see citing works
Granneman, J. G., Li, P., Zhu, Z., & Lu, Y. (2005) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00009.2005 · Cited by 298 · see citing works
Hondares, E., Rosell, M., Díaz-Delfín, J., Olmos, Y., Monsalve, M., Iglesias, R., Villarroya, F., & Giralt, M. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.252775 · Cited by 295 · see citing works
Caloric Restriction Leads to Browning of White Adipose Tissue through Type 2 Immune Signaling
Fabbiano, S., Suárez-Zamorano, N., Rigo, D., Veyrat‐Durebex, C., Đokić, A., Colin, D., & Trajkovski, M. (2016) · Cell Metabolism · doi:10.1016/j.cmet.2016.07.023 · Cited by 291 · see citing works
Xue, R., Lynes, M. D., Dreyfuss, J. M., Shamsi, F., Schulz, T. J., Zhang, H., Huang, T. L., Townsend, K. L., Li, Y., Takahashi, H., et al. (2015) · Nature Medicine · doi:10.1038/nm.3881 · Cited by 292 · see citing works
Almind, K., Manieri, M., Sivitz, W. I., Cinti, S., & Kahn, C. R. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0610416104 · Cited by 286 · see citing works
Xue, B., Rim, J.-S., Hogan, J. C., Coulter, A. A., Koza, R. A., & Kozak, L. P. (2007) · Journal of Lipid Research · doi:10.1194/jlr.m600287-jlr200 · Cited by 288 · see citing works
Self-citationUCP1-independent Thermogenesis in White Adipose Tissue of Cold-acclimated Ucp1 -/- Mice
Ukropec, J., Anunciado, R. V. P., Ravussin, Y., Hulver, M. W., & Kozak, L. P. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m606114200 · Cited by 284 · see citing works
Self-citationBrown adipose tissue: physiological function and evolutionary significance
Oelkrug, R., Polymeropoulos, E. T., & Jastroch, M. (2015) · Journal of Comparative Physiology B · doi:10.1007/s00360-015-0907-7 · Cited by 283 · see citing works
CD81 controls beige fat progenitor cell growth and energy balance via FAK signaling
Oguri, Y., Shinoda, K., Kim, H., Alba, D. L., Bolus, W. R., Wang, Q., Brown, Z., Pradhan, R., Tajima, K., Yoneshiro, T., et al. (2020) · Cell · doi:10.1016/j.cell.2020.06.021 · Cited by 250 · see citing works
Cellular origins of cold‐induced brown adipocytes in adult mice
Lee, Y., Petkova, A. P., Konkar, A. A., & Granneman, J. G. (2014) · The FASEB Journal · doi:10.1096/fj.14-263038 · Cited by 278 · see citing works
O-GlcNAc Transferase Enables AgRP Neurons to Suppress Browning of White Fat
Ruan, H.-B., Dietrich, M. O., Liu, Z.-W., Zimmer, M. R., Li, M.-D., Singh, J. P., Zhang, K., Yin, R., Wu, J., Horvath, T. L., et al. (2014) · Cell · doi:10.1016/j.cell.2014.09.010 · Cited by 281 · see citing works
Paradoxical resistance to diet-induced obesity in UCP1-deficient mice
Liu, X., Rossmeisl, M., McClaine, J. W., & Kozak, L. P. (2003) · Journal of Clinical Investigation · doi:10.1172/jci200315737 · Cited by 281 · see citing works
Self-citationPharmacological and nutritional agents promoting browning of white adipose tissue
Bonet, M. L., Oliver, P., & Palou, A. (2012) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2012.12.002 · Cited by 276 · see citing works
Distinction of white, beige and brown adipocytes derived from mesenchymal stem cells
Park, A. (2014) · World Journal of Stem Cells · doi:10.4252/wjsc.v6.i1.33 · Cited by 274 · see citing works
Yoneshiro, T., Aita, S., Kawai, Y., Iwanaga, T., & Saito, M. (2012) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.111.018606 · Cited by 271 · see citing works
Paradoxical resistance to diet-induced obesity in UCP1-deficient mice
Liu, X., Rossmeisl, M., McClaine, J. W., & Kozak, L. P. (2003) · Journal of Clinical Investigation · doi:10.1172/jci15737 · Cited by 265 · see citing works
Self-citationMyomiR-133 regulates brown fat differentiation through Prdm16
Trajkovski, M., Ahmed, K., Esau, C., & Stoffel, M. (2012) · Nature Cell Biology · doi:10.1038/ncb2612 · Cited by 263 · see citing works
UCP1 mRNA does not produce heat
Nedergaard, J., & Cannon, B. (2013) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2013.01.009 · Cited by 264 · 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
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
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
Brown Fat and the Myth of Diet-Induced Thermogenesis
Kozak, L. P. (2010) · Cell Metabolism · doi:10.1016/j.cmet.2010.03.009 · Cited by 243 · see citing works
Self-citationNAG-1/GDF-15 prevents obesity by increasing thermogenesis, lipolysis and oxidative metabolism
Chrysovergis, K., Wang, X., Kosak, J., Lee, S.-H., Kim, J. S., Foley, J. F., Travlos, G., Singh, S., Baek, S. J., & Eling, T. E. (2014) · International Journal of Obesity · doi:10.1038/ijo.2014.27 · Cited by 241 · see citing works
The Adipose Tissue Phenotype of Hormone‐Sensitive Lipase Deficiency in Mice
Wang, S. P., Laurin, N., Himms‐Hagen, J., Rudnicki, M. A., Levy, E. H., Robert, M., Pan, L., Oligny, L. L., & Mitchell, G. A. (2001) · Obesity Research · doi:10.1038/oby.2001.15 · Cited by 236 · see citing works
The adipose organ: morphological perspectives of adipose tissues
Cinti, S. (2001) · Proceedings of The Nutrition Society · doi:10.1079/pns200192 · Cited by 228 · see citing works
Induction 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
Brown adipose tissue and thermogenesis
Fenzl, A., & Kiefer, F. W. (2014) · Hormone Molecular Biology and Clinical Investigation · doi:10.1515/hmbci-2014-0022 · Cited by 227 · 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
Ebf2 is a selective marker of brown and beige adipogenic precursor cells
Wang, W., Kissig, M., Rajakumari, S., Huang, L., Lim, H., Won, K., & Seale, P. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1412685111 · Cited by 222 · see citing works
Lipid signaling in adipose tissue: Connecting inflammation & metabolism
Masoodi, M., Kuda, O., Rossmeisl, M., Flachs, P., & Kopecký, J. (2014) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2014.09.023 · Cited by 218 · see citing works
White-to-brown transdifferentiation of omental adipocytes in patients affected by pheochromocytoma
Frontini, A., Vitali, A., Perugini, J., Murano, I., Romiti, C., Ricquier, D., Guerrieri, M., & Cinti, S. (2013) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2013.02.005 · Cited by 211 · see citing works
Adipocyte differentiation and transdifferentiation: plasticity of the adipose organ.
Cinti, S. (2002) · Journal of Endocrinological Investigation · doi:10.1007/bf03344046 · Cited by 213 · see citing works
Retinaldehyde dehydrogenase 1 regulates a thermogenic program in white adipose tissue
Kiefer, F. W., Vernochet, C., O’Brien, P., Spoerl, S., Brown, J. D., Nallamshetty, S., Zeyda, M., Stulnig, T. M., Cohen, D. E., Kahn, C. R., et al. (2012) · Nature Medicine · doi:10.1038/nm.2757 · Cited by 210 · see citing works
Browning of white fat: agents and implications for beige adipose tissue to type 2 diabetes
Kaisanlahti, A., & Glumoff, T. (2018) · Journal of Physiology and Biochemistry · doi:10.1007/s13105-018-0658-5 · Cited by 213 · see citing works
Dong, J., Dong, Y., Dong, Y., Chen, F., Mitch, W. E., & Zhang, L. (2016) · International Journal of Obesity · doi:10.1038/ijo.2015.200 · Cited by 212 · see citing works
Brown adipose tissue activity as a target for the treatment of obesity/insulin resistance
Poher, A.-L., Altirriba, J., Veyrat‐Durebex, C., & Rohner‐Jeanrenaud, F. (2015) · Frontiers in Physiology · doi:10.3389/fphys.2015.00004 · Cited by 213 · see citing works
Murano, I., Barbatelli, G., Giordano, A., & Cinti, S. (2009) · Journal of Anatomy · doi:10.1111/j.1469-7580.2008.01001.x · Cited by 208 · see citing works
Brown Adipose Tissue in Adult Humans: A Metabolic Renaissance
Lee, P. C., Swarbrick, M. M., & Ho, K. K. Y. (2013) · Endocrine Reviews · doi:10.1210/er.2012-1081 · Cited by 207 · see citing works
Han, J. S., Meng, Q., Shen, L., & Wu, G. (2018) · Lipids in Health and Disease · doi:10.1186/s12944-018-0657-0 · Cited by 207 · see citing works
The brown fat secretome: metabolic functions beyond thermogenesis
Wang, G.-X., Zhao, X.-Y., & Lin, J. D. (2015) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2015.03.002 · Cited by 206 · see citing works
Madsen, L., Pedersen, L. M., Lillefosse, H. H., Fjære, E., Brønstad, I., Hao, Q., Petersen, R. K., Hallenborg, P., Ma, T., Matteis, R. D., et al. (2010) · PLoS ONE · doi:10.1371/journal.pone.0011391 · Cited by 195 · see citing works
Uncoupling protein 1 expression and high-fat diets
Fromme, T., & Klingenspor, M. (2010) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00411.2010 · Cited by 200 · see citing works
Browning of white adipose tissue: lessons from experimental models
Bargut, T. C. L., Souza‐Mello, V., Águila, M. B., & Mandarim‐de‐Lacerda, C. A. (2017) · Hormone Molecular Biology and Clinical Investigation · doi:10.1515/hmbci-2016-0051 · Cited by 200 · see citing works
IGF1 Shapes Macrophage Activation in Response to Immunometabolic Challenge
Spadaro, O., Camell, C. D., Bosurgi, L., Nguyen, K., Youm, Y., Rothlin, C. V., & Dixit, V. D. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.03.046 · Cited by 196 · see citing works
Scimè, A., Grenier, G., Huh, M. S., Gillespie, M. A., Bevilacqua, L., Harper, M.-E., & Rudnicki, M. A. (2005) · Cell Metabolism · doi:10.1016/j.cmet.2005.10.002 · Cited by 199 · see citing works
UCP1: its involvement and utility in obesity
Kozak, L. P., & Anunciado‐Koza, R. P. (2008) · International Journal of Obesity · doi:10.1038/ijo.2008.236 · Cited by 200 · see citing works
Self-citation
- Authors
- Guerra, C., Koza, R. A., Yamashita, H., Walsh, K., & Kozak, L. P.
- Affiliations
- Jackson Laboratory (US)
- Venue
- Journal of Clinical Investigation
- Published
- 1998-07-15
- Volume
- 102
- Issue
- 2
- Pages
- 412-420
- ISSN
- 0021-9738 (ISSN-L)
- PMC
- PMC508900
- OpenAlex
- W2025530025
- Cited by
- 635
- References
- 45
- Citations by year
- 2026: 5 · 2025: 7 · 2024: 6 · 2023: 12 · 2022: 19 · 2021: 28 · 2020: 25 · 2019: 36 · 2018: 38 · 2017: 43 · 2016: 43 · 2015: 52 · 2014: 51 · 2013: 53 · 2012: 37
- FWCI
- 5.33
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Clinical Investigation (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- The Mouseion at the JAXlibrary (Jackson Laboratory) (submittedVersion)
- Topics
- Health Sciences › Medicine › Physiology › Adipose Tissue and Metabolism
- Health Sciences › Medicine › Epidemiology › Adipokines, Inflammation, and Metabolic Diseases
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Peroxisome Proliferator-Activated Receptors
- Keywords
- brown adipocytes, white adipose tissue, UCP1, mitochondrial uncoupling proteins, genetic variation, inbred mouse strains, recombinant inbred lines, beta3-adrenergic agonists, CL316,243, cold exposure, adrenergic signaling, retroperitoneal fat, interscapular brown fat, weight gain, high-fat diet, adiposity
- MeSH terms
- Uncoupling Protein 1, Animals, Body Weight, Adipose Tissue, Brown, Carrier Proteins, Cell Differentiation, Gene Expression Regulation, Ion Channels, Male, Membrane Proteins, Mice, Inbred C57BL, Obesity, RNA, Messenger, Adipocytes, Mitochondrial Proteins, Mice
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