MicroRNAs in brown and beige fat
Abstract
Brown adipose tissue (BAT) dissipates energy as heat and its activity correlates with leanness in human adults. Understanding the mechanisms behind the activation of BAT and the process of "browning", i.e. the appearance of inducible brown adipocytes called beige or brite (brown-in-white) cells in white adipose tissue (WAT), is of great interest for developing novel therapies to combat obesity. MicroRNAs (miRNAs) are small transcriptional regulators that control gene expression in a variety of tissues, including WAT and BAT. Recently, miRNAs were reported to regulate browning. Nevertheless, further studies are needed to fully understand the miRNA networks that are involved in the control of brown and beige/brite adipocytes. Particularly, most miRNAs have so far been studied in mice, underlining the importance of additional human studies. In this review, we focus on the regulation of brown fat by miRNAs including their role in promoting or inhibiting the browning process. In recent years, RNA-based therapeutical approaches have entered clinical trials for treatment of other diseases, thus miRNAs could potentially be used to enhance brown and beige fat mass and activity as novel therapies against overweight and its complications.
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White adipose tissue functions as an important endocrine organ regulating metabolism through releasing adipokines, in addition to energy storage and adaptive thermogenesis.
“Presently, it is acknowledged that white adipose tissue (WAT) not only has functions in energy storage and adaptive thermogenesis but also serves as an important endocrine organ, regulating metabolism through releasing adipokines [73].”
From Exerkines and Sarcopenia: Unveiling the Mechanism Behind Exercise-Induced Mitochondrial Homeostasis (2025) · cites this paper as [73]
Cites
Ng, M., Fleming, T., Robinson, M., Thomson, B., Graetz, N., Margono, C., Mullany, E. C., Biryukov, S., Abbafati, C., Abera, S. F., et al. (2014) · The Lancet · doi:10.1016/s0140-6736(14)60460-8 · Cited by 11,952 · see citing works
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
Grundy, S. M., Brewer, H. B., Cleeman, J. I., Smith, S. C., & Lenfant, C. (2004) · Circulation · doi:10.1161/01.cir.0000111245.75752.c6 · Cited by 5,982 · see citing works
Regulation of microRNA biogenesis
Ha, M., & Kim, V. N. (2014) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3838 · Cited by 5,462 · see citing works
(2008) · doi:10.1038/nrg2290 · Cited by 5,199 · see citing works
A PGC1-α-dependent myokine that drives brown-fat-like development of white fat and thermogenesis
Boström, P., Wu, J., Jedrychowski, M. P., Korde, A., Ye, L., Lo, J. C., Rasbach, K. A., Boström, E. A., Choi, J. H., Long, J. Z., et al. (2012) · Nature · doi:10.1038/nature10777 · Cited by 4,810 · see citing works
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
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
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
Processing of primary microRNAs by the Microprocessor complex
Denli, A. M., Tops, B. B. J., Plasterk, R. H. A., Ketting, R. F., & Hannon, G. J. (2004) · Nature · doi:10.1038/nature03049 · Cited by 2,784 · see citing works
An Extensive Class of Small RNAs in <i>Caenorhabditis elegans</i>
Lee, R. C., & Ambros, V. (2001) · Science · doi:10.1126/science.1065329 · Cited by 2,358 · 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
Gene silencing by microRNAs: contributions of translational repression and mRNA decay
Huntzinger, E., & Izaurralde, E. (2011) · Nature Reviews Genetics · doi:10.1038/nrg2936 · Cited by 2,339 · 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
Exosome and Exosomal MicroRNA: Trafficking, Sorting, and Function
Zhang, J., Li, S., Li, L., Li, M., Guo, C., Yao, J., & Mi, S. (2015) · Genomics Proteomics & Bioinformatics · doi:10.1016/j.gpb.2015.02.001 · Cited by 2,189 · 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
Adipose-derived circulating miRNAs regulate gene expression in other tissues
Thomou, T., Mori, M. A., Dreyfuss, J. M., Konishi, M., Sakaguchi, M., Wolfrum, C., Rao, T. N., Winnay, J. N., Garcia-Martin, R., Grinspoon, S. K., et al. (2017) · Nature · doi:10.1038/nature21365 · Cited by 1,539 · see citing works
FGF21 regulates PGC-1α and browning of white adipose tissues in adaptive thermogenesis
Fisher, F. M., Kleiner, S., Douris, N., Fox, E. C., Mepani, R. J., Verdeguer, F., Wu, J., Kharitonenkov, A., Flier, J. S., Maratos-Flier, E., et al. (2012) · Genes & Development · doi:10.1101/gad.177857.111 · Cited by 1,478 · see citing works
Plasma MicroRNA Profiling Reveals Loss of Endothelial MiR-126 and Other MicroRNAs in Type 2 Diabetes
Zampetaki, A., Kiechl, S. J., Drozdov, I. A., Willeit, P., Mayr, U., Prokopi, M., Mayr, A., Weger, S., Oberhollenzer, F., Bonora, E., et al. (2010) · Circulation Research · doi:10.1161/circresaha.110.226357 · Cited by 1,457 · see citing works
Tracking adipogenesis during white adipose tissue development, expansion and regeneration
Wang, Q. A., Tao, C., Gupta, R. K., & Scherer, P. E. (2013) · Nature Medicine · doi:10.1038/nm.3324 · Cited by 1,262 · see citing works
Quantitative and stoichiometric analysis of the microRNA content of exosomes
Chevillet, J. R., Kang, Q., Ruf, I. K., Briggs, H., Vojtech, L. N., Hughes, S. M., Cheng, H. H., Arroyo, J. D., Meredith, E. K., Gallichotte, E. N., et al. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1408301111 · Cited by 1,105 · see citing works
New role of bone morphogenetic protein 7 in brown adipogenesis and energy expenditure
Tseng, Y.-H., Kokkotou, E., Schulz, T. J., Huang, T. L., Winnay, J. N., Taniguchi, C. M., Tran, T. T., Suzuki, R., Espinoza, D. O., Yamamoto, Y., et al. (2008) · Nature · doi:10.1038/nature07221 · Cited by 1,099 · see citing works
Bray, G. A., Frühbeck, G., Ryan, D. H., & Wilding, J. P. H. (2016) · The Lancet · doi:10.1016/s0140-6736(16)00271-3 · Cited by 1,036 · 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
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
Foster, D. O., & Frydman, M. L. (1978) · Canadian Journal of Physiology and Pharmacology · doi:10.1139/y78-015 · Cited by 652 · see citing works
Mammalian Cyclic Nucleotide Phosphodiesterases: Molecular Mechanisms and Physiological Functions
Francis, S. H., Blount, M. A., & Corbin, J. D. (2011) · Physiological Reviews · doi:10.1152/physrev.00030.2010 · Cited by 644 · see citing works
The distribution of brown adipose tissue in the human.
Heaton, J. M. (1972) · PubMed · Cited by 606 · see citing works
The microRNA miR-181 targets the homeobox protein Hox-A11 during mammalian myoblast differentiation
Naguibneva, I., Ameyar‐Zazoua, M., Polesskaya, A., Ait‐Si‐Ali, S., Groisman, R., Souidi, M., Cuvellier, S., & Harel‐Bellan, A. (2006) · Nature Cell Biology · doi:10.1038/ncb1373 · Cited by 572 · see citing works
Kong, L., Zhu, J., Han, W., Jiang, X., Xu, M., Zhao, Y., Dong, Q., Pang, Z., Guan, Q., Gao, L., et al. (2010) · Acta Diabetologica · doi:10.1007/s00592-010-0226-0 · Cited by 529 · see citing works
The Browning of White Adipose Tissue: Some Burning Issues
Nedergaard, J., & Cannon, B. (2014) · Cell Metabolism · doi:10.1016/j.cmet.2014.07.005 · Cited by 500 · see citing works
Hox genes in hematopoiesis and leukemogenesis
Argiropoulos, B., & Humphries, R. K. (2007) · Oncogene · doi:10.1038/sj.onc.1210760 · Cited by 492 · 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
A Smooth Muscle-Like Origin for Beige Adipocytes
Long, J. Z., Svensson, K. J., Tsai, L. T.-Y., Zeng, X., Roh, H. C., Kong, X., Rao, R. R., Lou, J., Lokurkar, I. A., Baur, W. E., et al. (2014) · Cell Metabolism · doi:10.1016/j.cmet.2014.03.025 · Cited by 462 · 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
Targeting the Circulating MicroRNA Signature of Obesity
Ortega, F. J., Mercader, J. M., Catalán, V., Moreno‐Navarrete, J. M., Pueyo, N., Sabater, M., Gómez‐Ambrosi, J., Anglada, R., Fernández‐Formoso, J. A., Ricart, W., et al. (2013) · Clinical Chemistry · doi:10.1373/clinchem.2012.195776 · Cited by 443 · see citing works
A role of miR‐27 in the regulation of adipogenesis
Lin, Q., Gao, Z., Alarcon, R. M., Ye, J., & Yun, Z. (2009) · FEBS Journal · doi:10.1111/j.1742-4658.2009.06967.x · Cited by 438 · see citing works
Long noncoding RNAs regulate adipogenesis
Sun, L., Goff, L. A., Trapnell, C., Alexander, R., Lo, K. A., Hacisuleyman, E., Sauvageau, M., Tazón‐Vega, B., Kelley, D. R., Hendrickson, D. G., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1222643110 · Cited by 423 · see citing works
miR-27a is a negative regulator of adipocyte differentiation via suppressing PPARγ expression
Kim, S., Kim, A., Lee, H. W., Son, Y. H., Lee, G. Y., Lee, J.-W., Lee, Y. S., & Kim, J. B. (2010) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2010.01.012 · Cited by 414 · see citing works
microRNA miR-27b impairs human adipocyte differentiation and targets PPARγ
Karbiener, M., Fischer, C., Nowitsch, S., Opriessnig, P., Papak, C., Ailhaud, G., Dani, C., Amri, E.-Z., & Scheideler, M. (2009) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2009.09.098 · Cited by 409 · see citing works
Adenosine activates brown adipose tissue and recruits beige adipocytes via A2A receptors
Gnad, T., Scheibler, S., von Kügelgen, I., Scheele, C. C., Kilić, A., Glöde, A., Hoffmann, L. S., Reverte-Salisa, L., Horn, P., Mutlu, S., et al. (2014) · Nature · doi:10.1038/nature13816 · Cited by 394 · see citing works
Self-citationTransdifferentiation 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 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
Vienberg, S. G., Geiger, J., Madsen, S., & Dalgaard, L. T. (2016) · Acta Physiologica · doi:10.1111/apha.12681 · Cited by 375 · see citing works
Type beta transforming growth factor controls the adipogenic differentiation of 3T3 fibroblasts.
Ignotz, R. A., & Massagué, J. (1985) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.82.24.8530 · Cited by 363 · see citing works
Deiuliis, J. A. (2015) · International Journal of Obesity · doi:10.1038/ijo.2015.170 · Cited by 352 · see citing works
Mir193b–365 is essential for brown fat differentiation
Sun, L., Xie, H., Mori, M. A., Alexander, R., Yuan, B., Hattangadi, S. M., Liu, Q., Kahn, C. R., & Lodish, H. F. (2011) · Nature Cell Biology · doi:10.1038/ncb2286 · Cited by 310 · 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
microRNAs in the Regulation of Adipogenesis and Obesity
McGregor, R. A., & Choi, M. (2011) · Current Molecular Medicine · doi:10.2174/156652411795677990 · Cited by 286 · see citing works
miR-155 regulates differentiation of brown and beige adipocytes via a bistable circuit
Chen, Y., Siegel, F., Kipschull, S., Haas, B., Fröhlich, H., Meister, G., & Pfeifer, A. (2013) · Nature Communications · doi:10.1038/ncomms2742 · Cited by 285 · see citing works
Self-citationZhi, J., Melia, A. T., Guerciolini, R., Chung, J., Kinberg, J. A., Hauptman, J. B., & Patel, I. H. (1994) · Clinical Pharmacology & Therapeutics · doi:10.1038/clpt.1994.104 · Cited by 278 · see citing works
MyomiR-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
Pescador, N., Pérez‐Barba, M., Ibarra, J. M., Anchuelo, A. C., Martínez-Larrad, M. T., & Serrano‐Ríos, M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0077251 · Cited by 259 · see citing works
Willeit, P., Skroblin, P., Moschen, A. R., Yin, X., Kaudewitz, D., Zampetaki, A., Barwari, T., Whitehead, M., Ramírez, C. M., Goedeke, L., et al. (2016) · Diabetes · doi:10.2337/db16-0731 · Cited by 257 · 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
The Asparaginyl Hydroxylase Factor Inhibiting HIF-1α Is an Essential Regulator of Metabolism
Zhang, N., Fu, Z., Linke, S., Chicher, J., Gorman, J. J., Visk, D., Haddad, G. G., Poellinger, L., Peet, D. J., Powell, F. L., et al. (2010) · Cell Metabolism · doi:10.1016/j.cmet.2010.03.001 · Cited by 244 · 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
BROWN ADIPOSE TISSUE, β3-ADRENERGIC RECEPTORS, AND OBESITY
Lowell, M., & Flier, M. (1997) · Annual Review of Medicine · doi:10.1146/annurev.med.48.1.307 · Cited by 237 · see citing works
A Long Noncoding RNA Transcriptional Regulatory Circuit Drives Thermogenic Adipocyte Differentiation
Zhao, X.-Y., Li, S., Wang, G.-X., Yu, Q., & Lin, J. D. (2014) · Molecular Cell · doi:10.1016/j.molcel.2014.06.004 · Cited by 230 · see citing works
Foshay, K. M., & Gallicano, G. I. (2008) · Developmental Biology · doi:10.1016/j.ydbio.2008.11.016 · Cited by 225 · see citing works
Zaragosi, L., Wdziekonski, B., Lebrigand, K., Villageois, P., Mari, B. P., Waldmann, R., Dani, C., & Barbry, P. (2011) · Genome biology · doi:10.1186/gb-2011-12-7-r64 · Cited by 224 · see citing works
Tseng, Y.-H., Butte, A. J., Kokkotou, E., Yechoor, V. K., Taniguchi, C. M., Kriauciunas, K. M., Cypess, A. M., Niinobe, M., Yoshikawa, K., Patti, M. E., et al. (2005) · Nature Cell Biology · doi:10.1038/ncb1259 · Cited by 222 · see citing works
Coates, P. J., Nenutil, R., McGregor, A., Picksley, S. M., Crouch, D. H., Hall, P. A., & Wright, E. G. (2001) · Experimental Cell Research · doi:10.1006/excr.2001.5166 · Cited by 207 · see citing works
He, M. Y., Xu, Z., Ding, T., Kuang, D., & Zheng, L. (2009) · Cellular and Molecular Immunology · doi:10.1038/cmi.2009.45 · Cited by 199 · see citing works
Worm, J., Stenvang, J., Petri, A., Frederiksen, K. S., Obad, S., Elmén, J., Hedtjärn, M., Straarup, E. M., Hansen, J. B., & Kauppinen, S. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkp577 · Cited by 192 · see citing works
Fu, T., Seok, S., Choi, S.-E., Huang, Z., Suino-Powell, K., Xu, H., Kemper, B., & Kemper, J. (2014) · Molecular and Cellular Biology · doi:10.1128/mcb.00596-14 · Cited by 187 · see citing works
Mori, M. A., Thomou, T., Boucher, J., Lee, K. Y., Lallukka, S., Kim, J. K., Torriani, M., Yki‐Järvinen, H., Grinspoon, S. K., Cypess, A. M., et al. (2014) · Journal of Clinical Investigation · doi:10.1172/jci73468 · Cited by 183 · see citing works
Exosomal microRNA miR-92a concentration in serum reflects human brown fat activity
Chen, Y., Buyel, J. J., Hanssen, M. J. W., Siegel, F., Pan, R., Naumann, J., Schell, M. J., van der Lans, A. A. J. J., Schlein, C., Fröhlich, H., et al. (2016) · Nature Communications · doi:10.1038/ncomms11420 · Cited by 181 · see citing works
Self-citationMicroRNAs in adipose tissue: their role in adipogenesis and obesity
Hilton, C., Neville, M. J., & Karpe, F. (2012) · International Journal of Obesity · doi:10.1038/ijo.2012.59 · Cited by 174 · see citing works
Aging leads to a programmed loss of brown adipocytes in murine subcutaneous white adipose tissue
Rogers, N. H., Landa, A., Park, S., & Smith, R. G. (2012) · Aging Cell · doi:10.1111/acel.12010 · Cited by 171 · see citing works
Santovito, D., Nardis, V. D., Marcantonio, P., Mandolini, C., Paganelli, C., Vitale, E., Buttitta, F., Bucci, M., Mezzetti, A., Consoli, A., et al. (2014) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2013-3843 · Cited by 171 · see citing works
MicroRNA-26 Family Is Required for Human Adipogenesis and Drives Characteristics of Brown Adipocytes
Karbiener, M., Pisani, D. F., Frontini, A., Oberreiter, L. M., Lang, E., Vegiopoulos, A., Mössenböck, K., Bernhardt, G. A., Mayr, T., Hildner, F., et al. (2013) · Stem Cells · doi:10.1002/stem.1603 · Cited by 169 · see citing works
Brown, Beige, and White: The New Color Code of Fat and Its Pharmacological Implications
Pfeifer, A., & Hoffmann, L. S. (2014) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev-pharmtox-010814-124346 · Cited by 163 · see citing works
Self-citationNicholls, D. G., BERNSON, V. S. M., & Heaton, G. M. (1978) · Proceedings of the Fourth International Symposium on Polarization Phenomena in Nuclear Reactions · doi:10.1007/978-3-0348-5559-4_9 · Cited by 160 · see citing works
Distinct expression of muscle‐specific MicroRNAs (myomirs) in brown adipocytes
Waldén, T. B., Timmons, J. A., Keller, P., Nedergaard, J., & Cannon, B. (2008) · Journal of Cellular Physiology · doi:10.1002/jcp.21621 · Cited by 157 · see citing works
Long non-coding RNA ADNCR suppresses adipogenic differentiation by targeting miR-204
Li, M., Sun, X., Cai, H., Sun, Y., Plath, M. W., Li, C., Lan, X., Lei, C., Lin, F., Bai, Y., et al. (2016) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2016.05.003 · Cited by 156 · see citing works
MiR-27 orchestrates the transcriptional regulation of brown adipogenesis
Sun, L., & Trajkovski, M. (2013) · Metabolism · doi:10.1016/j.metabol.2013.10.004 · Cited by 155 · see citing works
Kang, T., Lu, W., Xu, W., Anderson, L. M., Bacanamwo, M., Thompson, W. E., Chen, Y. E., & Liu, D. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.514372 · Cited by 154 · see citing works
MicroRNA‐455 regulates brown adipogenesis via a novel HIF1an‐AMPK‐PGC1α signaling network
Zhang, H., Guan, M., Townsend, K. L., Huang, T. L., An, D., Yan, X., Xue, R., Schulz, T. J., Winnay, J. N., Mori, M. A., et al. (2015) · EMBO Reports · doi:10.15252/embr.201540837 · Cited by 150 · see citing works
miR-133a Regulates Adipocyte Browning In Vivo
Liu, W., Bi, P., Shan, T., Yang, X., Yin, H., Wang, Y.-X., Liu, N., Rudnicki, M. A., & Kuang, S. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003626 · Cited by 144 · see citing works
MicroRNA-30c promotes human adipocyte differentiation and co-represses PAI-1 and ALK2
Karbiener, M., Neuhold, C., Opriessnig, P., Prokesch, A., Bogner-Strauss, J., & Scheideler, M. (2011) · RNA Biology · doi:10.4161/rna.8.5.16153 · Cited by 136 · see citing works
Huang, Y., Zheng, Y., Jin, C., Li, X., Jia, L., & Li, W. (2016) · Scientific Reports · doi:10.1038/srep28897 · Cited by 136 · see citing works
MicroRNA-378 controls classical brown fat expansion to counteract obesity
Pan, D., Mao, C., Quattrochi, B., Friedline, R. H., Zhu, L. J., Jung, D. Y., Kim, J. K., Lewis, B. C., & Wang, Y. (2014) · Nature Communications · doi:10.1038/ncomms5725 · Cited by 132 · see citing works
miR-30 Promotes Thermogenesis and the Development of Beige Fat by Targeting RIP140
Hu, F., Wang, M., Xiao, T., Yin, B., He, L., Meng, W., Dong, M., & Liu, F. (2015) · Diabetes · doi:10.2337/db14-1117 · Cited by 132 · see citing works
The contribution of brown adipose tissue to heat production in the new‐born rabbit.
Hull, D., & Segall, M. (1965) · The Journal of Physiology · doi:10.1113/jphysiol.1965.sp007773 · Cited by 128 · see citing works
Insig-1 “brakes” lipogenesis in adipocytes and inhibits differentiation of preadipocytes
Li, J., Takaishi, K., Cook, W. S., McCorkle, S. K., & Unger, R. H. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1133426100 · Cited by 124 · see citing works
Meakin, P. J., Harper, A. J., Hamilton, D. L., Gallagher, J. R., McNeilly, A. D., Burgess, L. A., Vaanholt, L. M., Bannon, K. A., Latcham, J., Hussain, I., et al. (2011) · Biochemical Journal · doi:10.1042/bj20110512 · Cited by 119 · see citing works
Kong, X., Yu, J., Bi, J., Qi, H., Di, W., Wu, L., Wang, L., Zha, J., Lv, S., Zhang, F., et al. (2014) · Diabetes · doi:10.2337/db14-0395 · Cited by 115 · see citing works
Sérino, M., Menghini, R., Fiorentino, L., Amoruso, R., Mauriello, A., Lauro, D., Sbraccia, P., Hribal, M. L., Lauro, R., & Federici, M. (2007) · Diabetes · doi:10.2337/db07-0360 · Cited by 113 · see citing works
MicroRNAs Are Required for the Feature Maintenance and Differentiation of Brown Adipocytes
Kim, H.-J., Cho, H., Alexander, R., Patterson, H. C., Gu, M., Lo, K. A., Xu, D., Goh, V. J., Nguyen, L. N., Chai, X., et al. (2014) · Diabetes · doi:10.2337/db14-0466 · Cited by 105 · see citing works
Skårn, M., Namløs, H. M., Noordhuis, P., Wang, M.-Y., Meza‐Zepeda, L. A., & Myklebost, O. (2011) · Stem Cells and Development · doi:10.1089/scd.2010.0503 · Cited by 98 · see citing works
Dicer1–miR-328–Bace1 signalling controls brown adipose tissue differentiation and function
Oliverio, M., Schmidt, E. B., Mauer, J., Baitzel, C., Hansmeier, N. R., Khani, S., Konieczka, S., Pradas-Juni, M., Brodesser, S., Van, T.-M., et al. (2016) · Nature Cell Biology · doi:10.1038/ncb3316 · Cited by 97 · see citing works
Distinct functions for RIP140 in development, inflammation, and metabolism
Nautiyal, J., Christian, M., & Parker, M. G. (2013) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2013.05.001 · Cited by 94 · see citing works
miRNA-32 Drives Brown Fat Thermogenesis and Trans-activates Subcutaneous White Fat Browning in Mice
Ng, R., Hussain, N. A., Zhang, Q., Chang, C. T., Li, H., Fu, Y., Cao, L., Han, W., Stünkel, W., & Xu, F. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.04.035 · Cited by 93 · see citing works
ETO/MTG8 Is an Inhibitor of C/EBPβ Activity and a Regulator of Early Adipogenesis
Rochford, J. J., Semple, R. K., Laudes, M., Boyle, K. B., Christodoulides, C., Mulligan, C., Lelliott, C. J., Schinner, S., Hadaschik, D., Mahadevan, M., et al. (2004) · Molecular and Cellular Biology · doi:10.1128/mcb.24.22.9863-9872.2004 · Cited by 87 · see citing works
Li, S., Mi, L., Yu, L., Yu, Q., Liu, T., Wang, G.-X., Zhao, X.-Y., Wu, J., & Lin, J. D. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1703494114 · Cited by 84 · see citing works
Circulating microRNAs: Emerging Biomarkers of Liver Disease
Arrese, M. A., Eguchi, A., & Feldstein, A. E. (2015) · Seminars in Liver Disease · doi:10.1055/s-0034-1397348 · Cited by 82 · see citing works
Peripheral blood microRNA-15a is a potential biomarker for type 2 diabetes mellitus and pre-diabetes
Al‐Kafaji, G., Al-Mahroos, G., Al-Sayed, N., Hasan, Z. A., Nawaz, S., & Bakhiet, M. (2015) · Molecular Medicine Reports · doi:10.3892/mmr.2015.4416 · Cited by 77 · see citing works
Deficiency of TNFα Converting Enzyme (TACE/ADAM17) Causes a Lean, Hypermetabolic Phenotype in Mice
Gelling, R. W., Yan, W., Al‐Noori, S., Pardini, A. W., Morton, G. J., Ogimoto, K., Schwartz, M. W., & Dempsey, P. J. (2008) · Endocrinology · doi:10.1210/en.2008-0775 · Cited by 74 · see citing works
miR-32 and its target SLC45A3 regulate the lipid metabolism of oligodendrocytes and myelin
Shin, D., Howng, S. Y. B., Ptáček, L. J., & Fu, Y. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.03.054 · Cited by 68 · see citing works
Myostatin signals through miR-34a to regulate Fndc5 expression and browning of white adipocytes
Ge, X., Sathiakumar, D., Lua, B.-N., Kukreti, H., Lee, M., & McFarlane, C. (2016) · International Journal of Obesity · doi:10.1038/ijo.2016.110 · Cited by 68 · see citing works
Fitter, S., Vandyke, K., Gronthos, S., & Zannettino, A. C. W. (2012) · Journal of Molecular Endocrinology · doi:10.1530/jme-12-0003 · Cited by 65 · see citing works
miR-125b affects mitochondrial biogenesis and impairs brite adipocyte formation and function
Giroud, M., Pisani, D., Karbiener, M., Barquissau, V., Ghandour, R., Tews, D., Fischer-Posovszky, P., Chambard, J., Knippschild, U., Niemi, T., et al. (2016) · Molecular Metabolism · doi:10.1016/j.molmet.2016.06.005 · Cited by 64 · see citing works
Identification of miR-106b-93 as a negative regulator of brown adipocyte differentiation
Wu, Y., Zuo, J., Zhang, Y., Xie, Y., Hu, F., Chen, L., Liu, B., & Liu, F. (2013) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2013.08.016 · Cited by 61 · see citing works
Profiling peripheral micro RNA s in obesity and type 2 diabetes mellitus
Wu, L., Dai, X., Zhan, J., Zhang, Y., Zhang, H., Zhang, H., Zeng, S.-H., & Xi, W. (2015) · Apmis · doi:10.1111/apm.12389 · Cited by 55 · see citing works
Woodward, J., & SAGGERSON, E. D. (1986) · Biochemical Journal · doi:10.1042/bj2380395 · Cited by 53 · see citing works
Cell-free microRNAs as cancer biomarkers: the odyssey of miRNAs through body fluids
Javidi, M. A., Ahmadi, A., Bakhshinejad, B., Nouraee, N., Babashah, S., & Sadeghizadeh, M. (2014) · Medical Oncology · doi:10.1007/s12032-014-0295-y · Cited by 53 · see citing works
MicroRNAs involved in the browning process of adipocytes
Arias, N., Aguirre, L., Fernández‐Quintela, A., González, M. A., Lasa, A., Miranda, J., Macarulla, M. T., & Portillo, M. P. (2015) · Journal of Physiology and Biochemistry · doi:10.1007/s13105-015-0459-z · Cited by 51 · see citing works
Dickson, L. M., Gandhi, S., Layden, B. T., Cohen, R., & Wicksteed, B. L. (2016) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00114.2016 · Cited by 50 · see citing works
Cinti, S., Zancanaro, C., Sbarbati, A., Cicolini, M., Vogel, P., Ricquier, D., & Fakan, S. (1989) · Biology of the Cell · doi:10.1111/j.1768-322x.1989.tb00883.x · Cited by 45 · see citing works
Helms, M. W., Kemming, D., Contag, C. H., et al. (2009) · Cancer Research · doi:10.1158/0008-5472.can-08-4154 · Cited by 41 · see citing works
Control of brown adipose tissue lipolysis and respiration by adenosine
Szillat, D., & Bukowiecki, L. J. (1983) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1983.245.6.e555 · Cited by 40 · see citing works
Role of adenosine as an endogenous regulator of respiration in hamster brown adipocytes
Schimmel, R. J., & McCARTHY, L. (1984) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.1984.246.3.c301 · Cited by 40 · see citing works
Jiao, Y., Sun, K., Zhao, L., et al. (2011) · Acta Pharmacologica Sinica · doi:10.1038/aps.2011.163 · Cited by 37 · see citing works
MiR-193bandmiR-365-1are not required for the development and function of brown fat in the mouse
Feuermann, Y., Kang, K., Gavrilova, O., Haetscher, N., Jang, S. J., Yoo, K. H., Jiang, C., Gonzalez, F. J., Robinson, G. W., & Hennighausen, L. G. (2013) · RNA Biology · doi:10.4161/rna.27239 · Cited by 35 · see citing works
An ultrastructural study of adipocyte precursors from epididymal fat pads of adult rats in culture.
Cinti, S., CIGOLINI, M., Gazzanelli, G., & Bosello, O. (1985) · PubMed · Cited by 13 · see citing works
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Ghesmati, Z., Rashid, M., Fayezi, S., Gieseler, F., Alizadeh, E., & Darabi, M. (2024) · Reviews in Endocrine and Metabolic Disorders · doi:10.1007/s11154-023-09850-0 · Cited by 139 · see citing works
Exerkines and Sarcopenia: Unveiling the Mechanism Behind Exercise-Induced Mitochondrial Homeostasis
Wang, J., Jia, D., Zhang, Z., & Wang, D. (2025) · Metabolites · doi:10.3390/metabo15010059 · Cited by 23 · see citing works
- Authors
- Goody, D., & Pfeifer, A.
- Affiliations
- University of Bonn (DE)
- Corresponding author
- Pfeifer, Alexander
- ORCID
- Pfeifer, Alexander
- Venue
- Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids
- Publisher
- Elsevier BV
- Published
- 2019-01
- Volume
- 1864
- Issue
- 1
- Pages
- 29-36
- ISSN
- 1388-1981 (ISSN-L)
- OpenAlex
- W2799933422
- Cited by
- 54
- References
- 117
- Citations by year
- 2026: 3 · 2025: 3 · 2024: 5 · 2023: 8 · 2022: 6 · 2021: 11 · 2020: 10 · 2019: 8
- FWCI
- 0.95
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Physiology › Adipose Tissue and Metabolism
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
- Health Sciences › Medicine › Epidemiology › Adipokines, Inflammation, and Metabolic Diseases
- Keywords
- microRNA, brown adipose tissue, beige adipocytes, browning, white adipose tissue, thermogenesis, obesity, RNA therapeutics, gene expression regulation
- MeSH terms
- Adipose Tissue, Beige, Animals, Adipose Tissue, Brown, Humans, MicroRNAs, Adipogenesis
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