Insights into brown adipose tissue evolution and function from non-model organisms
Abstract
Brown adipose tissue (BAT) enables adaptive thermoregulation through heat production that is catalyzed by mitochondrial uncoupling protein 1 (UCP1). BAT is frequently studied in rodent model organisms, and recently in adult humans to treat metabolic diseases. However, complementary studies of many non-model species, which have diversified to many more ecological niches, may significantly broaden our understanding of BAT regulation and its physiological roles. This Review highlights the research on non-model organisms, which was instrumental to the discovery of BAT function, and the unique evolutionary history of BAT/UCP1 in mammalian thermogenesis. The comparative biology of BAT provides a powerful integrative approach that could identify conserved and specialized functional changes in BAT and UCP1 by considering species diversity, ecology and evolution, and by fusing multiple scientific disciplines such as physiology and biochemistry. Thus, resolving the complete picture of BAT biology may fail if comparative studies of non-model organisms are neglected.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
Irisin, derived from the cleavage of FNDC5 and released after exercise or muscle shivering, causes the transformation of white fat cells into cells with a phenotype similar to brown fat cells.
“In particular, irisin derived from the cleavage of fibronectin type III domain containing protein 5 (FNDC5) and released after exercise or muscle shivering, causes the transformation of white fat cells (storage adipose tissue) into cells with a phenotype similar to that of brown fat cells.”
From MOSH Syndrome (Male Obesity Secondary Hypogonadism): Clinical Assessment and Possible Therapeutic Approaches (2018) · cites this paper as [44]
Cites
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
PRDM16 controls a brown fat/skeletal muscle switch
Seale, P., Bjork, B., Yang, W., Kajimura, S., Chin, S., Kuang, S., Scimè, A., Devarakonda, S., Conroe, H. M., Erdjument-Bromage, H., et al. (2008) · Nature · doi:10.1038/nature07182 · Cited by 2,347 · cited 2× · see citing works
“that brown adipocytes and myocytes derive from common progenitors (Seale et al., 2008).”
BackgroundUnexpected 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
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
Impacts of the Cretaceous Terrestrial Revolution and KPg extinction on mammal diversification
Meredith, R. W., Janečka, J. E., Gatesy, J., Ryder, O. A., Fisher, C. A., Teeling, E. C., Goodbla, A., Eizirik, E., Simão, T. L. L., Stadler, T., et al. (2011) · Science · doi:10.1126/science.1211028 · Cited by 1,464 · see citing works
Mice lacking mitochondrial uncoupling protein are cold-sensitive but not obese
Enerbäck, S., Jacobsson, A., Simpson, E. M., Guerra, C., Yamashita, H., Harper, M.-E., & Kozak, L. P. (1997) · Nature · doi:10.1038/387090a0 · Cited by 1,379 · see citing works
Feldmann, H. M., Golozoubova, V., Cannon, B., & Nedergaard, J. (2009) · Cell Metabolism · doi:10.1016/j.cmet.2008.12.014 · Cited by 1,318 · see citing works
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
The Placental Mammal Ancestor and the Post–K-Pg Radiation of Placentals
O’Leary, M. A., Bloch, J. I., Flynn, J. J., Gaudin, T. J., Giallombardo, A., Giannini, N. P., Goldberg, S. L., Kraatz, B., Luo, Z., Meng, J., et al. (2013) · Science · doi:10.1126/science.1229237 · Cited by 1,194 · 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
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
Structure of mitochondrial ADP/ATP carrier in complex with carboxyatractyloside
Pebay‐Peyroula, E., Dahout-Gonzalez, C., Kahn, R., Trézéguet, V., Lauquin, G. J. ‐., & Brandolin, G. (2003) · Nature · doi:10.1038/nature02056 · Cited by 998 · 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
Smith, R. E., & Horwitz, B. A. (1969) · Physiological Reviews · doi:10.1152/physrev.1969.49.2.330 · Cited by 715 · see citing works
UCP1 in Brite/Beige Adipose Tissue Mitochondria Is Functionally Thermogenic
Shabalina, I. G., Petrovič, N., de Jong, J. M. A., Kalinovich, A., Cannon, B., & Nedergaard, J. (2013) · Cell Reports · doi:10.1016/j.celrep.2013.10.044 · Cited by 637 · see citing works
Guerra, C., Koza, R. A., Yamashita, H., Walsh, K., & Kozak, L. P. (1998) · Journal of Clinical Investigation · doi:10.1172/jci3155 · Cited by 635 · see citing works
The Biology of Mitochondrial Uncoupling Proteins
Rousset, S., Alves‐Guerra, M., Mozo, J., Miroux, B., Cassard, A., Bouillaud, F., & Ricquier, D. (2004) · Diabetes · doi:10.2337/diabetes.53.2007.s130 · Cited by 556 · see citing works
Analysis and Interpretation of Microplate-Based Oxygen Consumption and pH Data
Divakaruni, A. S., Paradyse, A. R., Ferrick, D. A., Murphy, A. N., & Jastroch, M. (2014) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/b978-0-12-801415-8.00016-3 · Cited by 525 · see citing works
Self-citationOnly UCP1 can mediate adaptive nonshivering thermogenesis in the cold
Golozoubova, V., Hohtola, E., Matthias, A., Jacobsson, A., Cannon, B., & Nedergaard, J. (2001) · The FASEB Journal · doi:10.1096/fj.00-0536fje · Cited by 503 · 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
The Regulation and Physiology of Mitochondrial Proton Leak
Divakaruni, A. S., & Brand, M. D. (2011) · Physiology · doi:10.1152/physiol.00046.2010 · Cited by 484 · 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 · cited 2× · see citing works
“…to cold environmental temperatures, a centrally processed cold-sensation induces the release of noradrenaline from efferent sympathetic postganglionic nerve fibers in BAT to activate a collection of α- and β-adrenergic receptors residing in the brown adipose plasma membrane (Bartness et al., 2010).”
BackgroundHeaton, G. M., Wagenvoord, R. J., Kemp, A., & Nicholls, D. G. (1978) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1978.tb12045.x · Cited by 407 · see citing works
Aquila, H., Link, T. A., & Klingenberg, M. (1985) · The EMBO Journal · doi:10.1002/j.1460-2075.1985.tb03941.x · Cited by 368 · see citing works
Ishibashi, J., & Seale, P. (2010) · Science · doi:10.1126/science.1190816 · Cited by 344 · 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
UCP1-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
Brown 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
Self-citationParadoxical 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
Pharmacological 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
Ricquier, D., & Kader, J. (1976) · Biochemical and Biophysical Research Communications · doi:10.1016/0006-291x(76)90849-4 · Cited by 269 · 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
Cold‐Induced Recruitment of Brown Adipose Tissue Thermogenesis
Klingenspor, M. (2003) · Experimental Physiology · doi:10.1113/eph8802508 · Cited by 258 · see citing works
The so‐called hibernating gland
Rasmussen, A. T. (1923) · Journal of Morphology · doi:10.1002/jmor.1050380106 · Cited by 227 · see citing works
UCP2 and UCP3 rise in starved rat skeletal muscle but mitochondrial proton conductance is unchanged
Cadenas, S., Buckingham, J. A., Samec, S., Seydoux, J., Din, N., Dulloo, A. G., & Brand, M. D. (1999) · FEBS Letters · doi:10.1016/s0014-5793(99)01540-9 · Cited by 227 · see citing works
Complete cDNA-derived amino acid sequence of rat brown fat uncoupling protein.
Bouillaud, F., Weissenbach, J., & Ricquier, D. (1986) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)35962-8 · Cited by 222 · see citing works
UCP1 deficiency increases susceptibility to diet‐induced obesity with age
Kontani, Y., Wang, Y., Kimura, K., Inokuma, K. ‐., Saito, M., Suzuki‐Miura, T., Wang, Z., Sato, Y., Mori, N., & Yamashita, H. (2005) · Aging Cell · doi:10.1111/j.1474-9726.2005.00157.x · Cited by 207 · see citing works
White adipose tissue contributes to UCP1-independent thermogenesis
Granneman, J. G., Burnazi, M., Zhu, Z., & Schwamb, L. A. (2003) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00197.2003 · Cited by 205 · see citing works
Cadenas, S., Echtay, K. S., Harper, J. A., Jekabsons, M. B., Buckingham, J. A., Grau, E., Abuin, A., Chapman, H., Clapham, J. C., & Brand, M. D. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m109736200 · Cited by 199 · see citing works
Berg, F., Gustafson, U., & Andersson, L. (2006) · PLoS Genetics · doi:10.1371/journal.pgen.0020129 · Cited by 169 · see citing works
Adaptive thermogenesis and thermal conductance in wild-type and UCP1-KO mice
Meyer, C. W., Willershäuser, M., Jastroch, M., Rourke, B. C., Fromme, T., Oelkrug, R., Heldmaier, G., & Klingenspor, M. (2010) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00021.2009 · Cited by 162 · see citing works
Self-citationGenomic evidence reveals a radiation of placental mammals uninterrupted by the KPg boundary
Liu, L., Zhang, J., Rheindt, F. E., Lei, F., Qu, Y., Wang, Y., Zhang, Y., Sullivan, C., Nie, W., Wang, J., et al. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1616744114 · Cited by 150 · see citing works
Crichton, P. G., Lee, Y., & Kunji, E. R. S. (2017) · Biochimie · doi:10.1016/j.biochi.2016.12.016 · Cited by 144 · see citing works
Jastroch, M., Wuertz, S., Kloas, W., & Klingenspor, M. (2005) · Physiological Genomics · doi:10.1152/physiolgenomics.00070.2005 · Cited by 126 · see citing works
Self-citationLong-Term Cold Adaptation Does Not Require FGF21 or UCP1
Keipert, S., Kutschke, M., Ost, M., Schwarzmayr, T., van Schothorst, E. M., Lamp, D., Brachthäuser, L., Hamp, I., Mazibuko, S. E., Hartwig, S., et al. (2017) · Cell Metabolism · doi:10.1016/j.cmet.2017.07.016 · Cited by 122 · see citing works
Self-citationHeldmaier, G. (1971) · Journal of Comparative Physiology A · Cited by 120 · see citing works
Melatonin stimulates Growth of Brown Adipose Tissue
Heldmaier, G., & Hoffmann, K. H. (1974) · Nature · doi:10.1038/247224a0 · Cited by 120 · see citing works
Brite/beige fat and UCP1 — is it thermogenesis?
Keipert, S., & Jastroch, M. (2014) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2014.02.008 · Cited by 114 · see citing works
Self-citationZitterfreie W�rmebildung und K�rpergr��e bei S�ugetieren
Heldmaier, G. (1971) · Journal of Comparative Physiology A · doi:10.1007/bf00304134 · Cited by 113 · see citing works
Cold adaptation in pigs depends on UCP3 in beige adipocytes
Lin, J., Cao, C., Tao, C., Ye, R., Dong, M., Zheng, Q., Wang, C., Jiang, X., Qin, G., Yan, C., et al. (2017) · Journal of Molecular Cell Biology · doi:10.1093/jmcb/mjx018 · Cited by 101 · see citing works
Inactivation of thermogenic UCP1 as a historical contingency in multiple placental mammal clades
Gaudry, M. J., Jastroch, M., Treberg, J. R., Hofreiter, M., Paijmans, J. L. A., Starrett, J., Wales, N., Signore, A. V., Springer, M. S., & Campbell, K. L. (2017) · Science Advances · doi:10.1126/sciadv.1602878 · Cited by 98 · see citing works
Self-citationDehdashti, A. R., Mermillod, B., Rüfenacht, D. A., Reverdin, A., & de Tribolet, N. (2003) · Cerebrovascular Diseases · doi:10.1159/000073898 · Cited by 97 · see citing works
Hampton, M. E., Melvin, R. G., & Andrews, M. T. (2013) · PLoS ONE · doi:10.1371/journal.pone.0085157 · Cited by 91 · see citing works
Lovegrove, B. G., Lobban, K. D., & Levesque, D. L. (2014) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2014.1304 · Cited by 89 · see citing works
Stier, A., Bize, P., Habold, C., Bouillaud, F., Massemin, S., & Criscuolo, F. (2013) · Journal of Experimental Biology · doi:10.1242/jeb.092700 · Cited by 87 · see citing works
Marsupial uncoupling protein 1 sheds light on the evolution of mammalian nonshivering thermogenesis
Jastroch, M., Withers, K., Taudien, S., Frappell, P. B., Helwig, M., Fromme, T., Hirschberg, V., Heldmaier, G., McAllan, B. M., Firth, B. T., et al. (2007) · Physiological Genomics · doi:10.1152/physiolgenomics.00183.2007 · Cited by 85 · see citing works
Self-citationKeipert, S., Kutschke, M., Lamp, D., Brachthäuser, L., Neff, F., Meyer, C. W., Oelkrug, R., Kharitonenkov, A., & Jastroch, M. (2015) · Molecular Metabolism · doi:10.1016/j.molmet.2015.04.006 · Cited by 85 · see citing works
Self-citationMeasurement of Proton Leak and Electron Leak in Isolated Mitochondria
Affourtit, C., Quinlan, C. L., & Brand, M. D. (2011) · Methods in molecular biology · doi:10.1007/978-1-61779-382-0_11 · Cited by 82 · see citing works
Molecular evolution of UCP1 and the evolutionary history of mammalian non-shivering thermogenesis
Hughes, D. A., Jastroch, M., Stoneking, M., & Klingenspor, M. (2009) · BMC Evolutionary Biology · doi:10.1186/1471-2148-9-4 · Cited by 80 · see citing works
Self-citationDifferential gene expression in white and brown preadipocytes
Boeuf, S., Klingenspor, M., Hal, N. L. W. F.-V., SCHNEIDER, T., Keijer, J., & Klaus, S. (2001) · Physiological Genomics · doi:10.1152/physiolgenomics.00048.2001 · Cited by 80 · see citing works
Structure–Function Relationship in UCP1
Klingenberg, M., Echtay, K., Bienengraeber, M., Winkler, E., & Huang, S. (1999) · International Journal of Obesity · doi:10.1038/sj.ijo.0800939 · Cited by 79 · see citing works
Nonshivering thermogenesis protects against defective calcium handling in muscle
Aydin, J., Shabalina, I. G., Place, N., Reiken, S. R., Zhang, S., Bellinger, A. M., Nedergaard, J., Cannon, B., Marks, A. R., Bruton, J. D., et al. (2008) · The FASEB Journal · doi:10.1096/fj.08-113712 · Cited by 79 · see citing works
Evolution of brown fat: its absence in marsupials and monotremes
Hayward, J. S., & Lisson, P. A. (1992) · Canadian Journal of Zoology · doi:10.1139/z92-025 · Cited by 77 · see citing works
Brown fat in a protoendothermic mammal fuels eutherian evolution
Oelkrug, R., Goetze, N., Exner, C., Lee, Y., Ganjam, G. K., Kutschke, M., Müller, S., Stöhr, S., Tschöp, M. H., Crichton, P. G., et al. (2013) · Nature Communications · doi:10.1038/ncomms3140 · Cited by 75 · see citing works
Self-citationOelkrug, R., Heldmaier, G., & Meyer, C. W. (2010) · Journal of Comparative Physiology B · doi:10.1007/s00360-010-0503-9 · Cited by 73 · see citing works
Self-citationIdentification of a Functioning Mitochondrial Uncoupling Protein 1 in Thymus
Carroll, A. M., Haines, L. R., Pearson, T. W., Fallon, P. G., Walsh, C. M., Brennan, C. M., Breen, E. P., & Porter, R. K. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m413315200 · Cited by 68 · see citing works
Trzcionka, M., Withers, K., Klingenspor, M., & Jastroch, M. (2008) · Journal of Experimental Biology · doi:10.1242/jeb.016519 · Cited by 68 · see citing works
Self-citationRose, R. W., West, A. K., Ye, J., McCormack, G. H., & Colquhoun, E. Q. (1999) · Physiological and Biochemical Zoology · doi:10.1086/316709 · Cited by 60 · see citing works
Uncoupling protein 1 controls reactive oxygen species in brown adipose tissue
Jastroch, M. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1709064114 · Cited by 60 · see citing works
Self-citationTranscriptional Activation of the Human ucp1 Gene in a Rodent Cell Line
González‐Barroso, M. M., Pecqueur, C., Gelly, C., Sanchı́s, D., Alves‐Guerra, M., Bouillaud, F., Ricquier, D., & Cassard, A. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m001678200 · Cited by 59 · see citing works
Pig has no uncoupling protein 1
Hou, L., Shi, J., Cao, L., Xu, G., Hu, C. Y., & Wang, C. (2017) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2017.04.118 · Cited by 59 · see citing works
A Comparative Survey of Brown Fat in the Neck and Axilla of Mammals at Birth
Rowlatt, U., Mrosovsky, N., & English, A. (2009) · Biology of the Neonate · doi:10.1159/000240303 · Cited by 58 · see citing works
Brown fat, thermogenesis and physiological birth in a marsupial
Loudon, A. S. I., Rothwell, N. J., & Stock, M. J. (1985) · Comparative Biochemistry and Physiology Part A Physiology · doi:10.1016/0300-9629(85)90912-0 · Cited by 53 · see citing works
Nonshivering Thermogenesis in Marsupials: Absence of Thermogenic Response to β3-Adrenergic Agonists
Nicol, S. C., Pavlides, D., & Andersen, N. A. (1997) · Comparative Biochemistry and Physiology Part A Physiology · doi:10.1016/s0300-9629(96)00357-x · Cited by 51 · see citing works
Energetics of Reproduction in the Lesser Hedgehog Tenrec, Echinops telfairi (Martin)
Poppitt, S. D., Speakman, J. R., & Racey, P. A. (1994) · Physiological Zoology · doi:10.1086/physzool.67.4.30163874 · Cited by 50 · see citing works
Avian UCP: The Killjoy in the Evolution of the Mitochondrial Uncoupling Proteins
Emre, Y., Hurtaud, C., Ricquier, D., Bouillaud, F., Hughes, J., & Criscuolo, F. (2007) · Journal of Molecular Evolution · doi:10.1007/s00239-007-9020-1 · Cited by 49 · see citing works
Grabek, K. R., Behn, C. D., Barsh, G. S., Hesselberth, J. R., & Martin, S. L. (2015) · eLife · doi:10.7554/elife.04517 · Cited by 37 · see citing works
Ballinger, M. A., Hess, C., Napolitano, M. W., Bjork, J. A., & Andrews, M. T. (2016) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00463.2015 · Cited by 35 · see citing works
Rousset, S., Alves‐Guerra, M., Ouadghiri-Bencherif, S., Kozak, L. P., Miroux, B., Richard, D., Bouillaud, F., Ricquier, D., & Cassard, A. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m306980200 · Cited by 34 · see citing works
Evolution of UCP1 Transcriptional Regulatory Elements Across the Mammalian Phylogeny
Gaudry, M. J., & Campbell, K. L. (2017) · Frontiers in Physiology · doi:10.3389/fphys.2017.00670 · Cited by 33 · see citing works
Mzilikazi, N., Jastroch, M., Meyer, C. W., & Klingenspor, M. (2007) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00427.2007 · Cited by 32 · see citing works
Self-citationLevesque, D. L., Lobban, K. D., & Lovegrove, B. G. (2014) · Journal of Comparative Physiology B · doi:10.1007/s00360-014-0858-4 · Cited by 31 · see citing works
Mitochondrial uncoupling protein 1 expression in thymocytes
Adams, A. E., Carroll, A. M., Fallon, P. G., & Porter, R. K. (2008) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2008.04.020 · Cited by 31 · see citing works
Images of mitochondrial UCP 1 in mouse thymocytes using confocal microscopy
Adams, A. E., Hanrahan, O., Nolan, D. P., Voorheis, H. P., Fallon, P. G., & Porter, R. K. (2007) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2007.10.003 · Cited by 30 · see citing works
Bradley, R. J., Howell, J. H., Romine, W. O., CARL, G., & Kemp, G. (1976) · Biochemical and Biophysical Research Communications · doi:10.1016/0006-291x(76)91184-0 · Cited by 30 · see citing works
When pigs fly, UCP1 makes heat
Jastroch, M., & Andersson, L. (2015) · Molecular Metabolism · doi:10.1016/j.molmet.2015.02.005 · Cited by 29 · see citing works
Self-citationPolymeropoulos, E. T., Jastroch, M., & Frappell, P. B. (2011) · Journal of Comparative Physiology B · doi:10.1007/s00360-011-0623-x · Cited by 28 · see citing works
Self-citationImmunodetection of UCP1 in rat thymocytes
Carroll, A. M., Haines, L. R., Pearson, T. W., Brennan, C. M., Breen, E. P., & Porter, R. K. (2004) · Biochemical Society Transactions · doi:10.1042/bst0321066 · Cited by 26 · see citing works
Novel reptilian uncoupling proteins: molecular evolution and gene expression during cold acclimation
Schwartz, T. S., Murray, S. A., & Seebacher, F. (2008) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2007.1761 · Cited by 23 · see citing works
Increased homeothermy during reproduction in a basal placental mammal
Levesque, D. L., & Lovegrove, B. G. (2014) · Journal of Experimental Biology · doi:10.1242/jeb.098848 · Cited by 23 · see citing works
Shore, A., Emes, R. D., Wessely, F., Kemp, P. R., Cillo, C., D'Armiento, M. R., Hoggard, N., & Lomax, M. A. (2013) · Frontiers in Genetics · doi:10.3389/fgene.2012.00304 · Cited by 10 · see citing works
WOLF–BISON INTERACTIONS IN YELLOWSTONE NATIONAL PARK
Smith, D. W., Mech, L. D., Meagher, M., Clark, W. E., Jaffe, R., Phillips, M. K., & Mack, J. A. (2000) · Journal of Mammalogy · doi:10.1644/1545-1542(2000)081
Flagged first, then by citations
2 of the 94 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Grigg, G. C., Nowack, J., Bicudo, J. E. P. W., Bal, N. C., Woodward, H. N., & Seymour, R. S. (2021) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.12822 · Cited by 103 · see citing works
Bal, N. C., & Periasamy, M. (2020) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2019.0135 · Cited by 91 · see citing works
De Lorenzo, A., Noce, A., Moriconi, E., Rampello, T., Marrone, G., Di Daniele, N., & Rovella, V. (2018) · Nutrients · doi:10.3390/nu10040474 · Cited by 68 · see citing works
“Thus, regulating thermogenesis, exerting an anti-inflammatory action and reducing macrophage migration to adipose tissue [43,44].”
BackgroundRedox control of non-shivering thermogenesis
Lettieri‐Barbato, D. (2019) · Molecular Metabolism · doi:10.1016/j.molmet.2019.04.002 · Cited by 50 · see citing works
Chronic cold exposure induces mitochondrial plasticity in deer mice native to high altitudes
Mahalingam, S., Cheviron, Z. A., Storz, J. F., McClelland, G. B., & Scott, G. R. (2020) · The Journal of Physiology · doi:10.1113/jp280298 · Cited by 51 · see citing works
The rs1421085 variant within FTO promotes brown fat thermogenesis
Zhang, Z., Chen, N., Yin, N., Liu, R., He, Y., Li, D., Tong, M., Gao, A., Lu, P., Zhao, Y., et al. (2023) · Nature Metabolism · doi:10.1038/s42255-023-00847-2 · Cited by 40 · see citing works
Adipose ABHD6 regulates tolerance to cold and thermogenic programs
Poursharifi, P., Attané, C., Mugabo, Y., Al‐Mass, A., Ghosh, A., Schmitt, C., Zhao, S., Guida, J., Lussier, R., Erb, H., et al. (2020) · JCI Insight · doi:10.1172/jci.insight.140294 · Cited by 39 · see citing works
Is Endothermy an Evolutionary By-Product?
Seebacher, F. (2020) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2020.02.006 · Cited by 37 · see citing works
Thermoregulation in hibernating mammals: The role of the “thyroid hormones system”
Frare, C., Williams, C. T., & Drew, K. L. (2020) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2020.111054 · Cited by 33 · see citing works
Brown adipocyte ATF4 activation improves thermoregulation and systemic metabolism
Paulo, E., Zhang, Y., Masand, R., Huynh, T. L., Seo, Y., Swaney, D. L., Soucheray, M., Stevenson, E. J., Jimenez‐Morales, D., Krogan, N. J., et al. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109742 · Cited by 26 · see citing works
Proteostasis in thermogenesis and obesity
Bartelt, A., & Widenmaier, S. B. (2020) · Biological Chemistry · doi:10.1515/hsz-2019-0427 · Cited by 26 · see citing works
Gaudry, M. J., Campbell, K. L., & Jastroch, M. (2018) · Handbook of Experimental Pharmacology · doi:10.1007/164_2018_116 · Cited by 24 · see citing works
Self-citationImportance of adipocyte browning in the evolution of endothermy
Jastroch, M., & Seebacher, F. (2020) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2019.0134 · Cited by 24 · see citing works
Self-citationAlnabulsi, A., Cash, B., Hu, Y., Silina, L., Alnabulsi, A., & Murray, G. I. (2019) · International Journal of Cancer · doi:10.1002/ijc.32198 · Cited by 23 · see citing works
Sellayah, D. (2019) · Journal of the Endocrine Society · doi:10.1210/js.2018-00363 · Cited by 21 · see citing works
Lee, K., Lee, Y., Kim, K., Chei, S., Jin, H., Oh, H., & Lee, B.-Y. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21062153 · Cited by 21 · see citing works
Robertson, C. E., & Wilsterman, K. (2020) · Journal of Experimental Biology · doi:10.1242/jeb.215350 · Cited by 20 · see citing works
Disruption of thermogenic UCP1 predated the divergence of pigs and peccaries
Fyda, T. J., Spencer, C., Jastroch, M., & Gaudry, M. J. (2020) · Journal of Experimental Biology · doi:10.1242/jeb.223974 · Cited by 17 · see citing works
Self-citationAdropin stimulates proliferation but suppresses differentiation in rat primary brown preadipocytes
Jasaszwili, M., Wojciechowicz, T., Strowski, M. Z., Nowak, K. W., & Skrzypski, M. (2020) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2020.108536 · Cited by 17 · see citing works
Shin, K. C., Huh, J. Y., Ji, Y., Han, J. S., Han, S. M., Park, J., Nahmgoong, H., Lee, W. T., Jeon, Y. G., Kim, B., et al. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111806 · Cited by 16 · see citing works
Verifying Feighner’s Hypothesis; Anorexia Nervosa Is Not a Psychiatric Disorder
Södersten, P., Brodin, U., Zandian, M., & Bergh, C. E. K. (2019) · Frontiers in Psychology · doi:10.3389/fpsyg.2019.02110 · Cited by 13 · see citing works
Convergent molecular evolution of thermogenesis and circadian rhythm in Arctic ruminants
Li, M., Li, X., Wu, Z., Zhang, G., Wang, N., Dou, M., Liu, S., Yang, C., Meng, G., Sun, H., et al. (2023) · Proceedings of the Royal Society B: Biological Sciences · doi:10.1098/rspb.2023.0538 · Cited by 12 · see citing works
Patel, B. V., Yao, F., Howenstine, A., Takenaka, R., Hyatt, J. A., Sears, K. E., & Shewchuk, B. M. (2020) · Journal of Molecular Biology · doi:10.1016/j.jmb.2020.09.022 · Cited by 12 · see citing works
Lu, W.-H., Chang, Y., & Huang, Y. (2021) · Frontiers in Pediatrics · doi:10.3389/fped.2020.612279 · Cited by 11 · see citing works
Brown Adipose Tissue: A Short Historical Perspective
Trayhurn, P. (2022) · Methods in molecular biology · doi:10.1007/978-1-0716-2087-8_1 · Cited by 12 · see citing works
Polyamine metabolism in macrophage–adipose tissue function and homeostasis
Pisani, D. F., Lettieri‐Barbato, D., & Ivanov, S. (2024) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2024.05.008 · Cited by 13 · see citing works
Holzman, M. A., Ryckman, A., Finkelstein, T. M., Landry‐Truchon, K., Schindler, K. A., Bergmann, J. M., Jeannotte, L., & Mansfield, J. H. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.632303 · Cited by 11 · see citing works
Gaudry, M. J., Keuper, M., & Jastroch, M. (2019) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2019.06.006 · Cited by 9 · see citing works
Self-citationMendes, T., Silva, L., Almeida, D., & Antunes, A. (2020) · Genomics · doi:10.1016/j.ygeno.2020.01.023 · Cited by 8 · see citing works
Gaudry, M. J., & Jastroch, M. (2021) · Comparative Biochemistry and Physiology Part B Biochemistry and Molecular Biology · doi:10.1016/j.cbpb.2021.110613 · Cited by 7 · see citing works
Self-citationPreadaptivity of Noncontractile Thermogenesis in the Evolution of Warm-Bloodedness in Vertebrates
Cherlin, V. A. (2023) · Biology Bulletin Reviews · doi:10.1134/s2079086423060051 · Cited by 7 · see citing works
Evolution of plasticity: metabolic compensation for fluctuating energy demands at the origin of life
Seebacher, F., & Beaman, J. E. (2022) · Journal of Experimental Biology · doi:10.1242/jeb.243214 · Cited by 6 · see citing works
Chazarin, B., Benhaim-Delarbre, M., Brun, C., Anzeraey, A., Bertile, F., & Terrien, J. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23084254 · Cited by 6 · see citing works
Equid Adaptations to Cold Environments
Cao, Q. L., Pukazhenthi, B. S., Bapodra, P., Lowe, S., & Bhatnagar, Y. V. (2023) · Fascinating life sciences · doi:10.1007/978-3-031-27144-1_8 · Cited by 5 · see citing works
Zhang, Z., Chen, N., Liu, R., Yin, N., He, Y., Li, D., Tong, M., Gao, A., Lu, P., Li, H., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.08.13.456245 · Cited by 4 · see citing works
Habuta, M., Fujita, H., Sato, K., Bando, T., Inoue, J., Kondo, Y., Miyaishi, S., Kumon, H., & Ohuchi, H. (2019) · Cell and Tissue Research · doi:10.1007/s00441-019-03113-8 · Cited by 3 · see citing works
Heimann, A. S., Singh, P., Ferro, E. S., Greenway, F. L., & Krongrad, A. (2025) · Diabetes/Metabolism Research and Reviews · doi:10.1002/dmrr.70056 · Cited by 3 · see citing works
Teplova, P. O., Kuznetsova, E. V., Gorbunova, A., Markevich, L. N., & Zakharova, N. M. (2025) · Comparative Biochemistry and Physiology Part A Molecular & Integrative Physiology · doi:10.1016/j.cbpa.2025.111953 · Cited by 1 · see citing works
Alvarez‐Salas, E., Soberanes-Chávez, P., Andrade, A., Dolores-SanJuan, J. L., García-Luna, C., Matamoros‐Trejo, G., & de Gortari, P. (2025) · Frontiers in Endocrinology · doi:10.3389/fendo.2025.1676754 · Cited by 1 · see citing works
Paulo, E., Wu, Y., & Wang, B. (2026) · iScience · doi:10.1016/j.isci.2026.116442 · Cited by 1 · see citing works
Cardiac Natriuretic Peptide System: A Link between Adipose Tissue, Obesity, and Insulin Resistance
Öztop, M. (2022) · IntechOpen eBooks · doi:10.5772/intechopen.104560 · Cited by 1 · see citing works
Wärmehaushalt: Adaptation und Regulation
Hildebrandt, J., Bleckmann, H., & Homberg, U. (2021) · Springer eBooks · doi:10.1007/978-3-662-61595-9_10 · Cited by 1 · see citing works
Paulo, E., Zhang, Y., Masand, R., Huynh, T. L., Seo, Y., Swaney, D. L., Soucheray, M., Jimenez‐Morales, D., Krogan, N. J., & Wang, B. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/610220
Two-Level Organization of Thermogenesis in Adipose Tissue: a Morphofunctional Hypothesis
Elsukova, E. I. (2019) · Journal of Evolutionary Biochemistry and Physiology · doi:10.1134/s0022093019050065
Mamushi, M. (2020) · SUNScholar (Stellenbosch University)
Paraspinal structures of thermoregulation
Gaivoronsky, I. V., Родионов, А. А., Gaivoronskiy, A. I., Gaivoronskaya, M. G., Ничипорук, Г. И., Александровна, Г. И., & Khabibullina, N. K. (2020) · Bulletin of the Russian Military Medical Academy · doi:10.17816/brmma50080
Browning of subcutaneous adipose tissue in wild-caught rodents of Siberia
Elsukova, E. I., & Yakunenkov, A. V. (2021) · IOP Conference Series Earth and Environmental Science · doi:10.1088/1755-1315/848/1/012226
RETRACTED: A chemical signal that promotes insect survival via thermogenesisPreprint
Zhao, L., Zhou, J., Chen, J., Zhang, X., Zhang, H., guo, L., Li, D., Ning, J., Wang, X., Jin, W., et al. (2023) · Research Square · doi:10.21203/rs.3.rs-2756320/v1
RetractedPreadaptivity of Non-Contractive Thermogenesis in the Evolution of Warm-Bloodedness in Vertebrates
Cherlin, V. A. (2023) · Успехи современной биологии · doi:10.31857/s004213242304004x
Branching out beyond canonical brown adipocyte function
Bank, H. C. V., & Simcox, J. (2024) · Cell Metabolism · doi:10.1016/j.cmet.2024.04.011
Tóth, B. B., Hegedűs, G., Virág, E., Pethő, G. T., Laczkó, L., & Fésüs, L. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.05.16.594487
Evolution of UCP1 Gene and Its Significance to Temperature Adaptation in Rodents
Liang, X., Wu, M., Nong, Q., Yang, S., Kan, T., & Feng, P. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26052155
Tóth, B. B., Hegedűs, G., Virág, E., Pethő, G. T., Laczkó, L., & Fésüs, L. (2025) · iScience · doi:10.1016/j.isci.2025.112969
Terrien, J. (2025) · Revue de primatologie · doi:10.4000/14ycc
Rôle des flux de lactate dans le métabolisme des tissus adipeux beiges et bruns
Lagarde, D. (2020) · theses.fr (ABES) · doi:10.70675/6dfcfe91z26c5z42a8z8f53zb5a5be6082a4
- Authors
- Jastroch, M., Oelkrug, R., & Keipert, S.
- Affiliations
- Philipps University of Marburg (DE)
- University of Lübeck (DE)
- Helmholtz Munich (DE)
- Corresponding author
- Jastroch, Martin
- Venue
- Journal of Experimental Biology
- Publisher
- The Company of Biologists
- Published
- 2018-03-07
- Volume
- 221
- Issue
- Suppl_1
- ISSN
- 0022-0949 (ISSN-L)
- 1477-9145
- OpenAlex
- W2793768356
- Cited by
- 55
- References
- 94
- Citations by year
- 2026: 1 · 2025: 6 · 2024: 3 · 2023: 6 · 2022: 5 · 2021: 8 · 2020: 16 · 2019: 7 · 2018: 3
- FWCI
- 1.12
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Experimental Biology (publishedVersion)
- PubMed (publishedVersion)
- Site cant be reached (submittedVersion)
- PuSH - Publication Server of Helmholtz Zentrum München (submittedVersion)
- Funders
- Deutsches Diabetes Zentrum
- Topics
- Health Sciences › Medicine › Physiology › Adipose Tissue and Metabolism
- Physical Sciences › Environmental Science › Ecology › Physiological and biochemical adaptations
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Bat Biology and Ecology Studies
- Keywords
- brown adipose tissue, UCP1, thermogenesis, non-model organisms, comparative biology, mammalian evolution, mitochondrial uncoupling, species diversity, metabolic disorders
- MeSH terms
- Uncoupling Protein 1, Animals, Adipose Tissue, Brown, Biological Evolution, Mammals, Thermogenesis
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