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Sympathetic and sensory innervation of brown adipose tissue
Open accessAbstract
The innervation of brown adipose tissue (BAT) by the sympathetic nervous system (SNS) is incontrovertible and, with its activation, functions as the principal, if not exclusive, stimulator of BAT thermogenesis. The parasympathetic innervation of BAT only appears in two minor BAT depots, but not in the major interscapular BAT (IBAT) depot. BAT thermogenesis is triggered by the release of norepinephrine from its sympathetic nerve terminals, stimulating β3-adrenoceptors that turns on a cascade of intracellular events ending in activation of uncoupling protein-1 (UCP-1). BAT also has sensory innervation that may function to monitor BAT lipolysis, a response necessary for activation of UCP-1 by fatty acids, or perhaps responding in a feedback manner to BAT temperature changes. The central sympathetic outflow circuits ultimately terminating in BAT have been revealed by injecting the retrograde viral transneuronal tract tracer, pseudorabies virus, into the tissue; moreover, there is a high degree of colocalization of melanocortin 4-receptor mRNA on these neurons across the neural axis. The necessary and sufficient central BAT SNS outflow sites that are activated by various thermogenic stimuli are not precisely known. In a chronic decerebration procedure, IBAT UCP-1 gene expression can be triggered by fourth ventricular injections of melanotan II, the melanocortin 3/4 receptor agonist, suggesting that there is sufficient hindbrain neural circuitry to generate thermogenic responses with this stimulation. The recent recognition of BAT in normal adult humans suggests a potential target for stimulation of energy expenditure by BAT to help mitigate increased body fat storage.
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“These nerves express tyrosine hydroxylase, the enzyme responsible for the secretion of the catecholamine hormone NE 84.”
From Inter‐organ communication: a gatekeeper for metabolic health (2019) · cites this paper as [84]
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Cites
Positional cloning of the mouse obese gene and its human homologue
Zhang, Y., Proenca, R., Maffei, M., Barone, M., Leopold, L., & Friedman, J. M. (1994) · Nature · doi:10.1038/372425a0 · Cited by 13,419
Prevalence of Overweight and Obesity in the United States, 1999-2004
Ogden, C. L., Carroll, M. D., Curtin, L. R., McDowell, M. A., Tabak, C. J., & Flegal, K. M. (2006) · JAMA · doi:10.1001/jama.295.13.1549 · Cited by 8,720
Brown Adipose Tissue: Function and Physiological Significance
CANNON, B., & NEDERGAARD, J. (2004) · Physiological Reviews · doi:10.1152/physrev.00015.2003 · Cited by 6,433
Leptin and the regulation of body weight in mammals
Friedman, J. M., & Halaas, J. L. (1998) · Nature · doi:10.1038/27376 · Cited by 5,405
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
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
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
Excess Deaths Associated With Underweight, Overweight, and Obesity
Flegal, K. M. (2005) · JAMA · doi:10.1001/jama.293.15.1861 · Cited by 2,811
Fat Mobilization in Adipose Tissue Is Promoted by Adipose Triglyceride Lipase
Zimmermann, R., Bogner‐Strauß, J. G., Haemmerle, G., Schoiswohl, G., Birner‐Gruenberger, R., Riederer, M., Lass, A., Neuberger, G., Eisenhaber, F., Hermetter, A., et al. (2004) · Science · doi:10.1126/science.1100747 · Cited by 2,121
The James-Lange Theory of Emotions: A Critical Examination and an Alternative Theory
Cannon, W. B. (1927) · The American Journal of Psychology · doi:10.2307/1415404 · Cited by 1,899
Flagged first, then by citations
1 of the 295 references couldn’t be matched to a known paper.
Research works printed but not linked: 3
- Gesner C . Medici Tigurini Historiae Animalium Liber I de Quadrupedibusuiuiparis. Froschauer, 1551, pp 840–844.
- Heldmaier G, Klaus S, Wiesinger H, Friedrichs U, Wenzel M . Cold acclimation and thermogenesis. In: Malan A, Canguilhem B (eds). Living in the Cold II. John Libbey Eurotext: Montrouge, France, 1989, pp 347–358.
- Song CK, Smith B, Nguyen N, Bartness TJ . Convergence of Efferent and Afferent Circuits to White Adipose Tissue in Siberian Hamsters. Society for Neuroscience: Neuroscience Meeting Planner Chicago, IL, Online 2009.
Cited by
Sorted by citations
What we talk about when we talk about fat
Rosen, E. D., & Spiegelman, B. M. (2014) · Cell · doi:10.1016/j.cell.2013.12.012 · Cited by 2,373
“Classic brown adipocytes cluster as specific depots located in the interscapular and perirenal regions of rodents and are richly innervated and vascularized (Bartness et al., 2010b).”
Adipocyte dysfunctions linking obesity to insulin resistance and type 2 diabetes.
Guilherme, A., Virbasius, J. V., Puri, V., & Czech, M. P. (2008) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2391 · Cited by 2,292
Brown Remodeling of White Adipose Tissue by SirT1-Dependent Deacetylation of Pparγ
Qiang, L., Wang, L., Kon, N., Zhao, W., Lee, S., Zhang, Y., ROSENBAUM, M. S., Zhao, Y., Gu, W. J., Farmer, S. R., et al. (2012) · Cell · doi:10.1016/j.cell.2012.06.027 · Cited by 816
“This might be related to sympathetic innervation, a key modulator of BAT and Ucp1 induction in WAT (Bartness et al., 2010).”
Adipose tissue in control of metabolism
Luo, L., & Liu, M. (2016) · Journal of Endocrinology · doi:10.1530/joe-16-0211 · Cited by 764
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 697
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 487
Physical Activity and Exercise in the Regulation of Human Adipose Tissue Physiology
Thompson, D., Karpe, F., Lafontan, M., & Frayn, K. N. (2012) · Physiological Reviews · doi:10.1152/physrev.00012.2011 · Cited by 425
Broussard, J. L., Ehrmann, D. A., Van Cauter, E., Tasali, E., & Brady, M. J. (2012) · Annals of Internal Medicine · doi:10.7326/0003-4819-157-8-201210160-00005 · Cited by 364
Neural innervation of white adipose tissue and the control of lipolysis
Bartness, T. J., Liu, Y., Shrestha, Y. B., & Ryu, V. (2014) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2014.04.001 · Cited by 370
“Because we also have reviewed the SNS innervation of WAT recently and across the years (e.g., Bartness et al., 1993, 2010, 2005; Bartness and Song, 2007a,b), we will make every attempt not to repeat this information, although some reiteration is necessary.”
BackgroundMethodInfluentialSelf-citationCinti, S. (2012) · Disease Models & Mechanisms · doi:10.1242/dmm.009662 · Cited by 370
“Dynamics of adipose organ composition Innervation and adaptation to temperature changes The adipose organ is innervated (Bartness and Bamshad, 1998; Giordano et al., 2008; Bartness et al., 2010), enabling it to interface with the nervous system and respond to physiological and environmental cues.”
BackgroundFischer, K., Ruiz, H. H., Jhun, K., Finan, B., Oberlin, D. J., van der Heide, V., Kalinovich, A., Petrovič, N., Wolf, Y., Clemmensen, C., et al. (2017) · Nature Medicine · doi:10.1038/nm.4316 · Cited by 333
Saper, C. B., & Stornetta, R. L. (2004) · Elsevier eBooks · doi:10.1016/b978-0-12-374245-2.00023-1 · Cited by 325
Enriori, P. J., Sinnayah, P., Simonds, S. E., Rudaz, C. G., & Cowley, M. A. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.2336-11.2011 · Cited by 319
“BAT is innervated exclusively by the SNS (Bartness et al., 2010).”
BackgroundSensory and sympathetic nervous system control of white adipose tissue lipolysis
Bartness, T. J., Shrestha, Y. B., Vaughan, C. H., Schwartz, G. J., & Song, C. K. (2010) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2009.08.031 · Cited by 289
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 297
“…afferent signals to the preoptic area in the hypothalamus (Morrison et al. 2014) and to control regions in the brain stem (Nautiyal et al. 2008; Bartness et al. 2010), leading to the activation of postganglionic sympathetic fibers that release noradrenaline to activate BAT (reviewed by Lowell…”
BackgroundBrown-adipose-tissue macrophages control tissue innervation and homeostatic energy expenditure
Wolf, Y., Boura‐Halfon, S., Cortese, N., Haimon, Z., Shalom, H. S., Kuperman, Y., Kalchenko, V., Brandis, A. S., David, E., Segal-Hayoun, Y., et al. (2017) · Nature Immunology · doi:10.1038/ni.3746 · Cited by 264
“Each murine iBAT lobe displays postganglionic sympathetic innervation 26, as can be visualized in Thy1-YFP animals (Fig.”
Secretin-Activated Brown Fat Mediates Prandial Thermogenesis to Induce Satiation
Li, Y., Schnabl, K., Gabler, S.-M., Willershäuser, M., Reber, J., Karlas, A., Laurila, S., Lahesmaa, M., u Din, M., Bast-Habersbrunner, A., et al. (2018) · Cell · doi:10.1016/j.cell.2018.10.016 · Cited by 228
GABAergic RIP-Cre Neurons in the Arcuate Nucleus Selectively Regulate Energy Expenditure
Kong, D., Tong, Q., Ye, C., Koda, S., Fuller, P. M., Krashes, M. J., Vong, L., Ray, R. S., Olson, D. P., & Lowell, B. B. (2012) · Cell · doi:10.1016/j.cell.2012.09.020 · Cited by 215
Central Fibroblast Growth Factor 21 Browns White Fat via Sympathetic Action in Male Mice
Douris, N., Stevanovic, D. M., Fisher, F. M., Cisu, T. I., Chee, M. J., Nguyen, N. L., Zarebidaki, E., Adams, A. C., Kharitonenkov, A., Flier, J. S., et al. (2015) · Endocrinology · doi:10.1210/en.2014-2001 · Cited by 215
Self-citationBrown Adipose Crosstalk in Tissue Plasticity and Human Metabolism
Schéele, C., & Wolfrum, C. (2019) · Endocrine Reviews · doi:10.1210/endrev/bnz007 · Cited by 224
“BAT also exhibits afferent neurons, which feedback on brain regions controlling sympathetic activation of BAT (97).”
BackgroundCohen, P., & Spiegelman, B. M. (2016) · Molecular Biology of the Cell · doi:10.1091/mbc.e15-10-0749 · Cited by 217
“Adipose tissue, particularly brown fat, is also extensively innervated with sympathetic fibers that stimulate lipolysis in the setting of fasting, leptin administration, and cold exposure (Bartness et al., 2010a,b; Zeng et al., 2015).”
BackgroundAdipose tissue at single-cell resolution
Maniyadath, B., Zhang, Q., Gupta, R. K., & Mandrup, S. (2023) · Cell Metabolism · doi:10.1016/j.cmet.2023.02.002 · Cited by 218
Brown Adipose Tissue—A Translational Perspective
Carpentier, A. C., Blondin, D. P., Haman, F., & Richard, D. (2022) · Endocrine Reviews · doi:10.1210/endrev/bnac015 · Cited by 218
Gestational Hypoxia and Developmental Plasticity
Ducsay, C. A., Goyal, R., Pearce, W. J., Wilson, S. M., Hu, X., & Zhang, L. (2018) · Physiological Reviews · doi:10.1152/physrev.00043.2017 · Cited by 208
Central Control of Brown Adipose Tissue Thermogenesis
Morrison, S. F., Madden, C. J., & Tupone, D. (2012) · Frontiers in Endocrinology · doi:10.3389/fendo.2012.00005 · Cited by 199
“Another group of afferents likely to influence BAT thermogenesis (Niijima, 1999) arise from both BAT (Bartness et al., 2010) and white adipose tissue (Song et al.”
BackgroundHypothalamic-autonomic control of energy homeostasis
Seoane‐Collazo, P., Fernø, J., González, F., Diéguez, C., Leis, R., Nogueiras, R., & López, M. (2015) · Endocrine · doi:10.1007/s12020-015-0658-y · Cited by 189
Rutin ameliorates obesity through brown fat activation
Yuan, X., Wei, G., You, Y., Huang, Y., Lee, H. J., Dong, M., Lin, J., Hu, T., Zhang, H., Zhang, C.-H., et al. (2016) · The FASEB Journal · doi:10.1096/fj.201600459rr · Cited by 184
“Although we cannot exclude the possibility that rutin regulates whole-body energy metabolism via enhancing BAT metabolic activity through stimulating the sympathetic nervous system (50), the cellular experiments indicated that rutin directly activated BAT oxidation in vitro (Fig.”
BackgroundNogueiras, R., Pérez-Tilve, D., Veyrat-Durebex, C., Morgan, D. A., Varela, L., Haynes, W. G., Patterson, J. T., Disse, E., Pfluger, P. T., López, M., et al. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.5977-08.2009 · Cited by 182
The adipose organ: white‐brown adipocyte plasticity and metabolic inflammation
Smorlesi, A., Frontini, A., Giordano, A., & Cinti, S. (2012) · Obesity Reviews · doi:10.1111/j.1467-789x.2012.01039.x · Cited by 189
Inter‐organ communication: a gatekeeper for metabolic health
Castillo‐Armengol, J., Fajas, L., & Lopez‐Mejia, I. C. (2019) · The EMBO Reports · doi:10.15252/embr.201947903 · Cited by 178
“Finally, FGF 21 can be produced by WAT; and BMP 8 b and FGF 21 can be produced by BAT, after cold activation and promote thermogenesis in a paracrine manner. hydroxylase, the enzyme responsible for the secretion of the catecholamine hormone NE [84].”
The physiological control of eating: signals, neurons, and networks
Watts, A. G., Kanoski, S. E., Sanchez-Watts, G., & Langhans, W. (2022) · Physiological Reviews · doi:10.1152/physrev.00028.2020 · Cited by 168
Brito, M. N., Brito, N. A., Baro, D. J., Song, C. K., & Bartness, T. J. (2007) · Endocrinology · doi:10.1210/en.2007-0621 · Cited by 167
Self-citationBartolomucci, A., Cabassi, A., Govoni, P., Ceresini, G., Cero, C., Berra, D., Dadomo, H., Franceschini, P., Dell’Omo, G., Parmigiani, S., et al. (2009) · PLoS ONE · doi:10.1371/journal.pone.0004331 · Cited by 173
Adipose Organ Development and Remodeling
Cinti, S. (2018) · Comprehensive physiology · doi:10.1002/cphy.c170042 · Cited by 197
Neuro-mesenchymal units control ILC2 and obesity via a brain–adipose circuit
Cardoso, F., Klein Wolterink, R. G. J., Godinho-Silva, C., Domingues, R. G., Ribeiro, H., da Silva, J. A., Mahú, I., Domingos, A. I., & Veiga-Fernandes, H. (2021) · Nature · doi:10.1038/s41586-021-03830-7 · Cited by 159
Contreras, C., González, F., Fernø, J., Diéguez, C., Rahmouni, K., Nogueiras, R., & López, M. (2014) · Annals of Medicine · doi:10.3109/07853890.2014.919727 · Cited by 167
Free radicals and male reproduction.
Agarwal, A. K., & Allamaneni, S. S. R. (2011) · PubMed · Cited by 154
Neuroimmune Interactions in Peripheral Organs
Wolterink, R. G. J. K., Wu, G. S., Chiu, I. M., & Veiga‐Fernandes, H. (2022) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-111020-105359 · Cited by 166
The role of leptin in health and disease
Ramos-Lobo, A. M., & Donato, J. (2017) · Temperature · doi:10.1080/23328940.2017.1327003 · Cited by 172
“BAT is innervated by the sympathetic nervous system and the activation of UCP1 is mainly regulated by b3-adrenergic receptors.(128) Rats treated with leptin showed increased oxygen consumption and UCP1 mRNA expression, and this response is elevated after fasting.”
BackgroundUCP1-independent thermogenesis
Roesler, A. A., & Kazak, L. (2020) · Biochemical Journal · doi:10.1042/bcj20190463 · Cited by 163
Central nervous system regulation of organismal energy and glucose homeostasis
Myers, M. G., Affinati, A. H., Richardson, N. E., & Schwartz, M. W. (2021) · Nature Metabolism · doi:10.1038/s42255-021-00408-5 · Cited by 165
CRTC3 links catecholamine signalling to energy balance
Song, Y., Altarejos, J. Y., Goodarzi, M. O., Inoue, H., Guo, X., Berdeaux, R., Kim, J., Goode, J., Igata, M., Paz, J. C., et al. (2010) · Nature · doi:10.1038/nature09564 · Cited by 155
Fibroblast growth factor 21 and browning of white adipose tissue
Cuevas-Ramos, D., Mehta, R., & Aguilar-Salinas, C. A. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2019.00037 · Cited by 149
Song, C. K., Vaughan, C. H., Keen‐Rhinehart, E., Harris, R. B. S., Richard, D., & Bartness, T. J. (2008) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00174.2008 · Cited by 146
Self-citationAdipose tissue: friend or foe?
Hassan, M. S., Latif, N., & Yacoub, M. H. (2012) · Nature Reviews Cardiology · doi:10.1038/nrcardio.2012.148 · Cited by 146
Hypothalamus-adipose tissue crosstalk: neuropeptide Y and the regulation of energy metabolism
Zhang, W., Cline, M. A., & Gilbert, E. R. (2014) · Nutrition & Metabolism · doi:10.1186/1743-7075-11-27 · Cited by 144
Immune and non-immune functions of adipose tissue leukocytes
Trim, W. V., & Lynch, L. (2021) · Nature reviews. Immunology · doi:10.1038/s41577-021-00635-7 · Cited by 155
Song, C. K., Schwartz, G. J., & Bartness, T. J. (2008) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.90786.2008 · Cited by 141
Self-citationGeerling, J. J., Boon, M. R., Kooijman, S., Parlevliet, E. T., Havekes, L. M., Romijn, J. A., Meurs, I. M., & Rensen, P. C. N. (2014) · Journal of Lipid Research · doi:10.1194/jlr.r045013 · Cited by 137
Brito, N. A., Brito, M. N., & Bartness, T. J. (2008) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00068.2008 · Cited by 137
Self-citationCentral Nervous System Regulation of Brown Adipose Tissue
Morrison, S. F., & Madden, C. J. (2014) · Comprehensive physiology · doi:10.1002/cphy.c140013 · Cited by 161
Johansen, O. S., Ma, T., Hansen, J. B., Markussen, L. K., Schreiber, R., Reverte-Salisa, L., Dong, H., Christensen, D. P., Sun, W., Gnad, T., et al. (2021) · Cell · doi:10.1016/j.cell.2021.04.037 · Cited by 134
Szewczyk‐Golec, K., Woźniak, A., & Reiter, R. J. (2015) · Journal of Pineal Research · doi:10.1111/jpi.12257 · Cited by 153
Burwell, R. G., Aujla, R. K., Grevitt, M. P., Dangerfield, P., Moulton, A., Randell, T. L., & Anderson, S. (2009) · Scoliosis · doi:10.1186/1748-7161-4-24 · Cited by 130
Vaughan, C. H., Zarebidaki, E., Ehlen, J. C., & Bartness, T. J. (2014) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/b978-0-12-411619-1.00011-2 · Cited by 124
“…outflow from brain to BAT (Bamshad, Song, & Bartness, 1999; Oldfield et al., 2002; Song et al., 2008; Zhang et al., 2011) and destruction of the SNS innervation of BAT blocks or severely diminishes BAT responses to all thermogenic challenges tested to date (for review, see Bartness et al., 2010).”
BackgroundSelf-citationObesity: A neuroimmunometabolic perspective
Larabee, C. M., Neely, O. C., & Domingos, A. I. (2020) · Nature Reviews Endocrinology · doi:10.1038/s41574-019-0283-6 · Cited by 123
Central control of thermogenesis
Clapham, J. C. (2011) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.10.014 · Cited by 128
Sex differences in sympathetic innervation and browning of white adipose tissue of mice
Kim, S.-N., Jung, Y.-S., Kwon, H.-J., Seong, J. K., Granneman, J. G., & Lee, Y.-H. (2016) · Biology of Sex Differences · doi:10.1186/s13293-016-0121-7 · Cited by 122
“While BAT is more densely innervated by peripheral sympathetic nerves than WAT [10, 11], innervation levels of adipose tissues positively correlate with the ability to recruit brown adipocytes in WAT [12].”
BackgroundBellocchio, L., Gómez, E. S., Quarta, C., Metna‐Laurent, M., Cardinal, P., Binder, E., Cannich, A., Delamarre, A., Häring, M., Martín‐Fontecha, M., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1218573110 · Cited by 118
“To further confirm the activation of peripheral SNS under our study conditions, we analyzed different biochemical parameters also in the brown adipose tissue (BAT), an organ whose functions are critically under the control of the SNS (37).”
MethodRole of leptin resistance in the development of obesity in older patients
Picard, F., Carter, S., Caron, A., & Richard, D. (2013) · Clinical Interventions in Aging · doi:10.2147/cia.s36367 · Cited by 134
“46 Indeed, it has been shown that intracerebroventricular administration of leptin significantly increases insulin sensitivity, glucose utilization, and glucose uptake in peripheral tissue including BAT.”
InfluentialKolditz, C.-I., & Langin, D. (2010) · Current Opinion in Clinical Nutrition & Metabolic Care · doi:10.1097/mco.0b013e32833bed6a · Cited by 124
The Circadian Clock in the Ventromedial Hypothalamus Controls Cyclic Energy Expenditure
Orozco-Solís, R., Aguilar‐Arnal, L., Murakami, M., Peruquetti, R. L., Ramadori, G., Coppari, R., & Sassone‐Corsi, P. (2016) · Cell Metabolism · doi:10.1016/j.cmet.2016.02.003 · Cited by 123
“This parallels the notions that the BAT is densely innervated by sympathetic efferents (Bartness et al., 2010) and that the sympathetic system controls circadian peripheral functions, including the cyclic fluctuation of epinephrine(Gamble et al.”
BackgroundBrown Adipose Tissue Has Sympathetic-Sensory Feedback Circuits
Ryu, V., Garretson, J. T., Liu, Y., Vaughan, C. H., & Bartness, T. J. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.3306-14.2015 · Cited by 113
“By contrast, WAT stores/releases lipid and adipokines and has afferents sensitive to both increases in SNS drive (Bartness et al., 2010a) and to leptin (Murphy et al., 2013), that latter perhaps conveying the amounts of stored lipid via this neural conduit (Bartness et al., 2014).”
BackgroundSelf-citationGLP-1 Influences Food and Drug Reward
Hayes, M. R., & Schmidt, H. D. (2016) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2016.02.005 · Cited by 108
Transcriptional Control of Brown and Beige Fat Development and Function
Shapira, S. N., & Seale, P. (2018) · Obesity · doi:10.1002/oby.22334 · Cited by 111
“Cold is sensed through the central nervous system, which rapidly elicits sympathetic outflow to brown and white adipose depots (17, 18).”
BackgroundLafontan, M. (2011) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00168.2011 · Cited by 118
Cognitive and autonomic determinants of energy homeostasis in obesity
Richard, D. (2015) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2015.103 · Cited by 113
Hypothalamic control of brown adipose tissue thermogenesis
Labbé, S. M., Caron, A., Lanfray, D., Monge-Roffarello, B., Bartness, T. J., & Richard, D. (2015) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2015.00150 · Cited by 112
“SNS Control of Brown Adipose Tissue BAT thermogenesis is highly dependent on the SNS (Bartness et al., 2010; Bartness and Ryu, 2015).”
BackgroundInfluentialSelf-citationJastroch, M., Giroud, S., Barrett, P., Geiser, F., Heldmaier, G., & Herwig, A. (2016) · Journal of Neuroendocrinology · doi:10.1111/jne.12437 · Cited by 105
“BAT thermogenesis is controlled by dense innervation of sympathetic nerve fibres descending from the central nervous system (92, 93).”
BackgroundVaughan, C. H., & Bartness, T. J. (2012) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00640.2011 · Cited by 104
Self-citationHypothalamus and thermogenesis: Heating the BAT, browning the WAT
Contreras, C., Nogueiras, R., Diéguez, C., Medina‐Gómez, G., & López, M. (2016) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2016.08.002 · Cited by 104
Liu, X., Zhang, Z., Song, Y., Xie, H., & Dong, M. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.1065263 · Cited by 102
Traveling from the hypothalamus to the adipose tissue: The thermogenic pathway
Contreras, C., Nogueiras, R., Diéguez, C., Rahmouni, K., & López, M. (2017) · Redox Biology · doi:10.1016/j.redox.2017.04.019 · Cited by 104
“Furthermore there is evidence for anatomical connection between the PVH and the BAT [4,63,114].”
BackgroundParisi, V., Rengo, G., Filardi, P. P., Pagano, G., Femminella, G. D., Paolillo, S., Petraglia, L., Gambino, G., Caruso, A., Grimaldi, M. G., et al. (2016) · Circulation Research · doi:10.1161/circresaha.115.307765 · Cited by 101
Townsend, K. L., An, D., Lynes, M. D., Huang, T. L., Zhang, H., Goodyear, L. J., & Tseng, Y. (2012) · Antioxidants and Redox Signaling · doi:10.1089/ars.2012.4536 · Cited by 97
“Based on the data collected in this study, we propose that BMP7, after binding to its receptor–heterodimer on the cell surface of mature brown adipocytes [1], activates the SMAD and p38-ATF2 signaling pathways [2], followed by increased expression of mitochondrial fatty acid transporter, CPT1 [3], which is further act…”
Understanding the brown adipocyte as a contributor to energy homeostasis
Chechi, K., Carpentier, A. C., & Richard, D. (2013) · Trends in Endocrinology & Metabolism · doi:10.1016/j.tem.2013.04.002 · Cited by 99
Purinergic transmission in blood vessels
Ralevic, V., & Dunn, W. R. (2015) · Autonomic Neuroscience · doi:10.1016/j.autneu.2015.04.007 · Cited by 95
“, 2003), or sensory (Bartness and Bamshad, 1998; Bartness et al., 2010) innervation is limited.”
BackgroundBatokines: Mediators of Inter-Tissue Communication (a Mini-Review)
Yang, F. T., & Stanford, K. I. (2022) · Current Obesity Reports · doi:10.1007/s13679-021-00465-7 · Cited by 100
“BAT activation upon cold exposure is due to increased sympathetic outflow of norepinephrine [16] which primarily acts on β3-adrenergic receptors.”
BackgroundMannerås, L., Cajander, S. B., Lönn, M., & Stener‐Victorin, E. (2009) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.90947.2008 · Cited by 95
Regulatory microRNAs in Brown, Brite and White Adipose Tissue
Gharanei, S., Shabir, K., Brown, J. E. P., Weickert, M. O., Barber, T. M., Kyrou, I., & Randeva, H. S. (2020) · Cells · doi:10.3390/cells9112489 · Cited by 100
Functional involvement of β3-adrenergic receptors in melanoma growth and vascularization
Monte, M. D., Casini, G., Filippi, L., Nicchia, G. P., Svelto, M., & Bagnoli, P. (2013) · Journal of Molecular Medicine · doi:10.1007/s00109-013-1073-6 · Cited by 93
“thermogenesis [19], while subsequently it has been described to play important roles in the pathophysiology of the cardiovascular system [20] and the urinary tract [21, 22].”
BackgroundBrain–gut–adipose-tissue communication pathways at a glance
Yi, C., & Tschöp, M. H. (2012) · Disease Models & Mechanisms · doi:10.1242/dmm.009902 · Cited by 98
“Are there neurochemical characteristics specific to each subtype of preautonomic neuron that enable their connections to peripheral organs or tissues (Bartness et al., 2010a; Oldfield et al., 2007; Oldfield et al., 2002)?”
BackgroundBrown adipose tissue as an anti‐obesity tissue in humans
Chechi, K., Nedergaard, J., & Richard, D. (2013) · Obesity Reviews · doi:10.1111/obr.12116 · Cited by 98
“to interscapular BAT, being the most commonly studied classical BAT depot) are distributed in most brain areas including forebrain, midbrain and brainstem such as the preoptic area, zona incerta, suprachiasmatic nucleus, retrochiasmatic area, dorsomedial hypothalamus, paraventricular hypothalamus, lateral hypothalamus…”
BackgroundPeripheral Innervation in the Regulation of Glucose Homeostasis
Lin, E. E., Scott-Solomon, E., & Kuruvilla, R. (2020) · Trends in Neurosciences · doi:10.1016/j.tins.2020.10.015 · Cited by 92
“Parasympathetic nerves are barely detected in adipose tissue, and their role in adipose functions have been proposed to be minor [68].”
BackgroundNeuropathy and neural plasticity in the subcutaneous white adipose depot
Blaszkiewicz, M., Willows, J. W., Dubois, A. L., Waible, S., DiBello, K., Lyons, L. L., Johnson, C. P., Paradie, E., Banks, N., Motyl, K., et al. (2019) · PLOS ONE · doi:10.1371/journal.pone.0221766 · Cited by 87
Xiong, X.-Q., Chen, W.-W., Han, Y., Zhou, Y.-B., Zhang, F., Gao, X.-Y., & Zhu, G.-Q. (2012) · Hypertension · doi:10.1161/hypertensionaha.112.198002 · Cited by 85
Henriques, F. D. S., Bedard, A. H., Guilherme, A., Kelly, M., Chi, J., Zhang, P., Lifshitz, L. M., Bellve, K. D., Rowland, L. A., Yenilmez, B., et al. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.107998 · Cited by 83
“, 2009) and are controlled by activation of local sympathetic nerve fiber (SNF) activity (Bartness et al., 2010; Chi et al., 2018; Guilherme et al., 2019; Jiang et al., 2017).”
Perivascular Adipose Tissue: the Sixth Man of the Cardiovascular System
Cheng, C. K., Bakar, H. A., Gollasch, M., & Huang, Y. (2018) · Cardiovascular Drugs and Therapy · doi:10.1007/s10557-018-6820-z · Cited by 84
Induction of thermogenic adipocytes: molecular targets and thermogenic small molecules
Song, N.-J., Chang, S., Li, D. Y., Villanueva, C. J., & Park, K. W. (2017) · Experimental & Molecular Medicine · doi:10.1038/emm.2017.70 · Cited by 81
Adipocyte dedifferentiation in health and diseases
Song, T., & Kuang, S. (2019) · Clinical Science · doi:10.1042/cs20190128 · Cited by 82
Nguyen, N. L. T., Barr, C. L., Ryu, V., Cao, Q., Xue, B., & Bartness, T. J. (2016) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00344.2016 · Cited by 75
“In addition, the SNS outflow to WAT and BAT in Siberian hamsters has been extensively characterized (5, 8) and the SNS innervation of their fat tissues is comparable to other mammals with more similarities than differences in the general pattern (2, 42).”
BackgroundSelf-citationLoss of MyoD Promotes Fate Transdifferentiation of Myoblasts Into Brown Adipocytes
Wang, C., Liu, W., Nie, Y., Qaher, M., Horton, H. E., Yue, F., Asakura, A., & Kuang, S. (2017) · EBioMedicine · doi:10.1016/j.ebiom.2017.01.015 · Cited by 78
“This observation suggests that additional factors, such as Notch signaling and sympathetic innervation (Bartness et al., 2010; Pasut et al., 2016), may be required to induce UCP1 expression in the transdifferentiated MyoD adipocytes.”
BackgroundIntact innervation is essential for diet-induced recruitment of brown adipose tissue
Fischer, A. W., Schlein, C., Cannon, B., Heeren, J., & Nedergaard, J. (2018) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00443.2018 · Cited by 74
Poggioli, R., Ueta, C. B., Drigo, R. A. E., Castillo, M., Fonseca, T. L., & Bianco, A. C. (2013) · Obesity · doi:10.1002/oby.20338 · Cited by 77
“β3-induced acceleration of VO2 reflects the potential for adaptive thermogenesis and is thought to take place predominantly in BAT (13, 32).”
BackgroundPham, T. L., He, J., Kakazu, A. H., Jun, B., Bazan, N. G., & Bazán, H. E. P. (2017) · Journal of Biological Chemistry · doi:10.1074/jbc.m117.801472 · Cited by 71
“The PEDF-R is enriched in white and brown adipose tissues, which are innervated by sensory calcitonin gene-related peptide (CGRP)- and substance P (SP)-positive nerves (17, 18).”
BackgroundThe Importance of Peripheral Nerves in Adipose Tissue for the Regulation of Energy Balance
Blaszkiewicz, M., Willows, J. W., Johnson, C. P., & Townsend, K. L. (2019) · Biology · doi:10.3390/biology8010010 · Cited by 71
Peripheral neuropeptide Y Y1 receptors regulate lipid oxidation and fat accretion
Zhang, L., Macia, L., Turner, N. A., Enriquez, R. F., Riepler, S. J., Nguyen, A., Lin, S., Lee, N. J., Shi, Y. C., Yulyaningsih, E., et al. (2009) · International Journal of Obesity · doi:10.1038/ijo.2009.232 · Cited by 69
Adrenergic regulation of cellular plasticity in brown, beige/brite and white adipose tissues
Ramseyer, V. D., & Granneman, J. G. (2016) · Adipocyte · doi:10.1080/21623945.2016.1145846 · Cited by 68
“sympathetic innervation of both BAT and WAT has been demonstrated consistently by a variety of methods (for review see refs.(14,17)) including immunochemical detection of tyrosine hydroxylase,(22-26) fluorogold retrograde tracing(27) and electrical recording of nerve activity.”
MethodAdler, E. S., Hollis, J. H., Clarke, I. J., Grattan, D. R., & Oldfield, B. J. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.2591-12.2012 · Cited by 69
Neuronal systems and circuits involved in the control of food intake and adaptive thermogenesis
Caron, A., & Richard, D. (2016) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.13263 · Cited by 69
Metadata
- Authors
- Bartness, T. J., Vaughan, C. H., & Song, C. K.
- Affiliations
- Georgia State University (US)
- Corresponding author
- Bartness, T J
- ORCID
- Bartness, T J
- Venue
- International Journal of Obesity
- Published
- 2010-10
- Volume
- 34
- Issue
- S1
- Pages
- S36-S42
- ISSN
- 0307-0565 (ISSN-L)
- 1476-5497
- PMC
- PMC3999344
- OpenAlex
- W1991845771
- Cited by
- 459
- References
- 295
- Citations by year
- 2026: 17 · 2025: 20 · 2024: 29 · 2023: 32 · 2022: 29 · 2021: 22 · 2020: 35 · 2019: 28 · 2018: 25 · 2017: 33 · 2016: 29 · 2015: 26 · 2014: 18 · 2013: 29 · 2012: 41
- FWCI
- 2.86
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- International Journal of Obesity (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Diabetes and Digestive and Kidney Diseases (R37DK35254, R37DK035254)
- Topics
- Health Sciences › Medicine › Physiology (medical) › Adipose Tissue and Metabolism
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Regulation of Appetite and Obesity
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Lipid metabolism and biosynthesis
- Keywords
- brown adipose tissue, sympathetic innervation, parasympathetic innervation, thermogenesis, norepinephrine, beta3-adrenergic receptor, UCP1, sensory innervation, melanocortin-4 receptor, melanotan II, energy expenditure, pseudorabies virus tracing
- MeSH terms
- Uncoupling Protein 1, Animals, Adipose Tissue, Brown, Humans, Ion Channels, Sympathetic Nervous System, Thermogenesis, Mitochondrial Proteins
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