Cited by 459Adipose Tissue and MetabolismRegulation of Appetite and ObesityLipid metabolism and biosynthesis

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Sympathetic and sensory innervation of brown adipose tissue

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Bartness, T J, Vaughan, C H, Song, C K·2010·International Journal of Obesity

DOI 10.1038/ijo.2010.182PMC PMC3999344

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Abstract

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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Background
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Background
Energetic responses to cold temperatures in rats lacking forebrain-caudal brain stem connections
Nautiyal, K. M., Dailey, M. J., Brito, N. A., Brito, M. N., Harris, R. B. S., Bartness, T. J., & Grill, H. J. (2008) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.90394.2008 · Cited by 29
Self-citation
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Background
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BackgroundInfluential
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“As a sympathetic nerve enrichment organ (50, 51), cold-induced enlargement of BAT is well defined (28).”
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Inhibition of the central melanocortin system decreases brown adipose tissue activity
Kooijman, S., Boon, M. R., Parlevliet, E. T., Geerling, J. J., van de Pol, V., Romijn, J. A., Havekes, L. M., Meurs, I., & Rensen, P. C. N. (2014) · Journal of Lipid Research · doi:10.1194/jlr.m045989 · Cited by 27
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BackgroundMethodInfluential
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Background
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“BAT is known to be strongly innervated by the sympathetic nervous system, which activates BAT following a variety of stimuli, of which cold exposure is the best known (76).”
Background
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“BAT activation has also been related to adrenoreceptor stimulation in response to cold temperatures which is translated in increased levels of UPC1 and in browning of white adipocytes [9,10].”
Background
Increased fat:carbohydrate oxidation ratio in Il1ra −/− mice on a high-fat diet is associated with increased sympathetic tone
Chida, D., Hashimoto, O., Kuwahara, M., Sagara, H., Osaka, T., Tsubone, H., & Iwakura, Y. (2008) · Diabetologia · doi:10.1007/s00125-008-1075-z · Cited by 20
Somatosensory innervation of adipose tissues
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“We have found that UCP-1 mRNA upregulation in BAT after an optimal dose of cocoa flavanol is markedly attenuated by co-administration of β3 blocker.”
BackgroundInfluential
Noradrenaline enhances angiotensin II responses via p38 MAPK activation after hypoxia/re‐oxygenation in renal interlobar arteries
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“A considerable expression has been shown particularly in brown adipose tissue (Bartness et al. 2010).”
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Reversine promotes browning of white adipocytes by suppressing miR‐133a
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“The sparse knowledge regarding systemic or neural mediation of muscle thermogenesis stands in stark contrast to the detailed understanding of the neural processes controlling the induction of brown adipose tissue (BAT) thermogenesis (Bartness et al., 2010; Contreras et al., 2017; Morrison and Nakamura, 2019).”
Background
Repeated Cold Stress Enhances the Acute Restraint Stress-Induced Hyperthermia in Mice
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“…retrograde tracing in various rodent models has shown that iBAT innervation can originate from or integrate with the PVN; however, the cell types, neuromodulators, and their mechanistic functions have not been fully elucidated (Bamshad et al., 1999; Bartness et al., 2010; Oldfield et al., 2002).”
Weighing in on the role of brown adipose tissue for treatment of obesity
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“These neurons contain neuropeptides which are regulators of energy metabolism and are under the influence of peripheral factors such as leptin and insulin—allowing the possibility that key neuronal populations are master regulators of both energy intake and energy expenditure.(9,19) Thus, BAT as a therapeutic target f…”
Background
Leptin overexpression in VTA trans-activates the hypothalamus whereas prolonged leptin action in either region cross-desensitizes
Scarpace, P. J., Matheny, M. E., Kirichenko, N., Gao, Y., Tümer, N., & Zhang, Y. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2012.09.005 · Cited by 17
“The activation signals are believed to be transmitted via neural projections that originate from the hypothalamus or nucleus of the solitary tract (NTS) (Bartness et al., 2010).”
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Novel Aspects of White Adipose Tissue Browning by Thyroid Hormones
Krause, K. (2019) · Experimental and Clinical Endocrinology & Diabetes · doi:10.1055/a-1020-5354 · Cited by 18
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“The isotype β3-AR was initially found abundantly expressed in white and brown adipose rodent tissue, where it mediates lipolysis and thermogenesis [59,60].”
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Activation of brown adipose tissue thermogenesis by electrical stimulation to the dorsal surface of the tissue in rats
Iwami, M., Alkayed, F., Shiina, T., Taira, K., & Shimizu, Y. (2013) · Biomedical Research · doi:10.2220/biomedres.34.173 · Cited by 17
“BAT thermogenesis is activated by sympathetic nerves that richly innervate the tissue (2, 3, 9).”
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RFamide neuropeptides inhibit murine and human adipose differentiation
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“In particular, the sympathetic nervous system (SNS) and related noradrenergic signaling are the most important mechanisms for conveying the homeostatic response to cold stress (65, 66).”
Background
An Intact Dorsomedial Hypothalamic Nucleus, but Not the Subzona Incerta or Reuniens Nucleus, Is Necessary for Short-Day Melatonin Signal-Induced Responses in Siberian Hamsters
Leitner, C., & Bartness, T. J. (2010) · Neuroendocrinology · doi:10.1159/000320474 · Cited by 16
Self-citation
GPSM1 in POMC neurons impairs brown adipose tissue thermogenesis and provokes diet-induced obesity
Tang, M., Zhang, Y., Zhang, R., Zhang, Y., Zheng, J., Wang, D., Wang, X., Yan, J. Y., & Hu, C. (2023) · Molecular Metabolism · doi:10.1016/j.molmet.2023.101839 · Cited by 15
“As activation of sympathetic nervous system (SNS) could increase BAT thermogenesis [28,29], we next assessed whether ablation of GPSM1 in POMC neurons impacted the delivery of the SNS signals in the brain to BAT.”
Background
MAFB in macrophages regulates cold-induced neuronal density in brown adipose tissue
Yadav, M. K., Ishida, M., Gogoleva, N., Liao, C.-W., Salim, F. N., Kanai, M., Kuno, A., Hayashi, T., Shahri, Z. J., Kulathunga, K., et al. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.113978 · Cited by 16
Hypothalamic expression of anorexigenic and orexigenic hormone receptors in obese femalesNeotomodon alstoni:Effect of fasting
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Osteocyte Apoptosis Contributes to Cold Exposure-induced Bone Loss
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Repeated Oral Administration of Flavan-3-ols Induces Browning in Mice Adipose Tissues through Sympathetic Nerve Activation
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“It has been well-investigated that SNS activation, induced by cold stress or treatment of adrenaline agonists, enhances nonshivering thermogenesis through the activation of Ucp-1 [31].”
Background
Acute brown adipose tissue temperature response to cold in monosodium glutamate-treated Siberian hamsters
Leitner, C., & Bartness, T. J. (2009) · Brain Research · doi:10.1016/j.brainres.2009.07.062 · Cited by 15
Self-citation
Genetics-based manipulation of adipose tissue sympathetic innervation
François, M., Qualls‐Creekmore, E., Berthoud, H., Münzberg, H., & Yu, S. (2017) · Physiology & Behavior · doi:10.1016/j.physbeh.2017.08.024 · Cited by 14
“The functional necessity of the SNS for intact BAT function is demonstrated by surgical and chemical denervation methods, which block or greatly reduce most cold-induced BAT adaptations like UCP1 induction, increased blood flow, higher mitochondrial density, enhanced glucose uptake and activation of thyroid-activating…”
BackgroundInfluential
Molecular and cellular regulation of thermogenic fat
Wang, C., Wang, X., & Hu, W. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1215772 · Cited by 14
Macrophages dispose of catecholamines in adipose tissue
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Vigorous-Intensity Physical Activities Are Associated with High Brown Adipose Tissue Density in Humans
Tanaka, R., Fuse, S., Kuroiwa, M., Amagasa, S., Endo, T., Ando, A., Kime, R., Kurosawa, Y., & Hamaoka, T. (2020) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph17082796 · Cited by 14
Adipose tissue microenvironments during aging: Effects on stimulated lipolysis
Camell, C. D. (2022) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2022.159118 · Cited by 16
Distinct morphology of cardiac‐ and brown adipose tissue‐projecting neurons in the stellate ganglia of mice
Barrett, M. S., Hegarty, D. M., Habecker, B. A., & Aicher, S. A. (2022) · Physiological Reports · doi:10.14814/phy2.15334 · Cited by 14
“It has traditionally been thought that each BAT pad is innervated exclusively by ipsilateral sympathetic efferents (Bartness et al., 2010; Foster et al., 1982; Hamilton et al., 1989).”
Background
PACAP up-regulates the expression of apolipoprotein D in 3T3-L1 adipocytes. DRG/3T3-L1 co-cultures study
Kosacka, J., Schröder, T., Bechmann, I., Klöting, N., Nowicki, M., Mittag, A., Gericke, M., Spanel-Borowski, K., & Blüher, M. (2011) · Neuroscience Research · doi:10.1016/j.neures.2010.09.009 · Cited by 14
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In a Model of Batten Disease, Palmitoyl Protein Thioesterase-1 Deficiency Is Associated with Brown Adipose Tissue and Thermoregulation Abnormalities
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“In brown adipose tissue, sympathetic innervation has been amply demonstrated and its activation has a pivotal role in thermogenesis during cold exposure [31].”
Background
Dramatically Amplified Thoracic Sympathetic Postganglionic Excitability and Integrative Capacity Revealed with Whole-Cell Patch-Clamp Recordings
McKinnon, M., Tian, K., Li, Y., Sokoloff, A. J., Galvin, M. L., Choi, M. H., Prinz, A. A., & Hochman, S. (2019) · eNeuro · doi:10.1523/eneuro.0433-18.2019 · Cited by 13
“…organs in a discrete location (celiac ganglion, superior/inferior mesenteric ganglion), thoracic paravertebral chain ganglia are associated with control of dispersed tissue systems such as vasculature, brown adipose tissue, sweat glands, and piloerector muscles (Jänig, 2006; Bartness et al., 2010).”
Background
Hypothalamic CDK4 regulates thermogenesis by modulating sympathetic innervation of adipose tissues
Castillo‐Armengol, J., Barquissau, V., Geller, S., Ji, H., Severi, I., Venema, W., Fernandez, E. A., Moret, C., Huber, K., Leal-Esteban, L. C., et al. (2020) · EMBO Reports · doi:10.15252/embr.201949807 · Cited by 13
“Tyro-sine hydroxylase-expressing nervous fibers (TH fibers) in BAT secrete norepinephrine, the principal stimulator of BAT activity, locally (Bartness et al , 2010).”
[11C]carfentanil PET imaging for studying the peripheral opioid system in vivo: effect of photoperiod on mu-opioid receptor availability in brown adipose tissue
Sun, L., Aarnio, R., Herre, E. A., Kärnä, S., Palani, S., Virtanen, H., Liljenbäck, H., Virta, J., Honkaniemi, A., Oikonen, V., et al. (2022) · European Journal of Nuclear Medicine and Molecular Imaging · doi:10.1007/s00259-022-05969-5 · Cited by 13
“BAT is innervated by a large number of sympathetic nerves, which control thermogenesis [15, 16].”
Background
The medial preoptic area modulates autonomic function under resting and stress conditions
Fassini, A., Scopinho, A. A., Alves, F. H. F., Fortaleza, E. A. T., & Corrêa, F. M. D. A. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2017.09.026 · Cited by 13
“The sympathetic nervous system densely innervates brown adipose tissue (Bartness et al., 2010).”
Balanced control of thermogenesis by nuclear receptor corepressors in brown adipose tissue
Richter, H. J., Hauck, A. K., Batmanov, K., Inoue, S., So, B. N., Kim, M., Emmett, M. J., Cohen, R., & Lazar, M. A. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2205276119 · Cited by 11
“ns 0 2 4 extracellular matrix (36) external encapsulating structure (36) collagen-containing extracellular matrix (27) CC: NCoR1 targets induced in NCoR1/2 BAT-dKO (525)”
Background
Caffeine: a potential mechanism for anti-obesity
Wang, M., Guo, W. Y., & Chen, J. (2024) · Purinergic Signalling · doi:10.1007/s11302-024-10022-1 · Cited by 13
“…interacts with β3-ARs to promote thermogenesis [96]; the activation of β3-ARs promotes the increased expression of cyclic adenosine monophosphate (cAMP) which activates protein kinase A (PKA), stimulates lipolysis, releases free fatty acids, and induces the expression of UCP1 [91, 93, 94, 97, 98].”
Endocrine and autocrine/paracrine modulators of brown adipose tissue mass and activity as novel therapeutic strategies against obesity and type 2 diabetes
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“Catecholamines, epinephrine and norepinephrine are released from the medulla of the adrenal gland as part of a flight-or-fight response and from the sympathetic nerve terminals [14].”
Background
From Beats to Metabolism: the Heart at the Core of Interorgan Metabolic Cross Talk
Romero-Becerra, R., Santamans, A. M., Arcones, A. C., & Sabio, G. (2023) · Physiology · doi:10.1152/physiol.00018.2023 · Cited by 12
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Systems genetic analysis of brown adipose tissue function
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“1 module, and semaphorin-3A is involved in the growth and plasticity of the sympathetic innervation of various tissue (15), including BAT (8).”
Background
Brown Adipose Tissue (BAT) detection by 18F-FDG PET and thyroid hormone level(s)—a systematic review
Santhanam, P., Ahima, R. S., Mammen, J. S., Giovanella, L., & Treglia, G. (2018) · Endocrine · doi:10.1007/s12020-018-1698-x · Cited by 12
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Distributed Forebrain Sites Mediate Melatonin-Induced Short-Day Responses in Siberian Hamsters
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Fatty Acids Rescue the Thermogenic Function of Sympathetically Denervated Brown Fat
Cao, Q., Wang, S., Wang, H., Cui, X., Jing, J., Yu, L., Shi, H., & Xue, B. (2021) · Biomolecules · doi:10.3390/biom11101428 · Cited by 10
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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
Publisher: Springer Science and Business Media LLC
Published: 2010-10
Volume: 34
Issue: S1
Pages: S36-S42
ISSN: 0307-0565 (ISSN-L)
1476-5497
DOI: 10.1038/ijo.2010.182
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
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
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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Sympathetic and sensory innervation of brown adipose tissue

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