Cited by 289Adipose Tissue and MetabolismRegulation of Appetite and ObesityLipid metabolism and biosynthesis

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Sensory and sympathetic nervous system control of white adipose tissue lipolysis

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Bartness, Timothy J., Shrestha, Y.B., Vaughan, C.H., Schwartz, G.J., Song, C.K.·2010·Molecular and Cellular Endocrinology

DOI 10.1016/j.mce.2009.08.031PMC PMC2826518

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Abstract

Circulating factors are typically invoked to explain bidirectional communication between the CNS and white adipose tissue (WAT). Thus, initiation of lipolysis has been relegated primarily to adrenal medullary secreted catecholamines and the inhibition of lipolysis primarily to pancreatic insulin, whereas signals of body fat levels to the brain have been ascribed to adipokines such as leptin. By contrast, evidence is given for bidirectional communication between brain and WAT occurring via the sympathetic nervous system (SNS) and sensory innervation of this tissue. Using retrograde transneuronal viral tract tracers, the SNS outflow from brain to WAT has been defined. Functionally, sympathetic denervation of WAT blocks lipolysis to a variety of lipolytic stimuli. Using anterograde transneuronal viral tract tracers, the sensory input from WAT to brain has been defined. Functionally, these WAT sensory nerves respond electrophysiologically to increases in WAT SNS drive suggesting a possible neural negative feedback loop to regulate lipolysis.

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Mishra, G., & Townsend, K. L. (2024) · Molecules and Cells · doi:10.1016/j.mocell.2024.100030 · Cited by 17
“…their roles in adipose tissues, and determining what sensory neuropeptide functions are distinct from those mediated by sympathetic nerves (Bartness et al., 2010a, 2010b; Bartness and Kay Song, 2005; Harris, 2018, 2012; Makwana et al., 2021; Nguyen et al., 2018; Wang et al., 2022;…”
Regulation of Lipolysis in Adipose Tissue and Clinical Significance
Li, X., & Sun, K. (2018) · Advances in experimental medicine and biology · doi:10.1007/978-981-13-1286-1_11 · Cited by 17
Neuroimmune regulation of white adipose tissues
Qian, X., Meng, X., Zhang, S., & Zeng, W. (2021) · FEBS Journal · doi:10.1111/febs.16213 · Cited by 17
Adipose Tissue-Derived Extracellular Vesicles: A Promising Biomarker and Therapeutic Strategy for Metabolic Disorders
Liu, W., Liu, T., Zhao, Q., Ma, J., Jiang, J., & Shi, H. (2023) · Stem Cells International · doi:10.1155/2023/9517826 · Cited by 21
“The sympathetic nervous system is intimately involved in the development and function of adipose tissue [162 – 165].”
Background
Gene therapy approaches for obesity-induced adipose neuropathy: Device-targeted AAV-mediated neurotrophic factor delivery to adipocytes in subcutaneous adipose
Blaszkiewicz, M., Tao, T., Mensah-Arhin, K., Willows, J. W., Bates, R., Huang, W., Cao, L., Smith, R. L., & Townsend, K. L. (2024) · Molecular Therapy · doi:10.1016/j.ymthe.2024.02.035 · Cited by 17
Peripheral elimination of the sympathetic nervous system stimulates immunocyte retention in lymph nodes and ameliorates collagen type II arthritis
Klatt, S., Stangl, H., Kunath, J., Lowin, T., Pongratz, G., & Straub, R. H. (2016) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2016.02.006 · Cited by 16
“…provision of energy-rich fuels because catecholamines via b2-adrenoceptor signaling liberate glucose and free fatty acids needed by the energy-consuming immune system (reviewed in (Bartness et al., 2010; Frauwirth and Thompson, 2004; Ghesquière et al., 2014; Nonogaki, 2000; Straub et al., 2010)).”
Background
The Relationship between Sleep Bruxism Intensity and Renalase Concentration—An Enzyme Involved in Hypertension Development
Martynowicz, H., Wieckiewicz, M. A., Poręba, R., Wojakowska, A., Smardz, J., Januszewska, L., Markiewicz−Górka, I., Mazur, G. J., Pawlas, K., & Gać, P. (2019) · Journal of Clinical Medicine · doi:10.3390/jcm9010016 · Cited by 15
“A decreased concentration of catecholamines in obese subjects has also been reported in previous studies [15,16].”
Result
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 nature of signals for adipose tissue sensory neurons remains unknown but it is predicted that the sensory information from adipose tissue could play an important role to influence adipocyte and depot size, inflammatory and metabolic responses [32].”
BackgroundInfluential
Reciprocal signaling between adipose tissue depots and the central nervous system
Puente-Ruiz, S. C., & Jaïs, A. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.979251 · Cited by 17
“Importantly, sympathetic outflow to the adipose tissue is the principal initiator of adipose tissue lipolysis (Fredholm and Karlsson, 1970; Youngstrom and Bartness, 1995; Dodt et al., 2003; Bartness et al., 2010).”
Background
The Neuronal and Non-Neuronal Pathways of Sodium-Glucose Cotransporter-2 Inhibitor on Body Weight-Loss and Insulin Resistance
Dong, M., Chen, H., Wen, S., Yuan, Y., Yang, L., Li, Y., Yuan, X., Xu, D., & Zhou, L. (2023) · Diabetes Metabolic Syndrome and Obesity · doi:10.2147/dmso.s399367 · Cited by 17
“SGLT2i May Improve the Adipose IR Through the Sympathetic Nervous System (SNS) It is worth noting that adipose tissue is innervated only by sympathetic nerve, which makes it an important regulator of fat mobilization.(81) Norepinephrine binds to β3 adrenergic receptors, stimulates hormone-sensitive lipase and promotes…”
Background
The potential mechanisms underlying the modulating effect of perirenal adipose tissue on hypertension: Physical compression, paracrine, and neurogenic regulation
Sun, J.-Y., Su, Z., Yang, J., Sun, W. Y., & Kong, X. (2024) · Life Sciences · doi:10.1016/j.lfs.2024.122511 · Cited by 14
From fasting to fat reshaping: exploring the molecular pathways of intermittent fasting-induced adipose tissue remodeling
Vo, N., Zhang, Q., & Sung, H. (2024) · Journal of Pharmacy & Pharmaceutical Sciences · doi:10.3389/jpps.2024.13062 · Cited by 17
Innate lymphoid cells as novel regulators of obesity and its‐associated metabolic dysfunction
Yang, D., Yang, W., Tian, Z., van Velkinburgh, J. C., Song, J. J., Wu, Y., & Ni, B. (2016) · Obesity Reviews · doi:10.1111/obr.12397 · Cited by 17
“nephrine, epinephrine) and the adrenocortical hormone (61),”
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
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
Neuropeptide Y potentiates beta-adrenergic stimulation of lipolysis in 3T3-L1 adipocytes
Li, R., Guan, H., & Yang, K. (2012) · Regulatory Peptides · doi:10.1016/j.regpep.2012.06.002 · Cited by 15
“Furthermore, sympathetic stimulation is a critical driver of lipolysis in white adipose tissue [33].”
Background
Evaluation of the Synuclein-γ (SNCG) Gene as a PPARγ Target in Murine Adipocytes, Dorsal Root Ganglia Somatosensory Neurons, and Human Adipose Tissue
Dunn, T. N., Akiyama, T., Lee, H. W., Kim, J. B., Knotts, T. A., Smith, S. R., Sears, D. D., Carstens, E. E., & Adams, S. H. (2015) · PLoS ONE · doi:10.1371/journal.pone.0115830 · Cited by 15
Vagal Hyperactivity Due to Ventromedial Hypothalamic Lesions Increases Adiponectin Production and Release
Suzuki, Y., Shimizu, H., Ishizuka, N., Kubota, N., Kubota, T., Senoo, A., Kageyama, H., Osaka, T., Hirako, S., Kim, H.-J., et al. (2014) · Diabetes · doi:10.2337/db13-0636 · Cited by 14
“The autonomic nervous system may be involved in regulation of adiponectin production and release in adipose tissues, and adipose tissue is innervated by sympathetic nerves (36); however, results for involvement of the sympathetic nervous system in adiponectin production and release in humans and animals are in conflic…”
Background
Lack of Melanopsin Is Associated with Extreme Weight Loss in Mice upon Dietary Challenge
Aytürk, D. G., Castrucci, A. M. D. L., Carr, D. E., Keller, S. R., & Provencio, I. (2015) · PLoS ONE · doi:10.1371/journal.pone.0127031 · Cited by 14
“Although lipolysis in white adipose tissue (WAT) is controlled through humoral signals such as adipokines, insulin, and adrenal cathecholamines, within the past decade it has become increasingly clear that sympathetic innervation of WAT depots also plays a significant role in regulating lipolysis.[10] For example, the…”
Background
Brain insulin signaling suppresses lipolysis in the absence of peripheral insulin receptors and requires the MAPK pathway
Metz, M., O’Hare, J., Cheng, B., Puchowicz, M., Buettner, C., & Scherer, T. (2023) · Molecular Metabolism · doi:10.1016/j.molmet.2023.101723 · Cited by 13
“Because the sympathetic nervous system and adrenergic signaling is the major driver of WAT lipolysis we assessed hormone-sensitive lipase (HSL) phosphorylation at Ser563 and Ser660, which activates HSL and is an established indicator of sympathetic nervous system outflow to WAT [28,29].”
Background
Leptin deficiency impairs adipogenesis and browning response in mouse mesenchymal progenitors
Veličković, K., Leija, H. A. L., Kosic, B., Sacks, H. S., Symonds, M. E., & Sottile, V. (2023) · European Journal of Cell Biology · doi:10.1016/j.ejcb.2023.151342 · Cited by 13
Repeated immobilization stress induces catecholamine production in rat mesenteric adipocytes
Vargovič, P., Ukropec, J., Lauková, M., Kurdiová, T., Baláž, M., MANZ, B., Ukropcová, B., & Květňanský, R. (2012) · Stress · doi:10.3109/10253890.2012.736046 · Cited by 13
“Differences in NE levels observed among various fat pads are consistent with previously described findings that the action of SNS is quite variable, and clear differences exist in sympathetic innervation among various WATs and BAT (for review, see Bartness et al. 2010).”
Background
Apolipoprotein A-IV Enhances Fatty Acid Uptake by Adipose Tissues of Male Mice via Sympathetic Activation
Zhu, Q., Weng, J., Shen, M., Fish, J., Shen, Z.-J., Coschigano, K. T., Davidson, W. S., Tso, P., Shi, H., & Lo, C. C. (2020) · Endocrinology · doi:10.1210/endocr/bqaa042 · Cited by 14
“BAT is intensely innervated by sympathetic nerves (48).”
Background
Cannabinoid CB1 Receptor Deletion from Catecholaminergic Neurons Protects from Diet-Induced Obesity
Srivastava, R. K., de Azúa, I. R., Conrad, A., Purrio, M., & Lutz, B. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms232012635 · Cited by 12
Brain-to-BAT - and Back?: Crosstalk between the Central Nervous System and Thermogenic Adipose Tissue in Development and Therapy of Obesity
Till, A., Fries, C., & Fenske, W. K. (2022) · Brain Sciences · doi:10.3390/brainsci12121646 · Cited by 12
“[60], one general mechanism for vital WAT-to-brain feedback is mediated by sensory neurons that innervate WAT and afferent signaling to dorsal route ganglia (DRG).”
Background
Interrogating autonomic peripheral nervous system neurons with viruses – A literature review
Feng, M., Xiang, B., Li, F., Wang, Q., Xu, W., & Xiang, H. (2020) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2020.108958 · Cited by 11
High-fat diet promotes adrenaline production by visceral adipocytes
Gomes, A., Soares, R. A., Costa, R., Marino, F., Cosentino, M., Malagón, M. M., & Ribeiro, L. V. P. T. (2019) · European Journal of Nutrition · doi:10.1007/s00394-019-01971-0 · Cited by 11
Topographical mapping of catecholaminergic axon innervation in the flat-mounts of the mouse atria: a quantitative analysis
Zhang, Y., Bizanti, A., Harden, S. W., Chen, J., Bendowski, K. T., Hoover, D. B., Gozal, D., Shivkumar, K., Heal, M., Tappan, S. J., et al. (2023) · Scientific Reports · doi:10.1038/s41598-023-27727-9 · Cited by 9
Loss of cAMP Signaling in CD11c Immune Cells Protects Against Diet-Induced Obesity
Zeng, L., Herdman, D. S., Lee, S. M., Tao, A., Das, M., Bertin, S., Eckmann, L., Mahata, S. K., Wu, P., Hara, M., et al. (2023) · Diabetes · doi:10.2337/db22-1035 · Cited by 9
Smooth muscle cell-derived Cxcl12 directs macrophage accrual and sympathetic innervation to control thermogenic adipose tissue
Lee, D., Benvie, A. M., Steiner, B. M., Kolba, N. J., Ford, J. G., McCabe, S. M., Jiang, Y., & Berry, D. C. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.114169 · Cited by 9
“8,9 Therefore, the amount of BAT innervation is correlated with thermogenic capacity and macronutrient burning potential.”
Impact of high-fat diet on vasoconstrictor reactivity of white and brown adipose tissue resistance arteries
Hazra, S., Henson, G. D., Bramwell, R. C., Donato, A. J., & Lesniewski, L. A. (2018) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00278.2018 · Cited by 9
Chronic VEGFR-3 signaling preserves dendritic arborization and sensitization under stress
Chakraborty, A., Upadhya, R., Usman, T. A., Shetty, A. K., & Rutkowski, J. M. (2021) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2021.08.007 · Cited by 9
Transcriptional Response of White Adipose Tissue to Withdrawal of Vitamin B3
Shi, W., Hegeman, M. A., Doncheva, A. I., van der Stelt, I., Bekkenkamp‐Grovenstein, M., van Schothorst, E. M., Brenner, C., de Boer, V. C. J., & Keijer, J. (2019) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201801100 · Cited by 8
FABP4 Expression in Subcutaneous Adipose Tissue Is Independently Associated with Circulating Triglycerides in Obesity
Osorio-Conles, Ó., Ibarzábal, A., Balibrea, J. M., Vidal, J., Ortega, E., & de Hollanda, A. (2023) · Journal of Clinical Medicine · doi:10.3390/jcm12031013 · Cited by 9
“Bidirectional communication exists between the brain and WAT occurring via the sympathetic nervous system [35].”
Background
Activation of β-adrenergic receptor signaling prevents glucocorticoid-induced obesity and adipose tissue dysfunction in male mice
Gado, M., Heinrich, A., Wiedersich, D., Sameith, K., Dahl, A., Alexaki, V. I., Swarbrick, M. M., Baschant, U., Grafe, I., Perakakis, N., et al. (2023) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00259.2022 · Cited by 8
Synergistic induction of interleukin-6 expression by endothelin-1 and cyclic AMP in adipocytes
Chai, S.-P., Juan, C.-C., Kao, P.-H., Wang, D. S., & Fong, J. C. (2012) · International Journal of Obesity · doi:10.1038/ijo.2012.11 · Cited by 8
Sex specific effect of ATPase inhibitory factor 1 on body weight: studies in high fat diet induced obese mice and genetic association studies in humans
Kwak, S., Chung, I., Kang, J. H., Perakakis, N., Yoo, E. H., Lee, J., Jung, H. T., Mun, B.-R., Choi, W.-S., Kim, O. Y., et al. (2020) · Metabolism · doi:10.1016/j.metabol.2020.154171 · Cited by 8
Noradrenaline and ATP regulate adiponectin exocytosis in white adipocytes: Disturbed adrenergic and purinergic signalling in obese and insulin-resistant mice
Musovic, S., Komai, A. M., Said, M. K., Shrestha, M. M., Wu, Y., Asterholm, I. W., & Olofsson, C. S. (2022) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2022.111619 · Cited by 8

Authors: Bartness, T. J., Shrestha, Y. B., Vaughan, C. H., Schwartz, G. J., & Song, C. K.
Affiliations: Georgia State University (US)
Albert Einstein College of Medicine (US)
Corresponding author: Bartness, Timothy J.
ORCID: Bartness, Timothy J.
Schwartz, G.J.
Venue: Molecular and Cellular Endocrinology
Publisher: Elsevier BV
Published: 2010-04
Volume: 318
Issue: 1-2
Pages: 34-43
ISSN: 0303-7207 (ISSN-L)
DOI: 10.1016/j.mce.2009.08.031
PMC: PMC2826518
OpenAlex: W1990112639
Cited by: 289
References: 180
Citations by year: 2026: 10 · 2025: 11 · 2024: 16 · 2023: 22 · 2022: 23 · 2021: 15 · 2020: 12 · 2019: 21 · 2018: 14 · 2017: 19 · 2016: 13 · 2015: 27 · 2014: 18 · 2013: 15 · 2012: 24
FWCI: 1.94
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Molecular and Cellular Endocrinology (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: white adipose tissue, lipolysis, sympathetic nervous system, sensory innervation, sympathetic denervation, anterograde and retrograde tracing, catecholamines, insulin, leptin, adipokines
MeSH terms: Animals, Humans, Lipolysis, Sensory Receptor Cells, Sympathetic Nervous System, Adipose Tissue, White

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Sensory and sympathetic nervous system control of white adipose tissue lipolysis

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