Neuronal control of peripheral insulin sensitivity and glucose metabolism

Ruud, Johan; Steculorum, Sophie M.; Brüning, Jens C.

doi:10.1038/ncomms15259

Cited by 245Regulation of Appetite and ObesityPancreatic function and diabetesAdipokines, Inflammation, and Metabolic Diseases

Neuronal control of peripheral insulin sensitivity and glucose metabolism

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Ruud, Johan, Steculorum, Sophie M., Brüning, Jens C.·2017·Nature Communications

DOI 10.1038/ncomms15259PMC PMC5418592

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Abstract

The central nervous system (CNS) has an important role in the regulation of peripheral insulin sensitivity and glucose homeostasis. Research in this dynamically developing field has progressed rapidly due to techniques allowing targeted transgenesis and neurocircuitry mapping, which have defined the primary responsive neurons, associated molecular mechanisms and downstream neurocircuitries and processes involved. Here we review the brain regions, neurons and molecular mechanisms by which the CNS controls peripheral glucose metabolism, particularly via regulation of liver, brown adipose tissue and pancreatic function, and highlight the potential implications of these regulatory pathways in type 2 diabetes and obesity. The brain controls peripheral glucose metabolism, for example by modulating hepatic gluconeogenesis or by regulating glucose uptake into brown adipose tissue. Here, the authors review the brain regions, neurons and molecular mechanisms involved in these processes, and discuss their relevance to disease.

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Insulin action in the hypothalamus has a crucial role in the modulation of whole-body glucose metabolism.
“In line with experimental evidence from animals30, previous correlational findings from humans indicate a crucial role of insulin action in the hypothalamus for the modulation of whole-body glucose metabolism3,4.”
From Brain insulin action on peripheral insulin sensitivity in women depends on menstrual cycle phase (2023) · cites this paper as [30]
The section ‘Of mice and men: IR signalling in the human brain’ reports that improved whole-body insulin sensitivity after intranasal insulin correlated with increased hypothalamic activity in humans. It describes a hypothalamic mechanism as possible, however, and says the studies do not definitively establish a physiological role for endogenous insulin in the human brain. The claim’s ‘crucial role’ is stronger than that human evidence supports. (LLM, conf=0.83)
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Central Insulin Administration Improves Whole-Body Insulin Sensitivity via Hypothalamus and Parasympathetic Outputs in Men
Heni, M., Wagner, R., Kullmann, S., Veit, R., Mat Husin, H., Linder, K., Benkendorff, C., Peter, A., Stefan, N., Häring, H.-U., et al. (2014) · Diabetes · doi:10.2337/db14-0477 · Cited by 167 · see citing works
Glutamatergic Preoptic Area Neurons That Express Leptin Receptors Drive Temperature-Dependent Body Weight Homeostasis
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Divergent Regulation of Energy Expenditure and Hepatic Glucose Production by Insulin Receptor in Agouti-Related Protein and POMC Neurons
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Hypothalamic AgRP‐neurons control peripheral substrate utilization and nutrient partitioning
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Modulation of AgRP-neuronal function by SOCS3 as an initiating event in diet-induced hypothalamic leptin resistance
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Melanocortin 4 receptors in autonomic neurons regulate thermogenesis and glycemia
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Intranasal Insulin Enhances Postprandial Thermogenesis and Lowers Postprandial Serum Insulin Levels in Healthy Men
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Leptin Engages a Hypothalamic Neurocircuitry to Permit Survival in the Absence of Insulin
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Starvation after AgRP neuron ablation is independent of melanocortin signaling
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Activation of KATP channels suppresses glucose production in humans
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Insulin Activates Erk1/2 Signaling in the Dorsal Vagal Complex to Inhibit Glucose Production
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Gs-coupled GPCR signalling in AgRP neurons triggers sustained increase in food intake
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The Brain–to–Pancreatic Islet Neuronal Map Reveals Differential Glucose Regulation From Distinct Hypothalamic Regions
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Regulation of Glucose Tolerance and Sympathetic Activity by MC4R Signaling in the Lateral Hypothalamus
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Ribosomal S6K1 in POMC and AgRP Neurons Regulates Glucose Homeostasis but Not Feeding Behavior in Mice
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Insulin-Dependent Activation of MCH Neurons Impairs Locomotor Activity and Insulin Sensitivity in Obesity
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Inhibition of P2Y6 Signaling in AgRP Neurons Reduces Food Intake and Improves Systemic Insulin Sensitivity in Obesity
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Myeloid-Cell-Derived VEGF Maintains Brain Glucose Uptake and Limits Cognitive Impairment in Obesity
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Glut4 expression defines an insulin-sensitive hypothalamic neuronal population
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Hypothalamic glucagon signals through the KATP channels to regulate glucose production
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Anorexia and Impaired Glucose Metabolism in Mice With Hypothalamic Ablation of Glut4 Neurons
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Is Brain Insulin Action Relevant to the Control of Plasma Glucose in Humans?
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HypoMap—a unified single-cell gene expression atlas of the murine hypothalamus
Steuernagel, L., Lam, B. Y. H., Klemm, P., Dowsett, G. K. C., Bauder, C. A., Tadross, J. A., Hitschfeld, T. S., del Rio Martin, A., Chen, W., de Solis, A. J., et al. (2022) · Nature Metabolism · doi:10.1038/s42255-022-00657-y · Cited by 267 · see citing works
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Role of c-Jun N-terminal Kinase (JNK) in Obesity and Type 2 Diabetes
Yung, J. H. M., & Giacca, A. (2020) · Cells · doi:10.3390/cells9030706 · Cited by 267 · see citing works
Central nervous pathways of insulin action in the control of metabolism and food intake
Kullmann, S., Kleinridders, A., Small, D. M., Fritsche, A., Häring, H.-U., Preissl, H., & Heni, M. (2020) · The Lancet Diabetes & Endocrinology · doi:10.1016/s2213-8587(20)30113-3 · Cited by 233 · see citing works
Brain insulin signalling in metabolic homeostasis and disease
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The brain and immune system prompt energy shortage in chronic inflammation and ageing
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Functionally distinct POMC-expressing neuron subpopulations in hypothalamus revealed by intersectional targeting
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Oxidative stress: The nexus of obesity and cognitive dysfunction in diabetes
Li, H., Ren, J. L., Li, Y., Wu, Q., & Wei, J. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1134025 · Cited by 148 · see citing works
Brain insulin sensitivity is linked to adiposity and body fat distribution
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Food Perception Primes Hepatic ER Homeostasis via Melanocortin-Dependent Control of mTOR Activation
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Contribution of specific ceramides to obesity-associated metabolic diseases
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Neurodegenerative Diseases: Implications of Environmental and Climatic Influences on Neurotransmitters and Neuronal Hormones Activities
Ayeni, E. A., Aldossary, A. M., Ayejoto, D. A., Gbadegesin, L. A., Alshehri, A. A., Alfassam, H. A., Afewerky, H. K., Almughem, F. A., Saidu, M. B., & Tawfik, E. A. (2022) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph191912495 · Cited by 114 · see citing works
Empagliflozin Improves Insulin Sensitivity of the Hypothalamus in Humans With Prediabetes: A Randomized, Double-Blind, Placebo-Controlled, Phase 2 Trial
Kullmann, S., Hummel, J., Wagner, R. J., Dannecker, C., Vosseler, A., Fritsche, L., Veit, R., Kantartzis, K., Machann, J., Birkenfeld, A. L., et al. (2021) · Diabetes Care · doi:10.2337/dc21-1136 · Cited by 112 · see citing works
Insulin signalling in tanycytes gates hypothalamic insulin uptake and regulation of AgRP neuron activity
Porniece, M., Cremer, A. L., Klemm, P., Steuernagel, L., Sundaram, S. M., Jaïs, A., Hausen, A. C., Tao, J., Secher, A., Pedersen, T. Å., et al. (2021) · Nature Metabolism · doi:10.1038/s42255-021-00499-0 · Cited by 107 · see citing works
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The hypothalamus for whole-body physiology: from metabolism to aging
Liu, T., Xu, Y., Yi, C., Tong, Q., & Cai, D. (2021) · Protein & Cell · doi:10.1007/s13238-021-00834-x · Cited by 103 · see citing works
NPY mediates the rapid feeding and glucose metabolism regulatory functions of AgRP neurons
Engström, L., Pereira, M. M. A., Solís, A. J. D., Fenselau, H., & Brüning, J. C. (2020) · Nature Communications · doi:10.1038/s41467-020-14291-3 · Cited by 99 · see citing works
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Hypothalamic Control of Systemic Glucose Homeostasis: The Pancreas Connection
Pozo, M., & Claret, M. (2018) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2018.05.001 · Cited by 98 · see citing works
Alzheimer’s disease as type 3 diabetes: understanding the link and implications
Kciuk, M., Kruczkowska, W., Gałęziewska, J., Wanke, K., Kałuzińska-Kołat, Ż., Aleksandrowicz, M., & Kontek, R. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms252211955 · Cited by 98 · see citing works
Intranasal Targeting of Hypothalamic PTP1B and TCPTP Reinstates Leptin and Insulin Sensitivity and Promotes Weight Loss in Obesity
Dodd, G. T., Xirouchaki, C. E., Eramo, M. J., Mitchell, C. A., Andrews, Z. B., Henry, B. A., Cowley, M. A., & Tiganis, T. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.08.019 · Cited by 94 · see citing works
Alkaloidal Phytoconstituents for Diabetes Management: Exploring the Unrevealed Potential
Behl, T., Gupta, A. K., Albratty, M., Najmi, A., Meraya, A. M., Alhazmi, H. A., Anwer, M. K., Bhatia, S., & BUNGAU, S. G. (2022) · Molecules · doi:10.3390/molecules27185851 · Cited by 93 · see citing works
Hypothalamic glucose-sensing mechanisms
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Reciprocal activity of AgRP and POMC neurons governs coordinated control of feeding and metabolism
Solís, A. J. D., Río-Martín, A. D., Radermacher, J., Chen, W., Steuernagel, L., Bauder, C. A., Eggersmann, F. R., Morgan, D. A., Lena, C. A., Sue, M. W., et al. (2024) · Nature Metabolism · doi:10.1038/s42255-024-00987-z · Cited by 91 · see citing works
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Pavlovian Conditioning of Immunological and Neuroendocrine Functions
Hadamitzky, M., Lückemann, L., Pacheco‐López, G., & Schedlowski, M. (2019) · Physiological Reviews · doi:10.1152/physrev.00033.2018 · Cited by 87 · see citing works
Insulin sensitivity predicts cognitive decline in individuals with prediabetes
Willmann, C., Brockmann, K., Wagner, R. J., Kullmann, S., Preissl, H. T., Schnauder, G., Maetzler, W., Gasser, T., Berg, D., Eschweiler, G. W., et al. (2020) · BMJ Open Diabetes Research & Care · doi:10.1136/bmjdrc-2020-001741 · Cited by 83 · see citing works
Roles of Alkaloids from Medicinal Plants in the Management of Diabetes Mellitus
Adhikari, B. (2021) · Journal of Chemistry · doi:10.1155/2021/2691525 · Cited by 83 · see citing works
Stimulation of the hepatoportal nerve plexus with focused ultrasound restores glucose homoeostasis in diabetic mice, rats and swine
Cotero, V. E., Graf, J. F., Miwa, H., Hirschstein, Z., Qanud, K., Huerta, T. S., Tai, N., Ding, Y., Jimenez-Cowell, K., Tomaio, J. N., et al. (2022) · Nature Biomedical Engineering · doi:10.1038/s41551-022-00870-w · Cited by 80 · see citing works
Insulin Resistance in Peripheral Tissues and the Brain: A Tale of Two Sites
Rhea, E. M., Banks, W. A., & Raber, J. (2022) · Biomedicines · doi:10.3390/biomedicines10071582 · Cited by 76 · see citing works
Review of the role of the nervous system in glucose homoeostasis and future perspectives towards the management of diabetes
Güemes, A., & Georgiou, P. (2018) · Bioelectronic Medicine · doi:10.1186/s42234-018-0009-4 · Cited by 75 · see citing works
Role of Mitochondrial Stress Protein HSP60 in Diabetes-Induced Neuroinflammation
Liyanagamage, D. S. N. K., & Martinus, R. D. (2020) · Mediators of Inflammation · doi:10.1155/2020/8073516 · Cited by 72 · see citing works
Glutamine Synthetase: Localization Dictates Outcome
Castegna, A., & Menga, A. (2018) · Genes · doi:10.3390/genes9020108 · Cited by 73 · see citing works
Multiple target tissue effects of GLP-1 analogues on non-alcoholic fatty liver disease (NAFLD) and non-alcoholic steatohepatitis (NASH)
Bifari, F., Manfrini, R., Dei, M., Berra, C., Siano, M., Zuin, M. G., Paroni, R. C., & Folli, F. B. (2018) · Pharmacological Research · doi:10.1016/j.phrs.2018.09.025 · Cited by 69 · see citing works
Regulation of systemic metabolism by the autonomic nervous system consisting of afferent and efferent innervation.
Imai, J., & Katagiri, H. (2021) · International Immunology · doi:10.1093/intimm/dxab023 · Cited by 63 · see citing works
Central Nervous System Control of Glucose Homeostasis: A Therapeutic Target for Type 2 Diabetes?
Mirzadeh, Z., Faber, C. L., & Schwartz, M. W. (2022) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev-pharmtox-052220-010446 · Cited by 68 · see citing works
Naked-eye point-of-care testing platform based on a pH-responsive superwetting surface: toward the non-invasive detection of glucose
Gao, Z. F., Sann, E. E., Lou, X., Liu, R., Dai, J., Zuo, X., Xia, F., & Jiang, L. (2018) · NPG Asia Materials · doi:10.1038/s41427-018-0024-7 · Cited by 66 · see citing works
CNS control of the endocrine pancreas
Faber, C. L., Deem, J., Campos, C. A. L., Taborsky, G., & Morton, G. J. (2020) · Diabetologia · doi:10.1007/s00125-020-05204-6 · Cited by 50 · see citing works
The insulin resistant brain: impact on whole-body metabolism and body fat distribution
Heni, M. (2024) · Diabetologia · doi:10.1007/s00125-024-06104-9 · Cited by 73 · see citing works
CerS6-dependent ceramide synthesis in hypothalamic neurons promotes ER/mitochondrial stress and impairs glucose homeostasis in obese mice
Hammerschmidt, P., Steculorum, S. M., Bandet, C. L., Río-Martín, A. D., Steuernagel, L., Kohlhaas, V., Feldmann, M., Varela, L., Majcher, A., Correia, M. Q., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-42595-7 · Cited by 60 · see citing works
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Hypothalamic AMPK as a possible target for energy balance-related diseases
López, M. (2022) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2022.04.007 · Cited by 59 · see citing works
Brain control of energy homeostasis: implications for anti-obesity pharmacotherapy
Johansen, V. B. I., Petersen, J., Lund, J., Mathiesen, C. V., Fenselau, H., & Clemmensen, C. (2025) · Cell · doi:10.1016/j.cell.2025.06.010 · Cited by 53 · see citing works
Novel approaches to restore beta cell function in prediabetes and type 2 diabetes
Salunkhe, V. A., Veluthakal, R., Kahn, S. E., & Thurmond, D. C. (2018) · Diabetologia · doi:10.1007/s00125-018-4658-3 · Cited by 57 · see citing works
Clinical Trials in Prader–Willi Syndrome: A Review
Mahmoud, R., Kimonis, V. E., & Butler, M. G. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24032150 · Cited by 52 · see citing works
Insulin resistance and bioenergetic manifestations: Targets and approaches in Alzheimer's disease
Sharma, V., & Singh, T. G. (2020) · Life Sciences · doi:10.1016/j.lfs.2020.118401 · Cited by 51 · see citing works
Sphingolipid metabolism in brain insulin resistance and neurological diseases
Mei, M., Liu, M., Mei, Y., Zhao, J., & Li, Y. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1243132 · Cited by 50 · see citing works
Health benefits attributed to 17α-estradiol, a lifespan-extending compound, are mediated through estrogen receptor α
Mann, S. N., Hadad, N., Holte, M. N., Rothman, A. R., Sathiaseelan, R., Mondal, S. A., Agbaga, M., Unnikrishnan, A., Subramaniam, M., Hawse, J. R., et al. (2020) · eLife · doi:10.7554/elife.59616 · Cited by 50 · see citing works
The Impact of Intermittent Fasting on Brain-Derived Neurotrophic Factor, Neurotrophin 3, and Rat Behavior in a Rat Model of Type 2 Diabetes Mellitus
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Authors: Ruud, J., Steculorum, S. M., & Brüning, J. C.
Affiliations: University of Cologne (DE)
Corresponding author: Brüning, Jens C.
ORCID: Steculorum, Sophie M.
Brüning, Jens C.
Venue: Nature Communications
Publisher: Springer Science and Business Media LLC
Published: 2017-05-04
Volume: 8
Issue: 1
Pages: 15259-15259
ISSN: 2041-1723 (ISSN-L)
DOI: 10.1038/ncomms15259
PMC: PMC5418592
OpenAlex: W2610903113
Cited by: 245
References: 106
Citations by year: 2026: 21 · 2025: 24 · 2024: 22 · 2023: 29 · 2022: 35 · 2021: 40 · 2020: 32 · 2019: 16 · 2018: 24 · 2017: 2
FWCI: 2.46
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0 (tdm)
creativecommons.org/licenses/by/4.0 (vor)
Locations: Nature Communications (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
Kölner Universitäts PublikationsServer (Universität zu Köln) (publishedVersion)
RePEc: Research Papers in Economics (submittedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
MPG.PuRe (Max Planck Society) (submittedVersion)
Funders: European Commission (2007–2013, FP7 2007-2013, FP7/2007, 266408)
Deutsche Forschungsgemeinschaft (FP7/2007–2013, BR 1492/7-1)
Vetenskapsrådet (FP7/2007-2013, 2013-530)
Servier
Topics: Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Regulation of Appetite and Obesity
Health Sciences › Medicine › Surgery › Pancreatic function and diabetes
Health Sciences › Medicine › Epidemiology › Adipokines, Inflammation, and Metabolic Diseases
Keywords: insulin sensitivity, glucose homeostasis, central nervous system regulation, hepatic gluconeogenesis, pancreatic function, type 2 diabetes, obesity, neurocircuitry, brain regions
MeSH terms: Adipose Tissue, Central Nervous System, Diabetes Mellitus, Type 2, Glucose, Humans, Insulin Resistance, Liver, Neurons, Obesity, Pancreas

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Neuronal control of peripheral insulin sensitivity and glucose metabolism

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