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Metabolism

Evidence That the Sympathetic Nervous System Elicits Rapid, Coordinated, and Reciprocal Adjustments of Insulin Secretion and Insulin Sensitivity During Cold Exposure

  1. Gregory J. Morton1,
  2. Kenjiro Muta1,
  3. Karl J. Kaiyala2,
  4. Jennifer M. Rojas1,
  5. Jarrad M. Scarlett1,3,
  6. Miles E. Matsen1,
  7. Jarrell T. Nelson1,
  8. Nikhil K. Acharya1,
  9. Francesca Piccinini4,
  10. Darko Stefanovski5,
  11. Richard N. Bergman4,
  12. Gerald J. Taborsky Jr.6,
  13. Steven E. Kahn6 and
  14. Michael W. Schwartz1⇑
  1. 1University of Washington Diabetes Institute, Department of Medicine, University of Washington, Seattle, WA
  2. 2Department of Oral Health Sciences, School of Dentistry, University of Washington, Seattle, WA
  3. 3Department of Pediatric Gastroenterology and Hepatology, Seattle Children’s Hospital, Seattle, WA
  4. 4Diabetes and Obesity Research Institute, Cedars-Sinai Medical Center, Los Angeles, CA
  5. 5New Bolton Center, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, PA
  6. 6Veterans Affairs Puget Sound Health Care System, Department of Veterans Affairs Medical Center, Seattle, WA
  1. Corresponding author: Michael W. Schwartz, mschwart{at}u.washington.edu.
  1. G.J.M. and K.M. contributed equally to this work.

Diabetes 2017 Apr; 66(4): 823-834. https://doi.org/10.2337/db16-1351
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Abstract

Dynamic adjustment of insulin secretion to compensate for changes of insulin sensitivity that result from alteration of nutritional or metabolic status is a fundamental aspect of glucose homeostasis. To investigate the role of the brain in this coupling process, we used cold exposure as an experimental paradigm because the sympathetic nervous system (SNS) helps to coordinate the major shifts of tissue glucose utilization needed to ensure that increased thermogenic needs are met. We found that glucose-induced insulin secretion declined by 50% in rats housed at 5°C for 28 h, and yet, glucose tolerance did not change, owing to a doubling of insulin sensitivity. These potent effects on insulin secretion and sensitivity were fully reversed by returning animals to room temperature (22°C) for 4 h or by intravenous infusion of the α-adrenergic receptor antagonist phentolamine for only 30 min. By comparison, insulin clearance was not affected by cold exposure or phentolamine infusion. These findings offer direct evidence of a key role for the brain, acting via the SNS, in the rapid, highly coordinated, and reciprocal changes of insulin secretion and insulin sensitivity that preserve glucose homeostasis in the setting of cold exposure.

Footnotes

  • This article contains Supplementary Data online at http://diabetes.diabetesjournals.org/lookup/suppl/doi:10.2337/db16-1351/-/DC1.

  • J.M.R. is currently affiliated with Early Regulatory Toxicology, Non-clinical Development, Novo Nordisk A/S, Måløv, Denmark.

  • Received November 6, 2016.
  • Accepted January 3, 2017.
  • © 2017 by the American Diabetes Association.
http://www.diabetesjournals.org/content/license

Readers may use this article as long as the work is properly cited, the use is educational and not for profit, and the work is not altered. More information is available at http://www.diabetesjournals.org/content/license.

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Evidence That the Sympathetic Nervous System Elicits Rapid, Coordinated, and Reciprocal Adjustments of Insulin Secretion and Insulin Sensitivity During Cold Exposure
Gregory J. Morton, Kenjiro Muta, Karl J. Kaiyala, Jennifer M. Rojas, Jarrad M. Scarlett, Miles E. Matsen, Jarrell T. Nelson, Nikhil K. Acharya, Francesca Piccinini, Darko Stefanovski, Richard N. Bergman, Gerald J. Taborsky, Steven E. Kahn, Michael W. Schwartz
Diabetes Apr 2017, 66 (4) 823-834; DOI: 10.2337/db16-1351

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Evidence That the Sympathetic Nervous System Elicits Rapid, Coordinated, and Reciprocal Adjustments of Insulin Secretion and Insulin Sensitivity During Cold Exposure
Gregory J. Morton, Kenjiro Muta, Karl J. Kaiyala, Jennifer M. Rojas, Jarrad M. Scarlett, Miles E. Matsen, Jarrell T. Nelson, Nikhil K. Acharya, Francesca Piccinini, Darko Stefanovski, Richard N. Bergman, Gerald J. Taborsky, Steven E. Kahn, Michael W. Schwartz
Diabetes Apr 2017, 66 (4) 823-834; DOI: 10.2337/db16-1351
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