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Is Dynamic Autocrine Insulin Signaling Possible? A Mathematical Model Predicts Picomolar Concentrations of Extracellular Monomeric Insulin within Human Pancreatic Islets

Journal Article · · PLoS ONE
 [1];  [1];  [2];  [2]
  1. University of Louisville, KY (United States)
  2. University of British Columbia, Vancouver, BC (Canada)

Insulin signaling is essential for β-cell survival and proliferation in vivo. Insulin also has potent mitogenic and anti-apoptotic actions on cultured β-cells, with maximum effect in the high picomolar range and diminishing effect at high nanomolar doses. In order to understand whether these effects of insulin are constitutive or can be subjected to physiological modulation, it is essential to estimate the extracellular concentration of monomeric insulin within an intact islet. Unfortunately, the in vivo concentration of insulin monomers within the islet cannot be measured directly with current technology. Here, we present the first mathematical model designed to estimate the levels of monomeric insulin within the islet extracellular space. Insulin is released as insoluble crystals that exhibit a delayed dissociation into hexamers, dimers, and eventually monomers, which only then can act as signaling ligands. The rates at which different forms of insulin dissolve in vivo have been estimated from studies of peripheral insulin injection sites. We used this and other information to formulate a mathematical model to estimate the local insulin concentration within a single islet as a function of glucose. Model parameters were estimated from existing literature. Components of the model were validated using experimental data, if available. Model analysis predicted that the majority of monomeric insulin in the islet is that which has been returned from the periphery, and the concentration of intra-islet monomeric insulin varies from β50–300 pM when glucose is in the physiological range. Thus, our results suggest that the local concentration of monomeric insulin within the islet is in the picomolar ‘sweet spot’ range of insulin doses that activate the insulin receptor and have the most potent effects on β-cells in vitro. Together with experimental data, these estimations support the concept that autocrine/paracrine insulin signalling within the islet is dynamic, rather than constitutive and saturated.

Research Organization:
Univ. of Louisville, KY (United States)
Sponsoring Organization:
USDOE; National Institutes of Health (NIH); Canadian Institutes for Health Research; Juvenile Diabetes Research Foundation; Michael Smith Foundation; Canadian Diabetes Association
Grant/Contract Number:
EM0000197; R01-DE019243; P30-ES014443
OSTI ID:
1904774
Journal Information:
PLoS ONE, Vol. 8, Issue 6; ISSN 1932-6203
Publisher:
Public Library of ScienceCopyright Statement
Country of Publication:
United States
Language:
English

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Cited By (6)

Insulin secretion from beta cells in intact mouse islets is targeted towards the vasculature journal May 2014
A live-cell, high-content imaging survey of 206 endogenous factors across five stress conditions reveals context-dependent survival effects in mouse primary beta cells journal March 2015
Inter-domain tagging implicates caveolin-1 in insulin receptor trafficking and Erk signaling bias in pancreatic beta-cells journal May 2016
Insulin secretion from beta cells within intact islets: Location matters journal March 2015
Effects of insulin on human pancreatic cancer progression modeled in vitro text January 2014
B Cell Receptor Affinity for Insulin Dictates Autoantigen Acquisition and B Cell Functionality in Autoimmune Diabetes journal November 2016

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