A Cellular Automaton Model As a First Model-Based Assessment of Interacting Mechanisms for Insulin Granule Transport in Beta Cells

Overview

Journal Cells

Publisher MDPI

Specialties Biochemistry
Biophysics
Cell Biology
Molecular Biology

Date 2020 Jun 24

PMID 32570905

Citations 3

Authors

Michael Muller

Mathias Glombek

Jeldrick Powitz

Dennis Bruning

Ingo Rustenbeck

Affiliations

Soon will be listed here.

Abstract

In this paper a first model is derived and applied which describes the transport of insulin granules through the cell interior and at the membrane of a beta cell. A special role is assigned to the actin network, which significantly influences the transport. For this purpose, microscopically measured actin networks are characterized and then further ones are artificially generated. In a Cellular Automaton model, phenomenological laws for granule movement are formulated and implemented. Simulation results are compared with experiments, primarily using TIRF images and secretion rates. In this respect, good similarities are already apparent. The model is a first useful approach to describe complex granule transport processes in beta cells, and offers great potential for future extensions. Furthermore, the model can be used as a tool to validate hypotheses and associated mechanisms regarding their effect on exocytosis or other processes. For this purpose, the source code for the model is provided online.

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References

Schulze T, Morsi M, Reckers K, Bruning D, Seemann N, Panten U . Metabolic amplification of insulin secretion is differentially desensitized by depolarization in the absence of exogenous fuels. Metabolism. 2017; 67:1-13. DOI: 10.1016/j.metabol.2016.10.008. View

Axelrod D . Selective imaging of surface fluorescence with very high aperture microscope objectives. J Biomed Opt. 2001; 6(1):6-13. DOI: 10.1117/1.1335689. View

Nesher R, Cerasi E . Modeling phasic insulin release: immediate and time-dependent effects of glucose. Diabetes. 2002; 51 Suppl 1:S53-9. DOI: 10.2337/diabetes.51.2007.s53. View

Hatlapatka K, Matz M, Schumacher K, Baumann K, Rustenbeck I . Bidirectional insulin granule turnover in the submembrane space during K(+) depolarization-induced secretion. Traffic. 2011; 12(9):1166-78. DOI: 10.1111/j.1600-0854.2011.01231.x. View

Ohara-Imaizumi M, Nakamichi Y, Tanaka T, Ishida H, Nagamatsu S . Imaging exocytosis of single insulin secretory granules with evanescent wave microscopy: distinct behavior of granule motion in biphasic insulin release. J Biol Chem. 2001; 277(6):3805-8. DOI: 10.1074/jbc.C100712200. View

Rorsman P, Renstrom E . Insulin granule dynamics in pancreatic beta cells. Diabetologia. 2003; 46(8):1029-45. DOI: 10.1007/s00125-003-1153-1. View

Pimenta W, Korytkowski M, Mitrakou A, Jenssen T, Yki-Jarvinen H, Evron W . Pancreatic beta-cell dysfunction as the primary genetic lesion in NIDDM. Evidence from studies in normal glucose-tolerant individuals with a first-degree NIDDM relative. JAMA. 1995; 273(23):1855-61. View

van Haeften T . Early disturbances in insulin secretion in the development of type 2 diabetes mellitus. Mol Cell Endocrinol. 2002; 197(1-2):197-204. DOI: 10.1016/s0303-7207(02)00267-8. View

Mourad N, Nenquin M, Henquin J . Metabolic amplifying pathway increases both phases of insulin secretion independently of beta-cell actin microfilaments. Am J Physiol Cell Physiol. 2010; 299(2):C389-98. DOI: 10.1152/ajpcell.00138.2010. View

10.

White S, Del Rey A, Sanchez G . Modeling epidemics using cellular automata. Appl Math Comput. 2020; 186(1):193-202. PMC: 7127728. DOI: 10.1016/j.amc.2006.06.126. View

11.

Vitale M, Seward E, TRIFARO J . Chromaffin cell cortical actin network dynamics control the size of the release-ready vesicle pool and the initial rate of exocytosis. Neuron. 1995; 14(2):353-63. DOI: 10.1016/0896-6273(95)90291-0. View

12.

Kasai K, Fujita T, Gomi H, Izumi T . Docking is not a prerequisite but a temporal constraint for fusion of secretory granules. Traffic. 2008; 9(7):1191-203. DOI: 10.1111/j.1600-0854.2008.00744.x. View

13.

Lang T, Wacker I, Wunderlich I, Rohrbach A, Giese G, Soldati T . Role of actin cortex in the subplasmalemmal transport of secretory granules in PC-12 cells. Biophys J. 2000; 78(6):2863-77. PMC: 1300873. DOI: 10.1016/S0006-3495(00)76828-7. View

14.

Del Prato S . Loss of early insulin secretion leads to postprandial hyperglycaemia. Diabetologia. 2003; 46 Suppl 1:M2-8. DOI: 10.1007/s00125-002-0930-6. View

15.

Heinemann F, Vogel S, Schwille P . Lateral membrane diffusion modulated by a minimal actin cortex. Biophys J. 2013; 104(7):1465-75. PMC: 3617436. DOI: 10.1016/j.bpj.2013.02.042. View

16.

Heaslip A, Nelson S, Lombardo A, Previs S, Armstrong J, Warshaw D . Cytoskeletal dependence of insulin granule movement dynamics in INS-1 beta-cells in response to glucose. PLoS One. 2014; 9(10):e109082. PMC: 4195697. DOI: 10.1371/journal.pone.0109082. View

17.

Bruning D, Reckers K, Drain P, Rustenbeck I . Glucose but not KCl diminishes submembrane granule turnover in mouse beta-cells. J Mol Endocrinol. 2017; 59(3):311-324. DOI: 10.1530/JME-17-0063. View

18.

Wawrezinieck L, Rigneault H, Marguet D, Lenne P . Fluorescence correlation spectroscopy diffusion laws to probe the submicron cell membrane organization. Biophys J. 2005; 89(6):4029-42. PMC: 1366968. DOI: 10.1529/biophysj.105.067959. View

19.

Torquato , Lu . Chord-length distribution function for two-phase random media. Phys Rev E Stat Phys Plasmas Fluids Relat Interdiscip Topics. 1993; 47(4):2950-2953. DOI: 10.1103/physreve.47.2950. View

20.

Kalwat M, Thurmond D . Signaling mechanisms of glucose-induced F-actin remodeling in pancreatic islet β cells. Exp Mol Med. 2013; 45:e37. PMC: 3789261. DOI: 10.1038/emm.2013.73. View