A new multicompartmental reaction-diffusion modeling method links transient membrane attachment of E. coli MinE to E-ring formation

Satya Nanda Vel Arjunan, Masaru Tomita

Research output: Contribution to journalArticle

51 Citations (Scopus)

Abstract

Many important cellular processes are regulated by reaction-diffusion (RD) of molecules that takes place both in the cytoplasm and on the membrane. To model and analyze such multicompartmental processes, we developed a lattice-based Monte Carlo method, Spatiocyte that supports RD in volume and surface compartments at single molecule resolution. Stochasticity in RD and the excluded volume effect brought by intracellular molecular crowding, both of which can significantly affect RD and thus, cellular processes, are also supported. We verified the method by comparing simulation results of diffusion, irreversible and reversible reactions with the predicted analytical and best available numerical solutions. Moreover, to directly compare the localization patterns of molecules in fluorescence microscopy images with simulation, we devised a visualization method that mimics the microphotography process by showing the trajectory of simulated molecules averaged according to the camera exposure time. In the rod-shaped bacterium Escherichia coli, the division site is suppressed at the cell poles by periodic pole-to-pole oscillations of the Min proteins (MinC, MinD and MinE) arising from carefully orchestrated RD in both cytoplasm and membrane compartments. Using Spatiocyte we could model and reproduce the in vivo MinDE localization dynamics by accounting for the previously reported properties of MinE. Our results suggest that the MinE ring, which is essential in preventing polar septation, is largely composed of MinE that is transiently attached to the membrane independently after recruited by MinD. Overall, Spatiocyte allows simulation and visualization of complex spatial and reaction-diffusion mediated cellular processes in volumes and surfaces. As we showed, it can potentially provide mechanistic insights otherwise difficult to obtain experimentally.

Original languageEnglish
Pages (from-to)35-53
Number of pages19
JournalSystems and Synthetic Biology
Volume4
Issue number1
DOIs
Publication statusPublished - 2010 Feb

Fingerprint

Escherichia coli
Membranes
Poles
Molecules
Cytoplasm
Visualization
Monte Carlo Method
Crowding
Fluorescence microscopy
Fluorescence Microscopy
Bacteria
Monte Carlo methods
Cameras
Trajectories
Proteins

Keywords

  • Bacterial cytoskeleton
  • Diffusion-limited
  • E-Cell
  • E-ring
  • FtsZ
  • Multiscale
  • Noise
  • Spatial gradient

ASJC Scopus subject areas

  • Biotechnology
  • Bioengineering
  • Molecular Biology

Cite this

A new multicompartmental reaction-diffusion modeling method links transient membrane attachment of E. coli MinE to E-ring formation. / Arjunan, Satya Nanda Vel; Tomita, Masaru.

In: Systems and Synthetic Biology, Vol. 4, No. 1, 02.2010, p. 35-53.

Research output: Contribution to journalArticle

@article{618d9a1f8e944b878c4161957a8af3c9,
title = "A new multicompartmental reaction-diffusion modeling method links transient membrane attachment of E. coli MinE to E-ring formation",
abstract = "Many important cellular processes are regulated by reaction-diffusion (RD) of molecules that takes place both in the cytoplasm and on the membrane. To model and analyze such multicompartmental processes, we developed a lattice-based Monte Carlo method, Spatiocyte that supports RD in volume and surface compartments at single molecule resolution. Stochasticity in RD and the excluded volume effect brought by intracellular molecular crowding, both of which can significantly affect RD and thus, cellular processes, are also supported. We verified the method by comparing simulation results of diffusion, irreversible and reversible reactions with the predicted analytical and best available numerical solutions. Moreover, to directly compare the localization patterns of molecules in fluorescence microscopy images with simulation, we devised a visualization method that mimics the microphotography process by showing the trajectory of simulated molecules averaged according to the camera exposure time. In the rod-shaped bacterium Escherichia coli, the division site is suppressed at the cell poles by periodic pole-to-pole oscillations of the Min proteins (MinC, MinD and MinE) arising from carefully orchestrated RD in both cytoplasm and membrane compartments. Using Spatiocyte we could model and reproduce the in vivo MinDE localization dynamics by accounting for the previously reported properties of MinE. Our results suggest that the MinE ring, which is essential in preventing polar septation, is largely composed of MinE that is transiently attached to the membrane independently after recruited by MinD. Overall, Spatiocyte allows simulation and visualization of complex spatial and reaction-diffusion mediated cellular processes in volumes and surfaces. As we showed, it can potentially provide mechanistic insights otherwise difficult to obtain experimentally.",
keywords = "Bacterial cytoskeleton, Diffusion-limited, E-Cell, E-ring, FtsZ, Multiscale, Noise, Spatial gradient",
author = "Arjunan, {Satya Nanda Vel} and Masaru Tomita",
year = "2010",
month = "2",
doi = "10.1007/s11693-009-9047-2",
language = "English",
volume = "4",
pages = "35--53",
journal = "Systems and Synthetic Biology",
issn = "1872-5325",
publisher = "Springer Netherlands",
number = "1",

}

TY - JOUR

T1 - A new multicompartmental reaction-diffusion modeling method links transient membrane attachment of E. coli MinE to E-ring formation

AU - Arjunan, Satya Nanda Vel

AU - Tomita, Masaru

PY - 2010/2

Y1 - 2010/2

N2 - Many important cellular processes are regulated by reaction-diffusion (RD) of molecules that takes place both in the cytoplasm and on the membrane. To model and analyze such multicompartmental processes, we developed a lattice-based Monte Carlo method, Spatiocyte that supports RD in volume and surface compartments at single molecule resolution. Stochasticity in RD and the excluded volume effect brought by intracellular molecular crowding, both of which can significantly affect RD and thus, cellular processes, are also supported. We verified the method by comparing simulation results of diffusion, irreversible and reversible reactions with the predicted analytical and best available numerical solutions. Moreover, to directly compare the localization patterns of molecules in fluorescence microscopy images with simulation, we devised a visualization method that mimics the microphotography process by showing the trajectory of simulated molecules averaged according to the camera exposure time. In the rod-shaped bacterium Escherichia coli, the division site is suppressed at the cell poles by periodic pole-to-pole oscillations of the Min proteins (MinC, MinD and MinE) arising from carefully orchestrated RD in both cytoplasm and membrane compartments. Using Spatiocyte we could model and reproduce the in vivo MinDE localization dynamics by accounting for the previously reported properties of MinE. Our results suggest that the MinE ring, which is essential in preventing polar septation, is largely composed of MinE that is transiently attached to the membrane independently after recruited by MinD. Overall, Spatiocyte allows simulation and visualization of complex spatial and reaction-diffusion mediated cellular processes in volumes and surfaces. As we showed, it can potentially provide mechanistic insights otherwise difficult to obtain experimentally.

AB - Many important cellular processes are regulated by reaction-diffusion (RD) of molecules that takes place both in the cytoplasm and on the membrane. To model and analyze such multicompartmental processes, we developed a lattice-based Monte Carlo method, Spatiocyte that supports RD in volume and surface compartments at single molecule resolution. Stochasticity in RD and the excluded volume effect brought by intracellular molecular crowding, both of which can significantly affect RD and thus, cellular processes, are also supported. We verified the method by comparing simulation results of diffusion, irreversible and reversible reactions with the predicted analytical and best available numerical solutions. Moreover, to directly compare the localization patterns of molecules in fluorescence microscopy images with simulation, we devised a visualization method that mimics the microphotography process by showing the trajectory of simulated molecules averaged according to the camera exposure time. In the rod-shaped bacterium Escherichia coli, the division site is suppressed at the cell poles by periodic pole-to-pole oscillations of the Min proteins (MinC, MinD and MinE) arising from carefully orchestrated RD in both cytoplasm and membrane compartments. Using Spatiocyte we could model and reproduce the in vivo MinDE localization dynamics by accounting for the previously reported properties of MinE. Our results suggest that the MinE ring, which is essential in preventing polar septation, is largely composed of MinE that is transiently attached to the membrane independently after recruited by MinD. Overall, Spatiocyte allows simulation and visualization of complex spatial and reaction-diffusion mediated cellular processes in volumes and surfaces. As we showed, it can potentially provide mechanistic insights otherwise difficult to obtain experimentally.

KW - Bacterial cytoskeleton

KW - Diffusion-limited

KW - E-Cell

KW - E-ring

KW - FtsZ

KW - Multiscale

KW - Noise

KW - Spatial gradient

UR - http://www.scopus.com/inward/record.url?scp=76149129015&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=76149129015&partnerID=8YFLogxK

U2 - 10.1007/s11693-009-9047-2

DO - 10.1007/s11693-009-9047-2

M3 - Article

VL - 4

SP - 35

EP - 53

JO - Systems and Synthetic Biology

JF - Systems and Synthetic Biology

SN - 1872-5325

IS - 1

ER -