Cytoplasmic flows as signatures for the mechanics of mitotic positioning

Ehssan Nazockdast, Abtin Rahimian, Daniel Needleman, Michael Shelley

Research output: Contribution to journalArticle

Abstract

The proper positioning of mitotic spindle in the single-cell Caenorhabditis elegans embryo is achieved initially by the migration and rotation of the pronuclear complex (PNC) and its two associated astral microtubules (MTs). Pronuclear migration produces global cytoplasmic flows that couple the mechanics of all MTs, the PNC, and the cell periphery with each other through their hydrodynamic interactions (HIs). We present the first computational study that explicitly accounts for detailed HIs between the cytoskeletal components and demonstrate the key consequences of HIs for the mechanics of pronuclear migration. First, we show that, because of HIs between the MTs, the cytoplasm-filled astral MTs behave like a porous medium, with its permeability decreasing with increasing the number of MTs. We then directly study the dynamics of PNC migration under various force-Transduction models, including the pushing or pulling of MTs at the cortex and the pulling of MTs by cytoplasmically bound force generators. Although achieving proper position and orientation on reasonable time scales does not uniquely choose a model, we find that each model produces a different signature in its induced cytoplasmic flow. We suggest that cytoplasmic flows can be used to differentiate between mechanisms.

Original languageEnglish (US)
Pages (from-to)3261-3270
Number of pages10
JournalMolecular Biology of the Cell
Volume28
Issue number23
DOIs
StatePublished - Nov 7 2017

Fingerprint

Mechanics
Microtubules
Hydrodynamics
Spindle Apparatus
Caenorhabditis elegans
Permeability
Cytoplasm
Embryonic Structures

ASJC Scopus subject areas

  • Molecular Biology
  • Cell Biology

Cite this

Cytoplasmic flows as signatures for the mechanics of mitotic positioning. / Nazockdast, Ehssan; Rahimian, Abtin; Needleman, Daniel; Shelley, Michael.

In: Molecular Biology of the Cell, Vol. 28, No. 23, 07.11.2017, p. 3261-3270.

Research output: Contribution to journalArticle

Nazockdast, E, Rahimian, A, Needleman, D & Shelley, M 2017, 'Cytoplasmic flows as signatures for the mechanics of mitotic positioning', Molecular Biology of the Cell, vol. 28, no. 23, pp. 3261-3270. https://doi.org/10.1091/mbc.E16-02-0108
Nazockdast, Ehssan ; Rahimian, Abtin ; Needleman, Daniel ; Shelley, Michael. / Cytoplasmic flows as signatures for the mechanics of mitotic positioning. In: Molecular Biology of the Cell. 2017 ; Vol. 28, No. 23. pp. 3261-3270.
@article{cfbd187e7a26446a9c1a8b83076101c5,
title = "Cytoplasmic flows as signatures for the mechanics of mitotic positioning",
abstract = "The proper positioning of mitotic spindle in the single-cell Caenorhabditis elegans embryo is achieved initially by the migration and rotation of the pronuclear complex (PNC) and its two associated astral microtubules (MTs). Pronuclear migration produces global cytoplasmic flows that couple the mechanics of all MTs, the PNC, and the cell periphery with each other through their hydrodynamic interactions (HIs). We present the first computational study that explicitly accounts for detailed HIs between the cytoskeletal components and demonstrate the key consequences of HIs for the mechanics of pronuclear migration. First, we show that, because of HIs between the MTs, the cytoplasm-filled astral MTs behave like a porous medium, with its permeability decreasing with increasing the number of MTs. We then directly study the dynamics of PNC migration under various force-Transduction models, including the pushing or pulling of MTs at the cortex and the pulling of MTs by cytoplasmically bound force generators. Although achieving proper position and orientation on reasonable time scales does not uniquely choose a model, we find that each model produces a different signature in its induced cytoplasmic flow. We suggest that cytoplasmic flows can be used to differentiate between mechanisms.",
author = "Ehssan Nazockdast and Abtin Rahimian and Daniel Needleman and Michael Shelley",
year = "2017",
month = "11",
day = "7",
doi = "10.1091/mbc.E16-02-0108",
language = "English (US)",
volume = "28",
pages = "3261--3270",
journal = "Molecular Biology of the Cell",
issn = "1059-1524",
publisher = "American Society for Cell Biology",
number = "23",

}

TY - JOUR

T1 - Cytoplasmic flows as signatures for the mechanics of mitotic positioning

AU - Nazockdast, Ehssan

AU - Rahimian, Abtin

AU - Needleman, Daniel

AU - Shelley, Michael

PY - 2017/11/7

Y1 - 2017/11/7

N2 - The proper positioning of mitotic spindle in the single-cell Caenorhabditis elegans embryo is achieved initially by the migration and rotation of the pronuclear complex (PNC) and its two associated astral microtubules (MTs). Pronuclear migration produces global cytoplasmic flows that couple the mechanics of all MTs, the PNC, and the cell periphery with each other through their hydrodynamic interactions (HIs). We present the first computational study that explicitly accounts for detailed HIs between the cytoskeletal components and demonstrate the key consequences of HIs for the mechanics of pronuclear migration. First, we show that, because of HIs between the MTs, the cytoplasm-filled astral MTs behave like a porous medium, with its permeability decreasing with increasing the number of MTs. We then directly study the dynamics of PNC migration under various force-Transduction models, including the pushing or pulling of MTs at the cortex and the pulling of MTs by cytoplasmically bound force generators. Although achieving proper position and orientation on reasonable time scales does not uniquely choose a model, we find that each model produces a different signature in its induced cytoplasmic flow. We suggest that cytoplasmic flows can be used to differentiate between mechanisms.

AB - The proper positioning of mitotic spindle in the single-cell Caenorhabditis elegans embryo is achieved initially by the migration and rotation of the pronuclear complex (PNC) and its two associated astral microtubules (MTs). Pronuclear migration produces global cytoplasmic flows that couple the mechanics of all MTs, the PNC, and the cell periphery with each other through their hydrodynamic interactions (HIs). We present the first computational study that explicitly accounts for detailed HIs between the cytoskeletal components and demonstrate the key consequences of HIs for the mechanics of pronuclear migration. First, we show that, because of HIs between the MTs, the cytoplasm-filled astral MTs behave like a porous medium, with its permeability decreasing with increasing the number of MTs. We then directly study the dynamics of PNC migration under various force-Transduction models, including the pushing or pulling of MTs at the cortex and the pulling of MTs by cytoplasmically bound force generators. Although achieving proper position and orientation on reasonable time scales does not uniquely choose a model, we find that each model produces a different signature in its induced cytoplasmic flow. We suggest that cytoplasmic flows can be used to differentiate between mechanisms.

UR - http://www.scopus.com/inward/record.url?scp=85033445073&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85033445073&partnerID=8YFLogxK

U2 - 10.1091/mbc.E16-02-0108

DO - 10.1091/mbc.E16-02-0108

M3 - Article

C2 - 28331070

AN - SCOPUS:85033445073

VL - 28

SP - 3261

EP - 3270

JO - Molecular Biology of the Cell

JF - Molecular Biology of the Cell

SN - 1059-1524

IS - 23

ER -