aPKC-mediated displacement and actomyosin-mediated retention polarize Miranda in Drosophila neuroblasts

Matthew Robert Hannaford, Anne Ramat, Nicolas Loyer, Jens Januschke (Lead / Corresponding author)

Research output: Contribution to journalArticle

7 Citations (Scopus)
77 Downloads (Pure)

Abstract

Cell fate assignment in the nervous system of vertebrates and invertebrates often hinges on the unequal distribution of molecules during progenitor cell division. We address asymmetric fate determinant localization in the developing Drosophila nervous system, specifically the control of the polarized distribution of the cell fate adapter protein Miranda. We reveal a step-wise polarization of Miranda in larval neuroblasts and find that Miranda’s dynamics and cortical association are differently regulated between interphase and mitosis. In interphase Miranda binds to the plasma membrane. Then, before nuclear envelope breakdown, Miranda is phosphorylated by aPKC and displaced into the cytoplasm. This clearance is necessary for the subsequent establishment of asymmetric Miranda localization. After nuclear envelope breakdown, actomyosin activity is required to maintain Miranda asymmetry. Therefore, phosphorylation by aPKC and differential binding to the actomyosin network are required at distinct phases of the cell cycle to polarize fate determinant localization in neuroblasts.
Original languageEnglish
Article numbere29939
Number of pages22
JournaleLife
Volume7
DOIs
Publication statusPublished - 24 Jan 2018

Fingerprint

Actomyosin
Interphase
Nuclear Envelope
Neurology
Nervous System
Drosophila
Cells
Phosphorylation
Invertebrates
Hinges
Cell membranes
Mitosis
Cell Division
Vertebrates
Cell Cycle
Cytoplasm
Stem Cells
Cell Membrane
Association reactions
Polarization

Keywords

  • Actomyosin/metabolism
  • Animals
  • Cell Cycle Proteins/metabolism
  • Drosophila Proteins/metabolism
  • Drosophila/growth & development
  • Larva/growth & development
  • Neurons/physiology
  • Phosphorylation
  • Protein Binding
  • Protein Kinase C/metabolism
  • Protein Processing, Post-Translational
  • Stem Cells/physiology

Cite this

@article{b7630f8a93464dbe84f257282b4f5c2c,
title = "aPKC-mediated displacement and actomyosin-mediated retention polarize Miranda in Drosophila neuroblasts",
abstract = "Cell fate assignment in the nervous system of vertebrates and invertebrates often hinges on the unequal distribution of molecules during progenitor cell division. We address asymmetric fate determinant localization in the developing Drosophila nervous system, specifically the control of the polarized distribution of the cell fate adapter protein Miranda. We reveal a step-wise polarization of Miranda in larval neuroblasts and find that Miranda’s dynamics and cortical association are differently regulated between interphase and mitosis. In interphase Miranda binds to the plasma membrane. Then, before nuclear envelope breakdown, Miranda is phosphorylated by aPKC and displaced into the cytoplasm. This clearance is necessary for the subsequent establishment of asymmetric Miranda localization. After nuclear envelope breakdown, actomyosin activity is required to maintain Miranda asymmetry. Therefore, phosphorylation by aPKC and differential binding to the actomyosin network are required at distinct phases of the cell cycle to polarize fate determinant localization in neuroblasts.",
keywords = "Actomyosin/metabolism, Animals, Cell Cycle Proteins/metabolism, Drosophila Proteins/metabolism, Drosophila/growth & development, Larva/growth & development, Neurons/physiology, Phosphorylation, Protein Binding, Protein Kinase C/metabolism, Protein Processing, Post-Translational, Stem Cells/physiology",
author = "Hannaford, {Matthew Robert} and Anne Ramat and Nicolas Loyer and Jens Januschke",
note = "Work in J.J.’s laboratory is supported by Wellcome and the Royal Society Sir Henry Dale fellowship 100031Z/12/Z. M.R.H is supported by an MRC studentship funded by these grants: G1000386/1, MR/J50046X/1, MR/K500896/1, MR/K501384/1. The tissue imaging facility is supported by the grant WT101468 from Wellcome.",
year = "2018",
month = "1",
day = "24",
doi = "10.7554/eLife.29939",
language = "English",
volume = "7",
journal = "eLife",
issn = "2050-084X",
publisher = "eLife Sciences Publications Ltd.",

}

aPKC-mediated displacement and actomyosin-mediated retention polarize Miranda in Drosophila neuroblasts. / Hannaford, Matthew Robert; Ramat, Anne; Loyer, Nicolas; Januschke, Jens (Lead / Corresponding author).

In: eLife, Vol. 7, e29939, 24.01.2018.

Research output: Contribution to journalArticle

TY - JOUR

T1 - aPKC-mediated displacement and actomyosin-mediated retention polarize Miranda in Drosophila neuroblasts

AU - Hannaford, Matthew Robert

AU - Ramat, Anne

AU - Loyer, Nicolas

AU - Januschke, Jens

N1 - Work in J.J.’s laboratory is supported by Wellcome and the Royal Society Sir Henry Dale fellowship 100031Z/12/Z. M.R.H is supported by an MRC studentship funded by these grants: G1000386/1, MR/J50046X/1, MR/K500896/1, MR/K501384/1. The tissue imaging facility is supported by the grant WT101468 from Wellcome.

PY - 2018/1/24

Y1 - 2018/1/24

N2 - Cell fate assignment in the nervous system of vertebrates and invertebrates often hinges on the unequal distribution of molecules during progenitor cell division. We address asymmetric fate determinant localization in the developing Drosophila nervous system, specifically the control of the polarized distribution of the cell fate adapter protein Miranda. We reveal a step-wise polarization of Miranda in larval neuroblasts and find that Miranda’s dynamics and cortical association are differently regulated between interphase and mitosis. In interphase Miranda binds to the plasma membrane. Then, before nuclear envelope breakdown, Miranda is phosphorylated by aPKC and displaced into the cytoplasm. This clearance is necessary for the subsequent establishment of asymmetric Miranda localization. After nuclear envelope breakdown, actomyosin activity is required to maintain Miranda asymmetry. Therefore, phosphorylation by aPKC and differential binding to the actomyosin network are required at distinct phases of the cell cycle to polarize fate determinant localization in neuroblasts.

AB - Cell fate assignment in the nervous system of vertebrates and invertebrates often hinges on the unequal distribution of molecules during progenitor cell division. We address asymmetric fate determinant localization in the developing Drosophila nervous system, specifically the control of the polarized distribution of the cell fate adapter protein Miranda. We reveal a step-wise polarization of Miranda in larval neuroblasts and find that Miranda’s dynamics and cortical association are differently regulated between interphase and mitosis. In interphase Miranda binds to the plasma membrane. Then, before nuclear envelope breakdown, Miranda is phosphorylated by aPKC and displaced into the cytoplasm. This clearance is necessary for the subsequent establishment of asymmetric Miranda localization. After nuclear envelope breakdown, actomyosin activity is required to maintain Miranda asymmetry. Therefore, phosphorylation by aPKC and differential binding to the actomyosin network are required at distinct phases of the cell cycle to polarize fate determinant localization in neuroblasts.

KW - Actomyosin/metabolism

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KW - Cell Cycle Proteins/metabolism

KW - Drosophila Proteins/metabolism

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KW - Larva/growth & development

KW - Neurons/physiology

KW - Phosphorylation

KW - Protein Binding

KW - Protein Kinase C/metabolism

KW - Protein Processing, Post-Translational

KW - Stem Cells/physiology

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