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Journal of Cell ScienceVolume 131, Issue 1, 1 January 2018, Article number jcs.212159

NudE regulates dynein at kinetochores but is dispensable for other dynein functions in the C. elegans early embryo(Article)(Open Access)

  • aInstituto de Biologia Molecular e Celular, Universidade do Porto, Porto, 4200-135, Portugal
  • bInstituto de Investigação e Inovação em Saúde (i3S), Universidade do Porto, Porto, 4200-135, Portugal

Abstract

In mitosis, themolecular motor dynein is recruited to kinetochores by the Rod-Zw10-Zwilch complex (RZZ) and Spindly to control spindle assembly checkpoint (SAC) signaling and microtubule attachment. How the ubiquitous dynein co-factors Lis1 and NudE contribute to these functions remains poorly understood. Here, we show that the C. elegans NudE homolog NUD-2 is dispensable for dynein- and LIS-1-dependent mitotic spindle assembly in the zygote. This facilitates functional characterization of kinetochore-localized NUD-2, which is recruited by the CENP-F-like proteins HCP-1 and HCP-2 independently of RZZ- Spindly and dynein-LIS-1. Kinetochore dynein levels are reduced in Δnud-2 embryos, and, as occurs upon RZZ inhibition, loss of NUD-2 delays the formation of load-bearing kinetochore-microtubule attachments and causes chromatin bridges in anaphase. Survival of Δnud-2 embryos requires a functional SAC, and kinetochores without NUD-2 recruit an excess of SAC proteins. Consistent with this, SAC signaling in early Δnud-2 embryos extends mitotic duration and prevents high rates of chromosome mis-segregation. Our results reveal that both NUD-2 and RZZ-Spindly are essential for dynein function at kinetochores, and that the gain in SAC strength during early embryonic development is relevant under conditions that mildly perturb mitosis. © 2018. Published by The Company of Biologists Ltd.

Author keywords

DyneinKinetochoreLis1NDE1NudEPAFAH1B1RZZSpindle assembly checkpoint

Indexed keywords

EMTREE drug terms:dynein adenosine triphosphataseHCP 1 proteinHCP 2 proteinmicroorganism proteinNudE proteinunclassified drugCaenorhabditis elegans proteincarrier proteincell cycle proteindynein adenosine triphosphatasehcp-1 protein, C elegansHCP-2 protein, C eleganslis-1 protein, C elegansmicrotubule associated proteinnonhistone protein
EMTREE medical terms:ArticleCaenorhabditis eleganschromosome segregationcontrolled studyembryoembryo developmentenzyme regulationintracellular signalingkinetochoreM phase cell cycle checkpointmitosis spindlenonhumanparasite survivalpriority journalprotein assemblyprotein functionprotein localizationprotein protein interactionzygoteanimalCaenorhabditis elegansembryologykinetochoreM phase cell cycle checkpointmetabolismmicrotubulesignal transductionspindle apparatus
MeSH:AnimalsCaenorhabditis elegansCaenorhabditis elegans ProteinsCarrier ProteinsCell Cycle ProteinsChromosomal Proteins, Non-HistoneChromosome SegregationDyneinsKinetochoresM Phase Cell Cycle CheckpointsMicrotubule-Associated ProteinsMicrotubulesSignal TransductionSpindle Apparatus

Chemicals and CAS Registry Numbers:

dynein adenosine triphosphatase; carrier protein, 80700-39-6;

Caenorhabditis elegans Proteins; Carrier Proteins; Cell Cycle Proteins; Chromosomal Proteins, Non-Histone; Dyneins; hcp-1 protein, C elegans; HCP-2 protein, C elegans; lis-1 protein, C elegans; Microtubule-Associated Proteins

Funding details

Funding sponsor Funding number Acronym
P40 OD010440
Fundação Portugal Telecom
ERC-2013-StG-338410-DYNEINOME
Norte-01-0145-FEDER-000029,IF/01015/2013/CP1157/CT0006
European Molecular Biology Organization
See opportunities by EMBO		EMBO
European Metrology Programme for Innovation and ResearchEMPIR
NORTE 2020

  • 1

    We thank Arshad Desai for critical reading of the manuscript and Risa Kitagawa for C. elegans strain RQ283. Some strains were provided by the Caenorhabditis Genetics Center (CGC), which is funded by NIH Office of Research Infrastructure Programs (P40 OD010440).

  • 2

    This project was funded by the European Research Council under the European Union’s Seventh Framework Programme (ERC grant agreement no. ERC-2013-StG-338410-DYNEINOME to R.G.), and the European Union’s Horizon 2020 Research and Innovation Programme (ERC grant agreement no. ERC-2014-StG-640553-ACTOMYO to A.X.C.). Additional funding was from the European Molecular Biology Organization (Installation Grant; R.G.), from the Fundaçaõ para a Ciência e a Tecnologia (IF/01015/2013/CP1157/CT0006; R.G.), and from the project ‘Norte-01-0145-FEDER-000029, Advancing cancer research: from basic knowledge to application’, supported by the Norte Portugal Regional Operational Programme (NORTE 2020), under the PORTUGAL 2020 Partnership Agreement through the European Regional Development Fund (FEDER). Deposited in PMC for immediate release.

  • ISSN: 00219533
  • CODEN: JNCSA
  • Source Type: Journal
  • Original language: English
  • DOI: 10.1242/jcs.212159
  • PubMed ID: 29192061
  • Document Type: Article
  • Publisher: Company of Biologists Ltd

  Gassmann, R.; Instituto de Biologia Molecular e Celular, Universidade do Porto, Porto, Portugal;
© Copyright 2019 Elsevier B.V., All rights reserved.

Cited by 6 documents

Celestino, R. , Henen, M.A. , Gama, J.B.
A transient helix in the disordered region of dynein light intermediate chain links the motor to structurally diverse adaptors for cargo transport
(2019) PLoS Biology
Pintard, L. , Bowerman, B.
Mitotic cell division in caenorhabditis elegans
(2019) Genetics
Edwards, F. , Maton, G. , Gareil, N.
BUB-1 promotes amphitelic chromosome biorientation via multiple activities at the kinetochore
(2018) eLife
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