Literature DB >> 21642510

Clustering of nuclei in multinucleated hyphae is prevented by dynein-driven bidirectional nuclear movements and microtubule growth control in Ashbya gossypii.

Sandrine Grava1, Miyako Keller, Sylvia Voegeli, Shanon Seger, Claudia Lang, Peter Philippsen.   

Abstract

During filamentous fungus development, multinucleated hyphae employ a system for long-range nuclear migration to maintain an equal nuclear density. A decade ago the microtubule motor dynein was shown to play a central role in this process. Previous studies with Ashbya gossypii revealed extensive bidirectional movements and bypassings of nuclei, an autonomous cytoplasmic microtubule (cMT) cytoskeleton emanating from each nucleus, and pulling of nuclei by sliding of cMTs along the cortex. Here, we show that dynein is the sole motor for bidirectional movements and bypassing because these movements are concomitantly decreased in mutants carrying truncations of the dynein heavy-chain DYN1 promoter. The dynactin component Jnm1, the accessory proteins Dyn2 and Ndl1, and the potential dynein cortical anchor Num1 are also involved in the dynamic distribution of nuclei. In their absence, nuclei aggregate to different degrees, whereby the mutants with dense nuclear clusters grow extremely long cMTs. As in budding yeast, we found that dynein is delivered to cMT plus ends, and its activity or processivity is probably controlled by dynactin and Num1. Together with its role in powering nuclear movements, we propose that dynein also plays (directly or indirectly) a role in the control of cMT length. Those combined dynein actions prevent nuclear clustering in A. gossypii and thus reveal a novel cellular role for dynein.

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Year:  2011        PMID: 21642510      PMCID: PMC3147418          DOI: 10.1128/EC.05095-11

Source DB:  PubMed          Journal:  Eukaryot Cell        ISSN: 1535-9786


  46 in total

1.  A split motor domain in a cytoplasmic dynein.

Authors:  A Straube; W Enard; A Berner; R Wedlich-Söldner; R Kahmann; G Steinberg
Journal:  EMBO J       Date:  2001-09-17       Impact factor: 11.598

2.  Dynein supports motility of endoplasmic reticulum in the fungus Ustilago maydis.

Authors:  Roland Wedlich-Söldner; Irene Schulz; Anne Straube; Gero Steinberg
Journal:  Mol Biol Cell       Date:  2002-03       Impact factor: 4.138

3.  The Aspergillus cytoplasmic dynein heavy chain and NUDF localize to microtubule ends and affect microtubule dynamics.

Authors:  G Han; B Liu; J Zhang; W Zuo; N R Morris; X Xiang
Journal:  Curr Biol       Date:  2001-05-01       Impact factor: 10.834

4.  Dynamic positioning of mitotic spindles in yeast: role of microtubule motors and cortical determinants.

Authors:  E Yeh; C Yang; E Chin; P Maddox; E D Salmon; D J Lew; K Bloom
Journal:  Mol Biol Cell       Date:  2000-11       Impact factor: 4.138

5.  Genetic evidence for a microtubule-destabilizing effect of conventional kinesin and analysis of its consequences for the control of nuclear distribution in Aspergillus nidulans.

Authors:  N Requena; C Alberti-Segui; E Winzenburg; C Horn; M Schliwa; P Philippsen; R Liese; R Fischer
Journal:  Mol Microbiol       Date:  2001-10       Impact factor: 3.501

6.  Asymmetric loading of Kar9 onto spindle poles and microtubules ensures proper spindle alignment.

Authors:  Dimitris Liakopoulos; Justine Kusch; Sandrine Grava; Jackie Vogel; Yves Barral
Journal:  Cell       Date:  2003-02-21       Impact factor: 41.582

7.  Cortical Num1p interacts with the dynein intermediate chain Pac11p and cytoplasmic microtubules in budding yeast.

Authors:  M Farkasovsky; H Küntzel
Journal:  J Cell Biol       Date:  2001-01-22       Impact factor: 10.539

8.  Cytoplasmic dynein is required to oppose the force that moves nuclei towards the hyphal tip in the filamentous ascomycete Ashbya gossypii.

Authors:  C Alberti-Segui; F Dietrich; R Altmann-Jöhl; D Hoepfner; P Philippsen
Journal:  J Cell Sci       Date:  2001-03       Impact factor: 5.285

9.  A PAK-like protein kinase is required for maturation of young hyphae and septation in the filamentous ascomycete Ashbya gossypii.

Authors:  Y Ayad-Durieux; P Knechtle; S Goff; F Dietrich; P Philippsen
Journal:  J Cell Sci       Date:  2000-12       Impact factor: 5.285

10.  The role of the lissencephaly protein Pac1 during nuclear migration in budding yeast.

Authors:  Wei-Lih Lee; Jessica R Oberle; John A Cooper
Journal:  J Cell Biol       Date:  2003-02-03       Impact factor: 10.539

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  11 in total

Review 1.  Cytoplasmic dynein and early endosome transport.

Authors:  Xin Xiang; Rongde Qiu; Xuanli Yao; Herbert N Arst; Miguel A Peñalva; Jun Zhang
Journal:  Cell Mol Life Sci       Date:  2015-05-23       Impact factor: 9.261

2.  Nuclear repulsion enables division autonomy in a single cytoplasm.

Authors:  Cori A Anderson; Umut Eser; Therese Korndorf; Mark E Borsuk; Jan M Skotheim; Amy S Gladfelter
Journal:  Curr Biol       Date:  2013-10-03       Impact factor: 10.834

3.  Organization of organelles within hyphae of Ashbya gossypii revealed by electron tomography.

Authors:  Romain Gibeaux; Dominic Hoepfner; Ivan Schlatter; Claude Antony; Peter Philippsen
Journal:  Eukaryot Cell       Date:  2013-06-14

Review 4.  Nuclear movement in fungi.

Authors:  Xin Xiang
Journal:  Semin Cell Dev Biol       Date:  2017-12-11       Impact factor: 7.727

5.  Mechanism of nuclear movements in a multinucleated cell.

Authors:  Romain Gibeaux; Antonio Z Politi; Peter Philippsen; François Nédélec
Journal:  Mol Biol Cell       Date:  2017-01-11       Impact factor: 4.138

6.  The actin capping protein in Aspergillus nidulans enhances dynein function without significantly affecting Arp1 filament assembly.

Authors:  Jun Zhang; Rongde Qiu; Xin Xiang
Journal:  Sci Rep       Date:  2018-07-30       Impact factor: 4.379

7.  Reverse-engineering forces responsible for dynamic clustering and spreading of multiple nuclei in developing muscle cells.

Authors:  Angelika Manhart; Mafalda Azevedo; Mary Baylies; Alex Mogilner
Journal:  Mol Biol Cell       Date:  2020-03-04       Impact factor: 4.138

8.  FHIP and FTS proteins are critical for dynein-mediated transport of early endosomes in Aspergillus.

Authors:  Xuanli Yao; Xiangfeng Wang; Xin Xiang
Journal:  Mol Biol Cell       Date:  2014-05-28       Impact factor: 4.138

9.  Clustered nuclei maintain autonomy and nucleocytoplasmic ratio control in a syncytium.

Authors:  Samantha E R Dundon; Shyr-Shea Chang; Abhishek Kumar; Patricia Occhipinti; Hari Shroff; Marcus Roper; Amy S Gladfelter
Journal:  Mol Biol Cell       Date:  2016-05-18       Impact factor: 4.138

Review 10.  A nuclear contortionist: the mitotic migration of Magnaporthe oryzae nuclei during plant infection.

Authors:  Mariel A Pfeifer; Chang Hyun Khang
Journal:  Mycology       Date:  2018-06-12
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