Cargando…
The Kinetochore-Microtubule Coupling Machinery Is Repurposed in Sensory Nervous System Morphogenesis
Dynamic coupling of microtubule ends to kinetochores, built on the centromeres of chromosomes, directs chromosome segregation during cell division. Here, we report that the evolutionarily ancient kinetochore-microtubule coupling machine, the KMN (Knl1/Mis12/Ndc80-complex) network, plays a critical r...
Autores principales: | , , , , , , , , , , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Cell Press
2019
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6436928/ https://www.ncbi.nlm.nih.gov/pubmed/30827898 http://dx.doi.org/10.1016/j.devcel.2019.02.002 |
_version_ | 1783406870416850944 |
---|---|
author | Cheerambathur, Dhanya K. Prevo, Bram Chow, Tiffany-Lynn Hattersley, Neil Wang, Shaohe Zhao, Zhiling Kim, Taekyung Gerson-Gurwitz, Adina Oegema, Karen Green, Rebecca Desai, Arshad |
author_facet | Cheerambathur, Dhanya K. Prevo, Bram Chow, Tiffany-Lynn Hattersley, Neil Wang, Shaohe Zhao, Zhiling Kim, Taekyung Gerson-Gurwitz, Adina Oegema, Karen Green, Rebecca Desai, Arshad |
author_sort | Cheerambathur, Dhanya K. |
collection | PubMed |
description | Dynamic coupling of microtubule ends to kinetochores, built on the centromeres of chromosomes, directs chromosome segregation during cell division. Here, we report that the evolutionarily ancient kinetochore-microtubule coupling machine, the KMN (Knl1/Mis12/Ndc80-complex) network, plays a critical role in neuronal morphogenesis. We show that the KMN network concentrates in microtubule-rich dendrites of developing sensory neurons that collectively extend in a multicellular morphogenetic event that occurs during C. elegans embryogenesis. Post-mitotic degradation of KMN components in sensory neurons disrupts dendritic extension, leading to patterning and functional defects in the sensory nervous system. Structure-guided mutations revealed that the molecular interface that couples kinetochores to spindle microtubules also functions in neuronal development. These results identify a cell-division-independent function for the chromosome-segregation machinery and define a microtubule-coupling-dependent event in sensory nervous system morphogenesis. |
format | Online Article Text |
id | pubmed-6436928 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2019 |
publisher | Cell Press |
record_format | MEDLINE/PubMed |
spelling | pubmed-64369282019-04-10 The Kinetochore-Microtubule Coupling Machinery Is Repurposed in Sensory Nervous System Morphogenesis Cheerambathur, Dhanya K. Prevo, Bram Chow, Tiffany-Lynn Hattersley, Neil Wang, Shaohe Zhao, Zhiling Kim, Taekyung Gerson-Gurwitz, Adina Oegema, Karen Green, Rebecca Desai, Arshad Dev Cell Article Dynamic coupling of microtubule ends to kinetochores, built on the centromeres of chromosomes, directs chromosome segregation during cell division. Here, we report that the evolutionarily ancient kinetochore-microtubule coupling machine, the KMN (Knl1/Mis12/Ndc80-complex) network, plays a critical role in neuronal morphogenesis. We show that the KMN network concentrates in microtubule-rich dendrites of developing sensory neurons that collectively extend in a multicellular morphogenetic event that occurs during C. elegans embryogenesis. Post-mitotic degradation of KMN components in sensory neurons disrupts dendritic extension, leading to patterning and functional defects in the sensory nervous system. Structure-guided mutations revealed that the molecular interface that couples kinetochores to spindle microtubules also functions in neuronal development. These results identify a cell-division-independent function for the chromosome-segregation machinery and define a microtubule-coupling-dependent event in sensory nervous system morphogenesis. Cell Press 2019-03-25 /pmc/articles/PMC6436928/ /pubmed/30827898 http://dx.doi.org/10.1016/j.devcel.2019.02.002 Text en © 2019 The Authors http://creativecommons.org/licenses/by/4.0/ This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/). |
spellingShingle | Article Cheerambathur, Dhanya K. Prevo, Bram Chow, Tiffany-Lynn Hattersley, Neil Wang, Shaohe Zhao, Zhiling Kim, Taekyung Gerson-Gurwitz, Adina Oegema, Karen Green, Rebecca Desai, Arshad The Kinetochore-Microtubule Coupling Machinery Is Repurposed in Sensory Nervous System Morphogenesis |
title | The Kinetochore-Microtubule Coupling Machinery Is Repurposed in Sensory Nervous System Morphogenesis |
title_full | The Kinetochore-Microtubule Coupling Machinery Is Repurposed in Sensory Nervous System Morphogenesis |
title_fullStr | The Kinetochore-Microtubule Coupling Machinery Is Repurposed in Sensory Nervous System Morphogenesis |
title_full_unstemmed | The Kinetochore-Microtubule Coupling Machinery Is Repurposed in Sensory Nervous System Morphogenesis |
title_short | The Kinetochore-Microtubule Coupling Machinery Is Repurposed in Sensory Nervous System Morphogenesis |
title_sort | kinetochore-microtubule coupling machinery is repurposed in sensory nervous system morphogenesis |
topic | Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6436928/ https://www.ncbi.nlm.nih.gov/pubmed/30827898 http://dx.doi.org/10.1016/j.devcel.2019.02.002 |
work_keys_str_mv | AT cheerambathurdhanyak thekinetochoremicrotubulecouplingmachineryisrepurposedinsensorynervoussystemmorphogenesis AT prevobram thekinetochoremicrotubulecouplingmachineryisrepurposedinsensorynervoussystemmorphogenesis AT chowtiffanylynn thekinetochoremicrotubulecouplingmachineryisrepurposedinsensorynervoussystemmorphogenesis AT hattersleyneil thekinetochoremicrotubulecouplingmachineryisrepurposedinsensorynervoussystemmorphogenesis AT wangshaohe thekinetochoremicrotubulecouplingmachineryisrepurposedinsensorynervoussystemmorphogenesis AT zhaozhiling thekinetochoremicrotubulecouplingmachineryisrepurposedinsensorynervoussystemmorphogenesis AT kimtaekyung thekinetochoremicrotubulecouplingmachineryisrepurposedinsensorynervoussystemmorphogenesis AT gersongurwitzadina thekinetochoremicrotubulecouplingmachineryisrepurposedinsensorynervoussystemmorphogenesis AT oegemakaren thekinetochoremicrotubulecouplingmachineryisrepurposedinsensorynervoussystemmorphogenesis AT greenrebecca thekinetochoremicrotubulecouplingmachineryisrepurposedinsensorynervoussystemmorphogenesis AT desaiarshad thekinetochoremicrotubulecouplingmachineryisrepurposedinsensorynervoussystemmorphogenesis AT cheerambathurdhanyak kinetochoremicrotubulecouplingmachineryisrepurposedinsensorynervoussystemmorphogenesis AT prevobram kinetochoremicrotubulecouplingmachineryisrepurposedinsensorynervoussystemmorphogenesis AT chowtiffanylynn kinetochoremicrotubulecouplingmachineryisrepurposedinsensorynervoussystemmorphogenesis AT hattersleyneil kinetochoremicrotubulecouplingmachineryisrepurposedinsensorynervoussystemmorphogenesis AT wangshaohe kinetochoremicrotubulecouplingmachineryisrepurposedinsensorynervoussystemmorphogenesis AT zhaozhiling kinetochoremicrotubulecouplingmachineryisrepurposedinsensorynervoussystemmorphogenesis AT kimtaekyung kinetochoremicrotubulecouplingmachineryisrepurposedinsensorynervoussystemmorphogenesis AT gersongurwitzadina kinetochoremicrotubulecouplingmachineryisrepurposedinsensorynervoussystemmorphogenesis AT oegemakaren kinetochoremicrotubulecouplingmachineryisrepurposedinsensorynervoussystemmorphogenesis AT greenrebecca kinetochoremicrotubulecouplingmachineryisrepurposedinsensorynervoussystemmorphogenesis AT desaiarshad kinetochoremicrotubulecouplingmachineryisrepurposedinsensorynervoussystemmorphogenesis |