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A transport and retention mechanism for the sustained distal localization of Spn-F–IKKε during Drosophila bristle elongation

Stable localization of the signaling complex is essential for the robust morphogenesis of polarized cells. Cell elongation involves molecular signaling centers that coordinately regulate intracellular transport and cytoskeletal structures. In Drosophila bristle elongation, the protein kinase IKKε is...

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Autores principales: Otani, Tetsuhisa, Oshima, Kenzi, Kimpara, Akiyo, Takeda, Michiko, Abdu, Uri, Hayashi, Shigeo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Company of Biologists 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4510591/
https://www.ncbi.nlm.nih.gov/pubmed/26092846
http://dx.doi.org/10.1242/dev.121863
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author Otani, Tetsuhisa
Oshima, Kenzi
Kimpara, Akiyo
Takeda, Michiko
Abdu, Uri
Hayashi, Shigeo
author_facet Otani, Tetsuhisa
Oshima, Kenzi
Kimpara, Akiyo
Takeda, Michiko
Abdu, Uri
Hayashi, Shigeo
author_sort Otani, Tetsuhisa
collection PubMed
description Stable localization of the signaling complex is essential for the robust morphogenesis of polarized cells. Cell elongation involves molecular signaling centers that coordinately regulate intracellular transport and cytoskeletal structures. In Drosophila bristle elongation, the protein kinase IKKε is activated at the distal tip of the growing bristle and regulates the shuttling movement of recycling endosomes and cytoskeletal organization. However, how the distal tip localization of IKKε is established and maintained during bristle elongation is unknown. Here, we demonstrate that IKKε distal tip localization is regulated by Spindle-F (Spn-F), which is stably retained at the distal tip and functions as an adaptor linking IKKε to cytoplasmic dynein. We found that Javelin-like (Jvl) is a key regulator of Spn-F retention. In jvl mutant bristles, IKKε and Spn-F initially localize to the distal tip but fail to be retained there. In S2 cells, particles that stain positively for Jvl or Spn-F move in a microtubule-dependent manner, whereas Jvl and Spn-F double-positive particles are immobile, indicating that Jvl and Spn-F are transported separately and, upon forming a complex, immobilize each other. These results suggest that polarized transport and selective retention regulate the distal tip localization of the Spn-F–IKKε complex during bristle cell elongation.
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spelling pubmed-45105912015-09-29 A transport and retention mechanism for the sustained distal localization of Spn-F–IKKε during Drosophila bristle elongation Otani, Tetsuhisa Oshima, Kenzi Kimpara, Akiyo Takeda, Michiko Abdu, Uri Hayashi, Shigeo Development Research Article Stable localization of the signaling complex is essential for the robust morphogenesis of polarized cells. Cell elongation involves molecular signaling centers that coordinately regulate intracellular transport and cytoskeletal structures. In Drosophila bristle elongation, the protein kinase IKKε is activated at the distal tip of the growing bristle and regulates the shuttling movement of recycling endosomes and cytoskeletal organization. However, how the distal tip localization of IKKε is established and maintained during bristle elongation is unknown. Here, we demonstrate that IKKε distal tip localization is regulated by Spindle-F (Spn-F), which is stably retained at the distal tip and functions as an adaptor linking IKKε to cytoplasmic dynein. We found that Javelin-like (Jvl) is a key regulator of Spn-F retention. In jvl mutant bristles, IKKε and Spn-F initially localize to the distal tip but fail to be retained there. In S2 cells, particles that stain positively for Jvl or Spn-F move in a microtubule-dependent manner, whereas Jvl and Spn-F double-positive particles are immobile, indicating that Jvl and Spn-F are transported separately and, upon forming a complex, immobilize each other. These results suggest that polarized transport and selective retention regulate the distal tip localization of the Spn-F–IKKε complex during bristle cell elongation. The Company of Biologists 2015-07-01 /pmc/articles/PMC4510591/ /pubmed/26092846 http://dx.doi.org/10.1242/dev.121863 Text en © 2015. Published by The Company of Biologists Ltd http://creativecommons.org/licenses/by/3.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Article
Otani, Tetsuhisa
Oshima, Kenzi
Kimpara, Akiyo
Takeda, Michiko
Abdu, Uri
Hayashi, Shigeo
A transport and retention mechanism for the sustained distal localization of Spn-F–IKKε during Drosophila bristle elongation
title A transport and retention mechanism for the sustained distal localization of Spn-F–IKKε during Drosophila bristle elongation
title_full A transport and retention mechanism for the sustained distal localization of Spn-F–IKKε during Drosophila bristle elongation
title_fullStr A transport and retention mechanism for the sustained distal localization of Spn-F–IKKε during Drosophila bristle elongation
title_full_unstemmed A transport and retention mechanism for the sustained distal localization of Spn-F–IKKε during Drosophila bristle elongation
title_short A transport and retention mechanism for the sustained distal localization of Spn-F–IKKε during Drosophila bristle elongation
title_sort transport and retention mechanism for the sustained distal localization of spn-f–ikkε during drosophila bristle elongation
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4510591/
https://www.ncbi.nlm.nih.gov/pubmed/26092846
http://dx.doi.org/10.1242/dev.121863
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