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Heterotrimeric kinesin-II is necessary and sufficient to promote different stepwise assembly of morphologically distinct bipartite cilia in Drosophila antenna

Structurally diverse sensory cilia have evolved from primary cilia, a microtubule-based cellular extension engaged in chemical and mechanical sensing and signal integration. The diversity is often associated with functional specialization. The olfactory receptor neurons in Drosophila, for example, e...

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Detalles Bibliográficos
Autores principales: Jana, Swadhin C., Girotra, Mukul, Ray, Krishanu
Formato: Texto
Lenguaje:English
Publicado: The American Society for Cell Biology 2011
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3057702/
https://www.ncbi.nlm.nih.gov/pubmed/21233284
http://dx.doi.org/10.1091/mbc.E10-08-0712
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author Jana, Swadhin C.
Girotra, Mukul
Ray, Krishanu
author_facet Jana, Swadhin C.
Girotra, Mukul
Ray, Krishanu
author_sort Jana, Swadhin C.
collection PubMed
description Structurally diverse sensory cilia have evolved from primary cilia, a microtubule-based cellular extension engaged in chemical and mechanical sensing and signal integration. The diversity is often associated with functional specialization. The olfactory receptor neurons in Drosophila, for example, express three distinct bipartite cilia displaying different sets of olfactory receptors on them. Molecular description underlying their assembly and diversification is still incomplete. Here, we show that the branched and the slender olfactory cilia develop in two distinct step-wise patterns through the pupal stages before the expression of olfactory receptor genes in olfactory neurons. The process initiates with a thin procilium growth from the dendrite apex, followed by volume increment in successive stages. Mutations in the kinesin-II subunit genes either eliminate or restrict the cilia growth as well as tubulin entry into the developing cilia. Together with previous results, our results here suggest that heterotrimeric kinesin-II is the primary motor engaged in all type-I sensory cilia assembly in Drosophila and that the cilia structure diversity is achieved through additional transports supported by the motor during development.
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spelling pubmed-30577022011-05-30 Heterotrimeric kinesin-II is necessary and sufficient to promote different stepwise assembly of morphologically distinct bipartite cilia in Drosophila antenna Jana, Swadhin C. Girotra, Mukul Ray, Krishanu Mol Biol Cell Articles Structurally diverse sensory cilia have evolved from primary cilia, a microtubule-based cellular extension engaged in chemical and mechanical sensing and signal integration. The diversity is often associated with functional specialization. The olfactory receptor neurons in Drosophila, for example, express three distinct bipartite cilia displaying different sets of olfactory receptors on them. Molecular description underlying their assembly and diversification is still incomplete. Here, we show that the branched and the slender olfactory cilia develop in two distinct step-wise patterns through the pupal stages before the expression of olfactory receptor genes in olfactory neurons. The process initiates with a thin procilium growth from the dendrite apex, followed by volume increment in successive stages. Mutations in the kinesin-II subunit genes either eliminate or restrict the cilia growth as well as tubulin entry into the developing cilia. Together with previous results, our results here suggest that heterotrimeric kinesin-II is the primary motor engaged in all type-I sensory cilia assembly in Drosophila and that the cilia structure diversity is achieved through additional transports supported by the motor during development. The American Society for Cell Biology 2011-03-15 /pmc/articles/PMC3057702/ /pubmed/21233284 http://dx.doi.org/10.1091/mbc.E10-08-0712 Text en © 2011 Jana et al. This article is distributed by The American Society for Cell Biology under license from the author(s). Two months after publication it is available to the public under an Attribution–Noncommercial–Share Alike 3.0 Unported Creative Commons License (http://creativecommons.org/licenses/by-nc-sa/3.0). “ASCB®,“ “The American Society for Cell Biology®,” and “Molecular Biology of the Cell®” are registered trademarks of The American Society of Cell Biology.
spellingShingle Articles
Jana, Swadhin C.
Girotra, Mukul
Ray, Krishanu
Heterotrimeric kinesin-II is necessary and sufficient to promote different stepwise assembly of morphologically distinct bipartite cilia in Drosophila antenna
title Heterotrimeric kinesin-II is necessary and sufficient to promote different stepwise assembly of morphologically distinct bipartite cilia in Drosophila antenna
title_full Heterotrimeric kinesin-II is necessary and sufficient to promote different stepwise assembly of morphologically distinct bipartite cilia in Drosophila antenna
title_fullStr Heterotrimeric kinesin-II is necessary and sufficient to promote different stepwise assembly of morphologically distinct bipartite cilia in Drosophila antenna
title_full_unstemmed Heterotrimeric kinesin-II is necessary and sufficient to promote different stepwise assembly of morphologically distinct bipartite cilia in Drosophila antenna
title_short Heterotrimeric kinesin-II is necessary and sufficient to promote different stepwise assembly of morphologically distinct bipartite cilia in Drosophila antenna
title_sort heterotrimeric kinesin-ii is necessary and sufficient to promote different stepwise assembly of morphologically distinct bipartite cilia in drosophila antenna
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3057702/
https://www.ncbi.nlm.nih.gov/pubmed/21233284
http://dx.doi.org/10.1091/mbc.E10-08-0712
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