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Tissue specific requirement of Drosophila Rcd4 for centriole duplication and ciliogenesis

Panda, Pallavi and Kovacs, Levente and Dzhindzhev, Nikola and Fatalska, Agnieszka and Persico, Veronica and Geymonat, Marco and Riparbelli, Maria Giovanna and Callaini, Giuliano and Glover, David M. (2020) Tissue specific requirement of Drosophila Rcd4 for centriole duplication and ciliogenesis. Journal of Cell Biology, 219 (8). Art. No. e201912154. ISSN 0021-9525. PMCID PMC7401805. https://resolver.caltech.edu/CaltechAUTHORS:20200624-070312017

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Abstract

Rcd4 is a poorly characterized Drosophila centriole component whose mammalian counterpart, PPP1R35, is suggested to function in centriole elongation and conversion to centrosomes. Here, we show that rcd4 mutants exhibit fewer centrioles, aberrant mitoses, and reduced basal bodies in sensory organs. Rcd4 interacts with the C-terminal part of Ana3, which loads onto the procentriole during interphase, ahead of Rcd4 and before mitosis. Accordingly, depletion of Ana3 prevents Rcd4 recruitment but not vice versa. We find that neither Ana3 nor Rcd4 participates directly in the mitotic conversion of centrioles to centrosomes, but both are required to load Ana1, which is essential for such conversion. Whereas ana3 mutants are male sterile, reflecting a requirement for Ana3 for centriole development in the male germ line, rcd4 mutants are fertile and have male germ line centrioles of normal length. Thus, Rcd4 is essential in somatic cells but is not absolutely required in spermatogenesis, indicating tissue-specific roles in centriole and basal body formation.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1083/jcb.201912154DOIArticle
http://www.ncbi.nlm.nih.gov/pmc/articles/pmc7401805/PubMed CentralArticle
ORCID:
AuthorORCID
Panda, Pallavi0000-0001-7572-6728
Kovacs, Levente0000-0002-3226-3740
Dzhindzhev, Nikola0000-0001-9866-3600
Geymonat, Marco0000-0002-8792-0517
Glover, David M.0000-0003-0956-0103
Additional Information:© 2020 Panda et al. This article is available under a Creative Commons License (Attribution 4.0 International, as described at https://creativecommons.org/licenses/by/4.0/). Submitted: 27 December 2019; Revised: 1 April 2020; Accepted: 13 May 2020. We wish to thank K. Oras and A. Madich (The University of Cambridge Department of Genetics Fly Facility) for injections of Rcd4 and Ana3 transgenes, N. Lawrence (Gurdon Institute Imaging Facility, Cambridge, UK) for assistance with SIM, and all members of the Glover group for their enthusiastic comments and suggestions. The work was supported by an Investigator Award from the Wellcome Trust (award no. RG84496) to D.M. Glover at the University of Cambridge. Research in the California Institute of Technology laboratory reported in this publication was supported by the National Institute of Neurological Disorders and Stroke of the National Institutes of Health under award no. R01NS113930. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. The authors declare no competing financial interests. Author contributions: Conceptualization: P. Panda and D.M. Glover. Investigation: P. Panda carried out most of the experiments, L. Kovacs – some genetic analyses, A. Fatalska and M. Geymonat – protein complex formation between Rcd4 and Ana3, N. Dzhindzhev – initially identified Ana3 as an interactor of Rcd4, pilot localization studies of Rcd4 in cultured cells, V. Persico – electron microscopy. Visualization: P. Panda. Writing – original draft: P. Panda and D.M. Glover. Writing- review and editing: P. Panda and D.M. Glover. Supervision: M.G. Riparbelli, G. Callaini, and D.M. Glover. Funding acquisition: D.M. Glover.
Funders:
Funding AgencyGrant Number
Wellcome TrustRG84496
NIHR01NS113930
Issue or Number:8
PubMed Central ID:PMC7401805
Record Number:CaltechAUTHORS:20200624-070312017
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20200624-070312017
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:103976
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:24 Jun 2020 14:31
Last Modified:05 Oct 2020 17:07

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