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The Bric-à-Brac BTB/POZ transcription factors are necessary in niche cells for germline stem cells establishment and homeostasis through control of BMP/DPP signaling in the Drosophila melanogaster ovary

Miscopein Saler, Laurine and Hauser, Virginie and Bartoletti, Mathieu and Mallart, Charlotte and Malartre, Marianne and Lebrun, Laura and Pret, Anne-Marie and Théodore, Laurent and Chalvet, Fabienne and Netter, Sophie (2020) The Bric-à-Brac BTB/POZ transcription factors are necessary in niche cells for germline stem cells establishment and homeostasis through control of BMP/DPP signaling in the Drosophila melanogaster ovary. PLOS Genetics, 16 (11). Art. No. e1009128. ISSN 1553-7404. PMCID PMC7643948. https://resolver.caltech.edu/CaltechAUTHORS:20201215-141038893

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Abstract

Many studies have focused on the mechanisms of stem cell maintenance via their interaction with a particular niche or microenvironment in adult tissues, but how formation of a functional niche is initiated, including how stem cells within a niche are established, is less well understood. Adult Drosophila melanogaster ovary Germline Stem Cell (GSC) niches are comprised of somatic cells forming a stack called a Terminal Filament (TF) and associated Cap and Escort Cells (CCs and ECs, respectively), which are in direct contact with GSCs. In the adult ovary, the transcription factor Engrailed is specifically expressed in niche cells where it directly controls expression of the decapentaplegic (dpp) gene encoding a member of the Bone Morphogenetic Protein (BMP) family of secreted signaling molecules, which are key factors for GSC maintenance. In larval ovaries, in response to BMP signaling from newly formed niches, adjacent primordial germ cells become GSCs. The bric-à-brac paralogs (bab1 and bab2) encode BTB/POZ domain-containing transcription factors that are expressed in developing niches of larval ovaries. We show here that their functions are necessary specifically within precursor cells for TF formation during these stages. We also identify a new function for Bab1 and Bab2 within developing niches for GSC establishment in the larval ovary and for robust GSC maintenance in the adult. Moreover, we show that the presence of Bab proteins in niche cells is necessary for activation of transgenes reporting dpp expression as of larval stages in otherwise correctly specified Cap Cells, independently of Engrailed and its paralog Invected (En/Inv). Moreover, strong reduction of engrailed/invected expression during larval stages does not impair TF formation and only partially reduces GSC numbers. In the adult ovary, Bab proteins are also required for dpp reporter expression in CCs. Finally, when bab2 was overexpressed at this stage in somatic cells outside of the niche, there were no detectable levels of ectopic En/Inv, but ectopic expression of a dpp transgene was found in these cells and BMP signaling activation was induced in adjacent germ cells, which produced GSC-like tumors. Together, these results indicate that Bab transcription factors are positive regulators of BMP signaling in niche cells for establishment and homeostasis of GSCs in the Drosophila ovary.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1371/journal.pgen.1009128DOIArticle
http://www.ncbi.nlm.nih.gov/pmc/articles/pmc7643948/PubMed CentralArticle
ORCID:
AuthorORCID
Bartoletti, Mathieu0000-0003-3648-5524
Mallart, Charlotte0000-0003-4183-221X
Pret, Anne-Marie0000-0001-6042-6140
Chalvet, Fabienne0000-0002-0832-6430
Netter, Sophie0000-0003-2477-6164
Additional Information:© 2020 Saler et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Received: July 17, 2019; Accepted: September 22, 2020; Published: November 5, 2020. We thank S. Gaumer for advice on statistical analysis. Stocks obtained from the Bloomington Drosophila Stock Center (NIH P40OD018537) were used in this study, as well as from the Vienna Drosophila RNAi Center (VDRC, Austria). We thank A. Boivin, A. Bardin, M. Boube, J-L. Couderc, D. Godt, J-R. Huynh, A. Kopp, J. Montagne, T. Williams, R. Xi and T. Xie for providing fly stocks, and for providing antibodies, J-L. Couderc, D. Godt and T. Williams, as well as the Developmental Studies Hybridoma Bank developed under the auspices of the NICHD and maintained by The University of Iowa, Department of Biological Sciences, Iowa City, IA 52242. The work on this project by all the authors was funded by the Centre National de la Recherche Scientifique Français (CNRS http://www.cnrs.fr/en) grant number 9ADO29 06 0B1INSB SEAMP and the Ligue Contre le Cancer (M31420). L.M.S, M.B. and C.M. were recipients of doctoral fellowships from the MESR (Ministère de l’Enseignement supérieur et de la Recherche, France) and M.B. received an additional thesis grant from the Fondation ARC pour la Recherche sur le Cancer. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Data Availability: All relevant data are within the manuscript and its Supporting Information files. The authors have declared that no competing interests exist.
Funders:
Funding AgencyGrant Number
Centre National de la Recherche Scientifique9ADO29 06 0B1INSB SEAMP
Ligue Contre le CancerM31420
Ministère de l’Enseignement supérieur et de la RechercheUNSPECIFIED
Fondation ARC pour la Recherche sur le CancerUNSPECIFIED
NIHP40OD018537
Issue or Number:11
PubMed Central ID:PMC7643948
Record Number:CaltechAUTHORS:20201215-141038893
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20201215-141038893
Official Citation:Miscopein Saler L, Hauser V, Bartoletti M, Mallart C, Malartre M, Lebrun L, et al. (2020) The Bric-à-Brac BTB/POZ transcription factors are necessary in niche cells for germline stem cells establishment and homeostasis through control of BMP/DPP signaling in the Drosophila melanogaster ovary. PLoS Genet 16(11): e1009128. https://doi.org/10.1371/journal.pgen.1009128
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:107105
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:15 Dec 2020 22:27
Last Modified:15 Dec 2020 22:27

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