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Wolbachia control stem cell behavior and stimulate germline proliferation in Filarial Nematodes

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Foray, V
Fattouh, N
Landmann, F

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Cell Press
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Although symbiotic interactions are ubiquitous in the living world, examples of developmental symbioses are still scarce. We show here the crucial role of Wolbachia in the oogenesis of filarial nematodes, a class of parasites of biomedical and veterinary relevance. We applied newly developed techniques to demonstrate the earliest requirements of Wolbachia in the parasite germline preceding the production of faulty embryos in Wolbachia-depleted nematodes. We show that Wolbachia stimulate germline proliferation in a cell-autonomous manner, and not through nucleotide supplementation as previously hypothesized. We also found Wolbachia to maintain the quiescence of a pool of germline stem cells to ensure a constant delivery of about 1,400 eggs per day for many years. The loss of quiescence upon Wolbachia depletion as well as the disorganization of the distal germline suggest that Wolbachia are required to execute the proper germline stem cell developmental program in order to produce viable eggs and embryos.

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MetaToul (Metabolomics & Fluxomics Facilities, Toulouse, France, www.metatoul.fr, MetaboHUB-ANR-11-INBS-0010) and its staff members are gratefully acknowledged for carrying out metabolome analyses. We are grateful to NIH/NIAID Filariasis Research Reagent Resource Center (www.filariasiscenter.org) for providing B. malayi and A. viteae specimens. We acknowledge the imaging facility MRI, member of the national infrastructure France-BioImaging supported by the French National Research Agency (ANR-10-INBS-04, Investments for the Future). A part of the biological material was obtained thanks to the insectarium platform located on the Institut de Recherche pour le Developpement (IRD) campus and belonging to the network Vectopole Sud (Montpellier, France). We thank Pascale Cossart for critical advice and Jeremy Foster for proofreading and corrections. We are also grateful to Coralie Martin for advice on filarial nematode rearing techniques. This work was supported by the Fondation pour la Recherche Medicale (ARF20150934088) and the ATIP-Avenir program.

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Foray V, Pérez-Jiménez MM, Fattouh N, Landmann F. Wolbachia Control Stem Cell Behavior and Stimulate Germline Proliferation in Filarial Nematodes. Dev Cell. 2018 Apr 23;45(2):198-211.e3. doi: 10.1016/j.devcel.2018.03.017. PMID: 29689195.

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