Hierarchical stem cell topography splits growth and homeostatic functions in the fish gill
- Centre for Organismal Studies, Heidelberg University, Germany
- Heidelberg University, Germany
- Centro Andaluz de Biología del Desarrollo, Universidad Pablo de Olavide, Spain
- Murdoch Children's Research Institute, Royal Children's Hospital, Australia
- National Institute for Basic Biology, National Institutes of Natural Sciences, Japan
Abstract
While lower vertebrates contain adult stem cells (aSCs) that maintain homeostasis and drive un-exhaustive organismal growth, mammalian aSCs display mainly the homeostatic function. Here we use lineage analysis in the fish gill to address aSCs and report separate stem cell populations for homeostasis and growth. These aSCs are fate-restricted during the entire post-embryonic life and even during re-generation paradigms. We use chimeric animals to demonstrate that p53 mediates growth coordination among fate-restricted aSCs, suggesting a hierarchical organisation among lineages in composite organs like the fish gill. Homeostatic and growth aSCs are clonal but differ in their topology; modifications in tissue architecture can convert the homeostatic zone into a growth zone, indicating a leading role for the physical niche defining stem cell output. We hypothesise that physical niches are main players to restrict aSCs to a homeostatic function in animals with fixed adult size.
Data availability
All data analysed for this study is included in the manuscript and supporting files. Raw sequencing data have been deposited in GEO under accession code GSE130939
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Transcriptome analysts of a growth domain and a differentiated domain of the medaka gillNCBI Gene Expression Omnibus, GSE130939.
Article and author information
Author details
Elizabeth Mayela Ambrosio
Diana-Patricia Danciu
Juan R Martínez-Morales
Anna Marciniak-Czochra
Funding
Deutsche Forschungsgemeinschaft (SFB873/A11)
- Lazaro Centanin
Deutsche Forschungsgemeinschaft (SFB873/B08)
- Anna Marciniak-Czochra
University of Melbourne (Melbourne Research Fellowship / Graduate Student Fellowship)
- Julian Stopler
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Ethics
Animal experimentation: Experimental procedures with fish were performed in accordance with the German animal welfare law and approved by the local government (Tierschutzgesetz {section sign}11, Abs. 1, Nr. 1, husbandry permit number AZ 35-9185.64/BH; line generation permit number AZ 35-9185.81/G-145-15), and with the approval from the Institutional Animal Care and Use Committees of the National Institute for Basic Biology, Japan.
Copyright
© 2019, Stolper et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Hierarchical stem cell topography splits growth and homeostatic functions in the fish gill
eLife 8:e43747.
https://doi.org/10.7554/eLife.43747
Further reading
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The formation of large endolysosomal structures in unfertilized eggs ensures that lysosomes remain dormant before fertilization, and then shift into clean-up mode after the egg-to-embryo transition.
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Ribonucleoprotein (RNP) granules are membraneless electron-dense structures rich in RNAs and proteins, and involved in various cellular processes. Two RNP granules in male germ cells, intermitochondrial cement and the chromatoid body (CB), are associated with PIWI-interacting RNAs (piRNAs) and are required for transposon silencing and spermatogenesis. Other RNP granules in male germ cells, the reticulated body and CB remnants, are also essential for spermiogenesis. In this study, we disrupted FBXO24, a testis-enriched F-box protein, in mice and found numerous membraneless electron-dense granules accumulated in sperm flagella. Fbxo24 knockout (KO) mice exhibited malformed flagellar structures, impaired sperm motility, and male infertility, likely due to the accumulation of abnormal granules. The amount and localization of known RNP granule-related proteins were not disrupted in Fbxo24 KO mice, suggesting that the accumulated granules were distinct from known RNP granules. Further studies revealed that RNAs and two importins, IPO5 and KPNB1, abnormally accumulated in Fbxo24 KO spermatozoa and that FBXO24 could ubiquitinate IPO5. In addition, IPO5 and KPNB1 were recruited to stress granules, RNP complexes, when cells were treated with oxidative stress or a proteasome inhibitor. These results suggest that FBXO24 is involved in the degradation of IPO5, disruption of which may lead to the accumulation of abnormal RNP granules in sperm flagella.
