Abstract
The potency of post-embryonic stem cells can only be addressed in the living organism, by labeling single cells after embryonic development and following their descendants. Recently, transplantation experiments involving permanently labeled cells revealed multipotent neural stem cells (NSCs) of embryonic origin in the medaka retina. To analyze whether NSC potency is affected by developmental progression, as reported for the mammalian brain, we developed an inducible toolkit for clonal labeling and non-invasive fate tracking. We used this toolkit to address post-embryonic stem cells in different tissues and to functionally differentiate transient progenitor cells from permanent, bona fide stem cells in the retina. Using temporally controlled clonal induction, we showed that post-embryonic retinal NSCs are exclusively multipotent and give rise to the complete spectrum of cell types in the neural retina. Intriguingly, and in contrast to any other vertebrate stem cell system described so far, long-term analysis of clones indicates a preferential mode of asymmetric cell division. Moreover, following the behavior of clones before and after external stimuli, such as injuries, shows that NSCs in the retina maintained the preference for asymmetric cell division during regenerative responses. We present a comprehensive analysis of individual post-embryonic NSCs in their physiological environment and establish the teleost retina as an ideal model for studying adult stem cell biology at single cell resolution.
Highlights
Embryonic progenitor and stem cells generate new differentiated cells during the initial phases of development
We generated and used the Gaudí toolkit to reveal the occurrence of retinal stem cells (RSCs) in an already functional eye, and to demonstrate that individual RSCs generate the entire repertoire of cell types in the neural retina
Our results indicate two stereotypic behaviors among RSCs in medaka: (1) there is no variation in potency among individual stem cells in the fish neural retina; and (2) the preference for asymmetric divisions is not altered by age or during tissue repair
Summary
Embryonic progenitor and stem cells generate new differentiated cells during the initial phases of development. The switch from embryonic to postembryonic stem cells is in general accompanied by loss of potency: while pluripotent cells can generate all cell types during early. Cre-mediated recombination was recently validated in fish (Gupta and Poss, 2012; Hans et al, 2009; Knopf et al, 2011; Mosimann et al, 2011; Nakamura et al, 2010; Singh et al, 2012), allowing long-term lineage of stem cells of embryonic origin (Pan et al, 2013)
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