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Differential RA responsiveness directs formation of functionally distinct spermatogonial populations at the initiation of spermatogenesis in the mouse.

ABSTRACT: In the mammalian testis, sustained spermatogenesis relies on spermatogonial stem cells (SSCs); their progeny either remain as stem cells (self-renewal) or proliferate and differentiate to enter meiosis in response to retinoic acid (RA). Here, we sought to uncover elusive mechanisms regulating a key switch fundamental to spermatogonial fate: the capacity of spermatogonia to respond to RA. Using the developing mouse testis as a model, we found that spermatogonia and precursor prospermatogonia exhibit a heterogeneous capacity to respond to RA with at least two underlying causes. First, progenitor spermatogonia are prevented from responding to RA by catabolic activity of cytochrome P450 family 26 enzymes. Second, a smaller subset of undifferentiated spermatogonia enriched for SSCs exhibit catabolism-independent RA insensitivity. Moreover, for the first time, we observed that precursor prospermatogonia are heterogeneous and comprise subpopulations that exhibit the same differential RA responsiveness found in neonatal spermatogonia. We propose a novel model by which mammalian prospermatogonial and spermatogonial fates are regulated by their intrinsic capacity to respond (or not) to the differentiation signal provided by RA before, and concurrent with, the initiation of spermatogenesis.

SUBMITTER: Velte EK

PROVIDER: S-EPMC6602341 | biostudies-literature | 2019 May

REPOSITORIES: biostudies-literature

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Differential RA responsiveness directs formation of functionally distinct spermatogonial populations at the initiation of spermatogenesis in the mouse.

Velte Ellen K EK Niedenberger Bryan A BA Serra Nicholas D ND Singh Anukriti A Roa-DeLaCruz Lorena L Hermann Brian P BP Geyer Christopher B CB

Development (Cambridge, England) 20190513 12

In the mammalian testis, sustained spermatogenesis relies on spermatogonial stem cells (SSCs); their progeny either remain as stem cells (self-renewal) or proliferate and differentiate to enter meiosis in response to retinoic acid (RA). Here, we sought to uncover elusive mechanisms regulating a key switch fundamental to spermatogonial fate: the capacity of spermatogonia to respond to RA. Using the developing mouse testis as a model, we found that spermatogonia and precursor prospermatogonia exhi ...[more]

PMID: 31023878

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Project description:The superficial layers of the medial entorhinal cortex (MEC) contain spatially selective neurons that are crucial for spatial navigation and memory. These highly specialized neurons include grid cells, border cells, head-direction cells, and irregular spatially selective cells. In addition, MEC neurons display a large variability in their spike patterns at a millisecond time scale. In this study, we analyzed spike trains of neurons in the MEC superficial layers of mice and found that these neurons can be classified into two groups based on their propensity to fire spike doublets at 125-250 Hz. The two groups, labeled "bursty" and "non-bursty" neurons, differed in their spike waveforms and interspike interval adaptation but displayed a similar mean firing rate. Grid cell spatial periodicity was more commonly observed in bursty than in non-bursty neurons. In contrast, most neurons with head-direction selectivity or those that fired at the border of the environment were non-bursty neurons. During theta oscillations, both bursty and non-bursty neurons fired preferentially near the end of the descending phase of the cycle, but the spikes of bursty neurons occurred at an earlier phase than those of non-bursty neurons. Finally, analysis of spike-time crosscorrelations between simultaneously recorded neurons suggested that the two cell classes are differentially coupled to fast-spiking interneurons: bursty neurons were twice as likely to have excitatory interactions with putative interneurons as non-bursty neurons. These results demonstrate that bursty and non-bursty neurons are differentially integrated in the MEC network and preferentially encode distinct spatial signals.Significance statementWe report that neurons in the superficial layers of the medial entorhinal cortex can be classified based on their tendency to fire bursts of action potentials at 125-250 Hz. The relevance of this classification is demonstrated by the types of spatial information preferentially encoded by bursty and non-bursty neurons. Grid-like spatial periodicity is more commonly observed in bursty neurons, whereas most cells with head-direction selectivity or those that are firing at the border of the environment are non-bursty neurons. This work indicates that the spatial firing patterns of neurons in the medial entorhinal cortex can be predicted by electrophysiological features reflecting the synaptic inputs and/or integrating properties of the neurons.

Dataset Information

Differential RA responsiveness directs formation of functionally distinct spermatogonial populations at the initiation of spermatogenesis in the mouse.

Publications

Differential RA responsiveness directs formation of functionally distinct spermatogonial populations at the initiation of spermatogenesis in the mouse.

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