The first round of mouse spermatogenesis is a distinctive program that lacks the self-renewing spermatogonia stage

Yoshida, Shosei; Sukeno, Mamiko; Nakagawa, Takako; Ohbo, Kazuyuki; Nagamatsu, Go; Suda, Toshio; Nabeshima, Yo Ichi

doi:10.1242/dev.02316

Cited by 337 publications

(321 citation statements)

References 37 publications

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“…This finding corroborates previous studies indicating that prespermatogenic germ cells are a heterogeneous population differing not only in their localization in seminiferous epithelium and morphology but also in their expression of specific molecular markers such as transcription factor OCT-4, tyrosine kinase receptor c-KIT and Melanoma antigen-A4 (MAGE-A4) (Fukuda et al, 1975;Gaskell et al, 2004;Yoshida et al, 2006;Ohmura et al, 2008).…”

Section: Discussionsupporting

confidence: 92%

Neonatal Gonocyte Differentiation in Mongolian GerbilMeriones unguiculatusInvolves Asynchronous Maturation of Seminiferous Cords and Rapid Formation of Transitional Cell Stage

Pinto

Botta

Taboga

et al. 2010

The Anatomical Record

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This study describes the neonatal differentiation of the Mongolian gerbil gonocytes, focusing on the relationship between its relocation to the basement membrane, apoptosis and postrelocation changes and also the distribution of androgen receptors (AR). Testes of gerbils from 1 to 35 days of age (d) were examined by high resolution light microscopy and immunocytochemistry for proteins PCNA, VASA, and AR as well as by the TUNEL method. Gonocytes were quantified according to degree of relocation into nonrelocated, relocating and relocated. Most of them were found in the center of seminiferous cords at 1 d but a small number of relocating and relocated gonocytes were already visible in the first postnatal day. After relocation, gonocytes change phenotypically to a transitional stage designated herein prospermatogonia. Both gonocyte relocation and transformation into spermatogonial lineage occur asynchronously in the seminiferous cords, mainly after 7 d. Gonocyte proliferation began before but peak after their relocation to basement membrane at the prospermatogonia stage. Higher levels of gonocyte apoptosis were found at 7 d and 21 d. From this time onward gonocytes were not found. Gonocytes and prospermatogonia showed high amounts of AR in their cytoplasm contrary to spermatogonial subtypes, indicating a possible AR inactivation in these cells. In conclusion, the process of gonocyte relocation in the gerbil extends until the second postnatal week, leads to their rapid differentiation into prospermatogonia and occurs simultaneously with the loss of androgen sensitivity. Differently from other laboratory rodents, the events regarding gonocyte maturation in the gerbil last longer and occur asynchronously in seminiferous cords. Anat Rec,

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Section: Discussionsupporting

confidence: 92%

Neonatal Gonocyte Differentiation in Mongolian GerbilMeriones unguiculatusInvolves Asynchronous Maturation of Seminiferous Cords and Rapid Formation of Transitional Cell Stage

Pinto

Botta

Taboga

et al. 2010

The Anatomical Record

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“…The signals underlying the fate of these two subpopulations were thought to be under the control of somatic cells but yet unidentified (25). According to our study, it is now conceivable that the signal committing gonocytes to differentiation as A1 spermatogonia relies on RA-activated RARA in SC.…”

Section: Resultsmentioning

confidence: 58%

“…The neonatal testis at PN6 contains two distinct populations of undifferentiated GC: gonocyte-derived undifferentiated spermatogonia and gonocytes that are able to differentiate directly into A1 spermatogonia to initiate the first prepubertal wave of spermatogenesis (2,25). The signals underlying the fate of these two subpopulations were thought to be under the control of somatic cells but yet unidentified (25).…”

Section: Resultsmentioning

confidence: 99%

Retinoic acid induces Sertoli cell paracrine signals for spermatogonia differentiation but cell autonomously drives spermatocyte meiosis

Raverdeau

Gély-Pernot

Féret

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

195

253

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Direct evidence for a role of endogenous retinoic acid (RA), the active metabolite of vitamin A in the initial differentiation and meiotic entry of spermatogonia, and thus in the initiation of spermatogenesis is still lacking. RA is synthesized by dedicated enzymes, the retinaldehyde dehydrogenases (RALDH), and binds to and activates nuclear RA receptors (RARA, RARB, and RARG) either within the RA-synthesizing cells or in the neighboring cells. In the present study, we have used a combination of somatic genetic ablations and pharmacological approaches in vivo to show that during the first, prepubertal, spermatogenic cycle ( i ) RALDH-dependent synthesis of RA by Sertoli cells (SC), the supporting cells of the germ cell (GC) lineage, is indispensable to initiate differentiation of A aligned into A1 spermatogonia; ( ii ) RARA in SC mediates the effects of RA, possibly through activating Mafb expression, a gene whose Drosophila homolog is mandatory to GC differentiation; ( iii ) RA synthesized by premeiotic spermatocytes cell autonomously induces meiotic initiation through controlling the RAR-dependent expression of Stra8 . Furthermore, we show that RA of SC origin is no longer necessary for the subsequent spermatogenic cycles but essential to spermiation. Altogether, our data establish that the effects of RA in vivo on spermatogonia differentiation are indirect, via SC, but direct on meiotic initiation in spermatocytes, supporting thereby the notion that, contrary to the situation in the female, RA is necessary to induce meiosis in the male.

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“…The discrepancy between the first wave and the adult spermatogonia phenotype was expected. Even in the normal testis the spermatogonia in the first wave of spermatogenesis differ from the adult spermatogonia: their differentiation is accelerated and their progenitors are most likely gonocytes instead of SSCs (Yoshida et al ., 2006). …”

Section: Discussionmentioning

confidence: 99%

E2F1 controls germ cell apoptosis during the first wave of spermatogenesis

et al. 2015

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SummaryCell cycle control during spermatogenesis is a highly complex process owing to the control of the mitotic expansion of the spermatogonial cell population and following meiosis, induction of DNA breaks during meiosis and the high levels of physiological germ‐cell apoptosis. We set out to study how E2F1, a key controller of cell cycle, apoptosis, and DNA damage responses, functions in the developing and adult testis. We first analyzed the expression pattern of E2f1 during post‐natal testis development using RNA in situ hybridization, which showed a differential expression pattern of E2f1 in the adult and juvenile mouse testes. To study the function of E2f1, we took advantage of the E2F1−/− mouse line, which was back‐crossed to C57Bl/6J genetic background. E2f1 loss led to a severe progressive testicular atrophy beginning at the age of 20 days. Spermatogonial apoptosis during the first wave of spermatogenesis was decreased. However, already in the first wave of spermatogenesis an extensive apoptosis of spermatocytes was observed. In the adult E2F1−/− testes, the atrophy due to loss of spermatocytes was further exacerbated by loss of spermatogonial stem cells. Surprisingly, only subtle changes in global gene expression array profiling were observed in E2F1−/− testis at PND20. To dissect the changes in each testicular cell type, an additional comparative analysis of the array data was performed making use of previously published data on transcriptomes of the individual testicular cell types. Taken together, our data indicate that E2F1 has a differential role during first wave of spermatogenesis and in the adult testis, which emphasizes the complex nature of cell cycle control in the developing testis.

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The first round of mouse spermatogenesis is a distinctive program that lacks the self-renewing spermatogonia stage

Cited by 337 publications

References 37 publications

Neonatal Gonocyte Differentiation in Mongolian GerbilMeriones unguiculatusInvolves Asynchronous Maturation of Seminiferous Cords and Rapid Formation of Transitional Cell Stage

Neonatal Gonocyte Differentiation in Mongolian GerbilMeriones unguiculatusInvolves Asynchronous Maturation of Seminiferous Cords and Rapid Formation of Transitional Cell Stage

Retinoic acid induces Sertoli cell paracrine signals for spermatogonia differentiation but cell autonomously drives spermatocyte meiosis

E2F1 controls germ cell apoptosis during the first wave of spermatogenesis

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