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      The Role of Retinoic Acid (RA) in Spermatogonial Differentiation1

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          Abstract

          Retinoic acid (RA) directs the sequential, but distinct, programs of spermatogonial differentiation and meiotic differentiation that are both essential for the generation of functional spermatozoa. These processes are functionally and temporally decoupled, as they occur in distinct cell types that arise over a week apart, both in the neonatal and adult testis. However, our understanding is limited in terms of what cellular and molecular changes occur downstream of RA exposure that prepare differentiating spermatogonia for meiotic initiation. In this review, we describe the process of spermatogonial differentiation and summarize the current state of knowledge regarding RA signaling in spermatogonia.

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          DNA methylation of retrotransposon genes is regulated by Piwi family members MILI and MIWI2 in murine fetal testes.

          Satomi Kuramochi-Miyagawa, Toshiaki Watanabe, Kengo Gotoh … (2008)
          Silencing of transposable elements occurs during fetal gametogenesis in males via de novo DNA methylation of their regulatory regions. The loss of MILI (miwi-like) and MIWI2 (mouse piwi 2), two mouse homologs of Drosophila Piwi, activates retrotransposon gene expression by impairing DNA methylation in the regulatory regions of the retrotransposons. However, as it is unclear whether the defective DNA methylation in the mutants is due to the impairment of de novo DNA methylation, we analyze DNA methylation and Piwi-interacting small RNA (piRNA) expression in wild-type, MILI-null, and MIWI2-null male fetal germ cells. We reveal that defective DNA methylation of the regulatory regions of the Line-1 (long interspersed nuclear elements) and IAP (intracisternal A particle) retrotransposons in the MILI-null and MIWI2-null male germ cells takes place at the level of de novo methylation. Comprehensive analysis shows that the piRNAs of fetal germ cells are distinct from those previously identified in neonatal and adult germ cells. The expression of piRNAs is reduced under MILI- and MIWI2-null conditions in fetal germ cells, although the extent of the reduction differs significantly between the two mutants. Our data strongly suggest that MILI and MIWI2 play essential roles in establishing de novo DNA methylation of retrotransposons in fetal male germ cells.
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            Essential role of Plzf in maintenance of spermatogonial stem cells.

            Jose Costoya, Robin M. Hobbs, Maria Barna … (2004)
            Little is known of the molecular mechanisms whereby spermatogonia, mitotic germ cells of the testis, self-renew and differentiate into sperm. Here we show that Zfp145, encoding the transcriptional repressor Plzf, has a crucial role in spermatogenesis. Zfp145 expression was restricted to gonocytes and undifferentiated spermatogonia and was absent in tubules of W/W(v) mutants that lack these cells. Mice lacking Zfp145 underwent a progressive loss of spermatogonia with age, associated with increases in apoptosis and subsequent loss of tubule structure but without overt differentiation defects or loss of the supporting Sertoli cells. Spermatogonial transplantation experiments revealed a depletion of spermatogonial stem cells in the adult. Microarray analysis of isolated spermatogonia from Zfp145-null mice before testis degeneration showed alterations in the expression profile of genes associated with spermatogenesis. These results identify Plzf as a spermatogonia-specific transcription factor in the testis that is required to regulate self-renewal and maintenance of the stem cell pool.
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              Plzf is required in adult male germ cells for stem cell self-renewal.

              F. William Buaas, Andrew Kirsh, Manju Sharma … (2004)
              Adult germline stem cells are capable of self-renewal, tissue regeneration and production of large numbers of differentiated progeny. We show here that the classical mouse mutant luxoid affects adult germline stem cell self-renewal. Young homozygous luxoid mutant mice produce limited numbers of normal spermatozoa and then progressively lose their germ line after birth. Transplantation studies showed that germ cells from mutant mice did not colonize recipient testes, suggesting that the defect is intrinsic to the stem cells. We determined that the luxoid mutant contains a nonsense mutation in the gene encoding Plzf, a transcriptional repressor that regulates the epigenetic state of undifferentiated cells, and showed that Plzf is coexpressed with Oct4 in undifferentiated spermatogonia. This is the first gene shown to be required in germ cells for stem cell self-renewal in mammals.
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                Author and article information

                Journal
                Journal ID (nlm-ta): Biol Reprod
                Journal ID (iso-abbrev): Biol. Reprod
                Journal ID (publisher-id): bire
                Title: Biology of Reproduction
                Publisher: Society for the Study of Reproduction, Inc.
                ISSN (Print): 0006-3363
                ISSN (Electronic): 1529-7268
                Publication date (Electronic): 11 November 2015
                Publication date (Print): January 2016
                Publication date PMC-release: 11 November 2015
                Volume: 94
                Issue: 1
                Electronic Location Identifier: 10
                Affiliations
                [3 ]Department of Anatomy and Cell Biology, Brody School of Medicine, East Carolina University, Greenville, North Carolina
                [4 ]East Carolina Diabetes and Obesity Institute, Brody School of Medicine, East Carolina University, Greenville, North Carolina
                Author notes
                [2 ]Correspondence: Christopher B. Geyer, Brody School of Medicine at East Carolina University, 600 Moye Blvd., Greenville, NC 27834. E-mail: geyerc@ 123456ecu.edu
                Article
                Serial Item and Contribution ID: bire-93-06-21 Publisher ID: Manuscript Number: BIOLREPROD/2015/135145
                DOI: 10.1095/biolreprod.115.135145
                PMC ID: 4809555
                PubMed ID: 26559678
                SO-VID: a1f77e69-40f5-4a25-b8f6-0fc3f004e7fe
                Copyright © © 2016 by the Society for the Study of Reproduction, Inc.
                License:

                This article is available under a Creative Commons License 4.0 (Attribution-Non-Commercial), as described at http://creativecommons.org/licenses/by-nc/4.0.

                History
                Date received : 1 September 2015
                Date revision received : 29 September 2015
                Date accepted : 6 November 2015
                Categories
                Subject: Articles
                Subject: Minireview

                Keywords: developmental biology,differentiation,gonocyte,prospermatogonia,retinoic acid,retinoids,spermatogenesis,spermatogonia,testis
                Data availability:
                Keywords: developmental biology, differentiation, gonocyte, prospermatogonia, retinoic acid, retinoids, spermatogenesis, spermatogonia, testis

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