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WIREs Dev Biol
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From cyst to tubule: innovations in vertebrate spermatogenesis

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Although vertebrates share many common traits, their germline development and function exhibit significant divergence. In particular, this article focuses on their spermatogenesis. The fundamental elements that constitute vertebrate spermatogenesis and the evolutionary changes that occurred upon transition from water to land will be discussed. The life‐long continuity of spermatogenesis is supported by the function of stem cells. Series of mitotic and meiotic germ cell divisions are ‘incomplete’ due to incomplete cytokinesis, forming syncytia interconnected via intercellular bridges (ICBs). Throughout this process, germ cells are supported by appropriate microenvironments established primarily by somatic Sertoli cells. In anamniotes (fish and amphibians) spermatogenesis progresses in cysts, in which developing germ cell syncytia are individually encapsulated by Sertoli cells. Accordingly, Sertoli cells undergo turnover with germ cells that they nourish. This mode of cystic spermatogenesis is also observed in nonvertebrates as insects. In amniotes (reptiles, birds, and mammals), however, Sertoli cells do not turn over but comprise a persistent structure of seminiferous tubules. Sertoli cells nourish different stages of germ cells simultaneously in distinct regions of their surface. This function of Sertoli cells is spatiotemporally orchestrated, and the seminiferous epithelial cycle and spermatogenic wave make the seminiferous tubules a high‐throughput factory for sperm production. Furthermore, contrary to the organized differentiating cells, undifferentiated spermatogonia that comprise the stem cell compartment exhibit active motion over the basal layer of seminiferous tubules and the frequent breakdown of ICBs. Thus, amniote seminiferous tubules represent a typical facultative (or open) niche environment without a stem cell tethering anatomically defined niche. WIREs Dev Biol 2016, 5:119–131. doi: 10.1002/wdev.204 This article is categorized under: Gene Expression and Transcriptional Hierarchies > Cellular Differentiation Adult Stem Cells, Tissue Renewal, and Regeneration > Tissue Stem Cells and Niches Adult Stem Cells, Tissue Renewal, and Regeneration > Environmental Control of Stem Cells
Schematic drawing of cystic spermatogenesis observed in fish and amphibians. In anamniote testes, a cyst of Sertoli cells surrounds each germ cell syncytium. Sertoli cells share their fate with the developing germ cell syncytium that they nourish, and eventually degrade when germ cells mature and spermiate. Such a turnover of both germ cells and Sertoli cells suggests the presence of self‐renewing stem cells for both cell types. While germline stem cells are identified in some fish species, the Sertoli stem cells remain hypothetical. Tight junctions are established between Sertoli cells that cover haploid spermatids and more advanced germ cells. The spatial organization of cysts within the testis varies highly between species. They are aligned in the order of development in some fish, while others do not have such a polarized organization.
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Incomplete division in spermatogenesis. In general, spermatogenic differentiation accompanies incomplete mitotic and meiotic divisions, in which incomplete cytokinesis leaves the daughter cells interconnected through intercellular bridges. The number of premeiotic mitotic divisions varies between species. (Modified with permission from Ref . Copyright 1975 Saunders)
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General outline of vertebrate germline development, see text for details. Processes in the red‐dotted line appear to be lost in mammals. *The process of stem cell establishment in females (in fish or amphibians) has not been clearly elucidated.
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Behavior of undifferentiated populations of spermatogonia in mouse seminiferous tubules. (a) Seemingly random migration of GFRα1‐positive (GFRα1+) spermatogonia observed by intravital live imaging: the trajectories of 11 spermatogonia for 48 h are shown. Blood vessels running between the tubules are observed in black. (b) The GFRα1+ spermatogonia weave their way (black trajectory for 21 h) between immotile Sertoli cells (colored trajectories). Bars indicate 50 µm. (a, b: Reprinted from Ref .) (c) Continual interconversion between singly isolated and syncytial GFRa1+ spermatogonia in adult mice is schematically shown on the basis of live imaging observations.
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Seminiferous epithelial cycle and spermatogenic wave. (a) A schematic explanation of the seminiferous epithelial cycle in mice. The self‐renewing pool gives rise to the first step of differentiating cells periodically with a particular interval (8.6 days in mice), which corresponds to the length of one seminiferous epithelial cycle. The differentiating germ cells subsequently differentiate into sperm after periods of four cycles, which is how four different steps of germ cells are simultaneously nourished by a single Sertoli cell. A cycle is divided into different stages on the basis of the combination of germ cell types. Duration of a cycle and the number of stages in a cycle is species‐specific. See text for details. (b) A diagram showing the spermatogenic wave in mice. Roman numerals indicate the local stages of a seminiferous epithelial cycle. The areas where spermiation occurs (in particular those in stages VII and VIII in mice) are colored. Over time, the stages of the seminiferous epithelial cycle progress periodically, as indicated for two positions by circles. Because the temporal order of the stages is recapitulated by the spatial order along the tubules, the area of spermiation progressively shifts along the tubules like a wave (leftward in this scheme). The pattern of the wave is simple in mice but varies among species. See text for details.
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Spermatogenesis in seminiferous tubules in amniotes. (a) In amniote testis, seminiferous tubules loop out of the rete testes connected to the epididymis. (Reprinted with permission from Ref . Copyright 2006 University of Tokyo Press) (b) In seminiferous tubules, different steps of germ cells are found among Sertoli cells, which are quiescent in their cell cycle and comprise single‐layered epithelium inside the tubules. (c) Each Sertoli cell simultaneously nourishes different (typically four) steps of germ cells in different areas of their plasma membrane (illustrated by colors; from basal to the apical side). Germ cells turn over as they mature on the surface of Sertoli cells, which in contrast never turn over during adulthood. (d) A diagram of a single rat Sertoli cell, showing its columnar shape (approximately 90 µm in height) and numerous processes of cytoplasmic sheets that form crypts for different stages of germ cells, as indicated by the same colors as in (c). (Modified with permission from Ref . Copyright 1983 John Wiley & Sons Ltd.)
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