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Book ChapterDOI

6 The Functional Morphology of Teleost Gonads

01 Jan 1983-Fish Physiology (Academic Press)-Vol. 9, pp 223-275
TL;DR: This chapter discusses the functional morphology of teleost gonads and a two cell-type model involving thecal and granulosa cell layers has been proposed for the production of these two steroids for the first time in lower vertebrates.
Abstract: Publisher Summary This chapter discusses the functional morphology of teleost gonads. Information presented in this chapter indicates that there are several processes of germ cell development, which are closely associated with changes in cellular activities of somatic cell elements. Recent studies on biochemical aspects of vitellogenesis in teleosts have shown that the hepatic and ovarian yolk proteins are similar to those of amphibian species. An in vitro method involving the separation of the follicular components has facilitated investigations of the detailed mechanism of the production of two major follicular steroid hormones. As a result of the usage of this technique, a two cell-type model involving thecal and granulosa cell layers has been proposed for the production of these two steroids for the first time in lower vertebrates. With further refinements this well characterized incubation procedure should provide an excellent system for studying the molecular basis of the mechanism of gonadotropin action on follicular steroidogenesis.
Citations
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Journal ArticleDOI
TL;DR: The genetic mechanisms underpinning oocyte and embryo growth and development are a priority for research and the products synthesized in ovoand the mechanisms controlling their expression are likely to play a central role in determining egg quality.
Abstract: Factors affecting egg quality are determined by the intrinsic properties of the egg itself and the environment in which the egg is fertilized and subsequently incubated. Egg quality in fish is very variable. Some of the factors affecting egg quality in fish are known, but many (probably most) are unknown. Components that do affect egg quality include the endocrine status of the female during the growth of the oocyte in the ovary, the diet of the broodfish, the complement of nutrients deposited into the oocyte, and the physiochemical conditions of the water in which the eggs are subsequently incubated. In captive broodfish, the husbandry practices to which fish are subjected are probably a major contributory factor affecting egg quality. Our knowledge of the genetic influences on egg quality is very limited indeed. We know that parental genes strongly influence both fecundity and egg quality, but almost nothing is known about gene expression and/or mRNA translation in fish oocytes/embryos. This is surprising because the products synthesized in ovoand the mechanisms controlling their expression are likely to play a central role in determining egg quality. The genetic mechanisms underpinning oocyte and embryo growth and development are a priority for research

807 citations


Cites background from "6 The Functional Morphology of Tele..."

  • ...The major developmental events occurring during oocyte development can be broadly classi®ed into six phases, according to the state of oocyte growth; they are: oogenesis, primary oocyte growth, cortical alveolus stage, vitellogenesis, maturation and ovulation (Nagahama, 1983; Selman et al., 1986, 1993; Bromage and Cumaranatunga, 1988; Tyler, 1991; Tyler and Sumpter, 1996)....

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  • ...…classi®ed into six phases, according to the state of oocyte growth; they are: oogenesis, primary oocyte growth, cortical alveolus stage, vitellogenesis, maturation and ovulation (Nagahama, 1983; Selman et al., 1986, 1993; Bromage and Cumaranatunga, 1988; Tyler, 1991; Tyler and Sumpter, 1996)....

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Journal ArticleDOI
Abstract: An important component of many studies of fish reproductive biology is the assessment of the stage of gonad development of individual fish. The methods in use vary from highly detailed to cursory, but there are few reviews of their reliability or usefulness. This review examines histology, measurements of oocyte size, staging based on the appearance of whole oocytes, staging based on the external appearance of the ovary, and gonad indices. Histology is the most accurate technique, but it is time- consuming and expensive. Staging based on the appearance of whole oocytes can be a useful alternative but may be inaccurate with oocytes in transitional stages of development. Staging based on the external appearance of the ovary is the simplest and most rapid method, but it may be subjective and its accuracy is uncertain. Oocyte size may be used as a predictor of developmental stage if the size ranges of the various stages are known, but the sizes of different oocyte stages may overlap, which complicates this approach. Oocyte size may be used on its own to measure development but gives little information on the physiological status of the ovaries. Gonad indices (gonad size relative to body size) provide a useful insight into changes in ovary size and complement results obtained using staging methods. However, gonad indices, like oocyte size, may be biased when samples of fish of different body sizes are compared.

793 citations

Journal ArticleDOI
TL;DR: The mechanisms that control oocyte growth are addressed in this review, albeit that the available information, as in all other vertebrates, is very limited.
Abstract: Oocyte growth and development is an important issue in fish and fisheries biology. This paper reviews the information available on oocyte growth patterns and the rates and dynamics of oocyte growth in teleosts. In synchronous spawners, the weight of the gonad may represent as much as 40% of the overall body weight of the fish. In asynchronous spawners, the weight of the mature ovary is considerably less than in synchronous ovulators, but the ovary shows a more regular periodicity and may grow repeatedly many times during the breeding season. There is a huge variability in egg size in teleosts, with the largest known measuring up to 8 cm in diameter. Within the limits of variance set by genetic constraints, egg size may vary between populations of the same species. Oocytes in all teleosts undergo the same basic pattern of growth: oogenesis, primary oocyte growth, cortical alveolus stage, vitellogenesis, maturation and ovulation. The mechanisms that control oocyte growth are addressed in this review, albeit that the available information, as in all other vertebrates, is very limited. The main hormones that have been shown to affect ovarian growth are gonadotrophin, thyroid hormones, growth hormone, insulin and insulin-like growth factors. An overview of the determinants of fecundity, with particular reference to oocyte recruitment and atresia, is the focus of the second part of the paper. Genetics and nutrition have major effects on fecundity, and studies so far suggest that the determinants of fecundity usually operate during the early part of gametogenesis. The role of atresia in determining fecundity is less clear. The final part of this review highlights some areas of study that are priorities for research on ovarian development in fish.

782 citations


Cites background from "6 The Functional Morphology of Tele..."

  • ...During the primary growth phase, an acellular vitelline envelope develops around the oocyte and continues to differentiate and increase in complexity throughout the remainder of oocyte growth; this layer is often referred to as the zona radiata, zona pellucida or chorion vitelline envelope (Anderson, 1967; Ulrich, 1969; Azevedo, 1974; Wourms, 1976; Tesoriero, 1978; Nagahama, 1983; Riehl, 1984; Wallace, 1985; Bromage and Cumaranatunga, 1988) and eventually forms the tough outer coating of the egg, termed the chorion....

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  • ...The ability of oocytes to sequester VTG on reaching a certain 'critical' size may be a function of the development of patency, that is, the opening of intercellular channels through the follicular tissues to the oocyte surface, thus allowing blood-borne proteins to reach the oocyte surface (Nagahama, 1983; Wallace, 1985; Tyler et al., 1991a), or alternatively, it may be due to the expression of VTG receptors on the oocyte surface at this time....

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  • ...If one considers an oocyte of a rainbow trout during primary growth, it increases in diameter from 10-20/~m to 100-200 #m (Nagahama, 1983; Sumpter et al., 1984); this equates to at least a 1000-fold, and up to a 5000-fold, increase in volume....

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  • ...Cortical alveoli are the first distinct cytoplasmic structures within the oocyte that can be discerned at the level of the light microscope (Wallace and Selman, 1981; Nagahama, 1983; Sumpter et al., 1984; Selman and Wallace, 1989)....

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Journal ArticleDOI
TL;DR: Findings on the identification of steroidal mediators involved in each process of gametogenesis, and the sites and mechanisms of action of the mediators are reviewed.
Abstract: The pituitary-gonadal axis plays an important role in regulating gametogenesis in vertebrates. In most cases, gonadotropins act through the biosynthesis of gonadal steroid hormones which in turn mediate various stages of gametogenesis. A series of studies in our laboratory using several species of teleost fishes as experimental animals has provided new information about the endocrine regulation of gametogenesis, including oocyte growth, oocyte maturation, spermatogenesis and sperm maturation. This article briefly reviews our findings on the identification of steroidal mediators involved in each process of gametogenesis, and the sites and mechanisms of action of the mediators. These observations collectively demonstrate the appropriateness of using teleost fishes as valid models for examining hormonal influences on gametogenesis. Such models could also have applications and validity for vertebrates in general.

733 citations


Cites background from "6 The Functional Morphology of Tele..."

  • ...However, certain species do seem to have some of the appropriate histochemical and ultrastructural features for steroidogenesis (Nagahama, 1983)....

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  • ...The thecal layer contains fibroblasts, collagen fibers, and capillaries, and, in some species, special thecal cells (Nagahama, 1983)....

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  • ...These cells possess ultrastructural features commonly found in steroid-producing cells such as agranular endoplasmic reticulum and mitochondria with tubular cristae (Nagahama, 1983)....

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Journal ArticleDOI
TL;DR: This article showed that oocyte maturation is a three-step induction process involving gonadotropin (LH), maturation-inducing hormone (MIH), and maturationpromoting factor (MPF).
Abstract: A period of oocyte growth is followed by a process called oocyte maturation (the resumption of meiosis) which occurs prior to ovulation and is a prerequisite for successful fertilization. Our studies using fish models have revealed that oocyte maturation is a three-step induction process involving gonadotropin (LH), maturation-inducing hormone (MIH), and maturation-promoting factor (MPF). LH acts on the ovarian follicle layer to produce MIH (17α, 20β-dihydroxy-4-pregnen-3-one, 17α, 20β-DP, in most fishes). The interaction of ovarian thecal and granulosa cell layers (two-cell type model), is required for the synthesis of 17α,20β-DP. The dramatic increase in the capacity of postvitellogenic follicles to produce 17α,20β-DP in response to LH is correlated with decreases in P450c17 (P450c17-I) and P450 aromatase (oP450arom) mRNA and increases in the novel form of P450c17 (P450c17-II) and 20β-hydroxysteroid dehydrogenase (20β-HSD) mRNA. Transcription factors such as Ad4BP/SF-1, Foxl2, and CREB may be involved in the regulation of expression of these steroidogenic enzymes. A distinct family of G-protein-coupled membrane-bound MIH receptors has been shown to mediate non-genomic actions of 17α, 20β-DP. The MIH signal induces the de novo synthesis of cyclin B from the stored mRNA, which activates a preexisting 35 kDa cdc2 kinase via phosphorylation of its threonine 161 by cyclin-dependent kinase activating kinase, thus producing the 34 kDa active cdc2 (active MPF). Upon egg activation, MPF is inactivated by degradation of cyclin B. This process is initiated by the 26S proteasome through the first cut in its NH2 terminus at lysine 57.

698 citations

References
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Journal ArticleDOI
TL;DR: Teleosts offer examples of virtually every conceivable type of ovarian physiology and provide a wealth of experimental material for exploring the cellular and hormonal mechanisms which regulate oocyte recruitment and growth throughout ovarian recrudescence.
Abstract: SYNOPSIS. Four principal stages of oocyte growth are recognized among teleosts. During gonadotropin-independent primary growth, multiple nucleoli form as well as a Balbiani body which eventually disperses throughout the ooplasm. The first gonadotropin-dependent stage involves the formation of yolk vesicles, the precursors to the cortical alveoli. True vitellogenesis follows during which vitellogenin is sequestered from the maternal blood and packaged into yolk granules or spheres. The latter generally fuse centripetally at some time during oocyte growth to give a continuous fluid phase surrounded by a peripheral layer of cytoplasm containing the cortical alveoli. Maturation represents the final stage and is accompanied in many teleosts by water uptake; among marine teleosts with pelagic eggs, most of the final egg volume may be achieved by this process. Ovaries may be synchronous, asynchronous, or group-synchronous. Among the latter, a clutch of oocytes may be recruited from an asynchronous population of earlier stages into any of the subsequent stages. In teleosts which spawn repeatedly, recruitment of new clutches can usually be associated with the transition of a previously recruited clutch from one stage to the next. Teleosts thus offer examples of virtually every conceivable type of ovarian physiology and provide a wealth of experimental material for exploring the cellular and hormonal mechanisms which regulate oocyte recruitment and growth throughout ovarian recrudescence.

1,270 citations

Journal ArticleDOI
TL;DR: Variations in these testis-types are discussed particularly in light of modifications leading to the production of spermatozeugmata or spermatophores, as well as nuclear elongation, coupled with possible elongation of the sperm midpiece, is characteristic of most species wherein fer?
Abstract: Synopsis. Tubular structure of the teleost testis can be divided into two basic types distinguished from each other by the distribution of spermatogonia. In most teleosts, spermatogonia occur along the length of the tubules, but in atheriniform fishes they are confined to the terrriinus of the tubule. Variations in these testis-types are discussed particularly in light of modifications leading to the production of spermatozeugmata or spermatophores. Teleost boundary cells are located immediately outside of the tubule basement mem? brane. Previous reports homologizing "lobule boundary cells" with Leydig or Sertoli cells are in error. Leydig cells have been described for species of teleosts wherein they have previously been thought to be absent and are a typical component of the interstitium. Sperm morphology reflects mode of reproduction. Nuclear elongation, coupled with possible elongation of the sperm midpiece, is characteristic of most species wherein fer? tilization is internal. Teleost sperm lack an acrosome.

539 citations

Journal ArticleDOI
TL;DR: The maternal-fetal trophic relationships in each of the major groups of fishes are systematically reviewed and Pertinent anatomical, histological, ultrastructural, developmental, physiological, and biochemical studies are considered.
Abstract: SYNOPSIS. Viviparity in the vertebrate line first makes its evolutionary appearance among fishes. It has independently evolved in a number of divergent piscine lineages. The 54 families of extant fishes that bear living young include 40 families of chondrichthyans (sharks and rays), one montypic family of coelacanths ( Latimeria ), and 13 families of teleosts. There is fossil evidence for viviparity in holocephalans and chondrosteans. Viviparity predominates among sharks and rays (40 families, 99 genera, 420 species) but is less widespread among teleosts (13 families, 122 genera, 510 species). Following an historical introduction, the organization of the female reproductive system, sites of gestation, developmental sequences and superfetation are considered. The evolution of viviparity establishes specialized maternal-fetal relationships, viz. , 1) developmental, 2) morphological, 3) trophic, 4) osmoregulatory, 5) respiratory, 6) endocrinological, and 7) immunological. While the latter four categories are briefly noted the major emphasis is on the trophic relationship and its morphological and developmental basis. First, a general overview is presented and then the maternal-fetal trophic relationships in each of the major groups of fishes are systematically reviewed. Pertinent anatomical, histological, ultrastructural, developmental, physiological, and biochemical studies are considered. Viviparous fishes are either lecithotrophic, i.e. , exclusively yolk dependent, or matrotrophic, i.e. , in receipt of a continuous supply of maternal nutrients during gestation. Nutrient transfer is accomplished by 1) oophagy and adelphophagy, 2) placental analogues, and 3) the yolk sac placenta. Placental analogues include: external epithelial absorptive surfaces, e.g. , skin, fins, gills; trophonemata, modifications of the uterine epithelia for the secretion of histotrophe or “uterine milk”; branchial placentae, close apposition between gill epithelia and either uterine or ovarian epithelial villi; the yolk sac; pericardial amnion and chorion; follicular pseudoplacenta, close apposition between follicle cells and embryonic absorptive epithelia; hypertrophied gut; and trophotaeniae, external rosette or ribbon-like projections of the embryonic gut. Among chondrichthyans, the yolk sac placenta (840–1,050%), trophonematal secretion and embryonic absorbtion of histotrophe (1,680–4,900%) and oophagy and adelphophagy (1.2 × 106%) are the most efficient methods of nutrient transfer. Among teleosts, the follicular pseudoplacenta (1,800–3,900%), trophotaeniae (8,400%) and absorption of ovarian histotrophe through surface epithelia and a hypertrophied gut (1,100–34,000%) are the most efficient. These values stand in contrast to the 30%40% loss of dry weight characteristic of oviparous fishes and viviparous lecithotrophes.

501 citations

Journal ArticleDOI
TL;DR: The endocrine processes which control oocyte maturation and ovulation have been studied in vitro in the trout Salmo gairdneri and it is shown that 17α-hydroxy-20β-dihydroprogesterone plays a preferential role in initiating maturation.
Abstract: The endocrine processes which control oocyte maturation (resumption of meiosis) and ovulation have been studied in vitro in the trout Salmo gairdneri. Follicular maturation is ultimately under the control of a pituitary gonadotropin which induces the follicle to synthesize specific steroids; these steroids act in turn directly on the oocyte to promote maturation. The systematic study of the in vitro efficiency of various steroids have shown that 17α-hydroxy-20β-dihydroprogesterone plays a preferential role in initiating maturation; this steroid has a high affinity for a plasma protein system. The efficiency of this steroid, similarly to the efficiency of the gonadotropin, can be modulated by other circulating steroids. The precise chronology of some events of follicle maturation have been defined using inhibitors of protein and RNA synthesis.The ovulatory process (sensu stricto: expulsion of matured oocyte from the follicular envelopes) has been experimentally dissociated from oocyte maturation, and some ...

290 citations

Journal ArticleDOI
TL;DR: Very different testicular structures and spermatogenetic patterns have been found in fish of the teleost group and studies of their endocrine patterns suggest that the GTH involved is controlled by external (mainly temperature but also photoperiod) and gonadal factors.
Abstract: Very different testicular structures and spermatogenetic patterns have been found in fish of the teleost group. Two types of structures may be identified: (i) a tubular type with no lumen (in cypri...

257 citations