Following brief overviews of fish thyroidal and reproductive endocrine ... where the main roles of TH involve regulation of growth, development and, as discussed.
Reviews in Fish Biology and Fisheries
6, 165-200 (1996)
Interrelationships between thyroidal and reproductive endocrine systems in fish DANIEL ‘Department “Department
G. CYR’ of Fisheries of Zoology,
and J.G.
EALES2
and Oceans, Maurice Lamontagne University of Manitoba, Winnipeg,
Institute, Manitoba,
Contents Introduction Fish thyroidal system Fish reproductive endocrinology Temporal relationships between thyroidal and reproductive Effects of thyroidal status on reproductive function
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Canada
status
Quebec,
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324
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page 165 167 168 169 172
Males Females Ovarian development and vitellogenesis Thyroid hormones within the egg Effects of reproductive Biological implications Summary Acknowledgements References
status on thyroidal
function
179 183 184 186 186
Introduction
Although fish thyroidal and reproductive systems have been researched extensively, they have been studied largely in isolation from each other. The potential for interactions between the two systems is considerable. Interactions have been suggested (Pickford and Atz, 1957; Berg et al., 1959; Ball, 1960; Matty, 1960, 1985; Dodd and Matty, 1964; Gorbman, 1969; Singh, 1970; Sage and Bern, 1971; Dodd, 1975, 1983; Donaldson and Hunter, 1983), and reviewed more extensively by Eales (1979), Nagahama (1983), Leatherland (1987, 1994), and Dickhoff et al. (1989). Sage (1973) has pointed out the structural similarities between thyroid-stimulating hormone (TSH)” and gonadotrophins and suggested some role of the thyroid in regulation of fish reproduction. Theoretically, thyroid hormones (TH) might influence any aspect of female or male reproductive function from the level of the brain to the level of receptors for gonadal steroids, and to the expression of secondary sexual characteristics (Fig. 1). By parallel reasoning, gonadal steroids and other reproductive hormones might influence any aspect of thyroid function or TH action. Our present objective is to review literature relating to the interrelationships between *Table
1 lists abbreviations
0960-3
166 0
1996 Chapman
used herein. & Hall
166
Cyr and Eales
thyroidal and reproductive systems in fish, including some of our recent studies on salmonids. Following brief overviews of fish thyroidal and reproductive endocrine function, we first examine the temporal relationships (correlations) between the two systems. We then consider effects of TH on various levels of reproductive endocrine function, and next consider effects of reproductive hormones on thyroidal function. Despite few recent experimental studies, we conclude that numerous interactions between the two systems do occur, and that they are highly complex, involving multiple levels of regulation in both systems. These interactions may aid not only in control of reproductive function itself, but also in regulation of metabolism, energy provision and somatic growth during the period of reproduction. THYROID
I
REPRODUCTIVE
SYSTEM
--d
BRAIN
-+I
SYSTEM
BRAIN
4
GnRH
PITUITARY
I
GTH I AND II 1
THYROID
1 +-A
I I I I
I T4
1
--T3
TARGET CELLS
I I I I I I
-
4
--
I
SEX STEROIDS
--b
Fig. 1. Potential sites of action of TH (T4 and Ts) on the reproductive system and potential sites of action of male and female gonadal steroids on the thyroidal system of fish. Abbreviations as in Table 1.
Thyroid and reproduction Table 1. Abbreviations 5’D 1 l-KT CAMP dbcAMP DHP FSH GllRH GSI GTH GVBD hCG ki G LH MBC PDE T T3 T4
TH TRH TSH Yrnaz VTG
Fish thyroidal
used in this review 5’-deiodinase 1 1-ketotestosterone Cyclic adenosine monophosphate Dibutyryl CAMP Progestogens (see text) 17P-oestradiol Follicle-stimulating hormone Gonadotrophin-releasing hormone Gonadal-somatic index Gonadotrophin Germinal vesicle break down Human chorionic gonadotrophin Affinity of Ta for receptor sites Enzyme-substrate affinity Luteinizing hormone Maximum binding capacity Phosphodiesterase Testosterone 3,5,3’-triiodo+thyronine L-thyroxine (= tetraiodothyronine) Thyroid hormone(s) Thyrotrophin-releasing hormone (= TSH-releasing Thyroid-stimulating hormone (= thyrotrophin) Level of functional enzyme Vitellogenin
Ea
167
in fish
hormone)
system
The thyroidal system is controlled partly by the brain-pituitary axis (Fig. 1) (Eales and Brown, 1993). Neurosecretory cells from the hypothalamus impinge directly on thyrotrope cells in the pituitary and regulate the release of TSH. The chemical factors involved in this release have not been identified, but hypothalamic control is achieved primarily by the inhibition of TSH cells. TSH acts on the thyroid and promotes synthesis and release of TH which, in the few teleost species examined, is primarily L-thyroxine (Td). About 99% of circulating Tq is bound reversibly to plasma proteins, but the free Tg fraction exchanges across the cell membrane and may involve one or more transport systems. Tg is metabolized by several intracellular pathways, but a significant proportion can be converted to 3,5,3’-triiodo-L-thyronine (Ts) by enzymatic monodeiodination of the outer aromatic ring. This step is critical to the regulation of thyroidal status, because T3 has about a ten-fold greater affinity than T4 for putative nuclear receptor sites. Thus T4 is probably a weakly active prohormone while peripherally derived Ts is the active hormone. Ts enters the circulation where, like Tq, it binds to proteins with approximately 1% of T3 free in plasma. Actions of Ts on target cells are poorly understood in fish. However, as in mammals, Ts probably binds to a nuclear receptor-T3 complex which in turn binds to a short DNA sequence known as the thyroid-response element. This temporary association initiates transcription of TH-dependent genes. In endothermic vertebrates, TH play major roles in regulating thermogenesis by modulating numerous
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Cyv and Eales
facets of metabolism. Such effects have not yet been demonstrated convincingly in fish, where the main roles of TH involve regulation of growth, development and, as discussed here, aspects of reproduction. One problem is studying the fish thyroidal system involves evaluation of the level of thyroidal function (thyroidal status), which has been measured in numerous ways. These include histological and ultrastructural indices, indices based on the thyroidal uptake and metabolism of radioiodide, measurement by immunoassay of circulating total or free TH levels, TH kinetics used to estimate TH degradation rates and plasma-to-tissue exchange rates, TH concentrations in various tissues, metabolic enzymatic conversions of TH and especially T4 to T3 (deiodinase) conversion, and properties of the putative nuclear receptor sites. The advantages and disadvantages of these various indices have been reviewed by Eales and Brown (1993). The most reliable criteria probably relate to the availability of T3 (the biologically active hormone) to the tissue receptor sites. Other indices, although providing an indication of adjustment in some aspect of thyroidal function, may not necessarily reflect alteration of thyroidal status as defined in the above terms. Unfortunately much of the older literature involves use of these potentially less reliable techniques. While we should not ignore what amounts to a very large body of older literature on the topic of thyroidal and reproductive functions, inference should be moderated, particularly where histological and radioiodide uptake measurements are concerned. Fish reproductive
endocrinology
The endocrine control of reproduction of both female and male fish involves a brainpituitary-gonadal axis (Fig. 1). Neurons from hypothalamic centres regulate the release of gonadotrophins from the pituitary gland with both stimulatory and inhibitory regulation (Peter et al., 1991). Neurons that secrete GTH (gonadotrophin)-releasing hormone(s) (GnRHs) release GnRH in the vicinity of pituitary gonadotrope cells which bind to a specific receptor on the gonadotrope and stimulate the release of GTH (Habibi and Peter, 1991). Dopamine both exerts an inhibitory effect on the release of GnRH from the hypothalamus and acts directly on the gonadotropes to inhibit GTH release (Chang et al., 1990; Peter et al., 1991). In Atlantic croaker (Micropogonias undulatus, Sciaenidae), however, dopamine does not appear to inhibit the release of GTHII by the pituitary (Copeland and Thomas, 1989). There are two GTH forms; one structurally related to follicle-stimulating hormone, FSH (GTH I) and the other to luteinizing hormone, LH (GTHII) O(awauchi et al., 1989). It would appear that in fish, as in other vertebrates, GTHI is primarily involved in gametogenesis and steroidogenesis while GTH II alters steroidogenesis to stimulate the final stages of gametogenesis (Swanson, 1991). Depending on gender and phase of reproduction, GTHs stimulate the synthesis of steroids which include testosterone (T), 11 -ketotestosterone (11 -KT), 17P-oestradiol (Es) and progestogens (DHP) (Kime, 1993). In a recent review, Kime (1993) indicates that in over 35 species of fish that have been examined, 1701, 20P-dihydroxy-4-pregnen-3-one is the primary progestogen produced by fish ovarian follicles. Other novel progestogens have also been identified (Kime, 1993), and will be referred to as DHP in this review. The steroids act on target tissues to regulate gamete maturation, coordinate reproduction, and contribute to the development of gender-specific morphological and behavioural secondary sexual characteristics.
169
Thyroid and reproduction in fish
Generalization concerning fish reproductive endocrinology is difficult due to different species-specific reproductive strategies. However, early oocyte development is governed primarily by rising blood levels of GTHI, which binds to type1 GTH receptors on both thecal and granulosa cells of the oocyte. It stimulates thecal cells to synthesize T, some of which is transferred to granulosa cells where aromatase converts T to Ez. Both steroid hormones are secreted into the blood. An exception to this two-cell model for Ea synthesis has been proposed for mummichog (Fundulus heteroclitus, Cyprinodontidae), in which follicle cells can secrete Ez in the absence of thecal cells (Petrino et al., 1989). Circulating E2 binds to hepatic nuclear receptors and induces the production of yolk proteins such as vitellogenin (VTG) (Lazier and MacKay, 1993; Valotaire et al., 1993). During this phase when oocyte development is greatly increased, VTG secreted into blood binds to receptors on oocyte membranes, and is then internalized and enzymatically cleaved into phosvitin and lipovitellins. These are deposited in fluid-filled yolk granules which eventually fuse to form a homogeneous distribution of yolk within the oocyte (Tyler, 1991; Lancaster and Tyler, 1994). While in salmonids VTG is the most important contributor to egg yolk, in the winter flounder (Pseudopleuvonectes americanus, Pleuronectidae), other plasma-derived lipoproteins distinct from VTG are also transported into the developing oocyte and may represent a greater contribution to the yolk in the oocyte (Nagler and Idler, 1990). In salmonids, as oocyte development proceeds, plasma levels of GTHI diminish while GTH II levels rise (Swanson, 1991). Type II GTH receptors which bind GTH II are found exclusively on granulosa cells, where GTHII induces the production of the maturational steroid DHP, which in turn induces ovulation (Swanson, 1991; Yan et al., 1991, 1992). In male fish, GTH I and GTH II stimulate testicular steroidogenesis and spermatogenesis. Ultrastructural features of Leydig and Sertoli cells suggest both cells synthesize androgens, but their relative steroidogenic contributions have not been determined (Nagahama, 1983; Fostier et al., 1983). Both GTHI and II are equipotent in stimulating production of 1 l-KT and DHP by testicular fragments, but in later stages of spermatogenesis, GTHII has a greater potency for stimulating DHP (Planas et al., 1993). In most fish species examined, testes produce both T and 1 l-KT (Fostier et al., 1983). In contrast to mammals, dihydrotestosterone does not appear to be a prominent androgen in fish. High doses of T maintain spermatogenesis in hypophysectomized goldfish (Carassius auratus, Cyprinidae) (Billard, 1974), suggesting an androgen role in this process. Increased levels of DHP are associated with spermiation and may play a role in the final stages of sperm maturation (Sakai et al., 1989). Temporal
relationships
between
thyroidal
and reproductive
status
Temporal relationships (correlations) between thyroidal status and reproductive status have been studied for several cyclostomes, elasmobranchs and acipenserines and for about 50 species of teleosts over their annual or reproductive cycles. Thyroidal indices used in early studies included the histological appearance of pituitary thyrotropes or thyroid tissue, thyroidal uptake of radioiodide or protein-bound iodine levels in thyroid or plasma; later and probably more reliable studies involved measurements of plasma T4 or T3 by radioimmunoassay, thyroidal protease activity, TH receptor levels or TH deiodinase activity. Reproductive status was assessed from the gonadal-somatic index (GSI),
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histological appearance of gonads, development of secondary sexual characteristics, reproductive behaviour, or more recently from plasma levels of the sex steroids as determined by radioimmunoassay. In most cases some correlation exists between the thyroidal index and reproductive status, but the nature and extent of the relationship varies with taxon, type of life cycle, and reproductive strategy. In the Southern Hemisphere lamprey, Geotria australis, plasma Ts levels and hepatic T4 deiodination to Ts fell progressively during the upstream migration with little change in T4 (Leatherland et al., 1990). Levels of TH were not clearly related to the later stages of gonadal development. In other lamprey (Petvomyzon) species, Reese (1902) and Fontaine and Leloup (1950) reported low thyroid activity at spawning based respectively on thyroid structure and blood hormonal iodine levels, but Homsey (1977) found elevated blood T4 at spawning, especially in females. In oviparous elasmobranchs, thyroid activity as measured by several different indices was lowest in immature females and greatest at the peak of egg development and vitellogenesis; in males, elevation in thyroid activity was less pronounced (Guariglia, 1937; Ram-i, 1937; Olivereau, 1949b; Leloup, 195 1; Clements, 1957; Dodd and Matty, 1964; Mellinger, 1966; Sage and Jackson, 1973; Lewis and Dodd, 1974; Dodd, 1975, 1983; Leloup et al., 1976). A correlation also exists between thyroidal function and female gestation of ovoviviparous species (Zenza, 1937; Leloup, 1949a,b; Olivereau, 1949a; Woodhead, 1964, 1966). Russian literature indicates a close correlation between acipenserine gonadal maturation and thyroidal status (Pickford and Atz, 1957; Ball, 1960; Matty, 1960). Thyroid activity may also be high during the prespawning migration, at spawning and after spawning (Zaitzev, 1961, 1966). In the non-salmonid teleosts, correlations between thyroidal and reproductive status have been examined for the following families: Amphipnoidae (Srivastava and Sathyanesan, 1971; Towheed et al., 1987); Anabantidae (Chakraborti et al., 1983; Mama and Bhattacharya, 1989); Anguillidae (Callamand and Fontaine, 1942; Bemardi, 1948; Leloup, 1959); Bagridae (Singh and Sathyanesan, 1968); Carangidae (Ivleva, 1989); Catostomidae (Stacey et al., 1984); Cichlidae (Weber et al., 1992); Clariidae (Singh et al., 1974; Nayak and Singh, 1991; Sinha et al., 1992); Clupeidae (Buchmann, 1940; Batal’yants, 1968); Cobitidae (Lieber, 1936); Coregonidae (Zaitzev, 197 1; Lahti and Linqvist, 1986); Cyprinidae (Barrington and Many, 1954; Yaron, 1969); several cyprinodonts, Poeciliidae (Stolk, 1951; Bromage and Sage, 1968; Sage and Bromage, 1970a,b; Young and Ball, 1982, 1983; Berg et af., 1959; Sokol, 1961), Hemiramphidae (Stalk, 1956) and Oryziidae (Nishikawa, 1976); Engraulidae (Ivleva, 1989); Esocidae (Zaitzev, 1955); Gadidae (Woodhead 1959a,b; Wiggs, 1974; Ivleva, 1989); Gasterosteidae (Honma et al., 1977); Gobiidae (Tamura and Honma, 1970, 1973; Iwata and Homna, 1985); Heteropneustidae (Singh et al., 1974); Ictaluridae (Burke and Leatherland, 1983; MacKenzie et al., 1989); Mullidae (Lafaurie and Fromento, 1980); Plecoglossidae (Honma, 1959; Honma and Tamura, 1963; Homna and Ikarashi, 1985); Pleuronectidae (Hickman, 1962; Osbom and Simpson, 1978; Eales and Fletcher, 1982), and Serranidae (Lafaurie and Fromento, 1980). There is a general positive correlation between several thyroidal indices and reproductive status in the majority of the above teleosts that breed seasonally. This is despite major differences in habitat and life history. Thyroidal activity usually increases during early gonadal development, is maintained or enhanced during the period of
Thyroid and reproduction in fish
171
reproduction, and commonly decreases during or after spawning itself. In female ovoviviparous cyprinodonts, which do not follow a seasonal cycle but go through a breeding cycle every few weeks, there is likewise an increase in thyroidal function during the first part of each cycle. There are some exceptions to the general pattern described for seasonal breeders, and in some instances thyroidal function may decrease once vitellogenesis gets under way (Burke and Leatherland, 1983). In other instances no clear-cut relationship between reproductive and thyroidal functions was reported (Osborn and Simpson, 1978; Ivleva, 1989). However, in several cases, lack of a significant relationship may reflect the method of statistical analysis in which all seasonal values were correlated to state of gonadal development, possibly obscuring relationships confined to particular phases of the reproductive cycle. As noted previously (Ball, 1960; Many, 1960; Sage, 1973; Eales, 1979; Leatherland, 1987), the temporal changes in the thyroidal and reproductive systems imply some interdependence in non-salmonids. Temporal relationships between thyroidal and reproductive status have been examined for at least twelve species in the family Salmonidae, within the genera Oncorhynchus, Salvo and Salvelinus. Several indices of thyroidal status have been used, but in the majority of cases, TH circulating levels were measured. These species include the normally anadromous coho salmon, 0. kisutch (Sower and Shreck, 1982; Leatherland and Sonstegard, 1980a, 1987; Leatherland and Flett, 1991); sockeye salmon, 0. nerka (Ichikawa et al., 1974; Biddiscombe and Idler, 1983); chinook salmon, 0. tschawytscha (Robertson and Wexler, 1960, 1962; Robertson et al., 1961, 1962); chum salmon, 0. beta (LJeda et al., 1984); pink salmon, 0. gorbuscha (Leatherland et al., 1989~); Atlantic salmon, Salmo salar (Olivereau, 1954; Leloup and Fontaine, 1960; Fontaine and Leloup, 1962; Dickhoff et al., 1989; Eales et al., 1991; Youngson and Webb, 1993), and normally non-anadromous species including rainbow trout, 0. myh?ss (Robertson and Chaney, 1953; Robertson et al., 1961; Osborn et al., 1978; Cyr et al., 1988a; Pavlidis et al., 1991); 0. rhodurus (Fujioka et al., 1990); brown trout, SaZmo trutta (Swift, 1955, 1959; Pickering and Christie, 1981; Norberg et al., 1989); brook trout, Salvelinus fontinalis (White and Henderson, 1977); lake trout, Salvelinus namaycush (Foster et al., 1993), and Salvelinus Zeucomaenus pluvias (Homna and Tamura, 1965). The most pronounced and reproducible changes in thyroidal function occur in the anadromous forms, which either migrate to the ocean or complete their life cycle in the unnatural Great Lakes environment. There is a progressive decline in both plasma T4 and T3 with upstream migration to the spawning grounds for both males and females. Thyroid function is high in the early stages of gonadal maturation but decreases as vitellogenesis and testes development proceed. However, TH and particularly T3 plasma levels are often higher in males than in females just prior to spawning and may even increase at this time (Nagahama et al., 1982; Biddiscombe and Idler, 1983; Ueda et al., 1984). In a few studies on non-anadromous forms, no clear-cut correlations were observed between circulating TH levels and reproductive status (Osbom et al., 1978; Foster et al., 1993), but in most other studies the relationship between the two systems resembled that for the anadromous forms, with higher thyroidal activity at the end of the growth phase and the start of gonadal development, followed by a decrease during gonadal growth, and sometimes an increase at spawning. This spawning increase seems to occur particularly in males (Fujioka et al., 1990). Following spawning, there is resurgence in thyroid activity as the fish enters the growth phase of its annual cycle.
172
Cyr and Eales Interpretation of seasonal correlations in many salmonids is complicated by simultaneous variation in factors such as nutritional status, water temperature, photoperiod, and migratory behaviour with its associated metabolic demands. To minimize such potentially confounding effects we studied relationships between circulating sex steroid levels, gonadal development and circulating TH levels in hatchery-maintained female rainbow trout under a constant temperature and feeding regimen, but we manipulated photoperiod to alter spawning time (Whitehead and Bromage, 1980; Duston and Bromage, 1986, 1987). In this way seasonal correlations could be compared between trout of similar age, with spawning time as the primary variable (Cyr et al., 1988a). Serum T3 and T4 levels were highest during early ovarian development, but serum TH decreased as serum Ez levels increased. These relationships prevailed regardless of photoperiod-induced changes in spawning time. Pavlidis et al. (1991) have also shown for two strains of rainbow trout, held under different photocycles for two reproductive cycles, that minimum T3 and T4 plasma concentrations occurred during the spawning period and that TH concentrations were lower in mature as opposed to non-spawning females. Thus both T3 and Tg serum levels are elevated temporarily during early ovarian development in rainbow trout, reinforcing the emerging view that TH may play a role in the initiation or regulation of early stages of oogenesis in salmonid fish. Significant circulating levels of certain sex steroids can be detected outside the reproductive period and may be related to changes in TH levels. In immature anadromous amago salmon, 0. masou (Nagahama et al., 1982) and 0. kisutch (Patino and Shreck, 1986) no plasma E2 was detected during Parr-smolt transformation. However, in 0. nzasou (Yamada ef al., 1989, 1993b) and 0. kisutch (Sower et al., 1984, 1992; Lewis et al., 1992) elevations in E2 and T occurred during Parr-smolt transformation and coincided with a surge in Tq. Because the gonads are poorly developed in both sexes at this period of development, Yamada et al. (1989) suggested that the T may have been produced in the head-kidney with the aromatization to Ez occurring in the brain. T4 levels were correlated with androgen levels in flow challenged male Atlantic salmon (Youngson and McLay, 1989). All the above temporal relationships in both salmonids and non-salmonids, while suggestive, do not show that thyroid function influences reproductive diction or vice versa. Firstly, several indices have been used to evaluate thyroidal function, and the reliability of some of the older indices may be in doubt (Eales and Brown, 1993). Secondly, any temporal correlations between thyroidal and reproductive status require confirmation by controlled experiment. These are explored below. However, these correlational studies are of considerable significance in confirming that experimentally determined relationships based on laboratory studies may indeed be borne out by observations during the natural or quasinatural reproductive cycle. Effects of thyroidal
status on reproductive
function
MALES
Numerous workers have attempted to either reduce thyroidal status (by using thyroid inhibitors, primarily thiocyanate, perchlorate, thiouracil, and most commonly thiourea, or by radiothyroidectomy), or to enhance thyroidal status by administration of thyroid powder, TH or TSH. They then examined changes in testes development and maturation,
Thyroid and reproduction in fish
173
GSI, morphological secondary sexual characteristics or reproductive behaviour. Such studies have been undertaken on several species of tropical cyprinodonts (Kroeckert, 1935; Chambers, 1951; Grobstein and Bellamy, 1939; Smith and Everett, 1943; Goldsmith et al., 1944; Nigrelli et al., 1946; Hopper, 1950, 1952, 1965; Buser and Bougis, 1951; Chambers, 1951; Gaiser, 1952; Vivien and Gaiser, 1952; Smith et al., 1953; Pickford, 1954; Harris, 1959; Plugfelder, 1959; Grosso, 1961; Hopper and Wallace, 1970; Pandey and Leatherland, 1970); the cyprinids Phoxinus phoxinus (Barrington and Matty, 1952; Scott, 1953; Fortune, 1955; Barrington, 1964), and Pimephales promelas (Lanno and Dixon, 1994); Hypseleotris galli, Eliotrididae (MacKay, 1973); Cymatogaster aggregata, Embiotocidae (Wiebe, 1968); 0. nerka, Salmonidae (McBride and Van Overbeeke, 1974), and Channa punctatus, Channidae (Belsare, 1965). Most of these studies involved use of thiourea to inhibit TH secretion. It usually had little effect on the mature testes, but inhibited early testes development. This may mean that TH are required for early testes development, through direct action on the testes or through action at the level of the pituitary gonadotropes. However, thiourea could exert extrathyroidal action (Chambers, 1953; Eales, 1981) and modify activities of gonadotropes or testicular cells directly. While there is clearly doubt on the interpretation of experiments employing thiourea, other thyroid inhibitors (perchlorate, thiocyanate and propylthiouracil) also blocked thyroid function and inhibited testes function. However, extrathyroidal actions of these inhibitors are difficult to rule out also, because in most instances no attempts were made to offset the effects of the thyroid inhibitors by TH replacement therapy. In the few experiments in which TH were administered, results were equivocal. Perhaps the most convincing evidence for a role of TH in testes development is the study of Baker-Cohen (1961) in which the platyfish Xiphophorus maculatus (Poeciliidae) was radiothyroidectomized, resulting in a major inhibition of testes development, which was reinstated by TH treatment. Nuclear Ta receptors have been identified in Leydig cells of the freshwater climbing perch, Anabas testudineus, Anabantidae (Jana and Bhattacharya, 1993), where there is a single form of Ts receptor with an affinity similar to that of the hepatic nuclear T3 receptor. Primary cultures of Leydig cells incubated for 3 h with Ts secreted more androgens and had higher protein levels than control cells (Jana and Bhattacharya, 1993). Stimulation was dose dependent, but T3 concentrations needed to stimulate androgen secretion were lo-fold greater than levels present in plasma. Appreciable T3 (5 ngg-r) occurs in chum salmon testes when spermatozoa are forming, consistent with a T3 role during early gamete and/or testes maturation (Tagawa et al., 1994). While there are few data on TH effects on male fish reproduction for any given species model, studies to date from diverse species suggest that TH involvement in fish testes function could be a fruitful area for research. A role of TH in testes development is consistent with recent mammalian literature. For example, Ts receptors have been reported recently in the rat testis (Jannini et al., 1990) and Ts modifies proliferation and differentiation of Sertoli cells in neonatal rats (Cooke et al., 1994). FEMALES
Ovarian development and vitellogenesis Numerous early studies conducted mainly on tropical cyprinodonts and cyprinids have examined the concept of TH involvement in female teleost reproduction. As described
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Cyr and Eales
above for male fish, modification of thyroidal status by chemical inhibitors (primarily thiourea) or radiothyroidectomy usually suppressed female reproductive functions (Mukherjee, 1975), and in some instances normal function could be reinstated with TH treatment (reviews: Pickford and Atz, 1957; Sage, 1973; Eales, 1979). Some recent studies are also consistent with the view that experimental depression of thyroidal status is associated with reduced ovarian function in rainbow trout (Ruby et al., 1993) and in Pimephales (Lanno and Dixon, 1994). Despite ambiguity in the interpretation of a number of the early experiments, particularly those employing chemical thyroid inhibitors (see ‘Males’ above), TH may play roles in early ovarian development and vitellogenesis, and in final maturation. These are discussed below. Experimental studies have confirmed synergism between TH and GTH during early ovarian development. Addition of T4 for 8 and 17 weeks to aquarium water stimulated ovarian maturation in immature goldfish, while the same treatment in hypophysectomized adults was ineffectual; however, following hypophysectomy, Tctreated adults were more sensitive to partially purified salmon GTH (SG-GlOO) than untreated adults (Hurlburt, 1977). For the female stellate sturgeon (Acipenser stellatus, Acipenseridae), Detlaf and Davydova (1974, 1979) showed that Ts administration restored oocyte responsiveness to GTH in females kept at low temperature, a condition which otherwise delays sexual development. In Anabas, T4 enhanced in vitro the cholesterol-depleting action of fish crude GTH (SG-GIOO) or ovine LH on the ovary (Sen and Bhattacharya, 1981). Because Tq was only effective if added 2 h prior to GTH treatment, TH may exert a priming action. In the guppy (Poecilia reticulata, Poeciliidae), addition of T4 to aquarium water decreased both spawning interval and brood time (Lam and Loy, 1985). In female rainbow trout, we found that physiological elevation in plasma Ts levels, alone or in combination with salmon GTH (SG-GlOO), increased GSI of trout treated for 21 days (Cyr and Eales, 1988a). This increase was greater in trout treated with Ts and GTH than in trout treated with GTH alone. Treatment for 21 days with sodium ipodate, a potent thyroid inhibitor (Cyr and Eales, 1986), decreased circulating levels of both Ts and T4, and caused a 45% decrease in GSI. These data support previous studies in suggesting that Ts somehow acts synergistically with GTH to enhance ovarian development and that Ts may amplify effects of low GTH levels. To determine if Ts altered sensitivity of ovarian follicles to GTH, female trout were fed Trsupplemented food pellets (4 or 12 ppm) for 7 days to augment plasma Ts levels approximately 4and 15-fold respectively. Following Ta treatment, ovarian fragments were incubated in a defined culture medium containing GTH (SG-GlOO), and Ez release into the medium was used as the index of ovarian sensitivity to GTH. Ez release from ovaries of trout fed 4 ppm Ts was almost twice that of controls, while E2 release from ovaries of trout fed 12 ppm Ts was not enhanced. Clearly Ts influences ovarian GTH sensitivity in a dose-dependent manner; a low physiological Ta dose enhances GTH action, while a higher non-physiological Ts dose has no effect. This biphasic action of T3 may account for certain discrepancies between results of previous experiments investigating effects of TH on fish reproduction. To determine if TH act directly on the trout ovary to enhance GTH action, we isolated ovarian follicle cell layers and incubated them with GTH (SG-GlOO) and/or TH (Cyr and Eales, 1988b). While TH alone exerted no action, T3 was effective within 3 h in stimulating GTH-induced Ez release; Tq was less potent. When GTH-treated follicles were exposed to non-physiological TH levels, there was either no stimulation or an
Thyroid and reproduction
in fish
175
inhibition of Es release, confirming the in vivo biphasic T3 action. Direct in vitro TH actions on ovarian follicles have since been reported also in the daily-spawning medaka (Oryzias latipes, Oryziidae, Soyano et al., 1993). In this species, T3 amplified GTHinduced Es secretion during vitellogenesis. The stimulatory effect of T3 occurred only between 32 and 26 h prior to ovulation. These two studies demonstrate that the effectiveness of T3 stimulation is limited by both its concentration range and a narrow temporal window. How might T3 enhance GTH action to promote ovarian steroid hormone synthesis? According to current dogma, the predominant action of TH on target cells involves temporary binding of T3 to a nuclear receptor protein which then links with DNA to initiate transcription. T3 action on the fish ovary may involve nuclear receptors. Chakraborti et al. (1986) reported nuclear T 3 receptors in Anabas ovary. These receptors had an affinity for T3 exceeding that for hepatic receptors, implying some differences between the receptors in the two tissues. Bandyopadhyay and Bhattacharya (1994) have since achieved a 580-fold purification of the putative TH receptors in the Anabas ovary, and concluded that it is a disulphide-linked dimer. The greatest abundance of TH receptors occurred during the prespawning phase when the plasma Ts was highest (Mama and Bhattacharya, 1989). Soyano et al. (1989) also reported nuclear TH receptors in the medaka, and described ovarian 5’-monodeiodinase activity, indicating local T4 to Ts conversion in the ovary. However, in our own studies on rainbow trout (Cyr and Eales, 1988b) we found that although cycloheximide (an inhibitor of protein synthesis by transcription blockage) generally lowered the effectiveness of GTH in stimulating ovarian Es release, it did not block the GTH-enhancing effects of Ts. This suggested a transcription-independent action of Ta. Studies on mammals indicate that not all TH actions occur at the level of nuclear receptors. In rat thymus cells, TH act at the level of the plasma membrane to stimulate rapid uptake of sugars, amino acids and Ca2+, an intracellular regulator (review: Segal and Ingbar, 1986). A comparable calcium-linked mechanism may exist in the fish ovary to explain the rapid (3 h) action of T3 to enhance GTH effects. GTH action on the fish ovary involves an increase in intracellular cyclic adenosine monophosphate (CAMP) achieved through GTH-receptor mediated stimulation of membrane adenylate cyclase (Goetz, 1991). As confirmation of this, incubation of rainbow trout ovarian follicles for 18 h with dibutyryl CAMP (dbcAMP) duplicated GTH action and caused release of E2 (Cyr and Eales, 1989a). Of particular significance, T3 enhanced this effect of dbcAMP to release E2 in the absence of exogenous GTH. Furthermore, T3 did not modify GTH (SG-GIOO) action in the presence of forskolin, an adenylate cyclase agonist which enhances CAMP production. In combination, these results point to a GTH-independent action of T3 on regulation of CAMP levels, and indicate the most likely T3 effect may be to suppress CAMP degradation by decreasing phosphodiesterase (PDE) activity. In support of this view we found the GTH-enhancing effect of T3 was not blocked by theophylline, a PDE inhibitor. A similar type of result has been reported recently for progesterone secretion by human luteinized granulosa cells, where Ta enhanced response to human chorionic gonadotrophin (hCG) by amplifying the CAMP transduction pathway. Furthermore, Ta stimulation was lost in the presence of 1-methyl-3-isobutylxanthine, a PDE inhibitor, indicating that Ta increased follicular steroid production by suppressing PDE activity
176
Cyr and Eales (Goldman et al., 1993). The mechanism whereby Ta might inhibit PDE activity in fish is not known. However, in porcine brain, Ts inhibits Ca2+-calmodulin activation of CAMP-dependent PDE (Rao et al., 1987). TH also increases cell Ca2+ uptake (Segal and Ingbar, 1986). Thus, T3 might inhibit PDE activity of trout ovarian follicles by altering a Ca2+-dependent s’g 1 nal transduction pathway (Cyr and Eales, 1989a). The general similarity between the results on humans and rainbow trout suggests that T3 regulation of ovarian function may be highly conserved during vertebrate evolution. Measurements of PDE activity in ovarian follicles treated with Ts are needed to demonstrate conclusively that this represents the action of Ts in fish. In fish, as in other vertebrates, both egg follicular layers (theta and granulosa) are needed to synthesize Ez (Nagahama, 1983). To determine the site of TH action, thecal or granulosa cells of brook trout were isolated and incubated for 18 h. Thecal cells were cultured in the presence of GTH (SG-GIOO) or GTH + Ts. GTH alone caused a significant doubling in T release relative to unstimulated follicles, and GTH + Ts caused a further significant increase (Fig. 2). Thus T3 enhanced the action of GTH to stimulate T synthesis. Because granulosa cells are involved predominantly in the aromatization of T to E2, and because aromatization does not depend on GTH (Nagahama, 1983), these cells were incubated with T or T + Ts, and the E2 content of the medium measured. Ts caused a significant 30% increase in the conversion of T to Es by the granulosa cells (Fig. 3). Thus Ts enhances both production of T and its aromatization to Ez. In humans, the conversion of androstenedione to Ez is increased markedly in both hyperthyroid
b
2 -
oM
GTH
GTH + T,
Fig. 2. T content of medium (mean ? SEM; N = 3) after 18 h incubation of brook trout ovarian thecal cells with GTH (0.5 pgml-l) or GTH + T3 (1.9 X lOUs M). Control follicles were incubated in medium alone (M). Letters: a, p < 0.05 significantly different from medium alone; b, p < 0.01 significantly different from GTH alone.
Thyroid and reproduction
177
in fish
6-
T
b
5-
c4 E 2 g 373 g 8 0 *-
1 -
oM
T
T+T,
Fig. 3. Ez content of the medium (mean 2 SEM; II = 3) after 18 h incubation of brook trout ovarian granulosa cells with testosterone (100 mgml-I) or testosterone + Ts (1.9 X 10m8 M). Control follicles were incubated in medium alone (M). Letters: a, p < 0.05 significantly different from medium alone; b, p < 0.05 significantly different from testosterone alone.
males and females (Southren et al., 1974), indicating that some common mechanism of regulation of EZ production by TH may exist in vertebrates. TH play an important role in the induction of hepatic vitellogenesis in amphibians (Huber et al., 1979; Wangh, 1982; Wangh and Shneider, 1982; Rabelo and Tata, 1993). TH may also be involved in initiating vitellogenesis in elasmobranchs (Dodd, 1983). Lewis and Dodd (1974) surgically thyroidectomized spotted dogfish (Scyliorhinus canicula, Scyliorhinidae) in May, and determined effects on ovarian development between October and January. Ovaries of thyroidectomized fish contained oocytes with no evidence of vitellogenesis, whereas ovaries of intact controls contained mature vitellogenic oocytes with diameters comparable to those at natural ovulation. In some teleosts thyroidal status may be high during vitellogenesis, consistent with a role in this process. In Hypseleotris, high levels of thiourea inhibited vitellogenesis. However, this effect may have been due to thiourea toxicity (MacKay, 1973). In salmonids, circulating T3 is low during vitellogenesis and Kwon et al. (1993) found that Ts ( 10e7 M) did not enhance significantly the Ez-induced VTG synthesis by male rainbow trout hepatocytes in vitro. Tq, but not T3, exerted a modest but significant stimulation of VTG uptake by rainbow trout denuded oocytes examined in vitro (Shibata et al., 1993). In goldfish (Bailey, 1957), spotted dogfish (Woodhead, 1969b), Atlantic cod (Gadus morhua, Gadidae) (Woodhead, 1969a) and rainbow trout (Takashima et al., 1972), Tq
178
Cyr and EaZes
consistently depressed either plasma VTG or Es elevation of plasma VTG. Possibly T4 enhances VTG uptake from plasma into eggs, and thereby depletes plasma VTG levels. A few studies indicate that TH may be required in the final stages of oocyte maturation, and in some instances a natural elevation in thyroidal status occurs at this time. In the carp (Cyprinus carpio, Cyprinidae) treatment of post-vitellogenic ovarian fragments with DHP was more effective in producing mature oocytes in the presence of Ts (Epler and Bieniarz, 1983); T3 alone was modestly effective. In Anabas, T3, and to a lesser extent Tb enhanced cholesterol conversion to progesterone through a mechanism depending on specific protein synthesis (Sen and Bhattacharya, 1981; Kaul and Bhattacharya, 1988; Guin et al., 1993). Dickhoff et al. (1989) and Sullivan et al. (1989) showed that for rainbow trout, T3 in vitro increased GTH (SG-GlOO) stimulation of germinal vesicle breakdown (GVBD) through DHP production. Ts was less effective at high concentrations and was most effective at low GTH levels. If T3 acts to inhibit PDE and the breakdown of CAMP (Cyr and Eales, 1989a), it would have greater scope for action at low GTH levels. Because T3 levels are usually modest at GVBD in salmonids, and because GTH levels are high at this time, Sullivan et al. (1989) have queried the physiological relevance of this phenomenon. Mylonas et al. (1994) have suggested that in species such as the brown trout with a high natural plasma T3 level, T3 administration may not enhance GnRH action on ovulation and furthermore may have deleterious effects on the offspring. In conclusion, TH are undoubtedly involved in several species in synergizing with GTH during oocyte maturation. This seems to be particularly so in the early stages of egg development. In some instances this may involve TH interaction with nuclear receptors to induce protein synthesis. However, in trout, Ts appears to act directly on ovarian follicles to enhance GTH-stimulated CAMP production. Ts may rapidly stimulate thecal cells to inhibit PDE activity by a mechanism independent of new protein synthesis, and possibly by a membrane-regulated Ca2+ movement. Ts also acts on granulosa cells and increases conversion of T to Es. Circulating TH levels rise during early ovarian development when GTH levels are low, and T3 may be necessary at this time to enhance the GTH signal and initiate oogenesis and Es production leading to vitellogenesis. Thyroid hormones
within
the egg
Total T4 and T3 concentrations have been measured by radioimmunoassay in extracts from whole unfertilized and fertilized eggs and egg yolk of salmonids (Kobuke et aZ., 1987; Tagawa and Hirano, 1987, 1990; Greenblatt et al., 1989; Leatherland et al., olivaceus, 1989a,b; DeJesus and Hirano, 1992); Japanese flounder (Paralichthys Pleuronectidae) (Tanangonan et al., 1989; Tagawa et al., 1990a); striped bass (Morone saxatilis, Serranidae) (Parker and Specker, 1990); conger eel (Conger conger, Anguillidae) (Yamano et al., 1991); red sea bream (Pagrus major, Sparidae) (Kimura et al., 1992); black sea bream (Tanaka et al., 1991); tilapia (Oreochromis mossambicus, Cichlidae) (Reddy et al., 1992; Weber et al., 1992); and rabbitfish (Siganus guttatus, Siganidae) (Ayson and Lam, 1993). Concentrations of TH vary between species and also within species such as tilapia (Reddy et al., 1992; Weber et al., 1992). There is a trend for egg TH levels to be higher in freshwater as opposed to saltwater species (Tagawa et al., 1990b). As anticipated, the source of the egg TH appears to be from the maternal circulation, because TH injection into gravid females enhances TH levels in eggs (Brown
Thyroid and reproduction
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in fish
et al., 1987; Ayson and Lam, 1993). TH accumulation occurs progressively through egg development but the profile of change with time depends on species, and may not always relate directly to plasma TH levels (Leatherland et al., 1989b; Weber et al., 1992). The mechanism of TH uptake into eggs has not been established and several processes may be involved (Weber et al., 1992). Firstly, some TH will undoubtedly enter eggs on account of the lipophilic properties of TH and their low molecular size. TH may also be transported into eggs by mechanisms comparable to those described for the trout hepatocyte (Riley and Eales, 1993, 1994). The retention of TH inside the egg could be enhanced by TH binding to egg constituents, including VTG or its derivatives. TH may also be taken up into eggs bound to VTG or some other plasma protein. There is no direct evidence to show that TH are transported into the eggs with VTG. Indeed Flett and Leatherland (1989a), using electrophoresis, concluded that whilst Es induced VTG synthesis it did not affect serum binding sites for either Ta or T4 in rainbow trout. However, Tg binds to VTG in plasma of both goldfish (MacKenzie, 1986) and channel catfish (MacKenzie et al., 1987). Furthermore, using gel chromatography, we found that a small amount of Th but not Ts, did bind to Esinduced plasma VTG in rainbow trout (Cyr and Eales, 1989b, 1992). Also, in coho salmon, Hara and Sullivan, using immunoprecipitation, reported that [lz51]T4 coprecipitated with VTG (Specker and Sullivan, 1994). Thus VTG is a candidate molecule for transporting T4 in plasma and into eggs. Es induces other changes in plasma TH-binding proteins, including an increase in lipoproteins (Babin, 1992; Cyr and Eales, 1992). In the winter flounder, high-density lipoproteins, with molecular weights similar to those which bind T 4 are taken up by eggs during vitellogenesis (Nagler and Idler, 1990) and might also transport T4 into eggs. The role of TH in eggs has been the subject of considerable recent speculation, and there are several possible physiological consequences. Firstly, there may be no advantage, because TH accumulation in the egg may be the fortuitous outcome of the lipophilic properties, diffusibility and binding features of TH. Secondly, sequestered TH may provide, following its general deiodination, an important source of iodide for use by the developing thyroid. The greater abundance of TH in eggs of freshwater fish as opposed to saltwater fish (Tagawa et al., 1990b) supports this view. Although iodide may not be limiting in later developmental stages possessing gills, which can gain iodide from the surrounding water (Eales and Brown, 1993), it might be limiting in prehatching stages. Thirdly, TH may play some permissive role in early development prior to endogenous TH production. While effects of TH on larval development are well established (Inui and Miwa, 1985; Reddy and Lam, 1992) a post-fertilization role of maternally derived TH in influencing very early development or in enhancing survival is less clear (Leatherland et al., 1989a; Tagawa et al., 1990a; Ayson and Lam, 1993). However, positive effects of TH on survival and swimbladder inflation were reported in the striped bass (Brown et al., 1988, 1989; Brown and Bern, 1989). Possibly some species may require a minimal level of TH for early growth and development; it is more difficult to envision a physiological role for supranormal TH levels in eggs, unless the eggs are commonly in a TH-deficient state. This is unlikely from the standpoint of natural selection.
Effects of reproductive
status on thyroidal
function
Effects of reproductive
status on the thyroidal
system have been determined
from
180
Cyr and EaZes histological or ultrastructural changes in pituitary thyrotropes or thyroid tissue and from radiochemical indices of thyroid status. Experimental procedures have involved (a) surgical or irradiation gonadectomy, or administration of a gonadotrope inhibitor to suppress reproductive function, and (b) administration of GnRH, GTHs or sex steroids to simulate enhanced reproductive activity. Gonadectomy did not modify thyroid histological appearance in senile kokanee salmon, 0. nerka (Robertson and Wexler, 1962) or Channa (Belsare, 1966), but led to suppression of thyroidal status in anadromous sockeye salmon (Donaldson and McBride, 1974) and Anabas (Chakraborti et al., 1983). In Poecilia latipinna (Poeciliidae), ovariectomy enhanced thyrotrope activity (young and Ball, 1979). Methallibure, an inhibitor of GTH secretion in fish (Hoar et al., 1967; Pandey, 1970), consistently decreased not only gonadotrope activity, but also thyrotrope and thyroidal activity in taxonomically diverse species (Pandey, 1970; Pandey and Leatherland, 1970; MacKay, 1973; Gan-Chaudhuri and Rao, 1988). Direct actions of methallibure on thyrotropes or thyroid tissue cannot be excluded (Pandey and Leatherland, 1970; MacKay, 1973). However, methallibure was effective in adults and not in juveniles (Pandey and Leatherland, 1970), suggesting some action on the thyroid through modification of gonadal function. The effects of GnRH or GTHs on the fish thyroidal system are varied. Donaldson and McBride (1974) administered GTH (SG-GlOO) to gonadectomized sockeye salmon and found an increase in thyroid epithelial cell height. MacKenzie et al. (1984) injected mammalian GnRH-pimidazole into goldfish without changing plasma T3 or T4 levels. In the sea lamprey (Petvomyzon marinus, Petromyzontidae), plasma Tq is increased by both GnRH and GTH (Sower et al., 1985). This may stem from the stimulation of gonadal function but, as the authors suggest, GnRH could stimulate the thyrotropes. GTH might also exert some action on the thyroid but effects of fish GTH on the thyroid appear unlikely because in the medaka GTH fails to enhance thyroidal Tq release in vitro (Okimoto et al., 1991), and in Anabas thyroid suppression due to ovariectomy cannot be offset by GTH injection (Chakraborti et al., 1983). Several workers have observed the effects of oestrogens, primarily Ea, on the pituitary-thyroid axis of fish. The types of effects exerted by Es depend on species. In several Indian freshwater teleosts, Es consistently enhances thyroidal status as judged by a variety of criteria (Singh, 1968, 1969a,b; Chakraborti et al., 1983; Jumaluddin et al., 1983; Bandyopadhyay et al., 1991). On the other hand, in rainbow trout, goldfish, eels and medaka (Sage and Bromage, 1970b; Olivereau and Olivereau, 1979; Olivereau et al., 1981; Young and Ball, 1979; Leatherland, 1985; Cyr et al., 1988b; Flett and Leatherland, 1989a,b; Yamada et al., 1993a), E2 depresses criteria of thyroidal status and plasma Ts, accompanied by no change or a decrease in plasma Tq. These species differences do not appear to be due to use of different techniques for determining thyroidal status. In only a few cases was the thyroid system unresponsive to Es treatment (van Overbeeke and McBride, 1971; Milne and Leatherland, 1978). This may represent in these instances the limited scope for further thyroidal depression due to hypothyroidism associated with fasting (Milne and Leatherland, 1980). In contrast, the effects of the androgens, primarily T and methyltestosterone, are more consistent between species; they tend to elevate thyroidal status (Singh, 1968, 1969a,b; Hunt and Eales, 1979; Fagerlund et al., 1980; Leatherland, 1985; Leatherland and Sonstegard, 1980b; Ikuta et al., 1985; MacLatchy and Eales, 1988; Shelbourn et al, 1992;
Thyroid and reproduction
in fish
181
Schwerdtfeger, 1979; Yamada et al., 1993a,b). In only a few instances did androgens not seem to affect plasma TH levels (Milne and Leatherland, 1978; Leatherland, 1985). Steroid hormones probably influence thyroidal status at a variety of levels involving changes in peripheral metabolism of TH (see below). Nevertheless, based on several studies, steroid hormones appear to exert direct effects on fish thyroid tissue independent of TSH (Singh, 1968, 1969a,b, 1978; Sage and Bromage, 1970b; Jumaluddin et al., 1983; Chakraborti and Bhattacharya, 1984; Bandyopadbyay et al., 1991). Although gonadal steroids can exert dramatic and species-consistent effects on the thyroid function, physiological interpretations are difficult. Many studies involved use of immature fish of both genders, and probable responses of adult fish in various stages of the reproductive cycle were inferred. Furthermore, doses of steroids have not always fallen in a physiologically relevant range. While most early studies focused on the actions of gonadal steroids on the brainpituitary-thyroid axis, more recent studies have involved the influence of steroids on the peripheral metabolism of TH, and TH actions on target tissues. Es decreases epithelial cell height in some teleosts without modifying circulating T4 levels (Olivereau et al., 1981; Leatherland, 1985) suggesting that Es also depresses T4 clearance. To address this possibility we determined the effects of Es on plasma T4 and its kinetics in immature rainbow trout of both genders (Cyr and Eales, 1990). Es consistently decreased T4 plasma clearance rate (2348%) and Tq secretion/degradation rate (3341%). In addition, [1251]T4 conversion to 1251- and [1251]Ta were depressed, indicating reduced outer-ring (5’) deiodination of T4 to T s. In support of this, although the T3 plasma clearance rate was unaltered by Ez, the T3 plasma appearance rate was depressed by 63%. Analyses of liver and bile indicated no alteration in biliary excretion of either T4 or Ta. Thus, much of the effect of Es to depress T4 secretion/degradation rate was probably caused by decreased conversion of T4 to Ta in peripheral tissues. This was confirmed by in vitro measurements. Monodeiodination of T4 to Ts was assessed on the hepatic microsomal fractions incubated with [1251]T4 at the trout acclimation temperature of 12 “C (Cyr et al., 1988b). Prior E2 injection greatly depressed the 5’-monodeiodinase V,,, (level of functional enzyme) with no major change in Km (enzyme-substrate affinity), indicating that Ez decreased the amount of functional deiodinase in liver. This action of Es to suppress T4 to Ta conversion has since been confirmed in the rainbow trout by Flett and Leatherland (1989b) and Okimoto et al. (1991), and in the lamprey Geotvia by Leatherland et al. (1990). Unlike Es, androgens may enhance fish peripheral TH metabolism. In immature rainbow trout, T and its derivatives increased T4 degradation rate and in vivo T4 to Ts conversion (Hunt and Eales, 1979). In Arctic charr (Salvelinus alpinus, Salmonidae), T increased V,,, of 5’-monodeiodinase without altering Km (MacLatchy and Eales, 1988). However, in rainbow trout, Yamada et al. (1993a,b) reported T4 5’-deiodinase insensitivity to the doses of T which they used. Because the relative proportion of E2 and T may change during the reproductive cycle, and because both hormones have the potential to influence the peripheral production of Ts in opposite ways, it is of future interest to study effects of the plasma Es/T ratio in regulating thyroidal status in adult female rainbow trout and in other species. TH are highly insoluble in water and their transport is facilitated by plasma proteins which non-covalently bind TH and increase the latter’s effective solubility (McNabb, 1992). Levels of these TH-binding proteins can change in mammals, altering plasma
182
Cyr and Eales total TH concentrations, proportion of plasma TH in free form, plasma TH kinetic parameters and availability of TH for cell uptake. However, for T4 at least, the absolute level of free hormone may remain unchanged due to compensatory feedback adjustments by the brain-pituitary-thyroid axis. For example, during human pregnancy, elevated plasma EZ levels stimulate synthesis of T4-binding globulin, increase total T4 level and proportion of bound T4 in the plasma, but cause minor change in free TJ concentration. TH in fish are also bound to plasma proteins. Based on electrophoretic (Falkner and Eales, 1973) and competitive-binding (Eales, 1987) analyses, salmonid plasma contains a high-affinity/low-capacity class of sites, and a low-affinity/high-capacity class of sites; each class is capable of binding both Tg and Ts. There may also be a third site class specific for T3 (Eales, 1987; Cyr and Eales, 1989b). When immature trout of either gender are injected with E2, the proportion of total circulating T4 or T3 in the free dialysable form is decreased, indicating some changes in TH-protein sites (Cyr and Eales, 1989b, 1992). Competitive-binding studies indicated that the Ea increased the capacity of the low-affinity site, and this was confirmed by gel filtration using either [1251]T4 or [ 1251]Ts (Cyr and Eales, 1989b, 1992). The two main TH-binding proteins corresponded to molecular sizes of 150 kDa and 55 kDa. Analyses with saturating TJ or Ts levels indicated the 55 kDa fraction as the high-affinity site and the 150 kDa fraction as the low-affinity site. The latter site capacity was elevated by Ea. E2 also induced VTG synthesis and increased the plasma lipoprotein fraction. Both of these fractions bound Tq, but not Ta, and hence may play a role in the transport and cellular (oocyte) uptake of T4 (see ‘Thyroid Hormones within the egg’). The above studies involved Ez injection into immature trout of both genders. It is important to conduct similar studies on adult females. E2 may also influence properties of putative TH receptors in target tissues. Bres et al. (1990) showed that following E2 injections, the maximum binding capacity (MBC), or number of hepatic nuclear Ta receptors, was decreased, with no change in kd (affinity of T3 for receptor sites). T3 MBC also decreases under conditions in which plasma Ta is lowered (Bres et al., 1990), so this effect of E2 might be explained by its simultaneous action to depress plasma Ts (Cyr et al., 1988b). However, in trout injected with EP on days 0 and 3 and sampled on day 11, plasma Ts had already returned to normal, but there was still a decrease in Ts MBC. This suggests that Es may have a prolonged effect on T3 MBC not explained entirely by its action to also depress plasma T3. As molecular markers regulated by TH-receptor-induced gene transcription become available, it will be interesting to correlate the MBC of the TH receptor with cellular actions of Ts in Ez-treated fish. While there are complications in interpretation due to possible differences in species responses, steroid doses, mode of steroid administration, and stage in the annual or breeding cycle when steroids were administered, certain generalizations emerge. In many species E2 suppresses thyroidal status, and this is achieved by its action at a multitude of levels, ranging from direct actions on the thyroid and possibly the thyrotropes, to actions on the synthesis of TH-binding proteins in plasma, to hepatic T4to-TO converting enzymes, and to abundance of T3-binding putative nuclear receptors. In these particular species, thyroidal status generally decreases during vitellogenesis as E2 levels rise. In contrast, in several Indian freshwater teleosts, Es stimulates thyroidal status at a number of levels; in these species, thyroidal status tends to increase during
Thyroid and reproduction
in fish
183
vitellogenesis. Thus in species where TH may have a role in vitellogenesis, Ez does not inhibit thyroidal status; however, in species where TH play no clear-cut role in vitellogenesis, Ea contributes to maintenance of depressed thyroidal status. Androgens tend instead either to enhance thyroidal status or to exert no effect. Again they may act at several levels of the thyroidal system. Biological
implications
Reproductive biology and reproductive strategy vary greatly between fish taxa. For example, semelparous anadromous salmonids or catadromous eels breed but once, with maximum commitment of energy to this single reproductive event; some ovoviviparous elasmobranchs have a long reproductive cycle (22 month gestation in Squalus acanthias); temperate teleosts usually breed once a year; some ovoviviparous or viviparous tropical species may produce young in small numbers at regular intervals, or have a breeding cycle every few weeks. These fundamental differences in breeding biology between fish species will be accompanied by major differences in timing of secretion of pituitary and gonadal sex steroids for both genders. Because of differences in reproductive endocrinology, relationships between thyroid function and reproductive events are likely to be highly species specific. Furthermore, TH are closely associated with changes in energy balance (Eales, 1979, 1988; Dickhoff et al., 1989; Leatherland, 1994). Thus the timing and extent of energetic demands are likely to be very different between a one-time reproducer such as the sockeye salmon, and a tropical cyprinodont producing a small number of young on a frequent and regular basis. For these reasons, sweeping generalizations across all taxa relating reproductive and thyroid function are unwarranted. Also, simplistic general correlations between indices of thyroidal status and indices of reproductive status (GSI) based on an entire seasonal cycle may be misleading; we emphasize that a functional relationship may apply only over a particular phase of the gonadal cycle. One consistent feature for most fish is a significant level of thyroid activity at the very early vitellogenic stages of gonadal development (Eales, 1979). Both in vivo and in vitro experimental studies, employing GTH forms and TH in combination, indicate that while TH may not by themselves be effective, they facilitate gonad-stimulating actions of GTH. For example, TH tend to exert their greatest ovarian effects at low GTH levels, supporting the view that TH are required for initiation of ovarian development and commitment to reproduction. Thyroidal status is closely correlated with energy balance in fish (Eales, 1988; Dickhoff et al., 1989; Leatherland, 1994). Consequently, thyroidal status may indicate the metabolic readiness of fish to engage in energy-demanding reproduction. TH may achieve their effect by enhancing the potency of the low GTH levels produced at the onset of preparation for reproduction. However, once a commitment to reproduction has been made, TH may: be unimportant for gonadal development in some semelparous species (Cyr et al., 1988a; Leatherland, 1994). Indeed, plasma TH levels, and particularly Ts levels, fall dramatically in salmonids accompanying gonadal growth, vitellogenesis and spermatogenesis, and no clear-cut role of TH has been established at this time. The progressive fall in thyroidal status during this phase of the cycle may reflect the decrease in metabolic reserves, accentuated in some instances by cessation of feeding (McBride, 1967), and upstream migration. Some TH may also be withdrawn from circulation into
184
Cyr and Eales the developing egg. However, there is also strong evidence that rising Es levels depress salmonid thyroid function and plasma Ta during this phase. One consequence of the multifactorially depressed thyroidal status may be inhibition of somatic growth which competes with energy-demanding gonadal growth (Wootton, 1984). In contrast, in some iteroparous fish, TH levels may increase during vitellogenesis. This again could reflect a role of TH as indicators of metabolic state; TH may provide the signal that there are adequate metabolic reserves for gonadal development to continue to the next stage. In salmonids and some other species, there is also mounting experimental evidence that TH are associated in a permissive way with final stages of gonadal maturation, involving the production of DHP and GVBD in females, and spermiation in males. In several instances, TH levels may increase at this time, and in some taxa, such as salmonids, may be higher in males. The levels of TH may again relate to the metabolic state and the potential energetic reserves of the fish. The physical act of spawning is energetically demanding for both genders and may be particularly demanding if nestguarding is involved. Although thyroidal status in prespawners may be at a much lower level than at other times of year, it may still provide a relative index of metabolic readiness to complete spawning. Thus TH level may be important also in contributing to the timing of final gonadal development and spawning events. Thyroidal status, as judged by a variety of criteria, is low in almost all cases after spawning, but usually increases to pre-reproductive levels shortly thereafter. This increase is often correlated with resumption of somatic growth and in rainbow trout is associated with an increase in plasma T, which is known to exert anabolic actions. Furthermore, androgens can increase Ta production and plasma T3, while androgens and GH can act synergistically to promote somatic growth (Higgs et al., 1982). The possible relationships between reproductive and thyroidal systems in fish have been recognized by several previous investigators (see Introduction). Some workers (Leatherland 1993, 1994) have proposed that the links between these two systems are tenuous, but it appears to us that despite the varied life histories and reproductive strategies of different fish taxa, there is indeed a close relationship between on the one hand the gonadotrophic and steroid hormones which specifically regulate reproductive events, and on the other hand the hormones, such as TH, which respond to changes in the metabolic state of the fish. By a complex interplay these endocrine systems may contribute to regulation of competing growth and reproductive processes, and ensure that the latter proceed under conditions where the energetic resources render reproduction potentially viable. Summary Temporal profiles of thyroidal status and reproductive function have been compared for many species of teleost and non-teleost fish of both genders. Despite major interspecies differences in reproductive biology and reproductive strategy, and problems associated with evaluation of thyroidal status, significant temporal relationships exist for most species between thyroidal status and gonadal state over at least certain phases of the reproductive cycle. While suggestive, these general correlations do not establish any causal relationship between the two systems. Experimental studies carried out mainly on female teleosts, but including species with different reproductive strategies, indicate that a certain thyroidal status may be
Thyroid and reproduction
185
in fish
required for early gonadal (oocyte) development and reproduction to proceed. For the rainbow trout, Ts is more active in this regard than T4. T3 is particularly effective at low GTH concentrations, and may play a key role at the onset of gonadal development and commitment to reproduction. One component of Ts action involves cellular mechanisms independent of de nova protein synthesis. Ts may achieve this effect by blocking PDE and thereby decreasing the rate of degradation of GTH-generated intracellular CAMP In other species, THs may be required during the later stages of vitellogenesis. At this stage TH actions seem to depend on de nova protein synthesis. Final oocyte maturation and possibly spawning behaviour may also be influenced by TH even though the TH plasma levels are low at this time. After reproduction there is usually an increase in thyroidal status associated with the growth phase of the life cycle. In several species, including salmonids, there is a reciprocal relationship between thyroidal status and plasma E2 levels. Experimental data show that E2 contributes to the depression in plasma Ta by modifying several aspects of the peripheral metabolism of TH and inhibiting hepatic 5’-deiodinase (5’D) converting T4 to Ts. T and other androgens tend to enhance T s formation and thyroidal status, and as such may contribute to somatic growth following reproduction (Fig. 4). TH are associated with metabolism and energy balance; reproductive hormones are
HYPOTHALAMUS
BINDING
..-+
T3
T4
c.’
+.-+..I *..-
,’
.
*’
t
TARGET ORGAN J-4
5D + T3
NUCLEAR
L
4’
.’
PROTEINS
GENE
Q.”
RECEPTOR t EXPRESSION
LIVER
E2
,l *’ a’
+ NUCLEAR
GENE
RECEPTOR 4 EXPRESSION
Fig. 4. Possible sites of interaction and effects of thyroid hormones on the reproductive effects of gonadal steroids on thyroidal function in fish. Abbreviations as in Table 1.
system and
186
Cyr and Eales
responsible for the development of gonads and reproduction. Because reproduction is energetically demanding, direct and indirect interactions between the two systems are anticipated. The general role of Ta may be to signal metabolic competence to proceed with the next stage of reproduction. The most fundamental specific role may be to enhance GTH actions in initiating early gonadal development, but in some species TH may play permissive roles in vitellogenesis, final gonadal maturation and spawning. However, TH are also growth-promoting. At certain phases of the reproductive cycle, when energy reserves are being depleted and energy is being channelled to the gonads, it may be advantageous for steroid hormones (Ea) to contribute to suppression of thyroidal status. Clearly, sweeping generalizations concerning the relationship between reproductive function and thyroidal status are likely to be misleading and unrealistic. Because of the great differences in reproductive biology, strategies of energy allocation, environment and behaviour between fish species, it is necessary to investigate each taxon in its own right. Acknowledgements
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Accepted 12 September 1995
