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Endocrine manipulations of spawning in cultured fish: from hormones to genes

Identifieur interne : 001506 ( Istex/Corpus ); précédent : 001505; suivant : 001507

Endocrine manipulations of spawning in cultured fish: from hormones to genes

Auteurs : Yonathan Zohar ; Constantinos C. Mylonas

Source :

RBID : ISTEX:7AD9FA8759B62D9D615F6D5BD0A677853FBB88F4

Abstract

Almost all fish reared in captivity exhibit some form of reproductive dysfunction. In females, there is often failure to undergo final oocyte maturation, ovulation and spawning; while in males milt production may be reduced and of low quality. These dysfunctions are due to the fact that fish in captivity do not experience the conditions of the spawning grounds, and as a result there is a failure of the pituitary to release the maturational gonadotropin, luteinizing hormone (LH). Reproductive hormones have been utilized since the 1930s to stimulate reproductive processes and induce ovulation/spermiation and spawning. The first methods employed freshly ground pituitaries collected from reproductively mature fish, which contained gonadotropins (mainly LH) and induced steroidogenesis and gonadal maturation. Eventually, purified gonadotropins became available, both of piscine and mammalian origin, e.g., carp or salmon gonadotropin, and human chorionic gonadotropin. In the 1970s, spawning induction methods begun employing the newly discovered gonadotropin-releasing hormone (GnRH), which induces the secretion of the fish's own gonadotropin from the pituitary, thereby overcoming the endocrine failure observed in captive broodstocks. Development of highly potent, synthetic agonists of GnRH (GnRHa) constituted the next generation of hormonal manipulation therapies, and created a surge in the use of hormones to control reproductive processes in aquaculture. The most recent development is the incorporation of GnRHa into polymeric sustained-release delivery systems, which release the hormone over a period of days to weeks. These delivery systems alleviate the need for multiple treatments and induce (a) long-term elevation in sperm production and (b) multiple spawning in fish with asynchronous or multiple-batch group-synchronous ovarian physiology. Based on the recent discovery of GnRH multiplicity in fish and the increasing understanding of its functional significance, new GnRH agonists can be designed for more potent, affordable and physiologically-compatible spawning induction therapies. Future strategies for improved spawning manipulations will be based on understanding the captivity-induced alterations in the GnRH system, and on new approaches for their repair at the level of GnRH gene expression and release.

Url:
DOI: 10.1016/S0044-8486(01)00584-1

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ISTEX:7AD9FA8759B62D9D615F6D5BD0A677853FBB88F4

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<div type="abstract" xml:lang="en">Almost all fish reared in captivity exhibit some form of reproductive dysfunction. In females, there is often failure to undergo final oocyte maturation, ovulation and spawning; while in males milt production may be reduced and of low quality. These dysfunctions are due to the fact that fish in captivity do not experience the conditions of the spawning grounds, and as a result there is a failure of the pituitary to release the maturational gonadotropin, luteinizing hormone (LH). Reproductive hormones have been utilized since the 1930s to stimulate reproductive processes and induce ovulation/spermiation and spawning. The first methods employed freshly ground pituitaries collected from reproductively mature fish, which contained gonadotropins (mainly LH) and induced steroidogenesis and gonadal maturation. Eventually, purified gonadotropins became available, both of piscine and mammalian origin, e.g., carp or salmon gonadotropin, and human chorionic gonadotropin. In the 1970s, spawning induction methods begun employing the newly discovered gonadotropin-releasing hormone (GnRH), which induces the secretion of the fish's own gonadotropin from the pituitary, thereby overcoming the endocrine failure observed in captive broodstocks. Development of highly potent, synthetic agonists of GnRH (GnRHa) constituted the next generation of hormonal manipulation therapies, and created a surge in the use of hormones to control reproductive processes in aquaculture. The most recent development is the incorporation of GnRHa into polymeric sustained-release delivery systems, which release the hormone over a period of days to weeks. These delivery systems alleviate the need for multiple treatments and induce (a) long-term elevation in sperm production and (b) multiple spawning in fish with asynchronous or multiple-batch group-synchronous ovarian physiology. Based on the recent discovery of GnRH multiplicity in fish and the increasing understanding of its functional significance, new GnRH agonists can be designed for more potent, affordable and physiologically-compatible spawning induction therapies. Future strategies for improved spawning manipulations will be based on understanding the captivity-induced alterations in the GnRH system, and on new approaches for their repair at the level of GnRH gene expression and release.</div>
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<note type="content">Fig. 1: Mean titers (±s.e.m.) expressed as optical density (OD) of hCG antibodies in the plasma of striped bass at different times after injection with hCG (n=4) or saline (n=6). Two-year-old striped bass weighing (450 g) were held in 2.2 m3 tanks at 18°C. On days 0 and 60, one group was injected intra-muscularly with 500 IU kg−1 body weight of hCG (Sigma) dissolved in 0.9% saline, while a control group was injected with saline alone (0.5 ml kg−1). The concentration of hCG antibodies in the plasma was measured using an hCG non-competitive, solid phase ELISA. The mean anti-hCG titers were significantly elevated in response to the hCG injections (two-way ANOVA, P≤0.0001). (Y. Zohar and S. Wehage, unpublished).</note>
<note type="content">Fig. 2: Mean (±s.e.m.) plasma hormone levels (ng ml−1) and cumulative % oocyte maturation of cultured striped bass (n=7) after two injections (arrows) of GnRHa (15 μg kg−1) or saline during the spawning season (April). Fish (4–8 kg) were maintained in a flow-through system supplied with Chesapeake Bay water (4–2 g l−1 salinity; 7–18°C) and had a mean oocyte diameter of 850 (±20) μm at the start of the experiment. With the exception of plasma 17,20β,21-P, all hormone profiles were significantly changed by the GnRHa treatment (ANOVA, P≤0.05). The horizontal hatched bar indicates the time when atretic oocytes could be seen in the biopsies. Most GnRHa-injected females reached the peripheral GV stage, but only one ovulated within the duration of the study.</note>
<note type="content">Fig. 3: Mean (±s.e.m.) plasma hormone levels of cultured female white bass at various stages of final oocyte maturation (FOM), induced by treatment with a GnRHa-implant (EVAc; 50 μg kg−1). Data from individual fish were pooled according to maturation stage (sample sizes are shown in parentheses) as follows: after GnRHa treatment but before the onset of FOM (pre-FOM), germinal vesicle migration (mGV), after GV breakdown (GVBD) and after ovulation (post-OV). Sample means that were significantly different from the previous maturation stage are indicated by asterisks (ANOVA, DNMR; *P≤0.05, **P≤0.01) (from Mylonas et al., 1997b).</note>
<note type="content">Fig. 4: Daily egg production (ml tank−1) of red porgy (Pagrus pagrus) in response to treatment with GnRHa in the form of a single injection (15 μg kg−1) or a sustained-release delivery system (Fad-sa microspheres; 50 μg kg−1). The experiments were carried out at the Meneou Marine Aquaculture Research Station, Fisheries Department, Republic of Cyprus during the Spring spawning season of 1997. Each tank contained five females and seven males, of mean (±S.D.) weight of 1.4 (±0.3) and 1.1±(0.2) kg, respectively.</note>
<note type="content">Fig. 5: Mean (±s.e.m.) total expressible milt production of European seabass (Dicentrarchus labrax) treated with GnRHa in various ways. Fish (n=8) were treated with either a single GnRHa injection (25 μg kg−1), GnRHa microspheres (Fad-sa; 50 μg kg−1) or a GnRHa implant (EVAc; 50 μg kg−1). Fish treated with GnRHa produced significantly higher amounts of milt than controls for the first 7 days after treatment (ANOVA, DNMR, P≤0.05). Moreover, fish treated with GnRHa-delivery systems continued to produce higher amounts of milt for up to 35 days after treatment (ANOVA, DNMR, P≤0.05). (from Sorbera et al., 1996).</note>
<note type="content">Fig. 6: Mean (n=2) daily in vitro release of hCG from a poly[ortho-acetate] delivery system (A), and plasma hCG levels (n=2) and cumulative % ovulation of striped bass (n=5) treated with this delivery system at a dose of 3600 IU hCG kg−1 (B).</note>
<note type="content">Table 1: Representative applications of hormonal manipulations for the induction of final maturation and spawning of male (M) and female (F) broodstock using various gonadotropin (GtH) preparations</note>
<note type="content">Table 2: Representative applications of hormonal manipulations with agonists of gonadotropin-releasing hormone (GnRHa) for the induction of final maturation and spawning of male (M) and female (F) broodstocks</note>
<note type="content">Table 3: Representative applications of sustained-release GnRHa-delivery systems for the induction of final maturation and spawning of male (M) and female (F) broodstocks</note>
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<ce:doi>10.1016/S0044-8486(01)00584-1</ce:doi>
<ce:copyright type="full-transfer" year="2001">Elsevier Science B.V.</ce:copyright>
</item-info>
<head>
<ce:title>Endocrine manipulations of spawning in cultured fish: from hormones to genes</ce:title>
<ce:author-group>
<ce:author>
<ce:given-name>Yonathan</ce:given-name>
<ce:surname>Zohar</ce:surname>
<ce:cross-ref refid="COR1">*</ce:cross-ref>
<ce:cross-ref refid="AFF1">
<ce:sup>a</ce:sup>
</ce:cross-ref>
<ce:e-address>zohar@umbi.umd.edu</ce:e-address>
</ce:author>
<ce:author>
<ce:given-name>Constantinos C</ce:given-name>
<ce:surname>Mylonas</ce:surname>
<ce:cross-ref refid="AFF2">
<ce:sup>b</ce:sup>
</ce:cross-ref>
<ce:e-address>mylonas@imbc.gr</ce:e-address>
</ce:author>
<ce:affiliation id="AFF1">
<ce:label>a</ce:label>
<ce:textfn>Center of Marine Biotechnology, University of Maryland Biotechnology Institute, 701 E. Pratt Street, Baltimore, MD 21202, USA</ce:textfn>
</ce:affiliation>
<ce:affiliation id="AFF2">
<ce:label>b</ce:label>
<ce:textfn>Institute of Marine Biology of Crete, P.O. Box 2214, Iraklion, Crete 71003, Greece</ce:textfn>
</ce:affiliation>
<ce:correspondence id="COR1">
<ce:label>*</ce:label>
<ce:text>Corresponding author. Tel.: +1-410-234-8803; fax: +1-410-234-8896</ce:text>
</ce:correspondence>
</ce:author-group>
<ce:date-received day="1" month="10" year="2000"></ce:date-received>
<ce:date-accepted day="31" month="12" year="2000"></ce:date-accepted>
<ce:abstract>
<ce:section-title>Abstract</ce:section-title>
<ce:abstract-sec>
<ce:simple-para>Almost all fish reared in captivity exhibit some form of reproductive dysfunction. In females, there is often failure to undergo final oocyte maturation, ovulation and spawning; while in males milt production may be reduced and of low quality. These dysfunctions are due to the fact that fish in captivity do not experience the conditions of the spawning grounds, and as a result there is a failure of the pituitary to release the maturational gonadotropin, luteinizing hormone (LH). Reproductive hormones have been utilized since the 1930s to stimulate reproductive processes and induce ovulation/spermiation and spawning. The first methods employed freshly ground pituitaries collected from reproductively mature fish, which contained gonadotropins (mainly LH) and induced steroidogenesis and gonadal maturation. Eventually, purified gonadotropins became available, both of piscine and mammalian origin, e.g., carp or salmon gonadotropin, and human chorionic gonadotropin. In the 1970s, spawning induction methods begun employing the newly discovered gonadotropin-releasing hormone (GnRH), which induces the secretion of the fish's own gonadotropin from the pituitary, thereby overcoming the endocrine failure observed in captive broodstocks. Development of highly potent, synthetic agonists of GnRH (GnRHa) constituted the next generation of hormonal manipulation therapies, and created a surge in the use of hormones to control reproductive processes in aquaculture. The most recent development is the incorporation of GnRHa into polymeric sustained-release delivery systems, which release the hormone over a period of days to weeks. These delivery systems alleviate the need for multiple treatments and induce (a) long-term elevation in sperm production and (b) multiple spawning in fish with asynchronous or multiple-batch group-synchronous ovarian physiology. Based on the recent discovery of GnRH multiplicity in fish and the increasing understanding of its functional significance, new GnRH agonists can be designed for more potent, affordable and physiologically-compatible spawning induction therapies. Future strategies for improved spawning manipulations will be based on understanding the captivity-induced alterations in the GnRH system, and on new approaches for their repair at the level of GnRH gene expression and release.</ce:simple-para>
</ce:abstract-sec>
</ce:abstract>
<ce:keywords class="keyword">
<ce:section-title>Keywords</ce:section-title>
<ce:keyword>
<ce:text>Induced spawning</ce:text>
</ce:keyword>
<ce:keyword>
<ce:text>GnRH</ce:text>
</ce:keyword>
<ce:keyword>
<ce:text>GnRH genes</ce:text>
</ce:keyword>
<ce:keyword>
<ce:text>Gonadotropin</ce:text>
</ce:keyword>
<ce:keyword>
<ce:text>Delivery systems</ce:text>
</ce:keyword>
<ce:keyword>
<ce:text>Broodstock management</ce:text>
</ce:keyword>
</ce:keywords>
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<affiliation>Center of Marine Biotechnology, University of Maryland Biotechnology Institute, 701 E. Pratt Street, Baltimore, MD 21202, USA</affiliation>
<description>Corresponding author. Tel.: +1-410-234-8803; fax: +1-410-234-8896</description>
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<abstract lang="en">Almost all fish reared in captivity exhibit some form of reproductive dysfunction. In females, there is often failure to undergo final oocyte maturation, ovulation and spawning; while in males milt production may be reduced and of low quality. These dysfunctions are due to the fact that fish in captivity do not experience the conditions of the spawning grounds, and as a result there is a failure of the pituitary to release the maturational gonadotropin, luteinizing hormone (LH). Reproductive hormones have been utilized since the 1930s to stimulate reproductive processes and induce ovulation/spermiation and spawning. The first methods employed freshly ground pituitaries collected from reproductively mature fish, which contained gonadotropins (mainly LH) and induced steroidogenesis and gonadal maturation. Eventually, purified gonadotropins became available, both of piscine and mammalian origin, e.g., carp or salmon gonadotropin, and human chorionic gonadotropin. In the 1970s, spawning induction methods begun employing the newly discovered gonadotropin-releasing hormone (GnRH), which induces the secretion of the fish's own gonadotropin from the pituitary, thereby overcoming the endocrine failure observed in captive broodstocks. Development of highly potent, synthetic agonists of GnRH (GnRHa) constituted the next generation of hormonal manipulation therapies, and created a surge in the use of hormones to control reproductive processes in aquaculture. The most recent development is the incorporation of GnRHa into polymeric sustained-release delivery systems, which release the hormone over a period of days to weeks. These delivery systems alleviate the need for multiple treatments and induce (a) long-term elevation in sperm production and (b) multiple spawning in fish with asynchronous or multiple-batch group-synchronous ovarian physiology. Based on the recent discovery of GnRH multiplicity in fish and the increasing understanding of its functional significance, new GnRH agonists can be designed for more potent, affordable and physiologically-compatible spawning induction therapies. Future strategies for improved spawning manipulations will be based on understanding the captivity-induced alterations in the GnRH system, and on new approaches for their repair at the level of GnRH gene expression and release.</abstract>
<note type="content">Fig. 1: Mean titers (±s.e.m.) expressed as optical density (OD) of hCG antibodies in the plasma of striped bass at different times after injection with hCG (n=4) or saline (n=6). Two-year-old striped bass weighing (450 g) were held in 2.2 m3 tanks at 18°C. On days 0 and 60, one group was injected intra-muscularly with 500 IU kg−1 body weight of hCG (Sigma) dissolved in 0.9% saline, while a control group was injected with saline alone (0.5 ml kg−1). The concentration of hCG antibodies in the plasma was measured using an hCG non-competitive, solid phase ELISA. The mean anti-hCG titers were significantly elevated in response to the hCG injections (two-way ANOVA, P≤0.0001). (Y. Zohar and S. Wehage, unpublished).</note>
<note type="content">Fig. 2: Mean (±s.e.m.) plasma hormone levels (ng ml−1) and cumulative % oocyte maturation of cultured striped bass (n=7) after two injections (arrows) of GnRHa (15 μg kg−1) or saline during the spawning season (April). Fish (4–8 kg) were maintained in a flow-through system supplied with Chesapeake Bay water (4–2 g l−1 salinity; 7–18°C) and had a mean oocyte diameter of 850 (±20) μm at the start of the experiment. With the exception of plasma 17,20β,21-P, all hormone profiles were significantly changed by the GnRHa treatment (ANOVA, P≤0.05). The horizontal hatched bar indicates the time when atretic oocytes could be seen in the biopsies. Most GnRHa-injected females reached the peripheral GV stage, but only one ovulated within the duration of the study.</note>
<note type="content">Fig. 3: Mean (±s.e.m.) plasma hormone levels of cultured female white bass at various stages of final oocyte maturation (FOM), induced by treatment with a GnRHa-implant (EVAc; 50 μg kg−1). Data from individual fish were pooled according to maturation stage (sample sizes are shown in parentheses) as follows: after GnRHa treatment but before the onset of FOM (pre-FOM), germinal vesicle migration (mGV), after GV breakdown (GVBD) and after ovulation (post-OV). Sample means that were significantly different from the previous maturation stage are indicated by asterisks (ANOVA, DNMR; *P≤0.05, **P≤0.01) (from Mylonas et al., 1997b).</note>
<note type="content">Fig. 4: Daily egg production (ml tank−1) of red porgy (Pagrus pagrus) in response to treatment with GnRHa in the form of a single injection (15 μg kg−1) or a sustained-release delivery system (Fad-sa microspheres; 50 μg kg−1). The experiments were carried out at the Meneou Marine Aquaculture Research Station, Fisheries Department, Republic of Cyprus during the Spring spawning season of 1997. Each tank contained five females and seven males, of mean (±S.D.) weight of 1.4 (±0.3) and 1.1±(0.2) kg, respectively.</note>
<note type="content">Fig. 5: Mean (±s.e.m.) total expressible milt production of European seabass (Dicentrarchus labrax) treated with GnRHa in various ways. Fish (n=8) were treated with either a single GnRHa injection (25 μg kg−1), GnRHa microspheres (Fad-sa; 50 μg kg−1) or a GnRHa implant (EVAc; 50 μg kg−1). Fish treated with GnRHa produced significantly higher amounts of milt than controls for the first 7 days after treatment (ANOVA, DNMR, P≤0.05). Moreover, fish treated with GnRHa-delivery systems continued to produce higher amounts of milt for up to 35 days after treatment (ANOVA, DNMR, P≤0.05). (from Sorbera et al., 1996).</note>
<note type="content">Fig. 6: Mean (n=2) daily in vitro release of hCG from a poly[ortho-acetate] delivery system (A), and plasma hCG levels (n=2) and cumulative % ovulation of striped bass (n=5) treated with this delivery system at a dose of 3600 IU hCG kg−1 (B).</note>
<note type="content">Table 1: Representative applications of hormonal manipulations for the induction of final maturation and spawning of male (M) and female (F) broodstock using various gonadotropin (GtH) preparations</note>
<note type="content">Table 2: Representative applications of hormonal manipulations with agonists of gonadotropin-releasing hormone (GnRHa) for the induction of final maturation and spawning of male (M) and female (F) broodstocks</note>
<note type="content">Table 3: Representative applications of sustained-release GnRHa-delivery systems for the induction of final maturation and spawning of male (M) and female (F) broodstocks</note>
<subject>
<genre>Keywords</genre>
<topic>Induced spawning</topic>
<topic>GnRH</topic>
<topic>GnRH genes</topic>
<topic>Gonadotropin</topic>
<topic>Delivery systems</topic>
<topic>Broodstock management</topic>
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