Growth hormone stimulates hepatic thyroxine 5′-monodeiodinase activity and 3,5,3′-triiodothyronine levels in rainbow trout (Salmo gairdneri)

doi:10.1016/0016-6480(90)90002-4

General and Comparative Endocrinology

Volume 78, Issue 2, May 1990, Pages 164-172

https://doi.org/10.1016/0016-6480(90)90002-4 Get rights and content

Abstract

Intraperitoneal injection of rainbow trout (Salmo gairdneri) with 0.4 μg/g of human growth hormone (hGH) increased plasma levels of 3,5,3′-triiodo-l-thyronine (T₃) and V_max of the hepatic microsomal 5′-monodeiodinase enzyme (5′D) that converts thyroxine (T₄) to T₃, with no effect on K_m or plasma T₄ levels. A dose of 0.4 μg hGH/g increased both plasma T₃ and V_max as early as 8 hr postinjection (pi). Maximal levels for both parameters occurred at 24 hr pi and significant stimulation was sustained to 48 hr pi. In trout injected with hGH over a dose range of 0.1–1.0 μg/g and sampled at 24 hr pi, both V_max and plasma T₃ increased in a dose-dependent manner. It is concluded that the increase in the level of functional hepatic 5′D may contribute to the rapid hGH-induced elevation in plasma T₃.

References (34)

M. Bradford
A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein dye binding
Anal. Biochem
(1976)
D.G. Cyr et al.
The influence of short-term 17β-estradiol treatment on plasma T₃ levels and in vitro hepatic T₄ 5′-monodeiodination activity in rainbow trout, Salmo gairdneri
Gen. Comp. Endocrinol
(1988)
A. deLuze et al.
Fish growth hormone enhances peripheral conversion of thyroxine to triiodothyronine in the eel
Gen. Comp. Endocrinol
(1984)
E.M. Donaldson et al.
Hormonal enhancement of growth in fish
P. Fok et al.
Regulation of plasma T₃ levels in T₄-challenged rainbow trout, Salmo gairdneri
Gen. Comp. Endocrinol
(1984)
D.A. Higgs et al.
Application of thyroid and steroid hormones as anabolic agents in fish culture
Comp. Biochem. Physiol. B
(1982)
T. Kayes
Effects of hypophysectomy, beef growth hormone replacement therapy, pituitary autotransplantation, and environmental salinity on growth in the black bullhead (Ictalurus melas)
Gen. Comp. Endocrinol
(1977)
D.L. MacLatchy et al.
Shortterm treatment with testosterone increases plasma 3,5,3′-triiodo-l-thyronine and hepatic l-thyroxine 5′-monodeiodinase levels in arctic charr, Salvelinus alpinus
Gen. Comp. Endocrinol
(1988)
R.L. Saunders et al.
The effect of orally administered 3,5,3′-triiodo-l-thyronine on growth and salinity tolerance of Atlantic salmon (Salmo salar L.)
Aquaculture
(1985)
C.A. Shields et al.
Thyroxine 5′-monodeiodinase in hepatocytes of rainbow trout, Salmo gairdneri: Distribution, effects of starvation, and exogenous inhibitors
Gen. Comp. Endocrinol
(1986)

M.M. Vijayan et al.

Effect of cortisol on the in vitro hepatic conversion of thyroxine to triiodothyronine in brook charr (Salvelinus fontinalis Mitchell)

Gen. Comp. Endocrinol

(1988)

S. Brown et al.

Physical injury due to injection or blood removal causes transitory elevations of plasma thyroxine in rainbow trout, Salmo gairdneri

Canad. J. Zool

(1978)

A. deLuze et al.

Stimulation de la conversion périphérique de la thyroxine en triiodothyronine par l'hormone somatotrope ovine chez l'anguille (Anguilla anguilla)

C.R. Hebd. Seances Acad. Sci. Ser. D

(1982)

A. deLuze et al.

Régulation hypophysaire de la 5′-désiodation peripherique de la thyroxine chez l'Anguille

J. Physiol

(1987)

J.G. Eales

The peripheral metabolism of thyroid hormones and regulation of thyroidal status in poikilotherms

Canad. J. Zool

(1985)

U.H.M. Fagerlund et al.

The potential of using the anabolic hormones 17α-methyl testosterone and (or) 3,5,3′-triiodo-thyronine in the freshwater rearing of coho salmon (Oncorhynchus kisutch) and the effects of subsequent seawater performance

Canad. J. Zool

(1980)

K.J. Farbridge et al.

Interaction between ovine growth hormone and triiodo-l-thyronine on metabolic reserves of rainbow trout, Salmo gairdneri

J. Fish Physiol. Biochem

(1988)

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IDs play an important role in controlling phases of fish development and other metabolic processes associated to growth. Deiodination is increased in liver, heart and brain during the process of smoltification in salmonids likely due to the action of growth hormone, which results in higher levels of T3 in blood (MacLatchy and Eales, 1990; MacLatchy et al., 1992; Morin et al., 1993). However, such response was only observed in vivo, suggesting that growth hormone acts on the thyroid pathway indirectly (Sweeting and Eales, 1992b).
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Significant increase in T3 and T4 levels has been observed in Caspian roach (Rutilus rutilus caspicus) exposed to waterborne manganese (Hoseini et al., 2014) and in zebrafish exposed to butachlor (Chang et al., 2013). Maclatchy and Eales (1990) suggest that an increase in T4 level could be a consequence of the decreased GH levels. In addition, the increased level of T4 might be either due to increase in TSH secretion or sensitivity of thyroid follicles to TSH (Grau et al., 1985) or may be due to inhibition of 5′-deiodinase (responsible for accelerating peripheral deiodination of T4 to T3 in plasma) (Gupta and Premabati, 2002).
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Domestication has produced faster-growing strains of animals for use in agriculture, but selection has been applied with little knowledge of the underlying genetic changes that arose throughout the process. Mammals and birds have been domesticated for thousands of years whereas fish have been domesticated only recently; therefore, wild progenitor strains remain for comparison. Rainbow trout (Oncorhynchus mykiss) have undergone intensive selection and domesticated strains grow more rapidly than extant wild strains. To assess physiological pathways altered by domestication, whole-genome mRNA expression was measured in brain, muscle and liver of size-matched domestic and wild trout using a 16K (cGRASP) salmonid microarray. A large number of genes differed between strains, ranging from 3% of genes in brain to 9% in muscle. Domestic fish had more down-regulated genes in the brain relative to wild fish, whereas more genes were up-regulated in domestic liver and muscle. Relative to wild fish, there was a down-regulation of cell division and an up-regulation of structural genes in the brain of domestic fish. In liver from domestic fish, there was an up-regulation of genes related to transport with a down-regulation of lipid binding. Analysis of the functional categories for muscle indicated that most pathways, including pathways related to metabolism and catabolism, were up-regulated in domestic fish. Comparison of these results to other genomic studies on transgenic, domestic and wild salmonids suggests that similar physiological pathways are altered systemically to support faster rates of growth, regardless of the underlying genetic alteration that has caused the altered growth.
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To elucidate possible mechanisms behind the endocrine control of parr–smolt transformation, the daily plasma profiles in thyroid hormones (TH; free thyroxine (FT₄), total thyroxine (TT₄), and total 3,5,3′-triiodothyronine (TT₃)), growth hormone (GH) and cortisol were studied in Atlantic salmon parr and smolts under simulated-natural winter (8 L:16D) and spring (16.5 L:7.5D) photoperiods, respectively. Overall, TT₄, TT₃ and GH levels were higher in smolts than in parr, whereas FT₄ levels fluctuated within the same range in parr and smolts. Significant diurnal changes in plasma TH were present in parr. Both FT₄ and TT₄ levels increased during the photophase and decreased during the scotophase, while TT₃ levels followed an inverse pattern. Growth hormone showed no significant changes in parr. Changes in FT₄, TT₄, GH, and cortisol, but not TT₃, levels, were observed in smolts with peak levels during both the photophase and scotophase for FT₄, TT₄ and GH. Plasma cortisol was not assayed in parr but in smolts the peaks were associated with dusk and dawn. In addition to the general increases in TH, GH and cortisol, the distinct endocrine differences in nighttime levels between parr in the winter and smolts in the spring suggest different interactions between TH, GH, cortisol and melatonin at these different time points. These spring scotophase endocrine profiles may represent synergistic hormone interactions that promote smolt development, similar to the synergistic endocrine interactions shown to accelerate anuran metamorphosis. The variations in these diurnal rhythms between parr and smolts may represent part of the endocrine mechanism for the translation of seasonal information during salmon smoltification.
Seasonal and circadian time-dependent dual action of GH on somatic growth and ovarian development in the Asian catfish, Clarias batrachus (Linn.): Role of temperature
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Citation Excerpt :
Injections (0.2 ml) were given intraperitonialy on alternate days over a period of one month during both the reproductive phases. The doses of GH were selected based on literature available in fishes (Maclatchy and Eales, 1990; Berghman et al., 1996). Having known that C. batrachus remains inactive during December–January with regard to general growth, reproductive activity and feeding etc. (Sinha et al., 1992), a little higher doses of GH (if considered in term of μg/fish) was injected during this period of experimentation as compared to the doses used during the months of March–April.
Effect of growth hormone (GH), injected either at the morning or evening, on the somatic and ovarian development of the Asian catfish, Clarias batrachus was studied during the late quiescence and early recrudescence phase of the reproductive cycle. GH treatment during the late quiescence phase (December–January; 11L: 13D, average water temperature 16.2 ± 1°C) failed to exert any impact on the somatic or ovarian development, except that it increased plasma testosterone marginally, and decreased hepatic level of triglycerides (TG); while during the early recrudescence phase (March–April; 12.4L: 11.20D; average water temperature—28.4 ± 2 °C), GH had significant circadian time-dependent effect on somatic and ovarian development. GH injection at morning stimulated ovarian growth and development, as was evident from the dose-dependent significant increase in ovarian weight, gonadosomatic index, plasma levels of testosterone and estradiol-17β following GH treatment. The ovarian morphology also revealed the advancement in follicular development in GH treated fish. GH also induced remarkable increase in ovarian levels of TG, free cholesterol (CF) and phospholipids (PL) with concomitant declines in their hepatic levels. However, evening hour GH injection provoked appreciable increase in body weight without having any significant impact on ovarian weight and GSI. Few oocytes in the ovary of evening hour GH treated fish exhibited advanced stages of development, but number of such advanced stage oocytes was significantly much less than the morning hour GH injected fish. Ovarian TG and PL remained unchanged, while their hepatic levels were increased. The temporal synergism between GH and other intrinsic factors regulating body growth and gonadal development may be suggested herewith to be considered prior to administration of GH in fishes. This study has immense practical use in aquaculture.
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We here analyzed the effect of a mild hyperosmotic challenge on the activities of deiodinases type I (D1) and II (D2) in the trout liver, and D1 in kidney and gill, two organs involved in osmoregulation. FW-adapted immature rainbow trout were transferred to 5‰ SW and killed 0.5, 1, 2, 4, 8 12, 24 and 48 h post-transfer (PT). Fish maintained in FW served as controls. Hepatic, renal and branchial D1 and hepatic D2 activities were assessed as well as circulating levels of T₃, T₄ and cortisol. Hyperosmotic challenge elicited significant and sustained decreases in kidney D1 and liver D2 activities at 8 h PT, which returned to control values at 48 h PT. In contrast, liver and gill D1 activities exhibited no significant change throughout the study. Also, significant increases in circulating T₄ at 2–4 and 48 h PT were observed. Circulating T₃ remained unmodified until 24–48 h PT, when it rose sharply. Simultaneously, cortisol showed a trend towards increase during the initial 4 h PT, which attained significance at 48 h PT. The present findings demonstrate that a mild hypertonic challenge is sufficient to elicit responses in the trout thyroidal axis. Hormonal changes in the circulatory compartment are in accordance with those previously described for migratory salmonids. A novel aspect of our findings is the organ-specific differential response exhibited by ORD-enzymes when trout are exposed to a mildly different osmotic environment. Our findings further establish the uniqueness of fish thyroid physiology, and can be of value in further understanding the evolutionary aspects of this ORD family of deiodinases.

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Growth hormone stimulates hepatic thyroxine 5′-monodeiodinase activity and 3,5,3′-triiodothyronine levels in rainbow trout (Salmo gairdneri)

Abstract

Anal. Biochem

Gen. Comp. Endocrinol

Gen. Comp. Endocrinol

Gen. Comp. Endocrinol

Comp. Biochem. Physiol. B

Gen. Comp. Endocrinol

Gen. Comp. Endocrinol

Aquaculture

Gen. Comp. Endocrinol

Gen. Comp. Endocrinol

Physical injury due to injection or blood removal causes transitory elevations of plasma thyroxine in rainbow trout, Salmo gairdneri

Canad. J. Zool

Stimulation de la conversion périphérique de la thyroxine en triiodothyronine par l'hormone somatotrope ovine chez l'anguille (Anguilla anguilla)

C.R. Hebd. Seances Acad. Sci. Ser. D

Régulation hypophysaire de la 5′-désiodation peripherique de la thyroxine chez l'Anguille

J. Physiol

The peripheral metabolism of thyroid hormones and regulation of thyroidal status in poikilotherms

Canad. J. Zool

The potential of using the anabolic hormones 17α-methyl testosterone and (or) 3,5,3′-triiodo-thyronine in the freshwater rearing of coho salmon (Oncorhynchus kisutch) and the effects of subsequent seawater performance

Canad. J. Zool

Interaction between ovine growth hormone and triiodo-l-thyronine on metabolic reserves of rainbow trout, Salmo gairdneri

J. Fish Physiol. Biochem