Antagonism between prolactin and thyroid hormone in amphibian development

Etkin, William; Gona, Amos G.

doi:10.1002/jez.1401650209

Cited by 145 publications

(23 citation statements)

References 8 publications

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“…The possibility suggests itself that we are dealing with a substance of goitrogenic properties. Support for the possibility of goitrogenicity of prolactin is provided by our earlier experiments (10) in which normal bullfrog tadpoles treated with prolactin entered into metamorphic stasis and yet their thyroids reached a high level of activation as judged by histological criteria. This evidence was indicative of a goitrogen-like effect since prolactin had induced activation of the gland without a physiological indication of release of active hormone.…”

Section: Discussionmentioning

confidence: 94%

Prolactin as a Goitrogenic Agent in Amphibia¹

Gona

1967

Endocrinology

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The nature of the inhibitory action of mammalian prolactin on the development of bullfrog tadpoles was investigated. Tadpoles injected ip with 20 jug of thyroxine (T 4 ) and 2 or 4 mg of ovine prolactin (NIH-P-S-7) underwent metamorphic changes in parallel with T 4 -injected controls. By contrast, tadpoles injected with 4 IU of bovine thyrotropic hormone (TSH) and either 4.0 or 0.4 mg of prolactin entered into developmental stasis after showing early signs of metamorphic climax, while TSH-injected controls completed the various metamorphic steps, including tail resorption. Histological examination of the thyroids of animals treated with both TSH and prolactin revealed an extremely high degree of hypertrophy and hyperplasia, with more pronounced depletion of the colloid than in TSH-injected controls. It is concluded that in these experiments prolactin acts at the level of the thyroid and that it has goitrogenic properties. (Endocrinology 8 1 : 748, 1967) P ROLACTIN appears to possess a great diversity of actions in different vertebrates aside from its well-known effects in mammals. For example, it elicits "waterdrive," or second metamorphosis, in the red eft stage of the common newt (1, 2). Another role concerns osmoregulation in fish (3). Excess growth in tadpoles carrying ectopic pituitary transplants was reported by Etkin and Lehrer (4), who postulated that this was the result of an increased rate of prolactin secretion by the ectopic pituitaries which are freed from the normally existing hypothalamic inhibition of prolactin release. Other investigations demonstrated that mammalian prolactin has a marked growth-promoting effect in tadpoles (5-8). Olivereau (9) reported a thyroid-stimulating effect of prolactin in eels and concluded that this hormone acts as a thyrotropin-releasing factor in these fish. More recently, it was found (10) that mammalian prolactin inhibits metamor-

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Section: Discussionmentioning

confidence: 94%

Prolactin as a Goitrogenic Agent in Amphibia¹

Gona

1967

Endocrinology

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“…It has also been reported that mammalian PRL counteracts the effects of TH when added to cultured tadpole tissues (5,6). These observations have led to a widely held belief that PRL has the biological role of a ''juvenile'' hormone in amphibian metamorphosis (7,8). It was predicted that the levels of endogenous PRL, just like that of JH in insects, should be high at premetamorphosis and prometamorphosis stages and then drop at the climax of metamorphosis (7).…”

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confidence: 99%

“…These observations have led to a widely held belief that PRL has the biological role of a ''juvenile'' hormone in amphibian metamorphosis (7,8). It was predicted that the levels of endogenous PRL, just like that of JH in insects, should be high at premetamorphosis and prometamorphosis stages and then drop at the climax of metamorphosis (7). However, the direct measurements of both endogenous PRL mRNA (9,10) and protein levels of PRL in the serum (11,12) showed them to be low at premetamorphosis and prometamorphosis stages rising substantially only at the climax of metamorphosis, a result that does not support a juvenilizing role for endogenous PRL.…”

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Prolactin is not a juvenile hormone in Xenopus laevis metamorphosis

Huang

Brown

2000

Proc. Natl. Acad. Sci. U.S.A.

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Prolactin (PRL) is widely considered to be the juvenile hormone of anuran tadpoles and to counteract the effects of thyroid hormone (TH), the hormone that controls amphibian metamorphosis. This putative function was concluded mainly from experiments in which mammalian PRL was injected into tadpoles or added to cultured tadpole tissues. In this study, we show that overexpression of ovine or Xenopus laevis PRL in transgenic X. laevis does not prolong tadpole life, establishing that PRL does not play a role in the life cycle of amphibians that is equivalent to that of juvenile hormone in insect metamorphosis. However, overexpression of PRL produces tailed frogs by reversing specifically some but not all of the programs of tail resorption and stimulating growth of fibroblasts in the tail. Whereas TH induces muscle resorption in tails of these transgenics, the tail fibroblasts continue to proliferate resulting in a fibrotic tail that is resistant to TH.

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“…However, the results do not indicate whether the differences between the capacities of these grafts to inhibit the action of thyroxine results from quantitative and/or qualitiative changes in the glands. At a first glance it would appear that the results of these experiments do not support the bihormonal model of meta-326 A. DERBY morphosis proposed by Etkin and Gona, 1967, in which prolactin activity is highest during premetamorphosis and decreases during prometamorphosis to a minimum at climax. However, before such a judgment can be made the following point should be considered.…”

Section: Derby and Etkin ('68) Demonstrated That A Pituitary Implantmentioning

confidence: 56%

Inhibition of thyroxine induced tail resorption in vitro by pituitary grafts from different stages of metamorphosis

Derby

1970

J. Exp. Zool.

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It has been previously demonstrated that isolated pieces (discs) from the tail fins of tadpoles (R. pipiens), survive in vitro for several weeks and respond to thyroxine by undergoing resorption. In addition, discs into which tadpole pituitary glands have been implanted or discs that have been injected with either prolactin or growth hormone undergo a delayed pattern of resorption on expsoure to thyroxine when compared to discs treated with thyroxine alone.Pituitaries were taken from early prometamorphic, climax and froglet stages and were implanted into tail discs cut from tadpoles in early prometamorphosis. These discs were maintained in thyroxine solutions. As controls, unimplanted discs were treated with thyroxine or maintained in Hanks solution. In a second series of experiments, tail discs were cut from tadpoles at progressive stages of prometamorphosis and treated with thyroxine solutions.The results demonstrate that pituitaries taken from different stages in the life cycle of this animal differ in their capacity to inhibit thyroxine induced tail resorption. The most effective inhibition is demonstrated by early prometamorphic pituitaries, followed by climax pituitaries. Froglet glands exhibit little activity. The results also demonstrate that the response of tail tissues to thyroxine increases during early prometamorphosis and with increasing rapidity during the last third of this period. These results are in harmony with the concept that amphibian metamorphosis may be dependent upon a bihormonal system in which thyroid hormone promotes while a prolactin-like hormone counteracts this process.

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Antagonism between prolactin and thyroid hormone in amphibian development

Cited by 145 publications

References 8 publications

Prolactin as a Goitrogenic Agent in Amphibia¹

Prolactin as a Goitrogenic Agent in Amphibia¹

Prolactin is not a juvenile hormone in Xenopus laevis metamorphosis

Inhibition of thyroxine induced tail resorption in vitro by pituitary grafts from different stages of metamorphosis

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Antagonism between prolactin and thyroid hormone in amphibian development

Cited by 145 publications

References 8 publications

Prolactin as a Goitrogenic Agent in Amphibia1

Prolactin as a Goitrogenic Agent in Amphibia1

Prolactin is not a juvenile hormone in Xenopus laevis metamorphosis

Inhibition of thyroxine induced tail resorption in vitro by pituitary grafts from different stages of metamorphosis

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Prolactin as a Goitrogenic Agent in Amphibia¹

Prolactin as a Goitrogenic Agent in Amphibia¹