Interrenal activity during metamorphosis of the tiger salamander, Ambystoma tigrinum

Carr, James A.; Norris, David O.

doi:10.1016/0016-6480(88)90295-x

Cited by 28 publications

(6 citation statements)

References 33 publications

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“…In the newt, Triturus alpestri,s, allografts placed on newly metamorphosed animals were rejected more slowly than those placed on fully adult newts (133). In the axolod, induced to metamorphose by immersion in TH, lymphocyte numbers were decreased during metamorphosis in comparison with untreated controls (134), If immunosuppression is associated with natural metamorphosis in tirodeles, the mechanism responsible for this putative immunosuppression could be the satne as that for anuran species, elevated CH, As has been observed for several anuran species, CH are significantly elevated in tiger salamanders (Ambystoma !igrintim) during naturally occurring metamorphosis (135), Are amphibians more susceptible to environmental pathogens at metamorphosis?…”

Section: Do Any Tadpole Lymphocytes Persist Through Metamorphosis?mentioning

confidence: 99%

Metamorphosis and the amphibian immune system

Rollins‐Smith

1998

Immunological Reviews

249

221

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Studies of the ontogeny of immunity in a limited number of representative amphibians have shown that while the immune systems of the larval forms are competent to defend against potential pathogens in the temporary ponds they inhabit, they are not equivalent to the mature immune systems that develop after metamorphosis. Metamorphosis is a critical time of transition when increased concentrations of metamorphic hormones, principally thyroid hormones (TH) and corticosteroid hormones (CH), orchestrate the loss or reorganization of many tissues and organ systems, including the immune system. Immune system reorganization may serve to eliminate unnecessary lymphocytes that could be destructive if they recognized newly emerging adult-specific antigens on the adult tissues. Increased corticosteroids during metamorphosis appear to induce apoptosis of susceptible lymphocytes. This cell death can be inhibited in vitro or in vivo by the corticosteroid receptor antagonist, RU486. A coordinate increase in both TH and CH at metamorphosis may be common to all amphibians that undergo metamorphosis. Current evidence suggests that the central hypothalamic mediator that induces pituitary production of both thyroid-stimulating hormone and adrenocorticotropic hormone in larval amphibians is corticotropin-releasing hormone. Most amphibians probably survive the temporary immunosuppression associated with metamorphosis with no deleterious effects. However, it is hypothesized that if environmental stressors result in the induction of metamorphosis at a less than optimal body size and state of immune maturation, the immune system destruction would be more significant, and the amphibians could be at greater risk of infection and death.

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Section: Do Any Tadpole Lymphocytes Persist Through Metamorphosis?mentioning

confidence: 99%

Metamorphosis and the amphibian immune system

Rollins‐Smith

1998

Immunological Reviews

249

221

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“…Corticosteroids, like thyroid hormone, regulate gene transcription by binding to nuclear receptors. Plasma corticosteroid concentrations rise markedly during metamorphic climax in several anuran species (Jaffe 1981, Krug et al 1983, Jolivet-Jaudet & Leloup-Hatey 1984, Kikuyama et al 1986) and in the urodele Ambystoma tigrinum (Carr & Norris 1988). This rise in plasma corticosteroids is largely synchronous with the rise in thyroid hormone production (Kikuyama et al 1993, Denver 1998.…”

Section: Introductionmentioning

confidence: 99%

Developmental expression and hormonal regulation of glucocorticoid and thyroid hormone receptors during metamorphosis in Xenopus laevis

Krain¹,

Denver²

2004

Journal of Endocrinology

102

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Corticosteroids, the primary circulating vertebrate stress hormones, are known to potentiate the actions of thyroid hormone in amphibian metamorphosis. Environmental modulation of the production of stress hormones may be one way that tadpoles respond to variation in their larval habitat, and thus control the timing of metamorphosis. Thyroid hormone and corticosteroids act through structurally similar nuclear receptors, and interactions at the transcriptional level could lead to regulation of common pathways controlling metamorphosis. To better understand the roles of corticosteroids in amphibian metamorphosis we analyzed the developmental and hormonedependent expression of glucocorticoid receptor (GR) mRNA in the brain (diencephalon), intestine and tail of Xenopus laevis tadpoles. We compared the expression patterns of GR with expression of thyroid hormone receptor beta (TR ). In an effort to determine the relationship between nuclear hormone receptor expression and levels of ligand, we also analyzed changes in wholebody content of 3,5,3 -triiodothyronine (T 3 ), thyroxine, and corticosterone (CORT). GR transcripts of 8, 4 and 2 kb were detected in all tadpole tissues, but only the 4 and 2 kb transcripts could be detected in embryos. The level of GR mRNA was low during premetamorphosis in the brain but increased significantly during prometamorphosis, remained at a constant level throughout metamorphosis, and increased to its highest level in the juvenile frog. GR mRNA level in the intestine remained relatively constant, but increased in the tail throughout metamorphosis, reaching a maximum at metamorphic climax. The level of GR mRNA was increased by treatment with CORT in the intestine but not in the brain or tail. TR mRNA level increased in the brain, intestine and tail during metamorphosis and was induced by treatment with T 3 . Analysis of possible crossregulatory relationships between GRs and TRs showed that GR mRNA was upregulated by exogenous T 3 (50 nM) in the tail but downregulated in the brain of premetamorphic tadpoles. Exogenous CORT (100 nM) upregulated TR mRNA in the intestine. Our findings provide evidence for tissuespecific positive, negative and crossregulation of nuclear hormone receptors during metamorphosis of X. laevis. The synergy of CORT with T 3 on tadpole tail resorption may depend on the accelerated accumulation of GR transcripts in this tissue during metamorphosis, which may be driven by rising plasma thyroid hormone titers.

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“…Our highest CORT dose produced whole‐body content levels of 2961.38 ± 321.25 pg/g (mean ± SE ), which were similar to whole‐body content found in larval A. jeffersonianum exposed to confinement protocol (~3000 pg/g) by Chambers et al (2011). Other studies on Ambystoma CORT content mostly considered only larger adults and only measured blood plasma CORT content, which ranged from approximately 200–45000 pg/ml (Carr & Norris, 1988; Cooperman et al, 2004; Homan et al, 2003a; 2003b; Houck et al, 1996; Millikin et al, 2019). However, Baugh et al (2018) showed there is a fairly tight correlation ( r = .81) between blood plasma and whole‐body CORT content (in frogs), but that whole‐body CORT levels measured approximately 80%–85% lower than plasma CORT.…”

Section: Resultsmentioning

confidence: 99%

Exposure to glucocorticoids alters life history strategies in a facultatively paedomorphic salamander

2021

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Polyphenisms, where two or more alternative, environmentally‐cued phenotypes are produced from the same genotype, arise through variability in the developmental rate and timing of phenotypic traits. Many of these developmental processes are controlled or influenced by endogenous hormones, such as glucocorticoids, which are known to regulate a wide array of vertebrate ontogenetic transitions. Using the mole salamander, Ambystoma talpoideum, as a model, we investigated the role of glucocorticoids in regulating facultative paedomorphosis, an ontogenetic polyphenism where individuals may delay metamorphosis into terrestrial adults. Instead, individuals reproduce as aquatic paedomorphic adults. Paedomorphosis often occurs when aquatic conditions remain favorable, while metamorphosis typically occurs in response to deteriorating or “stressful” aquatic conditions. Since glucocorticoids are central to the vertebrate stress response and are known to play a central role in regulating obligate metamorphosis in amphibians, we hypothesized that they are key regulators of paedomorphic life history strategies. To test this hypothesis, we compared development of larvae in outdoor mesocosms exposed to Low, Medium, and High exogenous doses of corticosterone (CORT). Results revealed that body size and the proportion of paedomorphs were both inversely proportional to exogenous CORT doses and whole‐body CORT content. Consistent with known effects of CORT on obligate metamorphosis in amphibians, our results link glucocorticoids to ontogenetic transitions in facultatively paedomorphic salamanders. We discuss our results in the context of theoretical models and the suite of environmental cues known to influence facultative paedomorphosis.

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Interrenal activity during metamorphosis of the tiger salamander, Ambystoma tigrinum

Cited by 28 publications

References 33 publications

Metamorphosis and the amphibian immune system

Metamorphosis and the amphibian immune system

Developmental expression and hormonal regulation of glucocorticoid and thyroid hormone receptors during metamorphosis in Xenopus laevis

Exposure to glucocorticoids alters life history strategies in a facultatively paedomorphic salamander

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