Effect of glucocorticoids on androgen biosynthesis in the testes of the toad <i>Rhinella arenarum</i> (Amphibia, Anura)

Czuchlej, Silvia Cristina; Volonteri, María Clara; Regueira, Eleonora; Ceballos, Nora R.

doi:10.1002/jez.2232

Cited by 10 publications

(4 citation statements)

References 70 publications

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“…Sertoli cell‐specific GR knockout mice displayed distinct morphological changes, including atypical germ cells and immature‐like Leydig cells, indicating that Sertoli cell GRs are required to maintain normal male reproduction (Hazra et al., 2014). By contrast, high levels of GC or sGC exposure negatively impact testes function, including induction of Leydig cell apoptosis and inhibition of spermatogenesis (Czuchlej et al., 2019). We have previously reported that Beta exposure did not affect reproductive function in this same cohort of animals (Moisiadis et al., 2017).…”

Section: Discussionmentioning

confidence: 99%

Prenatal maternal glucocorticoid exposure modifies sperm miRNA profiles across multiple generations in the guinea‐pig

Hamada,

Casciaro,

Moisiadis

et al. 2024

The Journal of Physiology

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Maternal stress and glucocorticoid exposure during pregnancy have multigenerational effects on neuroendocrine function and behaviours in offspring. Importantly, effects are transmitted through the paternal lineage. Altered phenotypes are associated with profound differences in transcription and DNA methylation in the brain. In the present study, we hypothesized that maternal prenatal synthetic glucocorticoid (sGC) exposure in the F0 pregnancy will result in differences in miRNA levels in testes germ cells and sperm across multiple generations, and that these changes will associate with modified microRNA (miRNA) profiles and gene expression in the prefrontal cortex (PFC) of subsequent generations. Pregnant guinea‐pigs (F0) were treated with multiple courses of the sGC betamethasone (Beta) (1 mg kg–1; gestational days 40, 41, 50, 51, 60 and 61) in late gestation. miRNA levels were assessed in testes germ cells and in F2 PFC using the GeneChip miRNA 4.0 Array and candidate miRNA measured in epididymal sperm by quantitative real‐time PCR. Maternal Beta exposure did not alter miRNA levels in germ cells derived from the testes of adult male offspring. However, there were significant differences in the levels of four candidate miRNAs in the sperm of F1 and F2 adult males. There were no changes in miRNA levels in the PFC of juvenile F2 female offspring. The present study has identified that maternal Beta exposure leads to altered miRNA levels in sperm that are apparent for at least two generations. The fact that differences were confined to epididymal sperm suggests that the intergenerational effects of Beta may target the epididymis. imageKey points Paternal glucocorticoid exposure prior to conception leads to profound epigenetic changes in the brain and somatic tissues in offspring, and microRNAs (miRNAs) in sperm may mediate these changes. We show that there were significant differences in the miRNA profile of epididymal sperm in two generations following prenatal glucocorticoid exposure that were not observed in germ cells derived from the testes. The epididymis is a probable target for intergenerational programming. The effects of prenatal glucocorticoid treatment may span multiple generations.

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Section: Discussionmentioning

confidence: 99%

Prenatal maternal glucocorticoid exposure modifies sperm miRNA profiles across multiple generations in the guinea‐pig

Hamada,

Casciaro,

Moisiadis

et al. 2024

The Journal of Physiology

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“…The common toad, Rhinella arenarum , is a bufonid widely distributed in southern South America, categorized as “Least Concern” under the IUCN Red List (Kwet et al, 2004). This species has been subject of extensive research in areas such as endocrinology (e.g., Czuchlej et al, 2019; Scaia et al, 2019; Volonteri & Ceballos, 2010) and organ histology (e.g., Farias et al, 2003; Hermida & Farías, 2009; Regueira et al, 2016). In addition, early life stages have been used in ecotoxicological studies (e.g., Aronzon et al, 2020; Asparch et al, 2020; Liendro et al, 2015; Mardirosian et al, 2017; Peluso et al, 2022; Svartz et al, 2012), including the assessment of the effects of agrochemicals on gonadal development (Svartz et al, 2016).…”

Section: Introductionmentioning

confidence: 99%

Gonadal morphogenesis in the South American toad Rhinella Arenarum (Anura, Bufonidae) unveils an extremely delayed rate of sex differentiation

Piazza

Czuchlej

Gómez

et al. 2023

Journal of Morphology

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Among anurans, Bufonids are recognized for their retarded sex differentiation. However, few studies have addressed gonadal morphogenesis in this family. Here, we analyzed the early gonadogenesis in laboratory‐reared Rhinella arenarum. Few germ cells were identified in the genital ridge at Gosner stage 26. At metamorphosis, somatic cells and germ cells were observed in the outer region of the undifferentiated gonad, whereas the central region was occupied by stromal tissue. A cortico‐medullary organization was first recognized on Day 7 postmetamorphosis. The cortex was composed of germ cells and encompassing epithelial cells, whereas the medulla contained cells presumptively derived from the coelomic epithelium. Medullary somatic cells formed metameric knots along the length of the undifferentiated gonad. Consequently, a series of 12–14 gonomeres became recognizable externally. The first sign of ovarian differentiation was observed on Day 15 postmetamorphosis, when a cavity was formed within each gonomere. In contrast, testes were recognized by a uniform distribution of germ cells and intermingled somatic cells, as the division into cortex and medulla was lost. By Day 50 postmetamorphosis, the gonadal metameric organization was still apparent both in the ovaries and testes. Follicles containing diplotene oocytes were observed within the ovary. In the testis, an incipient lobular architecture was recognized without initiation of meiosis within the seminiferous cords. These observations reveal an extremely delayed gonadal development in R. arenarum, not reported previously for other anuran species. In addition, the late differentiation of the gonads contrasted with the early appearance of follicles in the Bidder's organ. Lastly, we observed that delayed metamorphs exhibited an undifferentiated gonad, demonstrating that gonadogenesis in this species is more dependent on somatic development than on age.

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“…Similar results were found in male amphibians, where high plasma levels of CORT were negatively associated with courtship behavior (Moore & Miller, 1984), plasma androgen levels (Orchinik et al, 1988) and calling behavior (Marler & Ryan, 1996), or both (Burmeister et al, 2001). Also, chronic CORT treatment resulted in fewer spermatids in Rana pipiens (Tsai et al, 2003) and in vitro CORT treatment resulted in inhibition of androgen production in Rhinella arenarum testicles (Czuchlej et al, 2018). Thus, the elevation of CORT by exposure to a stressor or by exogenous treatment can inhibit the synthesis of sex steroids, potentially affecting gametogenesis and reproductive behavior (Carr, 2011).…”

Section: Introductionmentioning

confidence: 99%

Effects of corticosterone treatment and wound healing on reproductive traits of American bullfrogs

2021

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During reproductive season, calling anuran males display high testosterone (T) and episodically high corticosterone (CORT) plasma levels, which are positively associated with higher calling rates and immunocompetence. However, exposure to constant stress stimuli can result in chronically elevated CORT levels, possibly leading to inhibition of reproductive and immune activity. Reproduction and immune responses are energetically expensive, so when an animal is immunologically challenged, a tradeoff might be expressed, with CORT potentially mediating it. Our aim was to test how episodic and chronic CORT treatments, alongside wound healing, would affect reproduction in American bullfrog males (Lithobates catesbeianus). Forty animals were divided in four groups: Episodic CORT (daily transdermic application of CORT), placebo (daily transdermic application of sesame oil), chronic CORT (subcutaneous CORT silastic implants), and sham control (subcutaneous empty silastic implants). One week after treatments began, animals were punctured in the leg with a biopsy needle and the wound was photographed after 45 days to determine wound healing status (WS). Blood samples were collected throughout the experiment to measure CORT and T plasma levels. After animal euthanasia, testes were dissected, fixed, and analyzed histologically to determine spermatogenic activity (germinative cyst [GmC] morphometrics). As expected, the episodic CORT treatment had no effect on T plasma levels or spermatogenic activity. On the other hand, chronic CORT treatment reduced GmC morphometric traits, indicating suppression of reproduction, although T levels were not altered. In addition, animals from sham control and chronic CORT treatments with higher T levels presented higher WS, which indicates an immune‐enhancing T effect.

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Effect of glucocorticoids on androgen biosynthesis in the testes of the toad Rhinella arenarum (Amphibia, Anura)

Cited by 10 publications

References 70 publications

Prenatal maternal glucocorticoid exposure modifies sperm miRNA profiles across multiple generations in the guinea‐pig

Prenatal maternal glucocorticoid exposure modifies sperm miRNA profiles across multiple generations in the guinea‐pig

Gonadal morphogenesis in the South American toad Rhinella Arenarum (Anura, Bufonidae) unveils an extremely delayed rate of sex differentiation

Effects of corticosterone treatment and wound healing on reproductive traits of American bullfrogs

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