In ovo metabolism of progesterone to 5β-pregnanedione in chicken eggs: Implications for how yolk progesterone influences embryonic development

Paitz, Ryan T.; Cagney, Erin

doi:10.1016/j.ygcen.2019.113221

Cited by 12 publications

(9 citation statements)

References 67 publications

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“…Androstenedione converts to etiocholanolone and its conjugates with little evidence of conversions to other biologically active steroids, such as testosterone or progesterone [17,18,32]. In both birds and mammals, progesterone is converted to pregnanolone or other similar forms which are often conjugated and do not act via progesterone, androgen, oestrogen or glucocorticoid receptors [17,[19][20][21]30,31,[33][34][35]. Glucocorticoids are also rapidly metabolized, producing more polar, conjugated forms (birds [22,36], mammals [37] and reptiles [38]).…”

Section: The Problem: Embryonic Metabolism Of Maternal Steroidsmentioning

confidence: 99%

“…see [4,10]). On the other hand, recent physiological studies demonstrate that embryos rapidly metabolize maternal steroids into supposedly inert forms before they reach the developing embryo [17][18][19][20][21]. Because these steroid metabolites do not bind with classical steroid receptors, it suggests that embryos may 'win' in parent-offspring conflict by buffering themselves from maternal control [13,14].…”

Section: Introductionmentioning

confidence: 99%

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Maternally derived hormones, neurosteroids and the development of behaviour

Mouton

Duckworth

2021

Proc. R. Soc. B.

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In a wide range of taxa, there is evidence that mothers adaptively shape the development of offspring behaviour by exposing them to steroids. These maternal effects have major implications for fitness because, by shaping early development, they can permanently alter how offspring interact with their environment. However, theory on parent–offspring conflict and recent physiological studies showing that embryos rapidly metabolize maternal steroids have placed doubt on the adaptive significance of these hormone-mediated maternal effects. Reconciling these disparate perspectives requires a mechanistic understanding of the pathways by which maternal steroids can influence neural development. Here, we highlight recent advances in developmental neurobiology and psychiatric pharmacology to show that maternal steroid metabolites can have direct neuro-modulatory effects potentially shaping the development of neural circuitry underlying ecologically relevant behavioural traits. The recognition that maternal steroids can act through a neurosteroid pathway has critical implications for our understanding of the ecology and evolution of steroid-based maternal effects. Overall, compared to the classic view, a neurosteroid mechanism may reduce the evolutionary lability of hormone-mediated maternal effects owing to increased pleiotropic constraints and frequently influence long-term behavioural phenotypes in offspring.

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Section: The Problem: Embryonic Metabolism Of Maternal Steroidsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Maternally derived hormones, neurosteroids and the development of behaviour

Mouton

Duckworth

2021

Proc. R. Soc. B.

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“…It is mainly produced during the yolk formation period by granulosa cells of the preovulatory follicle (Huang et al, 1979). It is well known that yolk progesterone could elicit direct effects on embryo via activation of progesterone receptors (Conneely & Jericevic, 2002), or can be converted to other steroids such as 5β‐pregnanedione (Kumar et al, 2018; Paitz & Cagney, 2019), androgens, estrogens, or glucocorticoids (Payne & Hales, 2004). As for corticosterone, some studies suggest that prenatal exposure to maternal progesterone has detrimental effects on the chick.…”

Section: Introductionmentioning

confidence: 99%

Yolk corticosterone and progesterone levels in Greater Rhea (Rhea americana) eggs vary in a changing social environment

et al. 2022

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Maternal hormones in avian egg yolks may signal and prepare offspring for the prevailing conditions. However, this adjustment requires some degree of flexibility in regulating yolk hormone deposition. The Greater Rhea (Rhea americana) has a particular mating system that combines mixed polygyny and polyandry, communal nesting, and exclusive paternal care of chicks. In this species, we previously found that yolk hormone deposition varies among eggs of different captive populations and could influence chicks' physiology and behavior. However, it is still unknown whether females can modify yolk hormone deposition in a changing social environment. Using a captive population of Greater Rheas, in this study, we quantified yolk hormone levels before and after a reduction in the number of females present in the population. We found that females deposited on average higher yolk corticosterone and lower yolk progesterone after the change in their social environment. Since corticosterone deposited into the yolk comes exclusively from the female's plasma, our results suggest that females had, on average, higher plasma corticosterone levels. The change in the number of females may increase the events of male-male competitions, courtships, and matings, leading to an increase of corticosterone in the females' plasma and then into their eggs. Since we previously found that higher yolk corticosterone and lower yolk progesterone were associated with the production of chicks that have an attenuated stress response, the present study results suggest that yolk hormone deposition is mediated by flexible mechanisms that could adjust development to the prevailing conditions.

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“…In particular, developing embryos may be constrained in their ability to regulate exposure to maternal steroids. Fish embryos eliminate maternal steroids to the surrounding water (Paitz et al, 2016) and amniotic vertebrates metabolize maternal steroids in the developing extraembryonic membranes (Diczfalusy, 1969, Paitz & Bowden, 2008Paitz & Cagney, 2019). However, the only contact a developing terrestrial clutch has with water is via rain or hydration provided by parents (typically the male: Crump, 1974;Delia et al, 2020;Dugas, 2018).…”

Section: Introductionmentioning

confidence: 99%

“…In egg‐laying amniotes like birds and reptiles, maternal steroids initially present in the yolk are subject to metabolism by the embryo (partially via extraembryonic membranes), a process thought to regulate the amount of steroid that reaches the developing embryo (Kumar et al, 2019; Paitz & Bowden, 2013). As anamniotes, amphibians lack the extraembryonic membranes that modulate embryonic exposure to maternal steroids in other vertebrates (Paitz & Bowden, 2008, 2010, 2013; Paitz & Cagney, 2019). However, the lack of these extraembryonic membranes alone does not preclude embryos from regulating their exposure to steroids.…”

Section: Introductionmentioning

confidence: 99%

Steroid levels in frog eggs: Manipulations, developmental changes, and implications for maternal steroid effects

Paitz

Dugas

2021

J Exp Zool Pt A

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Exposure to maternally derived steroids during embryonic development can elicit phenotypic effects in the resulting offspring. Studies of maternal steroid effects, especially rich in mammals and birds, have offered exciting insights into the evolution of maternal effects in vertebrates. To extend this literature, we quantified levels of steroids in the eggs of four neotropical dendrobatid frogs that lay terrestrial clutches, a reproductive strategy that has evolved multiple times in amphibians.Building on our observational results, we then manipulated levels of pregnenolone and progesterone in eggs of one species and examined how this affected steroid levels during development. Eggs of all four species had detectable steroids levels, with progestogens being more abundant than androgens and glucocorticoids. Estrogens could not be detected. Immersion of frog eggs in a solution containing pregnenolone and progesterone resulted in elevated levels of both steroids early in development, but levels declined and were similar to those in unmanipulated eggs by the end of development. Treated eggs also exhibited a transient increase in levels of steroids that can be produced from pregnenolone and progesterone. Overall, our findings demonstrate that frog eggs contain steroids similar to what has been observed in other egg-laying vertebrates. During development, steroid levels are dynamic, further suggesting developing embryos regulate exposure to maternal steroids. These results set the stage for investigating the causes and consequences of maternal steroid effects in frogs.

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In ovo metabolism of progesterone to 5β-pregnanedione in chicken eggs: Implications for how yolk progesterone influences embryonic development

Cited by 12 publications

References 67 publications

Maternally derived hormones, neurosteroids and the development of behaviour

Maternally derived hormones, neurosteroids and the development of behaviour

Yolk corticosterone and progesterone levels in Greater Rhea (Rhea americana) eggs vary in a changing social environment

Steroid levels in frog eggs: Manipulations, developmental changes, and implications for maternal steroid effects

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