Exogenous 17<i>β</i>‐oestradiol (<scp>E2</scp>) modifies thymus growth and regionalization in European sea bass <i>Dicentrarchus labrax</i>

Seemann, Frauke; Knigge, Thomas; Olivier, Stéphanie; Monsinjon, Tiphaine

doi:10.1111/jfb.12626

Cited by 18 publications

(16 citation statements)

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“…From mammals, we know that sex steroids influence both thymus differentiation and thymus involution (Staples et al, 1999; Zoller & Kersh, 2006). Recent research has shown that the thymus of fish expresses estrogen receptors and that their thymus development and functionality are sensitive to estrogens (Paiola et al, 2017, 2018; Seemann et al, 2015). Thus, the relation between sex steroids and thymus involution is an intriguing avenue to explore.…”

Section: Resultsmentioning

confidence: 99%

“…However, as shown by the present study and by Lam et al (2002), expansion and rapid growth of the thymus takes place only during the juvenile period of zebrafish. This thymus development pattern appears to be more generally realized in teleost fish, with the thymus being the first lymphoid organ to differentiate morphologically (Davidson & Zon, 2004; Rombout et al, 2005; Seemann et al, 2015; Zapata et al, 2006) and becoming only functional in the juvenile period (Falk‐Petersen, 2005; Hunt & Rice, 2008; Lam et al, 2004; Mulero et al, 2007; O'Neill, 1989; Parichy et al, 2009; Tatner & Manning, 1983). This late onset of thymus development and adaptive immune systems appears to be expressed in all teleost species that have been studied to date.…”

Section: Discussionmentioning

confidence: 99%

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Thymus development in the zebrafish (Danio rerio) from an ecoimmunology perspective

et al. 2020

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The thymus is present in all gnathostome vertebrates and is an essential organ for the adaptive immune system via the generation of functional mature T‐cells. Over the life span of mammals, the thymus undergoes morphological and functional alterations, including an age‐related involution, which in humans starts in early life. Life history tradeoffs have been suggested as possible reasons for thymus involution. While in teleost fish, only a few studies have investigated alterations of thymus structure and function over different life stages, resulting in a fragmented database. Here, we investigated the thymus growth of zebrafish (Danio rerio) from early life, throughout puberty and reproductive stage, up to 1‐year‐old. We assessed thymus growth by histological and morphometric analyses and thymocyte numbers. Thymus function was assessed by measuring the transcripts of the thymocyte marker genes, ikaros, tcrα, and tcrδ. Additionally, we analyzed gonad maturity and tail homogenate vitellogenin concentrations to align thymus status with the status of the reproductive system. Our results showed that the zebrafish thymus, in contrast to the human thymus, grew strongly during early life and puberty but started to undergo involution when the fish reached the reproductive age. The involution was characterized by reduced thymus area and thymocyte number, altered histoarchitecture, and decreasing thymocyte marker gene transcript levels. Our findings suggest that age‐related changes of the zebrafish thymus do exist and could be partly explained in terms of resource tradeoffs, but also in terms of the ontogenetically late development of a functional adaptive immune system in teleosts.

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Thymus development in the zebrafish (Danio rerio) from an ecoimmunology perspective

et al. 2020

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“…The gene has been described as an important player in the rainbow trout immune response against bacteria and viruses as well correlated with increasing parasite intensity in PKD pathogenesis (Gorgoglione et al, 2013;Wang et al, 2011). However, considering the evidence of EE2 in the literature as an immunosuppressor (Cabas et al, 2012;Cuesta et al, 2007;Milla et al, 2011;Rodenas et al, 2015;Saha et al, 2004;Seemann et al, 2016;Seemann et al, 2015;Thilagam et al, 2009) the downregulation of only one immune gene hardly accounts for immunomodulation. Surprisingly, the most significant downregulated BP was cellular response to organic substance.…”

Section: Discussionmentioning

confidence: 99%

“…There is now also growing evidence that estrogenic endocrine disrupting compounds (EEDCs) can have immunomodulatory effects in fish (Casanova-Nakayama et al, 2011;Milla et al, 2011). EEDCs have been reported to modulate the innate (Cabas et al, 2012;Milla et al, 2011;Seemann et al, 2016;Seeman et al, 2013) and adaptive immune response (Casanova-Nakayama et al, 2011;Cuesta et al, 2007;Rodenas et al, 2015;Saha et al, 2004;Seemann et al, 2015;Thilagam et al, 2009) in various fish species. For example, concerning the innate immune response in sea bass, Dicentrarchus labrax, an EEDC, 17α-Ethinylestradiol (EE2) was shown to downregulated pro-inflammatory cytokines il1β and tnfα (Seeman et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

Transcriptomic analysis of the impacts of ethinylestradiol (EE2) and its consequences for proliferative kidney disease outcome in rainbow trout (Oncorhynchus mykiss)

Bailey

Siebenthal

Rehberger

et al. 2019

Comparative Biochemistry and Physiology Part C: Toxicology &

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Freshwater fish are threatened by the cumulative impact of multiple stressors. The purpose of this study was to unravel the molecular and organism level reactions of rainbow trout, Oncorhynchus mykiss, to the combined impact of two such stressors that occur in the natural habitat of salmonids. Fish were infected with either the myxozoan parasite, Tetracapsuloides bryosalmonae, which causes proliferative kidney disease (PKD), or exposed to ethinylestradiol (EE2) an estrogenic endocrine disrupting compound, or to a combination of both (PKD x EE2). PKD is a slow progressive chronic disease here we focused on a later time point (130-day postinfection (d.p.i)) when parasite intensity in the fish kidney has already started to decrease. At 130 d.p.i, RNA-seq technology was applied to the posterior kidney, the main target organ for parasite development. This resulted with 280 (PKD), 14 (EE2) and 444 (PKD x EE2) differentially expressed genes (DEGs) observed in the experimental groups. In fish exposed to the combination of stressors (PKD x EE2), a number of pathways were regulated that were neither observed in the single stressor groups. Parasite infection, alone and in combination with EE2, only resulted in a low intensity immune response that negatively correlated with an upregulation of genes involved in a variety of metabolic and inflammation resolution processes. This could indicate a trade-off whereby the host increases investment in recovery/resolution processes over immune responses at a later stage of disease. When PKD infection took place under simultaneous exposure to EE2 (PKD x EE2), parasite intensity decreased and pathological alterations in the posterior kidney were reduced in comparison to the PKD only condition. These findings suggest that EE2 modulated these response profiles in PKD infected fish, attenuating the disease impact on the fish.

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“…Similarly, the thymus, which plays a critical role in the immune response of higher vertebrates, is a known target of endogenous estrogens (Zoller and Kersh ). For example, exposure of European sea bass ( Dicentrarchus labrax ) to exogenous estrogens was recently reported to affect thymic growth and regionalization in juveniles, which may have persistent consequences for the immune function of adults (Seemann et al ).…”

Section: Knowledge Gaps In Endocrine Screening and Testingmentioning

confidence: 99%

Current limitations and recommendations to improve testing for the environmental assessment of endocrine active substances

Coady

Biever

Denslow

et al. 2017

Integr Environ Assess Manag

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In the present study, existing regulatory frameworks and test systems for assessing potential endocrine active chemicals are described, and associated challenges are discussed, along with proposed approaches to address these challenges. Regulatory frameworks vary somewhat across geographies, but all basically evaluate whether a chemical possesses endocrine activity and whether this activity can result in adverse outcomes either to humans or to the environment. Current test systems include in silico, in vitro, and in vivo techniques focused on detecting potential endocrine activity, and in vivo tests that collect apical data to detect possible adverse effects. These test systems are currently designed to robustly assess endocrine activity and/or adverse effects in the estrogen, androgen, and thyroid hormone signaling pathways; however, there are some limitations of current test systems for evaluating endocrine hazard and risk. These limitations include a lack of certainty regarding: 1) adequately sensitive species and life stages; 2) mechanistic endpoints that are diagnostic for endocrine pathways of concern; and 3) the linkage between mechanistic responses and apical, adverse outcomes. Furthermore, some existing test methods are resource intensive with regard to time, cost, and use of animals. However, based on recent experiences, there are opportunities to improve approaches to and guidance for existing test methods and to reduce uncertainty. For example, in vitro high‐throughput screening could be used to prioritize chemicals for testing and provide insights as to the most appropriate assays for characterizing hazard and risk. Other recommendations include adding endpoints for elucidating connections between mechanistic effects and adverse outcomes, identifying potentially sensitive taxa for which test methods currently do not exist, and addressing key endocrine pathways of possible concern in addition to those associated with estrogen, androgen, and thyroid signaling. Integr Environ Assess Manag 2017;13:302–316. © 2016 The Authors. Integrated Environmental Assessment and Management published by Wiley Periodicals, Inc. on behalf of Society of Environmental Toxicology & Chemistry (SETAC)

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Exogenous 17β‐oestradiol (E2) modifies thymus growth and regionalization in European sea bass Dicentrarchus labrax

Cited by 18 publications

References 58 publications

Thymus development in the zebrafish (Danio rerio) from an ecoimmunology perspective

Thymus development in the zebrafish (Danio rerio) from an ecoimmunology perspective

Transcriptomic analysis of the impacts of ethinylestradiol (EE2) and its consequences for proliferative kidney disease outcome in rainbow trout (Oncorhynchus mykiss)

Current limitations and recommendations to improve testing for the environmental assessment of endocrine active substances

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