Aging and retinoid X receptor agonists on masculinization of female Pomacea canaliculata, with a critical appraisal of imposex evaluation in the Ampullariidae

Giraud-Billoud, Maximiliano; Castro-Vázquez, Alfredo

doi:10.1016/j.ecoenv.2018.10.096

Cited by 11 publications

(6 citation statements)

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“…Unlike the previously mentioned caenogastropods, the genital system of both sexes of P. canaliculata develops from a primordial gonoduct, which can be observed from hatching [33], and from a primordial copulatory apparatus (CApp), which starts to develop between 3-5 days after hatching [33]. In adult males, this CApp reaches full development, while in young females it remains as a rudiment, corresponding to the stage 1 described by Giraud-Billoud and Castro-Vazquez [25]. It is notable, however, that the female CApp would continue its development after sexual maturity is reached, and even in old age.…”

Section: Introductionmentioning

confidence: 84%

“…Likewise, some field and laboratory studies have shown that representatives of the genus Pomacea may be useful for environmental risk assessment of diverse chemical pollutants in nature, i.e., elements (arsenic, As; cadmium, Cd; copper, Cu; mercury, Hg; lead, Pb; uranium, U; zinc, Zn) [10,[17][18][19][20][21], the herbicide glyphosate [22], the insecticides cypermethrin, bifentrin and imidacloprid [23,24]. On the other hand, under controlled laboratory conditions, organotin compounds cause a masculinizing effect on adult (4 months old) females of P. canaliculata [25,26].…”

Section: Introductionmentioning

confidence: 99%

“…It is notable, however, that the female CApp would continue its development after sexual maturity is reached, and even in old age. Growth of the female CApp is also promoted by RXR agonists and is associated with a greater expression of the RXR receptor in the CApp [ 25 ].…”

Section: Introductionmentioning

confidence: 99%

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Evaluation of female masculinization in Pomacea canaliculata (Caenogastropoda, Ampullariidae) induced by tributyltin, heavy metals, and uranium in culture water

Giraud-Billoud

Campoy-Diaz

Muñoz

et al. 2022

Environ Anal Health Toxicol

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All female Pomacea canaliculata develop a small, male-like copulatory apparatus a few days after birth, which growths slowly until sexual maturity, and even further in older age. Previous studies have found trace elements like mercury (Hg), arsenic (As) and uranium (U) in tap water used for snail culture, and that these elements were accumulated in snail tissues. Here, we test whether the presence of these metals at maximum allowed concentrations (Environmental Protection Agency - EPA) in aquarium water could affect the development of the copulatory apparatus in mature females. Females of different ages were used as controls, grown in reconstituted metal-free water with or without the addition of Hg, As and U, as well as tributyltin (TBT), a compound used as masculinizing agent. Six and seven months old females cultured in tap water showed a longer penis and penile sheath, and a greater overall development of the copulatory apparatus, measured by an index (DI), as compared with same-age females cultured in reconstituted water. Moreover, when females were exposed to Hg, As or U at the maximum contaminant levels for human consumption allowed by EPA regulations, there was no further development of the copulatory apparatus, while there was a clearly positive effect in TBT-exposed females. This study confirms the masculinizing effect of organotin compounds on female copulatory apparatus and discusses the usefulness of the development of these organs as a bioindicator of environmental pollution.

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Section: Introductionmentioning

confidence: 84%

Section: Introductionmentioning

confidence: 99%

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Evaluation of female masculinization in Pomacea canaliculata (Caenogastropoda, Ampullariidae) induced by tributyltin, heavy metals, and uranium in culture water

Giraud-Billoud

Campoy-Diaz

Muñoz

et al. 2022

Environ Anal Health Toxicol

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“…RXR belongs to the NR 2 B nuclear receptor family and can form a dimer with peroxisome-activated receptor gamma (PPARγ), a member of the nuclear receptor super family ( Giraud-Billoud and Castro-Vazquez, 2019 , Koshiishi et al, 2019 ). Being a selective RXR receptor agonist, Bexarotene can stimulate the RXR-PPAR γ dimer formation by activating RXR, and the activated dimer can, in turn, regulate the expression of downstream genes and serve as a variety of haematogenic role ( Escudero et al, 2015 ).…”

Section: Discussionmentioning

confidence: 99%

iTRAQ-derived quantitative proteomics uncovers the neuroprotective property of bexarotene in a mice model of cerebral ischemia–reperfusion injury

Liu

Wang

Chen

et al. 2022

Saudi Pharmaceutical Journal

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“…Regarding PPARγ actions, Pascoal et al 67 showed that the PPARγ ligand Rosi elicited the same imposex response in N. lapillus as TBT. However, Giraud-Billoud et al 68 reported that Rosi was not able to induce imposex in a phylogenetically distant gastropod Pomacea canaliculata. This difference indicates that different molecular mechanisms may regulate imposex induction in ampullariid and neogastropod species suggesting that the direct role of PPARγ in imposex deserves further investigation.…”

Section: Discussionmentioning

confidence: 99%

RXR Expression in Marine Gastropods with Different Sensitivity to Imposex Development

Giulianelli

Primost

Lanari

et al. 2020

Sci Rep

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The superposition of male sexual characteristics in female marine gastropods (imposex) represents one of the clearest ecological examples of organotin-mediated endocrine disruption. Recent evidences suggest that signaling pathways mediated by members of the nuclear receptor superfamily, RXR and PPARγ, are involved in the development of this pseudohermaphroditic condition. Here, we identified significant differences in RXR expression in two caenogastropod species from Nuevo Gulf, Argentina, Buccinanops globulosus and Trophon geversianus, which present clear contrast in imposex incidence. In addition, B. globulosus males from a polluted and an unpolluted area showed differences in RXR expression. Conversely, PPARγ levels were similar between both analyzed species. These findings indicate specie-specific RXR and PPARγ expression, suggesting a major role of RXR in the induction of imposex. Endocrine disrupting chemicals are compounds that alter the normal functioning of the endocrine system of both humans and wildlife 1. One of most relevant examples of environmental endocrine disruption in marine gastropods is the phenomenon of imposex 2 , described as an irreversible syndrome in which a female develops male-type genital organs, such as the penis and vas deferens 3,4. Imposex is intimately associated with tributyltin (TBT) marine environmental pollution 5. TBT is a common compound in marine antifouling paints, currently used in several countries 6 despite having been banned worldwide for more than 10 years 7. Although imposex levels appear to be reduced in some regions of the planet 8,9 after global ban of organotin antifoulant paints, assessing the incidence of imposex as a biomarker of TBT contamination seems to be a valuable indicator in other regions of the world such as Latin America 10-12 or South Africa 13 where TBT-based antifouling paints are still in use. The use of TBT, under controlled laboratory conditions, diluted in the water or directly injected to gastropods, was able to induce imposex in several caenogastropods 14-19. Different mechanisms have been proposed to explain the induction of imposex by TBT such as an increase in androgen levels, the involvement of penis morphogenetic/retrogressive factor, or even an increase in the neuropeptide alanine-proline-glycine-tryptophan amide 20. However, a considerable body of evidence indicates that TBT-induced imposex involves the abnormal modulation of the retinoid X receptor (RXR) signaling pathway 20-23. RXR are members of the nuclear receptor superfamily of transcription factors 24. They are activated by retinoic acid, the main derivative of vitamin A, involved in multiple signaling pathways critical for embryonic development, metabolic processes, differentiation and apoptosis in vertebrates 25,26. Although retinoid physiology is poorly understood in marine gastropods 27 , recent findings support their role during gonad maturation 28. RXR was cloned in different caenogastropods, namely, Thais clavigera 18 , Nucella lapillus 14 , Ilyanassa obsoleta 29 , Hex...

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Aging and retinoid X receptor agonists on masculinization of female Pomacea canaliculata, with a critical appraisal of imposex evaluation in the Ampullariidae

Cited by 11 publications

References 57 publications

Evaluation of female masculinization in Pomacea canaliculata (Caenogastropoda, Ampullariidae) induced by tributyltin, heavy metals, and uranium in culture water

Evaluation of female masculinization in Pomacea canaliculata (Caenogastropoda, Ampullariidae) induced by tributyltin, heavy metals, and uranium in culture water

iTRAQ-derived quantitative proteomics uncovers the neuroprotective property of bexarotene in a mice model of cerebral ischemia–reperfusion injury

RXR Expression in Marine Gastropods with Different Sensitivity to Imposex Development

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