ECB-ART-49339
Biology (Basel)
2021 Feb 01;102:. doi: 10.3390/biology10020103.
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Gene Expression Changes after Parental Exposure to Metals in the Sea Urchin Affect Timing of Genetic Programme of Embryo Development.
Masullo T
,
Biondo G
,
Natale MD
,
Tagliavia M
,
Bennici CD
,
Musco M
,
Ragusa MA
,
Costa S
,
Cuttitta A
,
Nicosia A
.
Abstract
It is widely accepted that phenotypic traits can be modulated at the epigenetic level so that some conditions can affect the progeny of exposed individuals. To assess if the exposure of adult animals could result in effects on the offspring, the Mediterranean sea urchin and its well-characterized gene regulatory networks (GRNs) was chosen as a model. Adult animals were exposed to known concentrations of zinc and cadmium (both individually and in combination) for 10 days, and the resulting embryos were followed during the development. The oxidative stress occurring in parental gonads, embryo phenotypes and mortality, and the expression level of a set of selected genes, including members of the skeletogenic and endodermal GRNs, were evaluated. Increased oxidative stress at F0, high rates of developmental aberration with impaired gastrulation, in association to deregulation of genes involved in skeletogenesis (dri, hex, sm50, p16, p19, msp130), endodermal specification (foxa, hox11/13b, wnt8) and epigenetic regulation (kat2A, hdac1, ehmt2, phf8 and UBE2a) occurred either at 24 or 48 hpf. Results strongly indicate that exposure to environmental pollutants can affect not only directly challenged animals but also their progeny (at least F1), influencing optimal timing of genetic programme of embryo development, resulting in an overall impairment of developmental success.
PubMed ID: 33535713
PMC ID: PMC7912929
Article link: Biology (Basel)
Grant support: [+]
wp3 CIPE-Centro Internazionale di Studi avanzati su Ambiente e Salute-CISAS
Article Images: [+] show captions
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Figure 1. Redox response system of P. lividus reproductive tissues (testis and ovary) after exposures to high (H), low (L) doses of Cd, Zn or a mix of both metals, as reported in Table 1. (A) Total ROS amount; (B) catalase activity; (C) relative HSP70 protein amount; (D) relative HSP60 protein amount; (E) relative HSP90 protein amount. Bars represent the mean values from the three different experiments ± SD. Statistical significance among testis and ovary results is shown as asterisks (*: p < 0.05; **: p < 0.01; ***: p < 0.001). Letters denote statistical significance of treated specimens vs. controls (b: p < 0.01; a: p < 0.001). |
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Figure 2. Embryo morphological abnormalities at 24 and 48 hpf and percentages in response to the different treatments (Cd, Zn and Mix of them) experienced by parentals. Data corresponding to embryos from means of three experiments are shown; SD were lower than 5%. L: low concentration; H: high concentration; Ab: abnormal. |
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Figure 3. Parental exposures to low doses of Zn and metal mixture (as defined in Table 1) induce alterations in the mRNA expression of development and epigenetic related genes at 24 hpf. RT-qPCR results showing the mRNA levels of indicated genes in P. lividus offspring, with respect to 18S at 24 hpf. Bars represent mean ± SD. Values were considered statistically significant at p less than 0.05 (*). |
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Figure 4. Parental exposures to low doses of Zn and metal mixture (as defined in Table 1) induce alterations in the mRNA expression of development and epigenetic related genes at 48 hpf. RT-qPCR results showing the mRNA levels of indicated genes in P. lividus offspring, with respect to 18S at 48 hpf. Bars represent mean ± SD. Values were considered statistically significant at p less than 0.05 (*). |
References [+] :
Anello,
Developmental effects of the protein kinase inhibitor kenpaullone on the sea urchin embryo.
2018, Pubmed,
Echinobase
Anello, Developmental effects of the protein kinase inhibitor kenpaullone on the sea urchin embryo. 2018, Pubmed , Echinobase
Ben-Tabou de-Leon, Gene regulation: gene control network in development. 2007, Pubmed , Echinobase
Bertoldo, Impacts of and interactions between environmental stress and epigenetic programming during early embryo development. 2015, Pubmed
Bessodes, Reciprocal signaling between the ectoderm and a mesendodermal left-right organizer directs left-right determination in the sea urchin embryo. 2012, Pubmed , Echinobase
Bishop, Zinc stimulates the production of toxic reactive oxygen species (ROS) and inhibits glutathione reductase in astrocytes. 2007, Pubmed
Bonaventura, UVB radiation prevents skeleton growth and stimulates the expression of stress markers in sea urchin embryos. 2005, Pubmed , Echinobase
Bonduriansky, Rethinking heredity, again. 2012, Pubmed
Briggs, In the beginning...animal fertilization and sea urchin development. 2006, Pubmed , Echinobase
Cao, Accumulation and oxidative stress biomarkers in Japanese flounder larvae and juveniles under chronic cadmium exposure. 2010, Pubmed
Cavalieri, Environmental epigenetics in zebrafish. 2017, Pubmed
Chen, LncRNA Functions as a New Emerging Epigenetic Factor in Determining the Fate of Stem Cells. 2020, Pubmed
Clark, Molecular mechanisms underpinning transgenerational plasticity in the green sea urchin Psammechinus miliaris. 2019, Pubmed , Echinobase
Costa, An Intronic cis-Regulatory Element Is Crucial for the Alpha Tubulin Pl-Tuba1a Gene Activation in the Ciliary Band and Animal Pole Neurogenic Domains during Sea Urchin Development. 2017, Pubmed , Echinobase
Davidson, Emerging properties of animal gene regulatory networks. 2010, Pubmed
Di Natale, Aberrant gene expression profiles in Mediterranean sea urchin reproductive tissues after metal exposures. 2019, Pubmed , Echinobase
Donelson, Transgenerational plasticity mitigates the impact of global warming to offspring sex ratios. 2015, Pubmed
Du, Oxidative damage and cellular defense mechanisms in sea urchin models of aging. 2013, Pubmed , Echinobase
Duboc, Left-right asymmetry in the sea urchin embryo is regulated by nodal signaling on the right side. 2005, Pubmed , Echinobase
Dupont, Impact of near-future ocean acidification on echinoderms. 2010, Pubmed , Echinobase
Evans, Transcriptomic responses to ocean acidification in larval sea urchins from a naturally variable pH environment. 2013, Pubmed , Echinobase
Evans, Transcriptomic responses to seawater acidification among sea urchin populations inhabiting a natural pH mosaic. 2017, Pubmed , Echinobase
Gadhia, Trace metals alter DNA repair and histone modification pathways concurrently in mouse embryonic stem cells. 2012, Pubmed
Garfield, The impact of gene expression variation on the robustness and evolvability of a developmental gene regulatory network. 2013, Pubmed , Echinobase
Genchi, The Effects of Cadmium Toxicity. 2020, Pubmed
Gilbert, Ecological developmental biology: environmental signals for normal animal development. 2012, Pubmed
Gildor, Comparative Study of Regulatory Circuits in Two Sea Urchin Species Reveals Tight Control of Timing and High Conservation of Expression Dynamics. 2015, Pubmed , Echinobase
Goncalves, Rapid transcriptional acclimation following transgenerational exposure of oysters to ocean acidification. 2016, Pubmed
Gupta, Heat shock proteins in toxicology: how close and how far? 2010, Pubmed
Hamdoun, Embryo stability and vulnerability in an always changing world. 2007, Pubmed
Henikoff, Epigenetics, cellular memory and gene regulation. 2016, Pubmed
Hofmann, Living in the now: physiological mechanisms to tolerate a rapidly changing environment. 2010, Pubmed
Howard-Ashby, Gene families encoding transcription factors expressed in early development of Strongylocentrotus purpuratus. 2006, Pubmed , Echinobase
John, Developmental Epigenetics: Phenotype and the Flexible Epigenome. 2018, Pubmed
Klosin, Mechanisms, timescales and principles of trans-generational epigenetic inheritance in animals. 2016, Pubmed
Knudson, Of sea urchins and worms: development and cancer. 2004, Pubmed , Echinobase
La Torre, Assessment and Monitoring of Fish Quality from a Coastal Ecosystem under High Anthropic Pressure: A Case Study in Southern Italy. 2020, Pubmed
Lapraz, A deuterostome origin of the Spemann organiser suggested by Nodal and ADMPs functions in Echinoderms. 2015, Pubmed , Echinobase
Lister, Dietary pollutants induce oxidative stress, altering maternal antioxidant provisioning and reproductive output in the temperate sea urchin Evechinus chloroticus. 2016, Pubmed , Echinobase
Lister, Maternal antioxidant provisioning mitigates pollutant-induced oxidative damage in embryos of the temperate sea urchin Evechinus chloroticus. 2017, Pubmed , Echinobase
Livak, Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. 2001, Pubmed
Livingstone, Contaminant-stimulated reactive oxygen species production and oxidative damage in aquatic organisms. 2001, Pubmed
Lyko, The DNA methyltransferase family: a versatile toolkit for epigenetic regulation. 2018, Pubmed
Marshall, Transgenerational plasticity in the sea: context-dependent maternal effects across the life history. 2008, Pubmed
Martinez-Zamudio, Environmental epigenetics in metal exposure. 2011, Pubmed
Martínez-Soto, Seasonal variation and sources of dissolved trace metals in Maó Harbour, Minorca Island. 2016, Pubmed
Matranga, Long-term environmental exposure to metals (Cu, Cd, Pb, Zn) activates the immune cell stress response in the common European sea star (Asterias rubens). 2012, Pubmed , Echinobase
Matranga, Embryonic development and skeletogenic gene expression affected by X-rays in the Mediterranean sea urchin Paracentrotus lividus. 2010, Pubmed , Echinobase
Migliaccio, Maternal Exposure to Cadmium and Manganese Impairs Reproduction and Progeny Fitness in the Sea Urchin Paracentrotus lividus. 2015, Pubmed , Echinobase
Morroni, First molecular evidence of the toxicogenetic effects of copper on sea urchin Paracentrotus lividus embryo development. 2019, Pubmed , Echinobase
Munday, Transgenerational acclimation of fishes to climate change and ocean acidification. 2014, Pubmed
Navarro, Transcriptional response of stress genes to metal exposure in zebra mussel larvae and adults. 2011, Pubmed
Nicosia, Characterization of Translationally Controlled Tumour Protein from the Sea Anemone Anemonia viridis and Transcriptome Wide Identification of Cnidarian Homologues. 2018, Pubmed
Nicosia, Transcriptional and biochemical effects of cadmium and manganese on the defense system of Octopus vulgaris paralarvae. 2015, Pubmed
Peter, Assessing regulatory information in developmental gene regulatory networks. 2017, Pubmed , Echinobase
Poustka, A global view of gene expression in lithium and zinc treated sea urchin embryos: new components of gene regulatory networks. 2007, Pubmed , Echinobase
Ragusa, A Survey on Tubulin and Arginine Methyltransferase Families Sheds Light on P. lividus Embryo as Model System for Antiproliferative Drug Development. 2019, Pubmed , Echinobase
Ragusa, Coexposure to sulfamethoxazole and cadmium impairs development and attenuates transcriptional response in sea urchin embryo. 2017, Pubmed , Echinobase
Ragusa, Metallothionein Gene Family in the Sea Urchin Paracentrotus lividus: Gene Structure, Differential Expression and Phylogenetic Analysis. 2017, Pubmed , Echinobase
Ragusa, Effects of cadmium exposure on sea urchin development assessed by SSH and RT-qPCR: metallothionein genes and their differential induction. 2013, Pubmed , Echinobase
Roccheri, Cadmium induces the expression of specific stress proteins in sea urchin embryos. 2004, Pubmed , Echinobase
Schäfer, Sex-specific biochemical and histological differences in gonads of sea urchins (Psammechinus miliaris) and their response to phenanthrene exposure. 2011, Pubmed , Echinobase
Shama, Transgenerational effects persist down the maternal line in marine sticklebacks: gene expression matches physiology in a warming ocean. 2016, Pubmed
Stamateris, The expression and distribution of Wnt and Wnt receptor mRNAs during early sea urchin development. 2010, Pubmed , Echinobase
Strader, Ocean acidification promotes broad transcriptomic responses in marine metazoans: a literature survey. 2020, Pubmed
Sultan, Development in context: the timely emergence of eco-devo. 2007, Pubmed
Turturici, Perturbation of Developmental Regulatory Gene Expression by a G-Quadruplex DNA Inducer in the Sea Urchin Embryo. 2018, Pubmed , Echinobase
Varotto, DNA damage and transcriptional changes in the gills of mytilus galloprovincialis exposed to nanomolar doses of combined metal salts (Cd, Cu, Hg). 2013, Pubmed
Varrella, Toxic Diatom Aldehydes Affect Defence Gene Networks in Sea Urchins. 2016, Pubmed , Echinobase
Vergara-Amado, Differential expression of stress candidate genes for thermal tolerance in the sea urchin Loxechinus albus. 2017, Pubmed , Echinobase
Wah Chu, Synergistic toxicity of multiple heavy metals is revealed by a biological assay using a nematode and its transgenic derivative. 2002, Pubmed
Wong, Transcriptomics reveal transgenerational effects in purple sea urchin embryos: Adult acclimation to upwelling conditions alters the response of their progeny to differential pCO2 levels. 2018, Pubmed , Echinobase
Zhao, Transgenerational effects of ocean warming on the sea urchin Strongylocentrotus intermedius. 2018, Pubmed , Echinobase
Zheng, Different effects of low- and high-dose waterborne zinc on Zn accumulation, ROS levels, oxidative damage and antioxidant responses in the liver of large yellow croaker Pseudosciaena crocea. 2017, Pubmed
de-Leon, Information processing at the foxa node of the sea urchin endomesoderm specification network. 2010, Pubmed , Echinobase