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Sci Rep
2018 Mar 15;81:4610. doi: 10.1038/s41598-018-22861-1.
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Biotic and environmental stress induces nitration and changes in structure and function of the sea urchin major yolk protein toposome.
Castellano I
,
Migliaccio O
,
Ferraro G
,
Maffioli E
,
Marasco D
,
Merlino A
,
Zingone A
,
Tedeschi G
,
Palumbo A
.
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The major yolk protein toposome plays crucial roles during gametogenesis and development of sea urchins. We previously found that nitration of toposome increases in the gonads of a Paracentrotus lividus population living in a marine protected area affected by toxic blooms of Ostreospsis cf. ovata, compared to control populations. This modification is associated with ovatoxin accumulation, high levels of nitric oxide in the gonads, and a remarkable impairment of progeny development. However, nothing is known about the environmental-mediated-regulation of the structure and biological function of toposome. Here, we characterize through wide-ranging biochemical and structural analyses the nitrated toposome of sea urchins exposed to the bloom, and subsequently detoxified. The increased number of nitrated tyrosines in toposome of sea urchins collected during algal bloom induced structural changes and improvement of the Ca2+-binding affinity of the protein. After 3 months'' detoxification, ovatoxin was undetectable, and the number of nitric oxide-modified tyrosines was reduced. However, the nitration of specific residues was irreversible and occurred also in embryos treated with metals, used as a proxy of environmental pollutants. The structural and functional changes of toposome caused by nitration under adverse environmental conditions may be related to the defective development of sea urchins'' progeny.
Figure 3. Scheme of nitrated residues of toposome. Sequence coverage and nitrated residues of toposome of sea urchins collected prior to the bloom (C), at the bloom phase (T0), and after stabulation in sea water for 56 (T1) and 92 days (T2). The figure shows the sequence coverage of toposome and the nitrated residues indicated as a black line.
Figure 4. Structural properties and Ca2+ affinity of toposome. Far UV CD and intrinsic fluorescence spectra of toposome purified from control and T0 animals. CD spectra (panel a,b) measured in 10 mM Tris-HCl buffer at pH = 7.8 and 10 °C. Spectra of the proteins (0.1 mg mL−1) were compared with that obtained for a sample upon treatment with EDTA and after addition of 1 mM Ca2+. Intrinsic fluorescence spectra (panel c,d) measured in 10 mM Tris-HCl buffer at pH = 7.8 and 20 °C. Spectra of the proteins (0.05 mg mL−1) were compared with those obtained for the protein upon addition of increasing concentration of Ca2+ (protein to Ca2+ molar ratio between 1:0.3 and 1:20).
Figure 5. Ca2+ binding properties of toposome. ITC Calorimetric raw and integrated data for C (20 µM) titration with CaCl2 (2 mM). Data fitting was achieved with ‘one set of sites’ model.
Figure 6. Pattern of nitrated proteins in sea urchin embryos after metals treatment. (a) Early blastula stage. (b) Swimming blastula stage. 1 = Control in sea water, 2 = Mn2+ 1.8 × 10−5 M, 3 = Mn2+ 3.6 × 10−5 M, 4 = Mn2+ 7.8 × 10−5 M, 5 = Mn2+ 15.5 × 10−5 M, 6 = Mn2+ 31.2 × 10−5 M, 7 = Cd2+ 5 × 10−7 M, 8 = Cd2+ 10−6 M, 9 = 5.2 × 10−6 M. Representative experiment showing the western blot analysis with anti-nitrotyrosine (anti-NT) antibodies. Anti-actin is used as loading control.
Figure 7. Scheme of nitrated residues of toposome after metals treatment. Nitrated residues are indicated as a black line. In red the residues found nitrated also in samples collected at bloom (T0) or after stabulation (T1, T2) in sea water (see Fig. 3 for the comparison).
Brooks,
The major yolk protein of sea urchins is endocytosed by a dynamin-dependent mechanism.
2004, Pubmed,
Echinobase
Brooks,
The major yolk protein of sea urchins is endocytosed by a dynamin-dependent mechanism.
2004,
Pubmed
,
Echinobase
Bryan,
Methods to detect nitric oxide and its metabolites in biological samples.
2007,
Pubmed
Castellano,
The diatom-derived aldehyde decadienal affects life cycle transition in the ascidian Ciona intestinalis through nitric oxide/ERK signalling.
2015,
Pubmed
Castellano,
Shedding light on ovothiol biosynthesis in marine metazoans.
2016,
Pubmed
,
Echinobase
Cervello,
Evidence of a precursor-product relationship between vitellogenin and toposome, a glycoprotein complex mediating cell adhesion.
1989,
Pubmed
,
Echinobase
Coccetti,
The CK2 phosphorylation of catalytic domain of Cdc34 modulates its activity at the G1 to S transition in Saccharomyces cerevisiae.
2008,
Pubmed
Dev,
Comparative biochemical analysis of the major yolk protein in the sea urchin egg and coelomic fluid.
2014,
Pubmed
,
Echinobase
Evans,
Transcriptomic responses to ocean acidification in larval sea urchins from a naturally variable pH environment.
2013,
Pubmed
,
Echinobase
Ghisaura,
Proteomic dataset of Paracentrotus lividus gonads of different sexes and at different maturation stages.
2016,
Pubmed
,
Echinobase
Ghisaura,
Proteomic changes occurring along gonad maturation in the edible sea urchin Paracentrotus lividus.
2016,
Pubmed
,
Echinobase
Giga,
Purification of the most abundant protein in the coelomic fluid of a sea urchin which immunologically cross reacts with 23S glycoprotein in the sea urchin eggs.
1985,
Pubmed
,
Echinobase
Giga,
Purification and physical chemical characterization of 23S glycoprotein from sea urchin (Anthocidaris crassispina) eggs.
1985,
Pubmed
,
Echinobase
Gratwohl,
Storage, ultrastructural targeting and function of toposomes and hyalin in sea urchin embryogenesis.
1991,
Pubmed
,
Echinobase
Hayley,
Biochemical analysis of the interaction of calcium with toposome: a major protein component of the sea urchin egg and embryo.
2008,
Pubmed
,
Echinobase
Hayley,
Biochemical analysis of a Ca2+-dependent membrane-membrane interaction mediated by the sea urchin yolk granule protein, toposome.
2006,
Pubmed
,
Echinobase
Ischiropoulos,
Protein tyrosine nitration--an update.
2009,
Pubmed
Kummer,
Nitration of tyrosine 10 critically enhances amyloid β aggregation and plaque formation.
2011,
Pubmed
Kuo,
NO is necessary and sufficient for egg activation at fertilization.
2000,
Pubmed
,
Echinobase
Lister,
Maternal antioxidant provisioning mitigates pollutant-induced oxidative damage in embryos of the temperate sea urchin Evechinus chloroticus.
2017,
Pubmed
,
Echinobase
Malkin,
A crystalline protein of high molecular weight from cytoplasmic granules in sea urchin eggs and embryos.
1965,
Pubmed
,
Echinobase
Matese,
Regulated exocytosis and sequential construction of the extracellular matrix surrounding the sea urchin zygote.
1997,
Pubmed
,
Echinobase
Matranga,
Functional characterization of toposomes from sea urchin blastula embryos by a morphogenetic cell aggregation assay.
1986,
Pubmed
,
Echinobase
Migliaccio,
Subtle reproductive impairment through nitric oxide-mediated mechanisms in sea urchins from an area affected by harmful algal blooms.
2016,
Pubmed
,
Echinobase
Migliaccio,
Stress response to cadmium and manganese in Paracentrotus lividus developing embryos is mediated by nitric oxide.
2014,
Pubmed
,
Echinobase
Migliaccio,
Maternal Exposure to Cadmium and Manganese Impairs Reproduction and Progeny Fitness in the Sea Urchin Paracentrotus lividus.
2015,
Pubmed
,
Echinobase
Mohri,
Nitric oxide (NO) increase at fertilization in sea urchin eggs upregulates fertilization envelope hardening.
2008,
Pubmed
,
Echinobase
Noll,
The toposome, essential for sea urchin cell adhesion and development, is a modified iron-less calcium-binding transferrin.
2007,
Pubmed
,
Echinobase
Noll,
Characterization of toposomes from sea urchin blastula cells: a cell organelle mediating cell adhesion and expressing positional information.
1985,
Pubmed
,
Echinobase
Radi,
Protein tyrosine nitration: biochemical mechanisms and structural basis of functional effects.
2013,
Pubmed
Reed,
A set of constructed type spectra for the practical estimation of peptide secondary structure from circular dichroism.
1997,
Pubmed
Santella,
Fertilization in echinoderms.
2012,
Pubmed
,
Echinobase
Scaturro,
The oligomeric integrity of toposome is essential for its morphogenetic function.
1998,
Pubmed
,
Echinobase
Thaler,
Nitric oxide in oocyte maturation, ovulation, fertilization, cleavage and implantation: a little dab'll do ya.
2003,
Pubmed
Toffolo,
Phosphorylation of neuronal Lysine-Specific Demethylase 1LSD1/KDM1A impairs transcriptional repression by regulating interaction with CoREST and histone deacetylases HDAC1/2.
2014,
Pubmed
Unuma,
A Protein Identical to the Yolk Protein Is Stored in the Testis in Male Red Sea Urchin, Pseudocentrotus depressus.
1998,
Pubmed
,
Echinobase
Unuma,
The major yolk protein is synthesized in the digestive tract and secreted into the body cavities in sea urchin larvae.
2009,
Pubmed
,
Echinobase
Unuma,
Quantitative changes in yolk protein and other components in the ovary and testis of the sea urchin Pseudocentrotus depressus.
2003,
Pubmed
,
Echinobase
Unuma,
Accumulation of the major yolk protein and zinc in the agametogenic sea urchin gonad.
2011,
Pubmed
,
Echinobase
Unuma,
Zinc-binding property of the major yolk protein in the sea urchin - implications of its role as a zinc transporter for gametogenesis.
2007,
Pubmed
,
Echinobase
Unuma,
The sea urchin major yolk protein is synthesized mainly in the gut inner epithelium and the gonadal nutritive phagocytes before and during gametogenesis.
2010,
Pubmed
,
Echinobase
Wessel,
Cell surface changes in the egg at fertilization.
2009,
Pubmed
,
Echinobase
