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The diatom-derived aldehyde decadienal affects life cycle transition in the ascidian Ciona intestinalis through nitric oxide/ERK signalling.

Castellano I, Ercolesi E, Romano G, Ianora A, Palumbo A - Open Biol (2015)

Bottom Line: PUAs, including 2,4-trans-decadienal (DD), induce deleterious effects on embryonic and larval development of several planktonic and benthic organisms.DD affects redox balance by reducing total glutathione and NO levels.By biochemical and quantitative gene expression analysis, we identify the NO-signalling network affected by DD, including the upregulation of ERK phosphatase mkp1 and consequent reduction of ERK phosphorylation, with final changes in the expression of downstream ERK target genes.

View Article: PubMed Central - PubMed

Affiliation: Stazione Zoologica Anton Dohrn, Villa Comunale, 80121 Naples, Italy.

ABSTRACT
Polyunsaturated aldehydes (PUAs) are fatty-acid-derived metabolites produced by some microalgae, including different diatom species. PUAs are mainly produced as a wound-activated defence mechanism against microalgal predators or released from senescent cells at the end of a bloom. PUAs, including 2,4-trans-decadienal (DD), induce deleterious effects on embryonic and larval development of several planktonic and benthic organisms. Here, we report on the effects of DD on larval development and metamorphosis of the ascidian Ciona intestinalis. Ciona larval development is regulated by the cross-talking of different molecular events, including nitric oxide (NO) production, ERK activation and caspase 3-dependent apoptosis. We report that treatment with DD at the competence larval stage results in a delay in metamorphosis. DD affects redox balance by reducing total glutathione and NO levels. By biochemical and quantitative gene expression analysis, we identify the NO-signalling network affected by DD, including the upregulation of ERK phosphatase mkp1 and consequent reduction of ERK phosphorylation, with final changes in the expression of downstream ERK target genes. Overall, these results give new insights into the molecular pathways induced in marine organisms after exposure to PUAs during larval development, demonstrating that this aldehyde affects key checkpoints of larval transition from the vegetative to the reproductive life stage.

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Decadienal (DD) induces ERK dephosphorylation. Middle stage larvae were treated with 0.5 µg ml−1 DD. Samples collected after 2, 4 and 8 h of treatment were examined for ERK activation. (a) Representative experiment showing a Western blot with anti-P-ERK and anti-ERK antibodies. (b) Histograms representing densitometric data analyses of P-ERK versus ERK intensity bands from three independent experiments reported as means ± s.e.m. and assessed by unpaired t-test. Asterisks represent significant differences with respect to the control: **p < 0.01, ***p < 0.001.
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RSOB140182F5: Decadienal (DD) induces ERK dephosphorylation. Middle stage larvae were treated with 0.5 µg ml−1 DD. Samples collected after 2, 4 and 8 h of treatment were examined for ERK activation. (a) Representative experiment showing a Western blot with anti-P-ERK and anti-ERK antibodies. (b) Histograms representing densitometric data analyses of P-ERK versus ERK intensity bands from three independent experiments reported as means ± s.e.m. and assessed by unpaired t-test. Asterisks represent significant differences with respect to the control: **p < 0.01, ***p < 0.001.

Mentions: ERK activation represents a key event in Ciona life cycle transition. Its inhibition hampers the wave of apoptosis and subsequent metamorphosis of the ascidian [27,28]. We therefore decided to investigate the effect of DD on ERK phosphorylation. DD induced a significant decrease in P-ERK as early as 2 h post-treatment (figure 5a). The densitometric analysis of the P-ERK immunopositive bands with respect to the constitutive ERK band revealed a significant reduction of ERK phosphorylation at 2, 4 and 8 h after treatment (figure 5b).Figure 5.


The diatom-derived aldehyde decadienal affects life cycle transition in the ascidian Ciona intestinalis through nitric oxide/ERK signalling.

Castellano I, Ercolesi E, Romano G, Ianora A, Palumbo A - Open Biol (2015)

Decadienal (DD) induces ERK dephosphorylation. Middle stage larvae were treated with 0.5 µg ml−1 DD. Samples collected after 2, 4 and 8 h of treatment were examined for ERK activation. (a) Representative experiment showing a Western blot with anti-P-ERK and anti-ERK antibodies. (b) Histograms representing densitometric data analyses of P-ERK versus ERK intensity bands from three independent experiments reported as means ± s.e.m. and assessed by unpaired t-test. Asterisks represent significant differences with respect to the control: **p < 0.01, ***p < 0.001.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4389792&req=5

RSOB140182F5: Decadienal (DD) induces ERK dephosphorylation. Middle stage larvae were treated with 0.5 µg ml−1 DD. Samples collected after 2, 4 and 8 h of treatment were examined for ERK activation. (a) Representative experiment showing a Western blot with anti-P-ERK and anti-ERK antibodies. (b) Histograms representing densitometric data analyses of P-ERK versus ERK intensity bands from three independent experiments reported as means ± s.e.m. and assessed by unpaired t-test. Asterisks represent significant differences with respect to the control: **p < 0.01, ***p < 0.001.
Mentions: ERK activation represents a key event in Ciona life cycle transition. Its inhibition hampers the wave of apoptosis and subsequent metamorphosis of the ascidian [27,28]. We therefore decided to investigate the effect of DD on ERK phosphorylation. DD induced a significant decrease in P-ERK as early as 2 h post-treatment (figure 5a). The densitometric analysis of the P-ERK immunopositive bands with respect to the constitutive ERK band revealed a significant reduction of ERK phosphorylation at 2, 4 and 8 h after treatment (figure 5b).Figure 5.

Bottom Line: PUAs, including 2,4-trans-decadienal (DD), induce deleterious effects on embryonic and larval development of several planktonic and benthic organisms.DD affects redox balance by reducing total glutathione and NO levels.By biochemical and quantitative gene expression analysis, we identify the NO-signalling network affected by DD, including the upregulation of ERK phosphatase mkp1 and consequent reduction of ERK phosphorylation, with final changes in the expression of downstream ERK target genes.

View Article: PubMed Central - PubMed

Affiliation: Stazione Zoologica Anton Dohrn, Villa Comunale, 80121 Naples, Italy.

ABSTRACT
Polyunsaturated aldehydes (PUAs) are fatty-acid-derived metabolites produced by some microalgae, including different diatom species. PUAs are mainly produced as a wound-activated defence mechanism against microalgal predators or released from senescent cells at the end of a bloom. PUAs, including 2,4-trans-decadienal (DD), induce deleterious effects on embryonic and larval development of several planktonic and benthic organisms. Here, we report on the effects of DD on larval development and metamorphosis of the ascidian Ciona intestinalis. Ciona larval development is regulated by the cross-talking of different molecular events, including nitric oxide (NO) production, ERK activation and caspase 3-dependent apoptosis. We report that treatment with DD at the competence larval stage results in a delay in metamorphosis. DD affects redox balance by reducing total glutathione and NO levels. By biochemical and quantitative gene expression analysis, we identify the NO-signalling network affected by DD, including the upregulation of ERK phosphatase mkp1 and consequent reduction of ERK phosphorylation, with final changes in the expression of downstream ERK target genes. Overall, these results give new insights into the molecular pathways induced in marine organisms after exposure to PUAs during larval development, demonstrating that this aldehyde affects key checkpoints of larval transition from the vegetative to the reproductive life stage.

Show MeSH
Related in: MedlinePlus