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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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Related in: MedlinePlus

Mkp1 inhibition induces larval settlement. Hatched larvae were treated with 0.25 μM mkp inhibitor dusp1/6 I and examined after 4 h of treatment for larval settlement (a) and ERK activation (b). (a) The number of swimming larvae (white bars) and larvae just attached to the substrate (grey bars) were counted and reported as percentage of the total. (b) Western blot with anti-P-ERK and anti-ERK antibodies and relative histograms representing densitometric data analyses of P-ERK versus ERK intensity bands. Results are representative of five independent experiments. Data are expressed as means ± s.e.m. and were assessed by unpaired t-test. Asterisks represent significant differences with respect to the control: ***p < 0.001.
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RSOB140182F7: Mkp1 inhibition induces larval settlement. Hatched larvae were treated with 0.25 μM mkp inhibitor dusp1/6 I and examined after 4 h of treatment for larval settlement (a) and ERK activation (b). (a) The number of swimming larvae (white bars) and larvae just attached to the substrate (grey bars) were counted and reported as percentage of the total. (b) Western blot with anti-P-ERK and anti-ERK antibodies and relative histograms representing densitometric data analyses of P-ERK versus ERK intensity bands. Results are representative of five independent experiments. Data are expressed as means ± s.e.m. and were assessed by unpaired t-test. Asterisks represent significant differences with respect to the control: ***p < 0.001.

Mentions: To confirm the role of mkp1 in the regulation of ERK activity during larval development, we treated hatched larvae with 0.25 µM of the dual-specific phosphatase inhibitor (dusp 1/6 I). After 4 h of treatment, the inhibitor caused an increase in larval settlement, as assessed by the significant increase of larvae attached to the substrate and the concomitant decrease of swimming larvae with respect to the control (figure 7a). The specificity of the inhibitor for ERK activity was confirmed by the increase of ERK phosphorylation (figure 7b).Figure 7.


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)

Mkp1 inhibition induces larval settlement. Hatched larvae were treated with 0.25 μM mkp inhibitor dusp1/6 I and examined after 4 h of treatment for larval settlement (a) and ERK activation (b). (a) The number of swimming larvae (white bars) and larvae just attached to the substrate (grey bars) were counted and reported as percentage of the total. (b) Western blot with anti-P-ERK and anti-ERK antibodies and relative histograms representing densitometric data analyses of P-ERK versus ERK intensity bands. Results are representative of five independent experiments. Data are expressed as means ± s.e.m. and were assessed by unpaired t-test. Asterisks represent significant differences with respect to the control: ***p < 0.001.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

RSOB140182F7: Mkp1 inhibition induces larval settlement. Hatched larvae were treated with 0.25 μM mkp inhibitor dusp1/6 I and examined after 4 h of treatment for larval settlement (a) and ERK activation (b). (a) The number of swimming larvae (white bars) and larvae just attached to the substrate (grey bars) were counted and reported as percentage of the total. (b) Western blot with anti-P-ERK and anti-ERK antibodies and relative histograms representing densitometric data analyses of P-ERK versus ERK intensity bands. Results are representative of five independent experiments. Data are expressed as means ± s.e.m. and were assessed by unpaired t-test. Asterisks represent significant differences with respect to the control: ***p < 0.001.
Mentions: To confirm the role of mkp1 in the regulation of ERK activity during larval development, we treated hatched larvae with 0.25 µM of the dual-specific phosphatase inhibitor (dusp 1/6 I). After 4 h of treatment, the inhibitor caused an increase in larval settlement, as assessed by the significant increase of larvae attached to the substrate and the concomitant decrease of swimming larvae with respect to the control (figure 7a). The specificity of the inhibitor for ERK activity was confirmed by the increase of ERK phosphorylation (figure 7b).Figure 7.

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