Gene expression of Na+/K+-ATPase α-isoforms and FXYD proteins and potential modulatory mechanisms in euryhaline milkfish kidneys upon hypoosmotic challenges

Yang, Wenkai; Chao, Tse-Lih; Chuang, Hsin-Ju; Hu, Yao-Chung; Lorin‐Nebel, Catherine; Blondeau‐Bidet, Eva; Wu, Weite; Tang, Cheng-Hao; Tsai, Shu-Chuan; Lee, Tsung‐Han

doi:10.1016/j.aquaculture.2019.01.046

Cited by 8 publications

(2 citation statements)

References 52 publications

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“…7) as seen in gills of the diadromous salmon Salmo salar (Tipsmark, 2008), euryhaline pufferfish Tetraodon nigroviridis (Wang et al, 2008), and the euryhaline milkfish Chanos chanos (Yang et al, 2019a), which express the FXYD11 isoform. While interaction of the FXYD11 peptide with the (Na + , K + )-ATPase has been intensively investigated in fish gills (Tipsmark et al, 2010; Yang et al, 2013; Chang et al, 2016; Liang et al, 2017; Yang et al, 2019a), information on the functional interaction of the FXYD2 peptide with the (Na + , K + )-ATPase is scant (Silva et al, 2012; Yang et al, 2019b). While the present study has revealed regulatory effects of the FXYD2 peptide, its role in the physiological acclimation of crustaceans to different salinities remains unclear.…”

Section: Discussionmentioning

confidence: 99%

Effect of salinity on modulation by ATP, protein kinases and FXYD2 peptide of gill (Na⁺, K⁺)-ATPase activity in the swamp ghost crabUcides cordatus(Brachyura, Ocypodidae)

McNamara

Leone

Lucena

et al. 2020

Preprint

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The gill (Na+, K+)-ATPase is the main enzyme that underpins osmoregulatory ability in crustaceans that occupy biotopes like mangroves, characterized by salinity variation. We evaluated osmotic and ionic regulatory ability in the semi-terrestrial mangrove crab Ucides cordatus after 10-days acclimation to different salinities. We also analyzed modulation by exogenous FXYD2 peptide and by endogenous protein kinases A and C, and Ca2+- calmodulin-dependent kinase of (Na+, K+)-ATPase activity. Hemolymph osmolality was strongly hyper-/hypo-regulated in crabs acclimated at 2 to 35 ‰S. Cl- was well hyper-/hypo- regulated although Na+ much less so, becoming iso-natremic at high salinity. (Na+, K+)- ATPase activity was greatest in isosmotic crabs (26 ‰S), diminishing progressively from 18 and 8 ‰S (≈0.5 fold) to 2 ‰S (0.04-fold), and decreasing notably at 35 ‰S (0.07-fold). At low salinity, the (Na+, K+)-ATPase exhibited a low affinity ATP-binding site that showed Michaelis-Menten behavior. Above 18 ‰S, an additional, high affinity ATP-binding site, corresponding to 10-20% of total (Na+, K+)-ATPase activity appeared. Activity is stimulated by exogenous pig kidney FXYD2 peptide, while endogenous protein kinases A and C and Ca2+/calmodulin-dependent kinase all inhibit activity. This is the first demonstration of inhibitory phosphorylation of a crustacean (Na+, K+)-ATPase by Ca2+/calmodulin-dependent kinase. Curiously, hyper-osmoregulation in U. cordatus shows little dependence on gill (Na+, K+)-ATPase activity, suggesting a role for other ion transporters. These findings reveal that the salinity acclimation response in U. cordatus consists of a suite of osmoregulatory and enzymatic adjustments that maintain its osmotic homeostasis in a challenging, mangrove forest environment.Graphical abstractHighlightsGill (Na+, K+)-ATPase activity is greatest in isosmotic crabs, diminishing in lower and higher salinities.A high affinity ATP-binding site (10-20% of total activity) is exposed above 18 ‰S.Exogenous FXYD2 peptide stimulates activity; endogenous PKA, PKC and CaMK inhibit activity.First demonstration of inhibitory phosphorylation of crustacean (Na+, K+)-ATPase by CaMK.Hyper-osmoregulation shows little dependence on (Na+, K+)-ATPase activity.

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Section: Discussionmentioning

confidence: 99%

Effect of salinity on modulation by ATP, protein kinases and FXYD2 peptide of gill (Na⁺, K⁺)-ATPase activity in the swamp ghost crabUcides cordatus(Brachyura, Ocypodidae)

McNamara

Leone

Lucena

et al. 2020

Preprint

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“…These down-regulated genes may substantially impact overall energy metabolism (Anni et al, 2016). This is because salinity stress may lead to the downregulation of most genes involved in energy material metabolism pathways (Yang et al, 2019). Solan and Whiteley (2016) reported that shellfish would isolate the external environment and internal fluid by tightly closing the shell to provide short-time protection from stressful salinity.…”

Section: Response Characteristics Of P Maxima To Acute Salinity Stressmentioning

confidence: 99%

Transcriptomic Signatures of Pearl Oyster Pinctada Maxima in Response to Acute Salinity Stress

et al. 2022

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Acute salinity stress can impact many physiological processes of marine shellfish. The responses of Pinctada maxima to salinity stress, especially the osmotic pressure regulation and immune response, are of great significance to health. To investigate the molecular changes in response to acute salinity stress, the pearl oysters were transferred from 30 ppt (C) to 40 ppt (HS) and 20 ppt (LS) for 12 h, and the transcriptome analysis was conducted on the gills. Compared to the control, there were 6613 (3253 up-regulated and 3360 down-regulated) differentially expressed genes (DEGs), 4395 (2180 up-regulated and 2215 down-regulated) DEGs observed in HS and LS, respectively. The related molecular biological processes and potential functions were explored from enrichment analysis. A total of 332 KEGG pathways (including 1514 genes) and 308 KEGG pathways (including 731 genes) were enriched in C vs. HS and C vs. LS, respectively. In addition, there are 1559 DEGs shared by C vs. HS group and C vs. LS group, and the results of the KEGG function annotation showed that 7 DEGs were involved in membrane transport, and 34 DEGs were involved in the immune system. The correlation network for expression of genes shows that the expression of 3 genes was significantly correlated with each other in membrane transport, and there were significant correlations between the expression of 27 genes in immune response. The results of this study will be of great value in understanding the molecular basis of salinity stress adaptation in the pearl oyster P. maxima.

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Gill transcriptome analysis reveals the molecular response to the acute low-salinity stress in Cyclina sinensis

Ni¹,

Li²,

Liang³

et al. 2021

Aquaculture Reports

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Gene expression of Na+/K+-ATPase α-isoforms and FXYD proteins and potential modulatory mechanisms in euryhaline milkfish kidneys upon hypoosmotic challenges

Cited by 8 publications

References 52 publications

Effect of salinity on modulation by ATP, protein kinases and FXYD2 peptide of gill (Na⁺, K⁺)-ATPase activity in the swamp ghost crabUcides cordatus(Brachyura, Ocypodidae)

Effect of salinity on modulation by ATP, protein kinases and FXYD2 peptide of gill (Na⁺, K⁺)-ATPase activity in the swamp ghost crabUcides cordatus(Brachyura, Ocypodidae)

Transcriptomic Signatures of Pearl Oyster Pinctada Maxima in Response to Acute Salinity Stress

Gill transcriptome analysis reveals the molecular response to the acute low-salinity stress in Cyclina sinensis

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Gene expression of Na+/K+-ATPase α-isoforms and FXYD proteins and potential modulatory mechanisms in euryhaline milkfish kidneys upon hypoosmotic challenges

Cited by 8 publications

References 52 publications

Effect of salinity on modulation by ATP, protein kinases and FXYD2 peptide of gill (Na+, K+)-ATPase activity in the swamp ghost crabUcides cordatus(Brachyura, Ocypodidae)

Effect of salinity on modulation by ATP, protein kinases and FXYD2 peptide of gill (Na+, K+)-ATPase activity in the swamp ghost crabUcides cordatus(Brachyura, Ocypodidae)

Transcriptomic Signatures of Pearl Oyster Pinctada Maxima in Response to Acute Salinity Stress

Gill transcriptome analysis reveals the molecular response to the acute low-salinity stress in Cyclina sinensis

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Product

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Effect of salinity on modulation by ATP, protein kinases and FXYD2 peptide of gill (Na⁺, K⁺)-ATPase activity in the swamp ghost crabUcides cordatus(Brachyura, Ocypodidae)

Effect of salinity on modulation by ATP, protein kinases and FXYD2 peptide of gill (Na⁺, K⁺)-ATPase activity in the swamp ghost crabUcides cordatus(Brachyura, Ocypodidae)