Transcriptional analysis of renal dopamine-mediated Na+ homeostasis response to environmental salinity stress in Scatophagus argus

Abstract Background To control the osmotic pressure in the body, physiological adjustments to salinity fluctuations require the fish to regulate body fluid homeostasis in relation to environmental change via osmoregulation. Previous studies related to osmoregulation were focused primarily on the gil...

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Main Authors: Maoliang Su, Jianan Zhou, Zhengyu Duan, Junbin Zhang
Format: Article
Language:English
Published: BMC 2019-05-01
Series:BMC Genomics
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12864-019-5795-x
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spelling doaj-dbe519a56f8e4d30b6ae384287e4c8f92020-11-25T02:49:00ZengBMCBMC Genomics1471-21642019-05-0120111610.1186/s12864-019-5795-xTranscriptional analysis of renal dopamine-mediated Na+ homeostasis response to environmental salinity stress in Scatophagus argusMaoliang Su0Jianan Zhou1Zhengyu Duan2Junbin Zhang3Shenzhen Key Laboratory of Marine Bioresource & Eco-Environmental Science, College of Life Sciences and Oceanography, Shenzhen UniversityKey Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Ministry of Education, College of Fisheries and Life Sciences, Shanghai Ocean UniversityShenzhen Key Laboratory of Marine Bioresource & Eco-Environmental Science, College of Life Sciences and Oceanography, Shenzhen UniversityShenzhen Key Laboratory of Marine Bioresource & Eco-Environmental Science, College of Life Sciences and Oceanography, Shenzhen UniversityAbstract Background To control the osmotic pressure in the body, physiological adjustments to salinity fluctuations require the fish to regulate body fluid homeostasis in relation to environmental change via osmoregulation. Previous studies related to osmoregulation were focused primarily on the gill; however, little is known about another organ involved in osmoregulation, the kidney. The salinity adaptation of marine fish involves complex physiological traits, metabolic pathways and molecular and gene networks in osmoregulatory organs. To further explore of the salinity adaptation of marine fish with regard to the role of the kidney, the euryhaline fish Scatophagus argus was employed in the present study. Renal expression profiles of S. argus at different salinity levels were characterized using RNA-sequencing, and an integrated approach of combining molecular tools with physiological and biochemical techniques was utilized to reveal renal osmoregulatory mechanisms in vivo and in vitro. Results S. argus renal transcriptomes from the hyposaline stress (0‰, freshwater [FW]), hypersaline stress (50‰, hypersaline water [HW]) and control groups (25‰) were compared to elucidate potential osmoregulatory mechanisms. In total, 19,012 and 36,253 differentially expressed genes (DEGs) were obtained from the FW and HW groups, respectively. Based on the functional classification of DEGs, the renal dopamine system-induced Na+ transport was demonstrated to play a fundamental role in osmoregulation. In addition, for the first time in fish, many candidate genes associated with the dopamine system were identified. Furthermore, changes in environmental salinity affected renal dopamine release/reuptake by regulating the expression of genes related to dopamine reuptake (dat and nkaα1), vesicular traffic-mediated dopamine release (pink1, lrrk2, ace and apn), DAT phosphorylation (CaMKIIα and pkcβ) and internalization (akt1). The associated transcriptional regulation ensured appropriate extracellular dopamine abundance in the S. argus kidney, and fluctuations in extracellular dopamine produced a direct influence on Na+/K+-ATPase (NKA) expression and activity, which is associated with Na+ homeostasis. Conclusions These transcriptomic data provided insight into the molecular basis of renal osmoregulation in S. argus. Significantly, the results of this study revealed the mechanism of renal dopamine system-induced Na+ transport is essential in fish osmoregulation.http://link.springer.com/article/10.1186/s12864-019-5795-xScatophagus argusTranscriptomeSalinity stressDopamine transportNa+ homeostasis
collection DOAJ
language English
format Article
sources DOAJ
author Maoliang Su
Jianan Zhou
Zhengyu Duan
Junbin Zhang
spellingShingle Maoliang Su
Jianan Zhou
Zhengyu Duan
Junbin Zhang
Transcriptional analysis of renal dopamine-mediated Na+ homeostasis response to environmental salinity stress in Scatophagus argus
BMC Genomics
Scatophagus argus
Transcriptome
Salinity stress
Dopamine transport
Na+ homeostasis
author_facet Maoliang Su
Jianan Zhou
Zhengyu Duan
Junbin Zhang
author_sort Maoliang Su
title Transcriptional analysis of renal dopamine-mediated Na+ homeostasis response to environmental salinity stress in Scatophagus argus
title_short Transcriptional analysis of renal dopamine-mediated Na+ homeostasis response to environmental salinity stress in Scatophagus argus
title_full Transcriptional analysis of renal dopamine-mediated Na+ homeostasis response to environmental salinity stress in Scatophagus argus
title_fullStr Transcriptional analysis of renal dopamine-mediated Na+ homeostasis response to environmental salinity stress in Scatophagus argus
title_full_unstemmed Transcriptional analysis of renal dopamine-mediated Na+ homeostasis response to environmental salinity stress in Scatophagus argus
title_sort transcriptional analysis of renal dopamine-mediated na+ homeostasis response to environmental salinity stress in scatophagus argus
publisher BMC
series BMC Genomics
issn 1471-2164
publishDate 2019-05-01
description Abstract Background To control the osmotic pressure in the body, physiological adjustments to salinity fluctuations require the fish to regulate body fluid homeostasis in relation to environmental change via osmoregulation. Previous studies related to osmoregulation were focused primarily on the gill; however, little is known about another organ involved in osmoregulation, the kidney. The salinity adaptation of marine fish involves complex physiological traits, metabolic pathways and molecular and gene networks in osmoregulatory organs. To further explore of the salinity adaptation of marine fish with regard to the role of the kidney, the euryhaline fish Scatophagus argus was employed in the present study. Renal expression profiles of S. argus at different salinity levels were characterized using RNA-sequencing, and an integrated approach of combining molecular tools with physiological and biochemical techniques was utilized to reveal renal osmoregulatory mechanisms in vivo and in vitro. Results S. argus renal transcriptomes from the hyposaline stress (0‰, freshwater [FW]), hypersaline stress (50‰, hypersaline water [HW]) and control groups (25‰) were compared to elucidate potential osmoregulatory mechanisms. In total, 19,012 and 36,253 differentially expressed genes (DEGs) were obtained from the FW and HW groups, respectively. Based on the functional classification of DEGs, the renal dopamine system-induced Na+ transport was demonstrated to play a fundamental role in osmoregulation. In addition, for the first time in fish, many candidate genes associated with the dopamine system were identified. Furthermore, changes in environmental salinity affected renal dopamine release/reuptake by regulating the expression of genes related to dopamine reuptake (dat and nkaα1), vesicular traffic-mediated dopamine release (pink1, lrrk2, ace and apn), DAT phosphorylation (CaMKIIα and pkcβ) and internalization (akt1). The associated transcriptional regulation ensured appropriate extracellular dopamine abundance in the S. argus kidney, and fluctuations in extracellular dopamine produced a direct influence on Na+/K+-ATPase (NKA) expression and activity, which is associated with Na+ homeostasis. Conclusions These transcriptomic data provided insight into the molecular basis of renal osmoregulation in S. argus. Significantly, the results of this study revealed the mechanism of renal dopamine system-induced Na+ transport is essential in fish osmoregulation.
topic Scatophagus argus
Transcriptome
Salinity stress
Dopamine transport
Na+ homeostasis
url http://link.springer.com/article/10.1186/s12864-019-5795-x
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AT jiananzhou transcriptionalanalysisofrenaldopaminemediatednahomeostasisresponsetoenvironmentalsalinitystressinscatophagusargus
AT zhengyuduan transcriptionalanalysisofrenaldopaminemediatednahomeostasisresponsetoenvironmentalsalinitystressinscatophagusargus
AT junbinzhang transcriptionalanalysisofrenaldopaminemediatednahomeostasisresponsetoenvironmentalsalinitystressinscatophagusargus
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