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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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 |
work_keys_str_mv |
AT maoliangsu transcriptionalanalysisofrenaldopaminemediatednahomeostasisresponsetoenvironmentalsalinitystressinscatophagusargus AT jiananzhou transcriptionalanalysisofrenaldopaminemediatednahomeostasisresponsetoenvironmentalsalinitystressinscatophagusargus AT zhengyuduan transcriptionalanalysisofrenaldopaminemediatednahomeostasisresponsetoenvironmentalsalinitystressinscatophagusargus AT junbinzhang transcriptionalanalysisofrenaldopaminemediatednahomeostasisresponsetoenvironmentalsalinitystressinscatophagusargus |
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