Regulation of ammonia stress adaptation in <italic style="font-style: italic">Penaeus</italic> <italic style="font-style: italic">vannamei</italic> gills: responses of endoplasmic reticulum stress and Ca<sup>2+</sup> homeostasis

Wenheng LI; Changjian LI; Fang WANG; Zhitao HUANG; Hongwei SHAN

doi:10.1007/s00343-025-4279-x

Your Location：

Home >

Browse articles >

Regulation of ammonia stress adaptation in Penaeus vannamei gills: responses of endoplasmic reticulum stress and Ca²⁺ homeostasis

Biology | Updated：2025-12-16

- Regulation of ammonia stress adaptation in Penaeus vannamei gills: responses of endoplasmic reticulum stress and Ca²⁺ homeostasis
- Regulation of ammonia stress adaptation in Penaeus vannamei gills: responses of endoplasmic reticulum stress and Ca²⁺ homeostasis
- 海洋湖沼学报(英文) 2025年43卷第6期页码：1951-1961
- Affiliations：
  
  1.Key Laboratory of Mariculture (Ocean University of China), Ministry of Education, Qingdao 266003, China
  2.Lianyungang Marine and Fishery Development Promotion Center, Lianyungang 222000, China
  3.Norwegian Institute for Water Research (NIVA), Bergen 5006, Norway
- Author bio：
  
  shanhongwei@ouc.edu.cn
- Funds：
  
  the Natural Science Foundation of Shandong Province(ZR2022MC147);the Research Council of Norway(342628/L10;160016)
- DOI：10.1007/s00343-025-4279-x
  中图分类号：
- 收稿：2024-12-01，
  
  网络首发：2025-02-27，
  
  纸质出版：2025-11-01
- Accepted：
Scan QR Code
Wenheng LI, Changjian LI, Fang WANG, 等. Regulation of ammonia stress adaptation in Penaeus vannamei gills: responses of endoplasmic reticulum stress and Ca²⁺ homeostasis[J]. 海洋湖沼学报(英文), 2025,43(6):1951-1961.

LI Wenheng,LI Changjian,WANG Fang,et al.Regulation of ammonia stress adaptation in ,Penaeus ,vannamei gills: responses of endoplasmic reticulum stress and Ca,²⁺ homeostasis[J].Journal of Oceanology and Limnology,2025,43(06):1951-1961.
Wenheng LI, Changjian LI, Fang WANG, 等. Regulation of ammonia stress adaptation in Penaeus vannamei gills: responses of endoplasmic reticulum stress and Ca²⁺ homeostasis[J]. 海洋湖沼学报(英文), 2025,43(6):1951-1961. DOI： 10.1007/s00343-025-4279-x.

LI Wenheng,LI Changjian,WANG Fang,et al.Regulation of ammonia stress adaptation in ,Penaeus ,vannamei gills: responses of endoplasmic reticulum stress and Ca,²⁺ homeostasis[J].Journal of Oceanology and Limnology,2025,43(06):1951-1961. DOI： 10.1007/s00343-025-4279-x.

摘要

Abstract

Endoplasmic reticulum (ER) stress and Ca

homeostasis play important roles in the environmental adaptation of aquatic animals. To elucidate the response and correlation of ER stress and Ca

homeostasis in the gills of

Penaeus

vannamei

under ammonia stress

we investigated the expression levels of genes related to ER stress and Ca

homeostasis in the gills of

vannamei

exposed to 0- (control)

3.8-

7.6-

and 11.3-mg/L total ammonia nitrogen for 96 h. Results show that the relative gene expression levels of the ER stress indicators

Bip

eiF2α

ATF4

IRE1

and

XBP1s

were higher in the stress groups than in the control group at 12 and 48 h

reaching the maximum at 48 h (

0.05). However

at 96 h

the levels of these indicators were lower in the 7.6- and 11.3-mg/L groups than in the control group. The relative expression levels of

SERCA

RyR

MCU

and

Letm

were significantly higher in the stress groups than in the control group at 12

and 48 h (

0.05)

and the expression levels were positively correlated with the ammonia stress concentration. At 96 h

the expression levels of

SERCA

in the stress groups were lower than that in the control group

whereas the expression levels of

RyR

in the stress groups were significantly higher than that in the control group (

0.05). The relative expression levels of

MCU

were not significantly different fr

om those in the control group. The relative expression levels of

in the 7.6- and 11.3-mg/L groups were significantly lower than that in the control group during the ammonia stress period (

0.05). Pearson’s correlation analysis showed significant correlations among NH

-N levels

the expression of ER stress indicator genes

and the expression of genes related to the regulation of Ca

homeostasis. The above results indicate that ammonia stress could induce ER stress

and consequently changed the mitochondrial and ER Ca

homeostasis in the gills of

vannamei

which contribute to its adaptive mechanisms under adverse environmental conditions.

关键词

Keywords

references

Aguayo-Ortiz R , Espinoza-Fonseca L M . 2020 . Linking biochemical and structural states of SERCA: achievements, challenges, and new opportunities . International Journal of Molecular Sciences , 21 ( 11 ): 4146 , https://doi.org/10.3390/ijms21114146 https://doi.org/10.3390/ijms21114146 .

Allen G J P , Weihrauch D . 2021 . Exploring the versatility of the perfused crustacean gill as a model for transbranchial transport processes. Comparative Biochemistry and Physiology Part B : Biochemistry and Molecular Biology , 254 : 110572 , https://doi.org/10.1016/j.cbpb.2021.110572 https://doi.org/10.1016/j.cbpb.2021.110572 .

Bock F J , Tait S W G . 2020 . Mitochondria as multifaceted regulators of cell death . Nature Reviews Molecular Cell Biology , 21 ( 2 ): 85 - 100 , https://doi.org/10.1038/s41580-019-0173-8 https://doi.org/10.1038/s41580-019-0173-8 .

Catanzaro G , Rapino C , Oddi S et al . 2009 . Anandamide increases swelling and reduces calcium sensitivity of mitochondria . Biochemical and Biophysical Research Communications , 388 ( 2 ): 439 - 442 , https://doi.org/10.1016/j.bbrc.2009.08.037 https://doi.org/10.1016/j.bbrc.2009.08.037 .

Chami M , Gozuacik D , Lagorce D et al . 2001 . SERCA1 truncated proteins unable to pump calcium reduce the endoplasmic reticulum calcium concentration and induce apoptosis . The Journal of Cell Biology , 153 ( 6 ): 1301 - 1314 , https://doi.org/10.1083/jcb.153.6.1301 https://doi.org/10.1083/jcb.153.6.1301 .

Chang Z W , Chiang P C , Cheng W et al . 2015 . Impact of ammonia exposure on coagulation in white shrimp, Litopenaeus vannamei . Ecotoxicology and Environmental Safety , 118 : 98 - 102 , https://doi.org/10.1016/j.ecoenv.2015.04.019 https://doi.org/10.1016/j.ecoenv.2015.04.019 .

Chen D C , Ning F Y , Zhang J Y et al . 2020a . NF-κB pathway took part in the development of apoptosis mediated by miR-15a and oxidative stress via mitochondrial pathway in ammonia-treated chicken splenic lymphocytes. Science of the Total Environment , 729 : 139017 , https://doi.org/10.1016/j.scitotenv.2020.139017 https://doi.org/10.1016/j.scitotenv.2020.139017 .

Chen J C , Chen C T , Cheng S Y . 1994 . Nitrogen excretion and changes of hemocyanin, protein and free amino acid levels in the hemolymph of Penaeus monodon exposed to different concentrations of ambient ammonia-N at different salinity levels . Marine Ecology Progress Series , 110 : 85 - 94 , https://doi.org/10.3354/meps110085 https://doi.org/10.3354/meps110085 .

Chen J Q , Zhang S , Tong J Y et al . 2020b . Whole transcriptome-based miRNA-mRNA network analysis revealed the mechanism of inflammation-immunosuppressive damage caused by cadmium in common carp spleens. Science of the Total Environment , 717 : 137081 , https://doi.org/10.1016/j.scitotenv.2020.137081 https://doi.org/10.1016/j.scitotenv.2020.137081 .

Chu Q , Martinez T F , Novak S W et al . 2019 . Regulation of the ER stress response by a mitochondrial microprotein . Nature Communications , 10 ( 1 ): 4883 , https://doi.org/10.1038/s41467-019-12816-z https://doi.org/10.1038/s41467-019-12816-z .

Dudek J , Benedix J , Cappel S et al . 2009 . Functions and pathologies of BiP and its interaction partners . Cellular and Molecular Life Sciences , 66 ( 9 ): 1556 - 1569 , https://doi.org/10.1007/s00018-009-8745-y https://doi.org/10.1007/s00018-009-8745-y .

García-Casas P , Arias-del-Val J , Alvarez-Illera P et al . 2018 . Inhibition of Sarco-Endoplasmic Reticulum Ca 2+ ATPase extends the lifespan in C . elegans worms. Frontiers in Pharmacology , 9 : 669 , https://doi.org/10.3389/fphar.2018.00669 https://doi.org/10.3389/fphar.2018.00669 .

Giorgi C , Marchi S , Pinton P . 2018 . The machineries, regulation and cellular functions of mitochondrial calcium . Nature Reviews Molecular Cell Biology , 19 ( 11 ): 713 - 730 , https://doi.org/10.1038/s41580-018-0052-8 https://doi.org/10.1038/s41580-018-0052-8 .

Guo Y S , Hao D J , Hu H M . 2021 . High doses of dexamethasone induce endoplasmic reticulum stress-mediated apoptosis by promoting calcium ion influx-dependent CHOP expression in osteoblasts . Molecular Biology Reports , 48 ( 12 ): 7841 - 7851 , https://doi.org/10.1007/s11033-021-06806-y https://doi.org/10.1007/s11033-021-06806-y .

Hernández-Oliveras A , Zarain-Herzberg A . 2024 . The role of Ca 2+ -signaling in the regulation of epigenetic mechanisms. Cell Calcium , 117 : 102836 , https://doi.org/10.1016/j.ceca.2023.102836 https://doi.org/10.1016/j.ceca.2023.102836 .

Hu Z Y , Han D F , Zhang T T et al . 2022 . Ammonium induces oxidative stress, endoplasmic reticulum stres s, and apoptosis of hepatocytes in the liver cell line of grass carp ( Ctenopharyngodon idella ) . Environmental Science and Pollution Research , 30 ( 10 ): 27092 - 27102 , https://doi.org/10.1007/s11356-022-24072-8 https://doi.org/10.1007/s11356-022-24072-8 .

Huo J Z , Molkentin J D . 2024 . MCU genetically altered mice suggest how mitochondrial Ca 2+ regulates metabolism . Trends in Endocrinology & Metabolism , 35 ( 10 ): 918 - 928 , https://doi.org/10.1016/j.tem.2024.04.005 https://doi.org/10.1016/j.tem.2024.04.005 .

Lemmer I L , Willemsen N , Hilal N et al . 2021 . A guide to understanding endoplasmic reticulum stress in metabolic disorders. Molecular Metabolism , 47 : 101169 , https://doi.org/10.1016/j.molmet.2021.101169 https://doi.org/10.1016/j.molmet.2021.101169 .

Li W H , Wang Y , Li C J et al . 2024 . Responses and correlation among ER stress, Ca 2+ homeostasis, and fatty acid metabolism in Penaeus vannamei under ammonia stress. Aquatic Toxicology , 267 : 106837 , https://doi.org/10.1016/j.aquatox.2024.106837 https://doi.org/10.1016/j.aquatox.2024.106837 .

Liang Z X , Liu R , Zhao D P et al . 2016 . Ammonia exposure induces oxidative stress, endoplasmic reticulum stress and apoptosis in hepatopancreas of pacific white shrimp ( Litopenaeus vannamei ) . Fish & Shellfish Immunology , 54 : 523 - 528 , https://doi.org/10.1016/j.fsi.2016.05.009 https://doi.org/10.1016/j.fsi.2016.05.009 .

Livak K J , Schmittgen T D . 2001 . Analysis of relative gene expression data using real-time quantitative PCR and the 2 ΔΔ C t method . Methods , 25 ( 4 ): 402 - 408 , https://doi.org/10.1006/meth.2001.1262 https://doi.org/10.1006/meth.2001.1262 .

Marchi S , Patergnani S , Missiroli S et al . 2018 . Mitochondrial and endoplasmic reticulum calcium homeostasis and cell death . Cell Calcium , 69 : 62 - 72 , https://doi.org/10.1016/j.ceca.2017.05.003 https://doi.org/10.1016/j.ceca.2017.05.003 .

Murgia M , Rizzuto R . 2015 . Molecular diversity and pleiotropic role of the mitochondrial calcium uniporter . Cell Calcium , 58 ( 1 ): 11 - 17 , https://doi.org/10.1016/j.ceca.2014.11.001 https://doi.org/10.1016/j.ceca.2014.11.001 .

Preissler S , Chambers J E , Crespillo-Casado A et al . 2015 . Physiological modulation of BiP activity by trans -protomer engagement of the interdomain linker . eLife , 4 : e 08961 , https://doi.org/10.7554/eLife.08961 https://doi.org/10.7554/eLife.08961 .

Qiu J , Tan Y W , Hagenston A M et al . 2013 . Mitochondrial calcium uniporter Mcu controls excitotoxicity and is transcriptionally repressed by neuroprotective nuclear calcium signals. Nature Communications , 4 : 2034 , https://doi.org/10.1038/ncomms3034 https://doi.org/10.1038/ncomms3034 .

Read A , Schröder M . 2021 . The unfolded protein response: an overview . Biology , 10 ( 5 ): 384 , https://doi.org/10.3390/biology10050384 https://doi.org/10.3390/biology10050384 .

Shen C C , Tang D , Bai Y Z et al . 2021 . Comparative transcriptome analysis of the gills of Procambarus clarkii provide novel insights into the response mechanism of ammonia stress tolerance . Molecular Biology Reports , 48 ( 3 ): 2611 - 2618 , https://doi.org/10.1007/s11033-021-06315-y https://doi.org/10.1007/s11033-021-06315-y .

Sinha A K , Rasoloniriana R , Dasan A F et al . 2015 . Interactive effect of high environmental ammonia and nutritional status on ecophysiological performance of European sea bass ( Dicentrarchus labrax ) acclimated to reduced seawater salinities . Aquatic Toxicology , 160 : 39 - 56 , https://doi.org/10.1016/j.aquatox.2015.01.005 https://doi.org/10.1016/j.aquatox.2015.01.005 .

Souza-Neto F V , Jiménez-González S , Delgado-Valero B et al . 2021 . The interplay of mitochondrial oxidative stress and endoplasmic reticulum stress in cardiovascular fibrosis in obese rats . Antioxidants , 10 ( 8 ): 1274 , https://doi.org/10.3390/antiox10081274 https://doi.org/10.3390/antiox10081274 .

Suzuki C K , Bonifacino J S , Lin A Y et al . 1991 . Regulating the retention of T-cell receptor alpha chain variants within the endoplasmic reticulum: Ca 2+ -dependent association with BiP . The Journal of Cell Biology , 114 ( 2 ): 189 - 205 , https://doi.org/10.1083/jcb.114.2.189 https://doi.org/10.1083/jcb.114.2.189 .

Wang T , Li W H , Shan H W et al . 2021 . Responses of energy homeostasis and lipid metabolism in Penaeus vannamei exposed to ammonia stress. Aquaculture , 544 : 737092 , https://doi.org/10.1016/j.aquaculture.2021.737092 https://doi.org/10.1016/j.aquaculture.2021.737092 .

Xue S Q , Lin J W , Zhou Q et al . 2021 . Effect of ammonia stress on transcriptome and endoplasmic reticulum stress pathway for common carp ( Cyprinus carpio ) hepatopancreas. Aquaculture Reports , 20 : 100694 , https://doi.org/10.1016/j.aqrep.2021.100694 https://doi.org/10.1016/j.aqrep.2021.100694 .

Yao Y K , Chen S Y , Cao M T et al . 2017 . Antigen-specific CD8 + T cell feedback activates NLRP3 inflammasome in antigen-presenting cells through perforin. Nature Communications , 8 : 15402 , https://doi.org/10.1038/ncomms15402 https://doi.org/10.1038/ncomms15402 .

Zhang Y , Liu J Y , Zhuo H B et al . 2023 . Differential toxicity responses between hepatopancreas and gills in Litopenaeus vannamei under chronic Ammonia-N exposure . Animals , 13 ( 24 ): 3799 , https://doi.org/10.3390/ani13243799 https://doi.org/10.3390/ani13243799 .

浏览量

Downloads

CSCD

文章被引用时，请邮件提醒。

Submit

工具集

关联资源

Effect of dietary supplement of inactivated Lactobacillus plantarum Ep-M17 on growth performance, immune response, disease resistance, and intestinal microbiota in Penaeus vannamei

Antioxidation and ATPase activity in the gill of mud crab Scylla serrata under cold stress

2.5D编织结构复合材料温度场特征研究

双转子轴间滑油颗粒运动轨迹参数化模型

基于NSGA II算法分布度改进的ATREX发动机性能优化方法研究

Regulation of ammonia stress adaptation in Penaeus vannamei gills: responses of endoplasmic reticulum stress and Ca2+ homeostasis

Regulation of ammonia stress adaptation in Penaeus vannamei gills: responses of endoplasmic reticulum stress and Ca2+ homeostasis

DOI：10.1007/s00343-025-4279-x

摘要

Abstract

关键词

Keywords

references

Regulation of ammonia stress adaptation in Penaeus vannamei gills: responses of endoplasmic reticulum stress and Ca²⁺ homeostasis

Regulation of ammonia stress adaptation in Penaeus vannamei gills: responses of endoplasmic reticulum stress and Ca²⁺ homeostasis