Heat stress-induced endoplasmic reticulum stress promotes liver apoptosis in largemouth bass (Micropterus salmoides)

Zhao, Xin; Li, Caijuan; Liu, Enguang; Zhu, Hao; Ling, Qufei

doi:10.1016/j.aquaculture.2021.737401

Cited by 54 publications

(14 citation statements)

References 65 publications

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“…However, dietary histidine deficiency had no significant effect on the mRNA level of ATF6. In contrast to this study, ERS regulation was also involved in the ATF6-signalling pathway [ 32 , 51 ]. Activation of the IRE1 pathway by B-cell differentiation did not lead to the upregulation of the CHOP downstream genes in the ATF6 and PERK pathways [ 52 , 53 ].…”

Section: Discussionmentioning

confidence: 60%

“…In this study, dietary histidine deficiency activated the PEPK-signalling pathway and IRE1-signalling pathway with increased core gene expression of pepk , grp78 , eif2α , atf4 , chopα , ire1 , xbp1 , traf2 , ask1, and jnk1 , indicating that dietary histidine deficiency induced ERS. In aquatic animals, activation of the PEPK-signalling pathway and IRE1-signalling pathway resulted in ERS under heat stress in largemouth bass [ 32 ]. Furthermore, numerous studies have reported that adverse factors can induce ERS by affecting the expression of the core genes in the IRE1- and PERK-signalling pathways in blunt snout bream [ 17 ], common carp [ 18 , 19 ], Gibel carp [ 20 ], and grass carp [ 21 ].…”

Section: Discussionmentioning

confidence: 99%

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Histidine Deficiency Inhibits Intestinal Antioxidant Capacity and Induces Intestinal Endoplasmic-Reticulum Stress, Inflammatory Response, Apoptosis, and Necroptosis in Largemouth Bass (Micropterus salmoides)

Liang

Gao

et al. 2022

Antioxidants

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This 56-day study aimed to evaluate the effects of histidine levels on intestinal antioxidant capacity and endoplasmic-reticulum stress (ERS) in largemouth bass (Micropterus salmoides). The initial weights of the largemouth bass were (12.33 ± 0.01) g. They were fed six graded levels of histidine: 0.71% (deficient group), 0.89%, 1.08%, 1.26%, 1.48%, and 1.67%. The results showed that histidine deficiency significantly suppressed the intestinal antioxidant enzyme activities, including SOD, CAT, GPx, and intestinal level of GSH, which was supported by significantly higher levels of intestinal MDA. Moreover, histidine deficiency significantly lowered the mRNA level of nrf2 and upregulated the mRNA level of keap1, which further lowered the mRNA levels of the downstream genes sod, cat, and gpx. Additionally, histidine-deficiency-induced intestinal ERS, which was characterized by activating the PEPK-signalling pathway and IRE1-signalling pathway, including increased core gene expression of pepk, grp78, eif2α, atf4, chopα, ire1, xbp1, traf2, ask1, and jnk1. Dietary histidine deficiency also induced apoptosis and necroptosis in the intestine by upregulating the expressions of proapoptotic genes, including caspase 3, caspase 8, caspase 9, and bax, and necroptosis-related genes, including mlkl and ripk3, while also lowering the mRNA level of the antiapoptotic gene bcl-2. Furthermore, histidine deficiency activated the NF-κB-signalling pathway to induce an inflammatory response, improving the mRNA levels of the proinflammatory factors tnf-α, hepcidin 1, cox2, cd80, and cd83 and lowering the mRNA levels of the anti-inflammatory factors tgf-β1 and ikbα. Similarly, dietary histidine deficiency significantly lowered the intestinal levels of the anti-inflammatory factors TGF-β and IL-10 and upregulated the intestinal levels of the proinflammatory factor TNF-α, showing a trend similar to the gene expression of inflammatory factors. However, dietary histidine deficiency inhibited only the level of C3, and no significant effects were observed for IgM, IgG, HSP70, or IFN-γ. Based on the MDA and T-SOD results, the appropriate dietary histidine requirements of juvenile largemouth bass were 1.32% of the diet (2.81% dietary protein) and 1.47% of the diet (3.13% dietary protein), respectively, as determined by quadratic regression analysis.

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Section: Discussionmentioning

confidence: 60%

Section: Discussionmentioning

confidence: 99%

Histidine Deficiency Inhibits Intestinal Antioxidant Capacity and Induces Intestinal Endoplasmic-Reticulum Stress, Inflammatory Response, Apoptosis, and Necroptosis in Largemouth Bass (Micropterus salmoides)

Liang

Gao

et al. 2022

Antioxidants

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“…One of these genes, for example, is the eukaryotic translation initiation factor 2α kinase 3 (EIF2AK3), a key stress sensor able to activate UPR and inhibit ribosome assembly and protein synthesis, leading to translation inhibition (Wek, Jiang, & Anthony, 2006). Upregulation of UPR markers and liver tissue damage was also found in largemouth bass Micropterus salmoides acutely exposed to elevated temperature (Zhao et al, 2022), while in mice livers ER stress markers and Cnx/Crt genes upregulation persisted for 21 days after a thermal injury, indicating long-term functional alterations of hepatic functions (Song, Finnerty, Herndon, Boehning, & Jeschke, 2009). Such prolonged suppression of protein synthesis and ATP production will likely result in energy limitations, fitness decrease and suboptimal growth (Sokolova, Frederich, Bagwe, Lannig, & Sukhotin, 2012).…”

Section: Discussionmentioning

confidence: 99%

Timing specific parental effects of ocean warming in a coral reef fish

Bonzi,

Spinks,

Donelson

et al. 2023

Preprint

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Population and species persistence in a rapidly warming world will be determined by an organisms’ ability to acclimate to warmer conditions, especially across generations. There is potential for transgenerational acclimation, but the importance of ontogenetic timing in the transmission of environmentally induced parental effects remains mostly unknown. We aimed to disentangle the contributions of two critical ontogenetic stages (juvenile development and adult reproduction) to transgenerational plasticity, by exposing the coral reef fishAcanthochromis polyacanthusto simulated ocean warming with natural diel thermal fluctuations across two generations. By using hepatic transcriptomics, we discovered that the developmental environment of the offspring themselves had little effect on their acclimation potential at 2.5 months of life. Instead, the developmental experience of parents increased regulatory RNA production and protein synthesis, which could improve the offspring’s response to warming. Conversely, reproduction in warmer water elicited stress response mechanisms, with suppression of translation and mitochondrial respiration. Mismatches between temperatures in the parental ontogenetic thermal experience deeply affected offspring gene expression profiles, and detrimental effects were also evident when warming occurred both during parents’ development and reproduction. This study reveals that the previous generation’s developmental temperature contributes substantially to thermal acclimation potential during early life, however prolonged heat stress will likely have adverse effects on the species’ persistence.

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“…In this study, proteins eIF2α and ASNS were upregulated in NET-challenged fish. Accordingly, in largemouth bass exposed to heat stress, eIF2α gene was also reported to be upregulated, along with other UPR-related genes [ 34 ]. In contrast, ATF6 is first activated in the Golgi and then acts as a transcription factor of chaperones, such as the 78 kDa glucose-regulated protein (BiP/GRP78/HSPA5) and the 94 kDa glucose-regulated protein (HSP90B1), x-box-binding protein 1 (XBP1), and genes involved in the ER quality control machinery (e.g., calreticulin (CALRL)) [ 33 ].…”

Section: Discussionmentioning

confidence: 99%

Gilthead Seabream Liver Integrative Proteomics and Metabolomics Analysis Reveals Regulation by Different Prosurvival Pathways in the Metabolic Adaptation to Stress

Magalhães

Farinha

Blackburn

et al. 2022

IJMS

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The study of the molecular mechanisms of stress appraisal on farmed fish is paramount to ensuring a sustainable aquaculture. Stress exposure can either culminate in the organism’s adaptation or aggravate into a metabolic shutdown, characterized by irreversible cellular damage and deleterious effects on fish performance, welfare, and survival. Multiomics can improve our understanding of the complex stressed phenotype in fish and the molecular mediators that regulate the underlying processes of the molecular stress response. We profiled the stress proteome and metabolome of Sparus aurata responding to different challenges common to aquaculture production, characterizing the disturbed pathways in the fish liver, i.e., the central organ in mounting the stress response. Label-free shotgun proteomics and untargeted metabolomics analyses identified 1738 proteins and 120 metabolites, separately. Mass spectrometry data have been made fully accessible via ProteomeXchange, with the identifier PXD036392, and via MetaboLights, with the identifier MTBLS5940. Integrative multivariate statistical analysis, performed with data integration analysis for biomarker discovery using latent components (DIABLO), depicted the 10 most-relevant features. Functional analysis of these selected features revealed an intricate network of regulatory components, modulating different signaling pathways related to cellular stress, e.g., the mTORC1 pathway, the unfolded protein response, endocytosis, and autophagy to different extents according to the stress nature. These results shed light on the dynamics and extent of this species’ metabolic reprogramming under chronic stress, supporting future studies on stress markers’ discovery and fish welfare research.

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Heat stress-induced endoplasmic reticulum stress promotes liver apoptosis in largemouth bass (Micropterus salmoides)

Cited by 54 publications

References 65 publications

Histidine Deficiency Inhibits Intestinal Antioxidant Capacity and Induces Intestinal Endoplasmic-Reticulum Stress, Inflammatory Response, Apoptosis, and Necroptosis in Largemouth Bass (Micropterus salmoides)

Histidine Deficiency Inhibits Intestinal Antioxidant Capacity and Induces Intestinal Endoplasmic-Reticulum Stress, Inflammatory Response, Apoptosis, and Necroptosis in Largemouth Bass (Micropterus salmoides)

Timing specific parental effects of ocean warming in a coral reef fish

Gilthead Seabream Liver Integrative Proteomics and Metabolomics Analysis Reveals Regulation by Different Prosurvival Pathways in the Metabolic Adaptation to Stress

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