Regulation of apoptosis by Pacific oyster Crassostrea gigas reveals acclimation strategy to CO2 driven acidification

Wang, Xiudan; Li, Changmei; Jia, Zhihao; Xu, Tongxiao; Wang, Yilin; Sun, Mingzhu; Han, Shuhui; Wang, Xia; Qiu, Limei

doi:10.1016/j.ecoenv.2021.112235

Cited by 10 publications

(13 citation statements)

References 41 publications

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“…Ribosomal proteins have emerged as significant markers for physiological status evaluation under stress conditions in marine organisms (Jiao, Dai et al, 2021, Vieira, Braga et al, 2018. Eif1b participates in the assembly of the 43S complex during the mRNA translation of protein synthesis (Sun, Gong et al, 2015), remodeling the protein landscape to enhance stress survival during heat stress (Neef & Thiele, 2009), which is consistent with our previous findings (Wang et al, 2023a). Furthermore, Gst, a well-known antioxidant gene, shows increased expression and enzyme activity in marine organisms under high-temperature stress, aiding in combating oxidative stress induced by elevated temperatures (Guerriero, Bassem et al, 2018, Missionário, Travesso et al, 2023, Teixeira, Diniz et al, 2013.…”

Section: Discussionsupporting

confidence: 90%

“…Studies on phosphorylation in response to temperature stress in mollusks are lacking, as they are currently limited to the measurement of phosphorylation levels of specific proteins within specific pathways, such as SAPK/JNK (Evans & Somero, 2010) or p38 MAPK (Michaelidis, Hatzikamari et al, 2009) in MAPK pathway, p53 and p21 (Yao & Somero, 2013). To our knowledge, only our previous study has investigated the global phosphoproteomic response to high-temperature stress in mollusks (oysters), revealing a significant upregulation of phosphorylation level at the Ser74 site of an NF-κB/IκB protein under high-temperature stress, which exhibited divergent phosphorylation patterns between two differentially heat-adaptive species (Wang, Du et al, 2023a), while the conserved Ser32 and Ser36 sites showed no phosphorylation modification, suggesting a potential novel temperature-induced phosphorylation regulatory mechanisms in the NF-κB pathway for oysters.…”

Section: Introductionmentioning

confidence: 98%

“…Crassostrea gigas (C. gigas) and Crassostrea angulata (C. angulata) are two allopatric congeneric oyster species that adapt to relatively cold and warm habitats (Northern and Southern China coasts), respectively, exhibiting divergent temperature adaptation (Ghaffari, Wang et al, 2019, Haiyan, Guofan et al, 2008, Ren, Liu et al, 2010, Wang, Li et al, 2023b, Wang, Li et al, 2021. Previous study has found differential protein phosphorylation patterns in response to high-temperature stress between C. gigas and C. angulata (Wang et al, 2023a). Particularly, opposite phosphorylation levels have been observed in IκB (Ser74) suggesting that NF-κB/IκBα phosphorylation may be crucial in shaping divergent temperature adaptation between the oyster species.…”

Section: Introductionmentioning

confidence: 99%

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Novel Ser74 of NF-κB/CgIκBα Phosphorylated by MAPK/ERK Regulates Temperature Adaptation in Oysters

Wang,

Jiang,

et al. 2024

Preprint

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Phosphorylation of IkappaBalpha at Ser32 and Ser36 by IKKs during biotic stress triggers its ubiquitin-proteasome degradation, causing to the nuclear translocation of REL, representing a key cascade mechanism in metazoans conserved and immune core signaling pathway, NF-kappaB. However, studies on its response to abiotic stress and signal transduction by phosphorylation in mollusks are lacking. Here, we firstly report a novel heat-induced phosphorylation site (Ser74) at the major NF-kappaB/CgIkappaBalpha of oysters, phosphorylated by MAPK/CgERK1/2, which independently mediated the subsequent ubiquitin-proteasome degradation without phosphorylation at Ser32 and Ser36 and decreased thermal stability. The degradation of CgIkappaBalpha promoted CgREL nuclear translocation, which stimulated cell survival related gene expression to defend against thermal stress. The MAPK and NF-kappaB pathways exhibited stronger activation patterns in higher environmental temperature and in the warm-adapted Crassostrea angulata than those in the cold-adapted C. gigas-two allopatric congeneric oyster species with differential habitat temperatures. These findings unveil the complex and unique phosphorylation-mediated signal transduction mechanisms in marine invertebrates, and further expand our understanding of the evolution and function of established classical pathway crosstalk mechanisms.

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Section: Discussionsupporting

confidence: 90%

Section: Introductionmentioning

confidence: 98%

Section: Introductionmentioning

confidence: 99%

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Novel Ser74 of NF-κB/CgIκBα Phosphorylated by MAPK/ERK Regulates Temperature Adaptation in Oysters

Wang,

Jiang,

et al. 2024

Preprint

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“…Our findings corroborate with that of Ong et al [32] and Araújo et al [33], which indicated that the two environments exerted negative synergistic effects, causing cell toxicity and increasing apoptosis. Wang et al [34] reported that acidification increased caspase-3 gene activity in Pacific oyster (Crassostrea gigas) plasma, and Nash and Rahman [35] found that high-temperature conditions (32 • C) increased caspase-3 gene expression and apoptosis in American oyster (Crassostrea virginica). In addition, Zhang et al [36] reported that cell death occurs in the top shell (Trochus niloticus) under low pH and high-temperature conditions (30 • C).…”

Section: Discussionmentioning

confidence: 99%

Oxidative Stress and Apoptosis in Disk Abalone (Haliotis discus hannai) Caused by Water Temperature and pH Changes

Kim

Lee

et al. 2023

Antioxidants

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Ocean warming and acidification can induce oxidative stress in marine species, resulting in cellular damage and apoptosis. However, the effects of pH and water temperature conditions on oxidative stress and apoptosis in disk abalone are poorly understood. This study investigated, for the first time, the effects of different water temperatures (15, 20, and 25 °C) and pH levels (7.5 and 8.1) on oxidative stress and apoptosis in disk abalone by estimating levels of H2O2, malondialdehyde (MDA), dismutase (SOD), catalase (CAT), and the apoptosis-related gene caspase-3. We also visually confirmed apoptotic effects of different water temperatures and pH levels via in situ hybridization and terminal deoxynucleotidyl transferase dUTP nick end labeling assays. The levels of H2O2, MDA, SOD, CAT, and caspase-3 increased under low/high water temperature and/or low pH conditions. Expression of the genes was high under high temperature and low pH conditions. Additionally, the apoptotic rate was high under high temperatures and low pH conditions. These results indicate that changes in water temperature and pH conditions individually and in combination trigger oxidative stress in abalone, which can induce cell death. Specifically, high temperatures induce apoptosis by increasing the expression of the apoptosis-related gene caspase-3.

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“…Earlier studies reported that OA can alter immune system parameters in marine invertebrates [44][45][46][47][48][49][50][51]. Much less is known in marine fishes [52,53], and especially species of ecological and commercial importance, such as the European sea bass (Dicentrarchus labrax).…”

Section: Introductionmentioning

confidence: 99%

The extensive transgenerational transcriptomic effects of ocean acidification on the olfactory epithelium of a marine fish are associated with a better viral resistance

et al. 2022

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Background Progressive CO2-induced ocean acidification (OA) impacts marine life in ways that are difficult to predict but are likely to become exacerbated over generations. Although marine fishes can balance acid–base homeostasis efficiently, indirect ionic regulation that alter neurosensory systems can result in behavioural abnormalities. In marine invertebrates, OA can also affect immune system function, but whether this is the case in marine fishes is not fully understood. Farmed fish are highly susceptible to disease outbreak, yet strategies for overcoming such threats in the wake of OA are wanting. Here, we exposed two generations of the European sea bass (Dicentrarchus labrax) to end-of-century predicted pH levels (IPCC RCP8.5), with parents (F1) being exposed for four years and their offspring (F2) for 18 months. Our design included a transcriptomic analysis of the olfactory rosette (collected from the F2) and a viral challenge (exposing F2 to betanodavirus) where we assessed survival rates. Results We discovered transcriptomic trade-offs in both sensory and immune systems after long-term transgenerational exposure to OA. Specifically, RNA-Seq analysis of the olfactory rosette, the peripheral olfactory organ, from 18-months-old F2 revealed extensive regulation in genes involved in ion transport and neuronal signalling, including GABAergic signalling. We also detected OA-induced up-regulation of genes associated with odour transduction, synaptic plasticity, neuron excitability and wiring and down-regulation of genes involved in energy metabolism. Furthermore, OA-exposure induced up-regulation of genes involved in innate antiviral immunity (pathogen recognition receptors and interferon-stimulated genes) in combination with down-regulation of the protein biosynthetic machinery. Consistently, OA-exposed F2 challenged with betanodavirus, which causes damage to the nervous system of marine fish, had acquired improved resistance. Conclusion F2 exposed to long-term transgenerational OA acclimation showed superior viral resistance, though as their metabolic and odour transduction programs were altered, odour-mediated behaviours might be consequently impacted. Although it is difficult to unveil how long-term OA impacts propagated between generations, our results reveal that, across generations, trade-offs in plastic responses is a core feature of the olfactory epithelium transcriptome in OA-exposed F2 offspring, and will have important consequences for how cultured and wild fish interacts with its environment.

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Regulation of apoptosis by Pacific oyster Crassostrea gigas reveals acclimation strategy to CO2 driven acidification

Cited by 10 publications

References 41 publications

Novel Ser74 of NF-κB/CgIκBα Phosphorylated by MAPK/ERK Regulates Temperature Adaptation in Oysters

Novel Ser74 of NF-κB/CgIκBα Phosphorylated by MAPK/ERK Regulates Temperature Adaptation in Oysters

Oxidative Stress and Apoptosis in Disk Abalone (Haliotis discus hannai) Caused by Water Temperature and pH Changes

The extensive transgenerational transcriptomic effects of ocean acidification on the olfactory epithelium of a marine fish are associated with a better viral resistance

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