Ultrastructural variation and key ER chaperones response induced by heat stress in intestinal cells of sea cucumber Apostichopus japonicus

Wang, Shasha; Zheng, Yingqiu; Chen, Muyan; Storey, Kenneth B.

doi:10.1007/s00343-020-9265-8

Cited by 13 publications

(4 citation statements)

References 61 publications

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“…In fact, several Hsps have been characterized from different sea cucumber species. Among these are Hsp 90, Hsp 70, Hsp 60, and members of the small Hsp family [ 28 , 29 , 30 , 31 , 32 ]. These genes have been reported to be expressed by cells in the intestine, coelomocytes, and other tissues.…”

Section: Resultsmentioning

confidence: 99%

The Stress Response of the Holothurian Central Nervous System: A Transcriptomic Analysis

Cruz-González

Quesada-Díaz

Miranda-Negrón

et al. 2022

IJMS

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Injury to the central nervous system (CNS) results in permanent damage and lack of function in most vertebrate animals, due to their limited regenerative capacities. In contrast, echinoderms can fully regenerate their radial nerve cord (RNC) following transection, with little to no scarring. Investigators have associated the regenerative capacity of some organisms to the stress response and inflammation produced by the injury. Here, we explore the gene activation profile of the stressed holothurian CNS. To do this, we performed RNA sequencing on isolated RNC explants submitted to the stress of transection and enzyme dissection and compared them with explants kept in culture for 3 days following dissection. We describe stress-associated genes, including members of heat-shock families, ubiquitin-related pathways, transposons, and apoptosis that were differentially expressed. Surprisingly, the stress response does not induce apoptosis in this system. Other genes associated with stress in other animal models, such as hero proteins and those associated with the integrated stress response, were not found to be differentially expressed either. Our results provide a new viewpoint on the stress response in the nervous system of an organism with amazing regenerative capacities. This is the first step in deciphering the molecular processes that allow echinoderms to undergo fully functional CNS regeneration, and also provides a comparative view of the stress response in other organisms.

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Section: Resultsmentioning

confidence: 99%

The Stress Response of the Holothurian Central Nervous System: A Transcriptomic Analysis

Cruz-González

Quesada-Díaz

Miranda-Negrón

et al. 2022

IJMS

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“…An accumulation of unfolded or misfolded proteins in the ER induces the unfolded protein response (UPR), which is an evolutionarily conserved stress-detecting system used to adapt to changing environmental or stress conditions and, thereby, re-establish normal ER function (Raghunath et al, 2018). Our previous study reported the key ER chaperone response induced by HS in intestinal cells of sea cucumbers (Wang et al, 2021). A marked signature of the UPR stress response is the coordinated transcriptional up-regulation of resident ER chaperones such as the 78 kDa glucose-regulated protein (Grp78), heat shock protein 90 kDa beta (Grp94), and PDI family members (Lee, 2001;Ma and Hendershot, 2002;Dunlop et al, 2018).…”

Section: Heat Shock Response and Endoplasmic Reticulum Stressmentioning

confidence: 99%

PacBio Isoform Sequencing and Illumina RNA Sequencing Provide Novel Insights on Responses to Acute Heat Stress in Apostichopus japonicus Coelomocytes

et al. 2022

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Significant increases in global sea surface temperatures are expected with climate change and may cause a serious challenge for marine organisms cultured in aquatic environments that are characterized by short and long-term fluctuations in water temperatures. Apostichopus japonicus, a sea cucumber with high nutritional value and pharmacological properties, is an important economic species that is widely raised in aquaculture in China. In recent years, continuous extreme high temperatures (up to 30°C) have occurred frequently in summer leading to mass mortality of sea cucumbers cultured in semi-open shallow regions seriously restricting the sustainable development of sea cucumber aquaculture. In the present study, we combined RNA-seq and PacBio single-molecular real-time (SMRT) sequencing technology to unveil the potential mechanisms of response to acute heat stress in A. japonicus coelomocytes. A total of 1,375 differentially expressed genes (DEGs) were identified in a comparison of control and 48 h heat stress (HS) groups. Pathway enrichment analysis indicated that nine important pathways induced by HS were significantly enriched (q-value < 0.05) and mostly fell into four classes: folding, sorting, and degradation, immune and infectious diseases, signal transduction, and post-transcriptional regulation. Among them, all 41 genes connected with protein processing in endoplasmic reticulum were significantly up-regulated, and 12 of these were selected and validated via qPCR. Furthermore, changes in alternative splicing (AS) were also identified in sea cucumbers following HS. A total of 1,224 and 1,251 differential alternative splicing (DAS) events were identified using splice junction counts (JC only) and reads on target and junction counts (JCEC) as the input for rMATS in CO-HS comparison. We further found that the RNA splicing-related genes were enriched in the spliceosome pathway and showed DAS in control versus heat-stressed animals. In particular, we compared and confirmed that the hsfs1 gene, the master regulator of the heat shock response, showed differentially spliced exons in response to HS. This is the first comprehensive study showing that transcriptional and post-transcriptional (AS) controls are involved in the acute heat stress response of sea cucumber coelomocytes and provides novel insights into the molecular mechanisms of echinoderm adaptation to environmental stress.

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“…In fact, several Hsp have been characterized from different sea cucumber species. Among these are Hsp 90, Hsp 70, Hsp 60 and members of the small Hsp family [28][29] [30][31] [32]. These genes have been reported to be expressed by cells in the intestine, coelomocytes and many other tissues.…”

Section: Heat Shock Proteinsmentioning

confidence: 99%

Molecular Characterization of the Stress Response of the Holothurian Central Nervous System

Cruz-González¹,

Quesada-Díaz²,

Miranda-Negrón³

et al. 2022

Preprint

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Injury to the central nervous system (CNS), in most vertebrate animals, results in permanent damage and lack of function, due to their limited regenerative capacities. In contrast, echinoderms can fully regenerate their radial nerve cord (RNC) following transection, with little or no scarring. Investigators have associated the regenerative capacity of some organisms with the stress response and inflammation produced by the injury. Here we explore the gene activation profile of the stressed holothurian CNS. To do this, we performed RNA sequencing on isolated RNC explants submitted to the stress of transection and enzyme dissection and compared them to explants kept in culture for 3 days following dissection. We describe stress-associated genes, including members of heat-shock families, ubiquitin-related pathways, transposons, and apoptosis that were differentially expressed. Surprisingly, the stress response does not induce apoptosis in this system. Other genes associated with stress in other animal models, such as hero proteins and those associated with the integrated stress response, were not found to be differentially expressed either. Our results provide a new viewpoint on the stress response in the nervous system of an organism with an amazing regenerative capacity. This is the first step to deciphering the molecular processes that allow echinoderms to undergo fully functional CNS regeneration while also providing a comparative view for students of the stress response in other organisms.

show abstract

Ultrastructural variation and key ER chaperones response induced by heat stress in intestinal cells of sea cucumber Apostichopus japonicus

Cited by 13 publications

References 61 publications

The Stress Response of the Holothurian Central Nervous System: A Transcriptomic Analysis

The Stress Response of the Holothurian Central Nervous System: A Transcriptomic Analysis

PacBio Isoform Sequencing and Illumina RNA Sequencing Provide Novel Insights on Responses to Acute Heat Stress in Apostichopus japonicus Coelomocytes

Molecular Characterization of the Stress Response of the Holothurian Central Nervous System

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