Comp Biochem Physiol Part D Genomics Proteomics 2026 Mar 03;59:101801. doi: 10.1016/j.cbd.2026.101801.

Mechanisms of heat and hypoxia defense in the sea cucumber Apostichopus japonicus: Insights from ubiquitination regulation.

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Sea cucumbers Apostichopus japonicus are valuable resources for nature and food. High temperature and hypoxia are main kinds of stress factors for A. japonicus. Our study showed proteins from three stress-treatment groups (HT, LO and HT_LO) had high ubiquitin-conjugate levels. The mRNA expression of 6 ubiquitinating enzymes had a significant response, especially in HT_LO group. The global ubiquitinomes quantified a total of 1594 lysine ubiquitination sites on 924 proteins. Quantification values of 523, 387 and 804 Kub sites were differentially changed in HT, LO and HT_LO respectively. The top 3 up-regulated DUSs in HT vs C comparison were located in glyceraldehyde-3-phosphate dehydrogenase (GADPH), putative fatty acid-binding protein type 3-like (FABP3), heat shock protein 90-alpha (HSP90α). Some up-regulated DUSs were shared both in HT vs C comparison and LO vs C comparison, such as K(101) in FABP3 and K(104) in HSP90α. The ubiquitination quantitative level of sites in profilin (PFN), molecule interacting with CasL 3 (MICAL3), cytochrome P450 (CYP450) and HSP90α in HT_LO group markedly higher than those in the Control group. GO items associated with membrane and ribosome proteins, and KEGG pathways involved cellular degradation and ribosome, were significantly enriched in all stress-treatment groups. It was worth noting that mTOR signaling pathway, FoxO signaling pathway and TGF-β signaling pathway were significantly enriched only in HT_LO group compared with the Control group. Integrated analysis between ubiquitinome and transcriptomics data highlighted a variety of genes dysregulated in both the ubiquitination and the mRNA level. Our research may further help reveal the mechanism of stress response from the perspective of protein ubiquitination.

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