Ferroptosis resists intracellular Vibrio splendidus AJ01 mediated by ferroportin in sea cucumber Apostichopus japonicus

被引:0
|
作者
Wang, Chengyang [1 ]
Xiang, Yangxi [1 ,3 ]
Shao, Yina [1 ,3 ]
Li, Chenghua [1 ,2 ,3 ]
机构
[1] Ningbo Univ, State Key Lab Managing Biot & Chem Threats Qual &, Ningbo, Peoples R China
[2] Lab Marine Fisheries Sci & Food Prod Proc, Qingdao, Peoples R China
[3] Ningbo Univ, 818 Fenghua Rd, Ningbo 315211, Zhejiang, Peoples R China
关键词
Apostichopus japonicus; Ferroptosis; Vibrio splendidus; Ferrous iron; Ferroportin; CELL-DEATH; IRON HOMEOSTASIS; STRESS; MACROPHAGES; REGULATORS; TRANSPORT;
D O I
10.1016/j.fsi.2024.109585
中图分类号
S9 [水产、渔业];
学科分类号
0908 ;
摘要
Ferroptosis, a kind of programmed cell death, is characterized with iron-dependent lipid ROS buildup, which is considered as an important cellular immunity in resisting intracellular bacterial infection in mammalian macrophages. In this process, lipid ROS oxidizes the bacterial biofilm to inhibit intracellular bacteria. However, the function of ferroptosis in invertebrate remains unknown. In this study, the existence of ferroptosis in Apostichopus japonicus coelomocytes was confirmed, and its antibacterial mechanism was investigated. First, our results indicated that the expression of glutathione peroxidase (AjGPX4) was significantly inhibited by 0.21-fold (p < 0.01) after injecting A. japonicus with the ferroptosis inducer RSL3, and the contents of MDA (3.93-fold, p < 0.01), ferrous iron (1.40-fold, p < 0.01), and lipid ROS (3.10-fold, p < 0.01) were all significantly increased under this condition and simultaneously accompanied with mitochondrial contraction and disappearance of cristae, indicating the existence of ferroptosis in the coelomocytes of A. japonicus. Subsequently, the contents of ferrous iron (1.40-fold, p < 0.05), MDA (2.10-fold, p < 0.01), ROS (1.70-fold, p < 0.01), and lipid ROS (2.50-fold, p < 0.01) were all significantly increased, whereas the mitochondrial membrane potential and GSH/GSSG were markedly decreased by 0.68-fold (p < 0.05) and 0.69-fold (p < 0.01) under Vibrio splendidus (AJ01) infection. This process could be reversed by the iron-chelating agent deferoxamine mesylate, which indicated that AJ01 could induce coelomocytic ferroptosis. Moreover, the results demonstrated that the intracellular AJ01 load was clearly decreased to 0.49-fold (p < 0.05) and 0.06-fold (p < 0.01) after treating coelomocytes with RSL3 and ferrous iron, which indicated that enhanced ferroptosis could inhibit bacterial growth. Finally, subcellular localization demonstrated that ferrous iron efflux protein ferroportin (AjFPN) and intracellular AJ01 were colocalized in coelomocytes. After AjFPN interference (0.58-fold, p < 0.01), the signals of ferrous iron and lipid ROS levels in intracellular AJ01 were significantly reduced by 0.38-fold (p < 0.01) and 0.48-fold (p < 0.01), indicating that AjFPN was an important factor in the introduction of ferroptosis into intracellular bacteria. Overall, our findings indicated that ferroptosis could resist intracellular AJ01 infection via AjFPN. These findings provide a novel defense mechanism for aquatic animals against intracellular bacterial infection.
引用
收藏
页数:11
相关论文
共 50 条
  • [32] MiR-210, not let-7, regulates Akt gene expression against Vibrio splendidus infection in the sea cucumber Apostichopus japonicus
    Liu, Li
    Ning, Bingyu
    Zhan, Yaoyao
    Zhao, Tanjun
    Chang, Yaqing
    FISH & SHELLFISH IMMUNOLOGY, 2024, 153
  • [33] Effects of continuous and alternate administration of -glucan and mannan-oligosaccharide on the growth, immunity and resistance against Vibrio splendidus of sea cucumber Apostichopus japonicus (Selenka)
    Bai, Nan
    Zhang, Wenbing
    Mai, Kangsen
    Gu, Min
    Xu, Wei
    AQUACULTURE RESEARCH, 2013, 44 (10) : 1613 - 1624
  • [34] Dietary supplements of guanosine improve the growth, non-specific immunity of sea cucumber, Apostichopus japonicus Selenka, and its resistance against Vibrio splendidus
    Chen, X. R.
    Mai, K. S.
    Zhang, W. B.
    Tan, B. P.
    Yuan, Y. H.
    Wang, Q. C.
    Liang, H. O.
    Zhao, L. M.
    AQUACULTURE NUTRITION, 2018, 24 (01) : 571 - 578
  • [35] Effects of dietary Vibrio sp. 33 on growth, innate immunity, gut microbiota profile and disease resistance against Vibrio splendidus of juvenile sea cucumber Apostichopus japonicus
    Lu, Tianyu
    Wang, Chengyang
    Guo, Ming
    Li, Chenghua
    Shao, Yina
    DEVELOPMENTAL AND COMPARATIVE IMMUNOLOGY, 2024, 150
  • [36] AMPK-mediated glutaminolysis maintains coelomocytes redox homeostasis in Vibrio splendidus-challenged Apostichopus japonicus
    Zhou, Fangyuan
    Sun, Lianlian
    Shao, Yina
    Zhang, Xiumei
    Li, Chenghua
    FISH & SHELLFISH IMMUNOLOGY, 2022, 122 : 170 - 180
  • [37] Novel secreted STPKLRR from Vibrio splendidus AJ01 promotes pathogen internalization via mediating tropomodulin phosphorylation dependent cytoskeleton rearrangement
    Dai, Fa
    Guo, Ming
    Shao, Yina
    Li, Chenghua
    PLOS PATHOGENS, 2023, 19 (05)
  • [38] MiR-31 modulates coelomocytes ROS production via targeting p105 in Vibrio splendidus challenged sea cucumber Apostichopus japonicus in vitro and in vivo
    Lu, Meng
    Zhang, Pengjuan
    Li, Chenghua
    Zhang, Weiwei
    Jin, Chunhua
    Han, Qingxi
    FISH & SHELLFISH IMMUNOLOGY, 2015, 45 (02) : 293 - 299
  • [39] Effects of dietary live yeast Hanseniaspora opuntiae C21 on the immune and disease resistance against Vibrio splendidus infection in juvenile sea cucumber Apostichopus japonicus
    Ma, Yuexin
    Liu, Zhiming
    Yang, Zhiping
    Li, Ming
    Liu, Jiao
    Song, Jian
    FISH & SHELLFISH IMMUNOLOGY, 2013, 34 (01) : 66 - 73
  • [40] Dietary effect chitosan nanoparticles on growth performance, immunity and resistance against Vibrio splendidus in the sea cucumber Apostichopus japonicas
    Wang, Rongyue
    Li, Xiaofan
    Tang, Jinwei
    Liu, Juan
    Yin, Heng
    Li, Ruijun
    Ye, Shigen
    AQUACULTURE REPORTS, 2023, 30