Valence-dependent immune responses of earthworm coelomocytes: Toxicity pathways and molecular mechanisms of As (III) and As (V)-induced immunotoxicity

• Published in: The Science of the total environment 2024-12, Vol.957, p.177474, Article 177474
• Main Authors: Wang, Tingting, Li, Xiangxiang, He, Falin, Guo, Shuqi, Du, Fei, Song, Hengyu, Liu, Rutao
• Format: Article
• Language: English
• Subjects: Animals; Arsenates - toxicity; Arsenic - toxicity; Arsenites - toxicity; Binding interaction; Immunotoxicity; Inorganic arsenic; Lysosomal dysfunction; Lysosomes - drug effects; Muramidase; Oligochaeta - physiology; Soil Pollutants - toxicity
• ISSN: 0048-9697; 1879-1026; 1879-1026
• DOI: 10.1016/j.scitotenv.2024.177474

Epidemiological studies in inorganic arsenic (iAs) exposure populations have offered convincing evidence that exposure to arsenite (As (III)) and arsenate (As (V)) are linked to immune dysfunction and immunosuppression. However, the valence-dependent immunotoxicity mechanism of iAs has not been explored. In this work, we conducted a thorough investigation and comparison of lysosome dysfunction in As (III) and As (V) induced earthworm typical immune cells coelomocytes, and the binding reaction between As (III)/As (V) and immunoprotein lysozyme (LZM). Results indicated As (III) and As (V) induced severe alterations in NR uptake and caused serious damage to lysosomal membrane, particularly As (III). As (III) (21.24 %) had a stronger inhibitory effect on LZM activity in coelomocytes than As (V) (67.40 %), which showed a similar toxic trend as enzyme activity in vitro (As (III)-68.66 % and As (V)-78.50 %). LZM skeleton relaxation, secondary structural transformation, fluorescence sensitization and particle alteration provided evidence for As (III) trigger more grievous immunoprotein dysfunction. In conclusion, As (III) and As (V) triggered lysosomal membrane destruction in coelomocytes, as well as induced structural changes in LZM result in lysosomal hydrolase dysfunction in coelomocytes. Ultimately, cellular lysosome dysfunction and destruction, which leads to the normal immune system of the cells is disrupted. As (III) induced stronger immunosuppression through lysosome pathway than As (V). Our work reveals the degree of lysosome dysfunction triggered by As (III) and As (V) probably responsible for the valence-dependent immunosuppression patterns of iAs, and provide new insights for As toxicity assessment. [Display omitted] •The immunotoxicity pattern was related to the capacity to induce lysosomal damage.•Changes in structure of LZM cause the function of lysosomal hydrolase to be destroyed in coelomocytes.•As (III) triggers more severe lysosome membrane destabilization and lysosomal hydrolase damage than As (V).