Hypochlorous acid and taurine chloramine co-mediate the innate arm of anti-Vibrio immunity in oyster hemocytes.

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Hauptverfasser: Wu, Siwei, Bai, Jing, Zhang, Xiangyu, Mao, Fan, Luo, Huazeng, Zhou, Ziyuan, Tao, Wensi, Wang, Wei, Yu, Ziniu, Wong, Nai-Kei, Zhang, Yang
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Veröffentlicht: Free radical biology & medicine 2025
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author Wu, Siwei
Bai, Jing
Zhang, Xiangyu
Mao, Fan
Luo, Huazeng
Zhou, Ziyuan
Tao, Wensi
Wang, Wei
Yu, Ziniu
Wong, Nai-Kei
Zhang, Yang
author_facet Wu, Siwei
Bai, Jing
Zhang, Xiangyu
Mao, Fan
Luo, Huazeng
Zhou, Ziyuan
Tao, Wensi
Wang, Wei
Yu, Ziniu
Wong, Nai-Kei
Zhang, Yang
Wu, Siwei
Bai, Jing
Zhang, Xiangyu
Mao, Fan
Luo, Huazeng
Zhou, Ziyuan
Tao, Wensi
Wang, Wei
Yu, Ziniu
Wong, Nai-Kei
Zhang, Yang
collection PubMed - marine biology
contents Hypochlorous acid and taurine chloramine co-mediate the innate arm of anti-Vibrio immunity in oyster hemocytes. Wu, Siwei Bai, Jing Zhang, Xiangyu Mao, Fan Luo, Huazeng Zhou, Ziyuan Tao, Wensi Wang, Wei Yu, Ziniu Wong, Nai-Kei Zhang, Yang Animals Hemocytes Taurine Immunity, Innate Vibrio parahaemolyticus Hypochlorous Acid Ostreidae Reactive Oxygen Species Vibrio Infections Balanced and temporally coordinated generation of reactive oxygen species (ROS) and antioxidants is crucial to productive clearance of pathogens in marine molluscan invertebrates, such as the oyster. Despite the presence of an oyster homolog of the myeloperoxidase (MPO) gene in its genome and a hyperabundant pool of intracellular taurine, it remains unclear how precisely ROS-based antibacterial immunity and pro-survival antioxidant production are orchestrated during microbial infections. Herein, we leveraged HKOCl-3, an established probe selective for hypochlorous acid (HOCl), to visualize the dynamics of bactericidal HOCl production in oyster hemocytes challenged with Vibrio parahaemolyticus, a clinically significant Gram-negative pathogen. We hypothesized that taurine (2-aminoethanesulphonic acid), an organosulfur osmolyte that scavenges HOCl efficiently, forms taurine chloramine (TauCl) in vivo to modulate hemocytic immune response, while mitigating host injury. In molecular imaging and flow cytometry, rapid production of HOCl was observed following V. parahaemolyticus challenge. TMB (3,3',5,5'-tetramethylbenzidine) assay confirmed the concomitant formation of TauCl in oyster hemocytes under V. parahaemolyticus stimulation. This TauCl biosynthesis was executed by the cysteine dioxygenase and cysteine sulfinic acid decarboxylase (CDO/CSAD) pathway, as verified by qRT-PCR. The potency of TauCl bactericidal activity was broadly comparable to that of HOCl in bacterial clearance assay. As a pro-survival agent, TauCl mitigated apoptosis in V. parahaemolyticus-challenged hemocytes, while this effect could be nullified by the chloramine scavenger bilirubin. In terms of transcriptomic changes, TauCl stimulated the phagosomes, endocytosis, FoxO signaling pathways, and induced upregulation of various antioxidant enzymes, thereby favoring redox homeostasis in hemocytes. Activation of pro-survival transcription was achieved by TauCl direct binding to Keap1. Overall, our work demonstrated for the first time how phagocyte-derived HOCl and TauCl act as immune effectors within an intimately overlapping window of host defense, with theoretical implications for understanding ROS metabolism and immunomodulation in broader disease contexts.
format Artículo científico
id pubmed_40541803
institution PubMed
language en
publishDate 2025
publisher Free radical biology & medicine
record_format pubmed
spellingShingle Hypochlorous acid and taurine chloramine co-mediate the innate arm of anti-Vibrio immunity in oyster hemocytes.
Wu, Siwei
Bai, Jing
Zhang, Xiangyu
Mao, Fan
Luo, Huazeng
Zhou, Ziyuan
Tao, Wensi
Wang, Wei
Yu, Ziniu
Wong, Nai-Kei
Zhang, Yang
Animals
Hemocytes
Taurine
Immunity, Innate
Vibrio parahaemolyticus
Hypochlorous Acid
Ostreidae
Reactive Oxygen Species
Vibrio Infections
Hypochlorous acid and taurine chloramine co-mediate the innate arm of anti-Vibrio immunity in oyster hemocytes. Wu, Siwei Bai, Jing Zhang, Xiangyu Mao, Fan Luo, Huazeng Zhou, Ziyuan Tao, Wensi Wang, Wei Yu, Ziniu Wong, Nai-Kei Zhang, Yang Animals Hemocytes Taurine Immunity, Innate Vibrio parahaemolyticus Hypochlorous Acid Ostreidae Reactive Oxygen Species Vibrio Infections Balanced and temporally coordinated generation of reactive oxygen species (ROS) and antioxidants is crucial to productive clearance of pathogens in marine molluscan invertebrates, such as the oyster. Despite the presence of an oyster homolog of the myeloperoxidase (MPO) gene in its genome and a hyperabundant pool of intracellular taurine, it remains unclear how precisely ROS-based antibacterial immunity and pro-survival antioxidant production are orchestrated during microbial infections. Herein, we leveraged HKOCl-3, an established probe selective for hypochlorous acid (HOCl), to visualize the dynamics of bactericidal HOCl production in oyster hemocytes challenged with Vibrio parahaemolyticus, a clinically significant Gram-negative pathogen. We hypothesized that taurine (2-aminoethanesulphonic acid), an organosulfur osmolyte that scavenges HOCl efficiently, forms taurine chloramine (TauCl) in vivo to modulate hemocytic immune response, while mitigating host injury. In molecular imaging and flow cytometry, rapid production of HOCl was observed following V. parahaemolyticus challenge. TMB (3,3',5,5'-tetramethylbenzidine) assay confirmed the concomitant formation of TauCl in oyster hemocytes under V. parahaemolyticus stimulation. This TauCl biosynthesis was executed by the cysteine dioxygenase and cysteine sulfinic acid decarboxylase (CDO/CSAD) pathway, as verified by qRT-PCR. The potency of TauCl bactericidal activity was broadly comparable to that of HOCl in bacterial clearance assay. As a pro-survival agent, TauCl mitigated apoptosis in V. parahaemolyticus-challenged hemocytes, while this effect could be nullified by the chloramine scavenger bilirubin. In terms of transcriptomic changes, TauCl stimulated the phagosomes, endocytosis, FoxO signaling pathways, and induced upregulation of various antioxidant enzymes, thereby favoring redox homeostasis in hemocytes. Activation of pro-survival transcription was achieved by TauCl direct binding to Keap1. Overall, our work demonstrated for the first time how phagocyte-derived HOCl and TauCl act as immune effectors within an intimately overlapping window of host defense, with theoretical implications for understanding ROS metabolism and immunomodulation in broader disease contexts.
title Hypochlorous acid and taurine chloramine co-mediate the innate arm of anti-Vibrio immunity in oyster hemocytes.
topic Animals
Hemocytes
Taurine
Immunity, Innate
Vibrio parahaemolyticus
Hypochlorous Acid
Ostreidae
Reactive Oxygen Species
Vibrio Infections
url https://pubmed.ncbi.nlm.nih.gov/40541803/