Characterization of myeloperoxidase and its contribution to antimicrobial effect on extracellular traps in flounder (Paralichthys olivaceus)

Qiujie Gan; Heng Chi; Roy Ambli Dalmo; Xianghu Meng; Xiaoqian Tang; Jing Xing; Xiuzhen Sheng; Wenbin Zhan

doi:10.3389/fimmu.2023.1124813

Characterization of myeloperoxidase and its contribution to antimicrobial effect on extracellular traps in flounder (Paralichthys olivaceus)

Front Immunol. 2023 Jan 26:14:1124813. doi: 10.3389/fimmu.2023.1124813. eCollection 2023.

Authors

Qiujie Gan¹, Heng Chi^{1

2}, Roy Ambli Dalmo³, Xianghu Meng¹, Xiaoqian Tang^{1

2}, Jing Xing^{1

2}, Xiuzhen Sheng^{1

2}, Wenbin Zhan^{1

2}

Affiliations

¹ Laboratory of Pathology and Immunology of Aquatic Animals, KLMME, Ocean University of China, Qingdao, China.
² Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, Qingdao, China.
³ Norwegian College of Fishery Science, Faculty of Biosciences, Fisheries and Economics, UiT - the Arctic University of Norway, Tromsø, Norway.

Abstract

Myeloperoxidase (MPO) is a cationic leukocyte haloperoxidase and together with other proteins, they possess activities against various microorganisms and are involved in extracellular trap (ET) formation. The present work describes the gene and deduced protein sequences, and functions of MPO in flounder (PoMPO). The PoMPO possesses a 2313 bp open reading frame (ORF) that encodes a protein of 770 amino acids. The highest PoMPO mRNA expression levels were found in the head kidney, followed by peritoneal cells, gill, spleen, skin, muscle, and liver. PoMPO was expressed in MHCII⁺ and GCSFR⁺ cells which indicated that PoMPO mainly is expressed in flounder macrophages and granulocytes. Bacterial lipopolysaccharide-stimulated peritoneal leukocytes showed an increased protein level of PoMPO while it seemed that LPS also promoted the migration of MPO⁺ cells from the head kidney into the peripheral blood and peritoneal cavity. After phorbol 12-myristate 13-acetate (PMA) or bacterial stimulation, flounder leukocytes produced typical ET structures containing DNA with decoration by MPO. The ETs containing DNA and PoMPO effectively inhibited the proliferation of ET-trapped bacteria. Blocking PoMPO with antibodies decreased the enzymatic activity, which attenuated the antibacterial activity of ETs. This study pinpoints the involvement of ETs in flounder innate responses to pathogens.

Keywords: antibiosis; extracellular traps; fish; immune response; myeloperoxidase.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
Anti-Infective Agents*
Extracellular Traps*
Flounder* / genetics
Gene Expression Regulation
Peroxidase / genetics
Sequence Alignment

Substances

Peroxidase
Anti-Infective Agents

Grants and funding

This study was jointly supported by grants from the National Key Research and Development Program of China (2019YFD0900101), the National Natural Science Foundation of China (31872594 & 31730101), the Research Council of Norway (Forskiningsrådet, 301401) and the Young Talents Program of Ocean University of China (2019082).