Polyamine Putrescine Regulates Oxidative Stress and Autophagy of Hemocytes Induced by Lipopolysaccharides in Pearl Oyster Pinctada fucata martensii

The polyamine putrescine (Put) is a ubiquitous small cationic amine. It plays an essential role in controlling the innate immune response. However, little is known about its function in mollusks. In this study, the Put content was observed to increase in the serum of pearl oyster Pinctada fucata mar...

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Main Authors: Yanfei Cao, Yu Jiao, Shuzhi Zhan, Xueru Liang, Zhixin Li, Jiayi Chen, Xinwei Xiong, Zefeng Gu, Xiaodong Du, Zhe Zheng
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-12-01
Series:Frontiers in Physiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fphys.2021.781324/full
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author Yanfei Cao
Yu Jiao
Yu Jiao
Yu Jiao
Yu Jiao
Shuzhi Zhan
Xueru Liang
Zhixin Li
Jiayi Chen
Xinwei Xiong
Zefeng Gu
Xiaodong Du
Xiaodong Du
Xiaodong Du
Xiaodong Du
Zhe Zheng
Zhe Zheng
Zhe Zheng
Zhe Zheng
author_facet Yanfei Cao
Yu Jiao
Yu Jiao
Yu Jiao
Yu Jiao
Shuzhi Zhan
Xueru Liang
Zhixin Li
Jiayi Chen
Xinwei Xiong
Zefeng Gu
Xiaodong Du
Xiaodong Du
Xiaodong Du
Xiaodong Du
Zhe Zheng
Zhe Zheng
Zhe Zheng
Zhe Zheng
author_sort Yanfei Cao
collection DOAJ
description The polyamine putrescine (Put) is a ubiquitous small cationic amine. It plays an essential role in controlling the innate immune response. However, little is known about its function in mollusks. In this study, the Put content was observed to increase in the serum of pearl oyster Pinctada fucata martensii after 6 and 24 h of lipopolysaccharide (LPS) stimulation. Activities of superoxide dismutase (SOD), catalase (CAT), and glutathione peroxidase (GSH-Px) increased, and nitric oxide synthase was downregulated in the Put group (i.e., combined treatment with Put and LPS) compared with that in the LPS group (i.e., combined treatment with phosphate-buffered saline and LPS). Furthermore, activities of alkaline phosphatase and acid phosphatase were inhibited after 6 h of LPS stimulation. The expression levels of the nuclear factor kappa B, IκB kinase, Janus kinase, and signal transducer and activator of transcription proteins genes were all significantly suppressed at 12 and 24 h in the Put group. Pseudomonas aeruginosa and Bacillus subtilis grew better after being incubated with the serum from the Put group than that from the LPS group. Additionally, the Put treatment remarkably inhibited the autophagy of hemocytes mediated by the AMP-activated protein kinase-mammalian target of rapamycin-Beclin-1 pathway. This study demonstrated that Put can effectively inhibit the inflammatory response induced by LPS in pearl oysters. These results provide useful information for further exploration of the immunoregulatory functions of polyamines in bivalves and contribute to the development of immunosuppressive agents.
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spelling doaj.art-9859e02d83b94d7cbc8061037fc822642022-12-21T23:17:19ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2021-12-011210.3389/fphys.2021.781324781324Polyamine Putrescine Regulates Oxidative Stress and Autophagy of Hemocytes Induced by Lipopolysaccharides in Pearl Oyster Pinctada fucata martensiiYanfei Cao0Yu Jiao1Yu Jiao2Yu Jiao3Yu Jiao4Shuzhi Zhan5Xueru Liang6Zhixin Li7Jiayi Chen8Xinwei Xiong9Zefeng Gu10Xiaodong Du11Xiaodong Du12Xiaodong Du13Xiaodong Du14Zhe Zheng15Zhe Zheng16Zhe Zheng17Zhe Zheng18Fishery College, Guangdong Ocean University, Zhanjiang, ChinaFishery College, Guangdong Ocean University, Zhanjiang, ChinaPearl Breeding and Processing Engineering Technology Research Centre of Guangdong Province, Zhanjiang, ChinaGuangdong Science and Innovation Center for Pearl Culture, Zhanjiang, ChinaGuangdong Provincial Engineering Laboratory for Mariculture Organism Breeding, Zhanjiang, ChinaFishery College, Guangdong Ocean University, Zhanjiang, ChinaFishery College, Guangdong Ocean University, Zhanjiang, ChinaFishery College, Guangdong Ocean University, Zhanjiang, ChinaFishery College, Guangdong Ocean University, Zhanjiang, ChinaFishery College, Guangdong Ocean University, Zhanjiang, ChinaFishery College, Guangdong Ocean University, Zhanjiang, ChinaFishery College, Guangdong Ocean University, Zhanjiang, ChinaPearl Breeding and Processing Engineering Technology Research Centre of Guangdong Province, Zhanjiang, ChinaGuangdong Science and Innovation Center for Pearl Culture, Zhanjiang, ChinaGuangdong Provincial Engineering Laboratory for Mariculture Organism Breeding, Zhanjiang, ChinaFishery College, Guangdong Ocean University, Zhanjiang, ChinaPearl Breeding and Processing Engineering Technology Research Centre of Guangdong Province, Zhanjiang, ChinaGuangdong Science and Innovation Center for Pearl Culture, Zhanjiang, ChinaGuangdong Provincial Engineering Laboratory for Mariculture Organism Breeding, Zhanjiang, ChinaThe polyamine putrescine (Put) is a ubiquitous small cationic amine. It plays an essential role in controlling the innate immune response. However, little is known about its function in mollusks. In this study, the Put content was observed to increase in the serum of pearl oyster Pinctada fucata martensii after 6 and 24 h of lipopolysaccharide (LPS) stimulation. Activities of superoxide dismutase (SOD), catalase (CAT), and glutathione peroxidase (GSH-Px) increased, and nitric oxide synthase was downregulated in the Put group (i.e., combined treatment with Put and LPS) compared with that in the LPS group (i.e., combined treatment with phosphate-buffered saline and LPS). Furthermore, activities of alkaline phosphatase and acid phosphatase were inhibited after 6 h of LPS stimulation. The expression levels of the nuclear factor kappa B, IκB kinase, Janus kinase, and signal transducer and activator of transcription proteins genes were all significantly suppressed at 12 and 24 h in the Put group. Pseudomonas aeruginosa and Bacillus subtilis grew better after being incubated with the serum from the Put group than that from the LPS group. Additionally, the Put treatment remarkably inhibited the autophagy of hemocytes mediated by the AMP-activated protein kinase-mammalian target of rapamycin-Beclin-1 pathway. This study demonstrated that Put can effectively inhibit the inflammatory response induced by LPS in pearl oysters. These results provide useful information for further exploration of the immunoregulatory functions of polyamines in bivalves and contribute to the development of immunosuppressive agents.https://www.frontiersin.org/articles/10.3389/fphys.2021.781324/fullpolyaminesputrescineimmune regulationoxidative stressmolluskspearl oysters
spellingShingle Yanfei Cao
Yu Jiao
Yu Jiao
Yu Jiao
Yu Jiao
Shuzhi Zhan
Xueru Liang
Zhixin Li
Jiayi Chen
Xinwei Xiong
Zefeng Gu
Xiaodong Du
Xiaodong Du
Xiaodong Du
Xiaodong Du
Zhe Zheng
Zhe Zheng
Zhe Zheng
Zhe Zheng
Polyamine Putrescine Regulates Oxidative Stress and Autophagy of Hemocytes Induced by Lipopolysaccharides in Pearl Oyster Pinctada fucata martensii
Frontiers in Physiology
polyamines
putrescine
immune regulation
oxidative stress
mollusks
pearl oysters
title Polyamine Putrescine Regulates Oxidative Stress and Autophagy of Hemocytes Induced by Lipopolysaccharides in Pearl Oyster Pinctada fucata martensii
title_full Polyamine Putrescine Regulates Oxidative Stress and Autophagy of Hemocytes Induced by Lipopolysaccharides in Pearl Oyster Pinctada fucata martensii
title_fullStr Polyamine Putrescine Regulates Oxidative Stress and Autophagy of Hemocytes Induced by Lipopolysaccharides in Pearl Oyster Pinctada fucata martensii
title_full_unstemmed Polyamine Putrescine Regulates Oxidative Stress and Autophagy of Hemocytes Induced by Lipopolysaccharides in Pearl Oyster Pinctada fucata martensii
title_short Polyamine Putrescine Regulates Oxidative Stress and Autophagy of Hemocytes Induced by Lipopolysaccharides in Pearl Oyster Pinctada fucata martensii
title_sort polyamine putrescine regulates oxidative stress and autophagy of hemocytes induced by lipopolysaccharides in pearl oyster pinctada fucata martensii
topic polyamines
putrescine
immune regulation
oxidative stress
mollusks
pearl oysters
url https://www.frontiersin.org/articles/10.3389/fphys.2021.781324/full
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