Lysyl Oxidase-like Protein Recognizes Viral Envelope Proteins and Bacterial Polysaccharides against Pathogen Infection via Induction of Expression of Antimicrobial Peptides

Lysyl oxidases (LOXs) are copper-dependent monoamine oxidases, and they play critical roles in extracellular matrix (ECM) remodeling. The LOX and LOX-like (LOXL) proteins also have a variety of biological functions, such as development and growth regulation, tumor suppression, and cellular senescenc...

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Main Authors: Peng-Yuan Lu, Guo-Juan Niu, Pan-Pan Hong, Jin-Xing Wang
Format: Article
Language:English
Published: MDPI AG 2022-09-01
Series:Viruses
Subjects:
Online Access:https://www.mdpi.com/1999-4915/14/9/2072
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author Peng-Yuan Lu
Guo-Juan Niu
Pan-Pan Hong
Jin-Xing Wang
author_facet Peng-Yuan Lu
Guo-Juan Niu
Pan-Pan Hong
Jin-Xing Wang
author_sort Peng-Yuan Lu
collection DOAJ
description Lysyl oxidases (LOXs) are copper-dependent monoamine oxidases, and they play critical roles in extracellular matrix (ECM) remodeling. The LOX and LOX-like (LOXL) proteins also have a variety of biological functions, such as development and growth regulation, tumor suppression, and cellular senescence. However, the functions of LOXLs containing repeated scavenger receptor cysteine-rich (SRCR) domains in immunity are rarely reported. In this study, we characterized the antiviral and antibacterial functions of a lysyl oxidase-like (LOXL) protein containing tandem SRCR domains in <i>Marsupenaeus japonicus</i>. The mRNA level of <i>LoxL</i> was significantly upregulated in the hemocytes and intestines of shrimp challenged using white spot syndrome virus (WSSV) or bacteria. After the knockdown of <i>LoxL</i> via RNA interference, WSSV replication and bacterial loads were apparently increased, and the survival rate of the shrimp decreased significantly, suggesting that LOXL functions against pathogen infection in shrimp. Mechanistically, LOXL interacted with the envelope proteins of WSSV or with lipopolysaccharide and peptidoglycan from bacteria in shrimp challenged using WSSV or bacteria, and it promoted the expression of a battery of antimicrobial peptides (AMPs) via the induction of Dorsal nuclear translocation against viral and bacterial infection. Moreover, LOXL expression was also positively regulated by Dorsal in the shrimp challenged by pathogens. These results indicate that, by acting as a pattern recognition receptor, LOXL plays vital roles in antiviral and antibacterial innate immunity by enhancing the expression of AMPs in shrimp.
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spelling doaj.art-f38a85f32b5843a19413b2a03f4d89612023-11-23T19:29:07ZengMDPI AGViruses1999-49152022-09-01149207210.3390/v14092072Lysyl Oxidase-like Protein Recognizes Viral Envelope Proteins and Bacterial Polysaccharides against Pathogen Infection via Induction of Expression of Antimicrobial PeptidesPeng-Yuan Lu0Guo-Juan Niu1Pan-Pan Hong2Jin-Xing Wang3Shandong Provincial Key Laboratory of Animal Cells and Developmental Biology, School of Life Sciences, Shandong University, Qingdao 266237, ChinaShandong Provincial Key Laboratory of Animal Cells and Developmental Biology, School of Life Sciences, Shandong University, Qingdao 266237, ChinaShandong Provincial Key Laboratory of Animal Cells and Developmental Biology, School of Life Sciences, Shandong University, Qingdao 266237, ChinaShandong Provincial Key Laboratory of Animal Cells and Developmental Biology, School of Life Sciences, Shandong University, Qingdao 266237, ChinaLysyl oxidases (LOXs) are copper-dependent monoamine oxidases, and they play critical roles in extracellular matrix (ECM) remodeling. The LOX and LOX-like (LOXL) proteins also have a variety of biological functions, such as development and growth regulation, tumor suppression, and cellular senescence. However, the functions of LOXLs containing repeated scavenger receptor cysteine-rich (SRCR) domains in immunity are rarely reported. In this study, we characterized the antiviral and antibacterial functions of a lysyl oxidase-like (LOXL) protein containing tandem SRCR domains in <i>Marsupenaeus japonicus</i>. The mRNA level of <i>LoxL</i> was significantly upregulated in the hemocytes and intestines of shrimp challenged using white spot syndrome virus (WSSV) or bacteria. After the knockdown of <i>LoxL</i> via RNA interference, WSSV replication and bacterial loads were apparently increased, and the survival rate of the shrimp decreased significantly, suggesting that LOXL functions against pathogen infection in shrimp. Mechanistically, LOXL interacted with the envelope proteins of WSSV or with lipopolysaccharide and peptidoglycan from bacteria in shrimp challenged using WSSV or bacteria, and it promoted the expression of a battery of antimicrobial peptides (AMPs) via the induction of Dorsal nuclear translocation against viral and bacterial infection. Moreover, LOXL expression was also positively regulated by Dorsal in the shrimp challenged by pathogens. These results indicate that, by acting as a pattern recognition receptor, LOXL plays vital roles in antiviral and antibacterial innate immunity by enhancing the expression of AMPs in shrimp.https://www.mdpi.com/1999-4915/14/9/2072<i>Marsupenaeus japonicus</i>white spot syndrome virus<i>Vibro anguillarum</i>lysyl oxidase-likeDorsalpattern recognition receptor
spellingShingle Peng-Yuan Lu
Guo-Juan Niu
Pan-Pan Hong
Jin-Xing Wang
Lysyl Oxidase-like Protein Recognizes Viral Envelope Proteins and Bacterial Polysaccharides against Pathogen Infection via Induction of Expression of Antimicrobial Peptides
Viruses
<i>Marsupenaeus japonicus</i>
white spot syndrome virus
<i>Vibro anguillarum</i>
lysyl oxidase-like
Dorsal
pattern recognition receptor
title Lysyl Oxidase-like Protein Recognizes Viral Envelope Proteins and Bacterial Polysaccharides against Pathogen Infection via Induction of Expression of Antimicrobial Peptides
title_full Lysyl Oxidase-like Protein Recognizes Viral Envelope Proteins and Bacterial Polysaccharides against Pathogen Infection via Induction of Expression of Antimicrobial Peptides
title_fullStr Lysyl Oxidase-like Protein Recognizes Viral Envelope Proteins and Bacterial Polysaccharides against Pathogen Infection via Induction of Expression of Antimicrobial Peptides
title_full_unstemmed Lysyl Oxidase-like Protein Recognizes Viral Envelope Proteins and Bacterial Polysaccharides against Pathogen Infection via Induction of Expression of Antimicrobial Peptides
title_short Lysyl Oxidase-like Protein Recognizes Viral Envelope Proteins and Bacterial Polysaccharides against Pathogen Infection via Induction of Expression of Antimicrobial Peptides
title_sort lysyl oxidase like protein recognizes viral envelope proteins and bacterial polysaccharides against pathogen infection via induction of expression of antimicrobial peptides
topic <i>Marsupenaeus japonicus</i>
white spot syndrome virus
<i>Vibro anguillarum</i>
lysyl oxidase-like
Dorsal
pattern recognition receptor
url https://www.mdpi.com/1999-4915/14/9/2072
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