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Tenebrio molitor Spätzle 1b Is Required to Confer Antibacterial Defense Against Gram-Negative Bacteria by Regulation of Antimicrobial Peptides

Innate immunity is the ultimate line of defense against invading pathogens in insects. Unlike in the mammalian model, in the insect model, invading pathogens are recognized by extracellular receptors, which activate the Toll signaling pathway through an extracellular serine protease cascade. In the...

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Autores principales: Bae, Young Min, Jo, Yong Hun, Patnaik, Bharat Bhusan, Kim, Bo Bae, Park, Ki Beom, Edosa, Tariku Tesfaye, Keshavarz, Maryam, Kojour, Maryam Ali Mohammadie, Lee, Yong Seok, Han, Yeon Soo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8637286/
https://www.ncbi.nlm.nih.gov/pubmed/34867464
http://dx.doi.org/10.3389/fphys.2021.758859
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author Bae, Young Min
Jo, Yong Hun
Patnaik, Bharat Bhusan
Kim, Bo Bae
Park, Ki Beom
Edosa, Tariku Tesfaye
Keshavarz, Maryam
Kojour, Maryam Ali Mohammadie
Lee, Yong Seok
Han, Yeon Soo
author_facet Bae, Young Min
Jo, Yong Hun
Patnaik, Bharat Bhusan
Kim, Bo Bae
Park, Ki Beom
Edosa, Tariku Tesfaye
Keshavarz, Maryam
Kojour, Maryam Ali Mohammadie
Lee, Yong Seok
Han, Yeon Soo
author_sort Bae, Young Min
collection PubMed
description Innate immunity is the ultimate line of defense against invading pathogens in insects. Unlike in the mammalian model, in the insect model, invading pathogens are recognized by extracellular receptors, which activate the Toll signaling pathway through an extracellular serine protease cascade. In the Toll-NF-κB pathway, the extracellular spätzle protein acts as a downstream ligand for Toll receptors in insects. In this study, we identified a novel Spätzle isoform (TmSpz1b) from RNA sequencing database of Tenebrio molitor. TmSpz1b was bioinformatically analyzed, and functionally characterized for the antimicrobial function by RNA interference (RNAi). The 702 bp open reading frame of TmSpz1b encoded a putative protein of 233 amino acid residues. A conserved cystine-knot domain with seven cysteine residues in TmSpz1b was involved in three disulfide bridges and the formation of a spätzle dimer. TmSpz1b was mostly expressed in the hemocytes of T. molitor late instar larvae. The mRNA expression of TmSpz1b was highly induced in the hemocytes after Escherichia coli, Staphylococcus aureus, and Candida albicans stimulation of T. molitor larvae. TmSpz1b silenced larvae were significantly more susceptible to E. coli infection. In addition, RNAi-based functional assay characterized TmSpz1b to be involved in the positive regulation of antimicrobial peptide genes in hemocytes and fat bodies. Further, the TmDorX2 transcripts were downregulated in TmSpz1b silenced individuals upon E. coli challenge suggesting the relationship to Toll signaling pathway. These results indicate that TmSpz1b is involved in the T. molitor innate immunity, causes the sequestration of Gram-negative bacteria by the regulatory action of antimicrobial peptides, and enhances the survival of T. molitor larvae.
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spelling pubmed-86372862021-12-03 Tenebrio molitor Spätzle 1b Is Required to Confer Antibacterial Defense Against Gram-Negative Bacteria by Regulation of Antimicrobial Peptides Bae, Young Min Jo, Yong Hun Patnaik, Bharat Bhusan Kim, Bo Bae Park, Ki Beom Edosa, Tariku Tesfaye Keshavarz, Maryam Kojour, Maryam Ali Mohammadie Lee, Yong Seok Han, Yeon Soo Front Physiol Physiology Innate immunity is the ultimate line of defense against invading pathogens in insects. Unlike in the mammalian model, in the insect model, invading pathogens are recognized by extracellular receptors, which activate the Toll signaling pathway through an extracellular serine protease cascade. In the Toll-NF-κB pathway, the extracellular spätzle protein acts as a downstream ligand for Toll receptors in insects. In this study, we identified a novel Spätzle isoform (TmSpz1b) from RNA sequencing database of Tenebrio molitor. TmSpz1b was bioinformatically analyzed, and functionally characterized for the antimicrobial function by RNA interference (RNAi). The 702 bp open reading frame of TmSpz1b encoded a putative protein of 233 amino acid residues. A conserved cystine-knot domain with seven cysteine residues in TmSpz1b was involved in three disulfide bridges and the formation of a spätzle dimer. TmSpz1b was mostly expressed in the hemocytes of T. molitor late instar larvae. The mRNA expression of TmSpz1b was highly induced in the hemocytes after Escherichia coli, Staphylococcus aureus, and Candida albicans stimulation of T. molitor larvae. TmSpz1b silenced larvae were significantly more susceptible to E. coli infection. In addition, RNAi-based functional assay characterized TmSpz1b to be involved in the positive regulation of antimicrobial peptide genes in hemocytes and fat bodies. Further, the TmDorX2 transcripts were downregulated in TmSpz1b silenced individuals upon E. coli challenge suggesting the relationship to Toll signaling pathway. These results indicate that TmSpz1b is involved in the T. molitor innate immunity, causes the sequestration of Gram-negative bacteria by the regulatory action of antimicrobial peptides, and enhances the survival of T. molitor larvae. Frontiers Media S.A. 2021-11-18 /pmc/articles/PMC8637286/ /pubmed/34867464 http://dx.doi.org/10.3389/fphys.2021.758859 Text en Copyright © 2021 Bae, Jo, Patnaik, Kim, Park, Edosa, Keshavarz, Kojour, Lee and Han. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Physiology
Bae, Young Min
Jo, Yong Hun
Patnaik, Bharat Bhusan
Kim, Bo Bae
Park, Ki Beom
Edosa, Tariku Tesfaye
Keshavarz, Maryam
Kojour, Maryam Ali Mohammadie
Lee, Yong Seok
Han, Yeon Soo
Tenebrio molitor Spätzle 1b Is Required to Confer Antibacterial Defense Against Gram-Negative Bacteria by Regulation of Antimicrobial Peptides
title Tenebrio molitor Spätzle 1b Is Required to Confer Antibacterial Defense Against Gram-Negative Bacteria by Regulation of Antimicrobial Peptides
title_full Tenebrio molitor Spätzle 1b Is Required to Confer Antibacterial Defense Against Gram-Negative Bacteria by Regulation of Antimicrobial Peptides
title_fullStr Tenebrio molitor Spätzle 1b Is Required to Confer Antibacterial Defense Against Gram-Negative Bacteria by Regulation of Antimicrobial Peptides
title_full_unstemmed Tenebrio molitor Spätzle 1b Is Required to Confer Antibacterial Defense Against Gram-Negative Bacteria by Regulation of Antimicrobial Peptides
title_short Tenebrio molitor Spätzle 1b Is Required to Confer Antibacterial Defense Against Gram-Negative Bacteria by Regulation of Antimicrobial Peptides
title_sort tenebrio molitor spätzle 1b is required to confer antibacterial defense against gram-negative bacteria by regulation of antimicrobial peptides
topic Physiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8637286/
https://www.ncbi.nlm.nih.gov/pubmed/34867464
http://dx.doi.org/10.3389/fphys.2021.758859
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