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: Young Min Bae, Yong Hun Jo, Bharat Bhusan Patnaik, Bo Bae Kim, Ki Beom Park, Tariku Tesfaye Edosa, Maryam Keshavarz, Maryam Ali Mohammadie Kojour, Yong Seok Lee, Yeon Soo Han
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Publicado: Frontiers Media S.A. 2021
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Acceso en línea:https://doaj.org/article/36ecaaafdde54ffe93633d286212df38
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spelling oai:doaj.org-article:36ecaaafdde54ffe93633d286212df382021-11-18T08:35:12ZTenebrio molitor Spätzle 1b Is Required to Confer Antibacterial Defense Against Gram-Negative Bacteria by Regulation of Antimicrobial Peptides1664-042X10.3389/fphys.2021.758859https://doaj.org/article/36ecaaafdde54ffe93633d286212df382021-11-01T00:00:00Zhttps://www.frontiersin.org/articles/10.3389/fphys.2021.758859/fullhttps://doaj.org/toc/1664-042XInnate 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.Young Min BaeYong Hun JoBharat Bhusan PatnaikBo Bae KimKi Beom ParkTariku Tesfaye EdosaTariku Tesfaye EdosaMaryam KeshavarzMaryam KeshavarzMaryam Ali Mohammadie KojourYong Seok LeeYeon Soo HanFrontiers Media S.A.articleT. molitorspätzleinnate immunityantimicrobial peptidesRNA interferencePhysiologyQP1-981ENFrontiers in Physiology, Vol 12 (2021)
institution DOAJ
collection DOAJ
language EN
topic T. molitor
spätzle
innate immunity
antimicrobial peptides
RNA interference
Physiology
QP1-981
spellingShingle T. molitor
spätzle
innate immunity
antimicrobial peptides
RNA interference
Physiology
QP1-981
Young Min Bae
Yong Hun Jo
Bharat Bhusan Patnaik
Bo Bae Kim
Ki Beom Park
Tariku Tesfaye Edosa
Tariku Tesfaye Edosa
Maryam Keshavarz
Maryam Keshavarz
Maryam Ali Mohammadie Kojour
Yong Seok Lee
Yeon Soo Han
Tenebrio molitor Spätzle 1b Is Required to Confer Antibacterial Defense Against Gram-Negative Bacteria by Regulation of Antimicrobial Peptides
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.
format article
author Young Min Bae
Yong Hun Jo
Bharat Bhusan Patnaik
Bo Bae Kim
Ki Beom Park
Tariku Tesfaye Edosa
Tariku Tesfaye Edosa
Maryam Keshavarz
Maryam Keshavarz
Maryam Ali Mohammadie Kojour
Yong Seok Lee
Yeon Soo Han
author_facet Young Min Bae
Yong Hun Jo
Bharat Bhusan Patnaik
Bo Bae Kim
Ki Beom Park
Tariku Tesfaye Edosa
Tariku Tesfaye Edosa
Maryam Keshavarz
Maryam Keshavarz
Maryam Ali Mohammadie Kojour
Yong Seok Lee
Yeon Soo Han
author_sort Young Min Bae
title 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_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_sort tenebrio molitor spätzle 1b is required to confer antibacterial defense against gram-negative bacteria by regulation of antimicrobial peptides
publisher Frontiers Media S.A.
publishDate 2021
url https://doaj.org/article/36ecaaafdde54ffe93633d286212df38
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