TmPGRP-SA regulates Antimicrobial Response to Bacteria and Fungi in the Fat Body and Gut of Tenebrio molitor

Keshavarz, Maryam; Jo, Yong Hun; Edosa, Tariku Tesfaye; Bae, Young‐Min

doi:10.3390/ijms21062113

Cited by 17 publications

(13 citation statements)

References 57 publications

(108 reference statements)

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“…The sensitivity of T. molitor larvae with downregulated expression of TmSpz-like , TmSpz-4 , and TmSpz-6 to E. coli infections may be related to cross-talk between the Toll and IMD pathways. E. coli induces the activation of Spz in T. molitor larvae, suggesting that polymeric DAP-type PGN forms a complex with Tenebrio PGRP-SA to activate the Toll receptor ligand Spz [ 4 , 32 ]. The induction of the Toll pathway in Drosophila and T. molitor depends on the binding of Spz to Toll.…”

Section: Discussionmentioning

confidence: 99%

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TmSpz-like Plays a Fundamental Role in Response to E. coli but Not S. aureus or C. albican Infection in Tenebrio molitor via Regulation of Antimicrobial Peptide Production

Jang

Patnaik

Kojour

et al. 2021

IJMS

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The cystine knot protein Spätzle is a Toll receptor ligand that modulates the intracellular signaling cascade involved in the nuclear factor kappa B (NF-κB)-mediated regulation of antimicrobial peptide (AMP)-encoding genes. Spätzle-mediated activation of the Toll pathway is critical for the innate immune responses of insects against Gram-positive bacteria and fungi. In this study, the open reading frame (ORF) sequence of Spätzle-like from T. molitor (TmSpz-like) identified from the RNA sequencing dataset was cloned and sequenced. The 885-bp TmSpz-like ORF encoded a polypeptide of 294 amino acid residues. TmSpz-like comprised a cystine knot domain with six conserved cysteine residues that formed three disulfide bonds. Additionally, TmSpz-like exhibited the highest amino acid sequence similarity with T. castaneum Spätzle (TcSpz). In the phylogenetic tree, TmSpz-like and TcSpz were located within a single cluster. The expression of TmSpz-like was upregulated in the Malpighian tubules and gut tissues of T. molitor. Additionally, the expression of TmSpz-like in the whole body and gut of the larvae was upregulated at 24 h post-E. coli infection. The results of RNA interference experiments revealed that TmSpz-like is critical for the viability of E. coli-infected T. molitor larvae. Eleven AMP-encoding genes were downregulated in the E. coli-infected TmSpz-like knockdown larvae, which suggested that TmSpz-like positively regulated these genes. Additionally, the NF-κB-encoding genes (TmDorX1, TmDorX2, and TmRelish) were downregulated in the E. coli-infected TmSpz-like knockdown larvae. Thus, TmSpz-like plays a critical role in the regulation of AMP production in T. molitor in response to E. coli infection.

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Section: Discussionmentioning

confidence: 99%

“…Briefly, the TLR-NF-κB pathway in T. molitor is dependent on the cleaved form of Spz. This suggests that Spz proteins have promiscuous roles in the innate immunity of insects against pathogens [ 4 ]. Furthermore, Tm Spz proteins can function as central immune modulators for biosurfactant-mediated AMP production in T. molitor [ 5 ].…”

Section: Introductionmentioning

confidence: 99%

TmSpz-like Plays a Fundamental Role in Response to E. coli but Not S. aureus or C. albican Infection in Tenebrio molitor via Regulation of Antimicrobial Peptide Production

Jang

Patnaik

Kojour

et al. 2021

IJMS

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“… 34 , 36 Antimicrobial peptides are other humoral components that participate in the T. molitor immune response against fungal pathogens. 68 , 69 Thus, one limitation of our study and a future direction is to assess the contribution of these immune effectors against Sporothrix spp.…”

Section: Discussionmentioning

confidence: 99%

Tenebrio molitor as an Alternative Model to Analyze the Sporothrix Species Virulence

Lozoya-Pérez¹,

García-Carnero²,

Martínez-Álvarez³

et al. 2021

IDR

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Background Sporotrichosis is an increasing threat for humans, affecting mainly skin and subcutaneous tissues but that can cause disseminated infection in immunocompromised patients. Sporothrix schenckii, Sporothrix brasiliensis , and Sporothrix globosa are the main etiological agents of this mycosis, and each species show different virulence levels. The gold standard to assess fungal virulence is the mouse model that is expensive and time-consuming. Thus, invertebrate models have been reported as an alternative for the evaluation of fungal virulence. Here, we assessed whether Tenebrio molitor larvae could be a new alternative to study Sporothrix spp. virulence. Methods T. molitor larvae were inoculated with different doses of S. schenckii, S. brasiliensis , and S. globosa , and animal mortality, cytotoxicity, and immunological parameters were analyzed, including the ability to stimulate immunological priming. Results Mortality curves demonstrated that yeast-like cells were the best fungal morphology to kill larvae and showed a similar ranking in virulence than that reported in other animal models, ie, being S. brasiliensis and S. globosa the species with the highest and lowest virulence, respectively. The usefulness of this model was validated with the analysis of several S. schenckii strains with different virulence degrees, and changes in cytotoxicity, humoral and cellular immunological parameters. Low-virulence strains stimulated low levels of cytotoxicity, phenoloxidase activity, and hemocyte countings, and these immunological cells poorly uptake fungi. Moreover, using recombinant Gp70 from S. schenckii immunological priming was stimulated in larvae and this protected against a lethal dose of fungal cells from any of the three species under study. Conclusion The study demonstrated that T. molitor larvae are an appropriate alternative invertebrate model to analyze the virulence of S. schenckii, S. brasiliensis , and S. globosa . Additionally, hemocyte levels, phenoloxidase activity, cytotoxicity, uptake by hemocytes, and immunological priming are biological parameters that can be used to study the Sporothrix–T. molitor interaction.

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“…Under temporal distribution experiments, TmSpz1b was found to be induced more in hemocytes 6 h following the injection of E. coli, S. aureus , and C. albicans . In our previous studies we have used the same pathogens to identify the immunological role of Toll and IMD pathways through RNAi experiments ( Keshavarz et al, 2020 ). In normal conditions, T. molitor challenged by these pathogens shows higher survival rate.…”

Section: Discussionmentioning

confidence: 99%

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

Bae

Patnaik

et al. 2021

Front. Physiol.

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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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TmPGRP-SA regulates Antimicrobial Response to Bacteria and Fungi in the Fat Body and Gut of Tenebrio molitor

Cited by 17 publications

References 57 publications

TmSpz-like Plays a Fundamental Role in Response to E. coli but Not S. aureus or C. albican Infection in Tenebrio molitor via Regulation of Antimicrobial Peptide Production

TmSpz-like Plays a Fundamental Role in Response to E. coli but Not S. aureus or C. albican Infection in Tenebrio molitor via Regulation of Antimicrobial Peptide Production

Tenebrio molitor as an Alternative Model to Analyze the Sporothrix Species Virulence

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

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