TmSpz6 Is Essential for Regulating the Immune Response to Escherichia coli and Staphylococcus aureus Infection in Tenebrio molitor

Edosa, Tariku Tesfaye; Jo, Yong Hun; Keshavarz, Maryam; Bae, Young‐Min; Kim, Dong Hyun; Lee, Yong Seok

doi:10.3390/insects11020105

Cited by 27 publications

(28 citation statements)

References 54 publications

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“…The activation of AMPs is different depending on the pathogen used to challenge silkworms [ 38 , 41 , 60 ]. Our studies showed that the Toll pathways were both activated by Gram-positive and Gram-negative bacteria in B. mori ( Figure 1 and Figure 2 ), unlike in M. sexta or D. melanogaster [ 6 , 33 ], which is consistent with a recent study in Tenebrio molitor [ 61 ]. In addition, the activation of AMP genes was not absolutely specific following the challenge with E. coli or S. aureus ( Figure 2 ).…”

Section: Discussionsupporting

confidence: 92%

A Toll-Spätzle Pathway in the Immune Response of Bombyx mori

Bin

Sang

Pan

et al. 2020

Insects

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The Toll-Spätzle pathway is a crucial defense mechanism in insect innate immunity, it plays an important role in fighting against pathogens through the regulation of antimicrobial peptide gene expression. Although Toll and Spätzle (Spz) genes have been identified in Bombyx mori, little is known regarding the specific Spz and Toll genes members involved in innate immunity. There is also limited direct evidence of the interaction between Spz and Toll. In this study, the dual-luciferase reporter assay results showed that BmToll11 and BmToll9–1 could activate both drosomycin and diptericin promoters in S2 cells. Furthermore, BmToll11, BmToll9–1, and five BmSpzs genes were found to be significantly upregulated in B. mori infected by Escherichia coli and Staphylococcus aureus. Additionally, the yeast two-hybrid assay results confirmed that BmSpz2, but not other BmSpzs, could interact with both BmToll11 and BmToll9–1. These findings suggest that the activated BmSpz2 can bind with BmToll11 and BmToll9–1 to induce the expression of AMPs after the silkworm is infected by pathogens.

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Section: Discussionsupporting

confidence: 92%

A Toll-Spätzle Pathway in the Immune Response of Bombyx mori

Bin

Sang

Pan

et al. 2020

Insects

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“…Similarly, the previous in vitro experiments showed that E. coli induced the activation of spätzle in T. molitor larvae, suggesting that the polymeric DAP-type PGN forms a complex with Tenebrio PGRP-SA to activate the Toll receptor ligand, spätzle [30]. Similarly, in our recent publication we have reported TmSpz6 is important in regulating the AMPs production in response to E. coli [38] The survival results in our study support the induction analysis results, implying the importance of TmSpz4 in the defense response of T. molitor larvae against C. albicans and E. coli by regulating different AMPs production. Specifically, TmSpz4 silencing resulted in increased susceptibility of the larvae to E. coli and C. albicans infections.…”

Section: Discussionsupporting

confidence: 75%

TmSpz4 Plays an Important Role in Regulating the Production of Antimicrobial Peptides in Response to Escherichia coli and Candida albicans Infections

Edosa

Keshavarz

et al. 2020

IJMS

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Spätzle family proteins activate the Toll pathway and induce antimicrobial peptide (AMP) production against microbial infections. However, the functional importance of Tmspätzle4 (TmSpz4) in the immune response of Tenebrio molitor has not been reported. Therefore, here, we have identified and functionally characterized the role of TmSpz4 against bacterial and fungal infections. We showed that TmSpz4 expression was significantly induced in hemocytes at 6 h post-injection with Escherichia coli, Staphylococcus aureus, and Candida albicans. TmSpz4 knock-down significantly reduced larval survival against E. coli and C. albicans. To understand the reason for the survivability difference, the role of TmSpz4 in AMP production was examined in TmSpz4-silenced larvae following microbe injection. The AMPs that are active against Gram-negative bacteria, including TmTenecin-2, TmTenecin-4, TmAttacin-1a, TmDefensin-2, and TmCecropin-2, were significantly downregulated in response to E. coli in TmSpz4-silenced larvae. Similarly, the expression of TmTenecin-1, TmTenecin-3, TmThaumatin-like protein-1 and -2, TmDefensin-1, TmDefensin-2, and TmCecropin-2 were downregulated in response to C. albicans in TmSpz4-silenced larvae. In addition, the transcription factor NF-κB (TmDorX1 and TmDorX2) expression was significantly suppression in TmSpz4-silenced larvae. In conclusion, these results suggest that TmSpz4 plays a key role in regulating immune responses of T. molitor against to E. coli and C. albicans.

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“…Supporting our current survivability and AMP expression study results, attacins in Hyalophora cecropia [ 74 ], TmTen-4 in T. molitor [ 48 ], and TmTen-2 in T. molitor [ 71 ], which are glycine-rich AMPs, have been reported as being particularly effective against Gram-negative bacteria [ 71 ]. Similarly, in our recent publication we have reported TmSpz6 is important in regulating the AMPs production in response to E. coli [ 75 ]. Therefore, it can be said that the biosurfactant-activated AMPs enable larvae to be protected against E. coli .…”

Section: Discussionmentioning

confidence: 58%

Biosurfactants Induce Antimicrobial Peptide Production through the Activation of TmSpatzles in Tenebrio molitor

Edosa

Keshavarz

et al. 2020

IJMS

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Biosurfactant immunomodulatory activities in mammals, nematodes, and plants have been investigated. However, the immune activation property of biosurfactants in insects has not been reported. Therefore, here, we studied the defense response triggered by lipopeptides (fengycin and iturin A), glycolipids (rhamnolipid), and cyclic polypeptides (bacitracin) in the coleopteran insect, mealworm Tenebrio molitor. The in vitro antimicrobial activities against Gram-positive (Staphylococcus aureus) and Gram-negative (Escherichia coli) bacteria and fungi (Candida albicans) were assessed by mixing these pathogens with the hemolymph of biosurfactant-immune-activated larvae. E. coli growth was remarkably inhibited by this hemolymph. The antimicrobial peptide (AMP) induction results also revealed that all biosurfactants tested induced several AMPs, exclusively in hemocytes. The survivability analysis of T. molitor larvae challenged by E. coli (106 CFU/µL) at 24 h post biosurfactant-immune activation showed that fengycin, iturin A, and rhamnopid significantly increased survivability against E. coli. Biosurfactant-induced TmSpatzles activation was also monitored, and the results showed that TmSpz3 and TmSpz-like were upregulated in the hemocytes of iturin A-injected larvae, while TmSpz4 and TmSpz6 were upregulated in the fat bodies of the fengycin-, iturin A-, and rhamnolipid-injected larvae. Overall, these results suggest that lipopeptide and glycolipid biosurfactants induce the expression of AMPs in T. molitor via the activation of spätzle genes, thereby increasing the survivability of T. molitor against E. coli.

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TmSpz6 Is Essential for Regulating the Immune Response to Escherichia coli and Staphylococcus aureus Infection in Tenebrio molitor

Cited by 27 publications

References 54 publications

A Toll-Spätzle Pathway in the Immune Response of Bombyx mori

A Toll-Spätzle Pathway in the Immune Response of Bombyx mori

TmSpz4 Plays an Important Role in Regulating the Production of Antimicrobial Peptides in Response to Escherichia coli and Candida albicans Infections

Biosurfactants Induce Antimicrobial Peptide Production through the Activation of TmSpatzles in Tenebrio molitor

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