Regulation of the expression of nine antimicrobial peptide genes by TmIMD confers resistance against Gram-negative bacteria

Jo, Yong Hun; Patnaik, Bharat Bhusan; Hwang, Jihun; Park, Ki Beom; Ko, Hye Jin; Kim, Chang-Eun; Bae, Young‐Min; Jung, Woo Jin; Lee, Yong Seok

doi:10.1038/s41598-019-46222-8

Cited by 28 publications

(30 citation statements)

References 47 publications

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“…In a previous study, expression levels of TmTene1, TmTene2, TmTene4, TmAtt1a, TmAtt1b, TmAtt2, TmCole1, TmCole2, and TmDef2 were significantly reduced in E. coli-challenged T. molitor following silencing of immune deficiency (TmIMD) expression (Jo et al, 2019). These findings are consistent with our own, in which the expression levels of these genes were downregulated in the gut of E. coli-challenged T. molitor larvae following silencing of TmPGRP-LE.…”

Section: Discussionsupporting

confidence: 91%

“…of seven AMP genes, namely TmTene1, TmTene4, TmAtt1b, TmAtt2, TmCole1, TmCole2, and TmDef2, showed a dramatic reduction in the hemocytes of the dsTmPGRP-LE-injected group. We also know that the same AMPs were downregulated in the dsTmIMD, dsTmRelish, and dsTmDorX2-injected cohorts (Jo et al, 2019;Keshavarz et al, 2019). Moreover, in the fat body of dsTmPGRP-LE-injected insects, TmAtt1a, TmCole2, TmDef2, and TmCec2 were significantly suppressed following exposure to E. coli.…”

Section: Discussionmentioning

confidence: 90%

“…Moreover, in the fat body of dsTmPGRP-LE-injected insects, TmAtt1a, TmCole2, TmDef2, and TmCec2 were significantly suppressed following exposure to E. coli. Similarly, depletion of TmIMD, TmRelish, and TmDorX2 led to a reduction in the same AMPs in the larval fat body after E. coli infection (Jo et al, 2019;Keshavarz et al, 2019). Mortality assays and AMP expression analyses from our present work and those of others suggest that, in comparison to hemocytes and the fat body, the T. molitor gut plays a pivotal role in the response to E. coli infection via activation of the Imd pathway.…”

Section: Discussionmentioning

confidence: 96%

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Tenebrio molitor PGRP-LE Plays a Critical Role in Gut Antimicrobial Peptide Production in Response to Escherichia coli

Keshavarz

Edosa

2020

Front. Physiol.

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Invading pathogens are recognized by peptidoglycan recognition proteins (PGRPs) that induce translocation of NF-κB transcription proteins and expression of robust antimicrobial peptides (AMPs). Tenebrio molitor PGRP-LE (TmPGRP-LE) has been previously identified as a key sensor of Listeria monocytogenes infection. Here, we present that TmPGRP-LE is highly expressed in the gut of T. molitor larvae and 5-dayold adults in the absence of microbial infection. In response to Escherichia coli and Candida albicans infections, TmPGRP-LE mRNA levels are significantly upregulated in both the fat body and gut. Silencing of TmPGRP-LE by RNAi rendered T. molitor significantly more susceptible to challenge by E. coli infection and, to a lesser extent, Staphylococcus aureus and C. albicans infections. Reduction of TmPGRP-LE levels in the larval gut resulted in downregulation of eight AMP genes following exposure to E. coli, S. aureus, and C. albicans. However, the transcriptional levels of AMPs more rapidly reached a higher level in the dsEGFP-treated larval gut after challenge with E. coli, which may suggest that AMPs induction were more sensitive to E. coli than S. aureus and C. albicans. In addition, TmPGRP-LE RNAi following E. coli and C. albicans challenges had notable effects on TmRelish, TmDorsal X1 isoform (TmDorX1), and TmDorX2 expression level in the fat body and gut. Taken together, TmPGRP-LE acts as an important gut microbial sensor that induces AMPs via Imd activation in response to E. coli, whereas involvement of TmPGRP-LE in AMPs synthesize is barely perceptible in the hemocytes and fat body.

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Section: Discussionsupporting

confidence: 91%

Section: Discussionmentioning

confidence: 90%

Section: Discussionmentioning

confidence: 96%

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Tenebrio molitor PGRP-LE Plays a Critical Role in Gut Antimicrobial Peptide Production in Response to Escherichia coli

Keshavarz

Edosa

2020

Front. Physiol.

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“…Although we observed decreased levels of several AMPs in dsTmRelish-treated larvae following S. aureus, TmRelish depletion led to mild but significant mortality. In a previous study, the mRNA levels of TmTene1, TmTene2, TmTene4, TmDef2, TmCole1, TmCole2, TmAtta1a, TmAtta1b, and TmAtta2 were found to be significantly reduced in T. molitor following silencing of immune deficiency (TmIMD), an adapter molecule upstream of the Imd pathway, upon exposure to E. coli 63 . Similarly, upon E. coli challenge, expression of TmTene3, TmDef1, and the AMPs listed above, was downregulated in the gut of TmRelish-depleted larvae.…”

Section: Discussionmentioning

confidence: 90%

TmRelish is required for regulating the antimicrobial responses to Escherichia coli and Staphylococcus aureus in Tenebrio molitor

Keshavarz

Patnaik

et al. 2020

Sci Rep

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Relish, a transcription factor, is a critical downstream component of the immune deficiency (Imd) pathway and regulates host defense against bacterial infection by mediating antimicrobial peptide (AMP) synthesis. Understanding the immunological function of the mealworm beetle, Tenebrio molitor Relish (TmRelish) will be instructive in understanding insect immunity. In the present study, full-length oRf of TmRelish was retrieved from T. molitor-expressed sequence tags and RNA-seq database. The predicted TmRelish amino acid sequence contained an N-terminal Rel-homology domain; an Ig-like, plexin, and transcription factor domain; ankyrin repeat motifs; a nuclear localization signal; and a C-terminal death domain and shared the highly conserved structure of the Relish proteins of other insect species. TmRelish mRNA was detected in all developmental stages of the insect; however, the highest levels were detected in the larval gut tissue and adult hemocytes. TmRelish mRNA level was upregulated in the fat body, hemocyte, and gut tissue 9 h after infection of T. molitor larvae by the gram-negative bacteria, Escherichia coli. Furthermore, TmRelish knockdown led to significantly higher mortality of the E. coli-infected larvae, and significantly lower mortality of larvae infected with Staphylococcus aureus or Candida albicans. To elucidate the possible cause of mortality, we measured AMP transcription in the fat body, hemocytes, gut, and Malpighian tubules (MTs) of T. molitor larvae. TmRelish knockdown suppressed the expression of nine AMP genes in the larval fat body and gut tissue during E. coli infection, suggesting that TmRelish positively regulates AMP expression in both immunerelated tissues, in response to E. coli challenge. Furthermore, negative regulation of some AMPs by TmRelish in the MTs, gut and hemocytes in response to C. albicans infection suggests a crosstalk between the Toll and Imd pathways.

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“…This may be due to the use of feed-grade substrates as several insects as well as mealworms have vector potential for carrying Salmonella after exposure ( Skov et al, 2004 ; Roche et al, 2009 ; Blazar et al, 2011 ; Nordentoft et al, 2017 ; Crippen et al, 2012 , 2018 ; Wynants et al, 2019 ). Another explanation may be a potential capability of insects to fight incoming pathogens ( Wu et al, 2018 ; Jo et al, 2019 ; Keshavarz et al, 2020 ).…”

Section: Introductionmentioning

confidence: 99%

Salmonella Typhimurium Level in Mealworms (Tenebrio molitor) After Exposure to Contaminated Substrate

2020

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Findings of viable Salmonella spp., which are important foodborne pathogens, are seemingly not reported in mealworms (Tenebrio molitor) for feed and food. Still, the bacterial load of mealworms is naturally high and includes members of the Enterobacteriaceae family to which Salmonella belong. This indicates that Salmonella may be able to thrive in mealworms if introduced into the production. Therefore, this study aimed to assess the quantitative level of Salmonella enterica serovar Typhimurium (ST) in mealworms over a 14-day course after exposure to substrate contaminated with ST levels from 1.7 to 7.4 log CFU/g at start (i.e., day 0). The level of ST found in larvae was below the quantitative detection level (1 or 2 log CFU/g) on day 1 in larvae exposed to contamination levels of 1.7, 3.4, and 3.6 log CFU/g opposed to contamination levels of 5.4, 5.6, and 7.4 log CFU/g, respectively. The maximum level of ST detected in individual 1-g larvae samples was 5.8 log CFU/g, but the level varied among the triplicate samples from each sampling, and the highest average value was 5.3 ± 0.3. Beyond day 7, only larvae exposed to the contamination level of 7.4 log CFU/g were >1.0 log CFU/g in the triplicate samples. However, qualitative testing (10 g) showed the presence of ST in larvae until the end of the experiment on day 14 except for the lowest contamination level of 1.7 log CFU/g. Parallel testing of surface disinfected larvae indicated that some larvae may be ST-positive due to Salmonella residing on the surface only. Still, any detection of Salmonella is of concern from a food safety perspective. In substrate with contamination levels below 3.6 log CFU/g, the level of ST was below the quantitative detection limit within a few days. Still, ST was detected until the end of experiment on day 14 except for the lowest contamination level of 1.7 log CFU/g. This study indicates the importance of avoiding introduction of Salmonella into the production, e.g., via contaminated substrate in order to avoid Salmonella-positive larvae as they remained positive for at least 14 days (except at the lowest contamination level).

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Regulation of the expression of nine antimicrobial peptide genes by TmIMD confers resistance against Gram-negative bacteria

Cited by 28 publications

References 47 publications

Tenebrio molitor PGRP-LE Plays a Critical Role in Gut Antimicrobial Peptide Production in Response to Escherichia coli

Tenebrio molitor PGRP-LE Plays a Critical Role in Gut Antimicrobial Peptide Production in Response to Escherichia coli

TmRelish is required for regulating the antimicrobial responses to Escherichia coli and Staphylococcus aureus in Tenebrio molitor

Salmonella Typhimurium Level in Mealworms (Tenebrio molitor) After Exposure to Contaminated Substrate

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