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Autophagy in Tenebrio molitor Immunity: Conserved Antimicrobial Functions in Insect Defenses

The yellow mealworm beetle (Tenebrio molitor) has been exploited as an experimental model to unravel the intricacies of cellular and humoral immunity against pathogenic infections. Studies on this insect model have provided valuable insights into the phenotypic plasticity of immune defenses against...

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Autores principales: Jo, Yong Hun, Lee, Jung Hee, Patnaik, Bharat Bhusan, Keshavarz, Maryam, 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/PMC8202003/
https://www.ncbi.nlm.nih.gov/pubmed/34135896
http://dx.doi.org/10.3389/fimmu.2021.667664
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author Jo, Yong Hun
Lee, Jung Hee
Patnaik, Bharat Bhusan
Keshavarz, Maryam
Lee, Yong Seok
Han, Yeon Soo
author_facet Jo, Yong Hun
Lee, Jung Hee
Patnaik, Bharat Bhusan
Keshavarz, Maryam
Lee, Yong Seok
Han, Yeon Soo
author_sort Jo, Yong Hun
collection PubMed
description The yellow mealworm beetle (Tenebrio molitor) has been exploited as an experimental model to unravel the intricacies of cellular and humoral immunity against pathogenic infections. Studies on this insect model have provided valuable insights into the phenotypic plasticity of immune defenses against parasites and pathogens. It has thus been possible to characterize the hemocoelic defenses of T. molitor that rely on the recognition of non-self-components of pathogens by pattern recognition receptors (PRRs). The subsequent signaling cascade activating pathways such as the NF-κB controlled by Toll and IMD pathways lead to the synthesis of antimicrobial peptides (AMPs), onset of hemocyte-driven phagocytosis, and activation of the prophenoloxidase cascade regulating the process of melanization. Nevertheless, the activation of autophagy-mediated defenses of T. molitor against the facultative intracellular gram-positive bacterium Listeria monocytogenes provides clear evidence of the existence of a cross-talk between autophagy and the IMD pathway. Moreover, the identification of several autophagy-related genes (Atgs) in T. molitor transcriptome and expressed sequence tag (EST) databases has contributed to the understanding of the autophagy-signaling cascade triggered by L. monocytogenes challenge. Providing further evidence of the cross-talk hypothesis, TmRelish has been shown to be required not only for regulating the synthesis of AMPs through the PGRP-LE/IMD pathway activation but also for the expression of Atgs in T. molitor larvae following L. monocytogenes challenge. Notably, L. monocytogenes can stimulate the T. molitor innate immune system by producing molecules recognized by the multifunctional PRR (TmPGRP-LE), which stimulates intracellular activation of the IMD pathway and autophagy. Considering the conservation of autophagy components involved in combating intracellular pathogens, it will be interesting to extrapolate a dynamic cross-talk model of immune activation. This review summarizes the most significant findings on the regulation of autophagy in T. molitor during L. monocytogenes infection and on the role of the innate immunity machinery, including the NF-κB pathway, in the control of pathogenic load.
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spelling pubmed-82020032021-06-15 Autophagy in Tenebrio molitor Immunity: Conserved Antimicrobial Functions in Insect Defenses Jo, Yong Hun Lee, Jung Hee Patnaik, Bharat Bhusan Keshavarz, Maryam Lee, Yong Seok Han, Yeon Soo Front Immunol Immunology The yellow mealworm beetle (Tenebrio molitor) has been exploited as an experimental model to unravel the intricacies of cellular and humoral immunity against pathogenic infections. Studies on this insect model have provided valuable insights into the phenotypic plasticity of immune defenses against parasites and pathogens. It has thus been possible to characterize the hemocoelic defenses of T. molitor that rely on the recognition of non-self-components of pathogens by pattern recognition receptors (PRRs). The subsequent signaling cascade activating pathways such as the NF-κB controlled by Toll and IMD pathways lead to the synthesis of antimicrobial peptides (AMPs), onset of hemocyte-driven phagocytosis, and activation of the prophenoloxidase cascade regulating the process of melanization. Nevertheless, the activation of autophagy-mediated defenses of T. molitor against the facultative intracellular gram-positive bacterium Listeria monocytogenes provides clear evidence of the existence of a cross-talk between autophagy and the IMD pathway. Moreover, the identification of several autophagy-related genes (Atgs) in T. molitor transcriptome and expressed sequence tag (EST) databases has contributed to the understanding of the autophagy-signaling cascade triggered by L. monocytogenes challenge. Providing further evidence of the cross-talk hypothesis, TmRelish has been shown to be required not only for regulating the synthesis of AMPs through the PGRP-LE/IMD pathway activation but also for the expression of Atgs in T. molitor larvae following L. monocytogenes challenge. Notably, L. monocytogenes can stimulate the T. molitor innate immune system by producing molecules recognized by the multifunctional PRR (TmPGRP-LE), which stimulates intracellular activation of the IMD pathway and autophagy. Considering the conservation of autophagy components involved in combating intracellular pathogens, it will be interesting to extrapolate a dynamic cross-talk model of immune activation. This review summarizes the most significant findings on the regulation of autophagy in T. molitor during L. monocytogenes infection and on the role of the innate immunity machinery, including the NF-κB pathway, in the control of pathogenic load. Frontiers Media S.A. 2021-05-31 /pmc/articles/PMC8202003/ /pubmed/34135896 http://dx.doi.org/10.3389/fimmu.2021.667664 Text en Copyright © 2021 Jo, Lee, Patnaik, Keshavarz, 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 Immunology
Jo, Yong Hun
Lee, Jung Hee
Patnaik, Bharat Bhusan
Keshavarz, Maryam
Lee, Yong Seok
Han, Yeon Soo
Autophagy in Tenebrio molitor Immunity: Conserved Antimicrobial Functions in Insect Defenses
title Autophagy in Tenebrio molitor Immunity: Conserved Antimicrobial Functions in Insect Defenses
title_full Autophagy in Tenebrio molitor Immunity: Conserved Antimicrobial Functions in Insect Defenses
title_fullStr Autophagy in Tenebrio molitor Immunity: Conserved Antimicrobial Functions in Insect Defenses
title_full_unstemmed Autophagy in Tenebrio molitor Immunity: Conserved Antimicrobial Functions in Insect Defenses
title_short Autophagy in Tenebrio molitor Immunity: Conserved Antimicrobial Functions in Insect Defenses
title_sort autophagy in tenebrio molitor immunity: conserved antimicrobial functions in insect defenses
topic Immunology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8202003/
https://www.ncbi.nlm.nih.gov/pubmed/34135896
http://dx.doi.org/10.3389/fimmu.2021.667664
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