Autophagy Dually Induced by AMP Surplus and Oxidative Stress Enhances Hemocyte Survival and Bactericidal Capacity via AMPK Pathway in Crassostrea hongkongensis
Crassostrea hongkongensis (Hong Kong oyster) is an ecologically and economically valuable shellfish endemic to South/Southeast Asia. Due to ocean acidification and warming waters, they have become increasingly vulnerable to invading microbes including Vibrio parahaemolyticus, a significant foodborne...
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ftpubmed:oai:pubmedcentral.nih.gov:7325953 2023-05-15T15:58:50+02:00 Autophagy Dually Induced by AMP Surplus and Oxidative Stress Enhances Hemocyte Survival and Bactericidal Capacity via AMPK Pathway in Crassostrea hongkongensis Dang, Xin Wong, Nai-Kei Xie, Yongli Thiyagarajan, Vengatesen Mao, Fan Zhang, Xiangyu Lin, Yue Xiang, Zhiming Li, Jun Xiao, Shu Noor, Zohaib He, Yuanqiu Zhang, Yang Yu, Ziniu 2020-06-03 http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7325953/ https://doi.org/10.3389/fcell.2020.00411 en eng Frontiers Media S.A. http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7325953/ http://dx.doi.org/10.3389/fcell.2020.00411 Copyright © 2020 Dang, Wong, Xie, Thiyagarajan, Mao, Zhang, Lin, Xiang, Li, Xiao, Noor, He, Zhang and Yu. http://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. CC-BY Front Cell Dev Biol Cell and Developmental Biology Text 2020 ftpubmed https://doi.org/10.3389/fcell.2020.00411 2020-07-12T00:24:02Z Crassostrea hongkongensis (Hong Kong oyster) is an ecologically and economically valuable shellfish endemic to South/Southeast Asia. Due to ocean acidification and warming waters, they have become increasingly vulnerable to invading microbes including Vibrio parahaemolyticus, a significant foodborne human pathogen. In recent years, outbreaks of V. parahaemolyticus have emerged as a perennial phenomenon in parts of the world, necessitating to better understand the biology of host-pathogen interactions in this under-examined marine invertebrate. Although an immunologically relevant autophagy apparatus has been identified in Crassostrea gigas, an evolutionarily close mollusk cousin, the precise mechanistic details of C. hongkongensis autophagy during V. parahaemolyticus infection are still wanting. Here, we compellingly demonstrated that in vivo V. parahaemolyticus challenge robustly triggered autophagic signaling in C. hongkongensis hemocytes peaking at 6 h post-infection, which subsequently promoted bacterial clearance and dampened premature apoptosis. Simultaneously, a large surplus of adenosine monophosphate (AMP) and elevations in reactive oxygen species (ROS, specifically mitochondrial O(2)(–) and cellular H(2)O(2)) formation were observed post-infection. Extrinsically applied AMP and ROS could synergistically induce AMP-activated protein kinase (AMPK) phosphorylation to stimulate downstream autophagic events. V. parahaemolyticus infection-induced autophagy was pharmacologically shown to be AMPK-dependent in vivo. Overall, our results establish autophagy as a crucial arm of host defense against Vibrio infections in mollusks, and provide new insights into the underappreciated roles of ROS and AMP as co-regulators of autophagy. Text Crassostrea gigas Ocean acidification PubMed Central (PMC) Frontiers in Cell and Developmental Biology 8 |
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Cell and Developmental Biology |
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Cell and Developmental Biology Dang, Xin Wong, Nai-Kei Xie, Yongli Thiyagarajan, Vengatesen Mao, Fan Zhang, Xiangyu Lin, Yue Xiang, Zhiming Li, Jun Xiao, Shu Noor, Zohaib He, Yuanqiu Zhang, Yang Yu, Ziniu Autophagy Dually Induced by AMP Surplus and Oxidative Stress Enhances Hemocyte Survival and Bactericidal Capacity via AMPK Pathway in Crassostrea hongkongensis |
topic_facet |
Cell and Developmental Biology |
description |
Crassostrea hongkongensis (Hong Kong oyster) is an ecologically and economically valuable shellfish endemic to South/Southeast Asia. Due to ocean acidification and warming waters, they have become increasingly vulnerable to invading microbes including Vibrio parahaemolyticus, a significant foodborne human pathogen. In recent years, outbreaks of V. parahaemolyticus have emerged as a perennial phenomenon in parts of the world, necessitating to better understand the biology of host-pathogen interactions in this under-examined marine invertebrate. Although an immunologically relevant autophagy apparatus has been identified in Crassostrea gigas, an evolutionarily close mollusk cousin, the precise mechanistic details of C. hongkongensis autophagy during V. parahaemolyticus infection are still wanting. Here, we compellingly demonstrated that in vivo V. parahaemolyticus challenge robustly triggered autophagic signaling in C. hongkongensis hemocytes peaking at 6 h post-infection, which subsequently promoted bacterial clearance and dampened premature apoptosis. Simultaneously, a large surplus of adenosine monophosphate (AMP) and elevations in reactive oxygen species (ROS, specifically mitochondrial O(2)(–) and cellular H(2)O(2)) formation were observed post-infection. Extrinsically applied AMP and ROS could synergistically induce AMP-activated protein kinase (AMPK) phosphorylation to stimulate downstream autophagic events. V. parahaemolyticus infection-induced autophagy was pharmacologically shown to be AMPK-dependent in vivo. Overall, our results establish autophagy as a crucial arm of host defense against Vibrio infections in mollusks, and provide new insights into the underappreciated roles of ROS and AMP as co-regulators of autophagy. |
format |
Text |
author |
Dang, Xin Wong, Nai-Kei Xie, Yongli Thiyagarajan, Vengatesen Mao, Fan Zhang, Xiangyu Lin, Yue Xiang, Zhiming Li, Jun Xiao, Shu Noor, Zohaib He, Yuanqiu Zhang, Yang Yu, Ziniu |
author_facet |
Dang, Xin Wong, Nai-Kei Xie, Yongli Thiyagarajan, Vengatesen Mao, Fan Zhang, Xiangyu Lin, Yue Xiang, Zhiming Li, Jun Xiao, Shu Noor, Zohaib He, Yuanqiu Zhang, Yang Yu, Ziniu |
author_sort |
Dang, Xin |
title |
Autophagy Dually Induced by AMP Surplus and Oxidative Stress Enhances Hemocyte Survival and Bactericidal Capacity via AMPK Pathway in Crassostrea hongkongensis |
title_short |
Autophagy Dually Induced by AMP Surplus and Oxidative Stress Enhances Hemocyte Survival and Bactericidal Capacity via AMPK Pathway in Crassostrea hongkongensis |
title_full |
Autophagy Dually Induced by AMP Surplus and Oxidative Stress Enhances Hemocyte Survival and Bactericidal Capacity via AMPK Pathway in Crassostrea hongkongensis |
title_fullStr |
Autophagy Dually Induced by AMP Surplus and Oxidative Stress Enhances Hemocyte Survival and Bactericidal Capacity via AMPK Pathway in Crassostrea hongkongensis |
title_full_unstemmed |
Autophagy Dually Induced by AMP Surplus and Oxidative Stress Enhances Hemocyte Survival and Bactericidal Capacity via AMPK Pathway in Crassostrea hongkongensis |
title_sort |
autophagy dually induced by amp surplus and oxidative stress enhances hemocyte survival and bactericidal capacity via ampk pathway in crassostrea hongkongensis |
publisher |
Frontiers Media S.A. |
publishDate |
2020 |
url |
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7325953/ https://doi.org/10.3389/fcell.2020.00411 |
genre |
Crassostrea gigas Ocean acidification |
genre_facet |
Crassostrea gigas Ocean acidification |
op_source |
Front Cell Dev Biol |
op_relation |
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7325953/ http://dx.doi.org/10.3389/fcell.2020.00411 |
op_rights |
Copyright © 2020 Dang, Wong, Xie, Thiyagarajan, Mao, Zhang, Lin, Xiang, Li, Xiao, Noor, He, Zhang and Yu. http://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. |
op_rightsnorm |
CC-BY |
op_doi |
https://doi.org/10.3389/fcell.2020.00411 |
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Frontiers in Cell and Developmental Biology |
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