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Article: Autophagy dually induced by AMP surplus and oxidative stress enhances hemocyte survival and bactericidal capacity via AMPK pathway in Crassostrea hongkongensis

TitleAutophagy dually induced by AMP surplus and oxidative stress enhances hemocyte survival and bactericidal capacity via AMPK pathway in Crassostrea hongkongensis
Authors
KeywordsAMPK phosphorylation
apoptosis
autophagy
Hong Kong oyster
infection
Issue Date2020
PublisherFrontiers Research Foundation. The Journal's web site is located at https://www.frontiersin.org/journals/cell-and-developmental-biology
Citation
Frontiers in Cell and Developmental Biology, 2020, v. 8, p. article no. 411 How to Cite?
AbstractCrassostrea 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 O2– and cellular H2O2) 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.
Persistent Identifierhttp://hdl.handle.net/10722/294720
ISSN
2023 Impact Factor: 4.6
2023 SCImago Journal Rankings: 1.576
PubMed Central ID
ISI Accession Number ID

 

DC FieldValueLanguage
dc.contributor.authorDang, X-
dc.contributor.authorWong, NK-
dc.contributor.authorXie, Y-
dc.contributor.authorVengatesen, T-
dc.contributor.authorMao, F-
dc.contributor.authorZhang, X-
dc.contributor.authorLin, Y-
dc.contributor.authorXiang, Z-
dc.contributor.authorLi, J-
dc.contributor.authorXiao, S-
dc.contributor.authorNoor, Z-
dc.contributor.authorHe, Y-
dc.contributor.authorZhang, Y-
dc.contributor.authorYu, Z-
dc.date.accessioned2020-12-08T07:40:53Z-
dc.date.available2020-12-08T07:40:53Z-
dc.date.issued2020-
dc.identifier.citationFrontiers in Cell and Developmental Biology, 2020, v. 8, p. article no. 411-
dc.identifier.issn2296-634X-
dc.identifier.urihttp://hdl.handle.net/10722/294720-
dc.description.abstractCrassostrea 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 O2– and cellular H2O2) 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.-
dc.languageeng-
dc.publisherFrontiers Research Foundation. The Journal's web site is located at https://www.frontiersin.org/journals/cell-and-developmental-biology-
dc.relation.ispartofFrontiers in Cell and Developmental Biology-
dc.rightsThis Document is Protected by copyright and was first published by Frontiers. All rights reserved. It is reproduced with permission.-
dc.rightsThis work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.-
dc.subjectAMPK phosphorylation-
dc.subjectapoptosis-
dc.subjectautophagy-
dc.subjectHong Kong oyster-
dc.subjectinfection-
dc.titleAutophagy dually induced by AMP surplus and oxidative stress enhances hemocyte survival and bactericidal capacity via AMPK pathway in Crassostrea hongkongensis-
dc.typeArticle-
dc.identifier.emailVengatesen, T: rajan@hkucc.hku.hk-
dc.identifier.authorityVengatesen, T=rp00796-
dc.description.naturepublished_or_final_version-
dc.identifier.doi10.3389/fcell.2020.00411-
dc.identifier.pmid32656204-
dc.identifier.pmcidPMC7325953-
dc.identifier.scopuseid_2-s2.0-85086588567-
dc.identifier.hkuros320374-
dc.identifier.volume8-
dc.identifier.spagearticle no. 411-
dc.identifier.epagearticle no. 411-
dc.identifier.isiWOS:000543858200001-
dc.publisher.placeSwitzerland-
dc.identifier.issnl2296-634X-

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